Biohybrid microswimmer

A biohybrid microswimmer also known as biohybrid nanorobot, ^[1] can be defined as a microswimmer that consist of both biological and artificial constituents, for instance, one or several living microorganisms attached to one or various synthetic parts.

In recent years nanoscopic and mesoscopic objects have been designed to collectively move through direct inspiration from nature or by harnessing its existing tools. Small mesoscopic to nanoscopic systems typically operate at low Reynolds numbers (Re ≪ 1), and understanding their motion becomes challenging. For locomotion to occur, the symmetry of the system must be broken.

In addition, collective motion requires a coupling mechanism between the entities that make up the collective. To develop mesoscopic to nanoscopic entities capable of swarming behaviour, it has been hypothesised that the entities are characterised by broken symmetry with a well-defined morphology, and are powered with some material capable of harvesting energy. If the harvested energy results in a field surrounding the object, then this field can couple with the field of a neighbouring object and bring some coordination to the collective behaviour. Such robotic swarms have been categorised by an online expert panel as among the 10 great unresolved group challenges in the area of robotics. Although investigation of their underlying mechanism of action is still in its infancy, various systems have been developed that are capable of undergoing controlled and uncontrolled swarming motion by harvesting energy (e.g., light, thermal, etc.).

Over the past decade, biohybrid microrobots, in which living mobile microorganisms are physically integrated with untethered artificial structures, have gained growing interest to enable the active locomotion and cargo delivery to a target destination. In addition to the motility, the intrinsic capabilities of sensing and eliciting an appropriate response to artificial and environmental changes make cell-based biohybrid microrobots appealing for transportation of cargo to the inaccessible cavities of the human body for local active delivery of diagnostic and therapeutic agents.

Background

Basic features of an in vivo microrobot 

In a biohybrid approach, all three of these basic features can be realised either biologically by a microorganism, or artificially by synthetic attachments. Blue indicates biological entities (flagellated or target cells), red indicates artificial structures (attached tubes, helices, particles, or external devices). Arrows in the upper left panel indicate the motile actor, wave lines in the upper right panel indicate signal pathways. The lower panel shows how functionalities can be carried out based on cell-cell interactions or by synthetic cargo (red particles).

Biohybrid microswimmers can be defined as microswimmers that consist of both biological and artificial constituents, for instance, one or several living microorganisms attached to one or various synthetic parts. ^{[2] [3]} The pioneers of this field, ahead of their time, were Montemagno and Bachand with a 1999 work regarding specific attachment strategies of biological molecules to nanofabricated substrates enabling the preparation of hybrid inorganic/organic nanoelectromechanical systems, so called NEMS. ^[4] They described the production of large amounts of F1-ATPase from the thermophilic bacteria Bacillus PS3 for the preparation of F1-ATPase biomolecular motors immobilized on a nanoarray pattern of gold, copper or nickel produced by electron beam lithography. These proteins were attached to one micron microspheres tagged with a synthetic peptide. Consequently, they accomplished the preparation of a platform with chemically active sites and the development of biohybrid devices capable of converting energy of biomolecular motors into useful work. ^[3]

One of the most fundamental questions in science is what defines life. ^[5] Collective motion is one of the hallmarks of life. ^[6] This is commonly observed in nature at various dimensional levels as energized entities gather, in a concerted effort, into motile aggregated patterns. These motile aggregated events can be noticed, among many others, as dynamic swarms; e.g., unicellular organisms such as bacteria, locust swarms, or the flocking behaviour of birds. ^{[7] [8] [9]}

Ever since Newton established his equations of motion, the mystery of motion on the microscale has emerged frequently in scientific history, as famously demonstrated by a couple of articles that should be discussed briefly. First, an essential concept, popularized by Osborne Reynolds, is that the relative importance of inertia and viscosity for the motion of a fluid depends on certain details of the system under consideration. ^[3] The Reynolds number Re, named in his honor, quantifies this comparison as a dimensionless ratio of characteristic inertial and viscous forces:

${\displaystyle \mathrm {Re} ={\frac {\rho ul}{\mu }}}$

Here, ρ represents the density of the fluid; u is a characteristic velocity of the system (for instance, the velocity of a swimming particle); l is a characteristic length scale (e.g., the swimmer size); and μ is the viscosity of the fluid. Taking the suspending fluid to be water, and using experimentally observed values for u, one can determine that inertia is important for macroscopic swimmers like fish (Re = 100), while viscosity dominates the motion of microscale swimmers like bacteria (Re = 10⁻⁴). ^[3]

The overwhelming importance of viscosity for swimming at the micrometer scale has profound implications for swimming strategy. This has been discussed memorably by E. M. Purcell, who invited the reader into the world of microorganisms and theoretically studied the conditions of their motion. ^[10] In the first place, propulsion strategies of large scale swimmers often involve imparting momentum to the surrounding fluid in periodic discrete events, such as vortex shedding, and coasting between these events through inertia. This cannot be effective for microscale swimmers like bacteria: due to the large viscous damping, the inertial coasting time of a micron-sized object is on the order of 1 μs. The coasting distance of a microorganism moving at a typical speed is about 0.1 angstroms (Å). Purcell concluded that only forces that are exerted in the present moment on a microscale body contribute to its propulsion, so a constant energy conversion method is essential. ^{[10] [3]}

Microorganisms have optimized their metabolism for continuous energy production, while purely artificial microswimmers (microrobots) must obtain energy from the environment, since their on-board-storage-capacity is very limited. As a further consequence of the continuous dissipation of energy, biological and artificial microswimmers do not obey the laws of equilibrium statistical physics, and need to be described by non-equilibrium dynamics. ^[3] Mathematically, Purcell explored the implications of low Reynolds number by taking the Navier-Stokes equation and eliminating the inertial terms:

${\displaystyle {\begin{aligned}\mu \nabla ^{2}\mathbf {u} -{\boldsymbol {\nabla }}p&={\boldsymbol {0}}\\\end{aligned}}}$

where ${\displaystyle \mathbf {u} }$ is the velocity of the fluid and ${\displaystyle {\boldsymbol {\nabla }}p}$ is the gradient of the pressure. As Purcell noted, the resulting equation — the Stokes equation — contains no explicit time dependence. ^[10] This has some important consequences for how a suspended body (e.g., a bacterium) can swim through periodic mechanical motions or deformations (e.g., of a flagellum). First, the rate of motion is practically irrelevant for the motion of the microswimmer and of the surrounding fluid: changing the rate of motion will change the scale of the velocities of the fluid and of the microswimmer, but it will not change the pattern of fluid flow. Secondly, reversing the direction of mechanical motion will simply reverse all velocities in the system. These properties of the Stokes equation severely restrict the range of feasible swimming strategies. ^{[10] [3]}

Recent publications of biohybrid microswimmers include the use of sperm cells, contractive muscle cells, and bacteria as biological components, as they can efficiently convert chemical energy into movement, and additionally are capable of performing complicated motion depending on environmental conditions. In this sense, biohybrid microswimmer systems can be described as the combination of different functional components: cargo and carrier. The cargo is an element of interest to be moved (and possibly released) in a customized way. The carrier is the component responsible for the movement of the biohybrid, transporting the desired cargo, which is linked to its surface. The great majority of these systems rely on biological motile propulsion for the transportation of synthetic cargo for targeted drug delivery/ ^[2] There are also examples of the opposite case: artificial microswimmers with biological cargo systems. ^{[11] [12] [3]}

Over the past decade, biohybrid microrobots, in which living mobile microorganisms are physically integrated with untethered artificial structures, have gained growing interest to enable the active locomotion and cargo delivery to a target destination. ^{[13] [14] [15] [16]} In addition to the motility, the intrinsic capabilities of sensing and eliciting an appropriate response to artificial and environmental changes make cell-based biohybrid microrobots appealing for transportation of cargo to the inaccessible cavities of the human body for local active delivery of diagnostic and therapeutic agents. ^{[17] [18] [19]} Active locomotion, targeting and steering of concentrated therapeutic and diagnostic agents embedded in mobile microrobots to the site of action can overcome the existing challenges of conventional therapies. ^{[20] [21] [22]} To this end, bacteria have been commonly used with attached beads and ghost cell bodies. ^{[23] [24] [25] [26] [27] [28] [29] [30] [31]}

Bacterial biohybrids

See also: Bacterial motility

Bacteria-driven biohybrid microswimmers with a spherical body  ^[32]

(a) SEM images showing 2 μm diameter polystyrene microbeads, each attached by a few E. coli bacteria
(b) An illustration of the forces and torques exerted on the spherical microbead by its attached bacteria, where the force and the motor reaction torque of each bacterium are state dependent.

Artificial micro and nanoswimmers are small scale devices that convert energy into movement. ^{[33] [12]} Since the first demonstration of their performance in 2002, the field has developed rapidly in terms of new preparation methodologies, propulsion strategies, motion control, and envisioned functionality. ^{[34] [35]} The field holds promise for applications such as drug delivery, environmental remediation and sensing. The initial focus of the field was largely on artificial systems, but an increasing number of "biohybrids" are appearing in the literature. Combining artificial and biological components is a promising strategy to obtain new, well-controlled microswimmer functionalities, since essential functions of living organisms are intrinsically related to the capability to move. ^[36] Living beings of all scales move in response to environmental stimuli (e.g., temperature or pH), to look for food sources, to reproduce, or to escape from predators. One of the more well-known living microsystems are swimming bacteria, but directed motion occurs even at the molecular scale, where enzymes and proteins undergo conformational changes in order to carry out biological tasks. ^{[37] [3]}

Swimming bacterial cells have been used in the development of hybrid microswimmers. ^{[38] [39] [40] [41]} Cargo attachment to the bacterial cells might influence their swimming behavior. ^[3] Bacterial cells in the swarming state have also been used in the development of hybrid microswimmers. Swarming Serratia marcescens cells were transferred to PDMS-coated coverslips, resulting in a structure referred to as a "bacterial carpet" by the authors. Differently shaped flat fragments of this bacterial carpets, termed "auto-mobile chips", moved above the surface of the microscope slide in two dimensions. ^[42] Many other works have used Serratia marcescens swarming cells, ^{[43] [44] [45] [46] [47] [48]} as well as E. coli swarming cells  ^{[49] [23]} for the development of hybrid microswimmers. ^[3] Magnetotactic bacteria have been the focus of different studies due to their versatile uses in biohybrid motion systems. ^{[50] [51] [52] [53] [54] [3]}

Protist biohybrids

See also: Protist locomotion

Algal

Biohybrid Chlamydomonas reinhardtii microswimmers 

Top: Schematics of production steps for biohybrid C. reinhardtii.
Bottom: SEM images of bare microalgae (left) and biohybrid microalgae (right) coated with chitosan-coated iron oxide nanoparticles (CSIONPs). Images were pseudocolored. A darker green color on the right SEM image represents chitosan coating on microalgae cell wall. Orange-colored particles represents CSIONPs.

Chlamydomonas reinhardtii is a unicellular green microalga. The wild-type C. reinhardtii has a spherical shape that averages about 10 μm in diameter. ^[55] This microorganism can perceive the visible light and be steered by it (i.e., phototaxis) with high swimming speeds in the range of 100–200 μm s⁻¹. ^[19] It has natural autofluorescence that permits label-free fluorescent imaging. ^[55] C. reinhardtii has been actively explored as the live component of biohybrid microrobots for the active delivery of therapeutics. ^[19] They are biocompatible with healthy mammalian cells, leave no known toxins, mobile in the physiologically relevant media, and allow for surface modification to carry cargo on the cell wall. ^{[19] [56] [57] [58] [59]} Alternative attachment strategies for C. reinhardtii have been proposed for the assembly through modifying the interacting surfaces by electrostatic interactions ^{[19] [56]} and covalent bonding. ^{[60] [31]}

Robocoliths

Robocolith hybrids combining polydopamine and coccoliths 

EHUX coccolithophores are cultivated for isolation of coccoliths. When coccoliths (asymmetric morphology) are exposed to light, no collective motion is observed. Coccoliths are then mixed gently with dopamine solutions. Thus, polydopamine-coated coccoliths hybrids are obtained as a basis for design of Robocoliths. Light excitation and the asymmetry of Robocoliths generates a thermal flux of heat because of polydopamine's photothermal properties. Coupling of convection from neighboring Robocoliths transforms their movement into an aggregated collective motion. Robocolith functionalization is also proposed to prevent and control nonspecific attachment of biomacromolecules and possible diminution of the aggregation.

Asymmetric architecture of coccolith morphology 

(A) EHUX coccolithophores were cultivated successfully and visualized by SEM (scale bar, 4 μm).
(B) Following this, we broke and removed the cellular material from EHUX coccolithophores to isolate multiple (top; scale bar, 20 μm) and individual (bottom; scale bar, 1 μm) coccoliths, as visualized by SEM.
(C) AFM image of an individual coccolith. Micrograph size, 4 × 4 μm.
(D) AFM magnification the micrograph of an individual coccolith. Scale bar, 400 nm.
(E) Illustration of a coccolith, depicting its specific morphological parameters.
(F) Typical plotted values of the specific morphological parameters. Data are represented as mean ± SD (n = 55), where n is the number of coccoliths visualized by TEM.

Collective motion is one of the hallmarks of life. ^[6] In contrast to what is accomplished individually, multiple entities enable local interactions between each participant to occur in proximity. If we consider each participant in the collective behaviour as a (bio)physical transducer, then the energy will be converted from one type into another. The proxemics will then favour enhanced communication between neighbouring individuals via transduction of energy, leading to dynamic and complex synergetic behaviours of the composite powered structure. ^{[62] [61]}

In recent years nanoscopic and mesoscopic objects have been designed to collectively move through direct inspiration from nature or by harnessing its existing tools. ^{[63] [64] [65] [66]} Such robotic swarms were categorised by an online expert panel as among the 10 great unresolved group challenges in the area of robotics. ^[67] Although investigation of their underlying mechanism of action is still in its infancy, various systems have been developed that are capable of undergoing controlled and uncontrolled swarming motion by harvesting energy (e.g., light, thermal, etc.). ^[68] Importantly, this energy should be transformed into a net force for the system to move. ^[61]

Small mesoscopic to nanoscopic systems typically operate at low Reynolds numbers (Re ≪ 1), and understanding their motion becomes challenging. ^[69] For locomotion to occur, the symmetry of the system must be broken.14 In addition, collective motion requires a coupling mechanism between the entities that make up the collective. ^[61]

To develop mesoscopic to nanoscopic entities capable of swarming behaviour, it has been hypothesised that the entities are characterised by broken symmetry with a well-defined morphology, and are powered with some material capable of harvesting energy. If the harvested energy results in a field surrounding the object, then this field can couple with the field of a neighbouring object and bring some coordination to the collective behaviour. ^[61]

Emiliania huxleyi (EHUX) coccolithophore-derived asymmetric coccoliths stand out as candidates for the choice of a nano/mesoscopic object with broken symmetry and well-defined morphology. Besides the thermodynamical stability because of their calcite composition, ^[70] the critical advantage of EHUX coccoliths is their distinctive and sophisticated asymmetric morphology. EHUX coccoliths are characterised by several hammer-headed ribs placed to form a proximal and distal disc connected by a central ring. These discs have different sizes but also allow the coccolith to have a curvature, partly resembling a wagon wheel. ^[71] EHUX coccoliths can be isolated from EHUX coccolithophores, a unique group of unicellular marine algae that are the primary producers of biogenic calcite in the ocean. ^[72] Coccolithophores can intracellularly produce intricate three-dimensional mineral structures, such as calcium carbonate scales (i.e., coccoliths), in a process that is driven continuously by a specialized vesicle. ^[73]

Emiliania huxleyi protected with asymmetric coccoliths

After the process is finished, the formed coccoliths are secreted to the cell surface, where they form the exoskeleton (i.e., coccosphere). The broad diversity of coccolith architecture results in further possibilities for specific applications in nanotechnology  ^[74] or biomedicine. ^[75] Inanimate coccoliths from EHUX live coccolithophores, in particular, can be isolated easily in the laboratory with a low culture cost and fast reproductive rate and have a reasonably moderate surface area (~20 m²/g) exhibiting a mesoporous structure (pore size in the range of 4 nm). ^{[76] [61]}

Presumably, if harvesting of energy is done on both sides of the EHUX coccolith, then it will allow generation of a net force, which means movement in a directional manner. Coccoliths have immense potential for a multitude of applications, but to enable harvesting of energy, their surface properties must be finely tuned. ^[77] Inspired by the composition of adhesive proteins in mussels, dopamine self-polymerization into polydopamine is currently the most versatile functionalization strategy for virtually all types of materials. ^[78] Because of its surface chemistry and wide range of light absorption properties, polydopamine is an ideal choice for aided energy harvesting function on inert substrates. ^{[79] [80] [81]} In this work, we aim to exploit the benefits of polydopamine coating to provide advanced energy harvesting functionalities to the otherwise inert and inanimate coccoliths. Polydopamine (PDA has already been shown to induce movement of polystyrene beads because of thermal diffusion effects between the object and the surrounding aqueous solution of up to 2 °C under near-infrared (NIR) light excitation. ^[82] However, no collective behavior has been reported. Here, we prove, for the first time, that polydopamine can act as an active component to induce, under visible light (300–600 nm), collective behavior of a structurally complex, natural, and challenging-to-control architecture such as coccoliths. As a result, the organic-inorganic hybrid combination (coccolith-polydopamine) would enable design of Robocoliths. ^[61]

Dopamine polymerization proceeds in a solution, where it forms small colloidal aggregates that adsorb on the surface of the coccoliths, forming a confluent film. This film is characterized by high roughness, which translates into a high specific surface area and enhanced harvesting of energy. Because of the conjugated nature of the polymer backbone, polydopamine can absorb light over a broad electromagnetic spectrum, including the visible region. ^[61]

As a result, the surface of coccoliths is endowed with a photothermal effect, locally heating and creating convection induced by the presence of PDA. This local convection is coupled with another nearby local convection, which allows coupling between individual Robocoliths, enabling their collective motion (Figure 1). ^[61]

Therefore, when the light encounters the anisometric Robocoliths, they heat locally because of the photothermal conversion induced by the presence of PDA on their surface. The intense local heating produces convection that is different on either side of the Robocolith, causing its observed movement. Such convection can couple with the convection of a neighboring Robocolith, resulting in a "swarming" motion. In addition, the surface of Robocoliths is engineered to accommodate antifouling polymer brushes and potentially prevent their aggregation. Although a primary light-activated convective approach is taken as a first step to understand the motion of Robocoliths, a multitude of mechanistic approaches are currently being developed to pave the way for the next generation of multifunctional Robocoliths as swarming bio-micromachines. ^[61]

Biomedical applications

Biohybrid bacterial microswimmers 

Biohybrid diatomite microswimmer drug delivery system

Diatom frustule surface functionalised with photoactivable molecules (orange spheres) linked to vitamin B-12 (red sphere) acting as a tumor-targeting tag. The system can be loaded with chemotherapeutic drugs (light blue spheres), which can be selectively delivered to colorectal cancer cells. In addition, diatomite microparticles can be photoactivated to generate carbon monoxide or free radicals inducing tumor cell apoptosis.

Biohybrid microswimmers, mainly composed of integrated biological actuators and synthetic cargo carriers, have recently shown promise toward minimally invasive theranostic applications. ^{[86] [87] [88] [22]} Various microorganisms, including bacteria, ^{[23] [28]} microalgae, ^{[89] [19]} and spermatozoids, ^{[90] [91]} have been utilised to fabricate different biohybrid microswimmers with advanced medical functionalities, such as autonomous control with environmental stimuli for targeting, navigation through narrow gaps, and accumulation to necrotic regions of tumor environments. ^[92] Steerability of the synthetic cargo carriers with long-range applied external fields, such as acoustic or magnetic fields, ^{[11] [93]} and intrinsic taxis behaviours of the biological actuators toward various environmental stimuli, such as chemoattractants, ^[94] pH, and oxygen, ^{[95] [18]} make biohybrid microswimmers a promising candidate for a broad range of medical active cargo delivery applications. ^{[92] [83]}

Bacteria have a high swimming speed and efficiency in the low Reynolds (Re) number flow regime, are capable of sensing and responding to external environmental signals, and could be externally detected via fluorescence or ultrasound imaging techniques. ^{[96] [97] [98]} Due to their inherent sensing capabilities, various bacteria species have been investigated as potential anti-tumor agents and have been the subject of preclinical and clinical trials. ^{[99] [100] [101] [102] [103] [104]} The presence of different bacteria species in the human body, such as on the skin and the gut microenvironment, has promoted their use as potential theranostic agents or carriers in several medical applications. ^{[105] [83]}

On the other hand, specialised eukaryotic cells, such as red blood cells (RBCs), are one of the nature's most efficient passive carriers with high payload efficiency, deformability, degradability, and biocompatibility, and have also been used in various medical applications. ^{[106] [107] [108]} RBCs and RBC-derived nanovesicle, such as nanoerythrosomes, ^[109] have been successfully adopted as passive cargo carriers to enhance the circulation time of the applied substances in the body, ^[110] and to deliver different bioactive substances for the treatment of various diseases observed in the liver, spleen and lymph nodes, and also cancer via administrating through intravenous, intraperitoneal, subcutaneous, and inhalational routes. ^{[111] [112] [113] [114] [115]} For instance, decreased recognition of drug-loaded particles by immune cells was shown when attached to membranes of the RBCs prior to intravenous injection into mice. ^[116] Additionally, the altered bioaccumulation profile of nanocarriers was shown when conjugated onto the RBCs, boosting the delivery of nanocarriers to the target organs. ^[117] It was also reported that the half-life of Fasudil, a drug for pulmonary arterial hypertension, inside the body increased approximately sixfold to eightfold when it was loaded into nanoerythrosomes. ^{[115] [83]}

Superior cargo-carrying properties of the RBCs have also generated increased interest for their use in biohybrid microswimmer designs. Recently, active navigation and control of drug and superparamagnetic nanoparticle (SPION)-loaded RBCs were presented using sound waves and magnetic fields. ^[11] RBCs were further utilized in the fabrication of soft biohybrid microswimmers powered by motile bacteria for active cargo delivery applications. ^[93] RBCs, loaded with drug molecules and SPIONs, were propelled by bacteria and steered via magnetic fields, which were also capable of traveling through gaps smaller than their size due to the inherent high deformability of the RBCs. ^[83]

References

1. Kong, Xiangyi; Gao, Peng; Wang, Jing; Fang, Yi; Hwang, Kuo Chu (2023). "Advances of medical nanorobots for future cancer treatments". Journal of Hematology & Oncology. 16 (1): 74. doi: 10.1186/s13045-023-01463-z . PMC   10347767 . PMID   37452423.
2. Schwarz, Lukas; Medina-Sánchez, Mariana; Schmidt, Oliver G. (2017). "Hybrid Bio Micromotors". Applied Physics Reviews. 4 (3): 031301. Bibcode:2017ApPRv...4c1301S. doi: 10.1063/1.4993441 .
3. Bastos-Arrieta, Julio; Revilla-Guarinos, Ainhoa; Uspal, William E.; Simmchen, Juliane (2018). "Bacterial Biohybrid Microswimmers". Frontiers in Robotics and AI. 5: 97. doi: 10.3389/frobt.2018.00097 . PMC   7805739 . PMID   33500976. Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
4. Montemagno, Carlo; Bachand, George (1999). "Constructing nanomechanical devices powered by biomolecular motors". Nanotechnology. 10 (3): 225–231. Bibcode:1999Nanot..10..225M. doi:10.1088/0957-4484/10/3/301. S2CID   250910730.
5. Allen, Roland E.; Lidström, Suzy (2017). "Life, the Universe, and everything—42 fundamental questions". Physica Scripta. 92 (1): 012501. arXiv: 1804.08730 . Bibcode:2017PhyS...92a2501A. doi:10.1088/0031-8949/92/1/012501. S2CID   119444389.
6. Vicsek, Tamás; Zafeiris, Anna (2012). "Collective motion". Physics Reports. 517 (3–4): 71–140. arXiv: 1010.5017 . Bibcode:2012PhR...517...71V. doi:10.1016/j.physrep.2012.03.004. S2CID   119109873.
7. Darnton, Nicholas C.; Turner, Linda; Rojevsky, Svetlana; Berg, Howard C. (2010). "Dynamics of Bacterial Swarming". Biophysical Journal. 98 (10): 2082–2090. Bibcode:2010BpJ....98.2082D. doi:10.1016/j.bpj.2010.01.053. PMC   2872219 . PMID   20483315.
8. Topaz, Chad M.; d'Orsogna, Maria R.; Edelstein-Keshet, Leah; Bernoff, Andrew J. (2012). "Locust Dynamics: Behavioral Phase Change and Swarming". PLOS Computational Biology. 8 (8): e1002642. arXiv: 1207.4968 . Bibcode:2012PLSCB...8E2642T. doi: 10.1371/journal.pcbi.1002642 . PMC   3420939 . PMID   22916003.
9. Corcoran, Aaron J.; Hedrick, Tyson L. (2019). "Compound-V formations in shorebird flocks". eLife. 8. doi: 10.7554/eLife.45071 . PMC   6548498 . PMID   31162047.
10. Purcell, E. M. (1977). "Life at low Reynolds number". American Journal of Physics. 45 (1): 3–11. Bibcode:1977AmJPh..45....3P. doi:10.1119/1.10903.
11. Wu, Zhiguang; Li, Tianlong; Li, Jinxing; Gao, Wei; Xu, Tailin; Christianson, Caleb; Gao, Weiwei; Galarnyk, Michael; He, Qiang; Zhang, Liangfang; Wang, Joseph (2014). "Turning Erythrocytes into Functional Micromotors". ACS Nano. 8 (12): 12041–12048. doi:10.1021/nn506200x. PMC   4386663 . PMID   25415461.
12. Wang, Hong; Pumera, Martin (2015). "Fabrication of Micro/Nanoscale Motors". Chemical Reviews. 115 (16): 8704–8735. doi: 10.1021/acs.chemrev.5b00047 . PMID   26234432.
13. Ricotti, Leonardo; Trimmer, Barry; Feinberg, Adam W.; Raman, Ritu; Parker, Kevin K.; Bashir, Rashid; Sitti, Metin; Martel, Sylvain; Dario, Paolo; Menciassi, Arianna (2017). "Biohybrid actuators for robotics: A review of devices actuated by living cells". Science Robotics. 2 (12): eaaq0495. doi: 10.1126/scirobotics.aaq0495 . PMID   33157905. S2CID   29776467.
14. Alapan, Yunus; Yasa, Oncay; Yigit, Berk; Yasa, I. Ceren; Erkoc, Pelin; Sitti, Metin (2019). "Microrobotics and Microorganisms: Biohybrid Autonomous Cellular Robots". Annual Review of Control, Robotics, and Autonomous Systems. 2: 205–230. doi:10.1146/annurev-control-053018-023803. S2CID   139819519.
15. Chu, Dafeng; Dong, Xinyue; Shi, Xutong; Zhang, Canyang; Wang, Zhenjia (2018). "Neutrophil-Based Drug Delivery Systems". Advanced Materials. 30 (22): e1706245. Bibcode:2018AdM....3006245C. doi:10.1002/adma.201706245. PMC   6161715 . PMID   29577477.
16. Carlsen, Rika Wright; Sitti, Metin (2014). "Bio-Hybrid Cell-Based Actuators for Microsystems". Small. 10 (19): 3831–3851. doi:10.1002/smll.201400384. PMID   24895215.
17. Nguyen, Van Du; Han, Ji-Won; Choi, Young Jin; Cho, Sunghoon; Zheng, Shaohui; Ko, Seong Young; Park, Jong-Oh; Park, Sukho (2016). "Active tumor-therapeutic liposomal bacteriobot combining a drug (Paclitaxel)-encapsulated liposome with targeting bacteria (Salmonella Typhimurium)". Sensors and Actuators B: Chemical. 224: 217–224. Bibcode:2016SeAcB.224..217N. doi:10.1016/j.snb.2015.09.034.
18. Felfoul, Ouajdi; Mohammadi, Mahmood; Taherkhani, Samira; De Lanauze, Dominic; Zhong Xu, Yong; Loghin, Dumitru; Essa, Sherief; Jancik, Sylwia; Houle, Daniel; Lafleur, Michel; Gaboury, Louis; Tabrizian, Maryam; Kaou, Neila; Atkin, Michael; Vuong, Té; Batist, Gerald; Beauchemin, Nicole; Radzioch, Danuta; Martel, Sylvain (2016). "Magneto-aerotactic bacteria deliver drug-containing nanoliposomes to tumour hypoxic regions". Nature Nanotechnology. 11 (11): 941–947. Bibcode:2016NatNa..11..941F. doi:10.1038/nnano.2016.137. PMC   6094936 . PMID   27525475.
19. Yasa, Oncay; Erkoc, Pelin; Alapan, Yunus; Sitti, Metin (2018). "Microalga-Powered Microswimmers toward Active Cargo Delivery". Advanced Materials. 30 (45): e1804130. Bibcode:2018AdM....3004130Y. doi:10.1002/adma.201804130. PMID   30252963. S2CID   52823884.
20. Ceylan, Hakan; Giltinan, Joshua; Kozielski, Kristen; Sitti, Metin (2017). "Mobile microrobots for bioengineering applications". Lab on a Chip. 17 (10): 1705–1724. doi: 10.1039/C7LC00064B . PMID   28480466.
21. Li, Jinxing; Esteban-Fernández De Ávila, Berta; Gao, Wei; Zhang, Liangfang; Wang, Joseph (2017). "Micro/Nanorobots for biomedicine: Delivery, surgery, sensing, and detoxification". Science Robotics. 2 (4): eaam6431. doi:10.1126/scirobotics.aam6431. PMC   6759331 . PMID   31552379.
22. Erkoc, Pelin; Yasa, Immihan C.; Ceylan, Hakan; Yasa, Oncay; Alapan, Yunus; Sitti, Metin (2019). "Mobile Microrobots for Active Therapeutic Delivery". Advanced Therapeutics. 2. doi: 10.1002/adtp.201800064 . S2CID   88204894.
23. Park, Byung-Wook; Zhuang, Jiang; Yasa, Oncay; Sitti, Metin (2017). "Multifunctional Bacteria-Driven Microswimmers for Targeted Active Drug Delivery". ACS Nano. 11 (9): 8910–8923. doi:10.1021/acsnano.7b03207. PMID   28873304.
24. Behkam, Bahareh; Sitti, Metin (2007). "Bacterial flagella-based propulsion and on/Off motion control of microscale objects". Applied Physics Letters. 90 (2): 023902. Bibcode:2007ApPhL..90b3902B. doi:10.1063/1.2431454.
25. Behkam, Bahareh; Sitti, Metin (2008). "Effect of quantity and configuration of attached bacteria on bacterial propulsion of microbeads". Applied Physics Letters. 93 (22): 223901. Bibcode:2008ApPhL..93v3901B. doi:10.1063/1.3040318.
26. Mostaghaci, Babak; Yasa, Oncay; Zhuang, Jiang; Sitti, Metin (2017). "Bioadhesive Bacterial Microswimmers for Targeted Drug Delivery in the Urinary and Gastrointestinal Tracts". Advanced Science. 4 (6). doi:10.1002/advs.201700058. PMC   5473323 . PMID   28638787.
27. Schauer, Oliver; Mostaghaci, Babak; Colin, Remy; Hürtgen, Daniel; Kraus, David; Sitti, Metin; Sourjik, Victor (2018). "Motility and chemotaxis of bacteria-driven microswimmers fabricated using antigen 43-mediated biotin display". Scientific Reports. 8 (1): 9801. Bibcode:2018NatSR...8.9801S. doi:10.1038/s41598-018-28102-9. PMC   6023875 . PMID   29955099.
28. Singh, Ajay Vikram; Hosseinidoust, Zeinab; Park, Byung-Wook; Yasa, Oncay; Sitti, Metin (2017). "Microemulsion-Based Soft Bacteria-Driven Microswimmers for Active Cargo Delivery". ACS Nano. 11 (10): 9759–9769. doi:10.1021/acsnano.7b02082. PMID   28858477.
29. Stanton, Morgan M.; Park, Byung-Wook; Miguel-López, Albert; Ma, Xing; Sitti, Metin; Sánchez, Samuel (2017). "Biohybrid Microtube Swimmers Driven by Single Captured Bacteria". Small. 13 (19). doi:10.1002/smll.201603679. hdl: 2445/123481 . PMID   28299891.
30. Stanton, Morgan M.; Park, Byung-Wook; Vilela, Diana; Bente, Klaas; Faivre, Damien; Sitti, Metin; Sánchez, Samuel (2017). "Magnetotactic Bacteria Powered Biohybrids TargetE. Coli Biofilms". ACS Nano. 11 (10): 9968–9978. doi:10.1021/acsnano.7b04128. hdl: 2445/123493 . PMID   28933815.
31. Akolpoglu, Mukrime Birgul; Dogan, Nihal Olcay; Bozuyuk, Ugur; Ceylan, Hakan; Kizilel, Seda; Sitti, Metin (2020). "High-Yield Production of Biohybrid Microalgae for On-Demand Cargo Delivery". Advanced Science. 7 (16). doi:10.1002/advs.202001256. PMC   7435244 . PMID   32832367. Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
32. Zhuang, Jiang; Park, Byung-Wook; Sitti, Metin (2017). "Propulsion and Chemotaxis in Bacteria-Driven Microswimmers". Advanced Science. 4 (9). doi:10.1002/advs.201700109. PMC   5604384 . PMID   28932674. Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
33. Ozin, G. A.; Manners, I.; Fournier-Bidoz, S.; Arsenault, A. (2005). "Dream Nanomachines". Advanced Materials. 17 (24): 3011–3018. Bibcode:2005AdM....17.3011O. doi:10.1002/adma.200501767. S2CID   55293424.
34. Ismagilov, Rustem F.; Schwartz, Alexander; Bowden, Ned; Whitesides, George M. (2002). "Autonomous Movement and Self-Assembly". Angewandte Chemie International Edition. 41 (4): 652–654. doi: 10.1002/1521-3773(20020215)41:4<652::AID-ANIE652>3.0.CO;2-U .
35. Katuri, Jaideep; Ma, Xing; Stanton, Morgan M.; Sánchez, Samuel (2017). "Designing Micro- and Nanoswimmers for Specific Applications". Accounts of Chemical Research. 50 (1): 2–11. doi:10.1021/acs.accounts.6b00386. PMC   5244436 . PMID   27809479.
36. Vale, R. D.; Milligan, R. A. (2000). "The Way Things Move: Looking Under the Hood of Molecular Motor Proteins". Science. 288 (5463): 88–95. Bibcode:2000Sci...288...88V. doi:10.1126/science.288.5463.88. PMID   10753125.
37. Vogel, Pia D. (2005). "Nature's design of nanomotors". European Journal of Pharmaceutics and Biopharmaceutics. 60 (2): 267–277. doi:10.1016/j.ejpb.2004.10.007. PMID   15939237.
38. Di Leonardo, R.; Angelani, L.; Dell'Arciprete, D.; Ruocco, G.; Iebba, V.; Schippa, S.; Conte, M. P.; Mecarini, F.; De Angelis, F.; Di Fabrizio, E. (2010). "Bacterial ratchet motors". Proceedings of the National Academy of Sciences. 107 (21): 9541–9545. arXiv: 0910.2899 . Bibcode:2010PNAS..107.9541D. doi: 10.1073/pnas.0910426107 . PMC   2906854 . PMID   20457936.
39. Zhang, Zhenhai; Li, Zhifei; Yu, Wei; Li, Kejie; Xie, Zhihong; Shi, Zhiguo (2013). "Propulsion of liposomes using bacterial motors". Nanotechnology. 24 (18): 185103. Bibcode:2013Nanot..24r5103Z. doi:10.1088/0957-4484/24/18/185103. PMID   23579252. S2CID   40359976.
40. Stanton, Morgan M.; Simmchen, Juliane; Ma, Xing; Miguel-López, Albert; Sánchez, Samuel (2016). "Biohybrid Janus Motors Driven by Escherichia coli". Advanced Materials Interfaces. 3 (2). doi:10.1002/admi.201500505. S2CID   138755512.
41. Suh, Seungbeum; Traore, Mahama A.; Behkam, Bahareh (2016). "Bacterial chemotaxis-enabled autonomous sorting of nanoparticles of comparable sizes". Lab on a Chip. 16 (7): 1254–1260. doi:10.1039/C6LC00059B. hdl: 10919/77561 . PMID   26940033.
42. Darnton, Nicholas; Turner, Linda; Breuer, Kenneth; Berg, Howard C. (2004). "Moving Fluid with Bacterial Carpets". Biophysical Journal. 86 (3): 1863–1870. Bibcode:2004BpJ....86.1863D. doi:10.1016/S0006-3495(04)74253-8. PMC   1304020 . PMID   14990512.
43. Behkam, Bahareh; Sitti, Metin (2006). "Towards Hybrid Swimming Microrobots: Bacteria Assisted Propulsion of Polystyrene Beads". 2006 International Conference of the IEEE Engineering in Medicine and Biology Society. Vol. 2006. pp. 2421–2424. doi:10.1109/IEMBS.2006.259841. ISBN   1-4244-0032-5. PMID   17946113. S2CID   6409992.
44. Steager, Edward; Kim, Chang-Beom; Patel, Jigarkumar; Bith, Socheth; Naik, Chandan; Reber, Lindsay; Kim, Min Jun (2007). "Control of microfabricated structures powered by flagellated bacteria using phototaxis". Applied Physics Letters. 90 (26): 263901. Bibcode:2007ApPhL..90z3901S. doi:10.1063/1.2752721.
45. Mahmut Selman Sakar; Steager, Edward B.; Dal Hyung Kim; Agung Julius, A.; Kim, Minjun; Kumar, Vijay; Pappas, George J. (2011). "Modeling, control and experimental characterization of microbiorobots". The International Journal of Robotics Research. 30 (6): 647–658. doi:10.1177/0278364910394227. S2CID   36806.
46. Park, Sung Jun; Bae, Hyeoni; Kim, Joonhwuy; Lim, Byungjik; Park, Jongoh; Park, Sukho (2010). "Motility enhancement of bacteria actuated microstructures using selective bacteria adhesion". Lab on a Chip. 10 (13): 1706–1711. doi:10.1039/c000463d. PMID   20422075.
47. Traoré, Mahama A.; Sahari, Ali; Behkam, Bahareh (2011). "Computational and experimental study of chemotaxis of an ensemble of bacteria attached to a microbead". Physical Review E. 84 (6): 061908. Bibcode:2011PhRvE..84f1908T. doi:10.1103/PhysRevE.84.061908. hdl: 10919/24901 . PMID   22304117.
48. Kim, Hoyeon; Kim, Min Jun (2016). "Electric Field Control of Bacteria-Powered Microrobots Using a Static Obstacle Avoidance Algorithm". IEEE Transactions on Robotics. 32: 125–137. doi:10.1109/TRO.2015.2504370. S2CID   15062290.
49. Singh, Ajay Vikram; Sitti, Metin (2016). "Bacteria-Driven Particles: Patterned and Specific Attachment of Bacteria on Biohybrid Bacteria-Driven Microswimmers (Adv. Healthcare Mater. 18/2016)". Advanced Healthcare Materials. 5 (18): 2306. doi: 10.1002/adhm.201670097 .
50. Lu, Z., and Martel, S. (2006). "Preliminary investigation of bio-carriers using magnetotactic bacteria". In: Engineering in Medicine and Biology Society, 2006. EMBS'06. 28th Annual International Conference of the IEEE (New York, NY: IEEE), 3415–3418.
51. Faivre, Damien; Schüler, Dirk (2008). "Magnetotactic Bacteria and Magnetosomes". Chemical Reviews. 108 (11): 4875–4898. doi:10.1021/cr078258w. PMID   18855486.
52. Martel, Sylvain (2012). "Bacterial microsystems and microrobots". Biomedical Microdevices. 14 (6): 1033–1045. doi:10.1007/s10544-012-9696-x. PMID   22960952. S2CID   2894776.
53. Taherkhani, Samira; Mohammadi, Mahmood; Daoud, Jamal; Martel, Sylvain; Tabrizian, Maryam (2014). "Covalent Binding of Nanoliposomes to the Surface of Magnetotactic Bacteria for the Synthesis of Self-Propelled Therapeutic Agents". ACS Nano. 8 (5): 5049–5060. doi:10.1021/nn5011304. PMID   24684397.
54. Klumpp, Stefan; Lefevre, Christopher; Landau, Livnat; Codutti, Agnese; Bennet, Mathieu; Faivre, Damien (2017). "Magneto-Aerotaxis: Bacterial Motility in Magnetic Fields". Biophysical Journal. 112 (3): 567a. Bibcode:2017BpJ...112..567K. doi: 10.1016/j.bpj.2016.11.3052 .
55. Harris, Elizabeth H. (2001). "Chlamydomonasas Amodelorganism". Annual Review of Plant Physiology and Plant Molecular Biology. 52: 363–406. doi:10.1146/annurev.arplant.52.1.363. PMID   11337403.
56. Weibel, D. B.; Garstecki, P.; Ryan, D.; Diluzio, W. R.; Mayer, M.; Seto, J. E.; Whitesides, G. M. (2005). "Microoxen: Microorganisms to move microscale loads". Proceedings of the National Academy of Sciences. 102 (34): 11963–11967. Bibcode:2005PNAS..10211963W. doi: 10.1073/pnas.0505481102 . PMC   1189341 . PMID   16103369.
57. Hopfner, Ursula; Schenck, Thilo-Ludwig; Chávez, Myra-Noemi; Machens, Hans-Günther; Bohne, Alexandra-Viola; Nickelsen, Jörg; Giunta, Riccardo-Enzo; Egaña, José-Tomás (2014). "Development of photosynthetic biomaterials for in vitro tissue engineering". Acta Biomaterialia. 10 (6): 2712–2717. doi:10.1016/j.actbio.2013.12.055. PMID   24406198.
58. Centeno-Cerdas, Carolina; Jarquín-Cordero, Montserrat; Chávez, Myra Noemi; Hopfner, Ursula; Holmes, Christopher; Schmauss, Daniel; Machens, Hans-Günther; Nickelsen, Jörg; Egaña, José Tomás (2018). "Development of photosynthetic sutures for the local delivery of oxygen and recombinant growth factors in wounds". Acta Biomaterialia. 81: 184–194. doi:10.1016/j.actbio.2018.09.060. PMID   30287280. S2CID   52922420.
59. Schenck, Thilo Ludwig; Hopfner, Ursula; Chávez, Myra Noemi; Machens, Hans-Günther; Somlai-Schweiger, Ian; Giunta, Riccardo Enzo; Bohne, Alexandra Viola; Nickelsen, Jörg; Allende, Miguel L.; Egaña, José Tomás (2015). "Photosynthetic biomaterials: A pathway towards autotrophic tissue engineering". Acta Biomaterialia. 15: 39–47. doi:10.1016/j.actbio.2014.12.012. PMID   25536030.
60. Ng, Wei Ming; Che, Hui Xin; Guo, Chen; Liu, Chunzhao; Low, Siew Chun; Chieh Chan, Derek Juinn; Mohamud, Rohimah; Lim, Jitkang (2018). "Artificial Magnetotaxis of Microbot: Magnetophoresis versus Self-Swimming". Langmuir. 34 (27): 7971–7980. doi:10.1021/acs.langmuir.8b01210. PMID   29882671. S2CID   46953567.
61. Lomora, Mihai; Larrañaga, Aitor; Rodriguez-Emmenegger, Cesar; Rodriguez, Brian; Dinu, Ionel Adrian; Sarasua, Jose-Ramon; Pandit, Abhay (2021). "An engineered coccolith-based hybrid that transforms light into swarming motion". Cell Reports Physical Science. 2 (3): 100373. Bibcode:2021CRPS....200373L. doi:10.1016/j.xcrp.2021.100373. hdl: 10810/52638 . S2CID   233687429. Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
62. Herpich, Tim; Thingna, Juzar; Esposito, Massimiliano (2018). "Collective Power: Minimal Model for Thermodynamics of Nonequilibrium Phase Transitions". Physical Review X. 8 (3): 031056. arXiv: 1802.00461 . Bibcode:2018PhRvX...8c1056H. doi:10.1103/PhysRevX.8.031056. S2CID   89610765.
63. Abendroth, John M.; Bushuyev, Oleksandr S.; Weiss, Paul S.; Barrett, Christopher J. (2015). "Controlling Motion at the Nanoscale: Rise of the Molecular Machines". ACS Nano. 9 (8): 7746–7768. doi: 10.1021/acsnano.5b03367 . PMID   26172380.
64. Wang, Wei; Duan, Wentao; Ahmed, Suzanne; Mallouk, Thomas E.; Sen, Ayusman (2013). "Small power: Autonomous nano- and micromotors propelled by self-generated gradients". Nano Today. 8 (5): 531–554. doi:10.1016/j.nantod.2013.08.009.
65. Zhang, Jianhua; Guo, Jingjing; Mou, Fangzhi; Guan, Jianguo (2018). "Light-Controlled Swarming and Assembly of Colloidal Particles". Micromachines. 9 (2): 88. doi: 10.3390/mi9020088 . PMC   6187466 . PMID   30393364.
66. Di Leonardo, Roberto (2016). "Controlled collective motions". Nature Materials. 15 (10): 1057–1058. doi:10.1038/nmat4761. PMID   27658450.
67. Yang, Guang-Zhong; Bellingham, Jim; Dupont, Pierre E.; Fischer, Peer; Floridi, Luciano; Full, Robert; Jacobstein, Neil; Kumar, Vijay; McNutt, Marcia; Merrifield, Robert; Nelson, Bradley J.; Scassellati, Brian; Taddeo, Mariarosaria; Taylor, Russell; Veloso, Manuela; Wang, Zhong Lin; Wood, Robert (2018). "The grand challenges of Science Robotics". Science Robotics. 3 (14): eaar7650. doi: 10.1126/scirobotics.aar7650 . PMID   33141701. S2CID   3800579.
68. Wang, Wei; Duan, Wentao; Ahmed, Suzanne; Sen, Ayusman; Mallouk, Thomas E. (2015). "From One to Many: Dynamic Assembly and Collective Behavior of Self-Propelled Colloidal Motors". Accounts of Chemical Research. 48 (7): 1938–1946. doi:10.1021/acs.accounts.5b00025. PMID   26057233.
69. Nelson P.C. (2003) "Life in the slow lane: The low Reynolds-number world", In: Biological Physics: Energy, Information, Life, by W.H. Freeman, pages 158–194.
70. Karunadasa K.S.P., C.H. Manoratne, H.M.T.G.A. Pitawala and R.M.G. Rajapakse (2019) "Thermal decomposition of calcium carbonate (calcite polymorph) as examined by in-situ high-temperature X-ray powder diffraction", J. Phys. Chem. Solids, 134: 21–28.
71. Zhai, Peng-Wang; Hu, Yongxiang; Trepte, Charles R.; Winker, David M.; Josset, Damien B.; Lucker, Patricia L.; Kattawar, George W. (2013). "Inherent optical properties of the coccolithophore: Emiliania huxleyi". Optics Express. 21 (15): 17625–17638. Bibcode:2013OExpr..2117625Z. doi: 10.1364/OE.21.017625 . hdl: 11603/24962 . PMID   23938635.
72. Bolton, Clara T.; Hernández-Sánchez, María T.; Fuertes, Miguel-Ángel; González-Lemos, Saúl; Abrevaya, Lorena; Mendez-Vicente, Ana; Flores, José-Abel; Probert, Ian; Giosan, Liviu; Johnson, Joel; Stoll, Heather M. (2016). "Decrease in coccolithophore calcification and CO2 since the middle Miocene". Nature Communications. 7: 10284. Bibcode:2016NatCo...710284B. doi:10.1038/ncomms10284. PMC   4735581 . PMID   26762469.
73. Meldrum, Fiona C.; Cölfen, Helmut (2008). "Controlling Mineral Morphologies and Structures in Biological and Synthetic Systems". Chemical Reviews. 108 (11): 4332–4432. doi:10.1021/cr8002856. PMID   19006397.
74. Skeffington, Alastair W.; Scheffel, André (2018). "Exploiting algal mineralization for nanotechnology: Bringing coccoliths to the fore". Current Opinion in Biotechnology. 49: 57–63. doi: 10.1016/j.copbio.2017.07.013 . PMID   28822276.
75. Lomora, Mihai; Shumate, David; Rahman, Asrizal Abdul; Pandit, Abhay (2019). "Therapeutic Applications of Phytoplankton, with an Emphasis on Diatoms and Coccolithophores". Advanced Therapeutics. 2 (2). doi:10.1002/adtp.201800099. S2CID   139596031.
76. Jakob, Ioanna; Chairopoulou, Makrina Artemis; Vučak, Marijan; Posten, Clemens; Teipel, Ulrich (2017). "Biogenic calcite particles from microalgae-Coccoliths as a potential raw material". Engineering in Life Sciences. 17 (6): 605–612. Bibcode:2017EngLS..17..605J. doi:10.1002/elsc.201600183. PMC   5484330 . PMID   28701909.
77. Kim, Sang Hoon; Nam, Onyou; Jin, Eonseon; Gu, Man Bock (2019). "A new coccolith modified electrode-based biosensor using a cognate pair of aptamers with sandwich-type binding". Biosensors and Bioelectronics. 123: 160–166. doi:10.1016/j.bios.2018.08.021. PMID   30139622. S2CID   206176301.
78. Lee, H.; Dellatore, S. M.; Miller, W. M.; Messersmith, P. B. (2007). "Mussel-Inspired Surface Chemistry for Multifunctional Coatings". Science. 318 (5849): 426–430. Bibcode:2007Sci...318..426L. doi:10.1126/science.1147241. PMC   2601629 . PMID   17947576.
79. Ryu, Ji Hyun; Messersmith, Phillip B.; Lee, Haeshin (2018). "Polydopamine Surface Chemistry: A Decade of Discovery". ACS Applied Materials & Interfaces. 10 (9): 7523–7540. doi:10.1021/acsami.7b19865. PMC   6320233 . PMID   29465221.
80. Schanze, Kirk S.; Lee, Haeshin; Messersmith, Phillip B. (2018). "Ten Years of Polydopamine: Current Status and Future Directions". ACS Applied Materials & Interfaces. 10 (9): 7521–7522. doi: 10.1021/acsami.8b02929 . PMID   29510631.
81. Liu, Yanlan; Ai, Kelong; Lu, Lehui (2014). "Polydopamine and Its Derivative Materials: Synthesis and Promising Applications in Energy, Environmental, and Biomedical Fields". Chemical Reviews. 114 (9): 5057–5115. doi:10.1021/cr400407a. PMID   24517847.
82. Sun, Yunyu; Liu, Ye; Zhang, Dongmei; Zhang, Hui; Jiang, Jiwei; Duan, Ruomeng; Xiao, Jie; Xing, Jingjing; Zhang, Dafeng; Dong, Bin (2019). "Calligraphy/Painting Based on a Bioinspired Light-Driven Micromotor with Concentration-Dependent Motion Direction Reversal and Dynamic Swarming Behavior". ACS Applied Materials & Interfaces. 11 (43): 40533–40542. doi:10.1021/acsami.9b14402. PMID   31577118. S2CID   203638540.
83. Buss, Nicole; Yasa, Oncay; Alapan, Yunus; Akolpoglu, Mukrime Birgul; Sitti, Metin (2020). "Nanoerythrosome-functionalized biohybrid microswimmers". APL Bioengineering. 4 (2): 026103. doi:10.1063/1.5130670. PMC   7141839 . PMID   32548539. Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
84. Delasoie, Joachim; Schiel, Philippe; Vojnovic, Sandra; Nikodinovic-Runic, Jasmina; Zobi, Fabio (25 May 2020). "Photoactivatable Surface-Functionalized Diatom Microalgae for Colorectal Cancer Targeted Delivery and Enhanced Cytotoxicity of Anticancer Complexes". Pharmaceutics. 12 (5). MDPI AG: 480. doi: 10.3390/pharmaceutics12050480 . ISSN   1999-4923. PMC   7285135 . PMID   32466116. Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
85. Tramontano, Chiara; Chianese, Giovanna; Terracciano, Monica; de Stefano, Luca; Rea, Ilaria (2020-09-28). "Nanostructured Biosilica of Diatoms: From Water World to Biomedical Applications". Applied Sciences. 10 (19). MDPI AG: 6811. doi: 10.3390/app10196811 . ISSN   2076-3417. Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
86. Hosseinidoust, Zeinab; Mostaghaci, Babak; Yasa, Oncay; Park, Byung-Wook; Singh, Ajay Vikram; Sitti, Metin (2016). "Bioengineered and biohybrid bacteria-based systems for drug delivery". Advanced Drug Delivery Reviews. 106 (Pt A): 27–44. doi:10.1016/j.addr.2016.09.007. PMID   27641944.
87. Schwarz, Lukas; Medina-Sánchez, Mariana; Schmidt, Oliver G. (2017). "Hybrid Bio Micromotors". Applied Physics Reviews. 4 (3): 031301. Bibcode:2017ApPRv...4c1301S. doi: 10.1063/1.4993441 .
88. Bastos-Arrieta, Julio; Revilla-Guarinos, Ainhoa; Uspal, William E.; Simmchen, Juliane (2018). "Bacterial Biohybrid Microswimmers". Frontiers in Robotics and AI. 5: 97. doi: 10.3389/frobt.2018.00097 . PMC   7805739 . PMID   33500976.
89. Weibel, D. B.; Garstecki, P.; Ryan, D.; Diluzio, W. R.; Mayer, M.; Seto, J. E.; Whitesides, G. M. (2005). "Microoxen: Microorganisms to move microscale loads". Proceedings of the National Academy of Sciences. 102 (34): 11963–11967. Bibcode:2005PNAS..10211963W. doi: 10.1073/pnas.0505481102 . PMC   1189341 . PMID   16103369.
90. Xu, Haifeng; Medina-Sánchez, Mariana; Magdanz, Veronika; Schwarz, Lukas; Hebenstreit, Franziska; Schmidt, Oliver G. (2018). "Sperm-Hybrid Micromotor for Targeted Drug Delivery". ACS Nano. 12 (1): 327–337. arXiv: 1703.08510 . doi: 10.1021/acsnano.7b06398 . PMID   29202221.
91. Chen, Chuanrui; Chang, Xiaocong; Angsantikul, Pavimol; Li, Jinxing; Esteban-Fernández De Ávila, Berta; Karshalev, Emil; Liu, Wenjuan; Mou, Fangzhi; He, Sha; Castillo, Roxanne; Liang, Yuyan; Guan, Jianguo; Zhang, Liangfang; Wang, Joseph (2018). "Chemotactic Guidance of Synthetic Organic/Inorganic Payloads Functionalized Sperm Micromotors". Advanced Biosystems. 2. doi: 10.1002/adbi.201700160 . S2CID   103392074.
92. Alapan, Yunus; Yasa, Oncay; Yigit, Berk; Yasa, I. Ceren; Erkoc, Pelin; Sitti, Metin (2019). "Microrobotics and Microorganisms: Biohybrid Autonomous Cellular Robots". Annual Review of Control, Robotics, and Autonomous Systems. 2: 205–230. doi:10.1146/annurev-control-053018-023803. S2CID   139819519.
93. Alapan, Yunus; Yasa, Oncay; Schauer, Oliver; Giltinan, Joshua; Tabak, Ahmet F.; Sourjik, Victor; Sitti, Metin (2018). "Soft erythrocyte-based bacterial microswimmers for cargo delivery". Science Robotics. 3 (17). doi: 10.1126/scirobotics.aar4423 . PMID   33141741. S2CID   14003685.
94. Zhuang, Jiang; Sitti, Metin (2016). "Chemotaxis of bio-hybrid multiple bacteria-driven microswimmers". Scientific Reports. 6: 32135. Bibcode:2016NatSR...632135Z. doi:10.1038/srep32135. PMC   4995368 . PMID   27555465.
95. Zhuang, Jiang; Wright Carlsen, Rika; Sitti, Metin (2015). "PH-Taxis of Biohybrid Microsystems". Scientific Reports. 5: 11403. Bibcode:2015NatSR...511403Z. doi:10.1038/srep11403. PMC   4466791 . PMID   26073316.
96. Forbes, Neil S. (2010). "Engineering the perfect (Bacterial) cancer therapy". Nature Reviews Cancer. 10 (11): 785–794. doi:10.1038/nrc2934. PMC   3756932 . PMID   20944664.
97. Stanton, Morgan M.; Sánchez, Samuel (2017). "Pushing Bacterial Biohybrids to in Vivo Applications". Trends in Biotechnology. 35 (10): 910–913. doi:10.1016/j.tibtech.2017.04.008. hdl: 2445/123484 . PMID   28501457.
98. Bourdeau, Raymond W.; Lee-Gosselin, Audrey; Lakshmanan, Anupama; Farhadi, Arash; Kumar, Sripriya Ravindra; Nety, Suchita P.; Shapiro, Mikhail G. (2018). "Acoustic reporter genes for noninvasive imaging of microorganisms in mammalian hosts". Nature. 553 (7686): 86–90. Bibcode:2018Natur.553...86B. doi:10.1038/nature25021. PMC   5920530 . PMID   29300010.
99. Cann, S.H., Van Netten, J.P. and Van Netten, C. (2003) "Dr William Coley and tumour regression: a place in history or in the future", Postgraduate Medical Journal, 79(938): 672-680.
100. Felgner, Sebastian; Pawar, Vinay; Kocijancic, Dino; Erhardt, Marc; Weiss, Siegfried (2017). "Tumour-targeting bacteria-based cancer therapies for increased specificity and improved outcome". Microbial Biotechnology. 10 (5): 1074–1078. doi:10.1111/1751-7915.12787. PMC   5609243 . PMID   28771926.
101. Morales, A.; Eidinger, D.; Bruce, A.W. (1976). "Intracavitary Bacillus Calmette-guerin in the Treatment of Superficial Bladder Tumors". Journal of Urology. 116 (2): 180–182. doi:10.1016/S0022-5347(17)58737-6. PMID   820877.
102. Paterson, Yvonne; Guirnalda, Patrick D.; Wood, Laurence M. (2010). "Listeria and Salmonella bacterial vectors of tumor-associated antigens for cancer immunotherapy". Seminars in Immunology. 22 (3): 183–189. doi:10.1016/j.smim.2010.02.002. PMC   4411241 . PMID   20299242.
103. Felgner, Sebastian; Kocijancic, Dino; Frahm, Michael; Weiss, Siegfried (2016). "Bacteria in Cancer Therapy: Renaissance of an Old Concept". International Journal of Microbiology. 2016: 1–14. doi: 10.1155/2016/8451728 . PMC   4802035 . PMID   27051423.
104. Kocijancic, Dino; Felgner, Sebastian; Schauer, Tim; Frahm, Michael; Heise, Ulrike; Zimmermann, Kurt; Erhardt, Marc; Weiss, Siegfried (2017). "Local application of bacteria improves safety of Salmonella-mediated tumor therapy and retains advantages of systemic infection". Oncotarget. 8 (30): 49988–50001. doi:10.18632/oncotarget.18392. PMC   5564822 . PMID   28637010.
105. Maxmen, Amy (2017). "Living therapeutics: Scientists genetically modify bacteria to deliver drugs". Nature Medicine. 23 (1): 5–7. doi:10.1038/nm0117-5. PMID   28060795. S2CID   3989795.
106. Pierigè, F.; Serafini, S.; Rossi, L.; Magnani, M. (2008). "Cell-based drug delivery". Advanced Drug Delivery Reviews. 60 (2): 286–295. doi:10.1016/j.addr.2007.08.029. PMID   17997501.
107. Zhang, Haijun (2016). "Erythrocytes in nanomedicine: An optimal blend of natural and synthetic materials". Biomater. Sci. 4 (7): 1024–1031. doi:10.1039/C6BM00072J. PMID   27090487.
108. Villa, Carlos H.; Anselmo, Aaron C.; Mitragotri, Samir; Muzykantov, Vladimir (2016). "Red blood cells: Supercarriers for drugs, biologicals, and nanoparticles and inspiration for advanced delivery systems". Advanced Drug Delivery Reviews. 106 (Pt A): 88–103. doi:10.1016/j.addr.2016.02.007. PMC   5424548 . PMID   26941164.
109. Guido, Clara; Maiorano, Gabriele; Gutiérrez-Millán, Carmen; Cortese, Barbara; Trapani, Adriana; d'Amone, Stefania; Gigli, Giuseppe; Palamà, Ilaria Elena (2021). "Erythrocytes and Nanoparticles: New Therapeutic Systems". Applied Sciences. 11 (5): 2173. doi: 10.3390/app11052173 .
110. Hu, Che-Ming J.; Fang, Ronnie H.; Zhang, Liangfang (2012). "Erythrocyte-Inspired Delivery Systems". Advanced Healthcare Materials. 1 (5): 537–547. doi:10.1002/adhm.201200138. PMID   23184788. S2CID   205229117.
111. Kim, Sang-Hee; Kim, Eun-Joong; Hou, Joon-Hyuk; Kim, Jung-Mogg; Choi, Han-Gon; Shim, Chang-Koo; Oh, Yu-Kyoung (2009). "Opsonized erythrocyte ghosts for liver-targeted delivery of antisense oligodeoxynucleotides". Biomaterials. 30 (5): 959–967. doi:10.1016/j.biomaterials.2008.10.031. PMID   19027156.
112. Hu, Che-Ming J.; Fang, Ronnie H.; Luk, Brian T.; Chen, Kevin N. H.; Carpenter, Cody; Gao, Weiwei; Zhang, Kang; Zhang, Liangfang (2013). "'Marker-of-self' functionalization of nanoscale particles through a top-down cellular membrane coating approach". Nanoscale. 5 (7): 2664–2668. Bibcode:2013Nanos...5.2664H. doi:10.1039/c3nr00015j. PMC   3667603 . PMID   23462967.
113. Hu, Che-Ming J.; Fang, Ronnie H.; Copp, Jonathan; Luk, Brian T.; Zhang, Liangfang (2013). "A biomimetic nanosponge that absorbs pore-forming toxins". Nature Nanotechnology. 8 (5): 336–340. Bibcode:2013NatNa...8..336H. doi:10.1038/nnano.2013.54. PMC   3648601 . PMID   23584215.
114. Agnihotri, Jaya; Jain, Narendra Kumar (2013). "Biodegradable long circulating cellular carrier for antimalarial drug pyrimethamine". Artificial Cells, Nanomedicine, and Biotechnology. 41 (5): 309–314. doi: 10.3109/21691401.2012.743901 . PMID   23305602. S2CID   22401350.
115. Gupta, Nilesh; Patel, Brijeshkumar; Ahsan, Fakhrul (2014). "Nano-Engineered Erythrocyte Ghosts as Inhalational Carriers for Delivery of Fasudil: Preparation and Characterization". Pharmaceutical Research. 31 (6): 1553–1565. doi:10.1007/s11095-013-1261-7. PMC   5322565 . PMID   24449438.
116. Wibroe, Peter Popp; Anselmo, Aaron C.; Nilsson, Per H.; Sarode, Apoorva; Gupta, Vivek; Urbanics, Rudolf; Szebeni, Janos; Hunter, Alan Christy; Mitragotri, Samir; Mollnes, Tom Eirik; Moghimi, Seyed Moein (2017). "Bypassing adverse injection reactions to nanoparticles through shape modification and attachment to erythrocytes". Nature Nanotechnology. 12 (6): 589–594. Bibcode:2017NatNa..12..589W. doi:10.1038/nnano.2017.47. hdl: 10037/13642 . PMID   28396605.
117. Brenner, Jacob S.; Pan, Daniel C.; Myerson, Jacob W.; Marcos-Contreras, Oscar A.; Villa, Carlos H.; Patel, Priyal; Hekierski, Hugh; Chatterjee, Shampa; Tao, Jian-Qin; Parhiz, Hamideh; Bhamidipati, Kartik; Uhler, Thomas G.; Hood, Elizabeth D.; Kiseleva, Raisa Yu.; Shuvaev, Vladimir S.; Shuvaeva, Tea; Khoshnejad, Makan; Johnston, Ian; Gregory, Jason V.; Lahann, Joerg; Wang, Tao; Cantu, Edward; Armstead, William M.; Mitragotri, Samir; Muzykantov, Vladimir (2018). "Red blood cell-hitchhiking boosts delivery of nanocarriers to chosen organs by orders of magnitude". Nature Communications. 9 (1): 2684. Bibcode:2018NatCo...9.2684B. doi:10.1038/s41467-018-05079-7. PMC   6041332 . PMID   29992966.