Archaerhodopsin

Last updated

Archaerhodopsin proteins are a family of retinal-containing photoreceptors found in the archaea genera Halobacterium and Halorubrum . Like the homologous bacteriorhodopsin (bR) protein, archaerhodopsins harvest energy from sunlight to pump H+ ions out of the cell, establishing a proton motive force that is used for ATP synthesis. They have some structural similarities to the mammalian G protein-coupled receptor protein rhodopsin, but are not true homologs.

Contents

Archaerhodopsins differ from bR in that the claret membrane, in which they are expressed, includes bacterioruberin, a second chromophore thought to protect against photobleaching. Also, bR lacks the omega loop structure observed at the N-terminus of the structures of several archaerhodopsins.

Mutants of Archaerhodopsin-3 (AR3) are used as tools in optogenetics for neuroscience research. [1]

Trimeric complex of archaerhodopsin-2 (PDB: 2EI4). The two gray planes indicate the hydrocarbon boundaries of the lipid bilayer and were calculated with the ANVIL algorithm. 2ei4.gif
Trimeric complex of archaerhodopsin-2 (PDB: 2EI4). The two gray planes indicate the hydrocarbon boundaries of the lipid bilayer and were calculated with the ANVIL algorithm.

Etymology

The term archaerhodopsin is a portmanteau of archaea (the domain in which the proteins are found) and rhodopsin (a photoreceptor responsible for vision in the mammalian eye). [3]

archaea from Ancient Greek ἀρχαῖα (arkhaîa, "ancient"), the plural and neuter form of ἀρχαῖος (arkhaîos, "ancient"). [4]
rhodopsin from Ancient Greek ῥόδον (rhódon, "rose"), because of its pinkish color, and ὄψις (ópsis, "sight"). [5]

History

In the 1960s, a light driven proton pump was discovered in Halobacterium salinarum , and called Bacteriorhodopsin. Over the following years, there were various studies of the membrane of H. salinarum to determine the mechanism of these light-driven proton pumps.

In 1988, another Manabu Yoshida's group at Osaka University reported a novel light-sensitive proton pump from a strain of Halobacterium which they termed Archaerhodopsin. [3] A year later, the same group reported isolating the gene that encodes Archaerhodopsin. [6] [7]

Family members

Seven members of the archaerhodopsin family have been identified to date.

NameAbbr.OrganismGenBankUniProtPDBRef.
Archaerhodopsin-1AR1Halobacterium sp. Aus-1 J05165 P69052 1UAZ [3]
Archaerhodopsin-2AR2Halobacterium sp. Aus-2 S56354 P29563 3WQJ [8]
Archaerhodopsin-3AR3 or ArchHalorubrum sodomense GU045593 P96787 6S6C [9]
Archaerhodopsin-4AR4Halobacterium sp. xz515 AF306937 [10]
Archaerhodopsin-BD1AR-BD1 or HxARHalorubrum xinjiangense AY510709 Q6R5N7 [11]
Archaerhodopsin-HeHeArHalorubrum ejinorense LC073751 [12]
Archaerhodopsin-TP009AR-TP009Halorubrum sp. TP009 [13]

AR1 and AR2

Archaerhodopsin 1 and 2 (AR1 and AR2) were the first archaerhodopsins to be identified and are expressed by Halobacterium sp. Aus-1 and Aus-2 respectively. Both species were first isolated in Western Australia in the late 1980s. [3] [8] [6] The crystal structures of both proteins were solved by Kunio Ihara, Tsutomo Kouyama and co-workers at Nagoya University, together with collaborators at the Spring-8 synchrotron. [14]

AR3/Arch

AR3 is expressed by Halorubrum sodomense. [9] The organism was first identified in the Dead Sea in 1980 and requires a higher concentration of Mg2+ ions for growth than related halophiles. [15] The aop3 gene was cloned by Ihara and colleagues at Nagoya University in 1999 and the protein was found to share 59% sequence identity with bacteriorhodopsin. [9] The crystal structure of AR3 was solved by Anthony Watts at Oxford University and Isabel Moraes at the National Physical Laboratory, together with collaborators at Diamond Light Source. [16]

Mutants of Archaerhodopsin-3 (AR3) are widely used as tools in optogenetics for neuroscience research. [1]

AR3 has recently been introduced as a fluorescent voltage sensor. [17]

AR4

AR4 is expressed in Halobacterium species xz 515. The organism was first identified in a salt lake in Tibet. [10] [18] The gene encoding it was identified by H. Wang and colleagues in 2000. [19] In most bacteriorhodopsin homologs, H+ release to the extracellular medium takes place before a replacement ion is taken up from the cytosolic side of the membrane. Under the acidic conditions found in the organism's native habitat, the order of these stages in the AR4 photocycle is reversed. [20]

AR-BD1

AR-BD1 (also known as HxAR) is expressed by Halorubrum xinjiangense. [11] The organism was first isolated from Xiao-Er-Kule Lake in Xinjiang, China. [21]

HeAr

HeAR is expressed by Halorubrum ejinorense. [12] The organism was first isolated from Lake Ejinor in Inner Mongolia, China. [22]

AR-TP009/ArchT

AR-TP009 is expressed by Halorubrum sp. TP009. Its ability to act as a neural silencer has been investigated in mouse cortical pyramidal neurons. [13]

General features

Occurrence

Archaerhodopsin surface model. Archaerhodopsin tertiary structure surface model.jpg
Archaerhodopsin surface model.

Like other members of the microbial rhodopsin family, archaerhodopsins are expressed in specialised, protein-rich domains of the cell surface membrane, commonly called the claret membrane. In addition to ether lipids, the claret membrane contains bacterioruberin, (a 50-carbon carotenoid pigment) which is thought to protect against photobleaching. Atomic force microscope images of the claret membranes of several archaerhodopsins, show that the proteins are trimeric and are arranged in a hexagonal lattice. [23] Bacterioruberin has also been implicated in oligomerisation and may facilitate protein-protein interactions in the native membrane. [24] [25]

Function

Archaerhodopsins are active transporters, using the energy from sunlight to pump H+ ions out of the cell to generate a proton motive force that is used for ATP synthesis. Removal of the retinal cofactor (e.g. by treatment with hydroxylamine) abolishes the transporter function and dramatically alters the absorption spectra of the proteins. The proton pumping ability of AR3 has been demonstrated in recombinant E. coli cells [26] and of AR4 in liposomes. [20]

In the resting or ground state of archaerhodopsin, the bound retinal is in the all-trans form, but on absorption of a photon of light, it isomerizes to 13-cis. The protein surrounding the chromophore reacts to the change of shape and undergoes an ordered sequence of conformational changes, which are collectively known as the photocycle. These changes alter the polarity of the local environment surrounding titratable amino acid side chains inside the protein, enabling H+ to be pumped from the cytoplasm to the extracellular side of the membrane. The intermediate states of the photocycle may be identified by their absorption maxima. [20] [27]

Structures

Ground or resting state structure of Archaerhodopsin-3 PDB:6S6C. Archaerhodopsin-3 6S6C.gif
Ground or resting state structure of Archaerhodopsin-3 PDB:6S6C.

Crystal structures of the resting or ground states of AR1 (3.4 Å resolution), AR2 (1.8 Å resolution) and AR3 (1.07 and 1.3 Å) have been deposited in the Protein Data Bank. [14] [28] [16] Proteins possess seven transmembrane α-helices and a two-stranded extracellular-facing β-sheet. Retinal is covalently bonded via Schiff base to a lysine residue on helix G. [14] [16] [note 1] The conserved DLLxDGR sequence, close to the extracellular-facing N-terminus of both proteins, forms a tightly curved omega loop that has been implicated in bacterioruberin binding. [24] The cleavage of the first 6 amino acids and the conversion of Gln7 to a pyroglutamate (PCA) residue was also observed in AR3, as previously reported for bacteriorhodopsin. [16]

Use in research

Archaerhodopsins drive the hyperpolarization of the cell membrane by secreting protons in presence of light, thereby inhibiting action potential firing of neurons. [29] This process is associated with an increase in extracellular H+ (i.e. decreased pH linked to the activity of these proteins. These characteristics allow for Archaerhodopsins to be commonly used tools for optogenetic studies as they behave as transmission inhibition factors in presence of light. [30] When expressed within intracellular membranes, the proton pump activity increases the cytosolic pH, this functionality can be used for optogenetic acidification of lysosomes and synaptic vesicles when targeted to these organelles. [31]

Notes

  1. ↑ Helix G is the nearest transmembrane helix to the C-terminus.

Related Research Articles

<span class="mw-page-title-main">Rhodopsin</span> Light-sensitive receptor protein

Rhodopsin, also known as visual purple, is a protein encoded by the RHO gene and a G-protein-coupled receptor (GPCR). It is the opsin of the rod cells in the retina and a light-sensitive receptor protein that triggers visual phototransduction in rods. Rhodopsin mediates dim light vision and thus is extremely sensitive to light. When rhodopsin is exposed to light, it immediately photobleaches. In humans, it is regenerated fully in about 30 minutes, after which the rods are more sensitive. Defects in the rhodopsin gene cause eye diseases such as retinitis pigmentosa and congenital stationary night blindness.

<span class="mw-page-title-main">Bacteriorhodopsin</span> Protein used by single-celled organisms

Bacteriorhodopsin (Bop) is a protein used by Archaea, most notably by haloarchaea, a class of the Euryarchaeota. It acts as a proton pump; that is, it captures light energy and uses it to move protons across the membrane out of the cell. The resulting proton gradient is subsequently converted into chemical energy.

<span class="mw-page-title-main">Retinal</span> Chemical compound

Retinal is a polyene chromophore. Retinal, bound to proteins called opsins, is the chemical basis of visual phototransduction, the light-detection stage of visual perception (vision).

<span class="mw-page-title-main">Proteorhodopsin</span> Family of transmembrane proteins

Proteorhodopsin is a family of transmembrane proteins that use retinal as a chromophore for light-mediated functionality, in this case, a proton pump. pRhodopsin is found in marine planktonic bacteria, archaea and eukaryotes (protae), but was first discovered in bacteria.

<span class="mw-page-title-main">Opsin</span> Class of light-sensitive proteins

Animal opsins are G-protein-coupled receptors and a group of proteins made light-sensitive via a chromophore, typically retinal. When bound to retinal, opsins become retinylidene proteins, but are usually still called opsins regardless. Most prominently, they are found in photoreceptor cells of the retina. Five classical groups of opsins are involved in vision, mediating the conversion of a photon of light into an electrochemical signal, the first step in the visual transduction cascade. Another opsin found in the mammalian retina, melanopsin, is involved in circadian rhythms and pupillary reflex but not in vision. Humans have in total nine opsins. Beside vision and light perception, opsins may also sense temperature, sound, or chemicals.

Channelrhodopsins are a subfamily of retinylidene proteins (rhodopsins) that function as light-gated ion channels. They serve as sensory photoreceptors in unicellular green algae, controlling phototaxis: movement in response to light. Expressed in cells of other organisms, they enable light to control electrical excitability, intracellular acidity, calcium influx, and other cellular processes. Channelrhodopsin-1 (ChR1) and Channelrhodopsin-2 (ChR2) from the model organism Chlamydomonas reinhardtii are the first discovered channelrhodopsins. Variants that are sensitive to different colors of light or selective for specific ions have been cloned from other species of algae and protists.

<i>Halobacterium</i> Genus of archaea

Halobacterium is a genus in the family Halobacteriaceae.

<span class="mw-page-title-main">Electrochemical gradient</span> Gradient of electrochemical potential, usually for an ion that can move across a membrane

An electrochemical gradient is a gradient of electrochemical potential, usually for an ion that can move across a membrane. The gradient consists of two parts:

<span class="mw-page-title-main">Halorhodopsin</span> Family of transmembrane proteins


Halorhodopsin is a seven-transmembrane retinylidene protein from microbial rhodopsin family. It is a chloride-specific light-activated ion pump found in archaea known as halobacteria. It is activated by green light wavelengths of approximately 578nm. Halorhodopsin also shares sequence similarity to channelrhodopsin, a light-gated ion channel.

Retinylidene proteins, or rhodopsins in a broad sense, are proteins that use retinal as a chromophore for light reception. They are the molecular basis for a variety of light-sensing systems from phototaxis in flagellates to eyesight in animals. Retinylidene proteins include all forms of opsin and rhodopsin. While rhodopsin in the narrow sense refers to a dim-light visual pigment found in vertebrates, usually on rod cells, rhodopsin in the broad sense refers to any molecule consisting of an opsin and a retinal chromophore in the ground state. When activated by light, the chromophore is isomerized, at which point the molecule as a whole is no longer rhodopsin, but a related molecule such as metarhodopsin. However, it remains a retinylidene protein. The chromophore then separates from the opsin, at which point the bare opsin is a retinylidene protein. Thus, the molecule remains a retinylidene protein throughout the phototransduction cycle.

<i>Halobacterium salinarum</i> Species of archaeon

Halobacterium salinarum, formerly known as Halobacterium cutirubrum or Halobacterium halobium, is an extremely halophilic marine obligate aerobic archaeon. Despite its name, this is not a bacterium, but a member of the domain Archaea. It is found in salted fish, hides, hypersaline lakes, and salterns. As these salterns reach the minimum salinity limits for extreme halophiles, their waters become purple or reddish color due to the high densities of halophilic Archaea. H. salinarum has also been found in high-salt food such as salt pork, marine fish, and sausages. The ability of H. salinarum to survive at such high salt concentrations has led to its classification as an extremophile.

<span class="mw-page-title-main">Retinalophototroph</span>

A retinalophototroph is one of two different types of phototrophs, and are named for retinal-binding proteins they utilize for cell signaling and converting light into energy. Like all phototrophs, retinalophototrophs absorb photons to initiate their cellular processes. In contrast with chlorophototrophs, retinalophototrophs do not use chlorophyll or an electron transport chain to power their chemical reactions. This means retinalophototrophs are incapable of traditional carbon fixation, a fundamental photosynthetic process that transforms inorganic carbon into organic compounds. For this reason, experts consider them to be less efficient than their chlorophyll-using counterparts, chlorophototrophs.

Halorubrum is a genus in the family Halorubraceae. Halorubrum species are usually halophilic and can be found in waters with high salt concentration such as the Dead Sea or Lake Zabuye.

Optogenetics is a biological technique to control the activity of neurons or other cell types with light. This is achieved by expression of light-sensitive ion channels, pumps or enzymes specifically in the target cells. On the level of individual cells, light-activated enzymes and transcription factors allow precise control of biochemical signaling pathways. In systems neuroscience, the ability to control the activity of a genetically defined set of neurons has been used to understand their contribution to decision making, learning, fear memory, mating, addiction, feeding, and locomotion. In a first medical application of optogenetic technology, vision was partially restored in a blind patient with Retinitis pigmentosa.

<span class="mw-page-title-main">Sensory rhodopsin II</span>

Sensory rhodopsin II (SRII), also known as pharaonis phoborhodopsin (ppR), is a membrane protein of archaea, responsible generating the phototaxis signal. Sensory rhodopsin II is found in Halobacterium salinarum and Natronomonas pharaonis.

Halobacterium noricense is a halophilic, rod-shaped microorganism that thrives in environments with salt levels near saturation. Despite the implication of the name, Halobacterium is actually a genus of archaea, not bacteria. H. noricense can be isolated from environments with high salinity such as the Dead Sea and the Great Salt Lake in Utah. Members of the Halobacterium genus are excellent model organisms for DNA replication and transcription due to the stability of their proteins and polymerases when exposed to high temperatures. To be classified in the genus Halobacterium, a microorganism must exhibit a membrane composition consisting of ether-linked phosphoglycerides and glycolipids.

<span class="mw-page-title-main">Peter Hegemann</span> German biophysicist

Peter Hegemann is a Hertie Senior Research Chair for Neurosciences and a professor of Experimental Biophysics at the Department of Biology, Faculty of Life Sciences, Humboldt University of Berlin, Germany. He is known for his discovery of channelrhodopsin, a type of ion channels regulated by light, thereby serving as a light sensor. This created the field of optogenetics, a technique that controls the activities of specific neurons by applying light. He has received numerous accolades, including the Rumford Prize, the Shaw Prize in Life Science and Medicine, and the Albert Lasker Award for Basic Medical Research.

<span class="mw-page-title-main">Microbial rhodopsin</span> Retinal-binding proteins

Microbial rhodopsins, also known as bacterial rhodopsins, are retinal-binding proteins that provide light-dependent ion transport and sensory functions in halophilic and other bacteria. They are integral membrane proteins with seven transmembrane helices, the last of which contains the attachment point for retinal.

The lysosomal cystine transporter (LCT) family is part of the TOG Superfamily and includes secondary transport proteins that are derived from animals, plants, fungi and other eukaryotes. They exhibit 7 putative transmembrane α-helical spanners (TMSs) and vary in size between about 200 and 500 amino acyl residues, although most have between 300 and 400 residues.

Dieter Oesterhelt was a German biochemist. From 1980 until 2008, he was director of the Max Planck Institute for Biochemistry, Martinsried.

References

  1. 1 2 Flytzanis NC, Bedbrook CN, Chiu H, Engqvist MK, Xiao C, Chan KY, Sternberg PW, Arnold FH, Gradinaru V (2014). "Archaerhodopsin variants with enhanced voltage-sensitive fluorescence in mammalian and Caenorhabditis elegans neurons". Nature Communications. 5: 4894. Bibcode:2014NatCo...5.4894F. doi:10.1038/ncomms5894. PMC   4166526 . PMID   25222271.
  2. ↑ Postic, Guillaume; Ghouzam, Yassine; Guiraud, Vincent; Gelly, Jean-Christophe (2016). "Membrane positioning for high- and low-resolution protein structures through a binary classification approach". Protein Engineering, Design and Selection. 29 (3): 87–91. doi: 10.1093/protein/gzv063 . PMID   26685702.
  3. 1 2 3 4 Mukohata Y, Sugiyama Y, Ihara K, Yoshida M (March 1988). "An Australian halobacterium contains a novel proton pump retinal protein: archaerhodopsin". Biochemical and Biophysical Research Communications. 151 (3): 1339–45. doi:10.1016/S0006-291X(88)80509-6. PMID   2833260.
  4. ↑ Archaea in Wiktionary The free dictionary
  5. ↑ Rhodopsin in Wiktionary The free dictionary
  6. 1 2 Sugiyama Y, Maeda M, Futai M, Mukuhata Y (1989). "Isolation of a Gene That Encodes a New Retinal Protein, Archaerhodopsin, From Halobacterium Sp. Aus-1". J. Biol. Chem. 264 (35): 20859–62. doi: 10.1016/S0021-9258(19)30014-6 . PMID   2592356.
  7. ↑ Oren, A (1994). "Enzyme diversity in halophilic archaea" (PDF). Microbiología. 10 (3): 217–228. PMID   7873098. Archived from the original (PDF) on 4 July 2012. Retrieved 8 April 2018.
  8. 1 2 Uegaki K, Sugiyama Y, Mukohata Y (April 1991). "Archaerhodopsin-2, from Halobacterium sp. aus-2 further reveals essential amino acid residues for light-driven proton pumps". Archives of Biochemistry and Biophysics. 286 (1): 107–10. doi:10.1016/0003-9861(91)90014-A. PMID   1654776.
  9. 1 2 3 Ihara K, Umemura T, Katagiri I, Kitajima-Ihara T, Sugiyama Y, Kimura Y, Mukohata Y (January 1999). "Evolution of the archaeal rhodopsins: evolution rate changes by gene duplication and functional differentiation". Journal of Molecular Biology. 285 (1): 163–74. doi:10.1006/jmbi.1998.2286. PMID   9878396.
  10. 1 2 Li Q, Sun Q, Zhao W, Wang H, Xu D (June 2000). "Newly isolated archaerhodopsin from a strain of Chinese halobacteria and its proton pumping behavior". Biochimica et Biophysica Acta (BBA) - Biomembranes. 1466 (1–2): 260–6. doi:10.1016/S0005-2736(00)00188-7. PMID   10825447.
  11. 1 2 Geng X, Dai G, Chao L, Wen D, Kikukawa T, Iwasa T (2019). "Two consecutive polar amino acids at the end of helix E are important for fast turnover of the archaerhodopsin photocycle". Photochemistry and Photobiology. 95 (4): 980–989. doi: 10.1111/php.13072 . PMID   30548616. S2CID   56484521.
  12. 1 2 Chaoluomeng, Dai G, Kikukawa T, Ihara K, Iwasa T (2015). "Microbial Rhodopsins of Halorubrum Species Isolated From Ejinoor Salt Lake in Inner Mongolia of China". Photochem. Photobiol. Sci. 14 (11): 1974–82. doi: 10.1039/c5pp00161g . PMID   26328780.
  13. 1 2 Xue H, Chow BY, Zhou H, Klapoetke NC, Chuong A, Rajimehr R, Yang A, Baratta MV, Winkle J, Desimone R, Boyden ES (2011). "A high-light sensitivity optical neural silencer: Development and application to optogenetic control of non-human primate cortex". Frontiers in Systems Neuroscience. 5 (18): 1–8. doi: 10.3389/fnsys.2011.00018 . PMC   3082132 . PMID   21811444.
  14. 1 2 3 Enami N, Yoshimura K, Murakami M, Okumura H, Ihara K, Kouyama T (2006). "Crystal Structures of Archaerhodopsin-1 and -2: Common structural motif in archaeal light-driven proton pumps". J. Mol. Biol. 358 (3): 675–685. doi:10.1016/j.jmb.2006.02.032. PMID   16540121.
  15. ↑ Oren A (1983). "Halobacterium sodomense sp. nov. a Dead Sea Halobacterium with an extremely high magnesium requirement". International Journal of Systematic Bacteriology. 33 (2): 381–386. doi: 10.1099/00207713-33-2-381 .
  16. 1 2 3 4 5 Bada Juarez JF, Judge PJ, Adam S, Axford D, Vinals J, Birch J, Kwan TO, Hoi KK, Yen HY, Vial A, Milhiet PE, Robinson CV, Schapiro I, Moraes I, Watts A (2021). "Structures of the archaerhodopsin 3 transporter reveal that disordering of internal water networks underpins receptor sensitization". Nature Communications. 12 (1): 629. Bibcode:2021NatCo..12..629B. doi:10.1038/s41467-020-20596-0. PMC   7840839 . PMID   33504778.
  17. ↑ Kralj JM, Douglass AD, Hochbaum DR, Maclaurin D, Cohen AE (November 2011). "Optical recording of action potentials in mammalian neurons using a microbial rhodopsin". Nature Methods. 9 (1): 90–5. doi:10.1038/nmeth.1782. PMC   3248630 . PMID   22120467.
  18. ↑ Wang Y, Ma D, Zhao Y, Ming M, Wu J, Ding J (2012). "Light-driven proton pumps of archaerhodopsin and bacteriorhodopsin & polymer-matrix composite materials of those functional proteins". Acta Polymerica Sinica. 12 (7): 698–713. doi: 10.3724/SP.J.1105.2012.12051 .
  19. ↑ Wang, S. Zhan, Q. Sun, D. Xu, W. Zhao, W. Huang, Q. Li., 2000. Primary structure of helix C to helix G of a new retinal protein in H.sp.xz515. Chin. Sci. Bull., 45: 1108-1113.
  20. 1 2 3 Ming M, Lu M, Balashov SP, Ebrey TG, Li Q, Ding J (2006). "pH Dependence of Light-Driven Proton Pumping by an Archaerhodopsin From Tibet: Comparison With Bacteriorhodopsin". Biophys. J. 90 (9): 3322–32. Bibcode:2006BpJ....90.3322M. doi:10.1529/biophysj.105.076547. PMC   1432102 . PMID   16473896.
  21. ↑ Feng J, Zhou PJ, Liu SJ (2004). "Halorubrum xinjiangense sp. nov., a novel halophile isolated from saline lakes in China". International Journal of Systematic and Evolutionary Microbiology. 54 (5): 1789–1791. doi: 10.1099/ijs.0.63209-0 . PMID   15388744.
  22. ↑ Castillo AM, Gutiérrez MC, Kamekura M, Xue Y, Ma Y, Cowan DA, Jones BE, Grant WD, Ventosa A (2007). "Halorubrum Ejinorense Sp. Nov., Isolated From Lake Ejinor, Inner Mongolia, China". International Journal of Systematic and Evolutionary Microbiology. 57 (11): 2538–2542. doi: 10.1099/ijs.0.65241-0 . PMID   17978215.
  23. ↑ Tang L, Sun Q, Li Q, Huang Y, Wei Q, Zhang Y, Hu J, Zhang Z (2001). "Imaging bacteriorhodopsinlike molecules of claretmembranes from Tibet halobacteria xz515 by atomic force microscope". Chinese Science Bulletin. 46 (22): 1897–1900. Bibcode:2001ChSBu..46.1897T. doi:10.1007/BF02901167. S2CID   96378194.
  24. 1 2 Yoshimura K, Kouyama T (2008). "Structural Role of Bacterioruberin in the Trimeric Structure of Archaerhodopsin-2". Journal of Molecular Biology. 375 (5): 1267–81. doi:10.1016/j.jmb.2007.11.039. PMID   18082767.
  25. ↑ Chao S, Ding X, Cui H, Yang Y, Chen S, Watts A, Zhao X (2018). "In Situ Study of the Function of Bacterioruberin in the Dual-Chromophore Photoreceptor Archaerhodopsin-4". Angew. Chem. 57 (29): 8937–8941. doi:10.1002/anie.201803195. PMID   29781190.
  26. ↑ Gunapathy S, Kratx S, Chen Q, Hellingwerf K, de Groot H, Rothschild K, de Grip W (2019). "Redshifted and Near-infrared Active Analog Pigments Based upon Archaerhodopsin-3". Photochemistry and Photobiology. 95 (4): 959–968. doi:10.1111/php.13093. PMC   6849744 . PMID   30860604.
  27. ↑ Geng X, Dai G, Chao L, Wen D, Kikukawa T, Iwasa T (2019). "Two Consecutive Polar Amino Acids at the End of Helix E are Important for Fast Turnover of the Archaerhodopsin Photocycle". Photochemistry and Photobiology. 95 (4): 980–989. doi: 10.1111/php.13072 . PMID   30548616. S2CID   56484521.
  28. ↑ Kouyama T, Fujii R, Kanada S, Nakanishi T, Chan SK, Midori M (2014). "Structure of archaerhodopsin-2 at 1.8 Å Resolution". Acta Crystallogr D. 70 (10): 2692–701. doi:10.1107/S1399004714017313. PMC   4188009 . PMID   25286853.
  29. ↑ Chow BY, Han X, Dobry AS, Qian X, Chuong AS, Li M, Henninger MA, Belfort GM, Lin Y, Monahan PE, Boyden ES (January 2010). "High-performance genetically targetable optical neural silencing by light-driven proton pumps". Nature. 463 (7277): 98–102. Bibcode:2010Natur.463...98C. doi:10.1038/nature08652. PMC   2939492 . PMID   20054397.
  30. ↑ El-Gaby M, Zhang Y, Wolf K, Schwiening CJ, Paulsen O, Shipton OA (2016). "Archaerhodopsin Selectively and Reversibly Silences Synaptic Transmission through Altered pH". Cell Reports. 16 (8): 2259–68. doi:10.1016/j.celrep.2016.07.057. PMC   4999416 . PMID   27524609.
  31. ↑ Rost BR, Schneider F, Grauel MK, Wozny C, Bentz C, Blessing A, Rosenmund T, Jentsch TJ, Schmitz D, Hegemann P, Rosenmund C (December 2015). "Optogenetic acidification of synaptic vesicles and lysosomes". Nature Neuroscience. 18 (12): 1845–1852. doi:10.1038/nn.4161. PMC   4869830 . PMID   26551543.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.