Kiss-and-run fusion

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Kiss-and-run fusion is a type of synaptic vesicle release where the vesicle opens and closes transiently. In this form of exocytosis, the vesicle docks and transiently fuses at the presynaptic membrane and releases its neurotransmitters across the synapse, after which the vesicle can then be reused. [1] [2]

Contents

Kiss-and-run differs from full fusion, where the vesicle collapses fully into the plasma membrane and is then later retrieved by a clathrin-coat-dependent process. [3] The idea that neurotransmitter might be released in "quanta" by the fusion of synaptic vesicles with the presynaptic membrane was first introduced by Bernard Katz and Jose del Castillo in 1955, when the first EM images of nerve terminals first appeared. The possibility of transient fusion and rapid retrieval of vesicle membrane was proposed by Bruno Ceccarelli in 1973, after examining in the electron microscope strongly stimulated frog neuromuscular junctions, and indirectly supported by the work of his group in the following years, using electrophysiology, electron microscopy and quick freezing techniques. The actual term, kiss-and-run, was introduced by Ceccarelli's collaborators [2] after the first studies of simultaneous membrane capacitance and amperometric transmitter release measurements were performed and indicated that secretory products could actually be released during transient vesicle fusion. [4] Today, there is back and forth debate over full fusion and kiss-and-run fusion and which model portrays a more accurate picture of the mechanisms behind synaptic release. [5] The increased accumulation of partially empty secretory vesicles following secretion, observed in electron micrographs are the most compelling evidence in favor of the kiss-and-run model. Accumulation of partially empty vesicles following secretion suggests that during the secretory process, only a portion of the vesicular contents are able to exit the cell, which could only be possible if secretory vesicles were to temporarily establish continuity with the cell plasma membrane, expel a portion of their contents, then detach and reseal.

Discovery

Transient vesicle fusion was hypothesized by Katz and del Castillo in 1955.[ citation needed ] However, the first systematic studies were conducted by Ceccarelli et al. in 1973. Ceccarelli et al. studied frog neuromuscular junctions, stimulating them with markers such as horseradish peroxidase to identify endocytosed organelles, and using either mild stimulation (2 Hz) or strong stimulation (10 Hz) protocols for periods ranging from 20 minutes to 4 hours. [1] [6] At low stimulation for a period of 4 hours, Ceccarelli et al. found that there was an increase in horseradish peroxidase labeled vesicles over time, and no increases in large organelles, indicative of the vesicles fusing quickly with the presynaptic membrane and then separating from it after releasing its neurotransmitters. [1] They hypothesized that at low frequencies of stimulation, most of the vesicles are quickly re-formed from the presynaptic membrane during and after stimulation. [1] Further studies in Ceccarelli's lab accumulated evidence on the hypothesis of transient fusion by comparing electrophysiological and morphological data. In particular, images of vesicle fusions were examined on freeze-fractured presynaptic membranes and on electron-microscope images obtained from terminals quick-frozen few ms after the delivery of a single shock to the nerve. [7] In 1993 Alvarez de Toledo and colleagues directly demonstrated the occurrence of secretory product release during the momentary opening of a transiently fusng vesicle, by combining the measurement of membrane capacitance (that monitors changes in surface area) with amperometric detection of the release of mediators. [4] This led Fesce et al. [2] to recapitulate all the indirect evidence in favor of transient fusion and coin the term kiss-and-run. The most compelling evidence for transient or kiss-and-run fusion has come from the discovery of the porosome, [8] a permanent cup-shaped lipoprotein structure at the cell plasma membrane, where secretory vesicles transiently dock and fuse to release intra-vesicular contents from the cell.

Evidence for kiss-and-run

With the discovery of the kiss-and-run mechanism by Ceccarelli et al., there have been many subsequent studies done that give evidence supporting kiss-and-run fusion. All studies have suggested that there are two main advantages kiss-and-run fusion has over full fusion: 1) kiss-and-run enables more efficient vesicle recycling and 2) kiss-and-run can limit how much neurotransmitter is released due to a smaller fusion pore and a shorter time during which neurotransmitters can actually be released. One of the major problems of kiss-and-run evidence, and subsequently the basis for many counterarguments against kiss-and-run, is that because fusion is so short, it is very hard to capture an actual kiss-and-run event. [9] However, accumulation of partially empty vesicles following secretion strongly favors the kiss-and-run mechanism, suggesting that during the secretory process, only a portion of the vesicular contents are able to exit the cell, which could only be possible if secretory vesicles were to temporarily establish continuity with the cell plasma membrane, expel a portion of their contents, then detach and reseal. Since porosomes are permanent structures at the cell plasma membrane measuring just a fraction of the secretory vesicle size, demonstrates that secretory vesicles "transiently" dock and establish continuity, as opposed to complete collapse.

Rat pancreatic beta cells

Rat pancreatic beta cells release neurotransmitters through kiss-and-run fusion. In endocrine and neuroendocrine cells, synaptic-like vesicles (SLVs) undergo kiss-and-run, but it's been controversial whether large dense-core vesicles (LDCVs) also undergo kiss-and-run. [10] Studies have shown that LDCVs do undergo kiss-and-run exocytosis. [10] [11] MacDonald et al. used multiple approaches to test for kiss-and-run exocytosis in rat beta cells. By monitoring membrane patches of intact rat beta cells in the presence of 10 mM glucose and 5 mM forskolin, MacDonald et al. found that some vesicles underwent kiss-and-run, as seen by an exocytotic event followed by an endocytotic event of a similar magnitude. [10] Kiss-and-run events accounted for 25% of LDCV exocytosis and 28% of SLV exocytosis. [10] While LDCV kiss-and-run occurred 25% of the time in the presence of forskolin, in the absence of forskolin, LDCV kiss-and-run fusion occurred only 7% of the time. [10] Because forskolin raises cyclic AMP (cAMP) levels, cAMP seemingly plays a very important role in the mechanism in LDCV kiss-and-run fusion in rat pancreatic beta cells.

SLV (pore diameter: 0.8 +/- 0.1 nm) and LDCV (pore diameter: 1.4 +/- 0.1 nm) fusion pores during kiss-and-run have been shown to be big enough to allow for efflux of gamma-aminobutyric acid (GABA) and adenosine triphosphate (ATP), but are too small to release insulin in rat pancreatic beta cells. [10] Thus, the kiss-and-run mechanism could be implicated in medical complications involving insulin.

Hippocampal synapses

Kiss-and-run exocytosis has been shown to occur at the synapses of neurons located in the hippocampus. Studies using FM1-43, an amphiphile dye inserted into the vesicles or membrane as a marker, have been instrumental in supporting kiss-and-run in hippocampal synapses. In hippocampal synapses, vesicles have been shown to allow the normal release of glutamate, an excitatory neurotransmitter in the brain, without permitting FM1-43 dye to enter or escape from the vesicle, indicating a transient mechanism suggestive of kiss-and-run. [12] Increases in osmolarity have also been shown to permit less dye release in hippocampal synapses. In varying hypertonic solutions, 70% more FM1-43 dye was released from vesicles stimulated in 0.5 osM than from vesicles stimulated in 1.5 osM. [12] Vesicles located in hypertonic regions of the body therefore might be more likely to undergo a kiss-and-run mode of exocytosis.

Mitochondria

Mitochondria demonstrate kiss-and-run fusion in exchanging inner membrane materials. Studies using mitochondrial matrix-targeted green-photoactivated, red-fluorescent KFP and cyan-photoactivated, green-fluorescence PAGFP in rat cells have shown interactions where the KFP and PAGFP were transferred from one mitochondrion to another mitochondrion through transient fusion, suggesting a kiss-and-run mechanism. [13] Unlike full fusion of mitochondria, which resulted in a single organelle, transient kiss-and-run fusion of two mitochondria resulted in two distinct membranes. [13]

Manipulation of the optic atrophy 1 (Opa1) gene had interesting effects on fusion between mitochondria. Silencing the Opa1 gene decreased full fusion activity of mitochondria after 24 hours, and full fusion activity was completely eliminated after the Opa1 gene was silenced for 48 hours. [13] Transient kiss-and-run fusion activity remained the same after 24 hours of Opa1 silencing. [13] Kiss-and-run fusion is most common with low levels of Opa1 gene expression and extremely high levels of Opa1 gene expression. As a result, Opa1 expression governs fusion in mitochondria with regard to kiss-and-run.

Kiss-and-run fusion in mitochondria help to keep mitochondria in a reduced motility state for shorter period of time compared to full fusion. Liu et al. tested both kiss-and-run and full fusion and their effects on mitochondrial motility, and found that both forms of fusion resulted in decreased mitochondrial motility at first, but kiss-and-run fusion restored, and even increased, mitochondrial motility immediately after the kiss-and-run event was over. [13] Kiss-and-run fusion provides a better mechanism to control mitochondrial bioenergetics than full fusion.

Regulation

Calcium-dependent actin coating

Kiss-and-run fusion has been thought to be stabilized by an actin coating of vesicles. Testing for the vesicle uptake of FM1-43 to note when vesicles fused with the membrane allowed researchers to notice that actin coating is a necessary step for the kiss-and-run mechanism. Vesicles labelled with the Beta-actin-green fluorescent protein (GFP) fluoresced seconds after fusing with the presynaptic membrane (as shown by FM1-43 uptake), but non-fused vesicles never fluoresced, suggesting that an actin coating is required for kiss-and-run. [14] This actin coating came from the polymerization of actin monomers.

The actin coating process necessary for transient kiss-and-run fusion is mediated by calcium. Actin coating of vesicles was inhibited by BAPTA-AM, which removes calcium. With the absence of calcium through the use of BAPTA-AM, all fused vesicles remained attached to the presynaptic membrane but did not release its neurotransmitters, suggesting that calcium is required to make the actin coating, and that the actin coating is responsible in the mechanism for vesicle unloading or vesicle release. [14]

Myosin II

Kiss-and-run exocytosis is regulated by myosin II. Studies using total internal reflection fluorescence microscopy (TIRFM) in neuroendocrine PC12 cells showed that myosin II regulates fusion pore dynamics during kiss-and-run exocytosis. [15] Over-expression of normal myosin II regulatory light chain (RLC) in mRFP (monomeric red fluorescent protein) tagged tissue and Venus-tagged brain tissue resulted in prolonged release kinetics, while over-expression of a mutant form of myosin II RLC short shortened release kinetics. [15] Prolonged release kinetics is indicative of a slower closing of the fusion pore, so myosin II also regulates how much neurotransmitter is released during kiss-and-run exocytosis.

SNAREs

Much scholarly debate exists over the role of SNARE proteins in kiss-and-run exocytosis. SNARE proteins mediate vesicle fusion - the exocytosis of vesicles with the presynaptic membrane at the fusion pore. When a vesicle fuses with the presynaptic membrane, a SNARE transition occurs from a trans position to a cis position, followed by SNARE dissociation. [16] This process was thought to be irreversible. If kiss-and-run exocytosis occurs, however, then it would suggest that reversible association of SNARE proteins occurs and mediates the kiss-and-run mode of exocytosis. [16] Manipulation of the SNARE proteins during kiss-and-run may give more insight to how the two relate, and more scholarly research is required.

Related Research Articles

Chemical synapse

Chemical synapses are biological junctions through which neurons' signals can be sent to each other and to non-neuronal cells such as those in muscles or glands. Chemical synapses allow neurons to form circuits within the central nervous system. They are crucial to the biological computations that underlie perception and thought. They allow the nervous system to connect to and control other systems of the body.

Exocytosis

Exocytosis is a form of active transport and bulk transport in which a cell transports molecules out of the cell by secreting them through an energy-dependent process. Exocytosis and its counterpart, endocytosis, are used by all cells because most chemical substances important to them are large polar molecules that cannot pass through the hydrophobic portion of the cell membrane by passive means. Exocytosis is the process by which a large amount of molecules are released; thus it is a form of bulk transport.

In neuroscience, synaptic plasticity is the ability of synapses to strengthen or weaken over time, in response to increases or decreases in their activity. Since memories are postulated to be represented by vastly interconnected neural circuits in the brain, synaptic plasticity is one of the important neurochemical foundations of learning and memory.

Excitatory synapse

An excitatory synapse is a synapse in which an action potential in a presynaptic neuron increases the probability of an action potential occurring in a postsynaptic cell. Neurons form networks through which nerve impulses travel, each neuron often making numerous connections with other cells. These electrical signals may be excitatory or inhibitory, and, if the total of excitatory influences exceeds that of the inhibitory influences, the neuron will generate a new action potential at its axon hillock, thus transmitting the information to yet another cell.

Neuromuscular junction

A neuromuscular junction is a chemical synapse between a motor neuron and a muscle fiber. It allows the motor neuron to transmit a signal to the muscle fiber, causing muscle contraction.

Synaptic vesicle Neurotransmitters that are released at the synapse

In a neuron, synaptic vesicles store various neurotransmitters that are released at the synapse. The release is regulated by a voltage-dependent calcium channel. Vesicles are essential for propagating nerve impulses between neurons and are constantly recreated by the cell. The area in the axon that holds groups of vesicles is an axon terminal or "terminal bouton". Up to 130 vesicles can be released per bouton over a ten-minute period of stimulation at 0.2 Hz. In the visual cortex of the human brain, synaptic vesicles have an average diameter of 39.5 nanometers (nm) with a standard deviation of 5.1 nm.

End-plate potential

End plate potentials (EPPs) are the voltages which cause depolarization of skeletal muscle fibers caused by neurotransmitters binding to the postsynaptic membrane in the neuromuscular junction. They are called "end plates" because the postsynaptic terminals of muscle fibers have a large, saucer-like appearance. When an action potential reaches the axon terminal of a motor neuron, vesicles carrying neurotransmitters are exocytosed and the contents are released into the neuromuscular junction. These neurotransmitters bind to receptors on the postsynaptic membrane and lead to its depolarization. In the absence of an action potential, acetylcholine vesicles spontaneously leak into the neuromuscular junction and cause very small depolarizations in the postsynaptic membrane. This small response (~0.4mV) is called a miniature end plate potential (MEPP) and is generated by one acetylcholine-containing vesicle. It represents the smallest possible depolarization which can be induced in a muscle.

SNARE (protein)

SNARE proteins – "SNAPREceptor" – are a large protein family consisting of at least 24 members in yeasts and more than 60 members in mammalian cells. The primary role of SNARE proteins is to mediate vesicle fusion – the fusion of vesicles with the target membrane; this notably mediates exocytosis, but can also mediate the fusion of vesicles with membrane-bound compartments. The best studied SNAREs are those that mediate the neurotransmitter release of synaptic vesicles in neurons. These neuronal SNAREs are the targets of the neurotoxins responsible for botulism and tetanus produced by certain bacteria.

Neurotransmission

Neurotransmission is the process by which signaling molecules called neurotransmitters are released by the axon terminal of a neuron, and bind to and react with the receptors on the dendrites of another neuron a short distance away. A similar process occurs in retrograde neurotransmission, where the dendrites of the postsynaptic neuron release retrograde neurotransmitters that signal through receptors that are located on the axon terminal of the presynaptic neuron, mainly at GABAergic and glutamatergic synapses.

Synaptotagmin

Synaptotagmins (SYTs) constitute a family of membrane-trafficking proteins that are characterized by an N-terminal transmembrane region (TMR), a variable linker, and two C-terminal C2 domains - C2A and C2B. There are 17 isoforms in the mammalian synaptotagmin family. There are several C2-domain containing protein families that are related to synaptotagmins, including transmembrane (Ferlins, Extended-Synaptotagmin (E-Syt) membrane proteins, and MCTPs) and soluble (RIMS1 and RIMS2, UNC13D, synaptotagmin-related proteins and B/K) proteins. The family includes synaptotagmin 1, a Ca2+ sensor in the membrane of the pre-synaptic axon terminal, coded by gene SYT1.

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Complexin

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Axon terminal

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The ribbon synapse is a type of neuronal synapse characterized by the presence of an electron-dense structure, the synaptic ribbon, that holds vesicles close to the active zone. It is characterized by a tight vesicle-calcium channel coupling that promotes rapid neurotransmitter release and sustained signal transmission. Ribbon synapses undergo a cycle of exocytosis and endocytosis in response to graded changes of membrane potential. It has been proposed that most ribbon synapses undergo a special type of exocytosis based on coordinated multivesicular release. This interpretation has recently been questioned at the inner hair cell ribbon synapse, where it has been instead proposed that exocytosis is described by uniquantal release shaped by a flickering vesicle fusion pore.

Vesicle fusion is the merging of a vesicle with other vesicles or a part of a cell membrane. In the latter case, it is the end stage of secretion from secretory vesicles, where their contents are expelled from the cell through exocytosis. Vesicles can also fuse with other target cell compartments, such as a lysosome. Exocytosis occurs when secretory vesicles transiently dock and fuse at the base of cup-shaped structures at the cell plasma membrane called porosome, the universal secretory machinery in cells. Vesicle fusion may depend on SNARE proteins in the presence of increased intracellular calcium (Ca2+) concentration.

Active zone

The active zone or synaptic active zone is a term first used by Couteaux and Pecot-Dechavassinein in 1970 to define the site of neurotransmitter release. Two neurons make near contact through structures called synapses allowing them to communicate with each other. As shown in the adjacent diagram, a synapse consists of the presynaptic bouton of one neuron which stores vesicles containing neurotransmitter, and a second, postsynaptic neuron which bears receptors for the neurotransmitter, together with a gap between the two called the synaptic cleft. When an action potential reaches the presynaptic bouton, the contents of the vesicles are released into the synaptic cleft and the released neurotransmitter travels across the cleft to the postsynaptic neuron and activates the receptors on the postsynaptic membrane.

Synaptic fatigue

Synaptic fatigue, or short-term synaptic depression, is an activity-dependent form of short term synaptic plasticity that results in the temporary inability of neurons to fire and therefore transmit an input signal. It is thought to be a form of negative feedback in order to physiologically control particular forms of nervous system activity.

Membrane vesicle trafficking in eukaryotic animal cells involves movement of important biochemical signal molecules from synthesis-and-packaging locations in the Golgi body to specific 'release' locations on the inside of the plasma membrane of the secretory cell, in the form of Golgi membrane-bound micro-sized vesicles, termed membrane vesicles (MVs). In this process, the 'packed' cellular products are released/secreted outside the cell across its plasma membrane. However, this vesicular membrane is retained and recycled by the secretory cells. This phenomenon has a key role in synaptic neurotransmission, endocrine secretion, mucous secretion, granular-product secretion by neutrophils, etc. The scientists behind this discovery were awarded Nobel prize for the year 2013. In the prokaryotic gram-negative bacterial cells, membrane vesicle trafficking is mediated via bacterial outer membrane bounded nano-sized vesicles, called bacterial outer membrane vesicles (OMVs). In this case, however, the OMV membrane is secreted as well, along with OMV-contents to outside the secretion-active bacterium. This phenomenon has a key role in host-pathogen interactions, endotoxic shock in patients, invasion and infection of animals/plants, inter-species bacterial competition, quorum sensing, exocytosis, etc.

Synaptic stabilization Modifying synaptic strength via cell adhesion molecules

Synaptic stabilization is crucial in the developing and adult nervous systems and is considered a result of the late phase of long-term potentiation (LTP). The mechanism involves strengthening and maintaining active synapses through increased expression of cytoskeletal and extracellular matrix elements and postsynaptic scaffold proteins, while pruning less active ones. For example, cell adhesion molecules (CAMs) play a large role in synaptic maintenance and stabilization. Gerald Edelman discovered CAMs and studied their function during development, which showed CAMs are required for cell migration and the formation of the entire nervous system. In the adult nervous system, CAMs play an integral role in synaptic plasticity relating to learning and memory.

References

  1. 1 2 3 4 Ceccarelli, B.; Hurlbut, W. P.; Mauro, A. (1973). "Turnover of Transmitter and Synaptic Vesicles at the Frog Neuromuscular Junction". The Journal of Cell Biology. 57 (2): 499–524. doi:10.1083/jcb.57.2.499. PMC   2108980 . PMID   4348791.
  2. 1 2 3 Fesce, R; Grohovaz, F; Valtorta, F; Meldolesi, J (1994). "Neurotransmitter release: fusion or 'kiss-and-run'?". Trends in Cell Biology. 4 (1): 1–4. doi:10.1016/0962-8924(94)90025-6. PMID   14731821.
  3. ↑ Heuser, JE; Reese, TS (1973). "Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction". J. Cell Biol. 57 (2): 315–344. doi:10.1083/jcb.57.2.315. PMC   2108984 . PMID   4348786.
  4. 1 2 Alvarez de Toledo, G; Fernàndez-Chacòn, R; Fenràndez, JM (1993). "Release of secretory products during transient vesicle fusion". Nature. 363 (6429): 554–558. Bibcode:1993Natur.363..554D. doi:10.1038/363554a0. PMID   8505984. S2CID   4316497.
  5. ↑ He, L.; Wu, L. G. (2007). "The debate on the kiss-and-run fusion at synapses". Trends in Neurosciences. 30 (9): 447–455. doi:10.1016/j.tins.2007.06.012. PMID   17765328. S2CID   14792145.
  6. ↑ Ceccarelli, B.; Hurlbut, W. P.; Mauro, A. (1972). "Depletion of Vesicles from Frog Neuromuscular Junctions by Prolonged Tetanic Stimulation". The Journal of Cell Biology. 54 (1): 30–38. doi:10.1083/jcb.54.1.30. PMC   2108853 . PMID   4338962.
  7. ↑ Torri-Tarelli, F; Grohovaz, F; Fesce, R; Ceccarelli, B (1985). "Temporal coincidence between synaptic vesicle fusion and quantal secretion of acetylcholine". J. Cell Biol. 101 (4): 1386–1399. doi:10.1083/jcb.101.4.1386. PMC   2113930 . PMID   2995407.
  8. ↑ Lee JS, Jeremic A, Shin L, Cho WJ, Chen X, Jena BP (2012). "Neuronal porosome proteome: Molecular dynamics and architecture". J Proteomics. 75 (13): 3952–62. doi:10.1016/j.jprot.2012.05.017. PMC   4580231 . PMID   22659300.
  9. ↑ Rizzoli, S. O.; Jahn, R. (2007). "Kiss-and-run, Collapse and 'Readily Retrievable' Vesicles". Traffic. 8 (9): 1137–1144. doi: 10.1111/j.1600-0854.2007.00614.x . PMID   17645434. S2CID   12861292.
  10. 1 2 3 4 5 6 MacDonald, P. E.; Braun, M.; Galvanovskis, J.; Rorsman, P. (2006). "Release of small transmitters through kiss-and-run fusion pores in rat pancreatic β cells". Cell Metabolism. 4 (4): 283–290. doi:10.1016/j.cmet.2006.08.011. PMID   17011501.
  11. ↑ Artalejo, C. R.; Elhamdani, A.; Palfrey, H. C. (1998). "Secretion: Dense-core vesicles can kiss-and-run too". Current Biology. 8 (2): R62–R65. doi: 10.1016/s0960-9822(98)70036-3 . PMID   9427637.
  12. 1 2 Stevens, C. F.; Williams, J. H. (2000). ""Kiss and run" exocytosis at hippocampal synapses". Proceedings of the National Academy of Sciences. 97 (23): 12828–12833. Bibcode:2000PNAS...9712828S. doi:10.1073/pnas.230438697. PMC   18849 . PMID   11050187.
  13. 1 2 3 4 5 Liu, X.; Weaver, D.; Shirihai, O.; Hajnóczky, G. R. (2009). "Mitochondrial 'kiss-and-run': Interplay between mitochondrial motility and fusion–fission dynamics". The EMBO Journal. 28 (20): 3074–3089. doi:10.1038/emboj.2009.255. PMC   2771091 . PMID   19745815.
  14. 1 2 Miklavc, P.; Wittekindt, O. H.; Felder, E.; Dietl, P. (2009). "Ca2+-Dependent Actin Coating of Lamellar Bodies after Exocytotic Fusion: A Prerequisite for Content Release or Kiss-and-Run". Annals of the New York Academy of Sciences. 1152 (1): 43–52. Bibcode:2009NYASA1152...43M. doi:10.1111/j.1749-6632.2008.03989.x. PMID   19161375. S2CID   22589470.
  15. 1 2 Aoki, R.; Kitaguchi, T.; Oya, M.; Yanagihara, Y.; Sato, M.; Miyawaki, A.; Tsuboi, T. (2010). "Duration of fusion pore opening and the amount of hormone released are regulated by myosin II during kiss-and-run exocytosis". Biochemical Journal. 429 (3): 497–504. doi:10.1042/BJ20091839. PMID   20528772. S2CID   13640188.
  16. 1 2 Palfrey, H. C.; Artalejo, C. R. (2003). "Secretion: Kiss and run caught on film". Current Biology. 13 (10): R397–R399. doi:10.1016/s0960-9822(03)00320-8. PMID   12747851. S2CID   12807086.
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