Encyclopedia of Computational Neuroscience

Living Edition
| Editors: Dieter Jaeger, Ranu Jung

Biophysical Models of Calcium-Dependent Exocytosis

  • Victor MatveevEmail author
Living reference work entry

Latest version View entry history

DOI: https://doi.org/10.1007/978-1-4614-7320-6_178-2

Synonyms

Definition

Calcium-dependent exocytosis is the biochemically controlled fusion of the bilipid secretory vesicle membrane with the bilipid cell membrane, triggered by the binding of several calcium ions (Ca2+) to control proteins such as synaptotagmins anchored at the interface between these two membranes. Exocytosis results in the release of vesicle contents into the extracellular space, namely the release of neurotransmitter into the synaptic cleft in the case of neuronal synapses and neuromuscular junctions, or the secretion of hormone into the blood stream in the case of endocrine cells. Exocytosis also allows the transmembrane proteins contained in the vesicle membrane to be incorporated into the cell membrane, although such membrane protein trafficking is more characteristic of Ca2+-independent, constitutive exocytosis.

Detailed Description

In synapses, neuromuscular junctions, and endocrine cells, exocytosis of a...
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

This work was supported in part by NSF grant DMS-1517085

References

  1. Barg S, Ma X, Eliasson L, Galvanovskis J, Gopel SO, Obermuller S, Platzer J, Renstrom E, Trus M, Atlas D, Striessnig J, Rorsman P (2001) Fast exocytosis with few Ca2+ channels in insulin-secreting mouse pancreatic B cells. Biophys J 81:3308–3323PubMedPubMedCentralCrossRefGoogle Scholar
  2. Bennett MR, Farnell L, Gibson WG (2004) The facilitated probability of quantal secretion within an array of calcium channels of an active zone at the amphibian neuromuscular junction. Biophys J 86:2674–2690PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bertram R, Sherman A, Stanley EF (1996) Single-domain/bound calcium hypothesis of transmitter release and facilitation. Biophys J 75:1919–1931Google Scholar
  4. Bertram R, Smith GD, Sherman A (1999) Modeling study of the effects of overlapping Ca2+ microdomains on neurotransmitter release. Biophys J 76:735–750PubMedPubMedCentralCrossRefGoogle Scholar
  5. Beutner D, Voets T, Neher E, Moser T (2001) Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 29:681–690PubMedCrossRefPubMedCentralGoogle Scholar
  6. Bohme MA, Grasskamp AT, Walter AM (2018) Regulation of synaptic release-site Ca(2+) channel coupling as a mechanism to control release probability and short-term plasticity. FEBS Lett 592:3516–3531PubMedCrossRefPubMedCentralGoogle Scholar
  7. Bollmann JH, Sakmann B (2005) Control of synaptic strength and timing by the release-site Ca2+ signal. Nat Neurosci 8:426–434PubMedCrossRefGoogle Scholar
  8. Bollmann JH, Sakmann B, Borst JG (2000) Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289:953–957PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bornschein G, Schmidt H (2018) Synaptotagmin Ca(2+) sensors and their spatial coupling to presynaptic Cav channels in central cortical synapses. Front Mol Neurosci 11:494PubMedCrossRefPubMedCentralGoogle Scholar
  10. Bornschein G, Arendt O, Hallermann S, Brachtendorf S, Eilers J, Schmidt H (2013) Paired-pulse facilitation at recurrent Purkinje neuron synapses is independent of calbindin and parvalbumin during high-frequency activation. J Physiol 591:3355–3370PubMedPubMedCentralCrossRefGoogle Scholar
  11. Brachtendorf S, Eilers J, Schmidt H (2015) A use-dependent increase in release sites drives facilitation at calretinin-deficient cerebellar parallel-fiber synapses. Front Cell Neurosci 9:27PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bucurenciu I, Kulik A, Schwaller B, Frotscher M, Jonas P (2008) Nanodomain coupling between Ca2+ channels and Ca2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse. Neuron 57:536–545PubMedCrossRefPubMedCentralGoogle Scholar
  13. Chapman ER (2002) Synaptotagmin: a Ca(2+) sensor that triggers exocytosis? Nat Rev Mol Cell Biol 3:498–508PubMedCrossRefPubMedCentralGoogle Scholar
  14. Chen YD, Wang S, Sherman A (2008) Identifying the targets of the amplifying pathway for insulin secretion in pancreatic beta-cells by kinetic modeling of granule exocytosis. Biophys J 95:2226–2241PubMedPubMedCentralCrossRefGoogle Scholar
  15. Cho S, von Gersdorff H (2012) Ca(2+) influx and neurotransmitter release at ribbon synapses. Cell Calcium 52:208–216PubMedPubMedCentralCrossRefGoogle Scholar
  16. Chow RH, Ruden L, Neher E (1992) Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature 356:60–63PubMedCrossRefPubMedCentralGoogle Scholar
  17. Chung C, Raingo J (2013) Vesicle dynamics: how synaptic proteins regulate different modes of neurotransmission. J Neurochem 126:146–154PubMedCrossRefPubMedCentralGoogle Scholar
  18. Coggins M, Zenisek D (2009) Evidence that exocytosis is driven by calcium entry through multiple calcium channels in goldfish retinal bipolar cells. J Neurophysiol 101:2601–2619PubMedPubMedCentralCrossRefGoogle Scholar
  19. Dittman JS, Regehr WG (1998) Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 18:6147–6162PubMedPubMedCentralCrossRefGoogle Scholar
  20. Dittman JS, Kreitzer AC, Regehr WG (2000) Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J Neurosci 20:1374–1385PubMedPubMedCentralCrossRefGoogle Scholar
  21. Dittrich M, Pattillo JM, King JD, Cho S, Stiles JR, Meriney SD (2013) An excess-calciumbinding-site model predicts neurotransmitter release at the neuromuscular junction. Biophys J 104:2751–2763PubMedPubMedCentralCrossRefGoogle Scholar
  22. Dodge FA, Rahamimoff R (1967) Cooperative action of calcium ions in transmitter release at the neuromuscular junction. J Physiol 193:419–432PubMedPubMedCentralCrossRefGoogle Scholar
  23. Eggermann E, Bucurenciu I, Goswami SP, Jonas P (2012) Nanodomain coupling between Ca(2)(+) channels and sensors of exocytosis at fast mammalian synapses. Nat Rev Neurosci 13:7–21CrossRefGoogle Scholar
  24. Elmqvist D, Quastel DMJ (1965) A quantitative study of end-plate potentials in isolated human muscle. J Physiol 178:505–529PubMedPubMedCentralCrossRefGoogle Scholar
  25. Felmy F, Neher E, Schneggenburger R (2003) Probing the intracellular calcium sensitivity of transmitter release during synaptic facilitation. Neuron 37:801–811PubMedCrossRefPubMedCentralGoogle Scholar
  26. Gandasi NR, Yin P, Riz M, Chibalina MV, Cortese G, Lund PE, Matveev V, Rorsman P, Sherman A, Pedersen MG, Barg S (2017) Ca2+ channel clustering with insulin-containing granules is disturbed in type 2 diabetes. J Clin Invest 127:2353–2364PubMedPubMedCentralCrossRefGoogle Scholar
  27. Gentile L, Stanley EF (2005) A unified model of presynaptic release site gating by calcium channel domains. Eur J Neurosci 21:278–282PubMedCrossRefPubMedCentralGoogle Scholar
  28. Glavinovic MI, Rabie HR (2001) Monte Carlo evaluation of quantal analysis in the light of Ca2+ dynamics and the geometry of secretion. Pflugers Arch 443:132–145PubMedCrossRefPubMedCentralGoogle Scholar
  29. Han X, Wang CT, Bai J, Chapman ER, Jackson MB (2004) Transmembrane segments of syntaxin line the fusion pore of Ca2+-triggered exocytosis. Science 304:289–292PubMedCrossRefPubMedCentralGoogle Scholar
  30. Heidelberger R, Heinemann C, Neher E, Matthews G (1994) Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371:513–515PubMedCrossRefPubMedCentralGoogle Scholar
  31. Heil P, Neubauer H (2010) Summing across different active zones can explain the quasi-linear Ca-dependencies of exocytosis by receptor cells. Front Synaptic Neurosci 2:148PubMedPubMedCentralCrossRefGoogle Scholar
  32. Heinemann C, von Ruden L, Chow RH, Neher E (1993) A two-step model of secretion control in neuroendocrine cells. Pflugers Arch 424:105–112PubMedCrossRefGoogle Scholar
  33. Heinemann C, Chow RH, Neher E, Zucker RS (1994) Kinetics of the secretory response in bovine chromaffin cells following flash photolysis of caged Ca2+. Biophys J 67:2546–2557PubMedPubMedCentralCrossRefGoogle Scholar
  34. Hosoi N, Sakaba T, Neher E (2007) Quantitative analysis of calcium-dependent vesicle recruitment and its functional role at the calyx of Held synapse. J Neurosci 27:14286–14298PubMedPubMedCentralCrossRefGoogle Scholar
  35. Jahn R, Fasshauer D (2012) Molecular machines governing exocytosis of synaptic vesicles. Nature 490:201–207PubMedPubMedCentralCrossRefGoogle Scholar
  36. Johnson SL, Franz C, Kuhn S, Furness DN, Ruttiger L, Munkner S, Rivolta MN, Seward EP, Herschman HR, Engel J, Knipper M, Marcotti W (2010) Synaptotagmin IV determines the linear Ca2+ dependence of vesicle fusion at auditory ribbon synapses. Nat Neurosci 13:45–52PubMedCrossRefGoogle Scholar
  37. Kaeser PS, Regehr WG (2014) Molecular mechanisms for synchronous, asynchronous, and spontaneous neurotransmitter release. Annu Rev Physiol 76:333–363PubMedCrossRefGoogle Scholar
  38. Kasai H (1999) Comparative biology of Ca2+-dependent exocytosis: implications of kinetic diversity for secretory function. Trends Neurosci 22:88–93PubMedCrossRefGoogle Scholar
  39. Kochubey O, Schneggenburger R (2011) Synaptotagmin increases the dynamic range of synapses by driving Ca(2)+-evoked release and by clamping a near-linear remaining Ca(2)+ sensor. Neuron 69:736–748PubMedCrossRefGoogle Scholar
  40. Kochubey O, Han Y, Schneggenburger R (2009) Developmental regulation of the intracellular Ca2+ sensitivity of vesicle fusion and Ca2+-secretion coupling at the rat calyx of Held. J Physiol 587:3009–3023PubMedPubMedCentralCrossRefGoogle Scholar
  41. Lee JS, Ho WK, Neher E, Lee SH (2013) Superpriming of synaptic vesicles after their recruitment to the readily releasable pool. Proc Natl Acad Sci U S A 110:15079–15084PubMedPubMedCentralCrossRefGoogle Scholar
  42. Liley AW, North KA (1953) An electrical investigation of effects of repetitive stimulation on mammalian neuromuscular junction. J Neurophysiol 16:509–527PubMedCrossRefPubMedCentralGoogle Scholar
  43. Lou X, Scheuss V, Schneggenburger R (2005) Allosteric modulation of the presynaptic Ca2+ sensor for vesicle fusion. Nature 435:497–501PubMedCrossRefPubMedCentralGoogle Scholar
  44. Luo F, Bacaj T, Sudhof TC (2015a) Synaptotagmin-7 is essential for Ca2+-triggered delayed asynchronous release but not for Ca2+-dependent vesicle priming in retinal ribbon synapses. J Neurosci 35:11024–11033PubMedPubMedCentralCrossRefGoogle Scholar
  45. Luo F, Dittrich M, Cho S, Stiles JR, Meriney SD (2015b) Transmitter release is evoked with low probability predominately by calcium flux through single channel openings at the frog neuromuscular junction. J Neurophysiol 113:2480–2489PubMedPubMedCentralCrossRefGoogle Scholar
  46. Ma J, Kelly L, Ingram J, Price TJ, Meriney SD, Dittrich M (2015) New insights into short-term synaptic facilitation at the frog neuromuscular junction. J Neurophysiol 113:71–87PubMedCrossRefPubMedCentralGoogle Scholar
  47. Martin TF (2003) Tuning exocytosis for speed: fast and slow modes. Biochim Biophys Acta 1641:157–165PubMedCrossRefPubMedCentralGoogle Scholar
  48. Matveev V, Bertram R, Sherman A (2006) Residual Bound Ca2+ Can Account for the Effects of Ca2+ Buffers on Synaptic Facilitation. J Neurophysiol 96:3389–3397PubMedCrossRefPubMedCentralGoogle Scholar
  49. Matveev V (2016) Pade approximation of a stationary single-channel Ca2+ nanodomain. Biophys J 111:2062–2074PubMedPubMedCentralCrossRefGoogle Scholar
  50. Matveev V, Bertram R, Sherman A (2009) Ca2+ current versus Ca2+ channel cooperativity of exocytosis. J Neurosci 29:12196–12209PubMedPubMedCentralCrossRefGoogle Scholar
  51. Matveev V, Bertram R, Sherman A (2011) Calcium cooperativity of exocytosis as a measure of Ca(2)+ channel domain overlap. Brain Res 1398:126–138PubMedPubMedCentralCrossRefGoogle Scholar
  52. Meinrenken CJ, Borst JG, Sakmann B (2002) Calcium secretion coupling at calyx of Held governed by nonuniform channel-vesicle topography. J Neurosci 22:1648–1667PubMedPubMedCentralCrossRefGoogle Scholar
  53. Meinrenken CJ, Borst JG, Sakmann B (2003) Local routes revisited: the space and time dependence of the Ca2+ signal for phasic transmitter release at the rat calyx of Held. J Physiol 547:665–689PubMedPubMedCentralGoogle Scholar
  54. Michalski N, Goutman JD, Auclair SM, Boutet de Monvel J, Tertrais M, Emptoz A, Parrin A, Nouaille S, Guillon M, Sachse M, Ciric D, Bahloul A, Hardelin JP, Sutton RB, Avan P, Krishnakumar SS, Rothman JE, Dulon D, Safieddine S, Petit C (2017) Otoferlin acts as a Ca(2+) sensor for vesicle fusion and vesicle pool replenishment at auditory hair cell ribbon synapses. elife 6:e31013. https://elifesciences.org/articles/31013v1
  55. Millar AG, Zucker RS, Ellis-Davies GC, Charlton MP, Atwood HL (2005) Calcium sensitivity of neurotransmitter release differs at phasic and tonic synapses. J Neurosci 25:3113–3125PubMedPubMedCentralCrossRefGoogle Scholar
  56. Moghadam PK, Jackson MB (2013) The functional significance of synaptotagmin diversity in neuroendocrine secretion. Front Endocrinol 4:124CrossRefGoogle Scholar
  57. Montefusco F, Pedersen MG (2018) Explicit theoretical analysis of how the rate of exocytosis depends on local control by Ca(2+) channels. Comput Math Methods Med 2018:5721097PubMedPubMedCentralCrossRefGoogle Scholar
  58. Moser T, Neef A, Khimich D (2006) Mechanisms underlying the temporal precision of sound coding at the inner hair cell ribbon synapse. J Physiol 576:55–62PubMedPubMedCentralCrossRefGoogle Scholar
  59. Mutch SA, Kensel-Hammes P, Gadd JC, Fujimoto BS, Allen RW, Schiro PG, Lorenz RM, Kuyper CL, Kuo JS, Bajjalieh SM, Chiu DT (2011) Protein quantification at the single vesicle level reveals that a subset of synaptic vesicle proteins are trafficked with high precision. J Neurosci 31:1461–1470PubMedPubMedCentralCrossRefGoogle Scholar
  60. Nadkarni S, Bartol TM, Stevens CF, Sejnowski TJ, Levine H (2012) Short-term plasticity constrains spatial organization of a hippocampal presynaptic terminal. Proc Natl Acad Sci U S A 109:14657–14662PubMedPubMedCentralCrossRefGoogle Scholar
  61. Neher E (1998) Vesicle pools and Ca2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20:389–399PubMedCrossRefPubMedCentralGoogle Scholar
  62. Neher E (2012) Introduction: regulated exocytosis. Cell Calcium 52:196–198PubMedCrossRefPubMedCentralGoogle Scholar
  63. Neher E (2017) Some subtle lessons from the calyx of Held synapse. Biophys J 112:215–223PubMedPubMedCentralCrossRefGoogle Scholar
  64. Neher E, Sakaba T (2008) Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59:861–872PubMedCrossRefPubMedCentralGoogle Scholar
  65. Nouvian R, Neef J, Bulankina AV, Reisinger E, Pangrsic T, Frank T, Sikorra S, Brose N, Binz T, Moser T (2011) Exocytosis at the hair cell ribbon synapse apparently operates without neuronal SNARE proteins. Nat Neurosci 14:411–413PubMedCrossRefPubMedCentralGoogle Scholar
  66. Oheim M, Kirchhoff F, Stuhmer W (2006) Calcium microdomains in regulated exocytosis. Cell Calcium 40:423–439PubMedCrossRefPubMedCentralGoogle Scholar
  67. Pan B, Zucker RS (2009) A general model of synaptic transmission and short-term plasticity. Neuron 62:539–554PubMedPubMedCentralCrossRefGoogle Scholar
  68. Pangrsic T, Reisinger E, Moser T (2012) Otoferlin: a multi-C2 domain protein essential for hearing. Trends Neurosci 35:671–680PubMedCrossRefPubMedCentralGoogle Scholar
  69. Pedersen MG, Sherman A (2009) Newcomer insulin secretory granules as a highly calcium-sensitive pool. Proc Natl Acad Sci U S A 106:7432–7436PubMedPubMedCentralCrossRefGoogle Scholar
  70. Quastel DM, Guan YY, Saint DA (1992) The relation between transmitter release and Ca2+ entry at the mouse motor nerve terminal: role of stochastic factors causing heterogeneity. Neuroscience 51:657–671PubMedCrossRefPubMedCentralGoogle Scholar
  71. Raingo J, Khvotchev M, Liu P, Darios F, Li YC, Ramirez DM, Adachi M, Lemieux P, Toth K, Davletov B, Kavalali ET (2012) VAMP4 directs synaptic vesicles to a pool that selectively maintains asynchronous neurotransmission. Nat Neurosci 15:738–745PubMedPubMedCentralCrossRefGoogle Scholar
  72. Roux I, Safieddine S, Nouvian R, Grati M, Simmler MC, Bahloul A, Perfettini I, Le Gall M, Rostaing P, Hamard G, Triller A, Avan P, Moser T, Petit C (2006) Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell 127:277–289PubMedCrossRefPubMedCentralGoogle Scholar
  73. Rozov A, Bolshakov AP, Valiullina-Rakhmatullina F (2019) The ever-growing puzzle of asynchronous release. Front Cell Neurosci 13:28PubMedPubMedCentralCrossRefGoogle Scholar
  74. Sakaba T (2008) Two Ca(2+)-dependent steps controlling synaptic vesicle fusion and replenishment at the cerebellar basket cell terminal. Neuron 57:406–419PubMedCrossRefPubMedCentralGoogle Scholar
  75. Schmidt H, Brachtendorf S, Arendt O, Hallermann S, Ishiyama S, Bornschein G, Gall D, Schiffmann SN, Heckmann M, Eilers J (2013) Nanodomain coupling at an excitatory cortical synapse. Curr Biol 23:244–249PubMedCrossRefPubMedCentralGoogle Scholar
  76. Schneggenburger R, Neher E (2000) Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406:889–893PubMedCrossRefPubMedCentralGoogle Scholar
  77. Scimemi A, Diamond JS (2012) The number and organization of Ca2+ channels in the active zone shapes neurotransmitter release from Schaffer collateral synapses. J Neurosci 32:18157–18176PubMedPubMedCentralCrossRefGoogle Scholar
  78. Shahrezaei V, Delaney KR (2005) Brevity of the Ca2+ microdomain and active zone geometry prevent Ca2+-sensor saturation for neurotransmitter release. J Neurophysiol 94:1912–1919PubMedCrossRefPubMedCentralGoogle Scholar
  79. Shahrezaei V, Cao A, Delaney KR (2006) Ca2+ from one or two channels controls fusion of a single vesicle at the frog neuromuscular junction. J Neurosci 26:13240–13249PubMedPubMedCentralCrossRefGoogle Scholar
  80. Smith SM, Chen W, Vyleta NP, Williams C, Lee CH, Phillips C, Andresen MC (2012) Calcium regulation of spontaneous and asynchronous neurotransmitter release. Cell Calcium 52:226–233PubMedPubMedCentralCrossRefGoogle Scholar
  81. Sorensen JB (2004) Formation, stabilisation and fusion of the readily releasable pool of secretory vesicles. Pflugers Arch 448:347–362PubMedCrossRefPubMedCentralGoogle Scholar
  82. Stanley EF (2015) Single calcium channel domain gating of synaptic vesicle fusion at fast synapses; analysis by graphic modeling. Channels (Austin) 9:324–333CrossRefGoogle Scholar
  83. Stanley EF (2016) The nanophysiology of fast transmitter release. Trends Neurosci 39:183–197PubMedCrossRefPubMedCentralGoogle Scholar
  84. Sterling P, Matthews G (2005) Structure and function of ribbon synapses. Trends Neurosci 28:20–29PubMedCrossRefPubMedCentralGoogle Scholar
  85. Stevens CF, Wesseling JF (1998) Activity-dependent modulation of the rate at which synaptic vesicles become available to undergo exocytosis. Neuron 21:415–424PubMedCrossRefPubMedCentralGoogle Scholar
  86. Sun J, Pang ZP, Qin D, Fahim AT, Adachi R, Sudhof TC (2007) A dual-Ca2+-sensor model for neurotransmitter release in a central synapse. Nature 450:676–682PubMedPubMedCentralCrossRefGoogle Scholar
  87. Takamori S, Holt M, Stenius K, Lemke EA, Gronborg M, Riedel D, Urlaub H, Schenck S, Brugger B, Ringler P, Muller SA, Rammner B, Grater F, Hub JS, De Groot BL, Mieskes G, Moriyama Y, Klingauf J, Grubmuller H, Heuser J et al (2006) Molecular anatomy of a trafficking organelle. Cell 127:831–846PubMedCrossRefPubMedCentralGoogle Scholar
  88. Taschenberger H, Woehler A, Neher E (2016) Superpriming of synaptic vesicles as a common basis for intersynapse variability and modulation of synaptic strength. Proc Natl Acad Sci U S A 113:E4548–E4557PubMedPubMedCentralCrossRefGoogle Scholar
  89. Thoreson WB, Rabl K, Townes-Anderson E, Heidelberger R (2004) A highly Ca2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42:595–605PubMedPubMedCentralCrossRefGoogle Scholar
  90. Turecek J, Regehr WG (2018) Synaptotagmin 7 mediates both facilitation and asynchronous release at granule cell synapses. J Neurosci 38:3240–3251PubMedPubMedCentralCrossRefGoogle Scholar
  91. Turecek J, Regehr WG (2019) Neuronal regulation of fast synaptotagmin isoforms controls the relative contributions of synchronous and asynchronous release. Neuron 101:938–949.e4PubMedCrossRefPubMedCentralGoogle Scholar
  92. Verhage M, Toonen RF (2007) Regulated exocytosis: merging ideas on fusing membranes. Curr Opin Cell Biol 19:402–408PubMedCrossRefPubMedCentralGoogle Scholar
  93. Voets T (2000) Dissection of three Ca2+-dependent steps leading to secretion in chromaffin cells from mouse adrenal slices. Neuron 28:537–545PubMedCrossRefPubMedCentralGoogle Scholar
  94. Voets T, Neher E, Moser T (1999) Mechanisms underlying phasic and sustained secretion in chromaffin cells from mouse adrenal slices. Neuron 23:607–615PubMedCrossRefPubMedCentralGoogle Scholar
  95. von Ruden L, Neher E (1993) A Ca-dependent early step in the release of catecholamines from adrenal chromaffin cells. Science 262:1061–1065CrossRefGoogle Scholar
  96. Wadel K, Neher E, Sakaba T (2007) The coupling between synaptic vesicles and Ca2+ channels determines fast neurotransmitter release. Neuron 53:563–575PubMedCrossRefPubMedCentralGoogle Scholar
  97. Walter AM, Bohme MA, Sigrist SJ (2018) Vesicle release site organization at synaptic active zones. Neurosci Res 127:3–13PubMedCrossRefPubMedCentralGoogle Scholar
  98. Wang LY, Kaczmarek LK (1998) High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394:384–388PubMedCrossRefPubMedCentralGoogle Scholar
  99. Weber AM, Wong FK, Tufford AR, Schlichter LC, Matveev V, Stanley EF (2010) N-type Ca2+ channels carry the largest current: implications for nanodomains and transmitter release. Nat Neurosci 13:1348–1350PubMedCrossRefPubMedCentralGoogle Scholar
  100. Weber JP, Toft-Bertelsen TL, Mohrmann R, Delgado-Martinez I, Sorensen JB (2014) Synaptotagmin-7 is an asynchronous calcium sensor for synaptic transmission in neurons expressing SNAP-23. PLoS One 9:e114033PubMedPubMedCentralCrossRefGoogle Scholar
  101. Weiss JN (1997) The Hill equation revisited: uses and misuses. FASEB J 11:835–841PubMedCrossRefPubMedCentralGoogle Scholar
  102. Wolfel M, Schneggenburger R (2003) Presynaptic capacitance measurements and Ca2+ uncaging reveal submillisecond exocytosis kinetics and characterize the Ca2+ sensitivity of vesicle pool depletion at a fast CNS synapse. J Neurosci 23:7059–7068PubMedPubMedCentralCrossRefGoogle Scholar
  103. Wolfel M, Lou X, Schneggenburger R (2007) A mechanism intrinsic to the vesicle fusion machinery determines fast and slow transmitter release at a large CNS synapse. J Neurosci 27:3198–3210PubMedPubMedCentralCrossRefGoogle Scholar
  104. Worden MK, Bykhovskaia M, Hackett JT (1997) Facilitation at the lobster neuromuscular junction: a stimulus-dependent mobilization model. J Neurophysiol 78:417–428PubMedCrossRefPubMedCentralGoogle Scholar
  105. Wu MM, Llobet A, Lagnado L (2009) Loose coupling between calcium channels and sites of exocytosis in chromaffin cells. J Physiol 587:5377–5391PubMedPubMedCentralCrossRefGoogle Scholar
  106. Yamada MW, Zucker RS (1992) Time course of transmitter release calculated from stimulations of a calcium diffusion model. Biophys J 61:671–682PubMedPubMedCentralCrossRefGoogle Scholar
  107. Yang Y, Gillis KD (2004) A highly Ca2+-sensitive pool of granules is regulated by glucose and protein kinases in insulin-secreting INS-1 cells. J Gen Physiol 124:641–651PubMedPubMedCentralCrossRefGoogle Scholar
  108. Yang Y, Udayasankar S, Dunning J, Chen P, Gillis KD (2002) A highly Ca2+-sensitive pool of vesicles is regulated by protein kinase C in adrenal chromaffin cells. Proc Natl Acad Sci U S A 99:17060–17065PubMedPubMedCentralCrossRefGoogle Scholar
  109. Yao J, Gaffaney JD, Kwon SE, Chapman ER (2011) Doc2 is a Ca2+ sensor required for asynchronous neurotransmitter release. Cell 147:666–677PubMedPubMedCentralCrossRefGoogle Scholar
  110. Zucker RS, Fogelson AL (1986) Relationship between transmitter release and presynaptic calcium influx when calcium enters through discrete channels. Proc Natl Acad Sci U S A 83:3032–3036PubMedPubMedCentralCrossRefGoogle Scholar
  111. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355–405PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Department of Mathematical SciencesNew Jersey Institute of TechnologyNewarkUSA

Section editors and affiliations

  • Kim T. Blackwell
    • 1
  1. 1.Department of BioengineeringGeorge Mason UniversityFairfaxUSA