Myosin light chain kinase accelerates vesicle endocytosis at the calyx of held synapse

Journal of Neuroscience

Volumn 34, Issue 1, 2014, Pages 295-304

  Yue, Hai Yuan ^a   Xu, Jianhua ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Capacitance; Endocytosis; Myosin; Myosin light chain kinase; The calyx of Held; Vesicle

Indexed keywords

CALMODULIN; CLATHRIN; MYOSIN LIGHT CHAIN KINASE;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELL MIGRATION; ENDOCYTOSIS; EVOKED BRAIN STEM RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; HOMEOSTASIS; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION;

EID: 84891445273     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3744-13.2014     Document Type: Article

References (63)

1. Araki N, Hatae T, Furukawa A, Swanson JA (2003) Phosphoinositide-3-kinase-independent contractile activities associated with Fcgammareceptor-mediated phagocytosis and macropinocytosis in macrophages. J Cell Sci 116:247-257. Medline
2. Artalejo CR, Elhamdani A, Palfrey HC (1996) Calmodulin is the divalent cation receptor for rapid endocytosis, but not exocytosis, in adrenal chromaffin cells. Neuron 16:195-205. CrossRef Medline
3. Bourne J, Morgan JR, Pieribone VA (2006) Actin polymerization regulates clathrin coat maturation during early stages of synaptic vesicle recycling at lamprey synapses. J Comp Neurol 497:600-609. Medline
4. Brodin L, Löw P, Shupliakov O (2000) Sequential steps in clathrinmediated synaptic vesicle endocytosis. Curr Opin Neurobiol 10:312-320. Medline
5. Catterall WA, Leal K, Nanou E (2013) Calcium channels and short-term synaptic plasticity. J Biol Chem 288:10742-10749. Medline
6. Chandrasekar I, Huettner JE, Turney SG, Bridgman PC (2013) Myosin II regulates activity-dependent compensatory endocytosis at central synapses. J Neurosci 33:16131-16145. CrossRef Medline
7. 2+selectivity in the calmodulin regulation of CaV channels. Nature 451:830-834. CrossRef Medline
8. Fioravante D, Chu Y, Myoga MH, Leitges M, Regehr WG (2011) Calciumdependent isoforms of protein kinase C mediate posttetanic potentiation at the calyx of Held. Neuron 70:1005-1019. CrossRef Medline
9. Garcia JG, Verin AD, Schaphorst K, Siddiqui R, Patterson CE, Csortos C, Natarajan V (1999) Regulation of endothelial cell myosin light chain kinase by Rho, cortactin, and p60(src). Am J Physiol 276:L989-L998. Medline
10. Girao H, Geli MI, Idrissi FZ (2008) Actin in the endocytic pathway: from yeast to mammals. FEBS Lett 582:2112-2119. Medline
11. González-Forero D, Montero F, García-Morales V, Domínguez G, Gómez-Perez L, García-Verdugo JM, Moreno-López B (2012) Endogenous Rho-kinase signaling maintains synaptic strength by stabilizing the size of the readily releasable pool of synaptic vesicles. J Neurosci 32:68-84. CrossRef Medline
12. Gu C, Yaddanapudi S, Weins A, Osborn T, Reiser J, Pollak M, Hartwig J, Sever S (2010) Direct dynamin-actin interactions regulate the actin cytoskeleton. EMBO J 29:3593-3606. Medline
13. He L, Xue L, Xu J, McNeil BD, Bai L, Melicoff E, Adachi R, Wu LG (2009) Compound vesicle fusion increases quantal size and potentiates synaptic transmission. Nature 459:93-97. CrossRef Medline
14. 2+triggers a novel clathrin-independent but actin-dependent fast endocytosis in pancreatic beta cells. Traffic 9:910-923. CrossRef Medline
15. Hosoi N, Holt M, Sakaba T (2009) Calcium dependence of exo-and endocytotic coupling at a glutamatergic synapse. Neuron 63:216-229. CrossRef Medline
16. Hua Y, Woehler A, Kahms M, Haucke V, Neher E, Klingauf J (2013) Blocking endocytosis enhances short-term synaptic depression under conditions of normal availability of vesicles. Neuron 80:343-349. CrossRef Medline
17. Kovács M, Tóth J, Hetényi C, Málnási-Csizmadia A, Sellers JR (2004) Mechanism of blebbistatin inhibition of myosin II. J Biol Chem 279:35557-35563. Medline
18. Lee E, De Camilli P (2002) Dynamin at actin tails. Proc Natl Acad Sci USA 99:161-166. CrossRef Medline
19. Lee JS, Kim MH, Ho WK, Lee SH (2008) Presynaptic release probability and readily releasable pool size are regulated by two independent mechanisms during posttetanic potentiation at the calyx of Held synapse. J Neurosci 28:7945-7953. CrossRef Medline
20. Lee JS, Ho WK, Lee SH (2010) Post-tetanic increase in the fast-releasing synaptic vesicle pool at the expense of the slowly releasing pool. J Gen Physiol 136:259-272. Medline
21. Lindau M, Neher E (1988) Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflugers Arch 411:137-146. Medline
22. Liu JP, Sim AT, Robinson PJ (1994) Calcineurin inhibition of dynamin I GTPase activity coupled to nerve terminal depolarization. Science 265: 970-973. CrossRef Medline
23. Lukas TJ, Mirzoeva S, Slomczynska U, WattersonDM (1999) Identification of novel classes of protein kinase inhibitors using combinatorial peptide chemistry based on functional genomics knowledge. J Med Chem 42: 910-919. Medline
24. Maeno-Hikichi Y, Polo-Parada L, Kastanenka KV, Landmesser LT (2011) Frequency-dependent modes of synaptic vesicle endocytosis and exocytosis at adult mouse neuromuscular junctions. J Neurosci 31:1093-1105. CrossRef Medline
25. Mansfield PJ, Shayman JA, Boxer LA (2000) Regulation of polymorphonuclear leukocyte phagocytosis by myosin light chain kinase after activation of mitogen-activated protein kinase. Blood 95:2407-2412. Medline
26. Marchiando AM, Shen L, Graham WV, Weber CR, Schwarz BT, Austin JR 2nd, Raleigh DR, Guan Y, Watson AJ, Montrose MH, Turner JR (2010) Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J Cell Biol 189:111-126. Medline
27. Merrifield CJ, Perrais D, Zenisek D (2005) Coupling between clathrincoated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 121:593-606. CrossRef Medline
28. Mochida S, Kobayashi H, Matsuda Y, Yuda Y, Muramoto K, Nonomura Y (1994) Myosin II is involved in transmitter release at synapses formed between rat sympathetic neurons in culture. Neuron 13:1131-1142. CrossRef Medline
29. Mooren OL, Galletta BJ, Cooper JA (2012) Roles for actin assembly in endocytosis. Annu Rev Biochem 81:661-686. CrossRef Medline
30. Nairn AC, Picciotto MR (1994) Calcium/calmodulin-dependent protein kinases. Semin Cancer Biol 5:295-303. Medline
31. Nakanishi S, Kakita S, Takahashi I, Kawahara K, Tsukuda E, Sano T, Yamada K, Yoshida M, Kase H, Matsuda Y, Hashimoto Y, and Nonomuran Y (1992) Wortmannin, a microbial product inhibitor of myosin light chain kinase. J Biol Chem 267:2157-2163. Medline
32. Polo-Parada L, Plattner F, Bose C, Landmesser LT (2005) NCAM180 acting via a conserved C-terminal domain and MLCK is essential for effective transmission with repetitive stimulation. Neuron 46:917-931. CrossRef Medline
33. Poskanzer KE, Marek KW, Sweeney ST, Davis GW (2003) Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature 426:559-563. CrossRef Medline
34. Renden R, von Gersdorff H (2007) Synaptic vesicle endocytosis at a CNS nerve terminal: faster kinetics at physiological temperatures and increased endocytotic capacity during maturation. J Neurophysiol 98:3349-3359. CrossRef Medline
35. Ryan TA (1999) Inhibitors of myosin light chain kinase block synaptic vesicle pool mobilization during action potential firing. J Neurosci 19:1317-1323. Medline
36. Saitoh M, Ishikawa T, Matsushima S, Naka M, Hidaka H (1987) Selective inhibition of catalytic activity of smooth muscle myosin light chain kinase. J Biol Chem 262:7796-7801. Medline
37. Sakaba T, Neher E (2001) Calmodulin mediates rapid recruitment of fastreleasing synaptic vesicles at a calyx-type synapse. Neuron 32:1119-1131. CrossRef Medline
38. Sakaba T, Neher E (2003) Involvement of actin polymerization in vesicle recruitment at the calyx of Held synapse. J Neurosci 23:837-846. Medline
39. Sanders LC, Matsumura F, Bokoch GM, de Lanerolle P (1999) Inhibition of myosin light chain kinase by p21-activated kinase. Science 283:2083-2085. CrossRef Medline
40. Sankaranarayanan S, Ryan TA (2001) Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat Neurosci 4:129-136. Medline
41. Sankaranarayanan S, Atluri PP, Ryan TA (2003) Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat Neurosci 6:127-135. Medline
42. Schafer DA (2002) Coupling actin dynamics and membrane dynamics during endocytosis. Curr Opin Cell Biol 14:76-81. Medline
43. Schwarz BT, Wang F, Shen L, Clayburgh DR, Su L, Wang Y, Fu YX, Turner JR (2007) LIGHT signals directly to intestinal epithelia to cause barrier dysfunction via cytoskeletal and endocytic mechanisms. Gastroenterology 132:2383-2394. CrossRef Medline
44. Seabrooke S, Stewart BA (2011) Synaptic transmission and plasticity are modulated by nonmuscle myosin II at the neuromuscular junction of Drosophila. J Neurophysiol 105:1966-1976. CrossRef Medline
45. Shupliakov O, Bloom O, Gustafsson JS, Kjaerulff O, Low P, Tomilin N, Pieribone VA, Greengard P, Brodin L (2002) Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton. Proc Natl Acad Sci USA 99:14476-14481. CrossRef Medline
46. Srinivasan G, Kim JH, von Gersdorff H (2008) The pool of fast releasing vesicles is augmented by myosin light chain kinase inhibition at the calyx of Held synapse. J Neurophysiol 99:1810-1824. CrossRef Medline
47. Sun JY, Wu LG (2001) Fast kinetics of exocytosis revealed by simultaneous measurements of presynaptic capacitance and postsynaptic currents at a central synapse. Neuron 30:171-182. CrossRef Medline
48. Sun T, Wu XS, Xu J, McNeil BD, Pang ZP, Yang W, Bai L, Qadri S, Molkentin JD, Yue DT, Wu LG (2010) The role of calcium/calmodulin-activated calcineurin in rapid and slow endocytosis at central synapses. J Neurosci 30:11838-11847. CrossRef Medline
49. Tokuoka H, Goda Y (2006) Myosin light chain kinase is not a regulator of synaptic vesicle trafficking during repetitive exocytosis in cultured hippocampal neurons. J Neurosci 26:11606-11614. CrossRef Medline
50. Wu W, Xu J, Wu XS, Wu LG (2005) Activity-dependent acceleration of endocytosis at a central synapse. J Neurosci 25:11676-11683. CrossRef Medline
51. Wu XS, Wu LG (2009) Rapid endocytosis does not recycle vesicles within the readily releasable pool. J Neurosci 29:11038-11042. CrossRef Medline
52. 2+and calmodulin initiate all forms of endocytosis during depolarization at a nerve terminal. Nat Neurosci 12:1003-1010. Medline
53. Xu J, Wu LG (2005) The decrease in the presynaptic calcium current is a major cause of short-term depression at a calyx-type synapse. Neuron 46:633-645. CrossRef Medline
54. Xu J, McNeil B, Wu W, Nees D, Bai L, Wu LG (2008) GTP-independent rapid and slow endocytosis at a central synapse. Nat Neurosci 11:45-53. Medline
55. Xu J, Luo F, Zhang Z, Xue L, Wu XS, Chiang HC, Shin W, Wu LG (2013) SNARE proteins synaptobrevin, SNAP-25, and syntaxin are involved in rapid and slow endocytosis at synapses. Cell Rep 3:1414-1421. Medline
56. Xue L, Wu LG (2010) Post-tetanic potentiation is caused by two signalling mechanisms affecting quantal size and quantal content. J Physiol 588: 4987-4994. CrossRef Medline
57. Xue L, Zhang Z, McNeil BD, Luo F, Wu XS, Sheng J, Shin W, Wu LG (2012) Voltage-dependent calcium channels at the plasma membrane, but not vesicular channels, couple exocytosis to endocytosis. Cell Rep 1:632-638. Medline
58. Xue L, Sheng J, Wu XS, Wu W, Luo F, Shin W, Chiang HC, Wu LG (2013) Most vesicles in a central nerve terminal participate in recycling. J Neurosci 33:8820-8826. CrossRef Medline
59. Yamashita T, Hige T, Takahashi T (2005) Vesicle endocytosis requires dynamin-dependent GTP hydrolysis at a fast CNS synapse. Science 307: 124-127. CrossRef Medline
60. 2+. Nat Neurosci 13:838-844. Medline
61. Yao L, Sakaba T (2012) Activity-dependent modulation of endocytosis by calmodulin at a large central synapse. Proc Natl Acad Sci USA 109:291-296. CrossRef Medline
62. 2+dependence of clathrinmediated endocytosis. J Neurosci 32:3778-3785. CrossRef Medline
63. Yao LH, Rao Y, Bang C, Kurilova S, Varga K, Wang CY, Weller BD, Cho W, Cheng J, GongLW (2013) Actin polymerization does not provide direct mechanical forces for vesicle fission during clathrin-mediated endocytosis. J Neurosci 33:15793-15798. CrossRef Medline