Role of membrane cholesterol in spontaneous exocytosis at frog neuromuscular synapses: Reactive oxygen species-calcium interplay

Journal of Physiology

Volumn 592, Issue 22, 2014, Pages 4995-5009

  Petrov, Alexey M ^a   Yakovleva, Anastasiya A ^a   Zefirov, Andrey L ^a  

^a KAZAN STATE MEDICAL UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

3,4,5 TRIMETHOXYBENZOIC ACID 8 (DIETHYLAMINO)OCTYL ESTER; ACETYLCYSTEINE; APOCYNIN; BAPTA AM; CALCINEURIN; CALCIUM; CAPSAZEPINE; CHOLESTEROL; CYCLOSPORIN A; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; METHYL BETA CYCLODEXTRIN; OKADAIC ACID; PHOSPHATASE; PHOSPHATASE PROTEIN 2B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RUTHENIUM RED; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; ACETOPHENONE DERIVATIVE; BETA CYCLODEXTRIN DERIVATIVE; CAPSAICIN; CYCLOSPORIN; METHYL-BETA-CYCLODEXTRIN; VANILLOID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ANURA; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL MEMBRANE; CHELATION; CHOLESTEROL DEPLETION; CONTROLLED STUDY; DEPHOSPHORYLATION; DEPLETION; ENZYME ACTIVATION; EXOCYTOSIS; EXTRACELLULAR SPACE; INTRACELLULAR SPACE; LIPID PEROXIDATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PECTORIS MUSCLE; PRIORITY JOURNAL; SKELETAL MUSCLE; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; CALCIUM SIGNALING; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; RANIDAE; SYNAPTIC MEMBRANE;

ACETOPHENONES; ACETYLCYSTEINE; ANIMALS; BETA-CYCLODEXTRINS; CALCIUM; CALCIUM SIGNALING; CAPSAICIN; CHOLESTEROL; CYCLOSPORINE; EXOCYTOSIS; NEUROMUSCULAR JUNCTION; OKADAIC ACID; RANIDAE; REACTIVE OXYGEN SPECIES; RUTHENIUM RED; SYNAPTIC MEMBRANES; TRPV CATION CHANNELS;

EID: 84919669902     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.279695     Document Type: Article

References (51)

1. Andresen MC, Hofmann ME & Fawley JA (2012). The unsilent majority-TRPV1 drives "spontaneous" transmission of unmyelinated primary afferents within cardiorespiratory NTS. Am J Physiol Regul Integr Comp Physiol 303, R1207-1216.
2. Brown MS & Goldstein JL (1986). A receptor-mediated pathway for cholesterol homeostasis. Science 232, 34-47.
3. Carter AG, Vogt KE, Foster KA & RegehrWG (2002). Assessing the role of calcium-induced calcium release in short-term presynaptic plasticity at excitatory central synapses. J Neurosci 22, 21-28.
4. Cheung G & Cousin MA (2013). Synaptic vesicle generation from activity-dependent bulk endosomes requires calcium and calcineurin. J Neurosci 33, 3370-3379.
5. Chuang HH & Lin S (2009). Oxidative challenges sensitize the capsaicin receptor by covalent cysteine modification. Proc Natl Acad Sci U S A 106, 20097-20102.
6. Dason JS, Smith AJ, Marin L & Charlton MP (2010). Vesicular sterols are essential for synaptic vesicle cycling. J Neurosci 30, 15856-15865.
7. Dason JS, Smith AJ, Marin L & Charlton MP (2014). Cholesterol and F-actin are required for clustering of recycling synaptic vesicle proteins in the presynaptic plasma membrane. J Physiol 592, 621-633.
8. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
9. García-Martínez C, Morenilla-Palao C, Planells-Cases R, Merino JM, & Ferrer-Montiel A (2000). Identification of an aspartic residue in the P-loop of the vanilloid receptor that modulates pore properties. J Biol Chem 275, 32552-32558.
10. Giniatullin AR, Darios F, Shakirzyanova A, Davletov B & Giniatullin R (2006). SNAP25 is a pre-synaptic target for the depressant action of reactive oxygen species on transmitter release. J Neurochem98, 1789-1797.
11. Giniatullin AR & Giniatullin RA (2003). Dual action of hydrogen peroxide on synaptic transmission at the frog neuromuscular junction. J Physiol 552, 283-293.
12. Giniatullin AR, Grishin SN, Sharifullina ER, Petrov AM, Zefirov AL & Giniatullin RA (2005). Reactive oxygen species contribute to the presynaptic action of extracellular ATP at the frog neuromuscular junction. J Physiol 565, 229-242.
13. Goswami C, Rademacher N, Smalla KH, Kalscheuer V, Ropers HH, Gundelfinger ED, & Hucho T (2010). TRPV1 acts as a synaptic protein and regulates vesicle recycling. J Cell Sci 123, 2045-2057.
14. Guatimosim C, Hull C, Von Gersdorff H & Prado MA (2002). Okadaic acid disrupts synaptic vesicle trafficking in a ribbon-type synapse. J Neurochem82, 1047-1057.
15. HanW, Li H, Villar VA, Pascua AM, Dajani MI,Wang X, Natarajan A, Quinn MT, Felder RA, Jose PA & Yu Pv (2008). Lipid rafts keep NADPH oxidase in the inactive state in human renal proximal tubule cells. Hypertension 51, 481-487.
16. Jensen T, Edwards JG (2012). Calcineurin is required for TRPV1-induced long-term depression of hippocampal interneurons. Neurosci Let 510, 82-87.
17. Jia JY, Lamer S, Schumann M, Schmidt MR, Krause E & Haucke V (2006). Quantitative proteomics analysis of detergent-resistant membranes from chemical synapses: evidence for cholesterol as spatial organizer of synaptic vesicle cycling.Mol Cell Proteomics 5, 2060-2071.
18. Jin S, Zhou F, Katirai F & Li PL (2011). Lipid raft redox signaling: molecular mechanisms in health and disease. Antioxid Redox Signal 15, 1043-1083.
19. Kaeser PS & RegehrWG (2014). Molecular mechanisms for synchronous, asynchronous and spontaneous neurotransmitter release. Annu Rev Physiol 76, 333-363.
20. Kavalali ET & Monteggia LM (2012). Synaptic mechanisms underlying rapid antidepressant action of ketamine. Am J Psychiatry 169, 1150-1156.
21. Kim SH & Ryan TA (2010). CDK5 serves as a major control point in neurotransmitter release. Neuron 67, 797-809.
22. 2+ influx slows single synaptic vesicle endocytosis. J Neurosci 31, 16318-16326.
23. Marra V, Burden JJ, Thorpe JR, Smith IT, Smith SL, Hausser M, Branco T & Staras K (2012). A preferentially segregated recycling vesicle pool of limited size supports neurotransmission in native central synapses. Neuron 76, 579-589.
24. Miller EW, Dickinson BC & Chang CJ (2010). Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc Natl Acad Sci U S A 107, 15681-15686.
25. 2+ channels to ryanodine receptors at presynaptic terminals: amplification of exocytosis and plasticity. J Gen Physiol 115, 519-532.
26. Nishio N, TanicuchiW, Sugimura YK, Takiguchi N, Yamanaka M, Kiyoyuki Y, Yamada H, Miyazaki N, Yoshida M & Nakatsuka T (2013). Reactive oxygen species enhance excitatory synaptic transmission in rat spinal dorsal horn neurons by activating TRPA1 and TRPV1 channels. Neurosci 247, 201-212.
27. Ormerod KG, Rogasevskaia TP, Coorssen JR & Mercier AJ (2012). Cholesterol-independent effects of methyl-β-cyclodextrin on chemical synapses. PLoS One 7, e36395.
28. Petrov A.M. Giniatullin AR, Sitdikova GF & Zefirov AL (2008). The role of cGMP-dependent signaling pathway in synaptic vesicle cycle at the frog motor nerve terminals. J Neurosci 28, 13216-13222.
29. Petrov AM, Kasimov MR, Giniatullin AR, Tarakanova OI & Zefirov AL (2010). The role of cholesterol in the exo- and endocytosis of synaptic vesicles in frog motor nerve endings. Neurosci Behav Physiol 40, 894-901.
30. Petrov AM, Kudryashova KE, Odnoshivkina YG & Zefirov AL (2011). S{cyrillic}holesterol and lipid rats in the membrane of nerve terminal and membrane of synaptic vesicle. Neurochem J 5, 13-19.
31. Petrov AM, Naumenko NV, Uzinskaya KV, Giniatullin AR, Urazaev AK & Zefirov AL (2011). Increased non-quantal release of acetylcholine after inhibition of endocytosis by methyl-β-cyclodextrin: the role of vesicular acetylcholine transporter. Neuroscience 186, 1-12.
32. Picato-Juares G, Romero-Suarez S, Nieto-Posadas A, Llorente I, Jara-Oseguera A, Biggs M, Mclntosh TJ, Simon SA, Ladron-de-Guevara E, Islas L & Rosenbaum T (2011). Identification of a binding motif in the S5 helix that confers cholesterol sensitivity to the TRPV1 ion channel. J Biol Chem 286, 24966-24976.
33. Puchkov D & Haucke V (2013). Greasing the synaptic vesicle cycle by membrane lipids. Trends Cell Biol 23, 493-503.
34. Rodrigues HA, Lima RF, Fonseca MD, Amaral EA, Martinelli PM, Naves LA, GomezMV, Kushmerick C, PradoMA & Guatimosim C (2013). Membrane cholesterol regulates different modes of synaptic vesicle release and retrieval at the frog neuromuscular junction. Eur J Neurosci 38, 2978-2987.
35. Rose T, Schoenenberger P, Jezek K & Oertner TG (2013). Developmental refinement of vesicle cycling at Shaffer collateral synapses. Neuron 77, 1109-1121.
36. 2+ channels at perisynaptic glial cells of the frog neuromuscular junction. J Neurosci 16, 148-158.
37. 2+ signaling by axonal ryanodine receptors at the hippocampal mossy fiber synapse. Proc Natl Acad Sci U S A 105, 11998-12003.
38. Sodero AO,Weissmann C, Ledesmac MD & Dotti CG (2011). Cellular stress from excitatory neurotransmission contributes to cholesterol loss in hippocampal neurons aging in vitro. Neurobiol Aging 32, 1043-1053.
39. Song MY, Makino A & Yuan JX (2011). Role of reactive oxygen species and redox in regulating the function of transient receptor potential channels. Antioxid Redox Signal 15, 1549-1565.
40. Smith AJ, Sugita S & Charlton MP (2010). Cholesterol-dependent kinase activity regulates transmitter release from cerebellar synapses. J Neurosci 30, 6116-6121.
41. Tarakanova OI, Petrov AM & Zefirov AL (2011). The role of membrane cholesterol in neurotransmitter release from motor nerve terminals. Dokl Biol Sci 438, 138-140.
42. Teixeira G, Vieira LB, Gomez MV & Guatimosim C (2012). Cholesterol as a key player in the balance of evoked and spontaneous glutamate release in rat brain cortical synaptosomes. Neurochem Int 61, 1151-1159.
43. Tejada-Simon MV, Serrano F, Villasana LE, Kanterewicz BI, Wu GY, Quinn MT & Klann E (2005). Synaptic localization of a functional NADPH oxidase in the mouse hippocampus. Mol Cell Neurosci 29, 97-106.
44. Thyagarajan B, KrivitskayaN, Potian JG, Hognason K, Garcia CC & McArdle JJ (2009). Capsaicin protects mouse neuromuscular junctions from the neuroparalytic effects of botulinum neurotoxin A. J Pharmacol Exp Ther 331, 361-71.
45. Tong J, Borbat PP, Freed JH & Shin Y-K (2009). A scissors mechanism for stimulation of SNARE-mediated lipid mixing by cholesterol. Proc Natl Acad Sci U S A 106, 5141-6.
46. von Gersdorff H, Matthews G (1994). Inhibition of endocytosis by elevated internal calcium in a synaptic terminal. Nature 370, 652-655.
47. Wasser CR & Kavalali ET (2009). Leaky synapses: regulation of spontaneous neurotransmission in central synapses. Neuroscience 158, 177-188.
48. 2+ release channels (ryanodine receptors) by multiple mechanisms. J Biol Chem 274, 32680-32691.
49. 2 prosurvival effects in cultured endothelial cells. FASEB J 20:1501-1503.
50. Zamir O & Charlton MP (2006). Cholesterol and synaptic transmitter release at crayfish neuromuscular junctions. J Physiol 571, 83-99.
51. Zefirov A L & Petrov AM (2012). Lipids in the processes of exoand endocytosis of synaptic vesicles. Neurosci Behav Physiol 42, 144-152.