Increased Synaptophysin Is Involved in Inflammation-Induced Heat Hyperalgesia Mediated by Cyclin-Dependent Kinase 5 in Rats

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Zhang, Hong Hai ^a   Zhang, Xiao Qin ^a   Wang, Wen Yuan ^a   Xue, Qing Sheng ^a   Lu, Han ^a   Huang, Jin Lu ^b   Gui, Ting ^a   Yu, Bu Wei ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CYCLIN DEPENDENT KINASE 5; FREUND ADJUVANT; PROTEIN P25; PROTEIN P35; ROSCOVITINE; SNARE PROTEIN; SYNAPTOBREVIN 2; SYNAPTOPHYSIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN 1A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE COURSE; DISEASE DURATION; DRUG TARGETING; ENDOCYTOSIS; EXOCYTOSIS; HEAT SENSITIVITY; HYPERALGESIA; IMMUNOPRECIPITATION; INFLAMMATORY PAIN; MALE; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; SPINAL CORD DORSAL HORN; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; SYNAPTOSOME; UPREGULATION;

ANIMALS; BLOTTING, WESTERN; CYCLIN-DEPENDENT KINASE 5; FLUORESCENT ANTIBODY TECHNIQUE; FREUND'S ADJUVANT; HYPERALGESIA; IMMUNOPRECIPITATION; INFLAMMATION; MALE; PAIN; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTOPHYSIN; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

RATTUS;

EID: 84866979322     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046666     Document Type: Article

References (64)

1. Ji RR, Befort K, Brenner GJ, Woolf CJ, (2002) ERK MAP kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 upregulation and contributes to persistent inflammatory pain hypersensitivity. J Neurosci 22: 478-485.
2. Aley KO, Levine JD, (1999) Role of protein kinase A in the maintenance of inflammatory pain. J Neurosci 19: 2181-2186.
3. Premkumar LS, Ahern GP, (2000) Induction of vanilloid receptor channel activity by protein kinase C. Nature. 408: 985-990.
4. Tsai LH, Delalle I, Caviness VS, Chae T, (1994) p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature 371: 418-423.
5. Zheng M, Leung CL, Liem RKH, (1998) Region-specific expression of cyclin-dependent kinase 5 (cdk5) and its activators, p35 and p39, in the developing and adult rat central nervous system. J Neurobiol 35: 141-159.
6. Dhavan R, Tsai LH (2001) A decade of CDK5. Nat Rev Mol 749-759.
7. Tanaka T, Veeranna, Ohshima T, et al. (2001) Cyclin-dependent kinase 5 activity is critical for survival. J Nurosci 21: 550-558.
8. Pareek TK, Kulkarni AB, (2006) A New Player in Pain Signaling. Cell cycle 5: 585-588.
9. Pareek TK, Keller J, Kesavapany S, Pant HC, Iadarola MJ, et al. (2006) Cyclin-dependent kinase 5 activity regulates pain signaling. Proc. Natl. Acad. Sci. USA 103: 791-796.
10. Pareek TK, Keller J, Kesavapany S, Agarwal N, Kuner R, et al. (2007) Cyclin-dependent kinase 5 modulates nociceptive signaling through direct phosphorylation of transient receptor potential vanilloid 1, Proc Natl Acad Sci USA. 104: 660-665.
11. Yang YR, He Y, Zhang Y, Li Y, Han Y, et al. (2007) Activation of cyclin-dependent kinase 5 (Cdk5) in primary sensory and dorsal horn neurons by peripheral inflammation contributes to heat hyperalgesia. Pain 127: 109-120.
12. Kim SH, Ryan TA, (2010) CDK5 serves as a major control point in neurotransmitter release. Neuron 67: 797-809.
13. Tomizawa K, Ohta J, Matsushita M, Moriwaki A, Li ST, et al. (2002) Cdk5/p35 regulates neurotransmitter release through phosphorylation and downregulation of P/Q-type. J Neurosci 22: 2590-2597.
14. Lin RC, Scheller RH, (2000) Mechanisms of synaptic vesicle exocytosis. Annu Rev Cell Dev Biol 16: 19-49.
15. Jahn R, Scheller RH, (2006) SNAREs-engines for membrane fusion. Nature Reviews 7: 631-641.
16. Jahn R, Schiebler W, Ouimet C, Greengard P, (1985) A 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc Natl Acad Sci USA 82: 4237-4141.
17. Valtorta F, Pennuto M, Bonanomi D, Benfenati F, (2004) Synaptophysin: leading actor or walk-on role in synaptic vesicle exocytosis? Bioessays 26: 445-453.
18. Deák F, Schoch S, Liu X, Südhof TC, Kavalali ET, (2004) Synaptobrevin is essential for fast synaptic-vesicle endocytosis. Nat Cell Bio 6: 1102-1108.
19. Otto H, Hanson PI, Jahn R, (1997) Assembly and disassembly of a ternary complex of synaptobrevin, syntaxin, and SNAP-25 in the membrane of synaptic vesicles. Proc Natl Acad Sci USA 94: 6197-6201.
20. Van den Bogaart G, Holt MG, Bunt G, Riedel D, Wouters FS, et al. (2010) One SNARE complex is sufficient for membrane fusion. Nat Struct Mol 17: 358-364.
21. Alder J, Kanki H, Valtorta F, Greengard P, Poo M, (1995) Overexpression of synaptophysin enhances neurotransmitter secretion at Xenopus neuromuscular synapses. J Neurosci 15: 511-519.
22. Samuels BA, Hsueh YP, Shu T, Liang H, Tseng HC, et al. (2007) Cdk5 promotes synaptogenesis by regulating the subcellular distribution of the MAGUK family member CASK. Neuron 56: 823-837.
23. Marqueze-Pouey B, Wisden W, Malosio M, Betz H, (1991) Differential expression of synaptophysin and synaptoporin mRNAs in the postnatal rat central nervous system. J Neurosci 11: 3388-3397.
24. Chou AK, Muhammad R, Huang SM, Chen JT, Wu CL, et al. (2002) Altered synaptophysin expression in the rat spinal cord after chronic constriction injury of sciatic nerve. Neuro Lett 333: 155-158.
25. Lin JY, Peng B, Yang ZW, Min S, (2011) Number of synapses increased in the rat spinal dorsal horn after sciatic nerve transection: A stereological study. Brain Res Bull 84: 430-433.
26. CamprubiRobles M, Planells-Cases R, Ferrer-Montiel A, (2009) Differential contribution of SNARE-dependent exocytosis to inflammatory potentiation of TRPV1 in nociceptors. FEBS J 23: 3722-373.
27. Charlton E, (1995) Ethical guidelines for pain research in humans. Committee on Ethical Issues of the International Association for the Study of Pain. Pain 63: 277.
28. Yaksh TL, Rudy TA, (1976) Chronic catheterization of the spinal subarachnoid space. Physiology and behavior 17: 1031-1036.
29. Hargreaves K, Dubner R, Brown F, Flores C, Joris J, (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32: 77-88.
30. Bhaskar K, Shareef MM, Sharma VM, Shetty A, Ramamohan Y, et al. (2004) Co-purification and localization of Munc18-1 (p67) and Cdk5 with neuronal cytoskeletal proteins. Neurochem Int 44: 35-44.
31. Nikolic M, Dudek H, Kwon YT, Ramos Y, Tsai LH, (1996) The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes & development 10: 816-825.
32. Zhang B, Tao F, Liaw WJ, Bredt DS, Johns RA, et al. (2003) Effect of knock down of spinal cord PSD-93/chapsin-110 on persistent pain induced by complete Freund's adjuvant and peripheral nerve injury. Pain 106: 187-196.
33. Pollonini G, Gao V, Rabe A, Palminiello S, Albertini G, et al. (2008) Abnormal expression of synaptic proteins and neurotrophin-3 in the Down syndrome mouse model Ts65Dn. Neuroscience 156: 99-106.
34. Kunz S, Niederberger E, Ehnert C, Coste O, Pfenninger A, et al. (2004) The calpain inhibitor MDL 28170 prevents inflammation-induced neurofilament light chain breakdown in the spinal cord and reduces thermal hyperalgesia. Pain 110: 409-418.
35. Xie W, Uchida H, Nagai J, Ueda M, Chun J, et al. (2010) Calpain-mediated down-regulation of myelin-associated glycoprotein in lysophosphatidic acid-induced neuropathic pain. J. Neurochem. 113: 1002-1011.
36. Taniguchi S, Fujita Y, Hayashi S, Kakita A, Takahashi H, et al. (2001) Calpain-mediated degradation of p35 to p25 in postmortem human and rat brains. FEBS letters 489: 46-50.
37. van den Bogaart G, Holt MG, Bunt G, Riedel D, Wouters FS, et al. (2010) One SNARE complex is sufficient for membrane fusion. Nat Struct Mol 17: 358-364.
38. Chen YA, Scales SJ, Patel SM, Doung YC, Scheller RH, (1999) SNARE complex formation is triggered by Ca2+ and drives membrane fusion. Cell 97: 165-174.
39. Südhof TC, (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27: 509-547.
40. Washbourne P, Schiavo G, Montecucco C, (1995) Vesicle-associated membrane protein-2 (synaptobrevin-2) forms a complex with synaptophysin. Biochem J 305: 721-724.
41. Schoch S, Deák F, Königstorfer A, Mozhayeva M, Sara Y, et al. (2001) SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 294: 1117-1122.
42. Südhof TC, (1995) The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375: 645-653.
43. Pennuto M, Bonanomi D, Benfenati F, Valtorta F, (2003) Synaptophysin I controls the targeting of VAMP2/synaptobrevin II to synaptic vesicles. Mol Biol Cell 14: 4909-4919.
44. Edelmann L, Hanson P, Chapman E, Jahn R, (1995) Synaptobrevin binding to synaptophysin: a potential mechanism for controlling the exocytotic fusion machine. EMBO J 14: 224-231.
45. Becher A, Drenckhahn A, Pahner I, Margittai M, Jahn R, et al. (1999) The synaptophysin-synaptobrevin complex: a hallmark of synaptic vesicle maturation. J Neurosci 19: 1922-1931.
46. Eshkind LG, Leube RE, (1995) Mice lacking synaptophysin reproduce and form typical synaptic vesicles. Cell Tissue Res 282: 423-433.
47. Evans G, Cousin M, (2005) Tyrosine phosphorylation of synaptophysin in synaptic vesicle recycling. Biochem Soc Trans 33: 1350-1353.
48. Gordon SL, Leube RE, Cousin MA, (2011) Synaptophysin is required for synaptobrevin retrieval during synaptic vesicle endocytosis. J Neurosci 31: 14032-14036.
49. Kwon SE, Chapman ER, (2011) Synaptophysin regulates the kinetics of synaptic vesicle endocytosis in central neurons. Neuron 70: 847-854.
50. Tan TC, Valova VA, Malladi CS, Graham ME, Berven LA, et al. (2003) Cdk5 is essential for synaptic vesicle endocytosis. Nat Cell Biol 5: 701-710.
51. Ou CY, Poon VY, Maeder CI, Watanabe S, Lehrman EK, et al. (2010) Two cyclin-dependent kinase pathways are essential for polarized trafficking of presynaptic components. Cell 141: 846-858.
52. Janz R, Südhof TC, Hammer RE, Unni V, Siegelbaum SA, et al. (1999) Essential roles in synaptic plasticity for synaptogyrin I and synaptophysin I. Neuron. 24: 687-700.
53. Woolf CJ, Salter MW, (2000) Neuronal plasticity: increasing the gain in pain. Science 288: 1765-1768.
54. Pockett S, (1995) Spinal cord synaptic plasticity and chronic pain. Anesth Anal 80: 173-179.
55. Keda H, Heinke B, Ruscheweyh R, Sandkühler J, (2003) Synaptic plasticity in spinal lamina I projection neurons that mediate hyperalgesia. Science 299: 1237-1240.
56. Meijer L, Borgne A, Mulner O, Chong JPJ, Blow JJ, Inagaki N, et al. (1997) Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur J Biochem 243: 527-536.
57. Ino H, Ishizuka T, Chiba T, Tatibana M, (1994) Expression of Cdk5 (PSSALRE kinase), a neural cdc2-related protein kinase, in the mature and developing mouse central and peripheral nervous systems. Brain Res 661: 196-206.
58. Tsai LH, Takahashi T, Caviness V, Harlow E, (1993) Activity and expression pattern of cyclin-dependent kinase 5 in the embryonic mouse nervous system. Development 119: 1029-1040.
59. Matsushita M, Tomizawa K, Lu YF, Moriwaki A, Tokuda M, Itano T, et al. (1996) Distinct cellular compartment of cyclin-dependent kinase 5 (Cdk5) and neuron-specific Cdk5 activator protein (p35nck5a) in the developing rat cerebellum. Brain Res 734: 319-22.
60. Whittaker SR, Walton MI, Garrett MD, Workman P, (2004) The Cyclin-dependent kinase inhibitor CYC202 (R-roscovitine) inhibits retinoblastoma protein phosphorylation, causes loss of Cyclin D1, and activates the mitogen-activated protein kinase pathway. Cancer research 64: 262.
61. Nguyen M, Mushynski W, Julien J, Correspondence J, (2002) Cycling at the interface between neurodevelopment and neurodegeneration. Cell Death Diff 9: 1294-1306.
62. Alder J, Lu B, Valtorta F, Greengard P, Poo MM, (1992) Calcium-dependent transmitter secretion reconstituted in Xenopus oocytes: requirement for synaptophysin. Science 257: 657-661.
63. Rehm H, Wiedenmann B, Betz H, (1986) Molecular characterization of synaptophysin, a major calcium-binding protein of the synaptic vesicle membrane. EMBO J 5: 535-541.
64. Guo W, Wei F, Zou S, Robbins MT, Sugiyo S, et al. (2004) Group I metabotropic glutamate receptor NMDA receptor coupling and signaling cascade mediate spinal dorsal horn NMDA receptor 2B tyrosine phosphorylation associated with inflammatory hyperalgesia. J Neurosci 24: 9161-9173.