Possible involvement of syntaxin 1A downregulation in the late phase of allodynia induced by peripheral nerve injury

Neuroscience

Volumn 175, Issue , 2011, Pages 344-357

  Fukushima, T ^a   Takasusuki, T ^a   Tomitori, H ^b   Hori, Y ^a  

^a DOKKYO MEDICAL UNIVERSITY   (Japan)

^b CHIBA INSTITUTE OF SCIENCE   (Japan)

Author keywords

Allodynia; Antisense oligodeoxynucleotide; Double stranded RNA; MEPSCs; Spinal superficial dorsal horn; Syntaxin 1A

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; NEUROTRANSMITTER; SYNTAXIN 1A;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; MALE; MOUSE; NERVE ELONGATION; NERVE LIGATION; NERVE SPROUTING; NOCICEPTION; NONHUMAN; PATHOGENESIS; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; RNA INTERFERENCE; SPINAL CORD; SPINAL CORD DORSAL HORN; SYNAPSE;

ANIMALS; DISEASE MODELS, ANIMAL; DOWN-REGULATION; HYPERALGESIA; MALE; MICE; MICE, INBRED ICR; NEURONAL PLASTICITY; ORGAN CULTURE TECHNIQUES; PERIPHERAL NERVOUS SYSTEM DISEASES; POSTERIOR HORN CELLS; SCIATIC NEUROPATHY; SYNTAXIN 1;

EID: 78951495710     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.11.049     Document Type: Article

References (85)

1. Aguado F., Majo G., Ruiz-Montasell B., Llorens J., Marsal J., Blasi J. Syntaxin 1A and 1B display distinct distribution patterns in the rat peripheral nervous system. Neuroscience 1999, 88:437-446.
2. al-Ghoul W.M., Volsi G.L., Weinberg R.J., Rustioni A. Glutamate immunocytochemistry in the dorsal horn after injury or stimulation of the sciatic nerve of rats. Brain Res Bull 1993, 30:453-459.
3. Baba H., Doubell T.P., Woolf C.J. Peripheral inflammation facilitates Abeta fiber-mediated synaptic input to the substantia gelatinosa of the adult rat spinal cord. J Neurosci 1999, 19:859-867.
4. Balasubramanyan S., Stemkowski P.L., Stebbing M.J., Smith P.A. Sciatic chronic constriction injury produces cell-type-specific changes in the electrophysiological properties of rat substantia gelatinosa neurons. J Neurophysiol 2006, 96:579-590.
5. Bao L., Wang H.F., Cai H.-J., Tong Y.-G., Jin S.-X., Lu Y.-J., Grant G., Hoekfelt T., Zhang X. Peripheral axotomy induces only very limited sprouting of coarse myelinated afferents into inner lamina II of rat spinal cord. Eur J Neurosci 2002, 16:175-185.
6. Bester H., Beggs S., Woolf C.J. Changes in tactile stimuli-induced behavior and c-Fos expression in the superficial dorsal horn and in parabrachial nuclei after sciatic nerve crush. J Comp Neurol 2000, 428:45-61.
7. Bezprozvanny I., Scheller R.H., Tsien R.W. Functional impact of syntaxin on gating of N-type and Q-type calcium channels. Nature 1995, 378:623-626.
8. 2+ channel gating. Proc Natl Acad Sci U S A 2000, 97:13943-13948.
9. Campbell J.N., Meyer R.A. Mechanisms of neuropathic pain. Neuron 2006, 52:77-92.
10. Catterall W.A., Few A.P. Calcium channel regulation and presynaptic plasticity. Neuron 2008, 59:882-901.
11. Chen Y., Balasubramanyan S., Lai A.Y., Todd K.G., Smith P.A. Effects of sciatic nerve axotomy on excitatory synaptic transmission in rat substantia gelatinosa. J Neurophysiol 2009, 102:3203-3215.
12. Chou A.K., Muhammad R., Huang S.M., Chen J.T., Wu C.L., Lin C.R., Lee T.H., Lin S.H., Lu C.Y., Yang L.C. Altered synaptophysin expression in the rat spinal cord after chronic constriction injury of sciatic nerve. Neurosci Lett 2002, 333:155-158.
13. 2+ channels in the rat spinal cord following chronic constrictive nerve injury. Exp Brain Res 2002, 147:456-463.
14. Costigan M., Scholz J., Woolf C.J. Neuropathic pain: a maladaptive response of the nervous system to damage. Annu Rev Neurosci 2009, 32:1-32.
15. Cunha T.M., Verri W.A., Vivancos G.G., Moreira I.F., Reis S., Parada C.A., Cunha F.Q., Ferreira S.H. An electronic pressure-meter nociception paw test for mice. Braz J Med Biol Res 2004, 37:401-407.
16. 2d subunits of voltage-gated calcium channels. Trends Pharmacol Sci 2007, 28:220-228.
17. 2+ entry in mouse hippocampal neurons. Neurosci Lett 2007, 415:130-134.
18. Gerber S.H., Rah J.C., Min S.W., Liu X., de Wit H., Dulubova I., Meyer A.C., Rizo J., Arancillo M., Hammer R.E., Verhage M., Rosenmund C., Sudhof T.C. Conformational switch of syntaxin-1 controls synaptic vesicle fusion. Science 2008, 321:1507-1510.
19. Hughes D.I., Scott D.T., Todd A.J., Riddell J.S. Lack of evidence for sprouting of Ab afferents into the superficial laminas of the spinal cord dorsal horn after nerve section. J Neurosci 2003, 23:9491-9499.
20. Hylden J.L.K., Wilcox G.L. Intrathecal morphine in mice: a new technique. Eur J Pharmacol 1980, 67:313-316.
21. Ibuki T., Hama A.T., Wang X.T., Pappas G.D., Sagen J. Loss of GABA-immunoreactivity in the spinal dorsal horn of rats with peripheral nerve injury and promotion of recovery by adrenal medullary grafts. Neuroscience 1997, 76:845-858.
22. Igarashi M., Kozaki S., Terakawa S., Kawano S., Ide C., Komiya Y. Growth cone collapse and inhibition of neurite growth by Botulinum neurotoxin Ca: a t-SNARE is involved in axonal growth. J Cell Biol 1996, 134:205-215.
23. Inoue A., Akagawa K. Neuron-specific antigen HPC-1 from bovine brain reveals strong homology to epimorphin, an essential factor involved in epithelial morphogenesis: identification of an novel protein family. Biochem Biophys Res Commun 1992, 187:1144-1150.
24. Inoue A., Akagawa K. Neuron specific expression of a membrane protein, HPC-1: tissue distribution, and cellular and subcellular localization of immunoreactivity and mRNA. Brain Res Mol Brain Res 1993, 19:121-128.
25. Inoue A., Obata K., Akagawa K. Cloning and sequence analysis of cDNA for a neuronal cell membrane antigen, HPC-1. J Biol Chem 1992, 267:10613-10619.
26. Iwata H., Takasusuki T., Yamaguchi S., Hori Y. NMDA receptor 2B subunit-mediated synaptic transmission in the superficial dorsal horn of peripheral nerve-injured neuropathic mice. Brain Res 2007, 1135:92-101.
27. Jahn R., Scheller R.H. SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 2006, 7:631-643.
28. Jarvis S.E., Zamponi G.W. Distinct molecular determinants govern syntaxin 1A-mediated inactivation and G-protein inhibition of N-type calcium channels. J Neurosci 2001, 21:2939-2948.
29. 2+ channels, cytoplasmic messengers and proteins of the synaptic vesicle release complex. Trends Pharmacol Sci 2001, 22:519-525.
30. Jarvis S.E., Magga J.M., Beedle A.M., Braun J.E., Zamponi G.W. G protein modulation of N-type calcium channels is facilitated by physical interactions between syntaxin 1A and Gbg. J Biol Chem 2000, 275:6388-6394.
31. Jarvis S.E., Barr W., Feng Z.P., Hamid J., Zamponi G.W. Molecular determinants of syntaxin 1 modulation of N-type calcium channels. J Biol Chem 2002, 277:44399-44407.
32. Kato G., Kawasaki Y., Koga K., Uta D., Kosugi M., Yasaka T., Yoshimura M., Ji R.R., Strassman A.M. Organization of intralaminar and translaminar neuronal connectivity in the superficial spinal dorsal horn. J Neurosci 2009, 29:5088-5099.
33. 2+ concentration in the spinal dorsal horn in an animal model of neuropathic pain. Pain 1996, 68:85-96.
34. Keith R.K., Poage R.E., Yokoyama C.T., Catterall W.A., Meriney S.D. Bidirectional modulation of transmitter release by calcium channel/syntaxin interactions in vivo. J Neurosci 2007, 27:265-269.
35. Kimura K., Mizoguchi A., Ide C. Regulation of growth cone extension by SNARE proteins. J Histochem Cytochem 2003, 51:429-433.
36. Koerber H.R., Mirnics K., Brown P.B., Mendell L.M. Central sprouting and functional plasticity of regenerated primary afferents. J Neurosci 1994, 14:3655-3671.
37. Koh S., Yamamoto A., Inoue A., Inoue Y., Akagawa K., Kawamura Y., Kawamoto K., Tashiro Y. Immunoelectron microscopic localization of the HPC-1 antigen in rat cerebellum. J Neurocytol 1993, 22:995-1005.
38. Kohama I., Ishikawa K., Kocsis J.D. Synaptic reorganization in the substantia gelatinosa after peripheral nerve neuroma formation: aberrant innervation of lamina II neurons by Ab afferents. J Neurosci 2000, 20:1538-1549.
39. Kohno T., Moore K.A., Baba H., Woolf C.J. Peripheral nerve injury alters excitatory synaptic transmission in lamina II of the rat dorsal horn. J Physiol (Lond) 2003, 548:131-138.
40. Latremoliere A., Woolf C.J. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 2009, 10:895-926.
41. Lekan H.A., Carlton S.M., Coggeshall R.E. Sprouting of Ab fibers into lamina II of the rat dorsal horn in peripheral neuropathy. Neurosci Lett 1996, 208:147-150.
42. 2d-1 subunit upregulation contributes to peripheral nerve injury-induced tactile allodynia. J Neurosci 2004, 24:8494-8499.
43. 1 subunit mediates spinal hyperexcitability in pain modulation. Pain 2006, 125:20-34.
44. Liu X.-G., Sandkuehler J. Long-term potentiation of C-fiber-evoked potentials in the rat spinal dorsal horn is prevented by spinal N-methyl-d-aspartic acid receptor blockage. Neurosci Lett 1995, 191:43-46.
45. Liu X.-G., Sandkuehler J. Characterization of long-term potentiation of C-fiber-evoked potentials in spinal dorsal horn of adult rat: essential role of NK1 and NK2 receptors. J Neurophysiol 1997, 78:1973-1982.
46. Margittai M., Widengren J., Schweinberger E., Schroder G.F., Felekyan S., Haustein E., Konig M., Fasshauer D., Grubmuller H., Jahn R., Seidel C.A. Single-molecule fluorescence resonance energy transfer reveals a dynamic equilibrium between closed and open conformations of syntaxin 1. Proc Natl Acad Sci U S A 2003, 100:15516-15521.
47. Masliah E., Fagan A.M., Terry R.D., DeTeresa R., Mallory M., Gage F.H. Reactive synaptogenesis assessed by synaptophysin immunoreactivity is associated with GAP-43 in the dentate gyrus of the adult rat. Exp Neurol 1991, 113:131-142.
48. McMahon S.B., Lewin G., Bloom S.R. The consequences of long-term topical capsaicin application in the rat. Pain 1991, 44:301-310.
49. Mitchell S.J., Ryan T.A. Munc18-dependent regulation of synaptic vesicle exocytosis by syntaxin-1A in hippocampal neurons. Neuropharmacology 2005, 48:372-380.
50. Moller K.A., Johansson B., Berge O.G. Assessing mechanical allodynia in the rat paw with a new electronic algometer. J Neurosci Methods 1998, 84:41-47.
51. Moore K.A., Baba H., Woolf C.J. Synaptic transmission and plasticity in the superficial dorsal horn. Prog Brain Res 2000, 129:63-80.
52. Moore K.A., Kohno T., Karchewski L.A., Scholz J., Baba H., Woolf C.J. Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J Neurosci 2002, 22:6724-6731.
53. 2d-1 subunit following partial sciatic nerve injury. Brain Res Mol Brain Res 2001, 95:1-8.
54. Nguyen D., Deng P., Matthews E.A., Kim D.S., Feng G., Dickenson A.H., Xu Z.C., Luo Z.D. Enhanced pre-synaptic glutamate release in deep-dorsal horn contributes to calcium channel alpha-2-delta-1 protein-mediated spinal sensitization and behavioral hypersensitivity. Mol Pain 2009, 5:6.
55. Okamoto M., Baba H., Goldstein P.A., Higashi H., Shimoji K., Yoshimura M. Functional reorganization of sensory pathways in the rat spinal dorsal horn following peripheral nerve injury. J Physiol (Lond) 2001, 532:241-250.
56. Pubols L.M., Bowen D.C. Lack of central sprouting of primary afferent fibers after ricin deafferentation. J Comp Neurol 1988, 275:282-287.
57. Randic M., Jiang M.C., Cerne R. Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord. J Neurosci 1993, 13:5228-5241.
58. Ruiz-Montasell B., Aguado F., Majo G., Chapman E.R., Canals J.M., Marsal J., Blasi J. Differential distribution of syntaxin isoforms 1A and 1B in the rat central nervous system. Eur J Neurosci 1996, 8:2544-2552.
59. Sandkuehler J., Liu X. Induction of long-term potentiation at spinal synapses by noxious stimulation or nerve injury. Eur J Neurosci 1998, 10:2476-2480.
60. Sandkuhler J. Models and mechanisms of hyperalgesia and allodynia. Physiol Rev 2009, 89:707-758.
61. Sasaki M., Tohda C., Kuraishi Y. Region-specific increase in glutamate release from dorsal horn of rats with adjuvant inflammation. Neuroreport 1998, 9:3219-3222.
62. Scheibel M.E., Scheibel A.B. Terminal axonal patterns in cat spinal cord. II. The dorsal horn. Brain Res 1968, 9:32-58.
63. Schoffnegger D., Ruscheweyh R., Sandkuhler J. Spread of excitation across modality borders in spinal dorsal horn of neuropathic rats. Pain 2008, 135:300-310.
64. Schwartz E.S., Kim H.Y., Wang J., Lee I., Klann E., Chung J.M., Chung K. Persistent pain is dependent on spinal mitochondrial antioxidant levels. J Neurosci 2009, 29:159-168.
65. Seltzer Z., Dubner R., Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 1990, 43:205-218.
66. Shehab S.A., Spike R.C., Todd A.J. Evidence against cholera toxin B subunit as a reliable tracer for sprouting of primary afferents following peripheral nerve injury. Brain Res 2003, 964:218-227.
67. Shortland P., Woolf C.J. Chronic peripheral nerve section results in a rearrangement of the central axonal arborizations of axotomized Ab primary afferent neurons in the rat spinal cord. J Comp Neurol 1993, 330:65-82.
68. Snutch T.P. Targeting chronic and neuropathic pain: the N-type calcium channel comes of age. NeuroRx 2005, 2:662-670.
69. Sudhof T.C. The synaptic vesicle cycle. Annu Rev Neurosci 2004, 27:509-547.
70. Sun H., Xu J., Penna K.B.D., Benz R., Kinose F., Holder D.J., Koblan K.S., Gerhold D.L., Wang H. Dorsal horn-enriched genes identified by DNA microarray, in situ hybridization and immunohistochemistry. BMC Neurosci 2002, 3:11.
71. Szentagothai J. Neuronal and synaptic arrangement in the substantia gelatinosa rolandi. J Comp Neurol 1964, 122:219-239.
72. Takasusuki T., Fujiwara T., Yamaguchi S., Fukushima T., Akagawa K., Hori Y. Enhancement of synaptic transmission and nociceptive behaviour in HPC-1/syntaxin 1A knockout mice following peripheral nerve injury. Eur J Neurosci 2007, 26:2179-2187.
73. Toyoda H., Zhao M.G., Zhuo M. Enhanced quantal release of excitatory transmitter in anterior cingulate cortex of adult mice with chronic pain. Mol Pain 2009, 5:4.
74. 2+ channels. Neuroscience 2001, 104:599-607.
75. Wang H., Sun H., Della Penna K., Benz R.J., Xu J., Gerhold D.L., Holder D.J., Koblan K.S. Chronic neuropathic pain is accompanied by global changes in gene expression and shares pathobiology with neurodegenerative diseases. Neuroscience 2002, 114:529-546.
76. Watanabe T., Fujiwara T., Komazaki S., Yamaguchi K., Tajima O., Akagawa K. HPC-1/syntaxin 1A suppresses exocytosis of PC12 cells. J Biochem 1999, 125:685-689.
77. Westenbroek R.E., Sakurai T., Elliott E.M., Hell J.W., Starr T.V., Snutch T.P., Catterall W.A. Immunochemical identification and subcellular distribution of the alpha 1A subunits of brain calcium channels. J Neurosci 1995, 15:6403-6418.
78. Willis W.D., Coggeshall R.E. Sensory mechanisms of the spinal cord 2004, Kluwer Academic/Plenum Publishers, New York.
79. Wiser O., Bennett M.K., Atlas D. Functional interaction of syntaxin and SNAP-25 with voltage-sensitive L- and N-type Ca2+ channels. EMBO J 1996, 15:4100-4110.
80. Woolf C.J., Shortland P., Coggeshall R.E. Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 1992, 355:75-78.
81. Woolf C.J., Shortland P., Reynolds M., Ridings J., Doubell T., Coggeshall R.E. Reorganization of central terminals of myelinated primary afferents in the rat dorsal horn following peripheral axotomy. J Comp Neurol 1995, 360:121-134.
82. Wu M.N., Fergestad T., Lloyd T.E., He Y., Broadie K., Bellen H.J. Syntaxin 1A interacts with multiple exocytic proteins to regulate neurotransmitter release in vivo. Neuron 1999, 23:593-605.
83. Yamaguchi K., Nakayama T., Fujiwara T., Akagawa K. Enhancement of neurite-sprouting by suppression of HPC-1/syntaxin 1A activity in cultured vertebrate nerve cells. Brain Res 1996, 740:185-192.
84. Zhou Q., Xiao J., Liu Y. Participation of syntaxin 1A in membrane trafficking involving neurite elongation and membrane expansion. J Neurosci Res 2000, 61:321-328.
85. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.