Intrathecally administered Sema3A protein attenuates neuropathic pain behavior in rats with chronic constriction injury of the sciatic nerve

Neuroscience Research

Volumn 69, Issue 1, 2011, Pages 17-24

  Hayashi, Michiko ^a,d   Kamiya, Yoshinori ^a,d   Itoh, Hideki ^a   Higashi, Tomoko ^a,b   Miyazaki, Tomoyuki ^a,d   Funakoshi, Kengo ^a   Yamashita, Naoya ^a   Goshima, Yoshio ^a   Andoh, Tomio ^a,b   Yamada, Yoshitsugu ^c   Goto, Takahisa ^a  

^a YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b TEIKYO UNIVERSITY MIZONOKUCHI HOSPITAL   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d Pain Mechanism Research Group   (Japan)

Author keywords

Axonal guidance factor; Mechanical allodynia; Peripheral nerve injury; Spinal cord dorsal horn; Sprouting of myelinated nerve terminals; Synaptic re organization

Indexed keywords

NEUROPILIN 1; PLEXIN; SEMAPHORIN 3A;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HEAT INJURY; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; MALE; NERVE COMPRESSION; NERVE ENDING; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCIATIC NERVE; SPINAL CORD;

ANIMALS; CONSTRICTION, PATHOLOGIC; GLYCOPROTEINS; HYPERALGESIA; INJECTIONS, SPINAL; LECTINS; MALE; NERVE FIBERS, MYELINATED; NERVE TISSUE PROTEINS; NEURALGIA; PERIPHERAL NERVOUS SYSTEM DISEASES; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ATRIAL NATRIURETIC FACTOR; RECEPTORS, CELL SURFACE; SCIATIC NERVE; SCIATIC NEUROPATHY; SEMAPHORIN-3A; SPINAL CORD; SYNAPSES;

EID: 78649889197     PISSN: 01680102     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neures.2010.09.006     Document Type: Article

References (42)

1. Agudo M., Robinson M., Cafferty W., Bradbury E.J., Kilkenny C., Hunt S.P., McMahon S.B. Regulation of neuropilin 1 by spinal cord injury in adult rats. Mol. Cell. Neurosci. 2005, 28:475-484.
2. Ara J., Bannerman P., Hahn A., Ramirez S., Pleasure D. Modulation of sciatic nerve expression of class 3 semaphorins by nerve injury. Neurochem. Res. 2004, 29:1153-1159.
3. Bailey A.L., Ribeiro-da-Silva A. Transient loss of terminals from non-peptidergic nociceptive fibers in the substantia gelatinosa of spinal cord following chronic constriction injury of the sciatic nerve. Neuroscience 2006, 138:675-690.
4. Bao L., Wang H.F., Cai H.J., Tong Y.G., Jin S.X., Lu Y.J., Grant G., Hokfelt 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.
5. Bennett D.L., French J., Priestley J.V., McMahon S.B. NGF but not NT-3 or BDNF prevents the A fiber sprouting into lamina II of the spinal cord that occurs following axotomy. Mol. Cell. Neurosci. 1996, 8:211-220.
6. Bennett G.J., Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988, 33:87-107.
7. Doubell T.P., Mannion R.J., Woolf C.J. Intact sciatic myelinated primary afferent terminals collaterally sprout in the adult rat dorsal horn following section of a neighbouring peripheral nerve. J. Comp. Neurol. 1997, 380:95-104.
8. Gardell L.R., Wang R., Ehrenfels C., Ossipov M.H., Rossomando A.J., Miller S., Buckley C., Cai A.K., Tse A., Foley S.F., Gong B., Walus L., Carmillo P., Worley D., Huang C., Engber T., Pepinsky B., Cate R.L., Vanderah T.W., Lai J., Sah D.W., Porreca F. Multiple actions of systemic artemin in experimental neuropathy. Nat. Med. 2003, 9:1383-1389.
9. Goshima Y., Kawakami T., Hori H., Sugiyama Y., Takasawa S., Hashimoto Y., Kagoshima-Maezono M., Takenaka T., Misu Y., Strittmatter S.M. A novel action of collapsin: collapsin-1 increases antero- and retrograde axoplasmic transport independently of growth cone collapse. J. Neurobiol. 1997, 33:316-328.
10. Goshima Y., Nakamura F., Strittmatter P., Strittmatter S.M. Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature 1995, 376:509-514.
11. Goshima Y., Sasaki Y., Nakayama T., Ito T., Kimura T. Functions of semaphorins in axon guidance and neuronal regeneration. Jpn. J. Pharmacol. 2000, 82:273-279.
12. Hughes D.I., Scott D.T., Todd A.J., Riddell J.S. Lack of evidence for sprouting of Abeta afferents into the superficial laminas of the spinal cord dorsal horn after nerve section. J. Neurosci. 2003, 23:9491-9499.
13. Ji R.R., Strichartz G. Cell signaling and the genesis of neuropathic pain. Sci. STKE 2004, 2004:reE14.
14. Kaneko S., Iwanami A., Nakamura M., Kishino A., Kikuchi K., Shibata S., Okano H.J., Ikegami T., Moriya A., Konishi O., Nakayama C., Kumagai K., Kimura T., Sato Y., Goshima Y., Taniguchi M., Ito M., He Z., Toyama Y., Okano H. A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord. Nat. Med. 2006, 12:1380-1389.
15. 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. 2003, 548:131-138.
16. Lekan H.A., Carlton S.M., Coggeshall R.E. Sprouting of A beta fibers into lamina II of the rat dorsal horn in peripheral neuropathy. Neurosci. Lett. 1996, 208:147-150.
17. Mannion R.J., Doubell T.P., Coggeshall R.E., Woolf C.J. Collateral sprouting of uninjured primary afferent A-fibers into the superficial dorsal horn of the adult rat spinal cord after topical capsaicin treatment to the sciatic nerve. J. Neurosci. 1996, 16:5189-5195.
18. Molander C., Xu Q., Grant G. The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord. J. Comp. Neurol. 1984, 230:133-141.
19. Nagano M., Sakai A., Takahashi N., Umino M., Yoshioka K., Suzuki H. Decreased expression of glial cell line-derived neurotrophic factor signaling in rat models of neuropathic pain. Br. J. Pharmacol. 2003, 140:1252-1260.
20. Nakamura F., Ugajin K., Yamashita N., Okada T., Uchida Y., Taniguchi M., Ohshima T., Goshima Y. Increased proximal bifurcation of CA1 pyramidal apical dendrites in sema3A mutant mice. J. Comp. Neurol. 2009, 516:360-375.
21. Nakamura S., Myers R.R. Myelinated afferents sprout into lamina II of L3-5 dorsal horn following chronic constriction nerve injury in rats. Brain Res. 1999, 818:285-290.
22. Niclou S.P., Ehlert E.M., Verhaagen J. Chemorepellent axon guidance molecules in spinal cord injury. J. Neurotrauma 2006, 23:409-421.
23. Obata K., Yamanaka H., Dai Y., Mizushima T., Fukuoka T., Tokunaga A., Noguchi K. Differential activation of MAPK in injured and uninjured DRG neurons following chronic constriction injury of the sciatic nerve in rats. Eur. J. Neurosci. 2004, 20:2881-2895.
24. Obata K., Yamanaka H., Kobayashi K., Dai Y., Mizushima T., Katsura H., Fukuoka T., Tokunaga A., Noguchi K. Role of mitogen-activated protein kinase activation in injured and intact primary afferent neurons for mechanical and heat hypersensitivity after spinal nerve ligation. J. Neurosci. 2004, 24:10211-10222.
25. 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. 2001, 532:241-250.
26. Sakai A., Asada M., Seno N., Suzuki H. Involvement of neural cell adhesion molecule signaling in glial cell line-derived neurotrophic factor-induced analgesia in a rat model of neuropathic pain. Pain 2008, 137:378-388.
27. Shearer M.C., Niclou S.P., Brown D., Asher R.A., Holtmaat A.J., Levine J.M., Verhaagen J., Fawcett J.W. The astrocyte/meningeal cell interface is a barrier to neurite outgrowth which can be overcome by manipulation of inhibitory molecules or axonal signalling pathways. Mol. Cell. Neurosci. 2003, 24:913-925.
28. Takahashi T., Fournier A., Nakamura F., Wang L.H., Murakami Y., Kalb R.G., Fujisawa H., Strittmatter S.M. Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors. Cell 1999, 99:59-69.
29. Tanelian D.L., Barry M.A., Johnston S.A., Le T., Smith G.M. Semaphorin III can repulse and inhibit adult sensory afferents in vivo. Nat. Med. 1997, 3:1398-1401.
30. Tang X.Q., Cai J., Nelson K.D., Peng X.J., Smith G.M. Functional repair after dorsal root rhizotomy using nerve conduits and neurotrophic molecules. Eur. J. Neurosci. 2004, 20:1211-1218.
31. Tarpley J.W., Kohler M.G., Martin W.J. The behavioral and neuroanatomical effects of IB4-saporin treatment in rat models of nociceptive and neuropathic pain. Brain Res. 2004, 1029:65-76.
32. Tong Y.G., Wang H.F., Ju G., Grant G., Hokfelt T., Zhang X. Increased uptake and transport of cholera toxin B-subunit in dorsal root ganglion neurons after peripheral axotomy: possible implications for sensory sprouting. J. Comp. Neurol. 1999, 404:143-158.
33. Watanabe K., Konno S., Sekiguchi M., Sasaki N., Honda T., Kikuchi S. Increase of 200-kDa neurofilament-immunoreactive afferents in the substantia gelatinosa in allodynic rats induced by compression of the dorsal root ganglion. Spine 2007, 32:1265-1271.
34. Woolf C.J., Mannion R.J. Neuropathic pain: aetiology, symptoms, mechanisms, and management. Lancet 1999, 353:1959-1964.
35. Woolf C.J., Salter M.W. Neuronal plasticity: increasing the gain in pain. Science 2000, 288:1765-1769.
36. Woolf C.J., Shortland P., Coggeshall R.E. Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 1992, 355:75-78.
37. 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.
38. Yaksh T.L., Rudy T.A. Chronic catheterization of the spinal subarachnoid space. Physiol. Behav. 1976, 17:1031-1036.
39. Yamanaka H., Obata K., Fukuoka T., Dai Y., Kobayashi K., Tokunaga A., Noguchi K. Tissue plasminogen activator in primary afferents induces dorsal horn excitability and pain response after peripheral nerve injury. Eur. J. Neurosci. 2004, 19:93-102.
40. Yu T.W., Bargmann C.I. Dynamic regulation of axon guidance. Nat. Neurosci. 2001, (4 Suppl.):1169-1176.
41. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.
42. Zimmermann M. Pathobiology of neuropathic pain. Eur. J. Pharmacol. 2001, 429:23-37.