The critical role of spinal ceramide in the development of partial sciatic nerve ligation-induced neuropathic pain in mice

Biochemical and Biophysical Research Communications

Volumn 421, Issue 2, 2012, Pages 318-322

  Kobayashi, Yuka ^a   Kiguchi, Norikazu ^a   Maeda, Takehiko ^b   Ozaki, Masanobu ^b   Kishioka, Shiroh ^a  

^a WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^b NIIGATA UNIVERSITY OF PHARMACY AND APPLIED LIFE SCIENCES   (Japan)

Author keywords

Allodynia; Cytokines; Dorsal horn; Microglia; Sphingolipids

Indexed keywords

ADAPTOR PROTEIN; CD11B ANTIGEN; CERAMIDE; FUMONISIN B1; GW 4869; INTERLEUKIN 1BETA; MESSENGER RNA; PROTEIN IBA 1; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOMYELIN PHOSPHODIESTERASE INHIBITOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE RELEASE; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MOUSE; NERVE LIGATION; NEUROPATHIC PAIN; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; SCIATIC NERVE; SKIN SENSITIZATION; SPINAL CORD; SPINAL CORD DORSAL HORN;

ANILINE COMPOUNDS; ANIMALS; BENZYLIDENE COMPOUNDS; CERAMIDES; CYTOKINES; FUMONISINS; HYPERALGESIA; LIGATION; MALE; MICE; MICE, INBRED ICR; MICROGLIA; NEURALGIA; OXIDOREDUCTASES; PERIPHERAL NERVE INJURIES; RNA, MESSENGER; SCIATIC NERVE; SPHINGOMYELIN PHOSPHODIESTERASE; SPINAL CORD;

MUS;

EID: 84860427667     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.03.153     Document Type: Article

References (38)

1. Moalem G., Tracey D.J. Immune and inflammatory mechanisms in neuropathic pain. Brain Res. Rev. 2006, 51:240-264.
2. Renfrey S., Downton C., Featherstone J. The painful reality. Nat. Rev. Drug Discov. 2003, 2:175-176.
3. Scholz J., Woolf C.J. The neuropathic pain triad: neurons, immune cells and glia. Nat. Neurosci. 2007, 10:1361-1368.
4. Marchand F., Perretti M., McMahon S.B. Role of the immune system in chronic pain. Nat. Rev. Neurosci. 2005, 6:521-532.
5. Watkins L.R., Maier S.F. Glia: a novel drug discovery target for clinical pain. Nat. Rev. Drug Discov. 2003, 2:973-985.
6. Tsuda M., Inoue K., Salter M.W. Neuropathic pain and spinal microglia: a big problem from molecules in "small" glia. Trends Neurosci. 2005, 28:101-107.
7. Fuchs J.L., Moore J.A., Schwark H.D. Peripheral inflammation increases phosphoinositide activity in the rat dorsal horn. Brain Res. 2004, 1003:183-187.
8. Vanegas H., Schaible H.G. Prostaglandins and cyclooxygenases [correction of cycloxygenases] in the spinal cord. Prog. Neurobiol. 2001, 64:327-363.
9. Park K.A., Vasko M.R. Lipid mediators of sensitivity in sensory neurons. Trends Pharmacol. Sci. 2005, 26:571-577.
10. Inoue M., Rashid M.H., Fujita R., Contos J.J., Chun J., Ueda H. Initiation of neuropathic pain requires lysophosphatidic acid receptor signaling. Nat. Med. 2004, 10:712-718.
11. Patti G.J., Yanes O., Shriver L.P., Courade J.P., Tautenhahn R., Manchester M., Siuzdak G. Metabolomics implicates altered sphingolipids in chronic pain of neuropathic origin. Nat. Chem. Biol. 2012, 8:232-234.
12. Joseph E.K., Levine J.D. Caspase signalling in neuropathic and inflammatory pain in the rat. Eur. J. Neurosci. 2004, 20:2896-2902.
13. Ndengele M.M., Cuzzocrea S., Masini E., Vinci M.C., Esposito E., Muscoli C., Petrusca D.N., Mollace V., Mazzon E., Li D., Petrache I., Matuschak G.M., Salvemini D. Spinal ceramide modulates the development of morphine antinociceptive tolerance via peroxynitrite-mediated nitroxidative stress and neuroimmune activation. J. Pharmacol. Exp. Ther. 2009, 329:64-75.
14. Nakajima K., Tohyama Y., Kohsaka S., Kurihara T. Ceramide activates microglia to enhance the production/secretion of brain-derived neurotrophic factor (BDNF) without induction of deleterious factors in vitro. J. Neurochem. 2002, 80:697-705.
15. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.
16. Muscoli C., Doyle T., Dagostino C., Bryant L., Chen Z., Watkins L.R., Ryerse J., Bieberich E., Neumman W., Salvemini D. Counter-regulation of opioid analgesia by glial-derived bioactive sphingolipids. J. Neurosci. 2010, 30:15400-15408.
17. Doyle T., Chen Z., Muscoli C., Obeid L.M., Salvemini D. Intraplantar-injected ceramide in rats induces hyperalgesia through an NF-kappaB- and p38 kinase-dependent cyclooxygenase 2/prostaglandin E2 pathway. FASEB J. 2011, 25:2782-2791.
18. Hylden J.L., Wilcox G.L. Intrathecal morphine in mice. A new technique. Eur. J. Pharmacol. 1980, 67:313-316.
19. 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.
20. Kiguchi N., Maeda T., Kobayashi Y., Kishioka S. Up-regulation of tumor necrosis factor-alpha in spinal cord contributes to vincristine-induced mechanical allodynia in mice. Neurosci. Lett. 2008, 445:140-143.
21. Quintern L.E., Schuchman E.H., Levran O., Suchi M., Ferlinz K., Reinke H., Sandhoff K., Desnick R.J. Isolation of cDNA clones encoding human acid sphingomyelinase: occurrence of alternatively processed transcripts. EMBO J. 1989, 8:2469-2473.
22. Schuchman E.H., Suchi M., Takahashi T., Sandhoff K., Desnick R.J. Human acid sphingomyelinase. Isolation, nucleotide sequence and expression of the full-length and alternatively spliced cDNAs. J. Biol. Chem. 1991, 266:8531-8539.
23. Levran O., Desnick R.J., Schuchman E.H. Niemann-Pick disease: A frequent missense mutation in the acid sphingomyelinase gene of Ashkenazi Jewish type A and B patients. Proc. Natl. Acad. Sci. USA 1991, 88:3748-3752.
24. Devillard R., Galvani S., Thiers J.C., Guenet J.L., Hannun Y., Bielawski J., Negre-Salvayre A., Salvayre R., Auge N. Stress-induced sphingolipid signaling: role of type-2 neutral sphingomyelinase in murine cell apoptosis and proliferation. PLoS One 2010, 5:e9826.
25. Clarke C.J., Truong T.G., Hannun Y.A. Role for neutral sphingomyelinase-2 in tumor necrosis factor alpha-stimulated expression of vascular cell adhesion molecule-1 (VCAM) and intercellular adhesion molecule-1 (ICAM) in lung epithelial cells: p38 MAPK is an upstream regulator of nSMase2. J. Biol. Chem. 2007, 282:1384-1396.
26. Kiguchi N., Kobayashi Y., Kishioka S. Chemokines and cytokines in neuroinflammation leading to neuropathic pain. Curr. Opin. Pharmacol. 2011.
27. Cao L., Tanga F.Y., Deleo J.A. The contributing role of CD14 in toll-like receptor 4 dependent neuropathic pain. Neuroscience 2009, 158:896-903.
28. Ren K., Torres R. Role of interleukin-1beta during pain and inflammation. Brain Res. Rev. 2009, 60:57-64.
29. Milligan E.D., Watkins L.R. Pathological and protective roles of glia in chronic pain. Nat. Rev. Neurosci. 2009, 10:23-36.
30. Hanisch U.K. Microglia as a source and target of cytokines. Glia 2002, 40:140-155.
31. Akundi R.S., Candelario-Jalil E., Hess S., Hull M., Lieb K., Gebicke-Haerter P.J., Fiebich B.L. Signal transduction pathways regulating cyclooxygenase-2 in lipopolysaccharide-activated primary rat microglia. Glia 2005, 51:199-208.
32. Coull J.A., Beggs S., Boudreau D., Boivin D., Tsuda M., Inoue K., Gravel C., Salter M.W., De Koninck Y. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 2005, 438:1017-1021.
33. Samad T.A., Moore K.A., Sapirstein A., Billet S., Allchorne A., Poole S., Bonventre J.V., Woolf C.J. Interleukin-1beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 2001, 410:471-475.
34. Hirata H., Hibasami H., Yoshida T., Ogawa M., Matsumoto M., Morita A., Uchida A. Nerve growth factor signaling of p75 induces differentiation and ceramide-mediated apoptosis in Schwann cells cultured from degenerating nerves. Glia 2001, 36:245-258.
35. Kim M.Y., Linardic C., Obeid L., Hannun Y. Identification of sphingomyelin turnover as an effector mechanism for the action of tumor necrosis factor alpha and gamma-interferon. Specific role in cell differentiation. J. Biol. Chem. 1991, 266:484-489.
36. Ballou L.R., Chao C.P., Holness M.A., Barker S.C., Raghow R. Interleukin-1-mediated PGE2 production and sphingomyelin metabolism. Evidence for the regulation of cyclooxygenase gene expression by sphingosine and ceramide. J. Biol. Chem. 1992, 267:20044-20050.
37. Melcher T., Maas S., Herb A., Sprengel R., Seeburg P.H., Higuchi M. A mammalian RNA editing enzyme. Nature 1996, 379:460-464.
38. Ballou L.R., Laulederkind S.J., Rosloniec E.F., Raghow R. Ceramide signalling and the immune response. Biochim. Biophys. Acta 1996, 1301:273-287.