RhoA-inhibiting NSAIDs promote axonal myelination after spinal cord injury

Experimental Neurology

Volumn 231, Issue 2, 2011, Pages 247-260

  Xing, Bin ^a   Li, Hui ^a   Wang, Hongyu ^a   Mukhopadhyay, Dhriti ^a   Fisher, Daniel ^a   Gilpin, Christopher J ^a   Li, Shuxin ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Axon injury; Ibuprofen; Myelination; NSAIDs; RhoA; Spinal cord injury

Indexed keywords

IBUPROFEN; INDOMETACIN; NAPROXEN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; AXONAL MYELINATION; CENTRAL NERVOUS SYSTEM FUNCTION; CONTROLLED STUDY; CONTUSION; DRUG EFFICACY; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; MYELINATION; NERVE CELL NECROSIS; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; WHITE MATTER;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; AXONS; CELLS, CULTURED; FEMALE; IBUPROFEN; INDOMETHACIN; MYELIN SHEATH; NERVE FIBERS, MYELINATED; NERVE REGENERATION; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; RHOA GTP-BINDING PROTEIN; SPINAL CORD; SPINAL CORD INJURIES;

EID: 80052554144     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.06.018     Document Type: Article

References (72)

1. Akiyama Y., Radtke C., Kocsis J.D. Remyelination of the rat spinal cord by transplantation of identified bone marrow stromal cells. J. Neurosci. 2002, 22(15):6623-6630.
2. Barres B.A., Schmid R., Sendnter M., Raff M.C. Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 1993, 118(1):283-295.
3. Beattie M.S., Farooqui A.A., Bresnahan J.C. Review of current evidence for apoptosis after spinal cord injury. J. Neurotrauma 2000, 17(10):915-925.
4. Beattie M.S., Harrington A.W., Lee R., Kim J.Y., Boyce S.L., Longo F.M., Bresnahan J.C., Hempstead B.L., Yoon S.O. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 2002, 36(3):375-386.
5. Bernardo A., Bianchi D., Magnaghi V., Minghetti L. Peroxisome proliferator-activated receptor-gamma agonists promote differentiation and antioxidant defenses of oligodendrocyte progenitor cells. J. Neuropathol. Exp. Neurol. 2009, 68(7):797-808.
6. Bertrand J., Winton M.J., Rodriguez-Hernandez N., Campenot R.B., McKerracher L. Application of rho antagonist to neuronal cell bodies promotes neurite growth in compartmented cultures and regeneration of retinal ganglion cell axons in the optic nerve of adult rats. J. Neurosci. 2005, 25(5):1113-1121.
7. Blight A.R. Miracles and molecules-progress in spinal cord repair. Nat. Neurosci. 2002, 5:1051-1054. Suppl.
8. Brabeck C., Beschorner R., Conrad S., Mittelbronn M., Bekure K., Meyermann R., Schluesener H.J., Schwab J.M. Lesional expression of RhoA and RhoB following traumatic brain injury in humans. J. Neurotrauma 2004, 21(6):697-706.
9. Bracken M.B., Shepard M.J., Holford T.R., Leo-Summers L., Aldrich E.F., Fazl M., Fehlings M., Herr D.L., Hitchon P.W., Marshall L.F., et al. Administration of methylprednisolone for 24 or 48 hours or tirilazad mesylate for 48 hours in the treatment of acute spinal cord injury. Results of the Third National Acute Spinal Cord Injury Randomized Controlled Trial. National Acute Spinal Cord Injury Study. JAMA 1997, 277(20):1597-1604.
10. Butzkueven H., Zhang J.G., Soilu-Hanninen M., Hochrein H., Chionh F., Shipham K.A., Emery B., Turnley A.M., Petratos S., Ernst M., et al. LIF receptor signaling limits immune-mediated demyelination by enhancing oligodendrocyte survival. Nat. Med. 2002, 8(6):613-619.
11. Cao Q., Xu X.M., Devries W.H., Enzmann G.U., Ping P., Tsoulfas P., Wood P.M., Bunge M.B., Whittemore S.R. Functional recovery in traumatic spinal cord injury after transplantation of multineurotrophin-expressing glial-restricted precursor cells. J. Neurosci. 2005, 25(30):6947-6957.
12. Cao Q., He Q., Wang Y., Cheng X., Howard R.M., Zhang Y., DeVries W.H., Shields C.B., Magnuson D.S., Xu X.M., et al. Transplantation of ciliary neurotrophic factor-expressing adult oligodendrocyte precursor cells promotes remyelination and functional recovery after spinal cord injury. J. Neurosci. 2010, 30(8):2989-3001.
13. Conrad S., Schluesener H.J., Trautmann K., Joannin N., Meyermann R., Schwab J.M. Prolonged lesional expression of RhoA and RhoB following spinal cord injury. J. Comp. Neurol. 2005, 487(2):166-175.
14. Crowe M.J., Bresnahan J.C., Shuman S.L., Masters J.N., Beattie M.S. Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat. Med. 1997, 3(1):73-76.
15. Demjen D., Klussmann S., Kleber S., Zuliani C., Stieltjes B., Metzger C., Hirt U.A., Walczak H., Falk W., Essig M., et al. Neutralization of CD95 ligand promotes regeneration and functional recovery after spinal cord injury. Nat. Med. 2004, 10(4):389-395.
16. Dergham P., Ellezam B., Essagian C., Avedissian H., Lubell W.D., McKerracher L. Rho signaling pathway targeted to promote spinal cord repair. J. Neurosci. 2002, 22(15):6570-6577.
17. Dill J., Wang H., Zhou F.Q., Li S. Inactivation of glycogen synthase kinase-3 promotes axonal growth and recovery in the CNS. J. Neurosci. 2008, 28(36):8914-8928.
18. Dill J., Patel A.R., Yang X.L., Bachoo R., Powell C.M., Li S. A molecular mechanism for ibuprofen-mediated RhoA inhibition in neurons. J. Neurosci. 2010, 30(3):963-972.
19. Dubreuil C.I., Winton M.J., McKerracher L. Rho activation patterns after spinal cord injury and the role of activated Rho in apoptosis in the central nervous system. J. Cell Biol. 2003, 162(2):233-243.
20. Emery E., Aldana P., Bunge M.B., Puckett W., Srinivasan A., Keane R.W., Bethea J., Levi A.D. Apoptosis after traumatic human spinal cord injury. J. Neurosurg. 1998, 89(6):911-920.
21. Fischer D., Petkova V., Thanos S., Benowitz L.I. Switching mature retinal ganglion cells to a robust growth state in vivo: gene expression and synergy with RhoA inactivation. J. Neurosci. 2004, 24(40):8726-8740.
22. Fournier A.E., Takizawa B.T., Strittmatter S.M. Rho kinase inhibition enhances axonal regeneration in the injured CNS. J. Neurosci. 2003, 23(4):1416-1423.
23. Franklin R.J., Bayley S.A., Milner R., Ffrench-Constant C., Blakemore W.F. Differentiation of the O-2A progenitor cell line CG-4 into oligodendrocytes and astrocytes following transplantation into glia-deficient areas of CNS white matter. Glia 1995, 13(1):39-44.
24. Fu Q., Hue J., Li S. Nonsteroidal anti-inflammatory drugs promote axon regeneration via RhoA inhibition. J. Neurosci. 2007, 27(15):4154-4164.
25. Granneman J., Skoff R., Yang X. Member of the peroxisome proliferator-activated receptor family of transcription factors is differentially expressed by oligodendrocytes. J. Neurosci. Res. 1998, 51(5):563-573.
26. Groves A.K., Barnett S.C., Franklin R.J., Crang A.J., Mayer M., Blakemore W.F., Noble M. Repair of demyelinated lesions by transplantation of purified O-2A progenitor cells. Nature 1993, 362(6419):453-455.
27. Hara M., Takayasu M., Watanabe K., Noda A., Takagi T., Suzuki Y., Yoshida J. Protein kinase inhibition by fasudil hydrochloride promotes neurological recovery after spinal cord injury in rats. J. Neurosurg. 2000, 93(1 Suppl):94-101.
28. Horiuchi H., Ogata T., Morino T., Chuai M., Yamamoto H. Continuous intrathecal infusion of SB203580, a selective inhibitor of p38 mitogen-activated protein kinase, reduces the damage of hind-limb function after thoracic spinal cord injury in rat. Neurosci. Res. 2003, 47(2):209-217.
29. Huang E.J., Reichardt L.F. Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 2003, 72:609-642.
30. Huber A.B., Kolodkin A.L., Ginty D.D., Cloutier J.F. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu. Rev. Neurosci. 2003, 26:509-563.
31. Jensen N.A., West M.J., Celis J.E. Oligodendrocyte programmed cell death and central myelination deficiency induced in transgenic mice by synergism between c-Myc and Oct-6. J. Biol. Chem. 1999, 274(42):29921-29926.
32. John G.R., Shankar S.L., Shafit-Zagardo B., Massimi A., Lee S.C., Raine C.S., Brosnan C.F. Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nat. Med. 2002, 8(10):1115-1121.
33. Keirstead H.S., Nistor G., Bernal G., Totoiu M., Cloutier F., Sharp K., Steward O. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J. Neurosci. 2005, 25(19):4694-4705.
34. Kim G.M., Xu J., Xu J., Song S.K., Yan P., Ku G., Xu X.M., Hsu C.Y. Tumor necrosis factor receptor deletion reduces nuclear factor-kappaB activation, cellular inhibitor of apoptosis protein 2 expression, and functional recovery after traumatic spinal cord injury. J. Neurosci. 2001, 21(17):6617-6625.
35. Kim S.J., Jeon S., Shin E.Y., Kim E.G., Park J., Bae C.D. AMPA, not NMDA, activates RhoA GTPases and subsequently phosphorylates moesin. Exp. Mol. Med. 2004, 36(1):98-102.
36. Kippert A., Trajkovic K., Rajendran L., Ries J., Simons M. Rho regulates membrane transport in the endocytic pathway to control plasma membrane specialization in oligodendroglial cells. J. Neurosci. 2007, 27(13):3560-3570.
37. Kozma R., Sarner S., Ahmed S., Lim L. Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol. Cell. Biol. 1997, 17(3):1201-1211.
38. Kranenburg O., Poland M., van Horck F.P., Drechsel D., Hall A., Moolenaar W.H. Activation of RhoA by lysophosphatidic acid and Galpha12/13 subunits in neuronal cells: induction of neurite retraction. Mol. Biol. Cell 1999, 10(6):1851-1857.
39. Li S., Stys P.K. Mechanisms of ionotropic glutamate receptor-mediated excitotoxicity in isolated spinal cord white matter. J. Neurosci. 2000, 20(3):1190-1198.
40. Li S., Mealing G.A., Morley P., Stys P.K. Novel injury mechanism in anoxia and trauma of spinal cord white matter: glutamate release via reverse Na+-dependent glutamate transport. J. Neurosci. 1999, 19(14):RC16.
41. Louis J.C., Magal E., Muir D., Manthorpe M., Varon S. CG-4, a new bipotential glial cell line from rat brain, is capable of differentiating in vitro into either mature oligodendrocytes or type-2 astrocytes. J. Neurosci. Res. 1992, 31(1):193-204.
42. Louis J.C., Magal E., Takayama S., Varon S. CNTF protection of oligodendrocytes against natural and tumor necrosis factor-induced death. Science 1993, 259(5095):689-692.
43. McDonald J.W., Althomsons S.P., Hyrc K.L., Choi D.W., Goldberg M.P. Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity. Nat. Med. 1998, 4(3):291-297.
44. McGee A.W., Strittmatter S.M. The Nogo-66 receptor: focusing myelin inhibition of axon regeneration. Trends Neurosci. 2003, 26(4):193-198.
45. McTigue D.M., Tripathi R., Wei P., Lash A.T. The PPAR gamma agonist Pioglitazone improves anatomical and locomotor recovery after rodent spinal cord injury. Exp. Neurol. 2007, 205(2):396-406.
46. Mi S., Miller R.H., Lee X., Scott M.L., Shulag-Morskaya S., Shao Z., Chang J., Thill G., Levesque M., Zhang M., et al. LINGO-1 negatively regulates myelination by oligodendrocytes. Nat. Neurosci. 2005, 8(6):745-751.
47. Mi S., Miller R.H., Tang W., Lee X., Hu B., Wu W., Zhang Y., Shields C.B., Miklasz S., Shea D., et al. Promotion of central nervous system remyelination by induced differentiation of oligodendrocyte precursor cells. Ann. Neurol. 2009, 65(3):304-315.
48. Mueller B.K., Mack H., Teusch N. Rho kinase, a promising drug target for neurological disorders. Nat. Rev. Drug Discov. 2005, 4(5):387-398.
49. Neumann H., Schweigreiter R., Yamashita T., Rosenkranz K., Wekerle H., Barde Y.A. Tumor necrosis factor inhibits neurite outgrowth and branching of hippocampal neurons by a rho-dependent mechanism. J. Neurosci. 2002, 22(3):854-862.
50. Nicholas R.S., Stevens S., Wing M.G., Compston D.A. Microglia-derived IGF-2 prevents TNFalpha induced death of mature oligodendrocytes in vitro. J. Neuroimmunol. 2002, 124(1-2):36-44.
51. Nishio Y., Koda M., Kitajo K., Seto M., Hata K., Taniguchi J., Moriya H., Fujitani M., Kubo T., Yamashita T. Delayed treatment with Rho-kinase inhibitor does not enhance axonal regeneration or functional recovery after spinal cord injury in rats. Exp. Neurol. 2006, 200(2):392-397.
52. Park S.W., Yi J.H., Miranpuri G., Satriotomo I., Bowen K., Resnick D.K., Vemuganti R. Thiazolidinedione class of peroxisome proliferator-activated receptor gamma agonists prevents neuronal damage, motor dysfunction, myelin loss, neuropathic pain, and inflammation after spinal cord injury in adult rats. J. Pharmacol. Exp. Ther. 2007, 320(3):1002-1012.
53. Pearse D.D., Pereira F.C., Marcillo A.E., Bates M.L., Berrocal Y.A., Filbin M.T., Bunge M.B. cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat. Med. 2004, 10(6):610-616.
54. Sanchez-Gomez M.V., Alberdi E., Ibarretxe G., Torre I., Matute C. Caspase-dependent and caspase-independent oligodendrocyte death mediated by AMPA and kainate receptors. J. Neurosci. 2003, 23(29):9519-9528.
55. Schwab J.M., Conrad S., Elbert T., Trautmann K., Meyermann R., Schluesener H.J. Lesional RhoA+ cell numbers are suppressed by anti-inflammatory, cyclooxygenase-inhibiting treatment following subacute spinal cord injury. Glia 2004, 47(4):377-386.
56. Selmaj K., Raine C.S. Tumor necrosis factor mediates myelin damage in organotypic cultures of nervous tissue. Ann. N. Y. Acad. Sci. 1988, 540:568-570.
57. Shuman S.L., Bresnahan J.C., Beattie M.S. Apoptosis of microglia and oligodendrocytes after spinal cord contusion in rats. J. Neurosci. Res. 1997, 50(5):798-808.
58. Siegenthaler M.M., Tu M.K., Keirstead H.S. The extent of myelin pathology differs following contusion and transection spinal cord injury. J. Neurotrauma 2007, 24(10):1631-1646.
59. Sung J.K., Miao L., Calvert J.W., Huang L., Louis Harkey H., Zhang J.H. A possible role of RhoA/Rho-kinase in experimental spinal cord injury in rat. Brain Res. 2003, 959(1):29-38.
60. Syed Y.A., Hand E., Mobius W., Zhao C., Hofer M., Nave K.A., Kotter M.R. Inhibition of CNS remyelination by the presence of semaphorin 3A. J. Neurosci. 2011, 31(10):3719-3728.
61. Tamura M., Nakamura M., Ogawa Y., Toyama Y., Miura M., Okano H. Targeted expression of anti-apoptotic protein p35 in oligodendrocytes reduces delayed demyelination and functional impairment after spinal cord injury. Glia 2005, 51(4):312-321.
62. Tanaka H., Yamashita T., Yachi K., Fujiwara T., Yoshikawa H., Tohyama M. Cytoplasmic p21(Cip1/WAF1) enhances axonal regeneration and functional recovery after spinal cord injury in rats. Neuroscience 2004, 127(1):155-164.
63. Tontsch U., Archer D.R., Dubois-Dalcq M., Duncan I.D. Transplantation of an oligodendrocyte cell line leading to extensive myelination. Proc. Natl. Acad. Sci. U.S.A. 1994, 91(24):11616-11620.
64. Totoiu M.O., Keirstead H.S. Spinal cord injury is accompanied by chronic progressive demyelination. J. Comp. Neurol. 2005, 486(4):373-383.
65. Wang P.S., Wang J., Xiao Z.C., Pallen C.J. Protein-tyrosine phosphatase alpha acts as an upstream regulator of Fyn signaling to promote oligodendrocyte differentiation and myelination. J. Biol. Chem. 2009, 284(48):33692-33702.
66. Wang X., Budel S., Baughman K., Gould G., Song K.H., Strittmatter S.M. Ibuprofen enhances recovery from spinal cord injury by limiting tissue loss and stimulating axonal growth. J. Neurotrauma 2009, 26(1):81-95.
67. Warden P., Bamber N.I., Li H., Esposito A., Ahmad K.A., Hsu C.Y., Xu X.M. Delayed glial cell death following wallerian degeneration in white matter tracts after spinal cord dorsal column cordotomy in adult rats. Exp. Neurol. 2001, 168(2):213-224.
68. Wolf R.M., Wilkes J.J., Chao M.V., Resh M.D. Tyrosine phosphorylation of p190 RhoGAP by Fyn regulates oligodendrocyte differentiation. J. Neurobiol. 2001, 49(1):62-78.
69. Wu B., Ren X. Promoting axonal myelination for improving neurological recovery in spinal cord injury. J. Neurotrauma 2009, 26(10):1847-1856.
70. Yamashita T., Tucker K.L., Barde Y.A. Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth. Neuron 1999, 24(3):585-593.
71. Yune T.Y., Chang M.J., Kim S.J., Lee Y.B., Shin S.W., Rhim H., Kim Y.C., Shin M.L., Oh Y.J., Han C.T., et al. Increased production of tumor necrosis factor-alpha induces apoptosis after traumatic spinal cord injury in rats. J. Neurotrauma 2003, 20(2):207-219.
72. Yune T.Y., Lee J.Y., Jung G.Y., Kim S.J., Jiang M.H., Kim Y.C., Oh Y.J., Markelonis G.J., Oh T.H. Minocycline alleviates death of oligodendrocytes by inhibiting pro-nerve growth factor production in microglia after spinal cord injury. J. Neurosci. 2007, 27(29):7751-7761.