Cortical PKC inhibition promotes axonal regeneration of the corticospinal tract and forelimb functional recovery after cervical dorsal spinal hemisection in adult rats

Cerebral Cortex

Volumn 24, Issue 11, 2014, Pages 3069-3079

  Wang, Xiaofei ^a,b   Hu, Jianguo ^a,b   She, Yun ^a,b   Smith, George M ^c   Xu, Xiao Ming ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIANA UNIVERSITY   (United States)

^c UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

axonal regeneration; cortical plasticity; corticospinal tract; protein kinase C; spinal cord injury

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; N ACETYLGALACTOSAMINE 4 SULFATASE; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE C BETA1; UNCLASSIFIED DRUG; BIOTIN; BIOTINYLATED DEXTRAN AMINE; CARBAZOLE DERIVATIVE; CHONDROITIN ABC LYASE; DEXTRAN; ENZYME INHIBITOR; GLIAL FIBRILLARY ACIDIC PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CERVICAL SPINAL CORD INJURY; CONTROLLED STUDY; CONVALESCENCE; EMBRYO; ENZYME INHIBITION; FEMALE; FORELIMB; NERVE FIBER REGENERATION; NEUROANATOMY; NONHUMAN; PYRAMIDAL TRACT; RAT; SPINAL CORD HEMISECTION; SYNAPSE; ANALOGS AND DERIVATIVES; ANIMAL; ANIMAL EMBRYO; BRAIN CORTEX; CELL CULTURE; CYTOLOGY; DIAGNOSTIC USE; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; HEMISPHERIC DOMINANCE; MALE; METABOLISM; NERVE CELL; NERVE REGENERATION; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PSYCHOMOTOR PERFORMANCE; SPINAL CORD INJURIES; SPRAGUE DAWLEY RAT;

ANIMALS; BIOTIN; CARBAZOLES; CELLS, CULTURED; CEREBRAL CORTEX; CHONDROITIN ABC LYASE; DEXTRANS; DISEASE MODELS, ANIMAL; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; FEMALE; FORELIMB; FUNCTIONAL LATERALITY; GLIAL FIBRILLARY ACIDIC PROTEIN; MALE; NERVE REGENERATION; NEURONS; PREGNANCY; PROTEIN KINASE C; PSYCHOMOTOR PERFORMANCE; PYRAMIDAL TRACTS; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD INJURIES;

EID: 84910617786     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht162     Document Type: Article

References (47)

1. Anastassiadis T, Deacon SW, Devarajan K, Ma H, Peterson JR. 2011. Comprehensive assay of kinase catalytic activity reveals features of kinase inhibitor selectivity. Nat Biotechnol. 29:1039-1045.
2. Anderson KD, Gunawan A, Steward O. 2007. Spinal pathways involved in the control of forelimb motor function in rats. Exp Neurol. 206:318-331.
3. Balendran A, Hare GR, Kieloch A, Williams MR, Alessi DR. 2000. Further evidence that 3-phosphoinositide-dependent protein kinase-1 (PDK1) is required for the stability and phosphorylation of protein kinase C (PKC) isoforms. FEBS Lett. 484:217-223.
4. Benowitz LI, Goldberg DE, Madsen JR, Soni D, Irwin N. 1999. Inosine stimulates extensive axon collateral growth in the rat corticospinal tract after injury. Proc Natl Acad Sci USA. 96:13486-13490.
5. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB. 2002. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature. 416:636-640.
6. Bregman BS, Kunkel-Bagden E, Schnell L, Dai HN, Gao D, Schwab ME. 1995. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature. 378:498-501.
7. Brittis PA, Canning DR, Silver J. 1992. Chondroitin sulfate as a regulator of neuronal patterning in the retina. Science. 255:733-736.
8. Brock JH, Rosenzweig ES, Blesch A, Moseanko R, Havton LA, Edgerton VR, Tuszynski MH. 2010. Local and remote growth factor effects after primate spinal cord injury. J Neurosci. 30:9728-9737.
9. Cafferty WB, Yang SH, Duffy PJ, Li S, Strittmatter SM. 2007. Functional axonal regeneration through astrocytic scar genetically modified to digest chondroitin sulfate proteoglycans. J Neurosci. 27:2176-2185.
10. Chau CH, Shum DK, Li H, Pei J, Lui YY, Wirthlin L, Chan YS, Xu XM. 2004. Chondroitinase ABC enhances axonal regrowth through Schwann cell-seeded guidance channels after spinal cord injury. FASEB J. 18:194-196.
11. Clark JB, Bellegarrigue RB, Salcman M. 1985. Gunshot wound to the pons with functional neuroanatomical and electrophysiological correlation. Neurosurgery. 16:607-611.
12. Courtine G, Bunge MB, Fawcett JW, Grossman RG, Kaas JH, Lemon R, Maier I, Martin J, Nudo RJ, Ramon-Cueto A et al. 2007. Can experiments in nonhuman primates expedite the translation of treatments for spinal cord injury in humans? Nat Med. 13:561-566.
13. Farmer SF, Swash M, Ingram DA, Stephens JA. 1993. Changes in motor unit synchronization following central nervous lesions in man. J Physiol. 463:83-105.
14. Garcia-Alias G, Barkhuysen S, Buckle M, Fawcett JW. 2009. Chondroitinase ABC treatment opens a window of opportunity for taskspecific rehabilitation. Nat Neurosci. 12:1145-1151.
15. Hasegawa Y, Fujitani M, Hata K, Tohyama M, Yamagishi S, Yamashita T. 2004. Promotion of axon regeneration by myelin-Associated glycoprotein and Nogo through divergent signals downstream of Gi/ G. J Neurosci. 24:6826-6832.
16. Hill CE, Beattie MS, Bresnahan JC. 2001. Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp Neurol. 171:153-169.
17. Hill RL, Zhang YP, Burke DA, Devries WH, Zhang Y, Magnuson DS, Whittemore SR, Shields CB. 2009. Anatomical and functional outcomes following a precise, graded, dorsal laceration spinal cord injury in C57BL/6 mice. J Neurotrauma. 26:1-15.
18. Horner PJ, Gage FH. 2000. Regenerating the damaged central nervous system. Nature. 407:963-970.
19. Hsu JY, Xu XM. 2005. Early profiles of axonal growth and astroglial response after spinal cord hemisection and implantation of Schwann cell-seeded guidance channels in adult rats. J Neurosci Res. 82:472-483.
20. Jaken S. 1996. Protein kinase C isozymes and substrates. Curr Opin Cell Biol. 8:168-173.
21. Lehmann M, Fournier A, Selles-Navarro I, Dergham P, Sebok A, Leclerc N, Tigyi G, McKerracher L. 1999. Inactivation of Rho signaling pathway promotes CNS axon regeneration. J Neurosci. 19:7537-7547.
22. Li Y, Raisman G. 1994. Schwann cells induce sprouting in motor and sensory axons in the adult rat spinal cord. J Neurosci. 14:4050-4063.
23. Liu K, Lu Y, Lee JK, Samara R, Willenberg R, Sears-Kraxberger I, Tedeschi A, Park KK, Jin D, Cai B et al. 2010. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat Neurosci. 13:1075-1081.
24. Liu Y, Wang X, Lu CC, Kerman R, Steward O, Xu XM, Zou Y. 2008. Repulsive Wnt signaling inhibits axon regeneration after CNS injury. J Neurosci. 28:8376-8382.
25. Marzioni M, Francis H, Benedetti A, Ueno Y, Fava G, Venter J, Reichenbach R, Mancino MG, Summers R, Alpini G et al. 2006. Ca2+-dependent cytoprotective effects of ursodeoxycholic and tauroursodeoxycholic acid on the biliary epithelium in a rat model of cholestasis and loss of bile ducts. Am J Pathol. 168:398-409.
26. McGee AW, Strittmatter SM. 2003. The Nogo-66 receptor: Focusing myelin inhibition of axon regeneration. Trends Neurosci. 26:193-198.
27. Menezes K, de Menezes JR, Nascimento MA, Santos Rde S, Coelho-Sampaio T. 2010. Polylaminin, a polymeric form of laminin, promotes regeneration after spinal cord injury. FASEB J. 24:4513-4522.
28. Nathan PW. 1994. Effects on movement of surgical incisions into the human spinal cord. Brain. 117(Pt 2):337-346.
29. Newton AC. 2001. Protein kinase C: Structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chem Rev. 101:2353-2364.
30. Nielson JL, Sears-Kraxberger I, Strong MK, Wong JK, Willenberg R, Steward O. 2010. Unexpected survival of neurons of origin of the pyramidal tract after spinal cord injury. J Neurosci. 30: 11516-11528.
31. Ruitenberg MJ, Levison DB, Lee SV, Verhaagen J, Harvey AR, Plant GW. 2005. NT-3 expression from engineered olfactory ensheathing glia promotes spinal sparing and regeneration. Brain. 128: 839-853.
32. Savio T, Schwab ME. 1989. Rat CNS white matter, but not gray matter, is nonpermissive for neuronal cell adhesion and fiber outgrowth. J Neurosci. 9:1126-1133.
33. Schnell L, Schwab ME. 1990. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-Associated neurite growth inhibitors. Nature. 343:269-272.
34. Schwab ME, Bartholdi D. 1996. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev. 76:319-370.
35. Schwab ME, Caroni P. 1988. Oligodendrocytes and CNS myelin are nonpermissive substrates for neurite growth and fibroblast spreading in vitro. J Neurosci. 8:2381-2393.
36. Seif GI, Nomura H, Tator CH. 2007. Retrograde axonal degeneration "dieback" in the corticospinal tract after transection injury of the rat spinal cord: A confocal microscopy study. J Neurotrauma. 24:1513-1528.
37. Sivasankaran R, Pei J, Wang KC, Zhang YP, Shields CB, Xu XM, He Z. 2004. PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nat Neurosci. 7:261-268.
38. Spencer T, Domeniconi M, Cao Z, Filbin MT. 2003. New roles for old proteins in adult CNS axonal regeneration. Curr Opin Neurobiol. 13:133-139.
39. Suzuki T, Abe Y, McGehee DS, Keath JR, Yajima H, Sharma K, Brorson JR. 2004. Long-lived retrograde fluorescent labeling of corticospinal neurons in the living animal. Brain Res Brain Res Protoc. 13:183-188.
40. Teng YD, Lavik EB, Qu X, Park KI, Ourednik J, Zurakowski D, Langer R, Snyder EY. 2002. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc Natl Acad Sci USA. 99:3024-3029.
41. Thallmair M, Metz GA, Z'Graggen WJ, Raineteau O, Kartje GL, Schwab ME. 1998. Neurite growth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat Neurosci. 1:124-131.
42. Titsworth WL, Onifer SM, Liu NK, Xu XM. 2007. Focal phospholipases A2 group III injections induce cervical white matter injury and functional deficits with delayed recovery concomitant with Schwann cell remyelination. Exp Neurol. 207:150-162.
43. Tom VJ, Kadakia R, Santi L, Houle JD. 2009. Administration of chondroitinase ABC rostral or caudal to a spinal cord injury site promotes anatomical but not functional plasticity. J Neurotrauma. 26:2323-2333.
44. Wang KC, Koprivica V, Kim JA, Sivasankaran R, Guo Y, Neve RL, He Z. 2002. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature. 417:941-944.
45. Wu DY, Zheng JQ, McDonald MA, Chang B, Twiss JL. 2003. PKC isozymes in the enhanced regrowth of retinal neurites after optic nerve injury. Invest Ophthalmol Vis Sci. 44:2783-2790.
46. Yiu G, He Z. 2006. Glial inhibition of CNS axon regeneration. Nat Rev Neurosci. 7:617-627.
47. Zhang YP, Burke DA, Shields LB, Chekmenev SY, Dincman T, Zhang Y, Zheng Y, Smith RR, Benton RL, DeVries WH et al. 2008. Spinal cord contusion based on precise vertebral stabilization and tissue displacement measured by combined assessment to discriminate small functional differences. J Neurotrauma. 25:1227-1240.