cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury

Nature Medicine

Volumn 10, Issue 6, 2004, Pages 610-616

  Pearse, Damien D ^a   Pereira, Francisco C ^b   Marcillo, Alexander E ^a   Bates, Margaret L ^a   Berrocal, Yerko A ^a   Filbin, Marie T ^c   Bunge, Mary Bartlett ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUCLADESINE; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; PHOSPHODIESTERASE IV INHIBITOR; ROLIPRAM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CELL FUNCTION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CONTUSION; CONVALESCENCE; FEMALE; HYDROLYSIS; IN VIVO STUDY; MYELINATION; NERVE CELL; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE GRAFT; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; PROPRIOCEPTION; RAT; SCHWANN CELL; SENSORIMOTOR CORTEX; SEROTONINERGIC NERVE CELL; SIGNAL TRANSDUCTION; SPINAL CORD INJURY;

ANIMALS; AXONS; BRAIN STEM; BUCLADESINE; CELL TRANSPLANTATION; CYCLIC AMP; FEMALE; INTERLEUKIN-1; MOTOR ACTIVITY; NERVE REGENERATION; RATS; RATS, INBRED F344; RECOVERY OF FUNCTION; ROLIPRAM; SCHWANN CELLS; SECOND MESSENGER SYSTEMS; SEROTONIN; SPINAL CORD INJURIES; TUMOR NECROSIS FACTOR-ALPHA;

ANIMALIA;

EID: 2942720519     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm1056     Document Type: Article

References (50)

1. Schwab, M.E. & Bartholdi, D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol. Rev. 76, 319-370 (1996).
2. Fawcett, J.W. & Asher, R.A. The glial scar and central nervous system repair. Brain Res. Bull. 49, 377-391 (1999).
3. Silver, S. & Miller, J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5, 146-156 (2004).
4. Richardson, P.M., McGuinness, U.M. & Aguayo, A.J. Axons from CNS neurons regenerate into PNS grafts. Nature 284, 264-265 (1980).
5. David, S. & Aguayo, A.J. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 214, 931-933 (1981).
6. Bunge, M.B. Bridging areas of injury in the spinal cord. Neuroscientist 7, 325-339 (2001).
7. Bunge, M.B. Bridging the transected or contused adult rat spinal cord with Schwann cell and olfactory ensheathing glia transplants. Progr. Brain Res. 137, 275-282. (2002)
8. Takami, T. et al. Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J. Neurosci. 22, 6670-6681 (2002).
9. Song, H.J., Ming, G.L. & Poo, M.M. cAMP-induced switching in turning direction of nerve growth cones. Nature 388, 275-279 (1997).
10. Ming, G.L. et al. cAMP-dependent growth cone guidance by netrin-1. Neuron 19, 1225-1235 (1997).
11. Cal, D. et al. Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate. J. Neurosci. 21, 4731-4739 (2001).
12. Souness, J.E., Aldous, D. & Sargent, C. Immunosuppressive and anti-inflammatory effects of cyclic AMP phosphodiesterase (PDE) type 4 inhibitors. Immunopharmacology 47, 127-162 (2000).
13. Schultz, J.E. & Folkers, G. Unusual stereospecificity of the potential antidepressant rolipram on the cyclic AMP generating system from rat brain cortex. Pharmacopsychiatry 21, 83-86 (1988).
14. Lee, Y.B. etal. Role of tumor necrosis factor-α in neuronal and glial apoptosis after spinal cord injury. Exp. Neurol. 166, 190-195 (2000).
15. Nesic, O. et al. IL-1 receptor antagonist prevents apoptosis and caspase-3 activation after spinal cord injury. J. Neurotrauma 18, 947-956 (2001).
16. Akassoglou, K. et al. Oligodendrocyte apoptosis and primary demyelination induced by local TNF/p55TNF receptor signaling in the central nervous system of transgenic mice: models for multiple sclerosis with primary oligodendrogliopathy. Am. J. Pathol. 153, 801-813 (1998).
17. Tator, C.H. Update on the pathophysiology and pathology of acute spinal cord injury. Brain Pathol. 5, 407-413 (1995).
18. Popovich, P.G. et al. Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp. Neurol. 158, 351-365 (1999).
19. Meyer-Franke, A., Kaplan, M.R., Pfrieger, F.W. & Barres, B.A. Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron 15, 805-819 (1995).
20. 2+ calmodulin-stimulated adenylate cyclase in rat brain. Int. J. Mol. Med. 6, 377-389 (2000).
21. Troadec, J.D. et al. Activation of the mitogen-activated protein kinase (ERK(1/2)) signaling pathway by cyclic AMP potentiates the neuroprotective effect of the neurotransmitter noradrenaline on dopaminergic neurons. Mol. Pharmacol. 62, 1043-1052 (2002).
22. Nuydens, R., Nuyens, R., Cornelissen, F. & Geerts, H. The fast axonal transport in hippocampal neurones is acutely enhanced by db-cAMP. Neuroreport 4, 179-182 (1993).
23. Azhderian, E.M., Hefner, D., Lin, C.H., Kaczmarek, L.K. & Forscher, P. Cyclic AMP modulates fast axonal transport in Aplysia bag cell neurons by increasing the probability of single organelle movement. Neuron 12, 1223-1233 (1994).
24. Neumann, H. Molecular mechanisms of axonal damage in inflammatory central nervous system diseases. Curr. Opin. Neurol. 16, 267-273 (2003).
25. Kammer, G.M. The adenylate cyclase-cAMP-protein kinase A pathway and regulation of the immune response. Immunol. Today 9, 222-229 (1988).
26. Zidek, Z. Adenosine-cyclic AMP pathways and cytokine expression. Eur. Cytokine Netw. 10, 319-328 (1999).
27. Xu, J. et al. Methylprednisolone inhibition of TNF-α expression and NF-κB activation after spinal cord injury in rats. Brain Res. Mol. Brain Res. 59, 135-142 (1998).
28. Bethea, J.R. et al. Systemically administered interleukin-10 reduces tumor necrosis factor-α production and significantly improves functional recovery following traumatic spinal cord injury in rats. J. Neurotrauma 16, 851-863 (1999).
29. -, NGF-receptor) depends on growth inhibition. J. Cell Biol. 112, 457-467 (1991).
30. Morgan, L., Jessen, K.R. & Mirsky, R. Negative regulation of the P0 gene in Schwann cells: suppression of PO mRNA and protein induction in cultured Schwann cells by FGF2 and TGFβ1, TGFβ2 and TGFβ3. Development 120, 1399-1409 (1994).
31. Howe, D.G. & McCarthy, K.D. Retroviral inhibition of cAMP-dependent protein kinase inhibits myelination but not Schwann cell mitosis stimulated by interaction with neurons. J. Neurosci. 20, 3513-3521 (2000).
32. Viala, D. & Buser, P. The effects of DOPA and 5-HTP on rhythmic efferent discharges in hind limb nerves in the rabbit. Brain Res. 12, 437-443 (1969).
33. Ribotta, M.G. et al. Activation of locomotion in adult chronic spinal rats is achieved by transplantation of embryonic raphe cells reinnervating a precise lumbar level. J. Neurosci. 20, 5144-5152 (2000).
34. Barbeau, H. & Rossignol, S. Initiation and modulation of the Iocomotor pattern in the adult chronic spinal cat by noradrenergic, serotonergic and dopaminergic drugs. Brain Res. 546, 250-260 (1991).
35. Davies, S.J. et al. Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390, 680-683 (1997).
36. Bradbury, E.J. et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636-640 (2002).
37. Yamamoto, M. et al. Nerve growth factor (NGF), brain-derived neurotrophic factor (BDNF) and low-affinity nerve growth factor receptor (LNGFR) mRNA levels in cultured rat Schwann cells; differential time- and dose-dependent regulation by cAMP. Neurosci. Lett. 152, 37-40 (1993).
38. Neumann, S., Bradke, F., Tessier-Lavigne, M. & Basbaum, A.I. Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34, 885-893 (2002).
39. Qiu, J. et al. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34, 1-9 (2002).
40. Morrissey, T.K., Kleitman, N. & Bunge, R.P. Isolation and functional characterization of Schwann cells derived from adult peripheral nerve. J. Neurosci. 11, 2433-2442 (1991).
41. Gruner, J.A. A monitored contusion model of spinal cord injury in the rat. J. Neurotrauma 9, 123-128 (1992).
42. Xu, X.M., Guenard, V., Kleitman, N. & Bunge, M.B. Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J. Comp. Neurol. 351, 145-160 (1995).
43. West, N.R. & Collins, G.H. Cellular changes during repair of a cryogenic spinal cord injury in the rat: an electron microscopic study. J. Neuropathol. Exp. Neurol. 48, 94-108 (1989).
44. Bunge, M.B., Holets, V.R., Bates, M.L., Clarke, T.S. & Watson, B.D. Characterization of photochemically induced spinal cord injury in the rat by light and electron microscopy. Exp. Neurol. 127, 76-93 (1994).
45. Ludwin, S.K. Central nervous system demyelination and remyelination in the mouse: an ultrastructural study of cuprizone toxicity. Lab. Invest. 39, 597-612 (1978).
46. Basso, D.M., Beattie, M.S. & Bresnahan, J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 12, 1-21 (1995).
47. Metz, G.A., Merkler, D., Dietz, V., Schwab, M.E. & Fouad, K. Efficient testing of motor function in spinal cord injured rats. Brain Res. 883, 165-177 (2000).
48. de Medinaceli, L., Freed, W.J. & Wyatt, R.J. An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Exp. Neurol. 77, 634-643 (1982).
49. Scheff, S.W., Saucier, D.A. & Cain, M.E. A statistical method for analyzing rating scale data: the BBB locomotor score. J. Neurotrauma 19, 1251-1260 (2002).
50. Cohen, J. Statistical Power Analysis for the Behavioral Sciences edn. 2 (Erlbaum, Hillsdale, New Jersey, USA, 1988).