cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury (original) (raw)

• Schwab, M.E. & Bartholdi, D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol. Rev. 76, 319–370 (1996).
  Article CAS Google Scholar
• Fawcett, J.W. & Asher, R.A. The glial scar and central nervous system repair. Brain Res. Bull. 49, 377–391 (1999).
  Article CAS Google Scholar
• Silver, S. & Miller, J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5, 146–156 (2004).
  Article CAS Google Scholar
• Richardson, P.M., McGuinness, U.M. & Aguayo, A.J. Axons from CNS neurons regenerate into PNS grafts. Nature 284, 264–265 (1980).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• Bunge, M.B. Bridging areas of injury in the spinal cord. Neuroscientist 7, 325–339 (2001).
  Article CAS Google Scholar
• 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)
  Article Google Scholar
• 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).
  Article CAS Google Scholar
• Song, H.J., Ming, G.L. & Poo, M.M. cAMP-induced switching in turning direction of nerve growth cones. Nature 388, 275–279 (1997).
  Article CAS Google Scholar
• Ming, G.L. et al. cAMP-dependent growth cone guidance by netrin-1. Neuron 19, 1225–1235 (1997).
  Article CAS Google Scholar
• Cai, D. et al. Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate. J. Neurosci. 21, 4731–4739 (2001).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• Lee, Y.B. et al. Role of tumor necrosis factor-α in neuronal and glial apoptosis after spinal cord injury. Exp. Neurol. 166, 190–195 (2000).
  Article CAS Google Scholar
• Nesic, O. et al. IL-1 receptor antagonist prevents apoptosis and caspase-3 activation after spinal cord injury. J. Neurotrauma 18, 947–956 (2001).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• Tator, C.H. Update on the pathophysiology and pathology of acute spinal cord injury. Brain Pathol. 5, 407–413 (1995).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article Google Scholar
• Nijjar, M.S. & Nijjar, S.S. Domoic acid–induced neurodegeneration resulting in memory loss is mediated by Ca2+ overload and inhibition of Ca2+ calmodulin-stimulated adenylate cyclase in rat brain. Int. J. Mol. Med. 6, 377–389 (2000).
  CAS PubMed Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• Neumann, H. Molecular mechanisms of axonal damage in inflammatory central nervous system diseases. Curr. Opin. Neurol. 16, 267–273 (2003).
  Article CAS Google Scholar
• Kammer, G.M. The adenylate cyclase–cAMP–protein kinase A pathway and regulation of the immune response. Immunol. Today 9, 222–229 (1988).
  Article CAS Google Scholar
• Zidek, Z. Adenosine–cyclic AMP pathways and cytokine expression. Eur. Cytokine Netw. 10, 319–328 (1999).
  CAS PubMed Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• Morgan, L., Jessen, K.R. & Mirsky, R. The effects of cAMP on differentiation of cultured Schwann cells: progression from an early phenotype (04+) to a myelin phenotype (P0+, GFAP−, N-CAM−, NGF-receptor−) depends on growth inhibition. J. Cell Biol. 112, 457–467 (1991).
  Article CAS Google Scholar
• Morgan, L., Jessen, K.R. & Mirsky, R. Negative regulation of the P0 gene in Schwann cells: suppression of P0 mRNA and protein induction in cultured Schwann cells by FGF2 and TGFβ1, TGFβ2 and TGFβ3. Development 120, 1399–1409 (1994).
  CAS PubMed Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• Barbeau, H. & Rossignol, S. Initiation and modulation of the locomotor pattern in the adult chronic spinal cat by noradrenergic, serotonergic and dopaminergic drugs. Brain Res. 546, 250–260 (1991).
  Article CAS Google Scholar
• Davies, S.J. et al. Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390, 680–683 (1997).
  Article CAS Google Scholar
• Bradbury, E.J. et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636–640 (2002).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• Qiu, J. et al. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34, 1–9 (2002).
  Article Google Scholar
• 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).
  Article CAS Google Scholar
• Gruner, J.A. A monitored contusion model of spinal cord injury in the rat. J. Neurotrauma 9, 123–128 (1992).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• Ludwin, S.K. Central nervous system demyelination and remyelination in the mouse: an ultrastructural study of cuprizone toxicity. Lab. Invest. 39, 597–612 (1978).
  CAS PubMed Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article Google Scholar
• Cohen, J. Statistical Power Analysis for the Behavioral Sciences edn. 2 (Erlbaum, Hillsdale, New Jersey, USA, 1988).
  Google Scholar