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Mediators of Inflammation
Volume 2015, Article ID 251204, 14 pages
http://dx.doi.org/10.1155/2015/251204
Research Article

Neurotrauma and Inflammation: CNS and PNS Responses

Laboratório de Neurodegeneração e Reparo, Departamento de Patologia, Faculdade de Medicina, Hospital Universitário Clementino Fraga Filho, Universidade Federal do Rio de Janeiro, 21941-550 Rio de Janeiro, RJ, Brazil

Received 23 December 2014; Revised 24 February 2015; Accepted 9 March 2015

Academic Editor: Luc Vallières

Copyright © 2015 Bruno Siqueira Mietto et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. Lubińska, “Early course of Wallerian degeneration in myelinated fibres of the rat phrenic nerve,” Brain Research, vol. 130, no. 1, pp. 47–63, 1977. View at Publisher · View at Google Scholar · View at Scopus
  2. G. Stoll, S. Jander, and R. R. Myers, “Degeneration and regeneration of the peripheral nervous system: from Augustus Waller's observations to neuroinflammation,” Journal of the Peripheral Nervous System, vol. 7, no. 1, pp. 13–27, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. B. S. Mietto, R. M. Costa, S. V. de Lima, S. T. Ferreira, and A. M. B. Martinez, “Wallerian degeneration in injury and disease: concepts and prevention,” in Advanced Understanding of Neurodegenerative Diseases, R. C.-C. Chang, Ed., chapter 17, InTech, 2011. View at Publisher · View at Google Scholar
  4. A. Waller, “Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations of the alterations produced thereby in the structure of their primitive fibres,” Philosophical Transactions of the Royal Society of London, vol. 140, no. 0, pp. 423–429, 1850. View at Publisher · View at Google Scholar
  5. M. E. Vargas and B. A. Barres, “Why is Wallerian degeneration in the CNS so slow?” Annual Review of Neuroscience, vol. 30, pp. 153–179, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. M. P. Coleman and V. H. Perry, “Axon pathology in neurological disease: a neglected therapeutic target,” Trends in Neurosciences, vol. 25, no. 10, pp. 532–537, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. A. D. Gaudet, P. G. Popovich, and M. S. Ramer, “Wallerian degeneration: gaining perspective on inflammatory events after peripheral nerve injury,” Journal of Neuroinflammation, vol. 8, article 110, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Rotshenker, “Wallerian degeneration: the innate-immune response to traumatic nerve injury,” Journal of Neuroinflammation, vol. 8, article 109, pp. 1–14, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. A. DeFrancesco-Lisowitz, J. A. Lindborg, J. P. Niemi, and R. E. Zigmond, “The neuroimmunology of degeneration and regeneration in the peripheral nervous system,” Neuroscience, 2014. View at Publisher · View at Google Scholar
  10. A. E. Mautes, M. R. Weinzierl, F. Donovan, and L. J. Noble, “Vascular events after a spinal cord injury: contribution to secondary pathogenesis,” Physical Therapy, vol. 80, no. 7, pp. 673–687, 2000. View at Google Scholar · View at Scopus
  11. O. N. Hausmann, “Post-traumatic inflammation following spinal cord injury,” Spinal Cord, vol. 41, no. 7, pp. 369–378, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. F. M. Bareyre and M. E. Schwab, “Inflammation, degeneration and regeneration in the injured spinal cord: insights from DNA microarrays,” Trends in Neurosciences, vol. 26, no. 10, pp. 555–563, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. M. D. Norenberg, J. Smith, and A. Marcillo, “The pathology of human spinal cord injury: defining the problems,” Journal of Neurotrauma, vol. 21, no. 4, pp. 429–440, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. P. G. Popovich and T. B. Jones, “Manipulating neuroinflammatory reactions in the injured spinal cord: back to basics,” Trends in Pharmacological Sciences, vol. 24, no. 1, pp. 13–17, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. K. D. Beck, H. X. Nguyen, M. D. Galvan, D. L. Salazar, T. M. Woodruff, and A. J. Anderson, “Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment,” Brain, vol. 133, no. 2, pp. 433–447, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Makwana and G. Raivich, “Molecular mechanisms in successful peripheral regeneration,” The FEBS Journal, vol. 272, no. 11, pp. 2628–2638, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. Z.-L. Chen, W.-M. Yu, and S. Strickland, “Peripheral regeneration,” Annual Review of Neuroscience, vol. 30, pp. 209–233, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. B. Barrette, M.-A. Hébert, M. Filali et al., “Requirement of myeloid cells for axon regeneration,” The Journal of Neuroscience, vol. 28, no. 38, pp. 9363–9376, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. M. S. Narciso, B. D. S. Mietto, S. A. Marques et al., “Sciatic nerve regeneration is accelerated in galectin-3 knockout mice,” Experimental Neurology, vol. 217, no. 1, pp. 7–15, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. B. S. Mietto, S. Jurgensen, L. Alves et al., “Lack of galectin-3 speeds Wallerian degeneration by altering TLR and pro-inflammatory cytokine expressions in injured sciatic nerve,” The European Journal of Neuroscience, vol. 37, no. 10, pp. 1682–1690, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Taoka, K. Okajima, M. Uchiba et al., “Role of neutrophils in spinal cord injury in the rat,” Neuroscience, vol. 79, no. 4, pp. 1177–1182, 1997. View at Publisher · View at Google Scholar · View at Scopus
  22. P. G. Popovich, Z. Guan, P. Wei, I. Huitinga, N. Van Rooijen, and B. T. Stokes, “Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury,” Experimental Neurology, vol. 158, no. 2, pp. 351–365, 1999. View at Publisher · View at Google Scholar · View at Scopus
  23. D. P. Ankeny, Z. Guan, and P. G. Popovich, “B cells produce pathogenic antibodies and impair recovery after spinal cord injury in mice,” The Journal of Clinical Investigation, vol. 119, no. 10, pp. 2990–2999, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Leon, Y. Yin, J. Nguyen, N. Irwin, and L. I. Benowitz, “Lens injury stimulates axon regeneration in the mature rat optic nerve,” The Journal of Neuroscience, vol. 20, no. 12, pp. 4615–4626, 2000. View at Google Scholar · View at Scopus
  25. Y. Yin, M. T. Henzl, B. Lorber et al., “Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells,” Nature Neuroscience, vol. 9, no. 6, pp. 843–852, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. R. L. Ruff, L. McKerracher, and M. E. Selzer, “Repair and neurorehabilitation strategies for spinal cord injury,” Annals of the New York Academy of Sciences, vol. 1142, pp. 1–20, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. H. L. Harkey III, E. A. White IV, R. E. Tibbs Jr., and D. E. Haines, “A clinician's view of spinal cord injury,” Anatomical Record, Part B: New Anatomist, vol. 271, no. 1, pp. 41–48, 2003. View at Google Scholar · View at Scopus
  28. J. M. Simard, O. Tsymbalyuk, A. Ivanov et al., “Endothelial sulfonylurea receptor 1-regulated NCCa-ATP channels mediate progressive hemorrhagic necrosis following spinal cord injury,” The Journal of Clinical Investigation, vol. 117, no. 8, pp. 2105–2113, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. P. G. Popovich, S. Lemeshow, J. C. Gensel, and C. A. Tovar, “Independent evaluation of the effects of glibenclamide on reducing progressive hemorrhagic necrosis after cervical spinal cord injury,” Experimental Neurology, vol. 233, no. 2, pp. 615–622, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. G. Yiu and Z. He, “Glial inhibition of CNS axon regeneration,” Nature Reviews Neuroscience, vol. 7, no. 8, pp. 617–627, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Rolls, R. Shechter, and M. Schwartz, “The bright side of the glial scar in CNS repair,” Nature Reviews Neuroscience, vol. 10, no. 3, pp. 235–241, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. S. David and S. S. Ousman, “Recruiting the immune response to promote axon regeneration in the injured spinal cord,” The Neuroscientist, vol. 8, no. 1, pp. 33–41, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. R. J. Giger, E. R. Hollis II, and M. H. Tuszynski, “Guidance molecules in axon regeneration,” Cold Spring Harbor Perspectives in Biology, vol. 2, no. 7, Article ID a001867, 21 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Elkabes, E. M. DiCicco-Bloom, and I. B. Black, “Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function,” The Journal of Neuroscience, vol. 16, no. 8, pp. 2508–2521, 1996. View at Google Scholar · View at Scopus
  35. M. C. Caroleo, N. Costa, L. Bracci-Laudiero, and L. Aloe, “Human monocyte/macrophages activate by exposure to LPS overexpress NGF and NGF receptors,” Journal of Neuroimmunology, vol. 113, no. 2, pp. 193–201, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. A. M. Parr, C. H. Tator, and A. Keating, “Bone marrow-derived mesenchymal stromal cells for the repair of central nervous system injury,” Bone Marrow Transplantation, vol. 40, no. 7, pp. 609–619, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Kettenmann, U.-K. Hanisch, M. Noda, and A. Verkhratsky, “Physiology of microglia,” Physiological Reviews, vol. 91, no. 2, pp. 461–553, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. R. B. Rock, G. Gekker, S. Hu et al., “Role of microglia in central nervous system infections,” Clinical Microbiology Reviews, vol. 17, no. 4, pp. 942–964, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Zhou, G. Andonegui, C. H. Y. Wong, and P. Kubes, “Role of endothelial TLR4 for neutrophil recruitment into central nervous system microvessels in systemic inflammation,” The Journal of Immunology, vol. 183, no. 8, pp. 5244–5250, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. E. Kolaczkowska and P. Kubes, “Neutrophil recruitment and function in health and inflammation,” Nature Reviews Immunology, vol. 13, no. 3, pp. 159–175, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. M. R. Williams, V. Azcutia, G. Newton, P. Alcaide, and F. W. Luscinskas, “Emerging mechanisms of neutrophil recruitment across endothelium,” Trends in Immunology, vol. 32, no. 10, pp. 461–469, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. K. A. Kigerl, J. P. de Rivero Vaccari, W. D. Dietrich, P. G. Popovich, and R. W. Keane, “Pattern recognition receptors and central nervous system repair,” Experimental Neurology, vol. 258, pp. 5–16, 2014. View at Publisher · View at Google Scholar
  43. L. J. Noble, F. Donovan, T. Igarashi, S. Goussev, and Z. Werb, “Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events,” Journal of Neuroscience, vol. 22, no. 17, pp. 7526–7535, 2002. View at Google Scholar · View at Scopus
  44. V. W. Yong, “Metalloproteinases: mediators of pathology and regeneration in the CNS,” Nature Reviews Neuroscience, vol. 6, no. 12, pp. 931–944, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Jin, G. Yang, and G. Li, “Inflammatory mechanisms in ischemic stroke: role of inflammatory cells,” Journal of Leukocyte Biology, vol. 87, no. 5, pp. 779–789, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. D. P. Stirling, S. Liu, P. Kubes, and V. W. Yong, “Depletion of Ly6G/Gr-1 leukocytes after spinal cord injury in mice alters wound healing and worsens neurological outcome,” The Journal of Neuroscience, vol. 29, no. 3, pp. 753–764, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Yin, Q. Cui, H.-Y. Gilbert et al., “Oncomodulin links inflammation to optic nerve regeneration,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 46, pp. 19587–19592, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. T. Kurimoto, Y. Yin, G. Habboub et al., “Neutrophils express oncomodulin and promote optic nerve regeneration,” The Journal of Neuroscience, vol. 33, no. 37, pp. 14816–14824, 2013. View at Publisher · View at Google Scholar
  49. Y. Ren and W. Young, “Managing inflammation after spinal cord injury through manipulation of macrophage function,” Neural Plasticity, vol. 2013, Article ID 945034, 9 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. C. Shi and E. G. Pamer, “Monocyte recruitment during infection and inflammation,” Nature Reviews Immunology, vol. 11, no. 11, pp. 762–774, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. K. A. Kigerl, J. C. Gensel, D. P. Ankeny, J. K. Alexander, D. J. Donnelly, and P. G. Popovich, “Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord,” The Journal of Neuroscience, vol. 29, no. 43, pp. 13435–13444, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. A. R. Ferguson, R. N. Christensen, J. C. Gensel et al., “Cell death after spinal cord injury is exacerbated by rapid TNFα-induced trafficking of GluR2-lacking AMPARs to the plasma membrane,” The Journal of Neuroscience, vol. 28, no. 44, pp. 11391–11400, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. S. David and A. Kroner, “Repertoire of microglial and macrophage responses after spinal cord injury,” Nature Reviews Neuroscience, vol. 12, no. 7, pp. 388–399, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. D. J. Donnelly, E. E. Longbrake, T. M. Shawler et al., “Deficient CX3CR1 signaling promotes recovery after mouse spinal cord injury by limiting the recruitment andactivation of Ly6Clo/iNOS+ macrophages,” The Journal of Neuroscience, vol. 31, no. 27, pp. 9910–9922, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. A. E. Cardona, E. P. Pioro, M. E. Sasse et al., “Control of microglial neurotoxicity by the fractalkine receptor,” Nature Neuroscience, vol. 9, no. 7, pp. 917–924, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. S. de Lima, Y. Koriyama, T. Kurimoto et al., “Full-length axon regeneration in the adult mouse optic nerve and partial recovery of simple visual behaviors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 23, pp. 9149–9154, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Mueller, K. Wacker, E. B. Ringelstein, W. F. Hickey, Y. Imai, and R. Kiefer, “Rapid response of identified resident endoneurial macrophages to nerve injury,” The American Journal of Pathology, vol. 159, no. 6, pp. 2187–2197, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Mueller, C. Leonhard, K. Wacker et al., “Macrophage response to peripheral nerve injury: the quantitative contribution of resident and hematogenous macrophages,” Laboratory Investigation, vol. 83, no. 2, pp. 175–185, 2003. View at Publisher · View at Google Scholar · View at Scopus
  59. R. Wagner and R. R. Myers, “Schwann cells produce tumor necrosis factor alpha: expression in injured and non-injured nerves,” Neuroscience, vol. 73, no. 3, pp. 625–629, 1996. View at Publisher · View at Google Scholar · View at Scopus
  60. S. Shamash, F. Reichert, and S. Rotshenker, “The cytokine network of wallerian degeneration: tumor necrosis factor-α, interleukin-1α, and interleukin-1β,” The Journal of Neuroscience, vol. 22, no. 8, pp. 3052–3060, 2002. View at Google Scholar · View at Scopus
  61. H. Be'eri, F. Reichert, A. Saada, and S. Rotshenker, “The cytokine network of Wallerian degeneration: IL-10 and GM-CSF,” The European Journal of Neuroscience, vol. 10, no. 8, pp. 2707–2713, 1998. View at Publisher · View at Google Scholar · View at Scopus
  62. F. E. Perrin, S. Lacroix, M. Avilés-Trieueros, and S. David, “Involvement of monocyte chemoattractant protein-1 macrophage inflammatory protein-1alpha and interleukin-1beta in Wallerian degeneration,” Brain, vol. 128, part 4, pp. 854–866, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. D. Kim, S. Lee, and S. J. Lee, “Toll-like receptors in peripheral nerve injury and neuropathic pain,” Current Topics in Microbiology and Immunology, vol. 336, no. 1, pp. 169–186, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. I. Pineau and S. Lacroix, “Endogenous signals initiating inflammation in the injured nervous system,” Glia, vol. 57, no. 4, pp. 351–361, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Zedler and E. Faist, “The impact of endogenous triggers on trauma-associated inflammation,” Current Opinion in Critical Care, vol. 12, no. 6, pp. 595–601, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. H. Wekerle, M. Schwab, C. Linington, and R. Meyermann, “Antigen presentation in the peripheral nervous system: schwann cells present endogenous myelin autoantigens to lymphocytes,” European Journal of Immunology, vol. 16, no. 12, pp. 1551–1557, 1986. View at Publisher · View at Google Scholar · View at Scopus
  67. W. Baetas-da-Cruz, L. Alves, M. C. V. Pessolani et al., “Schwann cells express the macrophage mannose receptor and MHC class II. Do they have a role in antigen presentation?” Journal of the Peripheral Nervous System, vol. 14, no. 2, pp. 84–92, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Goethals, E. Ydens, V. Timmerman, and S. Janssens, “Toll-like receptor expression in the peripheral nerve,” Glia, vol. 58, no. 14, pp. 1701–1709, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. K. Takeda, T. Kaisho, and S. Akira, “Toll-like receptors,” Annual Review of Immunology, vol. 21, pp. 335–376, 2003. View at Publisher · View at Google Scholar · View at Scopus
  70. H. Lee, E.-K. Jo, S.-Y. Choi et al., “Necrotic neuronal cells induce inflammatory Schwann cell activation via TLR2 and TLR3: implication in Wallerian degeneration,” Biochemical and Biophysical Research Communications, vol. 350, no. 3, pp. 742–747, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. T. Kawai and S. Akira, “TLR signaling,” Cell Death & Differentiation, vol. 13, no. 5, pp. 816–825, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. A. Boivin, I. Pineau, B. Barrette et al., “Toll-like receptor signaling is critical for Wallerian degeneration and functional recovery after peripheral nerve injury,” The Journal of Neuroscience, vol. 27, no. 46, pp. 12565–12576, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. M. Murakami, Y. Nakatani, G.-I. Atsumi, K. Inoue, and I. Kudo, “Regulatory functions of phospholipase A2,” Critical Reviews in Immunology, vol. 17, no. 3-4, pp. 225–283, 1997. View at Publisher · View at Google Scholar · View at Scopus
  74. S. De, M. A. Trigueros, A. Kalyvas, and S. David, “Phospholipase A2 plays an important role in myelin breakdown and phagocytosis during wallerian degeneration,” Molecular and Cellular Neuroscience, vol. 24, no. 3, pp. 753–765, 2003. View at Publisher · View at Google Scholar · View at Scopus
  75. R. Martini, S. Fischer, R. López-Vales, and S. David, “Interactions between schwann cells and macrophages in injury and inherited demyelinating disease,” Glia, vol. 56, no. 14, pp. 1566–1577, 2008. View at Publisher · View at Google Scholar · View at Scopus
  76. R. López-Vales, X. Navarro, T. Shimizu et al., “Intracellular phospholipase A2 group IVA and group VIA play important roles in Wallerian degeneration and axon regeneration after peripheral nerve injury,” Brain, vol. 131, part 10, pp. 2620–2631, 2008. View at Publisher · View at Google Scholar
  77. J. Jung, W. Cai, H. K. Lee et al., “Actin polymerization is essential for myelin sheath fragmentation during Wallerian degeneration,” The Journal of Neuroscience, vol. 31, no. 6, pp. 2009–2015, 2011. View at Publisher · View at Google Scholar · View at Scopus
  78. D. Bastien and S. Lacroix, “Cytokine pathways regulating glial and leukocyte function after spinal cord and peripheral nerve injury,” Experimental Neurology, vol. 258, pp. 62–77, 2014. View at Publisher · View at Google Scholar
  79. A. M. B. Malbouisson, M. N. Ghabriel, and G. Allt, “Axonal degeneration in large and small nerve fibres. An electron-microscopic and morphometric study,” Journal of the Neurological Sciences, vol. 67, no. 3, pp. 307–318, 1985. View at Publisher · View at Google Scholar · View at Scopus
  80. A. M. B. Martinez and S. Canavarro, “Early myelin breakdown following sural nerve crush: a freeze-fracture study,” Brazilian Journal of Medical and Biological Research, vol. 33, no. 12, pp. 1477–1482, 2000. View at Publisher · View at Google Scholar · View at Scopus
  81. M. C. Raff, A. V. Whitmore, and J. T. Finn, “Axonal self-destruction and neurodegeneration,” Science, vol. 296, no. 5569, pp. 868–871, 2002. View at Publisher · View at Google Scholar · View at Scopus
  82. J. T. Wang, Z. A. Medress, and B. A. Barres, “Axon degeneration: molecular mechanisms of a self-destruction pathway,” The Journal of Cell Biology, vol. 196, no. 1, pp. 7–18, 2012. View at Publisher · View at Google Scholar · View at Scopus
  83. J. Gilley and M. P. Coleman, “Endogenous Nmnat2 is an essential survival factor for maintenance of health axons,” PLoS Biology, vol. 8, no. 1, Article ID e1000300, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. C. Leonhard, M. Müller, W. F. Hickey, E. B. Ringelstein, and R. Kiefer, “Lesion response of long-term and recently immigrated resident endoneurial macrophages in peripheral nerve explant cultures from bone marrow chimeric mice,” The European Journal of Neuroscience, vol. 16, no. 9, pp. 1654–1660, 2002. View at Publisher · View at Google Scholar · View at Scopus
  85. M. E. Vargas, J. Watanabe, S. J. Singh, W. H. Robinson, and B. A. Barres, “Endogenous antibodies promote rapid myelin clearance and effective axon regeneration after nerve injury,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 26, pp. 11993–11998, 2010. View at Publisher · View at Google Scholar · View at Scopus
  86. C. Fernandez-Valle, R. P. Bunge, and M. B. Bunge, “Schwann cells degrade myelin and proliferate in the absence of macrophages: evidence from in vitro studies of Wallerian degeneration,” Journal of Neurocytology, vol. 24, no. 9, pp. 667–679, 1995. View at Publisher · View at Google Scholar · View at Scopus
  87. V. H. Perry, J. W. Tsao, S. Fearn, and M. C. Brown, “Radiation-induced reductions in macrophage recruitment have only slight effects on myelin degeneration in sectioned peripheral nerves of mice,” The European Journal of Neuroscience, vol. 7, no. 2, pp. 271–280, 1995. View at Publisher · View at Google Scholar · View at Scopus
  88. E. Ydens, A. Cauwels, B. Asselbergh et al., “Acute injury in the peripheral nervous system triggers an alternative macrophage response,” Journal of Neuroinflammation, vol. 9, article 176, 17 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  89. S. Nadeau, M. Filali, J. Zhang et al., “Functional recovery after peripheral nerve injury is dependent on the pro-inflammatory cytokines IL-1β and TNF: implications for neuropathic pain,” The Journal of Neuroscience, vol. 31, no. 35, pp. 12533–12542, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. T. Komori, Y. Morikawa, T. Inada, T. Hisaoka, and E. Senba, “Site-specific subtypes of macrophages recruited after peripheral nerve injury,” NeuroReport, vol. 22, no. 17, pp. 911–917, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. J. K. Juranek, M. S. Geddis, F. Song et al., “RAGE deficiency improves postinjury sciatc nerve regeneration in type 1 diabetic mouse,” Diabetes, vol. 62, no. 3, pp. 931–943, 2013. View at Publisher · View at Google Scholar · View at Scopus
  92. L. A. Boven, M. van Meurs, M. van Zwam et al., “Myelin-laden macrophages are anti-inflammatory, consistent with foam cells in multiple sclerosis,” Brain, vol. 129, no. 2, pp. 517–526, 2006. View at Publisher · View at Google Scholar · View at Scopus
  93. A. Kroner, A. D. Greenhalgh, J. G. Zarruk et al., “TNF and increased intracellular iron alter macrophage polarization to a detrimental M1 phenotype in the injured spinal cord,” Neuron, vol. 83, no. 5, pp. 1098–1116, 2014. View at Publisher · View at Google Scholar
  94. E. J. Fry, C. Ho, and S. David, “A role for Nogo receptor in macrophage clearance from injured peripheral nerve,” Neuron, vol. 53, no. 5, pp. 649–662, 2007. View at Publisher · View at Google Scholar · View at Scopus
  95. E. I. Girolami, D. Bouhy, M. Haber, H. Johnson, and S. David, “Differential expression and potential role of SOCS1 and SOCS3 in Wallerian degeneration in injured peripheral nerve,” Experimental Neurology, vol. 223, no. 1, pp. 173–182, 2010. View at Publisher · View at Google Scholar · View at Scopus
  96. F. Reichert, A. Saada, and S. Rotshenker, “Peripheral nerve injury induces Schwann cells to express two macrophage phenotypes: phagocytosis and the galactose-specific lectin MAC-2,” The Journal of Neuroscience, vol. 14, no. 5, part 2, pp. 3231–3245, 1994. View at Google Scholar · View at Scopus
  97. M. P. Coleman and M. R. Freeman, “Wallerian degeneration, wlds, and nmnat,” Annual Review of Neuroscience, vol. 33, pp. 245–267, 2010. View at Publisher · View at Google Scholar · View at Scopus
  98. S. Rotshenker, “The role of galectin-3/MAC-2 in the activation of the innate-immune function of phagocytosis in microglia in injury and disease,” Journal of Molecular Neuroscience, vol. 39, no. 1-2, pp. 99–103, 2009. View at Publisher · View at Google Scholar · View at Scopus
  99. L. C. Ferraz, E. S. Bernardes, A. F. Oliveira et al., “Lack of galectin-3 alters the balance of innate immune cytokines and confers resistance to Rhodococcus equi infection,” European Journal of Immunology, vol. 38, no. 10, pp. 2762–2775, 2008. View at Publisher · View at Google Scholar · View at Scopus
  100. A. Filer, M. Bik, G. N. Parsonage et al., “Galectin 3 induces a distinctive pattern of cytokine and chemokine production in rheumatoid synovial fibroblasts via selective signaling pathways,” Arthritis and Rheumatism, vol. 60, no. 6, pp. 1604–1614, 2009. View at Publisher · View at Google Scholar · View at Scopus
  101. S. B. Jeon, H. J. Yoon, C. Y. Chang, H. S. Koh, S.-H. Jeon, and E. J. Park, “Galectin-3 exerts cytokine-like regulatory actions through the JAK-STAT pathway,” Journal of Immunology, vol. 185, no. 11, pp. 7037–7046, 2010. View at Publisher · View at Google Scholar · View at Scopus
  102. J. Dumic, S. Dabelic, and M. Flögel, “Galectin-3: an open-ended story,” Biochimica et Biophysica Acta—General Subjects, vol. 1760, no. 4, pp. 616–635, 2006. View at Publisher · View at Google Scholar · View at Scopus
  103. P. Gustavsson, C. E. Linsmeier, H. Leffler, and M. Kanje, “Galectin-3 inhibits Schwann cell proliferation in cultured sciatic nerve,” NeuroReport, vol. 18, no. 7, pp. 669–673, 2007. View at Publisher · View at Google Scholar · View at Scopus
  104. H. Inohara, S. Akahani, and A. Raz, “Galectin-3 stimulates cell proliferation,” Experimental Cell Research, vol. 245, no. 2, pp. 294–302, 1998. View at Publisher · View at Google Scholar · View at Scopus
  105. P. Dubový, “Wallerian degeneration and peripheral nerve conditions for both axonal regeneration and neuropathic pain induction,” Annals of Anatomy, vol. 193, no. 4, pp. 267–275, 2011. View at Publisher · View at Google Scholar · View at Scopus
  106. A. M. B. Martinez and L. C. V. Ribeiro, “Ultrastructural localization of calcium in peripheral nerve fibres undergoing Wallerian degeneration: an oxalate-pyroantimonate and X-ray microanalysis study,” Journal of Submicroscopic Cytology and Pathology, vol. 30, no. 3, pp. 451–458, 1998. View at Google Scholar · View at Scopus
  107. Q. Zhai, J. Wang, A. Kim et al., “Involvement of the ubiquitin-proteasome system in the early stages of Wallerian degeneration,” Neuron, vol. 39, no. 2, pp. 217–225, 2003. View at Publisher · View at Google Scholar · View at Scopus
  108. A. D. Guertin, D. P. Zhang, K. S. Mak, J. A. Alberta, and H. A. Kim, “Microanatomy of axon/glial signaling during Wallerian degeneration,” The Journal of Neuroscience, vol. 25, no. 13, pp. 3478–3487, 2005. View at Publisher · View at Google Scholar · View at Scopus
  109. Z.-L. Chen and S. Strickland, “Laminin γ1 is critical for Schwann cell differentiation, axon myelination, and regeneration in the peripheral nerve,” The Journal of Cell Biology, vol. 163, no. 4, pp. 889–899, 2003. View at Publisher · View at Google Scholar · View at Scopus
  110. M. Trupp, M. Rydén, H. Jörnvall et al., “Peripheral expression and biological activities of GDNF, a new neurotrophic factor for avian and mammalian peripheral neurons,” Journal of Cell Biology, vol. 130, no. 1, pp. 137–148, 1995. View at Publisher · View at Google Scholar · View at Scopus
  111. S. You, T. Petrov, P. H. Chung, and T. Gordon, “The expression of the low affinity nerve growth factor receptor in long-term denervated Schwann cells,” Glia, vol. 20, no. 2, pp. 87–100, 1997. View at Publisher · View at Google Scholar
  112. K. R. Jessen and R. Mirsky, “Negative regulation of myelination: relevance for development, injury, and demyelinating disease,” Glia, vol. 56, no. 14, pp. 1552–1565, 2008. View at Publisher · View at Google Scholar · View at Scopus
  113. P. J. Arthur-Farraj, M. Latouche, D. K. Wilton et al., “c-Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration,” Neuron, vol. 75, no. 4, pp. 633–647, 2012. View at Publisher · View at Google Scholar · View at Scopus
  114. A. BrosiusLutz and B. A. Barres, “Contrasting the glial response to axon injury in the central and peripheral nervous systems,” Developmental Cell, vol. 28, no. 1, pp. 7–17, 2014. View at Publisher · View at Google Scholar · View at Scopus
  115. J. W. Griffin, B. Pan, M. A. Polley, P. N. Hoffman, and M. H. Farah, “Measuring nerve regeneration in the mouse,” Experimental Neurology, vol. 223, no. 1, pp. 60–71, 2010. View at Publisher · View at Google Scholar · View at Scopus
  116. R. Deumens, A. Bozkurt, M. F. Meek et al., “Repairing injured peripheral nerves: bridging the gap,” Progress in Neurobiology, vol. 92, no. 3, pp. 245–276, 2010. View at Publisher · View at Google Scholar · View at Scopus
  117. M. A. Bisby and S. Chen, “Delayed Wallerian degeneration in sciatic nerves of C57BL/Ola mice is associated with impaired regeneration of sensory axons,” Brain Research, vol. 530, no. 1, pp. 117–120, 1990. View at Publisher · View at Google Scholar · View at Scopus
  118. M. C. Brown, E. R. Lunn, and V. H. Perry, “Consequences of slow Wallerian degeneration for regenerating motor and sensory axons,” Journal of Neurobiology, vol. 23, no. 5, pp. 521–536, 1992. View at Publisher · View at Google Scholar · View at Scopus
  119. S. Chen and M. A. Bisby, “Impaired motor axon regeneration in the C57BL/Ola mouse,” The Journal of Comparative Neurology, vol. 333, no. 3, pp. 449–454, 1993. View at Publisher · View at Google Scholar · View at Scopus
  120. D. Levy, P. Kubes, and D. W. Zochodne, “Delayed peripheral nerve degeneration, regeneration, and pain in mice lacking inducible nitric oxide synthase,” Journal of Neuropathology and Experimental Neurology, vol. 60, no. 5, pp. 411–421, 2001. View at Google Scholar · View at Scopus
  121. L. I. Benowitz and P. G. Popovich, “Inflammation and axon regeneration,” Current Opinion in Neurology, vol. 24, no. 6, pp. 577–583, 2011. View at Publisher · View at Google Scholar · View at Scopus
  122. S. David, P. E. Braun, D. L. Jackson, V. Kottis, and L. McKerracher, “Laminin overrides the inhibitory effects of peripheral nervous system and central nervous system myelin-derived inhibitors of neurite growth,” Journal of Neuroscience Research, vol. 42, no. 4, pp. 594–602, 1995. View at Publisher · View at Google Scholar · View at Scopus
  123. M. T. Filbin, “Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS,” Nature Reviews Neuroscience, vol. 4, no. 9, pp. 703–713, 2003. View at Publisher · View at Google Scholar · View at Scopus
  124. A. M. Winzeler, W. J. Mandemakers, M. Z. Sun, M. Stafford, C. T. Phillips, and B. A. Barres, “The lipid sulfatide is a novel myelin-associated inhibitor of CNS axon outgrowth,” The Journal of Neuroscience, vol. 31, no. 17, pp. 6481–6492, 2011. View at Publisher · View at Google Scholar · View at Scopus
  125. S. Rotshenker, S. Aamar, and V. Barak, “Interleukin-1 activity in lesioned peripheral nerve,” Journal of Neuroimmunology, vol. 39, no. 1-2, pp. 75–80, 1992. View at Publisher · View at Google Scholar · View at Scopus
  126. R. Seijffers, A. J. Allchorne, and C. J. Woolf, “The transcription factor ATF-3 promotes neurite outgrowth,” Molecular and Cellular Neuroscience, vol. 32, no. 1-2, pp. 143–154, 2006. View at Publisher · View at Google Scholar · View at Scopus
  127. H. M. Bomze, K. R. Bulsara, B. J. Iskandar, P. Caroni, and J. H. Pate Skene, “Spinal axon regeneration evoked by replacing two growth cone proteins in adult neurons,” Nature Neuroscience, vol. 4, no. 1, pp. 38–43, 2001. View at Publisher · View at Google Scholar · View at Scopus
  128. G. Raivich, M. Bohatschek, C. Da Costa et al., “The AP-1 transcription factor c-Jun is required for efficient axonal regeneration,” Neuron, vol. 43, no. 1, pp. 57–67, 2004. View at Publisher · View at Google Scholar · View at Scopus
  129. S. W. N. Thompson, A. B. Vernallis, J. K. Heath, and J. V. Priestley, “Leukaemia inhibitory factor is retrogradely transported by a distinct population of adult rat sensory neurons: co-localization with trkA and other neurochemical markers,” European Journal of Neuroscience, vol. 9, no. 6, pp. 1244–1251, 1997. View at Publisher · View at Google Scholar · View at Scopus
  130. W. B. J. Cafferty, N. J. Gardiner, I. Gavazzi et al., “Leukemia inhibitory factor determines the growth status of injured adult sensory neurons,” The Journal of Neuroscience, vol. 21, no. 18, pp. 7161–7170, 2001. View at Google Scholar · View at Scopus
  131. R. D. Gosselin, M. A. Dansereau, M. Pohl et al., “Chemokine network in the nervous system: a new target for pain relief,” Current Medicinal Chemistry, vol. 15, no. 27, pp. 2866–2875, 2008. View at Publisher · View at Google Scholar · View at Scopus
  132. M. Mäurer, K. V. Toyka, and R. Gold, “Immune mechanisms in acquired demyelinating neuropathies: lessons from animal models,” Neuromuscular Disorders, vol. 12, no. 4, pp. 405–414, 2002. View at Publisher · View at Google Scholar · View at Scopus
  133. J. Silver and J. H. Miller, “Regeneration beyond the glial scar,” Nature Reviews Neuroscience, vol. 5, no. 2, pp. 146–156, 2004. View at Publisher · View at Google Scholar · View at Scopus