Neuroimmune processes associated with Wallerian degeneration support neurotrophin-3-induced axonal sprouting in the injured spinal cord

Journal of Neuroscience Research

Volumn 91, Issue 10, 2013, Pages 1280-1291

  Chen, Qin ^a,b   Shine, H David ^a,b,c  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b CENTER FOR CELL AND GENE THERAPY   (United States)

^c MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Axonal sprouting; CD4+ T cells; Neuroimmune response; Neurotrophin 3; Spinal cord injury; Type 2 T helper cells; Wallerian degeneration

Indexed keywords

NEUROTROPHIN 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; NERVE SPROUTING; NEUROIMMUNOLOGY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; RAT; SPINAL CORD INJURY; TH2 CELL; WALLERIAN DEGENERATION; ADOPTIVE TRANSFER; ANIMAL; DISEASE MODEL; DRUG EFFECTS; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; IMMUNOMODULATION; METABOLISM; NERVE FIBER; NERVE REGENERATION; NEUTROPHIL CHEMOTAXIS; NUDE RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT;

ADOPTIVE TRANSFER; ANIMALS; AXONS; CHEMOTAXIS, LEUKOCYTE; DISEASE MODELS, ANIMAL; FEMALE; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; NERVE REGENERATION; NEUROIMMUNOMODULATION; NEUROTROPHIN 3; RATS; RATS, NUDE; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPINAL CORD INJURIES; TH2 CELLS; WALLERIAN DEGENERATION;

EID: 84882884131     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23257     Document Type: Article

References (59)

1. Babcock AA, Kuziel WA, Rivest S, Owens T. 2003. Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS. J Neurosci 23:7922-7930.
2. Baumgartner BJ, Shine HD. 1998. Neuroprotection of spinal motoneurons following targeted transduction with an adenoviral vector carrying the gene for glial cell-line derived neurotrophic factor. Exp Neurol 153:102-112.
3. Besser M, Wank R. 1999. Cutting edge: clonally restricted production of the neurotrophins brain-derived neurotrophic factor and neurotrophin-3 mRNA by human immune cells and Th1/Th2-polarized expression of their receptors. J Immunol 162:6303-6306.
4. Biernacki K, Prat A, Blain M, Antel J. 2001. Regulation of Th1 and Th2 lymphocyte migration by human adult brain endothelial cells. J Neuropathol Exp Neurol 60:1127-1136.
5. Braddfute S, Goodell M. 2003. Bradfute SB, Goodell MA 2003 Adenoviral transduction of mouse hematopoietic stem cells. Mol Ther 7:334-340.
6. Bradl M, Bauer J, Flügel A, Wekerle H, Lassmann H. 2005. Complementary contribution of CD4 and CD8 T lymphocytes to T-cell infiltration of the intact and the degenerative spinal cord. Am J Pathol 166:1450.
7. + effector T cell subsets: neuroprotection and repair. Clin Neurosci Res 6:86-96.
8. Cafferty WBJ, Strittmatter SM. 2006. The Nogo-Nogo receptor pathway limits a spectrum of adult CNS axonal growth. J Neurosci 26:12242-12250.
9. Cafferty WBJ, Duffy P, Huebner E, Strittmatter SM. 2010. MAG and OMgp synergize with Nogo-A to restrict axonal growth and neurological recovery after spinal cord trauma. J Neurosci 30:6825-6837.
10. Cardona AE, Huang D, Sasse ME, Ransohoff RM. 2006. Isolation of murine microglial cells for RNA analysis or flow cytometry. Nat Protoc 1:1947-1951.
11. Carson MJ, Reilly CR, Sutcliffe JG, Lo D. 1998. Mature microglia resemble immature antigen-presenting cells. Glia 22:72-85.
12. Chen Q, Zhou L, Shine HD. 2006. Expression of neurotrophin-3 promotes axonal plasticity in the acute but not chronic injured spinal cord. J Neurotrauma 23:1254-1260.
13. Chen Q, Smith GM, Shine HD. 2008. Immune activation is required for NT-3-induced axonal plasticity in chronic spinal cord injury. Exp Neurol 209:497-509.
14. + T lymphocytes are preferentially recruited to the ileum in Crohn's disease. Gut 53:1287-1294.
15. Côté M-P, Azzam GA, Lemay MA, Zhukareva V, Houle JD. 2011. Activity-dependent increase in neurotrophic factors is associated with an enhanced modulation of spinal reflexes after spinal cord injury. J Neurotrauma 28:299-309.
16. Engelhardt B, Ransohoff RM. 2005. The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol 26:485-495.
17. Engelhardt B, Ransohoff RM. 2012. Capture, crawl, cross: the T cell code to breach the blood-brain barriers. Trends Immunol 33:579-589.
18. Festing MFW, Lovell D, Sparrow S, May D, Connors TA. 1978. An athymic nude mutation in the rat. Nature 274:365-366.
19. Gaudet A, Popovich P, Ramer M. 2011. Wallerian degeneration: gaining perspective on inflammatory events after peripheral nerve injury. J Neuroinflam 8:110.
20. George R, Griffin JW. 1994. Delayed macrophage responses and myelin clearance during Wallerian degeneration in the central nervous system: the dorsal radiculotomy model. Exp Neurol 129:225-236.
21. Gomez-Pinilla F, Zhuang Y, Feng J, Ying Z, Fan G. 2011. Exercise impacts brain-derived neurotrophic factor plasticity by engaging mechanisms of epigenetic regulation. Eur J Neurosci 33:383-390.
22. Gordon S. 2003. Alternative activation of macrophages. Nat Rev Immunol 3:23-35.
23. Gowing G, Philips T, Van Wijmeersch B, Audet JN, Dewil M, Van Den Bosch L, Billiau AD, Robberecht W, Julien JP. 2008. Ablation of proliferating microglia does not affect motor neuron degeneration in amyotrophic lateral sclerosis caused by mutant superoxide dismutase. J Neurosci 28:10234-10244.
24. Grider MH, Chen Q, Shine HD. 2006. Semi-automated quantification of axonal densities in labeled CNS tissue. J Neurosci Methods 155:172-179.
25. Grill RJ, Murai K, Blesch A, Gage FH, Tuszynski MH. 1997. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J Neurosci 17:5560-5572.
26. Hagg T. 2006. Collateral sprouting as a target for improved function after spinal cord injury. J Neurotrauma 23:281-294.
27. Hagg T, Baker KA, Emsley JG, Tetzlaff W. 2005. Prolonged local neurotrophin-3 infusion reduces ipsilateral collateral sprouting of spared corticospinal axons in adult rats. Neuroscience 130:875-887.
28. Hauben E, Butovsky O, Nevo U, Yoles E, Moalem G, Agranov E, Mor F, Leibowitz-Amit R, Pevsner E, Akselrod S, Neeman M, Cohen IR, Schwartz M. 2000. Passive or active immunization with myelin basic protein promotes recovery from spinal cord contusion. J Neurosci 20:6421-6430.
29. Hendrix S, Nitsch R. 2007. The role of T helper cells in neuroprotection and regeneration. J Neuroimmunol 184:100-112.
30. Jones TB, Basso DM, Sodhi A, Pan JZ, Hart RP, MacCallum RC, Lee S, Whitacre CC, Popovich PG. 2002. Pathological CNS autoimmune disease triggered by traumatic spinal cord injury: implications for autoimmune vaccine therapy. J Neurosci 22:2690-2700.
31. Kuang RZ, Kalil K. 1990. Specificity of corticospinal axon arbors sprouting into denervated contralateral spinal cord. J Comp Neurol 302:461-472.
32. Lee JK, Geoffroy CG, Chan AF, Tolentino KE, Crawford MJ, Leal MA, Kang B, Zheng B. 2010. Assessing spinal axon regeneration and sprouting in Nogo-, MAG-, and OMgp-deficient mice. Neuron 66:663-670.
33. Liu K, Lu Y, Lee JK, Samara R, Willenberg R, Sears-Kraxberger I, Tedeschi A, Park KK, Jin D, Cai B, Xu B, Connolly L, Steward O, Zheng B, He Z. 2010. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat Neurosci 13:1075-1081.
34. Moalem G, Leibowitz-Amit R, Yoles E, Mor F, Cohen IR, Schwartz M. 1999. Autoimmune T cells protect neurons from secondary degeneration after central nervous system axotomy. Nat Med 5:49-55.
35. Moalem G, Gdalyahu A, Shani Y, Otten U, Lazarovici P, Cohen IR, Schwartz M. 2000. Production of neurotrophins by activated T cells: implications for neuroprotective autoimmunity. J Autoimmun 15:331-345.
36. Moalem G, Xu K, Yu L. 2004. T lymphocytes play a role in neuropathic pain following peripheral nerve injury in rats. Neuroscience 129:767-777.
37. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates. San Diego: Academic Press.
38. Ponomarev ED, Maresz K, Tan Y, Dittel BN. 2007. CNS-derived interleukin-4 is essential for the regulation of autoimmune inflammation and induces a state of alternative activation in microglial cells. J Neurosci 27:10714-10721.
39. Popovich PG, Longbrake EE. 2008. Can the immune system be harnessed to repair the CNS? Nat Rev Neurosci 9:481-493.
40. Popovich PG, Wei P, Stokes BT. 1997. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J Comp Neurol 377:443-464.
41. Ririe KM, Rasmussen RP, Wittwer CT. 1997. Product differentiation by analysis of DNA melting curves during the polymerase chain reaction. Anal Biochem 245:154-160.
42. Rosenzweig ES, Courtine G, Jindrich DL, Brock JH, Ferguson AR, Strand SC, Nout YS, Roy RR, Miller DM, Beattie MiS, Havton LA, Bresnahan JC, Edgerton VR, Tuszynski MH. 2010. Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat Neurosci 13:1505-1510.
43. Roy A, Liu X, Pahan K. 2007. Myelin basic protein-primed T cells induce neurotrophins in glial cells via α5β3 integrin. J Biol Chem 282:32222-32232.
44. Sato Y, Nakajima S, Shiraga N, Atsumi H, Yoshida S, Koller T, Gerig G, Kikinis R. 1998. Three-dimensional multi-scale line filter for segmentation and visualization of curvilinear structures in medical images. Med Imag Anal 2:143-168.
45. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative Ct method. Nat Protoc 3:1101-1108.
46. + or B, lymphocytes mediate facial motoneuron survival after facial nerve transection. Brain Behav Immun 17:393-402.
47. Sicotte M, Tsatas O, Jeong SY, Cai CQ, He Z, David S. 2003. Immunization with myelin or recombinant Nogo-66/MAG in alum promotes axon regeneration and sprouting after corticospinal tract lesions in the spinal cord. Mol Cell Neurosci 23:251-263.
48. Skihar V, Silva C, Chojnacki A, Döring A, Stallcup WB, Weiss S, Yong VW. 2009. Promoting oligodendrogenesis and myelin repair using the multiple sclerosis medication glatiramer acetate. Ptoc Natl Acad Sci U S A 106:17992-17997.
49. Thallmair M, Metz GAS, 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.
50. Tuszynski MH, Grill R, Jones LL, Brant A, Blesch A, Low K, Lacroix S, Lu P. 2003. NT-3 gene delivery elicits growth of chronically injured corticospinal axons and modestly improves functional deficits after chronic scar resection. Exp Neurol 181:47-56.
51. Tzeng SF, Huang HY. 2003. Downregulation of inducible nitric oxide synthetase by neurotrophin-3 in microglia. J Cell Biochem 90:227-233.
52. Tzeng SF, Huang HY, Lee TI, Jwo JK. 2007. Inhibition of lipopolysaccharide-induced microglial activation by preexposure to neurotrophin-3. J Neurosci Res 81:666-667.
53. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:research0034.
54. Vargas ME, Barres BA. 2007. Why is Wallerian degeneration in the CNS so slow? Annu Rev Neurosci 30:153-179.
55. Vos JG, Kreeftenberg JG, Kruijt BC, Kruizinga W, Steerenberg P. 1980. The athymic nude rat: II. Immunological characteristics. Clin Immunol Immunopathol 15:229-237.
56. Wang L, Hu B, Wong WM, Lu P, Wu W, Xu XM. 2009. Glial and axonal responses in areas of Wallerian degeneration of the corticospinal and dorsal ascending tracts after spinal cord dorsal funiculotomy. Neuropathology 29:230-241.
57. Zhang J, Geula C, Lu C, Koziel H, Hatcher LM, Roisen FJ. 2003. Neurotrophins regulate proliferation and survival of two microglial cell lines in vitro. Exp Neurol 183:469-481.
58. Zhou L, Shine HD. 2003. Neurotrophic factors expressed in both cortex and spinal cord induce axonal plasticity after spinal cord injury. J Neurosci Res 74:221-226.
59. Zhou L, Baumgartner BJ, Hill-Felberg SJ, McGowen LR, Shine HD. 2003. Neurotrophin-3 expressed in situ induces axonal plasticity in the adult injured spinal cord. J Neurosci 23:1424-1431.