Axonal regeneration after spinal cord injury in zebrafish and mammals: Differences, similarities, translation

Neuroscience Bulletin

Volumn 29, Issue 4, 2013, Pages 402-410

  Vajn, Katarina ^a   Plunkett, Jeffery A ^c   Tapanes Castillo, Alexis ^c   Oudega, Martin ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b University of Pittsburgh   (United States)

^c ST THOMAS UNIVERSITY   (United States)

Author keywords

axonal regeneration; functional recovery; growth inhibition; spinal cord injury; zebrafish

Indexed keywords

ATI 355; AXONIN 1; CHONDROITIN ABC LYASE; CYSTEINE AND GLYCINE RICH PROTEIN 1A; LUNG RESISTANCE PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA; MICRORNA 133B; MYELIN ASSOCIATED GLYCOPROTEIN; NERVE CELL ADHESION MOLECULE L1; NEUROMODULIN; NOGO A ANTIBODY; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN NOGO A; PROTEOCHONDROITIN SULFATE; SUPPRESSOR OF CYTOKINE SIGNALING 3; UNCLASSIFIED DRUG;

ASTROCYTE; HUMAN; LOCOMOTION; MAMMAL; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE GRAFT; NERVE SPROUTING; NONHUMAN; REVIEW; SCHWANN CELL; SPINAL CORD INJURY; SPINAL CORD TRANSSECTION; ZEBRA FISH;

ANIMALS; AXONS; MAMMALS; NERVE REGENERATION; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; ZEBRAFISH;

EID: 84881172973     PISSN: 16737067     EISSN: 19958218     Source Type: Journal    
DOI: 10.1007/s12264-013-1361-8     Document Type: Review

References (63)

1. Schwab ME, Bartholdi D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev 1996, 76: 319-370.
2. Cao HQ, Dong ED. An update on spinal cord injury research. Neurosci Bull 2013, 29: 94-102.
3. Becker T, Wullimann MF, Becker CG, Bernhardt RR, Schachner M. Axonal regrowth after spinal cord transection in adult zebrafish. J Comp Neurol 1997, 377: 577-595.
4. Hui SP, Dutta A, Ghosh S. Cellular response after crush injury in adult zebrafish spinal cord. Dev Dyn 2010, 239: 2962-2979.
5. ten Donkelaar HJ. Development and regenerative capacity of descending supraspinal pathways in tetrapods: a comparative approach. Adv Anat Embryol Cell Biol 2000, 154: iii-ix, 1-145.
6. Becker CG, Becker T (eds). Model organisms in Spinal Cord Regeneration. 1st ed. Weinheim, Germany: Wiley-VCH Verlag GmbH, 2007.
7. Hui SP, Monaghan JR, Voss SR, Ghosh S. Expression pattern of Nogo-A, MAG, and NgR in regenerating urodele spinal cord. Dev Dyn 2013, 242(7): 847-860.
8. Becker T, Bernhardt RR, Reinhard E, Wullimann MF, Tongiorgi E, Schachner M. Readiness of zebrafish brain neurons to regenerate a spinal axon correlates with differential expression of specific cell recognition molecules. J Neurosci 1998, 18: 5789-5803.
9. Becker CG, Lieberoth BC, Morellini F, Feldner J, Becker T, Schachner M. L1.1 is involved in spinal cord regeneration in adult zebrafish. J Neurosci 2004, 24: 7837-7842.
10. Becker T, Lieberoth BC, Becker CG, Schachner M. Differences in the regenerative response of neuronal cell populations and indications for plasticity in intraspinal neurons after spinal cord transection in adult zebrafish. Mol Cell Neurosci 2005, 30: 265-278.
11. Mei F, Christin Chong SY, Chan JR. Myelin-based inhibitors of oligodendrocyte myelination: clues from axonal growth and regeneration. Neurosci Bull 2013, 29: 177-188.
12. Shen Y, Tenney AP, Busch SA, Horn KP, Cuascut FX, Liu K, et al. PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 2009, 326: 592-596.
13. Fisher D, Xing B, Dill J, Li H, Hoang HH, Zhao Z, et al. Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors. J Neurosci 2011, 31: 14051-14066.
14. Garcia-Alias G, Fawcett JW. Training and anti-CSPG combination therapy for spinal cord injury. Exp Neurol 2012, 235: 26-32.
15. Oudega M, Chao OY, Avison DL, Bronson RT, Buchser WJ, Hurtado A, et al. Systemic administration of a deoxyribozyme to xylosyltransferase-1 mRNA promotes recovery after a spinal cord contusion injury. Exp Neurol 2012, 237: 170-179.
16. Galtrey CM, Kwok JC, Carulli D, Rhodes KE, Fawcett JW. Distribution and synthesis of extracellular matrix proteoglycans, hyaluronan, link proteins and tenascin-R in the rat spinal cord. Eur J Neurosci 2008, 27: 1373-1390.
17. Snow DM, Letourneau PC. Neurite outgrowth on a step gradient of chondroitin sulfate proteoglycan (CS-PG). J Neurobiol 1992, 23: 322-336.
18. Goldshmit Y, Sztal TE, Jusuf PR, Hall TE, Nguyen-Chi M, Currie PD. Fgf-dependent glial cell bridges facilitate spinal cord regeneration in zebrafish. J Neurosci 2012, 32: 7477-7492.
19. Becker CG, Becker T. Repellent guidance of regenerating optic axons by chondroitin sulfate glycosaminoglycans in zebrafish. J Neurosci 2002, 22: 842-853.
20. Oertle T, van der Haar ME, Bandtlow CE, Robeva A, Burfeind P, Buss A, et al. Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J Neurosci 2003, 23: 5393-5406.
21. Huber AB, Weinmann O, Brosamle C, Oertle T, Schwab ME. Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions. J Neurosci 2002, 22: 3553-3567.
22. Pernet V, Schwab ME. The role of Nogo-A in axonal plasticity, regrowth and repair. Cell Tissue Res 2012, 349: 97-104.
23. Brosamle C, Halpern ME. Nogo-Nogo receptor signalling in PNS axon outgrowth and pathfinding. Mol Cell Neurosci 2009, 40: 401-409.
24. Gonzenbach RR, Schwab ME. Disinhibition of neurite growth to repair the injured adult CNS: focusing on Nogo. Cell Mol Life Sci 2008, 65: 161-176.
25. Oudega M, Rosano C, Sadi D, Wood PM, Schwab ME, Hagg T. Neutralizing antibodies against neurite growth inhibitor NI-35/250 do not promote regeneration of sensory axons in the adult rat spinal cord. Neuroscience 2000, 100: 873-883.
26. Abdesselem H, Shypitsyna A, Solis GP, Bodrikov V, Stuermer CA. No Nogo66- and NgR-mediated inhibition of regenerating axons in the zebrafish optic nerve. J Neurosci 2009, 29: 15489-15498.
27. Schnaar RL, Lopez PH. Myelin-associated glycoprotein and its axonal receptors. J Neurosci Res 2009, 87: 3267-3276.
28. Mehta NR, Lopez PH, Vyas AA, Schnaar RL. Gangliosides and Nogo receptors independently mediate myelinassociated glycoprotein inhibition of neurite outgrowth in different nerve cells. J Biol Chem 2007, 282: 27875-27886.
29. Venkatesh K, Chivatakarn O, Sheu SS, Giger RJ. Molecular dissection of the myelin-associated glycoprotein receptor complex reveals cell type-specific mechanisms for neurite outgrowth inhibition. J Cell Biol 2007, 177: 393-399.
30. Lehmann F, Gathje H, Kelm S, Dietz F. Evolution of sialic acid-binding proteins: molecular cloning and expression of fish siglec-4. Glycobiology 2004, 14: 959-968.
31. Chen Z, Lee H, Henle SJ, Cheever TR, Ekker SC, Henley JR. Primary neuron culture for nerve growth and axon guidance studies in zebrafish (Danio rerio). PLoS one 2013, 8: e57539.
32. Viljetic B, Labak I, Majic S, Stambuk A, Heffer M. Distribution of mono-, di- and trisialo gangliosides in the brain of Actinopterygian fishes. Biochim Biophys Acta 2012, 1820: 1437-1443.
33. Lee JK, Geoffroy CG, Chan AF, Tolentino KE, Crawford MJ, Leal MA, et al. Assessing spinal axon regeneration and sprouting in Nogo-, MAG-, and OMgp-deficient mice. Neuron 2010, 66: 663-670.
34. Rossi F, Jankovski A, Sotelo C. Differential regenerative response of Purkinje cell and inferior olivary axons confronted with embryonic grafts: environmental cues versus intrinsic neuronal determinants. J Comp Neurol 1995, 359: 663-677.
35. Vaudano E, Campbell G, Hunt SP, Lieberman AR. Axonal injury and peripheral nerve grafting in the thalamus and cerebellum of the adult rat: upregulation of c-jun and correlation with regenerative potential. Eur J Neurosci 1998, 10: 2644-2656.
36. Benowitz LI, Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci 1997, 20: 84-91.
37. Zhang Y, Campbell G, Anderson PN, Martini R, Schachner M, Lieberman AR. Molecular basis of interactions between regenerating adult rat thalamic axons and Schwann cells in peripheral nerve grafts i. Neural cell adhesion molecules. J Comp Neurol 1995, 361: 193-209.
38. Kamiguchi H, Hlavin ML, Lemmon V. Role of L1 in neural development: what the knockouts tell us. Mol Cell Neurosci 1998, 12: 48-55.
39. Ma L, Yu YM, Guo Y, Hart RP, Schachner M. Cysteine- and glycine-rich protein 1a is involved in spinal cord regeneration in adult zebrafish. Eur J Neurosci 2012, 35: 353-365.
40. McCurley AT, Callard GV. Time course analysis of gene expression patterns in zebrafish eye during optic nerve regeneration. J Exp Neurosci 2010, 2010: 17-33.
41. Tran TC, Singleton C, Fraley TS, Greenwood JA. Cysteinerich protein 1 (CRP1) regulates actin filament bundling. BMC Cell Biol 2005, 6: 45.
42. Ma L, Greenwood JA, Schachner M. CRP1, a protein localized in filopodia of growth cones, is involved in dendritic growth. J Neurosci 2011, 31: 16781-16791.
43. Stoeckli ET, Kuhn TB, Duc Co, Ruegg MA, Sonderegger P. The axonally secreted protein axonin-1 is a potent substratum for neurite growth. J Cell Biol 1991, 112: 449-455.
44. Wolfer DP, Giger RJ, Stagliar M, Sonderegger P, Lipp HP. Expression of the axon growth-related neural adhesion molecule TAG-1/axonin-1 in the adult mouse brain. Anat Embryol (Berl) 1998, 197: 177-185.
45. Lin JF, Pan HC, Ma LP, Shen YQ, Schachner M. The cell neural adhesion molecule contactin-2 (TAG-1) is beneficial for functional recovery after spinal cord injury in adult zebrafish. PLoS One 2012, 7 (12): e52376.
46. Smith PD, Sun F, Park KK, Cai B, Wang C, Kuwako K, et al. SoCS3 deletion promotes optic nerve regeneration in vivo. Neuron 2009, 64: 617-623.
47. Park KK, Liu K, Hu Y, Smith PD, Wang C, Cai B, et al. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mToR pathway. Science 2008, 322: 963-966.
48. Liu K, Lu Y, Lee JK, Samara R, Willenberg R, Sears-Kraxberger I, et al. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat Neurosci 2010, 13: 1075-1081.
49. Abe N, Borson SH, Gambello MJ, Wang F, Cavalli V. Mammalian target of rapamycin (mToR) activation increases axonal growth capacity of injured peripheral nerves. J Biol Chem 2010, 285: 28034-28043.
50. Chugani DC, Rome LH, Kedersha NL. Evidence that vault ribonucleoprotein particles localize to the nuclear pore complex. J Cell Sci 1993, 106(Pt 1): 23-29.
51. Pan HC, Lin JF, Ma LP, Shen YQ, Schachner M. Major vault protein promotes locomotor recovery and regeneration after spinal cord injury in adult zebrafish. Eur J Neurosci 2013, 37: 203-211.
52. Komori N, Takemori N, Kim HK, Singh A, Hwang SH, Foreman RD, et al. Proteomics study of neuropathic and nonneuropathic dorsal root ganglia: altered protein regulation following segmental spinal nerve ligation injury. Physiol Genomics 2007, 29: 215-230.
53. Li JY, Volknandt W, Dahlstrom A, Herrmann C, Blasi J, Das B, et al. Axonal transport of ribonucleoprotein particles (vaults). Neuroscience 1999, 91: 1055-1065.
54. Steiner E, Holzmann K, Pirker C, Elbling L, Micksche M, Sutterluty H, et al. The major vault protein is responsive to and interferes with interferon-gamma-mediated STAT1 signals. J Cell Sci 2006, 119: 459-469.
55. Minaguchi T, Waite KA, Eng C. Nuclear localization of PTEN is regulated by Ca(2+) through a tyrosil phosphorylation-independent conformational modification in major vault protein. Cancer Res 2006, 66: 11677-11682.
56. Yu YM, Gibbs KM, Davila J, Campbell N, Sung S, Todorova TI, et al. MicroRNA miR-133b is essential for functional recovery after spinal cord injury in adult zebrafish. Eur J Neurosci 2011, 33: 1587-1597.
57. Liu NK, Wang XF, Lu QB, Xu XM. Altered microRNA expression following traumatic spinal cord injury. Exp Neurol 2009, 219: 424-429.
58. Carè A, Catalucci D, Felicetti F, Bonci D, Addario A, Gallo P, et al. MicroRNA-133 controls cardiac hypertrophy. Nat Med 2007, 13: 613-618.
59. Dong DL, Chen C, Huo R, Wang N, Li Z, Tu YJ, et al. Reciprocal repression between microRNA-133 and calcineurin regulates cardiac hypertrophy: a novel mechanism for progressive cardiac hypertrophy. Hypertension 2010, 55: 946-952.
60. Xu C, Lu Y, Pan Z, Chu W, Luo X, Lin H, et al. The musclespecific microRNAs miR-1 and miR-133 produce opposing effects on apoptosis by targeting HSP60, HSP70 and caspase-9 in cardiomyocytes. J Cell Sci 2007, 120: 3045-3052.
61. McKerracher L, Ferraro GB, Fournier AE. Rho signaling and axon regeneration. int Rev Neurobiol 2012, 105: 117-140.
62. Diaz-Ruiz A, Vergara P, Perez-Severiano F, Segovia J, Guizar-Sahagún G, Ibarra A, et al. Cyclosporin-A inhibits constitutive nitric oxide synthase activity and neuronal and endothelial nitric oxide synthase expressions after spinal cord injury in rats. Neurochem Res 2005, 30: 245-251.
63. Colak A, Karaoǧlan A, Barut S, Köktürk S, Akyildiz AI, Taşyürekli M. Neuroprotection and functional recovery after application of the caspase-9 inhibitor z-LEHD-fmk in a rat model of traumatic spinal cord injury. J Neurosurg Spine 2005, 2: 327-334.