Mechanisms of spinal cord injury regeneration in zebrafish: a systematic review

Document Type: Review Article

Authors

1 Medical Student, Iran University of Medical Sciences, Sina Trauma and Surgery Research Center, Tehran, Iran

2 Iran University of Medical Sciences, Sina Trauma and Surgery Research Center, Tehran, Iran

3 Tabriz University of Medical Sciences, Tabriz, Iran

4 Sina Trauma and Surgery Research Center, Tehran University of Medical Sciences, Tehran, 11365-3876, Iran

Abstract

Objective(s):To determine the molecular and cellular mechanisms of spinal cord regeneration in zebrafish.
Materials and Methods: Medical databases of PubMed and Scopus were searched with following key words: Zebrafish; spinal cord injuries; regeneration; recovery of function. The map of mechanisms was performed using Xmind software.
Results: Wnt/ß-catenin signaling, L1.1, L1.2, Major vault protein (MVP), contactin-2 and High mobility group box1 (HMGB1) had positive promoting effects on axonal re-growth while Ptena had an inhibitory effect. Neurogenesis is stimulated by Wnt/ß-catenin signaling as well as HMGB1, but inhibited by Notch signaling. Glial cells proliferate in response to fibroblast growth factor (fgf) signaling and Lysophosphatidic acid (LPA). Furthermore, fgf signaling pathway causes glia bridge formation in favor of axonal regeneration. LPA and HMGB1 in acute phase stimulate inflammatory responses around injury and suppress regeneration. LPA also induces microglia activation and neuronal death in addition to glia cell proliferation, but prevents neurite sprouting.
Conclusion: This study provides a comprehensive review of the known molecules and mechanisms in the current literature involved in the spinal cord injury (SCI) regeneration in zebrafish, in a time course manner. A better understanding of the whole determining mechanisms for the SCI regeneration should be considered as a main goal for future studies.

Keywords


1. Pinto L, Gotz M. Radial glial cell heterogeneity--the source of diverse progeny in the CNS. Prog Neurobiol 2007; 83:2-23.

2. Rahimi-Movaghar V, Yazdi A, Karimi M, Mohammadi M, Firouzi M, Zanjani LO, et al. Effect of decompression on complete spinal cord injury in rats. International Journal of Neuroscience 2008; 118:1359-1373.

3. Rahimi-Movaghar V, Vaccaro AR, Mohammadi M. Efficacy of surgical decompression in regard to motor recovery in the setting of conus medullaris injury. J Spinal Cord Med 2006; 29:32-38.

4. Rahimi-Movaghar V, Saadat S, Vaccaro AR, Ghodsi SM, Samadian M, Sheykhmozaffari A, et al. The efficacy of surgical decompression before 24 hours versus 24 to 72 hours in patients with spinal cord injury from T1 to L1–with specific consideration on ethics: a randomized controlled trial. Trials 2009; 10:77.

5. Rahimi-Movaghar V, Sayyah MK, Akbari H, Khorramirouz R, Rasouli MR, Moradi-Lakeh M, et al. Epidemiology of traumatic spinal cord injury in developing countries: a systematic review. Neuroepidemiology 2013; 41:65-85.

6. Becker CG, Becker T. Zebrafish as a model system for successful spinal cord regeneration.  Model organisms in spinal cord regeneration: John Wiley and Sons; 2007. 289-319.

7. Briona LK, Poulain FE, Mosimann C, Dorsky RI. Wnt/ß-catenin signaling is required for radial glial neurogenesis following spinal cord injury. Dev Biol 2015; 403:15-21.

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. Briona LK, Poulain FE, Mosimann C, Dorsky RI. Wnt/ss-catenin signaling is required for radial glial neurogenesis following spinal cord injury. Dev Biol 2015; 403:15-21.

10. Fleisch VC, Fraser B, Allison WT. Investigating regeneration and functional integration of CNS neurons: Lessons from zebrafish genetics and other fish species. Biochim Biophys Acta 2011; 1812:364-380.

11. Wang Z, Reynolds A, Kirry A, Nienhaus C, Blackmore MG. Overexpression of Sox11 promotes corticospinal tract regeneration after spinal injury while interfering with functional recovery. J Neurosci 2015; 35:3139-3145.

12. Yu YM, Cristofanilli M, Valiveti A, Ma L, Yoo M, Morellini F, et al. The extracellular matrix glycoprotein tenascin-C promotes locomotor recovery after spinal cord injury in adult zebrafish. Neuroscience 2011; 183:238-250.

13. Panic N, Leoncini E, de Belvis G, Ricciardi W, Boccia S. Evaluation of the endorsement of the preferred reporting items for systematic reviews and meta-analysis (PRISMA) statement on the quality of published systematic review and meta-analyses. PLoS One 2013; 8:e83138.

14. Hassannejad Z, Sharif-Alhoseini M, Shakouri-Motlagh A, Vahedi F, Zadegan SA, Mokhatab M, et al. Potential variables affecting the quality of animal studies regarding pathophysiology of traumatic spinal cord injuries. Spinal Cord 2015.

15. Barreiro-Iglesias A, Mysiak KS, Scott AL, Reimer MM, Yang Y, Becker CG, et al. Serotonin promotes development and regeneration of spinal motor neurons in zebrafish. Cell Rep. 2015; 13:924-932.

16. 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.

17. Becker T, Becker CG. Regenerating descending axons preferentially reroute to the gray matter in the presence of a general macrophage/microglial reaction caudal to a spinal transection in adult zebrafish. J Comp Neurol 2001; 433:131-147.

18. Bormann P, Roth LWA, Andel D, Ackermann M, Reinhard E. zfNLRR, a novel leucine-rich repeat protein is preferentially expressed during regeneration in zebrafish. Mol Cell Neurosci 1999; 13:167-179.

19. Briona LK, Dorsky RI. Radial glial progenitors repair the zebrafish spinal cord following transection. Exp Neurol 2014; 256:81-92.

20. Chen T, Yu Y, Hu C, Schachner M. L1.2, the zebrafish paralog of L1.1 and ortholog of the mammalian cell adhesion molecule L1 contributes to spinal cord regeneration in adult zebrafish. Restor Neurol Neurosci 2016; 34:325-335.

21. Dias TB, Yang YJ, Ogai K, Becker T, Becker CG. Notch signaling controls generation of motor neurons in the lesioned spinal cord of adult zebrafish. J Neurosci 2012; 32:3245-3252.

22. Fang P, Pan HC, Lin SL, Zhang WQ, Rauvala H, Schachner M, et al. HMGB1 contributes to regeneration after spinal cord injury in adult zebrafish. Mol Neurobiol 2014; 49:472-483.

23. Goldshmit Y, Matteo R, Sztal T, Ellett F, Frisca F, Moreno K, et al. Blockage of lysophosphatidic acid signaling improves spinal cord injury outcomes. Am J Pathol 2012; 181:978-992.

24. 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.

25. Guo Y, Ma L, Cristofanilli M, Hart RP, Hao A, Schachner M. Transcription factor Sox11b is involved in spinal cord regeneration in adult zebrafish. Neuroscience 2011; 172:329-341.

26. Hui SP, Nag TC, Ghosh S. Characterization of proliferating neural progenitors after spinal cord injury in adult zebrafish. PLoS One 2015; 10:e0143595.

27. Hui SP, Dutta A, Ghosh S. Cellular response after crush injury in adult zebrafish spinal cord. Dev Dyn 2010; 239:2962-2979.

28. Kuscha V, Barreiro-Iglesias A, Becker CG, Becker T. Plasticity of tyrosine hydroxylase and serotonergic systems in the regenerating spinal cord of adult zebrafish. J Comp Neurol 2012; 520:933-951.

29. Kuscha V, Frazer SL, Dias TB, Hibi M, Becker T, Becker CG. Lesion-induced generation of interneuron cell types in specific dorsoventral domains in the spinal cord of adult zebrafish. J Comp Neurol 2012; 520:3604-3616.

30. 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:e52376.

31. Liu D, Yu Y, Schachner M. Ptena, but not Ptenb, reduces regeneration after spinal cord injury in adult zebrafish. Exp Neurol 2014; 261:196-205.

32. Ma L, Shen YQ, Khatri HP, Schachner M. The asparaginyl endopeptidase legumain is essential for functional recovery after spinal cord injury in adult zebrafish. PLoS One 2014; 9:e95098.

33. 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.

34. Ogai K, Nakatani K, Hisano S, Sugitani K, Koriyama Y, Kato S. Function of Sox2 in ependymal cells of lesioned spinal cords in adult zebrafish. Neurosci Res 2014; 88:84-87.

35. Ogai K, Hisano S, Mawatari K, Sugitani K, Koriyama Y, Nakashima H, et al. Upregulation of anti-apoptotic factors in upper motor neurons after spinal cord injury in adult zebrafish. Neurochem Int 2012; 61:1202-1211.

36. 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.

37. Reimer MM, Kuscha V, Wyatt C, Sorensen I, Frank RE, Knuwer M, et al. Sonic hedgehog is a polarized signal for motor neuron regeneration in adult zebrafish. J Neurosci 2009; 29:15073-15082.

38. Reimer MM, Sorensen I, Kuscha V, Frank RE, Liu C, Becker CG, et al. Motor neuron regeneration in adult zebrafish. J Neurosci 2008; 28:8510-8516.

39. Schweitzer J, Gimnopoulos D, Lieberoth BC, Pogoda HM, Feldner J, Ebert A, et al. Contactin1a expression is associated with oligodendrocyte differentiation and axonal regeneration in the central nervous system of zebrafish. Mol Cell Neurosci 2007; 35:194-207.

40. Schweitzer J, Becker T, Becker CG, Schachner M. Expression of protein zero is increased in lesioned axon pathways in the central nervous system of adult zebrafish. GLIA 2003; 41:301-317.

41. Vajn K, Plunkett JA, Tapanes-Castillo A, Oudega M. Axonal regeneration after spinal cord injury in zebrafish and mammals: differences, similarities, translation. Neurosci Bull 2013; 29:402-410.

42. Yu Y, Schachner M. Syntenin-a promotes spinal cord regeneration following injury in adult zebrafish. Eur J Neurosci 2013; 38:2280-2289.

43. 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.