Modulation of gene expression during early stages of reconnection of the turtle spinal cord

Journal of Neurochemistry

Volumn 121, Issue 6, 2012, Pages 996-1006

  García, Gabriela ^a   Libisch, Gabriela ^b   Trujillo Cenóz, Omar ^a   Robello, Carlos ^b,c   Russo, Raúl E ^a  

^a INSTITUTO DE INVESTIGACIONES BIOLÓGICAS CLEMENTE ESTABLE   (Uruguay)

^b INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

^c DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

Author keywords

BLBP; Connexin 43; Pax6; Quantitative real time PCR; Regeneration; Spinal cord

Indexed keywords

BRAIN LIPID BINDING PROTEIN; CONNEXIN 43; HUB PROTEIN; LIPID BINDING PROTEIN; MESSENGER RNA; PROTEIN; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLBP GENE; CONTROLLED STUDY; CX43 GENE; GENE; GENE EXPRESSION PROFILING; HUB GENE; IMMUNOHISTOCHEMISTRY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PAX6 GENE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SPINAL CORD INJURY; SPINAL CORD REGENERATION; TURTLE;

AMINO ACID SEQUENCE; ANIMALS; EYE PROTEINS; GENE EXPRESSION PROFILING; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; PAIRED BOX TRANSCRIPTION FACTORS; REAL-TIME POLYMERASE CHAIN REACTION; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; SPINAL CORD; SPINAL CORD INJURIES; SPINAL CORD REGENERATION; TURTLES;

TESTUDINES; TRACHEMYS;

EID: 84862023389     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07750.x     Document Type: Article

References (55)

1. Anderson K. D., Morin M. A., Beckel-Mitchener A., Mobarak C. D., Neve R. L., Furneaux H. M., Burry R. and Perrone-Bizzozero N. I. (2000) Overexpression of HuD, but not of its truncated form HuD I+II, promotes GAP-43 gene expression and neurite outgrowth in PC12 cells in the absence of nerve growth factor. J. Neurochem. 75, 1103-1114. (Pubitemid 30660499)
2. Anderson K. D., Sengupta J., Morin M., Neve R. L., Valenzuela C. F. and Perrone-Bizzozero N. I. (2001) Overexpression of HuD accelerates neurite outgrowth and increases GAP-43 mRNA expression in cortical neurons and retinoic acid-induced embryonic stem cells in vitro. Exp. Neurol. 168, 250-258. (Pubitemid 32289761)
3. Anderson K. D., Merhege M. A., Morin M., Bolognani F. and Perrone-Bizzozero N. I. (2003) Increased expression and localization of the RNA-binding protein HuD and GAP-43 mRNA to cytoplasmic granules in DRG neurons during nerve regeneration. Exp. Neurol. 183, 100-108. (Pubitemid 37075860)
4. Anton E.S., Marchionni M. A., Lee K. F. and Rakic P. (1997) Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development 124, 3501-3510. (Pubitemid 27470034)
5. Arocho L. C., Figueroa J. D., Torrado A. I., Santiago J. M., Vera A. E. and Miranda J. D. (2011) Expression profile and role of EphrinA1 Ligand after spinal cord injury. Cell. Mol. Neurobiol. 31, 1057-1069.
6. Bel-Vialar S., Medevielle F. and Pituello F. (2007) The on/off of Pax6 controls the tempo of neuronal differentiation in the developing spinal cord. Dev. Biol. 305, 659-673. (Pubitemid 46686604)
7. Benraiss A., Arsanto J. P., Coulon J. and Thouveny Y. (1999) Neurogenesis during caudal spinal cord regeneration in adult newts. Dev. Genes. Evol. 209, 363-369. (Pubitemid 29261503)
8. Bruzzone R. and Dermietzel R. (2006) Structure and function of gap junctions in the developing brain. Cell Tissue Res. 326, 239-248. (Pubitemid 44435805)
9. Buffo A. (2007) Fate determinant expression in the lesioned brain: Olig2 induction and its implications for neuronal repair. Neurodegener. Dis. 4, 328-332.
10. Cheng A., Tang H., Cai J., Zhu M., Zhang X., Rao M. and Mattson M. P. (2004) Gap junctional communication is required to maintain mouse cortical neural progenitor cells in a proliferative state. Dev. Biol. 272, 203-216. (Pubitemid 38887295)
11. Courtès S., Vernerey J., Pujadas L., Magalon K., Cremer H., Soriano E., Durbec P. and Cayre M. (2011) Reelin controls progenitor cell migration in the healthy and pathological adult mouse brain. PLoS ONE 6, e20430.
12. Cronin M., Anderson P. N., Cook J. E., Green C. R. and Becker D. L. (2008) Blocking connexin43 expression reduces inflammation and improves functional recovery after spinal cord injury. Mol. Cell. Neurosci. 39, 152-160.
13. Duval N., Gomes D., Calaora V., Calabrese A., Meda P. and Bruzzone R. (2002) Cell coupling and Cx43 expression in embryonic mouse neural progenitor cells. J. Cell Sci. 115, 3241-3251. (Pubitemid 34960177)
14. Feng L., Hatten M. E. and Heintz N. (1994) Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12, 895-908. (Pubitemid 24126249)
15. Frantseva M. V., Kokarovtseva L., Naus C. G., Carlen P. L., MacFabe D. and Perez Velazquez J. L. (2002a) Specific gap junctions enhance the neuronal vulnerability to brain traumatic injury. J. Neurosci. 22, 644-653. (Pubitemid 34141745)
16. Frantseva M. V., Kokarovtseva L. and Perez Velazquez J. L. (2002b) Ischemia-induced brain damage depends on specific gap-junctional coupling. J. Cereb. Blood Flow Metab. 22, 453-62. (Pubitemid 34273601)
17. Fujiyoshi T., Kubo T., Chan C. C., Koda M., Okawa A., Takahashi K. and Yamazaki M. (2010) Interferon-c decreases chondroitin sulfate proteoglycan expression and enhances hindlimb function after spinal cord injury in mice. J.Neurotrauma 27, 2283-94.
18. Garré J. M., Retamal M. A., Cassina P., Barbeito L., Bukauskas F. F., Sáez J. C., Bennett M. V. and Abudara V. (2010) FGF-1 induces ATP release from spinal astrocytes in culture and opens pannexin and connexinhemichannels. PNAS 107, 22659-22664.
19. Haunerland N. H. and Spener F. (2004) Fatty acid-binding proteins-insights from genetic manipulations. Prog. Lipid Res. 43, 328-349. (Pubitemid 38952618)
20. Heins N., Malatesta P., Cecconi F., Nakafuku M., Tucker K. L., Hack M. A., Chapouton P., Barde Y. A. and Götz M. (2002) Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci. 5, 308-315. (Pubitemid 34279810)
21. Hinman M. N. and Lou H. (2008) Diverse molecular functions of Hu proteins. Cell. Mol. Life Sci. 65, 3168-3181.
22. Kohwi M., Osumi N., Rubenstein J. L. and Alvarez-Buylla A. (2005) Pax6 is required for making specific subpopulations of granule and periglomerularneurons in the olfactory bulb. J. Neurosci. 25, 6997-7003. (Pubitemid 41077007)
23. Kuo H. S., Tsai M. J., Huang M. C., Chiu C. W., Tsai C. Y., Lee M. J., Huang W. C., Lin Y. L., Kuo W. C. and Cheng H. (2011) Acid fibroblast growth factor and peripheral nerve grafts regulate Th2 cytokine expression, macrophage activation, polyamine synthesis, and neurotrophin expression in transected rat spinal cords. J. Neurosci. 31, 4137-4147.
24. Lee S. K. and Pfaff S. L. (2001) Transcriptional networks regulating neuronal identity in the developing spinal cord. Nat. Neurosci. 4, 1183-1191.
25. Lee I. H., Lindqvist E., Kiehn O., Widenfalk J. and Olson L. (2005) Glial and neuronal connexin expression patterns in the rat spinal cord during development and following injury. J. Comp. Neurol. 489, 1-10. (Pubitemid 40934669)
26. Maekawa M., Takashima N., Arai Y., Nomura T., Inokuchi K., Yuasa S. and Osumi N. (2005) Pax6 is required for production and maintenance of progenitor cells in postnatal hippocampal neurogenesis. Genes Cells 10, 1001-1014. (Pubitemid 41404009)
27. Marusich M. F., Furneaux H. M., Henion P. D. and Weston J. A. (1994) Hu neuronal proteins are expressed in proliferating neurogenic cells. J. Neurobiol. 25, 143-155. (Pubitemid 24029380)
28. Meletis K., Barnabé-Heider F., Carlen M., Evergren E., Tomilin N., Shupliakov O. and Frisén J. (2008) Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol. 6, e182.
29. Monaghan J. R., Walker J. A., Page R. B., Putta S., Beachy C. K. and Voss S. R. (2007) Early gene expression during natural spinal cord regeneration in the salamander Ambystomamexicanum. J. Neurochem. 101, 27-40. (Pubitemid 46426468)
30. Mothe A. J. and Tator C. H. (2005) Proliferation, migration, and differentiation of endogenous ependymal region stem/progenitor cells following minimal spinal cord injury in the adult rat. Neuroscience 131, 177-187. (Pubitemid 40170498)
31. Mountcastle V.B. (1980). Effects of spinal transection, in: Medical physiology V1 (Mountcastle V. B., ed), pp. 781-785. CV Mosby Company, St. Louis, MO, USA.
32. Nakase T., Söhl G., Theis M., Willecke K. and Naus C. C. (2004) Increased apoptosis and inflammation after focal brain ischemia in mice lacking connexin43 in astrocytes. Am. J. Pathol. 164, 2067-2075. (Pubitemid 38669354)
33. Nash B., Thomson C. E., Linington C., Arthur A. T., McClure J. D., McBride M. W. and Barnett S. C. (2011) Functional duality of astrocytes in myelination. J. Neurosci. 31, 13028-13038.
34. O'Carroll S. J., Alkadhi M., Nicholson L. F. and Green C. R. (2008) Connexin 43 mimetic peptides reduce swelling, astrogliosis, and neuronal cell death after spinal cord injury. Cell. Commun. Adhes. 15, 27-42.
35. Okano H. J. and Darnell R. B. (1997) A hierarchy of Hu RNA binding proteins indevelopingandadultneurons. J. Neurosci.17,3024-3037. (Pubitemid 27175816)
36. Parker T. J. and Harwell W. A. (1949) A text-book of zoology. MacMillan and Co., London.
37. Peng W., Cotrina M. L., Han X., Yu H., Bekar L., Blum L., Takano T., Tian G. F., Goldman S. A. and Nedergaard M. (2009) Systemic administration of an antagonist of the ATP-sensitive receptor P2X7 improves recovery after spinal cord injury. PNAS 106, 12489-12493.
38. Pinto L. and Götz M. (2007) Radial glial cell heterogeneity - the source of diverse progeny in the CNS. Prog. Neurobiol. 83, 2-23. (Pubitemid 47241312)
39. Profyris C., Cheema S. S., Zang D., Azari M. F., Boyle K. and Petratos S. (2004) Degenerative and regenerative mechanisms governing spinal cord injury. Neurobiol. Dis. 15, 415-436. (Pubitemid 38429958)
40. Quattrone A., Pascale A., Nogues X., Zhao W., Gusev P., Pacini A. and Alkon D. L. (2001) Posttranscriptional regulation of gene expression in learning by the neuronal ELAV-like mRNA-stabilizing proteins. PNAS 98, 11668-11673. (Pubitemid 32928786)
41. Rehermann M. I., Marichal N., Russo R. E. and Trujillo-Cenóz O. (2009) Neural reconnection in the transected spinal cord of the freshwater turtle Trachemys dorbignyi. J. Comp. Neurol. 515, 197-214.
42. Rehermann M. I., Santiñaque F., López-Carro B., Russo R. E. and Trujillo-Cenóz O. (2011) Cell proliferation and cytoarchitectural remodeling during spinal cord reconnection in the fresh-water turtle Trachemys dorbignyi. Cell Tissue Res. 344, 415-433.
43. Reimer M. M., Sörensen I., Kuscha V., Frank R. E., Liu C., Becker C. and Becker T. (2008) Motor neuron regeneration in adult zebrafish. J. Neurosci. 28, 8510-8516.
44. Russo R. E., Reali C., Radmilovich M., Fernández A. and Trujillo-Cenóz O. (2008) Connexin 43 delimits functional domains of neurogenic precursors in the spinal cord. J. Neurosci. 28, 3298-3309. (Pubitemid 351469315)
45. Siushansian R., Bechberger J. F., Cechetto D. F., Hachinski V. C. and Naus C. C. (2001) Connexin43 null mutation increases infarct size after stroke. J Comp Neurol. 440, 387-394. (Pubitemid 33041752)
46. Stensaas L. J. (1983) Regeneration in the spinal cord of the newt Notopthalmus (Triturus) pyrrhogaster, in Spinal cord reconstruction (Kao C.C., Bunge R.P. and Reier P.J., eds), pp. 121-149. Raven, New York.
47. Tanaka E. M. and Ferretti P. (2009) Considering the evolution of regeneration in the central nervous system. Nat. Rev. Neurosci. 10, 713-723.
48. Thuret S., Moon L. D. and Gage F. H. (2006) Therapeutic interventions after spinal cord injury. Nat. Rev. Neurosci. 7, 628-643. (Pubitemid 44106745)
49. Trujillo-Cenóz O., Fernández A., Radmilovich M., Reali C. and Russo R. E. (2007) Cytological organization of the central gelatinosa in the turtle spinal cord. J. Comp. Neurol. 502, 291-308. (Pubitemid 46595400)
50. Tysseling V.M., Mithal D., Sahni V., Birch D., Jung H., Belmadani A., Miller R.J. and Kessler J.A. (2011) SDF1 in the dorsal corticospinal tract promotes CXCR4 + cell migration after spinal cord injury. J. Neuroinflammation. 8, 16.
51. Vance J. A., Campenot R. B. and Vance D. E. (2010) The synthesis and transport of lipids for axonal growth and nerve regeneration. Biochim. Biophys. Acta 1486, 84-96.
52. Velardo M. J., Burger C., Williams P. R., Baker H. V., López M. C., Mareci T. H., White T. E., Muzyczka N. and Reier P. J. (2004) Patterns of Gene Expression Reveal a Temporally Orchestrated Wound Healing Response in the Injured Spinal Cord. J. Neurosci. 24, 8562-8576. (Pubitemid 39313779)
53. White R. E., McTigue D. M. and Jakeman L. B. (2010) Regional heterogeneity in astrocyte responses following contusive spinal cord injury in mice. J. Comp. Neurol. 518, 1370-1390.
54. Wu X., Yoo S. and Wrathall J. R. (2005) Real-time quantitative PCR analysis of temporal-spatial alterations in gene expression after spinal cord contusion. J. Neurochem. 93, 943-952. (Pubitemid 40695753)
55. Yamamoto S., Nagao M., Sugimori M. et al. (2001) Transcription factor expression and Notchdependent regulation of neural progenitors in the adult rat spinal cord. J. Neurosci. 21, 9814-9823. (Pubitemid 34184066)