Genome wide expression profiling during spinal cord regeneration identifies comprehensive cellular responses in zebrafish

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Hui, Subhra Prakash ^a,d   Sengupta, Dhriti ^a   Lee, Serene Gek Ping ^b   Sen, Triparna ^c,e   Kundu, Sudip ^a   Mathavan, Sinnakaruppan ^b   Ghosh, Sukla ^a  

^a UNIVERSITY OF CALCUTTA   (India)

^b GENOME INSTITUTE OF SINGAPORE   (Singapore)

^c Chittaranjan National Cancer Research Institute ^*  (India)

^d VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^e INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; GELATINASE B; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TRANSCRIPTION FACTOR SOX11; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTOME; ZEBRAFISH PROTEIN;

ANIMAL TISSUE; ARTICLE; ATF3 GENE; CELL CYCLE REGULATION; CELL DEATH; CELL MIGRATION; CELL PROLIFERATION; CLUSTER ANALYSIS; CONTROLLED STUDY; DBX2 GENE; EMBRYO PATTERN FORMATION; FIN (ORGAN); GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; INFLAMMATION; MICROARRAY ANALYSIS; MMP9 GENE; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; RETINA DEVELOPMENT; SIGNAL TRANSDUCTION; SOX11 GENE; SOX2 GENE; SOX3 GENE; SPATIOTEMPORAL ANALYSIS; SPINAL CORD REGENERATION; STAT3 GENE; TISSUE REGENERATION; TRANSCRIPTOMICS; ZEBRA FISH; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; GENETIC VARIABILITY; NERVE FIBER; NERVOUS SYSTEM INFLAMMATION; SOCS3 GENE; SPINE INJURY; UPREGULATION; ANIMAL; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; SPINAL CORD INJURY;

AMPHIBIA; DANIO RERIO; MAMMALIA; TELEOSTEI; VERTEBRATA;

ANIMALS; GENOME-WIDE ASSOCIATION STUDY; SPATIO-TEMPORAL ANALYSIS; SPINAL CORD INJURIES; SPINAL CORD REGENERATION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84903153983     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084212     Document Type: Article

References (127)

1. Akimenko MA, Mari-Beffa M, Becerra J, Geraudie J (2003) Old questions, new tools, and some answers to the mystery of fin regeneration. Dev Dyn 226: 190-201. (Pubitemid 36158165)
2. Padhi BK, Joly L, Tellis P, Smith A, Nanjappa P, et al. (2004) Screen for genes differentially expressed during regeneration of the zebrafish caudal fin. Dev Dyn 231: 527-541. (Pubitemid 39410887)
3. Poss KD, Wilson LG, Keating MT (2002) Heart regeneration in zebrafish. Science 298: 2188-2190. (Pubitemid 35471243)
4. Becker T, Wullimann MF, Becker CG, Bernhardt RR, Schachner M (1997) Axonal regrowth after spinal cord transection in adult zebrafish. J Comp Neurol 377: 577-595. (Pubitemid 27053550)
5. Cameron DA, Gentile KL, Middleton FA, Yurco P (2005) Gene expression profiles of intact and regenerating zebrafish retina. Mol Vis 11: 775-791. (Pubitemid 41410193)
6. Hui SP, Dutta A, Ghosh S (2010) Cellular response after crush injury in adult zebrafish spinal cord. Dev Dyn 239: 2962-2979.
7. Kizil C, Kaslin J, Kroehne V, Brand M (2012) Adult neurogenesis and brain regeneration in zebrafish. Dev Neurobiol 72: 429-461.
8. Marz M, Schmidt R, Rastegar S, Strahle U (2011) Regenerative response following stab injury in the adult zebrafish telencephalon. Dev Dyn 240: 2221-2231.
9. Baumgart EV, Barbosa JS, Bally-Cuif L, Gotz M, Ninkovic J (2012) Stab wound injury of the zebrafish telencephalon: a model for comparative analysis of reactive gliosis. Glia 60: 343-357.
10. Bernhardt RR (1999) Cellular and molecular bases of axonal regeneration in the fish central nervous system. Exp Neurol 157: 223-240.
11. Goldman D, Hankin M, Li Z, Dai X, Ding J (2001) Transgenic zebrafish for studying nervous system development and regeneration. Transgenic Res 10: 21-33. (Pubitemid 32180234)
12. Reimer MM, Sorensen I, Kuscha V, Frank RE, Liu C, et al. (2008) Motor neuron regeneration in adult zebrafish. J Neurosci 28: 8510-8516.
13. Nishidate M, Nakatani Y, Kudo A, Kawakami A (2007) Identification of novel markers expressed during fin regeneration by microarray analysis in medaka fish. Dev Dyn 236: 2685-2693. (Pubitemid 47450958)
14. Schebesta M, Lien CL, Engel FB, Keating MT (2006) Transcriptional profiling of caudal fin regeneration in zebrafish. ScientificWorldJournal 6 Suppl 1: 38-54. (Pubitemid 46155752)
15. Lien CL, Schebesta M, Makino S, Weber GJ, Keating MT (2006) Gene expression analysis of zebrafish heart regeneration. PLoS Biol 4: e260.
16. Mathavan S, Lee SG, Mak A, Miller LD, Murthy KR, et al. (2005) Transcriptome analysis of zebrafish embryogenesis using microarrays. PLoS Genet 1: 260-276.
17. Ghirnikar RS, Lee YL, Eng LF (1998) Inflammation in traumatic brain injury: role of cytokines and chemokines. Neurochem Res 23: 329-340. (Pubitemid 28109878)
18. Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420: 860-867. (Pubitemid 36019639)
19. Profyris C, Cheema SS, Zang D, Azari MF, Boyle K, et al. (2004) Degenerative and regenerative mechanisms governing spinal cord injury. Neurobiol Dis 15: 415-436. (Pubitemid 38429958)
20. Hedtjarn M, Mallard C, Hagberg H (2004) Inflammatory gene profiling in the developing mouse brain after hypoxia-ischemia. J Cereb Blood Flow Metab 24: 1333-1351. (Pubitemid 40019157)
21. Brewer KL, Bethea JR, Yezierski RP (1999) Neuroprotective effects of interleukin-10 following excitotoxic spinal cord injury. Exp Neurol 159: 484-493. (Pubitemid 29485234)
22. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A (2001) Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19: 683-765. (Pubitemid 32368050)
23. Li MO, Wan YY, Sanjabi S, Robertson AK, Flavell RA (2006) Transforming growth factor-beta regulation of immune responses. Annu Rev Immunol 24: 99-146.
24. Mattson MP, Barger SW, Furukawa K, Bruce AJ, Wyss-Coray T, et al. (1997) Cellular signaling roles of TGF beta, TNF alpha and beta APP in brain injury responses and Alzheimer's disease. Brain Res Brain Res Rev 23: 47-61. (Pubitemid 27090749)
25. Yoshimura A, Wakabayashi Y, Mori T (2010) Cellular and molecular basis for the regulation of inflammation by TGF-beta. J Biochem 147: 781-792.
26. Willis BC, Borok Z (2007) TGF-beta-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 293: L525-534. (Pubitemid 47358808)
27. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, et al. (2009) Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 29: 13435-13444.
28. Ho DM, Whitman M (2008) TGF-beta signaling is required for multiple processes during Xenopus tail regeneration. Dev Biol 315: 203-216.
29. 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. (Pubitemid 27016650)
30. Fraser DA, Pisalyaput K, Tenner AJ (2010) C1q enhances microglial clearance of apoptotic neurons and neuronal blebs, and modulates subsequent inflammatory cytokine production. J Neurochem 112:733-743.
31. Ding AH, Nathan CF, Stuehr DJ (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol 141: 2407-2412.
32. Deonarine K, Panelli MC, Stashower ME, Jin P, Smith K, et al. (2007) Gene expression profiling of cutaneous wound healing. J Transl Med 5: 11.
33. Sica A, Schioppa T, Mantovani A, Allavena P (2006) Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy. Eur J Cancer 42 : 717-727.
34. Colton CA (2009) Heterogeneity of microglial activation in the innate immune response in the brain. J Neuroimmune Pharmacol 4: 399-418.
35. Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM (2000) M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 164: 6166-6173. (Pubitemid 30408793)
36. Mori M, Gotoh T (2000) Regulation of nitric oxide production by arginine metabolic enzymes. Biochem Biophys Res Commun 275: 715-719.
37. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, et al. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25: 677-686. (Pubitemid 39457982)
38. Luk HW, Noble LJ, Werb Z (2003) Macrophages contribute to the maintenance of stable regenerating neurites following peripheral nerve injury. J Neurosci Res 73: 644-658. (Pubitemid 37071750)
39. Stoll G, Griffin JW, Li CY, Trapp BD (1989) Wallerian degeneration in the peripheral nervous system: participation of both Schwann cells and macrophages in myelin degradation. J Neurocytol 18: 671-683. (Pubitemid 20001442)
40. Lu X, Richardson PM (1993) Responses of macrophages in rat dorsal root ganglia following peripheral nerve injury. J Neurocytol 22: 334-341. (Pubitemid 23162786)
41. Hu P, McLachlan EM (2003) Distinct functional types of macrophage in dorsal root ganglia and spinal nerves proximal to sciatic and spinal nerve transections in the rat. Exp Neurol 184: 590-605. (Pubitemid 38182790)
42. Ling C, Zou T, Hsiao Y, Tao X, Chen ZL, et al. (2006) Disruption of tissue plasminogen activator gene reduces macrophage migration. Biochem Biophys Res Commun 349: 906-912. (Pubitemid 44380187)
43. Zou T, Ling C, Xiao Y, Tao X, Ma D, et al. (2006) Exogenous tissue plasminogen activator enhances peripheral nerve regeneration and functional recovery after injury in mice. J Neuropathol Exp Neurol 65: 78-86.
44. McEwen ML, Springer JE (2005) A mapping study of caspase-3 activation following acute spinal cord contusion in rats. J Histochem Cytochem 53: 809-819. (Pubitemid 40923456)
45. Yakovlev AG, Knoblach SM, Fan L, Fox GB, Goodnight R, et al. (1997) Activation of CPP32-like caspases contributes to neuronal apoptosis and neurological dysfunction after traumatic brain injury. J Neurosci 17: 7415-7424. (Pubitemid 27413272)
46. Springer JE, Azbill RD, Knapp PE (1999) Activation of the caspase-3 apoptotic cascade in traumatic spinal cord injury. Nat Med 5: 943-946. (Pubitemid 29372423)
47. Kedinger V, Alpy F, Tomasetto C, Thisse C, Thisse B, et al. (2005) Spatial and temporal distribution of the traf4 genes during zebrafish development. Gene Expr Patterns 5: 545-552. (Pubitemid 40331396)
48. Motoyama N, Wang F, Roth KA, Sawa H, Nakayama K, et al. (1995) Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267: 1506-1510.
49. Liao Q, Ozawa F, Friess H, Zimmermann A, Takayama S, et al. (2001) The anti-apoptotic protein BAG-3 is overexpressed in pancreatic cancer and induced by heat stress in pancreatic cancer cell lines. FEBS Lett 503: 151-157. (Pubitemid 32763196)
50. Song HD, Sun XJ, Deng M, Zhang GW, Zhou Y, et al. (2004) Hematopoietic gene expression profile in zebrafish kidney marrow. Proc Natl Acad Sci U S A 101: 16240-16245. (Pubitemid 39552829)
51. Ryu S, Holzschuh J, Erhardt S, Ettl AK, Driever W (2005) Depletion of minichromosome maintenance protein 5 in the zebrafish retina causes cell-cycle defect and apoptosis. Proc Natl Acad Sci U S A 102: 18467-18472. (Pubitemid 43011249)
52. Schlueter PJ, Peng G, Westerfield M, Duan C (2007) Insulin-like growth factor signaling regulates zebrafish embryonic growth and development by promoting cell survival and cell cycle progression. Cell Death Differ 14: 1095-1105. (Pubitemid 46785101)
53. Sheppard AM, Brunstrom JE, Thornton TN, Gerfen RW, Broekelmann TJ, et al. (1995) Neuronal production of fibronectin in the cerebral cortex during migration and layer formation is unique to specific cortical domains. Dev Biol 172: 504-518. (Pubitemid 26057820)
54. Chernoff EA, Stocum DL, Nye HL, Cameron JA (2003) Urodele spinal cord regeneration and related processes. Dev Dyn 226: 295-307. (Pubitemid 36158173)
55. Bai S, Thummel R, Godwin AR, Nagase H, Itoh Y, et al. (2005) Matrix metalloproteinase expression and function during fin regeneration in zebrafish: analysis of MT1-MMP, MMP2 and TIMP2. Matrix Biol 24: 247-260. (Pubitemid 40853875)
56. Monaghan JR, Walker JA, Page RB, Putta S, Beachy CK, et al. (2007) Early gene expression during natural spinal cord regeneration in the salamander Ambystoma mexicanum. J Neurochem 101: 27-40. (Pubitemid 46426468)
57. Smith A, Zhang J, Guay D, Quint E, Johnson A, et al. (2008) Gene expression analysis on sections of zebrafish regenerating fins reveals limitations in the whole-mount in situ hybridization method. Dev Dyn 237: 417-425. (Pubitemid 351312114)
58. Brockes JP (1997) Amphibian limb regeneration: rebuilding a complex structure. Science 276: 81-87.
59. Poss KD, Keating MT, Nechiporuk A (2003) Tales of regeneration in zebrafish. Dev Dyn 226: 202-210. (Pubitemid 36158166)
60. Nona SN, Thomlinson AM, Bartlett CA, Scholes J (2000) Schwann cells in the regenerating fish optic nerve: evidence that CNS axons, not the glia, determine when myelin formation begins. J Neurocytol 29: 285-300.
61. Tysseling VM, Mithal D, Sahni V, Birch D, Jung H, et al. (2011) SDF1 in the dorsal corticospinal tract promotes CXCR4 + cell migration after spinal cord injury. J Neuroinflammation 8: 16.
62. Daksis JI, Lu RY, Facchini LM, Marhin WW, Penn LJ (1994) Myc induces cyclin D1 expression in the absence of de novo protein synthesis and links mitogen-stimulated signal transduction to the cell cycle. Oncogene 9: 3635-3645. (Pubitemid 24359402)
63. Yudkovsky Y, Shteinberg M, Listovsky T, Brandeis M, Hershko A (2000) Phosphorylation of Cdc20/fizzy negatively regulates the mammalian cyclosome/APC in the mitotic checkpoint. Biochem Biophys Res Commun 271: 299-304. (Pubitemid 30444720)
64. Harris TE, Albrecht JH, Nakanishi M, Darlington GJ (2001) CCAAT/enhancer-binding protein-alpha cooperates with p21 to inhibit cyclin-dependent kinase-2 activity and induces growth arrest independent of DNA binding. J Biol Chem 276: 29200-29209.
65. Alldridge LC, Bryant CE (2003) Annexin 1 regulates cell proliferation by disruption of cell morphology and inhibition of cyclin D1 expression through sustained activation of the ERK1/2 MAPK signal. Exp Cell Res 290: 93-107. (Pubitemid 37153254)
66. Saul KE, Koke JR, Garcia DM (2010) Activating transcription factor 3 (ATF3) expression in the neural retina and optic nerve of zebrafish during optic nerve regeneration. Comp Biochem Physiol A Mol Integr Physiol 155: 172-182.
67. Tsujino H, Kondo E, Fukuoka T, Dai Y, Tokunaga A, et al. (2000) Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motorneurons: A novel neuronal marker of nerve injury. Mol Cell Neurosci 15: 170-182. (Pubitemid 30109120)
68. Raymond PA, Barthel LK, Bernardos RL, Perkowski JJ (2006) Molecular characterization of retinal stem cells and their niches in adult zebrafish. BMC Dev Biol 6: 36.
69. Cheung KK, Mok SC, Rezaie P, Chan WY (2008) Dynamic expression of Dab2 in the mouse embryonic central nervous system. BMC Dev Biol 8: 76.
70. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, et al. (2003) Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17: 126-140. (Pubitemid 36062514)
71. Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39: 749-765. (Pubitemid 37088088)
72. Ferri AL, Cavallaro M, Braida D, Di Cristofano A, Canta A, et al. (2004) Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 131: 3805-3819. (Pubitemid 39199387)
73. Adolf B, Chapouton P, Lam CS, Topp S, Tannhauser B, et al. (2006) Conserved and acquired features of adult neurogenesis in the zebrafish telencephalon. Dev Biol 295: 278-293. (Pubitemid 44041332)
74. Muneoka K, Bryant SV (1982) Evidence that patterning mechanisms in developing and regenerating limbs are the same. Nature 298: 369-371. (Pubitemid 12044288)
75. Stocum DL (1996) A conceptual framework for analyzing axial patterning in regenerating urodele limbs. Int J Dev Biol 40: 773-783.
76. Schnapp E, Kragl M, Rubin L, Tanaka EM (2005) Hedgehog signaling controls dorsoventral patterning, blastema cell proliferation and cartilage induction during axolotl tail regeneration. Development 132: 3243-3253. (Pubitemid 41167152)
77. Tanaka EM, Ferretti P (2009) Considering the evolution of regeneration in the central nervous system. Nat Rev Neurosci 10: 713-723.
78. Jessell TM (2000) Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 1: 20-29.
79. Briscoe J, Pierani A, Jessell TM, Ericson J (2000) A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101: 435-445.
80. Poh A, Karunaratne A, Kolle G, Huang N, Smith E, et al. (2002) Patterning of the vertebrate ventral spinal cord. Int J Dev Biol 46: 597-608. (Pubitemid 36849570)
81. Wilson L, Maden M (2005) The mechanisms of dorsoventral patterning in the vertebrate neural tube. Dev Biol 282: 1-13. (Pubitemid 40779924)
82. Guner B, Karlstrom RO (2007) Cloning of zebrafish nkx6.2 and a comprehensive analysis of the conserved transcriptional response to Hedge-hog/Gli signaling in the zebrafish neural tube. Gene Expr Patterns 7: 596-605. (Pubitemid 46464652)
83. Lufkin T (1996) Transcriptional control of Hox genes in the vertebrate nervous system. Curr Opin Genet Dev 6: 575-580.
84. Prince VE, Joly L, Ekker M, Ho RK (1998) Zebrafish hox genes: genomic organization and modified colinear expression patterns in the trunk. Development 125: 407-420. (Pubitemid 28102649)
85. Koshida S, Shinya M, Mizuno T, Kuroiwa A, Takeda H (1998) Initial anteroposterior pattern of the zebrafish central nervous system is determined by differential competence of the epiblast. Development 125: 1957-1966. (Pubitemid 28274382)
86. van den Akker E, Forlani S, Chawengsaksophak K, de Graaff W, Beck F, et al. (2002) Cdx1 and Cdx2 have overlapping functions in anteroposterior patterning and posterior axis elongation. Development 129: 2181-2193. (Pubitemid 34874231)
87. Liu JP (2006) The function of growth/differentiation factor 11 (Gdf11) in rostrocaudal patterning of the developing spinal cord. Development 133: 2865-2874.
88. Carpenter EM (2002) Hox genes and spinal cord development. Dev Neurosci 24: 24-34.
89. Dasen JS, Liu JP, Jessell TM (2003) Motor neuron columnar fate imposed by sequential phases of Hox-c activity. Nature 425: 926-933. (Pubitemid 37376919)
90. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274: 1123-1133. (Pubitemid 26389268)
91. Xu Q, Alldus G, Macdonald R, Wilkinson DG, Holder N (1996) Function of the Eph-related kinase rtk1 in patterning of the zebrafish forebrain. Nature 381: 319-322. (Pubitemid 26000129)
92. Flanagan JG (2006) Neural map specification by gradients. Curr Opin Neurobiol 16: 59-66.
93. Winberg ML, Mitchell KJ, Goodman CS (1998) Genetic analysis of the mechanisms controlling target selection: complementary and combinatorial functions of netrins, semaphorins, and IgCAMs. Cell 93: 581-591. (Pubitemid 28240719)
94. Roos M, Schachner M, Bernhardt RR (1999) Zebrafish semaphorin Z1b inhibits growing motor axons in vivo. Mech Dev 87: 103-117. (Pubitemid 29428090)
95. Devine CA, Key B (2008) Robo-Slit interactions regulate longitudinal axon pathfinding in the embryonic vertebrate brain. Dev Biol 313: 371-383. (Pubitemid 350298322)
96. Seijffers R, Mills CD, Woolf CJ (2007) ATF3 increases the intrinsic growth state of DRG neurons to enhance peripheral nerve regeneration. J Neurosci 27: 7911-7920. (Pubitemid 47173306)
97. Schweitzer J, Gimnopoulos D, Lieberoth BC, Pogoda HM, Feldner J, et al. (2007) Contactin1a expression is associated with oligodendrocyte differentiation and axonal regeneration in the central nervous system of zebrafish. Mol Cell Neurosci 35: 194-207. (Pubitemid 46843561)
98. Poss KD, Shen J, Keating MT (2000) Induction of lef1 during zebrafish fin regeneration. Dev Dyn 219: 282-286.
99. Kawakami Y, Rodriguez Esteban C, Raya M, Kawakami H, Marti M, et al. (2006) Wnt/beta-catenin signaling regulates vertebrate limb regeneration. Genes Dev 20: 3232-3237. (Pubitemid 44904844)
100. Stoick-Cooper CL, Moon RT, Weidinger G (2007) Advances in signaling in vertebrate regeneration as a prelude to regenerative medicine. Genes Dev 21: 1292-1315. (Pubitemid 46871034)
101. Ghosh S, Roy S, Seguin C, Bryant SV, Gardiner DM (2008) Analysis of the expression and function of Wnt-5a and Wnt-5b in developing and regenerating axolotl (Ambystoma mexicanum) limbs. Dev Growth Differ 50: 289-297. (Pubitemid 351661154)
102. Caubit X, Nicolas S, Le Parco Y (1997) Possible roles for Wnt genes in growth and axial patterning during regeneration of the tail in urodele amphibians. Dev Dyn 210: 1-10. (Pubitemid 27371928)
103. Shou J, Rim PC, Calof AL (1999) BMPs inhibit neurogenesis by a mechanism involving degradation of a transcription factor. Nat Neurosci 2: 339-345. (Pubitemid 30491276)
104. Wu HH, Ivkovic S, Murray RC, Jaramillo S, Lyons KM, et al. (2003) Autoregulation of neurogenesis by GDF11. Neuron 37: 197-207. (Pubitemid 36143816)
105. Jarnicki A, Putoczki T, Ernst M (2010) Stat3: linking inflammation to epithelial cancer - more than a "gut" feeling? Cell Div 5: 14.
106. Stadler JA, Shkumatava A, Norton WH, Rau MJ, Geisler R, et al. (2005) Histone deacetylase 1 is required for cell cycle exit and differentiation in the zebrafish retina. Dev Dyn 233: 883-889. (Pubitemid 40853465)
107. Yamaguchi M, Tonou-Fujimori N, Komori A, Maeda R, Nojima Y, et al. (2005) Histone deacetylase 1 regulates retinal neurogenesis in zebrafish by suppressing Wnt and Notch signaling pathways. Development 132: 3027-3043. (Pubitemid 41086737)
108. Harrison MR, Georgiou AS, Spaink HP, Cunliffe VT (2011) The epigenetic regulator Histone Deacetylase 1 promotes transcription of a core neurogenic programme in zebrafish embryos. BMC Genomics 12: 24.
109. Iskandar BJ, Rizk E, Meier B, Hariharan N, Bottiglieri T, et al. (2010) Folate regulation of axonal regeneration in the rodent central nervous system through DNA methylation. J Clin Invest 120: 1603-1616.
110. Kronenberg G, Endres M (2010) Neuronal injury: folate to the rescue? J Clin Invest 120: 1383-1386.
111. Herrmann JE, Imura T, Song B, Qi J, Ao Y, et al. (2008) STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J Neurosci 28: 7231-7243.
112. Byrnes KR, Stoica BA, Fricke S, Di Giovanni S, Faden AI (2007) Cell cycle activation contributes to post-mitotic cell death and secondary damage after spinal cord injury. Brain 130: 2977-2992. (Pubitemid 350033958)
113. Horner PJ, Gage FH (2000) Regenerating the damaged central nervous system. Nature 407: 963-970.
114. Thuret S, Moon LD, Gage FH (2006) Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 7: 628-643. (Pubitemid 44106745)
115. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121. (Pubitemid 32397092)
116. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863-14868. (Pubitemid 29003722)
117. Saldanha AJ (2004) Java Treeview-extensible visualization of microarray data. Bioinformatics 20: 3246-3248.
118. Dutta A, Sen T, Banerji A, Das S, Chatterjee A (2009) Studies on Multifunctional Effect of All-Trans Retinoic Acid (ATRA) on Matrix Metalloproteinase-2 (MMP-2) and Its Regulatory Molecules in Human Breast Cancer Cells (MCF-7). J Oncol 2009: 627840.
119. Braissant O, Wahli W (1998) Differential expression of peroxisome proliferator-activated receptor-alpha, -beta, and -gamma during rat embryonic development. Endocrinology 139: 2748-2754. (Pubitemid 28512383)
120. Hausmann ON (2003) Post-traumatic inflammation following spinal cord injury. Spinal Cord 41: 369-378.
121. Byrnes KR, Washington PM, Knoblach SM, Hoffman E, Faden AI (2011) Delayed inflammatory mRNA and protein expression after spinal cord injury. J Neuroinflammation 8: 130.
122. Carmichael ST, Archibeque I, Luke L, Nolan T, Momiy J, et al. (2005) Growth-associated gene expression after stroke: evidence for a growth-promoting region in peri-infarct cortex. Exp Neurol 193: 291-311. (Pubitemid 40616180)
123. Ahn YH, Lee G, Kang SK (2006) Molecular insights of the injured lesions of rat spinal cords: Inflammation, apoptosis, and cell survival. Biochem Biophys Res Commun 348: 560-570. (Pubitemid 44188602)
124. Aimone JB, Leasure JL, Perreau VM, Thallmair M (2004) Spatial and temporal gene expression profiling of the contused rat spinal cord. Exp Neurol 189: 204-221. (Pubitemid 39221816)
125. Mladinic M, Lefevre C, Del Bel E, Nicholls J, Digby M (2010) Developmental changes of gene expression after spinal cord injury in neonatal opossums. Brain Res 1363: 20-39.
126. Wakatsuki S, Saitoh F, Araki T (2011) ZNRF1 promotes Wallerian degeneration by degrading AKT to induce GSK3B-dependent CRMP2 phosphorylation. Nat Cell Biol 13: 1415-1423.
127. Hunt D, Hossain-Ibrahim K, Mason MR, Coffin RS, Lieberman AR, et al. (2004) ATF3 upregulation in glia during Wallerian degeneration: differential expression in peripheral nerves and CNS white matter. BMC Neurosci 5: 9.