Gene expression analysis of zebrafish retinal ganglion cells during optic nerve regeneration identifies KLF6a and KLF7a as important regulators of axon regeneration

Developmental Biology

Volumn 312, Issue 2, 2007, Pages 596-612

  Veldman, Matthew B ^a   Bemben, Michael A ^b   Thompson, Robert C ^a,b,c   Goldman, Daniel ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Gene expression; KLF6; KLF7; Microarray; Optic nerve; Regeneration; Retina; Retinal ganglion cell; SOCS3; Sox11; Zebrafish

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE EXPRESSION; IN SITU HYBRIDIZATION; LASER CAPTURE MICRODISSECTION; MICROARRAY ANALYSIS; NERVE FIBER REGENERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTIC NERVE; OPTIC NERVE INJURY; PRIORITY JOURNAL; RETINA GANGLION CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UNINDEXED SEQUENCE; UPREGULATION; ZEBRA FISH;

DANIO RERIO; MAMMALIA; TELEOSTEI;

EID: 36549068204     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2007.09.019     Document Type: Article

References (110)

1. Asch W.S., Leake D., Canger A.K., Passini M.A., Argenton F., and Schechter N. Cloning of zebrafish neurofilament cDNAs for plasticin and gefiltin: increased mRNA expression in ganglion cells after optic nerve injury. J. Neurochem. 71 (1998) 20-32
2. Ballestero R.P., Wilmot G.R., Leski M.L., Uhler M.D., and Agranoff B.W. Isolation of cDNA clones encoding RICH: a protein induced during goldfish optic nerve regeneration with homology to mammalian 2′,3′-cyclic-nucleotide 3′-phosphodiesterases. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 8621-8625
3. Barthel L.K., and Raymond P.A. In situ hybridization studies of retinal neurons. Methods Enzymol. 316 (2000) 579-590
4. Bartsch D., Ghirardi M., Skehel P.A., Karl K.A., Herder S.P., Chen M., Bailey C.H., and Kandel E.R. Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change. Cell 83 (1995) 979-992
5. Bastmeyer M., Beckmann M., Schwab M.E., and Stuermer C.A. Growth of regenerating goldfish axons is inhibited by rat oligodendrocytes and CNS myelin but not but not by goldfish optic nerve tract oligodendrocytelike cells and fish CNS myelin. J. Neurosci. 11 (1991) 626-640
6. Becker T., Wullimann M.F., Becker C.G., Bernhardt R.R., and Schachner M. Axonal regrowth after spinal cord transection in adult zebrafish. J. Comp. Neurol. 377 (1997) 577-595
7. Becker C.G., Lieberoth B.C., Morellini F., Feldner J., Becker T., and Schachner M. L1.1 is involved in spinal cord regeneration in adult zebrafish. J. Neurosci. 24 (2004) 7837-7842
8. Bergsland M., Werme M., Malewicz M., Perlmann T., and Muhr J. The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev. 20 (2006) 3475-3486
9. Bernhardt R.R. Cellular and molecular bases of axonal regeneration in the fish central nervous system. Exp. Neurol. 157 (1999) 223-240
10. Bernhardt R.R., Tongiorgi E., Anzini P., and Schachner M. Increased expression of specific recognition molecules by retinal ganglion cells and by optic pathway glia accompanies the successful regeneration of retinal axons in adult zebrafish. J. Comp. Neurol. 376 (1996) 253-264
11. Berry M., Carlile J., and Hunter A. Peripheral nerve explants grafted into the vitreous body of the eye promote the regeneration of retinal ganglion cell axons severed in the optic nerve. J. Neurocytol. 25 (1996) 147-170
12. Bisby M.A., and Tetzlaff W. Changes in cytoskeletal protein synthesis following axon injury and during axon regeneration. Mol. Neurobiol. 6 (1992) 107-123
13. Bonilla I.E., Tanabe K., and Strittmatter S.M. Small proline-rich repeat protein 1A is expressed by axotomized neurons and promotes axonal outgrowth. J. Neurosci. 22 (2002) 1303-1315
14. Bormann P., Zumsteg V.M., Roth L.W., and Reinhard E. Target contact regulates GAP-43 and alpha-tubulin mRNA levels in regenerating retinal ganglion cells. J. Neurosci. Res. 52 (1998) 405-419
15. Brauer A.U., Savaskan N.E., Kuhn H., Prehn S., Ninnemann O., and Nitsch R. A new phospholipid phosphatase, PRG-1, is involved in axon growth and regenerative sprouting. Nat. Neurosci. 6 (2003) 572-578
16. Chen A., Muzzio I.A., Malleret G., Bartsch D., Verbitsky M., Pavlidis P., Yonan A.L., Vronskaya S., Grody M.B., Cepeda I., Gilliam T.C., and Kandel E.R. Inducible enhancement of memory storage and synaptic plasticity in transgenic mice expressing an inhibitor of ATF4 (CREB-2) and C/EBP proteins. Neuron 39 (2003) 655-669
17. Chierzi S., and Fawcett J.W. Regeneration in the mammalian optic nerve. Restor. Neurol. Neurosci. 19 (2001) 109-118
18. Costigan M., Befort K., Karchewski L., Griffin R.S., D'Urso D., Allchorne A., Sitarski J., Mannion J.W., Pratt R.E., and Woolf C.J. Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci. 3 (2002) 16
19. Daniels R.H., Hall P.S., and Bokoch G.M. Membrane targeting of p21-activated kinase 1 (PAK1) induces neurite outgrowth from PC12 cells. EMBO J. 17 (1998) 754-764
20. Dickson B.J. Rho GTPases in growth cone guidance. Curr. Opin. Neurobiol. 11 (2001) 103-110
21. Diekmann H., Klinger M., Oertle T., Heinz D., Pogoda H.M., Schwab M.E., and Stuermer C.A. Analysis of the reticulon gene family demonstrates the absence of the neurite growth inhibitor Nogo-A in fish. Mol. Biol. Evol. 22 (2005) 1635-1648
22. Dieterich D.C., Bockers T.M., Gundelfinger E.D., and Kreutz M.R. Screening for differentially expressed genes in the rat inner retina and optic nerve after optic nerve crush. Neurosci. Lett. 317 (2002) 29-32
23. Doster S.K., Lozano A.M., Aguayo A.J., and Willard M.B. Expression of the growth-associated protein GAP-43 in adult rat retinal ganglion cells following axon injury. Neuron 6 (1991) 635-647
24. Dovas A., and Couchman J.R. RhoGDI: multiple functions in the regulation of Rho family GTPase activities. Biochem. J. 390 (2005) 1-9
25. Ellezam B., Dubreuil C., Winton M., Loy L., Dergham P., Selles-Navarro I., and McKerracher L. Inactivation of intracellular Rho to stimulate axon growth and regeneration. Prog. Brain Res. 137 (2002) 371-380
26. Fischer D., Heiduschka P., and Thanos S. Lens-injury-stimulated axonal regeneration throughout the optic pathway of adult rats. Exp. Neurol. 172 (2001) 257-272
27. Fischer D., Petkova V., Thanos S., and Benowitz L.I. Switching mature retinal ganglion cells to a robust growth state in vivo: gene expression and synergy with RhoA inactivation. J. Neurosci. 24 (2004) 8726-8740
28. Fischer P., Lehmann U., Sobota R.M., Schmitz J., Niemand C., Linnemann S., Haan S., Behrmann I., Yoshimura A., Johnston J.A., Muller-Newen G., Heinrich P.C., and Schaper F. The role of the inhibitors of interleukin-6 signal transduction SHP2 and SOCS3 for desensitization of interleukin-6 signalling. Biochem. J. 378 (2004) 449-460
29. Fournier A.E., and McKerracher L. Tubulin expression and axonal transport in injured and regenerating neurons in the adult mammalian central nervous system. Biochem. Cell. Biol. 73 (1995) 659-664
30. Fry E.J., Ho C., and David S. A role for Nogo receptor in macrophage clearance from injured peripheral nerve. Neuron 53 (2007) 649-662
31. Fu M., Zhang J., Tseng Y.H., Cui T., Zhu X., Xiao Y., Mou Y., De Leon H., Chang M.M., Hamamori Y., Kahn C.R., and Chen Y.E. Rad GTPase attenuates vascular lesion formation by inhibition of vascular smooth muscle cell migration. Circulation 111 (2005) 1071-1077
32. Gao Y., Deng K., Hou J., Bryson J.B., Barco A., Nikulina E., Spencer T., Mellado W., Kandel E.R., and Filbin M.T. Activated CREB is sufficient to overcome inhibitors in myelin and promote spinal axon regeneration in vivo. Neuron 44 (2004) 609-621
33. Giulian D., Des Ruisseux H., and Cowburn D. Biosynthesis and intra-axonal transport of proteins during neuronal regeneration. J. Biol. Chem. 255 (1980) 6494-6501
34. Goldman D., Hankin M., Li Z., Dai X., and Ding J. Transgenic zebrafish for studying nervous system development and regeneration. Transgenic Res. 10 (2001) 21-33
35. Graeber M.B., Raivich G., and Kreutzberg G.W. Increase of transferrin receptors and iron uptake in regenerating motor neurons. J. Neurosci. Res. 23 (1989) 342-345
36. Haas C.A., Donath C., and Kreutzberg G.W. Differential expression of immediate early genes after transection of the facial nerve. Neuroscience 53 (1993) 91-99
37. Herdegen T., Bastmeyer M., Bahr M., Stuermer C., Bravo R., and Zimmermann M. Expression of JUN, KROX, and CREB transcription factors in goldfish and rat retinal ganglion cells following optic nerve lesion is related to axonal sprouting. J. Neurobiol. 24 (1993) 528-543
38. Hieber V., Agranoff B.W., and Goldman D. Target-dependent regulation of retinal nicotinic acetylcholine receptor and tubulin RNAs during optic nerve regeneration in goldfish. J. Neurochem. 58 (1992) 1009-1015
39. Hieber V., Dai X., Foreman M., and Goldman D. Induction of alpha1-tubulin gene expression during development and regeneration of the fish central nervous system. J. Neurobiol. 37 (1998) 429-440
40. Johns P.R., Yoon M.G., and Agranoff B.W. Directed outgrowth of optic fibres regenerating in vitro. Nature 271 (1978) 360-362
41. Kabos P., Kabosova A., and Neuman T. Neuronal injury affects expression of helix-loop-helix transcription factors. NeuroReport 13 (2002) 2385-2388
42. Kajimura D., Dragomir C., Ramirez F., and Laub F. Identification of genes regulated by transcription factor KLF7 in differentiating olfactory sensory neurons. Gene 388 (2007) 34-42
43. Kamachi Y., Uchikawa M., and Kondoh H. Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet. 16 (2000) 182-187
44. Kile B.T., and Alexander W.S. The suppressors of cytokine signalling (SOCS). Cell. Mol. Life Sci. 58 (2001) 1627-1635
45. Kim Y., Ratziu V., Choi S.G., Lalazar A., Theiss G., Dang Q., Kim S.J., and Friedman S.L. Transcriptional activation of transforming growth factor beta1 and its receptors by the Kruppel-like factor Zf9/core promoter-binding protein and Sp1. Potential mechanisms for autocrine fibrogenesis in response to injury. J. Biol. Chem. 273 (1998) 33750-33758
46. Landreth G.E., and Agranoff B.W. Explant culture of adult goldfish retina: effect of prior optic nerve crush. Brain Res. 118 (1976) 299-303
47. Landreth G.E., and Agranoff B.W. Explant culture of adult goldfish retina: a model for the study of CNS regeneration. Brain Res. 161 (1979) 39-55
48. Laub F., Aldabe R., Ramirez F., and Friedman S. Embryonic expression of Kruppel-like factor 6 in neural and non-neural tissues. Mech. Dev. 106 (2001) 167-170
49. Laub F., Lei L., Sumiyoshi H., Kajimura D., Dragomir C., Smaldone S., Puche A.C., Petros T.J., Mason C., Parada L.F., and Ramirez F. Transcription factor KLF7 is important for neuronal morphogenesis in selected regions of the nervous system. Mol. Cell Biol. 25 (2005) 5699-5711
50. Leon S., Yin Y., Nguyen J., Irwin N., and Benowitz L.I. Lens injury stimulates axon regeneration in the mature rat optic nerve. J. Neurosci. 20 (2000) 4615-4626
51. Li C., and Hung Wong W. Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol. 2 (2001) 0032.1-0032.11
52. Lieberman A.R. The axon reaction: a review of the principal features of perikaryal responses to axon injury. Int. Rev. Neurobiol. 14 (1971) 49-124
53. Liu R.Y., and Snider W.D. Different signaling pathways mediate regenerative versus developmental sensory axon growth. J. Neurosci. 21 (2001) RC164
54. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001) 402-408
55. Lonze B.E., and Ginty D.D. Function and regulation of CREB family transcription factors in the nervous system. Neuron 35 (2002) 605-623
56. Lorber B., Berry M., and Logan A. Lens injury stimulates adult mouse retinal ganglion cell axon regeneration via both macrophage- and lens-derived factors. Eur. J. Neurosci. 21 (2005) 2029-2034
57. Lu X., and Richardson P.M. Inflammation near the nerve cell body enhances axonal regeneration. J. Neurosci. 11 (1991) 972-978
58. Lundquist E.A. Rac proteins and the control of axon development. Curr. Opin. Neurobiol. 13 (2003) 384-390
59. Luo L., Jan L.Y., and Jan Y.N. Rho family GTP-binding proteins in growth cone signalling. Curr. Opin. Neurobiol. 7 (1997) 81-86
60. Mansur K., Iwahashi Y., Kiryu-Seo S., Su Q., Namikawa K., Yodoi J., and Kiyama H. Up-regulation of thioredoxin expression in motor neurons after nerve injury. Brain Res. Mol. Brain Res. 62 (1998) 86-91
61. Matsumoto N., Kubo A., Liu H., Akita K., Laub F., Ramirez F., Keller G., and Friedman S.L. Developmental regulation of yolk sac hematopoiesis by Kruppel-like factor 6. Blood 107 (2006) 1357-1365
62. McDowell A.L., Dixon L.J., Houchins J.D., and Bilotta J. Visual processing of the zebrafish optic tectum before and after optic nerve damage. Vis. Neurosci. 21 (2004) 97-106
63. McKerracher L., and Higuchi H. Targeting Rho to stimulate repair after spinal cord injury. J. Neurotrauma 23 (2006) 309-317
64. McNamara R.K., Jiang Y., Streit W.J., and Lenox R.H. Facial motor neuron regeneration induces a unique spatial and temporal pattern of myristoylated alanine-rich C kinase substrate expression. Neuroscience 97 (2000) 581-589
65. Mead J.R., Hughes T.R., Irvine S.A., Singh N.N., and Ramji D.P. Interferon-gamma stimulates the expression of the inducible cAMP early repressor in macrophages through the activation of casein kinase 2. A potentially novel pathway for interferon-gamma-mediated inhibition of gene transcription. J. Biol. Chem. 278 (2003) 17741-17751
66. Miao T., Wu D., Zhang Y., Bo X., Subang M.C., Wang P., and Richardson P.M. Suppressor of cytokine signaling-3 suppresses the ability of activated signal transducer and activator of transcription-3 to stimulate neurite growth in rat primary sensory neurons. J. Neurosci. 26 (2006) 9512-9519
67. Miller F.D., Tetzlaff W., Bisby M.A., Fawcett J.W., and Milner R.J. Rapid induction of the major embryonic alpha-tubulin mRNA, T alpha 1, during nerve regeneration in adult rats. J. Neurosci. 9 (1989) 1452-1463
68. Mioduszewska B., Jaworski J., and Kaczmarek L. Inducible cAMP early repressor (ICER) in the nervous system-a transcriptional regulator of neuronal plasticity and programmed cell death. J. Neurochem. 87 (2003) 1313-1320
69. Molina C.A., Foulkes N.S., Lalli E., and Sassone-Corsi P. Inducibility and negative autoregulation of CREM: an alternative promoter directs the expression of ICER, an early response repressor. Cell 75 (1993) 875-876
70. Murphy P.G., Grondin J., Altares M., and Richardson P.M. Induction of interleukin-6 in axotomized sensory neurons. J. Neurosci. 15 (1995) 5130-5138
71. Narla G., Heath K.E., Reeves H.L., Li D., Giono L.E., Kimmelman A.C., Glucksman M.J., Narla J., Eng F.J., Chan A.M., Ferrari A.C., Martignetti J.A., and Friedman S.L. KLF6, a candidate tumor suppressor gene mutated in prostate cancer. Science 294 (2001) 2563-2566
72. Nasevicius A., and Ekker S.C. Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26 (2000) 216-220
73. Neumann S., and Woolf C.J. Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 23 (1999) 83-91
74. Ng J., and Luo L. Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron 44 (2004) 779-793
75. Nilsson A., Moller K., Dahlin L., Lundborg G., and Kanje M. Early changes in gene expression in the dorsal root ganglia after transection of the sciatic nerve; effects of amphiregulin and PAI-1 on regeneration. Brain Res. Mol. Brain Res. 136 (2005) 65-74
76. Ohtori S., Takahashi K., Moriya H., and Myers R.R. TNF-alpha and TNF-alpha receptor type 1 upregulation in glia and neurons after peripheral nerve injury: studies in murine DRG and spinal cord. Spine 29 (2004) 1082-1088
77. O'Sullivan A.L., Liongue C., Lewis R.S., Stephenson S.E., and Ward A.C. Cytokine receptor signaling through the Jak-Stat-Socs pathway in disease. Mol. Immunol. 44 (2007) 2497-2506
78. Pernet V., and Di Polo A. Synergistic action of brain-derived neurotrophic factor and lens injury promotes retinal ganglion cell survival, but leads to optic nerve dystrophy in vivo. Brain 129 (2006) 1014-1026
79. Persengiev S.P., Devireddy L.R., and Green M.R. Inhibition of apoptosis by ATFx: a novel role for a member of the ATF/CREB family of mammalian bZIP transcription factors. Genes Dev. 16 (2002) 1806-1814
80. Plunet W., Kwon B.K., and Tetzlaff W. Promoting axonal regeneration in the central nervous system by enhancing the cell body response to axotomy. J. Neurosci. Res. 68 (2002) 1-6
81. Qiu J., Cafferty W.B., McMahon S.B., and Thompson S.W. Conditioning injury-induced spinal axon regeneration requires signal transducer and activator of transcription 3 activation. J. Neurosci. 25 (2005) 1645-1653
82. Rosenfeldt H., Castellone M.D., Randazzo P.A., and Gutkind J.S. Rac inhibits thrombin-induced Rho activation: evidence of a Pak-dependent GTPase crosstalk. J. Mol. Signal 1 (2006) 8
83. Roth L.W., Bormann P., Wiederkehr C., and Reinhard E. Beta-thymosin, a modulator of the actin cytoskeleton is increased in regenerating retinal ganglion cells. Eur. J. Neurosci. 11 (1999) 3488-3498
84. Schafers M., Geis C., Svensson C.I., Luo Z.D., and Sommer C. Selective increase of tumour necrosis factor-alpha in injured and spared myelinated primary afferents after chronic constrictive injury of rat sciatic nerve. Eur. J. Neurosci. 17 (2003) 791-804
85. Schwab M.E. Nogo and axon regeneration. Curr. Opin. Neurobiol. 14 (2004) 118-124
86. Senut M.C., Gulati-Leekha A., and Goldman D. An element in the alpha1-tubulin promoter is necessary for retinal expression during optic nerve regeneration but not after eye injury in the adult zebrafish. J. Neurosci. 24 (2004) 7663-7673
87. Skene J.H. Axonal growth-associated proteins. Annu. Rev. Neurosci. 12 (1989) 127-156
88. Smith D.S., and Skene J.H. A transcription-dependent switch controls competence of adult neurons for distinct modes of axon growth. J. Neurosci. 17 (1997) 646-658
89. So K.F., and Aguayo A.J. Lengthy regrowth of cut axons from ganglion cells after peripheral nerve transplantation into the retina of adult rats. Brain Res. 328 (1985) 349-354
90. Starr R., Willson T.A., Viney E.M., Murray L.J., Rayner J.R., Jenkins B.J., Gonda T.J., Alexander W.S., Metcalf D., Nicola N.A., and Hilton D.J. A family of cytokine-inducible inhibitors of signalling. Nature 387 (1997) 917-921
91. Suske G., Bruford E., and Philipsen S. Mammalian SP/KLF transcription factors: bring in the family. Genomics 85 (2005) 551-556
92. Tachibana T., Noguchi K., and Ruda M.A. Analysis of gene expression following spinal cord injury in rat using complementary DNA microarray. Neurosci. Lett. 327 (2002) 133-137
93. Takeda M., Kato H., Takamiya A., Yoshida A., and Kiyama H. Injury-specific expression of activating transcription factor-3 in retinal ganglion cells and its colocalized expression with phosphorylated c-Jun. Invest Ophthalmol. Visual Sci. 41 (2000) 2412-2421
94. Tanabe K., Bonilla I., Winkles J.A., and Strittmatter S.M. Fibroblast growth factor-inducible-14 is induced in axotomized neurons and promotes neurite outgrowth. J. Neurosci. 23 (2003) 9675-9686
95. Tanaka H., Yamashita T., Yachi K., Fujiwara T., Yoshikawa H., and Tohyama M. Cytoplasmic p21(Cip1/WAF1) enhances axonal regeneration and functional recovery after spinal cord injury in rats. Neuroscience 127 (2004) 155-164
96. Taskinen H.S., Olsson T., Bucht A., Khademi M., Svelander L., and Roytta M. Peripheral nerve injury induces endoneurial expression of IFN-gamma, IL-10 and TNF-alpha mRNA. J. Neuroimmunol. 102 (2000) 17-25
97. Troy C.M., Muma N.A., Greene L.A., Price D.L., and Shelanski M.L. Regulation of peripherin and neurofilament expression in regenerating rat motor neurons. Brain Res. 529 (1990) 232-238
98. Tsujino H., Kondo E., Fukuoka T., Dai Y., Tokunaga A., Miki K., Yonenobu K., Ochi T., and Noguchi K. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury. Mol. Cell. Neurosci. 15 (2000) 170-182
99. Villegas-Perez M.P., Vidal-Sanz M., Bray G.M., and Aguayo A.J. Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. J. Neurosci. 8 (1988) 265-280
100. Vogelaar C.F., Hoekman M.F., Gispen W.H., and Burbach J.P. Homeobox gene expression in adult dorsal root ganglia during sciatic nerve regeneration: is regeneration a recapitulation of development?. Eur. J. Pharmacol. 480 (2003) 233-250
101. Wanner M., Lang D.M., Bandtlow C.E., Schwab M.E., Bastmeyer M., and Stuermer C.A. Reevaluation of the growth-permissive substrate properties of goldfish optic nerve myelin and myelin proteins. J. Neurosci. 15 (1995) 7500-7508
102. Ward Y., Yap S.F., Ravichandran V., Matsumura F., Ito M., Spinelli B., and Kelly K. The GTP binding proteins Gem and Rad are negative regulators of the Rho-Rho kinase pathway. J. Cell Biol. 157 (2002) 291-302
103. Watson W.E. Cellular responses to axotomy and to related procedures. Br. Med. Bull. 30 (1974) 112-115
104. Westerfield M. The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio). 4th ed. (2000), Univ. of Oregon Press, Eugene
105. Yamada K., and Miyamoto K. Basic helix-loop-helix transcription factors, BHLHB2 and BHLHB3; their gene expressions are regulated by multiple extracellular stimuli. Front. Biosci. 10 (2005) 3151-3171
106. Yamashita T., Fujitani M., Yamagishi S., Hata K., and Mimura F. Multiple signals regulate axon regeneration through the nogo receptor complex. Mol. Neurobiol. 32 (2005) 105-111
107. Yin Y., Cui Q., Li Y., Irwin N., Fischer D., Harvey A.R., and Benowitz L.I. Macrophage-derived factors stimulate optic nerve regeneration. J. Neurosci. 23 (2003) 2284-2293
108. Zhang K., Shen X., Wu J., Sakaki K., Saunders T., Rutkowski D.T., Back S.H., and Kaufman R.J. Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 124 (2006) 587-599
109. Zhao G., Shi L., Qiu D., Hu H., and Kao P.N. NF45/ILF2 tissue expression, promoter analysis, and interleukin-2 transactivating function. Exp. Cell Res. 305 (2005) 312-323
110. Zujovic V., Luo D., Baker H.V., Lopez M.C., Miller K.R., Streit W.J., and Harrison J.K. The facial motor nucleus transcriptional program in response to peripheral nerve injury identifies Hn1 as a regeneration-associated gene. J. Neurosci. Res. 82 (2005) 581-591