Metamorphosis and the regenerative capacity of spinal cord axons in Xenopus laevis

European Journal of Neuroscience

Volumn 33, Issue 1, 2011, Pages 9-25

  Gibbs, Kurt M ^a   Chittur, Sridar V ^a   Szaro, Ben G ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Axon regeneration; Microarray; Spinal cord injury; Thyroid hormone

Indexed keywords

LIOTHYRONINE; NEUROFILAMENT M PROTEIN; NEUROMODULIN; NEUROTENSIN; PERIPHERIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; THIAMAZOLE; THYROID HORMONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; METAMORPHOSIS; MICROARRAY ANALYSIS; NERVE CELL PLASTICITY; NERVE FIBER; NERVE FIBER GROWTH; NERVE REGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAPHE NUCLEUS; RETICULAR FORMATION; RHOMBENCEPHALON; SEROTONINERGIC NERVE CELL; SPINAL CORD INJURY; SPINAL CORD TRANSSECTION; TADPOLE; THYROID HORMONE BLOOD LEVEL; UPREGULATION; WOUND HEALING; XENOPUS LAEVIS;

ANIMALS; ANTITHYROID AGENTS; AXONS; BEHAVIOR, ANIMAL; CELL MOVEMENT; GENE EXPRESSION PROFILING; METAMORPHOSIS, BIOLOGICAL; METHIMAZOLE; MICROARRAY ANALYSIS; RECOVERY OF FUNCTION; RHOMBENCEPHALON; SPINAL CORD; SPINAL CORD INJURIES; SPINAL CORD REGENERATION; THYROID HORMONES; TRIIODOTHYRONINE; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 78650762068     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07477.x     Document Type: Article

References (86)

1. Arber, S., Ladle, D.R., Lin, J.H., Frank, E. & Jessell, T.M. (2000) ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell, 101, 485-498.
2. Asch, W.S., Leake, D., Canger, A.K., Passini, M.A., Argenton, F. & Schechter, N. (1998) Cloning of zebrafish neurofilament cDNAs for plasticin and gefiltin: increased mRNA expression in ganglion cells after optic nerve injury. J. Neurochem., 71, 20-32.
3. Beattie, M.S., Bresnahan, J.C. & Lopate, G. (1990) Metamorphosis alters the response to spinal cord transection in Xenopus laevis frogs. J. Neurobiol., 21, 1108-1122.
4. Becker, T., Bernhardt, R.R., Reinhard, E., Wullimann, M.F., Tongiorgi, E. & Schachner, M. (1998) Readiness of zebrafish brain neurons to regenerate a spinal axon correlates with differential expression of specific cell recognition molecules. J. Neurosci., 18, 5789-5803.
5. Brown, D.D. & Cai, L. (2007) Amphibian metamorphosis. Dev. Biol., 306, 20-33.
6. Brown, D.D., Wang, Z., Kanamori, A., Eliceiri, B., Furlow, J.D. & Schwartzman, R. (1995) Amphibian metamorphosis: a complex program of gene expression changes controlled by the thyroid hormone. Recent Prog. Horm. Res., 50, 309-315.
7. Brown, D.D., Wang, Z., Furlow, J.D., Kanamori, A., Schwartzman, R.A., Remo, B.F. & Pinder, A. (1996) The thyroid hormone-induced tail resorption program during Xenopus laevis metamorphosis. Proc. Natl. Acad. Sci. USA, 93, 1924-1929.
8. Buchholz, D.R., Heimeier, R.A., Das, B., Washington, T. & Shi, Y.B. (2007) Pairing morphology with gene expression in thyroid hormone-induced intestinal remodeling and identification of a core set of TH-induced genes across tadpole tissues. Dev. Biol., 303, 576-590.
9. Buckbinder, L. & Brown, D.D. (1993) Expression of the Xenopus laevis prolactin and thyrotropin genes during metamorphosis. Proc. Natl. Acad. Sci. USA, 90, 3820-3824.
10. Consolazione, A., Milstein, C., Wright, B. & Cuello, A.C. (1981) Immunocytochemical detection of serotonin with monoclonal antibodies. J. Histochem. Cytochem., 29, 1425-1430.
11. Damjanovski, S., Ishizuya-Oka, A. & Shi, Y.B. (1999) Spatial and temporal regulation of collagenases-3, -4, and stromelysin -3 implicates distinct functions in apoptosis and tissue remodeling during frog metamorphosis. Cell Res., 9, 91-105.
12. Das, B., Heimeier, R.A., Buchholz, D.R. & Shi, Y.B. (2009) Identification of direct thyroid hormone response genes reveals the earliest gene regulation programs during frog metamorphosis. J. Biol. Chem., 284, 34167-34178.
13. Delgermaa, L., Hayashi, N., Dorjsuren, D., Nomura, T., Thuy le, T.T. & Murakami, S. (2004) Subcellular localization of RPB5-mediating protein and its putative functional partner. Mol. Cell. Biol., 24, 8556-8566.
14. Dent, J.N. (1962) Limb regeneration in larvae and metamorphosing individuals of the South African clawed toad. J. Morphol., 110, 61-77.
15. Denver, R.J. (2008) Chordate metamorphosis: ancient control by iodothyronines. Curr. Biol., 18, R567-R569.
16. Denver, R.J., Pavgi, S. & Shi, Y.B. (1997) Thyroid hormone-dependent gene expression program for Xenopus neural development. J. Biol. Chem., 272, 8179-8188.
17. Di Giovanni, S., Knights, C.D., Rao, M., Yakovlev, A., Beers, J., Catania, J., Avantaggiati, M.L. & Faden, A.I. (2006) The tumor suppressor protein p53 is required for neurite outgrowth and axon regeneration. EMBO J., 25, 4084-4096.
18. Dodd, M.H.I. & Dodd, J.M. (1976) The biology of metamorphosis. In Lofts, B. (Ed.), Physiology of the Amphibia. Academic Press, New York, pp. 467-576.
19. Etkin, W. & Gilbert, L.I. (1968) Metamorphosis. A Problem in Developmental Biology. Appleton-Century-Crofts, New York.
20. Feng, L., Hatten, M.E. & Heintz, N. (1994) Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron, 12, 895-908.
21. Forehand, C.J. & Farel, P.B. (1982) Anatomical and behavioral recovery from the effects of spinal cord transection: dependence on metamorphosis in anuran larvae. J. Neurosci., 2, 654-662.
22. Gervasi, C. & Szaro, B.G. (1997) Sequence and expression patterns of two forms of the middle molecular weight neurofilament protein (NF-M) of Xenopus laevis. Brain Res. Mol. Brain Res., 48, 229-242.
23. Gervasi, C., Thyagarajan, A. & Szaro, B.G. (2003) Increased expression of multiple neurofilament mRNAs during regeneration of vertebrate central nervous system axons. J. Comp. Neurol., 461, 262-275.
24. Gibbs, K.M. & Szaro, B.G. (2006) Regeneration of descending projections in Xenopus laevis tadpole spinal cord demonstrated by retrograde double labeling. Brain Res., 1088, 68-72.
25. Goldshmit, Y., Walters, C.E., Scott, H.J., Greenhalgh, C.J. & Turnley, A.M. (2004) SOCS2 induces neurite outgrowth by regulation of epidermal growth factor receptor activation. J. Biol. Chem., 279, 16349-16355.
26. Gudernatsch, J.F. (1912) Feeding experiments in Tadpoles. I. The influence of specific organs given as on growth and differentiation: a contribution to the knowledge of organs with internal secretion. Arch. Ent.-mech. Org., 35, 457-483.
27. Hasan, S.J., Keirstead, H.S., Muir, G.D. & Steeves, J.D. (1993) Axonal regeneration contributes to repair of injured brainstem-spinal neurons in embryonic chick. J. Neurosci., 13, 492-507.
28. Hasegawa, K., Chang, W.W., Li, H., Berlin, Y., Ikeda, O., Kane-Goldsmith, N. & Grumet, M. (2005) Embryonic radial glia bridge spinal cord lesions and promote functional recovery following spinal cord injury. Exp. Neurol., 193, 394-410.
29. Hevner, R.F., Daza, R.A., Rubenstein, J.L., Stunnenberg, H., Olavarria, J.F. & Englund, C. (2003) Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Dev. Neurosci., 25, 139-151.
30. p) in Xenopus laevis. J. Embryol. Exp. Morphol., 34, 253-264.
31. Horlein, A.J., Naar, A.M., Heinzel, T., Torchia, J., Gloss, B., Kurokawa, R., Ryan, A., Kamei, Y., Soderstrom, M. & Glass, C.K. (1995) Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature, 377, 397-404.
32. Howdeshell, K.L. (2002) A model of the development of the brain as a construct of the thyroid system. Environ. Health Perspect., 110(Suppl. 3), 337-348.
33. Hutson, L.D. & Bothwell, M. (2001) Expression and function of Xenopus laevis p75(NTR) suggest evolution of developmental regulatory mechanisms. J. Neurobiol., 49, 79-98.
34. Jacobs, A.J., Swain, G.P., Snedeker, J.A., Pijak, D.S., Gladstone, L.J. & Selzer, M.E. (1997) Recovery of neurofilament expression selectively in regenerating reticulospinal neurons. J. Neurosci., 17, 5206-5220.
35. Jacobson, R.D., Virag, I. & Skene, J.H. (1986) A protein associated with axon growth, GAP-43, is widely distributed and developmentally regulated in rat CNS. J. Neurosci., 6, 1843-1855.
36. Johnson, K.G., McKinnell, I.W., Stoker, A.W. & Holt, C.E. (2001) Receptor protein tyrosine phosphatases regulate retinal ganglion cell axon outgrowth in the developing Xenopus visual system. J. Neurobiol., 49, 99-117.
37. Knerlich-Lukoschus, F., Juraschek, M., Blomer, U., Lucius, R., Mehdorn, H.M. & Held-Feindt, J. (2008) Force-dependent development of neuropathic central pain and time-related CCL2/CCR2 expression after graded spinal cord contusion injuries of the rat. J. Neurotrauma, 25, 427-448.
38. Kollros, J.J. (1981) Transitions in the nervous system during amphibian metamorphosis. In Gilbert, L.I. & Frieden, E. (Eds), Metamorphosis: A Problem in Developmental Biology. Plenum Press, New York, pp. 445-459.
39. Lancaster, C.A., Taylor-Harris, P.M., Self, A.J., Brill, S., van Erp, H.E. & Hall, A. (1994) Characterization of rhoGAP. A GTPase-activating protein for rho-related small GTPases. J. Biol. Chem., 269, 1137-1142.
40. Leloup, J. & Buscaglia, M. (1977) La triiodothyronine, hormone de la metamorphose des Amphibiens. C. R. Acad. Sci, 284, 2261-2263.
41. Lin, W. & Szaro, B.G. (1994) Maturation of neurites in mixed cultures of spinal cord neurons and muscle cells from Xenopus laevis embryos followed with antibodies to neurofilament proteins. J. Neurobiol., 25, 1235-1248.
42. ΔΔ method. Methods, 25, 402-408.
43. Marsh-Armstrong, N., Cai, L. & Brown, D.D. (2004) Thyroid hormone controls the development of connections between the spinal cord and limbs during Xenopus laevis metamorphosis. Proc. Natl. Acad. Sci. USA, 101, 165-170.
44. Mazella, J., Zsurger, N., Navarro, V., Chabry, J., Kaghad, M., Caput, D., Ferrara, P., Vita, N., Gully, D., Maffrand, J.P. & Vincent, J.P. (1998) The 100-kDa neurotensin receptor is gp95/sortilin, a non-G-protein-coupled receptor. J. Biol. Chem., 273, 26273-26276.
45. Michel, M.E. & Reier, P.J. (1979) Axonal-ependymal associations during early regeneration of the transected spinal cord in Xenopus laevis tadpoles. J. Neurocytol., 8, 529-548.
46. van Mier, P. & Ten Donkelaar, H.J. (1984) Early development of descending pathways from the brain stem to the spinal cord in Xenopus laevis. Anat. Embryol. (Berl.), 170, 295-306.
47. van Mier, P., Joosten, H.W., van Rheden, R. & Ten Donkelaar, H.J. (1986) The development of serotonergic raphespinal projections in Xenopus laevis. Int. J. Dev. Neurosci., 4, 465-475.
48. Milstein, C., Wright, B. & Cuello, A.C. (1983) The discrepancy between the cross-reactivity of a monoclonal antibody to serotonin and its immunohistochemical specificity. Mol. Immunol., 20, 113-123.
49. Muchow, M., Bossis, I. & Porter, T.E. (2005) Ontogeny of pituitary throtrophs and regulation by endogenous thryoid hormone feedback in the chick embryo. J. Endocrinol., 184, 407-416.
50. Nakanishi, H. (2003) Microglial functions and proteases. Mol. Neurobiol., 27, 163-176.
51. Nieuwkoop, P.D. & Faber, J. (1994) Normal Table of Xenopus laevis (Daudin). Garland, New York.
52. Norris, C.R. & Kalil, K. (1991) Guidance of callosal axons by radial glia in the developing cerebral cortex. J. Neurosci., 11, 3481-3492.
53. Nykjaer, A., Lee, R., Teng, K.K., Jansen, P., Madsen, P., Nielsen, M.S., Jacobsen, C., Kliemannel, M., Schwarz, E., Willnow, T.E., Hempstead, B.L. & Petersen, C.M. (2004) Sortilin is essential for proNGF-induced neuronal cell death. Nature, 427, 843-848.
54. Paulsen, S.J., Larsen, L.K., Jelsing, J., Janssen, U., Gerstmayer, B. & Vrang, N. (2009) Gene expression profiling of individual hypothalamic nuclei from single animals using laser capture microdissection and microarrays. J. Neurosci. Methods, 177, 87-93.
55. Piessevaux, J., Lavens, D., Montoye, T., Wauman, J., Catteeuw, D., Vandekerckhove, J., Belsham, D., Peelman, F. & Tavernier, J. (2006) Functional cross-modulation between SOCS proteins can stimulate cytokine signaling. J. Biol. Chem., 281, 32953-32966.
56. Raymond, P.A., Barthel, L.K., Bernardos, R.L. & Perkowski, J.J. (2006) Molecular characterization of retinal stem cells and their niches in adult zebrafish. BMC Dev. Biol., 6, 36.
57. Rehermann, M.I., Marichal, N., Russo, R.E. & Trujillo-Cenoz, O. (2009) Neural reconnection in the transected spinal cord of the freshwater turtle Trachemys dorbignyi. J. Comp. Neurol., 515, 197-214.
58. Sachs, L. (1984) Applied Statistics: A Handbook of Techniques. Springer-Verlag, New York.
59. Saunders, N.R., Balkwill, P., Knott, G., Habgood, M.D., Mollgard, K., Treherne, J.M. & Nicholls, J.G. (1992) Growth of axons through a lesion in the intact CNS of fetal rat maintained in long-term culture. Proc. Biol. Sci., 250, 171-180.
60. Shaw, G. (1992) A neurofilament-specific sequence motif. Trends Biochem. Sci., 17, 3405.
61. Shi, Y.B. (2000) Amphibian Metamorphosis: From Morphology to Molecular Biology. Wiley-Liss, New York.
62. Shi, Y.B. (2009) Dual functions of thyroid hormone receptors in vertebrate development: the roles of histone-modifying cofactor complexes. Thyroid, 19, 987-999.
63. Shi, Y.B. & Brown, D.D. (1993) The earliest changes in gene expression in tadpole intestine induced by thyroid hormone. J. Biol. Chem., 268, 20312-20317.
64. Simon, R., Tietge, J.E., Michalke, B., Degitz, S. & Schramm, K.W. (2002) Iodine species and the endocrine system: thyroid hormone levels in adult Danio rerio and developing Xenopus laevis. Anal. Bioanal. Chem., 372, 481-485.
65. Sims, R.T. (1962) Transection of the spinal cord in developing Xenopus laevis. J. Embryol. Exp. Morphol., 10, 115-126.
66. Singer, M., Nordlander, R.H. & Egar, M. (1979) Axonal guidance during embryogenesis and regeneration in the spinal cord of the newt: the blueprint hypothesis of neuronal pathway patterning. J. Comp. Neurol., 185, 1-21.
67. Skene, J.H., Jacobson, R.D., Snipes, G.J., McGuire, C.B., Norden, J.J. & Freeman, J.A. (1986) A protein induced during nerve growth (GAP-43) is a major component of growth-cone membranes. Science, 233, 783-786.
68. St.Germain, D.L., Schwartzman, R.A., Croteau, W., Kanamori, A., Wang, Z., Brown, D.D. & Galton, V.A. (1994) A thyroid hormone-regulated gene in Xenopus laevis encodes a type III iodothyronine 5-deiodinase. Proc. Natl. Acad. Sci. USA, 91, 7767-7771.
69. Szaro, B.G. & Gainer, H. (1988) Immunocytochemical identification of non-neuronal intermediate filament proteins in the developing Xenopus laevis nervous system. Brain Res. Dev. Brain Res., 43, 207-224.
70. Szaro, B.G., Lee, V.M. & Gainer, H. (1989) Spatial and temporal expression of phosphorylated and non-phosphorylated forms of neurofilament proteins in the developing nervous system of Xenopus laevis. Brain Res. Dev. Brain Res., 48, 87-103.
71. Takahashi, K., Yoshida, N., Murakami, N., Kawata, K., Ishizaki, H., Tanaka-Okamoto, M., Miyoshi, J., Zinn, A.R., Shime, H. & Inoue, N. (2007) Dynamic regulation of p53 subnuclear localization and senescence by MORC3. Mol. Biol. Cell, 18, 1701-1709.
72. Takeda, A., Goris, R.C. & Funakoshi, K. (2007) Regeneration of descending projections to the spinal motor neurons after spinal hemisection in the goldfish. Brain Res., 1155, 17-23.
73. Tata, J.R. (2006) Amphibian metamorphosis as a model for the developmental actions of thyroid hormone. Mol. Cell. Endocrinol., 246, 10-20.
74. Taylor, J.S.H., Jack, J.L. & Easter, S.S. Jr (1989) Is the capacity for optic nerve regeneration related to continued retinal ganglion cell production in the frog? A test of the hypothesis that neurogenesis and axon regeneration are obligatorily linked. Eur. J. Neurosci., 1, 626-638.
75. Ten Donkelaar, H.J. (2000) Development and regenerative capacity of descending supraspinal pathways in tetrapods: a comparative approach. Adv. Anat. Embryol. Cell Biol., 154, 1-145.
76. Tompkins, R. (1977) Grafting analysis of the periodic albino mutant of Xenopus laevis. Dev. Biol., 57, 460-464.
77. Undamatla, J. & Szaro, B.G. (2001) Differential expression and localization of neuronal intermediate filament proteins within newly developing neurites in dissociated cultures of Xenopus laevis embryonic spinal cord. Cell Motil. Cytoskeleton, 49, 16-32.
78. Wang, Z. & Brown, D.D. (1993) Thyroid hormone-induced gene expression program for amphibian tail resorption. J. Biol. Chem., 268, 16270-16278.
79. Weiss, P. & Rosetti, F. (1951) Growth responses of opposite sign among different neuron types exposed to thyroid hormone. Proc. Natl. Acad. Sci. USA, 37, 540-546.
80. Wetzel, D.M., Lee, V.M. & Erulkar, S.D. (1989) Long-term cultures of neurons from adult frog brain express GABA and glutamate-activated channels. J. Neurobiol., 20, 255-270.
81. Will, U. (1986) Mauthner neurons survive metamorphosis in anurans: a comparative HRP study on the cytoarchitecture of Mauthner neurons in amphibians. J. Comp. Neurol., 244, 111-120.
82. Yoshida, K., Suzuki, Y., Yamamoto, K. & Sinohara, H. (1999) cDNA sequencing of guinea pig alpha 2-HS glycoprotein, its expression in various tissues and acute phase expression. Biol. Chem., 380, 95-99.
83. Zhang, L. & McClellan, A.D. (1999) Axonal regeneration of descending brain neurons in larval lamprey demonstrated by retrograde double labeling. J. Comp. Neurol., 410, 612-626.
84. Zhang, S., Xia, Y.Y., Lim, H.C., Tang, F.R. & Feng, Z.W. (2010) NCAM-mediated locomotor recovery from spinal cord contusion injury involves neuroprotection, axon regeneration, and synaptogenesis. Neurochem. Int., 56, 919-929.
85. Zhao, Y. & Szaro, B.G. (1994) The return of phosphorylated and nonphosphorylated epitopes of neurofilament proteins to the regenerating optic nerve of Xenopus laevis. J. Comp. Neurol., 343, 158-172.
86. Zottoli, S.J. & Freemer, M.M. (2006) Recovery of C-starts, equilibrium and targeted feeding after whole spinal cord crush in the adult goldfish Carassius auratus. J. Exp. Biol., 206, 3015-3029.