Developmental expression of a neuron-specific β-tubulin in frog (Xenopus laevis): A marker for growing axons during the embryonic period

Journal of Comparative Neurology

Volumn 364, Issue 2, 1996, Pages 219-230

  Moody, Sally A ^a   Miller, Vicky ^b   Spanos, Anthony ^b   Frankfurter, Anthony ^b  

^a GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

axonogenesis; brain; cytoskeleton; microtubule proteins; neurogenesis

Indexed keywords

BETA TUBULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; EMBRYO; EMBRYO DEVELOPMENT; GASTRULATION; GENE EXPRESSION; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; AXONS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; EMBRYO, NONMAMMALIAN; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; ISOMERISM; MOLECULAR SEQUENCE DATA; NEURONS; TIME FACTORS; TUBULIN; XENOPUS LAEVIS;

EID: 0030027299     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960108)364:2<219::AID-CNE3>3.0.CO;2-8     Document Type: Article

References (64)

1. Alexander, J.E., D.F. Hunt, M.K. Lee, J. Shabanowitz, H. Michel, S.C. Berlin. T.L. McDonald, R.J. Sundberg, L.I. Rebhun, and A. Frankfurter (1991) Characterization of posttranslational modifications in neuronspecific class III beta-tubulin by mass spectrometry. Proc. Natl. Acad. Sci. USA 89:4685-4689.
2. Banerjee, A., and R.F. Luduena (1991) Distinct colchicine binding kinetics of bovine brain tubulin lacking the type III isotype of beta-tubulin. J. Biol. Chem. 266:1888-1891.
3. Banerjee, A., M.C. Roach, K.A. Wall, M.A. Lopata, D.W. Cleveland, and R.F. Luduena (1988) A monoclonal antibody against the type II isotype of β-tubulin. J. Biol. Chem. 263:3029-3034.
4. Banerjee, A., M.C. Roach, P. Treka, and R.F. Luduena (1990) Increased microtubule assembly in bovine brain tubulin lacking the type III isotype of beta-tubulin. J. Biol. Chem. 265:1794-1799.
5. Binder, L.I., A. Frankfurter, and L.I. Rebhun (1986) Differential localization of MAP2 and tau in mammalian neurons in situ. Dynamic aspects of microtubule biology. Ann. N.Y. Acad. Sci. 466:145-166.
6. Boucher, D., J.C. Larcher, F. Gros, and P. Denoulet (1994) Polyglutamylation of tubulin as a progressive regulator of in vitro interactions between the microtubule-associated protein tau and tubulin. Biochemistry 33: 12471-12477.
7. Burgoyne, R.D., M.A. Cambray-Deakin, S. Lewis, S. Sarkar, and N.J. Cowan (1988) Differential distribution of β-tubulin isotypes in cerebellum. EMBO J. 7:2311-2319.
8. Burns. R. (1991) α-, β- and Γ-tubulins: Sequence comparisons and structural constraints. Cell. Motil. Cytoskel. 20:181-189.
9. Charnas, L.R., B.G. Szaro, and H. Gainer (1992) Identification and developmental expression of a novel low molecular weight neuronal intermediate filament protein expressed in Xenopus laevis. J. Neurosci. 72:3010-3024.
10. Cleveland, D.W., M.A. Lopata, R.J. MacDonald, N.J. Cowan, W.J. Rutter, and M.W. Kirschner (1980) Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta- and gamma-actin genes using specific cloned cDNA probes. Cell 20:95-105.
11. Craig, A.M., and G. Banker (1994) Neuronal polarity. Annu. Rev. Neurosci. 17:267-310.
12. Dodd, J., S.B. Morton, D. Karagogeos, M. Yamamoto, and T.M. Jessell (1988) Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron 1:105-116.
13. Dotti, C.G., C.A. Sullivan, and G.A. Banker (1988) The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8:1454-1468.
14. Dunn, M.J. (1987) Two-dimensional gel electrophoresis of proteins. J. Chromatogr. 418:145-185.
15. Dworkin-Rastl, E., D.B. Kelley, and M.B. Dworkin (1986) Localization of specific mRNA sequences in Xenopus laevis embryos by in situ hybridization. J. Embryol. Exp. Morphol. 57:153-168.
16. Easter, S.S. Jr., L.S. Ross, and A. Frankfurter (1993) Initial tract formation in the mouse brain. J. Neurosci. 13:285-299.
17. Good, P.J., K. Richter, and I.E. Dawid (1989) The sequence of a nervous system-specific, class II β-tubulin gene from Xenopus laevis. Nucleic Acids Res. 17:8000.
18. Hagiwara, H., H. Yorifuji, R. Sato-Yoshitake, and N. Hirokowa (1994) Competition between motor molecules (kinesin and cytoplasmic dynein) and fibrous microtubule-associated proteins in binding to microtubules. J. Biol. Chem. 269:3581-3589.
19. Hall, A.K., A. Frankfurter, and S.J. Piszczkiewicz (1993) Neuron-specific class III beta-tubulin is expressed by dividing neuron precursors. Soc. Neurosci. Abstr. 79:1710.
20. Hall, J.L., L. Dudley, P.R. Dobner, S.A. Lewis, and N.J. Cowan (1983) Identification of two human beta-tubulin isotypes. Mol. Cell. Biol. 3:854-862.
21. Hartenstein, V. (1993) Early pattern of neuronal differentiation in the Xenopus embryonic brainstem and spinal cord. J. Comp. Neurol. 328:213-231.
22. Hayes, B.P., and A. Roberts. (1983) The anatomy of two functional types of mechanoreceptive "free" nerve-endings in the head skin of Xenopus embryos. Proc. R. Soc. London B. 218:61-76.
23. Hemmsati-Brivanlou, A., R.W. Mann, and R.M. Harland (1992) A protein expressed in the growth cones of embryonic vertebrate neurons defines a new class of intermediate filament protein. Neuron 3:417-428.
24. Huffman, P., and D.W. Cleveland (1988) Neurofilament and tubulin expression recapitulates the developmental program during axonal regeneration: Induction of a specific β-tubulin isotype. Proc. Natl. Acad. Sci. USA 35:4530-4533.
25. Holt, C. E., and WA. Harris (1983) Order in the initial retinotectal map in Xenopus: A new technique for labeling growing fibers. Nature 307:150-152.
26. Hoyle, H.D., and E.C. Raff (1990) Two Drosophila beta-tubulin isoforms are not functionally equivalent. J. Cell Biol. 111:1009-1026.
27. Hughes, A.F.W. (1968) Aspects of Neural Ontogeny. New York: Academic Press.
28. Jacobson, M., and S. Huang (1985) Neurite outgrowth traced by means of horseradish peroxidase inherited from neuronal ancestral cells in frog embryos. Dev. Biol. 220:102-113.
29. Jessell, T.M., M.A. Hynes, and J. Dodd (1990) Carbohydrate and carbohydrate-binding proteins in the nervous system. Annu. Rev. Neurosci. 73:227-255.
30. Joshi, H.C., and D.W. Cleveland (1989) Differential utilization of the available β-tubulin isotypes in differentiating neuntes. J. Cell Biol. 109:663-673.
31. Katsetos, C.D., A. Frankfurter, S. Christakos, E.L. Mancolly, I.N. Vlachos, and H. Urich (1993) Differential localization of class III, beta-tubulin isotype and calbindin-D28k defines distinct neuronal types in the developing human cerebellar cortex. J. Neuropathol. Exp. Neurol. 52:665-666.
32. Kullberg, R.W., T.L. Lenz, and M.W. Cohen (1977) Development of the myotomal neuromuscular junction in Xenopus laeuis: An electrophysiological and fine-structural study. Dev. Biol. 60:101-129.
33. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
34. Lamborghini, E.J. (1980) Rohon-Beard cells and other large neurons in Xenopus embryos originate during gastrulation. J. Comp. Neurol. 189: 323-333.
35. Lee, M.G., S.A. Lewis, C.D. Wilde, and N.J. Cowan (1983) Evolutionary history of a multigene family: An expressed human beta-tubulin gene and three processed pseudogenes. Cell 33:477-487.
36. Lee, M.K., L.I. Rebhun, and A. Frankfurter (1990a) Posttranslational modification of class III beta-tubulin. Proc. Natl. Acad. Sci. USA 87:7195-7199.
37. Lee, M.K., J.B. Tuttle, L.I. Rebhun, D.W. Cleveland, and A. Frankfurter (1990b) The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell. Motil. Cytoskel. 17:118-132.
38. Lewis, S.A., M.G. Lee, and N.J. Cowan (1985) Five mouse tubulin isotypes and their regulated expression during development. J. Cell Biol.202:852-861.
39. Lopata, M.A., and D.W. Cleveland (1987) In vivo microtubules are copolymers of available beta-tubulin isotypes: Localisation of each of six vertebrate beta-tubulin isotypes using polyclonal antibodies elicited by synthetic peptide antigens. J. Cell Biol. 205:11707-11720.
40. Marya, P.K., Z. Syed, P.E. Fraylich, and P.A. Eagles (1994) Kinesin and tau bind to distinct sites on microtubules. J. Cell Sci. 207:399-414.
41. McLean, I.W., and P.K. Nakane (1974) Periodate-lysine-paraformaldehyde fixative: A new fixative for immunoelectron microscopy. J. Histochem. Cytochem. 22:1077-1083.
42. Menezes, J.R.L., and M.B. Luskin (1993) The expression of neuron-specific class III β-tubulin defines a novel population of neurons in the proliferative zones of the developing cerebral cortex. Soc. Neurosci. Abstr. 10:29.
43. Moody, S.A., M.S. Quigg, and A. Frankfurter (1989) Development of peripheral trigeimnal system in the chick revealed by an isotype-specific anti-β-tubulin monoclonal antibody. J. Comp. Neurol. 279:567-580.
44. Nordlander, R.H. (1984) Developing descending neurons of the early Xenopus tail spinal cord. J. Comp. Neurol. 228:117-128.
45. Nordlander, R.H. (1993) Cellular and subcellular distribution of HNK-1 immunoreactivity in the neural tube of Xenopus. J. Comp. Neurol. 335:538-551.
46. Nordlander, R.H., S.T. Baden, and T.M.J. Ryba (1985) Development of early brainstem projections to the tail spinal cord of Xenopus. J. Comp. Neurol. 232:519-529.
47. Oschwald, R., K. Richter, and H. Grunz (1991) Localization of a nervous system-specific class II β-tubulin gene in Xenopus laevis embryos by whole-mount in situ hybridization. Int. J. Dev. Biol. 35:399-405.
48. Richter, K., H. Grunz, and I.B. Dawid (1988) Gene expression in the embryonic nervous system of Xenopus laevis. Proc. Natl. Acad. Sci. USA 85:8086-8090.
49. Roberts, A., and J.D.W. Clarke (1982) The neuroanatomy of an amphibian embryo spinal cord. Phil. Trans. R. Soc. London [Biol.] 196:195-212.
50. Roberts, A., S.R. Soffe, J.D.W. Clarke, and N. Dale (1983) Initiation and control of swimming in amphibian embryos. In A. Roberts and B.L. Roberts (eds): Neural Origin of Rhythmic Movements. Cambridge: Cambridge University Press, pp. 261-284.
51. 3, a Xenopus peripherin gene, requires an inductive signal for enhanced expression in anterior neural tissue. Development 207:701-714.
52. Sonderegger, P., and F.G. Rathjen (1992) Regulation of axonal growth in the vertebrate nervous system by interactions between glycoproteins belonging to two groups of the immunoglobin superfamily. J. Cell Biol. 119.1387-1394.
53. 4 integrin mRNA and protein and fibronectin in the early chicken embryo. Cell Adhesion Commun. 2:359-375.
54. Sternberger, L.A. (1986) Immunocytochemistry. New York: John Wiley and Sons.
55. Sullivan, K.F., (1988) Structure and utilization of tubulin isotypes. Annu. Rev. Cell Biol. 4:687-716.
56. Sullivan, K.F., and D.W. Cleveland (1986) Identification of conserved isotype-defining variable region sequences for four vertebrate beta-tubulin polypeptide classes. Proc. Natl. Acad. Sci. USA 83:4327-4331.
57. Szaro, B.C., V. Lee, and H. Gainer (1989) Spatial and temporal expression of phosphorylated and nonphosphorylated forms of neurofilament proteins in the developing nervous system of Xenopus laevis. Dev. Brain Res. 45:87-103.
58. Taylor, J.S.H., and A. Roberts (1983) The early development of the primary sensory neurons in the amphibian embryo. A scanning electron microscope study. J. Embryol. Exp. Morphol. 75:49-66.
59. ten Donkelaar, H.J., and R. de Boer-van Huizen (1982) Observations on the development of descending pathways from the brainstem to the spinal cord in the clawed toad Xenopus laevis. Anat. Embryol. 163:461-473.
60. van Mier, P., and H.J. ten Donkelaar (1984) Early development of descending pathways from the brainstem to the spinal cord in Xenopus laevis. Anat. Embryol. 170:295-306.
61. van Mier, P., and H.J. ten Donkelaar (1989) Structural and functional properties of reticulospinal neurons in the early-swimming stage Xenopus embryo. J. Neurosci. 9:25-37.
62. van Mier, P., H.W.J. Joosten, R. van Rheden, and H.J. ten Donkelaar (1986) The development of serotonegic raphe-spinal projections in Xenopus laevis. Int. J. Dev. Neurosci. 4:465-475.
63. Wilson, S.W., L.S. Ross, T. Parrett, and S.S. Easter (1990) The development of a simple scaffold of axon tracts in the brain of the embryonic zebrafish, Brachydanio rerio. Development 208:121-145.
64. Wormington, M. (1993) Poly (A) and translation: Developmental control. Curr. Opin. Cell Biol. 5:950-954.