STOP proteins are responsible for the high degree of microtubule stabilization observed in neuronal cells

Journal of Cell Biology

Volumn 142, Issue 1, 1998, Pages 167-179

  Guillaud, Laurent ^a   Bosc, Christophe ^a   Fourest Lieuvin, Anne ^a   Denarier, Eric ^a   Pirollet, Fabienne ^a   Lafanechère, Laurence ^a   Job, Didier ^a  

^a CEA GRENOBLE   (France)

Author keywords

Calmodulin; E STOP; Microtubule associated protein; Neuron; STOP

Indexed keywords

ANIMAL TISSUE; ARTICLE; CYTOSKELETON; EMBRYO; MICROTUBULE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN ISOLATION; PROTEIN STABILITY; RAT;

AMINO ACID SEQUENCE; ANIMALS; AXONS; CELLS, CULTURED; COLD; DRUG RESISTANCE; GANGLIA, SPINAL; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MOLECULAR SEQUENCE DATA; NEURONS; NOCODAZOLE; PC12 CELLS; RABBITS; RATS; TUBULIN; TYROSINE;

EID: 0032514256     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.142.1.167     Document Type: Article

References (57)

1. Baas, P.W., and F.J. Ahmad. 1992. The plus ends of stable microtubules are the exclusive nucleating structures for microtubules in the axon. J. Cell Biol. 116: 1231-1241.
2. Baas, P.W., and M.M. Black. 1990. Individual microtubules in the axon consist of domains that differ in both composition and stability. J. Cell Biol. 111: 495-509.
3. Baas, P.W., and S.R. Heidemann. 1986. Microtubule reassembly from nucleating fragments during the regrowth of amputated neurites. J. Cell Biol. 103: 917-927.
4. Baas, P.W., T.P. Pienkowski, K.A. Cimbalnik, K. Toyama, S. Bakalis, F.J. Ahmad, and K.S. Kosik. 1994. Tau confers drug stability but not cold stability to microtubules in living cells. J. Cell Sci. 107:135-143.
5. Barra, H.S., C.A. Arce, and C.E. Argaraña. 1988. Posttranslational tyrosination/detyrosination of tubulin. Mol. Neurobiol. 2:133-153.
6. Black, M.M., J.M. Cochran, and J.T. Kurdyla. 1984. Solubility properties of neuronal tubulin: evidence for labile and stable microtubules. Brain Res. 295:255-263.
7. Bosc, C., J.D. Cronk, F. Pirollet, M.D. Watterson, J. Haiech, D. Job, and R.L. Margolis. 1996. Cloning, expression and properties of the microtubule stabilizing protein STOP. Proc. Natl. Acad. Sci. USA. 93:2125-2130.
8. Bottenstein, J.E., and G.H. Sato. 1979. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc. Natl. Acad. Sci. USA. 76:514-517.
9. Brady, S.T., M. Tytell, and R.J. Lasek. 1984. Axonal tubulin and axonal microtubules: biochemical evidence for cold stability. J. Cell Biol. 99:1716-1724.
10. Brugg, B., D. Reddy, and A. Matus. 1993. Attenuation of microtubule-associated protein 1B expression by antisense oligodeoxynucleotides inhibits initiation of neurite outgrowth. Neuroscience. 52:489-496.
11. Bulinski, J.C., and G.G. Gundersen. 1991. Stabilization and post-translational modification of microtubules during cellular morphogenesis. BioEssays. 13: 285-293.
12. Burgoyne, R.D., and M.A. Cambray-Deakin. 1988. The cellular neurobiology of neuronal development: the cerebellar granule cell. Brain Res. Rev. 13:77-101.
13. Burgoyne, R.D. 1991. Cytoskeleton is a major neuronal organelle. In The Neuronal Cytoskeleton. R.D. Burgoyne, editor. Wiley-Liss, Inc., New York. 1-3.
14. Caceres, A., J. Mautino, and K.S. Kosik. 1992. Suppression of MAP2 in cultured cerebellar macroneurons inhibits minor neurite formation. Neuron. 9:607-618.
15. Cambray-Deakin, M.A. 1991. Cytoskeleton of the growing axon. In The Neuronal Cytoskeleton. R.D. Burgoyne, editor. Wiley-Liss, Inc. New York. 233-255.
16. Denarier, E., M. Aguezzoul, C. Jolly, C. Vourc'h, A. Roure, A. Andrieux, C. Bosc, and D. Job. 1998a. Genomic structure and chromosomal mapping of the mouse STOP gene (Mtap6). Biochem. Biophys. Res. Commun. 243:791-796.
17. Denarier, E., A. Fourest-Lieuvin, C. Bosc, E. Pirollet, A. Chapel, R.L. Margolis, and D. Job. 1998b. Nonneuronal isoforms of stop protein are responsible for microtubule cold stability in mammalian fibroblasts. Proc. Natl. Acad. Sci. USA. 75:6055-6060.
18. Drubin, D.G., S.C. Feinstein, E.M. Shooter, and M.W. Kirschner. 1985. Nerve growth factor-induced neurite outgrowth in PC12 cells involves the coordinate induction of microtubule assembly and assembly-promoting factors. J. Cell Biol. 101:1799-1807.
19. Esmaeli-Azad, B., J.H. McCarty, and S.C. Feinstein. 1994. Sense and antisense transfection analysis of tau function: tau influences net microtubule assembly, neurite outgrowth and neuritic stability. J. Cell Sci. 107:869-879.
20. Funakoshi, T., S. Takeda, and N. Hirokawa. 1996. Active transport of photoactivated tubulin molecules in growing axons revealed by a new electron microscopic analysis. J. Cell Biol. 133:1347-1353.
21. Greene, L.A., and A.S. Tischler. 1976. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. USA. 73:2424-2428.
22. Hanemaaijer, R., and I. Ginzburg. 1991. Involvement of mature tau isoforms in the stabilization of neurites in PC12 cells. J. Neurosci. Res. 30:163-171.
23. Hirokawa, N. 1994. Microtubule organization and dynamics dependent on microtubule-associated proteins. Curr. Opin. Cell Biol. 6:74-81.
24. Job, D., E.H. Fischer, and R.E. Margolis. 1981. Rapid disassembly of cold-stable microtubules by calmodulin. Proc. Natl. Acad. Sci. USA. 78:4679-4682.
25. Job, D., C.T. Rauch, E.H. Fischer, and R.L. Margolis. 1982. Recycling of cold-stable microtubules: evidence that cold stability is due to substoichiometric polymer blocks. Biochemistry. 21:509-515.
26. Job, D., C.T. Rauch, E.H. Fischer, and R.E. Margolis. 1983. Regulation of microtubule cold stability by calmodulin-dependent and -independent phosphorylation. Proc. Natl. Acad. Sci. USA. 80:3894-3898.
27. Kreis, T.E. 1987. Microtubules containing detyrosinated tubulin are less dynamic. EMBO (Eur. Mol. Biol. Organ.) J. 6:2597-2606.
28. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
29. Li, Y., and M.M. Black. 1996. Microtubule assembly and turnover in growing axons. J. Neurosci. 16:531-544.
30. Lieuvin, A., J.-C. Labbé, M. Dorée, and D. Job. 1994. Intrinsic microtubule stability in interphase cells. J. Cell Biol. 124:985-996.
31. Lim, S.-S., P.J. Sammak, and G.G. Borisy. 1989. Progressive and spatially differentiated stability of microtubules in developing neuronal cells. J. Cell Biol. 109:253-263.
32. MacRae, T.H. 1997. Tubulin post-translational modifications-enzymes and their mechanisms of action. Eur. J. Biochem. 244:265-278.
33. Mandelkow, E., and E.-M. Mandelkow. 1995. Microtubules and microtubule-associated proteins. Curr. Opin. Cell Biol. 7:72-81.
34. Mandelkow, E.-M., J. Biernat, G. Drewes, N. Gustke, B. Trinczek, and E. Mandelkow. 1995. Tau domains, phosphorylation, and interactions with microtubules. Neurobiol. Aging. 16:355-362.
35. 145) with microtubule-stabilizing and motility behavior. Proc. Natl. Acad. Sci. USA. 83:639-643.
36. Morris, J.R., and R.J. Lasek. 1982. Stable polymers of the axonal cytoskeleton: the axoplasmic ghost. J. Cell Biol. 92:192-198.
37. Okabe, S., and N. Hirokawa. 1988. Microtubule dynamics in nerve cells: analysis using microinjection of biotinylated tubulin into PC12 cells. J. Cell Biol. 107:651-664.
38. Okabe, S., and N. Hirokawa. 1990. Turnover of fluorescently labeled tubulin and actin in the axon. Nature. 343:479-482.
39. Okabe, S., and N. Hirokawa. 1992. Differential behaviour of photoactivated microtubules in growing axons of mouse and frog neurons. J. Cell Biol. 117: 105-120.
40. Paturle-Lafanechère, L., B. Eddé, P. Denoulet, A. Van Dorsselaer, H. Mazarguil, J.-P. Le Caer, J. Wehland, and D. Job. 1991. Charaterization of a major brain tubulin variant which cannot be tyrosinated. Biochemistry. 30:10523-10528.
41. Paturle-Lafanechère, L., M. Manier, N. Trigault, F. Pirollet, H. Mazarguil, and D. Job. 1994. Accumulation of delta 2-tubulin, a major tubulin variant that cannot be tyrosinated, in neuronal tissues and in stable microtubule assemblies. J. Cell Sci. 107:1529-1543.
42. Pignot-Paintrand, I. 1992. Orientation of human spermatozoa for electron microscopy: a fast, simple method. Micros. Res. Tech. 21:75-76.
43. Pirollet, F., D. Job, E.H. Fischer, and R.L. Margolis. 1983. Purification and characterization of sheep brain cold-stable microtubules. Proc. Natl. Acad. Sci. USA. 80:1560-1564.
44. Pirollet, F., C.T. Rauch, D. Job, and R.L. Margolis. 1989. Monoclonal antibody to microtubule-associated STOP protein: affinity purification of neuronal STOP activity and comparison of antigen with activity in neuronal and nonneuronal cell extracts. Biochemistry. 28:835-842.
45. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, New York.
46. Schulze, E., D.J. Asai, J.C. Bulinski, and M. Kirschner. 1987. Posttranslational modification and microtubule stability. J. Cell Biol. 105:2167-2177.
47. Sekimoto, S., T. Tashiro, and Y. Komiya. 1995. Two stages in neurite formation distinguished by differences in tubulin metabolism. J Neurochem. 64:354-363.
48. Sharma, N., Y. Kress, and B. Shafit-Zagardo. 1994. Antisense MAP-2 oligonucleotides induce changes in microtubule assembly and neuritic elongation in pre-existing neurites of rat cortical neurons. Cell Motil. Cytoskelet. 27:234-247.
49. Shea, T.B., M.L. Beermann, R.A. Nixon, and I. Fischer. 1992. Microtubule-associated protein tau is required for axonal neurite elaboration by neuroblastoma cells. J. Neurosci. Res. 32:363-374.
50. Takeda, S., T. Funakoshi, and N. Hirokawa. 1995. Tubulin dynamics in neuronal axons of living zebrafish embryos. Neuron. 14:1257-1264.
51. Takemura, R., S. Okabe, T. Umeyama, Y. Kanai, N.J. Cowan, and N. Hirokawa. 1992. Increased microtubule stability and alpha tuhulin acetylation in cells transfected with microtubule-associated proteins MAP1B, MAP2 or tau. J. Cell Sci. 103:953-964.
52. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA. 76:4350-4354.
53. Webb, B.C., and L. Wilson. 1980. Cold-stable microtubules from brain. Biochemistry. 19:1993-2001.
54. Wehland, J., and K. Weber. 1987. Turnover of the carboxy-terminal tyrosine of α-tubulin and means of reaching elevated levels of detyrosination in living cells. J. Cell Sci. 88:185-203.
55. Yamada, K.M., B.S. Spooner, and N.K. Wessells. 1970. Axon growth: roles of microfilaments and microtubules. Proc. Natl. Acad. Sci. USA. 66:1206-1212.
56. Yu, W., and P.W. Baas. 1995. The growth of the axon is not dependent upon net microtubule assembly at its distal tip. J. Neurosci. 15: 6827-6833.
57. Yu, W., M.J. Schwei, and P.W. Baas. 1996. Microtubule transport and assembly during axon growth. J. Cell Biol. 133:151-157.