Stathmin and its phosphoprotein family: General properties, biochemical and functional interaction with tubulin

Cell Structure and Function

Volumn 24, Issue 5, 1999, Pages 345-357

  Curmi, Patrick A ^a   Gavet, Olivier ^a   Charbaut, Elodie ^a   Ozon, Sylvie ^a   Lachkar Colmerauer, Sylvie ^a   Manceau, Valérie ^a   Siavoshian, Samila ^a   Maucuer, Alexandre ^a   Sobel, André ^a  

^a INSTITUT DU FER À MOULIN   (France)

Author keywords

Microtubule dynamics; Protein phosphorylation; RB3; SCG10; SCLIP

Indexed keywords

NERVE PROTEIN; PHOSPHOPROTEIN; PROTEIN RB3; PROTEIN SCG10; PROTEIN SCLIP; REGULATOR PROTEIN; STATHMIN; TUBULIN; UNCLASSIFIED DRUG;

BINDING AFFINITY; BIOCHEMISTRY; CELL ACTIVITY; CELL DIFFERENTIATION; CELL PROLIFERATION; CONFERENCE PAPER; CYTOSOL; DEPOLYMERIZATION; DYNAMICS; GOLGI COMPLEX; HUMAN; INTERPHASE; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; BINDING SITES; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL DIVISION; HUMANS; MEMBRANE PROTEINS; MICROTUBULE PROTEINS; MICROTUBULES; MODELS, BIOLOGICAL; NERVE GROWTH FACTORS; NEURONS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BINDING; STATHMIN; TUBULIN;

EID: 0032751977     PISSN: 03867196     EISSN: None     Source Type: Journal    
DOI: 10.1247/csf.24.345     Document Type: Conference Paper

References (88)

1. ANDERSEN, S.S. 1999. Balanced regulation of microtubule dynamics during the cell cycle: a contemporary view. BioEssays, 21: 53-60.
2. ANDERSEN, S.S.L., ASHFORD, A.J., TOURNEBIZE, R., GAVET, O., SOBEL, A., HYMAN, A.A., and KARSENTI, E. 1997. Mitotic chromatin regulates phosphorylation of Stathmin/Op18. Nature, 389: 640-643.
3. ANDERSON, D.J. and AXEL, R. 1985. Molecular probes for the development and plasticity of neural crest derivatives. Cell, 42: 649-662.
4. ANTONSSON, B., KASSEL, D., DI PAOLO, G., LUTJENS, R., RIEDERER, B.M., and GRENNINGLOH, G. 1998. Identification of in vitro phosphorylation sites in the growth cone protein SCG10. Effect of phosphorylation site mutants on microtubule-destabilizing activity. J. Biol. Chem., 273: 8439-8446.
5. ANTONSSON, B., LUTJENS, R., DI PAOLO, G., KASSEL, D., ALLET, B., BERNARD, A., CATSICAS, S., and GRENNINGLOH, G. 1997. Purification, characterization, and in vitro phosphorylation of the neuron-specific membrane-associated protein SCG10. Protein Expr. Purif., 9: 363-371.
6. BALOGH, A., MEGE, R.M., and SOBEL, A. 1996. Cell density dependent expression of stathmin in C2 myoblasts in culture. Exp. Cell Res., 224: 8-15.
7. BEILHARZ, E.J., ZHUKOVSKY, E., LANAHAN, A.A., WORLEY, P.F., NIKOLICH, K., and GOODMAN, L.J. 1998. Neuronal activity induction of the stathmin-like gene RB3 in the rat hippocampus: possible role in neuronal plasticity. J, Neurosci., 18: 9780-9789.
8. BELMONT, L.D. and MITCHISON, T.J. 1996. Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell, 84: 623-631.
9. BERETTA, L., BAILLY, E., BORNENS, M., and SOBEL, A. 1992. Cell cycle-dependent phosphorylation of stathmin: hyperphosphorylation in mitosis on cdc2 and PKA substrate sites. In Contrôle de la Division Cellulaire, Lyon, France, 6-8 juillet 1992.
10. BERETTA, L., BOUTTERIN, M.C., DROUVA, S., and SOBEL, A. 1989. Phosphorylation of a group of proteins related to the physiological, multihormonal regulations of the various cell types in the anterior pituitary gland. Endocrinology, 125: 1358-1364.
11. BERETTA, L., BOUTTERIN, M.C., and SOBEL, A. 1988. Phosphorylation of intracellular proteins related to the multihormonal regulation of prolactin: comparison of normal anterior pituitary cells in culture with the tumor-derived GH cell lines. Endocrinology, 122: 40-51.
12. BERETTA, L., DOBRANSKY, T., and SOBEL, A. 1993. Multiple phosphorylation of stathmin: identification of four sites phosphorylated in intact cells, and in vitro by cyclic-AMP dependent protein kinase and p34cdc2. J. Biol. Chem., 268: 20076-20084.
13. BERETTA, L., DUBOIS, M.F., SOBEL, A., and BENSAUDE, O. 1995. Stathmin is a major substrate for MAP-kinase activated during heat-shock and chemical stress in HeLa cells. Eur. J. Biochem., 221: 388-395.
14. BIÈCHE, I., LACHKAR, S., BECETTE, V., CIFUENTES-DIAZ, C., SOBEL, A., LIDEREAU, R., and CURMI, P. 1998. Overexpression of the stathmin gene in a subset of human breast cancer. Br. J. Cancer, 78: 701-709.
15. BRATTSAND, G., MARKLUND, U., NYLANDER, K., ROOS, G., and GULLBERG, M. 1994. Cell-cycle-regulated phosphorylation of oncoprotein 18 on ser16, ser25, and ser38. Eur. J. Biochem., 220: 359-368.
16. BRATTSAND, G., Roos, G., MARKLUND, U., UEDA, H., LANDBERG, G., NANBERG, E., SIDERAS, P., and GULLBERG, M. 1993. Quantitative analysis of the expression and regulation of an activation-regulated phosphoprotein (oncoprotein 18) in normal and neoplastic cells. Leukemia, 7: 569-579.
17. CAMOLETTO, P., PERETTO, P., BONFANTI, L., MANCEAU, V., SOBEL, A., and FASOLO, A. 1997. The cytosolic phosphoprotein stathmin is expressed in the olfactory system of the adult rat. Neuroreport, 8: 2825-2829.
18. CHNEIWEISS, H., CORDIER, J., and SOBEL, A. 1992. Stathmin phosphorylation is regulated in striatal neurons by vasoactive intestinal peptide and monoamines via multiple intracellular pathways. J. Neurochem., 58: 282-289.
19. COOPER, H.L., MCDUFFIE, E., and BRAVERMAN, R. 1989. Human peripheral lymphocyte growth regulation and response to phorbol esters is linked to synthesis and phosphorylation of the cytosolic protein, prosolin. J. Immunol., 143: 956-963.
20. CURMI, P., MAUCUER, A., ASSELIN, S., LECOURTOIS, M., CHAFFOTTE, A., SCHMITTER, J.M., and SOBEL, A. 1994. Molecular characterization of human stathmin expressed in Escherichia coli: site-directed mutagenesis of two phosphorylatable serines (Ser-25 and Ser-63). Biochem. J., 300: 331-338.
21. CURMI, P.A., ANDERSEN, S.S.L., LACHKAR, S., GAVET, O., KARSENTI, E., KNOSSOW, M., and SOBEL, A. 1997. The stathmin-tubulin interaction in vitro. J. Biol. Chem., 272: 25029-25036.
22. DI PAOLO, G., ANTONSSON, B., KASSEL, D., RIEDERER, B.M., and GRENNINGLOH, G. 1997. Phosphorylation regulates the microtubule-destabilizing activity of stathmin and its interaction with tubulin. FEBS Lett., 416: 149-152.
23. DI PAOLO, G., LUTJENS, R., OSEN-SAND, A., SOBEL, A., CATSICAS, S., and GRENNINOLOH, G. 1997. Differential distribution of stathmin and SCG10 in developing neurons in culture. J. Neurosci. Res., 50: 1000-1009.
24. 2-terminal region. J. Biol. Chem., 272: 5175-5182.
25. DOYE, V., BOUTTERIN, M.C., and SOBEL, A. 1990. Phosphorylation of stathmin and other proteins related to nerve growth factor-induced regulation of PC12 cells. J. Biol. Chem., 265: 11650-11655.
26. DOYE, V., KELLERMANN, O., BUC-CARON, M.H., and SOBEL, A. 1992. High expression of stathmin in multipotential teratocarcinoma and normal embryonic cells versus their early differentiated derivatives. Differentiation, 50: 89-96.
27. DOYE, V., SOUBRIER, F., BAUW, G., BOUTTERIN, M.C., BERETTA, L., KOPPEL, J., VANDEKERCKHOVE, J., and SOBEL, A. 1989. A single cDNA encodes two isoforms of stathmin, a developmentally regulated neuron-enriched phosphoprotein. J. Biol. Chem., 264: 12134-12137.
28. FRIEDRICH, B., GRÖNBERG, H., LANDSTRÖM, M., BERGH, A., and GULLBERG, M. 1995. Differentiation-stage specific expression of oncoprotein 18 in human and rat prostatic adenocarcinoma. Prostate, 27: 102-109.
29. GAVET, O., OZON, S., MANCEAU, V., LAWLER, S., CURMI, P., and SOBEL, A. 1998. The stathmin phosphoprotein family: intracellular localization and effects on the microtubule network. J. Cell Sci., 111: 3333-3346.
30. GHOSH, P.K., ANDERSON, N.G., COHEN, P., TAKETO, M., ATWEH, G.F., and LEBOWITZ, P. 1993. Expression of the leukemia-associated gene p18 in normal and malignant tissues: inactivation of expression in a patient with cleaved B-cell lymphoma/leukemia. Oncogens, 8: 2869-2872.
31. GULLBERG, M., NOREUS, K., BRATTSAND, G., FRIEDRICH, B., and SHINGLER, V. 1990. Purification and characterization of a 19-kilodalton intracellular protein. J. Biol. Chem., 265: 17499-17505.
32. HAILAT, N., STRAHLER, J.R., MELHEM, R.F., ZHU, X.X., BRODEUR, G., SEEGER, R.C., REYNOLDS, C.P., and HANASH, S.M. 1990. N-myc gene amplification in neuroblastoma is associated with altered phosphorylation of a proliferation related polypeptide (Op18). Oncogene, 5: 1615-1618.
33. HANASH, S.M., STRAHLER, J.R., KUICK, R., CHU, E.H.Y., and NICHOLS, D. 1988. Identification of a polypeptide associated with the malignant phenotype in the acute leukemia. J. Biol. Chem., 263: 12813-12815.
34. HORWITZ, S.B., SHEN, H.-J., HE, L., DITTMAR, P., NEEF, R., CHEN, J., and SCHUBART, U.K. 1997. The microtubule-destabilizing activity of metablastin (p19) is controlled by phosphorylation. J. Biol. Chem., 272: 8129-8132.
35. HOWELL, B., DEACON, H., and CASSIMERIS, L. 1997. Injection of antibodies against Op18 results in decreased microtubule catastrophe and increased microtubule polymer in vivo. Mol. Biol. Cell, 8: 165a.
36. HOWELL, B., LARSSON, N., GULLBERG, M., and CASSIMERIS, L. 1999. Dissociation of the tubulin-sequestering and microtubule catastrophe-promoting activities of oncoprotein 18/Stathmin. Mol. Biol. Cell, 10: 105-118.
37. JEHA, S., LUO, X.N., BERAN, M., KANTARJIAN, H., and ATWEH, G.F. 1996. Antisense RNA inhibition of phosphoprotein p18 expression abrogates the transformed phenotype of leukemic cells. Cancer Res., 56: 1445-1450.
38. JOURDAIN, L., CURMI, P., SOBEL, A., PANTALONI, D., and CARLIER, M.F. 1997. Stathmin: a tubulin-sequestering protein which forms a ternary T2S complex with two tubulin molecules. Biochemistry, 36: 10817-10821.
39. KOPPEL, J., BOUTTERIN, M.C., DOYE, V., PEYRO-SAINT-PAUL, H., and SOBEL, A. 1990. Developmental tissue expression and phylogenetic conservation of stathmin, a phosphoprotein associated with cell regulations. J. Biol. Chem., 265: 3703-3707.
40. KOPPEL, J., LOYER, P., MAUCUER, A., REHÁK, P., MANCEAU, V., GUGUEN-GUILLOUZO, C., and SOBEL, A. 1993. Induction of stathmin expression during liver regeneration. FEBS Lett., 331: 65-70.
41. LARSSON, N., MARKLUND, U., GRADIN, H.M., BRATTSAND, G., and GULLBERG, M. 1997. Control of microtubule dynamics by oncoprotein 18: dissection of the regulatory role of multisite phosphorylation during mitosis. Mol. Cell Biol., 17: 5530-5539.
42. LARSSON, N., MELANDER, H., MARKLUND, U., OSTERMAN, O., and GULLBERG, M. 1995. G2/M transition requires multisite phosphorylation of oncoprotein 18 by two distinct protein kinase systems. J. Biol. Chem., 270: 14175-14183.
43. LARSSON, N., SEGERMAN, B., MELANDER GRADIN, H., WANDZIOCH, E., CASSIMERIS, L., and GULLBERG, M. 1999. Mutations of oncoprotein 18/stathmin identify tubulin-directed regulatory activities distinct from tubulin association. Mol. Cell Biol., 19: 2242-2250.
44. LAWLER, S. 1998. Microtubule dynamics: if you need a shrink try stathmin/Op18. Current Biology, 8: R212-R214.
45. LAWLER, S., GAVET, O., RICH, T., and SOBEL, A. 1998. Stathmin overexpression in 293 cells affects signal transduction and the cell cycle. FEBS Lett., 421: 55-60.
46. LE GOUVELLO, S., CHNEIWEISS, H., TARANTINO, M., DEBRÉ, P., and SOBEL, A. 1991. Stathmin phosphorylation patterns discriminate between distinct transduction pathways of human T lymphocyte activation through CD2 triggering. FEBS Lett., 287: 80-84.
47. 2+/calmodulin-dependent kinase II after CD2 triggering of human T lymphocytes. J. Immunol., 161: 1113-1122.
48. LEIGHTON, I., CURMI, P., CAMPBELL, D.G., COHEN, P., and SOBEL, A. 1993. The phosphorylation of stathmin by MAP kinase. Molec. Cellul. Biochem., 127/128: 151-156.
49. LETOURNEAU, P.C. and RESSLER, A.H. 1984. Inhibition of neurite initiation and growth by taxol. J. Cell Biol., 98: 1355-1362.
50. LI, L. and COHEN, S. 1996. tsg101: A Novel Tumor Susceptibility Gene Isolated by Controlled Homozygous functional Knockout of Allelic Loci in Mammalian Cells. Cell, 85: 319-329.
51. LI, L., LI, X., FRANCKE, U., and COHEN, S.N. 1997. The tsg101 tumor susceptibility gene is located in chromosome 11 band p15 and is mutated in human breast cancer. Cell, 88: 143-154.
52. cdc2 kinase. J. Biol. Chem., 269: 10312-10318.
53. MANCEAU, V., GAVET, O., CURMI, P., and SOBEL, A. 1999. Stathmin interaction with hsc70 family proteins. Electrophoresis, 20: 409-417.
54. MARKLUND, U., BRATTSAND, G., SCHINGLER, V., and GULLBERG, M. 1993. Serine 25 of oncoprotein 18 is a major cytosolic target for the mitogen-activated kinase. J. Biol. Chem., 268: 15039-15047.
55. 2+/calmodulin-dependent kinase-Gr. Eur. J. Biochem., 225: 53-60.
56. MARKLUND, U., LARSSON, N., MELANDER GRADIN, H., BRATTSAND, G., and GULLBERO, M. 1996. Oncoprotein 18 is a phosphorylation-responsive regulator of microtubule dynamics. EMBO J., 15: 5290-5298.
57. MARKLUND, U., OSTERMAN, O., MELANDER, H., BERGH, A., and GULLBERG, M. 1994. The phenotype of a "cdc2 kinase target site-deficient" mutant of oncoprotein 18 reveals a role of this protein in cell cycle control. J. Biol. Chem., 269: 30626-30635.
58. MATSUO, N., KAWAMOTO, S., MATSUBARA, K., and OKUBO, K. 1998. A novel SCG10-related gene uniquely expressed in the nervous system. Gene, 215: 477-481.
59. MAUCUER, A., CAMONIS, J.H., and SOBEL, A. 1995. Stathmin interaction with a novel putative kinase and coiled-coil forming protein domains. Proc. Natl. Acad. Sci. USA, 92: 3100-3104.
60. MAUCUER, A., DOYE, V., and SOBEL, A. 1990. A single amino acid difference distinguishes the human and the rat sequences of Stathmin, a ubiquitous intracellular phosphoprotein associated with cell regulations. FEBS Lett., 264: 275-278.
61. MAUCUER, A., MOREAU, J., MECHALI, M., and SOBEL, A. 1993. The Stathmin gene family: phylogenetic conservation and developmental regulation in Xenopus. J. Biol. Chem., 268: 16420-16429.
62. MAUCUER, A., OZON, S., MANCEAU, V., GAVET, O., LAWLER, S., CURMI, P., and SOBEL, A. 1997. KIS is a protein kinase with an RNA recognition motif. J. Biol. Chem., 272: 23151-23156.
63. MELANDER GRANDIN, H., LARSSON, N., MARKLUND, U., and GULLBERG, M. 1998. Regulation of microtubule dynamics by extracellular signals: cAMP-dependent protein kinase switches off the activity of Oncoprotein 18 in intact cells. J. Cell Biol., 140: 1-11.
64. 2+/calmodulin-dependent kinase IV/Gr-dependent phosphorylation of oncoprotein 18. Mol. Cell Biol., 17: 3459-3467.
65. MELHEM, R.F., ZHU, X.X., HAILAT, N., STRAHLER, J.R., and HANASH, S.M. 1991. Characterization of the gene for a proliferation-related phosphoprotein (oncoprotein 18) expressed in high amounts in acute leukemia. J. Biol. Chem., 266: 17747-17753.
66. MORI, N., STEIN, R., SIGMUND, O., and ANDERSON, D.J. 1990. A cell type-preferred silencer element that controls the neural-specific expression of the SCG10 gene. Neuron, 4: 583-594.
67. NGUYEN, H.L., GRUBER, D., MCGRAW, T., SHEETZ, M.P., and BULINSKI, J.C. 1998. Stabilization and functional modulation of microtubules by microtubule-associated protein 4. Biol. Bull., 194: 354-357.
68. NORTHRUP, S.H. and ERICKSON, H.P. 1992. Kinetics of protein-protein association explained by Brownian dynamics computer simulation. Proc. Natl. Acad. Sci. USA, 89: 3338-3342.
69. NYLANDER, K., MARKLUND, U., BRATTSAND, G., GULLBERG, M., and Roos, G. 1995. Immunohistochemical detection of oncoprotein 18 (Op18) in malignant lymphomas. Histochem. J., 27: 155-160.
70. OKAZAKI, T., HIMI, T., PETERSON, C., and MORI, N. 1993. Induction of stathmin mRNA during liver regeneration. FEBS Lett., 336: 8-12.
71. OZON, S., BYK, T., and SOBEL, A. 1998. SCLIP: a novel SCG10-like protein of the stathmin family expressed in the nervous system. J. Neurochem, 70: 2386-2396.
72. OZON, S., EL MESTIKAWY, S., and SOBEL, A. 1999. Differential, regional and cellular expression of the stathmin family transcripts in the adult rat brian. J. Neurosci. Res., 56: 553-564.
73. OZON, S., MAUCUER, A., and SOBEL, A. 1997. The stathmin family: molecular and biological characterization of novel mammalian proteins expressed in the nervous system. Eur. J. Biochem., 248: 794-806.
74. PESCHANSKI, M., DOYE, V., HIRSCH, E., MARTY, L., DUSART, I., MANCEAU, V., and SOBEL, A. 1993. Stathmin: cellular localization of a major phosphoprotein in the adult rat CNS, with a note on human forebrain. J. Comp. Neurol., 337: 655-668.
75. RIEDERER, B.M., PELLIER, V., ANTONSSON, B., DI PAOLO, G., STIMPSON, S.A., LÜTJENS, R., CATSICAS, S., and GRENNINGLOH, G. 1997. Regulation of microtubule dynamics by the neuronal growth-associated protein SCG10. Proc. Natl. Acad. Sci. USA, 94: 741-745.
76. ++-regulated cytoskeletal and cAMP-regulated cytosolic phosphoproteins by two-dimensional electrophoresis. J. Biol. Chem., 257: 12231-12238.
77. SCHUBART, U.K., ALAGO, W., JR., and DANOFF, A. 1987. Properties of p19, a novel cAMP-dependent protein kinase substrate protein purified from bovine brain. J. Biol. Chem., 262: 11871-11877.
78. SCHUBART, U.K., DAS BANERJEE, M., and ENG, J. 1989. Homology between the cDNAs encoding phosphoprotein pi9 and SCG10 reveals a novel mammalian gene family preferentially expressed in developing brain. DNA, 8: 389-398.
79. SCHUBART, U.K., XU, J., FAN, W., CHENG, G., GOLDSTEIN, H., ALPINI, G., SHAFRITZ, D.A., AMAT, J.A., FAROOK, M., NORTON, W.T., OWEN, T.A., LIAN, J.B.,and STEIN, G.S. 1992. Widespread differentiation stage-specific expression of the gene encoding phosphoprotein p19 (metablastin) in mammalian cells. Differentiation, 51: 21-32.
80. SCHUBART, U.K., Yu, J.H., AMAT, J.A., WANG, Z.Q., HOFFMANK, M.K., and EDELMANN, W. 1996. Normal development of mice lacking metablastin (P19), a phosphoprotein implicated in cell cycle regulation. J. Biol. Chem., 271: 14062-14066.
81. SOBEL, A. 1991. Stathmin: a relay phosphoprotein for multiple signal transduction? Trends Biochem. Sci., 16: 301-305.
82. SOBEL, A., BOUTTERIN, M.C., BERETTA, L., CHNEIWEISS, H., DOYE, V., and PEYRO-SAINT-PAUL, H. 1989. Intracellular substrates for extracellular signaling: characterization of a ubiquitous, neuron-enriched phosphoprotein (Stathmin). J. Biol. Chem., 264: 3765-3772.
83. SOBEL, A. and TASHJIAN, A.H. Jr. 1983. Distinct patterns of cytoplasmic protein phosphorylation related to regulation of synthesis and release of prolactin by GH cells. J. Biol. Chem., 258: 10312-10324.
84. STEIN, R., MORI, N., MATTHEWS, K., LO, L.C., and ANDERSON, D.J. 1988. The NGF-inducible SCG10 mRNA encodes a novel membrane-bound protein present in growth cones and abundant in developing neurons. Neuron, 1: 463-476.
85. STRAHLER, J.R., LAMB, B.J., UNGAR, D.R., Fox, D.A., and HANASH, S.M. 1992. Cell cycle progression is associated with distinct patterns of phosphorylation of Op18. Biochem. Biophys. Res. Commun., 185: 197-203.
86. TANAKA, E., HO, T., and KIRSCHNER, M.W. 1995. The role of microtubule dynamics in growth cone motility and axonal growth. J. Cell Biol., 128: 139-155.
87. TOURNEBIZE, R., ANDERSEN, S.S.L., VERDE, F., DORÉE, M., KARSENTI, E., and HYMAN, A.A. 1997. Distinct roles of PP1 and PP2A-like phosphatases in control of microtubule dynamics during mitosis. EMBO J., 16: 5537-5549.
88. TOUTANT, M. and SOBEL, A. 1987. Protein phosphorylation in response to the tumor promoter TPA is dependent on the state of differentiation of muscle cells. Dev. Biol., 124: 370-378.