Serine 16 of stathmin as a cytosolic target for Ca2+/calmodulin- dependent kinase II after CD2 triggering of human T lymphocytes

Journal of Immunology

Volumn 161, Issue 3, 1998, Pages 1113-1122

  Le Gouvello, Sabine ^a,b   Manceau, Valérie ^a   Sobel, André ^a,c  

^a Inst Natl S et de la Rech U129   (France)

^b HENRI MONDOR HOSPITAL   (France)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD2 ANTIGEN; CD28 ANTIGEN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIN DEPENDENT KINASE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOPEPTIDE; PROTEIN KINASE (CALCIUM,CALMODULIN) II; SERINE; STATHMIN;

ARTICLE; CONTROLLED STUDY; CYTOSOL; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ANTIGENS, CD2; ANTIGENS, CD28; ANTIGENS, CD3; BINDING SITES; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CYTOSOL; ENZYME ACTIVATION; HUMANS; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MICROTUBULE PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; SERINE; STATHMIN; T-LYMPHOCYTES;

EID: 0032145275     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (81)

1. Janeway, C. A. J., and K. Bottomly. 1994. Signals and signs for lymphocyte responses. Cell 76:275.
2. Meuer, S. C., O. Acuto, R. E. Hussey, J. C. Hodgdon, K. A. Fitzgerald, S. F. Schlossman, and E. L. Reinherz. 1983. Evidence for the T3-associated 90K heterodimer as a T cell antigen receptor. Nature 303:808.
3. Davis, S. J., and P. A. van der Merwe. 1996. The structure and ligand interactions of CD2: implications for T-cell function. Immunol. Today 17:177.
4. Ward, S. G., C. H. June, and D. Olive. 1996. PI3-kinase: a pivotal pathway in T-cell activation? Immunol. Today 17:187.
5. 1 epitopes. J. Immunol. 135:1624.
6. Palacios, R. 1985. Mechanisms by which accessory cells contribute in growth of resting T lymphocytes initiated by OKT3 antibody. Eur. J. Immunol. 15:645.
7. Herold, C., A. Elhabazi, A. Bensussan, and L. Boumsell. 1995. Implication des molécules "CD" dans la transmission des signaux d'activation des lymphocytes T. médecine/sciences 11:669.
8. Howard, F. D., P. Moingeon, U. Moebius, D. J. Mac Conkey, B. Yandava, T. E. Gennert, and E. L. Reinherz. 1992. The CD3 ζ cytoplasmic domain mediates CD2-induced T cell activation. J. Exp. Med. 176:139.
9. Kanner, S. B., N. K. Damle, J. Blake, A. Aruffo, and J. A. Ledbetter. 1992. CD2/LFA3 ligation induces phospholipase-Cγ1 tyrosine phosphorylation and regulates CD3 signaling. J. Immunol. 148:2023.
10. Ley, S. C., A. A. Davies, B. Drucker, and M. J. Crumpton. 1991. the TCR/CD3 complex and CD2 stimulate the tyrosine phosphorylation of indistinguishable patterns of polypeptides in the human T leukemic cell line Jurkat. Eur. J. Immunol. 21:2203.
11. Weiss, A., G. Koretzky, R. C. Schatzman, and T. Kadlecek. 1991. Functional activation of the T-cell antigen receptor induces tyrosine phosphorylation of phospholipase Cgammal. Proc. Natl. Acad. Sci. USA 88:5484.
12. Imboden, J. B., and J. D. Stobo. 1985. Transmembrane signaling by the T cell antigen receptor. J. Exp. Med. 161:446.
13. Pantaleo, G., D. Olive, A. Poggi, W. J. Kozumbo, L. Moretta, and A. Moretta. 1987. Transmembrane signaling via the T11-dependent pathway of human T cell activation. Evidence for the involvement of 1,2-diacylglycerol and inositolphosphates. Eur. J. Immunol. 17:55.
14. 2 activity beside the phospholipase C pathway in human T lymphocytes. J. Immunol. 144:2359.
15. + T lymphocytes to form PAF-acether from alkyl-arachidonoyl-glycero-phosphocholine. J. Immunol. 149:1289.
16. Jin, Y. J., D. R. Kaplan, M. White, G. C. Spagnoli, T. M. Roberts, and E. L. Reinherz. 1990. Stimulation via CD3-Ti but not CD2 induces rapid tyrosine phosphorylation of a 68-kDa protein in the human Jurkat T cell line. J. Immunol. 144:647.
17. Samstag, Y., S. W. Henning, A. Bader, and S. C. Meuer. 1992. Dephosphorylation of pp19: a common second signal for human T cell activation mediated through different accessory molecules. Int. Immunol. 4:1255.
18. Hubert, P., P. Debré, L. Boumsell, and G. Bismuth. 1993. Tyrosine phosphorylation and association with phospholipase C(γ)-1 of the GAP-associated 62-kDa protein after CD2 stimulation of Jurkat T cell. J. Exp. Med. 178:1587.
19. Henning, S. W., S. C. Meuer, and Y. Samstag. 1994. Serine phosphorylation of a 67-kDa protein in human T lymphocytes represents an accessory receptor-mediated signaling event. J. Immunol. 152:4808.
20. le Gouvello, S., H. Chneiweiss, M. Tarantino, P. Debré, and A. Sobel. 1991. Stathmin phosphorylation patterns discriminate between distinct transduction pathways of human T lymphocyte activation through CD2 triggering. FEBS Lett. 287:80.
21. Sobel, A. 1991. Stathmin: a relay phosphoprotein for multiple signal transduction? Trends Biochem. Sci. 16:301.
22. Sobel, A., M. C. Boutterin, L. Beretta, H. Chneiweiss, V. Doye, and H. Peyro-Saint-Paul. 1989. Intracellular substrates for extracellular signaling: characterization of a ubiquitous, neuron-enriched phosphoprotein (stathmin). J. Biol. Chem. 264:3765.
23. Pasmantier, R., A. Danoff, N. Fleischer, and U. K. Schubart. 1986. P19, a hormonally regulated phosphoprotein of peptide-hormone producing cells: secretagogue-induced phosphorylation in AtT-20 mouse pituitary tumor cells and in rat and hamster insulinoma cells. Endocrinology 19:1229.
24. Cooper, H. L., E. McDuffie, and R. Braverman. 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.
25. Hanash, S. M., J. R. Strahler, R. Kuick, E. H. Y. Chu, and D. Nichols. 1988. Identification of a polypeptide associated with the malignant phenotype in the acute leukemia. J. Biol. Chem. 263:12813.
26. Peyron, J., C. Aussel, B. Ferrua, H. Häring, and M. Fehlmann. 1989. Phosphorylation of two cytosolic proteins. An early event of T-cell activation. Biochem. J. 258:505.
27. Hailat, N., J. R. Strahler, R. F. Melhem, X. X. Zhu, G. Brodeur, R. C. Seeger, C. P. Reynolds, and S. M. Hanash. 1990. N-myc gene amplification in neuroblastoma is associated with altered phosphorylation of a proliferation related polypeptide (Op 18). Oncogene 5:1615.
28. Belmont, L. D., and T. J. Mitchison. 1996. Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell 84: 623.
29. Curmi, P. A., S. S. L. Andersen, S. Lachkar, O. Gavet, E. Karsenti, M. Knossow, and A. Sobel. 1997. The stathmin tubulin interaction in vitro. J. Biol. Chem. 272:25029.
30. Jourdain, L., P. Curmi, A. Sobel, D. Pantaloni, and M. F. Carlier. 1997. Stathmin is a tubulih-sequestering protein which forms a ternary T2S complex with two tubulin molecules. Biochemistry 36:10817.
31. Horwitz, S. B., H. Shen, L. He, P. Dittmar, R. Neef, J. Chen, and U. K. Schubart. 1997. The microtubule-destabilizing activity of metablastin (pl9) is controlled by phosphorylation. J. Biol. Chem. 272:8129.
32. Larsson, N., U. Marklund, H. M. Gradin, G. Brattsand, and M. Gullberg. 1997. Control of microtubule dynamics by oncoprotein 18: dissection of the regulatory role of multisite phosphorylation during mitosis. Mol. Cell Biol. 17:5530.
33. 2+/calmodulin-dependent protein kinases. Exp. Eye Res. 51:277.
34. Chneiweiss, H., J. Cordier, and A. Sobel. 1992. Stathmin phosphorylation is regulated in striatal neurons by vasoactive intestinal peptide and monoamines via multiple intracellular pathways. J. Neurochem. 58:282.
35. Chneiweiss, H., L. Beretta, J. Cordier, M. C. Boutterin, J. Glowinski, and A. Sobel. 1989. Stathmin is a major phosphoprotein and cyclic AMP-dependent protein kinase substrate in mouse brain neurons but not in astrocytes in culture: regulation during ontogenesis. J. Neurochem. 53:856.
36. Beretta, L., T. Dobransky, and A. Sobel. 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.
37. Marklund, U., G. Brattsand, O. Osterman, P. I. Ohlsson, and M. Gullberg. 1993. Multiple signal transduction pathways induce phosphorylation of serines 16, 25 and 38 of oncoprotein 18 in T lymphocytes. J. Biol. Chem. 268:25671.
38. 2+/calmodulin-dependent kinase-Gr. Eur. J. Biochem. 225:53.
39. Leighton, I., P. Curmi, D. G. Campbell, P. Cohen, and A. Sobel. 1993. The phosphorylation of Stathmin by MAP kinase. Mol. Cell. Biochem. 127/128:151.
40. Curmi, P., A. Maucuer, S. Asselin, M. Lecourtois, A. Chaffotte, J. M. Schmitter, and A. Sobel. 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.
41. Doye, V., S. le Gouvello, T. Dobransky, H. Chneiweiss, L. Beretta, and A. Sobel. 1992. Expression of transfected Stathmin cDNA reveals novel phosphorylated forms associated with developmental and functional cell regulation. Biochem. J. 287:549.
42. Beverley, P. C. L., and R. E. Callard. 1981. Distinctive functional characteristics of human T lymphocytes defined by E resetting or a monoclonal anti-T cell antibody. Eur. J. Immunol. 11:329.
43. Hahn, W. C., E. Menu, A. L. M. Bothwell, P. J. Sims, and B. E. Bierer. 1992. Overlapping but nonidentical binding sites on CD2 for CD58 and a second ligand CD59. Science 256:1805.
44. Bernard, A., C. Gelin, B. Raynal, D. Pham, C. Gosse, and L. Boumsell. 1982. Phenomenon of human T cells resetting with sheep erythrocytes analyzed with monoclonal antibodies: "modulation" of a partially hidden epitope determining the conditions of interaction between T cells and erythrocytes. J. Exp. Med. 155:1317.
45. Friend, P., H. Tighe, S. Lim, J. Collrer, M. Dewtons, S. Thiru, and H. Waldmann. 1987. The use of monoclonal antibodies against activated human T cells following renal allografting in the baboon. Transplant. Proc. 19:4317.
46. Maucuer, A., V. Doye, and A. Sobel. 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.
47. Sobel, A., and A. H. Tashjian, 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.
48. Hemmings, H. C. J., A. C. Nairn, and P. Greengard. 1984. DARPP-32, a dopamine- and adenosine 3′:5′-monophosphate-regulated neuronal phosphoprotein. J. Biol. Chem. 259:14491.
49. cdc2 kinase. J. Biol. Chem. 269:10312.
50. Wang, Y. K., P.-C. Liao, J. Allison, D. A. Gage, P. C. Andrews, D. M. Lubman, S. M. Hanash, and J. R. Strahler. 1993. Phorbol 12-myristate 13-acetate-induced phosphorylation of Op18 in Jurkat T cells. J. Biol. Chem. 268:14269.
51. Richards, F. M., R. J. Milner, and S. Metcalfe. 1992. Inhibition of the serine/ threonine protein phosphatases PP1 and PP2A in lymphocytes: effect on mRNA levels for interleukin-2, IL-2Ra, krox-24, p53, hsc70, and cyclophilin. Immunology 76:642.
52. Haystead, T. A. J., A. T. R. Sim, D. Carling, R. C. Honnor, Y. Tsukitani, P. Cohen, and D. G. Hardie. 1989. Effects of the tumours promoter okadaic acid on intracellular protein phosphorylation and metabolism. Nature 337:78.
53. Skalhegg, B. S., K. Tasken, V. Hansson, M. S. Huitfeldt, T. Jahnsen, and T. Lea. 1994. Location of cAMP-dependent protein kinase type I with the TCR-CD3 complex. Science 263:84.
54. 2+/calmodulin-dependent protein kinase, CaM kinase-GR in human T lymphocytes. J. Biol. Chem. 268:20055.
55. 2+/calmodulin kinase. Nature 371:347.
56. Hama, N., F. Paliogianni, B. J. Fessler, and D. T. Boumpas. 1995. Calcium/ calmodulin-dependent protein kinase II downregulates both calcineurin and protein kinase C-mediated pathways for cytokine gene transcription in human T cells. J. Exp. Med. 181:1217.
57. 2+ signaling. J. Biol. Chem. 266:11309.
58. 2 in norepinephrine-induced arachidonic acid release in rabbit aortic smooth muscle. J. Biol. Chem. 271: 30149.
59. 2+/calmodulin-dependent protein kinase IV. J. Biol. Chem. 269:15520.
60. Maucuer, A., J. H. Camonis, and A. Sobel. 1995. Stathmin interaction with a novel putative kinase and coiled-coil forming protein domains. Proc. Natl. Acad. Sci. USA 92:3100.
61. 38. Eur. J. Biochem. 220:359.
62. ras couples the T cell antigen receptor to extracellular signal-regulated kinase 2 in T lymphocytes. J. Exp. Med. 178:1199.
63. rasin human T lymphocytes. J. Immunol. 146:3709.
64. ras. J. Exp. Med. 180:1067.
65. ras regulatory pathway coexist in T cell. Mol. Cell. Biol. 12:3305.
66. Amaral, M. C., A. M. Casillas, and A. E. Nel. 1993. Contrasting effects of two tumour promoters, phorbol myristate acetate and okadaic acid on T-cell responses and activation of p42 MAP-kinase/ERK-2. Immunology 79:24.
67. Waskiewicz, A. J., and J. A. Cooper. 1995. Mitogen and stress response pathway: MAP kinase cascades and phosphatase regulation in mammals and yeast. Curr. Opin. Cell Biol. 7:798.
68. Yang, S. Y., S. Chouaib, and B. Dupont. 1986. A common pathway for T lymphocyte activation involving both the CD3-Ti complex and CD2 sheep erythrocyte receptor determinants. J. Immunol. 137:1097.
69. Monostori, E., D. Desai, M. H. Brown, D. A. Cantrell, and M. J. Crumpton. 1990. Activation of human T lymphocytes via the CD2 antigen results in tyrosine phosphorylation of T cell antigen receptor ζ-chains. J. Immunol. 144:1010.
70. Endler-Jobst, B., B. Schraven, B. Hutmacher, and S. C. Meuer. 1991. Human T cell responses to IL-1 and IL-6 are dependent on signals mediated through CD2. J. Immunol. 146:1736.
71. Samstag, Y., A. Bader, and S. C. Meuer. 1991. A serine phosphatase is involved in CD2-mediated activation of human T lymphocytes and NK cells. J. Immunol. 147:788.
72. Miyano, O., I. Kameshita, and H. Fujisawa. 1992. Purification and characterization of a brain-specific multifunctional calmodulin-dependent protein kinase from rat cerebellum. J. Biol. Chem. 267:1198.
73. 2+/calmodulin-dependent protein kinase: expression in multiple human tissues. J. Biol. Chem. 268:5471.
74. 2+/calmodulin-dependent protein kinase. J. Biol. Chem. 267: 12197.
75. 2 in T-lymphocyte activation: implication in propagation of inflammatory reaction. Proc. Natl. Acad. Sci. USA 90:716.
76. Los, M., H. Schenk, K. Hexel, P. A. Baeuerle, W. Dröge, and K. Skhulze-Osthoff. 1995. IL-2 gene expression and NF-κB activation through CD28 requires reactive oxygen production by 5-lipoxygenase. EMBO J. 14:3731.
77. Rouleau, M., B. Mollereau, A. Bernard, D. Metivier, M. A. Rosenthal-Allieri, B. Charpentier, and A. Senik. 1994. Mitogenic CD2 mAb pairs predispose peripheral T cells to undergo apoptosis on interaction with a third CD2 mAb. J. Immunol. 152:4861.
78. Strahler, J. R., N. Hailat, B. J. Lamb, K. P. Rogers, J. A. Underbill, R. F. Melhem, D. Keim, X. X. Zhu, R. Kuick, D. A. Fox, and S. M. Hanash. 1992. Activation of resting peripheral blood lymphocytes through the TCR induces rapid phosphorylation of Op18. J. Immunol. 149:1191.
79. Feuerstein, N., and H. L. Cooper. 1983. Rapid protein phosphorylation induced by phorbol ester in HL-60 cells: unique alkali-stable phosphorylation of a 17 000-dalton protein detected by two dimensional gel electrophoresis. J. Biol. Chem. 258:10786.
80. Koppel, J., P. Loyer, A. Maucuer, P. Rehák, V. Manceau, C. Guguen-Guillouzo, and A. Sobel. 1993. Induction of stathmin expression during liver regeneration. FEBS Lett. 331:65.
81. Balogh, A., R. M. Mege, and A. Sobel. 1996. Cell density dependent expression of stathmin in C2 myoblasts in culture. Exp. Cell Res. 224:8.