Integrins regulate microtubule nucleating activity of centrosome through mitogen-activated protein kinase/extracellular signal-regulated kinase kinase/extracellular signal-regulated kinase (MEK/ERK) signaling

Journal of Biological Chemistry

Volumn 287, Issue 4, 2012, Pages 2520-2530

  Colello, Diane ^a   Mathew, Shomita ^a   Ward, Rachel ^a   Pumiglia, Kevin ^a   LaFlamme, Susan E ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTORS; CYTOSKELETONS; INTEGRINS; MICROTUBULE NUCLEATION; MICROTUBULES; MITOGEN ACTIVATED PROTEIN KINASE; NUCLEATING ACTIVITY; SIGNAL-REGULATED KINASE; SIGNALING COMPLEX; SIGNALING PATHWAYS;

AMINO ACIDS; ENZYMES; GLYCOPROTEINS; SIGNALING;

NUCLEATION;

ALANINE; ANDROGEN; ANDROGEN RECEPTOR; BETA1 INTEGRIN; GAMMA TUBULIN; INTEGRIN; MITOGEN ACTIVATED PROTEIN KINASE; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE; RAF PROTEIN; TYROSINE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL FUNCTION; CENTROSOME; CHO CELL; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; FEMALE; HORMONAL REGULATION; MICROTUBULE NUCLEATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD29; CENTROSOME; CHO CELLS; CRICETINAE; CRICETULUS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MAP KINASE KINASE KINASES; MAP KINASE SIGNALING SYSTEM; MICROTUBULES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-RAF; TUBULIN;

EID: 84856067195     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.254128     Document Type: Article

References (66)

1. Bornens, M. (2002) Centrosome composition and microtubule anchoring mechanisms. Curr. Opin. Cell Biol. 14, 25-34
2. Doxsey, S., McCollum, D., and Theurkauf, W. (2005) Centrosomes in cellular regulation. Annu. Rev. Cell Dev. Biol. 21, 411-434 (Pubitemid 41740641)
3. Lüders, J., and Stearns, T. (2007) Microtubule-organizing centers: a reevaluation. Nat. Rev. Mol. Cell Biol. 8, 161-167
4. Haren, L., Remy, M. H., Bazin, I., Callebaut, I., Wright, M., and Merdes, A. (2006) NEDD1-dependent recruitment of the γ-tubulin ring complex to the centrosome is necessary for centriole duplication and spindle assembly. J. Cell Biol. 172, 505-515 (Pubitemid 43243872)
5. Lüders, J., Patel, U. K., and Stearns, T. (2006) GCP-WD is a γ-tubulin targeting factor required for centrosomal and chromatin-mediated microtubule nucleation. Nat. Cell Biol. 8, 137-147
6. Teixidó-Travesa, N., Villén, J., Lacasa, C., Bertran, M. T., Archinti, M., Gygi, S. P., Caelles, C., Roig, J., and Lüders, J. (2010) The γ-TuRC revisited. A comparative analysis of interphase and mitotic human γ-TuRC redefines the set of core components and identifies the novel subunit GCP8. Mol. Biol. Cell 21, 3963-3972
7. Khodjakov, A., and Rieder, C. L. (1999) The sudden recruitment of γ-tubulin to the centrosome at the onset of mitosis and its dynamic exchange throughout the cell cycle do not require microtubules. J. Cell Biol. 146, 585-596 (Pubitemid 29388133)
8. Piehl, M., Tulu, U. S., Wadsworth, P., and Cassimeris, L. (2004) Centrosome maturation. Measurement of microtubule nucleation throughout the cell cycle by using GFP-tagged EB1. Proc. Natl. Acad. Sci. U.S.A. 101, 1584-1588 (Pubitemid 38234197)
9. Haren, L., Stearns, T., and Lüders, J. (2009) Plk1-dependent recruitment of γ-tubulin complexes to mitotic centrosomes involves multiple PCM components. PLoS One 4, e5976
10. Zhang, X., Chen, Q., Feng, J., Hou, J., Yang, F., Liu, J., Jiang, Q., and Zhang, C. (2009) Sequential phosphorylation of Nedd1 by Cdk1 and Plk1 is required for targeting of the γ-TuRC to the centrosome. J. Cell Sci. 122, 2240-2251
11. Colello, D., Reverte, C. G., Ward, R., Jones, C. W., Magidson, V., Khodjakov, A., and LaFlamme, S. E. (2010) Androgen and Src signaling regulate centrosome activity. J. Cell Sci. 123, 2094-2102
12. Di Domenico, M., Castoria, G., Bilancio, A., Migliaccio, A., and Auricchio, F. (1996) Estradiol activation of human colon carcinoma-derived Caco-2 cell growth. Cancer Res. 56, 4516-4521 (Pubitemid 26330464)
13. Migliaccio, A., Piccolo, D., Castoria, G., Di Domenico, M., Bilancio, A., Lombardi, M., Gong, W., Beato, M., and Auricchio, F. (1998) Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO J. 17, 2008-2018 (Pubitemid 28154530)
14. Boonyaratanakornkit, V., Scott, M. P., Ribon, V., Sherman, L., Anderson, S. M., Maller, J. L., Miller, W. T., and Edwards, D. P. (2001) Progesterone receptor contains a proline-rich motif that directly interacts with Src homology 3 domains and activates c-Src family tyrosine kinases. Mol. Cell 8, 269-280 (Pubitemid 32831545)
15. Peterziel, H., Mink, S., Schonert, A., Becker, M., Klocker, H., and Cato, A. C. (1999) Rapid signaling by androgen receptor in prostate cancer cells. Oncogene 18, 6322-6329
16. Migliaccio, A., Castoria, G., Di Domenico, M., de Falco, A., Bilancio, A., Lombardi, M., Barone, M. V., Ametrano, D., Zannini, M. S., Abbondanza, C., and Auricchio, F. (2000) Steroid-induced androgen receptor-oestradiol receptor β-Src complex triggers prostate cancer cell proliferation. EMBO J. 19, 5406-5417
17. Migliaccio, A., Castoria, G., Di Domenico, M., De Falco, A., Bilancio, A., and Auricchio, F. (2002) Src is an initial target of sex steroid hormone action. Ann. N.Y. Acad. Sci. 963, 185-190 (Pubitemid 34721710)
18. Sun, M., Yang, L., Feldman, R. I., Sun, X. M., Bhalla, K. N., Jove, R., Nicosia, S. V., and Cheng, J. Q. (2003) Activation of phosphatidylinositol 3-kinase/Akt pathway by androgen through interaction of p85α, androgen receptor, and Src. J. Biol. Chem. 278, 42992-43000 (Pubitemid 37345912)
19. Baron, S., Manin, M., Beaudoin, C., Leotoing, L., Communal, Y., Veyssiere, G., and Morel, L. (2004) Androgen receptor mediates nongenomic activation of phosphatidylinositol 3-OH kinase in androgen-sensitive epithelial cells. J. Biol. Chem. 279, 14579-14586 (Pubitemid 38618845)
20. Hynes, R. O. (2002) Integrins. Bidirectional, allosteric signaling machines. Cell 110, 673-687
21. Berrier, A. L., and Yamada, K. M. (2007) Cell-matrix adhesion. J. Cell Physiol. 213, 565-573 (Pubitemid 350058247)
22. Streuli, C. H., and Akhtar, N. (2009) Signal cooperation between integrins and other receptor systems. Biochem. J. 418, 491-506
23. Schwartz, M. A., and Ginsberg, M. H. (2002) Networks and cross-talk. Integrin signaling spreads. Nat. Cell Biol. 4, E65-E68 (Pubitemid 34308840)
24. Ylänne, J., Chen, Y., O'Toole, T. E., Loftus, J. C., Takada, Y., and Ginsberg, M. H. (1993) Distinct functions of integrin α and β subunit cytoplasmic domains in cell spreading and formation of focal adhesions. J. Cell Biol. 122, 223-233 (Pubitemid 23188813)
25. Bodeau, A. L., Berrier, A. L., Mastrangelo, A. M., Martinez, R., and LaFlamme, S. E. (2001) A functional comparison of mutations in integrin β cytoplasmic domains. Effects on the regulation of tyrosine phosphorylation, cell spreading, cell attachment, and β1 integrin conformation. J. Cell Sci. 114, 2795-2807 (Pubitemid 32785458)
26. Berrier, A. L., Martinez, R., Bokoch, G. M., and LaFlamme, S. E. (2002) The integrin β tail is required and sufficient to regulate adhesion signaling to Rac1. J. Cell Sci. 115, 4285-4291 (Pubitemid 35460699)
27. Hirsch, E., Barberis, L., Brancaccio, M., Azzolino, O., Xu, D., Kyriakis, J. M., Silengo, L., Giancotti, F. G., Tarone, G., Fässler, R., and Altruda, F. (2002) Defective Rac-mediated proliferation and survival after targeted mutation of the β1 integrin cytodomain. J. Cell Biol. 157, 481-492 (Pubitemid 34839811)
28. Tadokoro, S., Shattil, S. J., Eto, K., Tai, V., Liddington, R. C., de Pereda, J. M., Ginsberg, M. H., and Calderwood, D. A. (2003) Talin binding to integrin β tails. A final common step in integrin activation. Science 302, 103-106 (Pubitemid 37210697)
29. Legate, K. R., and Fässler, R. (2009) Mechanisms that regulate adaptor binding to β-integrin cytoplasmic tails. J. Cell Sci. 122, 187-198
30. O'Toole, T. E., Ylanne, J., and Culley, B. M. (1995) Regulation of integrin affinity states through an NPXY motif in the β subunit cytoplasmic domain. J. Biol. Chem. 270, 8553-8558
31. Kääpä, A., Peter, K., and Ylänne, J. (1999) Effects of mutations in the cytoplasmic domain of integrin β (1) to talin binding and cell spreading. Exp. Cell Res. 250, 524-534
32. Nieves, B., Jones, C. W., Ward, R., Ohta, Y., Reverte, C. G., and LaFlamme, S. E. (2010) The NPIY motif in the integrin β1 tail dictates the requirement for talin-1 in outside-in signaling. J. Cell Sci. 123, 1216-1226
33. Reverte, C. G., Benware, A., Jones, C. W., and LaFlamme, S. E. (2006) Perturbing integrin function inhibits microtubule growth from centrosomes, spindle assembly, and cytokinesis. J. Cell Biol. 174, 491-497 (Pubitemid 44231861)
34. LaFlamme, S. E., Nieves, B., Colello, D., and Reverte, C. G. (2008) Integrins as regulators of the mitotic machinery. Curr. Opin. Cell Biol. 20, 576-582
35. Khodjakov, A., Rieder, C. L., Sluder, G., Cassels, G., Sibon, O., and Wang, C. L. (2002) De novo formation of centrosomes in vertebrate cells arrested during S phase. J. Cell Biol. 158, 1171-1181
36. Efimov, A., Kharitonov, A., Efimova, N., Loncarek, J., Miller, P. M., Andreyeva, N., Gleeson, P., Galjart, N., Maia, A. R., McLeod, I. X., Yates, J. R., 3rd, Maiato, H., Khodjakov, A., Akhmanova, A., and Kaverina, I. (2007) Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev. Cell 12, 917-930 (Pubitemid 46805921)
37. Schmidt, J. W., Brugge, J. S., and Nelson, W. J. (1992) pp60src tyrosine kinase modulates P19 embryonal carcinoma cell fate by inhibiting neuronal but not epithelial differentiation. J. Cell Biol. 116, 1019-1033
38. Takayama, Y., Nada, S., Nagai, K., and Okada, M. (1997) Role of Csk in neural differentiation of the embryonic carcinoma cell line P19. FEBS Lett. 406, 11-16 (Pubitemid 27156948)
39. Bajaj, A., Zheng, Q., Adam, A., Vincent, P., and Pumiglia, K. (2010) Activation of endothelial ras signaling bypasses senescence and causes abnormal vascular morphogenesis. Cancer Res. 70, 3803-3812
40. White, R. A., Pan, Z., and Salisbury, J. L. (2000) GFP-centrin as a marker for centriole dynamics in living cells. Microsc. Res. Tech. 49, 451-457 (Pubitemid 30415704)
41. Salaycik, K. J., Fagerstrom, C. J., Murthy, K., Tulu, U. S., and Wadsworth, P. (2005) Quantification of microtubule nucleation, growth, and dynamics in wound-edge cells. J. Cell Sci. 118, 4113-4122 (Pubitemid 41488950)
42. Hirai, H., and Varmus, H. E. (1990) Site-directed mutagenesis of the SH2-and SH3-coding domains of c-src produces varied phenotypes, including oncogenic activation of p60c-src. Mol. Cell Biol. 10, 1307-1318 (Pubitemid 20104999)
43. Beeram, M., Patnaik, A., and Rowinsky, E. K. (2005) Raf. A strategic target for therapeutic development against cancer. J. Clin. Oncol. 23, 6771-6790 (Pubitemid 46194105)
44. Meraldi, P., and Nigg, E. A. (2002) The centrosome cycle. FEBS Lett. 521, 9-13 (Pubitemid 34628448)
45. Casenghi, M., Meraldi, P., Weinhart, U., Duncan, P. I., Körner, R., and Nigg, E. A. (2003) Polo-like kinase 1 regulates Nlp, a centrosome protein involved in microtubule nucleation. Dev. Cell 5, 113-125 (Pubitemid 36827346)
46. Roberts, P. J., and Der, C. J. (2007) Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 26, 3291-3310 (Pubitemid 46763022)
47. Kousteni, S., Bellido, T., Plotkin, L. I., O'Brien, C. A., Bodenner, D. L., Han, L., Han, K., DiGregorio, G. B., Katzenellenbogen, J. A., Katzenellenbogen, B. S., Roberson, P. K., Weinstein, R. S., Jilka, R. L., and Manolagas, S. C. (2001) Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors. Dissociation from transcriptional activity. Cell 104, 719-730 (Pubitemid 32241022)
48. Harrison, R. E., and Turley, E. A. (2001) Active erk regulates microtubule stability in H-ras-transformed cells. Neoplasia 3, 385-394 (Pubitemid 32988808)
49. Tolg, C., Hamilton, S. R., Morningstar, L., Zhang, J., Zhang, S., Esguerra, K. V., Telmer, P. G., Luyt, L. G., Harrison, R., McCarthy, J. B., and Turley, E. A. (2010) RHAMM promotes interphase microtubule instability and mitotic spindle integrity through MEK1/ERK1/2 activity. J. Biol. Chem. 285, 26461-26474
50. Daub, H., Gevaert, K., Vandekerckhove, J., Sobel, A., and Hall, A. (2001) Rac/Cdc42 and p65PAK regulate the microtubule-destabilizing protein stathmin through phosphorylation at serine 16. J. Biol. Chem. 276, 1677-1680 (Pubitemid 32109635)
51. Etienne-Manneville, S., and Hall, A. (2003) Cdc42 regulates GSK-3β and adenomatous polyposis coli to control cell polarity. Nature 421, 753-756 (Pubitemid 36227627)
52. Palazzo, A. F., Eng, C. H., Schlaepfer, D. D., Marcantonio, E. E., and Gundersen, G. G. (2004) Localized stabilization of microtubules by integrin-and FAK-facilitated Rho signaling. Science 303, 836-839 (Pubitemid 38174661)
53. Wen, Y., Eng, C. H., Schmoranzer, J., Cabrera-Poch, N., Morris, E. J., Chen, M., Wallar, B. J., Alberts, A. S., and Gundersen, G. G. (2004) EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat. Cell Biol. 6, 820-830 (Pubitemid 39207247)
54. Wittmann, T., and Waterman-Storer, C. M. (2005) Spatial regulation of CLASP affinity for microtubules by Rac1 and GSK3β in migrating epithelial cells. J. Cell Biol. 169, 929-939 (Pubitemid 41002869)
55. Grigoriev, I., Borisy, G., and Vorobjev, I. (2006) Regulation of microtubule dynamics in 3T3 fibroblasts by Rho family GTPases. Cell Motil. Cytoskeleton 63, 29-40 (Pubitemid 43157643)
56. Wickström, S. A., Lange, A., Hess, M. W., Polleux, J., Spatz, J. P., Krüger, M., Pfaller, K., Lambacher, A., Bloch, W., Mann, M., Huber, L. A., and Fässler, R. (2010) Integrin-linked kinase controls microtubule dynamics required for plasma membrane targeting of caveolae. Dev. Cell 19, 574-588
57. Zumbrunn, J., Kinoshita, K., Hyman, A. A., and Näthke, I. S. (2001) Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3 β phosphorylation. Curr. Biol. 11, 44-49 (Pubitemid 32062715)
58. Akhmanova, A., Hoogenraad, C. C., Drabek, K., Stepanova, T., Dortland, B., Verkerk, T., Vermeulen, W., Burgering, B. M., De Zeeuw, C. I., Grosveld, F., and Galjart, N. (2001) Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104, 923-935 (Pubitemid 32289284)
59. Watanabe, T., Noritake, J., Kakeno, M., Matsui, T., Harada, T., Wang, S., Itoh, N., Sato, K., Matsuzawa, K., Iwamatsu, A., Galjart, N., and Kaibuchi, K. (2009) Phosphorylation of CLASP2 by GSK-3β regulates its interaction with IQGAP1, EB1, and microtubules. J. Cell Sci. 122, 2969-2979
60. Fumoto, K., Hoogenraad, C. C., and Kikuchi, A. (2006) GSK-3β-regulated interaction of BICD with dynein is involved in microtubule anchorage at centrosome. EMBO J. 25, 5670-5682 (Pubitemid 44967751)
61. Migliaccio, A., Varricchio, L., De Falco, A., Castoria, G., Arra, C., Yamaguchi, H., Ciociola, A., Lombardi, M., Di Stasio, R., Barbieri, A., Baldi, A., Barone, M. V., Appella, E., and Auricchio, F. (2007) Inhibition of the SH3 domain-mediated binding of Src to the androgen receptor and its effect on tumor growth. Oncogene 26, 6619-6629 (Pubitemid 47573684)
62. Balasubramanian, N., Scott, D. W., Castle, J. D., Casanova, J. E., and Schwartz, M. A. (2007) Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts. Nat. Cell Biol. 9, 1381-1391 (Pubitemid 350201751)
63. Echarri, A., and Del Pozo, M. A. (2006) Caveolae internalization regulates integrin-dependent signaling pathways. Cell Cycle 5, 2179-2182 (Pubitemid 44546548)
64. Freeman, M. R., Cinar, B., and Lu, M. L. (2005) Membrane rafts as potential sites of nongenomic hormonal signaling in prostate cancer. Trends Endocrinol. Metab. 16, 273-279 (Pubitemid 41058759)
65. Cinar, B., Mukhopadhyay, N. K., Meng, G., and Freeman, M. R. (2007) Phosphoinositide 3-kinase-independent nongenomic signals transit from the androgen receptor to Akt1 in membrane raft microdomains. J. Biol. Chem. 282, 29584-29593 (Pubitemid 350043392)
66. Sandilands, E., and Frame, M. C. (2008) Endosomal trafficking of Src tyrosine kinase. Trends Cell Biol. 18, 322-329