EGFR/MEK/ERK/CDK5-dependent integrin-independent FAK phosphorylated on serine 732 contributes to microtubule depolymerization and mitosis in tumor cells

Cell Death and Disease

Volumn 4, Issue 10, 2013, Pages

  Rea, K ^a   Sensi, M ^a   Anichini, A ^a   Canevari, S ^a   Tomassetti, A ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

CDK5; EGFR; FAK; Microtubules; Mitosis

Indexed keywords

CYCLIN DEPENDENT KINASE 5; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; FOCAL ADHESION KINASE; INTEGRIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; ROSCOVITINE; SERINE;

ANTINEOPLASTIC ACTIVITY; ARTICLE; ASCITES TUMOR; CANCER CELL CULTURE; CELL MIGRATION; CELL PROLIFERATION; CHROMOSOME; CONTROLLED STUDY; DEPOLYMERIZATION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTERPHASE; MELANOMA CELL; MICROTUBULE; MICROTUBULE ASSEMBLY; MITOSIS; MITOSIS SPINDLE; MOLECULAR DYNAMICS; OVARY CANCER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; THYROID TUMOR; TUMOR CELL;

CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE 5; EPIDERMAL GROWTH FACTOR; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; HUMANS; INTEGRINS; MAP KINASE SIGNALING SYSTEM; MICROTUBULES; MITOSIS; NEOPLASMS; PHOSPHORYLATION; PHOSPHOSERINE; POLYMERIZATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; SPINDLE APPARATUS;

EID: 84887450073     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.353     Document Type: Article

References (37)

1. Schaller MD. Cellular functions of FAK kinases: Insight into molecular mechanisms and novel functions. J Cell Sci 2010; 123: 1007-1013.
2. Corsi JM, Houbron C, Billuart P, Brunet I, Bouvree K, Eichmann A et al. Autophosphorylation-independent and -dependent functions of focal adhesion kinase during development. J Biol Chem 2009; 284: 34769-34776.
3. Braren R, Hu H, Kim YH, Beggs HE, Reichardt LF, Wang R. Endothelial FAK is essential for vascular network stability, cell survival, and lamellipodial formation. J Cell Biol 2006; 172: 151-162.
4. Gabarra-Niecko V, Schaller MD, Dunty JM. FAK regulates biological processes important for the pathogenesis of cancer. Cancer Metastasis Rev 2003; 22: 359-374.
5. Zhao J, Pestell R, Guan JL. Transcriptional activation of cyclin D1 promoter by FAK contributes to cell cycle progression. Mol Biol Cell 2001; 12: 4066-4077.
6. Wang X, Urvalek AM, Liu J, Zhao J. Activation of KLF8 transcription by focal adhesion kinase in human ovarian epithelial and cancer cells. J Biol Chem 2008; 283: 13934-13942.
7. Calalb MB, Polte TR, Hanks SK. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: A role for Src family kinases. Mol Cell Biol 1995; 15: 954-963.
8. Schaller MD, Borgman CA, Parsons JT. Autonomous expression of a noncatalytic domain of the focal adhesion-Associated protein tyrosine kinase pp125FAK. Mol Cell Biol 1993; 13: 785-791.
9. Lietha D, Cai X, Ceccarelli DF, Li Y, Schaller MD, Eck MJ. Structural basis for the autoinhibition of focal adhesion kinase. Cell 2007; 129: 1177-1187.
10. Xie Z, Sanada K, Samuels BA, Shih H, Tsai LH. Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 2003; 114: 469-482.
11. Xie Z, Tsai LH. Cdk5 phosphorylation of FAK regulates centrosome-Associated miocrotubules and neuronal migration. Cell Cycle 2004; 3: 108-110.
12. Le Boeuf F, Houle F, Sussman M, Huot J. Phosphorylation of focal adhesion kinase (FAK) on Ser732 is induced by rho-dependent kinase and is essential for proline-rich tyrosine kinase-2-mediated phosphorylation of FAK on Tyr407 in response to vascular endothelial growth factor. Mol Biol Cell 2006; 17: 3508-3520.
13. Park AY, Shen TL, Chien S, Guan JL. Role of focal adhesion kinase Ser-732 phosphorylation in centrosome function during mitosis. J Biol Chem 2009; 284: 9418-9425.
14. Sensi M, Catani M, Castellano G, Nicolini G, Alciato F, Tragni G et al. Human cutaneous melanomas lacking MITF and melanocyte differentiation antigens express a functional Axl receptor kinase. J Invest Dermatol 2011; 131: 2448-2457.
15. Hanks SK, Calalb MB, Harper MC, Patel SK. Focal adhesion protein-Tyrosine kinase phosphorylated in response to cell attachment to fibronectin. Proc Natl Acad Sci USA 1992; 89: 8487-8491.
16. Laan L, Pavin N, Husson J, Romet-Lemonne G, van DM, Lopez MP et al. Cortical dynein controls microtubule dynamics to generate pulling forces that position microtubule asters. Cell 2012; 148: 502-514.
17. Juan G, Traganos F, James WM, Ray JM, Roberge M, Sauve DM et al. Histone H3 phosphorylation and expression of cyclins A and B1 measured in individual cells during their progression through G2 and mitosis. Cytometry 1998; 32: 71-77.
18. Harrison RE, Turley EA. Active erk regulates microtubule stability in H-ras-Transformed cells. Neoplasia 2001; 3: 385-394.
19. Roberts EC, Shapiro PS, Nahreini TS, Pages G, Pouyssegur J, Ahn NG. Distinct cell cycle timing requirements for extracellular signal-regulated kinase and phosphoinositide 3-kinase signaling pathways in somatic cell mitosis. Mol Cell Biol 2002; 22: 7226-7241.
20. Mitra SK, Hanson DA, Schlaepfer DD. Focal adhesion kinase: In command and control of cell motility. Nat Rev Mol Cell Biol 2005; 6: 56-68.
21. Tarcic G, Yarden Y. MAP Kinase activation by receptor tyrosine kinases: In control of cell migration. Methods Mol Biol 2010; 661: 125-135.
22. Lopes JP, Agostinho P. Cdk5: Multitasking between physiological and pathological conditions. Prog Neurobiol 2011; 94: 49-63.
23. Kotak S, Busso C, Gonczy P. Cortical dynein is critical for proper spindle positioning in human cells. J Cell Biol 2012; 199: 97-110.
24. Stevermann L, Liakopoulos D. Molecular mechanisms in spindle positioning: Structures and new concepts. Curr Opin Cell Biol 2012; 24: 816-824.
25. Thompson SL, Compton DA. Chromosome missegregation in human cells arises through specific types of kinetochore-microtubule attachment errors. Proc Natl Acad Sci USA 2011; 108: 17974-17978.
26. Sanhaji M, Friel CT, Wordeman L, Louwen F, Yuan J. Mitotic centromere-Associated kinesin (MCAK): A potential cancer drug target. Oncotarget 2011; 2: 935-947.
27. Liebl J, Furst R, Vollmar AM, Zahler S. Twice switched at birth: Cell cycle-independent roles of the 'neuron-specific' cyclin-dependent kinase 5 (Cdk5) in non-neuronal cells. Cell Signal 2011; 23: 1698-1707.
28. Harada T, Morooka T, Ogawa S, Nishida E. ERK induces p35, a neuron-specific activator of Cdk5, through induction of Egr1. Nat Cell Biol 2001; 3: 453-459.
29. Feldmann G, Mishra A, Hong SM, Bisht S, Strock CJ, Ball DW et al. Inhibiting the cyclindependent kinase CDK5 blocks pancreatic cancer formation and progression through the suppression of Ras-Ral signaling. Cancer Res 2010; 70: 4460-4469.
30. Geneste O, Copeland JW, Treisman R. LIM kinase and Diaphanous cooperate to regulate serum response factor and actin dynamics. J Cell Biol 2002; 157: 831-838.
31. Bénard J, De Silva J, De Blois MC, Boyer P, Duvilland P, Chiric E et al. Characterization of a human ovarian adenocarcinoma line, IGROV1, in tissue culture and in nude mice. Cancer Res 1985; 45: 4970-4979.
32. van den Berg-Bakker CA, Hagemeijer A, Franken-Postma EM, Smit VT, Kuppen PJ, van Ravenswaay C et al. Establishment and characterization of 7 ovarian carcinoma cell lines and one granulosa tumor cell line: Growth features and cytogenetics. Int J Cancer 1993; 53: 613-620.
33. Ramakrishna V, Negri DRM, Brusic V, Fontanelli R, Canevari S, Bolis G et al. Generation and phenotypic characterization of new human ovarian cancer lines with the identification of antigens potentially recognizable by HLA-restricted cytotoxic T cells. Int J Cancer 1997; 73: 143-150.
34. Tohyama K, Yoshida Y, Ohashi K, Sano E, Kobayashi H, Endo K et al. Production of multiple growth factors by a newly established human thyroid carcinoma cell line. Jpn J Cancer Res 1992; 83: 153-158.
35. Schweppe RE, Klopper JP, Korch C, Pugazhenthi U, Benezra M, Knauf JA et al. Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals crosscontamination resulting in cell line redundancy and misidentification. J Clin Endocrinol Metab 2008; 93: 4331-4341.
36. De Santis G, Miotti S, Mazzi M, Canevari S, Tomassetti A. E-cadherin directly contributes to PI3K/AKT activation by engaging the PI3K-p85 regulatory subunit to adherens junctions of ovarian carcinoma cells. Oncogene 2009; 28: 1206-1217.
37. Baldassarre G, Belletti B, Nicoloso MS, Schiappacassi M, Vecchione A, Spessotto P et al. p27(Kip1)-stathmin interaction influences sarcoma cell migration and invasion. Cancer Cell 2005; 7: 51-63.