Function of focal adhesion kinase scaffolding to mediate endophilin A2 phosphorylation promotes epithelial-mesenchymal transition and mammary cancer stem cell activities in vivo

Journal of Biological Chemistry

Volumn 288, Issue 5, 2013, Pages 3322-3333

  Fan, Huaping ^a   Zhao, Xiaofeng ^a   Sun, Shaogang ^a   Luo, Ming ^a   Guan, Jun Lin ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER DEVELOPMENT; DOWNSTREAM COMPONENTS; ENDOPHILIN; EPITHELIAL-MESENCHYMAL TRANSITION; FOCAL ADHESION KINASE; HUMAN BREAST CANCER; IN-VITRO; IN-VIVO; INTRACELLULAR SIGNALING; KINASE INHIBITION; KINASE-INDEPENDENT FUNCTIONS; MAMMARY CANCER; MAMMARY TUMORS; MURINE MODEL; MUTANT MICE; SURFACE EXPRESSION; TUMOR CELLS; TYROSINE KINASE;

ADHESION; AMINO ACIDS; CELL CULTURE; DISEASES; ENZYMES; GENE EXPRESSION; PHOSPHORYLATION; STEM CELLS; TUMORS;

SCAFFOLDS (BIOLOGY);

ENDOPHILIN; ENDOPHILIN A2; FOCAL ADHESION KINASE; PROTEIN TYROSINE KINASE; TUMOR MARKER; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER STEM CELL; CANCER THERAPY; CELL PROLIFERATION; EPITHELIAL MESENCHYMAL TRANSITION; FIBROBLAST; GENE MUTATION; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; TUMOR CELL; TUMOR GROWTH;

ACYLTRANSFERASES; ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FOCAL ADHESION KINASE 1; GENE KNOCK-IN TECHNIQUES; GENE KNOCKDOWN TECHNIQUES; HUMANS; LUNG NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; MATRIX METALLOPROTEINASE 14; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; NEOPLASTIC STEM CELLS; PHOSPHORYLATION; PROTEIN BINDING; SPHEROIDS, CELLULAR; SUPPRESSION, GENETIC; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL;

EID: 84873313062     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.420497     Document Type: Article

References (59)

1. Sjöblom, T., Jones, S., Wood, L. D., Parsons, D. W., Lin, J., Barber, T. D., Mandelker, D., Leary, R. J., Ptak, J., Silliman, N., Szabo, S., Buckhaults, P., Farrell, C., Meeh, P., Markowitz, S. D., Willis, J., Dawson, D., Willson, J. K., Gazdar, A. F., Hartigan, J., Wu, L., Liu, C., Parmigiani, G., Park, B. H., Bachman, K. E., Papadopoulos, N., Vogelstein, B., Kinzler, K. W., and Velculescu, V. E. (2006) The consensus coding sequences of human breast and colorectal cancers. Science 314, 268-274
2. Vogelstein, B., and Kinzler, K. W. (2004) Cancer genes and the pathways they control. Nat. Med. 10, 789-799
3. Luo, J., Solimini, N. L., and Elledge, S. J. (2009) Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 136, 823-837
4. Parsons, J. T. (2003) Focal adhesion kinase. The first ten years. J. Cell Sci. 116, 1409-1416
5. Schlaepfer, D. D., and Mitra, S. K. (2004) Multiple connections link FAK to cell motility and invasion. Curr. Opin. Genet. Dev. 14, 92-101
6. Siesser, P. M., and Hanks, S. K. (2006) The signaling and biological implications of FAK overexpression in cancer. Clin. Cancer Res. 12, 3233-3237
7. Schaller, M. D. (2001) Biochemical signals and biological responses elicited by the focal adhesion kinase. Biochim. Biophys. Acta 1540, 1-21
8. Zhao, J., and Guan, J. L. (2009) Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev. 28, 35-49
9. Golubovskaya, V. M., and Cance, W. G. (2007) Focal adhesion kinase and p53 signaling in cancer cells. Int. Rev. Cytol. 263, 103-153
10. McLean, G. W., Carragher, N. O., Avizienyte, E., Evans, J., Brunton, V. G., and Frame, M. C. (2005) The role of focal-adhesion kinase in cancer-A new therapeutic opportunity. Nat. Rev. Cancer 5, 505-515
11. McLean, G. W., Komiyama, N. H., Serrels, B., Asano, H., Reynolds, L., Conti, F., Hodivala-Dilke, K., Metzger, D., Chambon, P., Grant, S. G., and Frame, M. C. (2004) Specific deletion of focal adhesion kinase suppresses tumor formation and blocks malignant progression. Genes Dev. 18, 2998-3003
12. Lahlou, H., Sanguin-Gendreau, V., Zuo, D., Cardiff, R. D., McLean, G. W., Frame, M. C., and Muller, W. J. (2007) Mammary epithelial-specific disruption of the focal adhesion kinase blocks mammary tumor progression. Proc. Natl. Acad. Sci. U. S. A. 104, 20302-20307
13. Pylayeva, Y., Gillen, K. M., Gerald, W., Beggs, H. E., Reichardt, L. F., and Giancotti, F. G. (2009) Ras-and PI3K-dependent breast tumorigenesis in mice and humans requires focal adhesion kinase signaling. J. Clin. Invest. 119, 252-266
14. Luo, M., Fan, H., Nagy, T., Wei, H., Wang, C, Liu, S., Wicha, M. S., and Guan, J. L. (2009) Mammary epithelial-specific ablation of the focal adhesion kinase suppresses mammary tumorigenesis by affecting mammary cancer stem/progenitor cells. Cancer Res. 69, 466-474
15. Provenzano, P. P., Inman, D. R., Eliceiri, K. W., Beggs, H. E., and Keely, P. J. (2008) Mammary epithelial-specific disruption of focal adhesion kinase retards tumor formation and metastasis in a transgenic mouse model of human breast cancer. Am. J. Pathol. 173, 1551-1565
16. Han, D. C, Shen, T. L., and Guan, J. L. (2000) Role of Grb7 targeting to focal contacts and its phosphorylation by focal adhesion kinase in regulation of cell migration. J. Biol. Chem. 275, 28911-28917
17. Wu, X., Suetsugu, S., Cooper, L. A., Takenawa, T., and Guan, J. L. (2004) Focal adhesion kinase regulation of N-WASP subcellular localization and function. J. Biol. Chem. 279, 9565-9576
18. Vuori, K., Hirai, H., Aizawa, S., and Ruoslahti, E. (1996) Introduction of p130cas signaling complex formation upon integrin-mediated cell adhesion. A role for Src family kinases. Mol. Cell. Biol. 16, 2606-2613
19. Ruest, P. J., Shin, N. Y., Polte, T. R., Zhang, X., and Hanks, S. K. (2001) Mechanisms of CAS substrate domain tyrosine phosphorylation by FAK and Src. Mol. Cell. Biol. 21, 7641-7652
20. Schaller, M. D., and Parsons, J. T. (1995) pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol. Cell. Biol. 15, 2635-2645
21. Petit, V., Boyer, B., Lentz, D., Turner, C. E., Thiery, J. P., and Vallés, A. M. (2000) Phosphorylation of tyrosine residues 31 and 118 on paxillin regulates cell migration through an association with CRK in NBT-II cells. J. Cell Biol. 148, 957-970
22. Wu, X., Gan, B., Yoo, Y., and Guan, J. L. (2005) FAK-mediated src phosphorylation of endophilin A2 inhibits endocytosis of MT1-MMP and promotes ECM degradation. Dev. Cell 9, 185-196
23. Avizienyte, E., and Frame, M. C. (2005) Src and FAK signalling controls adhesion fate and the epithelial-to-mesenchymal transition. Curr. Opin. Cell Biol. 17, 542-547
24. Thiery, J. P., and Sleeman, J. P. (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev. Mol. Cell Biol. 7, 131-142
25. Avizienyte, E., Wyke, A. W., Jones, R. J., McLean, G. W., Westhoff, M. A., Brunton, V. G., and Frame, M. C. (2002) Src-induced de-regulation of E-cadherin in colon cancer cells requires integrin signalling. Nat Cell Biol. 4, 632-638
26. Bailey, K. M., and Liu, J. (2008) Caveolin-1 up-regulation during epithelial to mesenchymal transition is mediated by focal adhesion kinase. J. Biol. Chem. 283, 13714-13724
27. Cicchini, C, Laudadio, I., Citarella, F., Corazzari, M., Steindler, C, Conigliaro, A., Fantoni, A., Amicone, L., and Tripodi, M. (2008) TGFβ-induced EMT requires focal adhesion kinase (FAK) signaling. Exp. Cell Res. 314, 143-152
28. Nakamura, K., Yano, H, Schaefer, E., and Sabe, H. (2001) Different modes and qualities of tyrosine phosphorylation of Fak and Pyk2 during epithelial-mesenchymal transdifferentiation and cell migration. Analysis of specific phosphorylation events using site-directed antibodies. Oncogene 20, 2626-2635
29. Prunier, C, and Howe, P. H. (2005) Disabled-2 (Dab2) is required for transforming growth factor β-induced epithelial to mesenchymal transition (EMT). J. Biol. Chem. 280, 17540-17548
30. Strizzi, L., Bianco, C, Normanno, N., Seno, M., Wechselberger, C, Wallace-Jones, B., Khan, N. I., Hirota, M., Sun, Y., Sanicola, M., and Salomon, D. S. (2004) Epithelial mesenchymal transition is a characteristic of hyperplasias and tumors in mammary gland from MMTV-Cripto-1 transgenic mice. J. Cell. Physiol. 201, 266-276
31. Rodrigo, J. P., Dominguez, F., Suárez, V., Canel, M., Secades, P., and Chiara, M. D. (2007) Focal adhesion kinase and E-cadherin as markers for nodal metastasis in laryngeal cancer. Arch. Otolaryngol. Head Neck Surg. 133, 145-150
32. Mani, S. A., Guo, W., Liao, M. J., Eaton, E. N., Ayyanan, A., Zhou, A. Y., Brooks, M., Reinhard, F., Zhang, C. C, Shipitsin, M., Campbell, L. L., Polyak, K., Brisken, C, Yang, J., and Weinberg, R. A. (2008) The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715
33. Polyak, K., and Weinberg, R. A. (2009) Transitions between epithelial and mesenchymal states. Acquisition of malignant and stem cell traits. Nat Rev. Cancer 9, 265-273
34. Taube, J. H., Herschkowitz, J. I., Komurov, K., Zhou, A. Y., Gupta, S., Yang, J., Hartwell, K., Onder, T. T., Gupta, P. B., Evans, K. W., Hollier, B. G., Ram, P. T., Lander, E. S., Rosen, J. M., Weinberg, R. A., and Mani, S. A. (2010) Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc. Natl. Acad. Sci. U. S. A. 107, 15449-15454
35. Iliopoulos, D., Hirsch, H. A., Wang, G., and Struhl, K. (2011) Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc. Natl. Acad. Sci. U. S. A. 108, 1397-1402
36. Skarnes, W. C. (2000) Gene trapping methods for the identification and functional analysis of cell surface proteins in mice. Methods Enzymol. 328, 592-615
37. Kendall, S. K., Samuelson, L. C, Saunders, T. L., Wood, R. I., and Camper, S. A. (1995) Targeted disruption of the pituitary glycoprotein hormone a-subunit produces hypogonadal and hypothyroid mice. Genes Dev. 9, 2007-2019
38. Lakso, M., Pichel, J. G., Gorman, J. R., Sauer, B., Okamoto, Y., Lee, E., Alt, F. W., and Westphal, H. (1996) Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl. Acad. Sci. U. S. A. 93, 5860-5865
39. Guy, C T., Cardiff, R. D., and Muller, W. J. (1992) Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol. Cell. Biol. 12, 954-961
40. Fan, H., and Guan, J. L. (2011) Compensatory function of Pyk2 protein in the promotion of focal adhesion kinase (FAK)-null mammary cancer stem cell tumorigenicity and metastatic activity. J. Biol. Chem. 286, 18573-18582
41. Nagy, T., Wei, H, Shen, T. L., Peng, X., Liang, C. C., Gan, B., and Guan, J. L. (2007) Mammary epithelial-specific deletion of the focal adhesion kinase gene leads to severe lobulo-alveolar hypoplasia and secretory immaturity of the murine mammary gland. J. Biol. Chem. 282, 31766-31776
42. Wei, H, Wei, S., Gan, B., Peng, X., Zou, W., and Guan, J. L. (2011) Suppression of autophagy by FIP200 deletion inhibits mammary tumorigenesis. Genes Dev. 25, 1510-1527
43. Hu, Y., and Smyth, G. K. (2009) ELDA. Extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J. Immunol. Methods 347, 70-78
44. Thiery, J. P., Acloque, H., Huang, R. Y., and Nieto, M. A. (2009) Epithelialmesenchymal transitions in development and disease. Cell 139, 871-890
45. Peinado, H., Olmeda, D., and Cano, A. (2007) Snail, Zeb, and bHLH factors in tumour progression. An alliance against the epithelial phenotype? Nat Rev. Cancer 7, 415-428
46. Asselin-Labat, M. L., Sutherland, K. D., Barker, H, Thomas, R., Shackleton, M., Forrest, N. C, Hartley, L., Robb, L., Grosveld, F. G., Van der Wees, J., Lindeman, G. J., and Visvader, J. E. (2007) Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal cell differentiation. Nat. Cell Biol. 9, 201-209
47. Kouros-Mehr, H, Bechis, S. K., Slorach, E. M., Littlepage, L. E., Egeblad, M., Ewald, A. J., Pai, S. Y., Ho, I. C, and Werb, Z. (2008) GATA-3 links tumor differentiation and dissemination in a luminal breast cancer model. Cancer Cell 13, 141-152
48. Luo, M., and Guan, J. L. (2010) Focal adhesion kinase: a prominent determinant in breast cancer initiation, progression, and metastasis. Cancer Lett. 289, 127-139
49. Parsons, J. T., Slack-Davis, J., Tilghman, R., and Roberts, W. G. (2008) Focal adhesion kinase. Targeting adhesion signaling pathways for therapeutic intervention. Clin. Cancer Res. 14, 627-632
50. Zhao, X., Peng, X., Sun, S., Park, A. Y., and Guan, J. L. (2010) Role of kinase-independent and -dependent functions of FAK in endothelial cell survival and barrier function during embryonic development. J. Cell Biol. 189, 955-965
51. Lim, S. T., Chen, X. L., Lim, Y., Hanson, D. A., Vo, T. T., Howerton, K., Larocque, N., Fisher, S. J., Schlaepfer, D. D., and Ilic, D. (2008) Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation. Mol. Cell 29, 9-22
52. Kim, J., Villadsen, R., Sørlie, T., Fogh, L., Grønlund, S. Z., Fridriksdottir, A. J., Kuhn, I., Rank, F., Wielenga, V. T., Solvang, H., Edwards, P. A., Børresen-Dale, A. L., Rønnov-Jessen, L., Bissell, M. J., and Petersen, O. W. (2012) Tumor initiating but differentiated luminal-like breast cancer cells are highly invasive in the absence of basal-like activity. Proc. Natl. Acad. Sci. U. S. A. 109, 6124-6129
53. Celià-Terrassa, T., Meca-Cortés, O., Mateo, F., De Paz, A. M., Rubio, N., Arnal-Estapé, A., Ell, B. J., Bermudo, R., Díaz, A., Guerra-Rebollo, M., Lozano, J. J., Estarás, C., Ulloa, C., Álvarez-Simón, D., Milà, J., Vilella, R., Paciucci, R., Martínez-Balbás, M., De Herreros, A. G., Gomis, R. R., Kang, Y., Blanco, J., Fernández, P. L., and Thomson, T. M. (2012) Epithelialmesenchymal transition can suppress major attributesofhuman epithelial tumor-initiating cells. J. Clin. Invest. 122, 1849-1868
54. Hildebrand, J. D., Taylor, J. M., and Parsons, J. T. (1996) An SH3 domaincontaining GTPase-activating protein for Rho and Cdc42 associates with focal adhesion kinase. Mol. Cell. Biol. 16, 3169-3178
55. Liu, Y., Loijens, J. C., Martin, K. H., Karginov, A. V., and Parsons, J. T. (2002) The association of ASAP1, an ADP ribosylation factor-GTPase activating protein, with focal adhesion kinase contributes to the process of focal adhesion assembly. Mol. Biol. Cell 13, 2147-2156
56. Messina, S., Onofri, F., Bongiorno-Borbone, L., Giovedì, S., Valtorta, F., Girault, J. A., and Benfenati, F. (2003) Specific interactions of neuronal focal adhesion kinase isoforms with Src kinases and amphiphysin. J. Neurochem. 84, 253-265
57. Littlepage, L. E., Egeblad, M., and Werb, Z. (2005) Coevolution of cancer and stromal cellular responses. Cancer Cell 7, 499-500
58. Mueller, M. M., and Fusenig, N. E. (2004) Friends or foes-bipolar effects of the tumour stroma in cancer. Nat. Rev. Cancer 4, 839-849
59. Li, X. Y., Zhou, X., Rowe, R. G., Hu, Y., Schlaepfer, D. D., Ilić, D., Dressler, G., Park, A., Guan, J. L., and Weiss, S. J. (2011) Snail1 controls epithelialmesenchymal lineage commitment in focal adhesion kinase-null embryonic cells. J. Cell Biol. 195, 729-738