Focal adhesion kinase-related proline-rich tyrosine kinase 2 and focal adhesion kinase are co-overexpressed in early-stage and invasive ErbB-2-positive breast cancer and cooperate for breast cancer cell tumorigenesis and invasiveness

American Journal of Pathology

Volumn 173, Issue 5, 2008, Pages 1540-1550

  Behmoaram, Emy ^a   Bijian, Krikor ^a   Jie, Su ^a   Xu, Yingjie ^a   Darnel, Andrew ^a   Bismar, Tarek A ^b,c   Alaoui Jamali, Moulay A ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE 1; FOCAL ADHESION KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE;

ADVANCED CANCER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER INHIBITION; CANCER INVASION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; DOWN REGULATION; EARLY CANCER; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG METASTASIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; TISSUE DISTRIBUTION; TUMOR GROWTH;

EID: 55349138779     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2008.080292     Document Type: Article

References (66)

1. Du QS, Ren XR, Xie Y, Wang Q, Mei L, Xiong WC: Inhibition of PYK2-induced actin cytoskeleton reorganization: PYK2 autophosphorylation and focal adhesion targeting by FAK. J Cell Sci 2001, 114:2977-2987
2. Chen HC, Appeddu PA, Parsons JT, Hildebrand JD, Schaller MD, Guan JL: Interaction of focal adhesion kinase with cytoskeletal protein talin. J Biol Chem 1995, 270:16995-16999
3. Vadlamudi RK, Adam L, Nguyen D, Santos M, Kumar R: Differential regulation of components of the focal adhesion complex by heregulin: role of phosphatase SHP-2. J Cell Physiol 2002, 190:189-199
4. Giancotti FG, Ruoslahti E: Integrin signaling. Science 1999, 285:1028-1032
5. Sieg DJ, Hauck CR, Ilic D, Klingbeil CK, Schaefer E, Damsky CH, Schlaepfer DD: FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol 2000, 2:249-256
6. Andreev J, Simon JP, Sabatini DD, Kam J, Plowman G, Randazzo PA, Schlessinger J: Identification of a new Pyk2 target protein with Arf-GAP activity. Mol Cell Biol 1999, 19:2338-2350
7. Sieg DJ, Ilic D, Jones KC, Damsky CH, Hunter T, Schlaepfer DD: Pyk2 and Src-family protein-tyrosine kinases compensate for the loss of FAK in fibronectin-stimulated signaling events but Pyk2 does not fully function to enhance FAK- cell migration. EMBO J 1998, 17:5933-5947
8. Zheng C, Xing Z, Bian ZC, Guo C, Akbay A, Warner L, Guan JL: Differential regulation of Pyk2 and focal adhesion kinase (FAK): the C-terminal domain of FAK confers response to cell adhesion. J Biol Chem 1998, 273:2384-2389
9. Sabri A, Govindarajan G, Griffin TM, Byron KL, Samarel AM, Lucchesi PA: Calcium- and protein kinase C-dependent activation of the tyrosine kinase PYK2 by angiotensin II in vascular smooth muscle. Circ Res 1998, 83:841-851
10. Sasaki H, Nagura K, Ishino M, Tobioka H, Kotani K, Sasaki T: Cloning and characterization of cell adhesion kinase beta, a novel protein-tyrosine kinase of the focal adhesion kinase subfamily. J Biol Chem 1995, 270:21206-21219
11. Liu S, Thomas SM, Woodside DG, Rose DM, Kiosses WB, Pfaff M, Ginsberg MH: Binding of paxillin to alpha4 integrins modifies integrin-dependent biological responses. Nature 1999, 402:676-681
12. Lev S, Hernandez J, Martinez R, Chen A, Plowman G, Schlessinger J: Identification of a novel family of targets of PYK2 related to Drosophila retinal degeneration B (rdgB) protein. Mol Cell Biol 1999, 19:2278-2288
13. Matsuya M, Sasaki H, Aoto H, Mitaka T, Nagura K, Ohba T, Ishino M, Takahashi S, Suzuki R, Sasaki T: Cell adhesion kinase beta forms a complex with a new member: Hic-5, of proteins localized at focal adhesions. J Biol Chem 1998, 273:1003-1014
14. Ren XR, Du QS, Huang YZ, Ao SZ, Mei L, Xiong WC: Regulation of CDC42 GTPase by proline-rich tyrosine kinase 2 interacting with PSGAP, a novel Pleckstrin homology and Src homology 3 domain containing rhoGAP protein. J Cell Biol 2001, 152:971-984
15. Xiong W, Parsons JT: Induction of apoptosis after expression of PYK2, a tyrosine kinase structurally related to focal adhesion kinase. J Cell Biol 1997, 139:529-539
16. Frisch SM, Vuori K, Ruoslahti E, Chan-Hui PY: Control of adhesion-dependent cell survival by focal adhesion kinase. J Cell Biol 1996, 134:793-799
17. 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
18. Zhao J, Zheng C, Guan J: Pyk2 and FAK differentially regulate progression of the cell cycle. J Cell Sci 2000, 113:3063-3072
19. Lunn JA, Jacamo R, Rozengurt E: Preferential phosphorylation of focal adhesion kinase tyrosine 861 is critical for mediating an antiapoptotic response to hyperosmotic stress. J Biol Chem 2007, 282:10370-10379
20. Lipinski CA, Tran NL, Menashi E, Rohl C, Kloss J, Bay RC, Berens ME, Loftus JC: The tyrosine kinase pyk2 promotes migration and invasion of glioma cells. Neoplasia 2005, 7:435-445
21. Bogenrieder T, Herlyn M: Axis of evil: molecular mechanisms of cancer metastasis. Oncogene 2003, 22:6524-6536
22. de Amicis F, Lanzino M, Kisslinger A, Cali G, Chieffi P, Ando S, Mancini FP, Tramontano D: Loss of proline-rich tyrosine kinase 2 function induces spreading and motility of epithelial prostate cells. J Cell Physiol 2006, 209:74-80
23. Stanzione R, Picascia A, Chieffi P, Imbimbo C, Palmieri A, Mirone V, Staibano S, Franco R, De Rosa G, Schlessinger J, Tramontano D: Variations of proline-rich kinase Pyk2 expression correlate with prostate cancer progression. Lab Invest 2001, 81:51-59
24. Yano H, Mazaki Y, Kurokawa K, Hanks SK, Matsuda M, Sabe H: Roles played by a subset of integrin signaling molecules in cadherin-based cell-cell adhesion. J Cell Biol 2004, 166:283-295
25. Yano H, Uchida H, Iwasaki T, Mukai M, Akedo H, Nakamura K, Hashimoto S, Sabe H: Paxillin alpha and Crk-associated substrate exert opposing effects on cell migration and contact inhibition of growth through tyrosine phosphorylation. Proc Natl Acad Sci USA 2000, 97:9076-9081
26. Benlimame N, He Q, Jie S, Xiao D, Xu YJ, Loignon M, Schlaepfer DD, Alaoui-Jamali MA: FAK signaling is critical for ErbB-2/ErbB-3 receptor cooperation for oncogenic transformation and invasion. J Cell Biol 2005, 171:505-516
27. Yen L, Benlimame N, Nie ZR, Xiao D, Wang T, Al Moustafa AE, Esumi H, Milanini J, Hynes NE, Pages G, Alaoui-Jamali MA: Differential regulation of tumor angiogenesis by distinct ErbB homo- and heterodimers. Mol Biol Cell 2002, 13:4029-4044
28. Rubin MA, Dunn R, Strawderman M, Pienta KJ: Tissue microarray sampling strategy for prostate cancer biomarker analysis. Am J Surg Pathol 2002, 26:312-319
29. Alimandi M, Romano A, Curia MC, Muraro R, Fedi P, Aaronson SA, Di Fiore PP, Kraus MH: Cooperative signaling of ErbB3 and ErbB2 in neoplastic transformation and human mammary carcinomas. Oncogene 1995, 10:1813-1821
30. Pinkas-Kramarski R, Soussan L, Waterman H, Levkowitz G, Alroy I, Klapper L, Lavi S, Seger R, Ratzkin BJ, Sela M, Yarden Y: Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interactions. EMBO J 1996, 15:2452-2467
31. Cary LA, Guan JL: Focal adhesion kinase in integrin-mediated signaling. Front Biosci 1999, 4:D102-D113
32. Oktay MH, Oktay K, Hamele-Bena D, Buyuk A, Koss LG: Focal adhesion kinase as a marker of malignant phenotype in breast and cervical carcinomas. Hum Pathol 2003, 34:240-245
33. Watermann DO, Gabriel B, Jager M, Orlowska-Volk M, Hasenburg A, zur Hausen A, Gitsch G, Stickeler E: Specific induction of pp125 focal adhesion kinase in human breast cancer. Br J Cancer 2005, 93:694-698
34. Agochiya M, Brunton VG, Owens DW, Parkinson EK, Paraskeva C, Keith WN, Frame MC: Increased dosage and amplification of the focal adhesion kinase gene in human cancer cells. Oncogene 1999, 18:5646-5653
35. Cance WG, Harris JE, Iacocca MV, Roche E, Yang X, Chang J, Simkins S, Xu L: Immunohistochemical analyses of focal adhesion kinase expression in benign and malignant human breast and colon tissues: correlation with preinvasive and invasive phenotypes. Clin Cancer Res 2000, 6:2417-2423
36. Judson PL, He X, Cance WG, Van Le L: Overexpression of focal adhesion kinase, a protein tyrosine kinase, in ovarian carcinoma. Cancer 1999, 86:1551-1556
37. Owens LV, Xu L, Craven RJ, Dent GA, Weiner TM, Kornberg L, Liu ET, Cance WG: Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors. Cancer Res 1995, 55:2752-2755
38. Madan R, Smolkin MB, Cocker R, Fayyad R, Oktay MH: Focal adhesion proteins as markers of malignant transformation and prognostic indicators in breast carcinoma. Hum Pathol 2006, 37:9-15
39. Sun CK, Ng KT, Sun BS, Ho JW, Lee TK, Ng I, Poon RT, Lo CM, Liu CL, Man K, Fan ST: The significance of proline-rich tyrosine kinase2 (Pyk2) on hepatocellular carcinoma progression and recurrence. Br J Cancer 2007, 97:50-57
40. Guo HJ, Wang X, Liu YC, Wan YL, Yin HF, Li T, Zhu J: [Expression of proline-rich tyrosine kinase-2 (Pyk2) in gastric carcinoma and its significance]. Beijing Da Xue Xue Bao 2005, 37:261-264
41. Gutenberg A, Bruck W, Buchfelder M, Ludwig HC: Expression of tyrosine kinases FAK and Pyk2 in 331 human astrocytomas. Acta Neuropathol (Berl) 2004, 108:224-230
42. Schröder A, Delling G, Kaiser EA: [Expression analysis of protein tyrosine kinases of the FAK (focal adhesion kinase) family in osteosarcoma]. Pathologe 2002, 23:361-366
43. Zrihan-Licht S, Fu Y, Settleman J, Schinkmann K, Shaw L, Keydar I, Avraham S, Avraham H: RAFTK/Pyk2 tyrosine kinase mediates the association of p190 RhoGAP with RasGAP and is involved in breast cancer cell invasion. Oncogene 2000, 19:1318-1328
44. Lim Y, Lim ST, Tomar A, Gardel M, Bernard-Trifilo JA, Chen XL, Uryu SA, Canete-Soler R, Zhai J, Lin H, Schlaepfer WW, Nalbant P, Bokoch G, Ilic D, Waterman-Storer C, Schlaepfer DD: PyK2 and FAK connections to p190Rho guanine nucleotide exchange factor regulate RhoA activity, focal adhesion formation, and cell motility. J Cell Biol 2008, 180:187-203
45. Owen KA, Pixley FJ, Thomas KS, Vicente-Manzanares M, Ray BJ, Horwitz AF, Parsons JT, Beggs HE, Stanley ER, Bouton AH: Regulation of lamellipodial persistence, adhesion turnover, and motility in macrophages by focal adhesion kinase. J Cell Biol 2007, 179:1275-1287
46. Daub H, Weiss FU, Wallasch C, Ullrich A: Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 1996, 379:557-560
47. Hendriks BS, Orr G, Wells A, Wiley HS, Lauffenburger DA: Parsing ERK activation reveals quantitatively equivalent contributions from epidermal growth factor receptor and HER2 in human mammary epithelial cells. J Biol Chem 2005, 280:6157-6169
48. Jackson JG, St Clair P, Sliwkowski MX, Brattain MG: Blockade of epidermal growth factor- or heregulin-dependent ErbB2 activation with the anti-ErbB2 monoclonal antibody 2C4 has divergent downstream signaling and growth effects. Cancer Res 2004, 64:2601-2609
49. Kumagai T, Davis JG, Horie T, O'Rourke DM, Greene MI: The role of distinct p185neu extracellular subdomains for dimerization with the epidermal growth factor (EGF) receptor and EGF-mediated signaling. Proc Natl Acad Sci USA 2001, 98:5526-5531
50. Pinkas-Kramarski R, Shelly M, Guarino BC, Wang LM, Lyass L, Alroy I, Alimandi M, Kuo A, Moyer JD, Lavi S, Eisenstein M, Ratzkin BJ, Seger R, Bacus SS, Pierce JH, Andrews GC, Yarden Y: ErbB tyrosine kinases and the two neuregulin families constitute a ligand-receptor network. Mol Cell Biol 1998, 18:6090-6101
51. Qian X, O'Rourke DM, Fei Z, Zhang HT, Kao CC, Greene MI: Domain-specific interactions between the p185(neu) and epidermal growth factor receptor kinases determine differential signaling outcomes. J Biol Chem 1999, 274:574-583
52. Seton-Rogers SE, Lu Y, Hines LM, Koundinya M, LaBaer J, Muthuswamy SK, Brugge JS: Cooperation of the ErbB2 receptor and transforming growth factor beta in induction of migration and invasion in mammary epithelial cells. Proc Natl Acad Sci USA 2004, 101:1257-1262
53. Tikhomirov O, Carpenter G: Ligand-induced, p38-dependent apoptosis in cells expressing high levels of epidermal growth factor receptor and ErbB-2. J Biol Chem 2004, 279:12988-12996
54. Almeida EA, Ilic D, Han Q, Hauck CR, Jin F, Kawakatsu H, Schlaepfer DD, Damsky CH: Matrix survival signaling: from fibronectin via focal adhesion kinase to c-Jun NH(2)-terminal kinase. J Cell Biol 2000, 149:741-754
55. Hauck CR, Hsia DA, Schlaepfer DD: Focal adhesion kinase facilitates platelet-derived growth factor-BB-stimulated ERK2 activation required for chemotaxis migration of vascular smooth muscle cells. J Biol Chem 2000, 275:41092-41099
56. Klingbeil CK, Hauck CR, Hsia DA, Jones KC, Reider SR, Schlaepfer DD: Targeting Pyk2 to beta 1-integrin-containing focal contacts rescues fibronectin-stimulated signaling and haptotactic motility defects of focal adhesion kinase-null cells. J Cell Biol 2001, 152:97-110
57. Sawhney RS, Cookson MM, Omar Y, Hauser J, Brattain MG: Integrin alpha2-mediated ERK and calpain activation play a critical role in cell adhesion and motility via focal adhesion kinase signaling: identification of a novel signaling pathway. J Biol Chem 2006, 281:8497-8510
58. Schlaepfer DD, Hou S, Lim ST, Tomar A, Yu H, Lim Y, Hanson DA, Uryu SA, Molina J, Mitra SK: Tumor necrosis factor-alpha stimulates focal adhesion kinase activity required for mitogen-activated kinase-associated interleukin 6 expression. J Biol Chem 2007, 282:17450-17459
59. Schlaepfer DD, Jones KC, Hunter T: Multiple Grb2-mediated integrin-stimulated signaling pathways to ERK2/mitogen-activated protein kinase: summation of both c-Src- and focal adhesion kinase-initiated tyrosine phosphorylation events. Mol Cell Biol 1998, 18:2571-2585
60. Lebrun P, Baron V, Hauck CR, Schlaepfer DD, Van Obberghen E: Cell adhesion and focal adhesion kinase regulate insulin receptor substrate-1 expression. J Biol Chem 2000, 275:38371-38377
61. Renshaw MW, Price LS, Schwartz MA: Focal adhesion kinase mediates the integrin signaling requirement for growth factor activation of MAP kinase. J Cell Biol 1999, 147:611-618
62. Lahlou H, Sanguin-Gendreau V, Zuo D, Cardiff RD, McLean GW, Frame MC, Muller WJ: Mammary epithelial-specific disruption of the focal adhesion kinase blocks mammary tumor progression. Proc Natl Acad Sci USA 2007, 104:20302-20307
63. Slack-Davis JK, Martin KH, Tilghman RW, Iwanicki M, Ung EJ, Autry C, Luzzio MJ, Cooper B, Kath JC, Roberts WG, Parsons JT: Cellular characterization of a novel focal adhesion kinase inhibitor. J Biol Chem 2007, 282:14845-14852
64. Halder J, Lin YG, Merritt WM, Spannuth WA, Nick AM, Honda T, Kamat AA, Han LY, Kim TJ, Lu C, Tari AM, Bornmann W, Fernandez A, Lopez-Berestein G, Sood AK: Therapeutic efficacy of a novel focal adhesion kinase inhibitor TAE226 in ovarian carcinoma. Cancer Res 2007, 67:10976-10983
65. Roberts WG, Ung E, Whalen P, Cooper B, Hulford C, Autry C, Richter D, Emerson E, Lin J, Kath J, Coleman K, Yao L, Martinez-Alsina L, Lorenzen M, Berliner M, Luzzio M, Patel N, Schmitt E, LaGreca S, Jani J, Wessel M, Marr E, Griffor M, Vajdos F: Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562271. Cancer Res 2008, 68:1935-1944
66. Siu LL, Burns HA, Mileshkin L, Camidge DR, Rischin D, Chen EX, Jones S, Yin D, Fingert H: Phase 1 study of a focal adhesion kinase (FAK) inhibitor PF-00562271 in patients (pts) with advanced solid tumors. ASCO Annual Meeting Proceedings Part I. J Clin Oncol 2007, Abstract 3527