Crk adaptor proteins act as key signaling integrators for breast tumorigenesis

Breast Cancer Research

Volumn 14, Issue 3, 2012, Pages

  Fathers, Kelly E ^a   Bell, Emily S ^a   Rajadurai, Charles V ^a   Cory, Sean ^a   Zhao, Hong ^b   Mourskaia, Anna ^b   Zuo, Dongmei ^b   Madore, Jason ^c   Monast, Anie ^b   Mes Masson, Anne Marie ^d   Grosset, Andree Anne ^e   Gaboury, Louis ^e   Hallet, Michael ^a   Siegel, Peter ^b   Park, Morag ^a,b,f  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

^e INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^f HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AGAR; CRK ASSOCIATED SUBSTRATE PROTEIN; CRK LIKE PROTEIN; PROTEIN CDC42; SHORT HAIRPIN RNA; BCAR1 PROTEIN, HUMAN; INTEGRIN; NUCLEAR PROTEIN; ONCOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BONE METASTASIS; BREAST CANCER; BREAST TUMOR; CANCER CELL CULTURE; CANCER GROWTH; CANCER PATIENT; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SPREADING; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MAMMARY GLAND; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIBIA; TISSUE MICROARRAY; TUMOR GROWTH; ANIMAL; BONE TUMOR; CANCER INVASION; CELL MOTION; CELL TRANSFORMATION; EXPERIMENTAL NEOPLASM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METASTASIS; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BONE NEOPLASMS; BREAST NEOPLASMS; CDC42 GTP-BINDING PROTEIN; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CRK-ASSOCIATED SUBSTRATE PROTEIN; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTEGRINS; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-CRK; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84860621179     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr3183     Document Type: Article

References (52)

1. Mayer BJ, Hamaguchi M, Hanafusa H. A novel viral oncogene with structural similarity to phospholipase C. Nature 1988, 332:272-275. 10.1038/332272a0, 2450282.
2. Matsuda M, Tanaka S, Nagata S, Kojima A, Kurata T, Shibuya M. Two species of human CRK cDNA encode proteins with distinct biological activities. Mol Cell Biol 1992, 12:3482-3489. 364597, 1630456.
3. Chodniewicz D, Klemke RL. Regulation of integrin-mediated cellular responses through assembly of a CAS/Crk scaffold. Biochim Biophys Acta 2004, 1692:63-76. 10.1016/j.bbamcr.2004.03.006, 15246680.
4. Lamorte L, Royal I, Naujokas M, Park M. Crk adapter proteins promote an epithelial-mesenchymal-like transition and are required for HGF-mediated cell spreading and breakdown of epithelial adherens junctions. Mol Biol Cell 2002, 13:1449-1461. 10.1091/mbc.01-10-0477, 111118, 12006644.
5. Lamorte L, Rodrigues S, Naujokas M, Park M. Crk synergizes with epidermal growth factor for epithelial invasion and morphogenesis and is required for the met morphogenic program. J Biol Chem 2002, 277:37904-37911. 10.1074/jbc.M201743200, 12138161.
6. Rodrigues SP, Fathers KE, Chan G, Zuo D, Halwani F, Meterissian S, Park M. CrkI and CrkII function as key signaling integrators for migration and invasion of cancer cells. Mol Cancer Res 2005, 3:183-194.
7. Iwahara T, Akagi T, Shishido T, Hanafusa H. CrkII induces serum response factor activation and cellular transformation through its function in Rho activation. Oncogene 2003, 22:5946-5957. 10.1038/sj.onc.1206633, 12955073.
8. Senechal K, Heaney C, Druker B, Sawyers CL. Structural requirements for function of the Crkl adapter protein in fibroblasts and hematopoietic cells. Mol Cell Biol 1998, 18:5082-5090. 109093, 9710592.
9. Fathers KE, Rodrigues S, Zuo D, Murthy IV, Hallett M, Cardiff R, Park M. CrkII transgene induces atypical mammary gland development and tumorigenesis. Am J Pathol 2010, 176:446-460. 10.2353/ajpath.2010.090383, 2797903, 20008144.
10. Hemmeryckx B, van Wijk A, Reichert A, Kaartinen V, de Jong R, Pattengale PK, Gonzalez-Gomez I, Groffen J, Heisterkamp N. Crkl enhances leukemogenesis in BCR/ABL P190 transgenic mice. Cancer Res 2001, 61:1398-1405.
11. Takino T, Nakada M, Miyamori H, Yamashita J, Yamada KM, Sato H. CrkI adapter protein modulates cell migration and invasion in glioblastoma. Cancer Res 2003, 63:2335-2337.
12. Nishihara H, Tanaka S, Tsuda M, Oikawa S, Maeda M, Shimizu M, Shinomiya H, Tanigami A, Sawa H, Nagashima K. Molecular and immunohistochemical analysis of signaling adaptor protein Crk in human cancers. Cancer Lett 2002, 180:55-61. 10.1016/S0304-3835(01)00763-7, 11911970.
13. Feng R, Chen X, Yu Y, Su L, Yu B, Li J, Cai Q, Yan M, Liu B, Zhu Z. miR-126 functions as a tumour suppressor in human gastric cancer. Cancer Lett 298:50-63.
14. Miller CT, Chen G, Gharib TG, Wang H, Thomas DG, Misek DE, Giordano TJ, Yee J, Orringer MB, Hanash SM, Beer DG. Increased C-CRK proto-oncogene expression is associated with an aggressive phenotype in lung adenocarcinomas. Oncogene 2003, 22:7950-7957. 10.1038/sj.onc.1206529, 12970743.
15. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, Guise TA, Massague J. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 2003, 3:537-549. 10.1016/S1535-6108(03)00132-6, 12842083.
16. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J. Genes that mediate breast cancer metastasis to lung. Nature 2005, 436:518-524. 10.1038/nature03799, 1283098, 16049480.
17. Fillmore CM, Kuperwasser C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res 2008, 10:R25. 10.1186/bcr1982, 2397524, 18366788.
18. Dickins RA, Hemann MT, Zilfou JT, Simpson DR, Ibarra I, Hannon GJ, Lowe SW. Probing tumor phenotypes using stable and regulated synthetic microRNA precursors. Nat Genet 2005, 37:1289-1295.
19. Mak HH, Peschard P, Lin T, Naujokas MA, Zuo D, Park M. Oncogenic activation of the Met receptor tyrosine kinase fusion protein, Tpr-Met, involves exclusion from the endocytic degradative pathway. Oncogene 2007, 26:7213-7221. 10.1038/sj.onc.1210522, 17533376.
20. Fathers KE, Stone CM, Minhas K, Marriott JJ, Greenwood JD, Dumont DJ, Coomber BL. Heterogeneity of Tie2 expression in tumor microcirculation: influence of cancer type, implantation site, and response to therapy. Am J Pathol 2005, 167:1753-1762. 10.1016/S0002-9440(10)61256-4, 1613180, 16314485.
21. Briancon-Marjollet A, Ghogha A, Nawabi H, Triki I, Auziol C, Fromont S, Piche C, Enslen H, Chebli K, Cloutier JF, Castellani V, Debant A, Lamarche-Vane N. Trio mediates netrin-1-induced Rac1 activation in axon outgrowth and guidance. Mol Cell Biol 2008, 28:2314-2323. 10.1128/MCB.00998-07, 2268419, 18212043.
22. Ivshina AV, George J, Senko O, Mow B, Putti TC, Smeds J, Lindahl T, Pawitan Y, Hall P, Nordgren H, Wong JE, Liu ET, Bergh J, Kuznetsov VA, Miller LD. Genetic reclassification of histologic grade delineates new clinical subtypes of breast cancer. Cancer Res 2006, 66:10292-10301. 10.1158/0008-5472.CAN-05-4414, 17079448.
23. Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, Davies S, Fauron C, He X, Hu Z, Quackenbush JF, Stijleman IJ, Palazzo J, Marron JS, Nobel AB, Mardis E, Nielsen TO, Ellis MJ, Perou CM, Bernard PS. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 2009, 27:1160-1167. 10.1200/JCO.2008.18.1370, 2667820, 19204204.
24. Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP, Yang F, Talantov D, Timmermans M, Meijer-van Gelder ME, Yu J, Jatkoe T, Berns EM, Atkins D, Foekens JA. Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 2005, 365:671-679.
25. van de Vijver MJ, He YD, van't Veer LJ, Dai H, Hart AA, Voskuil DW, Schreiber GJ, Peterse JL, Roberts C, Marton MJ, Parrish M, Atsma D, Witteveen A, Glas A, Delahaye L, van der Velde T, Bartelink H, Rodenhuis S, Rutgers ET, Friend SH, Bernards R. A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med 2002, 347:1999-2009. 10.1056/NEJMoa021967, 12490681.
26. Loi S, Haibe-Kains B, Desmedt C, Wirapati P, Lallemand F, Tutt AM, Gillet C, Ellis P, Ryder K, Reid JF, Daidone MG, Pierotti MA, Berns EM, Jansen MP, Foekens JA, Delorenzi M, Bontempi G, Piccart MJ, Sotiriou C. Predicting prognosis using molecular profiling in estrogen receptor-positive breast cancer treated with tamoxifen. BMC Genomics 2008, 9:239. 10.1186/1471-2164-9-239, 2423197, 18498629.
27. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, Clark L, Bayani N, Coppe JP, Tong F, Speed T, Spellman PT, DeVries S, Lapuk A, Wang NJ, Kuo WL, Stilwell JL, Pinkel D, Albertson DG, Waldman FM, McCormick F, Dickson RB, Johnson MD, Lippman M, Ethier S, Gazdar A, Gray JW. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006, 10:515-527. 10.1016/j.ccr.2006.10.008, 2730521, 17157791.
28. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5:R80. 10.1186/gb-2004-5-10-r80, 545600, 15461798.
29. Demers M, Rose AA, Grosset AA, Biron-Pain K, Gaboury L, Siegel PM, St-Pierre Y. Overexpression of galectin-7, a myoepithelial cell marker, enhances spontaneous metastasis of breast cancer cells. Am J Pathol 176:3023-3031.
30. Senechal K, Halpern J, Sawyers CL. The CRKL adaptor protein transforms fibroblasts and functions in transformation by the BCR-ABL oncogene. J Biol Chem 1996, 271:23255-23261. 10.1074/jbc.271.38.23255, 8798523.
31. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Eystein Lonning P, Borresen-Dale AL. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 2001, 98:10869-10874. 10.1073/pnas.191367098, 58566, 11553815.
32. Nobes CD, Hall A. Rho, rac and cdc42 GTPases: regulators of actin structures, cell adhesion and motility. Biochem Soc Trans 1995, 23:456-459.
33. Mourskaia AA, Dong Z, Ng S, Banville M, Zwaagstra JC, O'Connor-McCourt MD, Siegel PM. Transforming growth factor-beta1 is the predominant isoform required for breast cancer cell outgrowth in bone. Oncogene 2009, 28:1005-1015. 10.1038/onc.2008.454, 19079339.
34. Klemke RL, Leng J, Molander R, Brooks PC, Vuori K, Cheresh DA. CAS/Crk coupling serves as a "molecular switch" for induction of cell migration. J Cell Biol 1998, 140:961-972. 10.1083/jcb.140.4.961, 2141747, 9472046.
35. Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, Damsky C, Bissell MJ. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 1997, 137:231-245. 10.1083/jcb.137.1.231, 2139858, 9105051.
36. Park CC, Zhang H, Pallavicini M, Gray JW, Baehner F, Park CJ, Bissell MJ. Beta1 integrin inhibitory antibody induces apoptosis of breast cancer cells, inhibits growth, and distinguishes malignant from normal phenotype in three dimensional cultures and in vivo. Cancer Res 2006, 66:1526-1535. 10.1158/0008-5472.CAN-05-3071, 2933188, 16452209.
37. Defilippi P, Di Stefano P, Cabodi S. p130Cas: a versatile scaffold in signaling networks. Trends Cell Biol 2006, 16:257-263. 10.1016/j.tcb.2006.03.003, 16581250.
38. Linghu H, Tsuda M, Makino Y, Sakai M, Watanabe T, Ichihara S, Sawa H, Nagashima K, Mochizuki N, Tanaka S. Involvement of adaptor protein Crk in malignant feature of human ovarian cancer cell line MCAS. Oncogene 2006, 25:3547-3556. 10.1038/sj.onc.1209398, 16491127.
39. Tavazoie SF, Alarcon C, Oskarsson T, Padua D, Wang Q, Bos PD, Gerald WL, Massague J. Endogenous human microRNAs that suppress breast cancer metastasis. Nature 2008, 451:147-152. 10.1038/nature06487, 2782491, 18185580.
40. Abassi YA, Vuori K. Tyrosine 221 in Crk regulates adhesion-dependent membrane localization of Crk and Rac and activation of Rac signaling. Embo J 2002, 21:4571-4582. 10.1093/emboj/cdf446, 126186, 12198159.
41. Eckert LB, Repasky GA, Ulku AS, McFall A, Zhou H, Sartor CI, Der CJ. Involvement of Ras activation in human breast cancer cell signaling, invasion, and anoikis. Cancer Res 2004, 64:4585-4592. 10.1158/0008-5472.CAN-04-0396, 15231670.
42. Campbell PM, Der CJ. Oncogenic Ras and its role in tumor cell invasion and metastasis. Semin Cancer Biol 2004, 14:105-114. 10.1016/j.semcancer.2003.09.015, 15018894.
43. Karnoub AE, Symons M, Campbell SL, Der CJ. Molecular basis for Rho GTPase signaling specificity. Breast Cancer Res Treat 2004, 84:61-71. 10.1023/B:BREA.0000018427.84929.5c, 14999155.
44. Qiu RG, Abo A, McCormick F, Symons M. Cdc42 regulates anchorage-independent growth and is necessary for Ras transformation. Mol Cell Biol 1997, 17:3449-3458. 232198, 9154844.
45. Tang DD, Zhang W, Gunst SJ. The adapter protein CrkII regulates neuronal Wiskott-Aldrich syndrome protein, actin polymerization, and tension development during contractile stimulation of smooth muscle. J Biol Chem 2005, 280:23380-23389. 10.1074/jbc.M413390200, 15834156.
46. Shibue T, Weinberg RA. Integrin beta1-focal adhesion kinase signaling directs the proliferation of metastatic cancer cells disseminated in the lungs. Proc Natl Acad Sci USA 2009, 106:10290-10295. 10.1073/pnas.0904227106, 2700942, 19502425.
47. Kren A, Baeriswyl V, Lehembre F, Wunderlin C, Strittmatter K, Antoniadis H, Fassler R, Cavallaro U, Christofori G. Increased tumor cell dissemination and cellular senescence in the absence of beta1-integrin function. Embo J 2007, 26:2832-2842. 10.1038/sj.emboj.7601738, 1894776, 17541405.
48. Mayer BJ, Hanafusa H. Association of the v-crk oncogene product with phosphotyrosine-containing proteins and protein kinase activity. Proc Natl Acad Sci USA 1990, 87:2638-2642. 10.1073/pnas.87.7.2638, 53745, 1690891.
49. Matsuda M, Mayer BJ, Fukui Y, Hanafusa H. Binding of transforming protein, P47gag-crk, to a broad range of phosphotyrosine-containing proteins. Science 1990, 248:1537-1539. 10.1126/science.1694307, 1694307.
50. Matsuda M, Mayer BJ, Hanafusa H. Identification of domains of the v-crk oncogene product sufficient for association with phosphotyrosine-containing proteins. Mol Cell Biol 1991, 11:1607-1613. 369454, 1705010.
51. Iwahara T, Akagi T, Fujitsuka Y, Hanafusa H. CrkII regulates focal adhesion kinase activation by making a complex with Crk-associated substrate, p130Cas. Proc Natl Acad Sci USA 2004, 101:17693-17698. 10.1073/pnas.0408413102, 539787, 15598735.
52. Watanabe T, Tsuda M, Makino Y, Ichihara S, Sawa H, Minami A, Mochizuki N, Nagashima K, Tanaka S. Adaptor molecule Crk is required for sustained phosphorylation of Grb2-associated binder 1 and hepatocyte growth factor-induced cell motility of human synovial sarcoma cell lines. Mol Cancer Res 2006, 4:499-510. 10.1158/1541-7786.MCR-05-0141, 16849525.