Tyrosine phosphatase SHP2 increases cell motility in triple-negative breast cancer through the activation of SRC-family kinases

Oncogene

Volumn 34, Issue 17, 2015, Pages 2272-2278

  Sausgruber, N ^a   Coissieux, M M ^a   Britschgi, A ^a   Wyckoff, J ^a,b   Aceto, N ^a,c   Leroy, C ^a,d   Stadler, M B ^a,e   Voshol, H ^d   Bonenfant, D ^d   Bentires Alj, M ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d NOVARTIS PHARMA AG   (Switzerland)

^e SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE SHP 2; TUMOR PROTEIN;

ANIMAL; BREAST TUMOR; CANCER TRANSPLANTATION; CELL MOTION; ENZYMOLOGY; FEMALE; GENETICS; HUMAN; METABOLISM; MOUSE; PATHOLOGY; TUMOR CELL LINE; TUMOR INVASION; XENOGRAFT;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; HETEROGRAFTS; HUMANS; MICE; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; SRC-FAMILY KINASES;

EID: 84933530310     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.170     Document Type: Article

References (29)

1. Perou CM. Molecular stratification of triple-negative breast cancers. Oncologist 2010; 15: 39-48.
2. Aceto N, Sausgruber N, Brinkhaus H, Gaidatzis D, Martiny-Baron G, Mazzarol G et al. Tyrosine phosphatase SHP2 promotes breast cancer progression and maintains tumor-initiating cells via activation of key transcription factors and a positive feedback signaling loop. Nat Med 2012; 18: 529-537.
3. Wang FM, Liu HQ, Liu SR, Tang SP, Yang L, Feng GS. SHP-2 promoting migration and metastasis of MCF-7 with loss of E-cadherin, dephosphorylation of FAK and secretion of MMP-9 induced by IL-1beta in vivo and in vitro. Breast Cancer Res Treat 2005; 89: 5-14.
4. Patsialou A, Wang Y, Lin J, Whitney K, Goswami S, Kenny PA et al. Selective gene-expression profiling of migratory tumor cells in vivo predicts clinical outcome in breast cancer patients. Breast Cancer Res 2012; 14 : R139.
5. Bonapace L, Wyckoff J, Oertner T, Van Rheenen J, Junt T, Bentires-Alj M. If you don't look, you won't see: intravital multiphoton imaging of primary and metastatic breast cancer. J Mammary Gland Biol Neoplasia 2012; 17: 125-129.
6. Zomer A, Beerling E, Vlug EJ, van Rheenen J. Real-time intravital imaging of cancer models. Clin Transl Oncol 2011; 13: 848-854.
7. Liu H, Patel MR, Prescher JA, Patsialou A, Qian D, Lin J et al. Cancer stem cells from human breast tumors are involved in spontaneous metastases in orthotopic mouse models. Proc Natl Acad Sci USA 2010; 107: 18115-18120.
8. Pawitan Y, Bjohle J, Amler L, Borg AL, Egyhazi S, Hall P et al. Gene expression profiling spares early breast cancer patients from adjuvant therapy: derived and validated in two population-based cohorts. Breast Cancer Res 2005; 7: R953-R964.
9. Yamaguchi H, Wyckoff J, Condeelis J. Cell migration in tumors. Curr Opin Cell Biol 2005; 17: 559-564.
10. Zhang SQ, Yang W, Kontaridis MI, Bivona TG, Wen G, Araki T et al. Shp2 regulates SRC family kinase activity and Ras/Erk activation by controlling Csk recruitment. Mol Cell 2004; 13: 341-355.
11. Ishizawar R, Parsons SJ. c-Src and cooperating partners in human cancer. Cancer Cell 2004; 6: 209-214.
12. Ren Y, Meng S, Mei L, Zhao ZJ, Jove R, Wu J. Roles of Gab1 and SHP2 in paxillin tyrosine dephosphorylation and Src activation in response to epidermal growth factor. J Biol Chem 2004; 279: 8497-8505.
13. Peng ZY, Cartwright CA. Regulation of the Src tyrosine kinase and Syp tyrosine phosphatase by their cellular association. Oncogene 1995; 11: 1955-1962.
14. Sachdev S, Bu Y, Gelman IH. Paxillin-Y118 phosphorylation contributes to the control of Src-induced anchorage-independent growth by FAK and adhesion. BMC Cancer 2009; 9: 12.
15. Roof RW, Haskell MD, Dukes BD, Sherman N, Kinter M, Parsons SJ. Phosphotyrosine (p-Tyr)-dependent and -independent mechanisms of p190 RhoGAP-p120 RasGAP interaction: Tyr 1105 of p190, a substrate for c-Src, is the sole p-Tyr mediator of complex formation. Mol Cell Biol 1998; 18: 7052-7063.
16. Sanders MA, Basson MD. p130cas but not paxillin is essential for Caco-2 intestinal epithelial cell spreading and migration on collagen IV. J Biol Chem 2005; 280: 23516-23522.
17. Iwasaki T, Nakata A, Mukai M, Shinkai K, Yano H, Sabe H et al. Involvement of phosphorylation of Tyr-31 and Tyr-118 of paxillin in MM1 cancer cell migration. Int J Cancer 2002; 97: 330-335.
18. Nakamura K, Yano H, Uchida H, Hashimoto S, Schaefer E, Sabe H. Tyrosine phosphorylation of paxillin alpha is involved in temporospatial regulation of paxillin-containing focal adhesion formation and F-actin organization in motile cells. J Biol Chem 2000; 275: 27155-27164.
19. Klinghoffer RA, Sachsenmaier C, Cooper JA, Soriano P. Src family kinases are required for integrin but not PDGFR signal transduction. EMBO J 1999; 18: 2459-2471.
20. Schober M, Raghavan S, Nikolova M, Polak L, Pasolli HA, Beggs HE et al. Focal adhesion kinase modulates tension signaling to control actin and focal adhesion dynamics. J Cell Biol 2007; 176: 667-680.
21. Fincham VJ, Frame MC. The catalytic activity of Src is dispensable for translocation to focal adhesions but controls the turnover of these structures during cell motility. EMBO J 1998; 17: 81-92.
22. Yu DH, Qu CK, Henegariu O, Lu X, Feng GS. Protein-tyrosine phosphatase Shp-2 regulates cell spreading, migration, and focal adhesion. J Biol Chem 1998; 273: 21125-21131.
23. Manes S, Mira E, Gomez-Mouton C, Zhao ZJ, Lacalle RA, Martinez AC. Concerted activity of tyrosine phosphatase SHP-2 and focal adhesion kinase in regulation of cell motility. Mol Cell Biol 1999; 19: 3125-3135.
24. Hartman ZR, Schaller MD, Agazie YM. The tyrosine phosphatase SHP2 regulates focal adhesion kinase to promote EGF-induced lamellipodia persistence and cell migration. Mol Cancer Res 2013; 11: 651-664.
25. Minn AJ, Gupta GP, Padua D, Bos P, Nguyen DX, Nuyten D et al. Lung metastasis genes couple breast tumor size and metastatic spread. Proc Natl Acad Sci USA 2007; 104: 6740-6745.
26. Wang W, Wyckoff JB, Frohlich VC, Oleynikov Y, Huttelmaier S, Zavadil J et al. Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling. Cancer Res 2002; 62: 6278-6288.
27. Britschgi A, Andraos R, Brinkhaus H, Klebba I, Romanet V, Muller U et al. JAK2/STAT5 inhibition circumvents resistance to PI3K/mTOR blockade: a rationale for cotargeting these pathways in metastatic breast cancer. Cancer Cell 2012; 22: 796-811.
28. Meijering E, Dzyubachyk O, Smal I. Methods for cell and particle tracking. Methods Enzymol 2012; 504: 183-200.
29. Dey JH, Bianchi F, Voshol J, Bonenfant D, Oakeley EJ, Hynes NE. Targeting fibroblast growth factor receptors blocks PI3K/AKT signaling, induces apoptosis, and impairs mammary tumor outgrowth and metastasis. Cancer Res 2010; 70: 4151-4162.