CD44-mediated activation of α5β1-integrin, cortactin and paxillin signaling underpins adhesion of basal-like breast cancer cells to endothelium and Fibronectin-enriched matrices

Oncotarget

Volumn 6, Issue 34, 2015, Pages 36762-36773

  McFarlane, Suzanne ^a   McFarlane, Cheryl ^a   Montgomery, Nicola ^a   Hill, Ashleigh ^a   Waugh, David J J ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Breast cancer; CD44; Fibronectin; Integrin; Vascular endothelium

Indexed keywords

BETA1 INTEGRIN; CORTACTIN; FIBRONECTIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HERMES ANTIGEN; PAXILLIN; VERY LATE ACTIVATION ANTIGEN 5; CD44 PROTEIN, HUMAN;

ARTICLE; BREAST CANCER; CANCER CELL; CELL ADHESION; CONTROLLED STUDY; CYTOSKELETON; ENDOTHELIUM; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; BIOSYNTHESIS; BREAST TUMOR; FEMALE; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANTIGENS, CD44; BREAST NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; CORTACTIN; FEMALE; FIBRONECTINS; HUMANS; INTEGRIN ALPHA5BETA1; PAXILLIN; SIGNAL TRANSDUCTION;

EID: 84946887258     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5461     Document Type: Article

References (30)

1. Mastro AM, Gay CV, Welch DR. The skeleton as a unique environment for breast cancer cells. Clin. Exp. Metastasis. 2003; 20:275-284.
2. Orr FW, Wang HH, Lafrenie RM, Scherbarth S, Nance DM. Interactions between cancer cells and the endothelium in metastasis. J. Pathol. 2000; 190:310-329.
3. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA. 2003; 100:3983-3988.
4. Wicha MS. Cancer stem cells and metastasis: lethal seeds. Clin Cancer Res. 2006; 12:5606-5607.
5. Klingbeil P, Natrajan R, Everitt G, Vatcheva R, Marchio C, Palacios J, Buerger H, Reis-Filho JS, Isacke CM. CD44 is overexpressed in basal-like breast cancers but is not a driver of 11p13 amplification. Breast Cancer Res Treat. 2010; 120:95-109.
6. Montgomery N, Hill A, McFarlane S, Neisen J, O'Grady A, Conlon S, Jirstrom K, Kay EW, Waugh DJ. CD44 enhances invasion of basal-like breast cancer cells by upregulating serine protease and collagen-degrading enzymatic expression and activity. Breast Cancer Res. 2012; 14:R84.
7. McFarlane S, Coulter JA, Tibbits P, O'Grady A, McFarlane C, Montgomery N, Hill A, McCarthy HO, Young LS, Kay EW, Isacke CM, Waugh DJJ. CD44 increases the efficiency of distant metastasis of breast cancer. Oncotarget. 2015; 6:11465-11476.
8. Balic M, Lin H, Young L, Hawes D, Giuliano A, McNamara G, Datar RH, Cote RJ. Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype. Clin. Cancer Res. 2006; 12:5615-5621.
9. Abraham BK, Fritz P, McClellan M, Hauptvogel P, Athelogou M, Brauch H. Prevalence of CD44+/CD24-/low cells in breast cancer may not be associated with clinical outcome but may favor distant metastasis. Clin. Cancer Res. 2005; 11:1154-1159.
10. Draffin JE, McFarlane S, Hill A, Johnston PG, Waugh DJ. CD44 potentiates the adherence of metastatic prostate and breast cancer cells to bone marrow endothelial cells. Cancer Res. 2004; 64:5702-5711.
11. Hill A, McFarlane S, Mulligan K, Gillespie H, Draffin JE, Trimble A, Ouhtit A, Johnston PG, Harkin DP, McCormick D, Waugh DJ. Cortactin underpins CD44-promoted invasion and adhesion of breast cancer cells to bone marrow endothelial cells. Oncogene. 2006; 25:6079-6091.
12. Nandi A, Estess P, Siegelman MH. Hyaluronan anchoring and regulation on the surface of vascular endothelial cells is mediated through the functionally active form of CD44. J. Biol. Chem. 2000; 275:14939-14948.
13. Siegelman MH, Stanescu D, Estess P. The CD44-initiated pathway of T-cell extravasation uses VLA-4 but not LFA-1 for firm adhesion. J. Clin. Invest. 2000; 105:683-691.
14. Nandi A, Estess P, Siegelman M. Bimolecular complex between rolling and firm adhesion receptors required for cell arrest; CD44 association with VLA-4 in T cell extravasation. Immunity. 2004; 20:455-465.
15. Fujisaki T1, Tanaka Y, Fujii K, Mine S, Saito K, Yamada S, Yamashita U, Irimura T. Eto S CD44 stimulation induces integrin-mediated adhesion of colorectal cancer cell lines to endothelial cells by up-regulation of integrins and c-Met and activation of integrins. Cancer Res. 1999; 59:4427-4434.
16. Luque A, Gomez M, Puzon W, Takada Y, Sanchez-Madrid F, Cabanas C. Activated conformations of very late activation integrins detected by a group of antibodies (HUTS) specific for a novel regulatory region (355-425) of the common beta 1 chain. J. Biol. Chem. 1996; 271:11067-11075.
17. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, Zhu Z, Hicklin D, Wu Y, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 2005; 438:820-827.
18. Yu S, Cai X, Wu C, Wu L, Wang Y, Liu Y, Yu Z, Qin S, Ma F, Thiery JP, Chen L. Adhesion glycoprotein CD44 functions as an upstream regulator of a network connecting ERK, AKT, and Hippo-YAP pathways in cancer progression. Oncotarget. 2015.
19. Weng QP, Andrabi K, Kozlowski MT, Grove JR, Avruch J. Multiple independent inputs are required for activation of the p70 S6 kinase. Mol Cell Biol. 1995; 15:2333-40.
20. Weng QP, Kozlowski M, Belham C, Zhang A, Comb MJ, Avruch J. Regulation of the p70 S6 kinase by phosphorylation in vivo. Analysis using site-specific anti-phosphopeptide antibodies. J Biol Chem. 1998; 273:16621-9.
21. Lee JL, Wang MJ, Sudhir PR, Chen JY. CD44 engagement promotes matrix-derived survival through the CD44-SRC-integrin axis in lipid rafts. Mol. Cell. Biol. 2008; 28:5710-5723.
22. Iczkowski KA, Omara-Opyene AL, Shah GV. The predominant CD44 splice variant in prostate cancer binds fibronectin, and calcitonin stimulates its expression. Anticancer Res. 2006; 26:2863-2872.
23. Wang HS, Hung Y, Su CH, Peng ST, Guo YJ, Lai MC, Liu CY, Hsu JW. CD44 cross-linking induces integrin-mediated adhesion and transendothelial migration in breast cancer cell line by up-regulation of LFA-1 (alpha L beta2) and VLA-4 (alpha4beta1). Exp. Cell Res. 2005; 304:116-126.
24. Bae YK, Kim A, Kim YK, Choi JE, Kang SH, Lee SJ. Fibronectin expression in carcinoma cells correlates with tumor aggressiveness and poor clinical outcome in patients with invasive breast cancer. Hum Pathol. 2013; 44:2028-2037.
25. Li Y, Tondravi M, Liu J, Smith E, Haudenschild CC, Kaczmarek M, Zhan X. Cortactin potentiates bone metastasis of breast cancer cells. Cancer Res. 2001; 61:6906-6911.
26. Myoui A, Nishimura R, Williams PJ, Hiraga T, Tamura D, Michigami T, Mundy GR, Yoneda T. C-SRC tyrosine kinase activity is associated with tumor colonization in bone and lung in an animal model of human breast cancer metastasis. Cancer Res. 2003; 63:5028-5033.
27. Zhang XH, Wang Q, Gerald W, Hudis CA, Norton L, Smid M, Foekens JA, Massague J. Latent bone metastasis in breast cancer tied to Src-dependent survival signals. Cancer Cell. 2009; 16:67-78.
28. Ouhtit A, Abd Elmageed ZY, Abdraboh ME, Lioe TF, Raj MH. In vivo evidence for the role of CD44s in promoting breast cancer metastasis to the liver. Am. J. Pathol. 2007; 171:2033-2039.
29. Dan T, Hewitt SM, Ohri N, Ly D, Soule BP, Smith SL, Matsuda K, Council C, Shankavaram U, Lippman ME, Mitchell JB, Camphausen K, Simone NL. CD44 is prognostic for overall survival in the NCI randomized trial on breast conservation with 25-year follow up. Breast Cancer Res Treat. 2014; 143:11-18.
30. Yoneda T, Williams PJ, Hiraga T, Niewolna M, Nishimura R. A bone-seeking clone exhibits different biological properties from the MDA-MB-231 parental human breast cancer cells and a brain-seeking clone in vivo and in vitro. J. Bone Miner. Res. 2001; 16:1486-1495.