Roles for GP IIb/IIIa and αvβ3 integrins in MDA-MB-231 cell invasion and shear flow-induced cancer cell mechanotransduction

Cancer Letters

Volumn 344, Issue 1, 2014, Pages 62-73

  Zhao, Fenglong ^a   Li, Li ^a   Guan, Liuyuan ^a   Yang, Hong ^a   Wu, Chunhui ^a   Liu, Yiyao ^a  

^a UNIVERSITY OF ELECTRONIC SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

Integrin; MDA MB 231 cells; NF B; PI3K Akt pathway; Shear stress

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; EPTIFIBATIDE; ETARACIZUMAB; FIBRINOGEN RECEPTOR; GELATINASE A; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; THROMBIN; VASCULOTROPIN; VITRONECTIN RECEPTOR;

ARTICLE; BREAST CARCINOMA; CANCER CELL; CANCER CELL CULTURE; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; INTRACELLULAR SIGNALING; MECHANOTRANSDUCTION; METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SHEAR FLOW; SHEAR STRESS; TUMOR INVASION;

INTEGRIN; MDA-MB-231 CELLS; NF-ΚB; PI3K/AKT PATHWAY; SHEAR STRESS;

BLOTTING, WESTERN; BREAST NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; HEMODYNAMICS; HUMANS; INTEGRIN ALPHAV; MECHANOTRANSDUCTION, CELLULAR; NEOPLASM INVASIVENESS; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRESS, MECHANICAL; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84893676358     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.10.019     Document Type: Article

References (60)

1. Geiger T.R., Peeper D.S. Metastasis mechanisms. Biochim. Biophys. Acta 2009, 1796:293-308.
2. Kannagi R. Carbohydrate-mediated cell adhesion involved in hematogenous metastasis of cancer. Glycoconj. J. 1997, 14:577-584.
3. Jalali S., del Pozo M.A., Chen K., Miao H., Li Y., Schwartz M.A., Shyy J.Y., Chien S. Integrin-mediated mechanotransduction requires its dynamic interaction with specific extracellular matrix (ECM) ligands. Proc. Natl. Acad. Sci. USA 2001, 98:1042-1046.
4. Balasubramanian L., Lo C.M., Sham J.S., Yip K.P. Remanent cell traction force in renal vascular smooth muscle cells induced by integrin-mediated mechanotransduction. Am. J. Physiol. Cell Physiol. 2013, 304:C382-C391.
5. Alenghat F.J., Ingber D.E. Mechanotransduction: all signals point to cytoskeleton, matrix, and integrins. Sci. STKE 2002, pe6.
6. Liu Y., Bajjuri K.M., Liu C., Sinha S.C. Targeting cell surface alpha(v)beta(3) integrin increases therapeutic efficacies of a legumain protease-activated auristatin prodrug. Mol. Pharm. 2012, 9:168-175.
7. Filardo E.J., Brooks P.C., Deming S.L., Damsky C., Cheresh D.A. Requirement of the NPXY motif in the integrin beta(3) subunit cytoplasmic tail for melanoma cell migration in vitro and in vivo. J. Cell Biol. 1995, 130:441-450.
8. Hsu M.Y., Shih D.T., Meier F.E., Van Belle P., Hsu J.Y., Elder D.E., Buck C.A., Herlyn M. Adenoviral gene transfer of beta(3) integrin subunit induces conversion from radial to vertical growth phase in primary human melanoma. Am. J. Pathol. 1998, 153:1435-1442.
9. Felding-Habermann B., O'Toole T.E., Smith J.W., Fransvea E., Ruggeri Z.M., Ginsberg M.H., Hughes P.E., Pampori N., Shattil S.J., Saven A., Mueller B.M. Integrin activation controls metastasis in human breast cancer. Proc. Natl. Acad. Sci. USA 2001, 98:1853-1858.
10. Manes T., Zheng D.Q., Tognin S., Woodard A.S., Marchisio P.C., Languino L.R. Alpha(v)beta(3) integrin expression up-regulates cdc2, which modulates cell migration. J. Cell Biol. 2003, 161:817-826.
11. Sahai E. Illuminating the metastatic process. Nat. Rev. Cancer 2007, 7:737-749.
12. Lonsdorf A.S., Kramer B.F., Fahrleitner M., Schonberger T., Gnerlich S., Ring S., Gehring S., Schneider S.W., Kruhlak M.J., Meuth S.G., Nieswandt B., Gawaz M., Enk A.H., Langer H.F. Engagement of alpha(IIb)beta(3) (GPIIb/IIIa) with alphanubeta3 integrin mediates interaction of melanoma cells with platelets: a connection to hematogenous metastasis. J. Biol. Chem. 2012, 287:2168-2178.
13. Liu Y., Zhao F., Gu W., Yang H., Meng Q., Zhang Y., Yang H., Duan Q. The roles of platelet GPIIb/IIIa and alpha(v)beta(3) integrins during HeLa cells adhesion, migration, and invasion to monolayer endothelium under static and dynamic shear flow. J. Biomed. Biotechnol. 2009, 2009:829243.
14. Gay L.J., Felding-Habermann B. Contribution of platelets to tumour metastasis. Nat. Rev. Cancer 2011, 11:123-134.
15. Wiesner T., Bugl S., Mayer F., Hartmann J.T., Kopp H.G. Differential changes in platelet VEGF, Tsp, CXCL12, and CXCL4 in patients with metastatic cancer. Clin. Exp. Metastasis 2010, 27:141-149.
16. Im J.H., Fu W., Wang H., Bhatia S.K., Hammer D.A., Kowalska M.A., Muschel R.J. Coagulation facilitates tumor cell spreading in the pulmonary vasculature during early metastatic colony formation. Cancer Res. 2004, 64:8613-8619.
17. Rivera J., Lozano M.L., Navarro-Nunez L., Vicente V. Platelet receptors and signaling in the dynamics of thrombus formation. Haematologica 2009, 94:700-711.
18. Jain S., Harris J., Ware J. Platelets: linking hemostasis and cancer. Arterioscler. Thromb. Vasc. Biol. 2010, 30:2362-2367.
19. Miao H., Yuan S., Wang Y., Tsygankov A., Chien S. Role of Cbl in shear-activation of PI3-kinase and JNK in endothelial cells. Biochem. Biophys. Res. Commun. 2002, 292:892-899.
20. Resendiz J.C., Feng S., Ji G., Francis K.A., Berndt M.C., Kroll M.H. Purinergic P2Y12 receptor blockade inhibits shear-induced platelet phosphatidylinositol 3-kinase activation. Mol. Pharmacol. 2003, 63:639-645.
21. Pavalko F.M., Gerard R.L., Ponik S.M., Gallagher P.J., Jin Y., Norvell S.M. Fluid shear stress inhibits TNF-alpha-induced apoptosis in osteoblasts: a role for fluid shear stress-induced activation of PI3-kinase and inhibition of caspase-3. J. Cell Physiol. 2003, 194:194-205.
22. Thamilselvan V., Craig D.H., Basson M.D. FAK association with multiple signal proteins mediates pressure-induced colon cancer cell adhesion via a Src-dependent PI3K/Akt pathway. FASEB J. 2007, 21:1730-1741.
23. Tsubaki M., Satou T., Itoh T., Imano M., Ogaki M., Yanae M., Nishida S. Reduction of metastasis, cell invasion, and adhesion in mouse osteosarcoma by YM529/ONO-5920-induced blockade of the Ras/MEK/ERK and Ras/PI3K/Akt pathway. Toxicol. Appl. Pharmacol. 2012, 259:402-410.
24. Yang H., Liu Z.H., Liu Y.Y., Lou C.C., Ren Z.L., Miyoshi H. Vascular gene transfer and drug delivery in vitro using low-frequency ultrasound and microbubbles. Acta Pharmacol. Sin. 2010, 31:515-522.
25. McCarty O.J., Mousa S.A., Bray P.F., Konstantopoulos K. Immobilized platelets support human colon carcinoma cell tethering, rolling, and firm adhesion under dynamic flow conditions. Blood 2000, 96:1789-1797.
26. Meng G., Liu Y., Lou C., Yang H. Emodin suppresses lipopolysaccharide-induced pro-inflammatory responses and NF-kappaB activation by disrupting lipid rafts in CD14-negative endothelial cells. Br. J. Pharmacol. 2010, 161:1628-1644.
27. Veiseh M., Gabikian P., Bahrami S.B., Veiseh O., Zhang M., Hackman R.C., Ravanpay A.C., Stroud M.R., Kusuma Y., Hansen S.J., Kwok D., Munoz N.M., Sze R.W., Grady W.M., Greenberg N.M., Ellenbogen R.G., Olson J.M. Tumor paint: a chlorotoxin:Cy5.5 bioconjugate for intraoperative visualization of cancer foci. Cancer Res. 2007, 67:6882-6888.
28. Brooks P.C., Stromblad S., Sanders L.C., von Schalscha T.L., Aimes R.T., Stetler-Stevenson W.G., Quigley J.P., Cheresh D.A. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha(v)beta(3). Cell 1996, 85:683-693.
29. Majumder M., Tutunea-Fatan E., Xin X., Rodriguez-Torres M., Torres-Garcia J., Wiebe R., Timoshenko A.V., Bhattacharjee R.N., Chambers A.F., Lala P.K. Co-expression of alpha(9)beta(1) integrin and VEGF-D confers lymphatic metastatic ability to a human breast cancer cell line MDA-MB-468LN. PLoS One 2012, 7:e35094.
30. Lee D.Y., Li Y.S., Chang S.F., Zhou J., Ho H.M., Chiu J.J., Chien S. Oscillatory flow-induced proliferation of osteoblast-like cells is mediated by alpha(v)beta(3) and beta(1) integrins through synergistic interactions of focal adhesion kinase and Shc with phosphatidylinositol 3-kinase and the Akt/mTOR/p70S6K pathway. J. Biol. Chem. 2010, 285:30-42.
31. Wang Y., Miao H., Li S., Chen K.D., Li Y.S., Yuan S., Shyy J.Y., Chien S. Interplay between integrins and FLK-1 in shear stress-induced signaling. Am. J. Physiol. Cell Physiol. 2002, 283:C1540-1547.
32. Liang S., Fu C., Wagner D., Guo H., Zhan D., Dong C., Long M. Two-dimensional kinetics of beta(2)-integrin and ICAM-1 bindings between neutrophils and melanoma cells in a shear flow. Am. J. Physiol. Cell Physiol. 2008, 294:C743-753.
33. Liao S.J., Zhou Y.H., Yuan Y., Li D., Wu F.H., Wang Q., Zhu J.H., Yan B., Wei J.J., Zhang G.M., Feng Z.H. Triggering of Toll-like receptor 4 on metastatic breast cancer cells promotes alpha(v)beta(3)-mediated adhesion and invasive migration. Breast Cancer Res. Treat. 2012, 133:853-863.
34. Hsu R.Y., Chan C.H., Spicer J.D., Rousseau M.C., Giannias B., Rousseau S., Ferri L.E. LPS-induced TLR4 signaling in human colorectal cancer cells increases beta(1) integrin-mediated cell adhesion and liver metastasis. Cancer Res. 2011, 71:1989-1998.
35. Jadhav S., Bochner B.S., Konstantopoulos K. Hydrodynamic shear regulates the kinetics and receptor specificity of polymorphonuclear leukocyte-colon carcinoma cell adhesive interactions. J. Immunol. 2001, 167:5986-5993.
36. Burdick M.M., McCaffery J.M., Kim Y.S., Bochner B.S., Konstantopoulos K. Colon carcinoma cell glycolipids, integrins, and other glycoproteins mediate adhesion to HUVECs under flow. Am. J. Physiol. Cell Physiol. 2003, 284:C977-987.
37. Zhang C., Liu Y., Gao Y., Shen J., Zheng S., Wei M., Zeng X. Modified heparins inhibit integrin alpha(IIb)beta(3) mediated adhesion of melanoma cells to platelets in vitro and in vivo. Int. J. Cancer 2009, 125:2058-2065.
38. Pelletier A.J., Kunicki T., Ruggeri Z.M., Quaranta V. The activation state of the integrin alpha(IIb)beta(3) affects outside-in signals leading to cell spreading and focal adhesion kinase phosphorylation. J. Biol. Chem. 1995, 270:18133-18140.
39. Tasneem S., Adam F., Minullina I., Pawlikowska M., Hui S.K., Zheng S., Miller J.L., Hayward C.P. Platelet adhesion to multimerin 1 in vitro: influences of platelet membrane receptors, von Willebrand factor and shear. J. Thromb. Haemost. 2009, 7:685-692.
40. Ko H.M., Kang J.H., Choi J.H., Park S.J., Bai S., Im S.Y. Platelet-activating factor induces matrix metalloproteinase-9 expression through Ca(2+)- or PI3K-dependent signaling pathway in a human vascular endothelial cell line. FEBS Lett. 2005, 579:6451-6458.
41. Kunita A., Kashima T.G., Morishita Y., Fukayama M., Kato Y., Tsuruo T., Fujita N. The platelet aggregation-inducing factor aggrus/podoplanin promotes pulmonary metastasis. Am. J. Pathol. 2007, 170:1337-1347.
42. Nieswandt B., Hafner M., Echtenacher B., Mannel D.N. Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res. 1999, 59:1295-1300.
43. Palumbo J.S., Talmage K.E., Massari J.V., La Jeunesse C.M., Flick M.J., Kombrinck K.W., Jirouskova M., Degen J.L. Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell-mediated elimination of tumor cells. Blood 2005, 105:178-185.
44. Tomita M., Shimizu T., Hara M., Ayabe T., Onitsuka T. Prognostic impact of thrombocytosis in resectable non-small cell lung cancer. Interact. Cardiovasc. Thorac. Surg. 2008, 7:613-615.
45. Amirkhosravi A., Mousa S.A., Amaya M., Blaydes S., Desai H., Meyer T., Francis J.L. Inhibition of tumor cell-induced platelet aggregation and lung metastasis by the oral GPIIb/IIIa antagonist XV454. Thromb. Haemost. 2003, 90:549-554.
46. Puerschel W.C., Gawaz M., Worret W.I., Ring J. Immunoreactivity of glycoprotein IIb is present in metastasized but not in non-metastasized primary malignant melanoma. Br. J. Dermatol. 1996, 135:883-887.
47. McCarty O.J., Jadhav S., Burdick M.M., Bell W.R., Konstantopoulos K. Fluid shear regulates the kinetics and molecular mechanisms of activation-dependent platelet binding to colon carcinoma cells. Biophys. J. 2002, 83:836-848.
48. Camerer E., Qazi A.A., Duong D.N., Cornelissen I., Advincula R., Coughlin S.R. Platelets, protease-activated receptors, and fibrinogen in hematogenous metastasis. Blood 2004, 104:397-401.
49. Langer H.F., Gawaz M. Platelet-vessel wall interactions in atherosclerotic disease. Thromb. Haemost. 2008, 99:480-486.
50. Matsuoka H., Tsubaki M., Yamazoe Y., Ogaki M., Satou T., Itoh T., Kusunoki T., Nishida S. Tamoxifen inhibits tumor cell invasion and metastasis in mouse melanoma through suppression of PKC/MEK/ERK and PKC/PI3K/Akt pathways. Exp. Cell Res. 2009, 315:2022-2032.
51. Stetler-Stevenson W.G. Type IV collagenases in tumor invasion and metastasis. Cancer Metastasis Rev. 1990, 9:289-303.
52. Maity G., Choudhury P.R., Sen T., Ganguly K.K., Sil H., Chatterjee A. Culture of human breast cancer cell line (MDA-MB-231) on fibronectin-coated surface induces pro-matrix metalloproteinase-9 expression and activity. Tumour Biol. 2011, 32:129-138.
53. Tan T.W., Yang W.H., Lin Y.T., Hsu S.F., Li T.M., Kao S.T., Chen W.C., Fong Y.C., Tang C.H. Cyr61 increases migration and MMP-13 expression via alpha(v)beta(3) integrin, FAK, ERK and AP-1-dependent pathway in human chondrosarcoma cells. Carcinogenesis 2009, 30:258-268.
54. Wang S., Basson M.D. Akt directly regulates focal adhesion kinase through association and serine phosphorylation: implication for pressure-induced colon cancer metastasis. Am. J. Physiol. Cell Physiol. 2011, 300:C657-670.
55. Takagi J., Petre B.M., Walz T., Springer T.A. Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell 2002, 110:599-611.
56. Craig D.H., Gayer C.P., Schaubert K.L., Wei Y., Li J., Laouar Y., Basson M.D. Increased extracellular pressure enhances cancer cell integrin-binding affinity through phosphorylation of beta(1)-integrin at threonine 788/789. Am. J. Physiol. Cell Physiol. 2009, 296:C193-204.
57. Huang Q., Shen H.M., Shui G., Wenk M.R., Ong C.N. Emodin inhibits tumor cell adhesion through disruption of the membrane lipid raft-associated integrin signaling pathway. Cancer Res. 2006, 66:5807-5815.
58. Leitinger B., Hogg N. The involvement of lipid rafts in the regulation of integrin function. J. Cell. Sci. 2002, 115:963-972.
59. Wei Y.Y., Chen Y.J., Hsiao Y.C., Huang Y.C., Lai T.H., Tang C.H. Osteoblasts-derived TGF-beta(1) enhance motility and integrin upregulation through Akt, ERK, and NF-kappaB-dependent pathway in human breast cancer cells. Mol. Carcinog. 2008, 47:526-537.
60. Haddad O., Chotard-Ghodsnia R., Verdier C., Duperray A. Tumor cell/endothelial cell tight contact upregulates endothelial adhesion molecule expression mediated by NF-kappaB: differential role of the shear stress. Exp. Cell Res. 2010, 316:615-626.