BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Crosstalk between integrin and receptor tyrosine kinase signaling in breast carcinoma progression

  • Soung, Young-Hwa (Department of Biochemistry and Molecular Biology, Louisiana State University Health Sciences Center) ;
  • Clifford, John L. (Department of Biochemistry and Molecular Biology, Louisiana State University Health Sciences Center) ;
  • Chung, Jun (Department of Biochemistry and Molecular Biology, Louisiana State University Health Sciences Center)
  • Received : 2010.05.01
  • Published : 2010.05.31
Download PDF
⟨ Previous Next ⟩

Abstract

This review explored the mechanism of breast carcinoma progression by focusing on integrins and receptor tyrosine kinases (or growth factor receptors). While the primary role of integrins was previously thought to be solely as mediators of adhesive interactions between cells and extracellular matrices, it is now believed that integrins also regulate signaling pathways that control cancer cell growth, survival, and invasion. A large body of evidence suggests that the cooperation between integrin and receptor tyrosine kinase signaling regulates certain signaling functions that are important for cancer progression. Recent developments on the crosstalk between integrins and receptor tyrosine kinases, and its implication in mammary tumor progression, are discussed.

Keywords

References

  1. Hanahan, D. and Weinberg, R. A. (2000) The hallmarks of cancer. Cell 100, 57-70. https://doi.org/10.1016/S0092-8674(00)81683-9
  2. Larsen, M., Artym, V. V., Green, J. A. and Yamada, K. M. (2006) The matrix reorganized: extracellular matrix remodeling and integrin signaling. Curr. Opin. Cell Biol. 18, 463-471. https://doi.org/10.1016/j.ceb.2006.08.009
  3. Giancotti, F. G. and Ruoslahti, E. (1999) Integrin signaling. Science 285, 1028-1032. https://doi.org/10.1126/science.285.5430.1028
  4. Perou, C. M., Sorlie, T., Eisen, M. B., van de Rijn, M., Jeffrey, S. S., Rees, C. A., Pollack, J. R., Ross, D. T., Johnsen, H., Akslen, L. A., Fluge, O., Pergamenschikov, A., Williams, C., Zhu, S. X., Lonning, P. E., Borresen-Dale, A. L., Brown, P. O. and Botstein, D. (2000) Molecular portraits of human breast tumours. Nature 406, 747-752. https://doi.org/10.1038/35021093
  5. Nielsen, T. O., Hsu, F. D., Jensen, K., Cheang, M., Karaca, G., Hu, Z., Hernandez-Boussard, T., Livasy, C., Cowan, D., Dressler, L., Akslen, L. A., Ragaz, J., Gown, A. M., Gilks, C. B., van de Rijn, M. and Perou, C. M. (2004) Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin. Cancer Res. 10, 5367-5374. https://doi.org/10.1158/1078-0432.CCR-04-0220
  6. Byers, S., Park, M., Sommers, C. and Seslar, S. (1994) Breast carcinoma: a collective disorder. Breast Cancer Res. Treat. 31, 203-215. https://doi.org/10.1007/BF00666154
  7. Shaw, L. M. (1999) Integrin function in breast carcinoma progression. J. Mammary. Gland. Biol. Neoplasia. 4, 367-376. https://doi.org/10.1023/A:1018766317055
  8. Aumailley, M., Pesch, M., Tunggal, L., Gaill, F. and Fassler, R. (2000) Altered synthesis of laminin 1 and absence of basement membrane component deposition in (beta)1 integrin-deficient embryoid bodies. J. Cell Sci. 113 Pt 2, 259-268.
  9. Plow, E. F., Haas, T. A., Zhang, L., Loftus, J. and Smith, J. W. (2000) Ligand binding to integrins. J. Biol. Chem. 275, 21785-21788. https://doi.org/10.1074/jbc.R000003200
  10. van der Flier, A. and Sonnenberg, A. (2001) Function and interactions of integrins. Cell Tissue. Res. 305, 285-298. https://doi.org/10.1007/s004410100417
  11. Aplin, A. E., Howe, A. K. and Juliano, R. L. (1999) Cell adhesion molecules, signal transduction and cell growth. Curr. Opin. Cell Biol. 11, 737-744. https://doi.org/10.1016/S0955-0674(99)00045-9
  12. Luo, B. H., Carman, C. V. and Springer, T. A. (2007) Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25, 619-647. https://doi.org/10.1146/annurev.immunol.25.022106.141618
  13. Bryan, B. A. and D'Amore, P. A. (2007) What tangled webs they weave: Rho-GTPase control of angiogenesis. Cell Mol. Life Sci. 64, 2053-2065. https://doi.org/10.1007/s00018-007-7008-z
  14. Kanda, S., Kanetake, H. and Miyata, Y. (2007) Role of Src in angiopoietin 1-induced capillary morphogenesis of endothelial cells: effect of chronic hypoxia on Src inhibition by PP2. Cell Signal 19, 472-480. https://doi.org/10.1016/j.cellsig.2006.07.014
  15. Ridley, A. (2000) Rho GTPases. Integrating integrin signaling. J. Cell Biol. 150, F107-109. https://doi.org/10.1083/jcb.150.4.F107
  16. Schwartz, M. A. and Shattil, S. J. (2000) Signaling networks linking integrins and rho family GTPases. Trends Biochem. Sci. 25, 388-391. https://doi.org/10.1016/S0968-0004(00)01605-4
  17. Bertotti, A., Comoglio, P. M. and Trusolino, L. (2006) Beta4 integrin activates a Shp2-Src signaling pathway that sustains HGF-induced anchorage-independent growth. J. Cell Biol. 175, 993-1003. https://doi.org/10.1083/jcb.200605114
  18. Klemke, R. L., Leng, J., Molander, R., Brooks, P. C., Vuori, K. and Cheresh, D. A. (1998) CAS/Crk coupling serves as a "molecular switch" for induction of cell migration. J. Cell Biol. 140, 961-972. https://doi.org/10.1083/jcb.140.4.961
  19. Collins, L. R., Ricketts, W. A., Yeh, L. and Cheresh, D. (1999) Bifurcation of cell migratory and proliferative signaling by the adaptor protein Shc. J. Cell Biol. 147, 1561-1568. https://doi.org/10.1083/jcb.147.7.1561
  20. Mariotti, A., Kedeshian, P. A., Dans, M., Curatola, A. M., Gagnoux-Palacios, L. and Giancotti, F. G. (2001) EGF-R signaling through Fyn kinase disrupts the function of integrin alpha6beta4 at hemidesmosomes: role in epithelial cell migration and carcinoma invasion. J. Cell Biol. 155, 447-458. https://doi.org/10.1083/jcb.200105017
  21. Moro, L., Dolce, L., Cabodi, S., Bergatto, E., Boeri Erba, E., Smeriglio, M., Turco, E., Retta, S. F., Giuffrida, M. G., Venturino, M., Godovac-Zimmermann, J., Conti, A., Schaefer, E., Beguinot, L., Tacchetti, C., Gaggini, P., Silengo, L., Tarone, G. and Defilippi, P. (2002) Integrin-induced epidermal growth factor (EGF) receptor activation requires c-Src and p130Cas and leads to phosphorylation of specific EGF receptor tyrosines. J. Biol. Chem. 277, 9405-9414. https://doi.org/10.1074/jbc.M109101200
  22. Mahabeleshwar, G. H., Feng, W., Reddy, K., Plow, E. F. and Byzova, T. V. (2007) Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis. Circ. Res. 101, 570-580. https://doi.org/10.1161/CIRCRESAHA.107.155655
  23. Somanath, P. R., Kandel, E. S., Hay, N. and Byzova, T. V. (2007) Akt1 signaling regulates integrin activation, matrix recognition, and fibronectin assembly. J. Biol. Chem. 282, 22964-22976. https://doi.org/10.1074/jbc.M700241200
  24. Schneller, M., Vuori, K. and Ruoslahti, E. (1997) Alphavbeta3 integrin associates with activated insulin and PDGF beta receptors and potentiates the biological activity of PDGF. EMBO J. 16, 5600-5607. https://doi.org/10.1093/emboj/16.18.5600
  25. Borges, E., Jan, Y. and Ruoslahti, E. (2000) Platelet-derived growth factor receptor beta and vascular endothelial growth factor receptor 2 bind to the beta 3 integrin through its extracellular domain. J. Biol. Chem. 275, 39867-39873. https://doi.org/10.1074/jbc.M007040200
  26. Soldi, R., Mitola, S., Strasly, M., Defilippi, P., Tarone, G. and Bussolino, F. (1999) Role of alphavbeta3 integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J. 18, 882-892. https://doi.org/10.1093/emboj/18.4.882
  27. Falcioni, R., Antonini, A., Nistico, P., Di Stefano, S., Crescenzi, M., Natali, P. G. and Sacchi, A. (1997) Alpha 6 beta 4 and alpha 6 beta 1 integrins associate with ErbB-2 in human carcinoma cell lines. Exp. Cell Res. 236, 76-85. https://doi.org/10.1006/excr.1997.3695
  28. Trusolino, L., Bertotti, A. and Comoglio, P. M. (2001) A signaling adapter function for alpha6beta4 integrin in the control of HGF-dependent invasive growth. Cell 107, 643-654. https://doi.org/10.1016/S0092-8674(01)00567-0
  29. Santoro, M. M., Gaudino, G. and Marchisio, P. C. (2003) The MSP receptor regulates alpha6beta4 and alpha3beta1 integrins via 14-3-3 proteins in keratinocyte migration. Dev. Cell 5, 257-271. https://doi.org/10.1016/S1534-5807(03)00201-6
  30. Lipscomb, E. A. and Mercurio, A. M. (2005) Mobilization and activation of a signaling competent alpha6beta4integrin underlies its contribution to carcinoma progression. Cancer Metastasis Rev. 24, 413-423. https://doi.org/10.1007/s10555-005-5133-4
  31. Maile, L. A. and Clemmons, D. R. (2002) The alphaVbeta3 integrin regulates insulin-like growth factor I (IGF-I) receptor phosphorylation by altering the rate of recruitment of the Src-homology 2-containing phosphotyrosine phosphatase-2 to the activated IGF-I receptor. Endocrinology 143, 4259-4264. https://doi.org/10.1210/en.2002-220395
  32. Baron, W., Shattil, S. J. and ffrench-Constant, C. (2002) The oligodendrocyte precursor mitogen PDGF stimulates proliferation by activation of alpha(v)beta3 integrins. EMBO J. 21, 1957-1966. https://doi.org/10.1093/emboj/21.8.1957
  33. Rabinovitz, I., Toker, A. and Mercurio, A. M. (1999) Protein kinase C-dependent mobilization of the alpha 6beta4 integrin from hemidesmosomes and its association with actin-rich cell protrusions drive the chemotactic migration of carcinoma cells. J. Cell Biol. 146, 1147-1160. https://doi.org/10.1083/jcb.146.5.1147
  34. Rabinovitz, I., Tsomo, L. and Mercurio, A. M. (2004) Protein kinase C-alpha phosphorylation of specific serines in the connecting segment of the beta 4 integrin regulates the dynamics of type II hemidesmosomes. Mol. Cell Biol. 24, 4351-4360. https://doi.org/10.1128/MCB.24.10.4351-4360.2004
  35. Germain, E. C., Santos, T. M. and Rabinovitz, I. (2009) Phosphorylation of a novel site on the {beta}4 integrin at the trailing edge of migrating cells promotes hemidesmosome disassembly. Mol. Biol. Cell 20, 56-67. https://doi.org/10.1091/mbc.E08-06-0646
  36. Trusolino, L. and Comoglio, P. M. (2002) Scatter-factor and semaphorin receptors: cell signalling for invasive growth. Nat. Rev. Cancer 2, 289-300. https://doi.org/10.1038/nrc779
  37. Mercurio, A. M., Bachelder, R. E., Rabinovitz, I., O'Connor, K. L., Tani, T. and Shaw, L. M. (2001) The metastatic odyssey: the integrin connection. Surg. Oncol. Clin. N. Am. 10, 313-328.
  38. Nguyen, B. P., Ryan, M. C., Gil, S. G. and Carter, W. G. (2000) Deposition of laminin 5 in epidermal wounds regulates integrin signaling and adhesion. Curr. Opin. Cell Biol. 12, 554-562. https://doi.org/10.1016/S0955-0674(00)00131-9
  39. Mercurio, A. M., Bachelder, R. E., Bates, R. C. and Chung, J. (2004) Autocrine signaling in carcinoma: VEGF and the alpha6beta4 integrin. Semin. Cancer Biol. 14, 115-122. https://doi.org/10.1016/j.semcancer.2003.09.016
  40. Chung, J. and Mercurio, A. M. (2004) Contributions of the alpha6 integrins to breast carcinoma survival and progression. Mol. Cells 17, 203-209.
  41. Mercurio, A. M. and Rabinovitz, I. (2001) Towards a mechanistic understanding of tumor invasion--lessons from the alpha6beta 4 integrin. Semin. Cancer Biol. 11, 129-141. https://doi.org/10.1006/scbi.2000.0364
  42. Chung, J., Bachelder, R. E., Lipscomb, E. A., Shaw, L. M. and Mercurio, A. M. (2002) Integrin (alpha 6 beta 4) regulation of eIF-4E activity and VEGF translation: a survival mechanism for carcinoma cells. J. Cell Biol. 158, 165-174. https://doi.org/10.1083/jcb.200112015
  43. Mercurio, A. M., Rabinovitz, I. and Shaw, L. M. (2001) The alpha 6 beta 4 integrin and epithelial cell migration. Curr. Opin. Cell Biol. 13, 541-545. https://doi.org/10.1016/S0955-0674(00)00249-0
  44. Head, B. P., Patel, H. H., Roth, D. M., Murray, F., Swaney, J. S., Niesman, I. R., Farquhar, M. G. and Insel, P. A. (2006) Microtubules and actin microfilaments regulate lipid raft/caveolae localization of adenylyl cyclase signaling components. J. Biol. Chem. 281, 26391-26399. https://doi.org/10.1074/jbc.M602577200
  45. de Laurentiis, A., Donovan, L. and Arcaro, A. (2007) Lipid rafts and caveolae in signaling by growth factor receptors. Open Biochem. J. 1, 12-32. https://doi.org/10.2174/1874091X00701010012
  46. Guo, W., Pylayeva, Y., Pepe, A., Yoshioka, T., Muller, W. J., Inghirami, G. and Giancotti, F. G. (2006) Beta 4 integrin amplifies ErbB2 signaling to promote mammary tumorigenesis. Cell 126, 489-502. https://doi.org/10.1016/j.cell.2006.05.047
  47. Gambaletta, D., Marchetti, A., Benedetti, L., Mercurio, A. M., Sacchi, A. and Falcioni, R. (2000) Cooperative signaling between alpha(6)beta(4) integrin and ErbB-2 receptor is required to promote phosphatidylinositol 3-kinasedependent invasion. J. Biol. Chem. 275, 10604-10610. https://doi.org/10.1074/jbc.275.14.10604
  48. Folgiero, V., Bachelder, R. E., Bon, G., Sacchi, A., Falcioni, R. and Mercurio, A. M. (2007) The alpha6beta4 integrin can regulate ErbB-3 expression: implications for alpha6 beta4 signaling and function. Cancer Res. 67, 1645-1652. https://doi.org/10.1158/0008-5472.CAN-06-2980
  49. Gilcrease, M. Z., Zhou, X., Lu, X., Woodward, W. A., Hall, B. E. and Morrissey, P. J. (2009) Alpha6beta4 integrin crosslinking induces EGFR clustering and promotes EGF-mediated Rho activation in breast cancer. J. Exp. Clin. Cancer Res. 28, 67. https://doi.org/10.1186/1756-9966-28-67
  50. Chung, J., Yoon, S. O., Lipscomb, E. A. and Mercurio, A. M. (2004) The Met receptor and alpha 6 beta 4 integrin can function independently to promote carcinoma invasion. J. Biol. Chem. 279, 32287-32293. https://doi.org/10.1074/jbc.M403809200
  51. Meyer, T., Marshall, J. F. and Hart, I. R. (1998) Expression of alphav integrins and vitronectin receptor identity in breast cancer cells. Br. J. Cancer 77, 530-536. https://doi.org/10.1038/bjc.1998.86
  52. Wong, N. C., Mueller, B. M., Barbas, C. F., Ruminski, P., Quaranta, V., Lin, E. C. and Smith, J. W. (1998) Alphav integrins mediate adhesion and migration of breast carcinoma cell lines. Clin. Exp. Metastasis. 16, 50-61. https://doi.org/10.1023/A:1006512018609
  53. Brooks, P. C., Stromblad, S., Klemke, R., Visscher, D., Sarkar, F. H. and Cheresh, D. A. (1995) Antiintegrin alpha v beta 3 blocks human breast cancer growth and angiogenesis in human skin. J. Clin. Invest. 96, 1815-1822. https://doi.org/10.1172/JCI118227
  54. Gramoun, A., Shorey, S., Bashutski, J. D., Dixon, S. J., Sims, S. M., Heersche, J. N. and Manolson, M. F. (2007) Effects of Vitaxin, a novel therapeutic in trial for metastatic bone tumors, on osteoclast functions in vitro. J. Cell Biochem. 102, 341-352. https://doi.org/10.1002/jcb.21296
  55. Eliceiri, B. P. (2001) Integrin and growth factor receptor crosstalk. Circ. Res. 89, 1104-1110. https://doi.org/10.1161/hh2401.101084
  56. Tuck, A. B., Elliott, B. E., Hota, C., Tremblay, E. and Chambers, A. F. (2000) Osteopontin-induced, integrindependent migration of human mammary epithelial cells involves activation of the hepatocyte growth factor receptor (Met). J. Cell Biochem. 78, 465-475. https://doi.org/10.1002/1097-4644(20000901)78:3<465::AID-JCB11>3.0.CO;2-C
  57. White, D. E. and Muller, W. J. (2007) Multifaceted roles of integrins in breast cancer metastasis. J. Mammary. Gland. Biol. Neoplasia. 12, 135-142. https://doi.org/10.1007/s10911-007-9045-5
  58. Colognato, H., Baron, W., Avellana-Adalid, V., Relvas, J. B., Baron-Van Evercooren, A., Georges-Labouesse, E. and ffrench-Constant, C. (2002) CNS integrins switch growth factor signalling to promote target-dependent survival. Nat. Cell Biol. 4, 833-841. https://doi.org/10.1038/ncb865
  59. Somanath, P. R., Malinin, N. L. and Byzova, T. V. (2009) Cooperation between integrin alphavbeta3 and VEGFR2 in angiogenesis. Angiogenesis 12, 177-185. https://doi.org/10.1007/s10456-009-9141-9
  60. Phillips, D. R., Prasad, K. S., Manganello, J., Bao, M. and Nannizzi-Alaimo, L. (2001) Integrin tyrosine phosphorylation in platelet signaling. Curr. Opin. Cell Biol. 13, 546-554. https://doi.org/10.1016/S0955-0674(00)00250-7
  61. Mori, S., Wu, C. Y., Yamaji, S., Saegusa, J., Shi, B., Ma, Z., Kuwabara, Y., Lam, K. S., Isseroff, R. R., Takada, Y. K. and Takada, Y. (2008) Direct binding of integrin alphavbeta3 to FGF1 plays a role in FGF1 signaling. J. Biol. Chem. 283, 18066-18075. https://doi.org/10.1074/jbc.M801213200
  62. Danen, E. H. and Yamada, K. M. (2001) Fibronectin, integrins, and growth control. J. Cell Physiol. 189, 1-13. https://doi.org/10.1002/jcp.1137
  63. Nista, A., Leonetti, C., Bernardini, G., Mattioni, M. and Santoni, A. (1997) Functional role of alpha4beta1 and alpha5beta1 integrin fibronectin receptors expressed on adriamycin-resistant MCF-7 human mammary carcinoma cells. Int. J. Cancer 72, 133-141. https://doi.org/10.1002/(SICI)1097-0215(19970703)72:1<133::AID-IJC19>3.0.CO;2-K
  64. Morozevich, G., Kozlova, N., Cheglakov, I., Ushakova, N. and Berman, A. (2009) Integrin alpha5beta1 controls invasion of human breast carcinoma cells by direct and indirect modulation of MMP-2 collagenase activity. Cell Cycle 8, 2219-2225. https://doi.org/10.4161/cc.8.14.8980
  65. Jia, Y., Zeng, Z. Z., Markwart, S. M., Rockwood, K. F., Ignatoski, K. M., Ethier, S. P. and Livant, D. L. (2004) Integrin fibronectin receptors in matrix metalloproteinase-1-dependent invasion by breast cancer and mammary epithelial cells. Cancer Res. 64, 8674-8681. https://doi.org/10.1158/0008-5472.CAN-04-0069
  66. Liu, Y., Pixley, R., Fusaro, M., Godoy, G., Kim, E., Bromberg, M. E. and Colman, R. W. (2009) Cleaved high-molecular-weight kininogen and its domain 5 inhibit migration and invasion of human prostate cancer cells through the epidermal growth factor receptor pathway. Oncogene 28, 2756-2765. https://doi.org/10.1038/onc.2009.132
  67. Cascone, I., Napione, L., Maniero, F., Serini, G. and Bussolino, F. (2005) Stable interaction between alpha5beta1 integrin and Tie2 tyrosine kinase receptor regulates endothelial cell response to Ang-1. J. Cell Biol. 170, 993-1004. https://doi.org/10.1083/jcb.200507082
  68. Zhang, X., Groopman, J. E. and Wang, J. F. (2005) Extracellular matrix regulates endothelial functions through interaction of VEGFR-3 and integrin alpha5beta1. J. Cell Physiol. 202, 205-214. https://doi.org/10.1002/jcp.20106
  69. Lee, J. W. and Juliano, R. L. (2002) The alpha5beta1 integrin selectively enhances epidermal growth factor signaling to the phosphatidylinositol-3-kinase/Akt pathway in intestinal epithelial cells. Biochim. Biophys. Acta. 1542, 23-31. https://doi.org/10.1016/S0167-4889(01)00161-6
  70. Rahman, S., Patel, Y., Murray, J., Patel, K. V., Sumathipala, R., Sobel, M. and Wijelath, E. S. (2005) Novel hepatocyte growth factor (HGF) binding domains on fibronectin and vitronectin coordinate a distinct and amplified Met-integrin induced signalling pathway in endothelial cells. BMC. Cell Biol. 6, 8. https://doi.org/10.1186/1471-2121-6-8
  71. Bell, L. N., Cai, L., Johnstone, B. H., Traktuev, D. O., March, K. L. and Considine, R. V. (2008) A central role for hepatocyte growth factor in adipose tissue angiogenesis. Am. J. Physiol. Endocrinol. Metab. 294, E336-344. https://doi.org/10.1152/ajpendo.00272.2007

Cited by

  1. The opposing roles of laminin-binding integrins in cancer vol.57-58, 2017, https://doi.org/10.1016/j.matbio.2016.08.007
  2. Crosstalk between insulin-like growth factor (IGF) receptor and integrins through direct integrin binding to IGF1 vol.34, 2017, https://doi.org/10.1016/j.cytogfr.2017.01.003
  3. Select cytoplasmic and membrane proteins increase the percentage of immobile integrins but do not affect the average diffusion coefficient of mobile integrins vol.405, pp.26, 2013, https://doi.org/10.1007/s00216-013-7279-1
  4. PSMA redirects cell survival signaling from the MAPK to the PI3K-AKT pathways to promote the progression of prostate cancer vol.10, pp.470, 2017, https://doi.org/10.1126/scisignal.aag3326
  5. Fungal adhesion protein guides community behaviors and autoinduction in a paracrine manner vol.110, pp.28, 2013, https://doi.org/10.1073/pnas.1308173110
  6. Sulfatase-mediated manipulation of the astrocyte-Schwann cell interface vol.65, pp.1, 2017, https://doi.org/10.1002/glia.23047
  7. Aptamer-mediated impairment of EGFR-integrin αvβ3 complex inhibits vasculogenic mimicry and growth of triple-negative breast cancers vol.7, 2017, https://doi.org/10.1038/srep46659
  8. Unraveling the role of membrane proteins Notch, Pvr, and EGFR in altering integrin diffusion and clustering vol.404, pp.8, 2012, https://doi.org/10.1007/s00216-012-6362-3
  9. On the trail of the glycan codes stored in cancer-related cell adhesion proteins vol.1861, pp.1, 2017, https://doi.org/10.1016/j.bbagen.2016.08.007
  10. Distinct ErbB2 receptor populations differentially interact with beta1 integrin in breast cancer cell models vol.12, pp.3, 2017, https://doi.org/10.1371/journal.pone.0174230
  11. The integrin alphav beta3 increases cellular stiffness and cytoskeletal remodeling dynamics to facilitate cancer cell invasion vol.15, pp.1, 2013, https://doi.org/10.1088/1367-2630/15/1/015003
  12. Implication of α2β1 integrin in anoikis of MCF-7 human breast carcinoma cells vol.80, pp.1, 2015, https://doi.org/10.1134/S0006297915010113
  13. Insulin-like Growth Factor (IGF) Signaling Requires αvβ3-IGF1-IGF Type 1 Receptor (IGF1R) Ternary Complex Formation in Anchorage Independence, and the Complex Formation Does Not Require IGF1R and Src Activation vol.288, pp.5, 2013, https://doi.org/10.1074/jbc.M112.412536
  14. β1-integrins signaling and mammary tumor progression in transgenic mouse models: implications for human breast cancer vol.13, pp.6, 2011, https://doi.org/10.1186/bcr2905
  15. The cancer cell adhesion resistome: mechanisms, targeting and translational approaches vol.398, pp.7, 2017, https://doi.org/10.1515/hsz-2016-0326
  16. Beta 1-integrin–c-Met cooperation reveals an inside-in survival signalling on autophagy-related endomembranes vol.7, 2016, https://doi.org/10.1038/ncomms11942
  17. Integrin Signaling in Mammary Epithelial Cells and Breast Cancer vol.2012, 2012, https://doi.org/10.5402/2012/493283
  18. Integrin alpha9 (ITGA9) expression and epigenetic silencing in human breast tumors vol.5, pp.5, 2011, https://doi.org/10.4161/cam.5.5.17949
  19. The effect of cell–ECM adhesion on signalling via the ErbB family of growth factor receptors vol.39, pp.2, 2011, https://doi.org/10.1042/BST0390568
  20. Signaling mechanism of cell adhesion molecules in breast cancer metastasis: potential therapeutic targets vol.128, pp.1, 2011, https://doi.org/10.1007/s10549-011-1499-x
  21. Endothelial-derived neuregulin is an important mediator of ischaemia-induced angiogenesis and arteriogenesis vol.93, pp.3, 2012, https://doi.org/10.1093/cvr/cvr352
  22. Interactions between αv-Integrin and HER2 and Their Role in the Invasive Phenotype of Breast Cancer Cells In Vitro and in Rat Brain vol.10, pp.7, 2015, https://doi.org/10.1371/journal.pone.0131842
  23. Discovery of Platyhelminth-Specific α/β-Integrin Families and Evidence for Their Role in Reproduction in Schistosoma mansoni vol.7, pp.12, 2012, https://doi.org/10.1371/journal.pone.0052519
  24. Inhibition of breast cancer growth and metastasis by a biomimetic peptide vol.4, pp.1, 2015, https://doi.org/10.1038/srep07139
  25. Charming neighborhoods on the cell surface: Plasma membrane microdomains regulate receptor tyrosine kinase signaling vol.27, pp.10, 2015, https://doi.org/10.1016/j.cellsig.2015.07.004
  26. Hydrophobic Fluorescent Probes Introduce Artifacts into Single Molecule Tracking Experiments Due to Non-Specific Binding vol.8, pp.9, 2013, https://doi.org/10.1371/journal.pone.0074200
  27. Role of the interaction between galectin-3 and cell adhesion molecules in cancer metastasis vol.69, 2015, https://doi.org/10.1016/j.biopha.2014.11.024
  28. Free-Radical Polymer Science Structural Cancer Model: A Review vol.2013, 2013, https://doi.org/10.1155/2013/143589
  29. Tenascin-C-derived Peptide TNIIIA2 Highly Enhances Cell Survival and Platelet-derived Growth Factor (PDGF)-dependent Cell Proliferation through Potentiated and Sustained Activation of Integrin α5β1 vol.289, pp.25, 2014, https://doi.org/10.1074/jbc.M113.546622
  30. Integrins and Cell Metabolism: An Intimate Relationship Impacting Cancer vol.18, pp.1, 2017, https://doi.org/10.3390/ijms18010189
  31. Integrin Trafficking and Tumor Progression vol.2012, 2012, https://doi.org/10.1155/2012/516789
  32. CB1 cannabinoid receptors promote maximal FAK catalytic activity by stimulating cooperative signaling between receptor tyrosine kinases and integrins in neuronal cells vol.25, pp.8, 2013, https://doi.org/10.1016/j.cellsig.2013.03.020
  33. The collagen receptor discoidin domain receptor 2 stabilizes SNAIL1 to facilitate breast cancer metastasis vol.15, pp.6, 2013, https://doi.org/10.1038/ncb2743
  34. Mechanisms of talin-dependent integrin signaling and crosstalk vol.1838, pp.2, 2014, https://doi.org/10.1016/j.bbamem.2013.07.017
  35. The C-terminal region of NELL1 mediates osteoblastic cell adhesion through integrin α3β1 vol.586, pp.16, 2012, https://doi.org/10.1016/j.febslet.2012.06.014
  36. The malignant social network vol.6, pp.4, 2012, https://doi.org/10.4161/cam.21294
  37. An integrin beta4-EGFR unit promotes hepatocellular carcinoma lung metastases by enhancing anchorage independence through activation of FAK–AKT pathway vol.376, pp.1, 2016, https://doi.org/10.1016/j.canlet.2016.03.023
  38. Involvement of the Integrin α1β1 in the Progression of Colorectal Cancer vol.9, pp.8, 2017, https://doi.org/10.3390/cancers9080096
  39. Neurohormonal Regulation of Tumor Growth vol.54, pp.1, 2018, https://doi.org/10.1134/S1022795418010064
  40. Impaired dermal wound healing in discoidin domain receptor 2-deficient mice associated with defective extracellular matrix remodeling vol.4, pp.1, 2011, https://doi.org/10.1186/1755-1536-4-5