The role of multicellular aggregation in the survival of ErbB2-positive breast cancer cells during extracellular matrix detachment

Journal of Biological Chemistry

Volumn 290, Issue 14, 2015, Pages 8722-8733

  Rayavarapu, Raju R ^a   Heiden, Brendan ^a   Pagani, Nicholas ^a   Shaw, Melissa M ^a   Shuff, Sydney ^a   Zhang, Siyuan ^a   Schafer, Zachary T ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; CELL SIGNALING; CYTOLOGY; DISEASES; MATRIX ALGEBRA; PATHOLOGY;

ANOIKIS; BREAST CANCER CELLS; CANCER CELLS; EXTRACELLULAR MATRICES; MOLECULAR MECHANISM;

CELLS;

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; MITOGEN ACTIVATED PROTEIN KINASE; UVOMORULIN; ERBB2 PROTEIN, HUMAN;

ANOIKIS; ARTICLE; BREAST CANCER CELL LINE; CELL AGGREGATION; CELL ASSAY; CELL FUNCTION; CELL INVASION; CELL MIGRATION; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ASSAY; EXTRACELLULAR MATRIX DETACHMENT; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; BREAST TUMOR; ENZYMOLOGY; EXTRACELLULAR MATRIX; FEMALE; HUMAN; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL LINE, TUMOR; EXTRACELLULAR MATRIX; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION;

EID: 84926512814     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.612754     Document Type: Article

References (54)

1. Nguyen, D. X., and Massagué, J. (2007) Genetic determinants of cancer metastasis. Nat. Rev. Genet 8, 341-352
2. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
3. Wan, L., Pantel, K., and Kang, Y. (2013) Tumor metastasis: moving new biological insights into the clinic. Nat. Med. 19, 1450-1464
4. Mehlen, P., and Puisieux, A. (2006) Metastasis: a question of life or death. Nat. Rev. Cancer 6, 449-458
5. Frisch, S. M., and Francis, H. (1994) Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124, 619-626
6. Frisch, S. M., and Screaton, R. A. (2001) Anoikis mechanisms. Curr. Opin. Cell Biol. 13, 555-562
7. Avivar-Valderas, A., Bobrovnikova-Marjon, E., Alan Diehl, J., Bardeesy, N., Debnath, J., and Aguirre-Ghiso, J. A. (2013) Regulation of autophagy during ECM detachment is linked to a selective inhibition of mTORC1 by PERK. Oncogene. 32, 4932-4940
8. Avivar-Valderas, A., Salas, E., Bobrovnikova-Marjon, E., Diehl, J. A., Nagi, C., Debnath, J., and Aguirre-Ghiso, J. A. (2011) PERK integrates autophagy and oxidative stress responses to promote survival during extracellular matrix detachment. Mol. Cell Biol. 31, 3616-3629
9. Buchheit, C. L., Rayavarapu, R. R., and Schafer, Z. T. (2012) The regulation of cancer cell death and metabolism by extracellular matrix attachment. Semin Cell Dev. Biol. 23, 402-411
10. Davison, C. A., Durbin, S. M., Thau, M. R., Zellmer, V. R., Chapman, S. E., Diener, J., Wathen, C., Leevy, W. M., and Schafer, Z. T. (2013) Antioxidant enzymes mediate survival of breast cancer cells deprived of extracellular matrix. Cancer Res. 73, 3704-3715
11. Fung, C., Lock, R., Gao, S., Salas, E., and Debnath, J. (2008) Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol. Biol. Cell 19, 797-806
12. Schafer, Z. T., Grassian, A. R., Song, L., Jiang, Z., Gerhart-Hines, Z., Irie, H. Y., Gao, S., Puigserver, P., and Brugge, J. S. (2009) Antioxidant and oncogene rescue of metabolic defects caused by loss of matrix attachment. Nature 461, 109-113
13. Whelan, K. A., Caldwell, S. A., Shahriari, K. S., Jackson, S. R., Franchetti, L. D., Johannes, G. J., and Reginato, M. J. (2010) Hypoxia suppression of Bim and Bmf blocks anoikis and luminal clearing during mammary morphogenesis. Mol. Biol. Cell 21, 3829-3837
14. Buchheit, C. L., Weigel, K. J., and Schafer, Z. T. (2014) Cancer cell survival during detachment from the ECM: multiple barriers to tumour progression. Nat. Rev. Cancer 14, 632-641
15. Grassian, A. R., Schafer, Z. T., and Brugge, J. S. (2011) ErbB2 stabilizes epidermal growth factor receptor (EGFR) expression via Erk and Sprouty2 in extracellular matrix-detached cells. J. Biol. Chem. 286, 79-90
16. Haenssen, K. K., Caldwell, S. A., Shahriari, K. S., Jackson, S. R., Whelan, K. A., Klein-Szanto, A. J., and Reginato, M. J. (2010) ErbB2 requires integrin α5 for anoikis resistance via Src regulation of receptor activity in human mammary epithelial cells. J. Cell Sci. 123, 1373-1382
17. Buchheit, C. L., Angarola, B. L., Steiner, A., Weigel, K. J., and Schafer, Z. T. (2014) Anoikis evasion in inflammatory breast cancer cells is mediated by Bim-EL sequestration. Cell Death Differ Dec 19. doi: 10.1038/cdd. 2014.1209
18. Arteaga, C. L., and Engelman, J. A. (2014) ERBB receptors: from oncogene discovery to basic science to mechanism-based cancer therapeutics. Cancer Cell 25, 282-303
19. Higgins, M. J., and Baselga, J. (2011) Targeted therapies for breast cancer. J. Clin. Invest. 121, 3797-3803
20. Moss, N. M., Barbolina, M. V., Liu, Y., Sun, L., Munshi, H. G., and Stack, M. S. (2009) Ovarian cancer cell detachment and multicellular aggregate formation are regulated by membrane type 1 matrix metalloproteinase: a potential role in I.p. metastatic dissemination. Cancer Res. 69, 7121-7129
21. Robertson, F. M., Bondy, M., Yang, W., Yamauchi, H., Wiggins, S., Kamrudin, S., Krishnamurthy, S., Le-Petross, H., Bidaut, L., Player, A. N., Barsky, S. H., Woodward, W. A., Buchholz, T., Lucci, A., Ueno, N. T., and Cristofanilli, M. (2010) Inflammatory breast cancer: the disease, the biology, the treatment. CA Cancer J. Clin. 60, 351-375
22. Douma, S., Van Laar, T., Zevenhoven, J., Meuwissen, R., Van Garderen, E., and Peeper, D. S. (2004) Suppression of anoikis and induction of metastasis by the neurotrophic receptor TrkB. Nature 430, 1034-1039
23. Geiger, T. R., and Peeper, D. S. (2007) Critical role for TrkB kinase function in anoikis suppression, tumorigenesis, and metastasis. Cancer Res. 67, 6221-6229
24. Onder, T. T., Gupta, P. B., Mani, S. A., Yang, J., Lander, E. S., and Weinberg, R. A. (2008) Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res. 68, 3645-3654
25. Bossy-Wetzel, E., and Green, D. R. (2000) Assays for cytochrome c release from mitochondria during apoptosis. Methods Enzymol. 322, 235-242
26. Adachi, M., Zhang, Y. B., and Imai, K. (2003) Mutation of BAD within the BH3 domain impairs its phosphorylation-mediated regulation. FEBS Lett. 551, 147-152
27. Wang, H. G., Pathan, N., Ethell, I. M., Krajewski, S., Yamaguchi, Y., Shibasaki, F., McKeon, F., Bobo, T., Franke, T. F., and Reed, J. C. (1999) Ca2+ -induced apoptosis through calcineurin dephosphorylation of BAD. Science 284, 339-343
28. Reginato, M. J., Mills, K. R., Becker, E. B., Lynch, D. K., Bonni, A., Muthuswamy, S. K., and Brugge, J. S. (2005) Bim regulation of lumen formation in cultured mammary epithelial acini is targeted by oncogenes. Mol. Cell Biol. 25, 4591-4601
29. Stott, S. L., Hsu, C. H., Tsukrov, D. I., Yu, M., Miyamoto, D. T., Waltman, B. A., Rothenberg, S. M., Shah, A. M., Smas, M. E., Korir, G. K., Floyd, F. P., Jr., Gilman, A. J., Lord, J. B., Winokur, D., Springer, S., Irimia, D., Nagrath, S., Sequist, L. V., Lee, R. J., Isselbacher, K. J., Maheswaran, S., Haber, D. A., and Toner, M. (2010) Isolation of circulating tumor cells using a micro-vortex-generating herringbone-chip. Proc. Natl. Acad. Sci. U.S.A. 107, 18392-18397
30. Reginato, M. J., Mills, K. R., Paulus, J. K., Lynch, D. K., Sgroi, D. C., Debnath, J., Muthuswamy, S. K., and Brugge, J. S. (2003) Integrins and EGFR coordinately regulate the pro-apoptotic protein Bim to prevent anoikis. Nat. Cell Biol. 5, 733-740
31. van Roy, F. (2014) Beyond E-cadherin: roles of other cadherin superfamily members in cancer. Nat. Rev. Cancer 14, 121-134
32. Perl, A. K., Wilgenbus, P., Dahl, U., Semb, H., and Christofori, G. (1998) A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 392, 190-193
33. Pece, S., Chiariello, M., Murga, C., and Gutkind, J. S. (1999) Activation of the protein kinase Akt/PKB by the formation of E-cadherin-mediated cellcell junctions. Evidence for the association of phosphatidylinositol 3-kinase with the E-cadherin adhesion complex. J. Biol. Chem. 274, 19347-19351
34. Pierceall, W. E., Woodard, A. S., Morrow, J. S., Rimm, D., and Fearon, E. R. (1995) Frequent alterations in E-cadherin and α- and β-catenin expression in human breast cancer cell lines. Oncogene. 11, 1319-1326
35. Goh, L. K., and Sorkin, A. (2013) Endocytosis of receptor tyrosine kinases. Cold Spring Harb. Perspect Biol. 5, a017459
36. Bremm, A., Walch, A., Fuchs, M., Mages, J., Duyster, J., Keller, G., Hermannstädter, C., Becker, K. F., Rauser, S., Langer, R., von Weyhern, C. H., Höfler, H., and Luber, B. (2008) Enhanced activation of epidermal growth factor receptor caused by tumor-derived E-cadherin mutations. Cancer Res. 68, 707-714
37. Schmelzle, T., Mailleux, A. A., Overholtzer, M., Carroll, J. S., Solimini, N. L., Lightcap, E. S., Veiby, O. P., and Brugge, J. S. (2007) Functional role and oncogene-regulated expression of the BH3-only factor Bmf in mammary epithelial anoikis and morphogenesis. Proc. Natl. Acad. Sci. U.S.A. 104, 3787-3792
38. Whelan, K. A., Schwab, L. P., Karakashev, S. V., Franchetti, L., Johannes, G. J., Seagroves, T. N., and Reginato, M. J. (2013) The oncogene HER2/neu (ERBB2) requires the hypoxia-inducible factor HIF-1 for mammary tumor growth and anoikis resistance. J. Biol. Chem. 288, 15865-15877
39. Weigel, K. J., Jakimenko, A., Conti, B. A., Chapman, S. E., Kaliney, W. J., Leevy, W. M., Champion, M. M., and Schafer, Z. T. (2014) CAF-Secreted IGFBPs Regulate Breast Cancer Cell Anoikis. Mol. Cancer Res. 12, 855-866
40. She, Q. B., Solit, D. B., Ye, Q., O'Reilly, K. E., Lobo, J., and Rosen, N. (2005) The BAD protein integrates survival signaling by EGFR/MAPK and PI3K/Akt kinase pathways in PTEN-deficient tumor cells. Cancer Cell 8, 287-297
41. Yonesaka, K., Zejnullahu, K., Okamoto, I., Satoh, T., Cappuzzo, F., Souglakos, J., Ercan, D., Rogers, A., Roncalli, M., Takeda, M., Fujisaka, Y., Philips, J., Shimizu, T., Maenishi, O., Cho, Y., Sun, J., Destro, A., Taira, K., Takeda, K., Okabe, T., Swanson, J., Itoh, H., Takada, M., Lifshits, E., Okuno, K., Engelman, J. A., Shivdasani, R. A., Nishio, K., Fukuoka, M., Varella-Garcia, M., Nakagawa, K., and Jänne, P. A. (2011) Activation of ERBB2 signaling causes resistance to the EGFR-directed therapeutic antibody cetuximab. Sci. Transl. Med. 3, 99ra86
42. Shen, X., and Kramer, R. H. (2004) Adhesion-mediated squamous cell carcinoma survival through ligand-independent activation of epidermal growth factor receptor. Am. J. Pathol. 165, 1315-1329
43. Lamouille, S., Xu, J., and Derynck, R. (2014) Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol. 15, 178-196
44. Kumar, S., Park, S. H., Cieply, B., Schupp, J., Killiam, E., Zhang, F., Rimm, D. L., and Frisch, S. M. (2011) A pathway for the control of anoikis sensitivity by E-cadherin and epithelial-to-mesenchymal transition. Mol. Cell Biol. 31, 4036-4051
45. Ocaña, O. H., Córcoles, R., Fabra, A., Moreno-Bueno, G., Acloque, H., Vega, S., Barrallo-Gimeno, A., Cano, A., and Nieto, M. A. (2012) Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer Cell 22, 709-724
46. Tsai, J. H., Donaher, J. L., Murphy, D. A., Chau, S., and Yang, J. (2012) Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell 22, 725-736
47. Chao, Y. L., Shepard, C. R., and Wells, A. (2010) Breast carcinoma cells re-express E-cadherin during mesenchymal to epithelial reverting transition. Mol. Cancer 9, 179
48. Kowalski, P. J., Rubin, M. A., and Kleer, C. G. (2003) E-cadherin expression in primary carcinomas of the breast and its distant metastases. Breast Cancer Res. 5, R217-R222
49. Fidler, I. J. (1973) The relationship of embolic homogeneity, number, size and viability to the incidence of experimental metastasis. Eur. J. Cancer 9, 223-227
50. Watanabe, S. (1954) The metastasizability of tumor cells. Cancer 7, 215-223
51. Fernandez, S. V., Robertson, F. M., Pei, J., Aburto-Chumpitaz, L., Mu, Z., Chu, K., Alpaugh, R. K., Huang, Y., Cao, Y., Ye, Z., Cai, K. Q., Boley, K. M., Klein-Szanto, A. J., Devarajan, K., Addya, S., and Cristofanilli, M. (2013) Inflammatory breast cancer (IBC): clues for targeted therapies. Breast Cancer Res. Treat 140, 23-33
52. Yu, M., Stott, S., Toner, M., Maheswaran, S., and Haber, D. A. (2011) Circulating tumor cells: approaches to isolation and characterization. J. Cell Biol. 192, 373-382
53. Wang, S. E., Narasanna, A., Perez-Torres, M., Xiang, B., Wu, F. Y., Yang, S., Carpenter, G., Gazdar, A. F., Muthuswamy, S. K., and Arteaga, C. L. (2006) HER2 kinase domain mutation results in constitutive phosphorylation and activation of HER2 and EGFR and resistance to EGFR tyrosine kinase inhibitors. Cancer Cell 10, 25-38
54. Witta, S. E., Gemmill, R. M., Hirsch, F. R., Coldren, C. D., Hedman, K., Ravdel, L., Helfrich, B., Dziadziuszko, R., Chan, D. C., Sugita, M., Chan, Z., Baron, A., Franklin, W., Drabkin, H. A., Girard, L., Gazdar, A. F., Minna, J. D., and Bunn, P. A., Jr. (2006) Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cancer Res. 66, 944-950