The oncogene HER2/neu (ERBB2) requires the hypoxia-inducible factor HIF-1 for mammary tumor growth and anoikis resistance

Journal of Biological Chemistry

Volumn 288, Issue 22, 2013, Pages 15865-15877

  Whelan, Kelly A ^a   Schwab, Luciana P ^b   Karakashev, Sergey V ^a   Franchetti, Lisa ^a   Johannes, Gregg J ^a   Seagroves, Tiffany N ^b   Reginato, Mauricio J ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CANCER CELLS; CELL SIGNALING; CYTOLOGY; DEFECTS; DISEASES; GENE EXPRESSION; GENE EXPRESSION REGULATION; MAMMALS; METABOLISM; OXYGEN;

ANOIKIS; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTORS; IN-VIVO; MAMMARY TUMORS; METABOLIC DEFECTS; ONCOGENESIS; REACTIVE OXYGEN SPECIES; RECEPTOR-TYROSINE KINASE; TUMOR GROWTH;

TUMORS;

BIM PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE;

ACINAR CELL; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOIKIS; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CANCER RESISTANCE; CELL HYPOXIA; CONTROLLED STUDY; FEMALE; GENE CONTROL; GENE DELETION; GENE EXPRESSION PROFILING; GENE NUMBER; GENE OVEREXPRESSION; GENE TARGETING; HIF1ALPHA GENE; HUMAN; HUMAN CELL; IN VIVO STUDY; METABOLIC DISORDER; MOUSE; NONHUMAN; ONCOGENE; ONCOGENE ERBB2; PHENOTYPE; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION;

MOUSE MAMMARY TUMOR VIRUS; MUS;

EID: 84878417516     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.426999     Document Type: Article

References (49)

1. Frisch, S. M., and Francis, H. (1994) Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124, 619-626 (Pubitemid 24064472)
2. Reginato, M. J., and Muthuswamy, S. K. (2006) Illuminating the center. Mechanisms regulating lumen formation and maintenance in mammary morphogenesis. J. Mammary Gland Biol. Neoplasia 11, 205-211 (Pubitemid 44869916)
3. Schwartz, M. A. (1997) Integrins, oncogenes, and anchorage independence. J. Cell Biol. 139, 575-578
4. Slamon, D. J., Godolphin, W., Jones, L. A., Holt, J. A., Wong, S. G., Keith, D. E., Levin, W. J., Stuart, S. G., Udove, J., and Ullrich, A. (1989) Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 244, 707-712 (Pubitemid 19147683)
5. 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 (Pubitemid 36986781)
6. Muthuswamy, S. K., Li, D., Lelievre, S., Bissell, M. J., and Brugge, J. S. (2001) ERBB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat. Cell Biol. 3, 785-792 (Pubitemid 32842683)
7. 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 (Pubitemid 47181532)
8. 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
9. Semenza, G. L. (2000) HIF-1. Mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. 88, 1474-1480
10. Generali, D., Berruti, A., Brizzi, M. P., Campo, L., Bonardi, S., Wigfield, S., Bersiga, A., Allevi, G., Milani, M., Aguggini, S., Gandolfi, V., Dogliotti, L., Bottini, A., Harris, A. L., and Fox, S. B. (2006) Hypoxia-inducible factor-1α expression predicts a poor response to primary chemoendocrine therapy and disease-free survival in primary human breast cancer. Clin. Cancer Res. 12, 4562-4568 (Pubitemid 44297805)
11. Semenza, G. L. (2003) Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3, 721-732
12. Laughner, E., Taghavi, P., Chiles, K., Mahon, P. C., and Semenza, G. L. (2001) HER2(neu) signaling increases the rate of hypoxia-inducible factor 1α (HIF-1α) synthesis. Novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol. Cell Biol. 21, 3995-4004 (Pubitemid 32476461)
13. Li, Y. M., Zhou, B. P., Deng, J., Pan, Y., Hay, N., and Hung, M. C. (2005) A hypoxia-independent hypoxia-inducible factor-1 activation pathway induced by phosphatidylinositol 3-kinase/Akt in HER2 overexpressing cells. Cancer Res. 65, 3257-3263 (Pubitemid 40524609)
14. 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
15. Whelan, K. A., and Reginato, M. J. (2011) Surviving without oxygen. Hypoxia regulation of mammary morphogenesis and anoikis. Cell Cycle 10, 2287-2294
16. Ryan, H. E., Poloni, M., McNulty, W., Elson, D., Gassmann, M., Arbeit, J. M., and Johnson, R. S. (2000) Hypoxia-inducible factor-1α is a positive factor in solid tumor growth. Cancer Res. 60, 4010-4015 (Pubitemid 30636574)
17. Schwab, L. P., Peacock, D. L., Majumdar, D., Ingels, J. F., Jensen, L. C., Smith, K. D., Cushing, R. C., and Seagroves, T. N. (2012) Hypoxia-inducible factor 1α promotes primary tumor growth and tumor-initiating cell activity in breast cancer. Breast Cancer Res. 14, R6
18. 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 (Pubitemid 40705763)
19. 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
20. Guy, C. T., Webster, M. A., Schaller, M., Parsons, T. J., Cardiff, R. D., and Muller, W. J. (1992) Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc. Natl. Acad. Sci. U.S.A. 89, 10578-10582
21. Gatza, M. L., Kung, H. N., Blackwell, K. L., Dewhirst, M. W., Marks, J. R., and Chi, J. T. (2011) Analysis of tumor environmental response and oncogenic pathway activation identifies distinct basal and luminal features in HER2-related breast tumor subtypes. Breast Cancer Res. 13, R62
22. Goonewardene, T. I., Sowter, H. M., and Harris, A. L. (2002) Hypoxia-induced pathways in breast cancer. Microsc. Res. Tech. 59, 41-48
23. Franovic, A., Holterman, C. E., Payette, J., and Lee, S. (2009) Human cancers converge at the HIF-2α oncogenic axis. Proc. Natl. Acad. Sci. U.S.A. 106, 21306-21311
24. Semenza, G. L. (2010) Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 29, 625-634
25. Gullick, W. J. (2002) A new model for ductal carcinoma in situ suggests strategies for treatment. Breast Cancer Res. 4, 176-178
26. Semenza, G. L. (2011) Hypoxia-inducible factor 1. Regulator of mitochondrial metabolism and mediator of ischemic preconditioning. Biochim. Biophys. Acta 1813, 1263-1268
27. Pedersen, K., Angelini, P. D., Laos, S., Bach-Faig, A., Cunningham, M. P., Ferrer-Ramón, C., Luque-García, A., García-Castillo, J., Parra-Palau, J. L., Scaltriti, M., Ramón y Cajal, S., Baselga, J., and Arribas, J. (2009) A naturally occurring HER2 carboxyl-terminal fragment promotes mammary tumor growth and metastasis. Mol. Cell Biol. 29, 3319-3331
28. Chrestensen, C. A., Shuman, J. K., Eschenroeder, A., Worthington, M., Gram, H., and Sturgill, T. W. (2007) MNK1 and MNK2 regulation in HER2-overexpressing breast cancer lines. J. Biol. Chem. 282, 4243-4252 (Pubitemid 47100950)
29. Bartosová, M., Parkkila, S., Pohlodek, K., Karttunen, T. J., Galbavý, S., Mucha, V., Harris, A. L., Pastorek, J., and Pastoreková, S. (2002) Expression of carbonic anhydrase IX in breast is associated with malignant tissues and is related to overexpression of c-erbB2. J. Pathol. 197, 314-321
30. Zhao, Y. H., Zhou, M., Liu, H., Ding, Y., Khong, H. T., Yu, D., Fodstad, O., and Tan, M. (2009) Up-regulation of lactate dehydrogenase A by ERBB2 through heat shock factor 1 promotes breast cancer cell glycolysis and growth. Oncogene 28, 3689-3701
31. Mackay, A., Jones, C., Dexter, T., Silva, R. L., Bulmer, K., Jones, A., Simpson, P., Harris, R. A., Jat, P. S., Neville, A. M., Reis, L. F., Lakhani, S. R., and O'Hare, M. J. (2003) cDNA microarray analysis of genes associated with ERBB2 (HER2/neu) overexpression in human mammary luminal epithelial cells. Oncogene 22, 2680-2688 (Pubitemid 36605615)
32. Pradeep, C. R., Zeisel, A., Köstler, W. J., Lauriola, M., Jacob-Hirsch, J., Haibe-Kains, B., Amariglio, N., Ben-Chetrit, N., Emde, A., Solomonov, I., Neufeld, G., Piccart, M., Sagi, I., Sotiriou, C., Rechavi, G., Domany, E., Desmedt, C., and Yarden, Y. (2012) Modeling invasive breast cancer. Growth factors propel progression of HER2-positive premalignant lesions. Oncogene 31, 3569-3583
33. Spangenberg, C., Lausch, E. U., Trost, T. M., Prawitt, D., May, A., Keppler, R., Fees, S. A., Reutzel, D., Bell, C., Schmitt, S., Schiffer, I. B., Weber, A., Brenner, W., Hermes, M., Sahin, U., Türeci, O., Koelbl, H., Hengstler, J. G., and Zabel, B. U. (2006) ERBB2-mediated transcriptional up-regulation of the α5β1 integrin fibronectin receptor promotes tumor cell survival under adverse conditions. Cancer Res. 66, 3715-3725
34. Zhang, H., Wong, C. C., Wei, H., Gilkes, D. M., Korangath, P., Chaturvedi, P., Schito, L., Chen, J., Krishnamachary, B., Winnard, P. T., Jr., Raman, V., Zhen, L., Mitzner, W. A., Sukumar, S., and Semenza, G. L. (2012) HIF-1-dependent expression of angiopoietin-like 4 and L1CAM mediates vascular metastasis of hypoxic breast cancer cells to the lungs. Oncogene 31, 1757-1770
35. Sowter, H. M., Ratcliffe, P. J., Watson, P., Greenberg, A. H., and Harris, A. L. (2001) HIF-1-dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors. Cancer Res. 61, 6669-6673 (Pubitemid 32896483)
36. Cormier-Regard, S., Nguyen, S. V., and Claycomb, W. C. (1998) Adrenomedullin gene expression is developmentally regulated and induced by hypoxia in rat ventricular cardiac myocytes. J. Biol. Chem. 273, 17787-17792 (Pubitemid 28355122)
37. Rohwer, N., Welzel, M., Daskalow, K., Pfander, D., Wiedenmann, B., Detjen, K., and Cramer, T. (2008) Hypoxia-inducible factor 1α mediates anoikis resistance via suppression of α5 integrin. Cancer Res. 68, 10113-10120
38. Padua, D., Zhang, X. H., Wang, Q., Nadal, C., Gerald, W. L., Gomis, R. R., and Massagué, J. (2008) TGFβ primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 133, 66-77 (Pubitemid 351442989)
39. 2 ratio and confers anoikis resistance to tumors. Cancer Cell 19, 401-415
40. Knuefermann, C., Lu, Y., Liu, B., Jin, W., Liang, K., Wu, L., Schmidt, M., Mills, G. B., Mendelsohn, J., and Fan, Z. (2003) HER2/PI-3K/Akt activation leads to a multidrug resistance in human breast adenocarcinoma cells. Oncogene 22, 3205-3212 (Pubitemid 36712932)
41. Tan, M., Jing, T., Lan, K. H., Neal, C. L., Li, P., Lee, S., Fang, D., Nagata, Y., Liu, J., Arlinghaus, R., Hung, M. C., and Yu, D. (2002) Phosphorylation on tyrosine-15 of p34(Cdc2) by ERBB2 inhibits p34(Cdc2) activation and is involved in resistance to taxol-induced apoptosis. Mol. Cell 9, 993-1004 (Pubitemid 34626669)
42. Harris, A. L. (2002) Hypoxia. A key regulatory factor in tumour growth. Nat. Rev. Cancer 2, 38-47
43. Sullivan, R., Paré, G. C., Frederiksen, L. J., Semenza, G. L., and Graham, C. H. (2008) Hypoxia-induced resistance to anticancer drugs is associated with decreased senescence and requires hypoxia-inducible factor-1 activity. Mol. Cancer Ther. 7, 1961-1973
44. Faber, A. C., Corcoran, R. B., Ebi, H., Sequist, L. V., Waltman, B. A., Chung, E., Incio, J., Digumarthy, S. R., Pollack, S. F., Song, Y., Muzikansky, A., Lifshits, E., Roberge, S., Coffman, E. J., Benes, C. H., Gómez, H. L., Baselga, J., Arteaga, C. L., Rivera, M. N., Dias-Santagata, D., Jain, R. K., and Engelman, J. A. (2011) BIM expression in treatment-naive cancers predicts responsiveness to kinase inhibitors. Cancer Discov. 1, 352-365
45. Semenza, G. L. (2010) HIF-1. Upstream and downstream of cancer metabolism. Curr. Opin. Genet. Dev. 20, 51-56
46. Wang, J., and Yi, J. (2008) Cancer cell killing via ROS. To increase or decrease, that is the question. Cancer Biol. Ther. 7, 1875-1884
47. Kim, J. W., Tchernyshyov, I., Semenza, G. L., and Dang, C. V. (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase. A metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 3, 177-185
48. Zhang, H., Bosch-Marce, M., Shimoda, L. A., Tan, Y. S., Baek, J. H., Wesley, J. B., Gonzalez, F. J., and Semenza, G. L. (2008) Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J. Biol. Chem. 283, 10892-10903
49. Bellot, G., Garcia-Medina, R., Gounon, P., Chiche, J., Roux, D., Pouysségur, J., and Mazure, N. M. (2009) Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol. Cell Biol. 29, 2570-2581