Hyperactivation of mammalian target of rapamycin complex 1 (mTORC1) promotes breast cancer progression through enhancing glucose starvation-induced autophagy and akt signaling

Journal of Biological Chemistry

Volumn 289, Issue 2, 2014, Pages 1164-1173

  Chen, Yongqiang ^a   Wei, Huijun ^a,d   Liu, Fei ^c   Guan, Jun Lin ^a,b  

^a Department of Internal Medicine   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AKT ACTIVATION; BREAST CANCER; HYPERACTIVATION; MAMMALIAN TARGET; MAMMARY TUMORS; NEGATIVE REGULATORS; POTENTIAL TARGETS; TUMOR CELLS;

ACTIVATION ANALYSIS; TUMORS;

DISEASES;

CRE RECOMBINASE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PROTEIN KINASE B; TAMOXIFEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; BREAST CANCER; CANCER GROWTH; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENSITOMETRY; FEMALE; GENE DELETION; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STARVATION; TSC1 GENE; TUMOR GROWTH;

AUTOPHAGY; BREAST CANCER; MOUSE; MTOR COMPLEX (MTORC); SIGNALING;

ANIMALS; AUTOPHAGY; CELL SURVIVAL; FEMALE; GLUCOSE; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NUDE; MICE, TRANSGENIC; MULTIPROTEIN COMPLEXES; NEOPLASM METASTASIS; PROTO-ONCOGENE PROTEINS C-AKT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TUMOR BURDEN; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS;

EID: 84891936587     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.526335     Document Type: Article

References (43)

1. Kwiatkowski, D. J. (2003) Tuberous sclerosis. From tubers to mTOR. Ann. Hum. Genet. 67, 87-96
2. Inoki, K., and Guan, K. L. (2009) Tuberous sclerosis complex. Implication from a rare genetic disease to common cancer treatment. Hum. Mol. Genet. 18, R94-100
3. Orlova, K. A., and Crino, P. B. (2010) The tuberous sclerosis complex. Ann. N.Y. Acad. Sci. 1184, 87-105
4. Ma, X. M., and Blenis, J. (2009) Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell Biol. 10, 307-318
5. Alessi, D. R., Pearce, L. R., and García-Martínez, J. M. (2009) New insights into mTOR signaling. mTORC2 and beyond. Sci. Signal 2, pe27
6. Hay, N., and Sonenberg, N. (2004) Upstream and downstream of mTOR. Genes Dev. 18, 1926-1945
7. Yu, Y., Yoon, S. O., Poulogiannis, G., Yang, Q., Ma, X. M., Villén, J., Kubica, N., Hoffman, G. R., Cantley, L. C., Gygi, S. P., and Blenis, J. (2011) Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling. Science 332, 1322-1326
8. Chan, E. Y. (2009) mTORC1 phosphorylates the ULK1-mAtg13-FIP200 autophagy regulatory complex. Sci. Signal 2, pe51
9. Mizushima, N., and Komatsu, M. (2011) Autophagy. Renovation of cells and tissues. Cell 147, 728-741
10. Chen, Y., and Klionsky, D. J. (2011) The regulation of autophagy. Unanswered questions. J. Cell Sci. 124, 161-170
11. Choi, A. M., Ryter, S. W., and Levine, B. (2013) Autophagy in human health and disease. N. Engl. J. Med. 368, 651-662
12. White, E. (2012) Deconvoluting the context-dependent role for autophagy in cancer. Nat. Rev. Cancer 12, 401-410
13. Rubinsztein, D. C., Mariño, G., and Kroemer, G. (2011) Autophagy and aging. Cell 146, 682-695
14. Hoshii, T., Tadokoro, Y., Naka, K., Ooshio, T., Muraguchi, T., Sugiyama, N., Soga, T., Araki, K., Yamamura, K., and Hirao, A. (2012) mTORC1 is essential for leukemia propagation but not stem cell self-renewal. J. Clin. Invest. 122, 2114-2129
15. Menon, S., Yecies, J. L., Zhang, H. H., Howell, J. J., Nicholatos, J., Harputlugil, E., Bronson, R. T., Kwiatkowski, D. J., and Manning, B. D. (2012) Chronic activation of mTOR complex 1 is sufficient to cause hepatocellular carcinoma in mice. Sci. Signal 5, ra24
16. Kladney, R. D., Cardiff, R. D., Kwiatkowski, D. J., Chiang, G. G., Weber, J. D., Arbeit, J. M., and Lu, Z. H. (2010) Tuberous sclerosis complex 1. An epithelial tumor suppressor essential to prevent spontaneous prostate cancer in aged mice. Cancer Res. 70, 8937-8947
17. Lee, D. F., Kuo, H. P., Chen, C. T., Hsu, J. M., Chou, C. K., Wei, Y., Sun, H. L., Li, L. Y., Ping, B., Huang, W. C., He, X., Hung, J. Y., Lai, C. C., Ding, Q., Su, J. L., Yang, J. Y., Sahin, A. A., Hortobagyi, G. N., Tsai, F. J., Tsai, C. H., and Hung, M. C. (2007) IKK suppression of TSC1 links inflammation and tumor angiogenesis via the mTOR pathway. Cell 130, 440-455
18. Radvanyi, L., Singh-Sandhu, D., Gallichan, S., Lovitt, C., Pedyczak, A., Mallo, G., Gish, K., Kwok, K., Hanna, W., Zubovits, J., Armes, J., Venter, D., Hakimi, J., Shortreed, J., Donovan, M., Parrington, M., Dunn, P., Oomen, R., Tartaglia, J., and Berinstein, N. L. (2005) The gene associated with trichorhinophalangeal syndrome in humans is overexpressed in breast cancer. Proc. Natl. Acad. Sci. U.S.A. 102, 11005-11010
19. Richardson, A. L., Wang, Z. C., De Nicolo, A., Lu, X., Brown, M., Miron, A., Liao, X., Iglehart, J. D., Livingston, D. M., and Ganesan, S. (2006) X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 9, 121-132
20. Curtis, C., Shah, S. P., Chin, S. F., Turashvili, G., Rueda, O. M., Dunning, M. J., Speed, D., Lynch, A. G., Samarajiwa, S., Yuan, Y., Gräf, S., Ha, G., Haffari, G., Bashashati, A., Russell, R., McKinney, S., METABRIC Group, Langerød, A., Green, A., Provenzano, E., Wishart, G., Pinder, S., Watson, P., Markowetz, F., Murphy, L., Ellis, I., Purushotham, A., Børresen-Dale, A. L., Brenton, J. D., Tavaré, S., Caldas, C., and Aparicio, S. (2012) The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 486, 346-352
21. Wei, H., Wei, S., Gan, B., Peng, X., Zou, W., and Guan, J. L. (2011) Suppression of autophagy by FIP200 deletion inhibits mammary tumorigenesis. Genes Dev. 25, 1510-1527
22. Uhlmann, E. J., Wong, M., Baldwin, R. L., Bajenaru, M. L., Onda, H., Kwiatkowski, D. J., Yamada, K., and Gutmann, D. H. (2002) Astrocytespecific TSC1 conditional knockout mice exhibit abnormal neuronal organization and seizures. Ann Neurol. 52, 285-296
23. Shen, T. L., Park, A. Y., Alcaraz, A., Peng, X., Jang, I., Koni, P., Flavell, R. A., Gu, H., and Guan, J. L. (2005) Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J. Cell Biol. 169, 941-952
24. Luo, M., Fan, H., Nagy, T., Wei, H., Wang, C., Liu, S., Wicha, M. S., and Guan, J. L. (2009) Mammary epithelial-specific ablation of the focal adhesion kinase suppresses mammary tumorigenesis by affecting mammary cancer stem/progenitor cells. Cancer Res. 69, 466-474
25. Fan, H., and Guan, J. L. (2011) Compensatory function of Pyk2 protein in the promotion of focal adhesion kinase (FAK)-null mammary cancer stem cell tumorigenicity and metastatic activity. J. Biol. Chem. 286, 18573-18582
26. Abbas, H. A., Maccio, D. R., Coskun, S., Jackson, J. G., Hazen, A. L., Sills, T. M., You, M. J., Hirschi, K. K., and Lozano, G. (2010) Mdm2 is required for survival of hematopoietic stem cells/progenitors via dampening of ROS-induced p53 activity. Cell Stem Cell 7, 606-617
27. Guy, C. T., Cardiff, R. D., and Muller, W. J. (1992) Induction of mammary tumors by expression of polyomavirus middle T oncogene. A transgenic mouse model for metastatic disease. Mol. Cell. Biol. 12, 954-961
28. Yang, S., Wang, X., Contino, G., Liesa, M., Sahin, E., Ying, H., Bause, A., Li, Y., Stommel, J. M., Dell'antonio, G., Mautner, J., Tonon, G., Haigis, M., Shirihai, O. S., Doglioni, C., Bardeesy, N., and Kimmelman, A. C. (2011) Pancreatic cancers require autophagy for tumor growth. Genes Dev. 25, 717-729
29. Lock, R., Roy, S., Kenific, C. M., Su, J. S., Salas, E., Ronen, S. M., and Debnath, J. (2011) Autophagy facilitates glycolysis during Ras-mediated oncogenic transformation. Mol. Biol. Cell 22, 165-178
30. Kon, M., Kiffin, R., Koga, H., Chapochnick, J., Macian, F., Varticovski, L., and Cuervo, A. M. (2011) Chaperone-mediated autophagy is required for tumor growth. Sci. Transl. Med. 3, 109ra117
31. Castets, P., Lin, S., Rion, N., Di Fulvio, S., Romanino, K., Guridi, M., Frank, S., Tintignac, L. A., Sinnreich, M., and Ruegg, M. A. (2013) Sustained activation of mTORC1 in skeletal muscle inhibits constitutive and starvation-induced autophagy and causes a severe, late-onset myopathy. Cell Metab. 17, 731-744
32. Klionsky, D. J., Abdalla, F. C., Abeliovich, H., Abraham, R. T., Acevedo-Arozena, A., Adeli, K., Agholme, L., Agnello, M., Agostinis, P., Aguirre-Ghiso, J. A., Ahn, H. J., Ait-Mohamed, O., Ait-Si-Ali, S., Akematsu, T., Akira, S., Al-Younes, H. M., Al-Zeer, M. A., Albert, M. L., Albin, R. L., Alegre-Abarrategui, J., Aleo, M. F., Alirezaei, M., Almasan, A., Almonte-Becerril, M., Amano, A., Amaravadi, R., Amarnath, S., Amer, A.O., Andrieu-Abadie, N., Anantharam, V., Ann, D. K., Anoopkumar-Dukie, S., Aoki, H., Apostolova, N., Arancia, G., Aris, J. P., Asanuma, K., Asare, N. Y., Ashida, H., Askanas, V., Askew, D. S., Auberger, P., Baba, M., Backues, S. K., Baehrecke, E. H., Bahr, B. A., Bai X. Y., Bailly, Y., Baiocchi, R., Baldini, G., Balduini, W., et al. (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8, 445-544
33. Lu, Z. H., Shvartsman, M. B., Lee, A. Y., Shao, J. M., Murray, M. M., Kladney, R. D., Fan, D., Krajewski, S., Chiang, G. G., Mills, G. B., and Arbeit, J. M. (2010) Mammalian target of rapamycin activator RHEB is frequently overexpressed in human carcinomas and is critical and sufficient for skin epithelial carcinogenesis. Cancer Res. 70, 3287-3298
34. Zoncu, R., Efeyan, A., and Sabatini, D. M. (2011) mTOR. From growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol. 12, 21-35
35. Dowling, R. J., Topisirovic, I., Alain, T., Bidinosti, M., Fonseca, B. D., Petroulakis, E., Wang, X., Larsson, O., Selvaraj, A., Liu, Y., Kozma, S. C., Thomas, G., and Sonenberg, N. (2010) mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science 328, 1172-1176
36. Guertin, D. A., and Sabatini, D. M. (2007) Defining the role of mTOR in cancer. Cancer Cell 12, 9-22
37. Ju, X., Katiyar, S., Wang, C., Liu, M., Jiao, X., Li, S., Zhou, J., Turner, J., Lisanti, M. P., Russell, R. G., Mueller, S. C., Ojeifo, J., Chen, W. S., Hay, N., and Pestell, R. G. (2007) Akt1 governs breast cancer progression in vivo. Proc. Natl. Acad. Sci. U.S.A. 104, 7438-7443
38. Chakraborty, S., Mohiyuddin, S. M., Gopinath, K. S., and Kumar, A. (2008) Involvement of TSC genes and differential expression of other members of the mTOR signaling pathway in oral squamous cell carcinoma. BMC Cancer 8, 163
39. Mathew, R., Karp, C. M., Beaudoin, B., Vuong, N., Chen, G., Chen, H. Y., Bray, K., Reddy, A., Bhanot, G., Gelinas, C., Dipaola, R. S., Karantza-Wadsworth, V., and White, E. (2009) Autophagy suppresses tumorigenesis through elimination of p62. Cell 137, 1062-1075
40. Takamura, A., Komatsu, M., Hara, T., Sakamoto, A., Kishi, C., Waguri, S., Eishi, Y., Hino, O., Tanaka, K., and Mizushima, N. (2011) Autophagydeficient mice develop multiple liver tumors. Genes Dev. 25, 795-800
41. Annibaldi, A., and Widmann, C. (2010) Glucose metabolism in cancer cells. Curr. Opin. Clin. Nutr. Metab. Care 13, 466-470
42. Shaw, R. J. (2006) Glucose metabolism and cancer. Curr. Opin. Cell Biol. 18, 598-608
43. Amaravadi, R. K. (2011) Cancer. Autophagy in tumor immunity. Science 334, 1501-1502