Induction of autophagy during extracellular matrix detachment promotes cell survival

Molecular Biology of the Cell

Volumn 19, Issue 3, 2008, Pages 797-806

  Fung, Christopher ^a   Lock, Rebecca ^a,b   Gao, Sizhen ^c   Salas, Eduardo ^a   Debnath, Jayanta ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; EPIDERMAL GROWTH FACTOR; PROTEIN BCL 2;

ANOIKIS; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL SURVIVAL; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA INTERFERENCE;

ANIMALS; APOPTOSIS; AUTOPHAGY; CELL ADHESION; CELL LINE; CELL SURVIVAL; DOGS; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; FIBROBLASTS; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTOR, EPIDERMAL GROWTH FACTOR; UBIQUITIN-ACTIVATING ENZYMES;

EID: 41449109334     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-10-1092     Document Type: Article

References (50)

1. Boya, P. et al. (2005). Inhibition of macroautophagy triggers apoptosis. Mol. Cell Biol. 25, 1025-1040.
2. Chambers, A. F., Groom, A. C., and MacDonald, I. C. (2002). Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2, 563-572.
3. Debnath, J., Baehrecke, E. H., and Kroemer, G. (2005). Does autophagy contribute to cell death? Autophagy 1, e10-e18.
4. Debnath, J., and Brugge, J. S. (2005). Modelling glandular epithelial cancers in three-dimensional cultures. Nat. Rev. Cancer 5, 675-688.
5. Debnath, J., Mills, K. R., Collins, N. L., Reginato, M. J., Muthuswamy, S. K., and Brugge, J. S. (2002). The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 111, 29-40.
6. Debnath, J., Muthuswamy, S. K., and Brugge, J. S. (2003). Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30, 256-268.
7. Degenhardt, K. et al. (2006). Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10, 51-64.
8. Edick, M. J., Tesfay, L., Lamb, L. E., Knudsen, B. S., and Miranti, C. K. (2007). Inhibition of integrin-mediated crosstalk with EGFR/Erk or Src signaling pathways in autophagic prostate epithelial cells induces caspase-independent death. Mol. Biol. Cell 18, 2481-2490.
9. Frisch, S. M. (1999). Methods for studying anoikis. Methods Mol. Biol. 129, 251-256.
10. Frisch, S. M., and Francis, H. (1994). Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124, 619-626.
11. Gilmore, A. P. (2005). Anoikis. Cell Death Differ. 12 (suppl 2), 1473-1477.
12. Hoyer-Hansen, M. et al. (2007). Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol. Cell 25, 193-205.
13. Inbal, B., Bialik, S., Sabanay, I., Shani, G., and Kimchi, A. (2002). DAP kinase and DRP-1 mediate membrane blebbing and the formation of autophagic vesicles during programmed cell death. J. Cell Biol. 157, 455-468.
14. Jin, S., DiPaola, R. S., Mathew, R., and White, E. (2007). Metabolic catastrophe as a means to cancer cell death. J. Cell Sci. 120, 379-383.
15. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., and Yoshimori, T. (2000). LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728.
16. Karantza-Wadsworth, V., Patel, S., Kravchuk, O., Chen, G., Mathew, R., Jin, S., and White, E. (2007). Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev. 21, 1621-1635.
17. Katsumi, A., Orr, A. W., Tzima, E., and Schwartz, M. A. (2004). Integrins in mechanotransduction. J. Biol. Chem. 279, 12001-12004.
18. Klionsky, D. J. et al. (2003). A unified nomenclature for yeast autophagy-related genes. Dev. Cell 5, 539-545.
19. Kouroku, Y., Fujita, E., Tanida, I., Ueno, T., Isoai, A., Kumagai, H., Ogawa, S., Kaufman, R. J., Kominami, E., and Momoi, T. (2007). ER stress (PERK/ eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ. 14, 230-239.
20. Kuma, A., Hatano, M., Matsui, M., Yamamoto, A., Nakaya, H., Yoshimori, T., Ohsumi, Y., Tokuhisa, T., and Mizushima, N. (2004). The role of autophagy during the early neonatal starvation period. Nature 432, 1032-1036.
21. Kuma, A., Matsui, M., and Mizushima, N. (2007). LC3, an autophagosome marker, can be incorporated into protein aggregates independent of autophagy: caution in the interpretation of LC3 localization. Autophagy 3, 323-328.
22. Lee, C. Y., and Baehrecke, E. H. (2001). Steroid regulation of autophagic programmed cell death during development. Development 128, 1443-1455.
23. Levine, B., and Klionsky, D. J. (2004). Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6, 463-477.
24. Levine, B., and Yuan, J. (2005). Autophagy in cell death: an innocent convict? J. Clin. Invest. 115, 2679-2688.
25. Liang, J. et al. (2007). The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nat. Cell Biol. 9, 218-224.
26. Liang, X. H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., and Levine, B. (1999). Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672-676.
27. Liu, Z. et al. (2006). Detachment-induced upregulation of XIAP and cIAP2 delays anoikis of intestinal epithelial cells. Oncogene 25, 7680-7690.
28. Lum, J. J., Bauer, D. E., Kong, M., Harris, M. H., Li, C., Lindsten, T., and Thompson, C. B. (2005). Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120, 237-248.
29. Martin, D. N., and Baehrecke, E. H. (2004). Caspases function in autophagic programmed cell death in Drosophila. Development 131, 275-284.
30. Mathew, R., Kongara, S., Beaudoin, B., Karp, C. M., Bray, K., Degenhardt, K., Chen, G., Jin, S., and White, E. (2007). Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev. 21, 1367-1381 [correction published in Genes Dev. (2007) 21, 1701].
31. Meley, D., Bauvy, C., Houben-Weerts, J. H., Dubbelhuis, P. F., Helmond, M. T., Codogno, P., and Meijer, A. J. (2006). AMP-activated protein kinase and the regulation of autophagic proteolysis. J. Biol. Chem. 281, 34870-34879.
32. Meredith, J. E., Jr., Fazeli, B., and Schwartz, M. A. (1993). The extracellular matrix as a cell survival factor. Mol. Biol. Cell 4, 953-961.
33. Mills, K. R., Reginato, M., Debnath, J., Queenan, B., and Brugge, J. S. (2004). Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) is required for induction of autophagy during lumen formation in vitro. Proc. Natl. Acad. Sci. USA 101, 3438-3443.
34. Miranti, C. K., and Brugge, J. S. (2002). Sensing the environment: a historical perspective on integrin signal transduction. Nat. Cell Biol. 4, E83-E90.
35. Ogata, M. et al. (2006). Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell Biol. 26, 9220-9231.
36. Ogier-Denis, E., and Codogno, P. (2003). Autophagy: a barrier or an adaptive response to cancer. Biochim. Biophys. Acta 1603, 113-128.
37. Pattingre, S., Tassa, A., Qu, X., Garuti, R., Liang, X. H., Mizushima, N., Packer, M., Schneider, M. D., and Levine, B. (2005). Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122, 927-939.
38. Petrovski, G., Zahuczky, G., Katona, K., Vereb, G., Martinet, W., Nemes, Z., Bursch, W., and Fesus, L. (2007). Clearance of dying autophagic cells of different origin by professional and non-professional phagocytes. Cell Death Differ. 14, 1117-1128.
39. Qu, X. et al. (2003). Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 112, 1809-1820.
40. Qu, X., Zou, Z., Sun, Q., Luby-Phelps, K., Cheng, P., Hogan, R. N., Gilpin, C., and Levine, B. (2007). Autophagy gene-dependent clearance of apoptotic cells during embryonic development. Cell 128, 931-946.
41. 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.
42. Rytomaa, M., Lehmann, K., and Downward, J. (2000). Matrix detachment induces caspase-dependent cytochrome c release from mitochondria: inhibition by PKB/Akt but not Raf signalling. Oncogene 19, 4461-4468.
43. Shimizu, S., Kanaseki, T., Mizushima, N., Mizuta, T., Arakawa-Kobayashi, S., Thompson, C. B., and Tsujimoto, Y. (2004). Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat. Cell Biol. 6, 1221-1228.
44. Talloczy, Z., Jiang, W., Virgin, H.W.T., Leib, D. A., Scheuner, D., Kaufman, R. J., Eskelinen, E. L., and Levine, B. (2002). Regulation of starvation- and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc. Natl. Acad. Sci. USA 99, 190-195.
45. Tanida, I., Minematsu-Ikeguchi, N., Ueno, T., and Kominami, E. (2005). Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1, 84-91.
46. Underwood, J. M., Imbalzano, K. M., Weaver, V. M., Fischer, A. H., Imbalzano, A. N., and Nickerson, J. A. (2006). The ultrastructure of MCF-10A acini. J. Cell Physiol. 208, 141-148.
47. Yan, S. R., Joseph, R. R., Rosen, K., Reginato, M. J., Jackson, A., Allaire, N., Brugge, J. S., Jobin, C., and Stadnyk, A. W. (2005). Activation of NF-kappaB following detachment delays apoptosis in intestinal epithelial cells. Oncogene 24, 6482-6491.
48. Yu, L., Alva, A., Su, H., Dutt, P., Freundt, E., Welsh, S., Baehrecke, E. H., and Lenardo, M. J. (2004). Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304, 1500-1502.
49. Yu, L., Wan, F., Dutta, S., Welsh, S., Liu, Z., Freundt, E., Baehrecke, E. H., and Lenardo, M. (2006). Autophagic programmed cell death by selective catalase degradation. Proc. Natl. Acad. Sci. USA 103, 4952-4957.
50. Yue, Z., Jin, S., Yang, C., Levine, A. J., and Heintz, N. (2003). Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl. Acad. Sci. USA 100, 15077-15082.