The C/EBPbeta isoform, liver-inhibitory protein (LIP), induces autophagy in breast cancer cell lines

Experimental Cell Research

Volumn 316, Issue 19, 2010, Pages 3227-3238

  Abreu, Maria M ^a   Sealy, Linda ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autophagy; Breast cancer cells; C EBPbeta; Cell death; Transcription factor

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; DNA; ACID; CEBPB PROTEIN, HUMAN; ISOPROTEIN; LIGHT CHAIN 3, HUMAN; MICROTUBULE ASSOCIATED PROTEIN;

APOPTOSIS; ARTICLE; AUTOPHAGY; BREAST CANCER; CANCER CELL CULTURE; CELL CYCLE; CELL DEATH; CELL GROWTH; CELL ORGANELLE; CYTOPLASM; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; MONITORING; PRIORITY JOURNAL; PROTEIN EXPRESSION; BREAST TUMOR; CELL PROLIFERATION; CELL VACUOLE; CYTOPLASM VESICLE; FEMALE; METABOLISM; NECROSIS; PATHOLOGY; TUMOR CELL LINE; ULTRASTRUCTURE;

ACIDS; APOPTOSIS; AUTOPHAGY; BREAST NEOPLASMS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOPLASMIC VESICLES; FEMALE; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; NECROSIS; PROTEIN ISOFORMS; VACUOLES;

EID: 77958104025     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.07.021     Document Type: Article

References (40)

1. Levine B., Klionsky D.J. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 2004, 6:463-477.
2. Meijer A.J., Codogno P. Regulation and role of autophagy in mammalian cells. Int. J. Biochem. Cell Biol. 2004, 36:2445-2462.
3. Wang C.W., Klionsky D.J. The molecular mechanism of autophagy. Mol. Med. 2003, 9:65-76.
4. Gozuacik D., Kimchi A. Autophagy and cell death. Curr. Top. Dev. Biol. 2007, 78:217-245.
5. Hippert M.M., O'Toole P.S., Thorburn A. Autophagy in cancer: good, bad, or both?. Cancer Res. 2006, 66:9349-9351.
6. Polager S., Ofir M., Ginsberg D. E2F1 regulates autophagy and the transcription of autophagy genes. Oncogene 2008, 27:4860-4864.
7. Tasdemir E., Maiuri M.C., Orhon I., Kepp O., Morselli E., Criollo A., Kroemer G. p53 represses autophagy in a cell cycle-dependent fashion. Cell Cycle 2008, 7:3006-3011.
8. Crighton D., Wilkinson S., O'Prey J., Syed N., Smith P., Harrison P.R., Gasco M., Garrone O., Crook T., Ryan K.M. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 2006, 126:121-134.
9. Descombes P., Chojkier M., Lichtsteiner S., Falvey E., Schibler U. LAP, a novel member of the C/EBP gene family, encodes a liver-enriched transcriptional activator protein. Genes Dev. 1990, 4:1541-1551.
10. Descombes P., Schibler U. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 1991, 67:569-579.
11. Baer M., Johnson P.F. Generation of truncated C/EBPbeta isoforms by in vitro proteolysis. J. Biol. Chem. 2000, 275:26582-26590.
12. Duong D.T., Waltner-Law M.E., Sears R., Sealy L., Granner D.K. Insulin inhibits hepatocellular glucose production by utilizing liver-enriched transcriptional inhibitory protein to disrupt the association of CREB-binding protein and RNA polymerase II with the phosphoenolpyruvate carboxykinase gene promoter. J. Biol. Chem. 2002, 277:32234-32242.
13. Bundy L.M., Wells S., Sealy L. C/EBPbeta-2 confers EGF-independent growth and disrupts the normal acinar architecture of human mammary epithelial cells. Mol. Cancer 2005, 4:43.
14. Eaton E., Hanlon M., Bundy L., Sealy L. Characterization of C/EBPbeta isoforms in normal versus neoplastic mammary epithelial cells. J. Cell. Physiol. 2001, 189:91-105.
15. Cohen G.M. Caspases: the executioners of apoptosis. Biochem. J. 1997, 326:1-16.
16. Klionsky D.J., Cuervo A.M., Seglen P.O. Methods for monitoring autophagy from yeast to human. Autophagy 2007, 3:181-206.
17. Paglin S., Hollister T., Delohery T., Hackett N., McMahill M., Sphicas E., Domingo D., Yahalom J. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res. 2001, 61:439-444.
18. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y., Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000, 19:5720-5728.
19. Geng J., Klionsky D.J. The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. "Protein modifications: beyond the usual suspects" review series. EMBO Rep. 2008, 9:859-864.
20. Høyer-Hansen M., Jäättelä M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ. 2007, 14:1576-1582.
21. Li Y., Bevilacqua E., Chiribau C.B., Majumder M., Wang C., Croniger C.M., Snider M.D., Johnson P.F., Hatzoglou M. Differential control of the CCAAT/enhancer-binding protein beta (C/EBPbeta) products liver-enriched transcriptional activating protein (LAP) and liver-enriched transcriptional inhibitory protein (LIP) and the regulation of gene expression during the response to endoplasmic reticulum stress. J. Biol. Chem. 2008, 283:22443-22456.
22. Raught B., Gingras A.C., James A., Medina D., Sonenberg N., Rosen J.M. Expression of a translationally regulated, dominant-negative CCAAT/enhancer-binding protein beta isoform and up-regulation of the eukaryotic translation initiation factor 2 alpha are correlated with neoplastic transformation of mammary epithelial cells. Cancer Res. 1996, 56:4382-4386.
23. Zahnow C.A., Younes P., Laucirica R., Rosen J.M. Overexpression of C/EBPbeta-LIP, a naturally occurring, dominant-negative transcription factor, in human breast cancer. J. Natl. Cancer Inst. 1997, 89:1887-1891.
24. Zahnow C.A., Cardiff R.D., Laucirica R., Medina D., Rosen J.M. A role for CCAAT/enhancer binding protein beta-liver-enriched inhibitory protein in mammary epithelial cell proliferation. Cancer Res. 2001, 61:261-269.
25. Liang X.H., Jackson S., Seaman M., Brown K., Kempkes B., Hibshoosh H. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999, 402:672-676.
26. Qu X., Yu J., Bhagat G., Furuya N., Hibshoosh H., Troxel A., Rosen J., Eskelinen E.L., Mizushima N., Ohsumi Y., Cattoretti G., Levine B. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 2003, 112:1809-1820.
27. Mariño G., Salvador-Montoliu N., Fueyo A., Knecht E., Mizushima N., López-Otín C. Tissue-specific autophagy alterations and increased tumorigenesis in mice deficient in Atg4C/autophagin-3. J. Biol. Chem. 2007, 282:18573-18583.
28. Williams A., Jahreiss L., Sarkar S., Saiki S., Menzies F.M., Ravikumar B., Rubinsztein D.C. Aggregate-prone proteins are cleared from the cytosol by autophagy: therapeutic implications. Curr. Top. Dev. Biol. 2006, 76:89-101.
29. Mathew R., Kongara S., Beaudoin B., Karp C.M., Bray K., Degenhardt K., Chen G., Jin S., White E. Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev. 2007, 21:1367-1381.
30. Degenhardt K., Mathew R., Beaudoin B., Bray K., Anderson D., Chen G., Mukherjee C., Shi Y., Gélinas C., Fan Y., Nelson D.A., Jin S., White E. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006, 10:51-64.
31. Grimm S.L., Rosen J.M. The role of C/EBPbeta in mammary gland development and breast cancer. J. Mammary Gland Biol. Neoplasia 2003, 8:191-204.
32. Watson C.J., Khaled W.T. Mammary development in the embryo and adult: a journey of morphogenesis and commitment. Development 2008, 135:995-1003.
33. Zarzynska J., Motyl T. Apoptosis and autophagy in involuting bovine mammary gland. J. Physiol. Pharmacol. 2008, 9:275-288.
34. Gajewska M., Sobolewska A., Kozlowski M., Motyl T. Role of autophagy in mammary gland development. J. Physiol. Pharmacol. 2008, 9:237-249.
35. Robinson G.W., Johnson P.F., Hennighausen L., Sterneck E. The C/EBPbeta transcription factor regulates epithelial cell proliferation and differentiation in the mammary gland. Genes Dev. 1998, 12:1907-1916.
36. Seagroves T.N., Krnacik S., Raught B., Gay J., Burgess-Beusse B., Darlington G.J., Rosen J.M. C/EBPbeta, but not C/EBPalpha, is essential for ductal morphogenesis, lobuloalveolar proliferation, and functional differentiation in the mouse mammary gland. Genes Dev. 1998, 12:1917-1928.
37. Meir O., Dvash E., Werman A., Rubinstein M. C/EBP-beta regulates endoplasmic reticulum stress-triggered cell death in mouse and human models. PLoS ONE 2010, 5:e9516.
38. Copetti T., Bertoli C., Dalla E., Demarchi F., Schneider C. p65/RelA modulates BECN1 transcription and autophagy. Mol. Cell. Biol. 2009, 29:2594-2608.
39. Li D.D., Wang L.L., Deng R., Tang J., Shen Y., Guo J.F., Wang Y., Xia L.P., Feng G.K., Liu Q.Q., Huang W.L., Zeng Y.X., Zhu X.F. The pivotal role of c-Jun NH2-terminal kinase-mediated Beclin 1 expression during anticancer agents-induced autophagy in cancer cells. Oncogene 2009, 28:886-898.
40. Degryse B., Bonaldi T., Scaffidi P., Muller S., Resnati M., Sanvito F., Arrigoni G., Bianchi M.E. The High Mobility Group (HMB) boxes of the nuclear protein HMG1 induce chemotaxis and cytoskeleton reorganization in rat smooth muscle cells. J. Cell Biol. 2001, 152:1197-1206.