Molecular symbiosis of CHOP and C/EBPβ isoform LIP contributes to endoplasmic reticulum stress-induced apoptosis

Molecular and Cellular Biology

Volumn 30, Issue 14, 2010, Pages 3722-3731

  Chiribau, Calin Bogdan ^a   Gaccioli, Francesca ^a   Huang, Charlie C ^a   Yuan, Celvie L ^a   Hatzoglou, Maria ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CCAAT ENHANCER BINDING PROTEIN BETA; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; ISOPROTEIN; PROTEASOME;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; CYTOPLASM; DNA TRANSFECTION; EMBRYO; ENDOPLASMIC RETICULUM STRESS; ENZYME DEGRADATION; FIBROBLAST; FLUORESCENCE ACTIVATED CELL SORTING; GENE TRANSLOCATION; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; NUCLEAR IMPORT; NULL CELL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYMBIOSIS; TRANSCRIPTION INITIATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; APOPTOSIS; BASE SEQUENCE; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELLS, CULTURED; DNA PRIMERS; ENDOPLASMIC RETICULUM; MICE; PROTEIN ISOFORMS; RATS; RECOMBINANT PROTEINS; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTOR CHOP; TRANSFECTION;

EID: 77954366843     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01507-09     Document Type: Article

References (56)

1. Akira, S., H. Isshiki, T. Sugita, O. Tanabe, S. Kinoshita, Y. Nishio, T. Nakajima, T. Hirano, and T. Kishimoto. 1990. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J. 9:1897-1906.
2. Buck, M., L. Zhang, N. A. Halasz, T. Hunter, and M. Chojkier. 2001. Nuclear export of phosphorylated C/EBPβ mediates the inhibition of albumin expression by TNFα. EMBO J. 20:6712-6723.
3. Buck, M., V. Poli, T. Hunter, and M. Chojkier. 2001. C/EBPβ phosphorylation by RSK creates a functional XEXD caspase inhibitory box critical for cell survival. Mol. Cell 8:807-816.
4. Cao, Z., R. M. Umek, and S. L. McKnight. 1991. Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes Dev. 5:1538-1552.
5. Descombes, P., and U. Schibler. 1991. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 67:569-579.
6. Descombes, P., M. Chojkier, S. Lichtsteiner, E. Falvey, and U. Schibler. 1990. LAP, a novel member of the C/EBP gene family, encodes a liver-enriched transcriptional activator protein. Genes Dev. 4:1541-1551.
7. Fan, H.-Y., Z. Liu, M. Shimada, E. Sterneck, P. F. Johnson, S. M. Hedrick, and J. S. Richards. 2009. MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science 324:938-941.
8. Fawcett, T. W., H. B. Eastman, J. L. Martindale, and N. J. Holbrook. 1996. Physical and functional association between GADD153 and CCAAT/enhancer-binding protein β during cellular stress. J. Biol. Chem. 271:14285-14289.
9. Floyd, Z. E., J. S. Trausch-Azar, E. Reinstein, A. Ciechanover, and A. L. Schwartz. 2001. The nuclear ubiquitin-proteasome system degrades MyoD. J. Biol. Chem. 276:22468-22474.
10. Fornerod, M., M. Ohno, M. Yoshida, and I. W. Mattaj. 1997. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90:1051-1060.
11. Freedman, D. A., and A. J. Levine. 1998. Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol. Cell. Biol. 18:7288-7293.
12. Halterman, M. W., C. De Jesus, D. A. Rempe, N. F. Schor, and H. J. Federoff. 2008. Loss of c/EBP-beta activity promotes the adaptive to apoptotic switch in hypoxic cortical neurons. Mol. Cell Neurosci. 38:125-137.
13. Harding, H. P., I. Novoa, Y. Zhang, R. Wek, M. Schapira, and D. Ron. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6:1099-1108.
14. Hata, K., R. Nishimura, M. Ueda, F. Ikeda, T. Matsubara, F. Ichida, K. Hisada, T. Nokubi, A. Yamaguchi, and T. Yoneda. 2005. A CCAAT/ enhancer binding protein beta isoform, liver-enriched inhibitory protein, regulates commitment of osteoblasts and adipocytes. Mol. Cell. Biol. 25:1971-1979.
15. Hattori, T., N. Ohoka, H. Hayashi, and K. Onozaki. 2003. C/EBP homologous protein (CHOP) up-regulates IL-6 transcription by trapping negative regulating NF-IL6 isoform. FEBS Lett. 541:33-39.
16. Hattori, T., N. Ohoka, Y. Inoue, H. Hayashi, and K. Onozaki. 2003. C/EBP family transcription factors are degraded by the proteasome but stabilized by forming dimer. Oncogene 22:1273-1280.
17. Haze, K., H. Yoshida, H. Yanagi, T. Yura, and K. Mori. 1999. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 10:3787-3799.
18. Heckman, C. A., M. A. Wheeler, and L. M. Boxer. 2003. Regulation of Bcl-2 expression by C/EBP in t(14;18) lymphoma cells. Oncogene 22:7891-7899.
19. Hetz, C., P. Bernasconi, J. Fisher, A. H. Lee, M. C. Bassik, B. Antonsson, G. S. Brandt, N. N. Iwakoshi, A. Schinzel, L. H. Glimcher, and S. J. Korsmeyer. 2006. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1α. Science 312:572-576.
20. Huang, C. C., C. B. Chiribau, M. Majumder, C. M. Chiang, R. C. Wek, R. J. Kelm, K. Khalili, M. D. Snider, and M. Hatzoglou. 2009. A bifunctional intronic element regulates the expression of the arginine/lysine transporter Cat-1 via mechanisms involving the purine-rich element binding protein A (Purα). J. Biol. Chem. 284:32312-32320.
21. Huang, C. J., C. Y. Lin, L. Haataja, T. Gurlo, A. E. Butler, R. A. Rizza, and P. C. Butler. 2007. High expression rates of human islet amyloid polypeptide induce endoplasmic reticulum stress mediated β-cell apoptosis, a characteristic of humans with type 2 but not type 1 diabetes. Diabetes 56:2016-2027.
22. Hungness, E. S., B. W. Robb, G. J. Luo, T. A. Protts, D. D. Hershko, and P. O. Hasselgren. 2002. Proteasome inhibitors activate the transcription factors C/EBP-β and -δ in human intestinal epithelial cells. Biochem. Biophys. Res. Commun. 290:469-474.
23. Jiang, H.-Y., S. A. Wek, B. C. McGrath, D. Lu, T. Hai, H. P. Harding, X. Wang, D. Ron, D. R. Cavener, and R. C. Wek. 2004. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol. Cell. Biol. 24:1365-1377.
24. Kuang, P. P., and R. H. Goldstein. 2005. Regulation of elastin gene transcription by proteasome dysfunction. Am. J. Physiol. Cell. Physiol. 279:766-773.
25. Li, Y., E. Bevilaqua, C. B. Chiribau, M. Majumder, C. Wang, C. M. Croniger, M. D. Snider, P. F. Johnson, and M. Hatzoglou. 2008. Differential control of the C/EBPβ products LAP and LIP and the regulation of gene expression during the response to endoplasmic reticulum stress. J. Biol. Chem. 283: 22443-22456.
26. Ma, Y., J. W. Brewer, J. A. Diehl, and L. M. Hendershot. 2002. Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318:1351-1365.
27. Marciniak, S. J., C. Y. Yun, S. Oyadomari, I. Novoa, Y. Zhang, R. Jungreis, K. Nagata, H. P. Harding, and D. Ron. 2004. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 18:3066-3077.
28. McBride, K. M., G. Banninger, C. McDonald, and N. C. Reich. 2002. Regulated nuclear import of the STAT1 transcription factor by direct binding of importin. EMBO J. 21:1754-1763.
29. McCullough, K. D., J. L. Martindale, L.-O. Klotz, T.-Y. Aw, and N. J. Holbrook. 2001. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 21:1249-1259.
30. Mehmood, R., N. Yasuhara, S. Oe, M. Nagai, and Y. Yoneda. 2009. Synergistic nuclear import of NeuroD1 and its partner transcription factor, E47, via heterodimerization. Exp. Cell Res. 315:1639-1652.
31. Ohoka, N., S. Yoshii, T. Hattori, K. Kitagawa, K. Onozaki, and H. Hayashi. 2005. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J. 24:1243-1255.
32. Ohoka, N., T. Hattori, K. Kitagawa, K. Onozaki, and H. Hayashi. 2007. Critical and functional regulation of CHOP (C/EBP homologous protein) through the N-terminal portion. J. Biol. Chem. 282:35687-35694.
33. Oyadomari, S., and M. Mori. 2004. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11:381-389.
34. Puthalakath, H., L. A. O'Reilly, P. Gunn, L. Lee, P. N. Kelly, N. D. Huntington, P. D. Hughes, E. M. Michalak, J. McKimm-Breschkin, N. Motoyama, T. Gotoh, S. Akira, P. Bouillet, and A. Strasser. 2007. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129:1337-1349.
35. Ramji, D. P., and Foka, P. 2002. CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem. J. 365:561-575.
36. Rivett, A. J., A. Palmer, and E. Knecht. 1992. Electron microscopic localization of the multicatalytic proteinase complex in rat liver and in cultured cells. J. Histochem. Cytochem. 40:1165-1172.
37. Ron, D., and J. F. Habener. 1992. CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBPβ and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev. 6:439-453.
38. Rutkowski, T., and R. J. Kaufman. 2004. A trip to the ER: coping with stress. Trends Cell Biol. 14:20-28.
39. Smink, J. J., V. Bégay, T. Schoenmaker, E. Sterneck, T. J. de Vries, and A. Leutz. 2009. Transcription factor C/EBPβ isoform ratio regulates osteoclastogenesis through MafB. EMBO J. 28:1769-1781.
40. Sprott, K. M., M. J. Chumley, J. M. Hanson, and R. T. Dobrowsky. 2002. Decreased activity and enhanced nuclear export of CCAAT-enhancer-binding protein beta during inhibition of adipogenesis by ceramide. Biochem. J. 365:181-191.
41. Su, N., and M. S. Kilberg. 2008. C/EBP homology protein (CHOP) interacts with activating transcription factor 4 (ATF4) and negatively regulates the stress-dependent induction of the asparagine synthetase gene. J. Biol. Chem. 283:35106-35117.
42. Tsai, B., Y. Ye, and T. A. Rapoport. 2002. Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat. Rev. Mol. Cell. Biol. 3:246-255.
43. Ubeda, M., X.-Z. Wang, H. Zinszner, I. Wo, J. F. Habener, and D. Ron. 1996. Stress-induced binding of the transcriptional factor CHOP to a novel DNA control element. Mol. Cell. Biol. 16:1479-1489.
44. Vallejo, M., D. Ron, C. P. Miller, and J. F. Habener. 1993. C/ATF, a member of the activating transcription factor family of DNA-binding proteins, dimerizes with CAAT/enhancer-binding proteins and directs their binding to cAMP response elements. Proc. Natl. Acad. Sci. U. S. A. 90:4679-4683.
45. von Mikecz, A. 2006. The nuclear ubiquitin-proteasome system. J. Cell Sci. 119:1977-1984.
46. Wang, X.-Z., B. Lawson, J. W. Brewer, H. Zinszner, A. Sanjay, L.-M. Mi, R. Boorstein, G. Kreibich, L. M. Hendershot, and D. Ron. 1996. Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol. Cell. Biol. 16:4273-4280.
47. Wang, X.-Z., M. Kuroda, J. Sok, N. Batchvarova, R. Kimmel, P. Chung, H. Zinszner, and D. Ron. 1998. Identification of novel stress-induced genes downstream of chop. EMBO J. 17:3619-3630.
48. Wei, W., H. Yang, M. Menconi, P. Cao, C. E. Chamberlain, and P. O. Hasselgren. 2007. Treatment of cultured myotubes with the proteasome inhibitor beta-lactone increases the expression of the transcription factor C/EBPβ. Am. J. Cell Physiol. 292:216-226.
49. Wei, W., H. Yang, M. Menconi, P. Cao, C. E. Chamberlain, V. Petkova, and P. O. Hasselgren. 2006. Degradation of C/EBPβ in cultured myotubes is calpain dependent. J. Cell Physiol. 208:386-398.
50. Yeh, W. C., Z. Cao, M. Classon, and S. L. McKnight. 1995. Cascade regulation of terminal adipocyte differentiation by three members of the C/EBP family of leucine zipper proteins. Genes Dev. 9:168-181.
51. Yoon, K., S. Zhu, S. J. Ewing, and R. C. Smart. 2007. Decreased survival of C/EBPβ-deficient keratinocytes is due to aberrant regulation of p53 levels and function. Oncogene 26:360-367.
52. Yoshida, H. 2007. ER stress and diseases. FEBS J. 274:630-658.
53. Yoshida, H., T. Matsui, A. Yamamoto, T. Okada, and K. Mori. 2001. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:881-891.
54. Zahnow, C. A. 2009. CCAAT/enhancer-binding protein beta: its role in breast cancer and associations with receptor tyrosine kinases. Expert Rev. Mol. Med. 11:e12.
55. Zahnow, C. A., R. D. Cardiff, R. Laucirica, D. Medina, and J. M. Rosen. 2001. A role for CCAAT/enhancer binding protein beta-liver-enriched inhibitory protein in mammary epithelial cell proliferation. Cancer Res. 61: 261-269.
56. Zinszner, H., M. Kuroda, X. Wang, N. Batchvarova, R. T. Lightfoot, H. Remotti, J. L. Stevens, and D. Ron. 1998. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12:982-995.