C/EBPγ suppresses senescence and inflammatory gene expression by heterodimerizing with C/EBPβ

Molecular and Cellular Biology

Volumn 33, Issue 16, 2013, Pages 3242-3258

  Huggins, Christopher J ^a   Malik, Radek ^a,c   Lee, Sook ^a   Salotti, Jacqueline ^a   Thomas, Sara ^a   Martin, Nancy ^a   Quiñones, Octavio A ^b   Alvord, W Gregory ^b   Olanich, Mary E ^a,d   Keller, Jonathan R ^a   Johnson, Peter F ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^c INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CCAAT ENHANCER BINDING PROTEIN; CCAAT ENHANCER BINDING PROTEIN BETA; CCAAT ENHANCER BINDING PROTEIN GAMMA; CYCLIN D1; PROTEIN P53; THROMBOSPONDIN 1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CARCINOGENICITY; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL DENSITY; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOSTASIS; DIMERIZATION; DNA BINDING; EMBRYO; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE INDUCTION; GENOTYPE; HETEROZYGOSITY; HUMAN; HUMAN CELL; MOUSE; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PROCESSING; RECURRENCE FREE SURVIVAL; SENESCENCE;

ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CCAAT-ENHANCER-BINDING PROTEINS; CELL AGING; CELL CYCLE; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; FIBROBLASTS; GENE DELETION; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; INFLAMMATION; MICE; MICE, INBRED C57BL; NEOPLASMS; NIH 3T3 CELLS; PROTEIN MULTIMERIZATION;

EID: 84881278255     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01674-12     Document Type: Article

References (47)

1. Campisi J. 2005. Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120:513-522.
2. Kuilman T, Michaloglou C, Mooi WJ, Peeper DS. 2010. The essence of senescence. Genes Dev. 24:2463-2479.
3. Lowe SW, Cepero E, Evan G. 2004. Intrinsic tumour suppression. Nature 432:307-315.
4. Coppe J-P, Desprez P-Y, Krtolica A, Campisi J. 2010. The senescenceassociated secretory phenotype: the dark side of tumor suppression. Annu. Rev. Pathol. 5:99-118.
5. Kang TW, Yevsa T, Woller N, Hoenicke L, Wuestefeld T, Dauch D, Hohmeyer A, Gereke M, Rudalska R, Potapova A, Iken M, Vucur M, Weiss S, Heikenwalder M, Khan S, Gil J, Bruder D, Manns M, Schirmacher P, Tacke F, Ott M, Luedde T, Longerich T, Kubicka S, Zender L. 2011. Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature 479:547-551.
6. Acosta JC, O'Loghlen A, Banito A, Guijarro MV, Augert A, Raguz S, Fumagalli M, Da Costa M, Brown C, Popov N, Takatsu Y, Melamed J, d'Adda di Fagagna F, Bernard D, Hernando E, Gil J. 2008. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 133:1006- 1018.
7. Kuilman T, Michaloglou C, Vredeveld LC, Douma S, van Doorn R, Desmet CJ, Aarden LA, Mooi WJ, Peeper DS. 2008. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 133:1019-1031.
8. Basu SK, Malik R, Huggins CJ, Lee S, Sebastian T, Sakchaisri K, Quinones OA, Alvord WG, Johnson PF. 2011. 3=UTR elements inhibit Ras-induced C/EBPbeta post-translational activation and senescence in tumour cells. EMBO J. 30:3714-3728.
9. Chien Y, Scuoppo C, Wang X, Fang X, Balgley B, Bolden JE, Premsrirut P, Luo W, Chicas A, Lee CS, Kogan SC, Lowe SW. 2011. Control of the senescence-associated secretory phenotype by NF-kappaB promotes senescence and enhances chemosensitivity. Genes Dev. 25:2125-2136.
10. Rodier F, Coppe JP, Patil CK, Hoeijmakers WA, Munoz DP, Raza SR, Freund A, Campeau E, Davalos AR, Campisi J. 2009. Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat. Cell Biol. 11:973-979.
11. Sebastian T, Malik R, Thomas S, Sage J, Johnson PF. 2005. C/EBPbeta cooperates with RB:E2F to implement Ras(V12)-induced cellular senescence. EMBO J. 24:3301-3312.
12. Parkin SE, Baer M, Copeland TD, Schwartz RC, Johnson PF. 2002. Regulation of CCAAT/enhancer-binding protein (C/EBP) activator proteins by heterodimerization with C/EBPgamma (Ig/EBP). J. Biol. Chem. 277:23563-23572.
13. Cooper C, Henderson A, Artandi S, Avitahl N, Calame K. 1995. Ig/EBP (C/EBP gamma) is a transdominant negative inhibitor of C/EBP family transcriptional activators. Nucleic Acids Res. 23:4371-4377.
14. Thomassin H, Hamel D, Bernier D, Guertin M, Belanger L. 1992. Molecular cloning of two C/EBP-related proteins that bind to the promoter and the enhancer of the alpha 1-fetoprotein gene. Further analysis of C/EBP beta and C/EBP gamma. Nucleic Acids Res. 20:3091-3098.
15. Lee S, Shuman JD, Guszczynski T, Sakchaisri K, Sebastian T, Copeland TD, Miller M, Cohen MS, Taunton J, Smart RC, Xiao Z, Yu L-R, Veenstra TD, Johnson PF. 2010. RSK-mediated phosphorylation in the C/EBP{beta} leucine zipper regulates DNA binding, dimerization, and growth arrest activity. Mol. Cell. Biol. 30:2621-2635.
16. Kaisho T, Tsutsui H, Tanaka T, Tsujimura T, Takeda K, Kawai T, Yoshida N, Nakanishi K, Akira S. 1999. Impairment of natural killer cytotoxic activity and interferon gamma production in CCAAT/enhancer binding protein gamma-deficient mice. J. Exp. Med. 190:1573-1582.
17. Bakiri L, Matsuo K, Wisniewska M, Wagner EF, Yaniv M. 2002.Promoter specificity and biological activity of tethered AP-1 dimers. Mol. Cell. Biol. 22:4952-4964.
18. Gao H, Parkin S, Johnson PF, Schwartz RC. 2002. C/EBP gamma has a stimulatory role on the IL-6 and IL-8 promoters. J. Biol. Chem. 277: 38827-38837.
19. Chen Z, Torrens JI, Anand A, Spiegelman BM, Friedman JM. 2005. Krox20 stimulates adipogenesis via C/EBPbeta-dependent and -independent mechanisms. Cell Metab. 1:93-106.
20. Kajimura S, Seale P, Kubota K, Lunsford E, Frangioni JV, Gygi SP, Spiegelman BM. 2009. Initiation of myoblast to brown fat switch by a PRDM16-C/EBP-beta transcriptional complex. Nature 460:1154-1158.
21. Reuter JS, Mathews DH. 2010. RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics 11:129.
22. Todaro GJ, Green H. 1963. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17:299-313.
23. Berthet C, Aleem E, Coppola V, Tessarollo L, Kaldis P. 2003. Cdk2 knockout mice are viable. Curr. Biol. 13:1775-1785.
24. Baer M, Johnson PF. 2000. Generation of truncated C/EBP isoforms by in vitro proteolysis. J. Biol. Chem. 275:26582-26590.
25. Lee S, Miller M, Shuman JD, Johnson PF. 2010. CCAAT/enhancerbinding protein beta DNA binding is auto-inhibited by multiple elements that also mediate association with p300/CREB-binding protein (CBP). J. Biol. Chem. 285:21399-21410.
26. Mizuno H, Kitada K, Nakai K, Sarai A. 2009. PrognoScan: a new database for meta-analysis of the prognostic value of genes. BMC Med. Genomics 2:18.
27. Gentleman R, Carey V, Bates D, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini A, Sawitzki G, Smith C, Smyth G, Tierney L, Yang J, Zhang J. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5:R80.
28. R Development Core Team. 2010. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.
29. Sebastian T, Johnson PF. 2006. Stop and go: anti-proliferative and mitogenic functions of the transcription factor C/EBPbeta. Cell Cycle 5:953- 957.
30. Malek NP, Sundberg H, McGrew S, Nakayama K, Kyriakides TR, Roberts JM. 2001. A mouse knock-in model exposes sequential proteolytic pathways that regulate p27Kip1 in G1 and S phase. Nature 413:323- 327.
31. Bartek J, Hodny Z, Lukas J. 2008. Cytokine loops driving senescence. Nat. Cell Biol. 10:887-889.
32. Jun JI, Lau LF. 2010. Cellular senescence controls fibrosis in wound healing. Aging 2:627-631.
33. Krizhanovsky V, Yon M, Dickins RA, Hearn S, Simon J, Miething C, Yee H, Zender L, Lowe SW. 2008. Senescence of activated stellate cells limits liver fibrosis. Cell 134:657-667.
34. Descombes P, Schibler U. 1991. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 67:569-579.
35. Sebastian T, Johnson PF. 2009. RasV12-mediated down-regulation of CCAAT/enhancer binding protein {beta} in immortalized fibroblasts requires loss of p19Arf and facilitates bypass of oncogene-induced senescence. Cancer Res. 69:2588-2598.
36. Oelgeschlager M, Janknecht R, Krieg J, Schreek S, Luscher B. 1996. Interaction of the co-activator CBP with Myb proteins: effects on Mybspecific transactivation and on the cooperativity with NF-M. EMBO J. 15:2771-2780.
37. Akira S, Isshiki H, Sugita T, Tanabe O, Kinoshita S, Nishio Y, Nakajima T, Hirano T, Kishimoto T. 1990. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J. 9:1897-1906.
38. Roman C, Platero JS, Shuman J, Calame K. 1990. Ig/EBP-1: a ubiquitously expressed immunoglobulin enhancer binding protein that is similar to C/EBP and heterodimerizes with C/EBP. Genes Dev. 4:1404-1415.
39. Newman JR, Keating AE. 2003. Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science 300:2097-2101.
40. Atwood AA, Sealy L. 2010. Regulation of C/EBPbeta1 by Ras in mammary epithelial cells and the role of C/EBPbeta1 in oncogene-induced senescence. Oncogene 29:6004-6015.
41. Staiger J, Lueben MJ, Berrigan D, Malik R, Perkins SN, Hursting SD, Johnson PF. 2009. C/EBPbeta regulates body composition, energy balance- related hormones and tumor growth. Carcinogenesis 30:832-840.
42. Sterneck E, Zhu S, Ramirez A, Jorcano JL, Smart RC. 2006. Conditional ablation of C/EBP beta demonstrates its keratinocyte-specific requirement for cell survival and mouse skin tumorigenesis. Oncogene 25:1272- 1276.
43. Zahnow CA. 2009. CCAAT/enhancer-binding protein beta: its role in breast cancer and associations with receptor tyrosine kinases. Expert Rev. Mol. Med. 11:e12.
44. Zhu S, Yoon K, Sterneck E, Johnson PF, Smart RC. 2002. CCAAT/ enhancer binding protein-beta is a mediator of keratinocyte survival and skin tumorigenesis involving oncogenic Ras signaling. Proc. Natl. Acad. Sci. U. S. A. 99:207-212.
45. Alberich-Jorda M, Wouters B, Balastik M, Shapiro-Koss C, Zhang H, Di Ruscio A, Radomska HS, Ebralidze AK, Amabile G, Ye M, Zhang J, Lowers I, Avellino R, Melnick A, Figueroa ME, Valk PJ, Delwel R, Tenen DG. 2013. C/EBPgamma deregulation results in differentiation arrest in acute myeloid leukemia. J. Clin. Invest. 122:4490-4504.
46. Sherr CJ, DePinho RA. 2000. Cellular senescence: mitotic clock or culture shock? Cell 102:407-410.
47. Okayama H, Kohno T, Ishii Y, Shimada Y, Shiraishi K, Iwakawa R, Furuta K, Tsuta K, Shibata T, Yamamoto S, Watanabe S, Sakamoto H, Kumamoto K, Takenoshita S, Gotoh N, Mizuno H, Sarai A, Kawano S, Yamaguchi R, Miyano S, Yokota J. 2012,Identification of genes upregulated in ALK-positive and EGFR/KRAS/ALK-negative lung adenocarcinomas.Cancer Res.72, 100-111