Phospho-ΔNp63α/NF-Y protein complex transcriptionally regulates DDIT3 expression in squamous cell carcinoma cells upon cisplatin exposure

Cell Cycle

Volumn 9, Issue 2, 2010, Pages 328-338

  Huang, Yiping ^a   Chuang, Alice Y ^a   Romano, Rose Anne ^b   Liégeois, Nanette J ^a   Sinha, Satrajit ^b   Trink, Barry ^a   Ratovitski, Edward ^a   Sidransky, David ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Downstream gene targets; p63; Phosphorylation; Platinum therapy; Squamous cell carcinomas; Transcriptional regulation

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 1; AURORA A KINASE; CELL CYCLE PROTEIN 20; CELL CYCLE PROTEIN 6; CISPLATIN; CLAUDIN 11; CYCLIN A2; CYCLIN B2; CYCLIN DEPENDENT KINASE 3 INHIBITOR; CYCLIN DEPENDENT KINASE 6; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 2C; DELTA NP63 ALPHA PROTEIN; DNA TOPOISOMERASE (ATP HYDROLYSING); G PROTEIN COUPLED RECEPTOR 54; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEAT SHOCK PROTEIN 70; HEAT SHOCK TRANSCRIPTION FACTOR 2; MATRIX METALLOPROTEINASE 28; METALLOPROTEINASE; NF YA TRANSCRIPTION FACTOR; NUCLEIC ACID BINDING PROTEIN; PLASMINOGEN ACTIVATOR; PROTEIN P73; SIRTUIN 1; STAT1 PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; UROCORTIN II; WNT2 PROTEIN; ANTINEOPLASTIC AGENT; ATM PROTEIN; CCAAT BINDING FACTOR; CELL CYCLE PROTEIN; DDIT3 PROTEIN, HUMAN; DNA BINDING PROTEIN; MESSENGER RNA; NFYA PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; TP63 PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN; TUMOR SUPPRESSOR PROTEIN;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CONTROLLED STUDY; DOWN REGULATION; DRUG EXPOSURE; GENE MUTATION; GENE TARGETING; GENETIC TRANSCRIPTION; HEAD AND NECK CANCER; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SQUAMOUS CELL CARCINOMA; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION; WILD TYPE; AMINO ACID SUBSTITUTION; GENE EXPRESSION REGULATION; GENETICS; HEAD AND NECK TUMOR; METABOLISM; MUTATION; PHOSPHORYLATION; PROTEIN DOMAIN;

AMINO ACID SUBSTITUTION; ANTINEOPLASTIC AGENTS; APOPTOSIS; CARCINOMA, SQUAMOUS CELL; CCAAT-BINDING FACTOR; CELL CYCLE PROTEINS; CISPLATIN; DNA-BINDING PROTEINS; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HUMANS; MUTATION; PHOSPHORYLATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN-SERINE-THREONINE KINASES; RNA, MESSENGER; TRANS-ACTIVATORS; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

EID: 74949113519     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.2.10432     Document Type: Article

References (71)

1. Zangen R, Ratovitski E, Sidransky D. DeltaNp63alpha levels correlate with clinical tumor response to cisplatin. Cell Cycle 2005; 4:1313-5.
2. Bonner JA, Harari PM, Giralt J, et al. Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N Engl J Med 2006; 354:567-78.
3. Appella E, Anderson C. Post-translational modifications and activation of p53 by genotoxic stresses. Eur J Biochem 2001; 268:2764-72.
4. Perez C, Pietenpol JA. Transcriptional programs regulated by p63 in normal epithelium and tumors. Cell Cycle 2007; 6:246-54.
5. Huang Y, Sen T, Nagpal JK, et al. ATM kinase is a master switch for the DeltaNp63alpha protein phosphorylation/ degradation in human head and neck squamous cell carcinoma cells upon DNA damage. Cell Cycle 2008; 7:2846-55.
6. Sakaguchi K, Herrera JE, Saito S, et al. DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes Dev 1998; 12:2831-41.
7. Holmberg CI, Tran SE, Eriksson JE, Sistonen L. Multisite phosphorylation provides sophisticated regulation of transcription factors. Trends Biochem Sci 2002; 27:619-27.
8. Ferdous A, O'Neal M, Nalley K, et al. Phosphorylation of the Gal4 DNA-binding domain is essential for activator mono-ubiquitylation and efficient promoter occupancy. Mol Biosyst 2008; 4:1116-25.
9. Bruck N, Vitoux D, Ferry C, et al. A coordinated phosphorylation cascade initiated by p38MAPK/MSK1 directs RARalpha to target promoters. EMBO J 2009; 28:34-47.
10. Krämer OH, Knauer SK, Greiner G, et al. A phosphorylation- acetylation switch regulates STAT1 signaling. Genes Dev 2009; 23:223-35.
11. Wu G, Osada M, Guo Z, et al. DeltaNp63alpha upregulates the Hsp70 gene in human cancer. Cancer Res 2005; 65:758-66.
12. Ghioni P, Bolognese F, Duijf PH, et al. Complex transcriptional effects of p63 isoforms: identification of novel activation and repression domains. Mol Cell Biol 2002; 22:8659-68.
13. Helton ES, Zhu J, Chen X. The unique NH2-terminally deleted (DeltaN) residues, the PXXP and PPXY motifs, are required for the transcriptional activity of the DeltaN variant of p63. J Biol Chem 2006; 281:2533-42.
14. Upadhyay S, Chatterjee A, Trink B, et al. TAp63gamma regulates hOGG1 and repair of oxidative damage in cancer cell lines. Biochem Biophys Res Commun 2007; 356:823-8.
15. Osada M, Nagakawa Y, Park H, et al. P63-specific activation of the BPAG-1e promoter. J. Invest. Derm 2005; 124:52-60.
16. Wu G, Nomoto S, Hoque M, et al. DeltaNp63alpha and TAp63alpha regulate transcription of genes with distinct biological functions in cancer and development. Cancer Res 2003; 63:2351-7.
17. Testa A, Donati G, Yan P, et al. Chromatin immunoprecipitation (ChIP) on chip experiments uncover a widespread distribution of NF-Y binding CCAAT sites outside of core promoters. J Biol Chem 2005; 280:13606-15.
18. Ceribelli M, Alcalay M, Viganò MA, Mantovani R. Repression of new p53 targets revealed by ChIP on chip experiments. Cell Cycle 2006; 5:1102-10.
19. Ortt K, Raveh E, Gat U, Sinha S. A chromatin immunoprecipitation screen in mouse keratinocytes reveals Runx1 as a direct transcriptional target of DeltaNp63. J Cell Biochem 2008; 104:1204-19.
20. Shaked H, Shiff I, Kott-Gutkowski M, Siegfried Z, Haupt Y, Simon I. Chromatin immunoprecipitation-on-chip reveals stress-dependent p53 occupancy in primary normal cells but not in established cell lines. Cancer Res 2008; 68:9671-7.
21. Mandic A, Hansson J, Linder S, Shoshan M. Cisplatin induces endoplasmic reticulum stress and nucleusindependent apoptotic signaling. J Biol Chem 2003; 278:9100-6.
22. Yoshida H, Okada T, Haze K, et al. Endoplasmic reticulum stress-induced formation of transcription factor complex ERSF including NF-Y (CBF) and activating transcription factors 6alpha and 6beta that activates the mammalian unfolded protein response. Mol Cell Biol 2001; 21:1239-48.
23. Wang XZ, Lawson B, Brewer JW, et al. Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol Cell Biol 1996; 16:4273-80.
24. Zinszner H, Kuroda M, Wang X, et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998; 12:982-95.
25. Collins GA, Tansey WP. The proteasome: a utility tool for transcription? Curr Opin Genet Dev 2006; 16:197-202.
26. Benhar M, Engelberg D, Levitzki A. Cisplatin-induced activation of the EGF receptor. Oncogene 2002; 21:8723-31.
27. Carrassa L, Broggini M, Erba E, Damia G. Chk1, but not Chk2, is involved in the cellular response to DNA damaging agents: differential activity in cells expressing or not p53. Cell Cycle 2004; 3:1177-81.
28. Furuya K, Ozaki T, Hanamoto T, et al. Stabilization of p73 by nuclear IkappaB kinase-alpha mediates cisplatin-induced apoptosis. J Biol Chem 2007; 282:18365-78.
29. Gately DP, Sharma A, Christen RD, Howell SB. Cisplatin and taxol activate different signal pathways regulating cellular injury-induced expression of GADD153. Br J Cancer 1996; 73:18-23.
30. He H, Soncin F, Grammatikakis N, et al. Elevated expression of heat shock factor (HSF) 2A stimulates HSF1-induced transcription during stress. J Biol Chem 2003; 278:35465-75.
31. Hogg D, Guidos C, Bailey D, et al. Cell cycle dependent regulation of the protein kinase TTK. Oncogene 1994; 9:89-96.
32. Kappes F, Fahrer J, Khodadoust MS, et al. DEK is a poly (ADP-ribose) acceptor in apoptosis and mediates resistance to genotoxic stress. Mol Cell Biol 2008; 28:3245-57.
33. Katula KS, Wright KL, Paul H, et al. Cyclin-dependent kinase activation and S-phase induction of the cyclin B1 gene are linked through the CCAAT elements. Cell Growth Differ 1997; 8:811-20.
34. Lanza M, Marinari B, Papoutsaki M, et al. Cross talks in the p53 family: DeltaNp63 is an anti-apoptotic target for DeltaNp73alpha and p53 gain-of-function mutants. Cell Cycle 2006; 5:1996-2004.
35. Leong CO, Vidnovic N, DeYoung MP, Sgroi D, Ellisen LW. The p63/p73 network mediates chemosensitivity to cisplatin in a biologically defined subset of primary breast cancers. J Clin Invest 2007; 117:1370-80.
36. Lee MY, Kim HJ, Kim MA, et al. Nek6 is involved in G2/M phase cell cycle arrest through DNA damage-nduced phosphorylation. Cell Cycle 2008; 7:2705-9.
37. Ma Y, Brewer JW, Diehl JA, Hendershot LM. Two distinct stress-signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J Mol Biol 2002; 318:1351-65.
38. Magan N, Szremska AP, Isaacs RJ, Stowell KM. Modulation of DNA topoisomerase IIalpha promoter activity by members of the Sp and NF-Y families of transcription factors. Biochem J 2003; 374:723-9.
39. Ostling P, Björk JK, Roos-Mattjus P, Mezger V, Sistonen L. Heat shock factor 2 (HSF2) contributes to inducible expression of hsp genes through interplay with HSF1. J Biol Chem 2007; 282:7077-86.
40. Pabla N, Huang S, Mi QS, Daniel R, Dong Z. ATRChk2 signaling in p53 activation and DNA damage response during cisplatin-induced apoptosis. J Biol Chem 2008; 283:6572-83.
41. Polci R, Peng A, Chen PL, Riley DJ, Chen Y. NIMArelated protein kinase 1 is involved early in the ionizing radiation-induced DNA damage response. Cancer Res 2004; 64:8800-3.
42. Petitjean A, Ruptier C, Tribollet V, et al. Properties of the six isoforms of p63: p53-like regulation in response to genotoxic stress and cross talk with DeltaNp73. Carcinogenesis 2008; 29:273-81.
43. Rai R, Phadnis A, Haralkar S, et al. Differential regulation of centrosome integrity by DNA damage response proteins. Cell Cycle 2008; 7:2225-33.
44. Rocco JW, Leong CO, Kuperwasser N, DeYoung MP, Ellisen LW. p63 mediates survival in squamous cell carcinoma by suppression of p73-dependent apoptosis. Cancer Cell 2006; 9:45-56.
45. Yamamoto K, Yoshida H, Kokame K, Kaufman RJ, Mori K. Differential contributions of ATF6 and XBP1 to the activation of endoplasmic reticulum stress-responsive cis-acting elements ERSE, UPRE and ERSEII. J Biochem 2004; 136:343-50.
46. Wei JH, Chou YF, Ou YH, Yeh YH, Tyan SW, Sun TP, et al. TTK/hMps1 participates in the regulation of DNA damage checkpoint response by phosphorylating CHK2 on threonine 68. J Biol Chem 2005; 280:7748-57.
47. Beretta C, Chiarelli A, Testoni B, Mantovani R, Guerrini L. Regulation of the cyclin-dependent kinase inhibitor p57Kip2 expression by p63. Cell Cycle 2005; 4:1625-31.
48. Candi E, Rufini A, Terrinoni A, et al. DeltaNp63 regulates thymic development through enhanced expression of FgfR2 and Jag2. Proc Natl Acad Sci USA 2007; 104:11999-20004.
49. Costanzo V, Robertson K, Ying CY, et al. Reconstitution of an ATM-dependent checkpoint that inhibits chromosomal DNA replication following DNA damage. Mol Cell 2000; 6:649-59.
50. Luo R, Lu JF, Hu Q, Maity SN. CBF/NF-Y controls endoplasmic reticulum stress induced transcription through recruitment of both ATF6 (N) and TBP. J Cell Biochem 2008; 104:1708-23.
51. Sun F, Xie Q, Ma J, Yang S, Chen Q, Hong A. Nuclear factor Y Is Required for Basal Activation and Chromatin Accessibility of Fibroblast Growth Factor Receptor 2 Promoter in Osteoblast-like Cells. J Biol Chem 2009; 284:3136-47.
52. Wilson LA, Yamamoto H, Singh G. Role of the transcription factor Ets-1 in cisplatin resistance. Mol Cancer Ther 2004; 3:823-32.
53. Imbriano C, Gurtner A, Cocchiarella F, et al. Direct p53 transcriptional repression: in vivo analysis of CCAAT-containing G2/M promoters. Mol Cell Biol 2005; 25:3737-51.
54. Benatti P, Basile V, Merico D, Fantoni LI, Tagliafico E, Imbriano C. A balance between NF-Y and p53 governs the pro- and anti-apoptotic transcriptional response. Nucl. Acids Res 2008; 36:1415-28.
55. Caretti G, Salsi V, Vecchi C, Imbriano C, Mantovani R. Dynamic recruitment of NF-Y and histone acetyl-transferases on cell cycle promoters. J Biol Chem 2003; 278:30435-40.
56. Donati G, Imbriano C, Mantovani R. Dynamic recruitment of transcription factors and epigenetic changes on the ER stress response gene promoters. Nucl. Acids Res 2006; 34:3116-27.
57. 2/M phase of the cell cycle. Nucl Acid Res 2006; 34:6272-85.
58. Kabe Y, Yamada J, Uga H, Yamaguchi Y, Wada T, Handa H. NF-Y is essential for the recruitment of RNA polymerase II and inducible transcription of several CCAAT box-containing genes. Mol Cell Biol 2005; 25:512-22.
59. Ubeda M, Habener JF. CHOP gene expression in response to endoplasmic-reticular stress requires NF-Y interaction with different domains of a conserved DNA-binding element. Nucl Acids Res 2000; 28:4987-97.
60. Bengoechea-Alonso MT, Ericsson J. A phosphorylation cascade controls the degradation of active SREBP1. J Biol Chem 2009; 284:5885-95.
61. Yoshida K, Ozaki T, Furuya K, et al. ATM-dependent nuclear accumulation of IKK-alpha plays an important role in the regulation of p73-mediated apoptosis in response to cisplatin. Oncogene 2008; 27:1183-8.
62. Hayakawa J, Mittal S, Wang Y, et al. Identification of promoters bound by c-Jun/ATF2 during rapid large-scale gene activation following genotoxic stress. Mol Cell 2004; 16:521-35.
63. Li QJ, Yang SH, Maeda Y, et al. MAP kinase phosphorylation-dependent activation of Elk-1 leads to activation of the co-activator p300. EMBO J 2003; 22:281-91.
64. Wu RC, Feng Q, Lonard DM, O'Malley BW. SRC-3 coactivator functional lifetime is regulated by a phospho-dependent ubiquitin time clock. Cell 2007; 129:1125-40.
65. Li C, Liang YY, Feng XH, et al. Essential phosphatases and a phospho-degron are critical for regulation of SRC-3/AIB1 coactivator function and turnover. Mol Cell 2008; 31:835-49.
66. Kim SY, Herbst A, Tworkowski KA, Salghetti SE, Tansey WP. Skp2 regulates Myc protein stability and activity. Mol Cell 2003; 11:1177-88.
67. Muratani M, Tansey WP. How the ubiquitin-proteasome system controls transcription. Nat Rev Mol Cell Biol 2003; 4:192-201.
68. Salghetti SE, Muratani M, Wijnen H, Futcher B, Tansey WP. Functional overlap of sequences that activate transcription and signal ubiquitin-mediated proteolysis. Proc Natl Acad Sci USA 2000; 97:3118-23.
69. Salghetti SE, Caudy AA, Chenoweth JG, Tansey WP. Regulation of transcriptional activation domain function by ubiquitin. Science 2001; 293:1651-3.
70. Birkaya B, Ortt K, Sinha S. Novel in vivo targets of DeltaNp63 in keratinocytes identified by a modified chromatin immunoprecipitation approach. BMC Mol Biol 2007; 8:43-52.
71. Ratovitski E, Patturajan M, Hibi K, et al. p53 associates with and targets DeltaNp63 into a protein degradation pathway. Proc Natl Acad Sci USA 2001; 98:1817-22.