HBP1-mediated transcriptional regulation of DNA methyltransferase 1 and its impact on cell senescence

Molecular and Cellular Biology

Volumn 33, Issue 5, 2013, Pages 887-903

  Pan, Kewu ^a   Chen, Yifan ^a   Roth, Mendel ^b   Wang, Weibin ^a   Wang, Shuya ^a   Yee, Amy S ^b   Zhang, Xiaowei ^a  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE 1; HIGH MOBILITY GROUP B PROTEIN; HMG BOX CONTAINING PROTEIN 1; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; DNA METHYLATION; DNA SEQUENCE; EMBRYO; GENE SEQUENCE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; PRIORITY JOURNAL; SENESCENCE;

ACETYLATION; CELL AGING; CELL LINE; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DOWN-REGULATION; GENES, P16; HIGH MOBILITY GROUP PROTEINS; HUMANS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPRESSOR PROTEINS; TRANSCRIPTIONAL ACTIVATION;

EID: 84874698936     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00637-12     Document Type: Article

References (66)

1. Avissar-Whiting M, Koestler DC, Houseman EA, Christensen BC, Kelsey KT, Marsit CJ. 2011. Polycomb group genes are targets of aberrant DNA methylation in renal cell carcinoma. Epigenetics 6:703-709.
2. Berletch JB, Andrews LG, Tollefsbol TO. 2007. A method to detect DNA methyltransferase I gene transcription in vitro in aging systems. Methods Mol. Biol. 371:73-80.
3. Liao X, Siu MK, Chan KY, Wong ES, Ngan HY, Chan QK, Li AS, Khoo US, Cheung AN. 2008. Hypermethylation of RAS effector related genes and DNA methyltransferase 1 expression in endometrial carcinogenesis. Int. J. Cancer 123:296-302.
4. Wang W, Gao J, Man XH, Li ZS, Gong YF. 2009. Significance of DNA methyltransferase-1 and histone deacetylase-1 in pancreatic cancer. Oncol. Rep. 21:1439-1447.
5. Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB, Harley CB, Shay JW, Lichtsteiner S, Wright WE. 1998. Extension of life-span by introduction of telomerase into normal human cells. Science 279:349-352.
6. Bond JA, Haughton MF, Rowson JM, Smith PJ, Gire V, Wynford-Thomas D, Wyllie FS. 1999. Control of replicative life span in human cells: barriers to clonal expansion intermediate between M1 senescence and M2 crisis. Mol. Cell. Biol. 19:3103-3114.
7. Bulavin DV, Fornace AJ, Jr. 2004. p38 MAP kinase's emerging role as a tumor suppressor. Adv. Cancer Res. 9:95-118.
8. Hornsby PJ. 2007. Senescence as an anticancer mechanism. J. Clin. Oncol. 25:1852-1857.
9. Cavaliéri Gomes C, da Silveira e Oliveira C, Santos Pimenta LG, De Marco L, Santiago Gomez R. 2009. Immunolocalization of DNMT1 and DNMT3a in salivary gland neoplasms. Pathobiology 76:136-140.
10. Sawada M, Kanai Y, Arai E, Ushijima S, Ojima H, Hirohashi S. 2007. Increased expression of DNA methyltransferase 1 (DNMT1) protein in uterine cervix squamous cell carcinoma and its precursor lesion. Cancer Lett. 251:211-219.
11. Yamagata Y, Maekawa R, Asada H, Taketani T, Tamura I, Tamura H, Ogane J, Hattori N, Shiota K, Sugino N. 2009. Aberrant DNA methylation status in human uterine leiomyoma. Mol. Hum. Reprod. 15:259-267.
12. Casillas MA, Jr, Lopatina N, Andrews LG, Tollefsbol TO. 2003. Transcriptional control of the DNA methyltransferases is altered in aging and neoplastically-transformed human fibroblasts. Mol. Cell. Biochem. 252: 33-43.
13. Imbesi M, Dzitoyeva S, Ng LW, Manev H. 2009. 5-Lipoxygenase and epigenetic DNA methylation in aging cultures of cerebellar granule cells. Neuroscience 164:1531-1537.
14. Li Y, Liu Y, Strickland FM, Richardson B. 2010. Age-dependent decreases in DNA methyltransferase levels and low transmethylation micronutrient levels synergize to promote overexpression of genes implicated in autoimmunity and acute coronary syndromes. Exp. Gerontol. 45:312-322.
15. Liu Y, Chen Y, Richardson B. 2009. Decreased DNA methyltransferase levels contribute to abnormal gene expression in "senescent" CD4(+)CD28(-) T cells. Clin. Immunol. 132:257-265.
16. Zhang X, Kim J, Ruthazer R, McDevitt MA, Wazer DE, Paulson KE, Yee AS. 2006. The HBP1 transcriptional repressor participates in RASinduced premature senescence. Mol. Cell. Biol. 26:8252-8266.
17. Berasi SP, Xiu M, Yee AS, Paulson KE. 2004. HBP1 repression of the p47phox gene: cell cycle regulation via the NADPH oxidase. Mol. Cell. Biol. 24:3011-3024.
18. Zhang JJ, Zhang L, Zhou K, Ye X, Liu C, Zhang L, Kang J, Cai C. 2011. Analysis of globalDNAmethylation by hydrophilic interaction ultra highpressure liquid chromatography tandem mass spectrometry. Anal. Biochem. 413:164-170.
19. Zhuma T, Tyrrell R, Sekkali B, Skavdis G, Saveliev A, Tolaini M, Roderick K, Norton T, Smerdon S, Sedgwick S, Festenstein R, Kioussis D. 1999. Human HMG box transcription factor HBP1: a role in hCD2 LCR function. EMBO J. 18:6396-6406.
20. Chen YC, Zhang XW, Niu XH, Xin DQ, Zhao WP, Na YQ, Mao ZB. 2010. Macrophage migration inhibitory factor is a direct target of HBP1-mediated transcriptional repression that is overexpressed in prostate cancer. Oncogene 29:3067-3078.
21. Tevosian SG, Shih HH, Mendelson KG, Sheppard KA, Paulson KE, Yee AS. 1997. HBP1: a HMG box transcriptional repressor that is targeted by the retinoblastoma family. Genes Dev. 11:383-396.
22. Lesage F, Hugnot JP, Amri EZ, Grimaldi P, Barhanin J, Lazdunski M. 1994. Expression cloning in K+ transport defective yeast and distribution of HBP1, a new putative HMG transcriptional regulator. Nucleic Acids Res. 22:3685-3688.
23. Lavender P, Vandel L, Bannister AJ, Kouzarides T. 1997. The HMG-box transcription factor HBP1 is targeted by the pocket proteins and E1A. Oncogene 14:2721-2728.
24. Chicas A, Wang X, Zhang C, McCurrach M, Zhao Z, Mert O, Dickins RA, Narita M, Zhan M, Lowe SW. 2010. Dissecting the unique role of the retinoblastoma tumor suppressor during cellular senescence. Cancer Cell 17:376-387.
25. Mao D, Hinds PW. 2010. p35 is required for CDK5 activation in cellular senescence. J. Biol. Chem. 285:14671-14680.
26. Sampson EM, Haque ZK, Ku MC, Tevosian SG, Albanese C, Pestell RG, Paulson KE, Yee AS. 2001. Negative regulation of the Wnt-beta-catenin pathway by the transcriptional repressor HBP1. EMBO J. 20:4500-4511.
27. Escamilla-Powers JR, Daniel CJ, Farrell A, Taylor K, Zhang X, Byers S, Sears R. 2010. The tumor suppressor protein HBP1 is a novel c-mycbinding protein that negatively regulates c-myc transcriptional activity. J. Biol. Chem. 285:4847-4858.
28. Sekkali B, Szabat E, Ktistaki E, Tolaini M, Roderick K, Harker N, Patel A, Williams K, Norton T, Kioussis D. 2005. Human high mobility group box transcription factor 1 affects thymocyte development and transgene variegation. J. Immunol. 175:5203-5212.
29. Gartel AL, Goufman E, Tevosian SG, Shih H, Tyner AL. 1998. Activation and repression of p21(WAF1/CIP1) transcription by RB binding proteins. Oncogene 17:3463-3469.
30. Lin KM, Zhao WG, Bhatnagar J, Zhao WD, Lu JP, Simko S, Schueneman A, Austin GE. 2001. Cloning and expression of human HBP1, a high mobility group protein that enhances myeloperoxidase (MPO) promoter activity. Leukemia 15:601-612.
31. Yao CJ, Works K, Romagnoli PA, Austin GE. 2005. Effects of overex-pression of HBP1 upon growth and differentiation of leukemic myeloid cells. Leukemia 19:1958-1968.
32. Lemercier C, Duncliffe K, Boibessot I, Zhang H, Verdel A, Angelov D, Khochbin S. 2000. Involvement of retinoblastoma protein and HBP1 in histone H10 gene expression. Mol. Cell. Biol. 20:6627-6637.
33. Li H, Wang W, Liu X, Paulson KE, Yee AS, Zhang X. 2010. Transcriptional factor HBP1 targets P16(INK4A), upregulating its expression and consequently is involved in Ras-induced premature senescence. Oncogene 29:5083-5094.
34. Wang W, Pan K, Chen Y, Huang C, Zhang X. 2012. The acetylation of transcription factor HBP1 by p300/CBP enhances p16INK4A expression. Nucleic Acids Res. 40:981-995.
35. Ohshiro K, Rayala SK, Wigerup C, Pakala SB, Natha RS, Gururaj AE, Molli PR, Månsson SS, Ramezani A, Hawley RG, Landberg G, Lee NH, Kumar R. 2010. Acetylation-dependent oncogenic activity of metastasisassociated protein 1 coregulator. EMBO Rep. 11:691-697.
36. Ramsey MR, He L, Forster N, Ory B, Ellisen LW. 2011. Physical association of HDAC1 and HDAC2 with p63 mediates transcriptional repression and tumor maintenance in squamous cell carcinoma. Cancer Res. 71:4373-4379.
37. Van Rechem C, Boulay G, Pinte S, Stankovic-Valentin N, Guérardel C, Leprince D. 2010. Differential regulation of HIC1 target genes by CtBP and NuRD, via an acetylation/SUMOylation switch, in quiescent versus proliferating cells. Mol. Cell. Biol. 30:4045-4059.
38. Shih HH, Tevosian SG, Yee AS. 1998. Regulation of differentiation by HBP1, a target of the retinoblastoma protein. Mol. Cell. Biol. 8:4732-4743.
39. Shih HH, Xiu M, Berasi SP, Sampson EM, Leiter A, Paulson KE, Yee AS. 2001. HMG box transcriptional repressor HBP1 maintains a proliferation barrier in differentiated liver tissue. Mol. Cell. Biol. 21:5723-5732.
40. Paulson EK, Rieger-Christ K, McDevitt MA, Kuperwasser C, Kim J, Unanue VE, Zhang X, Hu M, Ruthazer R, Berasi SP, Huang CY, Giri D, Kaufman S, Dugan JM, Blum J, Netto G, Wazer DE, Summerhayes IC, Yee AS. 2007. Alterations of the HBP1 transcriptional repressor are associated with invasive breast cancer. Cancer Res. 67:6136-6145.
41. Li H, Bian C, Liao L, Li J, Zhao RC. 2011. miR-17-5p promotes human breast cancer cell migration and invasion through suppression of HBP1. Breast Cancer Res. Treat. 126:565-575.
42. Yee AS, Shih HH, Tevosian SG. 1999. New perspectives on retinoblastoma family functions in differentiation. Front. Biosci. 3:532-547.
43. Jin SG, Kadam S, Pfeifer GP. 2010. Examination of the specificity of DNA methylation profiling techniques towards 5-methylcytosine and 5-hydroxymethylcytosine. Nucleic Acids Res. 38:e125. doi:10.1093/nar/gkq223.
44. Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL, Schübeler D. 2005. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat. Genet. 37:853-862.
45. Zhang Z, Tang H, Wang Z, Zhang B, Liu W, Lu H, Xiao L, Liu X, Wang R, Li X, Wu M, Li G. 2011. MiR-185 targets the DNA methyltransferases 1 and regulates global DNA methylation in human glioma. Mol. Cancer 10:124.
46. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A. 2009. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324:930-935.
47. Xiu M, Kim J, Sampson E, Huang CY, Davis RJ, Paulson KE, Yee AS. 2003. The transcriptional repressor HBP1 is a target of the p38 mitogenactivated protein kinase pathway in cell cycle regulation. Mol. Cell. Biol. 23:8890-8901.
48. Yee AS, Paulson EK, McDevitt MA, Rieger-Christ K, Summerhayes I, Berasi SP, Kim J, Huang CY, Zhang X. 2004. The HBP1 transcriptional repressor and the p38 MAP kinase: unlikely partners in G1 regulation and tumor suppression. Gene 336:1-13.
49. Zheng QH, Ma LW, Zhu WG, Zhang ZY, Tong TJ. 2006. p21Waf1/Cip1 plays a critical role in modulating senescence through changes of DNA methylation. J. Cell. Biochem. 98:1230-1248.
50. Swanson KA, Knoepfler PS, Huang K, Kang RS, Cowley SM, Laherty CD, Eisenman RN, Radhakrishnan I. 2004. HBP1 and Mad1 repressors bind the Sin3 corepressor PAH2 domain with opposite helical orientations. Nat. Struct. Mol. Biol. 11:738-746.
51. Lim JS, Park SH, Jang KL. 2011. All-trans retinoic acid induces cellular senescence by up-regulating levels of p16 and p21 via promoter hypomethylation. Biochem. Biophys. Res. Commun. 412:500-505.
52. Sun LQ, Lee DW, Zhang Q, Xiao W, Raabe EH, Meeker A, Miao D, Huso DL, Arceci RJ. 2004. Growth retardation and premature aging phenotypes in mice with disruption of the SNF2-like gene, PASG. Genes Dev. 18:1035-1046.
53. Kruse JP, Gu W. 2009. Modes of p53 regulation. Cell 137:609-622.
54. Bracken AP, Kohlbrecher DK, Dietrich N. 2007. The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes Dev. 21:525-530.
55. Cakouros D, Isenmann S, Cooper L, Zannettino A, Anderson P, Glackin C, Gronthos S. 2012. Twist-1 induces Ezh2 recruitment regulating histone methylation along the Ink4A/Arf locus in mesenchymal stem cells. Mol. Cell. Biol. 32:1433-1441.
56. Chen H, Gu X, Su IH, Bottino R, Contreras JL, Tarakhovsky A, Kim SK. 2009. Polycomb protein Ezh2 regulates pancreatic beta-cell Ink4a/Arf expression and regeneration in diabetes mellitus. Genes Dev. 23:975-985.
57. Simon AJ, Lange CA. 2008. Roles of the EZH2 histone methyltransferase in cancer epigenetics. Mutat. Res. 647:21-29.
58. Kotake Y, Cao R, Viatour P. 2007. pRB family proteins are required for H3K27 trimethylation and Polycomb repression complexes binding to and silencing p16INK4a tumor suppressor gene. Genes Dev. 21:49-54.
59. So AY, Jung JW, Lee S, Kim HS, Kang KS. 2011. DNA methyltransferase controls stem cell aging by regulating BMI1 and EZH2 through micro-RNAs. PLoS One 6:e19503. doi:10.1371/journal.pone.0019503.
60. Dhe-Paganon S, Syeda F, Park L. 2011. DNA methyl transferase 1: regulatory mechanisms and implications in health and disease. Int. J. Biochem. Mol. Biol. 2:58-66.
61. Felle M, Joppien S, Németh A, Diermeier S, Thalhammer V, Dobner T, Kremmer E, Kappler R, Längst G. 2011. The USP7/Dnmt1 complex stimulates the DNA methylation activity of Dnmt1 and regulates the stability of UHRF1. Nucleic Acids Res. 39:8355-8365.
62. Peng L, Yuan Z, Ling H, Fukasawa K, Robertson K, Olashaw N, Koomen J, Chen J, Lane WS, Seto E. 2011. SIRT1 deacetylates the DNA methyltransferase 1 (DNMT1) protein and alters its activities. Mol. Cell. Biol. 31:4720-4734.
63. Song J, Teplova M, Ishibe-Murakami S, Patel DJ. 2012. Structure-based mechanistic insights into DNMT1-mediated maintenance DNA methylation. Science 335:709-712.
64. Chik F, Szyf M. 2011. Effects of specific DNMT gene depletion on cancer cell transformation and breast cancer cell invasion; toward selective DNMT inhibitors. Carcinogenesis 32:224-232.
65. Shukla V, Coumoul X, Lahusen T, Wang RH, Xu X, Vassilopoulos A, Xiao C, Lee MH, Man YG, Ouchi M, Ouchi T, Deng CX. 2010. BRCA1 affects global DNA methylation through regulation of DNMT1. Cell Res. 20:1201-1215.
66. SSowin'ska A, Jagodzinski PP. 2007. RNA interference-mediated knockdown of DNMT1 and DNMT3B induces CXCL12 expression in MCF-7 breast cancer and AsPC1 pancreatic carcinoma cell lines. Cancer Lett. 255:153-159.