Elevated Bmi-1 expression is associated with dysplastic cell transformation during oral carcinogenesis and is required for cancer cell replication and survival

British Journal of Cancer

Volumn 96, Issue 1, 2007, Pages 126-133

  Kang, M K ^a,b   Kim, R H ^a   Kim, S J ^a   Yip, F K ^a   Shin, K H ^a,b   Dimri, G P ^c   Christensen, R ^a   Han, T ^a   Park, N H ^a,b  

^a UCLA SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Bmi 1; Keratinocytes; Oral cancer; p16INK4A; Polycomb; RNA interference

Indexed keywords

PROTEIN; PROTEIN BMI 1; PROTEIN P16INK4A; RNA; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CANCER STAGING; CARCINOGENESIS; CELL DIVISION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; CELL VIABILITY; CONTROLLED STUDY; DISEASE ASSOCIATION; EPITHELIUM DYSPLASIA; HISTOPATHOLOGY; HUMAN; HUMAN CELL; LEUKOPLAKIA; MOUTH CARCINOGENESIS; MOUTH CARCINOMA; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SQUAMOUS CELL CARCINOMA;

CARCINOMA, SQUAMOUS CELL; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; KERATINOCYTES; MOUTH NEOPLASMS; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SENSITIVITY AND SPECIFICITY; STAINING AND LABELING; TUMOR CELLS, CULTURED;

EID: 33846211524     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6603529     Document Type: Article

References (41)

1. Bea S, Tort F, Pinyol M, Puig X, Hernandez L, Hernandez S, Fernandez PL, van Lohuizen M, Colomer D, Campo E (2001) BMI-1 gene amplification and overexpression in hematological malignancies occur mainly in mantle cell lymphomas. Cancer Res 61: 2409-2412
2. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K (2006) Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 20: 1123-1136
3. Bracken AP, Pasini D, Capra M, Prosperini E, Colli E, Helin K (2003) EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J 22: 5323-5335
4. Breuer RH, Snijders PJ, Sutedja GT, Sewalt RG, Otte AP, Postmus PE, Meijer CJ, Raaphorst FM, Smit EF (2005) Expression of the p16(INK4a) gene product, methylation of the p16(INK4a) promoter region and expression of the polycomb-group gene BMI-1 in squamous cell lung carcinoma and premalignant endobronchial lesions. Lung Cancer 48: 299-306
5. Campisi J (2005) Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120: 513-522
6. Chen JH, Ozanne SE, Hales CN (2005) Heterogeneity in premature senescence by oxidative stress correlates with differential DNA damage during the cell cycle. DNA Repair 4: 1140-1148
7. Chen YJ, Lin SC, Kao T, Chang CS, Hong PS, Shieh TM, Chang KW (2004) Genome-wide profiling of oral squamous cell carcinoma. J Pathol 204: 326-332
8. Dimri GP (2005) What has senescence got to do with cancer? Cancer Cell 7: 505-512
9. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O, Peacocke M, Campisi J (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 92: 9363-9367
10. Dimri GP, Martinez JL, Jacobs JJ, Keblusek P, Itahana K, van Lohuizen M, Campisi J, Wazer DE, Band V (2002) The Bmi-1 oncogene induces telomerase activity and immortalizes human mammary epithelial cells. Cancer Res 62: 4736-4745
11. Dukers DF, van Galen JC, Giroth C, Jansen P, Sewalt RG, Otte AP, Kluin-Nelemans HC, Meijer CJ, Raaphorst FM (2004) Unique polycomb gene expression pattern in Hodgkin's lymphoma and Hodgkin's lymphoma-derived cell lines. Am J Pathol 164: 873-881
12. Gil J, Bernard D, Martinez D, Beach D (2004) Polycomb CBX7 has a unifying role in cellular lifespan. Nat Cell Biol 6: 67-72
13. Guney I, Wu S, Sedivy JM (2006) Reduced c-Myc signaling triggers telomere-independent senescence by regulating Bmi-1 and p16(INK4a). Proc Natl Acad Sci USA 103: 3645-3650
14. Harley CB, Futcher B, Greider CW (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345: 458-460
15. Itahana K, Campisi J, Dimri GP (2004) Mechanisms of cellular senescence in human and mouse cells. Biogerontol 5: 1-10
16. Itahana K, Zou Y, Itahana Y, Martinez JL, Beausejour C, Jacobs JJ, van Lohuizen M, Band V, Campisi J, Dimri GP (2003) Control of the replicative life span of human fibroblasts by p16 and the polycomb protein Bmi-1. Mol Cell Biol 23: 389-401
17. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M (1999) The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397: 164-168
18. Kang MK, Bibb C, Baluda MA, Rey O, Park N-H (2000) In vitro replication and differentiation of normal human oral keratinocytes. Exp Cell Res 258: 288-297
19. Kang MK, Guo W, Park N-H (1998) Replicative senescence of normal human oral keratinocytes is associated with the loss of telomerase activity without shortening of telomeres. Cell Growth & Differ 9: 85-95
20. Kang MK, Kameta A, Shin K-H, Baluda MA, Kim HR, Park N-H (2003) Senescence-associated genes in normal human oral keratinocytes. Exp Cell Res 287: 272-281
21. Karlseder J, Smogorzewska A, de Lange T (2002) Senescence induced by altered telomere state, not telomere loss. Science 295: 2446-2449
22. Kim JH, Yoon SY, Jeong SH, Kim SY, Moon SK, Joo JH, Lee Y, Choe IS, Kim JW (2004a) Overexpression of Bmi-1 oncoprotein correlates with axillary lymph node metastases in invasive ductal breast cancer. Breast 13: 383-388
23. Kim JH, Yoon SY, Kim CN, Joo JH, Moon SK, Choe IS, Choe YK, Kim JW (2004b) The Bmi-1 oncoprotein is overexpressed in human colorectal cancer and correlates with the reduced p16INK4a/p14ARF proteins. Cancer Lett 203: 217-224
24. Kim RH, Kang MK, Shin K-H, Oo ZM, Han T, Baluda MA, Park N-H (2006) Bmi-1 cooperates with human papillomavirus type 16 E6 to immortalize normal human oral keratinocytes. Exp Cell Res doi:10.1016/j.yexcr.2006.10.025
25. Lessard J, Sauvageau G (2003) Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 423: 255-260
26. Li S, Rosenberg JE, Donjacour AA, Botchkina IL, Hom YK, Cunha GR, Blackburn EH (2004) Rapid inhibition of cancer cell growth induced by lentiviral delivery and expression of mutant-template telomerase RNA and anti-telomerase short-interfering RNA. Cancer Res 64: 4833-4840
27. Li Z, Cao R, Wang M, Myers MP, Zhang Y, Xu RM (2006) Structure of a Bmi-1-Ring1B polycomb group ubiquitin ligase complex. J Biol Chem 281: 20643-20649
28. Liu L, Andrews LG, Tollefsbol TO (2006) Loss of the human polycomb group protein BMI1 promotes cancer-specific cell death. Oncogene 25: 4370-4375
29. Munro J, Stott FJ, Vousden KH, Peters G, Parkinson EK (1999) Role of the alternative INK4A proteins in human keratinocyte senescence: evidence for the specific inactivation of p16INK4A upon immortalization. Cancer Res 59: 2516-2521
30. Naldini L, Blomer U, Gallay P, Ory D, Mulligan R, Gage FH, Verma IM, Trono D (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272: 263-267
31. Nowak K, Kerl K, Fehr D, Kramps C, Gessner C, Killmer K, Samans B, Berwanger B, Christiansen H, Lutz W (2006) BMI1 is a target gene of E2F-1 and is strongly expressed in primary neuroblastomas. Nucl Acids Res 34: 1745-1754
32. Ohtani N, Zebedee Z, Huot TJ, Stinson JA, Sugimoto M, Ohashi Y, Sharrocks AD, Peters G, Hara E (2001) Opposing effects of Ets and Id proteins on p16INK4a expression during cellular senescence. Nature 409: 1067-1070
33. Park N-H, Gujuluva CN, Baek J-H, Min B-M, Cherrick HM, Shin K-H (1995) Combined oral carcinogenicity of HPV-16 and benzo(a)pyrene: an in vitro multistep carcinogenesis model. Oncogene 10: 2145-2153
34. Pirrotta V (1998) Polycombing the genome: PcG, trxG, and chromatin silencing. Cell 93: 333-336
35. Ramirez RD, Morales CP, Herbert BS, Rohde JM, Passons C, Shay JW, Wright WE (2001) Putative telomere-independent mechanisms of replicative aging reflect inadequate growth conditions. Genes Dev 15: 398-403
36. Rey O, Lee S, Park N-H (2000) Human papillomavirus type 16 E7 oncoprotein represses transcription of human fibronectin. J Virol 74: 4912-4918
37. Rubinson DA, Dillon CP, Kwiatkowski AV, Sievers C, Yang L, Kopinja J, Zhang M, McManus MT, Gertler FB, Scott ML, Van Parijs L (2003) A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat Genet 33: 401-406
38. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88: 593-602
39. Sparmann A, van Lohuizen M (2006) Polycomb silencers control cell fate, development and cancer. Nat Rev Cancer 6: 846-856
40. Stewart SA, Poon B, Jowett JBM, Xie Y, Chen ISY (1999) Lentiviral delivery of HIV-1 Vpr protein induces apoptosis in transformed cells. Proc Natl Acad Sci USA 96: 12039-12043
41. van Lohuizen M, Verbeek S, Scheijen B, Wientjens E, van der Gulden H, Berns A (1991) Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging. Cell 65: 737-752