High-mobility group A2 protein modulates hTERT transcription to promote tumorigenesis

Molecular and Cellular Biology

Volumn 31, Issue 13, 2011, Pages 2605-2617

  Li, Angela Ying Jian ^a,b   Lin, Her Helen ^a   Kuo, Ching Ying ^a,d   Shih, Hsiu Ming ^c   Wang, Clay Chia Chun ^b   Yen, Yun ^a,d   Ann, David Kong ^a,b,d  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^d Irell and Manella Graduate School of Biological Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP A2 PROTEIN; HISTONE DEACETYLASE 2; HISTONE H3; MESSENGER RNA; PREGNANCY SPECIFIC BETA1 GLYCOPROTEIN; TELOMERASE REVERSE TRANSCRIPTASE;

ARTICLE; CARCINOGENESIS; ENZYME ACTIVITY; HISTONE ACETYLATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; TELOMERE; TRANSCRIPTION REGULATION;

ACETYLATION; BASE SEQUENCE; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HELA CELLS; HEP G2 CELLS; HISTONE DEACETYLASE 2; HMGA2 PROTEIN; HUMANS; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; TELOMERASE; TRANSCRIPTION, GENETIC;

EID: 79959419265     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05447-11     Document Type: Article

References (66)

1. Ahmed, K. M., C. Y. Tsai, and W. H. Lee. 2010. Derepression of HMGA2 via removal of ZBRK1/BRCA1/CtIP complex enhances mammary tumorigenesis. J. Biol. Chem. 285:4464-4471.
2. Asai, A., et al. 2003. A novel telomerase template antagonist (GRN163) as a potential anticancer agent. Cancer Res. 63:3931-3939.
3. Benetti, R., M. Garcia-Cao, and M. A. Blasco. 2007. Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat. Genet. 39:243-250.
4. Berlingieri, M. T., et al. 1995. Inhibition of HMGI-C protein synthesis suppresses retrovirally induced neoplastic transformation of rat thyroid cells. Mol. Cell. Biol. 15:1545-1553.
5. Beroukhim, R., et al. 2010. The landscape of somatic copy-number alteration across human cancers. Nature 463:899-905.
6. Blackburn, E. H., C. W. Greider, and J. W. Szostak. 2006. Telomeres and telomerase: the path from maize, Tetrahymena and yeast to human cancer and aging. Nat. Med. 12:1133-1138.
7. Bryan, T. M., A. Englezou, M. A. Dunham, and R. R. Reddel. 1998. Telomere length dynamics in telomerase-positive immortal human cell populations. Exp. Cell Res. 239:370-378.
8. Campisi, J., and F. d'Adda di Fagagna. 2007. Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell Biol. 8:729-740.
9. Cleynen, I., and W. J. Van de Ven. 2008. The HMGA proteins: a myriad of functions (review). Int. J. Oncol. 32:289-305.
10. Cong, Y. S., and S. Bacchetti. 2000. Histone deacetylation is involved in the transcriptional repression of hTERT in normal human cells. J. Biol. Chem. 275:35665-35668.
11. Cong, Y. S., J. Wen, and S. Bacchetti. 1999. The human telomerase catalytic subunit hTERT: organization of the gene and characterization of the promoter. Hum. Mol. Genet. 8:137-142.
12. d'Adda di Fagagna, F., et al. 2003. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426:194-198.
13. Fedele, M., et al. 2006. HMGA2 induces pituitary tumorigenesis by enhancing E2F1 activity. Cancer Cell 9:459-471.
14. Furuta, S., et al. 2006. Removal of BRCA1/CtIP/ZBRK1 repressor complex on ANG1 promoter leads to accelerated mammary tumor growth contributed by prominent vasculature. Cancer Cell 10:13-24.
15. Fusco, A., and M. Fedele. 2007. Roles of HMGA proteins in cancer. Nat. Rev. Cancer. 7:899-910.
16. Geserick, C., A. Tejera, E. Gonzalez-Suarez, P. Klatt, and M. A. Blasco. 2006. Expression of mTert in primary murine cells links the growth-promoting effects of telomerase to transforming growth factor-beta signaling. Oncogene 25:4310-4319.
17. Gorgoulis, V. G., and T. D. Halazonetis. 2010. Oncogene-induced senescence: the bright and dark side of the response. Curr. Opin. Cell Biol. 22:816-827.
18. Hahn, W. C., et al. 1999. Creation of human tumour cells with defined genetic elements. Nature 400:464-468.
19. Hammond, S. M., and N. E. Sharpless. 2008. HMGA2, microRNAs, and stem cell aging. Cell 135:1013-1016.
20. Hanahan, D., and R. A. Weinberg. 2000. The hallmarks of cancer. Cell 100:57-70.
21. Hanahan, D., and R. A. Weinberg. 2011. Hallmarks of cancer: the next generation. Cell 144:646-674.
22. Harley, C. B., A. B. Futcher, and C. W. Greider. 1990. Telomeres shorten during ageing of human fibroblasts. Nature 345:458-460.
23. Herbig, U., W. A. Jobling, B. P. Chen, D. J. Chen, and J. M. Sedivy. 2004. Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol. Cell 14:501-513.
24. Hiyama, E., et al. 1996. Telomerase activity in human breast tumors. J. Natl. Cancer Inst. 88:116-122.
25. Horikawa, I., et al. 2002. Downstream E-box-mediated regulation of the human telomerase reverse transcriptase (hTERT) gene transcription: evidence for an endogenous mechanism of transcriptional repression. Mol. Biol. Cell 13:2585-2597.
26. Hou, M., et al. 2002. The histone deacetylase inhibitor trichostatin A derepresses the telomerase reverse transcriptase (hTERT) gene in human cells. Exp. Cell Res. 274:25-34.
27. Hug, N., and J. Lingner. 2006. Telomere length homeostasis. Chromosoma 115:413-425.
28. Indran, I., P. Hande, and S. Pervaiz. 2011. hTERT overexpression alleviates intracellular ROS production, improves mitochondrial function, and inhibits ROS-mediated apoptosis in cancer cells. Cancer Res. 71:266-276.
29. Jackson, S. R., et al. 2007. Antiadhesive effects of GRN163L-an oligonucleotide N3'->P5' thio-phosphoramidate targeting telomerase. Cancer Res. 67:1121-1129.
30. Johnson, J. E., et al. 2007. Whole-genome profiling in liposarcomas reveals genetic alterations common to specific telomere maintenance mechanisms. Cancer Res. 67:9221-9228.
31. Joseph, I., et al. 2010. The telomerase inhibitor imetelstat depletes cancer stem cells in breast and pancreatic cancer cell lines. Cancer Res. 70:9494-9504.
32. Karlseder, J., A. Smogorzewska, and T. de Lange. 2002. Senescence induced by altered telomere state, not telomere loss. Science 295:2446-2449.
33. Khair, L., L. Subramanian, B. A. Moser, and T. M. Nakamura. 2010. Roles of heterochromatin and telomere proteins in regulation of fission yeast telomere recombination and telomerase recruitment. J. Biol. Chem. 285: 5327-5337.
34. Kyo, S., et al. 2000. Sp1 cooperates with c-Myc to activate transcription of the human telomerase reverse transcriptase gene (hTERT). Nucleic Acids Res. 28:669-677.
35. Lee, J., et al. 2008. TERT promotes cellular and organismal survival independently of telomerase activity. Oncogene 27:3754-3760.
36. Lee, Y. S., and A. Dutta. 2007. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev. 21:1025-1030.
37. Lowe, S. W., E. Cepero, and G. Evan. 2004. Intrinsic tumour suppression. Nature 432:307-315.
38. Malini, E., et al. 2011. HMGA interactome: new insights from phage display technology. Biochemistry 50:3462-3468.
39. Mayr, C., M. T. Hemann, and D. P. Bartel. 2007. Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science 315: 1576-1579.
40. Meyerson, M., et al. 1997. hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell 90:785-795.
41. Mokbel, K., C. N. Parris, M. Ghilchik, G. Williams, and R. F. Newbold. 1999. The association between telomerase, histopathological parameters, and KI-67 expression in breast cancer. Am. J. Surg. 178:69-72.
42. Morin, G. B. 1989. The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats. Cell 59:521-529.
43. Narita, M., et al. 2006. A novel role for high-mobility group a proteins in cellular senescence and heterochromatin formation. Cell 126:503-514.
44. Nguyen, H. V., et al. 2006. SUMOylation attenuates sensitivity toward hypoxia-or desferroxamine-induced injury by modulating adaptive responses in salivary epithelial cells. Am. J. Pathol. 168:1452-1463.
45. Nishino, J., I. Kim, K. Chada, and S. J. Morrison. 2008. Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf expression. Cell 135:227-239.
46. Okawa, T., et al. 2007. The functional interplay between EGFR overexpression, hTERT activation, and p53 mutation in esophageal epithelial cells with activation of stromal fibroblasts induces tumor development, invasion, and differentiation. Genes Dev. 21:2788-2803.
47. Patel, U. A., et al. 1994. Expression and cDNA cloning of human HMGI-C phosphoprotein. Biochem. Biophys. Res. Commun. 201:63-70.
48. Poole, J. C., L. G. Andrews, and T. O. Tollefsbol. 2001. Activity, function, and gene regulation of the catalytic subunit of telomerase (hTERT). Gene 269: 1-12.
49. Salhab, M., W. G. Jiang, R. F. Newbold, and K. Mokbel. 2008. The expression of gene transcripts of telomere-associated genes in human breast cancer: correlation with clinico-pathological parameters and clinical outcome. Breast Cancer Res. Treat 109:35-46.
50. Saretzki, G., et al. 2008. Downregulation of multiple stress defense mechanisms during differentiation of human embryonic stem cells. Stem Cells. 26:455-464.
51. Serrano, M., A. W. Lin, M. E. McCurrach, D. Beach, and S. W. Lowe. 1997. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88:593-602.
52. Sgarra, R., et al. 2010. HMGA molecular network: from transcriptional regulation to chromatin remodeling. Biochim. Biophys. Acta 1799:37-47.
53. Shay, J. W., W. E. Wright, and H. Werbin. 1991. Defining the molecular mechanisms of human cell immortalization. Biochim. Biophys. Acta 1072: 1-7.
54. Shay, J. W., Y. Zou, E. Hiyama, and W. E. Wright. 2001. Telomerase and cancer. Hum. Mol. Genet. 10:677-685.
55. Shell, S., et al. 2007. Let-7 expression defines two differentiation stages of cancer. Proc. Natl. Acad. Sci. U. S. A. 104:11400-11405.
56. Smith, L. L., H. A. Coller, and J. M. Roberts. 2003. Telomerase modulates expression of growth-controlling genes and enhances cell proliferation. Nat. Cell Biol. 5:474-479.
57. Takakura, M., et al. 2001. Telomerase activation by histone deacetylase inhibitor in normal cells. Nucleic Acids Res. 29:3006-3011.
58. Wang, S., and J. Zhu. 2003. Evidence for a relief of repression mechanism for activation of the human telomerase reverse transcriptase promoter. J. Biol. Chem. 278:18842-18850.
59. Wang, X., et al. 2011. Overexpression of HMGA2 promotes metastasis and impacts survival of colorectal cancers. Clin. Cancer Res. 17:2570-2580.
60. Weir, B. A., et al. 2007. Characterizing the cancer genome in lung adenocarcinoma. Nature 450:893-898.
61. Won, J., J. Yim, and T. K. Kim. 2002. Sp1 and Sp3 recruit histone deacetylase to repress transcription of human telomerase reverse transcriptase (hTERT) promoter in normal human somatic cells. J. Biol. Chem. 277: 38230-38238.
62. Wood, L. J., J. F. Maher, T. E. Bunton, and L. M. Resar. 2000. The oncogenic properties of the HMG-I gene family. Cancer Res. 60:4256-4261.
63. Xu, D., et al. 2000. Downregulation of telomerase reverse transcriptase mRNA expression by wild type p53 in human tumor cells. Oncogene 19: 5123-5133.
64. Xu, M., W. Luo, D. J. Elzi, C. Grandori, and D. A. Galloway. 2008. NFX1 interacts with mSin3A/histone deacetylase to repress hTERT transcription in keratinocytes. Mol. Cell. Biol. 28:4819-4828.
65. Yang, C., et al. 2008. A key role for telomerase reverse transcriptase unit in modulating human embryonic stem cell proliferation, cell cycle dynamics, and in vitro differentiation. Stem Cells. 26:850-863.
66. Zhang, P., S. L. Chan, W. Fu, M. Mendoza, and M. P. Mattson. 2003. TERT suppresses apoptosis at a premitochondrial step by a mechanism requiring reverse transcriptase activity and 14-3-3 protein-binding ability. FASEB J. 17:767-769.