The HMGA1 protoncogene frequently deregulated in cancer is a transcriptional target of E2F1

Molecular Carcinogenesis

Volumn 52, Issue 7, 2013, Pages 526-534

  Massimi, Isabella ^a   Guerrieri, Francesca ^b,c   Petroni, Marialaura ^a   Veschi, Veronica ^a   Truffa, Silvia ^d   Screpanti, Isabella ^e   Frati, Luigi ^a   Levrero, Massimo ^b,c   Gulino, Alberto ^e,f   Giannini, Giuseppe ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b Laboratory of Gene Expression   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

^f IRCCS NEUROMED   (Italy)

Author keywords

Carcinogenesis; HMGA1 promoter; Sp1; Transcription

Indexed keywords

HMGA1 PROTEIN; PROTEIN; TRANSCRIPTION FACTOR E2F1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL PROLIFERATION; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPOPHYSIS TUMOR; LOSS OF FUNCTION MUTATION; MOUSE; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; THYROID TUMOR;

ANIMALS; BASE SEQUENCE; BINDING SITES; BLOTTING, WESTERN; CHROMATIN IMMUNOPRECIPITATION; E2F1 TRANSCRIPTION FACTOR; HMGA1A PROTEIN; HUMANS; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PITUITARY NEOPLASMS; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; RETINOBLASTOMA PROTEIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SP1 TRANSCRIPTION FACTOR; THYROID NEOPLASMS; TRANSCRIPTIONAL ACTIVATION;

MUS;

EID: 84879462597     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.21887     Document Type: Article

References (61)

1. Reeves R. Nuclear functions of the HMG proteins. Biochim Biophys Acta 2010; 1799: 3- 14.
2. Munshi N, Merika M, Yie J, Senger K, Chen G, Thanos D. Acetylation of HMG I(y) by CBP turns off IFN beta expression by disrupting the enhanceosome. Mol Cell 1998; 2: 457- 467.
3. Kim TK, Maniatis T. The mechanism of transcriptional synergy of an in vitro assembled interferon-beta enhanceosome. Mol Cell 1997; 1: 119- 129.
4. Thanos D, Maniatis T. Virus induction of human IFN beta gene expression requires the assembly of an enhanceosome. Cell 1995; 83: 1091- 1100.
5. Anand A, Chada K. In vivo modulation of Hmgic reduces obesity. Nat Genet 2000; 24: 377- 380.
6. Zhou X, Benson KF, Ashar HR, Chada K. Mutation responsible for the mouse pygmy phenotype in the developmentally regulated factor HMGI-C. Nature 1995; 376: 771- 774.
7. Battista S, Pentimalli F, Baldassarre G, et al. Loss of Hmga1 gene function affects embryonic stem cell lympho-hematopoietic differentiation. FASEB J 2003; 17: 1496- 1498.
8. Fedele M, Fidanza V, Battista S, et al. Haploinsufficiency of the Hmga1 gene causes cardiac hypertrophy and myelo-lymphoproliferative disorders in mice. Cancer Res 2006; 66: 2536- 2543.
9. Foti D, Chiefari E, Fedele M, et al. Lack of the architectural factor HMGA1 causes insulin resistance and diabetes in humans and mice. Nat Med 2005; 11: 765- 773.
10. Arlotta P, Tai AK, Manfioletti G, Clifford C, Jay G, Ono SJ. Transgenic mice expressing a truncated form of the high mobility group I-C protein develop adiposity and an abnormally high prevalence of lipomas. J Biol Chem 2000; 275: 14394- 14400.
11. Battista S, Fidanza V, Fedele M, et al. The expression of a truncated HMGI-C gene induces gigantism associated with lipomatosis. Cancer Res 1999; 59: 4793- 4797.
12. Fedele M, Visone R, De Martino I, et al. Expression of a truncated Hmga1b gene induces gigantism, lipomatosis and B-cell lymphomas in mice. Eur J Cancer 2010; 47: 470- 478.
13. Giancotti V, Berlingieri MT, DiFiore PP, Fusco A, Vecchio G, Crane-Robinson C. Changes in nuclear proteins on transformation of rat epithelial thyroid cells by a murine sarcoma retrovirus. Cancer Res 1985; 45: 6051- 6057.
14. Lund T, Holtlund J, Fredriksen M, Laland SG. On the presence of two new high mobility group-like proteins in HeLa S3 cells. FEBS Lett 1983; 152: 163- 167.
15. Wood LJ, Mukherjee M, Dolde CE, et al. HMG-I/Y, a new c-Myc target gene and potential oncogene. Mol Cell Biol 2000; 20: 5490- 5502.
16. Reeves R, Edberg DD, Li Y. Architectural transcription factor HMGI(Y) promotes tumor progression and mesenchymal transition of human epithelial cells. Mol Cell Biol 2001; 21: 575- 594.
17. Scala S, Portella G, Fedele M, Chiappetta G, Fusco A. Adenovirus-mediated suppression of HMGI(Y) protein synthesis as potential therapy of human malignant neoplasias. Proc Natl Acad Sci USA 2000; 97: 4256- 4261.
18. Baldassarre G, Fedele M, Battista S, et al. Onset of natural killer cell lymphomas in transgenic mice carrying a truncated HMGI-C gene by the chronic stimulation of the IL-2 and IL-15 pathway. Proc Natl Acad Sci USA 2001; 98: 7970- 7975.
19. Fedele M, Visone R, De Martino I, et al. HMGA2 induces pituitary tumorigenesis by enhancing E2F1 activity. Cancer Cell 2006; 9: 459- 471.
20. Zaidi MR, Okada Y, Chada KK. Misexpression of full-length HMGA2 induces benign mesenchymal tumors in mice. Cancer Res 2006; 66: 7453- 7459.
21. Fedele M, Pentimalli F, Baldassarre G, et al. Transgenic mice overexpressing the wild-type form of the HMGA1 gene develop mixed growth hormone/prolactin cell pituitary adenomas and natural killer cell lymphomas. Oncogene 2005; 24: 3427- 3435.
22. Xu Y, Sumter TF, Bhattacharya R, et al. The HMG-I oncogene causes highly penetrant, aggressive lymphoid malignancy in transgenic mice and is overexpressed in human leukemia. Cancer Res 2004; 64: 3371- 3375.
23. Sgarra R, Zammitti S, Lo Sardo A, et al. HMGA molecular network: From transcriptional regulation to chromatin remodeling. Biochim Biophys Acta 2010; 1799: 37- 47.
24. Fedele M, Fusco A. HMGA and cancer. Biochim Biophys Acta 2010; 1799: 48- 54.
25. Pierantoni GM, Rinaldo C, Mottolese M, et al. High-mobility group A1 inhibits p53 by cytoplasmic relocalization of its proapoptotic activator HIPK2. J Clin Invest 2007; 117: 693- 702.
26. Frasca F, Rustighi A, Malaguarnera R, et al. HMGA1 inhibits the function of p53 family members in thyroid cancer cells. Cancer Res 2006; 66: 2980- 2989.
27. Esposito F, Pierantoni GM, Battista S, et al. Interaction between HMGA1 and retinoblastoma protein is required for adipocyte differentiation. J Biol Chem 2009; 284: 25993- 26004.
28. Ueda Y, Watanabe S, Tei S, Saitoh N, Kuratsu J, Nakao M. High mobility group protein HMGA1 inhibits retinoblastoma protein-mediated cellular G0 arrest. Cancer Sci 2007; 98: 1893- 1901.
29. Chiappetta G, Tallini G, De Biasio MC, et al. Detection of high mobility group I HMGI(Y) protein in the diagnosis of thyroid tumors: HMGI(Y) expression represents a potential diagnostic indicator of carcinoma. Cancer Res 1998; 58: 4193- 4198.
30. Abe N, Watanabe T, Sugiyama M, et al. Determination of high mobility group I(Y) expression level in colorectal neoplasias: A potential diagnostic marker. Cancer Res 1999; 59: 1169- 1174.
31. Chiappetta G, Manfioletti G, Pentimalli F, et al. High mobility group HMGI(Y) protein expression in human colorectal hyperplastic and neoplastic diseases. Int J Cancer 2001; 91: 147- 151.
32. Abe N, Watanabe T, Masaki T, et al. Pancreatic duct cell carcinomas express high levels of high mobility group I(Y) proteins. Cancer Res 2000; 60: 3117- 3122.
33. Liau SS, Rocha F, Matros E, Redston M, Whang E. High mobility group AT-hook 1 (HMGA1) is an independent prognostic factor and novel therapeutic target in pancreatic adenocarcinoma. Cancer 2008; 113: 302- 314.
34. Bandiera A, Bonifacio D, Manfioletti G, et al. Expression of HMGI(Y) proteins in squamous intraepithelial and invasive lesions of the uterine cervix. Cancer Res 1998; 58: 426- 431.
35. Tamimi Y, van der Poel HG, Denyn MM, et al. Increased expression of high mobility group protein I(Y) in high grade prostatic cancer determined by in situ hybridization. Cancer Res 1993; 53: 5512- 5516.
36. Chiappetta G, Botti G, Monaco M, et al. HMGA1 protein overexpression in human breast carcinomas: Correlation with ErbB2 expression. Clin Cancer Res 2004; 10: 7637- 7644.
37. Donato G, Martinez Hoyos J, Amorosi A, et al. High mobility group A1 expression correlates with the histological grade of human glial tumors. Oncol Rep 2004; 11: 1209- 1213.
38. Giannini G, Di Marcotullio L, Ristori E, et al. HMGI(Y) and HMGI-C genes are expressed in neuroblastoma cell lines and tumors and affect retinoic acid responsiveness. Cancer Res 1999; 59: 2484- 2492.
39. Giannini G, Kim CJ, Marcotullio LD, et al. Expression of the HMGI(Y) gene products in human neuroblastic tumours correlates with differentiation status. Br J Cancer 2000; 83: 1503- 1509.
40. Pomeroy SL, Tamayo P, Gaasenbeek M, et al. Prediction of central nervous system embryonal tumour outcome based on gene expression. Nature 2002; 415: 436- 442.
41. Cerignoli F, Ambrosi C, Mellone M, et al. HMGA molecules in neuroblastic tumors. Ann N Y Acad Sci 2004; 1028: 122- 132.
42. Ogram SA, Reeves R. Differential regulation of a multipromoter gene. Selective 12-O-tetradecanoylphorbol-13-acetate induction of a single transcription start site in the HMG-I/Y gene. J Biol Chem 1995; 270: 14235- 14242.
43. Giannini G, Cerignoli F, Mellone M, et al. Molecular mechanism of HMGA1 deregulation in human neuroblastoma. Cancer Lett 2005; 228: 97- 104.
44. Cleynen I, Huysmans C, Sasazuki T, Shirasawa S, Van de Ven W, Peeters K. Transcriptional control of the human high mobility group A1 gene: Basal and oncogenic Ras-regulated expression. Cancer Res 2007; 67: 4620- 4629.
45. Giannini G, Cerignoli F, Mellone M, et al. High mobility group A1 is a molecular target for MYCN in human neuroblastoma. Cancer Res 2005; 65: 8308- 8316.
46. Pediconi N, Ianari A, Costanzo A, et al. Differential regulation of E2F1 apoptotic target genes in response to DNA damage. Nat Cell Biol 2003; 5: 552- 558.
47. Cao AR, Rabinovich R, Xu M, Xu X, Jin VX, Farnham PJ. Genome-wide analysis of transcription factor E2F1 mutant proteins reveals that N- and C-terminal protein interaction domains do not participate in targeting E2F1 to the human genome. J Biol Chem 2011; 286: 11985- 11996.
48. Elena C, Banchio C. Specific interaction between E2F1 and Sp1 regulates the expression of murine CTP:phosphocholine cytidylyltransferase alpha during the S phase. Biochim Biophys Acta 2010; 1801: 537- 546.
49. Rotheneder H, Geymayer S, Haidweger E. Transcription factors of the Sp1 family: Interaction with E2F and regulation of the murine thymidine kinase promoter. J Mol Biol 1999; 293: 1005- 1015.
50. Mussi P, Yu C, O'Malley BW, Xu J. Stimulation of steroid receptor coactivator-3 (SRC-3) gene overexpression by a positive regulatory loop of E2F1 and SRC-3. Mol Endocrinol 2006; 20: 3105- 3119.
51. Kel AE, Kel-Margoulis OV, Farnham PJ, Bartley SM, Wingender E, Zhang MQ. Computer-assisted identification of cell cycle-related genes: New targets for E2F transcription factors. J Mol Biol 2001; 309: 99- 120.
52. Seelan RS, Parthasarathy LK, Parthasarathy RN. E2F1 regulation of the human myo-inositol 1-phosphate synthase (ISYNA1) gene promoter. Arch Biochem Biophys 2004; 431: 95- 106.
53. Lanahan A, Williams JB, Sanders LK, Nathans D. Growth factor-induced delayed early response genes. Mol Cell Biol 1992; 12: 3919- 3929.
54. Takahashi Y, Rayman JB, Dynlacht BD. Analysis of promoter binding by the E2F and pRB families in vivo: Distinct E2F proteins mediate activation and repression. Genes Dev 2000; 14: 804- 816.
55. Jacks T, Fazeli A, Schmitt EM, Bronson RT, Goodell MA, Weinberg RA. Effects of an Rb mutation in the mouse. Nature 1992; 359: 295- 300.
56. Akaboshi S, Watanabe S, Hino Y, et al. HMGA1 is induced by Wnt/beta-catenin pathway and maintains cell proliferation in gastric cancer. Am J Pathol 2009; 175: 1675- 1685.
57. Cleynen I, Van de Ven WJ. The HMGA proteins: A myriad of functions (Review). Int J Oncol 2008; 32: 289- 305.
58. Chen HZ, Tsai SY, Leone G. Emerging roles of E2Fs in cancer: An exit from cell cycle control. Nat Rev Cancer 2009; 9: 785- 797.
59. Mellone M, Rinaldi C, Massimi I, et al. Human papilloma virus-dependent HMGA1 expression is a relevant step in cervical carcinogenesis. Neoplasia 2008; 10: 773- 781.
60. Pierantoni GM, Rinaldo C, Esposito F, Mottolese M, Soddu S, Fusco A. High Mobility Group A1 (HMGA1) proteins interact with p53 and inhibit its apoptotic activity. Cell Death Differ 2006; 13: 1554- 1563.
61. Petroni M, Veschi V, Prodosmo A, et al. MYCN sensitizes human neuroblastoma to apoptosis by HIPK2 activation through a DNA damage response. Mol Cancer Res 2011; 9: 67- 77.