Human papilloma virus-dependent HMGA1 expression is a relevant step in cervical carcinogenesis

Neoplasia

Volumn 10, Issue 8, 2008, Pages 773-781

  Mellone, Massimiliano ^a   Rinaldi, Christian ^a,b   Massimi, Isabella ^a   Petroni, Marialaura ^a   Veschi, Veronica ^a   Talora, Claudio ^a   Truffa, Silvia ^c   Stabile, Helena ^a   Frati, Luigi ^a   Screpanti, Isabella ^a   Gulino, Alberto ^a,b   Giannini, Giuseppe ^a,d  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b IRCCS NEUROMED   (Italy)

^c LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; NOTCH1 RECEPTOR; ONCOPROTEIN; PROTEIN P53; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HMGA1; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; DEREGULATION; GENE EXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; UTERINE CERVIX CANCER; WART VIRUS; WESTERN BLOTTING;

EID: 48249132920     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.08462     Document Type: Article

References (57)

1. Reeves R (2004). HMGA proteins: isolation, biochemical modifications, and nucleosome interactions. Methods Enzymol 375, 297-322.
2. Merika M and Thanos D (2001). Enhanceosomes. Curr Opin Genet Dev 11, 205-208.
3. Munshi N, Agalioti T, Lomvardas S, Merika M, Chen G, and Thanos D (2001). Coordination of a transcriptional switch by HMGI(Y) acetylation. Science 293, 1133-1136.
4. Munshi N, Merika M, Yie J, Senger K, Chen G, and Thanos D (1998). Acetylation of HMG I(Y) by CBP turns off IFNβ expression by disrupting the enhanceosome. Mol Cell 2, 457-467.
5. Thanos D and Maniatis T (1995). Virus induction of human IFNβ gene expression requires the assembly of an enhanceosome. Cell 83, 1091-1100.
6. Zhou X, Benson KF, Ashar HR, and Chada K (1995). Mutation responsible for the mouse pygmy phenotype in the developmentally regulated factor HMGI-C. Nature 376, 771-774.
7. Battista S, Fidanza V, Fedele M, Klein-Szanto AJ, Outwater E, Brunner H, Santoro M, Croce CM, and Fusco A (1999). The expression of a truncated HMGI-C gene induces gigantism associated with lipomatosis. Cancer Res 59, 4793-4797.
8. Chiappetta G, Bandiera A, Berlingieri MT, Visconti R, Manfioletti G, Battista S, Martinez-Tello FJ, Santoro M, Giancotti V, and Fusco A (1995). The expression of the high mobility group HMGI (Y) proteins correlates with the malignant phenotype of human thyroid neoplasias. Oncogene 10, 1307-1314.
9. Abe N, Watanabe T, Sugiyama M, Uchimura H, Chiappetta G, Fusco A, and Atomi Y (1999). Determination of high mobility group I(Y) expression level in colorectal neoplasias: a potential diagnostic marker. Cancer Res 59, 1169-1174.
10. Chiappetta G, Manfioletti G, Pentimalli F, Abe N, Di Bonito M, Vento MT, Giuliano A, Fedele M, Viglietto G, Santoro M, et al. (2001). High mobility group HMGI(Y) protein expression in human colorectal hyperplastic and neoplastic diseases. Int J Cancer 91, 147-151.
11. Fedele M, Bandiera A, Chiappetta G, Battista S, Viglietto G, Manfioletti G, Casamassimi A, Santoro M, Giancotti V, and Fusco A (1996). Human colorectal carcinomas express high levels of high mobility group HMGI(Y) proteins. Cancer Res 56, 1896-1901.
12. Bussemakers MJ, van de Ven WJ, Debruyne FM, and Schalken JA (1991). Identification of high mobility group protein I(Y) as potential progression marker for prostate cancer by differential hybridization analysis. Cancer Res 51, 606-611.
13. Tamimi Y, van der Poel HG, Denyn MM, Umbas R, Karthaus HF, Debruyne FM, and Schalken JA (1993). Increased expression of high mobility group protein I(Y) in high grade prostatic cancer determined by in situ hybridization. Cancer Res 53, 5512-5516.
14. Abe N, Watanabe T, Izumisato Y, Masaki T, Mori T, Sugiyama M, Chiappetta G, Fusco A, Fujioka Y, and Atomi Y (2002). Diagnostic significance of high mobility group I(Y) protein expression in intraductal papillary mucinous tumors of the pancreas. Pancreas 25, 198-204.
15. Masciullo V, Baldassarre G, Pentimalli F, Berlingieri MT, Boccia A, Chiappetta G, Palazzo J, Manfioletti G, Giancotti V, Viglietto G, et al. (2003). HMGA1 protein over-expression is a frequent feature of epithelial ovarian carcinomas. Carcinogenesis 24, 1191-1198.
16. Liu WM, Guerra-Vladusic FK, Kurakata S, Lupu R, and Kohwi-Shigematsu T (1999). HMG-I(Y) recognizes base-unpairing regions of matrix attachment sequences and its increased expression is directly linked to metastatic breast cancer phenotype. Cancer Res 59, 5695-5703.
17. Giannini G, Di Marcotullio L, Ristori E, Zani M, Crescenzi M, Scarpa S, Piaggio G, Vacca A, Peverali FA, Diana F, et al. (1999). HMGI(Y) and HMGI-C genes are expressed in neuroblastoma cell lines and tumors and affect retinoic acid responsiveness. Cancer Res 59, 2484-2492.
18. Chiappetta G, Tallini G, De Biasio MC, Manfioletti G, Martinez-Tello FJ, Pentimalli F, de Nigris F, Mastro A, Botti G, Fedele M, et al. (1998). 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 58, 4193-4198.
19. Giannini G, Kim CJ, Marcotullio LD, Manfioletti G, Cardinali B, Cerignoli F, Ristori E, Zani M, Frati L, Screpanti I, et al. (2000). Expression of the HMGI(Y) gene products in human neuroblastic tumours correlates with differentiation status. Br J Cancer 83, 1503-1509.
20. Reeves R, Edberg DD, and Li Y (2001). Architectural transcription factor HMGI(Y) promotes tumor progression and mesenchymal transition of human epithelial cells. Mol Cell Biol 21, 575-594.
21. Wood LJ, Maher JF, Bunton TE, and Resar LM (2000). The oncogenic properties of the HMG-I gene family. Cancer Res 60, 4256-4261.
22. Wood LJ, Mukherjee M, Dolde CE, Xu Y, Maher JF, Bunton TE, Williams JB, and Resar LM (2000). HMG-I/Y, a new c-Myc target gene and potential oncogene. Mol Cell Biol 20, 5490-5502.
23. Fedele M, Pentimalli F, Baldassarre G, Battista S, Klein-Szanto AJ, Kenyon L, Visone R, De Martino I, Ciarmiello A, Arra C, et al. (2005). 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 24, 3427-3435.
24. Xu Y, Sumter TF, Bhattacharya R, Tesfaye A, Fuchs EJ, Wood LJ, Huso DL, and Resar LM (2004). The HMG-I oncogene causes highly penetrant, aggressive lymphoid malignancy in transgenic mice and is overexpressed in human leukemia. Cancer Res 64, 3371-3375.
25. Fedele M, Visone R, De Martino I, Troncone G, Palmieri D, Battista S, Ciarmiello A, Pallante P, Arra C, Melillo RM, et al. (2006). HMGA2 induces pituitary tumorigenesis by enhancing E2F1 activity. Cancer Cell 9, 459-471.
26. Baldassarre G, Fedele M, Battista S, Vecchione A, Klein-Szanto AJ, Santoro M, Waldmann TA, Azimi N, Croce CM, and Fusco A (2001). 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 98, 7970-7975.
27. Frasca F, Rustighi A, Malaguarnera R, Altamura S, Vigneri P, Del Sal G, Giancotti V, Pezzino V, Vigneri R, and Manfioletti G (2006). HMGA1 inhibits the function of p53 family members in thyroid cancer cells. Cancer Res 66, 2980-2989.
28. Pierantoni GM, Rinaldo C, Esposito F, Mottolese M, Soddu S, and Fusco A (2006). High mobility group A1 (HMGA1) proteins interact with p53 and inhibit its apoptotic activity. Cell Death Differ 13, 1554-1563.
29. Pierantoni GM, Rinaldo C, Mottolese M, Di Benedetto A, Esposito F, Soddu S, and Fusco A (2007). High-mobility group A1 inhibits p53 by cytoplasmic relocalization of its proapoptotic activator HIPK2. J Clin Invest 117, 693-702.
30. D'Orazi G, Cecchinelli B, Bruno T, Manni I, Higashimoto Y, Saito S, Gostissa M, Coen S, Marchetti A, Del Sal G, et al. (2002). Homeodomain- interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nat Cell Biol 4, 11-19.
31. Cleynen I, Huysmans C, Sasazuki T, Shirasawa S, Van de Ven W, and Peeters K (2007). Transcriptional control of the human high mobility group A1 gene: basal and oncogenic Ras-regulated expression. Cancer Res 67, 4620-4629.
32. Giannini G, Cerignoli F, Mellone M, Massimi I, Ambrosi C, Rinaldi C, Dominici C, Frati L, Screpanti I, and Gulino A (2005). High mobility group A1 is a molecular target for MYCN in human neuroblastoma. Cancer Res 65, 8308-8316.
33. Munger K, Baldwin A, Edwards KM, Hayakawa H, Nguyen CL, Owens M, Grace M, and Huh K (2004). Mechanisms of human papillomavirus-induced oncogenesis. J Virol 78, 11451-11460.
34. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, and Munoz N (1999). Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189, 12-19.
35. zur Hausen H (2002). Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2, 342-350.
36. Dyson N, Howley PM, Munger K, and Harlow E (1989). The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243, 934-937.
37. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, and Howley PM (1990). The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63, 1129-1136.
38. Zagouras P, Stifani S, Blaumueller CM, Carcangiu ML, and Artavanis-Tsakonas S (1995). Alterations in Notch signaling in neoplastic lesions of the human cervix. Proc Natl Acad Sci USA 92, 6414-6418.
39. Nair P, Somasundaram K, and Krishna S (2003). Activated Notch1 inhibits p53-induced apoptosis and sustains transformation by human papillomavirus type 16 E6 and E7 oncogenes through a PI3K-PKB/Akt-dependent pathway. J Virol 77, 7106-7112.
40. Rangarajan A, Syal R, Selvarajah S, Chakrabarti O, Sarin A, and Krishna S (2001). Activated Notch1 signaling cooperates with papillomavirus oncogenes in transformation and generates resistance to apoptosis on matrix withdrawal through PKB/Akt. Virology 286, 23-30.
41. Veeraraghavalu K, Pett M, Kumar RV, Nair P, Rangarajan A, Stanley MA, and Krishna S (2004). Papillomavirus-mediated neoplastic progression is associated with reciprocal changes in JAGGED1 and manic fringe expression linked to notch activation. J Virol 78, 8687-8700.
42. Talora C, Cialfi S, Segatto O, Morrone S, Kim Choi J, Frati L, Paolo Dotto G, Gulino A, and Screpanti I (2005). Constitutively active Notch1 induces growth arrest of HPV-positive cervical cancer cells via separate signaling pathways. Exp Cell Res 305, 343-354.
43. Talora C, Sgroi DC, Crum CP, and Dotto GP (2002). Specific down-modulation of Notch1 signaling in cervical cancer cells is required for sustained HPV-E6/E7 expression and late steps of malignant transformation. Genes Dev 16, 2252-2263.
44. Lathion S, Schaper J, Beard P, and Raj K (2003). Notch1 can contribute to viral-induced transformation of primary human keratinocytes. Cancer Res 63, 8687-8694.
45. Nicolas M, Wolfer A, Raj K, Kummer JA, Mill P, van Noort M, Hui CC, Clevers H, Dotto GP, and Radtke F (2003). Notch1 functions as a tumor suppressor in mouse skin. Nat Genet 33, 416-421.
46. Lefort K, Mandinova A, Ostano P, Kolev V, Calpini V, Kolfschoten I, Devgan V, Lieb J, Raffoul W, Hohl D, et al. (2007). Notch1 is a p53 target gene involved in human keratinocyte tumor suppression through negative regulation of ROCK1/2 and MRCKα kinases. Genes Dev 21, 562-577.
47. Yugawa T, Handa K, Narisawa-Saito M, Ohno S, Fujita M, and Kiyono T (2007). Regulation of Notch1 gene expression by p53 in epithelial cells. Mol Cell Biol 27, 3732-3742.
48. Alimirah F, Panchanathan R, Davis FJ, Chen J, and Choubey D (2007). Restoration of p53 expression in human cancer cell lines upregulates the expression of Notch1: implications for cancer cell fate determination after genotoxic stress. Neoplasia 9, 427-434.
49. Bandiera A, Bonifacio D, Manfioletti G, Mantovani F, Rustighi A, Zanconati F, Fusco A, Di Bonito L, and Giancotti V (1998). Expression of HMGI(Y) proteins in squamous intraepithelial and invasive lesions of the uterine cervix. Cancer Res 58, 426-431.
50. Goodwin EC and DiMaio D (2000). Repression of human papillomavirus oncogenes in HeLa cervical carcinoma cells causes the orderly reactivation of dormant tumor suppressor pathways. Proc Natl Acad Sci USA 97, 12513-12518.
51. Sima N, Wang W, Kong D, Deng D, Xu Q, Zhou J, Xu G, Meng L, Lu Y, Wang S, et al. (2008). RNA interference against HPV16 E7 oncogene leads to viral E6 and E7 suppression in cervical cancer cells and apoptosis via upregulation of Rb and p53. Apoptosis 13, 273-281.
52. Bouallaga I, Massicard S, Yaniv M, and Thierry F (2000). An enhanceosome containing the Jun B/Fra-2 heterodimer and the HMG-I(Y) architectural protein controls HPV 18 transcription. EMBO Rep 1, 422-427.
53. Bouallaga I, Teissier S, Yaniv M, and Thierry F (2003). HMG-I(Y) and the CBP/p300 coactivator are essential for human papillomavirus type 18 enhanceosome transcriptional activity. Mol Cell Biol 23, 2329-2340.
54. Kinoshita T, Shirasawa H, Shino Y, Shimizu K, Moriya H, and Simizu B (1996). Human papillomavirus type 16 E6 protein up-regulates the expression of the high mobility group protein HMG-I(Y) gene in mouse 10T1/2 cells. Virus Res 42, 119-125.
55. Chow LT and Broker TR (1994). Papillomavirus DNA replication. Intervirology 37, 150-158.
56. Durst M, Glitz D, Schneider A, and zur Hausen H (1992). Human papillomavirus type 16 (HPV 16) gene expression and DNA replication in cervical neoplasia: analysis by in situ hybridization. Virology 189, 132-140.
57. Stoler MH, Rhodes CR, Whitbeck A, Wolinsky SM, Chow LT, and Broker TR (1992). Human papillomavirus type 16 and 18 gene expression in cervical neoplasias. Hum Pathol 23, 117-128.