Deregulation of HMGA1 expression induces chromosome instability through regulation of spindle assembly checkpoint genes

Oncotarget

Volumn 6, Issue 19, 2015, Pages 17342-17353

  Pierantoni, Giovanna Maria ^a   Conte, Andrea ^a   Rinaldo, Cinzia ^b   Tornincasa, Mara ^a   Gerlini, Raffaele ^a   Federico, Antonella ^a   Valente, Davide ^b   Medico, Enzo ^c   Fusco, Alfredo ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c Ist per la Ricerca Contro il Cancro   (Italy)

Author keywords

CIN; HMGA1; SAC; transcriptional regulation

Indexed keywords

BUB1 RELATED PROTEIN; HIGH MOBILITY GROUP A1A PROTEIN; MESSENGER RNA; PROTEIN MAD2; HIGH MOBILITY GROUP B PROTEIN;

ANAPHASE; ARTICLE; BUB1 GENE; BUB1B GENE; CANCER GROWTH; CHROMOSOMAL INSTABILITY; COLORECTAL CANCER; CONTROLLED STUDY; CYTOKINESIS; GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HMGA1 GENE; HUMAN; HUMAN CELL; IN VIVO STUDY; M PHASE CELL CYCLE CHECKPOINT; MAD2L1 GENE; METAPHASE; PROMETAPHASE; PROMOTER REGION; TRANSCRIPTION REGULATION; TTK GENE; 3T3 CELL LINE; ANIMAL; CHROMATIN IMMUNOPRECIPITATION; COLON TUMOR; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSFECTION; GENETICS; HELA CELL LINE; IMMUNOHISTOCHEMISTRY; MOUSE; POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOMAL INSTABILITY; COLONIC NEOPLASMS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, NEOPLASTIC; HELA CELLS; HMGB PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; M PHASE CELL CYCLE CHECKPOINTS; MICE; NIH 3T3 CELLS; POLYMERASE CHAIN REACTION; TRANSFECTION;

EID: 84938271643     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3944     Document Type: Article

References (47)

1. Johnson KR, Lehn DA, Reeves R. Alternative processing of mRNAs encoding mammalian chromosomal high-mobility-group proteins HMG-I and HMG-Y. Mol Cell Biol. 1989; 9:2114-2123.
2. Manfioletti G, Giancotti V, Bandiera A, Buratti E, Sautière P, Cary P, Crane-Robinson C, Coles B, Goodwin GH. cDNA cloning of the HMGI-C phosphoprotein, a nuclear protein associated with neoplastic and undifferentiated phenotypes. Nucleic Acids Res. 1991; 19:6793-6797.
3. Fusco A, Fedele M. Roles of the HMGA proteins in cancer. Nat Rev Cancer. 2007; 7:899-910.
4. Chiappetta G, Avantaggiato V, Visconti R, Fedele M, Battista S, Trapasso F, Merciai BM, Fidanza V, Giancotti V, Santoro M, Simeone , Fusco A. High level expression of the HMGA1 gene during embryonic development. Oncogene. 1996; 13:2439-2446.
5. 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.
6. Liau SS, Whang E. HMGA1 is a molecular determinant of chemoresistance to gemcitabine in pancreatic adenocarcinoma. Clin Cancer Res. 2008; 14:1470-1477.
7. Wood LJ, Maher JF, Bunton TE, Resar LM. The oncogenic properties of the HMG-I gene family. Cancer Res. 2000; 60:4256-4261.
8. 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.
9. Baldassarre G, Fedele M, Battista S, Vecchione A, Klein-Szanto AJ, Santoro M, Waldmann TA, Azimi N, Croce CM, Fusco A. 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 U S A. 2001; 98:7970-7975.
10. Belton A, Gabrovsky A, Bae YK, Reeves R, Iacobuzio-Donahue C, Huso DL, Resar LM. HMGA1 induces intestinal polyposis in transgenic mice and drives tumor progression and stem cell properties in colon cancer cells. PLoS One. 2012; 7:e30034.
11. Fedele M, Battista S, Kenyon L, Baldassarre G, Fidanza V, Klein-Szanto AJ, Parlow AF, Visone R, Pierantoni GM, Outwater E, Santoro M, Croce CM, Fusco A. Overexpression of the HMGA2 gene in transgenic mice leads to the onset of pituitary adenomas. Oncogene. 2002; 21:3190-3198.
12. Fedele M, Pentimalli F, Baldassarre G, Battista S, Klein-Szanto AJ, Kenyon L, Visone R, De Martino I, Ciarmiello A, Arra C, Viglietto G, Croce CM, Fusco A. 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.
13. Xu Y, Sumter TF, Bhattacharya R, Tesfaye A, Fuchs EJ, Wood LJ, Huso DL, Resar LM. 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.
14. Fedele M, Fusco A. HMGA and cancer. Biochim Biophys Acta. 2010; 1799:48-54. Review.
15. Mussnich P, D'Angelo D, Leone V, Croce CM, Fusco A. The High Mobility Group A proteins contribute to thyroid cell transformation by regulating miR-603 and miR-10b expression. Mol Oncol. 2013; 7:531-542.
16. Reeves R, Adair JE. Role of high mobility group (HMG) chromatin proteins in DNA repair. DNA Repair. 2005; 4:926-938.
17. Mertens F, Johansson B, Mitelman F. Isochromosomes in neoplasia. Genes Chromosomes Cancer. 1994; 10:221-230.
18. Fang X, Zhang P. Aneuploidy and tumorigenesis. Semin Cell Dev Biol. 2011; 22:595-601.
19. Rao CV, Yamada HY, Yao Y, Dai W. Enhanced genomic instabilities caused by deregulated microtubule dynamics and chromosome segregation: a perspective from genetic studies in mice. Carcinogenesis. 2009; 30:1469-1474.
20. Lin SF, Lin PM, Yang MC, Liu TC, Chang JG, Sue YC, Chen TP. Expression of hBUB1 in acute myeloid leukemia. Leuk Lymphoma. 2002; 43:385-391.
21. Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, Rosenwald A, Boldrick JC, Sabet H, Tran T, Yu X, Powell JI, Yang L, Marti GE, Moore T, Hudson J Jr, Lu L, Lewis DB, Tibshirani R, Sherlock G, Chan WC, Greiner TC, Weisenburger DD, Armitage JO, Warnke R, Levy R, Wilson W, Grever MR, Byrd JC, Botstein D, Brown PO, Staudt LM. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000; 403:503-511.
22. van't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH. Gene expression profiling predicts clinical outcome of breast cancer. Nature. 2002; 415:530-536.
23. Grabsch H, Takeno S, Parsons WJ, Pomjanski N, Boecking A, Gabbert HE, Mueller W. Overexpression of the mitotic checkpoint genes BUB1, BUBR1, and BUB3 in gastric cancer-association with tumour cell proliferation. J. Pathol. 2003; 200:16-22.
24. Shigeishi H, Oue N, Kuniyasu H, Wakikawa A, Yokozaki H, Ishikawa T, Yasui W. Expression of Bub1 gene correlates with tumor proliferating activity in human gastric carcinomas. Pathobiology. 2001; 69:24-29.
25. Chiappetta G, Manfioletti G, Pentimalli F, Abe N, Di Bonito M, Vento MT, Giuliano A, Fedele M, Viglietto G, Santoro M, Watanabe T, Giancotti V, Fusco A. High mobility group HMGI(Y) protein expression in human colorectal hyperplastic and neoplastic diseases. Int J Cancer. 2001; 91:1447-1451.
26. Fedele M, Bandiera A, Chiappetta G, Battista S, Viglietto G, Manfioletti G, Casamassimi A, Santoro M, Giancotti V, Fusco A. Human colorectal carcinomas express high levels of high mobility group HMGI(Y) proteins. Cancer Res. 1996; 56:1896-1901.
27. Puca F, Colamaio M, Federico A, Gemei M, Tosti N, Bastos AU, Del Vecchio L, Pece S, Battista S, Fusco A. HMGA1 silencing restores normal stem cell characteristics in colon cancer stem cells by increasing p53 levels. Oncotarget. 2014; 5:3234-3245.
28. Palmieri D, Valentino T, D'Angelo D, De Martino I, Postiglione I, Pacelli R, Croce CM, Fedele M, Fusco A. HMGA proteins promote ATM expression and enhance cancer cell resistance to genotoxic agents. Oncogene. 2011; 30:3024-3035.
29. Pegoraro S, Ros G, Piazza S, Sommaggio R, Ciani Y, Rosato A, Sgarra R, Del Sal G, Manfioletti G. HMGA1 promotes metastatic processes in basal-like breast cancer regulating EMT and stemness. Oncotarget. 2013; 4:1293-1308.
30. Kops GJ, Weaver BA, Cleveland DW. On the road to cancer: aneuploidy and the mitotic checkpoint. Nat Rev Cancer 2005; 5:773-785.
31. Gordon DJ, Resio B, Pellman D. Causes and consequences of aneuploidy in cancer. Nat Rev Genet. 2012; 13:189-203.
32. Hernando E, Nahlé Z, Juan G, Diaz-Rodriguez E, Alaminos M, Hemann M, Michel L, Mittal V, Gerald W, Benezra R, Lowe SW, Cordon-Cardo C. Rb inactivation promotes genomic instability by uncoupling cell cycle progression from mitotic control. Nature. 2004; 430:797-802.
33. Orr B, Compton DA. A double-edged sword: how oncogenes and tumor suppressor genes can contribute to chromosomal instability. Front Oncol. 2013; 3:164.
34. Ding Y, Hubert CG, Herman J, Corrin P, Toledo CM, Skutt-Kakaria K, Vazquez J, Basom R, Zhang B, Risler JK, Pollard SM, Nam DH, Delrow JJ, Zhu J, LeeJ, DeLucaJ, Olson JM, Paddison PJ. Cancer-Specific requirement for BUB1B/BUBR1 in human brain tumor isolates and genetically transformed cells. Cancer Discov. 2013; 3:198-211.
35. Schliekelman M, Cowley DO, O'Quinn R, Oliver TG, Lu L, Salmon ED, Van Dyke T. Impaired Bub1 function in vivo compromises tension-dependent checkpoint function leading to aneuploidy and tumorigenesis. Cancer Res. 2009; 69:45-54.
36. Chen X, Cheung ST, So S, Fan ST, Barry C, Higgins J, Lai KM, Ji J, Dudoit S, Ng IO, Van De Rijn M, Botstein D, Brown PO. Gene expression patterns in human liver cancers. Mol Biol Cell. 2002; 136:1929-1939.
37. Teixeira JH, Silva P, Faria J, Ferreira I, Duarte P, DelgadoML, Queirós O, Moreira R, BarbosaJ, Lopes CA, do Amaral JB, Monteiro LS, Bousbaa H. Clinicopathologic significance of BubR1 and Mad2 overexpression in oral cancer. Oral Dis. 2015 Mar 5, doi: 10.111/odi.12335.
38. Shichiri M, Yoshinaga K, Hisatomi H, Sugihara K, Hirata Y. Genetic and epigenetic inactivation of mitotic checkpoint genes hBUB1 and hBUBR1 and their relationship to survival. Cancer Res. 2002; 62:13-17.
39. Esposito F, Tornincasa M, Chieffi P, De Martino I, Pierantoni GM, Fusco A. High-mobility group A1 proteins regulate p53-mediated transcription of Bcl-2 gene. Cancer Res. 2010; 70:5379-5388.
40. Pierantoni GM, Battista S, Pentimalli F, Fedele M, Visone R, Federico A, Santoro M, Viglietto G, Fusco A. A truncated HMGA1 gene induces proliferation of the 3T3-L1 pre-adipocytic cells: a model of human lipomas. Carcinogenesis. 2003a; 24:1861-1869.
41. Myslinski E, Gérard MA, Krol A, Carbon P. Transcription of the human cell cycle regulated BUB1B gene requires hStaf/ZNF143. Nucleic Acids Res. 2007; 35:3453-3464.
42. Jeong SJ, Shin HJ, Kim SJ, Ha GH, Cho BI, Baek KH, Kim CM, Lee CW. Transcriptional abnormality of the hsMAD2 mitotic checkpoint gene is a potential link to hepatocellular carcinogenesis. Cancer Res. 2004; 64:8666-8673.
43. Salvatore G, Nappi TC, Salerno P, Jiang Y, Garbi C, Ugolini C, Miccoli P, Basolo F, Castellone MD, Cirafici AM, Melillo RM, Fusco A, Bittner ML, Santoro M. A cell proliferation and chromosomal instability signature in anaplastic thyroid carcinoma. Cancer Res. 2007; 67:10148-10158.
44. Pierantoni GM, Agosti V, Fedele M, Bond H, Caliendo I, Chiappetta G, Lo Coco F, Pane F, Turco MC, Morrone G, Venuta S, Fusco A. High-mobility group A1 proteins are overexpressed in human leukaemias. Biochem J. 2003; 372:145-150.
45. Esposito F, De Martino M, Petti MG, Forzati F, Tornincasa M, Federico A, Arra C, Pierantoni GM, Fusco A. HMGA1 pseudogenes as candidate proto-oncogenic competitive endogenous RNAs. Oncotarget. 2014; 5:8341-54.
46. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25:402-408.
47. Chiappetta G, Botti G, Monaco M, Pasquinelli R, Pentimalli F, Di Bonito M, D'Aiuto G, Fedele M, Luliano R, Palmieri EA, Pierantoni GM, Giancotti V, Fusco A. HMGA1 protein overexpression in human breast carcinomas: correlation with ErbB2 expression. Clin Cancer Res. 2004; 10:7637-7644.