High-mobility group A1 protein inhibits p53-mediated intrinsic apoptosis by interacting with Bcl-2 at mitochondria

Cell Death and Disease

Volumn 3, Issue 8, 2012, Pages

  Esposito, F ^a   Tornincasa, M ^a   Federico, A ^a   Chiappetta, G ^b   Pierantoni, G M ^a   Fusco, A ^a,c,d  

^a CNR   (Italy)

^b NATIONAL CANCER INSTITUTE   (Italy)

^c CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^d SEMM European School of Molecular Medicine Naples site   (Italy)

Author keywords

Apoptosis; Bcl 2; HMGA proteins; Mitochondria; P53

Indexed keywords

CYTOCHROME C; HIGH MOBILITY GROUP A PROTEIN; PROTEIN BCL 2; PROTEIN P53; CASPASE; HIGH MOBILITY GROUP A1A PROTEIN; RECOMBINANT PROTEIN;

APOPTOSIS; ARTICLE; BREAST CARCINOMA; CANCER CELL; COLON CARCINOMA; CORRELATION ANALYSIS; CYTOPLASM; EMBRYO; ENZYME INHIBITION; ENZYME RELEASE; HUMAN; HUMAN CELL; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; THYROID CARCINOMA; CELL LINE; CELL STRAIN HEK293; CELL STRAIN MCF 7; DRUG EFFECT; GENETIC TRANSCRIPTION; GENETICS; HELA CELL; METABOLISM; ULTRAVIOLET RADIATION;

APOPTOSIS; CASPASES; CELL LINE; CYTOCHROMES C; HEK293 CELLS; HELA CELLS; HMGA1A PROTEIN; HUMANS; MCF-7 CELLS; MITOCHONDRIA; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-BCL-2; RECOMBINANT PROTEINS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS;

EID: 84865792218     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2012.126     Document Type: Article

References (39)

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. (Pubitemid 19117812)
2. Nagpal S, Ghosn C, DiSepio D, Molina Y, Sutter M, Klein ES et al. Retinoid-dependent recruitment of a histone H1 displacement activity by retinoic acid receptor. J Biol Chem 1999; 274: 22563-22568.
3. Manfioletti G, Giancotti V, Bandiera A, Buratti E, Sautière P, Cary P et al. cDNA cloning of the HMGI-C phosphoprotein, a nuclear protein associated with neoplastic and undifferentiated phenotypes. Nucleic Acids Res 1991; 19: 6793-6797. (Pubitemid 21913116)
4. Thanos D, Maniatis T. The high mobility group protein HMG I(Y) is required for NF-kappa B-dependent virus induction of the human IFN-beta gene. Cell 1992; 71: 777-789.
5. Grosschedl R, Giese K, Pagel J. HMG domain proteins: architectural elements in the assembly of nucleoprotein structures. Trends Genet 1994; 10: 94-100. (Pubitemid 24075089)
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. Chiappetta G, Avantaggiato V, Visconti R, Fedele M, Battista S, Trapasso F et al. High level expression of the HMGI (Y) gene during embryonic development. Oncogene 1996; 13: 2439-2446. (Pubitemid 27026027)
8. Chiappetta G, Tallini G, De Biasio MC, Manfioletti G, Martinez-Tello FJ, Pentimalli F 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. (Pubitemid 28440579)
9. Fedele M, Bandiera A, Chiappetta G, Battista S, Viglietto G, Manfioletti G et al. Human colorectal carcinomas express high levels of high mobility group HMGI(Y) proteins. Cancer Res 1996; 56: 1896-1901. (Pubitemid 26118229)
10. Tamimi Y, van der Poel HG, Denyn MM, Umbas R, Karthaus HF, Debruyne FM 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. (Pubitemid 23342176)
11. Abe N, Watanabe T, Izumisato Y, Masaki T, Mori T, Sugiyama M et al. Diagnostic significance of high mobility group I(Y) protein expression in intraductal papillary mucinous tumors of the pancreas. Pancreas 2002; 25: 198-204. (Pubitemid 34815920)
12. Bandiera A, Bonifacio D, Manfioletti G, Mantovani F, Rustighi A, Zanconati F et al. Expression of HMGI(Y) proteins in squamous intraepithelial and invasive lesions of the uterine cervix. Cancer Res 1998; 58: 426-431. (Pubitemid 28087401)
13. Masciullo V, Baldassarre G, Pentimalli F, Berlingieri MT, Boccia A, Chiappetta G et al. HMGA1 protein over-expression is a frequent feature of epithelial ovarian carcinomas. Carcinogenesis 2003; 24: 1191-1198. (Pubitemid 36927059)
14. Chiappetta G, Botti G, Monaco M, Pasquinelli R, Pentimalli F, Di Bonito M et al. HMGA1 protein overexpression in human breast carcinomas: correlation with ErbB2 expression. Clin Cancer Res 2004; 10: 7637-7644. (Pubitemid 39557527)
15. Fusco A, Fedele M. Roles of the HMGA proteins in cancer. Nat Rev Cancer 2007; 7: 899-910.
16. Berlingieri MT, Manfioletti G, Santoro M, Bandiera A, Visconti R, Giancotti V et al. Inhibition of HMGI-C protein synthesis suppresses retrovirally induced neoplastic transformation of rat thyroid cells. Mol Cell Biol 1995; 15: 1545-1553.
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; 11: 4256-4261. (Pubitemid 30226120)
18. 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. (Pubitemid 44210358)
19. 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.
20. Pierantoni GM, Rinaldo C, Mottolese M, Di Benedetto A, Esposito F, Soddu S et al. High-mobility group A1 inhibits p53 by cytoplasmic relocalization of its proapoptotic activator HIPK2. J Clin Invest 2007; 117: 693-702. (Pubitemid 46348527)
21. Reef S, Zalckvar E, Shifman O, Bialik S, Sabanay H, Oren M et al. A short mitochondria form of p19ARF induces autophagy and caspase-independent cell death. Mol Cell 2006; 22: 463-475.
22. Akao Y, Otsuki Y, Kataoka S, Ito Y, Tsujimoto Y. Multiple subcellular localization of bcl-2: detection in nuclear outer membrane, endoplasmic reticulum membrane, and mitochondrial membranes. Cancer Res 1994; 54: 2468-2471. (Pubitemid 24138742)
23. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P et al. p53 has a direct apoptogenic role at the mitochondria. Mol Cell 2003; 11: 577-590. (Pubitemid 36385115)
24. Deng X, Gao F, Flagg T, Anderson J, May S. BCL2's flexible loop domain regulates p53 binding and survival. Mol Cell Biol 2006; 26: 4421-4434. (Pubitemid 43877564)
25. Chipuk JE, Green DR. Dissecting p53-dependent apoptosis. Cell Death Differ 2006; 13: 994-1002.
26. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M et al. Direct activation of Bax by p53 mediates mitochondria membrane permeabilization and apoptosis. Science 2004; 303: 1010-1014. (Pubitemid 38209704)
27. Arima Y, Nitta M, Kuninaka S, Zhang D, Fujiwara T, Taya Y et al. Transcriptional blockade induces p53-dependent apoptosis associated with translocation of p53 to mitochondria. J Biol Chem 2005; 280: 19166-19176. (Pubitemid 41379623)
28. Fedele M, Visone R, De Martino I, Troncone G, Palmieri D, Battista S et al. HMGA2 induces pituitary tumorigenesis by enhancing E2F1 activity. Cancer Cell 2006; 9: 459-471. (Pubitemid 43832192)
29. Vallone D, Battista S, Pierantoni GM, Fedele M, Casalino L, Santoro M et al. Neoplastic transformation of rat thyroid cells requires the junB and fra-1 gene induction which is dependent on the HMGI-C gene product. EMBO J 1997; 16: 5310-5321. (Pubitemid 27380139)
30. Tessari MA, Gostissa M, Altamura S, Sgarra R, Rustighi A, Salvagno C et al. Transcriptional activation of the cyclin A gene by the architectural transcription factor HMGA2. Mol Cell Biol 2003; 23: 9104-9116. (Pubitemid 37499800)
31. Reeves R, Adair JE. Role of high mobility group (HMG) chromatin proteins in DNA repair. DNA Repair 2005; 4: 926-938. (Pubitemid 40961597)
32. Kim HP, Kelly J, Leonard WJ. The basis for IL-2-induced IL-2 receptor alpha chain gene regulation: importance of two widely separated IL-2 response elements. Immunity 2001; 15: 159-172. (Pubitemid 32728329)
33. De Martino I, Visone R, Fedele M, Petrocca F, Palmieri D, Martinez Hoyos J et al. Regulation of microRNA expression by HMGA1 proteins. Oncogene 2009; 28: 1432-1442.
34. Thuault S, Valcourt U, Petersen M, Manfioletti G, Heldin CH, Moustakas A. Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition. J Cell Biol 2006; 174: 175-183. (Pubitemid 44079853)
35. Cattaruzzi G, Altamura S, Tessari MA, Rustighi A, Giancotti V, Pucillo C et al. The second AT-hook of the architectural transcription factor HMGA2 is determinant for nuclear localization and function. Nucleic Acids Res 2007; 35: 1751-1760. (Pubitemid 47061647)
36. Pierantoni GM, Fedele M, Pentimalli F, Benvenuto G, Pero R, Viglietto G et al. High mobility group I (Y) proteins bind HIPK2, a serine-threonine kinase protein which inhibits cell growth. Oncogene 2001; 20: 6132-6141. (Pubitemid 32964425)
37. Pallante P, Federico A, Berlingieri MT, Bianco M, Ferraro A, Forzati F et al. Loss of the CBX7 gene expression correlates with a highly malignant phenotype in thyroid cancer. Cancer Res 2008; 68: 6770-6778.
38. Federico A, Pallante P, Bianco M, Ferraro A, Esposito F, Monti M et al. Chromobox protein homologue 7 protein, with decreased expression in human carcinomas, positively regulates E-cadherin expression by interacting with the histone deacetylase 2 protein. Cancer Res 2009; 69: 7079-7087.
39. Pentimalli F, Dentice M, Fedele M, Pierantoni GM, Cito L, Pallante P et al. Suppression of HMGA2 protein synthesis could be a tool for the therapy of well differentiated liposarcomas overexpressing HMGA2. Cancer Res 2003; 63: 7423-7427. (Pubitemid 37413484)