Macroscopic differences in HMGA oncoproteins post-translational modifications: C-terminal phosphorylation of HMGA2 affects its DNA binding properties

Journal of Proteome Research

Volumn 8, Issue 6, 2009, Pages 2978-2989

  Sgarra, Riccardo ^a   Maurizio, Elisa ^a   Zammitti, Salvina ^a   Lo Sardo, Alessandra ^a   Giancotti, Vincenzo ^a   Manfioletti, Guidalberto ^a  

^a UNIVERSITY OF TRIESTE   (Italy)

Author keywords

Cancer; Chromatin; Mass spectrometry; Methylation; Phosphorylation

Indexed keywords

DNA; HIGH MOBILITY GROUP A PROTEIN; HIGH MOBILITY GROUP A2 PROTEIN; ONCOPROTEIN;

ARTICLE; CANCER CELL CULTURE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING;

AMINO ACID SEQUENCE; CELL LINE, TUMOR; CHROMATOGRAPHY, LIQUID; HMGA PROTEINS; HMGA2 PROTEIN; HMGN PROTEINS; HUMANS; MASS SPECTROMETRY; METHYLATION; MOLECULAR SEQUENCE DATA; NEOPLASMS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE ALIGNMENT; SERINE;

EID: 67049117516     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr900087r     Document Type: Article

References (40)

1. Hock, R.; Furusawa, T.; Ueda, T.; Bustin, M. HMG chromosomal proteins in development and disease. Trends Cell Biol. 2007, 17, 72-79. (Pubitemid 46206113)
2. Sgarra, R.; Rustighi, A.; Tessari, M. A.; Di Bernardo, J.; Altamura, S.; Fusco, A.; Manfioletti, G.; Giancotti, V. Nuclear phosphoproteins HMGA and their relationship with chromatin structure and cancer. FEBS Lett. 2004, 574, 1-8. (Pubitemid 39200885)
3. Fusco, A.; Fedele, M. Roles of HMGA proteins in cancer. Nat. Rev. Cancer 2007, 7, 899-910. (Pubitemid 350165857)
4. Fedele, M.; Visone, R.; De Martino, I.; Troncone, G.; Calmieri, D.; Battista, S.; Ciarmiello, A.; Pallante, P.; Arra, C.; Melillo, R. M.; Helin, K.; Croce, C. M.; Fusco, A. HMGA2 induces pituitary tumorigenesis by enhancing E2F1 activity. Cancer Cell 2006, 9, 459-471. (Pubitemid 43832192)
5. Pierantoni, G. M.; 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)
6. Frasca, F.; Rustighi, A.; Malaguarnera, R.; Altamura, S.; Vigneri, P.; Del Sal, G.; Giancotti, V.; Pezzino, V.; Vigneri, R.; Manfioletti, G. HMGA1 inhibits the function of p53 family members in thyroid cancer cells. Cancer Res. 2006, 66, 2980-2989.
7. Sgarra, R.; Tessari, M. A.; Di Bernardo, J.; Rustighi, A.; Zago, P.; Liberatori, S.; Armini, A.; Bini, L.; Giancotti, V.; Manfioletti, G. Discovering high mobility group A molecular partners in tumour cells. Proteomics 2005, 5, 1494-1506. (Pubitemid 40593259)
8. Pierantoni, G. M.; Esposito, F.; Giraud, S.; Bienvenut, W. V.; Diaz, J. J.; Fusco, A. Identification of new high mobility group A1 associated proteins. Proteomics 2007, 7, 3735-3742. (Pubitemid 350022279)
9. Sgarra, R.; Furlan, C.; Zammitti, S.; Lo Sardo, A.; Maurizio, E.; Di Bernardo, J.; Giancotti, V.; Manfioletti, G. Interaction proteomics of the HMGA chromatin architectural factors. Proteomics 2008, 8, 4721-4732.
10. Zhang, Q.; Wang, Y. High mobility group proteins and their posttranslational modifications. Biochim. Biophys. Acta 2008, 1784, 1159-1166.
11. Munshi, N.; Agalioti, T.; Lomvardas, S.; Merika, M.; Chen, G.; Thanos, D. Coordination of a transcriptional switch by HMGI(Y) acetylation. Science 2001, 293, 1133-1136. (Pubitemid 32758093)
12. Diana, F.; Sgarra, R.; Manfioletti, G.; Rustighi, A.; Poletto, D.; Sciortino, M. T.; Mastino, A.; Giancotti, V. A link between apoptosis and degree of phosphorylation of High Mobility Group A1a protein in leukemic cells. J. Biol. Chem. 2001, 276, 11354-11361. (Pubitemid 38089326)
13. Meggio, F.; Pinna, L. A. One-thousand-and-one substrates of protein kinase CK2? FASEB J. 2003, 17, 349-368. (Pubitemid 36292951)
14. Giancotti, V.; Bandiera, A.; Buratti, E.; Fusco, A.; Marzari, R.; Coles, B.; Goodwin, G. H. Comparison of multiple forms of the high mobility group I proteins in rodent and human cells. Identification of the human high mobility group I-C protein. Eur. J. Biochem. 1991, 23, 211-216.
15. Schwanbeck, R.; Manfioletti, G.; Wisniewski, J. R. Architecture of high mobility group protein I-C.DNA complex and its perturbation upon phosphorylation by Cdc2 kinase. J. Biol. Chem. 2000, 275, 1793-1801. (Pubitemid 30060801)
16. Di Agostino, S.; Fedele, M.; Chieffi, P.; Fusco, A.; Rossi, P.; Geremia, R.; Sette, C. Phosphorylation of high-mobility group protein A2 by Nek2 kinase during the first meiotic division in mouse spermatocytes. Mol. Biol. Cell 2004, 15, 1224-1232 (Pubitemid 38316229)
17. Sgarra, R.; Diana, F.; Bellarosa, C.; Dekleva, V.; Rustighi, A.; Toller, M.; Manfioletti, G.; Giancotti, V. During apoptosis of tumor cells HMGA1a protein undergoes methylation: identification of the modification site by mass spectrometry. Biochemistry 2003, 42, 3575-3585. (Pubitemid 36368652)
18. Zou, Y.; Webb, K.; Perna, A. D.; Zhang, Q.; Clarke, S.; Wang, Y. A mass spectrometric study on the in vitro methylation of HMGA1a and HMGA1b proteins by PRMTs: methylation specificity, the effect of binding to AT-rich duplex DNA, and the effect of C-terminal phosphorylation. Biochemistry 2007, 46, 7896-7906. (Pubitemid 47016071)
19. Osborne, T. C.; Obianyo, O.; Zhang, X.; Cheng, X.; Thompson, P. R. Protein arginine methyltransferase 1: positively charged residues in substrate peptides distal to the site of methylation are important for substrate binding and catalysis. Biochemistry 2007, 46, 13370-13381. (Pubitemid 350136376)
20. Goodwin, G. The high mobility group protein, HMGI-C. Int. J. Biochem. Cell Biol. 1998, 30, 761-766. (Pubitemid 28352737)
21. Meggio, F.; Pinna, L. A. One-thousand-and-one substrates of protein kinase CK2? FASEB J. 2003, 17, 349-368. (Pubitemid 36292951)
22. Marin, O.; Meggio, F.; Draetta, G.; Pinna, L. A. The consensus sequences for cdc2 kinase and for casein kinase-2 are mutually incompatible. A study with peptides derived from the beta-subunit of casein kinase-2. FEBS Lett. 1992, 301, 111-114.
23. Bianchi, M. E. Interaction of a protein from rat liver nuclei with cruciform DNA. EMBO J. 1988, 7, 843-849.
24. Brunetti, A.; Manfioletti, G.; Chiefari, E.; Goldfine, I. D.; Foti, D. Transcriptional regulation of human insulin receptor gene by the high-mobility group protein HMGI(Y). FASEB J. 2001, 15, 492-500. (Pubitemid 32141441)
25. Piekielko, A.; Drung, A.; Rogalla, P.; Schwanbeck, R.; Heyduk, T.; Gerharz, M.; Bullerdiek, J.; Wiśniewski, J. R. Distinct organization of DNA complexes of various HMGI/Y family proteins and their modulation upon mitotic phosphorylation. J. Biol. Chem. 2001, 276, 1984-1992. (Pubitemid 32109677)
26. Maher, J. F.; Nathans, D. Multivalent DNA-binding properties of the HMG-1 proteins. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 6716-6720. (Pubitemid 26230375)
27. Fedele, M.; Fidanza, V.; Battista, S.; Pentimalli, F.; Klein-Szanto, A. J.; Visone, R.; De Martino, I.; Curcio, A.; Morisco, C.; Del Vecchio, L.; Baldassarre, G.; Arra, C.; Viglietto, G.; Indolfi, C.; Croce, C. M.; Fusco, A. Haploinsufficiency of the Hmga1 gene causes cardiac hypertrophy and myelo-lymphoproliferative disorders in mice. Cancer Res. 2006, 66, 2536-2543.
28. Zhou, X.; Benson, K. F.; Ashar, H. R.; Chada, K. Mutation responsible for the mouse pygmy phenotype in the developmentally regulated factor HMGI-C. Nature (London) 1995, 376, 771-774.
29. Edberg, D. D.; Adkins, J. N.; Springer, D. L.; Reeves, R. Dynamic and differential in vivo modifications of the isoform HMGA1a and HMGA1b chromatin proteins. J. Biol. Chem. 2005, 280, 8961-8973. (Pubitemid 40409588)
30. Giancotti, V.; Bandiera, A.; Ciani, L.; Santoro, D.; Crane-Robinson, C.; Goodwin, G. H.; Boiocchi, M.; Dolcetti, R.; Casetta, B. High-mobility- group (HMG) proteins and histone H1 subtypes expression in normal and tumor tissues of mouse. Eur. J. Biochem. 1993, 213, 825-832. (Pubitemid 23125654)
31. Narita, M.; Narita, M.; Krizhanovsky, V.; Nuñez, S.; Chicas, A.; Hearn, S. A.; Myers, M. P.; Lowe, S. W. A novel role for high-mobility group a proteins in cellular senescence andheterochromatin formation. Cell 2006, 126, 503-514. (Pubitemid 44163608)
32. Zou, Y.; Wang, Y. Mass spectrometric analysis of high-mobility group proteins and their post-translational modifications in normal and cancerous human breast tissues. J. Proteome Res. 2007, 6, 2304-2314. (Pubitemid 46985118)
33. Fedele, M.; Berlingieri, M. T.; Scala, S.; Chiariotti, L.; Viglietto, G.; Rippel, V.; Bullerdiek, J.; Santoro, M.; Fusco, A. Truncated and chimeric HMGI-C genes induce neoplastic transformation of NIH3T3 murine fibroblasts. Oncogene 1998, 17, 413-418. (Pubitemid 28395904)
34. Li, Y.; Lu, J.; Prochownik, E. V. Dual role for SUMO E2 conjugase Ubc9 in modulating the transforming and growth-promoting properties of the HMGA1b architectural transcription factor. J. Biol. Chem. 2007, 282, 13363-13371. (Pubitemid 47100547)
35. Pierantoni, G. M.; 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 2003, 24, 1861-1869. (Pubitemid 38008527)
36. Wang, Q.; Zeng, M.; Wang, W.; Tang, J. The HMGB1 acidic tail regulates HMGB1 DNA binding specificity by a unique mechanism. Biochem. Biophys. Res. Commun. 2007, 360, 14-19. (Pubitemid 46992794)
37. Woods, A. S.; Ferré, S. Amazing stability of the arginine-phosphate electrostatic interaction. J. Proteome Res. 2005, 4, 1397-1402. (Pubitemid 41208697)
38. Odriozola, L.; Singh, G.; Hoang, T.; Chan, A. M. Regulation of PTEN activity by carboxyl-terminal autoinhibitory domain. J. Biol. Chem. 2007, 282, 23306-23315. (Pubitemid 47311930)
39. Raftopoulou, M.; Etienne-Manneville, S.; Self, A.; Nicholls, S.; Hall, A. Regulation of cell migration by the C2 domain of the tumor suppressor PTEN. Science 2004, 303, 1179-1181. (Pubitemid 38233580)
40. Marintcheva, B.; Marintchev, A.; Wagner, G.; Richardson, C. C. Acidic C-terminal tail of the ssDNA-binding protein of bacteriophage T7 and ssDNA compete for the same binding surface. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 1855-1860.