Conformational role for the C-terminal tail of the intrinsically disordered high mobility group A (HMGA) chromatin factors

Journal of Proteome Research

Volumn 10, Issue 7, 2011, Pages 3283-3291

  Maurizio, Elisa ^a   Cravello, Laetitia ^b   Brady, Liam ^b   Spolaore, Barbara ^c   Arnoldo, Laura ^a   Giancotti, Vincenzo ^a   Manfioletti, Guidalberto ^a   Sgarra, Riccardo ^a  

^a UNIVERSITY OF TRIESTE   (Italy)

^b WATERS CORPORATION   (United States)

^c UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP A PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; ELECTROSPRAY MASS SPECTROMETRY; ION MOBILITY SPECTROMETRY; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; CELL TRANSFORMATION, NEOPLASTIC; CHROMATIN; HMGA PROTEINS; HUMANS; METHYLATION; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEOMICS; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; STATIC ELECTRICITY;

EID: 79959941421     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200116w     Document Type: Article

References (39)

1. 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)
2. Sgarra, R.; Zammitti, S.; Lo Sardo, A.; Maurizio, E.; Arnoldo, L.; Pegoraro, S.; Giancotti, V.; Manfioletti, G. HMGA molecular network: From transcriptional regulation to chromatin remodeling Biochim. Biophys. Acta 2010, 1799, 37-47
3. Fusco, A.; Fedele, M. Roles of HMGA proteins in cancer Nat. Rev. Cancer 2007, 7, 899-910 (Pubitemid 350165857)
4. Thuault, S.; Valcourt, U.; Petersen, M.; Manfioletti, G.; Heldin, C. H.; Moustakas, A. Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition J. Cell Biol. 2006, 174, 175-83 (Pubitemid 44079853)
5. Tessari, M. A.; Gostissa, M.; Altamura, S.; Sgarra, R.; Rustighi, A.; Salvagno, C.; Caretti, G.; Imbriano, C.; Mantovani, R.; Del Sal, G.; Giancotti, V.; Manfioletti, G. Transcriptional activation of the cyclin A gene by the architectural transcription factor HMGA2 Mol. Cell. Biol. 2003, 23, 9104-16 (Pubitemid 37499800)
6. 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, 1554-63 (Pubitemid 44210358)
7. 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, 2980-89
8. Cleynen, I.; Van de Ven, W. J. The HMGA proteins: a myriad of functions Int. J. Oncol. 2008, 32, 289-305
9. Sgarra, R.; Maurizio, E.; Zammitti, S.; Lo Sardo, A.; Giancotti, V.; Manfioletti, G. Macroscopic differences in HMGA oncoproteins post-translational modifications: C-terminal phosphorylation of HMGA2 affects its DNA binding properties J. Proteome Res. 2009, 8, 2978-89
10. Zhang, Q.; Wang, Y. High mobility group proteins and their post-translational modifications Biochim. Biophys. Acta 2008, 1784, 1159-66
11. 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, 1861-69 (Pubitemid 38008527)
12. 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, 413-18 (Pubitemid 28395904)
13. 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, 13363-71 (Pubitemid 47100547)
14. Thuault, S.; Tan, E. J.; Peinado, H.; Cano, A.; Heldin, C. H.; Moustakas, A. HMGA2 and Smads co-regulate SNAIL1 expression during induction of epithelial-to-mesenchymal transition J. Biol. Chem. 2008, 283, 33437-46
15. Henriksen, J.; Stabell, M.; Meza-Zepeda, L. A.; Lauvrak, S. A.; Kassem, M.; Myklebost, O. Identification of target genes for wild type and truncated HMGA2 in mesenchymal stem-like cells BMC Cancer 2010, 10, 329
16. Uversky, V. N.; Dunker, A. K. Understanding protein non-folding Biochim. Biophys. Acta 2010, 1804, 1231-64
17. Uversky, V. N.; Oldfield, C. J.; Dunker, A. K. Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signaling J. Mol. Recognit. 2005, 18, 343-84 (Pubitemid 41341287)
18. Huth, J. R.; Bewley, C. A.; Nissen, M. S.; Evans, J. N.; Reeves, R.; Gronenborn, A. M.; Clore, G. M. The solution structure of an HMG-I(Y)-DNA complex defines a new architectural minor groove binding motif Nat. Struct. Biol. 1997, 4, 657-65 (Pubitemid 27323449)
19. Konermann, L.; Tong, X.; Pan, Y. Protein structure and dynamics studied by mass spectrometry: H/D exchange, hydroxyl radical labeling, and related approaches J. Mass Spectrom. 2008, 43, 1021-36
20. Yan, X.; Watson, J.; Ho, P. S.; Deinzer, M. L. Mass spectrometric approaches using electrospray ionization charge states and hydrogen-deuterium exchange for determining protein structures and their conformational changes Mol. Cell. Proteomics 2004, 3, 10-23 (Pubitemid 38701755)
21. Kanu, A. B.; Dwivedi, P.; Tam, M.; Matz, L.; Hill, H. H., Jr. Ion mobility-mass spectrometry J. Mass Spectrom. 2008, 43, 1-22 (Pubitemid 351251969)
22. Reeves, R.; Adair, J. E. Role of high mobility group (HMG) chromatin proteins in DNA repair DNA Repair (Amst) 2005, 4, 926-38 (Pubitemid 40961597)
23. Noro, B.; Licheri, B.; Sgarra, R.; Rustighi, A.; Tessari, M. A.; Chau, K. Y.; Ono, S. J.; Giancotti, V.; Manfioletti, G. Molecular dissection of the architectural transcription factor HMGA2 Biochemistry 2003, 42, 4569-77 (Pubitemid 36457626)
24. Frankel, A.; Yadav, N.; Lee, J.; Branscombe, T. L.; Clarke, S.; Bedford, M. T. The novel human protein arginine N-methyltransferase PRMT6 is a nuclear enzyme displaying unique substrate specificity J. Biol. Chem. 2002, 277, 3537-43 (Pubitemid 34953224)
25. Sgarra, R.; Lee, J.; Tessari, M. A.; Altamura, S.; Spolaore, B.; Giancotti, V.; Bedford, M. T.; Manfioletti, G. The AT-hook of the chromatin architectural transcription factor high mobility group A1a is arginine-methylated by protein arginine methyltransferase 6 J. Biol. Chem. 2006, 281, 3764-72 (Pubitemid 43847800)
26. Li, X.; Romero, P.; Rani, M.; Dunker, A. K.; Obradovic, Z. Predicting protein disorder for N-, C-, and internal regions Genome Inform. 1999, 10, 30-40
27. Kawase, T.; Sato, K.; Ueda, T.; Yoshida, M. Distinct domains in HMGB1 are involved in specific intramolecular and nucleosomal interactions Biochemistry 2008, 47, 13991-6
28. Watson, M.; Stott, K.; Thomas, J. O. Mapping intramolecular interactions between domains in HMGB1 using a tail-truncation approach J. Mol. Biol. 2007, 374, 1286-97 (Pubitemid 350122538)
29. 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, 14-9 (Pubitemid 46992794)
30. Knapp, S.; Müller, S.; Digilio, G.; Bonaldi, T.; Bianchi, M. E.; Musco, G. The long acidic tail of high mobility group box 1 (HMGB1) protein forms an extended and flexible structure that interacts with specific residues within and between the HMG boxes Biochemistry 2004, 43, 11992-7 (Pubitemid 39280544)
31. Pasheva, E.; Sarov, M.; Bidjekov, K.; Ugrinova, I.; Sarg, B.; Lindner, H.; Pashev, I. G. In vitro acetylation of HMGB-1 and -2 proteins by CBP: the role of the acidic tail Biochemistry 2004, 43, 2935-40 (Pubitemid 38327825)
32. Fontana, A.; Polverino de Laureto, P.; Spolaore, B.; Frare, E.; Picotti, P.; Zambonin, M. Probing protein structure by limited proteolysis Acta Biochim. Pol. 2004, 51, 299-321 (Pubitemid 38969296)
33. Fontana, A.; Polverino de Laureto, P.; De Filippis, V.; Scaramella, E.; Zambonin, M. Probing the partly folded states of proteins by limited proteolysis Fold. Des. 1997, 2, R17-26
34. Kaltashov, I. A.; Abzalimov, R. R. Do ionic charges in ESI MS provide useful information on macromolecular structure? J. Am. Soc. Mass. Spectrom. 2008, 19, 1239-46
35. Stuart, D.; Sellers, W. R. Linking somatic genetic alterations in cancer to therapeutics Curr. Opin. Cell Biol. 2009, 21, 304-10
36. Fedele, M.; Visone, R.; De Martino, I.; Palmieri, D.; Valentino, T.; Esposito, F.; Klein-Szanto, A.; Arra, C.; Ciarmiello, A.; Croce, C. M.; Fusco, A. Expression of a truncated Hmga1b gene induces gigantism, lipomatosis and B-cell lymphomas in mice Eur. J. Cancer 2010, 47, 470-8
37. 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, 1494-506 (Pubitemid 40593259)
38. Maasch, C.; Vater, A.; Buchner, K.; Purschke, W. G.; Eulberg, D.; Vonhoff, S.; Klussmann, S. Polyetheylenimine-polyplexes of Spiegelmer NOX-A50 directed against intracellular high mobility group protein A1 (HMGA1) reduce tumor growth in vivo J. Biol. Chem. 2010, 285, 40012-8
39. Halligan, B. D.; Ruotti, V.; Jin, W.; Laffoon, S.; Twigger, S. N.; Dratz, E. A. ProMoST (Protein Modification Screening Tool): A web-based tool for mapping protein modifications on two-dimensional gels Nucleic Acids Res. 2004, 32, W638-44