Mass spectrometric analysis of high-mobility group proteins and their post-translational modifications in normal and cancerous human breast tissues

Journal of Proteome Research

Volumn 6, Issue 6, 2007, Pages 2304-2314

  Zou, Yan ^a   Wang, Yinsheng ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Breast cancer; High mobility group proteins; Mass spectrometry; Metastasis; Post translational modifications

Indexed keywords

HIGH MOBILITY GROUP A PROTEIN; HIGH MOBILITY GROUP A1 PROTEIN; HIGH MOBILITY GROUP A1A PROTEIN; HIGH MOBILITY GROUP A1B PROTEIN; LYSINE; SERINE; UNCLASSIFIED DRUG;

ARTICLE; CANCER GROWTH; CANCER STAGING; CANCER TISSUE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; MASS SPECTROMETRY; METHYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION; PROTEIN MODIFICATION; TANDEM MASS SPECTROMETRY;

AMINO ACID SEQUENCE; BREAST; BREAST NEOPLASMS; FEMALE; HMGA1A PROTEIN; HMGA1B PROTEIN; HUMANS; LYSINE; METHYLATION; MOLECULAR SEQUENCE DATA; PROTEIN PROCESSING, POST-TRANSLATIONAL; SERINE; TANDEM MASS SPECTROMETRY;

EID: 34250851755     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr070072q     Document Type: Article

References (50)

1. Bustin, M.; Reeves, R. High-mobility-group chromosomal proteins: architectural components that facilitate chromatin function. Prog. Nucleic Acid Res. Mol. Biol. 1996, 54, 35-100.
2. Reeves, R. HMGA proteins: isolation, biochemical modifications, and nucleosome interactions. Methods Enzymol. 2004, 375, 297-322.
3. Reeves, R. Molecular biology of HMGA proteins: hubs of nuclear function. Gene 2001, 277, 63-81.
4. Reeves, R.; Beckerbauer, L. HMGI/Y proteins: flexible regulators of transcription and chromatin structure. Biochim. Biophysic. Acta 2001, 1519, 13-29.
5. Strauss, F.; Varshavsky, A. A protein binds to a satellite DNA repeat at three specific sites that would be brought into mutual proximity by DNA folding in the nucleosome. Cell 1984, 37, 889-901.
6. Solomon, M. J.; Strauss, F.; Varshavsky, A. A mammalian high mobility group protein recognizes any stretch of six A.T base pairs in duplex DNA. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 1276-80.
7. Reeves, R.; Elton, T. S.; Nissen, M. S.; Lehn, D.; Johnson, K. R. Posttranscriptional gene regulation and specific binding of the nonhistone protein HMG-I by the 3′ untranslated region of bovine interleukin 2 cDNA. Proc. Natl. Acad. Sci. U.S.A. 1987, 84, 6531-5.
8. Johnson, K. R.; Lehn, D. A.; Elton, T. S.; Barr, P. J.; Reeves, R. Complete murine cDNA sequence, genomic structure, and tissue expression of the high mobility group protein HMG-I(Y). J. Biol. Chem. 1988, 263, 18338-42.
9. Johnson, K. R.; Lehn, D. A.; Reeves, R. Alternative processing of mRNAs encoding mammalian chromosomal high-mobility-group proteins HMG-I and HMG-Y. Mol. Cell Biol. 1989, 9, 2114-23.
10. 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.
11. Dolde, C. E.; Mukherjee, M.; Cho, C.; Resar, L. M. HMG-I/Y in human breast cancer cell lines. Breast Cancer Res. Treat. 2002, 71, 181-91.
12. Treff, N. R.; Pouchnik, D.; Dement, G. A.; Britt, R. L.; Reeves, R. High-mobility group A1a protein regulates Ras/ERK signaling in MCF-7 human breast cancer cells. Oncogene 2004, 23, 777-85.
13. Takaha, N.; Hawkins, A. L.; Griffin, C. A.; Isaacs, W. B.; Coffey, D. S. High mobility group protein I(Y): a candidate architectural protein for chromosomal rearrangements in prostate cancer cells. Cancer Res. 2002, 62, 647-51.
14. Leman, E. S.; Madigan, M. C.; Brunagel, G.; Takaha, N.; Coffey, D. S.; Getzenberg, R. H. Nuclear matrix localization of high mobility group protein I(Y) in a transgenic mouse model for prostate cancer. J. Cell. Biochem. 2003, 88, 599-608.
15. 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, 1896-901.
16. Chiappetta, G.; Manfioletti, G.; Pentimalli, F.; Abe, N.; Di Bonito, M.; Vento, M. T.; 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, 147-51.
17. Abe, N.; Watanabe, T.; Izumisato, Y.; Suzuki, Y.; Masaki, T.; Mori, T.; Sugiyama, M.; Fusco, A.; Atomi, Y. High mobility group A1 is expressed in metastatic adenocarcinoma to the liver and intrahepatic cholangiocarcinoma, but not in hepatocellular carcinoma: its potential use in the diagnosis of liver neoplasms. J. Gastroenterol. 2003, 38, 1144-9.
18. Sarhadi, V. K.; Wikman, H.; Salmenkivi, K.; Kuosma, E.; Sioris, T.; Salo, J.; Karjalainen, A.; Knuutila, S.; Anttila, S. Increased expression of high mobility group A proteins in lung cancer. J. Pathol. 2006, 209, 206-12.
19. Chiappetta, G.; Tallini, G.; De Biasio, M. C.; Manfioletti, G.; Martinez-Tello, F. J.; Pentimalli, F.; de Nigris, F.; Mastro, A.; Botti, G.; Fedele, M.; Berger, N.; Santoro, M.; Giancotti, V.; Fusco, A. 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, 4193-8.
20. 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, 11354-61.
21. 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, 3575-85.
22. Banks, G. C.; Li, Y.; Reeves, R. Differential in vivo modifications of the HMGI(Y) nonhistone chromatin proteins modulate nucleosome and DNA interactions. Biochemistry 2000, 39, 8333-46.
23. Struhl, K. Gene regulation. A paradigm for precision. Science 2001, 293, 1054-5.
24. Munshi, N.; Agalioti, T.; Lomvardas, S.; Merika, M.; Chen, G.; Thanos, D. Coordination of a transcriptional switch by HMGI(Y) acetylation. Science 2001, 293, 1133-6.
25. Elton, T. S.; Reeves, R. Purification and postsynthetic modifications of Friend erythroleukemic cell high mobility group protein HMG-I. Anal. Biochem. 1986, 157, 53-62.
26. Giancotti, V.; Pani, B.; D'Andrea, P.; Berlingieri, M. T.; Di, Fiore, P. P.; Fusco, A.; Vecchio, G.; Philp, R.; Crane-Robinson, C.; Nicolas, R. H.; Wright, C. A.; Goodwin, G. H. Elevated levels of a specific class of nuclear phosphoproteins in cells transformed with v-ras and v-mos oncogenes and by cotransfection with c-myc and polyoma middle T genes. EMBO J. 1987, 6, 1981-7.
27. Palvimo, J.; Linnala-Kankkunen, A. Identification of sites on chromosomal protein HMG-I phosphorylated by casein kinase II. FEBS Lett. 1989, 257, 101-4.
28. Ferranti, P.; Malorni, A.; Marino, G.; Pucci, P.; Goodwin, G. H.; Manfioletti, G.; Giancotti, V. Mass spectrometric analysis of the HMGY protein from Lewis lung carcinoma. Identification of phosphorylation sites. J. Biol. Chem. 1992, 267, 22486-9.
29. Wang, D. Z.; Ray, P.; Boothby, M. Interleukin 4-inducible phosphorylation of HMG-I(Y) is inhibited by rapamycin. J. Biol. Chem. 1995, 270, 22924-32.
30. Zou, Y.; Wang, Y. Tandem mass spectrometry for the examination of the posttranslational modifications of high-mobility group A1 proteins: symmetric and asymmetric dimethylation of Arg25 in HMGA1a protein. Biochemistry 2005, 44, 6293-301.
31. Reeves, R.; Langan, T. A.; Nissen, M. S. Phosphorylation of the DNA-binding domain of nonhistone high-mobility group I protein by cdc2 kinase: reduction of binding affinity. Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 1671-5.
32. Nissen, M. S.; Langan, T. A.; Reeves, R. Phosphorylation by cdc2 kinase modulates DNA binding activity of high mobility group I nonhistone chromatin protein. J. Biol. Chem. 1991, 266, 19945-52.
33. Xiao, D. M.; Pak, J. H.; Wang, X.; Sato, T.; Huang, F. L.; Chen, H. C.; Huang, K. P. Phosphorylation of HMG-I by protein kinase C attenuates its binding affinity to the promoter regions of protein kinase C gamma and neurogranin/RC3 genes. J. Neurochem. 2000, 74, 392-9.
34. Sgarra, R.; Diana, F.; Rustighi, A.; Manfioletti, G.; Giancotti, V. Increase of HMGA1a protein methylation is a distinctive characteristic of leukaemic cells induced to undergo apoptosis. Cell Death Differ. 2003, 10, 386-9.
35. Edberg, D. D.; Bruce, J. E.; Siems, W. F.; Reeves, R. In vivo posttranslational modifications of the high mobility group a1a proteins in breast cancer cells of differing metastatic potential. Biochemistry 2004, 43, 11500-15.
36. Jiang, X.; Wang, Y. Acetylation and phosphorylation of high-mobility group A1 proteins in PC-3 human tumor cells. Biochemistry 2006, 45, 7194-201.
37. Munshi, N.; Merika, M.; Yie, J.; Senger, K.; Chen, G.; Thanos, D. Acetylation of HMG I(Y) by CBP turns off IFN beta expression by disrupting the enhanceosome. Mol. Cell 1998, 2, 457-67.
38. Zou, Y.; Jiang, X.; Wang, Y. Identification of novel in vivo phosphorylation sites in high mobility group N1 protein from the MCF-7 human breast cancer cells. Biochemistry 2004, 43, 6322-9.
39. Zougman, A.; Wisniewski, J. R. Beyond linker histones and high mobility group proteins: global profiling of perchloric acid soluble proteins. J. Proteome Res. 2006, 5, 925-34.
40. Gehrig, P. M.; Hunziker, P. E.; Zahariev, S.; Pongor, S. Fragmentation pathways of N(G)-methylated and unmodified arginine residues in peptides studied by ESI-MS/MS and MALDI-MS. J. Am. Soc. Mass Spectrom. 2004, 15, 142-9.
41. Brame, C. J.; Moran, M. F.; McBroom-Cerajewski, L. D. A mass spectrometry based method for distinguishing between symmetrically and asymmetrically dimethylated arginine residues. Rapid Commun. Mass Spectrom. 2004, 18, 877-81.
42. Evans, A.; Lennard, T. W.; Davies, B. R. High-mobility group protein 1(Y): metastasis-associated or metastasis-inducing? J. Surg. Oncol. 2004, 88, 86-99.
43. Ericsson, C.; Franzen, B.; Nister, M. Frozen tissue biobanks. Tissue handling, cryopreservation, extraction, and use for proteomic analysis. Acta Oncol. 2006, 45, 643-61.
44. Miranda, T. B.; Webb, K. J.; Edberg, D. D.; Reeves, R.; Clarke, S. Protein arginine methyltransferase 6 specifically methylates the nonhistone chromatin protein HMGA1a. Biochem. Biophys. Res. Commun. 2005, 336, 831-5.
45. 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.
46. McBride, A. E.; Silver, P. A. State of the arg: protein methylation at arginine comes of age. Cell 2001, 106, 5-8.
47. 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, 8961-73.
48. Reeves, R.; Edberg, D. D.; Li, Y. Architectural transcription factor HMGI(Y) promotes tumor progression and mesenchymal transition of human epithelial cells. Mol. Cell. Biol. 2001, 21, 575-94.
49. α and Src inhibitors. Oncogene 2006, 25, 3286-3295.
50. Pan, Q.; Bao, L. W.; Kleer, C. G.; Sabel, M. S.; Griffith, K. A.; Teknos, T. N.; Merajver, S. D. Protein kinase Cε is a predictive biomarker of aggressive breast cancer and a validated target for RNA interference anticancer therapy. Cancer Res. 2005, 65, 8366-8371.