Identification of novel in vivo phosphorylation sites in high mobility group N1 protein from the MCF-7 human breast cancer cells

Biochemistry

Volumn 43, Issue 20, 2004, Pages 6322-6329

  Zou, Yan ^a   Jiang, Xinzhao ^a   Wang, Yinsheng ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOLOGICAL ORGANS; CELLS; DNA; TUMORS;

CHROMOSOMAL PROTEINS; SERINE;

PROTEINS;

CHROMOSOME PROTEIN; HIGH MOBILITY GROUP N1 PROTEIN; PROLINE; SERINE;

ACIDITY; AMINO ACID SEQUENCE; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CELL STRAIN MCF 7; CONTROLLED STUDY; ELECTRIC POTENTIAL; HUMAN; HUMAN CELL; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; HMGN1 PROTEIN; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDES; PHOSPHORYLATION; SERINE;

MINK CELL FOCUS-FORMING VIRUS;

EID: 2442686765     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0362828     Document Type: Article

References (40)

1. Bustin, M., and Reeves, R. (1996) High-mobility-group chromosomal proteins: architectural components that facilitate chromatin function. Prog. Nucleic Acid Res. Mol. Biol. 54, 35-100.
2. Bustin, M., Lehn, D. A., and Landsman, D. (1990) Structural features of the HMG chromosomal proteins and their genes. Biochim. Biophys. Acta 1049, 231-243.
3. Reeves, R., and Nissen, M. S. (1999) Purification and assays for high mobility group HMG-I(Y) protein function. Methods Enzymol. 304, 155-188.
4. Schwanbeck, R., and Wisniewski, J. R. (1997) Cdc2 and mitogen-activated protein kinases modulate DNA binding properties of the putative transcriptional regulator Chironomus high mobility group protein I. J. Biol. Chem. 272, 27476-27483.
5. Bustin, M. (2001) Chromatin unfolding and activation by HMGN* chromosomal proteins. Trends Biochem. Sci. 26, 431-437.
6. Bustin, M. (2001) Revised nomenclature for high mobility group (HMG) chromosomal proteins. Trends Biochem. Sci. 26, 152-153.
7. Sandeen, G., Wood, W. I., and Felsenfeld, G. (1980) The interaction of high mobility proteins HMG14 and 17 with nucleosomes. Nucleic Acids Res. 8, 3757-3778.
8. Shirakawa, H., Herrera, J. E., Bustin, M., and Postnikov, Y. (2000) Targeting of high mobility group-14/-17 proteins in chromatin is independent of DNA sequence. J. Biol. Chem. 275, 37937-37944.
9. Birger, Y., West, K. L., Postnikov, Y. V., Lim, J. H., Furusawa, T., Wagner, J. P., Laufer, C. S., Kraemer, K. H., and Bustin, M. (2003) Chromosomal protein HMGN1 enhances the rate of DNA repair in chromatin. EMBO J. 22, 1665-1675.
10. Bhorjee, J. S. (1981) Differential phosphorylation of nuclear nonhistone high mobility group proteins HMG 14 and HMG 17 during the cell cycle. Proc. Natl. Acad. Sci. U.S.A. 78, 6944-6948.
11. Palvimo, J., Mahonen, A., and Maenpaa, P. H. (1987) Phosphorylation of high-mobility-group chromatin proteins by protein kinase C from rat brain. Biochim. Biophys. Acta 931, 376-383.
12. Palvimo, J., and Maenpaa, P. H. (1988) Binding of high-mobility-group proteins HMG 14 and HMG 17 to DNA and histone H1 as influenced by phosphorylation. Biochim. Biophys. Acta 952, 172-180.
13. Bergel, M., Herrera, J. E., Thatcher, B. J., Prymakowska-Bosak, M., Vassilev, A., Nakatani, Y., Martin, B., and Bustin, M. (2000) Acetylation of novel sites in the nucleosomal binding domain of chromosomal protein HMG-14 by p300 alters its interaction with nucleosomes. J. Biol. Chem. 275, 11514-11520.
14. Reeves, R., Chang, D., and Chung, S. C. (1981) Carbohydrate modifications of the high mobility group proteins. Proc. Natl. Acad. Sci. U.S.A. 78, 6704-6708.
15. Lund, T., and Berg, K. (1991) Metaphase-specific phosphorylations weaken the association between chromosomal proteins HMG 14 and 17, and DNA. FEBS Lett. 289, 113-116.
16. Spaulding, S. W., Fucile, N. W., Bofinger, D. P., and Sheflin, L. G. (1991) Cyclic adenosine 3′, 5′-monophosphate-dependent phosphorylation of HMG 14 inhibits its interactions with nucleosomes. Mol. Endocrinol. 5, 42-50.
17. Prymakowska-Bosak, M., Misteli, T., Herrera, J. E., Shirakawa, H., Birger, Y., Garfield, S., and Bustin, M. (2001) Mitotic phosphorylation prevents the binding of HMGN proteins to chromatin. Mol. Cell. Biol. 21, 5169-5178.
18. Prymakowska-Bosak, M., Hock, R., Catez, F., Lim, J. H., Birger, Y., Shirakawa, H., Lee, K., and Bustin, M. (2002) Mitotic phosphorylation of chromosomal protein HMGN1 inhibits nuclear import and promotes interaction with 14.3.3 proteins. Mol. Cell. Biol. 22, 6809-6819.
19. Walton, G. M., Spiess, J., and Gill, G. N. (1982) Phosphorylation of high mobility group 14 protein by cyclic nucleotide-dependent protein kinases. J. Biol. Chem. 257, 4661-4668.
20. Bofinger, D. P., Fucile, N. W., and Spaulding, S. W. (1988) A one-step preparative method for separating SER 6-phosphorylated HMG 14 from unphosphorylated HMG 14 and in vitro phosphorylation reaction components. Anal. Biochem. 170, 9-18.
21. Palvimo, J., Linnala-Kankkunen, A., and Maenpaa, P. H. (1983) Differential phosphorylation of high mobility group protein hmg 14 from calf thymus and avian erythrocytes by a cyclic gmp-dependent protein kinase. Biochem. Biophys. Res. Commun. 110, 378-382.
22. Walton, G. M., Spiess, J., and Gill, G. N. (1985) Phosphorylation of high mobility group protein 14 by casein kinase II. J. Biol. Chem. 260, 4745-4750.
23. Barratt, M. J., Hazzalin, C. A., Zhelev, N., and Mahadevan, L. C. (1994) A mitogen- and anisomycin-stimulated kinase phosphorylates HMG-14 in its basic amino-terminal domain in vivo and on isolated mononucleosomes. EMBO J. 13, 4524-4535.
24. Louie, D. F., Gloor, K. K., Galasinski, S. C., Resing, K. A., and Ahn, N. G. (2000) Phosphorylation and subcellular redistribution of high mobility group proteins 14 and 17, analyzed by mass spectrometry. Protein Sci. 9, 170-179.
25. Cano, E., Hazzalin, C. A., Kardalinou, E., Buckle, R. S., and Mahadevan, L. C. (1995) Neither ERK nor JNK/SAPK MAP kinase subtypes are essential for histone H3/HMG-14 phosphorylation or c-fos and c-jun induction. J. Cell Sci. 108, 3599-3609.
26. Hazzalin, C. A., Cano, E., Cuenda, A., Barratt, M. J., Cohen, P., and Mahadevan, L. C. (1996) p38/RK is essential for stress-induced nuclear responses: JNK/SAPKs and c-Jun/ATF-2 phosphorylation are insufficient. Curr. Biol. 6, 1028-1031.
27. Thomson, S., Clayton, A. L., Hazzalin, C. A., Rose, S., Barratt, M. J., and Mahadevan, L. C. (1999) The nucleosomal response associated with immediate-early gene induction is mediated via alternative MAP kinase cascades: MSK1 as a potential histone H3/HMG-14 kinase. EMBO J. 18, 4779-4793.
28. Soloaga, A., Thomson, S., Wiggin, G. R., Rampersaud, N., Dyson, M. H., Hazzalin, C. A., Mahadevan, L. C., and Arthur, J. S. (2003) MSK2 and MSK1 mediate the mitogen- and stress-induced phosphorylation of histone H3 and HMG-14. EMBO J. 22, 2788-2797.
29. Walton, G. M., and Gill, G. N. (1983) Identity of the in vivo phosphorylation site in high mobility group 14 protein in HeLa cells with the site phosphorylated by casein kinase II in vitro. J. Biol. Chem. 258, 4440-4446.
30. Resing, K. A., Johnson, R. S., and Walsh, K. A. (1995) Mass spectrometric analysis of 21 phosphorylation sites in the internal repeat of rat profilaggrin, precursor of an intermediate filament associated protein. Biochemistry 34, 9477-9487.
31. Ferranti, P., Malorni, A., Marino, G., Pucci, P., Goodwin, G. H., Manfioletti, G., and Giancotti, V. (1992) Mass spectrometric analysis of the HMGY protein from Lewis lung carcinoma. Identification of phosphorylation sites. J. Biol. Chem 267, 22486-22489.
32. Banks, G. C., Li, Y., and Reeves, R. (2000) Differential in vivo modifications of the HMGI(Y) nonhistone chromatin proteins modulate nucleosome and DNA interactions. Biochemistry 39, 8333-8346.
33. Diana, F., Sgarra, R., Manfioletti, G., Rustighi, A., Poletto, D., Sciortino, M. T., Mastino, A., and Giancotti, V. (2001) A link between apoptosis and degree of phosphorylation of high mobility group A1a protein in leukemic cells. J. Biol. Chem. 276, 11354-11361.
34. Sgarra, R., Diana, F., Bellarosa, C., Dekleva, V., Rustighi, A., Toller, M., Manfioletti, G., and Giancotti, V. (2003) During apoptosis of tumor cells HMGA1a protein undergoes methylation: identification of the modification site by mass spectrometry. Biochemistry 42, 3575-3585.
35. Trieschmann, L., Postnikov, Y. V., Rickers, A., and Bustin, M. (1995) Modular structure of chromosomal proteins HMG-14 and HMG-17: definition of a transcriptional enhancement domain distinct from the nucleosomal binding domain. Mol. Cell. Biol. 15, 6663-6669.
36. Catez, F., Brown, D. T., Misteli, T., and Bustin, M. (2002) Competition between histone H1 and HMGN proteins for chromatin binding sites. EMBO Rep. 3, 760-766.
37. Lim, J. H., Bustin, M., Ogryzko, V. V., and Postnikov, Y. V. (2002) Metastable macromolecular complexes containing high mobility group nucleosome-binding chromosomal proteins in HeLa nuclei. J. Biol. Chem. 277, 20774-20782.
38. Lu, K. P., Liou, Y. C., and Zhou, X. Z. (2002) Pinning down proline-directed phosphorylation signaling. Trends Cell. Biol. 12, 164-172.
39. Lu, K. P., Hanes, S. D., and Hunter, T. (1996) A human peptidylprolyl isomerase essential for regulation of mitosis. Nature 380, 544-547.
40. Wulf, G. M., Ryo, A., Wulf, G. G., Lee, S. W., Niu, T., Petkova, V., and Lu, K. P. (2001) Pinl is overexpressed in breast cancer and cooperates with Ras signaling in increasing the transcriptional activity of c-Jun towards cyclin D1. EMBO J. 20, 3459-3472.