Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1

Molecular and Cellular Biology

Volumn 23, Issue 8, 2003, Pages 2953-2968

  Hietakangas, Ville ^a   Ahlskog, Johanna K ^a,b   Jakobsson, Annika M ^a,b   Hellesuo, Maria ^a   Sahlberg, Niko M ^a   Holmberg, Carina I ^a,e   Mikhailov, Andrey ^a   Palvimo, Jorma J ^c   Pirkkala, Lila ^a,f   Sistonen, Lea ^a,b,d  

^a UNIVERSITY OF TURKU   (Finland)

^b ÅBO AKADEMI UNIVERSITY   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d TURKU CENTRE FOR BIOTECHNOLOGY   (Finland)

^e NORTHWESTERN UNIVERSITY   (United States)

^f Hormos Medical Ltd   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR 1; LYSINE; SERINE; SUMO 1 PROTEIN; SUMO 2 PROTEIN; SUMO PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; HEAT SHOCK RESPONSE; HEAT STRESS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MUTANT; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; TRANSCRIPTION INITIATION; UPREGULATION;

AMINO ACID SEQUENCE; BINDING SITES; CELL NUCLEUS; DNA-BINDING PROTEINS; HEAT-SHOCK RESPONSE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; K562 CELLS; LYSINE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SERINE; SUMO-1 PROTEIN; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UBIQUITINS;

EID: 0037385213     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.8.2953-2968.2003     Document Type: Article

References (66)

1. Appella, E., and C. W. Anderson. 2001. Post-translational modifications and activation of p53 by genotoxic stresses. Eur. J. Biochem. 268:2764-2772.
2. Ben-Neriah, Y. 2002. Regulatory functions of ubiquitination in the immune system. Nat. Immunol. 3:20-26.
3. Bies, J., J. Markus, and L. Wolff. 2002. Covalent attachment of the SUMO-1 protein to the negative regulatory domain of the c-Myb transcription factor modifies its stability and transactivation capacity. J. Biol. Chem. 277:8999-9009.
4. Chu, B., F. Soncin, B. D. Price, M. A. Stevenson, and S. K. Calderwood. 1996. Sequential phosphorylation by mitogen-activated protein kinase and glycogen synthase kinase 3 represses transcriptional activation by heat shock factor-1. J. Biol. Chem. 271:30847-30857.
5. Chu, B., R. Zhong, F. Soncin, M. A. Stevenson, and S. K. Calderwood. 1998. Transcriptional activity of heat shock factor 1 at 37°C is repressed through phosphorylation on two distinct serine residues by glycogen synthase kinase 3 and protein kinases Cα and Cζ. J. Biol. Chem. 273:18640-18646.
6. Cotto, J., S. Fox, and R. Morimoto. 1997. HSF1 granules: a novel stress-induced nuclear compartment of human cells. J. Cell Sci. 110:2925-2934.
7. Cotto, J. J., M. Kline, and R. I. Morimoto. 1996. Activation of heat shock factor 1 DNA binding precedes stress-induced serine phosphorylation. Evidence for a multistep pathway of regulation. J. Biol. Chem. 271:3355-3358.
8. 2-terminal kinase targeting and phosphorylation of heat shock factor-1 suppress its transcriptional activity. J. Biol. Chem. 275:18210-18218.
9. Desterro, J. M., M. S. Rodriguez, and R. T. Hay. 1998. SUMO-1 modification of IκBα inhibits NF-κB activation. Mol. Cell 2:233-239.
10. Duprez, E., A. J. Saurin, J. M. Desterro, V. Lallemand-Breitenbach, K. Howe, M. N. Boddy, E. Solomon, H. de The, R. T. Hay, and P. S. Freemont. 1999. SUMO-1 modification-of the acute promyelocytic leukaemia protein PML: implications for nuclear localisation. J. Cell Sci. 112:381-393.
11. Eloranta, J. J., and H. C. Hurst. 2002. Transcription factor AP-2 interacts with the SUMO-conjugating enzyme UBC9 and is sumolated in vivo. J. Biol. Chem. 277:30798-30804,
12. Fogal, V., M. Gostissa, P. Sandy, P. Zacchi, T. Sternsdorf, K. Jensen, P. P. Pandolfi, H. Will, C. Schneider, and G. Del Sal. 2000. Regulation of p53 activity in nuclear bodies by a specific PML isoform. EMBO J. 19:6185-6195.
13. Gostissa, M., A. Hengstermann, V. Fogal, P. Sandy, S. E. Schwarz, M. Scheffner, and G. Del Sal. 1999. Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J. 18:6462-6471.
14. Green, M., T. J. Schuetz, E. K. Sullivan, and R. E. Kingston. 1995. A heat shock-responsive domain of human HSF1 that regulates transcription activation domain function. Mol. Cell. Biol. 15:3354-3362.
15. Hartl, F. U., and M. Hayer-Hartl. 2002. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852-1858.
16. He, B., Y. H. Meng, and N. F. Mivechi. 1998. Glycogen synthase kinase 3β and extracellular signal-regulated kinase inactivate heat shock transcription factor 1 by facilitating the disappearance of transcriptionally active granules after heat shock. Mol. Cell. Biol. 18:6624-6633.
17. Holmberg, C. I., V. Hietakangas, A. Mikhailov, J. O. Rantanen, M. Kallio, A. Meinander, J. Hellman, N. Morrice, C. MacKintosh, R. I. Morimoto, J. E. Eriksson, and L. Sistonen. 2001. Phosphorylation of serine 230 promotes inducible transcriptional activity of heat shock factor 1. EMBO J. 20:3800-3810.
18. Holmberg, C. I., S. A. Illman, M. Kallio, A. Mikhailov, and L. Sistonen. 2000. Formation of nuclear HSF1 granules varies depending on stress stimuli. Cell Stress Chaperones 5:219-228.
19. Hong, Y., R. Rogers, M. J. Matunis, C. N. Mayhew, M. Goodson, O.-K. Park-Sarge, and K. D. Sarge. 2001. Regulation of heat shock transcription factor 1 by stress-induced SUMO-1 modification. J. Biol. Chem. 276:40263-40267.
20. Ishov, A. M., A. G. Sotnikov, D. Negorev, O. V. Vladimirova, N. Neff, T. Kamitani, E. T. Yeh, J. F. Strauss III, and G. G. Maul. 1999. PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J. Cell Biol. 147:221-234.
21. Jackson, P. K. 2001. A new RING for SUMO: wrestling transcriptional responses into nuclear bodies with PIAS family E3 SUMO ligases. Genes Dev. 15:3053-3058.
22. Johnson, E. S., and G. Blobel. 1997. Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J. Biol. Chem. 272:26799-26802.
23. Johnson, E. S., and A. A. Gupta. 2001. An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106:735-744.
24. Johnson, E. S., I. Schwienhorst, R. J. Dohmen, and G. Blobel. 1997. The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J. 16:5509-5519.
25. Jolly, C., and R. I. Morimoto. 1999. Stress and the cell nucleus: dynamics of gene expression and structural reorganization. Gene Expr. 7:261-270.
26. Jolly, C., L. Konecny, D. L. Grady, Y. A. Kutskova, J. J. Cotto, R. I. Morimoto, and C. Vourch. 2002. In vivo binding of active heat shock transcription factor 1 to human chromosome 9 heterochromatin during stress. J. Cell Biol. 156:775-781.
27. Jolly, C., R. I. Morimoto, M. Robert-Nicoud, and C. Vourc'h. 1997. HSF1 transcription factor concentrates in nuclear foci during heat shock: relationship with transcription sites. J. Cell Sci. 110:2935-2941.
28. Jolly, C., Y. Usson, and R. I. Morimoto. 1999. Rapid and reversible relocalization of heat shock factor 1 within seconds to nuclear stress granules. Proc. Natl. Acad. Sci. USA 96:6769-6774.
29. Kahyo, T., T. Nishida, and H. Yasuda. 2001. Involvement of PIAS1 in the sumoylation of tumor suppressor p53. Mol. Cell 8:713-718.
30. Kirsh, O., J. S. Seeler, A. Pichler, A. Gast, S. Muller, E. Miska, M. Mathieu, A. Harel-Bellan, T. Kouzarides, F. Melchior, and A. Dejean. 2002. The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. EMBO J. 21:2682-2691.
31. Kline, M. P., and R. I. Morimoto. 1997. Repression of the heat shock factor 1 transcriptional activation domain is modulated by constitutive phosphorylation. Mol. Cell. Biol. 17:2107-2115.
32. Knauf, U., E. M. Newton, J. Kyriakis, and R. E. Kingston. 1996. Repression of human heat shock factor 1 activity at control temperature by phosphorylation. Genes Dev. 10:2782-2793.
33. Kotaja, N., U. Karvonen, O. A. Jänne, and J. J. Palvimo. 2002. PIAS proteins modulate transcription factors by functioning as SUMO-1 ligases. Mol. Cell. Biol. 22:5222-5234.
34. Lindquist, S., and E. A. Craig. 1988. The heat-shock proteins. Annu. Rev. Genet. 22:631-677.
35. McMillan, D. R., X. Xiao, L. Shao, K. Graves, and I. J. Benjamin. 1998. Targeted disruption of heat shock transcription factor 1 abolishes thermotolerance and protection against heat-inducible apoptosis. J. Biol. Chem. 273:7523-7528.
36. Melchior, F. 2000. SUMO - nonclassical ubiquitin. Annu. Rev. Cell Dev. Biol. 16:591-626.
37. Morimoto, R. I. 1998. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12:3788-3796.
38. Mosser, D. D., N. G. Theodorakis, and R. I. Morimoto. 1988. Coordinate changes in'heat shock element-binding activity and HSP70 gene transcription rates in human cells. Mol. Cell. Biol. 8:4736-4744.
39. Müller, S., M. Berger, F. Lehembre, J. S. Seeler, Y. Haupt, and A. Dejean. 2000. c-Jun and p53 activity is modulated by SUMO-1 modification. J. Biol. Chem. 275:13321-13329.
40. Müller, S., M. J. Matunis, and A. Dejean. 1998. Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus. EMBO J. 17:61-70.
41. Nakai, A., M. Tanabe, Y. Kawazoe, J. Inazawa, R. I. Morimoto, and K. Nagata. 1997. HSF4, a new member of the human heat shock factor family which lacks properties of a transcriptional activator. Mol. Cell. Biol. 17:469-481.
42. Newton, E. M., U. Knauf, M. Green, and R. E. Kingston. 1996. The regulatory domain of human heat shock factor 1 is sufficient to sense heat stress. Mol. Cell. Biol. 16:839-846.
43. Pichler, A., A. Gast, J. S. Seeler, A. Dejean, and F. Melchior. 2002. The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108:109-120.
44. Pirkkala, L., T.-P. Alastalo, X. Zuo, I. J. Benjamin, and L. Sistonen. 2000. Disruption of heat shock factor 1 reveals an essential role in the ubiquitin proteolytic pathway. Mol. Cell. Biol. 20:2670-2675.
45. Pirkkala, L., P. Nykiinen, and L. Sistonen. 2001. Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J. 15:1118-1131.
46. Poukka, H., U. Karvonen, O. A. Jänne, and J. J. Palvimo. 2000. Covalent modification of the androgen receptor by small ubiquitin-like modifier 1 (SUMO-1). Proc. Natl. Acad. Sci. USA 97:14145-14150.
47. Rabindran, S. K., G. Giorgi, J. Clos, and C. Wu. 1991. Molecular cloning and expression of a human heat shock factor, HSF1. Proc. Natl. Acad. Sci. USA 88:6906-6910.
48. Rodriguez, M. S., C. Dargemont, and R. T. Hay. 2001. SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276:12654-12659.
49. Rodriguez, M. S., J. M. Desterro, S. Lain, C. A. Midgley, D. P. Lane, and R. T. Hay. 1999. SUMO-1 modification activates the transcriptional response of p53. EMBO J. 18:6455-6461.
50. Sachdev, S., L. Bruhn, H. Sieber, A. Pichler, F. Melchior, and R. Grosschedl. 2001. PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev. 15:3088-3103.
51. Saitoh, H., and J. Hinchey. 2000. Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 275:6252-6258.
52. Sapetschnig, A., G. Rischitor, H. Braun, A. Doll, M. Schergaut, F. Melchior, and G. Suske. 2002. Transcription factor Sp3 is silenced through SUMO modification by PIAS1. EMBO J. 21:5206-5215.
53. Sarge, K. D., S. P. Murphy, and R. I. Morimoto. 1993. Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Mol. Cell. Biol. 13:1392-1407.
54. Sarge, K. D., V. Zimarino, K. Holm, C. Wu, and R. I. Morimoto. 1991. Cloning and characterization of two mouse heat shock factors with distinct inducible and constitutive DNA-binding ability. Genes Dev. 5:1902-1911.
55. Schmidt, D., and S. Müller. 2002. Members of the PIAS family act as SUMO ligases for c-Jun and p53 and repress p53 activity. Proc. Natl. Acad. Sci. USA 99:2872-2877.
56. Schuetz, T. J., G. J. Gallo, L. Sheldon, P. Tempst, and R. E. Kingston. 1991. Isolation of a cDNA for HSF2: evidence for two heat shock factor genes in humans. Proc. Natl. Acad. Sci. USA 88:6911-6915.
57. Seeler, J. S., and A. Dejean. 2001. SUMO: of branched proteins and nuclear bodies. Oncogene 20:7243-7249.
58. Shi, Y., P. E. Kroeger, and R. I. Morimoto. 1995. The carboxyl-terminal transactivation domain of heat shock factor 1 is negatively regulated and stress responsive. Mol. Cell. Biol. 15:4309-4318.
59. Subramanian, L., M. D. Benson, and J. A. Iniguez-Lluhi. A synergy control motif within the attenuator domain of C/EBPα inhibits transcriptional synergy through its PIASy-enhanced modification by SUMO-1 or SUMO-3. J. Biol. Chem., in press.
60. Takahashi, Y., T. Kahyo, A. Toh-E, H. Yasuda, and Y. Kikuchi. 2001. Yeast Ull1/Siz1 is a novel SUMO1/Smt3 ligase for septin components and functions as an adaptor between conjugating enzyme and substrates. J. Biol. Chem. 276:48973-48977.
61. Wilson, V. G., and D. Rangasamy. 2001. Intracellular targeting of proteins by sumoylation. Exp. Cell Res. 271:57-65.
62. Wu, C. 1995. Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 11:441-469.
63. Xia, W., and R. Voellmy. 1997. Hyperphosphorylation of heat shock transcription factor 1 is correlated with transcriptional competence and slow dissociation of active factor trimers. J. Biol. Chem. 272:4094-4102.
64. Xiao, X., X. Zuo, A. A. Davis, D. R. McMillan, B. B. Curry, J. A. Richardson, and I. J. Benjamin. 1999. HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J. 18:5943-5952.
65. Zhong, S., S. Müller, S. Ronchetti, P. S. Freemont, A. Dejean, and P. P. Pandolfi. 2000. Role of SUMO-1-modified PML in nuclear body formation. Blood 95:2748-2752.
66. Zuo, J., D. Rungger, and R. Voellmy. 1995. Multiple layers of regulation of human heat shock transcription factor 1. Mol. Cell. Biol. 15:4319-4330.