Small heat-shock protein Hsp9 has dual functions in stress adaptation and stress-induced G2-M checkpoint regulation via Cdc25 inactivation in Schizosaccharomyces pombe

Biochemical and Biophysical Research Communications

Volumn 417, Issue 1, 2012, Pages 613-618

  Ahn, Jiwon ^a,c   Won, Misun ^a   Choi, Jeong Hae ^a   Kyun, Mi Lang ^a,d   Cho, Hae Sung ^a   Park, Hee Moon ^c   Kang, Chang Mo ^b   Chung, Kyung Sook ^a  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b Korea Institute of Radiation and Medical Science   (South Korea)

^c Chungnam National University   (South Korea)

^d University of Science and Technology (UST)   (South Korea)

Author keywords

14 3 3; Cdc25; G2 M checkpoint; Hsp9; Small heat shock protein; Stress

Indexed keywords

HEAT SHOCK PROTEIN 90; PROTEIN TYROSINE PHOSPHATASE;

ARTICLE; CELL CYCLE; CELL CYCLE REGULATION; CELL DEATH; CELL GROWTH; CELL STRESS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FUNGAL CELL; FUNGAL GENE; G2 PHASE CELL CYCLE CHECKPOINT; GENE DELETION; GENE OVEREXPRESSION; HEAT SENSITIVITY; HEAT TOLERANCE; IMMUNOPRECIPITATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SCHIZOSACCHAROMYCES POMBE;

14-3-3 PROTEINS; ADAPTATION, PHYSIOLOGICAL; G2 PHASE CELL CYCLE CHECKPOINTS; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; M PHASE CELL CYCLE CHECKPOINTS; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; SCHIZOSACCHAROMYCES POMBE PROTEINS;

SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

EID: 84855771386     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2011.12.017     Document Type: Article

References (33)

1. Kregel K.C. Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J. Appl. Physiol. 2002, 92:2177-2186.
2. Feder M.E., Hofmann G.E. Heat-shock proteins Molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 1999, 61:243-282.
3. Nakamoto H., Vigh L. The small heat shock proteins and their clients. Cell Mol. Life Sci. 2007, 64:294-306.
4. Eyles S.J., Gierasch L.M. Nature's molecular sponges: small heat shock proteins grow into their chaperone roles. Proc. Natl. Acad. Sci. USA 2010, 107:2727-2728.
5. Fu X., Liu C., Liu Y., Feng X., Gu L., Chen X., Chang Z. Small heat shock protein Hsp16.3 modulates its chaperone activity by adjusting the rate of oligomeric dissociation. Biochem. Biophys. Res. Commun. 2003, 310:412-420.
6. Michaud S., Morrow G., Marchand J., Tanguay R.M. Drosophila small heat shock proteins: cell and organelle-specific chaperones?. Prog. Mol. Subcell Biol. 2002, 28:79-101.
7. Jonak C., Mildner M., Klosner G., Paulitschke V., Kunstfeld R., Pehamberger H., Tschachler E., Trautinger F. The hsp27kD heat shock protein and p38-MAPK signaling are required for regular epidermal differentiation. J. Dermatol. Sci. 2011, 61:32-37.
8. Wieske M., Benndorf R., Behlke J., Dolling R., Grelle G., Bielka H., Lutsch G. Defined sequence segments of the small heat shock proteins HSP25 and alphaB-crystallin inhibit actin polymerization. Eur. J. Biochem. 2001, 268:2083-2090.
9. Pivovarova A.V., Mikhailova V.V., Chernik I.S., Chebotareva N.A., Levitsky D.I., Gusev N.B. Effects of small heat shock proteins on the thermal denaturation and aggregation of F-actin. Biochem. Biophys. Res. Commun. 2005, 331:1548-1553.
10. Yagi H., Sato A., Yoshida A., Hattori Y., Hara M., Shimamura J., Sakane I., Hongo K., Mizobata T., Kawata Y. Fibril formation of hsp10 homologue proteins and determination of fibril core regions: differences in fibril core regions dependent on subtle differences in amino acid sequence. J. Mol. Biol. 2008, 377:1593-1606.
11. Ling J., Zhao K., Cui Y.G., Li Y., Wang X., Li M., Xue K., Ma X., Liu J.Y. Heat shock protein 10 regulated apoptosis of mouse ovarian granulosa cells. Gynecol. Endocrinol. 2011, 27:63-71.
12. Arrigo A.P., Paul C., Ducasse C., Manero F., Kretz-Remy C., Virot S., Javouhey E., Mounier N., Diaz-Latoud C. Small stress proteins: novel negative modulators of apoptosis induced independently of reactive oxygen species. Prog. Mol. Subcell Biol. 2002, 28:185-204.
13. Dabir D.V., Trojanowski J.Q., Richter-Landsberg C., Lee V.M., Forman M.S. Expression of the small heat-shock protein alphaB-crystallin in tauopathies with glial pathology. Am. J. Pathol. 2004, 164:155-166.
14. Song T.F., Zhang Z.F., Liu L., Yang T., Jiang J., Li P. Small interfering RNA-mediated silencing of heat shock protein 27 (HSP27) Increases chemosensitivity to paclitaxel by increasing production of reactive oxygen species in human ovarian cancer cells (HO8910). J. Int. Med. Res. 2009, 37:1375-1388.
15. Varela J.C., Praekelt U.M., Meacock P.A., Planta R.J., Mager W.H. The Saccharomyces cerevisiae HSP12 gene is activated by the high- osmolarity glycerol pathway and negatively regulated by protein kinase A. Mol. Cell Biol. 1995, 15:6232-6245.
16. Pacheco A., Pereira C., Almeida M.J., Sousa M.J. Small heat-shock protein Hsp12 contributes to yeast tolerance to freezing stress. Microbiology 2009, 155:2021-2028.
17. Sales K., Brandt W., Rumbak E., Lindsey G. The LEA-like protein HSP 12 in Saccharomyces cerevisiae has a plasma membrane location and protects membranes against desiccation and ethanol-induced stress. Biochim. Biophys. Acta 2000, 1463:267-278.
18. Welker S., Rudolph B., Frenzel E., Hagn F., Liebisch G., Schmitz G., Scheuring J., Kerth A., Blume A., Weinkauf S., Haslbeck M., Kessler H., Buchner J. Hsp12 is an intrinsically unstructured stress protein that folds upon membrane association and modulates membrane function. Mol. Cell 2010, 39:507-520.
19. Karreman R.J., Dague E., Gaboriaud F., Quiles F., Duval J.F., Lindsey G.G. The stress response protein Hsp12p increases the flexibility of the yeast Saccharomyces cerevisiae cell wall. Biochim. Biophys. Acta 2007, 1774:131-137.
20. Orlandi I., Cavadini P., Popolo L., Vai M. Cloning, sequencing and regulation of a cDNA encoding a small heat- shock protein from Schizosaccharomyces pombe. Biochim. Biophys. Acta 1996, 1307:129-131.
21. Jang Y.J., Park S.K., Yoo H.S. Isolation of an HSP12-homologous gene of Schizosaccharomyces pombe suppressing a temperature-sensitive mutant allele of cdc4. Gene 1996, 172:125-129.
22. Moreno S., Klar A., Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 1991, 194:795-823.
23. Chung K.S., Won M., Lee S.B., Jang Y.J., Hoe K.L., Kim D.U., Lee J.W., Kim K.W., Yoo H.S. Isolation of a novel gene from Schizosaccharomyces pombe: stm1+ encoding a seven-transmembrane loop protein that may couple with the heterotrimeric Galpha 2 protein, Gpa2. J. Biol. Chem. 2001, 276:40190-40201.
24. Day A., Schneider C., Schneider B.L. Yeast cell synchronization. Methods Mol. Biol. 2004, 241:55-76.
25. Seibert V., Prohl C., Schoultz I., Rhee E., Lopez R., Abderazzaq K., Zhou C., Wolf D.A. Combinatorial diversity of fission yeast SCF ubiquitin ligases by homo- and heterooligomeric assemblies of the F-box proteins Pop1p and Pop2p. BMC Biochem. 2002, 3:22.
26. Kobayashi N., McEntee K. Identification of cis and trans components of a novel heat shock stress regulatory pathway in Saccharomyces cerevisiae. Mol. Cell Biol. 1993, 13:248-256.
27. Fernandes M., Xiao H., Lis J.T. Fine structure analyses of the Drosophila and Saccharomyces heat shock factor-heat shock element interactions. Nucleic Acids Res. 1994, 22:167-173.
28. McGowan C.H., Russell P. Human Wee1 kinase inhibits cell division by phosphorylating p34cdc2 exclusively on Tyr15. Embo. J. 1993, 12:75-85.
29. Gould K.L., Nurse P. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature 1989, 342:39-45.
30. King R.W., Jackson P.K., Kirschner M.W. Mitosis in transition. Cell 1994, 79:563-571.
31. van Heusden G.P. 14-3-3 Proteins: insights from genome-wide studies in yeast. Genomics 2009, 94:287-293.
32. Zeng Y., Piwnica-Worms H. DNA damage and replication checkpoints in fission yeast require nuclear exclusion of the Cdc25 phosphatase via 14-3-3 binding. Mol. Cell Biol. 1999, 19:7410-7419.
33. Lopez-Girona A., Furnari B., Mondesert O., Russell P. Nuclear localization of Cdc25 is regulated by DNA damage and a 14-3-3 protein. Nature 1999, 397:172-175.