C. elegans STI-1, the Homolog of Sti1/Hop, Is Involved in Aging and Stress Response

Journal of Molecular Biology

Volumn 390, Issue 4, 2009, Pages 604-617

  Song, Hyun Ok ^a   Lee, Wonhae ^b   An, Kiyoung ^c   Lee, Hye suk ^a   Cho, Jeong Hoon ^d   Park, Zee Yong ^a   Ahnn, Joohong ^e  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

^b National Institute of Scientific Investigation   (South Korea)

^c CKB Research Institute   (South Korea)

^d Chosun University   (South Korea)

^e Hanyang University   (South Korea)

Author keywords

aging; C. elegans; heat stress; sti 1; Sti1 Hop

Indexed keywords

ADAPTOR PROTEIN; CHAPERONE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN ORGANIZER PROTEIN; HEAVY METAL; TRANSCRIPTION FACTOR DAF 16; UNCLASSIFIED DRUG;

AGING; ARTICLE; CAENORHABDITIS ELEGANS; CELL STRESS; CONTROLLED STUDY; ENVIRONMENTAL STRESS; HEAT SHOCK; HEAT TOLERANCE; IMMUNOPRECIPITATION; IN VIVO STUDY; LETHALITY; LIFESPAN; LONGEVITY; MASS SPECTROMETRY; METAZOON; NEMATODE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHYSIOLOGICAL STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY; SUBFERTILITY;

CAENORHABDITIS ELEGANS; MAMMALIA; METAZOA; NEMATODA;

EID: 67649365446     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.05.035     Document Type: Article

References (56)

1. Morimoto R.I. Cells in stress: transcriptional activation of heat shock genes. Science 259 (1993) 1409-1410
2. Lindquist S. The heat-shock response. Annu. Rev. Biochem. 55 (1986) 1151-1191
3. Nicolet C.M., and Craig E.A. Isolation and characterization of STI1, a stress-inducible gene from Saccharomyces cerevisiae. Mol. Cell. Biol. 9 (1989) 3638-3646
4. Young J.C., Moarefi I., and Hartl F.U. Hsp90: a specialized but essential protein-folding tool. J. Cell Biol. 154 (2001) 267-273
5. Blatch G.L., Lassle M., Zetter B.R., and Kundra V. Isolation of a mouse cDNA encoding mSTI1, a stress-inducible protein containing the TPR motif. Gene 194 (1997) 277-282
6. Honore B., Leffers H., Madsen P., Rasmussen H.H., Vandekerckhove J., and Celis J.E. Molecular cloning and expression of a transformation-sensitive human protein containing the TPR motif and sharing identity to the stress-inducible yeast protein STI1. J. Biol. Chem. 267 (1992) 8485-8491
7. Chen S., and Smith D.F. Hop as an adaptor in the heat shock protein 70 (Hsp70) and hsp90 chaperone machinery. J. Biol. Chem. 273 (1998) 35194-35200
8. Prapapanich V., Chen S., and Smith D.F. Mutation of Hip's carboxy-terminal region inhibits a transitional stage of progesterone receptor assembly. Mol. Cell. Biol. 18 (1998) 944-952
9. Nelson G.M., Huffman H., and Smith D.F. Comparison of the carboxy-terminal DP-repeat region in the co-chaperones Hop and Hip. Cell Stress Chaperones 8 (2003) 125-133
10. Smith D.F., Sullivan W.P., Marion T.N., Zaitsu K., Madden B., McCormick D.J., and Toft D.O. Identification of a 60-kilodalton stress-related protein, p60, which interacts with hsp90 and hsp70. Mol. Cell. Biol. 13 (1993) 869-876
11. Odunuga O.O., Hornby J.A., Bies C., Zimmermann R., Pugh D.J., and Blatch G.L. Tetratricopeptide repeat motif-mediated Hsc70-mSTI1 interaction. Molecular characterization of the critical contacts for successful binding and specificity. J. Biol. Chem. 278 (2003) 6896-6904
12. Carrigan P.E., Nelson G.M., Roberts P.J., Stoffer J., Riggs D.L., and Smith D.F. Multiple domains of the co-chaperone Hop are important for Hsp70 binding. J. Biol. Chem. 279 (2004) 16185-16193
13. Prodromou C., Siligardi G., O'Brien R., Woolfson D.N., Regan L., Panaretou B., et al. Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones. EMBO J. 18 (1999) 754-762
14. Wegele H., Muschler P., Bunck M., Reinstein J., and Buchner J. Dissection of the contribution of individual domains to the ATPase mechanism of Hsp90. J. Biol. Chem. 278 (2003) 39303-39310
15. Richter K., Muschler P., Hainzl O., Reinstein J., and Buchner J. Sti1 is a non-competitive inhibitor of the Hsp90 ATPase. Binding prevents the N-terminal dimerization reaction during the ATPase cycle. J. Biol. Chem. 278 (2003) 10328-10333
16. Gershon H., and Gershon D. Detection of inactive enzyme molecules in ageing organisms. Nature 227 (1970) 1214-1217
17. Stadtman E.R., Starke-Reed P.E., Oliver C.N., Carney J.M., and Floyd R.A. Protein modification in aging. EXS 62 (1992) 64-72
18. Fargnoli J., Kunisada T., Fornace Jr. A.J., Schneider E.L., and Holbrook N.J. Decreased expression of heat shock protein 70 mRNA and protein after heat treatment in cells of aged rats. Proc. Natl Acad. Sci. USA 87 (1990) 846-850
19. Walker G.A., White T.M., McColl G., Jenkins N.L., Babich S., Candido E.P., et al. Heat shock protein accumulation is upregulated in a long-lived mutant of Caenorhabditis elegans. J. Gerontol. Ser. A 56 (2001) B281-B287
20. Murphy C.T., McCarroll S.A., Bargmann C.I., Fraser A., Kamath R.S., Ahringer J., et al. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424 (2003) 277-283
21. Tatar M., Khazaeli A.A., and Curtsinger J.W. Chaperoning extended life. Nature 390 (1997) 30
22. Walker G.A., and Lithgow G.J. Lifespan extension in C. elegans by a molecular chaperone dependent upon insulin-like signals. Aging Cell 2 (2003) 131-139
23. Morley J.F., and Morimoto R.I. Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol. Biol. Cell 15 (2004) 657-664
24. Lithgow G.J., White T.M., Melov S., and Johnson T.E. Thermotolerance and extended life-span conferred by single-gene mutations and induced by thermal stress. Proc. Natl Acad. Sci. USA 92 (1995) 7540-7544
25. Birnby D.A., Link E.M., Vowels J.J., Tian H., Colacurcio P.L., and Thomas J.H. A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in Caenorhabditis elegans. Genetics 155 (2000) 85-104
26. Heschl M.F., and Baillie D.L. Identification of a heat-shock pseudogene from Caenorhabditis elegans. Genome 32 (1989) 190-195
27. Vowels J.J., and Thomas J.H. Multiple chemosensory defects in daf-11 and daf-21 mutants of Caenorhabditis elegans. Genetics 138 (1994) 303-316
28. Inoue T., Hirata K., Kuwana Y., Fujita M., Miwa J., Roy R., and Yamaguchi Y. Cell cycle control by daf-21/Hsp90 at the first meiotic prophase/metaphase boundary during oogenesis in Caenorhabditis elegans. Dev. Growth Differ. 48 (2006) 25-32
29. Chen M.S., Silverstein A.M., Pratt W.B., and Chinkers M. The tetratricopeptide repeat domain of protein phosphatase 5 mediates binding to glucocorticoid receptor heterocomplexes and acts as a dominant negative mutant. J. Biol. Chem. 271 (1996) 32315-32320
30. Lassle M., Blatch G.L., Kundra V., Takatori T., and Zetter B.R. Stress-inducible, murine protein mSTI1. Characterization of binding domains for heat shock proteins and in vitro phosphorylation by different kinases. J. Biol. Chem. 272 (1997) 1876-1884
31. Zhang Y., Mian M.A., Chekhovskiy K., So S., Kupfer D., Lai H., and Roe B.A. Differential gene expression in Festuca under heat stress conditions. J. Exp. Bot. 56 (2005) 897-907
32. Kenyon C., Chang J., Gensch E., Rudner A., and Tabtiang R. A C. elegans mutant that lives twice as long as wild type. Nature 366 (1993) 461-464
33. Gems D., Sutton A.J., Sundermeyer M.L., Albert P.S., King K.V., Edgley M.L., et al. Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics 150 (1998) 129-155
34. Munoz M.J. Longevity and heat stress regulation in Caenorhabditis elegans. Mech. Ageing Dev. 124 (2003) 43-48
35. Henderson S.T., and Johnson T.E. daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr. Biol. 11 (2001) 1975-1980
36. Lee R.Y., Hench J., and Ruvkun G. Regulation of C. elegans DAF-16 and its human ortholog FKHRL1 by the daf-2 insulin-like signaling pathway. Curr. Biol. 11 (2001) 1950-1957
37. Lin K., Dorman J.B., Rodan A., and Kenyon C. daf-16: an HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278 (1997) 1319-1322
38. Yokoyama K., Fukumoto K., Murakami T., Harada S., Hosono R., Wadhwa R., et al. Extended longevity of Caenorhabditis elegans by knocking in extra copies of hsp70F, a homolog of mot-2 (mortalin)/mthsp70/Grp75. FEBS Lett. 516 (2002) 53-57
39. Cypser J.R., and Johnson T.E. Multiple stressors in Caenorhabditis elegans induce stress hormesis and extended longevity. J. Gerontol. Ser. A 57 (2002) B109-B114
40. Scheufler C., Brinker A., Bourenkov G., Pegoraro S., Moroder L., Bartunik H., et al. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101 (2000) 199-210
41. Flom G., Weekes J., Williams J.J., and Johnson J.L. Effect of mutation of the tetratricopeptide repeat and aspartate-proline 2 domains of Sti1 on Hsp90 signaling and interaction in Saccharomyces cerevisiae. Genetics 172 (2006) 41-51
42. Yashin A.I., Cypser J.R., Johnson T.E., Michalski A.I., Boyko S.I., and Novoseltsev V.N. Ageing and survival after different doses of heat shock: the results of analysis of data from stress experiments with the nematode worm Caenorhabditis elegans. Mech. Ageing Dev. 122 (2001) 1477-1495
43. Johnson T.E., Henderson S., Murakami S., de Castro E., de Castro S.H., Cypser J., et al. Longevity genes in the nematode Caenorhabditis elegans also mediate increased resistance to stress and prevent disease. J. Inherited Metab. Dis. 25 (2002) 197-206
44. Olsen A., Vantipalli M.C., and Lithgow G.J. Lifespan extension of Caenorhabditis elegans following repeated mild hormetic heat treatments. Biogerontology 7 (2006) 221-230
45. Galbadage T., and Hartman P.S. Repeated temperature fluctuation extends the life span of Caenorhabditis elegans in a daf-16-dependent fashion. Mech. Ageing Dev. 129 (2008) 507-514
46. Ogg S., Paradis S., Gottlieb S., Patterson G.I., Lee L., Tissenbaum H.A., and Ruvkun G. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389 (1997) 994-999
47. Guarente L., and Kenyon C. Genetic pathways that regulate ageing in model organisms. Nature 408 (2000) 255-262
48. Cherkasova V., Ayyadevara S., Egilmez N., and Shmookler Reis R. Diverse Caenorhabditis elegans genes that are upregulated in dauer larvae also show elevated transcript levels in long-lived, aged, or starved adults. J. Mol. Biol. 300 (2000) 433-448
49. Yu H., and Larsen P.L. DAF-16-dependent and independent expression targets of DAF-2 insulin receptor-like pathway in Caenorhabditis elegans include FKBPs. J. Mol. Biol. 314 (2001) 1017-1028
50. Park B.J., Lee D.G., Yu J.R., Jung S.K., Choi K., Lee J., et al. Calreticulin, a calcium-binding molecular chaperone, is required for stress response and fertility in Caenorhabditis elegans. Mol. Biol. Cell 12 (2001) 2835-2845
51. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77 (1974) 71-94
52. Mello C., and Fire A. DNA transformation. Methods Cell Biol. 48 (1995) 451-482
53. Lee W., Lee T.H., Park B.J., Chang J.W., Yu J.R., Koo H.S., et al. Caenorhabditis elegans calnexin is N-glycosylated and required for stress response. Biochem. Biophys. Res. Commun. 338 (2005) 1018-1030
54. Ahnn J., and Fire A. A screen for genetic loci required for body-wall muscle development during embryogenesis in Caenorhabditis elegans. Genetics 137 (1994) 483-498
55. Miller D.M., and Shakes D.C. Immunofluorescence microscopy. Methods Cell Biol. 48 (1995) 365-394
56. Cho J.H., Oh Y.S., Park K.W., Yu J., Choi K.Y., Shin J.Y., et al. Calsequestrin, a calcium sequestering protein localized at the sarcoplasmic reticulum, is not essential for body-wall muscle function in Caenorhabditis elegans. J. Cell Sci. 113 (2000) 3947-3958