Involvement of small heat shock proteins, trehalose, and lipids in the thermal stress management in Schizosaccharomyces pombe
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- 作者：Attila Glatz ; Ana-Maria Pilbat ; Gergely L. Németh…
- 关键词：S. pombe ; Fission yeast ; Heat stress ; Small Hsps ; Membrane ; Lipids ; Trehalose accumulation
- 刊名：Cell Stress and Chaperones
- 出版年：2016
- 出版时间：March 2016
- 年：2016
- 卷：21
- 期：2
- 页码：327-338
- 全文大小：1,446 KB
- 参考文献：Adamska I, Kloppstech K (1991) Evidence for the localization of the nuclear-coded 22-kDa heat-shock protein in a subfraction of thylakoid membranes. Eur J Biochem 198:375–381. doi:10.1111/j.1432-1033.1991.tb16025.x CrossRef PubMed
Argüelles JC (1994) Heat-shock response in a yeast tps1 mutant deficient in trehalose synthesis. FEBS Lett 350:266–270. doi:10.1016/0014-5793(94)00786-1 CrossRef PubMed
Balogh G, Horváth I, Nagy E et al (2005) The hyperfluidization of mammalian cell membranes acts as a signal to initiate the heat shock protein response. FEBS J 272:6077–6086. doi:10.1111/j.1742-4658.2005.04999.x CrossRef PubMed
Balogh G, Péter M, Liebisch G et al (2010) Lipidomics reveals membrane lipid remodelling and release of potential lipid mediators during early stress responses in a murine melanoma cell line. Biochim Biophys Acta 1801:1036–1047. doi:10.1016/j.bbalip.2010.04.011 CrossRef PubMed
Balogh G, Péter M, Glatz A et al (2013) Key role of lipids in heat stress management. FEBS Lett 587:1970–1980. doi:10.1016/j.febslet.2013.05.016 CrossRef PubMed
Balogi Z, Cheregi O, Giese KC et al (2008) A mutant small heat shock protein with increased thylakoid association provides an elevated resistance against UV-B damage in synechocystis 6803. J Biol Chem 283:22983–22991. doi:10.1074/jbc.M710400200 CrossRef PubMed PubMedCentral
Bausero M a, Bharti A, Page DT et al (2005) Silencing the hsp25 gene eliminates migration capability of the highly metastatic murine 4T1 breast adenocarcinoma cell. Tumour Biol 27:17–26. doi:10.1159/000090152 CrossRef PubMed PubMedCentral
Bellyei S, Szigeti A, Boronkai A et al (2007a) Inhibition of cell death by a novel 16.2 kD heat shock protein predominantly via Hsp90 mediated lipid rafts stabilization and Akt activation pathway. Apoptosis 12:97–112. doi:10.1007/s10495-006-0486-x CrossRef PubMed
Bellyei S, Szigeti A, Pozsgai E et al (2007b) Preventing apoptotic cell death by a novel small heat shock protein. Eur J Cell Biol 86:161–171. doi:10.1016/j.ejcb.2006.12.004 CrossRef PubMed
Blazquez M a, Stucka R, Feldmann H, Gancedo C (1994) Trehalose-6-P synthase is dispensable for growth on glucose but not for spore germination in Schizosaccharomyces pombe. J Bacteriol 176:3895–3902PubMed PubMedCentral
Brameshuber M, Weghuber J, Ruprecht V et al (2010) Imaging of mobile long-lived nanoplatforms in the live cell plasma membrane. J Biol Chem 285:41765–41771. doi:10.1074/jbc.M110.182121 CrossRef PubMed PubMedCentral
Briggs MS, Gierasch LM, Zlotnick a et al (1985) In vivo function and membrane binding properties are correlated for Escherichia coli lamB signal peptides. Science 228:1096–1099. doi:10.1126/science.3158076 CrossRef PubMed
Carpy A, Krug K, Graf S et al (2014) Absolute proteome and phosphoproteome dynamics during the cell cycle of Schizosaccharomyces pombe (fission yeast). Mol Cell Proteomics 13:1925–1936. doi:10.1074/mcp.M113.035824 CrossRef PubMed PubMedCentral
Chen D, Toone WM, Mata J et al (2003) Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 14:214–229. doi:10.1091/mbc.E02-08-0499 CrossRef PubMed PubMedCentral
Chowdary TK, Raman B, Ramakrishna T, Rao CM (2007) Interaction of mammalian Hsp22 with lipid membranes. Biochem J 401:437–445. doi:10.1042/BJ20061046 CrossRef PubMed PubMedCentral
Crowe JH (2007) Trehalose as a “chemical chaperone”: fact and fantasy. In: Csermely P, Vígh L (eds) Molecular aspects of the stress response: chaperones, membranes and networks. Springer, New York, pp 143–158CrossRef
de Miguel N, Echeverria PC, Angel SO (2005) Differential subcellular localization of members of the Toxoplasma gondii small heat shock protein family. Eukaryot Cell 4:1990–1997. doi:10.1128/EC.4.12.1990-1997.2005 CrossRef PubMed PubMedCentral
de Miguel N, Lebrun M, Heaslip A et al (2008) Toxoplasma gondii Hsp20 is a stripe-arranged chaperone-like protein associated with the outer leaflet of the inner membrane complex. Biol Cell 100:479–489. doi:10.1042/BC20080004 CrossRef PubMed PubMedCentral
De Virgilio C, Simmen U, Hottiger T et al (1990) Heat shock induces enzymes of trehalose metabolism, trehalose accumulation, and thermotolerance in Schizosaccharomyces pombe, even in the presence of cycloheximide. FEBS Lett 273:107–110. doi:10.1016/0014-5793(90)81062-S CrossRef PubMed
Delmas F, Pierre F, Coucheney F et al (2001) Biochemical and physiological studies of the small heat shock protein Lo18 from the lactic acid bacterium Oenococcus oeni. J Mol Microbiol Biotechnol 3:601–610PubMed
Eisenberg-Domovich Y, Kloppstech K, Ohad I (1994) Reversible membrane association of heat-shock protein 22 in Chlamydomonas reinhardtii during heat shock and recovery. Eur J Biochem 222:1041–1046. doi:10.1111/j.1432-1033.1994.tb18956.x CrossRef PubMed
Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17–27. doi:10.1093/glycob/cwg047 CrossRef
Eleutherio E, Panek A, De Mesquita JF et al (2015) Revisiting yeast trehalose metabolism. Curr Genet 61:263–274. doi:10.1007/s00294-014-0450-1 CrossRef PubMed
Elliott B, Haltiwanger RS, Futcher B (1996) Synergy between trehalose and Hsp104 for thermotolerance in Saccharomyces cerevisiae. Genetics 144:923–933PubMed PubMedCentral
Eyles SJ, Gierasch LM (2010) Nature’s molecular sponges: small heat shock proteins grow into their chaperone roles. Proc Natl Acad Sci U S A 107:2727–2728. doi:10.1073/pnas.0915160107 CrossRef PubMed PubMedCentral
Forsburg SL (2003) Growth and manipulation of S. pombe. Curr Protoc Mol Biol. doi:10.1002/0471142727.mb1316s64 , Chapter 13:Unit 13.16
Forsburg SL, Rhind N (2006) Basic methods for fission yeast. Yeast 23:173–183. doi:10.1002/yea.1347 CrossRef PubMed
Fujita R, Ounzain S, Wang ACY et al (2011) Hsp-27 induction requires POU4F2/Brn-3b TF in doxorubicin-treated breast cancer cells, whereas phosphorylation alters its cellular localization following drug treatment. Cell Stress Chaperones 16:427–439. doi:10.1007/s12192-011-0256-8 CrossRef PubMed PubMedCentral
Gancedo C, Flores CL (2004) The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi. FEMS Yeast Res 4:351–359. doi:10.1016/S1567-1356(03)00222-8 CrossRef PubMed
Gibney PA, Lu C, Caudy AA et al (2013) Yeast metabolic and signaling genes are required for heat-shock survival and have little overlap with the heat-induced genes. Proc Natl Acad Sci U S A 110:E4393–E4402. doi:10.1073/pnas.1318100110 CrossRef PubMed PubMedCentral
Gombos I, Crul T, Piotto S et al (2011) Membrane-lipid therapy in operation: the HSP co-inducer BGP-15 activates stress signal transduction pathways by remodeling plasma membrane rafts. PLoS One 6:e28818. doi:10.1371/journal.pone.0028818 CrossRef PubMed PubMedCentral
Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227. doi:10.1016/0163-7827(90)90002-3 CrossRef PubMed
Heckathorn SA, Downs CA, Sharkey TD, Coleman JS (1998) The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiol 116:439–444. doi:10.1104/pp.116.1.439 CrossRef PubMed PubMedCentral
Hirose M, Tohda H, Giga-Hama Y et al (2005) Interaction of a small heat shock protein of the fission yeast, Schizosaccharomyces pombe, with a denatured protein at elevated temperature. J Biol Chem 280:32586–32593. doi:10.1074/jbc.M504121200 CrossRef PubMed
Hohmann S, Neves MJ, de Koning W et al (1993) The growth and signalling defects of the ggs1 (fdp1/byp1) deletion mutant on glucose are suppressed by a deletion of the gene encoding hexokinase PII. Curr Genet 23:281–289. doi:10.1007/BF00310888 CrossRef PubMed
Horváth I, Multhoff G, Sonnleitner A, Vígh L (2008) Membrane-associated stress proteins: more than simply chaperones. Biochim Biophys Acta - Biomembr 1778:1653–1664. doi:10.1016/j.bbamem.2008.02.012 CrossRef
Kitagawa M, Matsumura Y, Tsuchido T (2000) Small heat shock proteins, IbpA and IbpB, are involved in resistances to heat and superoxide stresses in Escherichia coli. FEMS Microbiol Lett 184:165–171. doi:10.1016/S0378-1097(00)00038-0 CrossRef PubMed
Kitagawa M, Miyakawa M, Matsumura Y, Tsuchido T (2002) Escherichia coli small heat shock proteins, IbpA and IbpB, protect enzymes from inactivation by heat and oxidants. Eur J Biochem 269:2907–2917. doi:10.1046/j.1432-1033.2002.02958.x CrossRef PubMed
Krawchuk MD, Wahls WP (1999) High-efficiency gene targeting in Schizosaccharomyces pombe using a modular, PCR-based approach with long tracts of flanking homology. Yeast 15:1419–1427. doi:10.1002/(SICI)1097-0061(19990930)15:13<1419::AID-YEA466>3.0.CO;2-Q CrossRef PubMed PubMedCentral
Lackner D, Schmidt M, Wu S et al (2012) Regulation of transcriptome, translation, and proteome in response to environmental stress in fission yeast. Genome Biol 13:R25. doi:10.1186/gb-2012-13-4-r25 CrossRef PubMed PubMedCentral
Lee DH, Goldberg AL (1998) Proteasome inhibitors cause induction of heat shock proteins and trehalose, which together confer thermotolerance in Saccharomyces cerevisiae. Mol Cell Biol 18:30–38CrossRef PubMed PubMedCentral
Lee BY, Hefta SA, Brennan PJ (1992) Characterization of the major membrane protein of virulent Mycobacterium tuberculosis. Infect Immun 60:2066–2074PubMed PubMedCentral
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275. doi:10.1007/s10982-008-9035-9 PubMed
Marguerat S, Schmidt A, Codlin S et al (2012) Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell 151:671–683. doi:10.1016/j.cell.2012.09.019 CrossRef PubMed PubMedCentral
Matsuyama A, Arai R, Yashiroda Y et al (2006) ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat Biotechnol 24:841–847. doi:10.1038/nbt1222 CrossRef PubMed
Nagy E, Balogi Z, Gombos I et al (2007) Hyperfluidization-coupled membrane microdomain reorganization is linked to activation of the heat shock response in a murine melanoma cell line. Proc Natl Acad Sci U S A 104:7945–7950. doi:10.1073/pnas.0702557104 CrossRef PubMed PubMedCentral
Nitta K, Suzuki N, Honma D et al (2005) Ultrastructural stability under high temperature or intensive light stress conferred by a small heat shock protein in cyanobacteria. FEBS Lett 579:1235–1242. doi:10.1016/j.febslet.2004.12.095 CrossRef PubMed
Park HG, Han SI, Oh SY, Kang HS (2005) Cellular responses to mild heat stress. Cell Mol Life Sci 62:10–23. doi:10.1007/s00018-004-4208-7 CrossRef PubMed
Ribeiro MJS, Reinders A, Boller T et al (1997) Trehalose synthesis is important for the acquisition of thermotolerance in Schizosaccharomyces pombe. Mol Microbiol 25:571–581. doi:10.1046/j.1365-2958.1997.4961856.x CrossRef PubMed
Rojo M, Hovius R, Demel R et al (1991) Interaction of mitochondrial creatine kinase with model membranes a monolayer study. FEBS Lett 281:123–129. doi:10.1016/0014-5793(91)80374-C CrossRef PubMed
Sheff MA, Thorn KS (2004) Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21:661–670. doi:10.1002/yea.1130 CrossRef PubMed
Shiozaki K, Shiozaki M, Russell P (1997) Mcs4 mitotic catastrophe suppressor regulates the fission yeast cell cycle through the Wik1-Wis1-Spc1 kinase cascade. Mol Biol Cell 8:409–419
Singer M a, Lindquist S (1998) Multiple effects of trehalose on protein folding in vitro and in vivo. Mol Cell 1:639–648. doi:10.1016/S1097-2765(00)80064-7 CrossRef PubMed
Soto T, Fernandez J, Vicente-Soler J et al (1999) Accumulation of trehalose by overexpression of tps1, coding for trehalose-6-phosphate synthase, causes increased resistance to multiple stresses in the fission yeast Schizosaccharomyces pombe. Appl Environ Microbiol 65:2020–2024PubMed PubMedCentral
Sugino C, Hirose M, Tohda H et al (2009) Characterization of a sHsp of Schizosaccharomyces pombe, SpHsp15.8, and the implication of its functional mechanism by comparison with another sHsp, SpHsp16.0. Proteins 74:6–17. doi:10.1002/prot.22132 CrossRef PubMed
Taricani L, Feilotter HE, Weaver C, Young PG (2001) Expression of hsp16 in response to nucleotide depletion is regulated via the spc1 MAPK pathway in Schizosaccharomyces pombe. Nucleic Acids Res 29:3030–3040. doi:10.1093/nar/29.14.3030 CrossRef PubMed PubMedCentral
Török Z, Demel RA, Leenhouts JM, de Kruijff B (1994) Presequence-mediated intermembrane contact formation and lipid flow. A model membrane study. Biochemistry 33:5589–5594CrossRef PubMed
Török Z, Horváth I, Goloubinoff P et al (1997) Evidence for a lipochaperonin: association of active protein-folding GroESL oligomers with lipids can stabilize membranes under heat shock conditions. Proc Natl Acad Sci U S A 94:2192–2197. doi:10.1073/pnas.94.6.2192 CrossRef PubMed PubMedCentral
Török Z, Pilbat A-M, Gombos I et al (2012) Evidence on cholesterol-controlled lipid raft interaction of the small heat shock protein HSPB11. In: Henderson B, Pockley AG (eds) Cellular trafficking of cell stress proteins in health and disease. Springer Netherlands, Dordrecht, pp 75–85CrossRef
Tsvetkova NM, Horváth I, Török Z et al (2002) Small heat-shock proteins regulate membrane lipid polymorphism. Proc Natl Acad Sci U S A 99:13504–13509. doi:10.1073/pnas.192468399 CrossRef PubMed PubMedCentral
Verger R, Pattus F (1982) Lipid-protein interactions in monolayers. Chem Phys Lipids 30:189–227. doi:10.1016/0009-3084(82)90052-4 CrossRef
Vigh L, Maresca B, Harwood JL (1998) Does the membrane’s physical state control the expression of heat shock and other genes? Trends Biochem Sci 23:369–374. doi:10.1016/S0968-0004(98)01279-1 CrossRef PubMed
Vigh L, Escribá PV, Sonnleitner A et al (2005) The significance of lipid composition for membrane activity: new concepts and ways of assessing function. Prog Lipid Res 44:303–344. doi:10.1016/j.plipres.2005.08.001 CrossRef PubMed
Vigh L, Horváth I, Maresca B, Harwood JL (2007a) Can the stress protein response be controlled by “membrane-lipid therapy”? Trends Biochem Sci 32:357–363. doi:10.1016/j.tibs.2007.06.009 CrossRef PubMed
Vigh L, Nakamoto H, Landry J et al (2007b) Membrane regulation of the stress response from prokaryotic models to mammalian cells. Ann N Y Acad Sci 1113:40–51. doi:10.1196/annals.1391.027 CrossRef PubMed
Weidmann S, Rieu A, Rega M et al (2010) Distinct amino acids of the Oenococcus oeni small heat shock protein Lo18 are essential for damaged protein protection and membrane stabilization. FEMS Microbiol Lett 309:8–15. doi:10.1111/j.1574-6968.2010.01999.x PubMed
Welker S, Rudolph B, Frenzel E et al (2010) Hsp12 is an intrinsically unstructured stress protein that folds upon membrane association and modulates membrane function. Mol Cell 39:507–520. doi:10.1016/j.molcel.2010.08.001 CrossRef PubMed
Wood V, Harris MA, McDowall MD et al (2012) PomBase: a comprehensive online resource for fission yeast. Nucleic Acids Res 40:D695–D699. doi:10.1093/nar/gkr853 CrossRef PubMed PubMedCentral
Yoshida J, Tani T (2005) Hsp16p is required for thermotolerance in nuclear mRNA export in fission yeast Schizosaccharomyces pombe. Cell Struct Funct 29:125–138. doi:10.1247/csf.29.125 CrossRef PubMed
Zhang H, Fu X, Jiao W et al (2005) The association of small heat shock protein Hsp16.3 with the plasma membrane of Mycobacterium tuberculosis: dissociation of oligomers is a prerequisite. Biochem Biophys Res Commun 330:1055–1061. doi:10.1016/j.bbrc.2005.03.092 CrossRef PubMed - 作者单位：Attila Glatz (1)
Ana-Maria Pilbat (1)
Gergely L. Németh (1)
Katalin Vince-Kontár (1)
Katalin Jósvay (1)
Ákos Hunya (1)
Andor Udvardy (1)
Imre Gombos (1)
Mária Péter (1)
Gábor Balogh (1)
Ibolya Horváth (1)
László Vígh (1)
Zsolt Török (1)
1. Institute of Biochemistry, Biological Research Centre, Szeged, Hungary - 刊物主题：Biomedicine general; Cell Biology; Biochemistry, general; Immunology; Cancer Research; Neurosciences;
- 出版者：Springer Netherlands
- ISSN：1466-1268
文摘
Changes in the levels of three structurally and functionally different important thermoprotectant molecules, namely small heat shock proteins (sHsps), trehalose, and lipids, have been investigated upon heat shock in Schizosaccharomyces pombe. Both α-crystallin-type sHsps (Hsp15.8 and Hsp16) were induced after prolonged high-temperature treatment but with different kinetic profiles. The shsp null mutants display a weak, but significant, heat sensitivity indicating their importance in the thermal stress management. The heat induction of sHsps is different in wild type and in highly heat-sensitive trehalose-deficient (tps1Δ) cells; however, trehalose level did not show significant alteration in shsp mutants. The altered timing of trehalose accumulation and induction of sHsps suggest that the disaccharide might provide protection at the early stage of the heat stress while elevated amount of sHsps are required at the later phase. The cellular lipid compositions of two different temperature-adapted wild-type S. pombe cells are also altered according to the rule of homeoviscous adaptation, indicating their crucial role in adapting to the environmental temperature changes. Both Hsp15.8 and Hsp16 are able to bind to different lipids isolated from S. pombe, whose interaction might provide a powerful protection against heat-induced damages of the membranes. Our data suggest that all the three investigated thermoprotectant macromolecules play a pivotal role during the thermal stress management in the fission yeast.