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Small heat shock proteins from extremophiles: a review

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Abstract

Many microorganisms from extreme environments have been well characterized, and increasing access to genomic sequence data has recently allowed the analysis of the protein families related to stress responses. Heat shock proteins appear to be ubiquitous in extremophiles. In this review, we focus on the family of small heat shock proteins (sHSPs) from extremophiles, which are α-crystallin homologues. Like the α-crystallin eye lens proteins, sHSPs act as molecular chaperones and prevent aggregation of denatured proteins under heat and desiccation stress. Many putative sHSP homologues have been identified in the genomic sequences of all classes of extremophiles. Current studies of shsp gene expression have revealed mechanisms of regulation and activity distinct from other known hsp gene regulation systems. Biochemical studies on sHSPs are limited to thermophilic and hyperthermophilic organisms, and the only two available crystal structures of sHSPs from Methanocaldococcus jannaschii, a hyperthermophilic archaeon and a mesophilic eukaryote, have contributed significantly to an understanding of the mechanisms of action of sHSPs, although many aspects remain unclear.

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References

  • Allen SP, Polazzi JO, Gierse JK, Easton AM (1992) Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli. J Bacteriol 174:6938–6947

    CAS  PubMed  Google Scholar 

  • Cannio R, Contursi P, Rossi M, Bartolucci S (2001) Thermoadaptation of a mesophilic hygromycin B phosphotransferase by directed evolution in hyperthermophilic Archaea: selection of a stable genetic marker for DNA transfer into Sulfolobus solfataricus. Extremophiles 5:153–159

    Article  CAS  PubMed  Google Scholar 

  • Caspers GJ, Leunissen JA, de Jong WW (1995) The expanding small heat-shock protein family, and structure predictions of the conserved “alpha-crystallin domain”. J Mol Evol 40:238–248

    CAS  PubMed  Google Scholar 

  • Chang Z, et al (1996) Mycobacterium tuberculosis 16-kDa antigen (Hsp16.3) functions as an oligomeric structure in vitro to suppress thermal aggregation. J Biol Chem 271:7218–7223

    CAS  PubMed  Google Scholar 

  • Clark JI, Muchowski PJ (2000) Small heat-shock proteins and their potential role in human disease. Curr Opin Struct Biol 10:52–59

    CAS  PubMed  Google Scholar 

  • Das KP, Surewicz WK (1995) Temperature-induced exposure of hydrophobic surfaces and its effect on the chaperone activity of alpha-crystallin. FEBS Lett 369:321–325

    Article  CAS  PubMed  Google Scholar 

  • Derham BK, Harding JJ (2002) Effects of modifications of alpha-crystallin on its chaperone and other properties. Biochem J 364:711–717

    Article  CAS  PubMed  Google Scholar 

  • Ehrnsperger M, Lilie H, Gaestel M, Buchner J (1999) The dynamics of Hsp25 quaternary structure. Structure and function of different oligomeric species. J Biol Chem 274:14867–14874

    Article  CAS  PubMed  Google Scholar 

  • Fleischmann RD, et al (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512

    PubMed  Google Scholar 

  • Fraser CM, et al (1995) The minimal gene complement of Mycoplasma genitalium. Science 270:397–403

    CAS  PubMed  Google Scholar 

  • Haley DA, Horwitz J, Stewart PL (1998) The small heat-shock protein, alphaB-crystallin, has a variable quaternary structure. J Mol Biol 277:27–35

    Article  CAS  PubMed  Google Scholar 

  • Haley DA, Bova MP, Huang QL, McHaourab HS, Stewart PL (2000) Small heat-shock protein structures reveal a continuum from symmetric to variable assemblies. J Mol Biol 298:261–272

    Article  CAS  PubMed  Google Scholar 

  • Haslbeck M (2002) sHsps and their role in the chaperone network. Cell Mol Life Sci 59:1649–1657

    CAS  PubMed  Google Scholar 

  • Haslbeck M, et al (1999) Hsp26: a temperature-regulated chaperone. Embo J 18:6744–6751

    PubMed  Google Scholar 

  • Horwitz J (1992) Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89:10449–10453

    CAS  PubMed  Google Scholar 

  • Jacob U, Gaestel M, Katrin E, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268:1517–1520

    PubMed  Google Scholar 

  • Jong WW de, Caspers GJ, Leunissen JA (1998) Genealogy of the alpha-crystallin--small heat-shock protein superfamily. Int J Biol Macromol 22:151–162

    PubMed  Google Scholar 

  • Kawashima T, et al (2000) Archaeal adaptation to higher temperatures revealed by genomic sequence of Thermoplasma volcanium. Proc Natl Acad Sci USA 97:14257–14262

    Article  CAS  PubMed  Google Scholar 

  • Kim KK, Kim R, Kim SH (1998a) Crystal structure of a small heat-shock protein. Nature 394:595–599

    CAS  PubMed  Google Scholar 

  • Kim KK, Yokota H, Santoso S, Lerner D, Kim R, Kim SH (1998b) Purification, crystallization, and preliminary X-ray crystallographic data analysis of small heat shock protein homologue from Methanococcus jannaschii, a hyperthermophile. J Struct Biol 121:76–80

    Article  CAS  Google Scholar 

  • Kim R, Kim KK, Yokota H, Kim SH (1998c) Small heat shock protein of Methanococcus jannaschii, a hyperthermophile. Proc Natl Acad Sci USA 95:9129–9133

    Article  CAS  PubMed  Google Scholar 

  • Kim R, Lai, L, Lee, H-H, Cheong, G-W, Kim KK, Wu, Z, Yokota H, Marquese S, Kim SH (2003) On the mechanism of chaperone activity of the small heat-shock protein of Proc Natl Acad Sci USA 100:8151–8155

    Google Scholar 

  • Klein G, Laskowski RA, Taylor A, Lipinski KS (2001) IbpA/B small heat-shock protein of marine bacterium Vibrio harveyi binds to proteins aggregared in a cell during heat shock. Mar Biotechnol 3:346–354

    CAS  Google Scholar 

  • Klemenz R, Frohli E, Steiger RH, Schafer R, Aoyama A (1991) Alpha B-crystallin is a small heat shock protein. Proc Natl Acad Sci USA 88:3652–3656

    PubMed  Google Scholar 

  • Klemenz R, Andres AC, Frohli E, Schafer R, Aoyama A (1993) Expression of the murine small heat shock proteins hsp 25 and alpha B crystallin in the absence of stress. J Cell Biol 120:639–645

    PubMed  Google Scholar 

  • Klundert FA van de, et al (1998) The mammalian small heat-shock protein Hsp20 forms dimers and is a poor chaperone. Eur J Biochem 258:1014–1021

    PubMed  Google Scholar 

  • Kojima K, Nakamoto H (2002) Specific binding of a protein to a novel DNA element in the cyanobacterial small heat-shock protein gene. Biochem Biophys Res Commun 297:616

    Article  CAS  PubMed  Google Scholar 

  • Kokke BP, Leroux MR, Candido EP, Boelens WC, de Jong WW (1998) Caenorhabditis elegans small heat-shock proteins Hsp12.2 and Hsp12.3 form tetramers and have no chaperone-like activity. FEBS Lett 433:228–232

    Article  CAS  PubMed  Google Scholar 

  • Korber P, Zander T, Herschlag D, Bardwell JC (1999) A new heat shock protein that binds nucleic acids. J Biol Chem 274:249–256

    Article  CAS  PubMed  Google Scholar 

  • Korber P, Stahl JM, Nierhaus KH, Bardwell JC (2000) Hsp15: a ribosome-associated heat shock protein. EMBO J 19:741–748

    Article  CAS  PubMed  Google Scholar 

  • Kuczynska-Wisnik D, Laskowska E, Taylor A (2001) Transcription of the ibpB heat-shock gene is under control of sigma(32)- and sigma(54)-promoters, a third regulon of heat-shock response. Biochem Biophys Res Commun 284:57–64

    Article  CAS  PubMed  Google Scholar 

  • Laksanalamai P, Maeder DL, Robb FT (2001) Regulation and mechanism of action of the small heat shock protein from the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 183:5198–5202

    CAS  PubMed  Google Scholar 

  • Laksanalamai P, Jiemjit A, Bu Z, Maeder DL, Robb FT (2003) Multi-subunit assembly of the Pyrococcus furiosus small heat shock protein is essential for cellular protection at high temperature. Extremophiles 7:79–83

    CAS  PubMed  Google Scholar 

  • Laskowska E, Wawrzynow A, Taylor A (1996) IbpA and IbpB, the new heat-shock proteins, bind to endogenous Escherichia coli proteins aggregated intracellularly by heat shock. Biochimie 78:117–122

    Article  CAS  PubMed  Google Scholar 

  • Lee GJ, Vierling E (2000) A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol 122:189–198

    PubMed  Google Scholar 

  • Lee GJ, Pokala N, Vierling E (1995) Structure and in vitro molecular chaperone activity of cytosolic small heat shock proteins from pea. J Biol Chem 270:10432–10438

    PubMed  Google Scholar 

  • Lee GJ, Roseman AM, Saibil HR, Vierling E (1997) A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J 16:659–671

    PubMed  Google Scholar 

  • Leroux MR, Ma BJ, Batelier G, Melki R, Candido EP (1997) Unique structural features of a novel class of small heat shock proteins. J Biol Chem 272:12847–12853

    Article  CAS  PubMed  Google Scholar 

  • Lucas S, et al (2002) Construction of a shuttle vector for, and spheroplast transformation of, the hyperthermophilic archaeon Pyrococcus abyssi. Appl Environ Microbiol 68:5528–5536

    CAS  PubMed  Google Scholar 

  • Martusewitsch E, Sensen CW, Schleper C (2000) High spontaneous mutation rate in the hyperthermophilic archaeon Sulfolobus solfataricus is mediated by transposable elements. J Bacteriol 182:2574–2581

    Article  CAS  PubMed  Google Scholar 

  • Montfort RL van, Basha E, Friedrich KL, Slingsby C, Vierling E (2001) Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol 8:1025–1030

    PubMed  Google Scholar 

  • Muchowski PJ, Clark JI (1998) ATP-enhanced molecular chaperone functions of the small heat shock protein human alphaB crystallin. Proc Natl Acad Sci USA 95:1004–1009

    Article  CAS  PubMed  Google Scholar 

  • Muchowski PJ, Valdez MM, Clark JI (1999) AlphaB-crystallin selectively targets intermediate filament proteins during thermal stress. Invest Ophthalmol Vision Sci 40:951–958

    CAS  Google Scholar 

  • Nakamoto H, Suzuki N, Roy SK (2000) Constitutive expression of a small heat-shock protein confers cellular thermotolerance and thermal protection to the photosynthetic apparatus in cyanobacteria. FEBS Lett 483:169–174

    Article  CAS  PubMed  Google Scholar 

  • Narberhaus F (1999) Negative regulation of bacterial heat shock genes. Mol Microbiol 31:1–8

    CAS  PubMed  Google Scholar 

  • Narberhaus F (2002) Alpha-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev 66:64–93

    CAS  PubMed  Google Scholar 

  • Ng WV, et al (2000) Genome sequence of Halobacterium species NRC-1. Proc Natl Acad Sci USA 97:12176–12181

    CAS  PubMed  Google Scholar 

  • Nitsch M, Klumpp M, Lupas A, Baumeister W (1997) The thermosome: alternating alpha and beta-subunits within the chaperonin of the archaeon Thermoplasma acidophilum. J Mol Biol 267:142–149

    Article  CAS  PubMed  Google Scholar 

  • Nocker A, Hausherr T, Balsiger S, Krstulovic NP, Hennecke H, Narberhaus F (2001a) A mRNA-based thermosensor controls expression of rhizobial heat shock genes. Nucleic Acids Res 29:4800–4807

    CAS  PubMed  Google Scholar 

  • Nocker A, Krstulovic NP, Perret X, Narberhaus F (2001b) ROSE elements occur in disparate rhizobia and are functionally interchangeable between species. Arch Microbiol 176:44–51

    CAS  PubMed  Google Scholar 

  • Ritossa F (1962) A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia 18:571–573

    CAS  Google Scholar 

  • Robb FT (2003) Genomics of thermophiles. In: Fraser CM, Nelson KE (eds) Humana Press, Totowa, N.J. (in press)

  • Roy SK, Nakamoto H (1998) Cloning, characterization, and transcriptional analysis of a gene encoding an alpha-crystallin-related, small heat shock protein from the thermophilic cyanobacterium Synechococcus vulcanus. J Bacteriol 180:3997–4001

    CAS  PubMed  Google Scholar 

  • Roy SK, Hiyama T, Nakamoto H (1999) Purification and characterization of the 16-kDa heat-shock-responsive protein from the thermophilic cyanobacterium Synechococcus vulcanus, which is an alpha-crystallin-related, small heat shock protein. Eur J Biochem 262:406–416

    CAS  PubMed  Google Scholar 

  • Ruepp A, Rockel B, Gutsche I, Baumeister W, Lupas AN (2001) The Chaperones of the archaeon Thermoplasma acidophilum. J Struct Biol 135:126–138

    Article  CAS  PubMed  Google Scholar 

  • Sauer U, Durre P (1993) Sequence and molecular characterization of a DNA region encoding a small heat shock protein of Clostridium acetobutylicum. J Bacteriol 175:3394–3400

    CAS  Google Scholar 

  • Scharf KD, Siddique M, Vierling E (2001) The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing alpha-crystallin domains (Acd proteins). Cell Stress Chaperon 6:225–237

    CAS  PubMed  Google Scholar 

  • Servant P, Rapoport G, Mazodier P (1999) RheA, the repressor of hsp18 in Streptomyces albus G. Microbiology 145:2385–2391

    CAS  PubMed  Google Scholar 

  • Servant P, Grandvalet C, Mazodier P (2000) The RheA repressor is the thermosensor of the HSP18 heat shock response in Streptomyces albus. Proc Natl Acad Sci USA 97:3538–3543

    CAS  PubMed  Google Scholar 

  • Soto A, et al (1999) Heterologous expression of a plant small heat-shock protein enhances Escherichia coli viability under heat and cold stress. Plant Physiol 120:521–528

    CAS  PubMed  Google Scholar 

  • Sowers KR, Schreier HJ (1999) Gene transfer systems for the Archaea. Trends Microbiol 7:212–219

    Article  CAS  PubMed  Google Scholar 

  • Staker BL, Korber P, Bardwell JC, Saper MA (2000) Structure of Hsp15 reveals a novel RNA-binding motif. Embo J 19:749–757

    Article  CAS  PubMed  Google Scholar 

  • Stedman KM, Schleper C, Rumpf E, Zillig W (1999) Genetic requirements for the function of the archaeal virus SSV1 in Sulfolobus solfataricus: construction and testing of viral shuttle vectors. Genetics 152:1397–1405

    CAS  PubMed  Google Scholar 

  • Stedman KM, et al (2000) pING family of conjugative plasmids from the extremely thermophilic archaeon Sulfolobus islandicus: insights into recombination and conjugation in Crenarchaeota. J Bacteriol 182:7014–7020

    Article  CAS  PubMed  Google Scholar 

  • Studer S, Obrist M, Lentze N, Narberhaus F (2002) A critical motif for oligomerization and chaperone activity of bacterial alpha-heat shock proteins. Eur J Biochem 269:3578–3586

    Article  CAS  PubMed  Google Scholar 

  • Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta 1577:1–9

    Article  CAS  PubMed  Google Scholar 

  • Tomb JF, et al (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539–547

    CAS  PubMed  Google Scholar 

  • Trent JD (1996) A review of acquired thermotolerance, heat-shock proteins, and molecular chaperones in archaea. FEMS Microbiol Rev 18:249–258

    Article  CAS  Google Scholar 

  • Usui K, Yoshida T, Maruyama T, Yohda M (2001) Small heat shock protein of a hyperthermophilic archaeum, Thermococcus sp. strain KS-1, exists as a spherical 24 mer and its expression is highly induced under heat-stress conditions. J Biosci Bioeng 92:161–166

    Article  CAS  Google Scholar 

  • Valdez MM, Clark JI, Wu GJ, Muchowski PJ (2002) Functional similarities between the small heat shock proteins Mycobacterium tuberculosis HSP 16.3 and human alphaB-crystallin. Eur J Biochem 269:1806–1813

    CAS  PubMed  Google Scholar 

  • Vierke G, Engelmann A, Hebbeln C, Thomm M (2002) A novel archaeal transcriptional regulator of heat shock response. J Biol Chem 14:14

    Google Scholar 

  • Waldmann T, Nitsch M, Klumpp M, Baumeister W (1995) Expression of an archaeal chaperonin in E. coli: formation of homo- (alpha, beta) and hetero-oligomeric (alpha+beta) thermosome complexes. FEBS Lett 376:67–73

    Article  CAS  PubMed  Google Scholar 

  • Waters ER, Vierling E (1999) The diversification of plant cytosolic small heat shock proteins preceded the divergence of mosses. Mol Biol Evol 16:127–139

    CAS  PubMed  Google Scholar 

  • Worthington P, Hoang V, Perez-Pomares F, Blum P (2003) Targeted disruption of the alpha-amylase gene in the hyperthermophilic archaeon Sulfolobus solfataricus. J Bacteriol 185:482–488

    Article  CAS  PubMed  Google Scholar 

  • Yaoi T, Kagawa HK, Trent JD (1998) Chaperonin filaments: their formation and an evaluation of methods for studying them. Arch Biochem Biophys 356:55–62

    Article  CAS  PubMed  Google Scholar 

  • Zillig W, et al (1998) Genetic elements in the extremely thermophilic archaeon Sulfolobus. Extremophiles 2:131–140

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Frank T. Robb.

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Communicated by D.A. Cowan

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Laksanalamai, P., Robb, F.T. Small heat shock proteins from extremophiles: a review. Extremophiles 8, 1–11 (2004). https://doi.org/10.1007/s00792-003-0362-3

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