Skip to main content
SpringerLink
Log in

Understanding What Small Heat Shock Proteins Do for Bacterial Cells

  • Chapter
The Big Book on Small Heat Shock Proteins

Part of the book series: Heat Shock Proteins ((HESP,volume 8))

Abstract

Being initially discovered due to the increased transcription of their encoding genes under heat shock conditions, heat shock proteins (HSPs, interchangeably named as ‘stress proteins’ or ‘molecular chaperones’) are known for their dramatic increase in amount when an organism is exposed to a variety of stress conditions. The major known activity for HSPs is to prevent the aggregation of nascent polypeptide chains that are yet-folded or mature proteins that are denatured under stress conditions. By transiently binding to and subsequently releasing the client proteins, HSPs function to promote their folding and/or assembly in living organisms. Small heat shock proteins (sHSPs), being relatively small among the HSPs in terms of the molecular weight of a single polypeptide chain, was found to present in bacteria only years after they were first identified in animals and plants. In this chapter, I will provide a historical perspective on what we have learned about the structure, function and regulation of sHSPs in bacteria. Main aspects covered in this chapter include the following. sHSPs exist as large dynamic homo-oligomers and regulate their activities by modulating their oligomeric status in a stress-responsive manner; sHSPs exhibit effective chaperone-like activities under in vitro and in vivo conditions; The monomeric small heat shock proteins possess an immunoglobulin-like folding pattern; sHSPs associate with and affect the physical state of cellular membranes; sHSPs play a potential role for bacterial cells to enter the non-growing dormant state; The biological functions of sHSPs are explored via gene knockout studies. In the end, I will also briefly discuss some of the unresolved issues regarding the structure, function and regulation of sHSPs.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

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  PubMed Central  Google Scholar 

  • Amzel LM, Poljak RJ (1979) Three-dimensional structure of immunoglobulins. Annu Rev Biochem 48:961–967

    Article  CAS  PubMed  Google Scholar 

  • Arrigo AP, Welch WJ (1987) Characterization and purification of the small 28,000-dalton mammalian heat shock protein. J Biol Chem 262:15359–15369

    CAS  PubMed  Google Scholar 

  • Arrigo AP, Suhan JP, Welch WJ (1988) Dynamic changes in the structure and intracellular locale of the mammalian low-molecular-weight heat shock protein. Mol Cell Biol 8:5059–5071

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ashburner M, Bonner JJ (1979) The induction of gene activity in drosophilia by heat shock. Cell 17:241–254

    Article  CAS  PubMed  Google Scholar 

  • Behlke J, Lutsch G, Gaestel M, Bielka H (1991) Supramolecular structure of the recombinant murine small heat shock protein hsp25. FEBS Lett 288:119–122

    Article  CAS  PubMed  Google Scholar 

  • Booth RJ, Harris DP, Loe JM, Watson JD (1988) Antigenic proteins of M. leprae: complete sequence of the gene for the 18-kDa protein. J Immunol 140:597–601

    CAS  PubMed  Google Scholar 

  • Bova MP, Huang Q, Ding L, Horwitz J (2002) Subunit exchange, conformational stability, and chaperone-like function of the small heat shock protein 16.5 from Methanococcus jannaschii. J Biol Chem 277:38468–38475

    Article  CAS  PubMed  Google Scholar 

  • Capozzi V, Weidmann S, Fiocco D, Rieu A, Hols P, Guzzo J, Spano G (2011) Inactivation of a small heat shock protein affects cell morphology and membrane fluidity in Lactobacillus plantarum WCFS1. Res Microbiol 162:419–425

    Article  CAS  PubMed  Google Scholar 

  • Chang Z, Primm TP, Jakana J, Lee IH, Chiu W, Gilbert HF, Quiocho FA (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

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Lu YJ, Wang HW, Quan S, Chang Z, Sui SF (2003) Two-dimensional crystallization of a small heat shock protein HSP16.3 on lipid layer. Biochem Biophys Res Commun 310:360–366

    Article  CAS  PubMed  Google Scholar 

  • Cheney CM, Shearn A (1983) Developmental regulation of Drosophila imaginal disc proteins: synthesis of a heal-shock protein under non-heat-shock conditions. Dev Biol 95:325–330

    Article  CAS  PubMed  Google Scholar 

  • Collier NC, Heuser J, Levy MA, Schlesinger MJ (1988) Ultrastructural and biochemical analysis of the stress granule in chicken embryo fibroblasts. J Cell Biol 106:1131–1139

    Article  CAS  PubMed  Google Scholar 

  • Cooper S, Ruettinger T (1975) Temperature dependent alteration in bacterial protein composition. Biochem Biophys Res Commun 62:584–586

    Article  CAS  PubMed  Google Scholar 

  • Coucheney F, Gal L, Beney L, Lherminier J, Gervais P, Guzzo J (2005) A small HSP, Lo18, interacts with the cell membrane and modulates lipid physical state under heat shock conditions in a lactic acid bacterium. Biochim Biophys Acta 1720:92–98

    Article  CAS  PubMed  Google Scholar 

  • Craig EA, Lindquist S (1988) The heat-shock proteins. Annu Rev Genet 22:631–677

    Article  PubMed  Google Scholar 

  • Cunningham AF, Spreadbury CL (1998) Mycobacterial stationary phase induced by low oxygen tension: cell wall thickening and localization of the 16-kilodalton alpha-crystallin homolog. J Bacteriol 180:801–808

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Jong WW, Leunissen JAM, Voorter CEM (1993) Evolution of the α-crystallin/small heat-shock protein family. Mol Biol Evol 10:103–126

    PubMed  Google Scholar 

  • Ellis J (1987) Proteins as molecular chaperones. Nature 328:378–379

    Article  CAS  PubMed  Google Scholar 

  • Ezemaduka AN, Yu JY, Shi XD, Zhang KM, Yin CC, Fu X, Chang Z (2014) A small heat shock protein enables Escherichia coli to grow at a lethal temperature of 50°C conceivably by maintaining cell envelope integrity. J Bacteriol 196:2004–2011

    Article  PubMed  PubMed Central  Google Scholar 

  • Fu X, Chang Z (2004) Temperature-dependent subunit exchange and chaperone-like activities of Hsp16.3, a small heat shock protein from Mycobacterium tuberculosis. Biochem Biophys Res Commun 316:291–299

    Article  CAS  PubMed  Google Scholar 

  • Fu X, Li W, Mao Q, Chang Z (2003) Disulfide bonds convert small heat shock protein Hsp16.3 from a chaperone to a non-chaperone: implications for the evolution of cysteine in molecular chaperones. Biochem Biophys Res Commun 308:627–635

    Article  CAS  PubMed  Google Scholar 

  • Fu X, Liu C, Liu Y, Feng X, Gu L, Chen X, Chang Z (2004) Small heat shock protein Hsp16.3 modulates its chaperone activity by adjusting the rate of oligomeric dissociation. Biochem Biophys Res Commun 310:412–420

    Article  Google Scholar 

  • Fu X, Shi X, Yan L, Zhang H, Chang Z (2013a) In vivo substrate diversity and preference of small heat shock protein IbpB as revealed by using a genetically incorporated photo-crosslinker. J Biol Chem 288:31646–31654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu X, Shi XD, Yin LX, Liu JF, Joo KH, Lee JY, Chang Z (2013b) Small heat shock protein IbpB acts as a robust chaperone in living cells by hierarchically activating its multi-type substrate-binding residues. J Biol Chem 288:11897–11906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu L, Abulimiti A, Li W, Chang Z (2002) Monodisperse Hsp16.3 nonamer exhibits dynamic dissociation and reassociation, with the nonamer dissociation prerequisite for chaperone-like activity. J Mol Biol 319:517–526

    Article  CAS  PubMed  Google Scholar 

  • Guzzo J, Delmas F, Pierre F, Jobin MP, Samyn B, Van Beeumen J, Cavin JF, Diviès C (1997) A small heat shock protein from Leuconostoc oenos induced by multiple stresses and during stationary growth phase. Lett Appl Microbiol 24:393–396

    Article  CAS  PubMed  Google Scholar 

  • Henriques AO, Beall BW, Mran CP Jr (1997) CotM of Bacillus subtilis, a member of the α-crystallin family of stress proteins, is induced during development and participates in spore outer coat formation. J Bacteriol 179:1887–1897

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hockertz MK, Clark-Lewis I, Candido EP (1991) Studies of the small heat shock proteins of Caenorhabditis elegans using anti-peptide antibodies. FEBS Lett 280:375–378

    Article  CAS  PubMed  Google Scholar 

  • Horvath I, Glatz A, Varvasovszki V, Torok Z, Pali T, Balogh G, Kovacs E, Nadasdi L, Benko S, Joo F, Vigh L (1998) Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: identification of hsp17 as a “fluidity gene”. Proc Natl Acad Sci U S A 95:3513–3518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horváth I, Multhoff G, Sonnleitner A, Vígh L (2008) Membrane-associated stress proteins: more than simply chaperones. Biochim Biophys Acta 1778:1653–1664

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ingolia TD, Craig EA (1982) Four small Drosophila heat shock proteins are related to each other and to mammalian α-crystallin. Proc Natl Acad Sci U S A 79:2360–2364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Jiao W, Qian M, Li P, Zhao L, Chang Z (2005) The essential role of the flexible termini in the temperature-responsiveness of the oligomeric state and chaperone-like activity for the polydisperse small heat shock protein IbpB from Escherichia coli. J Mol Biol 347:871–884

    Article  CAS  PubMed  Google Scholar 

  • Jiao W, Hong W, Li P, Sun S, Ma J, Qian M, Hu M, Chang Z (2008) The dramatically increased chaperone activity of Small heat shock protein IbpB is retained for an extended period of time after the stress condition is removed. Biochem J 410:63–70

    Article  CAS  PubMed  Google Scholar 

  • Jobin MP, Delmas F, Garmyn D, Diviès C, Guzzo J (1997) Molecular characterization of the gene encoding an 18-kilodalton small heat shock protein associated with the membrane of Leuconostoc oenos. Appl Environ Microbiol 63:609–614

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, Bruford EA, Cheetham ME, Chen B, Hightower LE (2009) Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 14:105–111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kappé G, Boelens WC, de Jong WW (2010) Why proteins without the α-crystallin domain should not be included in the human small heat shock protein family HSPB. Cell Stress Chaperones 15:457–461

    Article  PubMed  PubMed Central  Google Scholar 

  • Kelley P, Schlesinger MJ (1978) The effect of amino-acid analogues and heat shock on gene expression in chicken embryo fibroblasts. Cell 15:1277–1286

    Article  CAS  PubMed  Google Scholar 

  • Kennaway CK, Benesch JLP, Gohlke U, Wang L, Robinson CV, Orlova EV, Saibi HR, Keep NH (2005) Dodecameric structure of the small heat shock protein Acr1 from Mycobacterium tuberculosis. J Biol Chem 280:33419–33425

    Article  CAS  PubMed  Google Scholar 

  • Key JL, Lin CY, Chen YM (1981) Heat shock proteins of higher plants. Proc Natl Acad Sci U S A 78:3526–3530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitagawa M, Miyakawa M, Matsumara 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

    Article  CAS  PubMed  Google Scholar 

  • Koninkx JF (1976) Protein synthesis in salivary glands of Drosophila hydei after experimental gene induction. Biochem J 58:623–628

    Google Scholar 

  • Laksanalamai P, Robb FT (2004) Small heat shock proteins from extremophiles: a review. Extremophiles 8:1–11

    Article  CAS  PubMed  Google Scholar 

  • Laskowska E, Wawrzynów 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 BY, Hefta SA, Brennan PJ (1992) Characterization of the major membrane protein of virulent Mycobacterium tuberculosis. Infect Immun 60:2066–2074

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lentze N, Aquilina JA, Lindbauer M, Robinson CV, Narberhaus F (2004) Temperature and concentration-controlled dynamics of rhizobial small heat shock proteins. Eur J Biochem 271:2494–2503

    Article  CAS  PubMed  Google Scholar 

  • Lewis K (2007) Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5:48–56

    Article  CAS  PubMed  Google Scholar 

  • Lewis MJ, Pelham HRB (1985) Involvement of ATP in the nuclear and nucleolar functions of the 70 kd heat shock protein. EMBO J 4:3137–3143

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis M, Helmsing PJ, Ashburner M (1975) Parallel changes in puffing activity and patterns of protein synthesis in salivary glands of Drosophila. Proc Natl Acad Sci U S A 72:3604–3608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maitre M, Weidmann S, Rieu A, Fenel D, Schoehn G, Ebel C, Coves J, Guzzo J (2012) The oligomer plasticity of the small heat-shock protein Lo18 from Oenococcus oeni influences its role in both membrane stabilization and protein protection. Biochem J 444:97–104

    Article  CAS  PubMed  Google Scholar 

  • Maitre M, Weidmann S, Dubois-Brissonnet F, David V, Covès J, Guzzo J (2014) Adaptation of the wine bacterium Oenococcus oeni to ethanol stress: role of the small heat shock protein Lo18 in membrane integrity. Appl Environ Microbiol 80:2973–2980

    Article  PubMed  PubMed Central  Google Scholar 

  • Mao Q, Ke D, Feng X, Chang Z (2001) Preheat treatment for Mycobacterium tuberculosis Hsp16.3: correlation between a structural Phase change at 60°C and a dramatic increase in chaperone-like activity. Biochem Biophys Res Commun 284:942–947

    Article  CAS  PubMed  Google Scholar 

  • Matuszewska M, Kuczyńska-Wiśnik D, Laskowska E, Liberek K (2005) The small heat shock protein IbpA of Escherichia coli cooperates with IbpB in stabilization of thermally aggregated proteins in a disaggregation competent state. J Biol Chem 280:12292–12298

    Article  CAS  PubMed  Google Scholar 

  • Mirault M-E, Goldschmidt-Clermont M, Moran L, Arrigo AP, Tissieres A (1978) The effect of heat shock on gene expression in Drosophila melanogaster. Cold Spring Harb Symp Quant Biol 42:819–827

    Article  CAS  PubMed  Google Scholar 

  • Miyake T, Araki S, Tsuchido T (1993) Synthesis and sedimentation of a subset of 15 kDa heat shock proteins in Escherichia coli cells recovering from sublethal heat stress. Biosci Biotechnol Biochem 57:578–583

    Article  CAS  Google Scholar 

  • Mogk A, Deuerling E, Vorderwülbecke S, Vierling E, Bukau B (2003a) Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol Microbiol 50:585–595

    Article  CAS  PubMed  Google Scholar 

  • Mogk A, Schlieker C, Friedrich KL, Schönfeld H-J, Vierling E, Bukau B (2003b) Refolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most efficiently by ClpB/DnaK. J Biol Chem 278:31033–31042

    Article  CAS  PubMed  Google Scholar 

  • Munro S, Pelham HRB (1986) An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46:291–300

    Article  CAS  PubMed  Google Scholar 

  • Nagao RT, Czarnecka E, Gurley WB, Schoffl F, Key JL (1985) Genes for low-molecular-weight heat shock proteins of soybeans: sequence analysis of a multigene family. Mol Cell Biol 5:3417–3428

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamoto H, Vígh L (2007) The small heat shock proteins and their clients. Cell Mol Life Sci 64:294–306

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nerland AH, Mustafa AS, Sweetser D, Godal T, Young RA (1988) A protein antigen of Mycobacterium leprae is related to a family of small heat shock proteins. J Bacteriol 170:5919–5921

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pelham HRB (1986) Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell 46:959–961

    Article  CAS  PubMed  Google Scholar 

  • Ratajczak E, Strózecka J, Matuszewska M, Zietkiewicz S, Kuczyńska-Wiśnik D, Laskowska E, Liberek K (2010) IbpA the small heat shock protein from Escherichia coli forms fibrils in the absence of its cochaperone IbpB. FEBS Lett 584:2253–2257

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ritossa F (1996) Discovery of the heat shock response. Cell Stress Chaperones 1:97–98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Russnak RH, Jones D, Candido EP (1983) Cloning and analysis of cDNA sequences coding for two 16 kilodalton heat shock proteins (hsps) in Caenorhabditis elegans: homology with the small hsps of Drosophila. Nucleic Acids Res 11:3187–3205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sauer U, Dürre 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  PubMed  PubMed Central  Google Scholar 

  • Servant P, Mazodier P (1995) Characterization of Streptomyces albus 18-kilodalton heat shock-responsive protein. J Bacteriol 177:2998–3003

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shearstone JR, Baneyx F (1999) Biochemical characterization of the small heat shock protein IbpB from Escherichia coli. J Biol Chem 274:9937–9945

    Article  CAS  PubMed  Google Scholar 

  • Shi X, Wang Z, Yan L, Ezemaduka AN, Fan G, Wang R, Fu X, Yin C, Chang Z (2011) Small heat shock protein AgsA forms dynamic fibrils. FEBS Lett 585:3396–3402

    Article  CAS  PubMed  Google Scholar 

  • Studer S, Narberhaus F (2000) Chaperone activity and homo- and hetero-oligomer formation of bacterial small heat shock proteins. J Biol Chem 275:37212–37218

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, MacRae TH (2005) Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci 62:2460–2476

    Article  CAS  PubMed  Google Scholar 

  • Thomas JG, Baneyx F (1998) Roles of the Escherichia coli small heat shock proteins IbpA and IbpB in thermal stress management: comparison with ClpA, ClpB, and HtpG in vivo. J Bacteriol 180:5165–5172

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tissieres A, Mitchell HK, Tracy VM (1974) Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. J Mol Biol 84:389–398

    Article  CAS  PubMed  Google Scholar 

  • Török Z, Goloubinoff P, Horváth I, Tsvetkova NM, Glatz A, Balogh G, Varvasovszki V, Los DA, Vierling E, Crowe JH, Vigh L (2001) Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding. Proc Natl Acad Sci U S A 98:3098–3103

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsvetkova NM, Horváth I, Török Z, Wolkers WF, Balogi Z, Shigapova N, Crowe LM, Tablin F, Vierling E, Crowe JH, Vigh L (2002) Small heat-shock proteins regulate membrane lipid polymorphism. Proc Natl Acad Sci U S A 99:13504–13509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Montfort RLM, 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

    Article  PubMed  Google Scholar 

  • van Noort JM, Bsibsi M, Nacken P, Gerritsen WH, Amor S (2012) The link between small heat shock proteins and the immune system. Int J Biochem Cell Biol 44:1670–1679

    Article  PubMed  Google Scholar 

  • Veinger L, Diamant S, Buchner J, Goloubinoff P (1998) The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J Biol Chem 273:11032–11037

    Article  CAS  PubMed  Google Scholar 

  • Verbon A, Hartskeerl RA, Schuitema A, Kolk AH, Young DB, Lathigra R (1992) The 14,000-molecular-weight antigen of Mycobacterium tuberculosis is related to the alpha-crystallin family of low-molecular-weight heat shock proteins. J Bacteriol 174:1352–1359

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang YB, Ezemaduka AN, Tang Y, Chang ZY (2009) Understanding the mechanism of the dormant dauer formation of C. elegans: from genetics to biochemistry. IUBMB Life 61:607–612

    Article  CAS  PubMed  Google Scholar 

  • Williams AF, Barclay AN (1988) The immunoglobulin superfamily–domains for cell surface recognition. Annu Rev Immunol 6:381–405

    Article  CAS  PubMed  Google Scholar 

  • Yamamori T, Ito K, Nakamura Y, Yura T (1978) Transient regulation of protein synthesis in Escherichia coli upon shift-up of growth temperature. J Bacteriol 134:1133–1140

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang H, Huang S, Dai H, Gong Y, Zheng C, Chang Z (1999) The Mycobacterium tuberculosis small heat shock protein Hsp16.3 exposes hydrophobic surfaces at mild conditions: conformational flexibility and molecular chaperone activity. Protein Sci 8:174–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young DB, Garbe TR (1991) Heat shock proteins and antigens of Mycobacterium tuberculosis. Infect Immun 59:3086–3093

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan Y, Crane DD, Barry CE 3rd (1996) Stationary phase-associated protein expression in Mycobacterium tuberculosis: function of the mycobacterial α-crystallin homolog. J Bacteriol 178:4484–4492

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan Y, Crane DD, Simpson RM, Zhu YQ, Hickey M, Sherman DR, Barry CE III (1998) The 16-kDa alpha-crystallin (Acr) protein of Mycobacterium tuberculosis is required for growth in macrophages. Proc Natl Acad Sci U S A 95:9578–9583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Fu X, Jiao W, Zhang X, Liu C, Chang Z (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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The author would like to thank Mr. Yang Liu (Peking University) for his kind assistance in preparing the figure, and Prof. Lawrence Hightower (University of Connecticut) for his kind editorial assistance. This work was supported by research grants from the National Basic Research Program of China (973 Program) (No. 2012CB917300) and the National Natural Science Foundation of China (No. 31170738) to Professor Zengyi Chang.

Author information

Authors and Affiliations

  1. State Key Laboratory of Protein and Plant Gene Research, Center for Protein Sciences, Center for History and Philosophy of Science, School of Life Sciences, Peking University, Beijing, 100871, China

    Zengyi Chang

Authors
  1. Zengyi Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zengyi Chang .

Editor information

Editors and Affiliations

  1. Department of Molecular Biology, Medical Biochemistry & Pathology Medical School Lab Cell & Developmental Genetics IBIS, Université Laval, Quebec, Québec, Canada

    Robert M. Tanguay

  2. Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, USA

    Lawrence E. Hightower

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Chang, Z. (2015). Understanding What Small Heat Shock Proteins Do for Bacterial Cells. In: Tanguay, R., Hightower, L. (eds) The Big Book on Small Heat Shock Proteins. Heat Shock Proteins, vol 8. Springer, Cham. https://doi.org/10.1007/978-3-319-16077-1_22

Download citation

Publish with us

Policies and ethics

Search

Navigation