Abstract
Several strategies have been put in place by organisms to adapt to their environment. One of these strategies is the production of stress proteins such as sHSPs, which have been widely described over the last 30 years for their role as molecular chaperones. Some sHSPs have, in addition, the particularity to exert a lipochaperone role by interacting with membrane lipids to maintain an optimal membrane fluidity. However, the mechanisms involved in this sHSP-lipid interaction remain poorly understood and described rather sporadically in the literature. This review gathers the information concerning the structure and function of these proteins available in the literature in order to highlight the mechanism involved in this interaction. In addition, analysis of primary sequence data of sHSPs available in database shows that sHSPs can interact with lipids via certain amino acid residues present on some β sheets of these proteins. These residues could have a key role in the structure and/or oligomerization dynamics of sHPSs, which is certainly essential for interaction with membrane lipids and consequently for maintaining optimal cell membrane fluidity.
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References
Ahn YJ, Zimmerman JL (2006) Introduction of the carrot HSP17.7 into potato (Solanum tuberosum L.) enhances cellular membrane stability and tuberization in vitro. Plant, Cell and Environment 29(1):95–104. https://doi.org/10.1111/j.1365-3040.2005.01403.x
Arena MP, Capozzi V, Longo A, Russo P, Weidmann S, Rieu A, Guzzo J, Spano G, Fiocco D (2019) The phenotypic analysis of Lactobacillus plantarum sHSP mutants reveals a potential role for HSP1 in cryotolerance. Front Microbiol, 10. https://doi.org/10.3389/fmicb.2019.00838
Augusteyn RC (2004) α-crystallin: a review of its structure and function. Clin Exp Optom 87(6):356–366. https://doi.org/10.1111/j.1444-0938.2004.tb03095.x
Bakthisaran R, Tangirala R, Rao C (2015) Small heat shock proteins: role in cellular functions and pathology. Biochimica et biophysica acta 1854(4):291–319. https://doi.org/10.1016/j.bbapap.2014.12.019
Balogi Z, Török Z, Balogh G, Jósvay K, Shigapova N, Vierling E, Vígh L, Horváth I (2005) “Heat shock lipid” in cyanobacteria during heat/light-acclimation. Arch Biochem Biophys 436(2):346–354. https://doi.org/10.1016/j.abb.2005.02.018
Balogi Z, Cheregi O, Giese KC, Juhász K, Vierling E, Vass I, Vígh L, Horváth I (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(34):22983–22991. https://doi.org/10.1074/jbc.m710400200
Baneyx F, Mujacic M (2004) Recombinant protein folding and misfolding in Escherichia coli. Nat Biotechnol 22(11):1399–1408. https://doi.org/10.1038/nbt1029
Basha E, O’Neill H, Vierling E (2012) Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci 37(3):106–117. https://doi.org/10.1016/j.tibs.2011.11.005
Beissinger M, Buchner J (1998) How chaperones fold proteins. Biol Chem 379(3):245–259
Berger F, Morellet N, Menu F, Potier P (1996) Cold shock and cold acclimation proteins in the psychrotrophic bacterium Arthrobacter globiformis SI55. J Bacteriol 178(11):2999–3007. https://doi.org/10.1128/jb.178.11.2999-3007.1996
Bhandari S, Biswas S, Chaudhary A, Dutta S, Suguna K (2019) Dodecameric structure of a small heat shock protein from Mycobacterium marinum M. Proteins: structure, function, and bioinformatics 87(5):365–379. https://doi.org/10.1002/prot.25657
Boelens WC (2014) Cell biological roles of αB-crystallin. Prog Biophys Mol Biol 115(1):3–10. https://doi.org/10.1016/j.pbiomolbio.2014.02.005
Boelens WC (2020) Structural aspects of the human small heat shock proteins related to their functional activities. Cell Stress Chaperones 25(4):581–591. https://doi.org/10.1007/s12192-020-01093-1
Booth IR (1985) Regulation of cytoplasmic pH in bacteria. Microbiol Rev 49(4):359–378. https://doi.org/10.1128/mr.49.4.359-378.1985
Boyle D, Takemoto L (1994) Immunolocalization of the C-terminal and N-terminal regions of alpha-A and alpha-B crystallins. Curr Eye Res 13(7):497–504. https://doi.org/10.3109/02713689408999881
Bozaykut P, Ozer NK, Karademir B (2014) Regulation of protein turnover by heat shock proteins. Free Radical Biol Med 77:195–209. https://doi.org/10.1016/j.freeradbiomed.2014.08.012
Bukau B, Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92(3):351–366. https://doi.org/10.1016/s0092-8674(00)80928-9
Bukau B, Weissman J, Horwich A (2006) Molecular chaperones and protein quality control. Cell 125(3):443–451. https://doi.org/10.1016/j.cell.2006.04.014
Capozzi V, Fiocco D, Weidmann S, Guzzo J, Spano G (2011) Increasing membrane protection in Lactobacillus plantarum cells overproducing small heat shock proteins. Annals of Microbiology 62(2):517–522. https://doi.org/10.1007/s13213-011-0285-7
Carra S, Alberti S, Arrigo PA, Benesch JL, Benjamin IJ, Boelens W, Bartelt-Kirbach B, Brundel BJJM, Buchner J, Bukau B, Carver JA, Ecroyd H, Emanuelsson C, Finet S, Golenhofen N, Goloubinoff P, Gusev N, Haslbeck M, Hightower LE, Tanguay RM (2017) The growing world of small heat shock proteins: from structure to functions. Cell Stress Chaperones 22(4):601–611. https://doi.org/10.1007/s12192-017-0787-8
Cashikar AG, Duennwald M, Lindquist SL (2005) A chaperone pathway in protein disaggregation. J Biol Chem 280(25):23869–23875. https://doi.org/10.1074/jbc.m502854200
Caspers GJ, Leunissen JAM, de Jong WW (1995) The expanding small heat-shock protein family, and structure predictions of the conserved “α-crystallin domain.” J Mol Evol 40(3):238–248. https://doi.org/10.1007/bf00163229
Chang Z, Primm TP, Jakana J, Lee IH, Serysheva I, 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(12):7218–7223. https://doi.org/10.1074/jbc.271.12.7218
Chang HC, Tang YC, Hayer-Hartl M, Hartl FU (2007) SnapShot: molecular chaperones, part I. Cell 128(1):212.e1-212.e2. https://doi.org/10.1016/j.cell.2007.01.001
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(2):360–366. https://doi.org/10.1016/j.bbrc.2003.09.026
Chen J, Feige MJ, Franzmann TM, Bepperling A, Buchner J (2010) Regions outside the α-crystallin domain of the small heat shock protein hsp26 are required for its dimerization. J Mol Biol 398(1):122–131. https://doi.org/10.1016/j.jmb.2010.02.022
Cocotl-Yañez M, Moreno S, Encarnación S, López-Pliego L, Castañeda M, Espín G (2014) A small heat-shock protein (Hsp20) regulated by RpoS is essential for cyst desiccation resistance in Azotobacter vinelandii. Microbiology 160(3):479–487. https://doi.org/10.1099/mic.0.073353-0
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. Biochimica et Biophysica Acta (BBA) - Biomembranes 1720(1–2):92–98. https://doi.org/10.1016/j.bbamem.2005.11.017
Csoboz B, Gombos I, Kóta Z, Dukic B, Klement É, Varga-Zsíros V, Lipinszki Z, Páli T, Vígh L, Török Z (2022) The small heat shock protein, HSPB1, interacts with and modulates the physical structure of membranes. Int J Mol Sci 23(13):7317. https://doi.org/10.3390/ijms23137317
Cunningham AF, Spreadbury CL (1998) Mycobacterial stationary phase induced by low oxygen tension: cell wall thickening and localization of the 16-kilodalton α-crystallin homolog. J Bacteriol 180(4):801–808. https://doi.org/10.1128/jb.180.4.801-808.1998
de Jong WW, Leunissen JA, Voorter CE (1993) Evolution of the alpha-crystallin/small heat-shock protein family. Mol Biol Evol. https://doi.org/10.1093/oxfordjournals.molbev.a039992
de Jong WW, Caspers GJ, Leunissen JAM (1998) Genealogy of the α-crystallin—small heat-shock protein superfamily. Int J Biol Macromol 22(3–4):151–162. https://doi.org/10.1016/s0141-8130(98)00013-0
De Maio A, Hightower LE (2020) Heat shock proteins and the biogenesis of cellular membranes. Cell Stress Chaperones 26(1):15–18. https://doi.org/10.1007/s12192-020-01173-2
De Maio A, Cauvi DM, Capone R, Bello I, Egberts WV, Arispe N, Boelens W (2019) The small heat shock proteins, HSPB1 and HSPB5, interact differently with lipid membranes. Cell Stress Chaperones 24(5):947–956. https://doi.org/10.1007/s12192-019-01021-y
Delbecq SP, Klevit RE (2013) One size does not fit all: the oligomeric states of αB crystallin. FEBS Lett 587(8):1073–1080. https://doi.org/10.1016/j.febslet.2013.01.021
Delbecq SP, Rosenbaum JC, Klevit RE (2015) A mechanism of subunit recruitment in human small heat shock protein oligomers. Biochemistry 54(28):4276–4284. https://doi.org/10.1021/acs.biochem.5b00490
Diaz D, Döbeli H, Yeboah-Manu D, Mensah-Quainoo E, Friedlein A, Soder N, Rondini S, Bodmer T, Pluschke G (2006) Use of the immunodominant 18-kilodalton small heat shock protein as a serological marker for exposure to Mycobacterium ulcerans. Clin Vaccine Immunol 13(12):1314–1321. https://doi.org/10.1128/cvi.00254-06
Ellis RJ (1990) The molecular chaperone concept. Seminars in cell biology 1(1):1–9
Ellis RJ, van der Vies SM, Hemmingsen SM (1989) The molecular chaperone concept. Biochemical Society symposium 55:145–153
Fu MS, De Sordi L, Mühlschlegel FA (2012) Functional characterization of the small heat shock protein Hsp12p from Candida albicans. PLoS ONE 7(8):e42894. https://doi.org/10.1371/journal.pone.0042894
Fu X, Jiao W, Chang Z (2006) Phylogenetic and biochemical studies reveal a potential evolutionary origin of small heat shock proteins of animals from bacterial class A. J Mol Evol 62(3):257–266. https://doi.org/10.1007/s00239-005-0076-5
Giese KC, Basha E, Catague BY, Vierling E (2005) Evidence for an essential function of the N terminus of a small heat shock protein in vivo, independent of in vitro chaperone activity. Proc Natl Acad Sci 102(52):18896–18901. https://doi.org/10.1073/pnas.0506169103
Glatz A, Pilbat AM, Németh GL, Vince-Kontár K, Jósvay K, Hunya Á, Udvardy A, Gombos I, Péter M, Balogh G, Horváth I, Vígh L, Török Z (2015) Involvement of small heat shock proteins, trehalose, and lipids in the thermal stress management in Schizosaccharomyces pombe. Cell Stress Chaperones 21(2):327–338. https://doi.org/10.1007/s12192-015-0662-4
Glover JR, Lindquist S (1998) Hsp104, Hsp70, and Hsp40. Cell 94(1):73–82. https://doi.org/10.1016/s0092-8674(00)81223-4
Guzzo J, Delmas F, Pierre F, Jobin M, Samyn B, Van Beeumen J, Cavin J, Diviès C (1997) A small heat shock protein from Leuconostoc oenos induced by multiple stresses and during stationary growth phase. Lett Appl Microbiol 24(5):393–396. https://doi.org/10.1046/j.1472-765x.1997.00042.x
Han MJ, Yun H, Lee SY (2008) Microbial small heat shock proteins and their use in biotechnology. Biotechnol Adv 26(6):591–609. https://doi.org/10.1016/j.biotechadv.2008.08.004
Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381(6583):571–580. https://doi.org/10.1038/381571a0
Haslbeck M, Miess A, Stromer T, Walter S, Buchner J (2005) Disassembling protein aggregates in the yeast cytosol. J Biol Chem 280(25):23861–23868. https://doi.org/10.1074/jbc.m502697200
Haslbeck M, Peschek J, Buchner J, Weinkauf S (2016) Structure and function of α-crystallins: traversing from in vitro to in vivo. Biochim Biophys Acta Gen Subj 1860(1):149–166. https://doi.org/10.1016/j.bbagen.2015.06.008
Haslbeck M, Vierling E (2015) A first line of stress defense: small heat shock proteins and their function in protein homeostasis. J Mol Biol 427(7):1537–1548. https://doi.org/10.1016/j.jmb.2015.02.002
Henriques AO, Beall BW, Moran CP (1997) CotM of Bacillus subtilis, a member of the alpha-crystallin family of stress proteins, is induced during development and participates in spore outer coat formation. J Bacteriol 179(6):1887–1897. https://doi.org/10.1128/jb.179.6.1887-1897.1997
Hilton GR, Benesch JLP (2012) Two decades of studying non-covalent biomolecular assemblies by means of electrospray ionization mass spectrometry. J R Soc Interface 9(70):801–816. https://doi.org/10.1098/rsif.2011.0823
Hilton GR, Hochberg GKA, Laganowsky A, McGinnigle SI, Baldwin AJ, Benesch JLP (2013) C-terminal interactions mediate the quaternary dynamics of αB-crystallin. Phil Trans R Society b: Biol Sci 368(1617):20110405. https://doi.org/10.1098/rstb.2011.0405
Horwitz J (1993) Proctor lecture. The function of alpha-crystallin. Investigative ophthalmology & visual science 34(1):10–22
Horwitz J (2003) Alpha-crystallin. Exp Eye Res 76(2):145–153. https://doi.org/10.1016/s0014-4835(02)00278-6
Ingolia TD, Craig EA (1982) Four small Drosophila heat shock proteins are related to each other and to mammalian alpha-crystallin. Proc Natl Acad Sci 79(7):2360–2364. https://doi.org/10.1073/pnas.79.7.2360
Jakob U, Gaestel M, Engel K, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268(3):1517–1520. https://doi.org/10.1016/s0021-9258(18)53882-5
Jee B, Singh Y, Yadav R, Lang F (2018) small Heat Shock Protein16.3 of Mycobacterium tuberculosis: after two decades of functional characterization. Cell Physiol Biochem 49(1):368–380. https://doi.org/10.1159/000492887
Junprung W, Supungul P, Tassanakajon A (2021) Structure, gene expression, and putative functions of crustacean heat shock proteins in innate immunity. Dev Comp Immunol 115:103875. https://doi.org/10.1016/j.dci.2020.103875
Kappé G, Leunissen, JAM, de Jong WW (2002).Evolution and diversity of prokaryotic small heat shock proteins. In Small Stress Proteins (pp. 1–17). Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-642-56348-5_1
Kim R, Kim KK, Yokota H, Kim SH (1998) Small heat shock protein of Methanococcus jannaschii, a hyperthermophile. Proc Natl Acad Sci 95(16):9129–9133. https://doi.org/10.1073/pnas.95.16.9129
Kim DH, Xu ZY, Na YJ, Yoo YJ, Lee J, Sohn EJ, Hwang I (2011) Small heat shock protein hsp17.8 functions as an AKR2A cofactor in the targeting of chloroplast outer membrane proteins in arabidopsis. Plant Physiology 157(1):132–146. https://doi.org/10.1104/pp.111.178681
Klaips CL, Jayaraj GG, Hartl FU (2017) Pathways of cellular proteostasis in aging and disease. J Cell Biol 217(1):51–63. https://doi.org/10.1083/jcb.201709072
Klevit RE (2020) Peeking from behind the veil of enigma: emerging insights on small heat shock protein structure and function. Cell Stress Chaperones 25(4):573–580. https://doi.org/10.1007/s12192-020-01092-2
Kriehuber T, Rattei T, Weinmaier T, Bepperling A, Haslbeck M, Buchner J (2010) Independent evolution of the core domain and its flanking sequences in small heat shock proteins. FASEB J 24(10):3633–3642. https://doi.org/10.1096/fj.10-156992
Kuczyńska-Wiśnik D, Matuszewska E, Laskowska E (2010) Escherichia coli heat-shock proteins IbpA and IbpB affect biofilm formation by influencing the level of extracellular indole. Microbiology 156(1):148–157. https://doi.org/10.1099/mic.0.032334-0
Lelj-Garolla B, Mauk AG (2011) Roles of the N- and C-terminal sequences in Hsp27 self-association and chaperone activity. Protein Sci 21(1):122–133. https://doi.org/10.1002/pro.761
Lentze N, Narberhaus F (2004) Detection of oligomerisation and substrate recognition sites of small heat shock proteins by peptide arrays. Biochem Biophys Res Commun 325(2):401–407. https://doi.org/10.1016/j.bbrc.2004.10.043
Lentze N, Studer S, Narberhaus F (2003) Structural and functional defects caused by point mutations in the α-crystallin domain of a bacterial α-heat shock protein. J Mol Biol 328(4):927–937. https://doi.org/10.1016/s0022-2836(03)00356-5
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(12):2494–2503. https://doi.org/10.1111/j.1432-1033.2004.04180.x
Lim J, Thomas T, Cavicchioli R (2000) Low temperature regulated DEAD-box RNA helicase from the Antarctic archaeon, Methanococcoides burtonii. J Mol Biol 297(3):553–567. https://doi.org/10.1006/jmbi.2000.3585
Lini N, Rehna EA, Shiburaj S, Maheshwari JJ, Shankernarayan NP, Dharmalingam K (2008) Functional characterization of a small heat shock protein from Mycobacterium leprae. BMC Microbiol 8:208. https://doi.org/10.1186/1471-2180-8-208
Longo A, Russo P, Capozzi V, Spano G, Fiocco D (2020) Knock out of sHSP genes determines some modifications in the probiotic attitude of Lactiplantibacillus plantarum. Biotech Lett 43(3):645–654. https://doi.org/10.1007/s10529-020-03041-6
Ma P, Li J, Qi L, Dong X (2021) The archaeal small heat shock protein hsp17.6 protects proteins from oxidative inactivation. Int J Mol Sci 22(5):2591. https://doi.org/10.3390/ijms22052591
Maaroufi H, Tanguay RM (2013) Analysis and phylogeny of small heat shock proteins from marine viruses and their cyanobacteria host. PLoS ONE 8(11):e81207. https://doi.org/10.1371/journal.pone.0081207
MacRae TH (2000) Structure and function of small heat shock/α-crystallin proteins: established concepts and emerging ideas. Cell Mol Life Sci 57(6):899–913. https://doi.org/10.1007/pl00000733
Mainz A, Peschek J, Stavropoulou M, Back KC, Bardiaux B, Asami S, Prade E, Peters C, Weinkauf S, Buchner J, Reif B (2015) The chaperone αB-crystallin uses different interfaces to capture an amorphous and an amyloid client. Nat Struct Mol Biol 22(11):898–905. https://doi.org/10.1038/nsmb.3108
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. Biochemical Journal 444(1):97–104. https://doi.org/10.1042/bj20120066
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(10):2973–2980. https://doi.org/10.1128/aem.04178-13
Mao Q, Chang Z (2001) Site-Directed mutation on the only universally conserved residue leu122 of small heat shock protein hsp16.3. Biochem Biophys Res Commun 289(5):1257–1261. https://doi.org/10.1006/bbrc.2001.6062
Marcion G, Seigneuric R, Chavanne E, Artur Y, Briand L, Hadi T, Gobbo J, Garrido C, Neiers F (2014) C-terminal amino acids are essential for human heat shock protein 70 dimerization. Cell Stress Chaperones 20(1):61–72. https://doi.org/10.1007/s12192-014-0526-3
Mogk A, Deuerling E, Vorderwülbecke S, Vierling E, Bukau B (2003) Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Molecular microbiology 50(2):585–595. https://doi.org/10.1046/j.1365-2958.2003.03710.x
Mogk A, Ruger-Herreros C, Bukau B (2019) Cellular functions and mechanisms of action of small heat shock proteins. Annu Rev Microbiol 73(1):89–110. https://doi.org/10.1146/annurev-micro-020518-115515
Morimoto R, Santoro M (1998) Stress–inducible responses and heat shock proteins: New pharmacologic targets for cytoprotection. Nat Biotechnol 16:833–838. https://doi.org/10.1038/nbt0998-833
Mörner CT (1894) (1894) Untersuchen der Proteinsubstanzen in licht-brechenden Medien des Auges. Hoppe-Seyler’s Z Physiol Chem 18:61–106
Münchbach M, Nocker A, Narberhaus F (1999) Multiple small heat shock proteins in rhizobia. Journal of bacteriology 181(1):83–90. https://doi.org/10.1128/JB.181.1.83-90.1999
Narberhaus F (2002) α-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev 66(1):64–93. https://doi.org/10.1128/mmbr.66.1.64-93.2002
Nitta K, Suzuki N, Honma D, Kaneko Y, Nakamoto H (2005) Ultrastructural stability under high temperature or intensive light stress conferred by a small heat shock protein in cyanobacteria. FEBS Lett 579(5):1235–1242. https://doi.org/10.1016/j.febslet.2004.12.095
Obuchowski I, Liberek K (2020) Small but mighty: a functional look at bacterial sHSPs. Cell Stress Chaperones 25(4):593–600. https://doi.org/10.1007/s12192-020-01094-0
Pidot SJ, Porter JL, Tobias NJ, Anderson J, Catmull D, Seemann T, Kidd S, Davies JK, Reynolds E, Dashper S, Stinear TP (2010) Regulation of the 18 kDa heat shock protein in Mycobacterium ulcerans: an alpha-crystallin orthologue that promotes biofilm formation. Mol Microbiol 78(5):1216–1231. https://doi.org/10.1111/j.1365-2958.2010.07401.x
Ponomarenko M, Stepanenko I, Kolchanov N (2013) Heat shock proteins in Brenner’s encyclopedia of genetics (pp. 402–405). Elsevier. https://doi.org/10.1016/b978-0-12-374984-0.00685-9
Poulain P, Gelly JC, Flatters D (2010) Detection and architecture of small heat shock protein monomers. PLoS ONE 5(4):e9990. https://doi.org/10.1371/journal.pone.0009990
Reinle K, Mogk A, Bukau B (2022) The diverse functions of small heat shock proteins in the proteostasis network. J Mol Biol 434(1):167157. https://doi.org/10.1016/j.jmb.2021.167157
Rodriguez Ospina S, Blazier D, Criado-Marrero M, Gould L, Gebru N, Beaulieu-Abdelahad D, Wang X, Remily-Wood E, Chaput D, Stevens S, Uversky V, Bickford P, Dickey C, Blair L (2022) Small heat shock protein 22 improves cognition and learning in the tauopathic brain. Int J Mol Sci 23(2):851. https://doi.org/10.3390/ijms23020851
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(2):406–416. https://doi.org/10.1046/j.1432-1327.1999.00380.x
Saji H, Iizuka R, Yoshida T, Abe T, Kidokoro S, Ishii N, Yohda M (2008) Role of the IXI/V motif in oligomer assembly and function of StHsp14.0, a small heat shock protein from the acidothermophilic archaeon, Sulfolobus tokodaii strain 7. Proteins: Structure, Function, and Bioinformatics 71(2):771–782. https://doi.org/10.1002/prot.21762
Santhanagopalan I, Degiacomi MT, Shepherd DA, Hochberg GKA, Benesch JLP, Vierling E (2018) It takes a dimer to tango: oligomeric small heat shock proteins dissociate to capture substrate. J Biol Chem 293(51):19511–19521. https://doi.org/10.1074/jbc.ra118.005421
Schopf JW (2006) Fossil evidence of Archaean life. Phil Trans R Soc b: Biol Sci 361(1470):869–885. https://doi.org/10.1098/rstb.2006.1834
Shatov V, Weeks S, Strelkov S, Gusev N (2018) The role of the arginine in the conserved n-terminal domain RLFDQxFG motif of human small heat shock proteins hspb1, hspb4, hspb5, hspb6, and hspb8. Int J Mol Sci 19(7):2112. https://doi.org/10.3390/ijms19072112
Siddique M, Gernhard S, von Koskull-Döring P, Vierling E, Scharf KD (2008) The plant sHSP superfamily: five new members in Arabidopsis thaliana with unexpected properties. Cell Stress Chaperones 13(2):183–197. https://doi.org/10.1007/s12192-008-0032-6
Singh K, Groth-Vasselli B, Kumosinski TF, Farnsworth PN (1995) α-Crystallin quaternary structure: molecular basis for its chaperone activity. FEBS Lett 372(2–3):283–287. https://doi.org/10.1016/0014-5793(95)00980-n
Studer S, Obrist M, Lentze N, Narberhaus F (2002) A critical motif for oligomerization and chaperone activity of bacterial α-heat shock proteins. Eur J Biochem 269(14):3578–3586. https://doi.org/10.1046/j.1432-1033.2002.03049.x
Sudnitsyna MV, Mymrikov ES, Seit-Nebi A, Gusev N (2012) The role of intrinsically disordered regions in the structure and functioning of small heat shock proteins. Curr Protein Pept Sci 13(1):76–85. https://doi.org/10.2174/138920312799277875
Sun Y, MacRae TH (2005) Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci 62(21):2460–2476. https://doi.org/10.1007/s00018-005-5190-4
Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression 1577(1):1–9. https://doi.org/10.1016/s0167-4781(02)00417-7
Tang YC, Chang HC, Hayer-Hartl M, Hartl FU (2007) SnapShot: molecular chaperones, part II. Cell 128(2):412.e1-412.e2. https://doi.org/10.1016/j.cell.2007.01.013
Tian H, Tan J, Zhang L, Gu X, Xu W, Guo X, Luo Y (2012) Increase of stress resistance in Lactococcus lactis via a novel food-grade vector expressing a shsp gene from Streptococcus thermophilus. Brazilian journal of microbiology: [publication of the Brazilian Society for Microbiology] 43(3):1157–1164. https://doi.org/10.1590/S1517-838220120003000043
Tikhomirova TS, Selivanova OM, Galzitskaya OV (2017) α-Crystallins are small heat shock proteins: functional and structural properties. Biochem Mosc 82(2):106–121. https://doi.org/10.1134/s0006297917020031
Tóth ME, Sántha M, Penke B, Vígh L (2015). How to stabilize both the proteins and the membranes: diverse effects of shsps in neuroprotection. in heat shock proteins (pp. 527–562). Springer International Publishing. https://doi.org/10.1007/978-3-319-16077-1_23
Tsvetkova NM, Horváth I, Török Z, Wolkers WF, Balogi Z, Shigapova N, Crowe LM, Tablin F, Vierling E, Crowe JH, Vígh L (2002) Small heat-shock proteins regulate membrane lipid polymorphism. Proc Natl Acad Sci 99(21):13504–13509. https://doi.org/10.1073/pnas.192468399
Tyedmers J, Mogk A, Bukau B (2010) Cellular strategies for controlling protein aggregation. Nat Rev Mol Cell Biol 11(11):777–788. https://doi.org/10.1038/nrm2993
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(12):1025–1030. https://doi.org/10.1038/nsb722
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(18):11032–11037. https://doi.org/10.1074/jbc.273.18.11032
Vigh L, Horváth I, Maresca B, Harwood JL (2007) Can the stress protein response be controlled by ‘membrane-lipid therapy’? Trends Biochem Sci 32(8):357–363. https://doi.org/10.1016/j.tibs.2007.06.009
Vogel C, Bashton M, Kerrison ND, Chothia C, Teichmann SA (2004) Structure, function and evolution of multidomain proteins. Curr Opin Struct Biol 14(2):208–216. https://doi.org/10.1016/j.sbi.2004.03.011
Wang K, Spector A (1995) Alpha-crystallin can act as a chaperone under conditions of oxidative stress. Invest Ophthalmol vis Sci 36(2):311–321
Waters ER, Vierling E (2020) Plant small heat shock proteins – evolutionary and functional diversity. New Phytol 227(1):24–37. https://doi.org/10.1111/nph.16536
Waters ER, Lee GJ, Vierling E (1996) Evolution, structure and function of the small heat shock proteins in plants. J Exp Bot 47(3):325–338. https://doi.org/10.1093/jxb/47.3.325
Weeks SD, Baranova EV, Heirbaut M, Beelen S, Shkumatov AV, Gusev NB, Strelkov SV (2014) Molecular structure and dynamics of the dimeric human small heat shock protein HSPB6. J Struct Biol 185(3):342–354. https://doi.org/10.1016/j.jsb.2013.12.009
Weidmann S, Rieu A, Rega M, Coucheney F, Guzzo J (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, No-No. https://doi.org/10.1111/j.1574-6968.2010.01999.x
Weidmann S, Maitre M, Laurent J, Coucheney F, Rieu A, Guzzo J (2017) Production of the small heat shock protein Lo18 from Oenococcus oeni in Lactococcus lactis improves its stress tolerance. Int J Food Microbiol 247:18–23. https://doi.org/10.1016/j.ijfoodmicro.2016.06.005
Wirth (2003) Les protéines de choc thermique (heat shock proteins-Hsps). II. Hsp70 : biomarqueur et acteur du stress cellulaire. . Facmv.Ulg.Ac.Be; meertens, marina. (n.d.). Annales02/2003. http://www.facmv.ulg.ac.be/amv/articles/2003_147_2_05.pdf
Yeh CH, Chang PFL, Yeh KW, Lin WC, Chen YM, Lin CY (1997) Expression of a gene encoding a 16.9-kDa heat-shock protein, Oshsp16.9, in Escherichia coli enhances thermotolerance. Proc Natl Acad Sci 94(20):10967–10972. https://doi.org/10.1073/pnas.94.20.10967
Yuan CX, Czarnecka-Verner E, Gurley WB (1997) Expression of human heat shock transcription factors 1 and 2 in HeLa cells and yeast. Cell Stress Chaperones 2(4):263. https://doi.org/10.1379/1466-1268(1997)002<0263:eohhst>2.3.co;2
Zara S, Antonio Farris G, Budroni M, Bakalinsky AT (2002) HSP12 is essential for biofilm formation by a Sardinian wine strain of S. cerevisiae. Yeast 19(3):269–276. https://doi.org/10.1002/yea.831
Zeng L, Tan J, Lu T, Lei Q, Chen C, Hu Z (2015) Small heat shock proteins and the endoplasmic reticulum: potential attractive therapeutic targets? Curr Mol Med 15(1):38–46. https://doi.org/10.2174/1566524015666150114111745
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(4):1055–1061. https://doi.org/10.1016/j.bbrc.2005.03.092
Żwirowski S, Kłosowska A, Obuchowski I, Nillegoda NB, Piróg A, Ziętkiewicz S, Bukau B, Mogk A, Liberek K (2017) Hsp70 displaces small heat shock proteins from aggregates to initiate protein refolding. EMBO J 36(6):783–796. https://doi.org/10.15252/embj.201593378
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This research was funded by Conseil Régional de Bourgogne, the Université de Bourgogne grant number 2021Y-09559, and the ministère de l’Enseignement supérieur de la Recherche, grant number MESR 2020–04.
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Bellanger, T., Weidmann, S. Is the lipochaperone activity of sHSP a key to the stress response encoded in its primary sequence?. Cell Stress and Chaperones 28, 21–33 (2023). https://doi.org/10.1007/s12192-022-01308-7
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DOI: https://doi.org/10.1007/s12192-022-01308-7