Abstract
The ever-increasing number of proteins identified as belonging to the family of small heat-shock proteins (shsps) and α-crystallins enables us to reassess the phylogeny of this ubiquitous protein family. While the prokaryotic and fungal representatives are not properly resolved, most of the plant and animal shsps and related proteins are clearly grouped in distinct clades, reflecting a history of repeated gene duplications. The members of the shsp family are characterized by the presence of a conserved homologous “α-crystallin domain,” which sometimes is present in duplicate. Predictions are made of secondary structure and solvent accessibility of this domain, which together with hydropathy profiles and intron positions support the presence of two similar hydrophobic β-sheet-rich motifs, connected by a hydrophilic α-helical region. Together with an overview of the newly characterized members of the shsp family, these data help to define this family as being involved as stable structural proteins and as molecular chaperones during normal development and induced under pathological and stressful conditions.
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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
Almoguera C, Jordano J (1992) Developmental and environmental concurrent expression of sunflower dry-seed-stored low-molecular-weight heat-shock protein and Lea mRNAs. Plant Mol Biol 19: 781–792
Arrigo A-P, Landry J (1994) Expression and function of the low-molecular-weight heat shock proteins. In: Morimoto RJ, Tissièeres A, Georgopoulos C (eds) The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, New York, pp 335–373
Atomi Y, Yamada S, Strohman R, Nonomura Y (1991) αB-Crystallin in skeletal muscle: purification and localization. J Biochem 110: 812–822
Bartling D, Bülter H, Liebeton K, Weiler EW (1992) An Arabidopsis thaliona cDNA clone encoding a 17.6 kDa clas II heat shock protein. Plant Mol Biol 18:1007–1008
Bhat SP, Nagineni CN (1989) αB subunit of lens-specific protein α-crystallin is present in other ocular and non-ocular tissues. Biochem Biophys Res Commun 158:319–325
Bouchard RA (1990) Characterization of expressed meiotic prophase repeat transcript clones of Lilium: meiosis-specific expression, relatedness, and affinities to small heat shock protein genes. Genome 33:68–79.
Candido EPM, Jones D, Dixon DK, Graham RW, Russnak RH, Kay RJ (1989) Structure, organization, and expression of the 16-kDa heat shock gene family of Caenorhabditis elegans. Genome 31:690–697
Cao M, Chao H, Doughty BL (1993) Cloning of a cDNA encoding an egg antigen homologue from Schistosoma mansoni. Mol Biochem Parasitol 58:169–172
Carver JA, Aquilina JA, Truscott RJW, Ralston GB (1992) Identification by 1H NMR spectroscopy of flexible extensions in bovine lens α-crystallin. FEBS Lett 311:143–149
Caspers G-J, Pennings J, de Jong WW (1994) A partial cDNA sequence corrects the human αA-crystallin primary structure. Exp Eye Res 59:125–126
Chen Q, Vierling E (1991) Analysis of conserved domains identifies a unique structural feature of a chloroplast heat shock protein. Mol Gen Genet 226:425–431
Cooper LF, Uoshima K (1994) Differential estrogenic regulation of small M1 heat shock protein expression in osteoblasts. J Biol Chem 269:7869–7873
de Jong WW, Leunissen JAM, Leenen PJM, Zweers A, Versteeg M (1988) Dogfish α-crystallin sequences: comparison with small heat shock proteins and Schistosoma egg antigen. J Biol Chem 263: 5141–5149
de Jong WW, Leunissen JAM, Voorter CEM (1993) Evolution of the α-crystallin/small heat-shock protein family. Mol Biol Evol 10: 103–126
de Jong WW, Zweers A, Versteeg M, Nuy-Terwindt EC (1984) Primary structures of the α-crystallin A chains of twenty-eight mammalian species, chicken and frog. Eur J Biochem 141:131–140
Felsenstein J (1993) PHYLIP: phylogeny inference package, version 3.5c. Distributed by the author, Department of Genetics, University of Washington, Seattle WA
Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284
Fröhli E, Aoyarna A, Klemenz R (1993) Cloning of the mouse hsp25 gene and an extremely conserved hsp25 pseudogene. Gene 128: 273–277
Gaestel M, Gotthardt R, Miller T (1993) Structure and organization of a marine gene encoding small heat-shock protein Hsp25. Gene 128:279–283
Gernold M, Knauf U, Gaestel M, Stahl J, Kloetzel P-M (1993) Development and tissue-specific distribution of mouse small heat shock protein hsp25. Dev Genet 14:103–111
Gribskov M, Luethy R, Eisenberg D (1990) Profile analysis. Methods Enzymol 193:146–159
Groenen PJTA, Merck KB, de Jong WW, Bloemendal H (1994) Structure and modifications of the junior chaperone α-crystallin: from lens transparency to molecular pathology. Eur J Biochem 225:1–19
Györgyey J, Gartner A, Nemeth K, Magyar Z, Hirt H, Heberle-Bors E, Dudits D (1991) Alfalfa heat shock genes are differentially expressed during somatic embryogenesis. Plant Mol Biol 16:999–1007
Heidelbach M, Skladny H, Schairer HU (1993a) Purification and characterization of SP21, a development-specific protein of the myxobacterium Stigmatella aurantiaca. J Bacteriol 175:905–908
Heidelbach M, Skladny H, Schairer HU (1993b) Heat shock and development induce synthesis of a low-molecular-weight stress-responsive protein in the myxobacterium Stigmatella aurantiaca. J Bacteriol 175:7479–7482
Helm KW, Abernethy RH (1990) Heat shock proteins and their mRNAs in dry and early imbibing embryos of wheat. Plant Physiol 93:1626–1633
Helm KW, LaFayette PR, Nagao RT, Key JL, Vierling E (1993) Localization of small heat shock proteins to the higher plant endomembrane system. Mol Cell Biol 13:238–247
Hendrick JP, Hartl FU (1993) Molecular chaperone functions of heatshock proteins. Anna Rev Biochem 62:349–384
Hickey E, Brandon SE, Potter R, Stein G, Stein J, Weber LA (1986) Sequence and organization of genes encoding the human 27 kDa heat shock protein. Nucleic Acids Res 14:4127–4145
Hoffman EP, Gerring SL, Corces VG (1987) The ovarian, ecdysterone, and heat-shock-responsive promoters of the Drosophila melanogaster hsp27 gene react very differently to perturbations of DNA sequence. Mol Cell Biol 7:973–981
Horwitz J (1992) α-Crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89:10449–10453
Howarth C (1990) Heat shock proteins in Sorghum bicolor and Pennisetum americanum. II. Stored RNA in sorghum seed and its relationship to heat shock protein synthesis during germination. Plant Cell Environ 13:57–64
Ingolia TD, Craig EA (1982) Four small heat shock proteins are related to each other and to mammalian α-crystallin. Proc Natl Acad Sci USA 79:2360–2364
Jakob U, Gaestel M, Engel K, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268:1517–1520
Jorgensen JA, Nguyen HT (1994) Isolation, sequence and expression of a cDNA encoding a Class I heat shock protein (HSP17.2) in maize. Plant Sci 97:169–175
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132
Kato K, Goto S, Inaguma Y, Hasegawa K, Morishita R, Asano T (1994) Purification and characterization of a 20-kDa protein that is highly homologous to αB crystallin. J Biol Chem 269:15302–15309
Kato K, Shinohara H, Kurobe N, Goto S, Inaguma Y, Ohshima K (1991) Immunoreactive αA-crystallin in rat non-lenticular tissues detected with a sensitive immunoassay method. Biochim Biophys Acta 1080:173–180
Klemenz R, Fröhli E, Steiger RH, Schäfer R, Aoyama A (1991) αB-Crystallin is a small heat shock protein. Proc Natl Acad Sci USA 88:3652–3656
Knack G, Liu Z, Kloppstech K (1992) Low molecular mass heat-shock proteins of a light-resistant photoautotrophic cell culture. Eur J Cell Biol 59:166–175
Krishna P, Felsheim RF, Larkin JC, Das A (1992) Structure and light-induced expression of a small heat-shock protein gene of Pharbitis nil. Plant Physiol 100:1772–1779
Kurtz S, Rossi J, Petko L, Lindquist S (1986) An ancient developmental induction: heat-shock proteins induced in sporulation and oogenesis. Science 231:1154–1157
Landry J, Chréden P, Lambert H, Hickey E, Weber LA (1989) Heat shock resistance conferred by expression of the human HSP27 gene in rodent cells. J Cell Biol 109:7–15
Lee DC, Kim RY, Wistow GJ (1993) An avian αB-crystallin: non-lens expression and sequence similarities with both small (HSP27) and large (HSP70) heat shock proteins. J Mol Biol 232:1221–1226
Li L-K, Spector A (1974) Circular dichroism and optical rotatory dispersion of the aggregates of purified polypeptides of alphacrystallin. Exp Eye Res 19:49–57
Lindquist S, Craig EA (1988) The heat shock proteins. Annu Rev Genet 22:631–677
Marin R, Valet JP, Tanguay RM (1993) Hsp23 and hsp26 exhibit distinct spatial and temporal patterns of constitutive expression in Drosophila adults. Dev Genet 14:69–77
Mehlen P, Briolay J, Smith L, Diaz Latoud C, Fabre N, Pauli D, Arrigo AP (1993) Analysis of the resistance to heat and hydrogen peroxide stresses in COS cells transiently expressing wild type or deletion mutants of the Drosophila 27-kDa heat-shock protein. Eur J Biochem 215:277–284
Merck KB, Groenen PJTA, Voorter CEM, de Haard-Hoekman WA, Horwitz J, Bloemendal H, de Jong WW (1993a) Structural and functional similarities of bovine α-crystallin and mouse small heat-shock protein: a family of chaperones. J Biol Chem 268:1046–1052
Merck KB, Horwitz J, Kersten M, Overkamp P, Gaestel M, Bloemendal H, de Jong WW (1993b) Comparison of the homologous carboxy-terminal domain and tail of α-crystallin and small heat shock protein. Mol Biol Rep 18:209–215
Miron T, Vancompernolle K, Vanderkerckhove J, Wilchek M, Geiger B (1991) A 25-kD inhibitor of actin polymerization is a low molecular weight mass heat shock protein. J Cell Biol 114:255–261
Morimoto RI, Tissières A, Georgopoulos C (eds) (1994) The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, New York
Moser D, Doenhoff MJ, Klinkert MQ (1992) A stage-specific calcium-binding protein expressed in eggs of Schistosoma mansoni. Mol Biochem Parasitol 51:229–238
Nene V, Dunne DW, Johnson KS, Taylor DW, Cordingley IS (1986) Sequence and expression of a major egg antigen from Schistosoma mansoni: homologies to heat shock proteins and α-crystallins. Mol Biochem Parasitol 21:179–188
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
Nicholl ID, Quinlan RA (1994) Chaperone activity of α-crystallin modulates intermediate filament assembly. EMBO J 13:945–953
Nover L, Scharf K-L, Neumann D (1989) Cytoplasmic heat shock granules are formed from precursor particles and are associated with a specific set of mRNAs. Mol Cell Biol 9:1298–1308
Patthy L (1994) Introns and exons. Curr Opin Struct Biol 4:383–392
Plesofsky-Vig N, Vig J, Brambl R (1992) Phylogeny of the α-crystallin-related heat-shock proteins. J Mol Evol 35:537–545
Raschke E, Baumann G, Schöffl F (1988) Nucleotide sequence analysis of soybean small heat shock protein genes belonging to two different multigene families. J Mol Biol 199:549–557
Rost B, Sander C (1993) Prediction of protein secondary structure at better than 70% accuracy. J Mol Biol 232:584–599
Rost B, Sander C (1994) Conservation and prediction of solvent accessibility in protein families. Proteins (in press)
Rost B, Sander C, Schneider R (1994) PHD—an automatic mail server for protein secondary structure prediction. Comp Appl Biosci 10: 53–60
Saitou N, Nei M (1987) The neighbor joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
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
Sawada K, Agata K, Eguchi G (1992) Crystallin gene expression in the process of lentodogenesis in cultures of chicken lens epithelial cells. Exp Eye Res 55:879–887
Shirakata M, Takagi T, Konishi K (1986) Isolation and characterization of a 29,000 dalton protein from ascidian (Halocynthia roretzi) body wall muscle. Comp Biochem Physiol 85B:71–76
Susek RE, Lindquist SL (1989) HSP26 of Saccharomyces cerevisiae is related to the superfamily of small heat shock proteins but is without a demonstrable function. Mol Cell Biol 9:5265–5271
Sweet M, Eisenberg D (1983) Correlation of sequence hydrophobicities measures similarities in three-dimensional protein structures. J Mol Biol 171:479–488
Takagi T, Yasunaga H, Nakamura A (1993) Structure of 29-kDa protein from ascidian (Halocynthia roretzi) body wall muscle. J Biochem 113:321–326
Takemoto L, Emmons T (1991) Truncation of αA-crystallin from the human lens. Exp Eye Res 53:811–813
Tardieu A, Delaye M (1988) Eye lens proteins and transparency: from light transmission theory to solution X-ray structural analysis. Annu Rev Biophys Chem 17:47–70
Tseng TS, Yeh KW, Yeh CH, Chang FC, Chen YM, Lin CY (1992) Two rice (Oryza sativa) full-length cDNA clones encoding low-molecular-weight heat-shock proteins. Plant Mol Biol 18:963–965
Tweedie S, Grigg ME, Ingram L, Selkirk ME (1993) The expression of a small heat shock protein homologue is developmentally regulated in Nippostrongylus brasiliensis. Mol Biochem Parasitol 61:149–154
Verbon A, Hartskeerl RA, Schuitema A, Kolk AHJ, 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
Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620
Vierling E, Sun A (1987) Developmental expression of heat shock proteins in higher plants. In: Cherry J (ed) Environmental stress in plants: biochemical and physiological mechanisms associated with environmental stress tolerance in plants. Springer-Verlag, New York, pp 343–354
Weng J, Wang Z-F, Nguyen HT (1991) Nucleotide sequence of a Triticum aestivum cDNA clone which is homologous to the 26 kDa chloroplast-localized heat shock protein gene of maize. Plant Mol Biol 17:255–258
Wilson R, Ainscough R, Anderson K, Baynes C, Berks M, Bonfield J, Burton J, Connel M, Copsey T, Cooper J, Coulson A, Craxton M, Dear S, Du Z, Durbin R, Favello A, Fraser A, Fulton L, Gardner A, Green P, Hawkins T, Hillier L, Jier M, Johnston L, Jones M, Kershaw J, Kirsten J, Laisster N, Latrielle P, Lightning J, Lloyd C, Mortimore B, O'Callaghan M, Parsons J, Percy C, Rifken L, Roopra A, Saunders D, Shownkeen R, Sims M, Smaldon N, Smith A, Smith M, Sonnhammer E, Staden R, Sulston J, Thierry-Mieg J, Thomas K, Vaudin M, Vaughan K, Waterston R, Watson A, Weinstock L, Wilkinson-Sproat J, Wohldman P (1994) 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature 368:32–38
Wistow G (1985) Domain structure and evolution in α-crystallins and small heat-shock proteins. FEBS Lett 181:1–6
Wistow GJ, Piatigorsky J (1988) Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem 57:479–504
Zimmerman JL, Petri W, Meselson M (1983) Accumulation of a specific subset of D. melanogaster heat shock mRNAs in normal development without heat shock. Cell 32:1161–1170
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Correspondence to: W.W. de Jong
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Caspers, GJ., Leunissen, J.A.M. & de Jong, W.W. The expanding small heat-shock protein family, and structure predictions of the conserved “α-crystallin domain”. J Mol Evol 40, 238–248 (1995). https://doi.org/10.1007/BF00163229
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DOI: https://doi.org/10.1007/BF00163229