Advertisement

Evolution of Bacterial Chaperonin 60 Paralogues and Moonlighting Activity

  • Shekhar C. Mande
  • C. M. Santosh Kumar
  • Aditi Sharma
Chapter
Part of the Heat Shock Proteins book series (HESP, volume 7)

Abstract

Around two thirds of genome sequenced bacteria encode one chaperonin 60 protein with the other third encoding between two and eight chaperonin 60 paralogues. A surprising finding is that these bacterial proteins have a wide, and growing, range of additional functions both within the bacterium, but principally when the Cpn60 protein exits the cell and exists on the bacterial cell wall or in the bacterium’s external milieu. These findings have occurred at the same time that it has been realised that bacterial Cpn60 proteins can assume lower oligomeric forms than that of the prototypic tetradecameric E. coli GroEL. It is possible that lower oligomeric forms of Cpn60 may more readily be secreted and interact with biopolymers in a distinct manner to that of the tetradecameric homologues and paralogues. How the Cpn60 moonlighting functions evolved is a key question to be addressed. To address this question we postulate that the chaperonin genes have been subject to different selective constraints over evolutionary time. Gene duplication, followed by sequence divergence, resulted in the evolution of paralogous Cpn60 proteins that have distinct moonlighting activities. Moreover, these functional variations might be acquired by incorporating chemically dissimilar substitutions at functionally important residues.

Keywords

Apical Domain Equatorial Domain groEL Gene Intermediate Domain Argininosuccinate Lyase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We thank Payel Ghosh and Pooja Gupta for stimulating discussions. The work was financially supported by the Department of Biotechnology (DBT), India. AS is a senior research fellow funded by University Grants Commission, India and CMSK is a research associate funded by the DBT.

References

  1. Archibald JM, Roger AJ (2002) Gene duplication and gene conversion shape the evolution of archaeal chaperonins. J Mol Biol 316:1041–1050PubMedCrossRefGoogle Scholar
  2. Archibald JM, Logsdon JM, Doolittle WF (1999) Recurrent paralogy in the evolution of archaeal chaperonins. Curr Biol 9:1053–1056PubMedCrossRefGoogle Scholar
  3. Archibald JM, Logsdon JM, Doolittle WF (2000) Origin and evolution of eukaryotic chaperonins: phylogenetic evidence for ancient duplications in CCT genes. Mol Biol Evol 17:1456–1466PubMedCrossRefGoogle Scholar
  4. Archibald JM, Blouin C, Doolittle WF (2001) Gene duplication and the evolution of group II chaperonins: implications for structure and function. J Struct Biol 135:157–169PubMedCrossRefGoogle Scholar
  5. Basu D, Khare G, Singh S, Tyagi A, Khosla S, Mande SC (2009) A novel nucleoid-associated protein of Mycobacterium tuberculosis is a sequence homolog of GroEL. Nucleic Acids Res 37:4944–4954PubMedCrossRefGoogle Scholar
  6. Bateman OA, Purkiss AG, van Montfort R, Slingsby C, Graham C, Wistow G (2003) Crystal structure of η-crystallin: adaptation of a class 1 aldehyde dehydrogenase for a new role in the eye lens. Biochemistry 42:4349–4356PubMedCrossRefGoogle Scholar
  7. Baumann P, Baumann L, Clark MA (1996) Levels of Buchnera aphidicola Chaperonin GroEL during growth of the aphid Schizaphis graminum. Curr Microbiol 32:279–285CrossRefGoogle Scholar
  8. Brocchieri L, Karlin S (2000) Conservation among HSP60 sequences in relation to structure, function, and evolution. Prot Sci 9:476–486CrossRefGoogle Scholar
  9. Cao MJ, Osatomi K, Matsuda R, Ohkubo M, Hara K, Ishihara T (2000) Purification of a novel serine proteinase inhibitor from the skeletal muscle of white croaker (Argyrosomus argentatus). Biochem Biophys Res Commun 272:485–489PubMedCrossRefGoogle Scholar
  10. Chaput M, Claes V, Portetelle D, Cludts I, Cravador A, Burny A, Gras H, Tartar A (1988) The neurotrophic factor neuroleukin is 90 % homologous with phosphohexose isomerase. Nature 332:454–455PubMedCrossRefGoogle Scholar
  11. Clark GW, Tillier ER (2010) Loss and gain of GroEL in the mollicutes. Biochem Cell Biol 88:185–194PubMedCrossRefGoogle Scholar
  12. Cummings L, Riley L, Black L, Souvorov A, Resenchuk S, Dondoshansky I, Tatusova T (2002) Genomic BLAST: custom-defined virtual databases for complete and unfinished genomes. FEMS Microbiol Lett 216:133–138PubMedCrossRefGoogle Scholar
  13. Dekker C, Willison KR, Taylor WR (2011) On the evolutionary origin of the chaperonins. Proteins 79:1172–1192PubMedCrossRefGoogle Scholar
  14. Dickson R, Weiss C, Howard RJ, Alldrich SP, Ellis RJ, Lorimer GH, Azem A, Viitanen PV (2000) Reconstitution of higher plant chloroplast chaperonin 60 tetradecamers active in protein folding. J Biol Chem 275:11829–11835PubMedCrossRefGoogle Scholar
  15. Fares MA, Ruiz-Gonza´ lez MX, Moya A, Elena SF, Barrio E (2002a) Endosymbiotic bacteria: GroEL buffers against deleterious mutations. Nature 417:398PubMedCrossRefGoogle Scholar
  16. Fares MA, Barrio E, Sabater-Mun˜oz B, Moya A (2002b) The evolution of the heat-shock protein GroEL from Buchnera, the primary endosymbiont of aphids, is governed by positive selection. Mol Biol Evol 19:1162–1170PubMedCrossRefGoogle Scholar
  17. Fares MA, Moya A, Barrio E (2005) Adaptive evolution in GroEL from distantly related endosymbiotic bacteria of insects. J Evol Biol 18:651–660PubMedCrossRefGoogle Scholar
  18. Farr GW, Fenton WA, Horwich AL (2007) Perturbed ATPase activity and not “close confinement” of substrate in the cis cavity affects rates of folding by tail-multiplied GroEL. Proc Natl Acad Sci U S A 104:5342–5347PubMedCrossRefGoogle Scholar
  19. Fischer HM, Babst M, Kaspar T, Acuña G, Arigoni F, Hennecke H (1993) One member of a groESL-like chaperonin multigene family in Bradyrhizobium japonicum is co-regulated with symbiotic nitrogen fixation genes. EMBO J 12:2901–2912PubMedGoogle Scholar
  20. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545PubMedGoogle Scholar
  21. Friedland JS, Shattock R, Remick DG, Griffin GE (1993) Mycobacterial 65-kD heat shock protein induces release of proinflammatory cytokines from human monocytic cells. Clin Exp Immunol 91:58–62PubMedCrossRefGoogle Scholar
  22. Garduño RA, Garduño E, Hoffman PS (1998) Surface-associated Hsp60 chaperonin of Legionella pneumophila mediates invasion in a HeLa cell model. Infect Immun 66:4602–4610PubMedGoogle Scholar
  23. Gervasoni P, Staudenmann W, James P, Gehrig P, Plückthun A (1996) β-Lactamase binds to GroEL in a conformation highly protected against hydrogen/deuterium exchange. Proc Natl Acad Sci U S A 93:12189–12194PubMedCrossRefGoogle Scholar
  24. Goldberg MA, Zhang J, Sondek S, Matthews CR, Fox RO, Horwich AL (1997) Native-like structure of a protein-folding intermediate bound to the chaperonin GroEL. Proc Natl Acad Sci U S A 94:1080–1085PubMedCrossRefGoogle Scholar
  25. Goyal K, Qamra R, Mande SC (2006) Multiple gene duplication and rapid evolution in the groEL gene: functional implications. J Mol Evol 63:781–787PubMedCrossRefGoogle Scholar
  26. Gurney ME, Heinrich SP, Lee MR, Yin HS (1986) Molecular cloning and expression of neuroleukin, a neurotrophic factor for spinal and sensory neurons. Science 234:566–574PubMedCrossRefGoogle Scholar
  27. Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–579PubMedCrossRefGoogle Scholar
  28. Hartl FU, Hayer-Hartl M (2003) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858CrossRefGoogle Scholar
  29. Hartl F, Martin J (1995) Molecular chaperones in cellular protein folding. Curr Opin Struct Biol 5:92–102PubMedCrossRefGoogle Scholar
  30. Hayer-Hartl MK, Martin J, Hartl FU (1995) Asymmetrical interaction of GroEL and GroES in the ATPase cycle of assisted protein folding. Science 269:836–841PubMedCrossRefGoogle Scholar
  31. He X, Zhang J (2005) Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169:1157–1164PubMedCrossRefGoogle Scholar
  32. Henderson B, Martin A (2011) Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect Immun 79:3476–3491PubMedCrossRefGoogle Scholar
  33. Hendriks W, Mulders JW, Bibby MA, Slingsby C, Bloemendal H, de Jong WW (1988) Duck lens ε-crystallin and lactate dehydrogenase B4 are identical: a single-copy gene product with two distinct functions. Proc Natl Acad Sci U S A 85:7114–7118PubMedCrossRefGoogle Scholar
  34. Horwich AL, Fenton WA, Chapman E, Farr GW (2007) Two families of chaperonin: physiology and mechanism. Annu Rev Cell Dev Biol 23:115–145PubMedCrossRefGoogle Scholar
  35. Huberts DH, van der Klei IJ (2010) Moonlighting proteins: an intriguing mode of multitasking. Biochim Biophys Acta 1803:520–525PubMedCrossRefGoogle Scholar
  36. Hughes L (1993) Contrasting evolutionary rates in the duplicate chaperonin genes of Mycobacterium tuberculosis and M. leprae. Mol Biol 10:1343–1359Google Scholar
  37. Huq S, Sueoka K, Narumi S, Arisaka F, Nakamoto H (2010) Comparative biochemical characterization of two GroEL homologs from the Cyanobacterium Synechococcuselongatus PCC 7942. Biosci Biotechnol Biochem 74:2273–2280PubMedCrossRefGoogle Scholar
  38. Jeffery CJ (1999) Moonlighting proteins. Trends Biochem Sci 24:8–11PubMedCrossRefGoogle Scholar
  39. Jeffery CJ (2004a) Molecular mechanisms for multitasking: recent crystal structures of moonlighting proteins. Curr Opin Struct Biol 14:663–668PubMedCrossRefGoogle Scholar
  40. Jeffery CJ (2004b) Moonlighting proteins: complications and implications for proteomics research. DDT: Targets 3:71–78Google Scholar
  41. Jeffery CJ (2009) Moonlighting proteins – an update. Mol Biosyst 5:345–350PubMedCrossRefGoogle Scholar
  42. Joshi MC, Sharma A, Kant S, Birah A, Gupta GP, Khan SR, Bhatnagar R, Banerjee N (2008) An insecticidal GroEL protein with chitin binding activity from Xenorhabdus nematophila. J Biol Chem 283:28287–28296PubMedCrossRefGoogle Scholar
  43. Kaufman BA, Kolesar JE, Perlman PS, Butow RA (2003) A function for the mitochondrial chaperonin Hsp60 in the structure and transmission of mitochondrial DNA nucleoids in Saccharomyces cerevisiae. J Cell Biol 163:457–461PubMedCrossRefGoogle Scholar
  44. Khan N, Alam K, Mande SC, Valluri VL, Hasnain SE, Mukhopadhyay S (2008) Mycobacterium tuberculosis heat shock protein 60 modulates immune response to PPD by manipulating the surface expression of TLR2 on macrophages. Cell Microbiol 10:1711–1722PubMedCrossRefGoogle Scholar
  45. Kirby AC, Meghji S, Nair SP, White P, Reddi K, Nishihara T, Nakashima K, Willis AC, Sim R, Wilson M, Henderson B (1995) The potent bone resorbing mediator of Actinobacillus actinomycetemcomitans is homologous to the molecular chaperone GroEL. J Clin Invest 96:1185–1194PubMedCrossRefGoogle Scholar
  46. Kong TH, Coates AR, Butcher PD, Hickman CJ, Shinnick TM (1993) Mycobacterium tuberculosis expresses two chaperonin-60 homologs. Proc Natl Acad Sci U S A 90:2608–2612PubMedCrossRefGoogle Scholar
  47. Kumar CMS, Mande SC (2011) Protein chaperones and non-protein substrates: on substrate promiscuity of GroEL. Curr Sci 100:1646–1653Google Scholar
  48. Kumar CMS, Khare G, Srikanth CV, Tyagi AK, Sardesai AA, Mande SC (2009) Facilitated oligomerization of mycobacterial GroEL: evidence for phosphorylation-mediated oligomerization. J Bacteriol 191:6525–6538PubMedCrossRefGoogle Scholar
  49. Lars Ditzel L, Lo we J, Stock D, Stetter K, Huber H, Huber R, Steinbacher S (1998) Crystal structure of the thermosome, the archaeal chaperonin and homolog of CCT. Cell 93:125–138CrossRefGoogle Scholar
  50. Lehel C, Los D, Wada H, Györgyei J, Horváth I, Kovács E, Murata N, Vigh L (1993) A second groEL-like gene, organized in a groESL operon is present in the genome of Synechocystis sp. PCC 6803. J Biol Chem 268:1799–1804PubMedGoogle Scholar
  51. Levy-Rimler G, Viitanen P, Weiss C, Sharkia R, Greenberg A, Niv A, Lustig A, Delarea Y, Azem A (2001) Type I chaperonins: not all are created equal. Eur J Biochem 268:3465–3472PubMedCrossRefGoogle Scholar
  52. Lewthwaite JC, Coates AR, Tormay P, Singh M, Mascagni P, Poole S, Roberts M, Sharp L, Henderson B (2001) Mycobacterium tuberculosis chaperonin 60.1 is a more potent cytokine stimulator than chaperonin 60.2 (Hsp 65) and contains a CD14-binding domain. Infect Immun 69:7349–7355PubMedCrossRefGoogle Scholar
  53. Lin CY, Huang YS, Li CH, Hsieh YT, Tsai NM, He PJ, Hsu WT, Yeh YC, Chiang FH, Wu MS, Chang CC, Liao KW (2009) Characterizing the polymeric status of Helicobacter pylori heat shock protein 60. Biochem Biophys Res Commun 388:283–289PubMedCrossRefGoogle Scholar
  54. Lund PA (2009) Multiple chaperonins in bacteria – why so many? FEMS Microbiol Rev 33:785–800PubMedCrossRefGoogle Scholar
  55. Lynch M, Force A (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459–473PubMedGoogle Scholar
  56. Mayhew M, da Silva AC, Martin J, Erdjument-Bromage H, Tempst P, Hartl FU (1996) Protein folding in the central cavity of the GroEL-GroES chaperonin complex. Nature 379:420–426PubMedCrossRefGoogle Scholar
  57. McCutcheon JP, McDonald BR, Moran NA (2009) Origin of an alternative genetic code in the extremely small and GC–rich genome of a bacterial symbiont. PLoS Genet 5:e1000565PubMedCrossRefGoogle Scholar
  58. Muro-Pastor AM, Ostrovsky P, Maloy S (1997) Regulation of gene expression by repressor localization: biochemical evidence that membrane and DNA binding by the PutA protein are mutually exclusive. J Bacteriol 179:2788–2791PubMedGoogle Scholar
  59. Ohno S (1970) Evolution by gene duplication. Springer, Berlin/Heidelberg/New York, pp 59–87Google Scholar
  60. Ojha A, Anand M, Bhatt A, Kremer L, Jacobs WR Jr, Hatfull GF (2005) GroEL1: a dedicated chaperone involved in mycolic acid biosynthesis during biofilm formation in mycobacteria. Cell 123:861–873PubMedCrossRefGoogle Scholar
  61. Ostrovsky de Spicer P, Maloy S (1993) PutA protein, a membrane-associated flavin dehydrogenase, acts as a redox-dependent transcriptional regulator. Proc Natl Acad Sci U S A 90:4295–4298PubMedCrossRefGoogle Scholar
  62. Piatigorsky J (1998) Multifunctional lens crystallins and corneal enzymes. More than meets the eye. Ann N Y Acad Sci 842:7–15PubMedCrossRefGoogle Scholar
  63. Piatigorsky J, Vistow GJ (1989) Enzyme/Crystallins: gene sharing as evolutionary strategy. Cell 57:197–199PubMedCrossRefGoogle Scholar
  64. Qamra R, Mande SC (2004) Crystal structure of the 65-kDa heat shock protein, chaperonin 60.2 of Mycobacterium tuberculosis. J Bacteriol 186:8105–8113PubMedCrossRefGoogle Scholar
  65. Qamra R, Srinivas V, Mande SC (2004) Mycobacterium tuberculosis GroEL homologues unusually exist as lower oligomers and retain the ability to suppress aggregation of substrate proteins. J Mol Biol 342:605–617PubMedCrossRefGoogle Scholar
  66. Ran L, Huang F, Ekman M, Klint J, Bergman B (2007) Proteomic analyses of the photo auto- and diazotrophically grown cyanobacterium Nostoc sp. PCC 73102. Microbiology 153:608–618PubMedCrossRefGoogle Scholar
  67. Rao T, Lund PA (2010) Differential expression of the multiple chaperonins of Mycobacterium smegmatis. FEMS Microbiol Lett 310:24–31PubMedCrossRefGoogle Scholar
  68. Read J, Pearce J, Li X, Muirhead H, Chirgwin J, Davies C (2001) The crystal structure of human phosphoglucose isomerase at 1.6 Å resolution: implications for catalytic mechanism, cytokine activity and haemolytic anaemia. J Mol Biol 309:447–463PubMedCrossRefGoogle Scholar
  69. Reddi K, Meghji S, Nair SP, Arnett TR, Miller AD, Preuss M, Wilson M, Henderson B, Hill P (1998) The Escherichia coli chaperonin 60 (groEL) is a potent stimulator of osteoclast formation. J Bone Miner Res 13:1260–1266PubMedCrossRefGoogle Scholar
  70. Riffo-Vasquez Y, Coates AR, Page CP, Spina D (2012) Mycobacterium tuberculosis chaperonin 60.1 inhibits leukocyte diapedesis in a murine model of allergic lung inflammation. Am J Respir Cell Mol Biol 47:245–252PubMedCrossRefGoogle Scholar
  71. Robinson CV, Groß M, Eyles SJ, Ewbank JJ, Mayhew M, Hartl F-U, Dobson CM, Radford SE (1995) Conformation of GroEL-bound α-lactalbumin probed by mass spectrometry. Nature 372:646–651CrossRefGoogle Scholar
  72. Rudolph B, Gebendorfer KM, Buchner J, Winter J (2010) Evolution of Escherichia coli for growth at high temperatures. J Biol Chem 285:19029–19034PubMedCrossRefGoogle Scholar
  73. Schneiker S et al (2007) Complete genome sequence of the myxobacterium Sorangium cellulosum. Nat Biotechnol 25:1281–1289PubMedCrossRefGoogle Scholar
  74. Schulz LC, Bahr JM (2003) Glucose-6-phosphate isomerase is necessary for embryo implantation in the domestic ferret. Proc Natl Acad Sci U S A 100:8561–8566PubMedCrossRefGoogle Scholar
  75. Schulz LC, Bahr JM (2004) Potential endocrine function of the glycolytic enzyme glucose-6-phosphate isomerase during implantation. Gen Comp Endocrinol 13:283–287CrossRefGoogle Scholar
  76. Sielaff B, Lee KS, Tsai FT (2011) Structural and functional conservation of Mycobacterium tuberculosis GroEL paralogs suggests that GroEL1 is a chaperonin. J Mol Biol 405:831–839PubMedCrossRefGoogle Scholar
  77. Stewart GR, Wernisch L, Stabler R, Mangan JA, Hinds J, Laing KG, Young DB, Butcher PD (2002) Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays. Microbiology 148:3129–3138PubMedGoogle Scholar
  78. Suzuki M, Ueno T, Iizuka R, Miura T, Zako T, Akahori R, Miyake T, Shimamoto N, Aoki M, Tanii T, Ohdomari I, Funatsu T (2008) Effect of the C-terminal truncation on the functional cycle of chaperonin GroEL: implication that the C-terminal region facilitates the transition from the folding-arrested to the folding-competent state. J Biol Chem 283:23931–23939PubMedCrossRefGoogle Scholar
  79. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCrossRefGoogle Scholar
  80. Tanaka N, Hiyama T, Nakamoto H (1997) Cloning, characterization and functional analysis of groESL operon from thermophilic cyanobacterium Synechococcus vulcanus. Biochem Biophys Acta 1343:335–348PubMedCrossRefGoogle Scholar
  81. Tanaka N, Haga A, Uemura H, Akiyama H, Funasaka T, Nagase H, Raz A, Nakamura KT (2002) Inhibition mechanism of cytokine activity of human autocrine motility factor examined by crystal structure analyses and site-directed mutagenesis studies. J Mol Biol 318:985–997PubMedCrossRefGoogle Scholar
  82. Tang YC, Chang HC, Roeben A, Wischnewski D, Wischnewski N, Kerner MJ, Hartl FU, Hayer-Hartl M (2006) Structural features of the GroEL-GroES nano-cage required for rapid folding of encapsulated protein. Cell 125:903–914PubMedCrossRefGoogle Scholar
  83. Techtmann SM, Robb FT (2010) Archaeal-like chaperonins in bacteria. Proc Natl Acad Sci U S A 107:20269–20274PubMedCrossRefGoogle Scholar
  84. Walden WE, Selezneva AI, Dupuy J, Volbeda A, Fontecilla-Camps JC, Theil EC, Volz K (2006) Structure of dual function iron regulatory protein 1 complexed with ferritin IRE-RNA. Science 314:1903–1908PubMedCrossRefGoogle Scholar
  85. Wang J, Herman C, Tipton K, Gross C, Weissman J (2002) Directed evolution of substrate-optimized GroEL/S chaperonins. Cell 111:1027–1039PubMedCrossRefGoogle Scholar
  86. Wast J, Fraunholz M, Zauner S, Douglas S, Maier UG (1999) Ancient gene duplication and differential gene flow in plastid lineages: the GroEL/Cpn60 example. J Mol Evol 48:112–117CrossRefGoogle Scholar
  87. Watanabe H, Takehana K, Date M, Shinozaki T, Raz A (1996) Tumor cell autocrine motility factor is the neuroleukin/phosphohexose isomerase polypeptide. Cancer Res 56:2960–2963PubMedGoogle Scholar
  88. Wistow GJ, Piatigorsky J (1988) Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem 57:479–504PubMedCrossRefGoogle Scholar
  89. Wistow GJ, Lietman T, Williams LA, Stapel SO, de Jong WW, Horwitz J, Piatigorsky J (1998) τ-crystallin/α-enolase: one gene encodes both an enzyme and a lens structural protein. J Cell Biol 107:2729–2736CrossRefGoogle Scholar
  90. Xu W, Seiter K, Feldman E, Ahmed T, Chiao JW (1996) The differentiation and maturation mediator for human myeloid leukemia cells shares homology with neuroleukin or phosphoglucose isomerase. Blood 87:4502–4506PubMedGoogle Scholar
  91. Xu Z, Horwich AL, Sigler PB (1997) The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 388:741–750PubMedCrossRefGoogle Scholar
  92. Yoshida N, Oeda K, Watanabe E, Mikami T, Fukita Y, Nishimura K, Komai K, Matsuda K (2001) Protein function. Chaperonin turned insect toxin. Nature 411:44PubMedCrossRefGoogle Scholar
  93. Zahn R, Spitzfaden C, Ottiger M, Wüthrich K, Plückthun A (1994) Destabilization of the complete protein secondary structure on binding to the chaperone GroEL. Nature 368:261–265PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Shekhar C. Mande
    • 1
  • C. M. Santosh Kumar
    • 1
  • Aditi Sharma
    • 1
  1. 1.National Centre for Cell Science (NCCS), NCCS ComplexUniversity of Pune Campus, GaneshkhindPuneIndia

Personalised recommendations