In vivo substrate diversity and preference of small heat shock protein IbpB as revealed by using a genetically incorporated photo-cross-linker

Journal of Biological Chemistry

Volumn 288, Issue 44, 2013, Pages 31646-31654

  Fu, Xinmiao ^a   Shi, Xiaodong ^a,b   Yan, Linxuan ^a   Zhang, Hanlin ^a   Chang, Zengyi ^a  

^a PEKING UNIVERSITY   (China)

^b XUZHOU MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE FUNCTIONS; METABOLIC ENZYMES; MOLECULAR CHAPERONES; NATURAL SUBSTRATES; PROTECTIVE EFFECTS; PROTEIN SYNTHESIS; RIBOSOMAL PROTEINS; SMALL HEAT SHOCK PROTEINS;

AMINO ACIDS; ENZYMES; ESCHERICHIA COLI; GENE ENCODING; METABOLISM; SUBSTRATES;

PROTEINS;

AMINO ACID TRANSFER RNA LIGASE; CELL PROTEIN; CHAPERONE; IBPB PROTEIN; N BENZOYLPHENYLALANINE; RIBOSOME PROTEIN; SMALL HEAT SHOCK PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; HEAT SHOCK; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION;

HEAT SHOCK PROTEIN; METABOLIC ENZYMES; MOLECULAR CHAPERONE; PHOTOCROSS-LINKING; PROTEIN AGGREGATION; PROTEIN FOLDING; RIBOSOMES; SMALL HEAT SHOCK PROTEINS; TRANSLATION; UNNATURAL AMINO ACID;

CROSS-LINKING REAGENTS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; PROTEIN BIOSYNTHESIS;

EID: 84887068645     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.501817     Document Type: Article

References (65)

1. Hartl, F. U., Bracher, A., and Hayer-Hartl, M. (2011) Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332
2. de Jong, W. W., Leunissen, J. A., and Voorter, C. E. (1993) Evolution of the α-crystallin/small heat-shock protein family. Mol. Biol. Evol. 10, 103-126 (Pubitemid 23040227)
3. Lindquist, S., and Craig, E. A. (1988) The heat-shock proteins. Annu. Rev. Genet. 22, 631-677 (Pubitemid 19156675)
4. Haslbeck, M., Franzmann, T., Weinfurtner, D., and Buchner, J. (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat. Struct. Mol. Biol. 12, 842-846 (Pubitemid 41486706)
5. Laskowska, E., Matuszewska, E., and Kuczyńska-Wisnik, D. (2010) Small heat shock proteins and protein-misfolding diseases. Curr. Pharm. Biotechnol. 11, 146-157
6. Clark, J. I., and Muchowski, P. J. (2000) Small heat-shock proteins and their potential role in human disease. Curr. Opin. Struct. Biol. 10, 52-59 (Pubitemid 30099327)
7. Morrow, G., Battistini, S., Zhang, P., and Tanguay, R. M. (2004) Decreased lifespan in the absence of expression of the mitochondrial small heat shock protein Hsp22 in Drosophila. J. Biol. Chem. 279, 43382-43385 (Pubitemid 39390636)
8. Richards, E. H., Hickey, E., Weber, L., and Master, J. R. (1996) Effect of overexpression of the small heat shock protein HSP27 on the heat and drug sensitivities of human testis tumor cells. Cancer Res. 56, 2446-2451 (Pubitemid 26154097)
9. Horwitz, J. (1992) α-Crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. U.S.A. 89, 10449-10453
10. Veinger, L., Diamant, S., Buchner, J., and 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 (Pubitemid 28204946)
11. Mogk, A., Deuerling, E., Vorderwülbecke, S., Vierling, E., and Bukau, B. (2003) Small heat shock proteins, ClpB and the DnaK system form a functional triad in reversing protein aggregation. Mol. Microbiol. 50, 585-595 (Pubitemid 37297136)
12. Lee, G. J., and Roseman., A. M., Saibil, H. R., Vierling, E. (1997) A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBOJ. 16, 659-671 (Pubitemid 27067794)
13. Cashikar, A. G., Duennwald, M., and Lindquist, S. L. (2005) A chaperone pathway in protein disaggregation. Hsp26 alters the nature of protein aggregates to facilitate reactivation by Hsp104. J. Biol. Chem. 280, 23869-23875 (Pubitemid 40884874)
14. Ehrnsperger, M., Gräber, S., Gaestel, M., and Buchner, J. (1997) Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBOJ. 16, 221-229 (Pubitemid 27049380)
15. Matuszewska, M., Kuczyńska-Wisnik, D., Laskowska, E., and 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
16. Jakob, U., Gaestel, M., Engel, K., and Buchner, J. (1993) Small heat shock proteins are molecular chaperones. J. Biol. Chem. 268, 1517-1520 (Pubitemid 23033534)
17. Welker, S., Rudolph, B., Frenzel, E., Hagn, F., Liebisch, G., Schmitz, G., Scheuring, J., Kerth, A., Blume, A., Weinkauf, S., Haslbeck, M., Kessler, H., and Buchner, J. (2010) Hsp12 is an intrinsically unstructured stress protein that folds upon membrane association and modulates membrane function. Mol. Cell 39, 507-520
18. Török, Z., Goloubinoff, P., Horváth, I., Tsvetkova, N. M., Glatz, A., Balogh, G., Varvasovszki, V., Los, D. A, Vierling, E., Crowe, J. H, and 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 (Pubitemid 32220805)
19. Nakamoto, H., and Vígh, L. (2007) The small heat shock proteins and their clients. Cell. Mol. Life Sci. 64, 294-306 (Pubitemid 46440201)
20. Basha, E., O'Neill, H., and Vierling, E. (2012) Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions. Trends Biochem. Sci. 37, 106-117
21. Jaya, N., Garcia, V., and Vierling, E. (2009) Substrate binding site flexibility of the small heat shock protein molecular chaperones. Proc. Natl. Acad. Sci. U.S.A. 106, 15604-15609
22. Arata, S., Hamaguchi, S., and Nose, K. (1995) Effects of the overexpression of the small heat shock protein, HSP27, on the sensitivity of human fibroblast cells exposed to oxidative stress. J. Cell. Physiol. 163, 458-465
23. Balogi, Z., Cheregi, O., Giese, K. C, Juhász, K., Vierling, E., Vass, I., Vígh, L., and 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, 22983-22991
24. Salinthone, S., Ba, M., Hanson, L., Martin, J. L., and Halayko., A. J., and Gerthoffer, W. T. (2007) Overexpression of human Hsp27 inhibits serum-induced proliferation in airway smooth muscle myocytes and confers resistance to hydrogen peroxide cytotoxicity. Am. J. Physiol. Lung Cell Mol Physiol 293, L1194-L1207 (Pubitemid 350159404)
25. Merck, K. B., and Groenen., P. J., Voorter, C. E., de Haard-Hoekman, W. A., Horwitz, J., Bloemendal, H., and de Jong, W. W. (1993) Structural and functional similarities of bovine α-crystallin and mouse small heat-shock protein. A family of chaperones. J. Biol. Chem. 268, 1046-1052 (Pubitemid 23019740)
26. 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 (Pubitemid 34213969)
27. Chang, Z., and Primm., T. P., Jakana, J., Lee, I. H., Serysheva, I., Chiu, W., Gilbert, H. F., and Quiocho, F. A. (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 (Pubitemid 26104163)
28. Gu, L., Abulimiti, A., Li, W., and 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 (Pubitemid 34729476)
29. Fu, X., Zhang, H., Zhang, X., Cao, Y., Jiao, W., Liu, C, Song, Y., Abulimiti, A., and Chang, Z. (2005) A dual role for the N-terminal region of Mycobacterium tuberculosis Hsp16.3 in self-oligomerization and binding denaturing substrate proteins. J. Biol. Chem. 280, 6337-6348 (Pubitemid 40341180)
30. Jiao, W., Qian, M., Li, P., Zhao, L., and Chang, Z. (2005) The essential role of the flexible terminiinthe 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 (Pubitemid 40357925)
31. Jiao, W., Hong, W., Li, P., Sun, S., Ma, J., Qian, M., Hu, M., and 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 (Pubitemid 351300325)
32. Basha, E., and Lee., G. J., Breci, L. A., Hausrath, A. C., and Buan., N. R., Giese, K. C., and Vierling, E. (2004) The identity ofproteins associated with asmall heat shock protein during heat stress in vivo indicates that these chaperones protect a wide range of cellular functions. J. Biol. Chem. 279, 7566-7575 (Pubitemid 38294635)
33. Bepperling, A., Alte, F., Kriehuber, T., Braun, N., Weinkauf, S., Groll, M., Haslbeck, M., and Buchner, J. (2012) Alternative bacterial two-component small heat shock protein systems. Proc. Natl. Acad. Sci. U.S.A. 109, 20407-20412
34. Fu, X., Shi, X., Yin, L., Liu, J., Joo, K., Lee, J., and Chang, Z. (2013) Small heat shock protein IbpB acts as a robust chaperone in living cells by hierarchically activating its multitype substrate-binding residues. J. Biol. Chem. 288, 11897-11906
35. Chin, J. W., and Martin., A. B., King, D. S., Wang, L., and Schultz, P. G. (2002) Addition of a photocross-linking amino acid to the genetic code of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 99, 11020-11024 (Pubitemid 34920872)
36. Farrell, I. S., Toroney, R., Hazen, J. L., and Mehl., R. A., and Chin, J. W. (2005) Photo-cross-linking interacting proteins with a genetically encoded benzophenone. Nat. Methods 2, 377-384 (Pubitemid 41130984)
37. Mohibullah, N., and Hahn, S. (2008) Site-specific cross-linking of TBP in vivo and in vitro reveals a direct functional interaction with the SAGA subunit Spt3. Genes Dev. 22, 2994-3006
38. Leng, F. (2012) Opportunity and challenge: 10 years of proteomics in China. Sci. China Life Sci. 55, 837-839
39. Hu, Y. (2012) Progress in protein structure and function studies in China during 2010-2011. Sci. China Life Sci. 55, 927-930
40. Zhang, M., Lin, S., Song, X., Liu, J., Fu, Y., Ge, X., Fu, X., Chang, Z., and Chen, P. R. (2011) A genetically incorporated cross-linker reveals chaperone cooperation in acid resistance. Nat. Chem. Biol. 7, 671-677
41. Perkins, D. N., and Pappin., D. J., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567 (Pubitemid 30007252)
42. Tatusov, R. L., and Koonin., E. V., and Lipman, D. J. (1997) A genomic perspective on protein families. Science 278, 631-637 (Pubitemid 27464953)
43. Kitagawa, M., Matsumura, Y., and Tsuchido, T. (2000) Small heat shock proteins, IbpA and IbpB, are involved in resistances to heat and superoxide stresses in Escherichia coli. FEMS Microbiol. Lett. 184, 165-171 (Pubitemid 30125335)
44. Kuczyńska-Wisńik, D., Kedzierska, S., Matuszewska, E., Lund, P., Taylor, A., Lipińska, B., and Laskowska, E. (2002) The Escherichia coli small heatshock proteins IbpA and IbpB prevent the aggregation of endogenous proteins denatured in vivo during extreme heat shock. Microbiology 148, 1757-1765 (Pubitemid 34679029)
45. Butland, G., Peregrín-Alvarez, J. M., Li, J., Yang, W., Yang, X., Canadien, V., Starostine, A., Richards, D., Beattie, B., Krogan, N., Davey, M., Parkinson, J., Greenblatt, J., and Emili, A. (2005) Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433, 531-537 (Pubitemid 40204311)
46. Rinas, U., Hoffmann, F., Betiku, E., Estapé, D., and Marten, S. (2007) Inclusion body anatomy and functioning of chaperone-mediated in vivo inclusion body disassembly during high-level recombinant protein production in Escherichia coli. J. Biotechnol. 127, 244-257 (Pubitemid 46107138)
47. Ratajczak, E., Zietkiewicz, S., and Liberek, K. (2009) Distinct activities of Escherichia coli small heat shock proteins IbpA and IbpB promote efficient protein disaggregation. J. Mol. Biol. 386, 178-189
48. Matuszewska, E., Kwiatkowska, J., Ratajczak, E., Kuczyńska- Wisńik, D., and Laskowska, E. (2009) Role of Escherichia coli heat shock proteins IbpA and IbpB in protection of alcohol dehydrogenase AdhE against heat inactivation in the presence of oxygen. Acta Biochim. Pol. 56, 55-61
49. Matuszewska, E., Kwiatkowska, J., Kuczynska-Wisnik, D., and Laskowska, E. (2008) Escherichia coli heat-shock proteins IbpA/B are involved in resistance to oxidative stress induced by copper. Microbiology 154, 1739-1747
50. Møller, I. M., Rogowska-Wrzesinska, A., and Rao, R. S. (2011) Protein carbonylation and metal-catalyzed protein oxidation in a cellular perspective. J. Proteomics 74, 2228-2242
51. Carver, J. A., and Lindner., R. A., Lyon, C, Canet, D., Hernandez, H., Dobson, C. M., and Redfield, C. (2002) The interaction of the molecular chaperone α-crystallin with unfolding α-lactalbumin: a structural and kinetic spectroscopic study. J. Mol. Biol. 318, 815-827 (Pubitemid 34729371)
52. Carver, J. A., Guerreiro, N., Nicholls, K. A., and Truscott, R. J. (1995) On the interaction of α-crystallin with unfolded proteins. Biochim. Biophys. Acta 1252, 251-260
53. Treweek, T. M., and Lindner., R. A., Mariani, M., and Carver, J. A. (2000) The small heat-shock chaperone protein, α-crystallin, does not recognize stable molten globule states of cytosolic proteins. Biochim. Biophys. Acta 1481, 175-188 (Pubitemid 30658094)
54. Farahbakhsh, Z. T., and Huang., Q. L., Ding, L. L., Altenbach, C, and Steinhoff., H. J., Horwitz, J., and Hubbell, W. L. (1995) Interaction of α-crystallin with spin-labeled peptides. Biochemistry 34, 509-516
55. Lindner, R. A., Kapur, A., and Carver, J. A. (1997) The interaction of the molecular chaperone, α-crystallin, with molten globule states of bovine α-lactalbumin. J. Biol. Chem. 272, 27722-27729 (Pubitemid 27473569)
56. Das, K. P., and Petrash., J. M., and Surewicz, W. K. (1996) Conformational properties of substrate proteins bound to a molecular chaperone α-crystallin. J. Biol. Chem. 271, 10449-10452 (Pubitemid 26145777)
57. Waters, E. R., and Nguyen., S. L., Eskandar, R., Behan, J., and Sanders-Reed, Z. (2008) The recent evolution of a pseudogene: diversity and divergence of a mitochondria-localized small heat shock protein in Arabidopsis thaliana. Genome 51, 177-186 (Pubitemid 351573623)
58. Waters, E. R., and Vierling, E. (1999) Chloroplast small heat shock proteins: evidence for atypical evolution of an organelle-localized protein. Proc. Natl. Acad. Sci. U.S.A. 96, 14394-14399 (Pubitemid 30000661)
59. Morrow, G., and Tanguay, R. M. (2012) Small heat shock protein expression and functions during development. Int. J. Biochem. Cell Biol. 44, 1613-1621
60. Yeh, C. H, Chang, P. F., and Yeh., K. W., Lin, W. C, Chen, Y. M., and Lin, C. Y. (1997) Expression of a gene encoding a 16.9-kDa heat-shock protein, Oshsp16.9, in Escherichia coli enhances thermotolerance. Proc. Natl. Acad. Sci. U.S.A. 94, 10967-10972
61. Muchowski, P. J., and Clark, J. I. (1998) ATP-enhanced molecular chaperone functions of the small heat shock protein human α-crystallin. Proc. Natl. Acad. Sci. U.S.A. 95, 1004-1009 (Pubitemid 28124902)
62. Soto, A., Allona, I., Collada, C, and Guevara., M. A., Casado, R., Rodriguez-Cerezo, E., Aragoncillo, C, and Gomez, L. (1999) Heterologous expression of a plant small heat-shock protein enhances Escherichia coli viability under heat and cold stress. Plant Physiol. 120, 521-528 (Pubitemid 29388196)
63. Mogk, A., Schlieker, C, and Friedrich., K. L., Schönfeld, H. J., Vierling, E., and Bukau, B. (2003) Refolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most efficiently by ClpB/DnaK. J. Biol. Chem. 278, 31033-31042 (Pubitemid 36994617)
64. Kerner, M. J., and Naylor., D. J., Ishihama, Y., Maier, T., Chang, H. C, Stines, A. P., Georgopoulos, C, Frishman, D., Hayer-Hartl, M., Mann, M., and Hartl, F. U. (2005) Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122, 209-220 (Pubitemid 41032985)
65. Lycklama A Nijeholt, J. A., and Driessen, A. J. (2012) The bacterial Sectranslocase: structure and mechanism. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 1016-1028