Bile salts act as effective protein-unfolding agents and instigators of disulfide stress in vivo

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 16, 2014, Pages

  Cremers, Claudia M ^a   Knoefler, Daniela ^a   Vitvitsky, Victor ^b   Banerjee, Ruma ^b   Jakob, Ursula ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Oxidation; Protein folding

Indexed keywords

CHOLIC ACID; DEOXYCHOLIC ACID; DISULFIDE; GLUTATHIONE; THIOL;

ARTICLE; BACTERIAL GROWTH; CELL SURVIVAL; CHEMICAL MODIFICATION; CHEMICAL STRESS; CONFORMATIONAL TRANSITION; CRITICAL MICELLE CONCENTRATION; CYTOSOL; DISULFIDE BOND; ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; LARGE RIBOSOMAL SUBUNIT; NONHUMAN; OXIDATION; OXIDATION REDUCTION POTENTIAL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CARBONYLATION; PROTEIN STABILITY; PROTEIN UNFOLDING; STEADY STATE;

OXIDATION; PROTEIN FOLDING;

BILE ACIDS AND SALTS; CHOLATES; CYTOSOL; DEOXYCHOLIC ACID; DISULFIDES; HUMANS; OXIDATION-REDUCTION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN UNFOLDING; STRESS, PHYSIOLOGICAL;

EID: 84899128105     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1401941111     Document Type: Article

References (37)

1. Ridlon JM, Kang DJ, Hylemon PB (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47(2):241-259. (Pubitemid 43276911)
2. Wells JE, Hylemon PB (2000) Identification and characterization of a bile acid 7alpha-dehydroxylation operon in Clostridium sp. strain TO-931, a highly active 7alpha-dehydroxylating strain isolated from human feces. Appl Environ Microbiol 66(3):1107-1113. (Pubitemid 30130033)
3. Begley M, Gahan CGM, Hill C (2005) The interaction between bacteria and bile. FEMS Microbiol Rev 29(4):625-651. (Pubitemid 41139175)
4. Ding JW, Andersson R, Soltesz V, Willén R, Bengmark S (1993) The role of bile and bile acids in bacterial translocation in obstructive jaundice in rats. Eur Surg Res 25(1):11-19. (Pubitemid 23089134)
5. Ogata Y, et al. (2003) Role of bile in intestinal barrier function and its inhibitory effect on bacterial translocation in obstructive jaundice in rats. J Surg Res 115(1):18-23. (Pubitemid 37323943)
6. Lorenzo-Zúñiga V, et al. (2003) Oral bile acids reduce bacterial overgrowth, bacterial translocation, and endotoxemia in cirrhotic rats. Hepatology 37(3):551-557. (Pubitemid 36258776)
7. Albalak A, Zeidel ML, Zucker SD, Jackson AA, Donovan JM (1996) Effects of submicellar bile salt concentrations on biological membrane permeability to low molecular weight non-ionic solutes. Biochemistry 35(24):7936-7945. (Pubitemid 26202534)
8. Prouty AM, Van Velkinburgh JC, Gunn JS (2002) Salmonella enterica serovar typhimurium resistance to bile: Identification and characterization of the tolQRA cluster. J Bacteriol 184(5):1270-1276. (Pubitemid 34157548)
9. Merritt ME, Donaldson JR (2009) Effect of bile salts on the DNA and membrane integrity of enteric bacteria. J Med Microbiol 58(Pt 12):1533-1541.
10. Ray MC, Germon P, Vianney A, Portalier R, Lazzaroni JC (2000) Identification by genetic suppression of Escherichia coli TolB residues important for TolB-Pal interaction. J Bacteriol 182(3):821-824. (Pubitemid 30054017)
11. Cabral DJ, Small DM, Lilly HS, Hamilton JA (1987) Transbilayer movement of bile acids in model membranes. Biochemistry 26(7):1801-1804.
12. Bernstein H, et al. (1999) Activation of the promoters of genes associated with DNA damage, oxidative stress, ER stress and protein malfolding by the bile salt, deoxycholate. Toxicol Lett 108(1):37-46. (Pubitemid 29333108)
13. Provenzano D, Schuhmacher DA, Barker JL, Klose KE (2000) The virulence regulatory protein ToxR mediates enhanced bile resistance in Vibrio cholerae and other pathogenic Vibrio species. Infect Immun 68(3):1491-1497. (Pubitemid 30108549)
14. Wholey W-Y, Jakob U (2012) Hsp33 confers bleach resistance by protecting elongation factor Tu against oxidative degradation in Vibrio cholerae. Mol Microbiol 83(5):981-991.
15. Winter J, Linke K, Jatzek A, Jakob U (2005) Severe oxidative stress causes inactivation of DnaK and activation of the redox-regulated chaperone Hsp33. Mol Cell 17(3):381-392. (Pubitemid 40193309)
16. Winter J, Ilbert M, Graf PCF, Özcelik D, Jakob U (2008) Bleach activates a redox-regulated chaperone by oxidative protein unfolding. Cell 135(4):691-701.
17. Cremers CM, Reichmann D, Hausmann J, Ilbert M, Jakob U (2010) Unfolding of metastable linker region is at the core of Hsp33 activation as a redox-regulated chaperone. J Biol Chem 285(15):11243-11251.
18. Tomoyasu T, Mogk A, Langen H, Goloubinoff P, Bukau B (2001) Genetic dissection of the roles of chaperones and proteases in protein folding and degradation in the Escherichia coli cytosol. Mol Microbiol 40(2):397-413. (Pubitemid 32391634)
19. Ilbert M, et al. (2007) The redox-switch domain of Hsp33 functions as dual stress sensor. Nat Struct Mol Biol 14(6):556-563. (Pubitemid 46871808)
20. Gerdes SY, et al. (2003) Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. J Bacteriol 185(19):5673-5684. (Pubitemid 37176479)
21. Pauli-Magnus C, Stieger B, Meier Y, Kullak-Ublick GA, Meier PJ (2005) Enterohepatic transport of bile salts and genetics of cholestasis. J Hepatol 43(2):342-357. (Pubitemid 40956889)
22. Kosower NS, Kosower EM (1995) Diamide: An oxidant probe for thiols. Methods Enzymol 251:123-133.
23. Pullar JM, Vissers MC, Winterbourn CC (2001) Glutathione oxidation by hypochlorous acid in endothelial cells produces glutathione sulfonamide as a major product but not glutathione disulfide. J Biol Chem 276(25):22120-22125.
24. Carr AC, Winterbourn CC (1997) Oxidation of neutrophil glutathione and protein thiols by myeloperoxidase-derived hypochlorous acid. Biochem J 327(Pt 1):275-281. (Pubitemid 27455490)
25. Seaver LC, Imlay JA (2001) Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183(24):7173-7181. (Pubitemid 33121851)
26. Dalle-Donne I, et al. (2009) Protein carbonylation: 2,4- dinitrophenylhydrazine reacts with both aldehydes/ketones and sulfenic acids. Free Radic Biol Med 46(10):1411-1419.
27. Nyström T (2005) Role of oxidative carbonylation in protein quality control and senescence. EMBO J 24(7):1311-1317.
28. Aslund F, Zheng M, Beckwith J, Storz G (1999) Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc Natl Acad Sci USA 96(11):6161-6165. (Pubitemid 29256636)
29. Kanemori M, Mori H, Yura T (1994) Induction of heat shock proteins by abnormal proteins results from stabilization and not increased synthesis of sigma 32 in Escherichia coli. J Bacteriol 176(18):5648-5653. (Pubitemid 24280497)
30. Hansen RE, Roth D, Winther JR (2009) Quantifying the global cellular thiol-disulfide status. Proc Natl Acad Sci USA 106(2):422-427.
31. Gray MJ, Wholey WY, Jakob U (2013) Bacterial responses to reactive chlorine species. Annu Rev Microbiol 67:141-160.
32. Gass J, Vora H, Hofmann AF, Gray GM, Khosla C (2007) Enhancement of dietary protein digestion by conjugated bile acids. Gastroenterology 133(1):16-23. (Pubitemid 47031127)
33. Robic S, Linscott KB, Aseem M, Humphreys EA, McCartha SR (2011) Bile acids as modulators of enzyme activity and stability. Protein J 30(8):539-545.
34. Jakob U, Muse W, Eser M, Bardwell JC (1999) Chaperone activity with a redox switch. Cell 96(3):341-352. (Pubitemid 29077588)
35. Prinz WA, Aslund F, Holmgren A, Beckwith J (1997) The role of the thioredoxin and glutaredoxin pathways in reducing protein disulfide bonds in the Escherichia coli cytoplasm. J Biol Chem 272(25):15661-15667. (Pubitemid 27265536)
36. Carmel-Harel O, Storz G (2000) Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 54:439-461.
37. Garg SK, Yan ZH, Vitvitsky V, Banerjee R (2010) Analysis of sulfur-containing metabolites involved in redox and methionine metabolism. Methods in Redox Signaling, ed Das D (Mary Ann Liebert, New York), pp 7-11.