Thiol-based redox switches.

Bastian Groitl, Ursula Jakob
Author Information
  1. Bastian Groitl: Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA.
  2. Ursula Jakob: Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA; Department of Biological Chemistry, University of Michigan, Ann Arbor, MI 48109, USA. Electronic address: ujakob@umich.edu.

Abstract

Regulation of protein function through thiol-based redox switches plays an important role in the response and adaptation to local and global changes in the cellular levels of reactive oxygen species (ROS). Redox regulation is used by first responder proteins, such as ROS-specific transcriptional regulators, chaperones or metabolic enzymes to protect cells against mounting levels of oxidants, repair the damage and restore redox homeostasis. Redox regulation of phosphatases and kinases is used to control the activity of select eukaryotic signaling pathways, making reactive oxygen species important second messengers that regulate growth, development and differentiation. In this review we will compare different types of reversible protein thiol modifications, elaborate on their structural and functional consequences and discuss their role in oxidative stress response and ROS adaptation. This article is part of a Special Issue entitled: Thiol-Based Redox Processes.

Keywords

References

  1. Trends Genet. 2001 Aug;17(8):465-72 [PMID: 11485819]
  2. Kidney Int Suppl. 2007 Aug;(106):S3-8 [PMID: 17653208]
  3. Cell. 2004 May 28;117(5):625-35 [PMID: 15163410]
  4. Antioxid Redox Signal. 2009 May;11(5):997-1014 [PMID: 18999917]
  5. J Biol Chem. 2004 May 7;279(19):19486-93 [PMID: 14757771]
  6. Structure. 1995 Mar 15;3(3):245-50 [PMID: 7788290]
  7. J Biol Chem. 2005 Jul 1;280(26):24857-63 [PMID: 15866871]
  8. Antioxid Redox Signal. 2013 May 20;18(15):1987-2015 [PMID: 23198756]
  9. FASEB J. 1995 Oct;9(13):1267-76 [PMID: 7557016]
  10. Antioxid Redox Signal. 2013 Jan 1;18(1):94-127 [PMID: 22746677]
  11. Cell Signal. 2012 May;24(5):981-90 [PMID: 22286106]
  12. Biochim Biophys Acta. 2014 Feb;1840(2):906-12 [PMID: 23939310]
  13. Free Radic Biol Med. 2005 Jun 15;38(12):1543-52 [PMID: 15917183]
  14. Science. 2003 Apr 25;300(5619):650-3 [PMID: 12714747]
  15. Antioxid Redox Signal. 2011 Mar 15;14(6):1049-63 [PMID: 20626317]
  16. Chem Res Toxicol. 2010 Nov 15;23(11):1633-46 [PMID: 20845928]
  17. Nat Struct Mol Biol. 2007 Jun;14(6):556-63 [PMID: 17515905]
  18. Biochem Biophys Res Commun. 2013 Mar 8;432(2):291-5 [PMID: 23396059]
  19. Nucleic Acids Res. 1994 Apr 11;22(7):1125-7 [PMID: 8165123]
  20. J Am Soc Mass Spectrom. 2007 Aug;18(8):1544-51 [PMID: 17604642]
  21. Blood. 2003 Jun 15;101(12):5033-8 [PMID: 12586629]
  22. Trends Biochem Sci. 1995 Sep;20(9):351-6 [PMID: 7482702]
  23. Biol Chem. 2002 Mar-Apr;383(3-4):347-64 [PMID: 12033427]
  24. Cell Mol Life Sci. 2013 Apr;70(7):1185-206 [PMID: 22926412]
  25. Biopolymers. 2014 Feb;101(2):165-72 [PMID: 23576224]
  26. Annu Rev Microbiol. 2002;56:263-87 [PMID: 12142479]
  27. Mol Cell. 2012 Jun 8;46(5):584-94 [PMID: 22681886]
  28. Nucleic Acids Res. 2009 Mar;37(4):1174-81 [PMID: 19129220]
  29. Proc Natl Acad Sci U S A. 2010 Jan 19;107(3):1071-6 [PMID: 20080625]
  30. Structure. 2000 Jun 15;8(6):605-15 [PMID: 10873855]
  31. J Biol Chem. 1998 Jan 30;273(5):3027-32 [PMID: 9446617]
  32. J Biol Chem. 2000 Jun 23;275(25):18759-66 [PMID: 10764757]
  33. Free Radic Biol Med. 2013 May;58:109-17 [PMID: 23376233]
  34. Antioxid Redox Signal. 2011 Mar 1;14(5):757-66 [PMID: 21067413]
  35. Am J Physiol Heart Circ Physiol. 2007 Mar;292(3):H1227-36 [PMID: 17172268]
  36. Cell. 2012 Mar 2;148(5):947-57 [PMID: 22385960]
  37. Annu Rev Microbiol. 2013;67:141-60 [PMID: 23768204]
  38. J Bacteriol. 1999 Mar;181(5):1375-9 [PMID: 10049365]
  39. Methods Enzymol. 2010;473:95-115 [PMID: 20513473]
  40. J Biol Chem. 2007 Apr 20;282(16):11885-92 [PMID: 17329258]
  41. Antioxid Redox Signal. 2012 Oct 15;17(8):1124-60 [PMID: 22531002]
  42. Int J Biochem Cell Biol. 2007;39(1):44-84 [PMID: 16978905]
  43. J Mol Biol. 2010 Sep 10;402(1):194-209 [PMID: 20643143]
  44. Mol Cell. 2005 Feb 4;17(3):381-92 [PMID: 15694339]
  45. J Biol Chem. 2011 Dec 2;286(48):41893-41903 [PMID: 21976664]
  46. Annu Rev Biochem. 1990;59:543-68 [PMID: 2197983]
  47. Subcell Biochem. 2007;44:27-40 [PMID: 18084888]
  48. Mol Cell. 2012 Sep 14;47(5):767-76 [PMID: 22819323]
  49. J Am Chem Soc. 2012 Feb 8;134(5):2500-3 [PMID: 22280304]
  50. Yao Xue Xue Bao. 2012 Mar;47(3):280-90 [PMID: 22645750]
  51. J Biol Chem. 2013 Nov 8;288(45):32241-32247 [PMID: 24062305]
  52. EMBO J. 2004 Jan 14;23(1):160-8 [PMID: 14685279]
  53. Biomol NMR Assign. 2014 Oct;8(2):279-81 [PMID: 23765287]
  54. Cell. 2008 Nov 14;135(4):691-701 [PMID: 19013278]
  55. Cell. 1999 Feb 5;96(3):341-52 [PMID: 10025400]
  56. J Biochem. 2011 Oct;150(4):345-56 [PMID: 21856739]
  57. Free Radic Biol Med. 2014 Jan;66:75-87 [PMID: 23899494]
  58. Brain Pathol. 2002 Jan;12(1):21-35 [PMID: 11770899]
  59. Antioxid Redox Signal. 2011 Aug 1;15(3):795-815 [PMID: 20969484]
  60. J Am Chem Soc. 2013 Dec 11;135(49):18673-81 [PMID: 24236406]
  61. J Biol Chem. 2004 May 7;279(19):20529-38 [PMID: 15023991]
  62. Curr Opin Chem Biol. 2011 Feb;15(1):103-12 [PMID: 21216657]
  63. Nat Struct Mol Biol. 2011 May;18(5):630-3 [PMID: 21460844]
  64. J Biol Chem. 2011 May 20;286(20):18048-55 [PMID: 21385867]
  65. FASEB J. 1993 Dec;7(15):1483-90 [PMID: 8262333]
  66. Structure. 2012 Mar 7;20(3):429-39 [PMID: 22405002]
  67. J Cell Biol. 2011 Mar 7;192(5):825-38 [PMID: 21357747]
  68. Mol Cell. 2012 Feb 10;45(3):398-408 [PMID: 22245228]
  69. Proc Natl Acad Sci U S A. 2002 May 14;99(10):7078-83 [PMID: 11983865]
  70. Nature. 2003 Oct 30;425(6961):980-4 [PMID: 14586471]
  71. Free Radic Biol Med. 2012 Oct 1;53(7):1522-30 [PMID: 22902630]
  72. Science. 1998 Mar 13;279(5357):1718-21 [PMID: 9497290]
  73. Methods Enzymol. 2013;527:41-63 [PMID: 23830625]
  74. Structure. 2001 May 9;9(5):377-87 [PMID: 11377198]
  75. EMBO J. 2000 Sep 15;19(18):5019-26 [PMID: 10990465]
  76. Nature. 2003 Jun 12;423(6941):769-73 [PMID: 12802338]
  77. Trends Biochem Sci. 2012 Dec;37(12):517-25 [PMID: 23018052]
  78. Biochemistry. 2010 Feb 16;49(6):1059-66 [PMID: 20070126]
  79. J Biol Chem. 1997 Jun 20;272(25):15661-7 [PMID: 9188456]
  80. Free Radic Biol Med. 1999 Aug;27(3-4):322-8 [PMID: 10468205]
  81. Subcell Biochem. 2007;44:61-81 [PMID: 18084890]
  82. Biochemistry. 2007 Jan 23;46(3):709-19 [PMID: 17223692]
  83. Antioxid Redox Signal. 2011 Mar 15;14(6):1023-37 [PMID: 20649472]
  84. Dev Comp Immunol. 2010 Apr;34(4):369-76 [PMID: 19958789]
  85. Methods Mol Biol. 2008;476:101-16 [PMID: 19157012]
  86. J Proteome Res. 2004 Nov-Dec;3(6):1228-33 [PMID: 15595732]
  87. Curr Opin Pharmacol. 2007 Aug;7(4):381-91 [PMID: 17662654]
  88. Redox Biol. 2014 Feb 03;2:395-9 [PMID: 24563858]
  89. Proc Natl Acad Sci U S A. 2013 Oct 1;110(40):E3780-9 [PMID: 24043785]
  90. Angew Chem Int Ed Engl. 2011 Feb 7;50(6):1342-5 [PMID: 21290508]
  91. Free Radic Biol Med. 2010 Dec 1;49(11):1603-16 [PMID: 20840865]
  92. Free Radic Res. 2012 Aug;46(8):975-95 [PMID: 22348603]
  93. Antioxid Redox Signal. 2011 Mar 15;14(6):1065-77 [PMID: 20799881]
  94. Structure. 2001 May 9;9(5):367-75 [PMID: 11377197]
  95. Methods Enzymol. 1995;252:283-92 [PMID: 7476363]
  96. Structure. 2004 Oct;12(10):1901-7 [PMID: 15458638]
  97. Antioxid Redox Signal. 2005 May-Jun;7(5-6):560-77 [PMID: 15890001]
  98. Nature. 2003 Jun 12;423(6941):773-7 [PMID: 12802339]
  99. Nature. 2003 Jul 31;424(6948):561-5 [PMID: 12891360]
  100. J Mol Biol. 2004 Oct 15;343(2):445-55 [PMID: 15451672]
  101. Methods Enzymol. 2013;528:3-25 [PMID: 23849856]
  102. PLoS Comput Biol. 2009 Aug;5(8):e1000461 [PMID: 19675666]
  103. Proc Natl Acad Sci U S A. 2007 May 22;104(21):8743-8 [PMID: 17502599]
  104. Annu Rev Genet. 2000;34:61-76 [PMID: 11092822]
  105. Experientia. 1994 Nov 30;50(11-12):1031-8 [PMID: 7988662]
  106. Methods Mol Biol. 2009;519:397-415 [PMID: 19381598]
  107. J Biol Chem. 2008 Jun 20;283(25):16961-5 [PMID: 18420576]
  108. Proc Natl Acad Sci U S A. 2004 Feb 17;101(7):1834-9 [PMID: 14766979]
  109. Proc Natl Acad Sci U S A. 2009 Apr 7;106(14):5557-62 [PMID: 19321422]
  110. Biol Chem. 2006 Oct-Nov;387(10-11):1351-5 [PMID: 17081106]
  111. Chem Res Toxicol. 2011 Apr 18;24(4):434-50 [PMID: 21391663]
  112. Proc Natl Acad Sci U S A. 2013 Apr 2;110(14):E1254-62 [PMID: 23487787]
  113. Free Radic Biol Med. 2008 Sep 1;45(5):549-61 [PMID: 18544350]
  114. J Exp Bot. 2008;59(7):1597-604 [PMID: 18048372]
  115. Cell. 1998 Jan 9;92(1):1-4 [PMID: 9489693]
  116. Proc Natl Acad Sci U S A. 1999 May 25;96(11):6161-5 [PMID: 10339558]
  117. Biochemistry. 2013 Aug 27;52(34):5920-7 [PMID: 23906287]
  118. J Biol Chem. 2013 Sep 13;288(37):26480-8 [PMID: 23861405]
  119. Annu Rev Biochem. 2008;77:755-76 [PMID: 18173371]
  120. Ann N Y Acad Sci. 2001 Apr;928:22-38 [PMID: 11795513]
  121. Mol Cells. 2011 Dec;32(6):491-509 [PMID: 22207195]
  122. Annu Rev Pharmacol Toxicol. 2004;44:325-47 [PMID: 14744249]
  123. Proc Natl Acad Sci U S A. 2008 Jun 17;105(24):8197-202 [PMID: 18287020]
  124. J Biol Chem. 2010 Apr 9;285(15):11243-51 [PMID: 20139072]
  125. Biochim Biophys Acta. 2013 Jan;1834(1):464-9 [PMID: 22819876]
  126. J Bacteriol. 2012 Oct;194(20):5495-503 [PMID: 22797754]
  127. Cell. 2002 Nov 15;111(4):471-81 [PMID: 12437921]
  128. J Biol Chem. 2000 Dec 8;275(49):38302-10 [PMID: 10976105]
  129. FASEB J. 2003 Jul;17(10):1195-214 [PMID: 12832285]

Grants

  1. R01 GM065318/NIGMS NIH HHS
  2. R01 GM102829/NIGMS NIH HHS
  3. R21 AI097893/NIAID NIH HHS
  4. GM065318/NIGMS NIH HHS

MeSH Term

Animals
Humans
Oxidation-Reduction
Oxidative Stress
Reactive Oxygen Species
Signal Transduction
Sulfhydryl Compounds

Chemicals

Reactive Oxygen Species
Sulfhydryl Compounds

Word Cloud

Created with Highcharts 10.0.0RedoxredoxregulationproteinswitchesimportantroleresponseadaptationlevelsreactiveoxygenspeciesROSusedstressRegulationfunctionthiol-basedplayslocalglobalchangescellularfirstresponderproteinsROS-specifictranscriptionalregulatorschaperonesmetabolicenzymesprotectcellsmountingoxidantsrepairdamagerestorehomeostasisphosphataseskinasescontrolactivityselecteukaryoticsignalingpathwaysmakingsecondmessengersregulategrowthdevelopmentdifferentiationreviewwillcomparedifferenttypesreversiblethiolmodificationselaboratestructuralfunctionalconsequencesdiscussoxidativearticlepartSpecialIssueentitled:Thiol-BasedProcessesThiol-basedDisulfidebondOxidativeSulfenicacid

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