دورية أكاديمية
Transmembrane helix hydrophobicity is an energetic barrier during the retrotranslocation of integral membrane ERAD substrates.
| العنوان: | Transmembrane helix hydrophobicity is an energetic barrier during the retrotranslocation of integral membrane ERAD substrates. |
|---|---|
| المؤلفون: | Guerriero CJ; Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260., Reutter KR; Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260., Augustine AA; Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260., Preston GM; Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260., Weiberth KF; Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260., Mackie TD; Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260., Cleveland-Rubeor HC; Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260., Bethel NP; Cardiovascular Research Institute, Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, CA 94158., Callenberg KM; Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260., Nakatsukasa K; Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260.; Division of Biological Science, Graduate School of Natural Sciences, Nagoya City University, Nagoya, Aichi 467-8501, Japan., Grabe M; Cardiovascular Research Institute, Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, CA 94158., Brodsky JL; Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260 jbrodsky@pitt.edu. |
| المصدر: | Molecular biology of the cell [Mol Biol Cell] 2017 Jul 15; Vol. 28 (15), pp. 2076-2090. Date of Electronic Publication: 2017 May 24. |
| نوع المنشور: | Journal Article |
| اللغة: | English |
| بيانات الدورية: | Publisher: American Society for Cell Biology Country of Publication: United States NLM ID: 9201390 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1939-4586 (Electronic) Linking ISSN: 10591524 NLM ISO Abbreviation: Mol Biol Cell Subsets: MEDLINE |
| أسماء مطبوعة: | Original Publication: Bethesda, MD : American Society for Cell Biology, c1992- |
| مواضيع طبية MeSH: | Endoplasmic Reticulum-Associated Degradation/*physiology , Membrane Proteins/*metabolism, Adenosine Triphosphatases/metabolism ; Cell Cycle Proteins/metabolism ; Endoplasmic Reticulum/metabolism ; Hydrophobic and Hydrophilic Interactions ; Membranes/metabolism ; Mutation ; Proteasome Endopeptidase Complex/metabolism ; Protein Folding ; Protein Translocation Systems/metabolism ; Protein Transport ; Saccharomyces cerevisiae/metabolism ; Saccharomyces cerevisiae Proteins/metabolism ; Ubiquitin/metabolism ; Ubiquitin-Protein Ligases/metabolism ; Ubiquitination |
| مستخلص: | Integral membrane proteins fold inefficiently and are susceptible to turnover via the endoplasmic reticulum-associated degradation (ERAD) pathway. During ERAD, misfolded proteins are recognized by molecular chaperones, polyubiquitinated, and retrotranslocated to the cytoplasm for proteasomal degradation. Although many aspects of this pathway are defined, how transmembrane helices (TMHs) are removed from the membrane and into the cytoplasm before degradation is poorly understood. In this study, we asked whether the hydrophobic character of a TMH acts as an energetic barrier to retrotranslocation. To this end, we designed a dual-pass model ERAD substrate, Chimera A*, which contains the cytoplasmic misfolded domain from a characterized ERAD substrate, Sterile 6* (Ste6p*). We found that the degradation requirements for Chimera A* and Ste6p* are similar, but Chimera A* was retrotranslocated more efficiently than Ste6p* in an in vitro assay in which retrotranslocation can be quantified. We then constructed a series of Chimera A* variants containing synthetic TMHs with a range of Δ G values for membrane insertion. TMH hydrophobicity correlated inversely with retrotranslocation efficiency, and in all cases, retrotranslocation remained Cdc48p dependent. These findings provide insight into the energetic restrictions on the retrotranslocation reaction, as well as a new computational approach to predict retrotranslocation efficiency. (© 2017 Guerriero et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0).) |
| References: | EMBO J. 1991 Dec;10(12):3777-85. (PMID: 1935899) Curr Biol. 2002 May 14;12(10):R366-71. (PMID: 12015140) Cell. 2003 Aug 22;114(4):511-20. (PMID: 12941278) J Gen Physiol. 2008 Jun;131(6):563-73. (PMID: 18474636) Mol Cell. 2010 Dec 22;40(6):917-26. (PMID: 21172657) Cell. 2008 Jan 11;132(1):101-12. (PMID: 18191224) Nature. 1996 Dec 5;384(6608):432-8. (PMID: 8945469) J Cell Biol. 2004 Apr;165(1):41-52. (PMID: 15078901) EMBO J. 1997 Nov 3;16(21):6325-36. (PMID: 9351815) Nature. 2004 Jun 24;429(6994):834-40. (PMID: 15215855) Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10037-41. (PMID: 11517324) Nat Struct Mol Biol. 2014 Apr;21(4):325-35. (PMID: 24699081) Cell. 2017 Mar 9;168(6):951-953. (PMID: 28283067) Mol Biol Cell. 1998 Jan;9(1):209-22. (PMID: 9437001) Am J Physiol Gastrointest Liver Physiol. 2000 Nov;279(5):G961-74. (PMID: 11052993) J Histochem Cytochem. 2003 Apr;51(4):545-8. (PMID: 12642634) J Biol Chem. 1996 Aug 23;271(34):20895-902. (PMID: 8702846) EMBO J. 2006 Oct 4;25(19):4557-66. (PMID: 16977321) Proc Natl Acad Sci U S A. 2011 Jun 21;108(25):10174-7. (PMID: 21606332) Cell. 2006 Jul 28;126(2):361-73. (PMID: 16873066) EMBO J. 2005 Jul 6;24(13):2284-93. (PMID: 15973433) J Biol Chem. 1996 Sep 20;271(38):22983-9. (PMID: 8798485) J Biol Chem. 2017 Feb 24;292(8):3112-3128. (PMID: 28077573) Mol Biol Cell. 1992 Feb;3(2):129-42. (PMID: 1550957) J Biol Chem. 2004 Sep 10;279(37):38369-78. (PMID: 15252059) Int J Biochem Cell Biol. 2013 Aug;45(8):1833-42. (PMID: 23732108) J Biol Chem. 2013 Jun 21;288(25):18506-20. (PMID: 23653356) Structure. 2008 May;16(5):715-26. (PMID: 18462676) Hum Mol Genet. 2006 Jan 15;15(2):189-99. (PMID: 16321991) Acta Crystallogr D Biol Crystallogr. 2002 Jun;58(Pt 6 No 1):899-907. (PMID: 12037327) Eur Biophys J. 2013 Mar;42(2-3):199-207. (PMID: 22588483) Curr Opin Struct Biol. 2009 Apr;19(2):209-17. (PMID: 19362814) Cell. 2010 Nov 12;143(4):579-91. (PMID: 21074049) J Biol Chem. 2009 May 29;284(22):14710-22. (PMID: 19324879) Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W665-7. (PMID: 15215472) J Mol Biol. 2016 May 8;428(9 Pt B):1861-9. (PMID: 26608813) Proc Natl Acad Sci U S A. 2006 Sep 12;103(37):13658-63. (PMID: 16954199) Protein Sci. 2014 Jan;23(1):34-46. (PMID: 24155053) Science. 2016 Feb 19;351(6275):871-5. (PMID: 26822609) Science. 1990 Jan 5;247(4938):79-82. (PMID: 2294595) Biochemistry. 2004 Oct 12;43(40):12716-22. (PMID: 15461443) Nature. 2007 Dec 13;450(7172):1026-30. (PMID: 18075582) Front Oncol. 2016 Aug 03;6:181. (PMID: 27536557) J Biol Chem. 1998 Nov 13;273(46):30344-51. (PMID: 9804797) Mol Biol Cell. 2006 Jan;17(1):203-12. (PMID: 16267277) Cell. 1990 Nov 2;63(3):503-13. (PMID: 2225064) Biochim Biophys Acta. 2012 Jan;1823(1):117-24. (PMID: 21945179) Cold Spring Harb Perspect Biol. 2013 Sep 01;5(9):null. (PMID: 23232094) Mol Cell Biol. 2002 Jan;22(2):626-34. (PMID: 11756557) Mol Cell. 2009 Apr 24;34(2):212-22. (PMID: 19394298) Biochim Biophys Acta. 2011 Mar;1808(3):925-36. (PMID: 20599420) Nature. 2001 Dec 6;414(6864):652-6. (PMID: 11740563) J Cell Biol. 2008 Jun 30;181(7):1095-105. (PMID: 18573918) Mol Biol Cell. 2009 Jul;20(14):3330-41. (PMID: 19458199) J Biol Chem. 1996 Nov 1;271(44):27280-4. (PMID: 8910302) J Biol Chem. 1993 Mar 15;268(8):5798-801. (PMID: 8449946) Nature. 2005 Jan 27;433(7024):377-81. (PMID: 15674282) EMBO J. 2009 Oct 7;28(19):2874-84. (PMID: 19696741) Nature. 1989 Aug 3;340(6232):400-4. (PMID: 2569166) Methods Mol Biol. 2010;619:365-76. (PMID: 20419421) Nature. 2006 Sep 14;443(7108):180-5. (PMID: 16943773) Cell. 1988 Jul 15;54(2):209-20. (PMID: 3292055) EMBO J. 1991 Oct;10(10):2783-93. (PMID: 1915263) Cell. 1995 Oct 6;83(1):129-35. (PMID: 7553864) EMBO J. 2002 Nov 1;21(21):5645-52. (PMID: 12411482) Curr Opin Cell Biol. 2012 Aug;24(4):460-6. (PMID: 22854296) Genes Dev. 2008 Dec 1;22(23 ):3308-19. (PMID: 19015277) EMBO J. 2000 May 15;19(10):2181-92. (PMID: 10811609) Biochem J. 2017 Feb 1;474(3):357-376. (PMID: 27903760) Cell Mol Life Sci. 2008 Aug;65(15):2360-71. (PMID: 18438607) J Mol Graph. 1996 Feb;14(1):33-8, 27-8. (PMID: 8744570) Nature. 1997 Aug 28;388(6645):891-5. (PMID: 9278052) Annu Rev Biophys. 2008;37:23-42. (PMID: 18573071) J Biol Chem. 2011 Mar 18;286(11):9443-56. (PMID: 21209460) Mol Biol Cell. 1996 Dec;7(12 ):2029-44. (PMID: 8970163) Annu Rev Genet. 1984;18:233-70. (PMID: 6397123) Antioxid Redox Signal. 2012 May 15;16(10):1119-28. (PMID: 22229892) J Mol Biol. 2015 Mar 13;427(5):999-1022. (PMID: 25277655) J Cell Biol. 2001 May 28;153(5):1061-70. (PMID: 11381090) Traffic. 2016 Apr;17 (4):341-50. (PMID: 27004930) Biochim Biophys Acta. 2016 Jul;1858(7 Pt B):1619-34. (PMID: 26853937) Biochim Biophys Acta. 2006 Aug;1758(8):976-88. (PMID: 16782047) Cell. 2016 Jul 14;166(2):394-407. (PMID: 27321670) EMBO J. 2002 Feb 15;21(4):615-21. (PMID: 11847109) J Cell Sci. 2007 Feb 15;120(Pt 4):682-91. (PMID: 17264153) Proc Natl Acad Sci U S A. 2013 Feb 26;110(9):3327-32. (PMID: 23401548) Cell. 2014 Sep 11;158(6):1375-88. (PMID: 25215493) Nat Cell Biol. 2002 Feb;4(2):134-9. (PMID: 11813000) J Biol Chem. 2014 Jul 4;289(27):19053-66. (PMID: 24860107) Biotechniques. 1999 Apr;26(4):680-2. (PMID: 10343905) Cell. 1995 Oct 6;83(1):121-7. (PMID: 7553863) Mol Biol Cell. 2000 May;11(5):1657-72. (PMID: 10793142) Cell. 2006 Jul 28;126(2):349-59. (PMID: 16873065) EMBO J. 1999 Mar 15;18(6):1492-505. (PMID: 10075921) Nature. 2004 Jun 24;429(6994):841-7. (PMID: 15215856) Mol Biol Cell. 1998 Oct;9(10 ):2767-84. (PMID: 9763443) Molecules. 2015 Feb 12;20(2):3027-49. (PMID: 25685910) Structure. 2015 Aug 4;23(8):1526-37. (PMID: 26118532) FEBS Lett. 2016 Mar;590(5):595-604. (PMID: 26849035) Genes Dev. 2001 Oct 15;15(20):2660-74. (PMID: 11641273) J Mol Biol. 2015 Sep 11;427(18):2948-65. (PMID: 25913688) Physiology (Bethesda). 2007 Apr;22:122-30. (PMID: 17420303) Mol Cell. 2013 Aug 8;51(3):297-309. (PMID: 23932713) Cell. 2016 Dec 1;167(6):1586-1597.e9. (PMID: 27912062) J Cell Biol. 1993 Dec;123(6 Pt 1):1355-63. (PMID: 8253836) Nat Biotechnol. 2003 Aug;21(8):921-6. (PMID: 12872131) Structure. 2016 Jan 5;24(1):127-39. (PMID: 26712278) Nat Cell Biol. 2014 Jan;16(1):77-86. (PMID: 24292014) Nat Rev Mol Cell Biol. 2008 Dec;9(12):944-57. (PMID: 19002207) Mol Biol Cell. 2003 Aug;14(8):3437-48. (PMID: 12925775) Physiol Rev. 2012 Apr;92(2):537-76. (PMID: 22535891) Gene. 2016 May 25;583(1):64-77. (PMID: 26945625) Science. 2009 Mar 27;323(5922):1718-22. (PMID: 19325113) J Biol Chem. 2011 Aug 19;286(33):29376-87. (PMID: 21708947) Nat Cell Biol. 2001 Jan;3(1):24-9. (PMID: 11146622) Mol Cell Biol. 1996 Aug;16(8):4378-86. (PMID: 8754838) J Cell Sci. 2014 Sep 15;127(Pt 18):3877-83. (PMID: 25146396) PLoS One. 2016 Feb 05;11(2):e0148327. (PMID: 26849222) EMBO J. 1994 Dec 15;13(24):6076-86. (PMID: 7529176) Methods Mol Biol. 2005;301:3-22. (PMID: 15917622) Nature. 2011 Jul 20;475(7356):324-32. (PMID: 21776078) Mol Cell. 2014 Apr 10;54(1):166-79. (PMID: 24685158) Mol Biol Cell. 2001 Oct;12(10):3226-41. (PMID: 11598205) J Mol Biol. 1993 Dec 5;234(3):779-815. (PMID: 8254673) |
| معلومات مُعتمدة: | K01 DK101584 United States DK NIDDK NIH HHS; P30 DK079307 United States DK NIDDK NIH HHS; P30 DK072506 United States DK NIDDK NIH HHS; T32 EB009383 United States EB NIBIB NIH HHS; R01 GM075061 United States GM NIGMS NIH HHS; T32 DK061296 United States DK NIDDK NIH HHS; R01 GM117593 United States GM NIGMS NIH HHS |
| المشرفين على المادة: | 0 (Cell Cycle Proteins) 0 (Membrane Proteins) 0 (Protein Translocation Systems) 0 (Saccharomyces cerevisiae Proteins) 0 (Ubiquitin) EC 2.3.2.27 (Ubiquitin-Protein Ligases) EC 3.4.25.1 (Proteasome Endopeptidase Complex) EC 3.6.1.- (Adenosine Triphosphatases) |
| تواريخ الأحداث: | Date Created: 20170526 Date Completed: 20171116 Latest Revision: 20181113 |
| رمز التحديث: | 20240628 |
| مُعرف محوري في PubMed: | PMC5509421 |
| DOI: | 10.1091/mbc.E17-03-0184 |
| PMID: | 28539401 |
| قاعدة البيانات: | MEDLINE |
| تدمد: | 1939-4586 |
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| DOI: | 10.1091/mbc.E17-03-0184 |