S-glutathionylation of cryptic cysteines enhances titin elasticity by blocking protein folding

Cell

Volumn 156, Issue 6, 2014, Pages 1235-1246

  Alegre Cebollada, Jorge ^a   Kosuri, Pallav ^a   Giganti, David ^a   Eckels, Edward ^a,b   Rivas Pardo, Jaime Andrés ^a   Hamdani, Nazha ^c   Warren, Chad M ^d   Solaro, R John ^d   Linke, Wolfgang A ^c   Fernández, Julio M ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b Ruhr University Bochum ^*  (United States)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIN; CYSTEINE; GLUTAREDOXIN; IMMUNOGLOBULIN;

ARTICLE; ELASTICITY; HEART MUSCLE CELL; HUMAN; HUMAN CELL; MECHANOTRANSDUCTION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN UNFOLDING; RIGIDITY; S GLUTATHIONYLATION; ALKYLATION; AMINO ACID SEQUENCE; CHEMICAL MODIFICATION; DISULFIDE BOND; GLUTATHIONYLATION; HUMAN TISSUE; MOLECULAR STABILITY; MUSCLE RIGIDITY; PROTEIN DOMAIN; PROTEIN REFOLDING;

BIOMECHANICAL PHENOMENA; CONNECTIN; CYSTEINE; ELASTICITY; GLUTAREDOXINS; HUMANS; MODELS, MOLECULAR; MYOCYTES, CARDIAC; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY;

EID: 84896321106     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.01.056     Document Type: Article

References (68)

1. J. Alegre-Cebollada, P. Kosuri, J.A. Rivas-Pardo, and J.M. Fernández Direct observation of disulfide isomerization in a single protein Nat. Chem. 3 2011 882 887
2. B.R. Anderson, J. Bogomolovas, S. Labeit, and H. Granzier Single molecule force spectroscopy on titin implicates immunoglobulin domain stability as a cardiac disease mechanism J. Biol. Chem. 288 2013 5303 5315
3. B.S. Avner, K.M. Shioura, S.B. Scruggs, M. Grachoff, D.L. Geenen, D.L. Helseth Jr., M. Farjah, P.H. Goldspink, and R.J. Solaro Myocardial infarction in mice alters sarcomeric function via post-translational protein modification Mol. Cell. Biochem. 363 2012 203 215
4. O. Ceyhan-Birsoy, P.B. Agrawal, C. Hidalgo, K. Schmitz-Abe, E.T. DeChene, L.C. Swanson, R. Soemedi, N. Vasli, S.T. Iannaccone, and P.B. Shieh et al. Recessive truncating titin gene, TTN, mutations presenting as centronuclear myopathy Neurology 81 2013 1205 1214
5. F.C. Chen, and O. Ogut Decline of contractility during ischemia-reperfusion injury: actin glutathionylation and its effect on allosteric interaction with tropomyosin Am. J. Physiol. Cell Physiol. 290 2006 C719 C727
6. C.S. Chung, K.R. Hutchinson, M. Methawasin, C. Saripalli, J.E. Smith 3rd, C.G. Hidalgo, X. Luo, S. Labeit, C. Guo, and H.L. Granzier Shortening of the elastic tandem immunoglobulin segment of titin leads to diastolic dysfunction Circulation 128 2013 19 28
7. I. Dalle-Donne, R. Rossi, G. Colombo, D. Giustarini, and A. Milzani Protein S-glutathionylation: a regulatory device from bacteria to humans Trends Biochem. Sci. 34 2009 85 96
8. A. del Rio, R. Perez-Jimenez, R. Liu, P. Roca-Cusachs, J.M. Fernandez, and M.P. Sheetz Stretching single talin rod molecules activates vinculin binding Science 323 2009 638 641
9. B. Efron The Jackknife, the Bootstrap, and Other Resampling Plans 1982 SIAM Philadelphia
10. J.M. Fernandez, and H. Li Force-clamp spectroscopy monitors the folding trajectory of a single protein Science 303 2004 1674 1678
11. A. Freiburg, K. Trombitas, W. Hell, O. Cazorla, F. Fougerousse, T. Centner, B. Kolmerer, C. Witt, J.S. Beckmann, and C.C. Gregorio et al. Series of exon-skipping events in the elastic spring region of titin as the structural basis for myofibrillar elastic diversity Circ. Res. 86 2000 1114 1121
12. M.M. Gallogly, and J.J. Mieyal Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress Curr. Opin. Pharmacol. 7 2007 381 391
13. B. Gerull, M. Gramlich, J. Atherton, M. McNabb, K. Trombitás, S. Sasse-Klaassen, J.G. Seidman, C. Seidman, H. Granzier, and S. Labeit et al. Mutations of TTN, encoding the giant muscle filament titin, cause familial dilated cardiomyopathy Nat. Genet. 30 2002 201 204
14. H.F. Gilbert Molecular and cellular aspects of thiol-disulfide exchange Adv. Enzymol. Relat. Areas Mol. Biol. 63 1990 69 172
15. H.F. Gilbert Thiol/disulfide exchange equilibria and disulfide bond stability Methods Enzymol. 251 1995 8 28
16. F.J. Giordano Oxygen, oxidative stress, hypoxia, and heart failure J. Clin. Invest. 115 2005 500 508
17. N. Hamdani, J. Krysiak, M.M. Kreusser, S. Neef, C.G. Dos Remedios, L.S. Maier, M. Krüger, J. Backs, and W.A. Linke Crucial role for Ca2(+)/calmodulin-dependent protein kinase-II in regulating diastolic stress of normal and failing hearts via titin phosphorylation Circ. Res. 112 2013 664 674
18. J.M. Hare Nitroso-redox balance in the cardiovascular system N. Engl. J. Med. 351 2004 2112 2114
19. D.S. Herman, L. Lam, M.R.G. Taylor, L.B. Wang, P. Teekakirikul, D. Christodoulou, L. Conner, S.R. DePalma, B. McDonough, and E. Sparks et al. Truncations of titin causing dilated cardiomyopathy N. Engl. J. Med. 366 2012 619 628
20. M. Itoh-Satoh, T. Hayashi, H. Nishi, Y. Koga, T. Arimura, T. Koyanagi, M. Takahashi, S. Hohda, K. Ueda, and T. Nouchi et al. Titin mutations as the molecular basis for dilated cardiomyopathy Biochem. Biophys. Res. Commun. 291 2002 385 393
21. C.P. Johnson, H.Y. Tang, C. Carag, D.W. Speicher, and D.E. Discher Forced unfolding of proteins within cells Science 317 2007 663 666
22. M.S. Kellermayer, and L. Grama Stretching and visualizing titin molecules: combining structure, dynamics and mechanics J. Muscle Res. Cell Motil. 23 2002 499 511
23. E. Klotzsch, M.L. Smith, K.E. Kubow, S. Muntwyler, W.C. Little, F. Beyeler, D. Gourdon, B.J. Nelson, and V. Vogel Fibronectin forms the most extensible biological fibers displaying switchable force-exposed cryptic binding sites Proc. Natl. Acad. Sci. USA 106 2009 18267 18272
24. P. Kosuri, J. Alegre-Cebollada, J. Feng, A. Kaplan, A. Ingles-Prieto, C.L. Badilla, B.R. Stockwell, J.M. Sanchez-Ruiz, A. Holmgren, and J.M. Fernandez Protein folding drives disulfide formation Cell 151 2012 794 806
25. C.C. Krieger, X. An, H.Y. Tang, N. Mohandas, D.W. Speicher, and D.E. Discher Cysteine shotgun-mass spectrometry (CS-MS) reveals dynamic sequence of protein structure changes within mutant and stressed cells Proc. Natl. Acad. Sci. USA 108 2011 8269 8274
26. H. Li, W.A. Linke, A.F. Oberhauser, M. Carrion-Vazquez, J.G. Kerkvliet, H. Lu, P.E. Marszalek, and J.M. Fernandez Reverse engineering of the giant muscle protein titin Nature 418 2002 998 1002
27. C.H. Lillig, C. Berndt, and A. Holmgren Glutaredoxin systems Biochim. Biophys. Acta 1780 2008 1304 1317
28. W.A. Linke, and M. Krüger The giant protein titin as an integrator of myocyte signaling pathways Physiology (Bethesda) 25 2010 186 198
29. W.A. Linke, V.I. Popov, and G.H. Pollack Passive and active tension in single cardiac myofibrils Biophys. J. 67 1994 782 792
30. J.D. Lovelock, M.M. Monasky, E.M. Jeong, H.A. Lardin, H. Liu, B.G. Patel, D.M. Taglieri, L. Gu, P. Kumar, and N. Pokhrel et al. Ranolazine improves cardiac diastolic dysfunction through modulation of myofilament calcium sensitivity Circ. Res. 110 2012 841 850
31. A. Martínez-Ruiz, and S. Lamas Signalling by NO-induced protein S-nitrosylation and S-glutathionylation: convergences and divergences Cardiovasc. Res. 75 2007 220 228
32. Y. Matsumoto, T. Hayashi, N. Inagaki, M. Takahashi, S. Hiroi, T. Nakamura, T. Arimura, K. Nakamura, N. Ashizawa, and M. Yasunami et al. Functional analysis of titin/connectin N2-B mutations found in cardiomyopathy J. Muscle Res. Cell Motil. 26 2005 367 374
33. O. Mayans, J. Wuerges, S. Canela, M. Gautel, and M. Wilmanns Structural evidence for a possible role of reversible disulphide bridge formation in the elasticity of the muscle protein titin Structure 9 2001 331 340
34. E.M. McNally Genetics: broken giant linked to heart failure Nature 483 2012 281 282
35. A. Minajeva, M. Kulke, J.M. Fernandez, and W.A. Linke Unfolding of titin domains explains the viscoelastic behavior of skeletal myofibrils Biophys. J. 80 2001 1442 1451
36. J.P. Mollica, T.L. Dutka, T.L. Merry, C.R. Lamboley, G.K. McConell, M.J. McKenna, R.M. Murphy, and G.D. Lamb S-glutathionylation of troponin I (fast) increases contractile apparatus Ca2+ sensitivity in fast-twitch muscle fibres of rats and humans J. Physiol. 590 2012 1443 1463
37. J. Nedrud, S. Labeit, M. Gotthardt, and H. Granzier Mechanics on myocardium deficient in the N2B region of titin: the cardiac-unique spring element improves efficiency of the cardiac cycle Biophys. J. 101 2011 1385 1392
38. N. Norton, D. Li, E. Rampersaud, A. Morales, E.R. Martin, S. Zuchner, S. Guo, M. Gonzalez, D.J. Hedges, P.D. Robertson National Heart, Lung, and Blood Institute GO Exome Sequencing Project and the Exome Sequencing Project Family Studies Project Team Exome sequencing and genome-wide linkage analysis in 17 families illustrate the complex contribution of TTN truncating variants to dilated cardiomyopathy Circ Cardiovasc Genet 6 2013 144 153
39. M.A. Pfeffer, and E. Braunwald Ventricular remodeling after myocardial infarction. Experimental observations and clinical implications Circulation 81 1990 1161 1172
40. I. Popa, P. Kosuri, J. Alegre-Cebollada, S. Garcia-Manyes, and J.M. Fernandez Force dependency of biochemical reactions measured by single-molecule force-clamp spectroscopy Nat. Protoc. 8 2013 1261 1276
41. B.L. Prosser, C.W. Ward, and W.J. Lederer X-ROS signaling: rapid mechano-chemo transduction in heart Science 333 2011 1440 1445
42. R. Rastaldo, P. Pagliaro, S. Cappello, C. Penna, D. Mancardi, N. Westerhof, and G. Losano Nitric oxide and cardiac function Life Sci. 81 2007 779 793
43. E.K. Rodriguez, W.C. Hunter, M.J. Royce, M.K. Leppo, A.S. Douglas, and H.F. Weisman A method to reconstruct myocardial sarcomere lengths and orientations at transmural sites in beating canine hearts Am. J. Physiol. 263 1992 H293 H306
44. G. Sánchez, Z. Pedrozo, R.J. Domenech, C. Hidalgo, and P. Donoso Tachycardia increases NADPH oxidase activity and RyR2 S-glutathionylation in ventricular muscle J. Mol. Cell. Cardiol. 39 2005 982 991
45. M. Schlierf, H. Li, and J.M. Fernandez The unfolding kinetics of ubiquitin captured with single-molecule force-clamp techniques Proc. Natl. Acad. Sci. USA 101 2004 7299 7304
46. M.L. Smith, D. Gourdon, W.C. Little, K.E. Kubow, R.A. Eguiluz, S. Luna-Morris, and V. Vogel Force-induced unfolding of fibronectin in the extracellular matrix of living cells PLoS Biol. 5 2007 e268
47. J. Somkuti, Z. Mártonfalvi, M.S. Kellermayer, and L. Smeller Different pressure-temperature behavior of the structured and unstructured regions of titin Biochim. Biophys. Acta 1834 2013 112 118
48. J. Swift, I.L. Ivanovska, A. Buxboim, T. Harada, P.C. Dingal, J. Pinter, J.D. Pajerowski, K.R. Spinler, J.W. Shin, and M. Tewari et al. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation Science 341 2013 1240104
49. M. Taylor, S. Graw, G. Sinagra, C. Barnes, D. Slavov, F. Brun, B. Pinamonti, E.E. Salcedo, W. Sauer, and S. Pyxaras et al. Genetic variation in titin in arrhythmogenic right ventricular cardiomyopathy-overlap syndromes Circulation 124 2011 876 885
50. K. Trombitás, M. Greaser, S. Labeit, J.P. Jin, M. Kellermayer, M. Helmes, and H. Granzier Titin extensibility in situ: entropic elasticity of permanently folded and permanently unfolded molecular segments J. Cell Biol. 140 1998 853 859
51. L. Tskhovrebova, J. Trinick, J.A. Sleep, and R.M. Simmons Elasticity and unfolding of single molecules of the giant muscle protein titin Nature 387 1997 308 312
52. C.M. Warren, P.R. Krzesinski, and M.L. Greaser Vertical agarose gel electrophoresis and electroblotting of high-molecular-weight proteins Electrophoresis 24 2003 1695 1702
53. M.B. West, B.G. Hill, Y.T. Xuan, and A. Bhatnagar Protein glutathiolation by nitric oxide: an intracellular mechanism regulating redox protein modification FASEB J. 20 2006 1715 1717
54. A.P. Wiita, S.R. Ainavarapu, H.H. Huang, and J.M. Fernandez Force-dependent chemical kinetics of disulfide bond reduction observed with single-molecule techniques Proc. Natl. Acad. Sci. USA 103 2006 7222 7227
55. C. Wu, C. Belenda, J.C. Leroux, and M.A. Gauthier Interplay of chemical microenvironment and redox environment on thiol-disulfide exchange kinetics Chemistry 17 2011 10064 10070
56. D. Bader, T. Masaki, and D.A. Fischman Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro J. Cell Biol. 95 1982 763 770
57. N.J. Darby, R.B. Freedman, and T.E. Creighton Dissecting the mechanism of protein disulfide isomerase: catalysis of disulfide bond formation in a model peptide Biochemistry 33 1994 7937 7947
58. S. Garcia-Manyes, L. Dougan, C.L. Badilla, J. Brujic, and J.M. Fernández Direct observation of an ensemble of stable collapsed states in the mechanical folding of ubiquitin Proc. Natl. Acad. Sci. USA 106 2009 10534 10539
59. P. Kosuri, J. Alegre-Cebollada, J. Feng, A. Kaplan, A. Inglés-Prieto, C.L. Badilla, B.R. Stockwell, J.M. Sanchez-Ruiz, A. Holmgren, and J.M. Fernández Protein folding drives disulfide formation Cell 151 2012 794 806
60. J. Layland, A.C. Cave, C. Warren, D.J. Grieve, E. Sparks, J.C. Kentish, R.J. Solaro, and A.M. Shah Protection against endotoxemia-induced contractile dysfunction in mice with cardiac-specific expression of slow skeletal troponin I FASEB J. 19 2005 1137 1139
61. B. Lee, and F.M. Richards The interpretation of protein structures: estimation of static accessibility J. Mol. Biol. 55 1971 379 400
62. C. Notredame, D.G. Higgins, and J. Heringa T-Coffee: A novel method for fast and accurate multiple sequence alignment J. Mol. Biol. 302 2000 205 217
63. A. Sali, and T.L. Blundell Comparative protein modelling by satisfaction of spatial restraints J. Mol. Biol. 234 1993 779 815
64. F.Q. Schafer, and G.R. Buettner Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple Free Radic. Biol. Med. 30 2001 1191 1212
65. S.B. Smith, L. Finzi, and C. Bustamante Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads Science 258 1992 1122 1126
66. R.J. Solaro, D.C. Pang, and F.N. Briggs The purification of cardiac myofibrils with Triton X-100 Biochim. Biophys. Acta 245 1971 259 262
67. S.M. Wang, M.L. Greaser, E. Schultz, J.C. Bulinski, J.J. Lin, and J.L. Lessard Studies on cardiac myofibrillogenesis with antibodies to titin, actin, tropomyosin, and myosin J. Cell Biol. 107 1988 1075 1083
68. L.D. Yates, and M.L. Greaser Quantitative determination of myosin and actin in rabbit skeletal muscle J. Mol. Biol. 168 1983 123 141