Structural and functional impact of site-directed methionine oxidation in myosin

Biochemistry

Volumn 50, Issue 47, 2011, Pages 10318-10327

  Klein, Jennifer C ^a   Moen, Rebecca J ^b   Smith, Evan A ^b   Titus, Margaret A ^b   Thomas, David D ^b  

^a ST OLAF COLLEGE   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTO-MYOSIN INTERACTION; ATP-ASE ACTIVITY; BIOLOGICAL AGING; CARDIOMYOPATHY LOOP; CELLULAR FUNCTION; DICTYOSTELIUM; DISEASE PROGRESSION; IN-VITRO; METHIONINE OXIDATION; MOLECULAR-LEVEL INSIGHTS; MYOSIN II; PEROXIDE TREATMENT; PROTEIN OXIDATION; REACTIVE OXYGEN AND NITROGEN SPECIES; SECONDARY STRUCTURES; SPECIFIC SITES; STRUCTURAL CHANGE; STRUCTURAL STATE;

AMINO ACIDS; BINDING SITES; ELECTRON SPIN RESONANCE SPECTROSCOPY; MUSCLE; PARAMAGNETIC RESONANCE; PARAMAGNETISM; PROTEINS;

OXIDATION;

ACTIN BINDING PROTEIN; ADENOSINE TRIPHOSPHATASE; LEUCINE; METHIONINE; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE;

AGING; ARTICLE; CARDIOMYOPATHY; DICTYOSTELIUM; DISEASE COURSE; ELECTRON SPIN RESONANCE; IN VITRO STUDY; MUTAGENESIS; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN INTERACTION; SPECTROSCOPY;

DICTYOSTELIUM; METHIONINE; MUSCLE, SKELETAL; MUTAGENESIS, SITE-DIRECTED; MYOSIN TYPE II; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTOZOAN PROTEINS;

DICTYOSTELIUM;

EID: 81855199913     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201279u     Document Type: Article

References (62)

1. Hoshi, T. and Heinemann, S. (2001) Regulation of cell function by methionine oxidation and reduction J. Physiol. 531, 1-11 (Pubitemid 32178022)
2. Davies, K. J. (2000) Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems IUBMB Life 50, 279-289 (Pubitemid 32289086)
3. Bigelow, D. J. and Squier, T. C. (2005) Redox modulation of cellular signaling and metabolism through reversible oxidation of methionine sensors in calcium regulatory proteins Biochim. Biophys. Acta 1703, 121-134 (Pubitemid 40170435)
4. Stadtman, E. R. (2006) Protein oxidation and aging Free Radical Res. 40, 1250-1258 (Pubitemid 44698274)
5. Emes, M. J. (2009) Oxidation of methionine residues: the missing link between stress and signalling responses in plants Biochem. J. 422, e1-2
6. Prentice, H. M., Moench, I. A., Rickaway, Z. T., Dougherty, C. J., Webster, K. A., and Weissbach, H. (2008) MsrA protects cardiac myocytes against hypoxia/reoxygenation induced cell death Biochem. Biophys. Res. Commun. 366, 775-778
7. Jackson, M. J. (2008) Redox regulation of skeletal muscle IUBMB Life 60, 497-501
8. Palomero, J. and Jackson, M. J. (2010) Redox regulation in skeletal muscle during contractile activity and aging J. Anim. Sci. 88, 1307-1313
9. Kinugawa, S., Tsutsui, H., Hayashidani, S., Ide, T., Suematsu, N., Satoh, S., Utsumi, H., and Takeshita, A. (2000) Treatment with dimethylthiourea prevents left ventricular remodeling and failure after experimental myocardial infarction in mice: role of oxidative stress Circ. Res. 87, 392-398
10. Maack, C., Kartes, T., Kilter, H., Schafers, H. J., Nickenig, G., Bohm, M., and Laufs, U. (2003) Oxygen free radical release in human failing myocardium is associated with increased activity of rac1-GTPase and represents a target for statin treatment Circulation 108, 1567-1574 (Pubitemid 37187782)
11. Moylan, J. S. and Reid, M. B. (2007) Oxidative stress, chronic disease, and muscle wasting Muscle Nerve 35, 411-429 (Pubitemid 46542961)
12. Reid, M. B. and Durham, W. J. (2002) Generation of reactive oxygen and nitrogen species in contracting skeletal muscle: potential impact on aging Ann. N.Y. Acad. Sci. 959, 108-116 (Pubitemid 34457556)
13. Reid, M. B. (2001) Invited Review: redox modulation of skeletal muscle contraction: what we know and what we don't J. Appl. Physiol. 90, 724-731 (Pubitemid 32118935)
14. Tidball, J. G. and Wehling-Henricks, M. (2007) The role of free radicals in the pathophysiology of muscular dystrophy J. Appl. Physiol. 102, 1677-1686 (Pubitemid 46571068)
15. Stadtman, E. R. and Berlett, B. S. (1997) Reactive oxygen-mediated protein oxidation in aging and disease Chem. Res. Toxicol. 10, 485-494 (Pubitemid 27217204)
16. Prochniewicz, E., Thompson, L. V., and Thomas, D. D. (2007) Age-related decline in actomyosin structure and function Exp. Gerontol. 42, 931-938 (Pubitemid 47418560)
17. Delbono, O. (2002) Molecular mechanisms and therapeutics of the deficit in specific force in ageing skeletal muscle Biogerontology 3, 265-270 (Pubitemid 35174239)
18. Lowe, D. A., Surek, J. T., Thomas, D. D., and Thompson, L. V. (2001) Electron paramagnetic resonance reveals age-related myosin structural changes in rat skeletal muscle fibers Am. J. Physiol. Cell Physiol. 280, C540-547
19. Lowe, D. A., Warren, G. L., Snow, L. M., Thompson, L. V., and Thomas, D. D. (2004) Muscle activity and aging affect myosin structural distribution and force generation in rat fibers J. Appl. Physiol. 96, 498-506 (Pubitemid 38140149)
20. Ghesquiere, B., Jonckheere, V., Colaert, N., Van Durme, J., Timmerman, E., Goethals, M., Schymkowitz, J., Rousseau, F., Vandekerckhove, J., and Gevaert, K. (2011) Redox proteomics of protein-bound methionine oxidation Mol. Cell. Proteomics 10, xxxx
21. Stadtman, E. R., Van Remmen, H., Richardson, A., Wehr, N. B., and Levine, R. L. (2005) Methionine oxidation and aging Biochim. Biophys. Acta 1703, 135-140 (Pubitemid 40170436)
22. Bigelow, D. J. and Squier, T. C. (2011) Thioredoxin-dependent redox regulation of cellular signaling and stress response through reversible oxidation of methionines Mol. Biosyst. 7, 2101-2109
23. Hardin, S. C., Larue, C. T., Oh, M. H., Jain, V., and Huber, S. C. (2009) Coupling oxidative signals to protein phosphorylation via methionine oxidation in Arabidopsis Biochem. J. 422, 305-312
24. Agbas, A. and Moskovitz, J. (2009) The Role of Methionine Oxidation/Reduction in the Regulation of Immune Response Curr. Signal Transduct. Ther. 4, 46-50
25. Carruthers, N. J. and Stemmer, P. M. (2008) Methionine oxidation in the calmodulin-binding domain of calcineurin disrupts calmodulin binding and calcineurin activation Biochemistry 47, 3085-3095 (Pubitemid 351364902)
26. Balog, E. M., Norton, L. E., Bloomquist, R. A., Cornea, R. L., Black, D. J., Louis, C. F., Thomas, D. D., and Fruen, B. R. (2003) Calmodulin oxidation and methionine to glutamine substitutions reveal methionine residues critical for functional interaction with ryanodine receptor-1 J. Biol. Chem. 278, 15615-15621 (Pubitemid 36799671)
27. Balog, E. M., Norton, L. E., Thomas, D. D., and Fruen, B. R. (2006) Role of calmodulin methionine residues in mediating productive association with cardiac ryanodine receptors Am. J. Physiol. Heart Circ. Physiol. 290, H794-799
28. Balog, E. M., Lockamy, E. L., Thomas, D. D., and Ferrington, D. A. (2009) Site-Specific Methionine Oxidation Initiates Calmodulin Degradation by the 20S Proteasome Biochemistry 48, 3005-3016
29. Erickson, J. R., Joiner, M. L., Guan, X., Kutschke, W., Yang, J., Oddis, C. V., Bartlett, R. K., Lowe, J. S., O'Donnell, S. E., Aykin-Burns, N., Zimmerman, M. C., Zimmerman, K., Ham, A. J., Weiss, R. M., Spitz, D. R., Shea, M. A., Colbran, R. J., Mohler, P. J., and Anderson, M. E. (2008) A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation Cell 133, 462-474 (Pubitemid 351608692)
30. Boschek, C. B., Jones, T. E., Smallwood, H. S., Squier, T. C., and Bigelow, D. J. (2008) Loss of the calmodulin-dependent inhibition of the RyR1 calcium release channel upon oxidation of methionines in calmodulin Biochemistry 47, 131-142
31. Anbanandam, A., Bieber Urbauer, R. J., Bartlett, R. K., Smallwood, H. S., Squier, T. C., and Urbauer, J. L. (2005) Mediating molecular recognition by methionine oxidation: conformational switching by oxidation of methionine in the carboxyl-terminal domain of calmodulin Biochemistry 44, 9486-9496 (Pubitemid 40962047)
32. Bartlett, R. K., Bieber Urbauer, R. J., Anbanandam, A., Smallwood, H. S., Urbauer, J. L., and Squier, T. C. (2003) Oxidation of Met144 and Met145 in calmodulin blocks calmodulin dependent activation of the plasma membrane Ca-ATPase Biochemistry 42, 3231-3238 (Pubitemid 36348631)
33. Sun, H., Gao, J., Ferrington, D. A., Biesiada, H., Williams, T. D., and Squier, T. C. (1999) Repair of oxidized calmodulin by methionine sulfoxide reductase restores ability to activate the plasma membrane Ca-ATPase Biochemistry 38, 105-112 (Pubitemid 29035676)
34. Prochniewicz, E., Thomas, D. D., and Thompson, L. V. (2005) Age-related decline in actomyosin function J. Gerontol., Ser. A 60, 425-431 (Pubitemid 40712857)
35. Prochniewicz, E., Lowe, D. A., Spakowicz, D. J., Higgins, L., O'Conor, K., Thompson, L. V., Ferrington, D. A., and Thomas, D. D. (2008) Functional, structural, and chemical changes in myosin associated with hydrogen peroxide treatment of skeletal muscle fibers Am. J. Physiol. Cell Physiol. 294, C613-626
36. Agafonov, R. V., Nesmelov, Y. E., Titus, M. A., and Thomas, D. D. (2008) Muscle and nonmuscle myosins probed by a spin label at equivalent sites in the force-generating domain Proc. Natl. Acad. Sci. U. S. A. 105, 13397-13402
37. Klein, J. C., Burr, A. R., Svensson, B., Kennedy, D. J., Allingham, J., Titus, M. A., Rayment, I., and Thomas, D. D. (2008) Actin-binding cleft closure in myosin II probed by site-directed spin labeling and pulsed EPR Proc. Natl. Acad. Sci. U. S. A. 105, 12867-12872
38. Prochniewicz, E., Zhang, Q., Howard, E. C., and Thomas, D. D. (1996) Microsecond rotational dynamics of actin: spectroscopic detection and theoretical simulation J. Mol. Biol. 255, 446-457 (Pubitemid 26105568)
39. Prochniewicz, E., Walseth, T. F., and Thomas, D. D. (2004) Structural dynamics of actin during active interaction with myosin: different effects of weakly and strongly bound myosin heads Biochemistry 43, 10642-10652 (Pubitemid 39096706)
40. Lanzetta, P. A., Alvarez, L. J., Reinach, P. S., and Candia, O. A. (1979) An improved assay for nanomole amounts of inorganic phosphate Anal. Biochem. 100, 95-97 (Pubitemid 10157636)
41. Fiske, C. H. and Subbarow, Y. (1925) The colorimetric Determination of Phosphorus J. Biol. Chem. 26, 375-400
42. Sreerama, N. and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set Anal. Biochem. 287, 252-260 (Pubitemid 32006234)
43. Budil, D. E., Lee, S., Saxena, S., and Freed, J. H. (1996) Nonlinear-least-squares analysis of slow-motion EPR spectra in one and two dimensions using a modified Levenberg-Marquardt algorithm J. Magn. Reson., Ser. A 120, 155-189 (Pubitemid 126751752)
44. Nesmelov, Y. E., Karim, C. B., Song, L., Fajer, P. G., and Thomas, D. D. (2007) Rotational dynamics of phospholamban determined by multifrequency electron paramagnetic resonance Biophys. J. 93, 2805-2812 (Pubitemid 47607816)
45. Nesmelov, Y. E., Agafonov, R. V., Burr, A. R., Weber, R. T., and Thomas, D. D. (2008) Structure and dynamics of the force-generating domain of myosin probed by multifrequency electron paramagnetic resonance Biophys. J. 95, 247-256
46. Pannier, M., Veit, S., Godt, A., Jeschke, G., and Spiess, H. W. (2000) Dead-time free measurement of dipole-dipole interactions between electron spins J. Magn. Reson. 142, 331-340
47. Pake, G. E. (1948) Nuclear Resonance Absorption in Hydrated Crystals: Fine Structure of the Proton Line J. Chem. Phys. 16, 327-336
48. Rabenstein, M. D. and Shin, Y. K. (1995) Determination of the distance between two spin labels attached to a macromolecule Proc. Natl. Acad. Sci. U. S. A. 92, 8239-8243
49. Steinhoff, H. J., Radzwill, N., Thevis, W., Lenz, V., Brandenburg, D., Antson, A., Dodson, G., and Wollmer, A. (1997) Determination of interspin distances between spin labels attached to insulin: comparison of electron paramagnetic resonance data with the X-ray structure Biophys. J. 73, 3287-3298 (Pubitemid 27525791)
50. Altenbach, C., Oh, K. J., Trabanino, R. J., Hideg, K., and Hubbell, W. L. (2001) Estimation of inter-residue distances in spin labeled proteins at physiological temperatures: experimental strategies and practical limitations Biochemistry 40, 15471-15482 (Pubitemid 34015174)
51. Jeschke, G. (2002) Distance measurements in the nanometer range by pulse EPR ChemPhysChem 3, 927-932
52. Jeschke, G., Koch, A., Jonas, U., and Godt, A. (2002) Direct conversion of EPR dipolar time evolution data to distance distributions J. Magn. Reson. 155, 72-82
53. Fraczkiewicz, R. and Braun, W. (1998) Exact and Efficient Analytical Calculation of the Accessible Surface Areas and Their Gradients for Macromolecules J. Comput. Chem. 19, 319-333 (Pubitemid 128592649)
54. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics J. Mol. Graphics 14 (33-38) 27-38
55. Schroder, R. R., Manstein, D. J., Jahn, W., Holden, H., Rayment, I., Holmes, K. C., and Spudich, J. A. (1993) Three-dimensional atomic model of F-actin decorated with Dictyostelium myosin S1 Nature 364, 171-174 (Pubitemid 23238204)
56. Bauer, C. B., Holden, H. M., Thoden, J. B., Smith, R., and Rayment, I. (2000) X-ray structures of the apo and MgATP-bound states of Dictyostelium discoideum myosin motor domain J. Biol. Chem. 275, 38494-38499 (Pubitemid 32009176)
57. Kim, Y. H., Berry, A. H., Spencer, D. S., and Stites, W. E. (2001) Comparing the effect on protein stability of methionine oxidation versus mutagenesis: steps toward engineering oxidative resistance in proteins Protein Eng. 14, 343-347 (Pubitemid 32655950)
58. Yergey, J., Heller, D., Hansen, G., Cotter, R. J., and Fenselau, C. (1983) Isotopic distributions in mass spectra of large molecules Anal. Chem. 55, 353-356
59. Zolkiewski, M., Redowicz, M. J., Korn, E. D., and Ginsburg, A. (1996) Thermal unfolding of Acanthamoeba myosin II and skeletal muscle myosin Biophys. Chem. 59, 365-371 (Pubitemid 26160122)
60. Passarelli, C., Petrini, S., Pastore, A., Bonetto, V., Sale, P., Gaeta, L. M., Tozzi, G., Bertini, E., Canepari, M., Rossi, R., and Piemonte, F. (2008) Myosin as a potential redox-sensor: an in vitro study J. Muscle Res. Cell Motil. 29, 119-126
61. Rasmussen, H. H., Hamilton, E. J., Liu, C. C., and Figtree, G. A. (2010) Reversible oxidative modification: implications for cardiovascular physiology and pathophysiology Trends Cardiovasc. Med. 20, 85-90
62. Passarelli, C., Di Venere, A., Piroddi, N., Pastore, A., Scellini, B., Tesi, C., Petrini, S., Sale, P., Bertini, E., Poggesi, C., and Piemonte, F. (2010) Susceptibility of isolated myofibrils to in vitro glutathionylation: Potential relevance to muscle functions Cytoskeleton 67, 81-89