Conserved Asp-137 is important for both structure and regulatory functions of cardiac α-tropomyosin (α-TM) in a novel transgenic mouse model expressing α-TM-D137L

Journal of Biological Chemistry

Volumn 288, Issue 23, 2013, Pages 16235-16246

  Yar, Sumeyye ^a   Chowdhury, Shamim A K ^a   Davis III, Robert T ^a   Kobayashi, Minae ^a   Monasky, Michelle M ^a   Rajan, Sudarsan ^b,c   Wolska, Beata M ^a   Gaponenko, Vadim ^a   Kobayashi, Tomoyoshi ^a   Wieczorek, David F ^b   Solaro, R John ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIAC FUNCTIONS; COILED-COIL STRUCTURE; DIASTOLIC DYSFUNCTION; HYDROPHOBIC RESIDUES; POST-TRANSLATIONAL MODIFICATIONS; REGULATORY FUNCTIONS; SPECTROSCOPY DATA; STRUCTURAL FLEXIBILITIES;

CALCIUM; DIFFERENTIAL SCANNING CALORIMETRY; HYDROPHOBICITY; MAMMALS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYSIOLOGY;

PHYSIOLOGICAL MODELS;

ALPHA TROPOMYOSIN; ASPARTIC ACID; LEUCINE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; DIFFERENTIAL SCANNING CALORIMETRY; HEART FUNCTION; HEART MUSCLE; HEART MUSCLE CELL; MOUSE; MUSCLE FIBER CONTRACTION; MYOFILAMENT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; SYSTOLIC DYSFUNCTION; THERMOSTABILITY; TRANSGENIC MOUSE;

ACTIN; CARDIAC MUSCLE; CARDIOVASCULAR DISEASE; FLEXIBILITY; MOUSE MODEL; MUSCLE; THIN FILAMENT; TRANSGENIC; TROPOMYOSIN; TROPONIN;

AMINO ACID SUBSTITUTION; ANIMALS; MICE; MICE, TRANSGENIC; MUTATION, MISSENSE; MYOCARDIAL CONTRACTION; MYOCARDIUM; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STABILITY; RATS; STROKE VOLUME; STRUCTURE-ACTIVITY RELATIONSHIP; TROPOMYOSIN;

MUS MUSCULUS;

EID: 84878750420     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.458695     Document Type: Article

References (56)

1. Parry, D. A., and Squire, J. M. (1973) Structural role of tropomyosin in muscle regulation. Analysis of the x-ray diffraction patterns from relaxed and contracting muscles. J. Mol. Biol. 75, 33-55
2. Haselgrove, J. C. (1973) X-ray evidence for a conformational change in the actin-containing filaments of vertebrate striated muscle. Cold Spring Harb. Symp. Quant. Biol. 37, 341-352
3. Lehman, W., Hatch, V., Korman, V., Rosol, M., Thomas, L., Maytum, R., Geeves, M. A., Van Eyk, J. E., Tobacman, L. S., and Craig, R. (2000) Tropomyosin and actin isoforms modulate the localization of tropomyosin strands on actin filaments. J. Mol. Biol. 302, 593-606
4. Vibert, P., Craig, R., and Lehman, W. (1997) Steric-model for activation of muscle thin filaments. J. Mol. Biol. 266, 8-14 (Pubitemid 27170513)
5. McKillop, D. F., and Geeves, M. A. (1993) Regulation of the interaction between actin and myosin subfragment-1. Evidence for 3 states of the thin filament. Biophys. J. 65, 693-701 (Pubitemid 23263882)
6. Straussman, R., Ben-Ya'acov, A., Woolfson, D. N., and Ravid, S. (2007) Kinking the coiled coil-negatively charged residues at the coiled-coil interface. J. Mol. Biol. 366, 1232-1242 (Pubitemid 46186385)
7. Chen, Y., and Lehrer, S. S. (2004) Distances between tropomyosin sites across the muscle thin filament using luminescence resonance energy transfer. Evidence for tropomyosin flexibility. Biochemistry 43, 11491-11499 (Pubitemid 39186970)
8. Singh, A., and Hitchcock-DeGregori, S. E. (2003) Local destabilization of the tropomyosin coiled coil gives the molecular flexibility required for actin binding. Biochemistry 42, 14114-14121 (Pubitemid 37499407)
9. Singh, A., and Hitchcock-DeGregori, S. E. (2006) Dual requirement for flexibility and specificity for binding of the coiled-coil tropomyosin to its target, actin. Structure 14, 43-50 (Pubitemid 43350072)
10. Nitanai, Y., Minakata, S., Maéda, K., Oda, N., and Maeda, Y. (2007) Crystal structures of tropomyosin. Flexible coiled-coil. Adv. Exp. Med. Biol. 592, 137-151
11. Sumida, J. P., Wu, E., and Lehrer, S. S. (2008) Conserved Asp-137 imparts flexibility to tropomyosin and affects function. J. Biol. Chem. 283, 6728-6734
12. Nevzorov, I. A., Nikolaeva, O. P., Kainov, Y. A., Redwood, C. S., and Levitsky, D. I. (2011) Conserved noncanonical residue Gly-126 confers instability to the middle part of the tropomyosin molecule. J. Biol. Chem. 286, 15766-15772
13. Monteiro, P. B., Lataro, R. C., Ferro, J. A., and Reinach Fde, C. (1994) Functional α-tropomyosin produced in Escherichia coli. A dipeptide extension can substitute the amino-terminal acetyl group. J. Biol. Chem. 269, 10461-10466
14. Gill, S. C., and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326 (Pubitemid 19277112)
15. Means, G. E., and Feeney, R. E. (1968) Reductive alkylation of amino groups in proteins. Biochemistry 7, 2192-2201
16. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe. A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
17. Kremneva, E., Boussouf, S., Nikolaeva, O., Maytum, R., Geeves, M. A., and Levitsky, D. I. (2004) Effects of two familial hypertrophic cardiomyopathy mutations in α-tropomyosin, Asp175Asn and Glu180Gly, on the thermal unfolding of actin-bound tropomyosin. Biophys. J. 87, 3922-3933 (Pubitemid 39602898)
18. Subramaniam, A., Jones, W. K., Gulick, J., Wert, S., Neumann, J., and Robbins, J. (1991) Tissue-specific regulation of the α-myosin heavy chain gene promoter in transgenic mice. J. Biol. Chem. 266, 24613-24620 (Pubitemid 21908985)
19. Muthuchamy, M., Grupp, I. L., Grupp, G., O'Toole, B. A., Kier, A. B., Boivin, G. P., Neumann, J., and Wieczorek, D. F. (1995) Molecular and physiological effects of overexpressing striated muscle β-tropomyosin in the adult murine heart. J. Biol. Chem. 270, 30593-30603
20. Gaffin, R. D., Peña, J. R., Alves, M. S., Dias, F. A., Chowdhury, S. A., Heinrich, L. S., Goldspink, P. H., Kranias, E. G., Wieczorek, D. F., and Wolska, B. M. (2011) Long-term rescue of a familial hypertrophic cardiomyopathy caused by a mutation in the thin filament protein, tropomyosin, via modulation of a calcium cycling protein. J. Mol. Cell Cardiol. 51, 812-820
21. Lang, R. M., Bierig, M., Devereux, R. B., Flachskampf, F. A., Foster, E., Pellikka, P. A., Picard, M. H., Roman, M. J., Seward, J., Shanewise, J. S., Solomon, S. D., Spencer, K. T., Sutton, M. S., and Stewart, W. J. (2005) Recommendations for chamber quantification. A report from the American Society of Echocardiography's Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J. Am. Soc. Echocardiogr. 18, 1440-1463 (Pubitemid 41821197)
22. Nagueh, S. F., Appleton, C. P., Gillebert, T. C., Marino, P. N., Oh, J. K., Smiseth, O. A., Waggoner, A. D., Flachskampf, F. A., Pellikka, P. A., and Evangelisa, A. (2009) Recommendations for the evaluation of left ventricular diastolic function by echocardiography. Eur. J. Echocardiogr. 10, 165-193
23. Wolska, B. M., and Solaro, R. J. (1996) Method for isolation of adult mouse cardiac myocytes for studies of contraction and microfluorimetry. Am. J. Physiol. 271, H1250-H1255
24. Louch, W. E., Sheehan, K. A., and Wolska, B. M. (2011) Methods in cardiomyocyte isolation, culture, and gene transfer. J. Mol. Cell Cardiol. 51, 288-298
25. 2+ and altered dynamics of contraction and relaxation in transgenic cardiac cells expressing β-tropomyosin. Circulation 98, 465-465
26. Brandt, P. W., Roemer, D., and Schachat, F. H. (1990) Co-operative activation of skeletal muscle thin filaments by rigor crossbridges. The effect of troponin C extraction. J. Mol. Biol. 212, 473-480
27. Fabiato, A. (1988) Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol. 157, 378-417
28. Godt, R. E., and Lindley, B. D. (1982) Influence of temperature upon contractile activation and isometric force production in mechanically skinned muscle-fibers of the frog. J. Gen. Physiol. 80, 279-297 (Pubitemid 12046029)
29. Scruggs, S. B., Hinken, A. C., Thawornkaiwong, A., Robbins, J., Walker, L. A., de Tombe, P. P., Geenen, D. L., Buttrick, P. M., and Solaro, R. J. (2009) Ablation of ventricular myosin regulatory light chain phosphorylation in mice causes cardiac dysfunction in situ and affects neighboring myofilament protein phosphorylation. J. Biol. Chem. 284, 5097-5106
30. Warren, C. M., Arteaga, G. M., Rajan, S., Ahmed, R. P., Wieczorek, D. F., and Solaro, R. J. (2008) Use of 2-D DIGE analysis reveals altered phosphorylation in a tropomyosin mutant (Glu54Lys) linked to dilated cardiomyopathy. Proteomics 8, 100-105
31. Yuan, C., Sheng, Q., Tang, H., Li, Y., Zeng, R., and Solaro, R. J. (2008) Quantitative comparison of sarcomeric phosphoproteomes of neonatal and adult rat hearts. Am. J. Physiol. Heart Circ. Physiol. 295, H647-H656
32. Kirk, J. A., MacGowan, G. A., Evans, C., Smith, S. H., Warren, C. M., Mamidi, R., Chandra, M., Stewart, A. F., Solaro, R. J., and Shroff, S. G. (2009) Left ventricular and myocardial function in mice expressing constitutively pseudophosphorylated cardiac troponin I. Circ. Res. 105, 1232-1239
33. Warren, C. M., and Greaser, M. L. (2003) Method for cardiac myosin heavy chain separation by sodium dodecyl sulfate gel electrophoresis. Anal. Biochem. 320, 149-151 (Pubitemid 36937078)
34. Kobayashi, T., Patrick, S. E., and Kobayashi, M. (2009) Ala Scanning of the inhibitory region of cardiac troponin I. J. Biol. Chem. 284, 20052-20060
35. Wider, G., and Wüthrich, K. (1999) NMR spectroscopy of large molecules and multimolecular assemblies in solution. Curr. Opin. Struct. Biol. 9, 594-601 (Pubitemid 29460586)
36. Gerken, T. A., Jentoft, J. E., Jentoft, N., and Dearborn, D. G. (1982) Intramolecular interactions of amino groups in 13C reductively methylated hen egg-white lysozyme. J. Biol. Chem. 257, 2894-2900
37. Kurinov, I. V., Mao, C., Irvin, J. D., and Uckun, F. M. (2000) X-ray crystallographic analysis of pokeweed antiviral protein-II after reductive methylation of lysine residues. Biochem. Biophys. Res. Commun. 275, 549-552
38. Rayment, I. (1997) Reductive alkylation of lysine residues to alter crystallization properties of proteins. Methods Enzymol. 276, 171-179
39. Potekhin, S. A., and Privalov, P. L. (1982) Co-operative blocks in tropomyosin. J. Mol. Biol. 159, 519-535
40. Sturtevant, J. M., Holtzer, M. E., and Holtzer, A. (1991) A scanning calorimetric study of the thermally induced unfolding of various forms of tropomyosin. Biopolymers 31, 489-495
41. Williams, D. L., Jr., and Swenson, C. A. (1981) Tropomyosin stability. Assignment of thermally induced conformational transitions to separate regions of the molecule. Biochemistry 20, 3856-3864
42. Nixon, B. R., Liu, B., Scellini, B., Tesi, C., Piroddi, N., Ogut, O., John Solaro, R., Ziolo, M. T., Janssen, P. M., Davis, J. P., Poggesi, C., and Biesiadecki, B. J. (2012) Tropomyosin Ser-283 pseudo-phosphorylation slows myofibril relaxation. Arch. Biochem. Biophys., doi: 10.1016/j.abb.2012.11.010
43. Schulz, E. M., Correll, R. N., Sheikh, H. N., Lofrano-Alves, M. S., Engel, P. L., Newman, G., Schultz Jel, J., Molkentin, J. D., Wolska, B. M., Solaro, R. J., and Wieczorek, D. F. (2012) Tropomyosin dephosphorylation results in compensated cardiac hypertrophy. J. Biol. Chem. 287, 44478-44489
44. Nadal-Ginard, B., and Mahdavi, V. (1989) Molecular basis of cardiac performance. Plasticity of the myocardium generated through protein isoform switches. J. Clin. Invest. 84, 1693-1700 (Pubitemid 20016170)
45. Rajan, S., Ahmed, R. P., Jagatheesan, G., Petrashevskaya, N., Boivin, G. P., Urboniene, D., Arteaga, G. M., Wolska, B. M., Solaro, R. J., Liggett, S. B., and Wieczorek, D. F. (2007) Dilated cardiomyopathy mutant tropomyosin mice develop cardiac dysfunction with significantly decreased fractional shortening and myofilament calcium sensitivity. Circ. Res. 101, 205-214 (Pubitemid 47196588)
46. Loong, C. K., Zhou, H. X., and Chase, P. B. (2012) Familial hypertrophic cardiomyopathy related E180G mutation increases flexibility of human cardiac α-tropomyosin. FEBS Lett. 586, 3503-3507
47. 2+ sensitivity and tropomyosin N-domain flexibility. J. Biol. Chem. 278, 41742-41748
48. Solaro, R. J., Henze, M., and Kobayashi, T. (2013) Integration of troponin I phosphorylation with cardiac regulatory networks. Circ. Res. 112, 355-366
49. Dubois, E., Richard, V., Mulder, P., Lamblin, N., Drobecq, H., Henry, J. P., Amouyel, P., Thuillez, C., Bauters, C., and Pinet, F. (2011) Decreased serine 207 phosphorylation of troponin T as a biomarker for left ventricular remodelling after myocardial infarction. Eur. Heart J. 32, 115-123
50. Scruggs, S. B., and Solaro, R. J. (2011) The significance of regulatory light chain phosphorylation in cardiac physiology. Arch. Biochem. Biophys. 510, 129-134
51. James, J., and Robbins, J. (2011) Signaling and myosin-binding protein C. J. Biol. Chem. 286, 9913-9919
52. Krenz, M., and Robbins, J. (2004) Impact of β-myosin heavy chain expression on cardiac function during stress. J. Am. Coll. Cardiol. 44, 2390-2397 (Pubitemid 39647615)
53. Korte, F. S., Herron, T. J., Rovetto, M. J., and McDonald, K. S. (2005) Power output is linearly related to MyHC content in rat skinned myocytes and isolated working hearts. Am. J. Physiol. Heart Circ. Physiol. 289, H801-H812 (Pubitemid 41129398)
54. Sun, Y. B., and Irving, M. (2010) The molecular basis of the steep force-calcium relation in heart muscle. J. Mol. Cell Cardiol. 48, 859-865
55. Solaro, R. J. (2009) Maintaining cooperation among cardiac myofilament proteins through thick and thin. J. Physiol. 587, 3
56. 2+-dependent photocrosslinking of tropomyosin residue 146 to residues 157-163 in the C-terminal domain of troponin I in reconstituted skeletal muscle thin filaments. J. Mol. Biol. 389, 575-583