Binding of myosin binding protein-C to myosin subfragment S2 affects contractility independent of a tether mechanism

Circulation Research

Volumn 95, Issue 9, 2004, Pages 930-936

  Harris, Samantha P ^a   Rostkova, Elena ^b   Gautel, Mathias ^b   Moss, Richard L ^c  

^a University of Washington   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Ca2+ sensitization; Cardiac muscle; Cardiac myocytes; Cardiomyopathy; Myocardial contractility; Transgenic mice

Indexed keywords

CALCIUM ION; MYOSIN BINDING PROTEIN C; MYOSIN SUBFRAGMENT; MYOSIN SUBFRAGMENT 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CARDIOMYOPATHY; ENZYME PHOSPHORYLATION; FRAMESHIFT MUTATION; HEART MUSCLE CONTRACTILITY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SKINNED MUSCLE FIBER; TRANSGENIC MOUSE;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALCIUM; CARRIER PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; MALE; MICE; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; MYOSIN SUBFRAGMENTS; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 7244245537     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000147312.02673.56     Document Type: Article

References (41)

1. Offer G, Moos C, Starr R. A new protein of the thick filaments of vertebrate skeletal myofibrils. Extractions, purification, and characterization. J Mol Biol. 1973;74:653-676.
2. Starr R, Offer G. The interaction of C-protein with heavy meromyosin and subfragment-2. Biochem J. 1978;171:813-916.
3. Okagaki T, Weber FE, Fischman DA, Vaughan KT, Mikawa T, Reinach FC. The major myosin-binding domain of skeletal muscle MyBP-C (C protein) resides in the COOH-terminal, immunoglobulin C2 motif. J Cell Biol. 1993;123:619-626.
4. Moos C, Offer G, Starr R, Bennett P. Interaction of C-protein with myosin, myosin rod and light meromyosin. J Mol Biol. 1975;97:1-9.
5. Gautel M, Zuffardi O, Freiburg A, Labeit S. Phosphorylation switches specific for the cardiac isoform of myosin binding protein-C: a modulator of cardiac contraction? EMBO J. 1995;14:1952-1960.
6. Gruen M, Prinz H, Gautel M. cAPK-phosphorylation controls the interaction of the regulatory domain of cardiac myosin binding protein C with myosin-S2 in an on-off fashion. FEBS Lett. 1999;453:254-259.
7. Gruen M, Gautel M. Mutations in β-myosin S2 that cause familial hypertrophic cardiomyopathy (FHC) abolish the interaction with the regulatory domain of myosin-binding protein-C. J Mol Biol. 1999;286:933-949.
8. Hartzell HC. Phosphorylation of C-protein in intact amphibian cardiac muscle. Correlation between 32P incorporation and twitch relaxation. J Gen Physiol. 1984;83:563-588.
9. 2+-calmodulin- dependent protein kinases. J Biol Chem. 1984;259:15587-15596.
10. Jeacocke SA, England PJ. Phosphorylation of a myofibrillar protein of Mr 150 000 in perfused rat heart, and the tentative identification of this protein as C-protein. FEBS Lett. 1980;122:129-132.
11. 2+ activation. J Physiol. 1991;439:701-715.
12. 2+ sensitive tension due to partial extraction of C-protein from rat skinned cardiac myocytes and rabbit skeletal muscle fibers. J Gen Physiol. 1991;97:1141-1163.
13. Harris SP, Bartley CR, Hacker TA, McDonald KS, Douglas PS, Greaser ML, Powers PA, Moss RL. Hypertrophic cardiomyopathy in cardiac myosin binding protein-C knockout mice. Circ Res. 2002;90:594-601.
14. Korte FS, McDonald KS, Harris SP, Moss RL. Loaded shortening, power output, and rate of force redevelopment are increased with knockout of cardiac myosin binding protein-C. Circ Res. 2003;93:752-758.
15. Palmer BM, Georgakopoulos D, Janssen PM, Wang Y, Alpert NR, Belardi DF, Harris SP, Moss RL, Burgon PG, Seidman CE, Seidman JG, Maughan DW, Kass DA. Role of Cardiac Myosin Binding Protein C in Sustaining Left Ventricular Systolic Stiffening. Circ Res. 2004;94:1249-1255.
16. 2+ in intact rat ventricular myocytes. J Physiol. 2000;528:151-156.
17. Kunst G, Kress KR, Gruen M, Uttenweiler D, Gautel M, Fink RH. Myosin binding protein C, a phosphorylation-dependent force regulator in muscle that controls the attachment of myosin heads by its interaction with myosin S2. Circ Res. 2000;86:51-58.
18. Patel JR, Fitzsimons DP, Buck SH, Muthuchamy M, Wieczorek DF, Moss RL. PKA accelerates rate of force development in murine skinned myocardium expressing alpha- or beta-tropomyosin. Am J Physiol. 2001;280:H2732-H2739.
19. McDonald KS, Wolff MR, Moss RL. Force-velocity and power-load curves in rat skinned cardiac myocytes. J Phyisol. 1998;511:519-531.
20. O'Farrell PH. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975;250:4007-4021.
21. Tibbits G, Koziol BJ, Roberts NK, Baldwin KM, Barnard RJ. Adaptation of the rat myocardium to endurance training. J Appl Physiol. 1978;44:85-89.
22. Craig R, Offer G. The location of C-protein in rabbit skeletal muscle. Proc R Soc Lond B Biol Sci. 1976;192:451-461.
23. Kulikovskaya I, McClellan G, Flavigny J, Carrier L, Winegrad S. Effect of MyBP-C binding to actin on contractility in heart muscle. J Gen Physiol. 2003;122:761-774.
24. Sebillon P, Bonne G, Flavigny J, Venin S, Rouche A, Fiszman M, Vikstrom K, Leinwand L, Carrier L, Schwartz K. COOH-terminal truncated human cardiac MyBP-C alters myosin filament organization. C R Acad Sci III. 2001;324:251-260.
25. Squire JM, Luther PK, Knupp C. Structural evidence for the interaction of C-protein (MyBP-C) with actin and sequence identification of a possible actin-binding domain. J Mol Biol. 2003;331:713-724.
26. Strang KT, Sweitzer NK, Greaser ML, Moss RL. Beta-adrenergic receptor stimulation increases unloaded shortening velocity of skinned single ventricular myocytes from rats. Circ Res. 1994;74:542-549.
27. Fentzke RC, Buck SH, Patel JR, Lin H, Wolska BM, Stojanovic MO, Martin AF, Solaro RJ, Moss RL, Leiden JM. Impaired cardiomyocyte relaxation and diastolic function in transgenic mice expressing slow skeletal troponin 1 in the heart. J Physiol. 1999;517:143-157.
28. Westfall MV, Turner I, Albayya FP, Metzger JM. Troponin I chimera analysis of the cardiac myofilament tension response to protein kinase A. Am J Physiol Cell Physiol. 2001;280:C324-3C32.
29. Gu J, Xu S, Yu LC. A model of cross-bridge attachment to actin in the A*M*ATP state based on x-ray diffraction from permeabilized rabbit psoas muscle. Biophys J. 2002;82:2123-2133.
30. Harris SP, Heller WT, Greaser ML, Moss RL, Trewhella J. Solution structure of heavy meromyosin by small-angle scattering. J Biol Chem. 2003;278:6034-6040.
31. Knight PJ. Dynamic behaviour of the head-tail junction of myosin. J Mol Biol. 1996;255:269-274.
32. Richard P, Charron P, Carrier L, Ledeuil C, Cheav T, Pichereau C, Benaiche A, Isnard R, Dubourg O, Burban M, Gueffet JP, Millaire A, Desnos M, Schwartz K, Hainque B, Komajda M. Hypertrophic cardiomyopathy: distribution of disease genes, spectrum of mutations, and implications for a molecular diagnosis strategy. Circulation. 2003;107:2227-2232.
33. Erdmann J, Daehmlow S, Wischke S, Senyuva M, Werner U, Raible J, Tanis N, Dyachenko S, Hummel M, Hetzer R, Regitz-Zagrosek V. Mutation spectrum in a large cohort of unrelated consecutive patients with hypertrophic cardiomyopathy. Clin Genet. 2003;64:339-349.
34. Woo A, Rakowski H, Liew JC, Zhao MS, Liew CC, Parker TG, Zeller M, Wigle ED, Sole MJ. Mutations of the beta myosin heavy chain gene in hypertrophic cardiomyopathy: critical functional sites determine prognosis. Heart. 2003;89:1179-1185.
35. Bonne G, Carrier L, Richard P, Hainque B, Schwartz K. Familial hypertrophic cardiomyopathy: From mutations to functional defects. Circ Res. 1998;83:580-593.
36. Erdmann J, Raible J, Maki-Abadi J, Hummel M, Hammann J, Wollnik B, Frantz E, Fleck E, Hetzer R, Regitz-Zagrosek V. Spectrum of clinical phenotypes and gene variants in cardiac myosin-binding protein C mutation carriers with hypertrophic cardiomyopathy. J Am Coll Cardiol. 2001;38:322-330.
37. Moolman JA, Reith S, Uhl K, Bailey S, Gautel M, Jeschke B, Fischer C, Ochs J, McKenna WJ, Klues H, Vosberg H. A newly created splice donor site in exon 25 of the MyBP-C gene is responsible for inherited hypertrophic cardiomypathy with incomplete disease penetrance. Circulation. 2000;101:1396-1402.
38. Rottbauer W, Gautel M, Zehelein J, Labeit S, Franz WM, Fischer C, Vollrath B, Mall G, Dietz R, Kubler W, Katus HA. Novel splice donor site mutation in the cardiac myosin-binding protein-C gene in familial hypertropic cardiomyapothy. Characterization of cardiac transcript and protein. J Clin Invest. 1997;100:475-482.
39. Byers PH. Killing the messenger: new insights into nonsense-mediated mRNA decay. J Clin Invest. 2002;109:3-6.
40. Mendell JT, Dietz HC. When the message goes awry: disease-producing mutations that influence mRNA content and performance. Cell. 2001;107:411-414.
41. Yang Q, Sanbe A, Osinska H, Hewett TE, Klevitsky R, Robbins J. In vivo modeling of myosin binding protein C familial hypertrophic cardiomyopathy. Circ Res. 1999;85:841-847.