Protein kinase D is a novel mediator of cardiac troponin I phosphorylation and regulates myofilament function

Circulation Research

Volumn 95, Issue 11, 2004, Pages 1091-1099

  Haworth, Robert S ^a   Cuello, Friederike ^a   Herron, Todd J ^a   Franzen, Gereon ^b   Kentish, Jonathan C ^a   Gautel, Mathias ^a   Avkiran, Metin ^a,c  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^c ST THOMAS HOSPITAL   (United Kingdom)

Author keywords

Calcium sensitivity; Cardiac troponin I; Contractile function; Crossbridge cycling kinetics; Protein kinase D; Protein phosphorylation

Indexed keywords

CALCIUM; CYCLIC AMP DEPENDENT PROTEIN KINASE; MYOMESIN; MYOSIN BINDING PROTEIN C; PROTEIN; PROTEIN KINASE D; TELETHONIN; TROPONIN I; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; DNA FINGERPRINTING; ENZYME KINETICS; HEART MUSCLE CELL; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RAT; STOICHIOMETRY; WILD TYPE;

ADULT; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CALCIUM SIGNALING; CARRIER PROTEINS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA, COMPLEMENTARY; HUMANS; ISOMETRIC CONTRACTION; MALE; MICROFILAMENTS; MIDDLE AGED; MOLECULAR SEQUENCE DATA; MUSCLE PROTEINS; MUTAGENESIS, SITE-DIRECTED; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOCYTES, CARDIAC; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN KINASE C; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, WISTAR; RECOMBINANT FUSION PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; TROPONIN I; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 9344230851     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000149299.34793.3c     Document Type: Article

References (44)

1. Valverde AM, Sinnett-Smith J, Van Lint J, Rozengurt E. Molecular cloning and characterization of protein kinase D: a target for diacyl-glycerol and phorbol esters with a distinctive catalytic domain. Proc Natl Acad Sci USA. 1994;91:8572-8576.
2. Johannes F-J, Prestle J, Eis S, Oberhagemann P, Pfizenmaier K. PKCμ is a novel, atypical member of the protein kinase C family. J Biol Chem. 1994;269:6140-6148.
3. Rozengurt E, Sinnett-Smith J, Zugaza JL. Protein kinase D: a novel target for diacylglycerol and phorbol esters. Biochem Soc Trans. 1997;25:565-571.
4. Van Lint J, Sinnett-Smith J, Rozengurt E. Expression and characterization of PKD, a phorbol ester and diacylglycerol-stimulated serine protein kinase. J Biol Chem. 1995;270:1455-1461.
5. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. The protein kinase complement of the human genome. Science. 2002;298:1912-1934.
6. Zugaza JL, Sinnett-Smith J, Rozengurt E. Protein kinase D (PKD) activation in intact cells through a protein kinase C-dependent signal transduction pathway. EMBO J. 1996;15:6220-6230.
7. Sturany S, Van Lint J, Müller F, Wilda M, Hameister H, Höcker M, Brey A, Gern U, Vandenheede J, Gress T, Adler G, Seufferlein T. Molecular cloning and characterization of the human protein kinase D2. J Biol Chem. 2001;276:3310-3318.
8. Hayashi A, Seki N, Hattori A, Kozuma S, Saito T. PKCv, a new member of the protein kinase C family, composes a fourth subfamily with PKCμ. Biochim Biophys Acta. 1999;1450:99-106.
9. Rykx A, De Kimpe L, Mikhalap S, Vantus T, Seufferlein T, Vandenheede JR, Van Lint J. Protein kinase D: a family affair. FEBS Lett. 2003;546:81-86.
10. + exchanger activity. Am J Physiol Cell Physiol. 1999;277:C1202-C1209.
11. 1-adrenergic receptor- and protein kinase C-mediated regulation. J Mol Cell Cardiol. 2000;32:1013-1023.
12. Ward DG, Ashton PR, Trayer HR, Trayer IP. Additional PKA phosphorylation sites in human cardiac troponin I. Eur J Biochem. 2001;268:179-185.
13. Mayans O, van der Ven PF, Wilm M, Mues A, Young P, Furst DO, Wilmanns M, Gautel M. Structural basis for activation of the titin kinase domain during myofibrillogenesis. Nature. 1998;395:863-869.
14. 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.
15. Obermann WM, Gautel M, Weber K, Furst DO. Molecular structure of the sarcomeric M band: mapping of titin and myosin binding domains in myomesin and the identification of a potential regulatory phosphorylation site in myomesin. EMBO J. 1997;16:211-220.
16. Gautel M, Fürst DO, Cocco A, Schiaffino S. Isoform transitions of the myosin binding protein C family in developing human and mouse muscles: lack of isoform transcomplementation in cardiac muscle. Circ Res. 1998;82:124-129.
17. Mues A, van der Ven PF, Young P, Fürst DO, Gautel M. Two immunoglobulin-like domains of the Z-disc portion of titin interact in a conformation-dependent way with telethonin. FEBS Lett. 1998;428:111-114.
18. Obermann WM, Gautel M, Steiner F, van der Ven PF, Weber K, Fürst DO. The structure of the sarcomeric M band: localization of defined domains of myomesin, M-protein, and the 250-kD carboxy-terminal region of titin by immunoelectron microscopy. J Cell Biol. 1996;134:1441-1453.
19. McDonald KS, Wolff MR, Moss RL. Force-velocity and power-load curves in rat skinned cardiac myocytes. J Physiol. 1998;511:519-531.
20. Herron TJ, Korte FS, McDonald KS. Loaded shortening and power output in cardiac myocytes are dependent on myosin heavy chain isoform expression. Am J Physiol Heart Circ Physiol. 2001;281:H1217-H222.
21. Moss RL. Sarcomere length-tension relations of frog skinned muscle fibres during calcium activation at short lengths. J Physiol. 1979;292:177-192.
22. Brenner B, Eisenberg E. Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution. Proc Natl Acad Sci U S A. 1986;83:3542-3546.
23. 2+ activation and relaxation in rat and guinea pig skinned trabeculae. Circ Res. 1998;83:179-186.
24. Vertommen D, Rider M, Ni YP, Waelkens E, Merlevede W, Vandenheede JR, Van Lint J. Regulation of protein kinase D by multisite phosphorylation: identification of phosphorylation sites by mass spectrometry and characterization by site-directed mutagenesis. J Biol Chem. 2000;275:19567- 19576.
25. Obermann WM, Plessmann U, Weber K, Fürst DO. Purification and biochemical characterization of myomesin, a myosin-binding and titin-binding protein, from bovine skeletal muscle. Eur J Biochem. 1995;233:110-115.
26. Metzger JM, Westfall MV. Covalent and noncovalent modification of thin filament action: the essential role of troponin in cardiac muscle regulation. Circ Res. 2004;94:146-158.
27. Mittmann K, Jaquet K, Heilmeyer LM, Jr. Ordered phosphorylation of a duplicated minimal recognition motif for cAMP-dependent protein kinase present in cardiac troponin I. FEBS Lett. 1992;302:133-137.
28. 2+-stimulated MgATPase of reconstituted actomyosin S-1. J Biol Chem. 1995;270:25445-25454.
29. 2+ affinity of cardiac troponin C. J Biol Chem. 1995;270:30773-30780.
30. Solaro RJ, Burkart EM. Functional defects in troponin and the systems biology of heart failure. J Mol Cell Cardiol. 2002;34:689-693.
31. Burkart EM, Sumandea MP, Kobayashi T, Nili M, Martin AF, Homsher E, Solaro RJ. Phosphorylation or glutamic acid substitution at protein kinase C sites on cardiac troponin I differentially depress myofilament tension and shortening velocity. J Biol Chem. 2003;278:11265-11272.
32. Buscemi N, Foster DB, Neverova I, Van Eyk JE. p21-Activated kinase increases the calcium sensitivity of rat triton-skinned cardiac muscle fiber bundles via a mechanism potentially involving novel phosphorylation of troponin I. Circ Res. 2002;91:509-516.
33. Iglesias T, Cabrera-Poch N, Mitchell MP, Naven TJ, Rozengurt E, Schiavo G. Identification and cloning of Kidins220, a novel neuronal substrate of protein kinase D. J Biol Chem. 2000;275:40048-40056.
34. Wang Y, Waldron RT, Dhaka A, Patel A, Riley MM, Rozengurt E, Colicelli J. The RAS effector RIN1 directly competes with RAF and is regulated by 14-3-3 proteins. Mol Cell Biol. 2002;22:916-926.
35. Takimoto E, Soergel DG, Janssen PM, Stull LB, Kass DA, Murphy AM. Frequency- and afterload-dependent cardiac modulation in vivo by troponin I with constitutively active protein kinase A phosphorylation sites. Circ Res. 2004;94:496-504.
36. Zhang R, Zhao J, Mandveno A, Potter JD. Cardiac troponin 1 phosphorylation increases the rate of cardiac muscle relaxation. Circ Res. 1995; 76:1028-1035.
37. Patel JR, Fitzsimons DP, Buck SH, Muthuchamy M, Wieczorek DF, Moss RL. PKA accelerates rate of force development in murine skinned myocardium expressing α- or β-tropomyosin. Am J Physiol Heart Circ Physiol. 2001;280:H2732-H2739.
38. Kentish JC, McCloskey DT, Layland J, Palmer S, Leiden JM, Martin AF, Solaro RJ. Phosphorylation of troponin I by protein kinase A accelerates relaxation and crossbridge cycle kinetics in mouse ventricular muscle. Circ Res. 2001;88:1059-1065.
39. Herron TJ, Korte S, McDonald KS. Power output is increased after phosphorylation of myofibrillar proteins in rat skinned cardiac myocytes. Circ Res. 2001;89:1184-1190.
40. Layland J, Kentish JC. Myofilament-based relaxant effect of isoprenaline revealed during work-loop contractions in rat cardiac trabeculae. J Physiol. 2002;544:171-182.
41. Zugaza JL, Waldron RT, Sinnett-Smith J, Rozengurt E. Bombesin, vasopressin, endothelin, bradykinin, and platelet-derived growth factor rapidly activate protein kinase D through a protein kinase C-dependent signal transduction pathway. J Biol Chem. 1997;272:23952-23960.
42. Haworth RS, Avkiran M. Inhibition of protein kinase D by resveratrol. Biochem Phamacol. 2001;62:1647-1651.
43. 2+ sensitivity and ATPase activity in the mouse myocardium. J Physiol. 2003;552:845-857.
44. Westfall MV, Borton AR. Role of troponin I phosphorylation in protein kinase C-mediated enhanced contractile performance of rat myocytes. J Biol Chem. 2003;278:33694-33700.