Length-dependent activation is modulated by cardiac troponin I bisphosphorylation at Ser23 and Ser24 but not by Thr143 phosphorylation

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 306, Issue 8, 2014, Pages

  Wijnker, Paul J M ^a   Sequeira, Vasco ^a   Foster, D Brian ^b   Li, Yuejin ^b   dos Remedios, Cristobal G ^c   Murphy, Anne M ^b   Stienen, Ger J M ^a,d   van der Velden, Jolanda ^a,e  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF SYDNEY   (Australia)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

^e ROYAL NETHERLANDS ACADEMY OF ARTS AND SCIENCES   (Netherlands)

Author keywords

Myofilament function; Protein phosphorylation; Troponin I

Indexed keywords

ALANINE; ASPARTIC ACID; CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; SERINE; THREONINE; TROPONIN I;

ARTICLE; CELL ACTIVATION; FORCE; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; LENGTH DEPENDENT MYOFILAMENT ACTIVATION; MEMBRANE PERMEABILITY; MODULATION; MYOFILAMENT; PHOSPHORYLATION AND DEPHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

MYOFILAMENT FUNCTION; PROTEIN PHOSPHORYLATION; TROPONIN I;

CALCIUM; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FEMALE; HUMANS; MALE; MIDDLE AGED; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; MYOFIBRILS; PHOSPHORYLATION; PHOSPHOSERINE; PHOSPHOTHREONINE; PROTEIN KINASE C; SARCOMERES; TROPONIN I;

EID: 84900827918     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00580.2013     Document Type: Article

References (44)

1. Allen DG, Kentish JC. The cellular basis of the length-tension relation in cardiac muscle. J Mol Cell Cardiol 17: 821-840, 1985.
2. Arteaga GM, Palmiter KA, Leiden JM, Solaro RJ. Attenuation of length dependence of calcium activation in myofilaments of transgenic mouse hearts expressing slow skeletal troponin I. J Physiol 526: 541-549, 2000.
3. Bers DM. Cardiac excitation-contraction coupling. Nature 415: 198-205, 2002.
4. Bodor GS, Oakeley AE, Allen PD, Crimmins DL, Ladenson JH, Anderson PA. Troponin I phosphorylation in the normal and failing adult human heart. Circulation 96: 1495-1500, 1997.
5. 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 278: 11265-11272, 2003.
6. Cazorla O, Szilagyi S, Vignier N, Salazar G, Krämer E, Vassort G, Carrier L, Lacampagne A. Length and protein kinase A modulations of myocytes in cardiac myosin binding protein C-deficient mice. Cardiovasc Res 69: 370-380, 2006.
7. de Tombe PP, Mateja RD, Tachampa K, Ait MY, Farman GP, Irving TC. Myofilament length dependent activation. J Mol Cell Cardiol 48: 851-858, 2010.
8. Fuchs F, Martyn DA. Length-dependent Ca(2+) activation in cardiac muscle: some remaining questions. J Muscle Res Cell Motil 26: 199-212, 2005.
9. Fukuda N, Wu Y, Farman G, Irving TC, Granzier H. Titin isoform variance and length dependence of activation in skinned bovine cardiac muscle. J Physiol 553: 147-154, 2003.
10. Hamdani N, Borbely A, Veenstra SP, Kooij V, Vrydag W, Zaremba R, dos Remedios CG, Niessen HW, Michel MC, Paulus WJ, Stienen GJ, van der Velden J. More severe cellular phenotype in human idiopathic dilated cardiomyopathy compared to ischemic heart disease. J Muscle Res Cell Motil 31: 289-301, 2010.
11. Hanft LM, Biesiadecki BJ, McDonald KS. Length dependence of striated muscle force generation is controlled by phosphorylation of cTnI at Serines 23/24. J Physiol 2013.
12. Hanft LM, McDonald KS. Length dependence of force generation exhibit similarities between rat cardiac myocytes and skeletal muscle fibres. J Physiol 588: 2891-2903, 2010.
13. Holubarsch C, Ruf T, Goldstein DJ, Ashton RC, Nickl W, Pieske B, Pioch K, Ludemann J, Wiesner S, Hasenfuss G, Posival H, Just H, Burkhoff D. Existence of the Frank-Starling mechanism in the failing human heart. Investigations on the organ, tissue, and sarcomere levels. Circulation 94: 683-689, 1996.
14. Kajiwara H, Morimoto S, Fukuda N, Ohtsuki I, Kurihara S. Effect of troponin I phosphorylation by protein kinase A on length-dependence of tension activation in skinned cardiac muscle fibers. Biochem Biophys Res Commun 272: 104-110, 2000.
15. Kobayashi T, Yang X, Walker LA, Van Breemen RB, Solaro RJ. A non-equilibrium isoelectric focusing method to determine states of phosphorylation of cardiac troponin I: identification of Ser-23 and Ser-24 as significant sites of phosphorylation by protein kinase C. J Mol Cell Cardiol 38: 213-218, 2005.
16. Konhilas JP, Irving TC, Wolska BM, Jweied EE, Martin AF, Solaro RJ, de Tombe PP. Troponin I in the murine myocardium: influence on length-dependent activation and interfilament spacing. J Physiol 547: 951-961, 2003.
17. 2+ sensitivity in human myocardium. Basic Res Cardiol 105: 289-300, 2010.
18. Messer AE, Gallon CE, McKenna WJ, dos Remedios CG, Marston SB. The use of phosphate-affinity SDS-PAGE to measure the cardiac troponin I phosphorylation site distribution in human heart muscle. Proteomics Clin Appl 3: 1371-1382, 2009.
19. Monasky MM, Taglieri DM, Jacobson AK, Haizlip KM, Solaro RJ, Janssen PM. Posttranslational modifications of myofilament proteins involved in length-dependent prolongation of relaxation in rabbit right ventricular myocardium. Arch Biochem Biophys 535: 22-29, 2013.
20. Montgomery DE, Rundell VL, Goldspink PH, Urboniene D, Geenen DL, de Tombe PP, Buttrick PM. Protein kinase C epsilon induces systolic cardiac failure marked by exhausted inotropic reserve and intact Frank-Starling mechanism. Am J Physiol Heart Circ Physiol 289: H1881-H1888, 2005.
21. Nagueh SF, Shah G, Wu Y, Torre-Amione G, King NM, Lahmers S, Witt CC, Becker K, Labeit S, Granzier HL. Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy. Circulation 110: 155-162, 2004.
22. Narolska NA, Piroddi N, Belus A, Boontje NM, Scellini B, Deppermann S, Zaremba R, Musters RJ, dos Remedios CG, Jaquet K, Foster DB, Murphy AM, van Eyk JE, Tesi C, Poggesi C, van der Velden J, Stienen GJM. Impaired diastolic function after exchange of endogenous troponin I with C-terminal truncated troponin I in human cardiac muscle. Circ Res 99: 1012-1020, 2006.
23. Neagoe C, Kulke M, del Monte F, Gwathmey JK, de Tombe PP, Hajjar RJ, Linke WA. Titin isoform switch in ischemic human heart disease. Circulation 106: 1333-1341, 2002.
24. Nixon BR, Thawornkaiwong A, Jin J, Brundage EA, Little SC, Davis JP, Solaro RJ, Biesiadecki BJ. AMP-activated protein kinase phosphorylates cardiac troponin I at Ser-150 to increase myofilament calcium sensitivity and blunt PKA-dependent function. J Biol Chem 287: 19136-19147, 2012.
25. Noland TA Jr, Raynor RL, Kuo JF. Identification of sites phosphorylated in bovine cardiac troponin I and troponin T by protein kinase C and comparative substrate activity of synthetic peptides containing the phosphorylation sites. J Biol Chem 264: 20778-20785, 1989.
26. 2+ activation of cardiac myofilaments and the end-systolic pressure-volume relation. J Muscle Res Cell Motil 28: 415-419, 2007.
27. Rain S, Handoko ML, Trip P, Gan CT, Westerhof N, Stienen GJM, Paulus WJ, Ottenheijm CA, Marcus JT, Dorfmüller P, Guignabert C, Humbert M, Macdonald P, Dos Remedios C, Postmus PE, Saripalli C, Hidalgo CG, Granzier HL, Vonk-Noordegraaf A, van der Velden J, de Man FS. Right ventricular diastolic impairment in patients with pulmonary arterial hypertension. Circulation 128: 2016-2025, 2013.
28. Rao VS, Korte FS, Razumova MV, Feest ER, Hsu H, Irving TC, Regnier M, Martyn DA. N-terminal phosphorylation of cardiac troponin-I reduces length-dependent calcium sensitivity of contraction in cardiac muscle. J Physiol 591: 475-490, 2013.
29. Ross J Jr, Braunwald E. Studies on starling's law of the heart. IX. The effects of impeding venous return on performance of the normal and failing human left ventricle. Circulation 30: 719-727, 1964.
30. Schwinger RH, Bohm M, Koch A, Schmidt U, Morano I, Eissner HJ, Uberfuhr P, Reichart B, Erdmann E. The failing human heart is unable to use the Frank-Starling mechanism. Circ Res 74: 959-969, 1994.
31. Sequeira V, Wijnker PJ, Nijenkamp LL, Kuster DW, Najafi A, Witjas-Paalberends R, Regan JA, Boontje N, ten Cate FJ, Germans T, Carrier L, Sadayappan S, van Slegtenhorst MA, Zaremba R, Foster DB, Murphy A, Poggesi C, dos Remedios CG, Stienen GJ, Ho CY, Michels M, van der Velden J. Perturbed length-dependent activation in human hypertrophic cardiomyopathy with missense sarcomeric gene mutations. Circ Res 112: 1491-1505, 2013.
32. Sumandea MP, Burkart EM, Kobayashi T, de Tombe PP, Solaro RJ. Molecular and integrated biology of thin filament protein phosphorylation in heart muscle. Ann NY Acad Sci 1015: 39-52, 2004.
33. Tachampa K, Wang H, Farman GP, de Tombe PP. Cardiac troponin I threonine 144: role in myofilament length dependent activation. Circ Res 101: 1081-1083, 2007.
34. ter Keurs HE, Rijnsburger WH, van Heuningen R, Nagelsmit MJ. Tension development and sarcomere length in rat cardiac trabeculae. Evidence of length-dependent activation. Circ Res 46: 703-714, 1980.
35. van der Velden J. Diastolic myofilament dysfunction in the failing human heart. Pflügers Arch 462: 155-163, 2011.
36. 2+-sensitivity of the contractile apparatus in end-stage human heart failure results from altered phosphorylation of contractile proteins. Cardiovasc Res 57: 37-47, 2003.
37. Verduyn SC, Zaremba R, van der Velden J, Stienen GJM. Effects of contractile protein phosphorylation on force development in permeabilized rat cardiac myocytes. Basic Res Cardiol 102: 476-487, 2007.
38. 2+ by phosphorylating troponin I on threonine-144. J Mol Cell Cardiol 41: 823-833, 2006.
39. Wijnker PJM, Foster DB, Tsao AL, Frazier AH, dos Remedios CG, Murphy AM, Stienen GJM, van der Velden J. Impact of site-specific phosphorylation of protein kinase A sites Ser23 and Ser24 of cardiac troponin I in human cardiomyocytes. Am J Physiol Heart Circ Physiol 304: H260-H268, 2013.
40. Williamson MP. The structure and function of proline-rich regions in proteins. Biochem J 297: 249-260, 1994.
41. Zaremba R, Merkus D, Hamdani N, Lamers JM, Paulus WJ, dos Remedios CG, Duncker DJ, Stienen GJ, van der Velden J. Quantitative analysis of myofilament protein phosphorylation in small cardiac biopsies. Proteomics Clin Appl 1: 1285-1290, 2007.
42. Zhang J, Guy MJ, Norman HS, Chen YC, Xu Q, Dong X, Guner H, Wang S, Kohmoto T, Young KH, Moss RL, Ge Y. Top-down quantitative proteomics identified phosphorylation of cardiac troponin I as a candidate biomarker for chronic heart failure. J Proteome Res 10: 4054-4065, 2011.
43. Zhang P, Kirk JA, Ji W, dos Remedios CG, Kass DA, van Eyk JE, Murphy AM. Multiple reaction monitoring to identify site-specific troponin I phosphorylated residues in the failing human heart. Circulation 126: 1828-1837, 2012.
44. 2+ affinity of cardiac troponin C. J Biol Chem 270: 30773-30780, 1995.