Posttranslational modifications of cardiac troponin T: An overview

Journal of Molecular and Cellular Cardiology

Volumn 63, Issue , 2013, Pages 47-56

  Streng, Alexander S ^a   de Boer, Douwe ^a   van der Velden, Jolanda ^b   van Dieijen Visser, Marja P ^a   Wodzig, Will K W H ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Cardiac physiology; Cardiac troponin T; Fragmentation; Phosphorylation

Indexed keywords

APOPTOSIS SIGNAL REGULATING KINASE 1; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALPAIN 1; CASPASE 3; P21 ACTIVATED KINASE 3; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C DELTA; PROTEIN KINASE C EPSILON; PROTEIN KINASE C XI; RAF PROTEIN; SERINE; THREONINE; TROPONIN T; UNCLASSIFIED DRUG;

ACUTE HEART INFARCTION; AMINO ACID SEQUENCE; ENZYME PHOSPHORYLATION; HEART FAILURE; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVIEW;

ACUTE MYOCARDIAL INFARCTION; AMI; APOPTOSIS SIGNAL-REGULATING KINASE 1; ASK1; CA(2+)/CALMODULIN-DEPENDENT PROTEIN KINASE II; CAMK II; CARDIAC PHYSIOLOGY; CARDIAC TROPONIN T; CARDIAC TROPONIN T, I, C; CTNT/I/C; END-STAGE RENAL DISEASE; ESRD; FRAGMENTATION; GEL FILTRATION CHROMATOGRAPHY; GFC; HEART FAILURE; HF; INORGANIC PHOSPHATE; LEFT VENTRICLE; LV; MASS SPECTROMETRY; MS; P(I); P21 ACTIVATED KINASE 1, 3; PAK1/3; PHOSPHORYLATION; PKA/C/D; POSTTRANSLATIONAL MODIFICATION; PP1; PP2A, PROTEIN PHOSPHATASE 1, 2A; PROTEIN KINASE A, C, D; PTM; RHO-A-DEPENDENT PROTEIN KINASE; RIGHT VENTRICLE; ROCK-II; RV; TM; TROPOMYOSIN;

ANIMALS; HUMANS; MYOCARDIUM; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; TROPONIN T;

EID: 84881500542     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.07.004     Document Type: Review

References (116)

1. Farah C.S., Reinach F.C. The troponin complex and regulation of muscle contraction. FASEB J 1995, 9:755-767.
2. Filatov V.L., Katrukha A.G., Bulargina T.V., Gusev N.B. Troponin: structure, properties, and mechanism of functioning. Biochemistry (Mosc) 1999, 64:969-985.
3. Gomes A.V., Potter J.D., Szczesna-Cordary D. The role of troponins in muscle contraction. IUBMB Life 2002, 54:323-333.
4. Gordon A.M., Homsher E., Regnier M. Regulation of contraction in striated muscle. Physiol Rev 2000, 80:853-924.
5. Tardiff J.C. Thin filament mutations: developing an integrative approach to a complex disorder. Circ Res 2011, 108:765-782.
6. 2+ with cardiac pump regulation and pump dynamics. Adv Physiol Educ 1999, 277:S155-S163.
7. Hinken A.C., Solaro R.J. A dominant role of cardiac molecular motors in the intrinsic regulation of ventricular ejection and relaxation. Physiology (Bethesda) 2007, 22:73-80.
8. Barany M. ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol 1967, 50(Suppl.):197-218.
9. 2+-ATPase activity. Am J Physiol 1996, 270:C1271-C1276.
10. Moreira C.M., Meira E.F., Vestena L., Stefanon I., Vassallo D.V., Padilha A.S. Tension cost correlates with mechanical and biochemical parameters in different myocardial contractility conditions. Clinics (Sao Paulo) 2012, 67:489-496.
11. Sun Y.B., Irving M. The molecular basis of the steep force-calcium relation in heart muscle. J Mol Cell Cardiol 2010, 48:859-865.
12. Solaro R.J., Rarick H.M. Troponin and tropomyosin: proteins that switch on and tune in the activity of cardiac myofilaments. Circ Res 1998, 83:471-480.
13. Solaro R.J. Sarcomere control mechanisms and the dynamics of the cardiac cycle. J Biomed Biotechnol 2010, 2010:105648.
14. Solaro R.J., Kobayashi T. Protein phosphorylation and signal transduction in cardiac thin filaments. J Biol Chem 2011, 286:9935-9940.
15. Murphy A.M. Another new kinase targets troponin I. Circ Res 2004, 95:1043-1045.
16. Kuster D.W., Sequeira V., Najafi A., Boontje N.M., Wijnker P.J., Witjas-Paalberends E.R., et al. GSK3β phosphorylates newly identified site in the proline-alanine-rich region of cardiac myosin-binding protein C and alters cross-bridge cycling kinetics in human: short communication. Circ Res 2013, 112:633-639.
17. Dong X., Sumandea C.A., Chen Y.C., Garcia-Cazarin M.L., Zhang J., Balke C.W., et al. Augmented phosphorylation of cardiac troponin I in hypertensive heart failure. J Biol Chem 2012, 287:848-857.
18. Hamdani N., Kooij V., van Dijk S., Merkus D., Paulus W.J., Remedios C.D., et al. Sarcomeric dysfunction in heart failure. Cardiovasc Res 2008, 77:649-658.
19. Murphy A.M. Heart failure, myocardial stunning, and troponin: a key regulator of the cardiac myofilament. Congest Heart Fail 2006, 12:32-38. [quiz 9-40].
20. Labugger R., Organ L., Collier C., Atar D., Van Eyk J.E. Extensive troponin I and T modification detected in serum from patients with acute myocardial infarction. Circulation 2000, 102:1221-1226.
21. Kranias E.G., Solaro R.J. Phosphorylation of troponin I and phospholamban during catecholamine stimulation of rabbit heart. Nature 1982, 298:182-184.
22. Kentish J.C., McCloskey D.T., Layland J., Palmer S., Leiden J.M., Martin A.F., et al. Phosphorylation of troponin I by protein kinase A accelerates relaxation and crossbridge cycle kinetics in mouse ventricular muscle. Circ Res 2001, 88:1059-1065.
23. Wijnker P.J., Foster D.B., Tsao A.L., Frazier A.H., Dos Remedios C., Murphy A.M., et al. Impact of site-specific phosphorylation of the protein kinase A sites Ser23 and Ser24 of cardiac troponin I in human cardiomyocytes. Am J Physiol Heart Circ Physiol 2013, 304:H260-H268.
24. Zhang P., Kirk J.A., Ji W., Dos Remedios C.G., Kass D.A., Van Eyk J.E., et al. Multiple reaction monitoring to identify site-specific troponin I phosphorylated residues in the failing human heart. Circulation 2012, 126:1828-1837.
25. Walker L.A., Walker J.S., Ambler S.K., Buttrick P.M. Stage-specific changes in myofilament protein phosphorylation following myocardial infarction in mice. J Mol Cell Cardiol 2010, 48:1180-1186.
26. 2+-sensitivity in human myocardium depends on the phosphorylation background. J Mol Cell Cardiol 2010, 48:954-963.
27. Layland J., Solaro R.J., Shah A.M. Regulation of cardiac contractile function by troponin I phosphorylation. Cardiovasc Res 2005, 66:12-21.
28. Metzger J.M., Westfall M.V. Covalent and noncovalent modification of thin filament action: the essential role of troponin in cardiac muscle regulation. Circ Res 2004, 94:146-158.
29. Solaro R.J., Rosevear P., Kobayashi T. The unique functions of cardiac troponin I in the control of cardiac muscle contraction and relaxation. Biochem Biophys Res Commun 2008, 369:82-87.
30. Gaze D.C., Collinson P.O. Multiple molecular forms of circulating cardiac troponin: analytical and clinical significance. Ann Clin Biochem 2008, 45:349-355.
31. Solaro R.J., Henze M., Kobayashi T. Integration of troponin I phosphorylation with cardiac regulatory networks. Circ Res 2013, 112:355-366.
32. Anderson P.A., Malouf N.N., Oakeley A.E., Pagani E.D., Allen P.D. Troponin T isoform expression in humans. A comparison among normal and failing adult heart, fetal heart, and adult and fetal skeletal muscle. Circ Res 1991, 69:1226-1233.
33. Anderson P.A., Greig A., Mark T.M., Malouf N.N., Oakeley A.E., Ungerleider R.M., et al. Molecular basis of human cardiac troponin T isoforms expressed in the developing, adult, and failing heart. Circ Res 1995, 76:681-686.
34. Mesnard-Rouiller L., Mercadier J.J., Butler-Browne G., Heimburger M., Logeart D., Allen P.D., et al. Troponin T mRNA and protein isoforms in the human left ventricle: pattern of expression in failing and control hearts. J Mol Cell Cardiol 1997, 29:3043-3055.
35. Consortium U. Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 2012, 40:D71-D75.
36. Jain E., Bairoch A., Duvaud S., Phan I., Redaschi N., Suzek B.E., et al. Infrastructure for the life sciences: design and implementation of the UniProt website. BMC Bioinformatics 2009, 10:136.
37. Jin J.P., Chong S.M. Localization of the two tropomyosin-binding sites of troponin T. Arch Biochem Biophys 2010, 500:144-150.
38. 2+-saturated form. Nature 2003, 424:35-41.
39. Wei B., Jin J.P. Troponin T isoforms and posttranscriptional modifications: evolution, regulation and function. Arch Biochem Biophys 2011, 505:144-154.
40. Li M.X., Wang X., Sykes B.D. Structural based insights into the role of troponin in cardiac muscle pathophysiology. J Muscle Res Cell Motil 2004, 25:559-579.
41. Perry S.V. Troponin T: genetics, properties and function. J Muscle Res Cell Motil 1998, 19:575-602.
42. Gusev N.B., Barskaya N.V., Verin A.D., Duzhenkova I.V., Khuchua Z.A., Zheltova A.O. Some properties of cardiac troponin T structure. Biochem J 1983, 213:123-129.
43. Villar-Palasi C., Kumon A. Purification and properties of dog cardiac troponin T kinase. J Biol Chem 1981, 256:7409-7415.
44. King M.M., Carlson G.M. Interaction of phosphorylase kinase with the 2′,3′-dialdehyde derivative of adenosine triphosphate. 2. Differential inactivation measured with various protein substrates. Biochemistry 1981, 20:4387-4393.
45. 2+-dependent protein kinase. Biochem J 1983, 209:189-195.
46. 2+-dependent protein kinase and its inhibition by troponin C and tropomyosin. Biochem J 1984, 218:361-369.
47. Noland T.A., Raynor R.L., Kuo J.F. 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 1989, 264:20778-20785.
48. Swiderek K., Jaquet K., Meyer H.E., Schachtele C., Hofmann F., Heilmeyer L.M. Sites phosphorylated in bovine cardiac troponin T and I. Characterization by 31P NMR spectroscopy and phosphorylation by protein kinases. Eur J Biochem 1990, 190:575-582.
49. Jideama N.M., Noland T.A., Raynor R.L., Blobe G.C., Fabbro D., Kazanietz M.G., et al. Phosphorylation specificities of protein kinase C isozymes for bovine cardiac troponin I and troponin T and sites within these proteins and regulation of myofilament properties. J Biol Chem 1996, 271:23277-23283.
50. 2+-stimulated actomyosin MgATPase activity. J Biol Chem 1991, 266:4974-4978.
51. 2+-dependent actomyosin MgATPase activity and troponin T binding to tropomyosin-F-actin complex. Biochem J 1992, 288(Pt 1):123-129.
52. Sumandea M.P., Pyle W.G., Kobayashi T., de Tombe P.P., Solaro R.J. Identification of a functionally critical protein kinase C phosphorylation residue of cardiac troponin T. J Biol Chem 2003, 278:35135-35144.
53. Sumandea M.P., Burkart E.M., Kobayashi T., De Tombe P.P., Solaro R.J. Molecular and integrated biology of thin filament protein phosphorylation in heart muscle. Ann N Y Acad Sci 2004, 1015:39-52.
54. Montgomery D.E., Chandra M., Huang Q., Jin J., Solaro R.J. Transgenic incorporation of skeletal TnT into cardiac myofilaments blunts PKC-mediated depression of force. Am J Physiol Heart Circ Physiol 2001, 280:H1011-H1018.
55. Steinberg S.F. Cardiac actions of protein kinase C isoforms. Physiology (Bethesda) 2012, 27:130-139.
56. Wu S.C., Solaro R.J. Protein kinase C zeta. A novel regulator of both phosphorylation and de-phosphorylation of cardiac sarcomeric proteins. J Biol Chem 2007, 282:30691-30698.
57. Bogoyevitch M.A., Parker P.J., Sugden P.H. Characterization of protein kinase C isotype expression in adult rat heart. Protein kinase C-epsilon is a major isotype present, and it is activated by phorbol esters, epinephrine, and endothelin. Circ Res 1993, 72:757-767.
58. Steinberg S.F., Goldberg M., Rybin V.O. Protein kinase C isoform diversity in the heart. J Mol Cell Cardiol 1995, 27:141-153.
59. Even-Faitelson L., Ravid S. PAK1 and aPKCzeta regulate myosin II-B phosphorylation: a novel signaling pathway regulating filament assembly. Mol Biol Cell 2006, 17:2869-2881.
60. Buscemi N., Foster D.B., Neverova I., Van Eyk J.E. 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.
61. Ke Y., Wang L., Pyle W.G., de Tombe P.P., Solaro R.J. Intracellular localization and functional effects of P21-activated kinase-1 (Pak1) in cardiac myocytes. Circ Res 2004, 94:194-200.
62. Monasky M.M., Taglieri D.M., Patel B.G., Chernoff J., Wolska B.M., Ke Y., et al. p21-activated kinase improves cardiac contractility during ischemia-reperfusion concomitant with changes in troponin-T and myosin light chain 2 phosphorylation. Am J Physiol Heart Circ Physiol 2012, 302:H224-H230.
63. Oh J.G., Jeong D., Cha H., Kim J.M., Lifirsu E., Kim J., et al. PICOT increases cardiac contractility by inhibiting PKCzeta activity. J Mol Cell Cardiol 2012, 53:53-63.
64. Jideama N.M., Crawford B.H., Hussain A.K., Raynor R.L. Dephosphorylation specificities of protein phosphatase for cardiac troponin I, troponin T, and sites within troponin T. Int J Biol Sci 2006, 2:1-9.
65. Jaquet K., Fukunaga K., Miyamoto E., Meyer H.E. A site phosphorylated in bovine cardiac troponin T by cardiac CaM kinase II. Biochim Biophys Acta 1995, 1248:193-195.
66. Iwasa T., Inoue N., Fukunaga K., Isobe T., Okuyama T., Miyamoto E. Purification and characterization of a multifunctional calmodulin-dependent protein kinase from canine myocardial cytosol. Arch Biochem Biophys 1986, 248:21-29.
67. Gotoh Y., Cooper J.A. Reactive oxygen species- and dimerization-induced activation of apoptosis signal-regulating kinase 1 in tumor necrosis factor-alpha signal transduction. J Biol Chem 1998, 273:17477-17482.
68. He X., Liu Y., Sharma V., Dirksen R.T., Waugh R., Sheu S.S., et al. ASK1 associates with troponin T and induces troponin T phosphorylation and contractile dysfunction in cardiomyocytes. Am J Pathol 2003, 163:243-251.
69. Vahebi S., Kobayashi T., Warren C.M., de Tombe P.P., Solaro R.J. Functional effects of rho-kinase-dependent phosphorylation of specific sites on cardiac troponin. Circ Res 2005, 96:740-747.
70. Sumandea M.P., Vahebi S., Sumandea C.A., Garcia-Cazarin M.L., Staidle J., Homsher E. Impact of cardiac troponin T N-terminal deletion and phosphorylation on myofilament function. Biochemistry 2009, 48:7722-7731.
71. Pfleiderer P., Sumandea M.P., Rybin V.O., Wang C., Steinberg S.F. Raf-1: a novel cardiac troponin T kinase. J Muscle Res Cell Motil 2009, 30:67-72.
72. McDonough J.L., Van Eyk J.E. Developing the next generation of cardiac markers: disease-induced modifications of troponin I. Prog Cardiovasc Dis 2004, 47:207-216.
73. Marston S.B., Walker J.W. Back to the future: new techniques show that forgotten phosphorylation sites are present in contractile proteins of the heart whilst intensively studied sites appear to be absent. J Muscle Res Cell Motil 2009, 30:93-95.
74. Sancho Solis R., Ge Y., Walker J.W. Single amino acid sequence polymorphisms in rat cardiac troponin revealed by top-down tandem mass spectrometry. J Muscle Res Cell Motil 2008, 29:203-212.
75. Zhang J., Zhang H., Ayaz-Guner S., Chen Y.C., Dong X., Xu Q., et al. Phosphorylation, but not alternative splicing or proteolytic degradation, is conserved in human and mouse cardiac troponin T. Biochemistry 2011, 50:6081-6092.
76. 2+-sensitive isoforms in the failing human heart. Circulation 1999, 99:384-391.
77. Noguchi T., Hunlich M., Camp P.C., Begin K.J., El-Zaru M., Patten R., et al. Thin-filament-based modulation of contractile performance in human heart failure. Circulation 2004, 110:982-987.
78. Goldspink P.H., Montgomery D.E., Walker L.A., Urboniene D., McKinney R.D., Geenen D.L., et al. Protein kinase Cepsilon overexpression alters myofilament properties and composition during the progression of heart failure. Circ Res 2004, 95:424-432.
79. 2+-sensitivity of the contractile apparatus in end-stage human heart failure results from altered phosphorylation of contractile proteins. Cardiovasc Res 2003, 57:37-47.
80. Messer A.E., Jacques A.M., Marston S.B. Troponin phosphorylation and regulatory function in human heart muscle: dephosphorylation of Ser23/24 on troponin I could account for the contractile defect in end-stage heart failure. J Mol Cell Cardiol 2007, 42:247-259.
81. Belin R.J., Sumandea M.P., Sievert G.A., Harvey L.A., Geenen D.L., Solaro R.J., et al. Interventricular differences in myofilament function in experimental congestive heart failure. Pflugers Arch 2011, 462:795-809.
82. Kameyama T., Chen Z., Bell S.P., VanBuren P., Maughan D., LeWinter M.M. Mechanoenergetic alterations during the transition from cardiac hypertrophy to failure in Dahl salt-sensitive rats. Circulation 1998, 98:2919-2929.
83. Noguchi T., Kihara Y., Begin K.J., Gorga J.A., Palmiter K.A., LeWinter M.M., et al. Altered myocardial thin-filament function in the failing Dahl salt-sensitive rat heart: amelioration by endothelin blockade. Circulation 2003, 107:630-635.
84. Hamdani N., de Waard M., Messer A.E., Boontje N.M., Kooij V., van Dijk S., et al. Myofilament dysfunction in cardiac disease from mice to men. J Muscle Res Cell Motil 2008, 29:189-201.
85. 2+-sensitivity in heart failure: increased or decreased?. J Mol Cell Cardiol 2008, 45:603-607.
86. Avner B.S., Shioura K.M., Scruggs S.B., Grachoff M., Geenen D.L., Helseth D.L., et al. Myocardial infarction in mice alters sarcomeric function via post-translational protein modification. Mol Cell Biochem 2012, 363:203-215.
87. van der Velden J., Merkus D., de Beer V., Hamdani N., Linke W.A., Boontje N.M., et al. Transmural heterogeneity of myofilament function and sarcomeric protein phosphorylation in remodeled myocardium of pigs with a recent myocardial infarction. Front Physiol 2011, 2:83.
88. Dubois E., Richard V., Mulder P., Lamblin N., Drobecq H., Henry J.P., et al. Decreased serine207 phosphorylation of troponin T as a biomarker for left ventricular remodelling after myocardial infarction. Eur Heart J 2011, 32:115-123.
89. Eiras S., Narolska N.A., van Loon R.B., Boontje N.M., Zaremba R., Jimenez C.R., et al. Alterations in contractile protein composition and function in human atrial dilatation and atrial fibrillation. J Mol Cell Cardiol 2006, 41:467-477.
90. 2+ handling in human chronic atrial fibrillation. Circulation 2006, 114:670-680.
91. Communal C., Sumandea M., de Tombe P., Narula J., Solaro R.J., Hajjar R.J. Functional consequences of caspase activation in cardiac myocytes. Proc Natl Acad Sci USA 2002, 99:6252-6256.
92. Di Lisa F., De Tullio R., Salamino F., Barbato R., Melloni E., Siliprandi N., et al. Specific degradation of troponin T and I by mu-calpain and its modulation by substrate phosphorylation. Biochem J 1995, 308(Pt 1):57-61.
93. Zhang Z., Biesiadecki B.J., Jin J.P. Selective deletion of the NH2-terminal variable region of cardiac troponin T in ischemia reperfusion by myofibril-associated mu-calpain cleavage. Biochemistry 2006, 45:11681-11694.
94. Mamidi R., Mallampalli S.L., Wieczorek D.F., Chandra M. Identification of two new regions in the N-terminal region of cardiac troponin T that have divergent effects on cardiac contractile function. J Physiol 2013, 591:1217-1234.
95. Madsen L.H., Christensen G., Lund T., Serebruany V.L., Granger C.B., Hoen I., et al. Time course of degradation of cardiac troponin I in patients with acute ST-elevation myocardial infarction. The ASSENT-2 troponin substudy. Circ Res 2006, 99:1141-1147.
96. Madsen L.H., Lund T., Grieg Z., Nygaard S., Holmvang L., Jurlander B., et al. Cardiac troponin I degradation in serum of patients with hypertrophic obstructive cardiomyopathy undergoing percutaneous septal ablation. Cardiology 2009, 114:167-173.
97. Katrukha A.G., Bereznikova A.V., Filatov V.L., Esakova T.V., Kolosova O.V., Pettersson K., et al. Degradation of cardiac troponin I: implication for reliable immunodetection. Clin Chem 1998, 44:2433-2440.
98. Wu A.H., Feng Y.J., Moore R., Apple F.S., McPherson P.H., Buechler K.F., et al. Characterization of cardiac troponin subunit release into serum after acute myocardial infarction and comparison of assays for troponin T and I. American Association for Clinical Chemistry Subcommittee on cTnI Standardization. Clin Chem 1998, 44:1198-1208.
99. Labugger R., McDonough J.L., Neverova I., Van Eyk J.E. Solubilization, two-dimensional separation and detection of the cardiac myofilament protein troponin T. Proteomics 2002, 2:673-678.
100. Michielsen E.C., Diris J.H., Kleijnen V.W., Wodzig W.K., Van Dieijen-Visser M.P. Investigation of release and degradation of cardiac troponin T in patients with acute myocardial infarction. Clin Biochem 2007, 40:851-855.
101. Diris J.H., Hackeng C.M., Kooman J.P., Pinto Y.M., Hermens W.T., van Dieijen-Visser M.P. Impaired renal clearance explains elevated troponin T fragments in hemodialysis patients. Circulation 2004, 109:23-25.
102. Michielsen E.C., Diris J.H., Hackeng C.M., Wodzig W.K., Van Dieijen-Visser M.P. Highly sensitive immunoprecipitation method for extracting and concentrating low-abundance proteins from human serum. Clin Chem 2005, 51:222-224.
103. Fahie-Wilson M.N., Carmichael D.J., Delaney M.P., Stevens P.E., Hall E.M., Lamb E.J. Cardiac troponin T circulates in the free, intact form in patients with kidney failure. Clin Chem 2006, 52:414-420.
104. Bates K.J., Hall E.M., Fahie-Wilson M.N., Kindler H., Bailey C., Lythall D., et al. Circulating immunoreactive cardiac troponin forms determined by gel filtration chromatography after acute myocardial infarction. Clin Chem 2010, 56:952-958.
105. Michielsen E.C., Diris J.H., Wodzig W.K., Van Dieijen-Visser M.P. Size-exclusion chromatography of circulating cardiac troponin T. Clin Chem 2006, 52:2306-2307. [author reply 7-9].
106. Michielsen E.C., Diris J.H., Kleijnen V.W., Wodzig W.K., Van Dieijen-Visser M.P. Interpretation of cardiac troponin T behaviour in size-exclusion chromatography. Clin Chem Lab Med 2006, 44:1422-1427.
107. Cardinaels E.P., Mingels A.M., van Rooij T., Collinson P.O., Prinzen F.W., van Dieijen-Visser M.P. Time-dependent degradation pattern of cardiac troponin T following myocardial infarction. Clin Chem 2013, 59:1083-1090.
108. Defilippi C., Seliger S.L., Kelley W., Duh S.H., Hise M., Christenson R.H., et al. Interpreting cardiac troponin results from high-sensitivity assays in chronic kidney disease without acute coronary syndrome. Clin Chem 2012, 58:1342-1351.
109. Ricchiuti V., Voss E.M., Ney A., Odland M., Anderson P.A., Apple F.S. Cardiac troponin T isoforms expressed in renal diseased skeletal muscle will not cause false-positive results by the second generation cardiac troponin T assay by Boehringer Mannheim. Clin Chem 1998, 44:1919-1924.
110. Davis G.K., Labugger R., Van Eyk J.E., Apple F.S. Cardiac troponin T is not detected in western blots of diseased renal tissue. Clin Chem 2001, 47:782-783.
111. Hessel M.H., Michielsen E.C., Atsma D.E., Schalij M.J., van der Valk E.J., Bax W.H., et al. Release kinetics of intact and degraded troponin I and T after irreversible cell damage. Exp Mol Pathol 2008, 85:90-95.
112. Jacobs L.H., Gerritsen K., Schwenk R., Cardinaels E.P., Wodzig W.K., Glatz J., et al. Ischemia and mechanical stretch in cultured cardiomyocytes and their varying effects on cardiac troponin release and degradation. The release of cardiac troponin; when where and how 2012, 81-109. Datawyse, Maastricht, [Thesis]. L.H. Jacobs (Ed.).
113. Mingels A.M., Cobbaert C.M., de Jong N., van den Hof W.F., van Dieijen-Visser M.P. Time- and temperature-dependent stability of troponin standard reference material 2921 in serum and plasma. Clin Chem Lab Med 2012, 50:1681-1684.
114. Van der Laarse A. Hypothesis: troponin degradation is one of the factors responsible for deterioration of left ventricular function in heart failure. Cardiovasc Res 2002, 56:8.
115. Lin Y., Fu Q., Zhu J., Miller J.M., Van Eyk J.E. Development of a qualitative sequential immunoassay for characterizing the intrinsic properties of circulating cardiac troponin I. Clin Chem 2010, 56:1307-1319.
116. Belin R.J., Sumandea M.P., Allen E.J., Schoenfelt K., Wang H., Solaro R.J., et al. Augmented protein kinase C-alpha-induced myofilament protein phosphorylation contributes to myofilament dysfunction in experimental congestive heart failure. Circ Res 2007, 101:195-204.