Changes in cardiac troponins with gestational age explain changes in cardiac muscle contractility in the sheep fetus

Journal of Applied Physiology

Volumn 111, Issue 1, 2011, Pages 236-243

  Posterino, Giuseppe Saverio ^a   Dunn, Stacey Leanne ^b,c   Botting, Kimberley Jae ^b,c   Wang, William ^b   Gentili, Sheridan ^b   Morrison, Janna Leigh ^b,c  

^a LA TROBE UNIVERSITY   (Australia)

^b UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Calcium; Heart

Indexed keywords

TROPONIN; TROPONIN C; TROPONIN I; TROPONIN T;

ANIMAL; ARTICLE; COMPARATIVE STUDY; EXCITATION CONTRACTION COUPLING; FETUS HEART; GESTATIONAL AGE; HEART CONTRACTION; HEART MUSCLE CELL; METABOLISM; MUSCLE STRENGTH; SHEEP;

ANIMALS; EXCITATION CONTRACTION COUPLING; FETAL HEART; GESTATIONAL AGE; MUSCLE STRENGTH; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; SHEEP; TROPONIN; TROPONIN C; TROPONIN I; TROPONIN T;

EID: 79960217388     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00067.2011     Document Type: Article

References (49)

1. Anderson PA, Glick KL, Manring A, Crenshaw C Jr. Developmental changes in cardiac contractility in fetal and postnatal sheep: in vitro and in vivo. Am J Physiol Heart Circ Physiol 247:H371-H379, 1984. (Pubitemid 14047348)
2. Barbera A, Giraud GD, Reller MD, Maylie J, Morton MJ, Thornburg KL. Right ventricular systolic pressure load alters myocyte maturation in fetal sheep. Am J Physiol Regul Integr Comp Physiol 279:R1157-R1164, 2000.
3. Bers DM. Cardiac excitation-contraction coupling. Nature 415:198-205, 2002. (Pubitemid 34059525)
4. Bubb KJ, Cock ML, Black MJ, Dodic M, Boon WM, Parkington HC, Harding R, Tare M. Intrauterine growth restriction delays cardiomyocyte maturation and alters coronary artery function in the fetal sheep. J Physiol 578:871-881, 2007. (Pubitemid 46165515)
5. Burrell JH, Boyn AM, Kumarasamy V, Hsieh A, Head SI, Lumbers ER. Growth and maturation of cardiac myocytes in fetal sheep in the second half of gestation. Anat Rec 274A: 952-961, 2003. (Pubitemid 37267779)
6. Danielson L, McMillen IC, Dyer JL, Morrison JL. Restriction of placental growth results in greater hypotensive response to alpha-adrenergic blockade in fetal sheep during late gestation. J Physiol 563:611-620, 2005. (Pubitemid 40360917)
7. Edwards LJ, Simonetta G, Owens JA, Robinson JS, McMillen IC. Restriction of placental and fetal growth in sheep alters fetal blood pressure responses to angiotensin II and captopril. J Physiol 515:897-904, 1999. (Pubitemid 29140122)
8. Gao L, Kennedy JM, Solaro RJ. Differential expression of TnI and TnT isoforms in rabbit heart during the perinatal period and during cardiovascular stress. J Mol Cell Cardiol 27:541-550, 1995.
9. Giraud GD, Louey S, Jonker S, Schultz J, Thornburg KL. Cortisol stimulates cell cycle activity in the cardiomyocyte of the sheep fetus. Endocrinology 147:3643-3649, 2006. (Pubitemid 44079367)
10. Godt RE, Fogaca RT, Nosek TM. Changes in force and calcium sensitivity in the developing avian heart. Can J Physiol Pharmacol 69:1692-1697, 1991.
11. Gomes AV, Potter JD, Szczesna-Cordary, D. The role of troponins in muscle contraction. IUBMB Life 54:323-333, 2002. (Pubitemid 36298251)
12. Jonker SS, Faber JJ, Anderson DF, Thornburg KL, Louey S, Giraud GD. Sequential growth of fetal sheep cardiac myocytes in response to simultaneous arterial and venous hypertension. Am J Physiol Regul Integr Comp Physiol 292:R913-R919, 2007. (Pubitemid 46207748)
13. Jonker SS, Zhang L, Louey S, Giraud GD, Thornburg KL, Faber JJ. Myocyte enlargement, differentiation, and proliferation kinetics in the fetal sheep heart. J Appl Physiol 102:1130-1142, 2007. (Pubitemid 46377041)
14. Kobayashi T, Jin L, de Tombe PP. Cardiac thin filament regulation. Pflügers Arch 457:37-46, 2008.
15. 2+ sensitivity due to titin and troponin-I isoform switching are not critically triggered by birth. Am J Physiol Heart Circ Physiol 291:H496-H506, 2006. (Pubitemid 44175054)
16. Laylanda J, Solarob RJ, Shaha AM. Regulation of cardiac contractile function by troponin I phosphorylation. Cardiovasc Res 66:12-21, 2005.
17. Li F, Wang X, Capasso JM, Gerdes AM. Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during postnatal development. J Mol Cell Cardiol 28:1737-1746, 1996. (Pubitemid 26300573)
18. Lim SS, Woodroofe MN, Lemanski LF. An analysis of contractile proteins in developing chick heart by SDS polyacrylamide gel electrophoresis and electron microscopy. J Embryol Exp Morph 77:1-14, 1983. (Pubitemid 14128736)
19. MacLaughlin SM, Walker SK, Kleemann DO, Sibbons JP, Tosh DN, Gentili S, Coulter CL, McMillen IC. Impact of periconceptional undernutrition on adrenal growth and adrenal insulin-like growth factor and steroidogenic enzyme expression in the sheep fetus during early pregnancy. Endocrinology 148:1911-1920, 2007. (Pubitemid 46457136)
20. Mahony L, Jones LR. Developmental changes in cardiac sarcoplasmic reticulum in sheep. J Biol Chem 261:15257-15265, 1986. (Pubitemid 17218105)
21. Martin AF, Ball K, Gao LZ, Kumar P, Solaro RJ. Identification and functional significance of troponin I isoforms in neonatal rat heart myofibrils. Circ Res 69:1244-1252, 1991.
22. McAuliffe JJ, Robbins J. Troponin T expression in normal and pressureloaded fetal sheep heart. Pediatr Res 29:580-585, 1991.
23. McCall SJ, Nassar R, Malouf NN, Saunders AJ, Oakeley AE, Henderson PM, Solaro RJ, Pielak GJ, Alexander KA, Anderson PAW. Development and cardiac contractility: cardiac troponin t isoforms and cytosolic calcium in rabbit. Pediatr Res 60:276-281, 2006. (Pubitemid 44267738)
24. Metzger JM, Michele DE, Rust EM, Borton AR, Westfall MV. Sarcomere thin filament regulatory isoforms. Evidence of a dominant effect of slow skeletal troponin I on cardiac contraction. J Biol Chem 278:13118-13123, 2003. (Pubitemid 36800080)
25. 2+-release activity and ryanodine receptor in sarcoplasmic-reticulum membranes during cardiac myogenesis. Biochem J 253:631-636, 1988.
26. Morrison JL, Botting KJ, Dyer JL, Williams SJ, Thornburg KL, McMillen IC. Restriction of placental function alters heart development in the sheep fetus. Am J Physiol Regul Integr Comp Physiol 293:R306-R313, 2007. (Pubitemid 47092189)
27. Morrison JL, Carmichael L, Homan J, Richardson BS. The effects of 'sleep promoting agents' on behavioural state in the ovine fetus. Dev Brain Res 103:1-8, 1997. (Pubitemid 27465705)
28. Nakanishi T, Seguchi M, Takao A. Development of the myocardial contractile system. Experientia 44:936-944, 1988. (Pubitemid 19050462)
29. Onishi J, Browne VA, Kono S, Stiffel VM, Gilbert RD. Effects of long-term hypoxia and troponin I phosphorylation on cardiac myofilament calcium responses in fetal and nonpregnant sheep. J Soc Gynecol Invest 11:1-8, 2004. (Pubitemid 38050184)
30. 2+ sensitivity of mammalian skinned cardiac and skeletal muscle fibres. J Physiol 480:45-60, 1994.
31. Parmacek MS, Bengur AR, Vora AJ, Leiden JM. The structure and regulation of expression of the murine fast skeletal troponin C gene. Identification of a developmentally regulated, muscle-specific transcriptional enhancer. J Biol Chem 265:15970-15976, 1990.
32. Parmacek MS, Leiden JM. Structure and expression of the murine slow/cardiac troponin C gene. J Biol Chem 264:13217-13225, 1989. (Pubitemid 19194899)
33. Parmacek MS, Solaro RJ. Biology of the troponin complex in cardiac myocytes. Progr Cardiovasc Dis 47:159-176, 2004. (Pubitemid 40037316)
34. Philips ID, Simonetta G, Owens JA, Robinson JS, Clarke IJ, McMillen IC. Placental restriction alters the functional development of the pituitary-adrenal axis in the sheep fetus during late gestation. Pediatr Res 40:861-866, 1996. (Pubitemid 26404197)
35. Reiser PJ, Westfall MV, Schiaffino S, Solaro RJ. Tension production and thin-filament protein isoforms in developing rat myocardium. Am J Physiol Heart Circ Physiol 267:H1589-H1596, 1994.
36. Rüegg JC. Cardiac contractility: how calcium activates the myofilaments. Naturwissenschaften 85:575-582, 1998. (Pubitemid 28562351)
37. Sabry MA, Dhoot GK. Identification and pattern of expression of a developmental isoform of troponin I in chicken and rat cardiac muscle. J Muscle Res Cell Motil 10:85-91, 1989.
38. Saggin L, Ausoni S, Gorza L, Sartore S, Schiaffino S. Troponin T switching in the developing rat heart. J Biol Chem 263:18488-18492, 1988. (Pubitemid 19005125)
39. Saggin L, Gorza L, Ausoni S, Schiaffino S. Troponin I switching in the developing heart. J Biol Chem 264:16299-16302, 1989. (Pubitemid 19238397)
40. Siedner S, Kruger M, Schroeter M, Metzler D, Roell W, Fleischmann BK, Hescheler J, Pfitzer G, Stehle R. Developmental changes in contractility and sarcomeric proteins from the early embryonic to the adult stage in the mouse heart. J Physiol 548:493-505, 2003. (Pubitemid 36527471)
41. Smolich JJ, Walker AM, Gordon RC, Adamson TM. Left and right ventricular myocardial morphometry in fetal, neonatal, and adult sheep. Am J Physiol Heart Circ Physiol 257:H1-H9, 1989.
42. Soonpaa MH, Field LJ. Assessment of cardiomyocyte DNA synthesis in normal and injured adult mouse hearts. Am J Physiol Heart Circ Physiol 272:H220-H226, 1997.
43. 2+-handling properties of the right ventricular papillary muscle in the late-gestation sheep fetus. J Appl Physiol 101:728-733, 2006. (Pubitemid 44352281)
44. Sundgren NC, Giraud GD, Schultz JM, Lasarev MR, Stork PJ, Thornburg KL. Extracellular signal-regulated kinase and phosphoinositol-3 kinase mediate IGF-1 induced proliferation of fetal sheep cardiomyocytes. Am J Physiol Regul Integr Comp Physiol 285:R1481-R1489, 2003. (Pubitemid 37464408)
45. Sundgren NC, Giraud GD, Stork PJ, Maylie JG, Thornburg KL. Angiotensin II stimulates hyperplasia but not hypertrophy in immature ovine cardiomyocytes. J Physiol 548:881-891, 2003. (Pubitemid 36592781)
46. Tohse N, Seki S, Kobayashi T, Tsutsuura M, Nagashima M, Yamada Y. Development of excitation-contraction coupling in cardiomyocytes. Jpn J Physiol 54:1-6, 2004. (Pubitemid 38470757)
47. 2+ and pH sensitivity. J Mol Cell Cardiol 43:107-118, 2007. (Pubitemid 47071918)
48. Woodcock EA, Matkovich SJ. Cardiomyocytes structure, function and associated pathologies. Int J Biochem Cell Biol 37:1746-1751, 2005. (Pubitemid 40961659)
49. Zhang S, Rattanatray L, MacLaughlin SM, Cropley JE, Suter CM, Molloy L, Kleemann D, Walker SK, Muhlhausler BS, Morrison JL, McMillen IC. Periconceptional undernutrition in normal and overweight ewes leads to increased adrenal growth and epigenetic changes in adrenal Igf2/H19 gene in offspring. FASEB J 24:2772-2782, 2010.