Unchanged sarcoplasmic reticulum Ca2+-ATPase activity, reduced Ca2+ sensitivity, and negative force-frequency relationship in transgenic rats overexpressing the mouse renin gene

Journal of Molecular Medicine

Volumn 76, Issue 7, 1998, Pages 533-544

  Zobel, Carsten ^a   Brixius, Klara ^a   Pietsch, Markus ^a   Münch, Götz ^a   Bölck, Birgit ^a   Schwinger, Robert H G ^a,b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b Medical Clinic III   (Germany)

Author keywords

Heart; Phospholamban; SERCA2; Skinned fibers; Transgenic rats

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CALCIUM ION; PHOSPHOLAMBAN; RENIN; SODIUM ION;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HEART CONTRACTION; HEART HYPERTROPHY; HYPERTENSION; MALE; MOUSE; MUSCLE TONE; MYOFILAMENT; NONHUMAN; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SARCOPLASMIC RETICULUM; SODIUM BALANCE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CALCIUM; CALCIUM-TRANSPORTING ATPASES; GENE EXPRESSION REGULATION; MICE; MUSCLE CONTRACTION; MUSCLE, SKELETAL; RATS; RENIN;

EID: 0031839441     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s001090050247     Document Type: Article

References (82)

1. Jeunemaitre X, Soubrier F, Kotelevtsev YV, Lifton RP, Williams CS, Charru A, Hunt SC, Hopkins PN, Williams RR, Lalouel JM, et al (1992) Molecular basis of human hypertension: role of angiotensinogen. Cell 71:169-180
2. Kurtz TW, St. Lezin EM (1992) Gene mapping in experimental hypertension. J Am Soc Nephrol 3:28-34
3. Doi Y, Atarashi K, Franco Saenz R, Mulrow P (1983) Adrenal renin: a possible regulator of aldosterone production. Clin Exp Hypertens 5:1119-1126
4. Ganten D, Hermann K, Bayer C, Unger T, Lang RE (1983) Angiotensin synthesis in the brain and increased turnover in hypertensive rats. Science 221:869-871
5. Nakamaru M, Misono KS, Naruse M, Workman RJ, Inagami T (1985) A role for the adrenal renin-angiotensin system in the regulation of potassium-stimulated aldosterone production. Endocrinology 117:1772-1778
6. Dzau VJ, Burt DW, Pratt RE (1988) Molecular biology of the renin-angiotensin system. Am J Physiol 255:F563-573
7. Ganten D, Lang RE, Lehmann E, Unger T (1984) Brain angiotensin: on the way to becoming a well-studied neuropeptide system. Biochem Pharmacol 33:3523-3528
8. Dzau VJ (1988) Circulating versus local renin-angiotensin system in cardiovascular homeostasis. Circulation 77:14-13
9. Lindpaintner K, Jin M, Wilhelm M, Toth M, Ganten D (1989) Aspects of molecular biology and biochemistry of the cardiac renin-angiotensin system. Br J Clin Pharmacol 27 [Suppl 2]:159S-165\S
10. Keuneke C, Yacullo R, Metzger R, Hellmann T, Peters J, Ganten D (1990) The role of tissue renin-angiotensin systems in hypertension and effects of chronic converting-enzyme inhibition. Eur Heart J 11 [Suppl D]:11-16
11. Zhao Y, Bader M, Kreutz R, Fernandez Alfonso M, Zimmermann F, Ganten U, Metzger R, Ganten D, Mullins JJ, Peters J (1993) Ontogenetic regulation of mouse Ren-2d renin gene in transgenic hypertensive rats, TGR(mREN2)27. Am J Physiol 265:E699-707
12. Mullins JJ, Peters J, Ganten D (1990) Fulminant hypertension in transgenic rats harbouring the mouse Ren-2 gene. Nature 344:541-544
13. Bachmann S, Peters J, Engler E, Ganten D, Mullins J (1992) Transgenic rats carrying the mouse renin gene-morphological characterization of a low-renin hypertension model. Kidney Int 41:24-36
14. Kurtz TW, Montano M, Chan L, Kabra P (1989) Molecular evidence of genetic heterogeneity in Wistar-Kyoto rats: implications for research with the spontaneously hypertensive rat. Hypertension 13:188-192
15. Flesch M, Schwinger RHG, Schiffer F, Frank K, Sudkamp M, Kuhn Regnier F, Arnold G, Böhm M (1996) Evidence for functional relevance of an enhanced expression of the Na(+)-Ca2+ exchanger in failing human myocardium. Circulation 94: 992-1002
16. Schwinger RHG, Böhm M, Müller Ehmsen J, Uhlmann R, Schmidt U, Stablein A, Uberfuhr P, Kreuzer E, Reichart B, Eissner HJ, et al (1993) Effect of inotropic stimulation on the negative force-frequency relationship in the failing human heart. Circulation 88:2267-2276
17. Müller-Ehmsen J, Brixius K, Schulze C, Schwinger RHG (1997) Na+ channel modulation and force-frequency relationship in human myocardium. Naunyn Schmiedebergs Arch Pharmacol 355:727-732
18. Schwinger RHG, Böhm M, Koch A, Uhlmann R, Uberfuhr P, Kreuzer E, Reichart B, Erdmann E (1993) Force-frequency-relation in human atrial and ventricular myocardium. Mol Cell Biochem 119:73-78
19. Fabiato A, Fabiato F (1979) Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J Physiol (Paris) 75:463-505
20. Morano I, Arndt H, Gartner C, Ruegg JC (1988) Skinned fibers of human atrium and ventricle: myosin isoenzymes and contractility. Circ Res 62:632-639
21. Schwinger RHG, Böhm M, Koch A, Schmidt U, Morano I, Eissner HJ, Uberfuhr P, Reichart B, Erdmann E (1994) The failing human heart is unable to use the Frank-Starling mechanism. Circ Res 74:959-969
22. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurements with the Folin phenol reagent. J Biol Chem 193:265-275
23. Schwinger RHG, Böhm M, Schmidt U, Karczewski P, Bavendiek U, Flesch M, Krause EG, Erdmann E (1995) Unchanged protein levels of SERCA II and phospholamban but reduced Ca2+ uptake and Ca(2+)-ATPase activity of cardiac sarcoplasmic reticulum from dilated cardiomyopathy patients compared with patients with nonfailing hearts. Circulation 92:3220-3228
24. Philipson KD, Nishimoto AY (1982) Na+-Ca2+ exchange in inside-out cardiac sarcolemmal vesicles. J Biol Chem 257:5111-5117
25. Reeves JP, Sutko JL (1979) Sodium-calcium ion exchange in cardiac membrane vesicles. Proc Natl Acad Sci USA 76:590-594
26. Erdmann E, Philipp G, Scholz H (1980) Cardiac glycoside receptor, (Na+ + K+)-ATPase activity and force of contraction in rat heart. Biochem Pharmacol 29:3219-3229
27. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350-4354
28. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
29. Movsesian MA, Karimi M, Green K, Jones LR (1994) Ca(2+)-transporting ATPase, phospholamban, and calsequestrin levels in nonfailing and failing human myocardium. Circulation 90:653-657
30. Rockman HA, Ono S, Ross RS, Jones LR, Karimi M, Bhargava V, Ross J Jr, Chien KR (1994) Molecular and physiological alterations in murine ventricular dysfunction. Proc Natl Acad Sci USA 91:2694-2698
31. Suzuki T, Wang JH (1986) Stimulation of bovine cardiac sarcoplasmic reticulum Ca2+ pump and blocking of phospholamban phosphorylation and dephosphorylation by a phospholamban monoclonal antibody. J Biol Chem 261:7018-7023
32. Kimura Y, Kurzydlowski K, Tada M, MacLennan DH (1997) Phospholamban inhibitory function is activated by depolymerization. J Biol Chem 272:15061-15064
33. Brixius K, Münch G, Bavendiek U, Bölck B, Schwinger RHG (1997) Frequency-induced force generation in human myocardium correlates with the activity, but not the protein expression of SERCA II. Proceeding of the 2nd International Meeting of the Working Group on Heart Failure, Cologne, 24-27 May 1997. Abstracts, p91
34. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
35. Lompre AM, Lambert F, Lakatta EG, Schwartz K (1991) Expression of sarcoplasmic reticulum Ca(2+)-ATPase and calsequestrin genes in rat heart during ontogenic development and aging. Circ Res 69:1380-1388
36. Takahashi T, Allen PD, Izumo S (1992) Expression of A-. B-. and C-type natriuretic peptide genes in failing and developing human ventricles. Correlation with expression of the Ca( 2+)-ATPase gene. Circ Res 71:9-17
37. Jouannot P, Halt PY (1975) Rat myocardial mechanics during pressure-induced hypertrophy development and reversal. Am J Physiol 229:355-364
38. Yin FC, Spurgeon HA, Weisfeldt ML, Lakatta EG (1980) Mechanical properties of myocardium from hypertrophied rat hearts. A comparison between hypertrophy induced by senescence and by aortic banding. Circ Res 46:292-300
39. Böhm M, Beuckelmann D, Diet F, Feiler G, Lohse MJ, Erdmann E (1988) Properties of cardiac alpha- and beta-adrenoceptors in spontaneously hypertensive rats. Naunyn Schmiedebergs Arch Pharmacol 338:383-391
40. Tawfik Schlieper H, Moll M, Schmid B, Schwinger RHG, Paul M, Ganten D, Böhm M (1995) Alterations of cardiac alpha- and beta-adrenoceptors and inotropic responsiveness in hypertensive transgenic rats harbouring the mouse renin gene (TGR(mREN2)27). Clin Exp Hypertens 17:631-648
41. Böhm M, Moll M, Schmid B, Paul M, Ganten D, Castellano M, Erdmann E (1994) Beta-adrenergic neuroeffector mechanisms in cardiac hypertrophy of renin transgenic rats. Hypertension 24:653-662
42. Brown L, Deighton NM, Bals S, Sohlmann W, Zerkowski HR, Michel MC, Brodde OE (1992) Spare receptors for beta-adrenoceptor-mediated positive inotropic effects of catecholamines in the human heart. J Cardiovasc Pharmacol 19:222-232
43. Lompre AM, Schwartz K, d'Albis A, Lacombe G, Van Thiem N, Swynghedauw B (1979) Myosin isoenzyme redistribution in chronic heart overload. Nature 282:105-107
44. Morano I, Adler K, Weismann K, Knorr A, Erdmann E, Böhm M (1993) Correlation of myosin heavy chain expression in the rat with cAMP in different models of hypertension-induced cardiac hypertrophy. J Mol Cell Cardiol 25:387-394
45. Rajamanickam C, Selvamurugan N, Arun S, Siddiqui MA (1992) Effect of cytosol on the regulation of expression of myosin heavy chain genes during cardiac hypertrophy. Cell Mol Biol (Noisy-le-grand) 38:81-89
46. Ojumaa K, Petrie JF, Balkman C, Hong C, Klein I (1994) Posttranscriptional modification of myosin heavy-chain gene expression in the hypertrophied rat myocardium. Proc Natl Acad Sci USA 91:3468-3472
47. Ohta K, Kim S, Wanibuchi H, Ganten D, Iwao H (1996) Contribution of local renin-angiotensin system to cardiac hypertrophy, phenotypic modulation, and remodeling in TGR(mREN2)27 transgenic rats. Circulation 94:785-791
48. Flesch M, Schiffer F, Zolk O, Pinto Y, Rosenkranz S, Hirth-Diet-rich C, Arnold G, Paul M, Böhm M (1997) Contractile systolic and diastolic dysfunction in renin-induced hypertensive cardiomyopathy. Hypertension 30:383-391
49. Winegrad S, Weisberg A (1987) Isozyme specific modification of myosin ATPase by cAMP in rat heart. Cire Res 60:384-392
50. Takeda N, Ohkubo T, Nakamura I, Suzuki H, Nagano M (1987) Mechanical catecholamine responsiveness and myosin isoenzyme pattern of pressure-overloaded rat ventricular myocardium. Basic Res Cardiol 82:370-374
51. Benforado JM (1958) Frequency-dependent pharmacological and physiological effects on the rat ventricle strip. J Pharmacol Exp Ther 122:86-100
52. Koch Weser J, Blinks JR (1963) The influence of the interval between beats on myocardial contractility. Pharmacol Rev 15:601-652
53. Forester GV, Mainwood GW (1974) Interval dependent inotropic effects in the rat myocardium and the effect of calcium. Pflügers Arch 352:189-196
54. Hoffman BF, Kelly Jr JJ (1959) Effect of rate and rhythm on contraction of rat papillary muscle. Am J Physiol 197: 1199-1204
55. Penefsky ZJ, Buckley NM, Litwak RS (1972) Effect of temperature and calcium on force-frequency relationships in mammalian ventricular myocardium. Pflügers Arch 332:271-282
56. Frampton JE, Harrison SM, Boyett MR, Orchard CH (1991) Ca2+ and Na+ in rat myocytes showing different force-frequency relationships. Am J Physiol 261:C739-750
57. Bers DM (1991) Species differences and the role of sodium-calcium exchange in cardiac muscle relaxation. Ann NY Acad Sci 639:375-385
58. Magyar CE, Wang J, Azuma KK, McDonough AA (1995) Reciprocal regulation of cardiac Na-K-ATPase and Na/Ca exchanger: hypertension, thyroid hormone, development. Am J Physiol 269:C675-682
59. Studer R, Reinecke H, Vetter R, Holtz J, Drexler H (1993) Enhanced expression and function of the Na+/Ca2+ exchanger in rat ventricular hypertrophy and in myocardium of neonatal rats (abstract). Circulation 88:86
60. Morano I, Hofmann F, Zimmer M, Ruegg JC (1985) The influence of P-light chain phosphorylation by myosin light chain kinase on the calcium sensitivity of chemically skinned heart fibres. FEBS Lett 189:221-224
61. Morano I, Bachle Stolz C, Katus A, Ruegg JC (1988) Increased calcium sensitivity of chemically skinned human atria by myosin light chain kinase. Basic Res Cardiol 83:350-359
62. Morano I, Lengsfeld M, Ganten U, Ganten D, Ruegg JC (1988) Chronic hypertension changes myosin isoenzyme pattern and decreases myosin phosphorylation in the rat heart. J Mol Cell Cardiol 20:875-886
63. Kranias EG, Garvey JL, Srivastava RD, Solaro RJ (1985) Phosphorylation and functional modifications of sarcoplasmic reticulum and myofibrils in isolated rabbit hearts stimulated with isoprenaline. Biochem J 226:113-121
64. Hofmann PA, Lange JH, 3rd (1994) Effects of phosphorylation of troponin I and C protein on isometric tension and velocity of unloaded shortening in skinned single cardiac myocytes from rats. Circ Res 74:718-726
65. Limas CJ, Spier SS, Kahlon J (1980) Enhanced calcium transport by sarcoplasmic reticulum in mild cardiac hypertrophy. J Mol Cell Cardiol 12:1103-1116
66. Malhotra A, Penpargkul S, Schaible T, Scheuer J (1981) Contractile proteins and sarcoplasmic reticulum in physiologic cardiac hypertrophy. Am J Physiol 241:H263-267
67. Limas CJ (1978) Calcium transport ATPase of cardiac sarcoplasmic reticulum in experimental hyperthyroidism. Am J Physiol 235:H745-752
68. Suko J (1973) The calcium pump of cardiac sarcoplasmic reticulum. Functional alterations at different levels of thyroid state in rabbits. J Physiol (Lond) 228:563-582
69. Zarain Herzberg A, Yano K, Elimban V, Dhalla NS (1994) Cardiac sarcoplasmic reticulum Ca(2+)-ATPase expression in streptozotocin-induced diabetic rat heart. Biochem Biophys Res Commun 203:113-120
70. Limas CJ, Cohn JN (1977) Defective calcium transport by cardiac sarcoplasmic reticulum in spontaneously hypertensive rats. Circ Res 40:162-169
71. Lee SW, Schwartz A, Adams RJ, Yamori Y, Whitmer K, Lane LK, Wallick ET (1983) Decrease in Na+,K+-ATPase activity and [3H]ouabain binding sites in sarcolemma prepared from hearts of spontaneously hypertensive rats. Hypertension 5:682-688
72. Clough DL, Pamnani MB, Haddy FJ (1983) Decreased myocardial Na+-K+-ATPase activity in one-kidney, one-clip hypertensive rats. Am J Physiol 245:H244-251
73. Studer R, Reinecke H, Vetter R, Holtz J, Drexler H (1997) Expression and function of the cardiac Na+/Ca2+ exchanger in postnatal development of the rat, in experimental-induced cardiac hypertrophy and in the failing human heart. Basic Res Cardiol 92 [Suppl 1]:53-58
74. Langer GA (1982) Sodium-calcium exchange in the heart. Annu Rev Physiol 44:435-449
75. Wallick ET, Lane LK, Schwartz A (1979) Biochemical mechanism of the sodium pump. Annu Rev Physiol 41:397-411
76. Tada M, Yamada M, Kadoma M, Inui M, Ohmori F (1982) Calcium transport by cardiac sarcoplasmic reticulum and phosphorylation of phospholamban. Mol Cell Biochem 46:73-95
77. Wegener AD, Jones LR (1984) Phosphorylation-induced mobility shift in phospholamban in sodium dodecyl sulfate-polyacrylamide gels. Evidence for a protein structure consisting of multiple identical phosphorylatable subunits. J Biol Chem 259: 1834-1841
78. Hawkins C, Xu A, Narayanan N (1994) Sarcoplasmic reticulum calcium pump in cardiac and slow twitch skeletal muscle but not last twitch skeletal muscle undergoes phosphorylation by endogenous and exogenous Ca2+/calmodulin-dependent protein kinase. Characterization of optimal conditions for calcium pump phosphorylation. J Biol Chem 269:31198-31206
79. Tarazi RC (1986) Cardiovascular hypertrophy in hypertension. Arthur C. Corcoran Memorial Lecture. Hypertension 8: 1187-1190
80. Tarazi RC, Levy MN (1982) Cardiac responses to increased after-load. State-of-the-art review. Hypertension 4:8-18
81. Grobecker H, Saavedra JM, Weise VK (1982) Biosynthetic enzyme activities and catecholamines in adrenal glands of genetic and experimental hypertensive rats. Circ Res 50:742-746
82. Kumano K, Upsher ME, Khairallah PA (1983) Beta adrenergic receptor response coupling in hypertrophied hearts. Hypertension 5:1175-1183