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Original Article

Myocardial Titin Hypophosphorylation Importantly Contributes to Heart Failure With Preserved Ejection Fraction in a Rat Metabolic Risk ModelClinical Perspective

Nazha Hamdani, Constantijn Franssen, André Lourenço, Inês Falcão-Pires, Dulce Fontoura, Sara Leite, Luisa Plettig, Begoña López, Coen A. Ottenheijm, Peter Moritz Becher, Arantxa González, Carsten Tschöpe, Javier Díez, Wolfgang A. Linke, Adelino F. Leite-Moreira, Walter J. Paulus
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https://doi.org/10.1161/CIRCHEARTFAILURE.113.000539
Circulation: Heart Failure. 2013;6:1239-1249
Originally published November 19, 2013
Nazha Hamdani
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Constantijn Franssen
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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André Lourenço
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Inês Falcão-Pires
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Dulce Fontoura
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Sara Leite
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Luisa Plettig
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Begoña López
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Coen A. Ottenheijm
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Peter Moritz Becher
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Arantxa González
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Carsten Tschöpe
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Javier Díez
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Wolfgang A. Linke
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Adelino F. Leite-Moreira
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Walter J. Paulus
From the Department of Physiology, Institute for Cardiovascular Research, VU University Medical Center, Amsterdam, The Netherlands (N.H., C.F., C.A.O., W.J.P.); Department of Cardiovascular Physiology, Ruhr University Bochum, Bochum, Germany (N.H., L.P., W.A.L.); Department of Physiology and Cardiothoracic Surgery, University of Porto, Porto, Portugal (A.L., I.F.-P., D.F., S.L., A.F.L.-M.); Division of Cardiovascular Sciences, Centre for Applied Medical Research, University of Navarra, Pamplona, Spain (B.L., A.G., J.D.); and Department of Cardiology and Pneumology, Charité–Universitätsmedizin Berlin, Berlin, Germany (P.M.B., C.T.).
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Abstract

Background—Obesity and diabetes mellitus are important metabolic risk factors and frequent comorbidities in heart failure with preserved ejection fraction. They contribute to myocardial diastolic dysfunction (DD) through collagen deposition or titin modification. The relative importance for myocardial DD of collagen deposition and titin modification was investigated in obese, diabetic ZSF1 rats after heart failure with preserved ejection fraction development at 20 weeks.

Methods and Results—Four groups of rats (Wistar-Kyoto, n=11; lean ZSF1, n=11; obese ZSF1, n=11, and obese ZSF1 with high-fat diet, n=11) were followed up for 20 weeks with repeat metabolic, renal, and echocardiographic evaluations and hemodynamically assessed at euthanization. Myocardial collagen, collagen cross-linking, titin isoforms, and phosphorylation were also determined. Resting tension (Fpassive)–sarcomere length relations were obtained in small muscle strips before and after KCl–KI treatment, which unanchors titin and allows contributions of titin and extracellular matrix to Fpassive to be discerned. At 20 weeks, the lean ZSF1 group was hypertensive, whereas both obese ZSF1 groups were hypertensive and diabetic. Only the obese ZSF1 groups had developed heart failure with preserved ejection fraction, which was evident from increased lung weight, preserved left ventricular ejection fraction, and left ventricular DD. The underlying myocardial DD was obvious from high muscle strip stiffness, which was largely (±80%) attributable to titin hypophosphorylation. The latter occurred specifically at the S3991 site of the elastic N2Bus segment and at the S12884 site of the PEVK segment.

Conclusions—Obese ZSF1 rats developed heart failure with preserved ejection fraction during a 20-week time span. Titin hypophosphorylation importantly contributed to the underlying myocardial DD.

  • diabetes mellitus
  • diastole
  • heart failure
  • myocardium
  • obesity
  • Received March 29, 2013.
  • Accepted August 30, 2013.
  • © 2013 American Heart Association, Inc.
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    Myocardial Titin Hypophosphorylation Importantly Contributes to Heart Failure With Preserved Ejection Fraction in a Rat Metabolic Risk ModelClinical Perspective
    Nazha Hamdani, Constantijn Franssen, André Lourenço, Inês Falcão-Pires, Dulce Fontoura, Sara Leite, Luisa Plettig, Begoña López, Coen A. Ottenheijm, Peter Moritz Becher, Arantxa González, Carsten Tschöpe, Javier Díez, Wolfgang A. Linke, Adelino F. Leite-Moreira and Walter J. Paulus
    Circulation: Heart Failure. 2013;6:1239-1249, originally published November 19, 2013
    https://doi.org/10.1161/CIRCHEARTFAILURE.113.000539

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    Myocardial Titin Hypophosphorylation Importantly Contributes to Heart Failure With Preserved Ejection Fraction in a Rat Metabolic Risk ModelClinical Perspective
    Nazha Hamdani, Constantijn Franssen, André Lourenço, Inês Falcão-Pires, Dulce Fontoura, Sara Leite, Luisa Plettig, Begoña López, Coen A. Ottenheijm, Peter Moritz Becher, Arantxa González, Carsten Tschöpe, Javier Díez, Wolfgang A. Linke, Adelino F. Leite-Moreira and Walter J. Paulus
    Circulation: Heart Failure. 2013;6:1239-1249, originally published November 19, 2013
    https://doi.org/10.1161/CIRCHEARTFAILURE.113.000539
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