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Original Article

Missense Mutations in Plakophilin-2 Cause Sodium Current Deficit and Associate With a Brugada Syndrome PhenotypeCLINICAL PERSPECTIVE

Marina Cerrone, Xianming Lin, Mingliang Zhang, Esperanza Agullo-Pascual, Anna Pfenniger, Halina Chkourko Gusky, Valeria Novelli, Changsung Kim, Tiara Tirasawadichai, Daniel P. Judge, Eli Rothenberg, Huei-Sheng Vincent Chen, Carlo Napolitano, Silvia G. Priori, Mario Delmar
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https://doi.org/10.1161/CIRCULATIONAHA.113.003077
Circulation. 2014;129:1092-1103
Originally published March 10, 2014
Marina Cerrone
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Xianming Lin
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Mingliang Zhang
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Esperanza Agullo-Pascual
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Anna Pfenniger
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Halina Chkourko Gusky
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Valeria Novelli
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Changsung Kim
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Tiara Tirasawadichai
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Daniel P. Judge
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Eli Rothenberg
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Huei-Sheng Vincent Chen
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Carlo Napolitano
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Silvia G. Priori
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Mario Delmar
From the Leon H. Charney Division of Cardiology (M.C., X.L., M.Z., E.A.-P., A.P., H.C.G., S.P., M.D.), and Cardiovascular Genetics Program (M.C., S.P.), NYU School of Medicine, New York, NY; Molecular Cardiology, Maugeri Foundation, Pavia, Italy (V.N., C.N., S.P.); Del E. Webb Center for Neuroscience, Aging & Stem Cell Research, Sanford-Burnham Medical Research Institute, La Jolla, CA (C.K., T.T., H.-S.V.C.); Department of Bioscience and Biotechnology, Sejong University, Seoul, Korea (C.K.); Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (D.P.J.); and Department of Pharmacology, NYU School of Medicine, New York, NY (E.R.).
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Abstract

Background—Brugada syndrome (BrS) primarily associates with the loss of sodium channel function. Previous studies showed features consistent with sodium current (INa) deficit in patients carrying desmosomal mutations, diagnosed with arrhythmogenic cardiomyopathy (or arrhythmogenic right ventricular cardiomyopathy). Experimental models showed correlation between the loss of expression of desmosomal protein plakophilin-2 (PKP2) and reduced INa. We hypothesized that PKP2 variants that reduce INa could yield a BrS phenotype, even without overt structural features characteristic of arrhythmogenic right ventricular cardiomyopathy.

Methods and Results—We searched for PKP2 variants in the genomic DNA of 200 patients with a BrS diagnosis, no signs of arrhythmogenic cardiomyopathy, and no mutations in BrS-related genes SCN5A, CACNa1c, GPD1L, and MOG1. We identified 5 cases of single amino acid substitutions. Mutations were tested in HL-1–derived cells endogenously expressing NaV1.5 but made deficient in PKP2 (PKP2-KD). Loss of PKP2 caused decreased INa and NaV1.5 at the site of cell contact. These deficits were restored by the transfection of wild-type PKP2, but not of BrS-related PKP2 mutants. Human induced pluripotent stem cell cardiomyocytes from a patient with a PKP2 deficit showed drastically reduced INa. The deficit was restored by transfection of wild type, but not BrS-related PKP2. Super-resolution microscopy in murine PKP2-deficient cardiomyocytes related INa deficiency to the reduced number of channels at the intercalated disc and increased separation of microtubules from the cell end.

Conclusions—This is the first systematic retrospective analysis of a patient group to define the coexistence of sodium channelopathy and genetic PKP2 variations. PKP2 mutations may be a molecular substrate leading to the diagnosis of BrS.

  • arrhythmogenic right ventricular dysplasia-cardiomyopathy
  • Brugada syndrome
  • desmosomes
  • plakophilin 2
  • sodium channels
  • Received April 8, 2013.
  • Accepted November 22, 2013.
  • © 2013 American Heart Association, Inc.

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    Missense Mutations in Plakophilin-2 Cause Sodium Current Deficit and Associate With a Brugada Syndrome PhenotypeCLINICAL PERSPECTIVE
    Marina Cerrone, Xianming Lin, Mingliang Zhang, Esperanza Agullo-Pascual, Anna Pfenniger, Halina Chkourko Gusky, Valeria Novelli, Changsung Kim, Tiara Tirasawadichai, Daniel P. Judge, Eli Rothenberg, Huei-Sheng Vincent Chen, Carlo Napolitano, Silvia G. Priori and Mario Delmar
    Circulation. 2014;129:1092-1103, originally published March 10, 2014
    https://doi.org/10.1161/CIRCULATIONAHA.113.003077

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    Missense Mutations in Plakophilin-2 Cause Sodium Current Deficit and Associate With a Brugada Syndrome PhenotypeCLINICAL PERSPECTIVE
    Marina Cerrone, Xianming Lin, Mingliang Zhang, Esperanza Agullo-Pascual, Anna Pfenniger, Halina Chkourko Gusky, Valeria Novelli, Changsung Kim, Tiara Tirasawadichai, Daniel P. Judge, Eli Rothenberg, Huei-Sheng Vincent Chen, Carlo Napolitano, Silvia G. Priori and Mario Delmar
    Circulation. 2014;129:1092-1103, originally published March 10, 2014
    https://doi.org/10.1161/CIRCULATIONAHA.113.003077
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