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Research ArticleArticle

Carbonylation Induces Heterogeneity in Cardiac Ryanodine Receptor Function in Diabetes Mellitus

Chun Hong Shao, Chengju Tian, Shouqiang Ouyang, Caronda J. Moore, Fadhel Alomar, Ina Nemet, Alicia D'Souza, Ryoji Nagai, Shelby Kutty, George J. Rozanski, Sasanka Ramanadham, Jaipaul Singh and Keshore R. Bidasee
Molecular Pharmacology September 2012, 82 (3) 383-399; DOI: https://doi.org/10.1124/mol.112.078352
Chun Hong Shao
Departments of Pharmacology and Experimental Neuroscience (C.H.S., C.T., S.O., C.J.M., F.A., K.R.B.), Cellular and Integrative Physiology (G.J.R.), and Environmental, Occupational, and Agricultural Health (K.R.B.), University of Nebraska Medical Center, Omaha, Nebraska; Department of Pharmacology, University of Dammam, Dammam, Kingdom of Saudi Arabia (F.A.); Laboratory for Carbohydrate, Peptide, and Glycopeptide Research, Rudjer Boskovic Institute, Zagreb, Croatia (I.N.); School of Forensic and Investigative Science, University of Central Lancashire, Preston, United Kingdom (A.D., J.S.); Laboratory of Food and Regulation Biology, Department of Bioscience, School of Agriculture, Tokai University, Tokyo, Japan (R.N.); Joint Division of Pediatric Cardiology, University of Nebraska/Creighton University and Children's Hospital and Medical Center, Omaha, Nebraska (S.K.); Department of Physiology and Biophysics, University of Alabama, Birmingham, Alabama (S.R.); and Nebraska Center for Redox Biology, Lincoln, Nebraska (K.R.B.)
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Chengju Tian
Departments of Pharmacology and Experimental Neuroscience (C.H.S., C.T., S.O., C.J.M., F.A., K.R.B.), Cellular and Integrative Physiology (G.J.R.), and Environmental, Occupational, and Agricultural Health (K.R.B.), University of Nebraska Medical Center, Omaha, Nebraska; Department of Pharmacology, University of Dammam, Dammam, Kingdom of Saudi Arabia (F.A.); Laboratory for Carbohydrate, Peptide, and Glycopeptide Research, Rudjer Boskovic Institute, Zagreb, Croatia (I.N.); School of Forensic and Investigative Science, University of Central Lancashire, Preston, United Kingdom (A.D., J.S.); Laboratory of Food and Regulation Biology, Department of Bioscience, School of Agriculture, Tokai University, Tokyo, Japan (R.N.); Joint Division of Pediatric Cardiology, University of Nebraska/Creighton University and Children's Hospital and Medical Center, Omaha, Nebraska (S.K.); Department of Physiology and Biophysics, University of Alabama, Birmingham, Alabama (S.R.); and Nebraska Center for Redox Biology, Lincoln, Nebraska (K.R.B.)
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Shouqiang Ouyang
Departments of Pharmacology and Experimental Neuroscience (C.H.S., C.T., S.O., C.J.M., F.A., K.R.B.), Cellular and Integrative Physiology (G.J.R.), and Environmental, Occupational, and Agricultural Health (K.R.B.), University of Nebraska Medical Center, Omaha, Nebraska; Department of Pharmacology, University of Dammam, Dammam, Kingdom of Saudi Arabia (F.A.); Laboratory for Carbohydrate, Peptide, and Glycopeptide Research, Rudjer Boskovic Institute, Zagreb, Croatia (I.N.); School of Forensic and Investigative Science, University of Central Lancashire, Preston, United Kingdom (A.D., J.S.); Laboratory of Food and Regulation Biology, Department of Bioscience, School of Agriculture, Tokai University, Tokyo, Japan (R.N.); Joint Division of Pediatric Cardiology, University of Nebraska/Creighton University and Children's Hospital and Medical Center, Omaha, Nebraska (S.K.); Department of Physiology and Biophysics, University of Alabama, Birmingham, Alabama (S.R.); and Nebraska Center for Redox Biology, Lincoln, Nebraska (K.R.B.)
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Caronda J. Moore
Departments of Pharmacology and Experimental Neuroscience (C.H.S., C.T., S.O., C.J.M., F.A., K.R.B.), Cellular and Integrative Physiology (G.J.R.), and Environmental, Occupational, and Agricultural Health (K.R.B.), University of Nebraska Medical Center, Omaha, Nebraska; Department of Pharmacology, University of Dammam, Dammam, Kingdom of Saudi Arabia (F.A.); Laboratory for Carbohydrate, Peptide, and Glycopeptide Research, Rudjer Boskovic Institute, Zagreb, Croatia (I.N.); School of Forensic and Investigative Science, University of Central Lancashire, Preston, United Kingdom (A.D., J.S.); Laboratory of Food and Regulation Biology, Department of Bioscience, School of Agriculture, Tokai University, Tokyo, Japan (R.N.); Joint Division of Pediatric Cardiology, University of Nebraska/Creighton University and Children's Hospital and Medical Center, Omaha, Nebraska (S.K.); Department of Physiology and Biophysics, University of Alabama, Birmingham, Alabama (S.R.); and Nebraska Center for Redox Biology, Lincoln, Nebraska (K.R.B.)
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Fadhel Alomar
Departments of Pharmacology and Experimental Neuroscience (C.H.S., C.T., S.O., C.J.M., F.A., K.R.B.), Cellular and Integrative Physiology (G.J.R.), and Environmental, Occupational, and Agricultural Health (K.R.B.), University of Nebraska Medical Center, Omaha, Nebraska; Department of Pharmacology, University of Dammam, Dammam, Kingdom of Saudi Arabia (F.A.); Laboratory for Carbohydrate, Peptide, and Glycopeptide Research, Rudjer Boskovic Institute, Zagreb, Croatia (I.N.); School of Forensic and Investigative Science, University of Central Lancashire, Preston, United Kingdom (A.D., J.S.); Laboratory of Food and Regulation Biology, Department of Bioscience, School of Agriculture, Tokai University, Tokyo, Japan (R.N.); Joint Division of Pediatric Cardiology, University of Nebraska/Creighton University and Children's Hospital and Medical Center, Omaha, Nebraska (S.K.); Department of Physiology and Biophysics, University of Alabama, Birmingham, Alabama (S.R.); and Nebraska Center for Redox Biology, Lincoln, Nebraska (K.R.B.)
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Ina Nemet
Departments of Pharmacology and Experimental Neuroscience (C.H.S., C.T., S.O., C.J.M., F.A., K.R.B.), Cellular and Integrative Physiology (G.J.R.), and Environmental, Occupational, and Agricultural Health (K.R.B.), University of Nebraska Medical Center, Omaha, Nebraska; Department of Pharmacology, University of Dammam, Dammam, Kingdom of Saudi Arabia (F.A.); Laboratory for Carbohydrate, Peptide, and Glycopeptide Research, Rudjer Boskovic Institute, Zagreb, Croatia (I.N.); School of Forensic and Investigative Science, University of Central Lancashire, Preston, United Kingdom (A.D., J.S.); Laboratory of Food and Regulation Biology, Department of Bioscience, School of Agriculture, Tokai University, Tokyo, Japan (R.N.); Joint Division of Pediatric Cardiology, University of Nebraska/Creighton University and Children's Hospital and Medical Center, Omaha, Nebraska (S.K.); Department of Physiology and Biophysics, University of Alabama, Birmingham, Alabama (S.R.); and Nebraska Center for Redox Biology, Lincoln, Nebraska (K.R.B.)
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Alicia D'Souza
Departments of Pharmacology and Experimental Neuroscience (C.H.S., C.T., S.O., C.J.M., F.A., K.R.B.), Cellular and Integrative Physiology (G.J.R.), and Environmental, Occupational, and Agricultural Health (K.R.B.), University of Nebraska Medical Center, Omaha, Nebraska; Department of Pharmacology, University of Dammam, Dammam, Kingdom of Saudi Arabia (F.A.); Laboratory for Carbohydrate, Peptide, and Glycopeptide Research, Rudjer Boskovic Institute, Zagreb, Croatia (I.N.); School of Forensic and Investigative Science, University of Central Lancashire, Preston, United Kingdom (A.D., J.S.); Laboratory of Food and Regulation Biology, Department of Bioscience, School of Agriculture, Tokai University, Tokyo, Japan (R.N.); Joint Division of Pediatric Cardiology, University of Nebraska/Creighton University and Children's Hospital and Medical Center, Omaha, Nebraska (S.K.); Department of Physiology and Biophysics, University of Alabama, Birmingham, Alabama (S.R.); and Nebraska Center for Redox Biology, Lincoln, Nebraska (K.R.B.)
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Ryoji Nagai
Departments of Pharmacology and Experimental Neuroscience (C.H.S., C.T., S.O., C.J.M., F.A., K.R.B.), Cellular and Integrative Physiology (G.J.R.), and Environmental, Occupational, and Agricultural Health (K.R.B.), University of Nebraska Medical Center, Omaha, Nebraska; Department of Pharmacology, University of Dammam, Dammam, Kingdom of Saudi Arabia (F.A.); Laboratory for Carbohydrate, Peptide, and Glycopeptide Research, Rudjer Boskovic Institute, Zagreb, Croatia (I.N.); School of Forensic and Investigative Science, University of Central Lancashire, Preston, United Kingdom (A.D., J.S.); Laboratory of Food and Regulation Biology, Department of Bioscience, School of Agriculture, Tokai University, Tokyo, Japan (R.N.); Joint Division of Pediatric Cardiology, University of Nebraska/Creighton University and Children's Hospital and Medical Center, Omaha, Nebraska (S.K.); Department of Physiology and Biophysics, University of Alabama, Birmingham, Alabama (S.R.); and Nebraska Center for Redox Biology, Lincoln, Nebraska (K.R.B.)
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Shelby Kutty
Departments of Pharmacology and Experimental Neuroscience (C.H.S., C.T., S.O., C.J.M., F.A., K.R.B.), Cellular and Integrative Physiology (G.J.R.), and Environmental, Occupational, and Agricultural Health (K.R.B.), University of Nebraska Medical Center, Omaha, Nebraska; Department of Pharmacology, University of Dammam, Dammam, Kingdom of Saudi Arabia (F.A.); Laboratory for Carbohydrate, Peptide, and Glycopeptide Research, Rudjer Boskovic Institute, Zagreb, Croatia (I.N.); School of Forensic and Investigative Science, University of Central Lancashire, Preston, United Kingdom (A.D., J.S.); Laboratory of Food and Regulation Biology, Department of Bioscience, School of Agriculture, Tokai University, Tokyo, Japan (R.N.); Joint Division of Pediatric Cardiology, University of Nebraska/Creighton University and Children's Hospital and Medical Center, Omaha, Nebraska (S.K.); Department of Physiology and Biophysics, University of Alabama, Birmingham, Alabama (S.R.); and Nebraska Center for Redox Biology, Lincoln, Nebraska (K.R.B.)
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George J. Rozanski
Departments of Pharmacology and Experimental Neuroscience (C.H.S., C.T., S.O., C.J.M., F.A., K.R.B.), Cellular and Integrative Physiology (G.J.R.), and Environmental, Occupational, and Agricultural Health (K.R.B.), University of Nebraska Medical Center, Omaha, Nebraska; Department of Pharmacology, University of Dammam, Dammam, Kingdom of Saudi Arabia (F.A.); Laboratory for Carbohydrate, Peptide, and Glycopeptide Research, Rudjer Boskovic Institute, Zagreb, Croatia (I.N.); School of Forensic and Investigative Science, University of Central Lancashire, Preston, United Kingdom (A.D., J.S.); Laboratory of Food and Regulation Biology, Department of Bioscience, School of Agriculture, Tokai University, Tokyo, Japan (R.N.); Joint Division of Pediatric Cardiology, University of Nebraska/Creighton University and Children's Hospital and Medical Center, Omaha, Nebraska (S.K.); Department of Physiology and Biophysics, University of Alabama, Birmingham, Alabama (S.R.); and Nebraska Center for Redox Biology, Lincoln, Nebraska (K.R.B.)
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Sasanka Ramanadham
Departments of Pharmacology and Experimental Neuroscience (C.H.S., C.T., S.O., C.J.M., F.A., K.R.B.), Cellular and Integrative Physiology (G.J.R.), and Environmental, Occupational, and Agricultural Health (K.R.B.), University of Nebraska Medical Center, Omaha, Nebraska; Department of Pharmacology, University of Dammam, Dammam, Kingdom of Saudi Arabia (F.A.); Laboratory for Carbohydrate, Peptide, and Glycopeptide Research, Rudjer Boskovic Institute, Zagreb, Croatia (I.N.); School of Forensic and Investigative Science, University of Central Lancashire, Preston, United Kingdom (A.D., J.S.); Laboratory of Food and Regulation Biology, Department of Bioscience, School of Agriculture, Tokai University, Tokyo, Japan (R.N.); Joint Division of Pediatric Cardiology, University of Nebraska/Creighton University and Children's Hospital and Medical Center, Omaha, Nebraska (S.K.); Department of Physiology and Biophysics, University of Alabama, Birmingham, Alabama (S.R.); and Nebraska Center for Redox Biology, Lincoln, Nebraska (K.R.B.)
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Jaipaul Singh
Departments of Pharmacology and Experimental Neuroscience (C.H.S., C.T., S.O., C.J.M., F.A., K.R.B.), Cellular and Integrative Physiology (G.J.R.), and Environmental, Occupational, and Agricultural Health (K.R.B.), University of Nebraska Medical Center, Omaha, Nebraska; Department of Pharmacology, University of Dammam, Dammam, Kingdom of Saudi Arabia (F.A.); Laboratory for Carbohydrate, Peptide, and Glycopeptide Research, Rudjer Boskovic Institute, Zagreb, Croatia (I.N.); School of Forensic and Investigative Science, University of Central Lancashire, Preston, United Kingdom (A.D., J.S.); Laboratory of Food and Regulation Biology, Department of Bioscience, School of Agriculture, Tokai University, Tokyo, Japan (R.N.); Joint Division of Pediatric Cardiology, University of Nebraska/Creighton University and Children's Hospital and Medical Center, Omaha, Nebraska (S.K.); Department of Physiology and Biophysics, University of Alabama, Birmingham, Alabama (S.R.); and Nebraska Center for Redox Biology, Lincoln, Nebraska (K.R.B.)
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Keshore R. Bidasee
Departments of Pharmacology and Experimental Neuroscience (C.H.S., C.T., S.O., C.J.M., F.A., K.R.B.), Cellular and Integrative Physiology (G.J.R.), and Environmental, Occupational, and Agricultural Health (K.R.B.), University of Nebraska Medical Center, Omaha, Nebraska; Department of Pharmacology, University of Dammam, Dammam, Kingdom of Saudi Arabia (F.A.); Laboratory for Carbohydrate, Peptide, and Glycopeptide Research, Rudjer Boskovic Institute, Zagreb, Croatia (I.N.); School of Forensic and Investigative Science, University of Central Lancashire, Preston, United Kingdom (A.D., J.S.); Laboratory of Food and Regulation Biology, Department of Bioscience, School of Agriculture, Tokai University, Tokyo, Japan (R.N.); Joint Division of Pediatric Cardiology, University of Nebraska/Creighton University and Children's Hospital and Medical Center, Omaha, Nebraska (S.K.); Department of Physiology and Biophysics, University of Alabama, Birmingham, Alabama (S.R.); and Nebraska Center for Redox Biology, Lincoln, Nebraska (K.R.B.)
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Abstract

Heart failure and arrhythmias occur at 3 to 5 times higher rates among individuals with diabetes mellitus, compared with age-matched, healthy individuals. Studies attribute these defects in part to alterations in the function of cardiac type 2 ryanodine receptors (RyR2s), the principal Ca2+-release channels on the internal sarcoplasmic reticulum (SR). To date, mechanisms underlying RyR2 dysregulation in diabetes remain poorly defined. A rat model of type 1 diabetes, in combination with echocardiography, in vivo and ex vivo hemodynamic studies, confocal microscopy, Western blotting, mass spectrometry, site-directed mutagenesis, and [3H]ryanodine binding, lipid bilayer, and transfection assays, was used to determine whether post-translational modification by reactive carbonyl species (RCS) represented a contributing cause. After 8 weeks of diabetes, spontaneous Ca2+ release in ventricular myocytes increased ∼5-fold. Evoked Ca2+ release from the SR was nonuniform (dyssynchronous). Total RyR2 protein levels remained unchanged, but the ability to bind the Ca2+-dependent ligand [3H]ryanodine was significantly reduced. Western blotting and mass spectrometry revealed RCS adducts on select basic residues. Mutation of residues to delineate the physiochemical impact of carbonylation yielded channels with enhanced or reduced cytoplasmic Ca2+ responsiveness. The prototype RCS methylglyoxal increased and then decreased the RyR2 open probability. Methylglyoxal also increased spontaneous Ca2+ release and induced Ca2+ waves in healthy myocytes. Treatment of diabetic rats with RCS scavengers normalized spontaneous and evoked Ca2+ release from the SR, reduced carbonylation of RyR2s, and increased binding of [3H]ryanodine to RyR2s. From these data, we conclude that post-translational modification by RCS contributes to the heterogeneity in RyR2 activity that is seen in experimental diabetes.

Footnotes

  • This work was supported in part by the National Institutes of Health National Heart, Lung, and Blood Institute [Grant HL085061]; the Edna Ittner Research Foundation; the American Diabetes Association [Grant 1-06-RA-11]; and a grant-in-aid from the Ministry of Education, Science, Sports, and Culture of Japan [Grant 18790619].

  • Article, publication date, and citation information can be found at http://molpharm.aspetjournals.org.

    http://dx.doi.org/10.1124/mol.112.078352.

  • ABBREVIATIONS:

    SR
    sarcoplasmic reticulum
    RyR2
    type 2 ryanodine receptor
    DMEM
    Dulbecco's modified Eagle's medium
    RCS
    reactive carbonyl species
    ROS
    reactive oxygen species
    CHAPS
    3-[(3-cholamidopropyl)dimethylammonio]-1-propanesulfonic acid
    MS
    mass spectrometry
    MS/MS
    tandem mass spectrometry
    TOF
    time of flight
    GA
    glycolaldehyde
    STZ
    streptozotocin
    MALDI
    matrix-assisted laser desorption ionization
    MGO
    methylglyoxal
    SERCA2
    sarco(endo)plasmic reticulum Ca2+-ATPase
    Py
    pyridoxamine
    Ag
    aminoguanidine
    cRyR2
    control type 2 ryanodine receptor
    dRyR2
    diabetic type 2 ryanodine receptor
    Ins-DRyR2
    insulin-treated diabetic type 2 ryanodine receptor.

  • Received February 20, 2012.
  • Accepted May 25, 2012.
  • Copyright © 2012 The American Society for Pharmacology and Experimental Therapeutics
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Molecular Pharmacology: 82 (3)
Molecular Pharmacology
Vol. 82, Issue 3
1 Sep 2012
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Research ArticleArticle

Carbonylation Induces Heterogeneity in RyR2 Function

Chun Hong Shao, Chengju Tian, Shouqiang Ouyang, Caronda J. Moore, Fadhel Alomar, Ina Nemet, Alicia D'Souza, Ryoji Nagai, Shelby Kutty, George J. Rozanski, Sasanka Ramanadham, Jaipaul Singh and Keshore R. Bidasee
Molecular Pharmacology September 1, 2012, 82 (3) 383-399; DOI: https://doi.org/10.1124/mol.112.078352

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Research ArticleArticle

Carbonylation Induces Heterogeneity in RyR2 Function

Chun Hong Shao, Chengju Tian, Shouqiang Ouyang, Caronda J. Moore, Fadhel Alomar, Ina Nemet, Alicia D'Souza, Ryoji Nagai, Shelby Kutty, George J. Rozanski, Sasanka Ramanadham, Jaipaul Singh and Keshore R. Bidasee
Molecular Pharmacology September 1, 2012, 82 (3) 383-399; DOI: https://doi.org/10.1124/mol.112.078352
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