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Integrative Physiology

Cortical Bone Stem Cell Therapy Preserves Cardiac Structure and Function After Myocardial InfarctionNovelty and Significance

Thomas E. Sharp, Giana J. Schena, Alexander R. Hobby, Timothy Starosta, Remus M. Berretta, Markus Wallner, Giulia Borghetti, Polina Gross, Daohai Yu, Jaslyn Johnson, Eric Feldsott, Danielle M. Trappanese, Amir Toib, Joseph E. Rabinowitz, Jon C. George, Hajime Kubo, Sadia Mohsin, Steven R. Houser
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https://doi.org/10.1161/CIRCRESAHA.117.311174
Circulation Research. 2017;121:1263-1278
Originally published September 14, 2017
Thomas E. Sharp
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Giana J. Schena
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Alexander R. Hobby
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Timothy Starosta
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Remus M. Berretta
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Markus Wallner
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Giulia Borghetti
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Polina Gross
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Daohai Yu
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Jaslyn Johnson
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Eric Feldsott
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Danielle M. Trappanese
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Amir Toib
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Joseph E. Rabinowitz
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Jon C. George
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Hajime Kubo
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Sadia Mohsin
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Steven R. Houser
From the Department of Physiology, Cardiovascular Research Center (T.E.S., G.J.S., A.R.H., T.S., R.M.B., M.W., G.B., P.G., J.J., E.F., D.M.T., A.T., J.C.G., H.K., S.M., S.R.H.), Department of Clinical Sciences, Temple Clinical Research Institute (D.Y.), and Department of Pharmacology, Center for Translational Medicine (J.E.R.), Temple University Lewis Katz School of Medicine, Philadelphia, PA; Department of Cardiology, Temple University Hospital, Philadelphia, PA (J.C.G.); Section of Pediatric Cardiology, St. Christopher’s Hospital for Children, Philadelphia, PA (A.T.); and Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD (T.S.).
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Abstract

Rationale: Cortical bone stem cells (CBSCs) have been shown to reduce ventricular remodeling and improve cardiac function in a murine myocardial infarction (MI) model. These effects were superior to other stem cell types that have been used in recent early-stage clinical trials. However, CBSC efficacy has not been tested in a preclinical large animal model using approaches that could be applied to patients.

Objective: To determine whether post-MI transendocardial injection of allogeneic CBSCs reduces pathological structural and functional remodeling and prevents the development of heart failure in a swine MI model.

Methods and Results: Female Göttingen swine underwent left anterior descending coronary artery occlusion, followed by reperfusion (ischemia–reperfusion MI). Animals received, in a randomized, blinded manner, 1:1 ratio, CBSCs (n=9; 2×107 cells total) or placebo (vehicle; n=9) through NOGA-guided transendocardial injections. 5–ethynyl–2′deoxyuridine (EdU)—a thymidine analog—containing minipumps were inserted at the time of MI induction. At 72 hours (n=8), initial injury and cell retention were assessed. At 3 months post-MI, cardiac structure and function were evaluated by serial echocardiography and terminal invasive hemodynamics. CBSCs were present in the MI border zone and proliferating at 72 hours post-MI but had no effect on initial cardiac injury or structure. At 3 months, CBSC-treated hearts had significantly reduced scar size, smaller myocytes, and increased myocyte nuclear density. Noninvasive echocardiographic measurements showed that left ventricular volumes and ejection fraction were significantly more preserved in CBSC-treated hearts, and invasive hemodynamic measurements documented improved cardiac structure and functional reserve. The number of EdU+ cardiac myocytes was increased in CBSC- versus vehicle- treated animals.

Conclusions: CBSC administration into the MI border zone reduces pathological cardiac structural and functional remodeling and improves left ventricular functional reserve. These effects reduce those processes that can lead to heart failure with reduced ejection fraction.

  • cell therapy
  • hemodynamics
  • myocardial infarction
  • stem cells
  • swine
  • ventricular remodeling
  • Received April 13, 2017.
  • Revision received August 30, 2017.
  • Accepted September 14, 2017.
  • © 2017 American Heart Association, Inc.

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    Cortical Bone Stem Cell Therapy Preserves Cardiac Structure and Function After Myocardial InfarctionNovelty and Significance
    Thomas E. Sharp, Giana J. Schena, Alexander R. Hobby, Timothy Starosta, Remus M. Berretta, Markus Wallner, Giulia Borghetti, Polina Gross, Daohai Yu, Jaslyn Johnson, Eric Feldsott, Danielle M. Trappanese, Amir Toib, Joseph E. Rabinowitz, Jon C. George, Hajime Kubo, Sadia Mohsin and Steven R. Houser
    Circulation Research. 2017;121:1263-1278, originally published September 14, 2017
    https://doi.org/10.1161/CIRCRESAHA.117.311174

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    Cortical Bone Stem Cell Therapy Preserves Cardiac Structure and Function After Myocardial InfarctionNovelty and Significance
    Thomas E. Sharp, Giana J. Schena, Alexander R. Hobby, Timothy Starosta, Remus M. Berretta, Markus Wallner, Giulia Borghetti, Polina Gross, Daohai Yu, Jaslyn Johnson, Eric Feldsott, Danielle M. Trappanese, Amir Toib, Joseph E. Rabinowitz, Jon C. George, Hajime Kubo, Sadia Mohsin and Steven R. Houser
    Circulation Research. 2017;121:1263-1278, originally published September 14, 2017
    https://doi.org/10.1161/CIRCRESAHA.117.311174
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