ArticleCirculation. Cardiovascular genetics2016
CD36 Is a Matrix Metalloproteinase-9 Substrate That Stimulates Neutrophil Apoptosis and Removal During Cardiac Remodeling.
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Article in Circulation. Cardiovascular genetics, 2016. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 69 papers, 2 of them syntheses that pooled it.
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69citing papers in PubMed, 2 pooled it
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69 citing papers in PubMed, 2 syntheses or guidelines pooled it, 96 citations in OpenAlex.
- Guidelines for measuring cardiac physiology in mice.American journal of physiology. Heart and circulatory physiology · 2018Guideline
- Guidelines for experimental models of myocardial ischemia and infarction.American journal of physiology. Heart and circulatory physiology · 2018Guideline
- Dendritic Cells Derived MMP9 Fuels Sepsis-Induced Cardiac Dysfunction Through JNK/AP1 Driven Pro-Inflammatory Cytokine and Nitric Oxide Storm.Inflammation · 2026Article
- The Fatty Acid Transporter CD36 Mediates Uptake, Biodistribution, and Cardioprotection by Small Extracellular Vesicles From HEK293 Cells.Journal of extracellular vesicles · 2026Article
- Cellular and molecular signals of cardiac wound healing after myocardial infarction.American journal of physiology. Heart and circulatory physiology · 2026Review
- Neutrophil death pathways in myocardial infarction: the balance between injury and repair.Frontiers in immunology · 2026Review
- Efferocytosis in myocardial infarction: the regulatory core from inflammation resolution to cardiac repair.Frontiers in immunology · 2026Review
- From inflammatory effectors to tissue sculptors: non-canonical functions of neutrophils in repair, barrier remodelling and fibrosis.Frontiers in immunology · 2026Review
- Hyperglycemia Induced in Sprague-Dawley Rats Modulates the Expression of CD36 and CD69 During Wound Healing.International journal of molecular sciences · 2025Article
- The role of matrix metalloproteinase expression levels in the pathogenesis of tympanosclerosis.European archives of oto-rhino-laryngology : official journal of the European Federation of Oto-Rhino-Laryngological Societies (EUFOS) : affiliated with the German Society for Oto-Rhino-Laryngology - Head and Neck Surgery · 2025Article
- Adaptive and Pathological Changes of the Cardiac Muscle in a Mouse Model of Renocardiac Syndrome: The Role of Nestin-Positive Cells.International journal of molecular sciences · 2025Article
- Mapping the knowledge of omics in myocardial infarction: A scientometric analysis in R Studio, VOSviewer, Citespace, and SciMAT.Medicine · 2025Article
- Unveiling macrophage dynamics and efferocytosis-related targets in diabetic kidney disease: insights from single-cell and bulk RNA-sequencing.Frontiers in immunology · 2025Article
- The immune checkpoint TIM-3/HMGB-1 axis in myocardial infarction.NPJ cardiovascular health · 2025Article
- FUT8 upregulates CD36 and its core fucosylation to accelerate pericyte-myofibroblast transition through the mitochondrial-dependent apoptosis pathway during AKI-CKD.Molecular medicine (Cambridge, Mass.) · 2024Article
- Macrophage profiling in atherosclerosis: understanding the unstable plaque.Basic research in cardiology · 2024Review
- Network Pharmacology and Experimental Validation to Explore Mechanism of Tetrahydropalmatine on Acute Myocardial Ischemia.Chinese journal of integrative medicine · 2023Article
- The phagocytic role of macrophage following myocardial infarction.Heart failure reviews · 2023Review
- The cardiac wound healing response to myocardial infarction.WIREs mechanisms of disease · 2023Review
- Riding the wave: a quantitative report of electrocardiogram utilization for myocardial infarction confirmation.American journal of physiology. Heart and circulatory physiology · 2022Article
9 more citing papers are in PubMed but not listed here.
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Authors and funding
15 authors at 5 institutions in 1 country.
Kristine Y DeLeon-PennellFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.). kdeleon@umc.edu mllindsey@umc.edu.
Yuan TianFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.).
Bai ZhangFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.).
Courtney A CatesFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.).
Rugmani Padmanabhan IyerFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.).
Presley CannonFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.).
Punit ShahFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.).
Paul AiyetanFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.).
Ganesh V HaladeFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.).
Yonggang MaFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.).
Elizabeth FlynnFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.).
Zhen ZhangFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.).
Yu-Fang JinFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.).
Hui ZhangFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.).
Merry L LindseyFrom the Department of Physiology and Biophysics, Mississippi Center for Heart Research, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., M.L.L.); San Antonio Cardiovascular Proteomics Center, University of Mississippi Medical Center, Jackson (K.Y.D.-P., Y.T., C.A.C., R.P.I., P.C., Y.M., E.F., Y.-F.J., M.L.L.); Department of Electrical and Computer Engineering (Y.-F.J.), The University of Texas at San Antonio, San Antonio; Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, MD (B.Z., P.S., P.A., Z.Z., H.Z.); Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham (G.V.H.); and Research Service, G.V. (Sonny) Montgomery Veterans Affairs Medical Center, Jackson, MS (M.L.L.). kdeleon@umc.edu mllindsey@umc.edu.
Johns Hopkins Medicine · USJohns Hopkins University · USThe University of Texas at San Antonio · USUniversity of Alabama at Birmingham · USJackson Memorial Hospital · US
Funding
STRUCTURAL VASCULAR ADAPTATION OF THE MICROCIRCULATIONP01HL051971 · NHLBI · UNIVERSITY OF MISSISSIPPI MEDICAL CENTER · PI ALEXANDER, BARBARA T · 1993 to 2018
$39.4MThe role of leptin in autoimmune-associated hypertensionP20GM104357 · NIGMS · UNIVERSITY OF MISSISSIPPI MED CTR · PI TAYLOR, ERIN BASSFORD · 2013 to 2022
$23.4MShared Resource CoresP01HL107153 · NHLBI · JOHNS HOPKINS UNIVERSITY · PI HART, GERALD WARREN · 2011 to 2017
$16.8MPATHOBIOLOGY OF OCCLUSIVE VASCULAR DISEASET32HL007446 · NHLBI · UNIVERSITY OF TEXAS HLTH SCIENCE CENTER · PI Jean Chrisostome Bopassa · 1985 to 2026
$8.9MThe Role of Macrophage-derived MMPs in LV RemodelingR01HL075360 · NHLBI · UNIVERSITY OF TEXAS HLTH SCIENCE CENTER · PI LINDSEY, MERRY L. · 2004 to 2018
$5.4MDHA Mechanisms in Obesity-mediated Cardiac Remodeling Post-Myocardial InfarctionR00AT006704 · NCCIH · UNIVERSITY OF ALABAMA AT BIRMINGHAM · PI HALADE, GANESH V · 2013 to 2015
$717kNeutrophil Polarization Following Myocardial InfarctionI01BX000505 · VA · VETERANS HEALTH ADMINISTRATION · PI LINDSEY, MERRY L. · 2009 to 2024
–BLRD VA I01 BX000505Intramural VA VA999999NCCIH NIH HHS R00 AT006704NCCIH NIH HHS R00AT006704NHLBI NIH HHS HHSN268201000032CNHLBI NIH HHS HHSN268201000036CNHLBI NIH HHS HL051971NHLBI NIH HHS N01-HV-00240NHLBI NIH HHS N01-HV-00244NHLBI NIH HHS P01 HL051971NHLBI NIH HHS P01 HL107153NHLBI NIH HHS P01HL107153NHLBI NIH HHS R01 HL075360NHLBI NIH HHS T32 HL007446NIGMS NIH HHS GM104357NIGMS NIH HHS P20 GM104357
Abstract
backgroundAfter myocardial infarction, the left ventricle undergoes a wound healing response that includes the robust infiltration of neutrophils and macrophages to facilitate removal of dead myocytes as well as turnover of the extracellular matrix. Matrix metalloproteinase (MMP)-9 is a key enzyme that regulates post-myocardial infarction left ventricular remodeling. METHODS AND
resultsInfarct regions from wild-type and MMP-9 null mice (n=8 per group) analyzed by glycoproteomics showed that of 541 N-glycosylated proteins quantified, 45 proteins were at least 2-fold upregulated or downregulated with MMP-9 deletion (all P<0.05). Cartilage intermediate layer protein and platelet glycoprotein 4 (CD36) were identified as having the highest fold increase in MMP-9 null mice. By immunoblotting, CD36 but not cartilage intermediate layer protein decreased steadily during the time course post-myocardial infarction, which identified CD36 as a candidate MMP-9 substrate. MMP-9 was confirmed in vitro and in vivo to proteolytically degrade CD36. In vitro stimulation of day 7 post-myocardial infarction macrophages with MMP-9 or a CD36-blocking peptide reduced phagocytic capacity. Dual immunofluorescence revealed concomitant accumulation of apoptotic neutrophils in the MMP-9 null group compared with wild-type group. In vitro stimulation of isolated neutrophils with MMP-9 decreased neutrophil apoptosis, indicated by reduced caspase-9 expression.
conclusionsOur data reveal a new cell-signaling role for MMP-9 through CD36 degradation to regulate macrophage phagocytosis and neutrophil apoptosis.
Indexed as
ApoptosisProteolysisAnimalsCD36 AntigensFemaleGene Expression Regulation, EnzymologicHeart VentriclesMaleMatrix Metalloproteinase 9MiceMice, Mutant StrainsMyocardial InfarctionMyocytes, CardiacNeutrophilsSignal TransductionCD36 AntigensMatrix Metalloproteinase 9Mmp9 protein, mouseextracellular matriximmunoblottinginfarctioninflammationmyocardialproteomics
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