Extracellular matrix remodeling following myocardial infarction influences the therapeutic potential of mesenchymal stem cells
Open accessAbstract
Introduction: Although stem cell therapy is a promising treatment for myocardial infarction, the minimal functional improvements observed clinically limit its widespread application. A need exists to maximize the therapeutic potential of these stem cells by first understanding what factors within the infarct microenvironment affect their ability to regenerate the necrotic tissue. In this study, we assessed both differentiation capacity and paracrine signaling as a function of extracellular matrix remodeling after myocardial infarction. Methods: Mechanical and compositional changes to the decellularized infarcted myocardium were characterized to understand how the extracellular environment, specifically, was altered as a function of time after coronary artery ligation in Sprague–Dawley rats. These alterations were first modeled in a polyacrylamide gel system to understand how the variables of composition and stiffness drive mesenchymal stem cell differentiation towards a cardiac lineage. Finally, the paracrine secretome was characterized as a function of matrix remodeling through gene and protein expression and conditioned media studies. Results: The decellularized infarct tissue revealed significant alterations in both the mechanical and compositional properties of the ECM with remodeling following infarction. This altered microenvironment dynamically regulates the potential for early cardiac differentiation. Whereas Nkx2.5 expression is limited in the presence of chronic remodeled matrix of increased stiffness, GATA4 expression is enhanced. In addition, the remodeled matrix promotes the expression of several proangiogenic, prosurvival, antifibrotic, and immunomodulatory growth factors. In particular, an increase in HGF and SDF1 expression and secretion by mesenchymal stem cells can rescue oxidatively stressed cardiomyocytes in vitro. Conclusions: This study demonstrated that decellularization of diseased tissue allows for the exclusive analysis of the remodeled matrix and its ability to influence significantly the cellular phenotype. Characterization of cell fate as a function of myocardial remodeling following infarction is critical in developing the ideal strategy for cell implantation to maximize tissue regeneration and to ultimately reduce the prevalence and severity of heart failure.
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Myocardial infarct triggers remodeling events that stiffen the ECM and change its chemical composition.
“Contrarily, myocardial infarct is known to trigger remodeling events that stiffen the ECM and change its chemical composition; yet when mesenchymal stem cells are seeded on infarcted tissue, the cells secrete higher levels of pro-survival and immunomodulatory growth factors120.”
From Towards organoid culture without Matrigel (2021) · cites this paper as [120]
When mesenchymal stem cells are seeded on infarcted tissue, the cells secrete higher levels of pro-survival and immunomodulatory growth factors.
“Contrarily, myocardial infarct is known to trigger remodeling events that stiffen the ECM and change its chemical composition; yet when mesenchymal stem cells are seeded on infarcted tissue, the cells secrete higher levels of pro-survival and immunomodulatory growth factors120.”
From Towards organoid culture without Matrigel (2021) · cites this paper as [120]
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- Authors
- Sullivan, K. E., Quinn, K. P., Tang, K. M., Georgakoudi, I., & Black, L. D.
- Affiliations
- Tufts University (US)
- Corresponding author
- Black, Lauren Deems
- Venue
- Stem Cell Research & Therapy
- Published
- 2014-01-24
- Volume
- 5
- Issue
- 1
- Pages
- 14-14
- ISSN
- 1757-6512 (ISSN-L)
- PMC
- PMC4055039
- OpenAlex
- W2110165642
- Cited by
- 117
- References
- 81
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 4 · 2023: 6 · 2022: 11 · 2021: 13 · 2020: 14 · 2019: 9 · 2018: 8 · 2017: 16 · 2016: 9 · 2015: 11 · 2014: 5
- FWCI
- 6.85
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Stem Cell Research & Therapy (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Heart, Lung, and Blood Institute (R00HL093358)
- Topics
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
- Keywords
- extracellular matrix remodeling, myocardial infarction, mesenchymal stem cells, cardiac differentiation, paracrine signaling, tissue stiffness, Nkx2.5, GATA4, hepatocyte growth factor, CXCL12, cardiomyocyte oxidative stress, heart failure, stem cell therapy
- MeSH terms
- Homeobox Protein Nkx-2.5, Animals, Cell Differentiation, Cells, Cultured, Extracellular Matrix, Male, Myocardial Infarction, Transcription Factors, Rats, Sprague-Dawley, Hepatocyte Growth Factor, Homeodomain Proteins, Paracrine Communication, Myocytes, Cardiac, Mesenchymal Stem Cell Transplantation, GATA4 Transcription Factor, Rats, Chemokine CXCL12, Mesenchymal Stem Cells
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