Progress in application of mesenchymal stem cells in treatment of acute myocardial infarction

doi:10.16352/j.issn.1001-6325.2023.01.0021

Abstract

Abstract: Acute myocardial infarction (AMI) is an ischemic myocardial necrosis caused by coronary artery occlusion, which can't be self-repaired through cardiomyocyte regeneration. The necrotic myocardium is replaced by fibrous scars during ventricular remodeling, ultimately leading to heart failure. The safety and efficacy of mesenchymal stem cells (MSCs) transplantation after AMI have been demonstrated by numerous preclinical and clinical studies. MSCs are composed of heterogeneous cells with multi-directional differentiation potential, which can regulate oxidative stress, and secrete a variety of cytokines and growth factors. After being implanted in vivo, MSCs play their roles in immunomodulatory, angiogenesis, anti-inflammatory, and anti-apoptosis through trans-differentiation, cell fusion, and paracrine. Currently, there has been a variety of access to implant MSCs, including intramyocardial injection, intracoronary infusion, and intravenous injection. In addition, the dose and timing of transplantation are also important factors affecting the therapeutic effect of MSCs. However, the low retention and survival rates of MSCs in infarcted myocardium after being transplanted limit their further effect and hinder their clinical translation. In recent years, new concepts, strategies, technologies, and methods for MSCs treatment have been proposed, including cell preconditioning, optimization of the infract local microenvironment, combined gene therapy or tissue engineering technology, exosome infusion, and targeted transplantation of stem cells and their exosomes, which significantly improve the transplantation efficiency and therapeutic effect of MSCs, and open a new chapter for the research and transformation of stem cells to repair the infarcted myocardium. This article reviews the progress of MSCs in repairing myocardial infarction in recent years.

Key words: mesenchymal stem cells, myocardial infarction, exosome

CLC Number:

R541.4

JIANG Yu, QIAN Haiyan. Progress in application of mesenchymal stem cells in treatment of acute myocardial infarction[J]. Basic & Clinical Medicine, 2023, 43(1): 21-29.

0
/ / Recommend

Add to citation manager EndNote|Reference Manager|ProCite|BibTeX|RefWorks

URL: http://journal11.magtechjournal.com/Jwk_jcyxylc/EN/10.16352/j.issn.1001-6325.2023.01.0021

http://journal11.magtechjournal.com/Jwk_jcyxylc/EN/Y2023/V43/I1/21

References

[1] Rojas-Rios P, Gonzalez-Reyes A. Concise review: The plasticity of stem cell niches: a general property behind tissue homeostasis and repair[J]. Stem Cells, 2014, 32: 852-859.
[2] Jackson KA, Mi T, Goodell MA. Hematopoietic potential of stem cells isolated from murine skeletal muscle[J]. Proc Natl Acad Sci U S A, 1999, 96: 14482-14486.
[3] Krause DS, Theise ND, Collector MI, et al. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell[J]. Cell, 2001, 105: 369-377.
[4] Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors[J]. Cell, 2006, 126: 663-676.
[5] Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells[J]. Science, 1999, 284: 143-147.
[6] Hodgkinson CP, Bareja A, Gomez JA, et al. Emerging concepts in paracrine mechanisms in regenerative cardiovascular medicine and biology[J]. Circ Res, 2016, 118: 95-107.
[7] Bergmann O, Bhardwaj RD, Bernard S, et al. Evidence for cardiomyocyte renewal in humans[J]. Science, 2009, 324: 98-102.
[8] Beltrami AP, Urbanek K, Kajstura J, et al. Evidence that human cardiac myocytes divide after myocardial infarction[J]. N Engl J Med, 2001, 344: 1750-1757.
[9] Yang YJ, Qian HY, Huang J, et al. Atorvastatin treatment improves survival and effects of implanted mesenchymal stem cells in post-infarct swine hearts[J]. Eur Heart J, 2008, 29: 1578-1590.
[10] Murry CE, Soonpaa MH, Reinecke H, et al. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts[J]. Nature, 2004, 428: 664-668.
[11] Nygren JM, Jovinge S, Breitbach M, et al. Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation[J]. Nat Med, 2004, 10: 494-501.
[12] Wu JM, Hsueh YC, Ch'ang HJ, et al. Circulating cells contribute to cardiomyocyte regeneration after injury[J]. Circ Res, 2015, 116: 633-641.
[13] Gnecchi M, Zhang Z, Ni A, et al. Paracrine mechanisms in adult stem cell signaling and therapy[J]. Circ Res, 2008, 103: 1204-1219.
[14] Tomita S, Li RK, Weisel RD, et al. Autologous transplantation of bone marrow cells improves damaged heart function[J]. Circulation, 1999, 100: II247-256.
[15] Mathiasen AB, Qayyum AA, Jorgensen E, et al. Bone marrow-derived mesenchymal stromal cell treatment in patients with severe ischaemic heart failure: a randomized placebo-controlled trial (MSC-HF trial)[J]. Eur Heart J, 2015, 36: 1744-1753.
[16] Heldman AW, DiFede DL, Fishman JE, et al. Transendocardial mesenchymal stem cells and mononuclear bone marrow cells for ischemic cardiomyopathy: the TAC-HFT randomized trial[J]. JAMA, 2014, 311: 62-73.
[17] Bartunek J, Behfar A, Dolatabadi D, et al. Cardiopoietic stem cell therapy in heart failure: the C-CURE (cardiopoietic stem cell therapy in heart failure) multicenter randomized trial with lineage-specified biologics[J]. J Am Coll Cardiol, 2013, 61: 2329-2338.
[18] Perin EC, Borow KM, Silva GV, et al. A phase II dose-escalation study of allogeneic mesenchymal precursor cells in patients with ischemic or nonischemic heart failure[J]. Circ Res, 2015, 117: 576-584.
[19] Hare JM, Traverse JH, Henry TD, et al. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction[J]. J Am Coll Cardiol, 2009, 54: 2277-2286.
[20] Pompilio G, Nigro P, Bassetti B, et al. Bone marrow cell therapy for ischemic heart disease: the never ending story[J]. Circ Res, 2015, 117: 490-493.
[21] Teng CJ, Luo J, Chiu RC, et al. Massive mechanical loss of microspheres with direct intramyocardial injection in the beating heart: implications for cellular cardiomyoplasty[J]. J Thorac Cardiovasc Surg, 2006, 132: 628-632.
[22] Zhang H, Chen H, Wang W, et al. Cell survival and redistribution after transplantation into damaged myocardium[J]. J Cell Mol Med, 2010, 14: 1078-1082.
[23] Zhang H, Song P, Tang Y, et al. Injection of bone marrow mesenchymal stem cells in the borderline area of infarcted myocardium: heart status and cell distribution[J]. J Thorac Cardiovasc Surg, 2007, 134: 1234-1240.
[24] Kehat I, Khimovich L, Caspi O, et al. Electromechanical integration of cardiomyocytes derived from human embryonic stem cells[J]. Nat Biotechnol, 2004, 22: 1282-1289.
[25] Garot J, Unterseeh T, Teiger E, et al. Magnetic reson-ance imaging of targeted catheter-based implantation of myogenic precursor cells into infarcted left ventricular myocardium[J]. J Am Coll Cardiol, 2003, 41: 1841-1846.
[26] Dick AJ, Guttman MA, Raman VK, et al. Magnetic resonance fluoroscopy allows targeted delivery of mesenchymal stem cells to infarct borders in Swine[J]. Circulation, 2003, 108: 2899-2904.
[27] Thompson CA, Nasseri BA, Makower J, et al. Percutaneous transvenous cellular cardiomyoplasty. A novel nonsurgical approach for myocardial cell transplantation[J]. J Am Coll Cardiol, 2003, 41: 1964-1971.
[28] Strauer BE, Brehm M, Zeus T, et al. Intracoronary, human autologous stem cell transplantation for myocardial regeneration following myocardial infarction[J]. Dtsch Med Wochenschr, 2001, 126: 932-938.
[29] Mayfield AE, Tilokee EL, Latham N, et al. The effect of encapsulation of cardiac stem cells within matrix-enriched hydrogel capsules on cell survival, post-ischemic cell retention and cardiac function[J]. Biomaterials, 2014, 35: 133-142.
[30] Askari AT, Unzek S, Popovic ZB, et al. Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy[J]. Lancet, 2003, 362: 697-703.
[31] Zhang M, Mal N, Kiedrowski M, et al. SDF-1 expression by mesenchymal stem cells results in trophic support of cardiac myocytes after myocardial infarction[J]. FASEB J, 2007, 21: 3197-3207.
[32] Taghavi S, George JC. Homing of stem cells to ischemic myocardium[J]. Am J Transl Res, 2013, 5: 404-411.
[33] Vicario J, Campos C, Piva J, et al. Transcoronary sinus administration of autologous bone marrow in patients with chronic refractory stable angina Phase 1[J]. Cardiovasc Radiat Med, 2004, 5: 71-76.
[34] Halkos ME, Zhao ZQ, Kerendi F, et al. Intravenous infusion of mesenchymal stem cells enhances regional perfusion and improves ventricular function in a porcine model of myocardial infarction[J]. Basic Res Cardiol, 2008, 103: 525-536.
[35] Hashemi SM, Ghods S, Kolodgie FD, et al. A placebo controlled, dose-ranging, safety study of allogenic mesenchymal stem cells injected by endomyocardial delivery after an acute myocardial infarction[J]. Eur Heart J, 2008, 29: 251-259.
[36] Lee ST, White AJ, Matsushita S, et al. Intramyocardial injection of autologous cardiospheres or cardiosphere-derived cells preserves function and minimizes adverse ventricular remodeling in pigs with heart failure post-myocardial infarction[J]. J Am Coll Cardiol, 2011, 57: 455-465.
[37] Traverse JH, Henry TD, Pepine CJ, et al. Effect of the use and timing of bone marrow mononuclear cell delivery on left ventricular function after acute myocardial infarc-tion: the TIME randomized trial[J]. JAMA, 2012, 308: 2380-2389.
[38] Traverse JH, Henry TD, Ellis SG, et al. Effect of intracoronary delivery of autologous bone marrow mononuclear cells 2 to 3 weeks following acute myocardial infarction on left ventricular function: the LateTIME randomized trial[J]. JAMA, 2011, 306: 2110-2119.
[39] Hou JF, Zhang H, Yuan X, et al. In vitro effects of low-level laser irradiation for bone marrow mesenchymal stem cells: proliferation, growth factors secretion and myogenic differentiation[J]. Lasers Surg Med, 2008, 40: 726-733.
[40] Mosser DD, Caron AW, Bourget L, et al. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis[J]. Mol Cell Biol, 1997, 17: 5317-5327.
[41] Li N, Zhang Q, Qian H, et al. Atorvastatin induces autophagy of mesenchymal stem cells under hypoxia and serum deprivation conditions by activating the mitogen-activated protein kinase/extracellular signal-regulated kinase pathway[J]. Chin Med J (Engl), 2014, 127: 1046-1051.
[42] Chandra M, Surendra K, Kapoor R K, et al. Oxidant stress mechanisms in heart failure[J]. Boll Chim Farm, 2000, 139: 149-152.
[43] Gurusamy N, Ray D, Lekli I, et al. Red wine antioxidant resveratrol-modified cardiac stem cells regenerate infarcted myocardium[J]. J Cell Mol Med, 2010, 14: 2235-2239.
[44] Drowley L, Okada M, Beckman S, et al. Cellular antioxidant levels influence muscle stem cell therapy[J]. Mol Ther, 2010, 18: 1865-1873.
[45] Stanley BA, Sivakumaran V, Shi S, et al. Thioredoxin reductase-2 is essential for keeping low levels of H(2)O(2) emission from isolated heart mitochondria[J]. J Biol Chem, 2011, 286: 33669-33677.
[46] Retuerto MA, Schalch P, Patejunas G, et al. Angiogenic pretreatment improves the efficacy of cellular cardiomyoplasty performed with fetal cardiomyocyte implantation[J]. J Thorac Cardiovasc Surg, 2004, 127: 1041-1049; discussion 1049-1051.
[47] Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy[J]. Nat Rev Cancer, 2008, 8: 592-603.
[48] Yang YJ, Qian HY, Huang J, et al. Combined therapy with simvastatin and bone marrow-derived mesenchymal stem cells increases benefits in infarcted swine hearts[J]. Arterioscler Thromb Vasc Biol, 2009, 29: 2076-2082.
[49] Han XJ, Li H, Liu CB, et al. Guanxin Danshen Formulation improved the effect of mesenchymal stem cells transplantation for the treatment of myocardial infarction probably via enhancing the engraftment[J]. Life Sci, 2019, 233: 116740.
[50] Hu S, Huang M, Nguyen PK, et al. Novel microRNA prosurvival cocktail for improving engraftment and function of cardiac progenitor cell transplantation[J]. Circulation, 2011, 124: S27-34.
[51] Ong SG, Lee WH, Huang M, et al. Cross talk of combined gene and cell therapy in ischemic heart disease: role of exosomal microRNA transfer[J]. Circulation, 2014, 130: S60-69.
[52] Langer R, Tirrell DA. Designing materials for biology and medicine[J]. Nature, 2004, 428: 487-492.
[53] Geckil H, Xu F, Zhang X, et al. Engineering hydrogels as extracellular matrix mimics[J]. Nanomedicine (Lond), 2010, 5: 469-484.
[54] Kutschka I, Chen IY, Kofidis T, et al. Collagen matrices enhance survival of transplanted cardiomyoblasts and contribute to functional improvement of ischemic rat hearts[J]. Circulation, 2006, 114: I167-173.
[55] Sekine H, Shimizu T, Hobo K, et al. Endothelial cell coculture within tissue-engineered cardiomyocyte sheets enhances neovascularization and improves cardiac function of ischemic hearts[J]. Circulation, 2008, 118: S145-152.
[56] Lai RC, Arslan F, Lee MM, et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury[J]. Stem Cell Res, 2010, 4: 214-222.
[57] Sluijter JP, Verhage V, Deddens J C, et al. Microvesicles and exosomes for intracardiac communication[J]. Cardiovasc Res, 2014, 102: 302-311.
[58] Yu B, Zhang X, Li X. Exosomes derived from mesenchymal stem cells[J]. Int J Mol Sci, 2014, 15: 4142-4157.
[59] Teng X, Chen L, Chen W, et al. Mesenchymal stem cell-derived exosomes improve the microenvironment of infarc-ted myocardium contributing to angiogenesis and anti-inflammation[J]. Cell Physiol Biochem, 2015, 37: 2415-2424.
[60] Shao L, Zhang Y, Lan B, et al. miRNA-sequence indicates that mesenchymal stem cells and exosomes have similar mechanism to enhance cardiac repair[J]. Biomed Res Int, 2017, 2017: 4150705.
[61] Ma T, Chen Y, Chen Y, et al. microRNA-132, delivered by mesenchymal stem cell-derived exosomes, promote angiogenesis in myocardial infarction[J]. Stem Cells Int, 2018, 2018: 3290372.
[62] Wei Z, Qiao S, Zhao J, et al. miRNA-181a over-expression in mesenchymal stem cell-derived exosomes influenced inflammatory response after myocardial ischemia-reperfu-sion injury[J]. Life Sci, 2019, 232: 116632.
[63] Xu R, Zhang F, Chai R, et al. Exosomes derived from pro-inflammatory bone marrow-derived mesenchymal stem cells reduce inflammation and myocardial injury via mediating macrophage polarization[J]. J Cell Mol Med, 2019, 23: 7617-7631.
[64] Huang P, Wang L, Li Q, et al. Atorvastatin enhances the therapeutic efficacy of mesenchymal stem cells-derived exosomes in acute myocardial infarction via up-regulating long non-coding RNA H19[J]. Cardiovasc Res, 2020, 116: 353-367.
[65] Sun SJ, Wei R, Li F, et al. Mesenchymal stromal cell-derived exosomes in cardiac regeneration and repair[J]. Stem Cell Reports, 2021, 16: 1662-1673.