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Current Stem Cell Research & Therapy

Editor-in-Chief

ISSN (Print): 1574-888X
ISSN (Online): 2212-3946

General Review Article

The Use of Mesenchymal Stem Cells and their Derived Extracellular Vesicles in Cardiovascular Disease Treatment

Author(s): Saeideh Gholamzadeh Khoei, Fateme Karimi Dermani, Sara Malih, Nashmin Fayazi and Mohsen Sheykhhasan*

Volume 15, Issue 7, 2020

Page: [623 - 638] Pages: 16

DOI: 10.2174/1574888X15666200501235201

Price: $65

Abstract

Background: Cardiovascular disease (CVD), including disorders of cardiac muscle and vascular, is the major cause of death globally. Many unsuccessful attempts have been made to intervene in the disease's pathogenesis and treatment. Stem cell-based therapies, as a regeneration strategy, cast a new hope for CVD treatment. One of the most well-known stem cells is mesenchymal stem cells (MSCs), classified as one of the adult stem cells and can be obtained from different tissues. These cells have superior properties, such as proliferation and highly specialized differentiation. On the other hand, they have the potential to modulate the immune system and anti-inflammatory activity. One of their most important features is the secreting the extracellular vesicles (EVs) like exosomes (EXOs) as an intercellular communication system mediating the different physiological and pathophysiological affairs.

Methods: In this review study, the importance of MSC and its secretory exosomes for the treatment of heart disease has been together and specifically addressed and the use of these promising natural and accessible agents is predicted to replace the current treatment modalities even faster than we imagine.

Results: MSC derived EXOs by providing a pro-regenerative condition allowing innate stem cells to repair damaged tissues successfully. As a result, MSCs are considered as the appropriate cellular source in regenerative medicine. In the plethora of experiments, MSCs and MSC-EXOs have been used for the treatment and regeneration of heart diseases and myocardial lesions.

Conclusion: Administration of MSCs has been provided a replacement therapeutic option for heart regeneration, obtaining great attention among the basic researcher and the medical doctors.

Keywords: Cardiovascular disease (CVD), Mesenchymal stem cells (MSCs), MSC derived exosomes (MSC-EXOs), cardiac muscle, exosomes, myocardial lesions.

[1]
Abubakar I, Tillmann T, Banerjee A. Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2015; 385(9963): 117-71.
[http://dx.doi.org/10.1016/S0140-6736(14)61682-2] [PMID: 25530442]
[2]
Gaziano TA, Bitton A, Anand S, Abrahams-Gessel S, Murphy A. Growing epidemic of coronary heart disease in low- and middle-income countries. Curr Probl Cardiol 2010; 35(2): 72-115.
[http://dx.doi.org/10.1016/j.cpcardiol.2009.10.002] [PMID: 20109979]
[3]
Niiranen TJ, Vasan RS. Epidemiology of cardiovascular disease: recent novel outlooks on risk factors and clinical approaches. Expert Rev Cardiovasc Ther 2016; 14(7): 855-69.
[http://dx.doi.org/10.1080/14779072.2016.1176528] [PMID: 27057779]
[4]
Mahla RS. Stem cells applications in regenerative medicine and disease therapeutics. Int J Cell Biol 2016.
[http://dx.doi.org/10.1155/2016/6940283]
[5]
Frieedenstein A, Petrakova K, Kurolesova A, Frolova G. He-trotopic of bone marrow. Analysis of precursor cells for oste-ogenic and hematopoetic tissue. Transplantacion 1968; 6(2): 230.
[6]
Marquez-Curtis LA, Janowska-Wieczorek A, McGann LE, Elliott JA. Mesenchymal stromal cells derived from various tissues: Biological, clinical and cryopreservation aspects. Cryobiology 2015; 71(2): 181-97.
[http://dx.doi.org/10.1016/j.cryobiol.2015.07.003] [PMID: 26186998]
[7]
Tabatabaei Qomi R, Sheykhhasan M. Adipose-derived stromal cell in regenerative medicine: A review. World J Stem Cells 2017; 9(8): 107-17.
[http://dx.doi.org/10.4252/wjsc.v9.i8.107] [PMID: 28928907]
[8]
Sheykhhasan M, Wong JKL, Seifalian AM. Human Adipose-Derived Stem Cells with Great Therapeutic Potential. Curr Stem Cell Res Ther 2019; 14(7): 532-48.
[http://dx.doi.org/10.2174/1574888X14666190411121528] [PMID: 30973112]
[9]
Trounson A, Thakar RG, Lomax G, Gibbons D. Clinical trials for stem cell therapies. BMC Med 2011; 9(1): 52.
[http://dx.doi.org/10.1186/1741-7015-9-52] [PMID: 21569277]
[10]
Sheykhhasan M, Manoochehri H, Pourjafar M, Fayazi N. Mesenchymal stem cells as a valuable agent in osteoarthritis treatment. Stem Cell Investig 2018; 5: 41.
[http://dx.doi.org/10.21037/sci.2018.11.04] [PMID: 30596081]
[11]
Sheykhhasan M. Mesenchymal stem cells and platelet derived concentrates in regenerative medicine. J Stem Cell Res Ther 2017; 2(5): 00079.
[12]
Sheykhhasan M, Manoochehri H, Samadi P, Fotouhi-Ardakani R, Kalhor N. Effect of Platelet-rich Plasma and Mesenchymal Stem Cells as Two Biological Alternatives in Rotator Cuff Injury Treatment: A Mini-review. J Mol Med (Berl) 2019; 7(3)
[13]
Ghiasi M, Kalhor N, Tabatabaei Qomi R, Sheykhhasan M. The effects of synthetic and natural scaffolds on viability and proliferation of adipose-derived stem cells. Front Life Sci 2016; 9(1): 32-43.
[http://dx.doi.org/10.1080/21553769.2015.1077477]
[14]
Sheykhhasan M. The perspective on bone marrow-derived mesenchymal stem cells application in regenerative medicine. Am J Transl Res 2015; 2474: 7378.
[15]
Sheykhhasan M, Qomi RT, Ghiasi M. Fibrin scaffolds design-ing in order to human adipose-derived mesenchymal stem cells differentiation to chondrocytes in the presence of TGF-β3. Int J Stem Cells 2015; 8(2): 219-27.
[http://dx.doi.org/10.15283/ijsc.2015.8.2.219] [PMID: 26634070]
[16]
Ghiasi M, Qomi RT, Kalhor N, Sheykhhasan M. Adipose-derived stem cells: An optimized protocol for isolation and proliferation. Acta Med Int 2016; 3(1): 116.
[http://dx.doi.org/10.5530/ami.2016.1.25]
[17]
Sheykhhasan M, Ghiasi M, Pak HB. The assessment of natu-ral scaffolds ability in chondrogenic differentiation of human adipose-derived mesenchymal stem cells. Internet J Med Up-date 2016; 11(2): 11-6.
[http://dx.doi.org/10.4314/ijmu.v11i2.4]
[18]
Castro-Manrreza ME, Montesinos JJ. Immunoregulation by mesenchymal stem cells: biological as-pects and clinical applications. J Immunol Res 2015.
[19]
Liu S, Zhou J, Zhang X, et al. Strategies to optimize adult stem cell therapy for tissue regeneration. Int J Mol Sci 2016; 17(6): 982.
[http://dx.doi.org/10.3390/ijms17060982] [PMID: 27338364]
[20]
Alvarez R, Lee H-L, Wang C-Y, Hong C. Characterization of the osteogenic potential of mesenchymal stem cells from human periodontal ligament based on cell surface markers. Int J Oral Sci 2015; 7(4): 213-9.
[http://dx.doi.org/10.1038/ijos.2015.42] [PMID: 26674423]
[21]
Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8(4): 315-7.
[http://dx.doi.org/10.1080/14653240600855905] [PMID: 16923606]
[22]
Marzban M, Mousavizadeh K, Bakhshayesh M, Vousooghi N, Vakilzadeh G, Torkaman-Boutorabi A. Effect of Multiple Intraperitoneal Injections of Human Bone Marrow Mesenchymal Stem Cells on Cuprizone Model of Multiple Sclerosis. Iran Biomed J 2018; 22(5): 312-21.
[http://dx.doi.org/10.29252/ibj.22.5.312] [PMID: 29409311]
[23]
Bagno L, Hatzistergos KE, Balkan W, Hare JM. Mesenchymal Stem Cell-Based Therapy for Cardiovascular Disease: Progress and Challenges. Mol Ther 2018; 26(7): 1610-23.
[http://dx.doi.org/10.1016/j.ymthe.2018.05.009] [PMID: 29807782]
[24]
Suzuki S, Narita Y, Yamawaki A, et al. Effects of extracellular matrix on differentiation of human bone marrow-derived mesenchymal stem cells into smooth muscle cell lineage: utility for cardiovascular tissue engineering. Cells Tissues Organs (Print) 2010; 191(4): 269-80.
[http://dx.doi.org/10.1159/000260061] [PMID: 19940434]
[25]
Gao F, Chiu SM, Motan DA, Zhang Z, Chen L, Ji HL, et al. Mesenchymal stem cells and immunomodulation: current sta-tus and future prospects. Cell Death Dis 2016; 7(1)e2062
[http://dx.doi.org/10.1038/cddis.2015.327]
[26]
D’souza N, Rossignoli F, Golinelli G, et al. Mesenchymal stem/stromal cells as a delivery platform in cell and gene therapies. BMC Med 2015; 13(1): 186.
[http://dx.doi.org/10.1186/s12916-015-0426-0] [PMID: 26265166]
[27]
Trounson A, McDonald C. Stem cell therapies in clinical trials: progress and challenges. Cell Stem Cell 2015; 17(1): 11-22.
[http://dx.doi.org/10.1016/j.stem.2015.06.007] [PMID: 26140604]
[28]
Schuleri KH, Feigenbaum GS, Centola M, et al. Autologous mesenchymal stem cells produce reverse remodelling in chronic ischaemic cardiomyopathy. Eur Heart J 2009; 30(22): 2722-32.
[http://dx.doi.org/10.1093/eurheartj/ehp265] [PMID: 19586959]
[29]
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 Am Coll Cardiol 2009; 54(24): 2277-86.
[http://dx.doi.org/10.1016/j.jacc.2009.06.055] [PMID: 19958962]
[30]
Camussi G, Deregibus MC, Cantaluppi V. Role of stem-cell-derived microvesicles in the paracrine action of stem cells. Portland Press Ltd. 2013.
[http://dx.doi.org/10.1042/BST20120192]
[31]
Tang YL, Zhao Q, Qin X, et al. Paracrine action enhances the effects of autologous mesenchymal stem cell transplantation on vascular regeneration in rat model of myocardial infarction. Ann Thorac Surg 2005; 80(1): 229-36.
[http://dx.doi.org/10.1016/j.athoracsur.2005.02.072] [PMID: 15975372]
[32]
Dykes IM. Exosomes in cardiovascular medicine. Cardiol Ther 2017; 6(2): 225-37.
[http://dx.doi.org/10.1007/s40119-017-0091-9] [PMID: 28526928]
[33]
Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 2006; 20(9): 1487-95.
[http://dx.doi.org/10.1038/sj.leu.2404296] [PMID: 16791265]
[34]
Arslan F, Lai RC, Smeets MB, et al. Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Res (Amst) 2013; 10(3): 301-12.
[http://dx.doi.org/10.1016/j.scr.2013.01.002] [PMID: 23399448]
[35]
Wang X, Chen Y, Zhao Z, et al. Engineered Exosomes With Ischemic Myocardium-Targeting Peptide for Targeted Therapy in Myocardial Infarction. J Am Heart Assoc 2018; 7(15)e008737
[PMID: 30371236] [http://dx.doi.org/10.1161/JAHA.118.008737]]
[36]
Olvera Lopez E, Jan A. Cardiovascular Disease StatPearls. Treasure Island, FL: StatPearls Publishing StatPearls Publish-ing LLC 2020.
[37]
Nystoriak MA, Bhatnagar A. Cardiovascular Effects and Benefits of Exercise. Front Cardiovasc Med 2018; 5: 135.
[http://dx.doi.org/10.3389/fcvm.2018.00135] [PMID: 30324108]
[38]
Kemp CD, Conte JV. The pathophysiology of heart failure. Cardiovasc Pathol 2012; 21(5): 365-71.
[http://dx.doi.org/10.1016/j.carpath.2011.11.007] [PMID: 22227365]
[39]
Mann DL, Bristow MR. Mechanisms and models in heart failure: the biomechanical model and beyond. Circulation 2005; 111(21): 2837-49.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.104.500546] [PMID: 15927992]
[40]
Yun CW, Lee SH. Enhancement of Functionality and Therapeutic Efficacy of Cell-Based Therapy Using Mesenchymal Stem Cells for Cardiovascular Disease. Int J Mol Sci 2019; 20(4)E982
[PMID: 30813471] [http://dx.doi.org/10.3390/ijms20040982]]
[41]
Wang Y, Zhang L, Li Y, et al. Exosomes/microvesicles from induced pluripotent stem cells deliver cardioprotective miRNAs and prevent cardiomyocyte apoptosis in the ischemic myocardium. Int J Cardiol 2015; 192: 61-9.
[http://dx.doi.org/10.1016/j.ijcard.2015.05.020] [PMID: 26000464]
[42]
Benjamin EJ, Virani SS, Callaway CW, et al. Heart Disease and Stroke Statistics-2018 Update: A Report From the American Heart Association. Circulation 2018; 137(12): e67-e492.
[http://dx.doi.org/10.1161/CIR.0000000000000558] [PMID: 29386200]
[43]
Hass R, Kasper C, Böhm S, Jacobs R. Different populations and sources of human mesenchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal 2011; 9: 12.
[http://dx.doi.org/10.1186/1478-811X-9-12] [PMID: 21569606]
[44]
Chen Y, Xiang LX, Shao JZ, et al. Recruitment of endogenous bone marrow mesenchymal stem cells towards injured liver. J Cell Mol Med 2010; 14(6B): 1494-508.
[http://dx.doi.org/10.1111/j.1582-4934.2009.00912.x] [PMID: 19780871]
[45]
Friedenstein AJ, Chailakhyan RK, Latsinik NV, Panasyuk AF, Keiliss-Borok IV. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 1974; 17(4): 331-40.
[http://dx.doi.org/10.1097/00007890-197404000-00001] [PMID: 4150881]
[46]
Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells science 1999.
[47]
Golpanian S, Wolf A, Hatzistergos KE, Hare JM. Rebuilding the damaged heart: mesenchymal stem cells, cell-based thera-py, and engineered heart tissue. Physiol Rev 2016; 96(3): 1127-68.
[http://dx.doi.org/10.1152/physrev.00019.2015] [PMID: 27335447]
[48]
Rasmusson I, Uhlin M, Le Blanc K, Levitsky V. Mesenchymal stem cells fail to trigger effector functions of cytotoxic T lymphocytes. J Leukoc Biol 2007; 82(4): 887-93.
[http://dx.doi.org/10.1189/jlb.0307140] [PMID: 17609339]
[49]
Ramasamy R, Fazekasova H, Lam EW-F, Soeiro I, Lombardi G, Dazzi F. Mesenchymal stem cells inhibit dendritic cell differentiation and function by preventing entry into the cell cycle. Transplantation 2007; 83(1): 71-6.
[http://dx.doi.org/10.1097/01.tp.0000244572.24780.54] [PMID: 17220794]
[50]
Majumdar MK, Keane-Moore M, Buyaner D, et al. Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J Biomed Sci 2003; 10(2): 228-41.
[http://dx.doi.org/10.1007/BF02256058] [PMID: 12595759]
[51]
Devine SM, Hoffman R. Role of mesenchymal stem cells in hematopoietic stem cell transplantation. Curr Opin Hematol 2000; 7(6): 358-63.
[http://dx.doi.org/10.1097/00062752-200011000-00007] [PMID: 11055509]
[52]
Ringdén O, Uzunel M, Rasmusson I, et al. Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation 2006; 81(10): 1390-7.
[http://dx.doi.org/10.1097/01.tp.0000214462.63943.14] [PMID: 16732175]
[53]
Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol 2008; 8(9): 726-36.
[http://dx.doi.org/10.1038/nri2395] [PMID: 19172693]
[54]
Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005; 105(4): 1815-22.
[http://dx.doi.org/10.1182/blood-2004-04-1559] [PMID: 15494428]
[55]
Giebel B, Kordelas L, Börger V. Clinical potential of mesenchymal stem/stromal cell-derived extracellular vesicles. Stem Cell Investig 2017; 4: 84.
[http://dx.doi.org/10.21037/sci.2017.09.06] [PMID: 29167805]
[56]
Gomes SA, Rangel EB, Premer C, et al. S-nitrosoglutathione reductase (GSNOR) enhances vasculogenesis by mesenchymal stem cells. Proc Natl Acad Sci USA 2013; 110(8): 2834-9.
[http://dx.doi.org/10.1073/pnas.1220185110] [PMID: 23288904]
[57]
Zhang Z, Yang J, Yan W, Li Y, Shen Z, Asahara T. Pretreat-ment of cardiac stem cells with exosomes derived from mes-enchymal stem cells enhances myocardial repair. J Am Heart Assoc 2016; 5(1)e002856
[PMID: 26811168] [http://dx.doi.org/10.1161/JAHA.115.002856]]
[58]
Shadmanfar S, Labibzadeh N, Emadedin M, et al. Intra-articular knee implantation of autologous bone marrow-derived mesenchymal stromal cells in rheumatoid arthritis patients with knee involvement: Results of a randomized, triple-blind, placebo-controlled phase 1/2 clinical trial. Cytotherapy 2018; 20(4): 499-506.
[http://dx.doi.org/10.1016/j.jcyt.2017.12.009] [PMID: 29428486]
[59]
Blanco JF, Villarón EM, Pescador D, et al. Autologous mesenchymal stromal cells embedded in tricalcium phosphate for posterolateral spinal fusion: results of a prospective phase I/II clinical trial with long-term follow-up. Stem Cell Res Ther 2019; 10(1): 63.
[http://dx.doi.org/10.1186/s13287-019-1166-4] [PMID: 30795797]
[60]
Ghoryani M, Shariati-Sarabi Z, Tavakkol-Afshari J, Ghasemi A, Poursamimi J, Mohammadi M. Amelioration of clinical symptoms of patients with refractory rheumatoid arthritis following treatment with autologous bone marrow-derived mesenchymal stem cells: A successful clinical trial in Iran. Biomed Pharmacother 2019; 109: 1834-40.
[http://dx.doi.org/10.1016/j.biopha.2018.11.056] [PMID: 30551438]
[61]
Davis ME, Hsieh PC, Takahashi T, et al. Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. Proc Natl Acad Sci USA 2006; 103(21): 8155-60.
[http://dx.doi.org/10.1073/pnas.0602877103] [PMID: 16698918]
[62]
Delafontaine P, Song Y-H, Li Y. Expression, regulation, and function of IGF-1, IGF-1R, and IGF-1 binding proteins in blood vessels. Arterioscler Thromb Vasc Biol 2004; 24(3): 435-44.
[http://dx.doi.org/10.1161/01.ATV.0000105902.89459.09] [PMID: 14604834]
[63]
Guo J, Zheng D, Li WF, Li HR, Zhang AD, Li ZC. Insulin-like growth factor 1 treatment of MSCs attenuates inflammation and cardiac dysfunction following MI. Inflammation 2014; 37(6): 2156-63.
[http://dx.doi.org/10.1007/s10753-014-9949-3] [PMID: 24942913]
[64]
Jung S, Kim JH, Yim C, Lee M, Kang HJ, Choi D. Therapeutic effects of a mesenchymal stem cell based insulin like growth factor 1/enhanced green fluorescent protein dual gene sorting system in a myocardial infarction rat model. Mol Med Rep 2018; 18(6): 5563-71.
[http://dx.doi.org/10.3892/mmr.2018.9561] [PMID: 30365087]
[65]
Kanda S, Mochizuki Y, Suematsu T, Miyata Y, Nomata K, Kanetake H. Sonic hedgehog induces capillary morphogenesis by endothelial cells through phosphoinositide 3-kinase. J Biol Chem 2003; 278(10): 8244-9.
[http://dx.doi.org/10.1074/jbc.M210635200] [PMID: 12514186]
[66]
Vokes SA, Yatskievych TA, Heimark RL, et al. Hedgehog signaling is essential for endothelial tube formation during vasculogenesis. Development 2004; 131(17): 4371-80.
[http://dx.doi.org/10.1242/dev.01304] [PMID: 15294868]
[67]
Pola R, Ling LE, Aprahamian TR, et al. Postnatal recapitulation of embryonic hedgehog pathway in response to skeletal muscle ischemia. Circulation 2003; 108(4): 479-85.
[http://dx.doi.org/10.1161/01.CIR.0000080338.60981.FA] [PMID: 12860919]
[68]
Roncalli J, Renault M-A, Tongers J, et al. Sonic hedgehog-induced functional recovery after myocardial infarction is enhanced by AMD3100-mediated progenitor-cell mobilization. J Am Coll Cardiol 2011; 57(24): 2444-52.
[http://dx.doi.org/10.1016/j.jacc.2010.11.069] [PMID: 21658566]
[69]
Shi S, Sun J, Meng Q, et al. Sonic hedgehog promotes endothelial differentiation of bone marrow mesenchymal stem cells via VEGF-D. J Thorac Dis 2018; 10(9): 5476-88.
[http://dx.doi.org/10.21037/jtd.2018.09.50] [PMID: 30416797]
[70]
Han J, Kim B, Shin J-Y, et al. Iron oxide nanoparticle-mediated development of cellular gap junction crosstalk to improve mesenchymal stem cells’ therapeutic efficacy for myocardial infarction. ACS Nano 2015; 9(3): 2805-19.
[http://dx.doi.org/10.1021/nn506732n] [PMID: 25688594]
[71]
Spees JL, Olson SD, Whitney MJ, Prockop DJ. Mitochondrial transfer between cells can rescue aerobic respiration. Proc Natl Acad Sci USA 2006; 103(5): 1283-8.
[http://dx.doi.org/10.1073/pnas.0510511103] [PMID: 16432190]
[72]
Bobis-Wozowicz S, Miekus K, Wybieralska E, Jarocha D, Zawisz A, Madeja Z, et al. Genetically modified adipose tissue− derived mesenchymal stem cells overexpressing CXCR4 display increased motility, invasiveness, and homing to bone marrow of NOD/SCID mice. Exp Hematol 2011; 39(6): 686-96.
[73]
Majka M, Sułkowski M, Badyra B, Musiałek P. Concise re-view: mesenchymal stem cells in cardiovascular regeneration: emerging research directions and clinical applications. Stem Cells Transl Med 2017; 6(10): 1859-67.
[http://dx.doi.org/10.1002/sctm.16-0484] [PMID: 28836732]
[74]
Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 2002; 105(1): 93-8.
[http://dx.doi.org/10.1161/hc0102.101442] [PMID: 11772882]
[75]
Moon MH, Kim SY, Kim YJ, et al. Human adipose tissue-derived mesenchymal stem cells improve postnatal neovascularization in a mouse model of hindlimb ischemia. Cell Physiol Biochem 2006; 17(5-6): 279-90.
[http://dx.doi.org/10.1159/000094140] [PMID: 16791003]
[76]
Ohnishi S, Yanagawa B, Tanaka K, et al. Transplantation of mesenchymal stem cells attenuates myocardial injury and dysfunction in a rat model of acute myocarditis. J Mol Cell Cardiol 2007; 42(1): 88-97.
[http://dx.doi.org/10.1016/j.yjmcc.2006.10.003] [PMID: 17101147]
[77]
Hida N, Nishiyama N, Miyoshi S, et al. Novel cardiac precursor-like cells from human menstrual blood-derived mesenchymal cells. Stem Cells 2008; 26(7): 1695-704.
[http://dx.doi.org/10.1634/stemcells.2007-0826] [PMID: 18420831]
[78]
Sato D, Otani H, Enoki C, Fujita M, Minato N, Iwasaka T. Phenotypic modulation and turnover of bone marrow-derived cells after myocardial infarction in rats. Cardiovasc Pathol 2011; 20(3): 146-55.
[http://dx.doi.org/10.1016/j.carpath.2010.04.001] [PMID: 20537926]
[79]
Zhang Z, Wang JA, Xu Y, et al. Menstrual blood derived mesenchymal cells ameliorate cardiac fibrosis via inhibition of endothelial to mesenchymal transition in myocardial infarction. Int J Cardiol 2013; 168(2): 1711-4.
[http://dx.doi.org/10.1016/j.ijcard.2013.03.126] [PMID: 23608402]
[80]
Jin L, Zhang J, Deng Z, et al. Mesenchymal stem cells ameliorate myocardial fibrosis in diabetic cardiomyopathy via the secretion of prostaglandin E2. Stem Cell Res Ther 2020; 11(1): 122.
[http://dx.doi.org/10.1186/s13287-020-01633-7] [PMID: 32183879]
[81]
Kaneko Y, Lee JY, Tajiri N, et al. Translating intracarotid artery transplantation of bone marrow-derived NCS-01 cells for ischemic stroke: Behavioral and histological readouts and mechanistic insights into stem cell therapy. Stem Cells Transl Med 2020; 9(2): 203-20.
[http://dx.doi.org/10.1002/sctm.19-0229] [PMID: 31738023]
[82]
Silva GV, Litovsky S, Assad JA, et al. Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Circulation 2005; 111(2): 150-6.
[http://dx.doi.org/10.1161/01.CIR.0000151812.86142.45] [PMID: 15642764]
[83]
Perin EC, Silva GV, Assad JA, et al. Comparison of intracoronary and transendocardial delivery of allogeneic mesenchymal cells in a canine model of acute myocardial infarction. J Mol Cell Cardiol 2008; 44(3): 486-95.
[http://dx.doi.org/10.1016/j.yjmcc.2007.09.012] [PMID: 18061611]
[84]
Zhao J-J, Liu XC, Kong F, et al. Bone marrow mesenchymal stem cells improve myocardial function in a swine model of acute myocardial infarction. Mol Med Rep 2014; 10(3): 1448-54.
[http://dx.doi.org/10.3892/mmr.2014.2378] [PMID: 25060678]
[85]
Rabbani S, Soleimani M, Sahebjam M, et al. Effects of endo-thelial and mesenchymal stem cells on improving myocardial function in a sheep animal model. J Tehran Heart Cent 2017; 12(2): 65-71.
[PMID: 28828021]
[86]
Lan X, Wang G, Xu X, et al. Stromal Cell-Derived Factor-1 Mediates Cardiac Allograft Tolerance Induced by Human Endometrial Regenerative Cell-Based Therapy. Stem Cells Transl Med 2017; 6(11): 1997-2008.
[http://dx.doi.org/10.1002/sctm.17-0091] [PMID: 28941322]
[87]
Pandey AC, Lancaster JJ, Harris DT, Goldman S, Juneman E. Cellular therapeutics for heart failure: focus on mesenchymal stem cells. Stem Cells Int 2017.
[http://dx.doi.org/10.1155/2017/9640108]
[88]
Kamdar F, John R, Eckman P, Colvin-Adams M, Shumway SJ, Liao K. Postcardiac transplant survival in the current era in patients receiving continuous-flow left ventricular assist devices. J Thorac Cardiovasc Surg 2013; 145(2): 575-81.
[http://dx.doi.org/10.1016/j.jtcvs.2012.09.095] [PMID: 23321132]
[89]
Butler J, Epstein SE, Greene SJ, et al. Intravenous allogeneic mesenchymal stem cells for nonischemic cardiomyopathy: safety and efficacy results of a phase II-A randomized trial. Circ Res 2017; 120(2): 332-40.
[http://dx.doi.org/10.1161/CIRCRESAHA.116.309717] [PMID: 27856497]
[90]
Hare JM, Fishman JE, Gerstenblith G, et al. Comparison of allogeneic vs autologous bone marrow–derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial. JAMA 2012; 308(22): 2369-79.
[http://dx.doi.org/10.1001/jama.2012.25321] [PMID: 23117550]
[91]
Patel AN, Mittal S, Turan G, et al. REVIVE trial: retrograde delivery of autologous bone marrow in patients with heart failure. Stem Cells Transl Med 2015; 4(9): 1021-7.
[http://dx.doi.org/10.5966/sctm.2015-0070] [PMID: 26217065]
[92]
Pandey AC, Semon JA, Kaushal D, et al. MicroRNA profiling reveals age-dependent differential expression of nuclear factor κB and mitogen-activated protein kinase in adipose and bone marrow-derived human mesenchymal stem cells. Stem Cell Res Ther 2011; 2(6): 49.
[http://dx.doi.org/10.1186/scrt90] [PMID: 22169120]
[93]
Chen S-L, Fang WW, Qian J, et al. Improvement of cardiac function after transplantation of autologous bone marrow mesenchymal stem cells in patients with acute myocardial infarction. Chin Med J (Engl) 2004; 117(10): 1443-8.
[PMID: 15498362]
[94]
Chen SL, Fang WW, Ye F, et al. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am J Cardiol 2004; 94(1): 92-5.
[http://dx.doi.org/10.1016/j.amjcard.2004.03.034] [PMID: 15219514]
[95]
Ruan W, Pan C-Z, Huang G-Q, Li Y-L, Ge J-B, Shu X-H. Assessment of left ventricular segmental function after autologous bone marrow stem cells transplantation in patients with acute myocardial infarction by tissue tracking and strain imaging. Chin Med J (Engl) 2005; 118(14): 1175-81.
[PMID: 16117862]
[96]
Roncalli J, Mouquet F, Piot C, et al. Intracoronary autologous mononucleated bone marrow cell infusion for acute myocardial infarction: results of the randomized multicenter BONAMI trial. Eur Heart J 2011; 32(14): 1748-57.
[http://dx.doi.org/10.1093/eurheartj/ehq455] [PMID: 21127322]
[97]
Houtgraaf JH, den Dekker WK, van Dalen BM, et al. First experience in humans using adipose tissue-derived regenerative cells in the treatment of patients with ST-segment elevation myocardial infarction. J Am Coll Cardiol 2012; 59(5): 539-40.
[http://dx.doi.org/10.1016/j.jacc.2011.09.065] [PMID: 22281257]
[98]
Lee J-W, Lee S-H, Youn Y-J, et al. A randomized, open-label, multicenter trial for the safety and efficacy of adult mesenchymal stem cells after acute myocardial infarction. J Korean Med Sci 2014; 29(1): 23-31.
[http://dx.doi.org/10.3346/jkms.2014.29.1.23] [PMID: 24431901]
[99]
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. JAMA 2014; 311(1): 62-73.
[http://dx.doi.org/10.1001/jama.2013.282909] [PMID: 24247587]
[100]
Gao LR, Chen Y, Zhang NK, et al. Intracoronary infusion of Wharton’s jelly-derived mesenchymal stem cells in acute myocardial infarction: double-blind, randomized controlled trial. BMC Med 2015; 13(1): 162.
[http://dx.doi.org/10.1186/s12916-015-0399-z] [PMID: 26162993]
[101]
Chullikana A, Majumdar AS, Gottipamula S, et al. Randomized, double-blind, phase I/II study of intravenous allogeneic mesenchymal stromal cells in acute myocardial infarction. Cytotherapy 2015; 17(3): 250-61.
[http://dx.doi.org/10.1016/j.jcyt.2014.10.009] [PMID: 25484310]
[102]
Mathiasen AB, Qayyum AA, Jørgensen 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). Eur Heart J 2015; 36(27): 1744-53.
[http://dx.doi.org/10.1093/eurheartj/ehv136] [PMID: 25926562]
[103]
Mathiasen AB, Qayyum AA, Jørgensen E, Helqvist S, Kofoed KF, Haack‐Sørensen M, et al. Bone marrow‐derived mesen-chymal stromal cell treatment in patients with ischaemic heart failure: final 4‐year follow‐up of the MSC‐HF trial. Eur Heart J 2015; 36(27): 1744-53.
[http://dx.doi.org/10.1093/eurheartj/ehv136] [PMID: 25926562]
[104]
Gao LR, Pei XT, Ding QA, et al. A critical challenge: dosage-related efficacy and acute complication intracoronary injection of autologous bone marrow mesenchymal stem cells in acute myocardial infarction. Int J Cardiol 2013; 168(4): 3191-9.
[http://dx.doi.org/10.1016/j.ijcard.2013.04.112] [PMID: 23651816]
[105]
Bartolucci J, Verdugo FJ, González PL, et al. Safety and effi-cacy of the intravenous infusion of umbilical cord mesen-chymal stem cells in patients with heart failure: a phase 1/2 randomized controlled trial (RIMECARD trial [randomized clinical trial of intravenous infusion umbilical cord mesen-chymal stem cells on cardiopathy]). Circ Res 2017; 121(10): 1192-204.
[http://dx.doi.org/10.1161/CIRCRESAHA.117.310712] [PMID: 28974553]
[106]
Bolli R, Hare JM, Henry TD, et al. Cardiovascular Cell Therapy Research Network (CCTRN). Rationale and Design of the SENECA (StEm cell iNjECtion in cAncer survivors) Trial. Am Heart J 2018; 201: 54-62.
[http://dx.doi.org/10.1016/j.ahj.2018.02.009] [PMID: 29910056]
[107]
Paitazoglou C, Bergmann MW, Vrtovec B, et al. Rationale and design of the European multicentre study on Stem Cell therapy in IschEmic Non-treatable Cardiac diseasE (SCIENCE). Eur J Heart Fail 2019; 21(8): 1032-41.
[http://dx.doi.org/10.1002/ejhf.1412] [PMID: 30790396]
[108]
Xu J-Y, Qian H-Y, Huang P-S, Xu J, Xiong Y-Y, Jiang W-Y, et al. Transplantation efficacy of autologous bone marrow mesen-chymal stem cells combined with atorvastatin for acute myo-cardial infarction (TEAM-AMI): rationale and design of a ran-domized, double-blind, placebo-controlled, multi-center, Phase II TEAM-AMI trial. Regen Med 2019.
[109]
Guijarro D, Lebrin M, Lairez O, et al. Intramyocardial transplantation of mesenchymal stromal cells for chronic myocardial ischemia and impaired left ventricular function: Results of the MESAMI 1 pilot trial. Int J Cardiol 2016; 209: 258-65.
[http://dx.doi.org/10.1016/j.ijcard.2016.02.016] [PMID: 26901787]
[110]
White IA, Sanina C, Balkan W, Hare JM. Mesenchymal Stem Cells in Cardiology. Methods Mol Biol 2016; 1416: 55-87.
[http://dx.doi.org/10.1007/978-1-4939-3584-0_4] [PMID: 27236666]
[111]
Huang L, Ma W, Ma Y, Feng D, Chen H, Cai B. Exosomes in mesenchymal stem cells, a new therapeutic strategy for cardiovascular diseases? Int J Biol Sci 2015; 11(2): 238-45.
[http://dx.doi.org/10.7150/ijbs.10725] [PMID: 25632267]
[112]
Dougherty JA, Mergaye M, Kumar N, Chen C-A, Angelos MG, Khan M. Potential role of exosomes in mending a broken heart: nanoshuttles propelling future clinical therapeutics forward. Stem Cells Int 2017.
[http://dx.doi.org/10.1155/2017/5785436]
[113]
Colombo M, Raposo G, Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 2014; 30: 255-89.
[http://dx.doi.org/10.1146/annurev-cellbio-101512-122326] [PMID: 25288114]
[114]
Khan M, Kishore R. Stem cell exosomes: cell-freetherapy for organ repair. Adult Stem Cells 2017; pp. 315-21.
[115]
Vrijsen KR, Maring JA, Chamuleau SA, et al. Exosomes from cardiomyocyte progenitor cells and mesenchymal stem cells stimulate angiogenesis via EMMPRIN. Adv Healthc Mater 2016; 5(19): 2555-65.
[http://dx.doi.org/10.1002/adhm.201600308] [PMID: 27570124]
[116]
Lai RC, Arslan F, Lee MM, et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res (Amst) 2010; 4(3): 214-22.
[http://dx.doi.org/10.1016/j.scr.2009.12.003] [PMID: 20138817]
[117]
Bian S, Zhang L, Duan L, Wang X, Min Y, Yu H. Extracellular vesicles derived from human bone marrow mesenchymal stem cells promote angiogenesis in a rat myocardial infarction model. J Mol Med (Berl) 2014; 92(4): 387-97.
[http://dx.doi.org/10.1007/s00109-013-1110-5] [PMID: 24337504]
[118]
Teng X, Chen L, Chen W, Yang J, Yang Z, Shen Z. Mesen-chymal stem cell-derived exosomes improve the microenvi-ronment of infarcted myocardium contributing to angiogenesis and anti-inflammation. Cell Physiol Biochem 2015; 37(6): 2415-24.
[http://dx.doi.org/10.1159/000438594] [PMID: 26646808]
[119]
Lv K, Li Q, Zhang L, et al. Incorporation of small extracellular vesicles in sodium alginate hydrogel as a novel therapeutic strategy for myocardial infarction. Theranostics 2019; 9(24): 7403-16.
[http://dx.doi.org/10.7150/thno.32637] [PMID: 31695776]
[120]
Liu X, Li X, Zhu W, et al. Exosomes from mesenchymal stem cells overexpressing MIF enhance myocardial repair. J Cell Physiol 2020.
[http://dx.doi.org/10.1002/jcp.29456] [PMID: 31960418]
[121]
Ma J, Zhao Y, Sun L, et al. Exosomes derived from AKt‐modified human umbilical cord mesenchymal stem cells improve cardiac regeneration and promote angiogenesis via activating platelet‐derived growth factor D. Stem Cells Transl Med 2017; 6(1): 51-9.
[http://dx.doi.org/10.5966/sctm.2016-0038] [PMID: 28170176]
[122]
Bobis-Wozowicz S, Kmiotek K, Kania K, et al. Diverse impact of xeno-free conditions on biological and regenerative properties of hUC-MSCs and their extracellular vesicles. J Mol Med (Berl) 2017; 95(2): 205-20.
[http://dx.doi.org/10.1007/s00109-016-1471-7] [PMID: 27638341]
[123]
He J-G, Xie Q-L, Li B-B, Zhou L, Yan D. Exosomes derived from IDO1-overexpressing rat bone marrow mesenchymal stem cells promote immunotolerance of cardiac allografts. Cell Transplant 2018; 27(11): 1657-83.
[http://dx.doi.org/10.1177/0963689718805375] [PMID: 30311501]
[124]
Sun X, Shan A, Wei Z, Xu B. Intravenous mesenchymal stem cell-derived exosomes ameliorate myocardial inflammation in the dilated cardiomyopathy. Biochem Biophys Res Commun 2018; 503(4): 2611-8.
[http://dx.doi.org/10.1016/j.bbrc.2018.08.012] [PMID: 30126637]
[125]
Ju C, Li Y, Shen Y, et al. Transplantation of cardiac mesen-chymal stem cell-derived exosomes for angiogenesis. J Cardiovasc Transl Res 2018; 11(5): 429-37.
[http://dx.doi.org/10.1007/s12265-018-9824-y] [PMID: 30276617]

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