Where are Cell-Based Therapies Heading? Current Limitations and Future Directions
DOI:
https://doi.org/10.17140/HROJ-4-144Keywords:
Congestive heart failure (CHF), Myocardial Infarction (MI), Adult stem cells, Mesenchymal stem cells (MSCs), Cardiac stem cells (CSCs), Cardiosphere-derived cells (CDCs)Abstract
Congestive heart failure (CHF) secondary to chronic coronary artery disease is a major cause
of morbidity and mortality worldwide. Its prevalence is increasing despite advances in medical
and device therapies. Adult stem cell therapies have emerged as a promising treatment generating
new cardiomyocytes and vessels, and are anticipated to reverse functional deterioration in
patients with congestive heart failure for whom heart transplantation is the only cure. This field
was enthusiastically studied in last two decades, revealing that the major beneficial outcomes
from cell therapy are associated with paracrine effects rather than direct differentiation. Accordingly,
paracrine factors (e.g., growth factors, cytokines and microRNAs) secreted from
stem cells reduce scar volume and myocyte apoptosis, increase myocyte proliferation and activate
endogenous cardiac stem cells to produce new myocytes. Moreover, functional efficacy
of progenitor cells isolated from the bone marrow, adipose tissue and the heart have shown
promising effects in preclinical animal models. These convincing results led to the initiation of
clinical trials using autologous and allogeneic stem cells, and progenitor cells. Although clinical
trials demonstrated their safety in humans, therapeutic efficacy is still inconclusive. This
review discusses the progress and limitations of cell-based therapies and alternative solutions
for future advancement.
KEY WORDS:; ; ;
; ; .
References
Mozaffarian D, Benjamin EJ, Go AS, et al; American Heart Association Statistics C, Stroke Statistics S. Heart disease and stroke statistics--2015 update: A report from the american heart association. Circulation. 2015; 131: e29-322. doi: 10.1161/ CIR.0000000000000152
Suzuki G. Translational research of adult stem cell therapy. World J Cardiol. 2015; 7: 707-718. doi: 10.4330/wjc.v7.i11.707
Anversa P, Kajstura J, Rota M, Leri A. Regenerating new heart with stem cells. J Clin Invest. 2013; 123: 62-70. doi: 10.1172/ JCI63068
Braunwald E. The war against heart failure: The lancet lecture. Lancet. 2015; 385: 812-824. doi: 10.1016/S0140- 6736(14)61889-4
Malliaras K, Zhang Y, Seinfeld J, et al. Cardiomyocyte proliferation and progenitor cell recruitment underlie thera-peutic regeneration after myocardial infarction in the adult mouse heart. EMBO Mol Med. 2013; 5: 191-209. doi: 10.1002/ emmm.201201737
Mangi AA, Noiseux N, Kong D, et al. Mesenchymal stem cells modified with akt prevent remodeling and restore perfor-mance of infarcted hearts. Nat Med. 2003; 9: 1195-1201.
Hodgkinson CP, Bareja A, Gomez JA, Dzau VJ. Emerging concepts in paracrine mechanisms in regenerative cardiovas-cular medicine and biology. Circ Res. 2016; 118: 95-107. doi: 10.1161/CIRCRESAHA.115.305373
Ibrahim AG, Cheng K, Marban E. Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Re-ports. 2014; 2: 606-619. doi: 10.1016/j.stemcr.2014.04.006
Bolli R, Ghafghazi S. Cell therapy needs rigorous translation-al studies in large animal models. J Am Coll Cardiol. 2015; 66: 2000-2004. doi: 10.1016/j.jacc.2015.09.002
Orenes-Pinero E, Montoro-Garcia S, Patel JV, Valdes M, Marin F, Lip GY. Role of micrornas in cardiac remodelling: New insights and future perspectives. Int J Cardiol. 2013; 167: 1651- 1659. doi: 10.1016/j.ijcard.2012.09.120
Sahoo S, Losordo DW. Exosomes and cardiac repair af-ter myocardial infarction. Circ Res. 2014; 114: 333-344. doi: 10.1161/CIRCRESAHA.114.300639
Schachinger V, Assmus B, Britten MB, et al. Transplanta-tion of progenitor cells and regeneration enhancement in acute myocardial infarction: Final one-year results of the topcare-ami trial. J Am Coll Cardiol. 2004; 44: 1690-1699. doi: 10.1016/j. jacc.2004.08.014
Gyongyosi M, Wojakowski W, Lemarchand P, et al. Meta-analysis of cell-based cardiac studies (accrue) in patients with acute myocardial infarction based on individual patient data. Circ Res. 2015; 116: 1346-1360. doi: 10.1161/CIRCRESA-HA.116.304346
Abdel-Latif A, Bolli R, Tleyjeh IM, et al. Adult bone marrow-derived cells for cardiac repair: A systematic review and meta-analysis. Arch Intern Med. 2007; 167: 989-997. doi: 10.1001/ archinte.167.10.989
Freyman T, Polin G, Osman H, et al. A quantitative, random-ized study evaluating three methods of mesenchymal stem cell delivery following myocardial infarction. Eur Heart J. 2006; 27: 1114-1122. doi: 10.1093/eurheartj/ehi818
Narita T, Shintani Y, Ikebe C, et al. The use of scaffold-free cell sheet technique to refine mesenchymal stromal cell-based therapy for heart failure. Mol Ther. 2013; 21: 860-867. doi: 10.1038/mt.2013.9
Willmann JK, Paulmurugan R, Rodriguez-Porcel M, et al. Imaging gene expression in human mesenchymal stem cells: From small to large animals. Radiology. 2009; 252: 117-127. doi: 10.1148/radiol.2513081616
Nguyen PK, Lan F, Wang Y, Wu JC. Imaging: Guiding the clinical translation of cardiac stem cell therapy. Circ Res. 2011; 109: 962-979. doi: 10.1161/CIRCRESAHA.111.242909
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. Arterioscler Thromb Vasc Biol. 2009; 29: 2076-2083. doi: 10.1161/ATVBA-HA.109.189662
Tang J, Wang J, Guo L, et al. Mesenchymal stem cells modi-fied with stromal cell-derived factor 1 alpha improve cardiac re-modeling via paracrine activation of hepatocyte growth factor in a rat model of myocardial infarction. Mol Cells. 2010; 29: 9-19. doi: 10.1007/s10059-010-0001-7
Gnecchi M, He H, Melo LG, et al. Early beneficial effects of bone marrow-derived mesenchymal stem cells overexpress-ing akt on cardiac metabolism after myocardial infarction. Stem Cells. 2009; 27: 971-979. doi: 10.1002/stem.12
Haider H, Jiang S, Idris NM, Ashraf M. Igf-1-overexpressing mesenchymal stem cells accelerate bone marrow stem cell mo-bilization via paracrine activation of sdf-1alpha/cxcr4 signaling to promote myocardial repair. Circ Res. 2008; 103: 1300-1308. doi: 10.1161/CIRCRESAHA.108.186742
Das R, Jahr H, van Osch GJ, Farrell E. The role of hypoxia in bone marrow-derived mesenchymal stem cells: Considerations for regenerative medicine approaches. Tissue Eng Part B Rev. 2010; 16: 159-168. doi: 10.1089/ten.teb.2009.0296
Huang J, Zhang Z, Guo J, et al. Genetic modification of mes-enchymal stem cells overexpressing ccr1 increases cell viabil-ity, migration, engraftment, and capillary density in the injured myocardium. Circ Res. 2010; 106: 1753-1762. doi: 10.1161/ CIRCRESAHA.109.196030
Shujia J, Haider HK, Idris NM, Lu G, Ashraf M. Stable ther-apeutic effects of mesenchymal stem cell-based multiple gene delivery for cardiac repair. Cardiovasc Res. 2008; 77: 525-533. doi: 10.1093/cvr/cvm077
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: 229-236. doi: 10.1016/j.athorac-sur.2005.02.072
Tang YL, Zhu W, Cheng M, et al. Hypoxic precondition-ing enhances the benefit of cardiac progenitor cell therapy for treatment of myocardial infarction by inducing cxcr4 expres-sion. Circ Res. 2009; 104: 1209-1216. doi: 10.1161/CIRCRE-SAHA.109.197723
Rosova I, Dao M, Capoccia B, Link D, Nolta JA. Hypoxic preconditioning results in increased motility and improved ther-apeutic potential of human mesenchymal stem cells. Stem Cells. 2008; 26(8): 2173-2182. doi: 10.1634/stemcells.2007-1104
Sanada F, Kim J, Czarna A, et al. C-kit-positive cardiac stem cells nested in hypoxic niches are activated by stem cell factor reversing the aging myopathy. Circ Res. 2014; 114: 41-55. doi: 10.1161/CIRCRESAHA.114.302500
Hahn JY, Cho HJ, Kang HJ, et al. Pre-treatment of mesen-chymal stem cells with a combination of growth factors enhanc-es gap junction formation, cytoprotective effect on cardiomyo-cytes, and therapeutic efficacy for myocardial infarction. J Am Coll Card. 2008; 51. doi: 10.1016/j.jacc.2007.11.040
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 Am Coll Cardiol. 2013; 61: 2329- 2338. doi: 10.1016/j.jacc.2013.02.071
Mastri M, Shah Z, McLaughlin T, et al. Activation of toll-like receptor 3 amplifies mesenchymal stem cell trophic factors and enhances therapeutic potency. Am J Physiol Cell Physiol. 2012; 303: C1021-C1033. doi: 10.1152/ajpcell.00191.2012
Suzuki G, Weil BR, Young RF, Canty JM. Toll-like recep-tor 3 activation of cardiosphere-derived cells amplifies myocyte regeneration and reverse LV remodeling in swine with ischemic cardiomyopathy. Circulation. 2016; 134: A14423.
Hu S, Huang M, Nguyen PK, et al. Novel microrna prosur-vival cocktail for improving engraftment and function of cardiac progenitor cell transplantation. Circulation. 2011; 124: S27-S34. doi: 10.1161/CIRCULATIONAHA.111.017954
Dakhlallah D, Zhang J, Yu L, Marsh CB, Angelos MG, Khan M. Microrna-133a engineered mesenchymal stem cells augment cardiac function and cell survival in the infarct heart. J Cardiovasc Pharmacol. 2015; 65: 241-251. doi: 10.1097/ FJC.0000000000000183
Gaetani R, Feyen DA, Verhage V, et al. Epicardial applica-tion of cardiac progenitor cells in a 3d-printed gelatin/hyaluronic acid patch preserves cardiac function after myocardial infarc-tion. Biomaterials. 2015; 61: 339-348. doi: 10.1016/j.biomateri-als.2015.05.005
Simpson D, Liu H, Fan TH, Nerem R, Dudley SC, Jr. A tis-sue engineering approach to progenitor cell delivery results in significant cell engraftment and improved myocardial remod-eling. Stem Cells. 2007; 25: 2350-2357. doi: 10.1634/stem-cells.2007-0132
Frederick JR, Fitzpatrick JR 3rd, McCormick RC, et al. Stro-mal cell-derived factor-1alpha activation of tissue-engineered endothelial progenitor cell matrix enhances ventricular func-tion after myocardial infarction by inducing neovasculogenesis. Circulation. 2010; 122: S107-S117. doi: 10.1161/CIRCULA-TIONAHA.109.930404
Christman KL, Vardanian AJ, Fang Q, Sievers RE, Fok HH, Lee RJ. Injectable fibrin scaffold improves cell transplant sur-vival, reduces infarct expansion, and induces neovasculature formation in ischemic myocardium. J Am Coll Cardiol. 2004; 44: 654-660. doi: 10.1016/j.jacc.2004.04.040
Liu J, Hu Q, Wang Z, et al. Autologous stem cell transplan-tation for myocardial repair. Am J Physiol Heart Circ Physiol. 2004; 287: H501-511. doi: 10.1152/ajpheart.00019.2004
Xiong Q, Hill KL, Li Q, et al. A fibrin patch-based enhanced delivery of human embryonic stem cell-derived vascular cell transplantation in a porcine model of postinfarction left ventric-ular remodeling. Stem Cells. 2011; 29: 367-375. doi: 10.1002/ stem.580
Gaetani R, Yin C, Srikumar N, et al. Cardiac-derived extra-cellular matrix enhances cardiogenic properties of human cardi-ac progenitor cells. Cell Transplantation. 2016; 25: 1653-1663. doi: 10.3727/096368915X689794
Lin YD, Yeh ML, Yang YJ, et al. Intramyocardial pep-tide nanofiber injection improves postinfarction ventricular remodeling and efficacy of bone marrow cell therapy in pigs. Circulation. 2010; 122: S132-S141. doi: 10.1161/CIRCULA-TIONAHA.110.939512
Danoviz ME, Nakamuta JS, Marques FL, et al. Rat adipose tissue-derived stem cells transplantation attenuates cardiac dys-function post infarction and biopolymers enhance cell retention. PLoS One. 2010; 5: e12077. doi: 10.1371/journal.pone.0012077
Itoh M, Nakayama K, Noguchi R, et al. Scaffold-free tubular tissues created by a bio-3d printer undergo remodeling and en-dothelialization when implanted in rat aortae. PLOS One. 2015; 10: 1-15. doi: 10.1371/journal.pone.0136681
Laschke MW, Menger MD. Life is 3D: Boosting spheroid function for tissue engineering. Trends in Biotechnology. 2016. doi: 10.1016/j.tibtech.2016.08.004
NI, Hibino N, Nakayama K. Principles of the kenzan method for robotic cell spheroid-based three-dimensional bioprinting. Tissue Eng Part B Rev. 2017; 23: 237-244. doi: 10.1089/ten. teb.2016.0322
Williams AR, Hatzistergos KE, Addicott B, et al. Enhanced effect of combining human cardiac stem cells and bone mar-row mesenchymal stem cells to reduce infarct size and to restore cardiac function after myocardial infarction. Circulation. 2013; 127: 213-223. doi: 10.1161/CIRCULATIONAHA.112.131110
Malliaras K, Smith RR, Kanazawa H, et al. Validation of contrast-enhanced magnetic resonance imaging to monitor re-generative efficacy after cell therapy in a porcine model of con-valescent myocardial infarction. Circulation. 2013; 128: 2764- 2775. doi: 10.1161/CIRCULATIONAHA.113.002863
Malliaras K, Li TS, Luthringer D, et al. Safety and effica-cy of allogeneic cell therapy in infarcted rats transplanted with mismatched cardiosphere-derived cells. Circulation. 2012; 125: 100-112. doi: 10.1161/CIRCULATIONAHA.111.042598
Suncion VY, Ghersin E, Fishman JE, et al. Does transendo-cardial injection of mesenchymal stem cells improve myocardial function locally or globally?: An analysis from the percutaneous stem cell injection delivery effects on neomyogenesis (poseidon) randomized trial. Circ Res. 2014; 114: 1292-1301. doi: 10.1161/ CIRCRESAHA.114.302854
Makkar RR, Smith RR, Cheng K, et al. Intracoronary car-diosphere-derived cells for heart regeneration after myocar-dial infarction (caduceus): A prospective, randomised phase 1 trial. Lancet. 2012; 379: 895-904. doi: 10.1016/S0140- 6736(12)60195-0
Malliaras K, Makkar RR, Smith RR, et al. Intracoronary cardiosphere-derived cells after myocardial infarction: Evidence for therapeutic regeneration in the final 1-year results of the ca-duceus trial. J Am Coll Card. 2014; 63: 110-120. doi: 10.1016/j. jacc.2013.08.724
Tokita Y, Tang XL, Li Q, et al. Repeated administrations of cardiac progenitor cells are markedly more effective than a single administration: A new paradigm in cell therapy. Circ Res. 2016; 119: 635-651. doi: 10.1161/CIRCRESAHA.116.308937
Gavira JJ, Nasarre E, Abizanda G, et al. Repeated implanta-tion of skeletal myoblast in a swine model of chronic myocar-dial infarction. Eur Heart J. 2010; 31: 1013-1021. doi: 10.1093/ eurheartj/ehp342
Malliaras K, Marban E. Cardiac cell therapy: Where we’ve been, where we are, and where we should be headed. Br Med Bull. 2011; 98: 161-185. doi: 10.1093/bmb/ldr018
Sanganalmath SK, Bolli R. Cell therapy for heart failure: A comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ Res. 2013; 113: 810-834. doi: 10.1161/CIRCRESAHA.113.300219
Tseliou E, Fouad J, Reich H, et al. Fibroblasts rendered an-tifibrotic, antiapoptotic, and angiogenic by priming with car-diosphere-derived extracellular membrane vesicles. J Am Coll Cardiol. 2015; 66(6): 599-611. doi: 10.1016/j.jacc.2015.05.068
Chakravarty T, Makkar RR, Ascheim DD, et al. ALLoge-neic heart STem cells to achieve myocardial regeneration (ALL-STAR) trial: Rationale and design. Cell Transplant. 2017; 26: 205-214.
Downloads
Published
How to Cite
Issue
Section
License

This work is licensed under a Creative Commons Attribution 4.0 International License.
All content published in Heart Research (HROJ) is licensed under the Creative Commons Attribution 4.0 International License (CC BY 4.0). This license allows anyone to copy, distribute, transmit, and adapt the work — including for commercial purposes — provided appropriate credit is given to the original author(s) and source.