Cell-based treatment represents a new generation in
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1 Viewpoints Mesenchymal Stem Cells as a Biological Drug for Heart Disease Where Are We With Cardiac Cell Based Therapy? Cristina Sanina, Joshua M. Hare Cell-based treatment represents a new generation in the evolution of biological therapeutics. A prototypic cell-based therapy, the mesenchymal stem cell, has successfully entered phase III pivotal trials for heart failure, signifying adequate enabling safety and efficacy data from phase I and II trials. Successful phase III trials can lead to approval of a new biological therapy for regenerative medicine. The use of stem or progenitor cells therapeutically is under investigation for the treatment of chronic diseases, including cardiovascular pathologies. 1 Not unusual for an early stage disruptive technology, early findings have led the field to an important and controversial cross-roads. Based in large part on disagreements surrounding mechanism of action of cell-based therapy, some authors have called for a reappraisal of the existing data, whereas others have concluded that the field has evolved too quickly into clinical practice and that we need to go back to the bench. 2 However, there are many historical examples including the notable examples of aspirin and opioids that were used therapeutically before the mechanisms of actions were fully understood. In the midst of this debate about mechanism of action of cell therapy, an emerging field of investigation that holds great promise needs to be highlighted. In this context, the development of mesenchymal stem cells has followed the characteristic trajectory of preclinical and clinical development, supported by data highly predictive of successful therapeutic outcome. Most importantly, because of its allogeneic potential, mesenchymal stem cells can be viewed as a true cellular biological therapy with the Original received February 22, 2015; revision received May 21, 2015; accepted June 15, In May 2015, the average time from submission to first decision for all original research papers submitted to Circulation Research was days. From the Interdisciplinary Stem Cell Institute (C.S., J.M.H.), Department of Medicine, Division of Cardiology (J.M.H.), and Department of Molecular and Cellular Pharmacology, University of Miami Miller School of Medicine, FL (J.M.H.). This manuscript was sent to Mark A. Sussman, Consulting Editor, for review by expert referees, editorial decision, and final disposition. Correspondence to Joshua M. Hare, MD, Interdisciplinary Stem Cell Institute, Biomedical Research Building, University of Miami Miller School of Medicine, 1501 NW 10th Ave, Room 908, PO Box (R125), Miami, FL jhare@med.miami.edu (Circ Res. 2015;117: DOI: /CIRCRESAHA ) 2015 American Heart Association, Inc. Circulation Research is available at DOI: /CIRCRESAHA capacity for high volume quality-controlled production and off the shelf usage. 3 What Are Mesenchymal Stem Cells? Mesenchymal Stem Cells (MSCs) are mesoderm-derived multipotent stromal cells that reside in embryonic and adult tissues, prototypically bone marrow. Having the capacity for self-renewal, MSCs maintain stemness (eg, multipotency) and exhibit immune-privileged, immunomodulatory, and proregenerative proprieties due, in part, to their secretome. 1 As such, culture-expanded MSCs represent a controlled and homogeneous stem cell population. Why MSCs Became One of the Top Choices? A large majority of early cell-based clinical trials for heart disease were designed for acute myocardial infarction (AMI) and conducted using autologous bone marrow mononuclear cells. The widespread use of bone marrow mononuclear cells can be attributed to immediate cell availability from the recipient. However, the efficacy was variable. Using global left ventricular ejection fraction as an end point, bone marrow mononuclear cell trials showed controversial results, and later trials tended to be negative. 4 Perhaps, one of the factors contributing to this discordance was the innate diversity of cell populations found in isolated bone marrow mononuclear cells between patients. All this has led to the search of more specific stem cell subpopulations with more specific identifying characterizations. Particularly, the field needed an adult stem cell that is easy to isolate, culture, and manipulate in ex vivo conditions. In this regard, MSCs, in part, because of their long standing record in regenerative medicine, proven safety, and potency, have emerged as a lead candidate cell type with accumulating clinical investigations using this stem cell population for AMI and chronic heart failure. 5 What Was Trajectory of Preclinical and Clinical Development of MSCs? Following experiments in rodents, multiple preclinical studies in different animal models of acute and chronic heart failure have been conducted, which together demonstrate favorable impact on left ventricle remodeling, driven largely by a 30% to 50% reduction in infarct scar size. 6 Accumulating data led to Food and Drug Administration (FDA) approval for testing MSC-therapy in early phase small clinical trials (pilot studies) that established the safety of both autologous and allogeneic MSCs. 7 The pilot studies have, in turn, guided the design of phase II clinical trials suggesting the optimal use of stem cells, methods, and cost-effective way to investigate clinical efficacy.
2 230 Circulation Research July 17, 2015 Nonstandard Abbreviations and Acronyms AMI LV MLHFQ MSCs SPECT acute myocardial infarction left ventricle Minnesota Living with Heart Failure questionnaire mesenchymal stem cells single-photon emission computed tomography MSC as a Therapeutic Agent It is valuable to consider MSC-based therapy in the context of general principles of therapeutic development. On the average, it takes 12 to 15 years and up to $5 billion to develop and launch a new drug. Given this paradigm, the decade of work on developing MSCs cannot and should not be dismissed. While only 1 of 10 investigational new drugs succeeds from phase I to FDA approval, the probability of success increases with the transition to later stages of clinical trial development. 8 MSCs have decisively passed phase II, a rigorously controlled phase, and have recently entered phase III trials. 1 New therapeutic development often must encounter The Valley of Death, which is a translational research gap during which time safety assessments for chemical and biological drugs are made. This period can often be intensified if animal models for the disease in question have deficiencies. 9 As a consequence, the attrition rate of drugs entering human trials even after passing preclinical translational research in animal models remains high, representing 90% in all areas. 10 Hence, it should be noted that substantial preclinical data supporting MSCs in the injured heart had emerged from highly representative large animal models, such as the porcine, which has similar cardiac anatomy and physiology as humans. 11 The remodeling process in these models is highly reminiscent of left ventricular Table 1. Results of Trials of Cell-Based Therapy in Chronic Heart Failure remodeling in humans and has accurately predicted phenotypic outcomes in clinical trials. Experiments in porcine models have been used to test both human cells in immunosuppressed animals, 6 as well as autologous cells. 12 Reasons for Failure of a New Therapeutic Strategy The generic reasons that explain the failure of a new therapeutic include poor understanding of drug pharmacology, 13 poor linkage between molecule-to-disease, 14 and variability in the underlying genetics/epigenetics in animals and humans. 15 MSC pharmacology has proven mechanisms of action which include MSC plasticity, secretion of numerous bioactive molecules, exosomes, and mitochondria transfer. These bioactive molecules, in turn, promote myocardial tissue growth through endogenous activation of angiogenesis, neurogenesis, immunomodulation, cardiac stem cell, and mature cardiomyocyte proliferation. 1 With regard to genetics/epigenetics in animals and humans, the use of human cells in animal models has justified the safety and potency of human MSCs, demonstrating that these cells are capable of replacing tissue loss and restoring cardiac function. 6 The use of allogeneic MSCs was initiated in animal models as well, contributing to a better understanding of the interdisciplinary nature of MSC biology particularly immune privilege proprieties that supported future studies in humans. Where Are We Now With Regard to Clinical Trials of MSCs? Since 2011, MSCs and related culture-expanded cell preparations have been tested in small trials for chronic heart failure. These trials have consistently shown that cell therapy in this clinical setting reduces MI scar size, reverses ventricular remodeling, improves 6-minute walk distance and quality of life, as measured with validated questionnaires (Table 1) Nevertheless, although multiple meta-analyses have debated whether or not the degree of cardiac functional improvements, Trial Name (No. of Patients) Δ6MWT MLHFQ MI SIZE EF Williams et al 6 (n=8) 18.3±8.3% SCIPIO 20 (n=21) ±3.5 g ( 30%) % MESOBLAST 23 (n=60) m* +5.2±9.3%* CADUCEUS 18 (n=25) m g ( 42%) POSEIDON 16 (n=30) m % +2.0%* C-CURE 19 (n=33) m ±10* +7.0% TAC-HFT 17 (n=59) m g ( 32.9%) MSC-HF (n=59) 4.4±5.1 g +5.5±3.8% 6MWT indicates 6-minute walk test; C-CURE, Cardiopoietic stem Cell therapy in heart failure; CADUCEUS, CArdiosphere-Derived autologous Stem CElls to Reverse ventricular dysfunction; EF, ejection fraction; MESOBLAST, A Phase II Dose-escalation Study to Assess the Feasibility and Safety of Transendocardial Delivery of Three Different Doses of Allogeneic Mesenchymal Precursor Cells (MPCs) in Subjects With Heart Failure; MI SIZE, myocardial infarction size/scar size; MLHFQ, Minnesota Living With Heart Failure Questionnaire MSC-HF, Mesenchymal Stromal Cells in chronic ischemic Heart Failure; POSEIDON, The Percutaneous Stem Cell Injection Delivery Effects on Neomyogenesis Pilot Study; SCIPIO, Cardiac Stem Cell Infusion in Patients With Ischemic CardiOmyopathy; and TAC-HFT, The Transendocardial Autologous Cells (hmsc or hbmc) in Ischemic Heart Failure Trial. *Not significant vs control. Not significant within-group. Data not published. 25 million mesenchymal precursor cell group.
3 Sanina and Hare Mesenchymal Stem Cells for Heart Disease 231 including increases in left ventricular ejection fraction, are significant, 2 there are not enough standardized clinical trials studying MSCs or related cells with appropriate sample sizes to confidently answer this question. A review of trials registered on clinicaltrials.gov revealed 34 MSC clinical trials for adult heart pathology (AMI, ischemic, and nonischemic chronic heart failure). Most studies remain in phases I and II (Figure A) but there are several phase III trials currently underway or completed (Table 2). 21 A major issue of note is the diversity of MSC clinical trials. Seven of these trials are multicentered and 1 is double-centered. Most of them (27) are small-sized trials, enrolling <100 patients per trial (Figure B and C) and only some are placebo-controlled. The MSC route of administration (intravenous, intracoronary, intramyocardial, and ; Figure D), cell dose, and cell origin (fetal-umbilical versus adult, autologous versus allogeneic, and bone-marrow versus adipose derived) are dissimilar in these clinical trials as well. Indeed, it is crucial to mention that MSC origin and location may define MSC characteristics and therefore influence MSC behavior. 3,22 These facts highlight the variability in MSC clinical trials, specifically with respect to study design, cell origin, and dose/ methods. In 2009, the first double-blinded allogeneic MSC clinical trial for AMI sponsored by Osiris demonstrated that intravenous infusion of allogeneic MSCs was well tolerated and lowered arrhythmic events and chest pain. 7 This trial started the era of allogeneic MSCs for heart disease and today, allogeneic MSC products are used in large clinical trials with enrollment targets in the thousands of patients. Success with these efforts could lead to approval of these products by the FDA. MSC Therapy Perspectives Given all of the above, MSC clinical trials have already crossed the Rubicon suggesting that cell-based therapy is safe, efficient, and efficacious. Biological drugs, such as stem cells, have a more arduous path to travel compared with Table 2. Phase II/III and III Clinical Trials of Cell-Based Therapy in Heart Disease Trial ID; Trial Location; No. of Patients Trial Name (Trial Stage) Cardiac Indication Delivery Method Cell Type Sponsor Primary End Points NCT ; Greece; 30 NCT ; Republic of Korea; 80 (final) NCT ; Russia; 50 NCT ; Republic of Korea; 135 NCT ; United States and Canada; 1730 NCT ; Belgium, Serbia; 33 (final) NCT ; Belgium, Hungary, Israel, Italy, Poland, Serbia, Spain, Sweden, Switzerland, United Kingdom; 240 NCT ; no location provided; 240 Allogeneic Stem Cells Implantation Combined With Coronary Bypass Grafting in Patients With Ischemic Cardiomyopathy (ongoing) Safety and Efficacy of Intracoronary Adult Human Mesenchymal Stem Cells After Acute Myocardial Infarction (SEED-MSC) (completed) ESTIMATION (on-going) RELIEF (on-going) DREAM-HF (on-going) C-CURE (completed) CHART-1 (on-going) THE CHART-2 TRIAL (not recruiting) Ischemic cardiomyopathy+cabg infarction infarction heart failure infarction Chronic heart failure (ischemic and nonischemic) Chronic heart failure secondary to ischemic cardiomyopathy Chronic advanced ischemic heart failure Congestive heart failure secondary to ischemic cardiomyopathy Intramyocardial/ intraoperative Intracoronary Intracoronary C-Cath injection catheter Allogeneic MSCs Allogeneic mesenchymal precursor cells (CEP ) marrow derived and cardiogenically oriented MSCs marrow derived mesenchymal cardiopoietic cells (C3BS-CQR-1) marrow derived mesenchymal cardiopoietic cells (C3BS-CQR-1) AHEPA University Hospital Yonsei University, collaboration with FCB- Pharmicell Co, Ltd Meshalkin Research Institute of Pathology of Circulation Pharmicell Co, Ltd Teva Pharmaceutical Industries, Israel Change in LVEF by EchoCG and myocardial segmental perfusion Absolute change in global LVEF by SPECT Change LVESV and LVEDV by MRI Change LVEF by MRI HF-MACE Change in LVEF MLHFQ 6-min walk test LVESV (absolute change 4%) in LVEF 6-min walk test CABG indicates coronary artery bypass grafting; C-CURE, Cardiopoietic stem Cell therapy in heart failure; CHART-1, Safety and Efficacy of Autologous Cardiopoietic Cells for Treatment of Ischemic Heart Failure; CHART-2 TRIAL, Congestive Heart Failure Cardiopoietic Regenerative Therapy; DREAM-HF, Allogeneic Mesenchymal Precursor Cells (CEP-41750) for the Treatment of Chronic Heart Failure; EchoCG, echocardiogram; ESTIMATION, ESTIMATION Study for Endocardial Mesenchymal Stem Cells Implantation in Patients After Acute Myocardial Infarction; HF- MACE, heart failure related major adverse cardiac events; LVEF, left ventricular ejection fraction; LVEDV, left ventricular end diastolic volume; LVESV, left ventricular end systolic volume; MSC, mesenchymal stem cell; MLHFQ, Minnesota Living with Heart Failure Questionnaire; RELIEF, A Randomized, Open labeled, multicenter Trial for Safety and Efficacy of Intracoronary Adult Human Mesenchymal stem Cells Acute Myocardial infarction; and SPECT, single-photon emission computed tomography.
4 232 Circulation Research July 17, 2015 A B C D Figure. Total number of MSC (mesenchymal stem cell) trials (n=34) found on clinicaltrials. gov for heart disease. The bar graph depicts the number of trials according to clinical phase (A). Total number of patients enrolled or estimated to be enrolled according trial phase (B). Average number of patients enrolled or estimated to be enrolled per trial (C). The diagram depicts the percentage of the route of cell administration in 34 clinical trials (intravenous [IV], intracoronary [IC], intramyocardial [IM], and [TE]; D). their chemical counterparts. The nature of a biological drug is more complicated, and in addition to safety and efficacy, raises ethical, political, and economic concerns that need to be addressed. MSCs are overcoming the majority of these challenges, and several efforts have resulted in phase III clinical trials that, if successful, could lead to approval. There are still unresolved issues regarding cell dose and number of treatments needed to reach the desired results. It is unclear whether MSC donors can influence cellular product efficacy. We certainly need to follow the established quality control standards for MSC products and define the patient population that is eligible and will benefit the most from cell therapy. In conclusion, MSC-based therapy for heart disease can be viewed in the context of a novel class of biological therapeutics and one that is following a characteristic drug development pipeline. Appropriate preclinical models have been used that can predict findings in humans and ensure safety. Finally, allogeneic MSC products, a biological drug with standardized quality controlled manufacturing, are demonstrated to be safe and effective in phase I and II clinical trials for AMI and chronic heart failure. 7,16 The current ongoing conduct of phase III trials are warranted and could lead to product approval. Enlarging efforts to conduct phase II and III trials should be encouraged and will contribute to advancing this field which has the potential to address large unmet medical needs and substantially influence human health. Sources of Funding Dr Hare is supported by National Institutes of Health Grants R01HL110737, R01HL084275, R01HL094849, R01HL107110, and UM1HL113460; the Starr Foundation; and the Soffer Family Foundation. Disclosures Dr Hare discloses a relationship with Vestion that includes equity, board membership, and consulting. C. Sanina reports no conflicts. References 1. Karantalis V, Hare JM. Use of mesenchymal stem cells for therapy of cardiac disease. Circ Res. 2015;116: doi: / CIRCRESAHA Nowbar AN, Mielewczik M, Karavassilis M, Dehbi HM, Shun-Shin MJ, Jones S, Howard JP, Cole GD, Francis DP; DAMASCENE writing group. Discrepancies in autologous bone marrow stem cell trials and enhancement of ejection fraction (DAMASCENE): weighted regression and meta-analysis. BMJ. 2014;348:g Caplan AI, Correa D. The MSC: an injury drugstore. Cell Stem Cell. 2011;9: doi: /j.stem Hare JM, Sanina C. Bone marrow mononuclear cell therapy and granulocyte colony-stimulating factor for acute myocardial infarction: Is it time to reconsider? J Am Coll Cardiol. 2015;65: doi: /j. jacc Williams AR, Hare JM. Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ Res. 2011;109: doi: / CIRCRESAHA Williams AR, Hatzistergos KE, Addicott B, McCall F, Carvalho D, Suncion V, Morales AR, Da Silva J, Sussman MA, Heldman AW, Hare JM. Enhanced effect of combining human cardiac stem cells and bone marrow mesenchymal stem cells to reduce infarct size and to restore cardiac function after myocardial infarction. Circulation. 2013;127: doi: /CIRCULATIONAHA Hare JM, Traverse JH, Henry TD, Dib N, Strumpf RK, Schulman SP, Gerstenblith G, DeMaria AN, Denktas AE, Gammon RS, Hermiller JB Jr, Reisman MA, Schaer GL, Sherman W. 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: doi: /j.jacc Hay M, Thomas DW, Craighead JL, Economides C, Rosenthal J. Clinical development success rates for investigational drugs. Nat Biotechnol. 2014;32: doi: /nbt Butler D. Translational research: crossing the valley of death. Nature. 2008;453: doi: /453840a. 10. A tale of two drugs. Nat Rev Drug Discov. 2006;5: nature.com/nrd/journal/v5/n10/full/nrd2167.html.
5 Sanina and Hare Mesenchymal Stem Cells for Heart Disease McCall FC, Telukuntla KS, Karantalis V, Suncion VY, Heldman AW, Mushtaq M, Williams AR, Hare JM. Myocardial infarction and intramyocardial injection models in swine. Nat Protoc. 2012;7: doi: /nprot Huang CC, Tsai HW, Lee WY, Lin WW, Chen DY, Hung YW, Chen JW, Hwang SM, Chang Y, Sung HW. A translational approach in using cell sheet fragments of autologous bone marrow-derived mesenchymal stem cells for cellular cardiomyoplasty in a porcine model. Biomaterials. 2013;34: doi: /j.biomaterials Ledford H. Translational research: 4 ways to fix the clinical trial. Nature. 2011;477: doi: /477526a. 14. Cook D, Brown D, Alexander R, March R, Morgan P, Satterthwaite G, Pangalos MN. Lessons learned from the fate of AstraZeneca s drug pipeline: a five-dimensional framework. Nat Rev Drug Discov. 2014;13: doi: /nrd Odom DT, Dowell RD, Jacobsen ES, Gordon W, Danford TW, MacIsaac KD, Rolfe PA, Conboy CM, Gifford DK, Fraenkel E. Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat Genet. 2007;39: doi: /ng Hare JM, Fishman JE, Gerstenblith G, et al. Comparison of allogeneic vs autologous bone marrow derived mesenchymal stem cells delivered by injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial. JAMA. 2012;308: doi: /jama 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: doi: /jama Makkar RR, Smith RR, Cheng K, Malliaras K, Thomson LE, Berman D, Czer LS, Marbán L, Mendizabal A, Johnston PV, Russell SD, Schuleri KH, Lardo AC, Gerstenblith G, Marbán E. Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. Lancet. 2012;379: doi: /S (12) 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: doi: /j. jacc Chugh AR, Beache GM, Loughran JH, Mewton N, Elmore JB, Kajstura J, Pappas P, Tatooles A, Stoddard MF, Lima JA, Slaughter MS, Anversa P, Bolli R. Administration of cardiac stem cells in patients with ischemic cardiomyopathy: the SCIPIO trial: surgical aspects and interim analysis of myocardial function and viability by magnetic resonance. Circulation. 2012;126:S54 S64. doi: /CIRCULATIONAHA Lee JW, Lee SH, Youn YJ, Ahn MS, Kim JY, Yoo BS, Yoon J, Kwon W, Hong IS, Lee K, Kwan J, Park KS, Choi D, Jang YS, Hong MK. 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: doi: /jkms Naftali-Shani N, Itzhaki-Alfia A, Landa-Rouben N, et al. The origin of human mesenchymal stromal cells dictates their reparative properties. J Am Heart Assoc. 2013;2:e doi: /JAHA Perin EC, Borow KM, Silva GV, DeMaria AN, Marroquin OC, Huang P, Traverse JH, Krum H, Skerrett D, Zheng Y, Willerson JT, Itescu S, Henry TD. A phase II dose-escalation study of allogeneic mesenchymal precursor cells in patients with ischemic or non-ischemic heart failure [published online before print July 6, 2015]. Circ Res. doi: / CIRCRESAHA Key Words: cell- and tissue-based therapy clinical trial chronic heart failure heart disease mesenchymal stem cells
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