Concurrent Isolation of 3 Distinct Cardiac Stem Cell Populations from a Single Human Heart Biopsy

Circulation Research

Volumn 121, Issue 2, 2017, Pages 113-124

  Monsanto, Megan M ^a   White, Kevin S ^a   Kim, Taeyong ^a   Wang, Bingyan J ^a   Fisher, Kristina ^a   Ilves, Kelli ^a   Khalafalla, Farid G ^a   Casillas, Alexandria ^a   Broughton, Kathleen ^a   Mohsin, Sadia ^a   Dembitsky, Walter P ^b   Sussman, Mark A ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b SHARP MEMORIAL HOSPITAL   (United States)

Author keywords

adult stem cells; biopsy; centrifugation; endothelial progenitor cells; heart failure; mesenchymal stem cells

Indexed keywords

CELL SURFACE MARKER; ENDOGLIN; THY 1 ANTIGEN;

ARTICLE; CARDIAC MUSCLE; CARDIAC STEM CELL; CELL ISOLATION; CELL POPULATION; CELL PROLIFERATION ASSAY; CELL SELECTION; CENTRIFUGATION; ENDOTHELIAL PROGENITOR CELL; EXPLANT; FLOW CYTOMETRY; HEART FAILURE; HEART MUSCLE BIOPSY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; MESENCHYMAL STEM CELL; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL TRANSPLANTATION; TISSUE REGENERATION; BIOPSY; CARDIAC MUSCLE CELL; CELL CULTURE; CELL SEPARATION; CYTOLOGY; ENDOTHELIUM CELL; HEART; MESENCHYMAL STROMA CELL; PHYSIOLOGY; PROCEDURES; STEM CELL;

BIOPSY; CELL SEPARATION; CELLS, CULTURED; ENDOTHELIAL CELLS; FLOW CYTOMETRY; HEART; HUMANS; MESENCHYMAL STROMAL CELLS; MYOCARDIUM; MYOCYTES, CARDIAC; STEM CELLS;

EID: 85021872253     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.310494     Document Type: Article

References (44)

1. 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.
2. Dixit P, Katare R. Challenges in identifying the best source of stem cells for cardiac regeneration therapy. Stem Cell Res Ther. 2015;6:26. doi: 10.1186/s13287-015-0010-8.
3. Assmus B, Schächinger V, Teupe C, Britten M, Lehmann R, Döbert N, Grünwald F, Aicher A, Urbich C, Martin H, Hoelzer D, Dimmeler S, Zeiher AM. Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI). Circulation. 2002;106:3009-3017.
4. Clifford DM, Fisher SA, Brunskill SJ, Doree C, Mathur A, Watt S, Martin-Rendon E. Stem cell treatment for acute myocardial infarction. Cochrane Database Syst Rev. 2012;15:CD006536.
5. 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;308:2369-2379. doi: 10.1001/jama.2012.25321.
6. Mills JS, Rao SV. REPAIR-AMI: stem cells for acute myocardial infarction. Future Cardiol. 2007;3:137-140. doi: 10.2217/14796678.3.2.137.
7. Traverse JH, Henry TD, Ellis SG, et al; Cardiovascular Cell Therapy ResearchNetwork. 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. JAMA. 2011;306:2110-2119. doi: 10.1001/jama.2011.1670.
8. Menasché P, Alfieri O, Janssens S, McKenna W, Reichenspurner H, Trinquart L, Vilquin JT, Marolleau JP, Seymour B, Larghero J, Lake S, Chatellier G, Solomon S, Desnos M, Hagège AA. The Myoblast Autologous Grafting in Ischemic Cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantation. Circulation. 2008;117:1189-1200. doi: 10.1161/CIRCULATIONAHA.107.734103.
9. Leri A, Kajstura J, Anversa P. Role of cardiac stem cells in cardiac pathophysiology: a paradigm shift in human myocardial biology. Circ Res. 2011;109:941-961. doi: 10.1161/CIRCRESAHA.111.243154.
10. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K, Leri A, Kajstura J, Nadal-Ginard B, Anversa P. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell. 2003;114:763-776.
11. Bearzi C et al. Human cardiac stem cells. Proc Natl Acad Sci USA. 2007;104:14068-14073.
12. Lyngbaek S, Schneider M, Hansen JL, Sheikh SP. Cardiac regeneration by resident stem and progenitor cells in the adult heart. Basic Res Cardiol. 2007;102:101-114. doi: 10.1007/s00395-007-0638-3.
13. 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;379:895-904. doi: 10.1016/S0140-6736(12)60195-0.
14. Bolli R, Chugh AR, D'Amario D, et al. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet. 2011;378:1847-1857. doi: 10.1016/S0140-6736(11)61590-0.
15. Mohsin S, Khan M, Nguyen J, Alkatib M, Siddiqi S, Hariharan N, Wallach K, Monsanto M, Gude N, Dembitsky W, Sussman MA. Rejuvenation of human cardiac progenitor cells with Pim-1 kinase. Circ Res. 2013;113:1169-1179. doi: 10.1161/CIRCRESAHA.113.302302.
16. Kulandavelu S, Karantalis V, Fritsch J, et al. Pim1 kinase overexpression enhances ckit(+) cardiac stem cell cardiac repair following myocardial infarction in swine. J Am Coll Cardiol. 2016;68:2454-2464. doi: 10.1016/j. jacc.2016.09.925.
17. Tokita Y, Tang XL, Li Q, Wysoczynski M, Hong KU, Nakamura S, Wu WJ, Xie W, Li D, Hunt G, Ou Q, Stowers H, Bolli R. 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.
18. 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;127:213-223. doi: 10.1161/CIRCULATIONAHA.112.131110.
19. Bernstein HS, Srivastava D. Stem cell therapy for cardiac disease. Pediatr Res. 2012;71:491-499. doi: 10.1038/pr.2011.61.
20. Miyahara Y, Nagaya N, Kataoka M, Yanagawa B, Tanaka K, Hao H, Ishino K, Ishida H, Shimizu T, Kangawa K, Sano S, Okano T, Kitamura S, Mori H. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med. 2006;12:459-465. doi: 10.1038/nm1391.
21. Gnecchi M, Zhang Z, Ni A, Dzau VJ. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res. 2008;103:1204-1219. doi: 10.1161/CIRCRESAHA.108.176826.
22. Malgieri A, Kantzari E, Patrizi MP, Gambardella S. Bone marrow and umbilical cord blood human mesenchymal stem cells: state of the art. Int J Clin Exp Med. 2010;3:248-269.
23. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop DJ, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315-317. doi: 10.1080/14653240600855905.
24. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105:1815-1822. doi: 10.1182/blood-2004-04-1559.
25. Kuraitis D, Ruel M, Suuronen EJ. Mesenchymal stem cells for cardiovascular regeneration. Cardiovasc Drugs Ther. 2011;25:349-362. doi: 10.1007/s10557-011-6311-y.
26. 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;54:2277-2286. doi: 10.1016/j.jacc.2009.06.055.
27. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964-967.
28. Peichev M, Naiyer AJ, Pereira D, Zhu Z, Lane WJ, Williams M, Oz MC, Hicklin DJ, Witte L, Moore MA, Rafii S. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood. 2000;95:952-958.
29. Gehling UM, Ergün S, Schumacher U, Wagener C, Pantel K, Otte M, Schuch G, Schafhausen P, Mende T, Kilic N, Kluge K, Schäfer B, Hossfeld DK, Fiedler W. In vitro differentiation of endothelial cells from AC133-positive progenitor cells. Blood. 2000;95:3106-3112.
30. Handgretinger R, Gordon PR, Leimig T, Chen X, Buhring HJ, Niethammer D, Kuci S. Biology and plasticity of CD133+ hematopoietic stem cells. Ann N Y Acad Sci. 2003;996:141-151.
31. Jujo K, Ii M, Losordo DW. Endothelial progenitor cells in neovascularization of infarcted myocardium. J Mol Cell Cardiol. 2008;45:530-544. doi: 10.1016/j.yjmcc.2008.08.003.
32. Lee WY, Wei HJ, Wang JJ, Lin KJ, Lin WW, Chen DY, Huang CC, Lee TY, Ma HY, Hwang SM, Chang Y, Sung HW. Vascularization and restoration of heart function in rat myocardial infarction using transplantation of human cbMSC/HUVEC core-shell bodies. Biomaterials. 2012;33:2127-2136. doi: 10.1016/j.biomaterials.2011.11.059.
33. Sharan R, Maron-Katz A, Shamir R. CLICK and EXPANDER: a system for clustering and visualizing gene expression data. Bioinformatics. 2003;19:1787-1799.
34. Ridzuan N, Al Abbar A, Yip WK, Maqbool M, Ramasamy R. Characterization and expression of senescence marker in prolonged passages of rat bone marrow-derived mesenchymal stem cells. Stem Cells Int. 2016;2016:8487264. doi: 10.1155/2016/8487264.
35. Shaer A, Azarpira N, Aghdaie MH, Esfandiari E. Isolation and characterization of human mesenchymal stromal cells derived from placental decidua basalis; umbilical cord Wharton's jelly and amniotic membrane. Pak J Med Sci. 2014;30:1022-1026. doi: 10.12669/pjms.305.4537.
36. Aliborzi G, Vahdati A, Mehrabani D, Hosseini SE, Tamadon A. Isolation, characterization and growth kinetic comparison of bone marrow and adipose tissue mesenchymal stem cells of Guinea Pig. Int J Stem Cells. 2016;9:115-123. doi: 10.15283/ijsc.2016.9.1.115.
37. Shi H, Drummond CA, Fan X, Haller ST, Liu J, Malhotra D, Tian J. Hiding inside? Intracellular expression of non-glycosylated c-kit protein in cardiac progenitor cells. Stem Cell Res. 2016;16:795-806. doi: 10.1016/j. scr.2016.04.017.
38. Chen CL, Faltusova K, Molik M, Savvulidi F, Chang KT, Necas E. Low c-Kit expression level induced by stem cell factor does not compromise transplantation of hematopoietic stem cells. Biol Blood Marrow Transplant. 2016;22:1167-1172. doi: 10.1016/j.bbmt.2016.03.017.
39. Babina M, Rex C, Guhl S, Thienemann F, Artuc M, Henz BM, Zuberbier T. Baseline and stimulated turnover of cell surface c-Kit expression in different types of human mast cells. Exp Dermatol. 2006;15:530-537. doi: 10.1111/j.1600-0625.2006.00446.x.
40. Fischer KM, Cottage CT, Wu W, Din S, Gude NA, Avitabile D, Quijada P, Collins BL, Fransioli J, Sussman MA. Enhancement of myocardial regeneration through genetic engineering of cardiac progenitor cells expressing Pim-1 kinase. Circulation. 2009;120:2077-2087. doi: 10.1161/CIRCULATIONAHA.109.884403.
41. Mohsin S, Khan M, Toko H, et al. Human cardiac progenitor cells engineered with Pim-I kinase enhance myocardial repair. J Am Coll Cardiol. 2012;60:1278-1287. doi: 10.1016/j.jacc.2012.04.047.
42. Sitte N, Saretzki G, von Zglinicki T. Accelerated telomere shortening in fibroblasts after extended periods of confluency. Free Radic Biol Med. 1998;24:885-893.
43. Butura A, Johansson I, Nilsson K, Wärngård L, Ingelman-Sundberg M, Schuppe-Koistinen I. Differentiation of human hepatoma cells during confluence as revealed by gene expression profiling. Biochem Pharmacol. 2004;67:1249-1258. doi: 10.1016/j.bcp.2003.10.033.
44. 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 metaanalysis. BMJ. 2014;348:g2688. doi: 10.1136/bmj.g2688.