Murine Models Demonstrate Distinct Vasculogenic and Cardiomyogenic cKit+ Lineages in the Heart

Circulation Research

Volumn 118, Issue 3, 2016, Pages 382-387

  Hatzistergos, Konstantinos E ^a   Hare, Joshua M ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiac; Cell differentiation; Cell and tissue based therapy; Coronary vessels; Endothelial cells; Myocytes

Indexed keywords

ALLELE; ANGIOGENESIS; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL REGENERATION; ENDOTHELIUM CELL; HEART MUSCLE CELL; HUMAN; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CARDIAC MUSCLE CELL; CORONARY BLOOD VESSEL; EMBRYOLOGY; GENETICS; GENOTYPE; HEART; METABOLISM; MORPHOGENESIS; PHENOTYPE; TRANSGENIC MOUSE;

STEM CELL FACTOR RECEPTOR;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CORONARY VESSELS; ENDOTHELIAL CELLS; GENOTYPE; HEART; MICE, TRANSGENIC; MORPHOGENESIS; MYOCYTES, CARDIAC; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-KIT;

EID: 84958554676     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.308061     Document Type: Article

References (49)

1. Hatzistergos KE, Takeuchi LM, Saur D, Seidler B, Dymecki SM, Mai JJ, White IA, Balkan W, Kanashiro-Takeuchi RM, Schally AV, Hare JM. cKit+ cardiac progenitors of neural crest origin. Proc Natl Acad Sci U S A. 2015;112:13051-13056. doi:10.1073/pnas.1517201112.
2. van Berlo JH, Kanisicak O, Maillet M, Vagnozzi RJ, Karch J, Lin SC, Middleton RC, Marbán E, Molkentin JD. c-kit+ cells minimally contribute cardiomyocytes to the heart. Nature. 2014;509:337-341. doi:10.1038/nature13309.
3. Sultana N, Zhang L, Yan J, Chen J, Cai W, Razzaque S, Jeong D, Sheng W, Bu L, Xu M, Huang GY, Hajjar RJ, Zhou B, Moon A, Cai CL. Resident c-kit(+) cells in the heart are not cardiac stem cells. Nat Commun. 2015;6:8701. doi:10.1038/ncomms9701.
4. Liu Q, Yang R, Huang X, Zhang H, He L, Zhang L, Tian X, Nie Y, Hu S, Yan Y, Zhang L, Qiao Z, Wang QD, Lui KO, Zhou B. Genetic lineage tracing identifies in situ Kit-expressing cardiomyocytes. Cell Res. 2015. 26:119-130. doi:10.1038/cr.2015.143.
5. Anversa P, Kajstura J. Ventricular myocytes are not terminally differentiated in the adult mammalian heart. Circ Res. 1998;83:1-14.
6. Beltrami AP, Urbanek K, Kajstura J, Yan SM, Finato N, Bussani R, Nadal- Ginard B, Silvestri F, Leri A, Beltrami CA, Anversa P. Evidence that human cardiac myocytes divide after myocardial infarction. N Engl J Med. 2001;344:1750-1757. doi:10.1056/NEJM200106073442303.
7. Mummery CL, Lee RT. Is heart regeneration on the right track? Nat Med. 2013;19:412-413doi:10.1038/nm.3158.
8. Alkass K, Panula J, Westman M, Wu TD, Guerquin-Kern JL, Bergmann O. No evidence for cardiomyocyte number expansion in preadolescent mice. Cell. 2015;163:1026-1036doi:10.1016/j.cell.2015.10.035.
9. Bergmann O, Zdunek S, Felker A, et al. Dynamics of cell generation and turnover in the human heart. Cell. 2015;161:1566-1575doi:10.1016/j.cell.2015.05.026.
10. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabé-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, Frisén J. Evidence for cardiomyocyte renewal in humans. Science. 2009;324:98- 102doi:10.1126/science.1164680.
11. van Berlo JH, Molkentin JD. An emerging consensus on cardiac regeneration. Nat Med. 2014;20:1386-1393doi:10.1038/nm.3764.
12. Senyo SE, Steinhauser ML, Pizzimenti CL, Yang VK, Cai L, Wang M, Wu TD, Guerquin-Kern JL, Lechene CP, Lee RT. Mammalian heart renewal by pre-existing cardiomyocytes. Nature. 2013;493:433-436. doi:10.1038/nature11682.
13. Hsieh PC, Segers VF, Davis ME, MacGillivray C, Gannon J, Molkentin JD, Robbins J, Lee RT. Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med. 2007;13:970-974. doi:10.1038/nm1618.
14. Quaini F, Urbanek K, Beltrami AP, Finato N, Beltrami CA, Nadal-Ginard B, Kajstura J, Leri A, Anversa P. Chimerism of the transplanted heart. N Engl J Med. 2002;346:5-15. doi:10.1056/NEJMoa012081.
15. Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, Pickel J, McKay R, Nadal-Ginard B, Bodine DM, Leri A, Anversa P. Bone marrow cells regenerate infarcted myocardium. Nature. 2001;410:701-705. doi:10.1038/35070587.
16. Wu SM, Fujiwara Y, Cibulsky SM, Clapham DE, Lien CL, Schultheiss TM, Orkin SH. Developmental origin of a bipotential myocardial and smooth muscle cell precursor in the mammalian heart. Cell. 2006;127:1137-1150. doi:10.1016/j.cell.2006.10.028.
17. Wu JM, Hsueh YC, Ch'ang HJ, Luo CY, Wu LW, Nakauchi H, Hsieh PC. Circulating cells contribute to cardiomyocyte regeneration after injury. Circ Res. 2015;116:633-641doi:10.1161/CIRCRESAHA.116.304564.
18. 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.
19. Urbanek K, Cesselli D, Rota M, Nascimbene A, De Angelis A, Hosoda T, Bearzi C, Boni A, Bolli R, Kajstura J, Anversa P, Leri A. Stem cell niches in the adult mouse heart. Proc Natl Acad Sci U S A. 2006;103:9226-9231. doi:10.1073/pnas.0600635103.
20. Bearzi C, Rota M, Hosoda T, et al. Human cardiac stem cells. Proc Natl Acad Sci U S A. 2007;104:14068-14073. doi:10.1073/pnas.0706760104.
21. Ellison GM, Vicinanza C, Smith AJ, et al. Adult c-kit(pos) cardiac stem cells are necessary and sufficient for functional cardiac regeneration and repair. Cell. 2013;154:827-842. doi:10.1016/j.cell.2013.07.039.
22. Barile L, Messina E, Giacomello A, Marbán E. Endogenous cardiac stem cells. Prog Cardiovasc Dis. 2007;50:31-48. doi:10.1016/j.pcad.2007.03.005.
23. Smith RR, Barile L, Cho HC, Leppo MK, Hare JM, Messina E, Giacomello A, Abraham MR, Marbán E. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation. 2007;115:896-908. doi:10.1161/CIRCULATIONAHA.106.655209.
24. Tomita Y, Matsumura K, Wakamatsu Y, Matsuzaki Y, Shibuya I, Kawaguchi H, Ieda M, Kanakubo S, Shimazaki T, Ogawa S, Osumi N, Okano H, Fukuda K. Cardiac neural crest cells contribute to the dormant multipotent stem cell in the mammalian heart. J Cell Biol. 2005;170:1135-1146. doi:10.1083/jcb.200504061.
25. 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.
26. 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-S64doi:10.1161/CIRCULATIONAHA.112.092627.
27. Keith MC, Bolli R. "String theory" of c-kit(pos) cardiac cells: A new paradigm regarding the nature of these cells that may reconcile apparently discrepant results. Circ Res. 2015;116:1216-1230. doi:10.1161/CIRCRESAHA.116.305557.
28. Yuasa S, Itabashi Y, Koshimizu U, Tanaka T, Sugimura K, Kinoshita M, Hattori F, Fukami S, Shimazaki T, Ogawa S, Okano H, Fukuda K. Transient inhibition of BMP signaling by Noggin induces cardiomyocyte differentiation of mouse embryonic stem cells. Nat Biotechnol. 2005;23:607-611. doi:10.1038/nbt1093.
29. Tallini YN, Greene KS, Craven M, Spealman A, Breitbach M, Smith J, Fisher PJ, Steffey M, Hesse M, Doran RM, Woods A, Singh B, Yen A, Fleischmann BK, Kotlikoff MI. c-kit expression identifies cardiovascular precursors in the neonatal heart. Proc Natl Acad Sci U S A. 2009;106:1808- 1813. doi:10.1073/pnas.0808920106.
30. Orr-Urtreger A, Avivi A, Zimmer Y, Givol D, Yarden Y, Lonai P. Developmental expression of c-kit, a proto-oncogene encoded by the W locus. Development. 1990;109:911-923.
31. Wilson YM, Richards KL, Ford-Perriss ML, Panthier JJ, Murphy M. Neural crest cell lineage segregation in the mouse neural tube. Development. 2004;131:6153-6162. doi:10.1242/dev.01533.
32. Bernex F, De Sepulveda P, Kress C, Elbaz C, Delouis C, Panthier JJ. Spatial and temporal patterns of c-kit-expressing cells in WlacZ/+ and WlacZ/WlacZ mouse embryos. Development. 1996;122:3023-3033.
33. Loffredo FS, Steinhauser ML, Gannon J, Lee RT. Bone marrow-derived cell therapy stimulates endogenous cardiomyocyte progenitors and promotes cardiac repair. Cell Stem Cell. 2011;8:389-398. doi:10.1016/j.stem.2011.02.002.
34. Naqvi N, Li M, Calvert JW, et al. A proliferative burst during preadolescence establishes the final cardiomyocyte number. Cell. 2014;157:795- 807. doi:10.1016/j.cell.2014.03.035.
35. Hatzistergos KE, Quevedo H, Oskouei BN, et al. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ Res. 2010;107:913-922. doi:10.1161/CIRCRESAHA.110.222703.
36. Suzuki G, Iyer V, Lee TC, Canty JM Jr. Autologous mesenchymal stem cells mobilize cKit+ and CD133+ bone marrow progenitor cells and improve regional function in hibernating myocardium. Circ Res. 2011;109:1044-1054. doi:10.1161/CIRCRESAHA.111.245969.
37. Fioret BA, Heimfeld JD, Paik DT, Hatzopoulos AK. Endothelial cells contribute to generation of adult ventricular myocytes during cardiac homeostasis. Cell Rep. 2014;8:229-241. doi:10.1016/j.celrep.2014.06.004.
38. Ubil E, Duan J, Pillai IC, Rosa-Garrido M, Wu Y, Bargiacchi F, Lu Y, Stanbouly S, Huang J, Rojas M, Vondriska TM, Stefani E, Deb A. Mesenchymal-endothelial transition contributes to cardiac neovascularization. Nature. 2014;514:585-590. doi:10.1038/nature13839.
39. Moretti A, Caron L, Nakano A, Lam JT, Bernshausen A, Chen Y, Qyang Y, Bu L, Sasaki M, Martin-Puig S, Sun Y, Evans SM, Laugwitz KL, Chien KR. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell. 2006;127:1151-1165. doi:10.1016/j.cell.2006.10.029.
40. Nakano H, Liu X, Arshi A, Nakashima Y, van Handel B, Sasidharan R, Harmon AW, Shin JH, Schwartz RJ, Conway SJ, Harvey RP, Pashmforoush M, Mikkola HK, Nakano A. Haemogenic endocardium contributes to transient definitive haematopoiesis. Nat Commun. 2013;4:1564. doi:10.1038/ncomms2569.
41. Christoforou N, Liau B, Chakraborty S, Chellapan M, Bursac N, Leong KW. Induced pluripotent stem cell-derived cardiac progenitors differentiate to cardiomyocytes and form biosynthetic tissues. PLoS One. 2013;8:e65963. doi:10.1371/journal.pone.0065963.
42. Christoforou N, Miller RA, Hill CM, Jie CC, McCallion AS, Gearhart JD. Mouse ES cell-derived cardiac precursor cells are multipotent and facilitate identification of novel cardiac genes. J Clin Invest. 2008;118:894- 903. doi:10.1172/JCI33942.
43. Malliaras K, Zhang Y, Seinfeld J, Galang G, Tseliou E, Cheng K, Sun B, Aminzadeh M, Marbán E. Cardiomyocyte proliferation and progenitor cell recruitment underlie therapeutic regeneration after myocardial infarction in the adult mouse heart. EMBO Mol Med. 2013;5:191-209. doi:10.1002/emmm.201201737.
44. Ali SR, Hippenmeyer S, Saadat LV, Luo L, Weissman IL, Ardehali R. Existing cardiomyocytes generate cardiomyocytes at a low rate after birth in mice. Proc Natl Acad Sci U S A. 2014;111:8850-8855. doi:10.1073/pnas.1408233111.
45. Zaruba MM, Soonpaa M, Reuter S, Field LJ. Cardiomyogenic potential of C-kit(+)-expressing cells derived from neonatal and adult mouse hearts. Circulation. 2010;121:1992-2000. doi:10.1161/CIRCULATIONAHA.109.909093.
46. Kubin T, Pöling J, Kostin S, Gajawada P, Hein S, Rees W, Wietelmann A, Tanaka M, Lörchner H, Schimanski S, Szibor M, Warnecke H, Braun T. Oncostatin M is a major mediator of cardiomyocyte dedifferentiation and remodeling. Cell Stem Cell. 2011;9:420-432. doi:10.1016/j.stem.2011.08.013.
47. Karantalis V, Suncion-Loescher VY, Bagno L, et al. Synergistic effects of combined cell therapy for chronic ischemic cardiomyopathy. J Am Coll Cardiol. 2015;66:1990-1999. doi:10.1016/j.jacc.2015.08.879.
48. 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.
49. Nadal-Ginard B, Ellison GM, Torella D. Response to Molkentin's letter to the editor regarding article, "the absence of evidence is not evidence of absence: the pitfalls of Cre knock-ins in the c-kit locus". Circ Res. 2014;115:e38-e39. doi:10.1161/CIRCRESAHA.115.305380.