Bmi1 + cardiac progenitor cells contribute to myocardial repair following acute injury

Stem Cell Research and Therapy

Volumn 7, Issue 1, 2016, Pages

  Valiente Alandi, Iñigo ^a,c   Albo Castellanos, Carmen ^a,d   Herrero, Diego ^a,b   Sanchez, Iria ^a   Bernad, Antonio ^a,b  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d Vivebiotech ^*  (Spain)

Author keywords

Bmi1; Cardiac progenitor cells; Myocardial infarction; Stem cells

Indexed keywords

BMI1 PROTEIN; DPPA5 PROTEIN; MARKER; OCTAMER TRANSCRIPTION FACTOR 4; PROM1 PROTEIN; SUZ12 PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BMI1 PROTEIN, MOUSE; GT(ROSA)26SOR NON-CODING RNA, MOUSE; ONCOPROTEIN; PHOTOPROTEIN; TAMOXIFEN; TRANSCRIPTOME; UNTRANSLATED RNA; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ACUTE HEART INFARCTION; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC MUSCLE CELL; CARDIAC STEM CELL; CELL ISOLATION; CELL TRACKING; CONTROLLED STUDY; GENE EXPRESSION; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; TISSUE REPAIR; TRANSCRIPTOMICS; AGONISTS; ANIMAL; CARDIAC MUSCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HEART INFARCTION; HUMAN; MALE; METABOLISM; PATHOLOGY; REGENERATION; SIGNAL TRANSDUCTION; STEM CELL; TRANSGENIC MOUSE;

ANIMALS; BACTERIAL PROTEINS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TRACKING; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; HUMANS; LUMINESCENT PROTEINS; MALE; MICE; MICE, TRANSGENIC; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC; POLYCOMB REPRESSIVE COMPLEX 1; PROTO-ONCOGENE PROTEINS; REGENERATION; RNA, UNTRANSLATED; SIGNAL TRANSDUCTION; STEM CELLS; TAMOXIFEN; TRANSCRIPTOME;

EID: 84979680830     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/s13287-016-0355-7     Document Type: Article

References (41)

1. Laflamme MA, Murry CE. Heart regeneration. Nature. 2011;473:326-35.
2. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S, et al. Evidence for cardiomyocyte renewal in humans. Science. 2009;324:98-102.
3. Kajstura J, Urbanek K, Perl S, Hosoda T, Zheng H, Ogorek B, et al. Cardiomyogenesis in the adult human heart. Circ Res. 2010;107:305-15.
4. Steinhauser ML, Lee RT. Regeneration of the heart. EMBO Mol Med. 2011;3:701-12.
5. van Berlo JH, Molkentin JD. An emerging consensus on cardiac regeneration. Nat Med. 2014;20:1386-93.
6. Malliaras K, Zhang Y, Seinfeld J, Galang G, Tseliou E, Cheng K, et al. Cardiomyocyte proliferation and progenitor cell recruitment underlie therapeutic regeneration after myocardial infarction in the adult mouse heart. EMBO Mol Med. 2013;5:191-209.
7. Senyo SE, Steinhauser ML, Pizzimenti CL, Yang VK, Cai L, Wang M, et al. Mammalian heart renewal by pre-existing cardiomyocytes. Nature. 2013;493:433-6.
8. Zhang Y, Zhong JF, Qiu H, Robb MacLellan W, Marban E, Wang C. Epigenomic reprogramming of adult cardiomyocyte-derived cardiac progenitor cells. Sci Rep. 2015;5:17686.
9. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell. 2003;114:763-76.
10. Galvez BG, Sampaolesi M, Barbuti A, Crespi A, Covarello D, Brunelli S, et al. Cardiac mesoangioblasts are committed, self-renewable progenitors, associated with small vessels of juvenile mouse ventricle. Cell Death Differ. 2008;15:1417-28.
11. Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y, et al. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A. 2003;100:12313-8.
12. Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, Morrison SJ. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature. 2003;425:962-7.
13. Park IK, Qian D, Kiel M, Becker MW, Pihalja M, Weissman IL, et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature. 2003;423:302-5.
14. Sangiorgi E, Capecchi MR. Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet. 2008;40:915-20.
15. Valiente-Alandi I, Albo-Castellanos C, Herrero D, Arza E, Garcia-Gomez M, Segovia JC, et al. Cardiac Bmi1(+) cells contribute to myocardial renewal in the murine adult heart. Stem Cell Res Ther. 2015;6:205.
16. Jesty SA, Steffey MA, Lee FK, Breitbach M, Hesse M, Reining S, et al. c-kit+ precursors support postinfarction myogenesis in the neonatal, but not adult, heart. Proc Natl Acad Sci U S A. 2012;109:13380-5.
17. Porrello ER, Mahmoud AI, Simpson E, Hill JA, Richardson JA, Olson EN, et al. Transient regenerative potential of the neonatal mouse heart. Science. 2011;331:1078-80.
18. Ellison GM, Vicinanza C, Smith AJ, Aquila I, Leone A, Waring CD, et al. Adult c-kit(pos) cardiac stem cells are necessary and sufficient for functional cardiac regeneration and repair. Cell. 2013;154:827-42.
19. Tallini YN, Greene KS, Craven M, Spealman A, Breitbach M, Smith J, et al. c-kit expression identifies cardiovascular precursors in the neonatal heart. Proc Natl Acad Sci U S A. 2009;106:1808-13.
20. 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.
21. Liu Q, Yang R, Huang X, Zhang H, He L, Zhang L, et al. Genetic lineage tracing identifies in situ Kit-expressing cardiomyocytes. Cell Res. 2016;26:119-30.
22. van Berlo JH, Kanisicak O, Maillet M, Vagnozzi RJ, Karch J, Lin SC, et al. c-kit + cells minimally contribute cardiomyocytes to the heart. Nature. 2014;509:337-41.
23. Sultana N, Zhang L, Yan J, Chen J, Cai W, Razzaque S, et al. Resident c-kit(+) cells in the heart are not cardiac stem cells. Nat Commun. 2015;6:8701.
24. Uchida S, De Gaspari P, Kostin S, Jenniches K, Kilic A, Izumiya Y, et al. Sca1-derived cells are a source of myocardial renewal in the murine adult heart. Stem Cell Rep. 2013;1:397-410.
25. Hoch M, Fischer P, Stapel B, Missol-Kolka E, Sekkali B, Scherr M, et al. Erythropoietin preserves the endothelial differentiation capacity of cardiac progenitor cells and reduces heart failure during anticancer therapies. Cell Stem Cell. 2011;9:131-43.
26. Liang SX, Khachigian LM, Ahmadi Z, Yang M, Liu S, Chong BH. In vitro and in vivo proliferation, differentiation and migration of cardiac endothelial progenitor cells (SCA1+/CD31+ side-population cells). J Thromb Haemost. 2011;9:1628-37.
27. Bailey B, Fransioli J, Gude NA, Alvarez Jr R, Zhang X, Gustafsson AB, et al. Sca-1 knockout impairs myocardial and cardiac progenitor cell function. Circ Res. 2012;111:750-60.
28. Moon JH, Heo JS, Kim JS, Jun EK, Lee JH, Kim A, et al. Reprogramming fibroblasts into induced pluripotent stem cells with Bmi1. Cell Res. 2011;21:1305-15.
29. Onder TT, Kara N, Cherry A, Sinha AU, Zhu N, Bernt KM, et al. Chromatin-modifying enzymes as modulators of reprogramming. Nature. 2012;483:598-602.
30. Zhou Y, Wang L, Vaseghi HR, Liu Z, Lu R, Alimohamadi S, et al. Bmi1 is a key epigenetic barrier to direct cardiac reprogramming. Cell Stem Cell. 2016;18:382-95.
31. Hsieh PC, Segers VF, Davis ME, MacGillivray C, Gannon J, Molkentin JD, et al. Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med. 2007;13:970-4.
32. Malliaras K, Ibrahim A, Tseliou E, Liu W, Sun B, Middleton RC, et al. Stimulation of endogenous cardioblasts by exogenous cell therapy after myocardial infarction. EMBO Mol Med. 2014;6:760-77.
33. Oberpriller JO, Oberpriller JC. Response of the adult newt ventricle to injury. J Exp Zool. 1974;187:249-53.
34. Jopling C, Sleep E, Raya M, Marti M, Raya A, Izpisua Belmonte JC. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature. 2010;464:606-9.
35. Kikuchi K, Holdway JE, Werdich AA, Anderson RM, Fang Y, Egnaczyk GF, et al. Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature. 2010;464:601-5.
36. Porrello ER, Mahmoud AI, Simpson E, Johnson BA, Grinsfelder D, Canseco D, et al. Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family. Proc Natl Acad Sci U S A. 2013;110:187-92.
37. Konfino T, Landa N, Ben-Mordechai T, Leor J. The type of injury dictates the mode of repair in neonatal and adult heart. J Am Heart Assoc. 2015;4:e001320.
38. Aurora AB, Porrello ER, Tan W, Mahmoud AI, Hill JA, Bassel-Duby R, et al. Macrophages are required for neonatal heart regeneration. J Clin Invest. 2014;124:1382-92.
39. Sen S, Sadek HA. Neonatal heart regeneration: mounting support and need for technical standards. J Am Heart Assoc. 2015;4:e001727.
40. Soonpaa MH, Kim KK, Pajak L, Franklin M, Field LJ. Cardiomyocyte DNA synthesis and binucleation during murine development. Am J Physiol. 1996;271:H2183-9.
41. Fioret BA, Heimfeld JD, Paik DT, Hatzopoulos AK. Endothelial cells contribute to generation of adult ventricular myocytes during cardiac homeostasis. Cell Rep. 2014;8:229-41.