Cardiac regeneration in vivo: MENDING the heart from within?

Stem Cell Research

Volumn 13, Issue 3, 2014, Pages 523-531

  Bergmann, Olaf ^a   Jovinge, Stefan ^b,c,d  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SPECTRUM HEALTH   (United States)

^c VAN ANDEL INSTITUTE   (United States)

^d LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

STEM CELL FACTOR;

ADULT; CARDIAC STEM CELL; CELL CYCLE; CELL LINE; CELL MATURATION; CELL METABOLISM; CELL NUCLEUS; CELL REGENERATION; CELL RENEWAL; HEART INFARCTION; HEART INJURY; HEART MUSCLE CELL; HEART REGENERATION; HOMEOSTASIS; HUMAN; IN VIVO STUDY; NEWBORN PERIOD; NONHUMAN; PLOIDY; POLYPLOIDY; REGENERATIVE ABILITY; REVIEW; TISSUE REGENERATION; TURNOVER TIME; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; HEART; PHYSIOLOGY; REGENERATION; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; HEART; HUMANS; REGENERATION; STEM CELLS;

EID: 84911371541     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2014.07.002     Document Type: Review

References (82)

1. Adler C.P. DNA in growing hearts of children. Biochemical and cytophotometric investigations. Beitr. Pathol. 1976, 158:173-202.
2. Adler C.P. The development and regenerative potential of cardiac muscle. The Development and Regenerative Potential of Cardiac Muscle 1991, 227-252. HAP, London. J.O. Oberpriller, J.C. Oberpriller, A. Mauro (Eds.).
3. Adler C.P., Friedburg H., Herget G.W., Neuburger M., Schwalb H. Variability of cardiomyocyte DNA content, ploidy level and nuclear number in mammalian hearts. Virchows Arch. 1996, 429(2-3):159-164.
4. Andersen D.C., Ganesalingam S., Jensen C.H., Sheikh S.P. Do neonatal mouse hearts regenerate following heart apex resection?. Stem Cell Rep. 2014, 2(4):406-413. 10.1016/j.stemcr.2014.02.008.
5. Ang K.L., Shenje L.T., Reuter S., Soonpaa M.H., Rubart M., Field L.J., Galinanes M. Limitations of conventional approaches to identify myocyte nuclei in histologic sections of the heart. [Comparative Study]. Am. J. Physiol. Cell Physiol. 2010, 298(6):C1603-C1609. 10.1152/ajpcell.00435.2009.
6. Anversa P., Kajstura J., Rota M., Leri A. Regenerating new heart with stem cells. J. Clin. Invest. 2013, 123(1):62-70. 10.1172/JCI63068.
7. Beltrami A.P., Barlucchi L., Torella D., Baker M., Limana F., Chimenti S., Anversa P. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 2003, 114(6):763-776.
8. Bergmann O., Jovinge S. Isolation of cardiomyocyte nuclei from post-mortem tissue. J. Vis. Exp. 2012, (65). 10.3791/4205.
9. Bergmann O., Bhardwaj R., Bernard S., Zdunek S., Barnabe-Heider F., Walsh S., Frisen J. Evidence for cardiomyocyte renewal in humans. Science 2009, 324(5923):98-102. 10.1126/science.1164680.
10. Bergmann O., Zdunek S., Alkass K., Druid H., Bernard S., Frisén J. Identification of cardiomyocyte nuclei and assessment of ploidy for the analysis of cell turnover. Exp. Cell Res. 2011, 327(2):188-194.
11. Bergmann O., Liebl J., Bernard S., Alkass K., Yeung M.S.Y., Steier P., Frisen J. The age of olfactory bulb neurons in humans. Neuron 2012, 74(4):634-639. 10.1016/j.neuron.2012.03.030.
12. Bersell K., Arab S., Haring B., Kühn B. Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury. Cell 2009, 138:257-270. 10.1016/j.cell.2009.04.060.
13. Bettencourt-Dias M., Mittnacht S., Brockes J.P. Heterogeneous proliferative potential in regenerative adult newt cardiomyocytes. J. Cell Sci. 2003, 116:4001-4009. 10.1242/jcs.00698.
14. Bolli R., Chugh A.R., D'Amario D., Loughran J.H., Stoddard M.F., Ikram S., Anversa P. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 2011, 378(9806):1847-1857. 10.1016/S0140-6736(11)61590-0.
15. Burns K.A., Ayoub A.E., Breunig J.J., Adhami F., Weng W.-L., Colbert M.C., Kuan C.-Y. Nestin-CreER mice reveal DNA synthesis by nonapoptotic neurons following cerebral ischemia hypoxia. Cereb. Cortex 2007, 17:2585-2592. 10.1093/cercor/bhl164.
16. Chong J.J.H., Yang X., Don C.W., Minami E., Liu Y.-W., Weyers J.J., Murry C.E. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 2014, 10.1038/nature13233.
17. De Saint-Hubert M., Prinsen K., Mortelmans L., Verbruggen A., Mottaghy F.M. Molecular imaging of cell death. Methods (San Diego, Calif.) 2009, 48:178-187. 10.1016/j.ymeth.2009.03.022.
18. Ellison Georgina M., Vicinanza C., Smith Andrew J., Aquila I., Leone A., Waring Cheryl D., Nadal-Ginard B. Adult c-kitpos cardiac stem cells are necessary and sufficient for functional cardiac regeneration and repair. Cell 2013, 154:827-842. 10.1016/j.cell.2013.07.039.
19. Eriksson P.S., Perfilieva E., Björk-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med. 1998, 4:1313-1317. 10.1038/3305.
20. Fant X., Srsen V., Espigat-Georger A., Merdes A. Nuclei of non-muscle cells bind centrosome proteins upon fusion with differentiating myoblasts. PLoS One 2009, 4:e8303.
21. Gaj T., Gersbach C.A., Barbas C.F. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 2013, 31:397-405. 10.1016/j.tibtech.2013.04.004.
22. Galvez B.G., Sampaolesi M., Barbuti A., Crespi A., Covarello D., Brunelli S., Cossu G. Cardiac mesoangioblasts are committed, self-renewable progenitors, associated with small vessels of juvenile mouse ventricle. Cell Death Differ. 2008, 15:1417-1428.
23. Herget G.W., Neuburger M., Plagwitz R., Adler C.P. DNA content, ploidy level and number of nuclei in the human heart after myocardial infarction. Cardiovasc. Res. 1997, 36(1):45-51.
24. Hosoda T., D'Amario D., Cabral-Da-Silva M.C., Zheng H., Padin-Iruegas M.E., Ogorek B., Leri A. Clonality of mouse and human cardiomyogenesis in vivo. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(40):17169-17174. 10.1073/pnas.0903089106.
25. Hsieh P., Segers V., Davis M., Macgillivray C., Gannon J., Molkentin J., Lee R.T. Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat. Med. 2007, 13(8):970-974. 10.1038/nm1618.
26. Huttner H.B., Bergmann O., Salehpour M., Racz A., Tatarishvili J., Lindgren E., Frisen J. The age and genomic integrity of neurons after cortical stroke in humans. Nat. Neurosci. 2014, 10.1038/nn.3706.
27. Jesty S.A., Steffey M.A., Lee F.K., Breitbach M., Hesse M., Reining S., Kotlikoff M.I. c-kit+ precursors support postinfarction myogenesis in the neonatal, but not adult, heart. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:13380-13385. 10.1073/pnas.1208114109.
28. Kajstura J., Leri A., Finato N., Di Loreto C., Beltrami C.A., Anversa P. Myocyte proliferation in end-stage cardiac failure in humans. Proc. Natl. Acad. Sci. U. S. A. 1998, 95(15):8801-8805.
29. Kajstura J., Gurusamy N., Ogorek B., Goichberg P., Clavo-Rondon C., Hosoda T., Anversa P. Myocyte turnover in the aging human heart. Circ. Res. 2010, 107(11):1374-1386. 10.1161/CIRCRESAHA.110.231498.
30. Kajstura J., Urbanek K., Perl S., Hosoda T., Zheng H., Ogórek B., Anversa P. Cardiomyogenesis in the adult human heart. Circ. Res. 2010, 107(2):305-315.
31. Kanoh M., Takemura G., Misao J., Hayakawa Y., Aoyama T., Nishigaki K., Fujiwara H. Significance of myocytes with positive DNA in situ nick end-labeling (TUNEL) in hearts with dilated cardiomyopathy: not apoptosis but DNA repair. Circulation 1999, 99:2757-2764. 10.1161/01.CIR.99.21.2757.
32. Kikuchi K., Holdway J.E., Werdich A.A., Anderson R.M., Fang Y., Egnaczyk G.F., Poss K.D. Primary contribution to zebrafish heart regeneration by gata4+ cardiomyocytes. Nature 2010, 464:601-605.
33. Laflamme M.A., Murry C.E. Heart regeneration. Nature 2011, 473:326-335. 10.1038/nature10147.
34. Laugwitz K.L., Moretti A., Lam J., Gruber P., Chen Y., Woodard S., Chien K. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 2005, 433(7026):647-653. 10.1038/nature03215.
35. Li X., Yang Y., Bu L., Guo X., Tang C., Song J., Lai L. Rosa26-targeted swine models for stable gene over-expression and Cre-mediated lineage tracing. Cell Res. 2014, 24:501-504. 10.1038/cr.2014.15.
36. Loffredo F.S., Steinhauser M.L., Gannon J., Lee R.T. Bone marrow-derived cell therapy stimulates endogenous cardiomyocyte progenitors and promotes cardiac repair. Cell Stem Cell 2011, 8(4):389-398. 10.1016/j.stem.2011.02.002.
37. Mahmoud A.I., Kocabas F., Muralidhar S.A., Kimura W., Koura A.S., Thet S., Sadek H.A. Meis1 regulates postnatal cardiomyocyte cell cycle arrest. Nature 2013, 497:249-253. 10.1038/nature12054.
38. Mallat Z., Fornes P., Costagliola R., Esposito B., Belmin J., Lecomte D., Tedgui A. Age and gender effects on cardiomyocyte apoptosis in the normal human heart. J. Gerontol. A: Biol. Med. Sci. 2001, 56:M719-M723.
39. Malliaras K., Makkar R.R., Smith R.R., Cheng K., Wu E., Bonow R.O., Marbán E. Intracoronary cardiosphere-derived cells after myocardial infarction: evidence for therapeutic regeneration in the final 1-year results of the CADUCEUS trial. J. Am. Coll. Cardiol. 2013, 10.1016/j.jacc.2013.08.724.
40. Martin C.M., Meeson A.P., Robertson S.M., Hawke T.J., Richardson J.A., Bates S., Garry D.J. Persistent expression of the ATP-binding cassette transporter, Abcg2, identifies cardiac SP cells in the developing and adult heart. Dev. Biol. 2004, 265:262-275.
41. Meckert P.C., Rivello H.G., Vigliano C., González P., Favaloro R., Laguens R. Endomitosis and polyploidization of myocardial cells in the periphery of human acute myocardial infarction. Cardiovasc. Res. 2005, 67:116-123.
42. Molkentin J.D., Houser S.R. Are resident c-Kit+ cardiac stem cells really all that are needed to mend a broken heart?. Circ. Res. 2013, 113(9):1037-1039. 10.1161/CIRCRESAHA.113.302564.
43. Mollova M., Bersell K., Walsh S., Savla J., Das L.T., Park S.-Y., Kühn B. Cardiomyocyte proliferation contributes to heart growth in young humans. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:1446-1451. 10.1073/pnas.1214608110.
44. Moretti A., Caron L., Nakano A., Lam J.T., Bernshausen A., Chen Y., Chien K.R. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 2006, 127:1151-1165.
45. Naqvi N., Li M., Calvert John W., Tejada T., Lambert Jonathan P., Wu J., Husain A. A proliferative burst during preadolescence establishes the final cardiomyocyte number. Cell 2014, 157:795-807. 10.1016/j.cell.2014.03.035.
46. Oh H., Bradfute S.B., Gallardo T.D., Nakamura T., Gaussin V., Mishina Y., Schneider M.D. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:12313-12318.
47. Olivetti G., Abbi R., Quaini F., Kajstura J., Cheng W., Nitahara J.A., Anversa P. Apoptosis in the failing human heart. N. Engl. J. Med. 1997, 336:1131-1141. 10.1056/NEJM199704173361603.
48. Passier R., van Laake L.W., Mummery C.L. Stem-cell-based therapy and lessons from the heart. Nature 2008, 453:322-329.
49. Porrello E.R., Mahmoud A.I., Simpson E., Hill J.A., Richardson J.A., Olson E.N., Sadek H.A. Transient regenerative potential of the neonatal mouse heart. Science 2011, 331(6020):1078-1080. 10.1126/science.1200708.
50. Porrello E.R., Mahmoud A.I., Simpson E., Johnson B.A., Grinsfelder D., Canseco D., Sadek H.A. Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:187-192. 10.1073/pnas.1208863110.
51. Poss K.D., Wilson L.G., Keating M.T. Heart regeneration in zebrafish. Science (New York, N.Y.) 2002, 298:2188-2190. 10.1126/science.1077857.
52. Puente Bao N., Kimura W., Muralidhar Shalini A., Moon J., Amatruda James F., Phelps Kate L., Sadek Hesham A. The oxygen-rich postnatal environment induces cardiomyocyte cell-cycle arrest through DNA damage response. Cell 2014, 157:565-579. 10.1016/j.cell.2014.03.032.
53. Rivello H.G., Meckert P.C., Vigliano C., Favaloro R., Laguens R.P. Cardiac myocyte nuclear size and ploidy status decrease after mechanical support. Cardiovasc. Pathol. 2001, 10(2):53-57. (doi: S1054-8807(01)00068-0 [pii]).
54. Rodriguez M., Schaper J. Apoptosis: measurement and technical issues. J. Mol. Cell. Cardiol. 2005, 38:15-20. 10.1016/j.yjmcc.2004.11.002.
55. Rota M., Hosoda T., De Angelis A., Arcarese M.L., Esposito G., Rizzi R., Kajstura J. The young mouse heart is composed of myocytes heterogeneous in age and function. Circ. Res. 2007, 101:387-399.
56. Sandstedt J., Jonsson M., Lindahl A., Jeppsson A., Asp J. C-kit+ CD45- cells found in the adult human heart represent a population of endothelial progenitor cells. Bas. Res. Cardiol. 2010, 105:545-556. 10.1007/s00395-010-0088-1.
57. Saraste A., Pulkki K., Kallajoki M., Heikkilä P., Laine P., Mattila S., Voipio-Pulkki L.M. Cardiomyocyte apoptosis and progression of heart failure to transplantation. Eur. J. Clin. Investig. 1999, 29:380-386.
58. Senyo S.E., Steinhauser M.L., Pizzimenti C.L., Yang V.K., Cai L., Wang M., Lee R.T. Mammalian heart renewal by pre-existing cardiomyocytes. Nature 2013, 493(7432):433-436. 10.1038/nature11682.
59. Smart N., Bollini S., Dube K.N., Vieira J.M., Zhou B., Davidson S., Riley P.R. De novo cardiomyocytes from within the activated adult heart after injury. Nature 2011, 474(7353):640-644. 10.1038/nature10188.
60. Smith R.R., Barile L., Cho H.C., Leppo M.K., Hare J.M., Messina E., Marbán E. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 2007, 115(7):896-908. 10.1161/CIRCULATIONAHA.106.655209.
61. Soonpaa M.H., Field L.J. Assessment of cardiomyocyte DNA synthesis in normal and injured adult mouse hearts. Am. J. Physiol. 1997, 272:H220-H226.
62. Soonpaa M.H., Kim K.K., Pajak L., Franklin M., Field L.J. Cardiomyocyte DNA synthesis and binucleation during murine development. Am. J. Physiol. 1996, 271(5 Pt 2):H2183-H2189.
63. Spalding K.L., Bhardwaj R.D., Buchholz B.A., Druid H., Frisén J. Retrospective birth dating of cells in humans. Cell 2005, 122:133-143.
64. Spalding K.L., Bergmann O., Alkass K., Bernard S., Salehpour M., Huttner H.B., Frisén J. Dynamics of hippocampal neurogenesis in adult humans. Cell 2013, 153:1219-1227. 10.1016/j.cell.2013.05.002.
65. Srsen V., Fant X., Heald R., Rabouille C., Merdes A. Centrosome proteins form an insoluble perinuclear matrix during muscle cell differentiation. BMC Cell Biol. 2009, 10:28.
66. Stamm C., Choi Y.-H., Nasseri B., Hetzer R. A heart full of stem cells: the spectrum of myocardial progenitor cells in the postnatal heart. Ther. Adv. Cardiovasc. Dis. 2009, 3:215-229.
67. Szibor M., Pöling J., Warnecke H., Kubin T., Braun T. Remodeling and dedifferentiation of adult cardiomyocytes during disease and regeneration. Cell. Mol. Life Sci. 2013, 10.1007/s00018-013-1535-6.
68. Takamatsu T., Nakanishi M., Fukuda M., Fujita S. Cytofluorometric nuclear DNA-determinations in infant, adolescent, adult and aging human hearts. Histochemistry 1983, 485-494.
69. Takemura G., Kanoh M., Minatoguchi S., Fujiwara H. Cardiomyocyte apoptosis in the failing heart-a critical review from definition and classification of cell death. Int. J. Cardiol. 2013, 167:2373-2386. 10.1016/j.ijcard.2013.01.163.
70. Tallini Y.N., Greene K.S., Craven M., Spealman A., Breitbach M., Smith J., Kotlikoff M.I. C-kit expression identifies cardiovascular precursors in the neonatal heart. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1808-1813.
71. Tatsuka M., Katayama H., Ota T., Tanaka T., Odashima S., Suzuki F., Terada Y. Multinuclearity and increased ploidy caused by overexpression of the aurora- and Ipl1-like midbody-associated protein mitotic kinase in human cancer cells. Cancer Res. 1998, 58:4811-4816.
72. Uchida S., De Gaspari P., Kostin S., Jenniches K., Kilic A., Izumiya Y., Braun T. Sca1-derived cells are a source of myocardial renewal in the murine adult heart. Stem Cell Rep. 2013, 1:397-410. 10.1016/j.stemcr.2013.09.004.
73. van Berlo J.H., Kanisicak O., Maillet M., Vagnozzi R.J., Karch J., Lin S.C., Molkentin J.D. c-kit cells minimally contribute cardiomyocytes to the heart. Nature 2014, 10.1038/nature13309.
74. Vliegen H.W., Eulderink F., Bruschke A.V., van Der Laarse A., Cornelisse C.J. Polyploidy of myocyte nuclei in pressure overloaded human hearts: a flow cytometric study in left and right ventricular myocardium. Am. J. Cardiovasc. Pathol. 1995, 5:27-31.
75. Walsh S., Pontén A., Fleischmann B.K., Jovinge S. Cardiomyocyte cell cycle control and growth estimation in vivo-an analysis based on cardiomyocyte nuclei. Cardiovasc. Res. 2010, 86:365-373. 10.1093/cvr/cvq005.
76. Wang J., Panáková D., Kikuchi K., Holdway J.E., Gemberling M., Burris J.S., Poss K.D. The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion. Development (Cambridge, Engl.) 2011, 138:3421-3430. 10.1242/dev.068601.
77. Wilson A., Laurenti E., Oser G., van Der Wath R.C., Blanco-Bose W., Jaworski M., Trumpp A. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008, 135:1118-1129.
78. Wohlschlaeger J., Levkau B., Brockhoff G., Schmitz K.J., von Winterfeld M., Takeda A., Baba H.A. Hemodynamic support by left ventricular assist devices reduces cardiomyocyte DNA content in the failing human heart. Circulation 2010, 121(8):989-996.
79. Xin M., Kim Y., Sutherland L.B., Murakami M., Qi X., McAnally J., Olson E.N. Hippo pathway effector Yap promotes cardiac regeneration. Proc. Natl. Acad. Sci. 2013, 110:13839-13844. 10.1073/pnas.1313192110.
80. Yoon C.-H., Koyanagi M., Iekushi K., Seeger F., Urbich C., Zeiher A.M., Dimmeler S. Mechanism of improved cardiac function after bone marrow mononuclear cell therapy. Role of cardiovascular lineage commitment. Circulation 2010, 21(18):2001-2011.
81. Zangi L., Lui K.O., von Gise A., Ma Q., Ebina W., Ptaszek L.M., Chien K.R. Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction. Nat. Biotechnol. 2013, 31(10):898-907. 10.1038/nbt.2682.
82. Zaruba M.M., Soonpaa M., Reuter S., Field L.J. Cardiomyogenic potential of C-kit(+)-expressing cells derived from neonatal and adult mouse hearts. Circulation 2010, 121(18):1992-2000. 10.1161/CIRCULATIONAHA.109.909093.