Isolation and characterization of resident endogenous c-Kit+ cardiac stem cells from the adult mouse and rat heart

Nature Protocols

Volumn 9, Issue 7, 2014, Pages 1662-1681

  Smith, Andrew J ^a,b   Lewis, Fiona C ^a,b   Aquila, Iolanda ^c   Waring, Cheryl D ^d   Nocera, Aurora ^c   Agosti, Valter ^c   Nadal Ginard, Bernardo ^a,b   Torella, Daniele ^c   Ellison, Georgina M ^a,c  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^d LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

STEM CELL FACTOR RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARDIAC STEM CELL; CELL COUNT; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINEAGE; CELL POPULATION; CELL RENEWAL; CELL SELECTION; CENTRIFUGATION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; MALE; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; RAT; ANIMAL; CELL CULTURE; CULTURE TECHNIQUE; CYTOLOGY; HEART MUSCLE; METABOLISM; STEM CELL;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; MICE; MYOCARDIUM; PROTO-ONCOGENE PROTEINS C-KIT; RATS; STEM CELLS;

EID: 84905273160     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2014.113     Document Type: Article

References (45)

1. Bergmann, O. et al. Evidence for cardiomyocyte renewal in humans. Science 324, 98-102 (2009).
2. Beltrami, A.P. et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114, 763-776 (2003).
3. Hierlihy, A.M. et al. The post-natal heart contains a myocardial stem cell population. FEBS Lett. 530, 239-243 (2002).
4. + cardiac stem cells are necessary and suffcient for functional cardiac regeneration and repair. Cell 154, 827-842 (2013).
5. Linke, A. et al. Stem cells in the dog heart are self-renewing, clonogenic, and multipotent and regenerate infarcted myocardium, improving cardiac function. Proc. Natl. Acad. Sci. USA 102, 8966-8971 (2005).
6. Ellison, G.M. et al. Endogenous cardiac stem cell activation by IGF-1/HGF intracoronary injection fosters survival and regeneration of the infarcted pig heart. J. Am. Coll. Cardiol. 58, 977-986 (2011).
7. Hou, X. et al. Isolation, characterisation and spatial distribution of cardiac progenitor cells in the sheep heart. J. Clin. Exp. Cardiolog. s6, 1-16 (2012).
8. Torella, D. et al. Biological properties and regenerative potential, in vitro and in vivo, of human cardiac stem cells isolated from each of the four chambers of the adult human heart. Circulation 114, 87 (2006).
9. Bearzi, C. et al. Human cardiac stem cells. Proc. Natl. Acad. Sci. USA 104, 14068-14073 (2007).
10. Oh, H. et al. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc. Natl. Acad. Sci. USA 100, 12313-12318 (2003).
11. van Vliet, P. et al. Progenitor cells isolated from the human heart: a potential cell source for regenerative therapy. Neth. Heart J. 16, 163-169 (2008).
12. Martin, C.M. et al. Persistent expression of the ATP-binding cassette transporter, Abcg2, identifes cardiac SP cells in the developing and adult heart. Dev. Biol. 265, 262-275 (2004).
13. Sanstedt, J. et al. Left atrium of the human heart contains a population of side population cells. Basic Res. Cardiol. 107, 255 (2012).
14. Messina, E. et al. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ. Res. 95, 911-921 (2004).
15. Chimenti, I. et al. Isolation and expansion of adult cardiac stem/progenitor cells in the form of cardiospheres from human cardiac biopsies and murine hearts. Methods Mol. Biol. 879, 327-338 (2012).
16. Tan, J.J. et al. Isolation and expansion of cardiosphere-derived stem cells. Curr. Protoc. Stem Cell Biol. 16, 2C.3.1-2C.3.12 (2011).
17. Chong, J.J. et al. Adult cardiac-resident MSC-like stem cells with a proepicardial origin. Cell Stem Cell 9, 527-540 (2011).
18. Limana, F. et al. Identifcation of myocardial and vascular precursor cells in human and mouse epicardium. Circ. Res. 101, 1255-1265 (2007).
19. Sampaolesi, M. et al. Cell therapy of primary myopathies. Arch. Ital. Biol. 143, 235-242 (2005).
20. + cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433, 647-653 (2005).
21. Bu, L. et al. Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature 460, 113-117 (2009).
22. Smits, A.M. et al. Human cardiomyocyte progenitor cells differentiate into functional mature cardiomyocytes: an in vitro model for studying human cardiac physiology and pathophysiology. Nat. Protoc. 4, 232-243 (2009).
23. Koninckx, R. et al. The cardiac atrial appendage stem cell: a new and promising candidate for myocardial repair. Cardiovasc. Res. 97, 413-423 (2013).
24. Beltrami, A.P. et al. Evidence that human cardiac myocytes divide after myocardial infarction. N. Engl. J. Med. 344, 1750-1757 (2001).
25. Ellison, G.M., Nadal-Ginard, B. & Torella, D. Optimizing cardiac repair and regeneration through activation of the endogenous cardiac stem cell compartment. J. Cardiovasc. Transl. Res. 5, 667-677 (2012).
26. Genead, R. et al. Islet-1 cells are cardiac progenitors present during the entire lifespan: from the embryonic stage to adulthood. Stem Cells Dev. 19, 1601-1615 (2010).
27. Dey, D. et al. Dissecting the molecular relationship among various cardiogenic progenitor cells. Circulation 112, 1253-1262 (2013).
28. Ellison, G.M. et al. Adult cardiac stem cells: identity, location and potential. in Adult Stem Cells 2nd edn, (ed. Turksen, K.) 47-90 (Springer, 2014).
29. Torella, D., Ellison, G.M., Karakikes, I. & Nadal-Ginard, B. Resident cardiac stem cells. Cell. Mol. Life Sci. 64, 661-673 (2007).
30. Silver, L.H., Hemwall, E.L., Marino, T.A. & Houser, S.R. Isolation and morphology of calcium-tolerant feline ventricular myocytes. Am. J. Physiol. 245, H891-H896 (1983).
31. Waring, C.D. et al. The adult heart responds to increased workload with physiologic hypertrophy, cardiac stem cell activation, and new myocyte formation. Eur. Heart J. doi:10.1093/eurheartj/ehs338 (2012).
32. + GATA-4 high rat cardiac stem cells foster adult cardiomyocyte survival through IGF-1 paracrine signalling. PLoS ONE 5, e14297 (2010).
33. Sperr, W.R. et al. The human cardiac mast cell: localisation, isolation, phenotype and functional characterisation. Blood 84, 3876-3884 (1994).
34. Gil-Perotín, S. et al. Adult neural stem cells from the subventricular zone: a review of the neurosphere assay. Anat. Rec. 296, 1435-1452 (2013).
35. Lauden, L. et al. Allogenicity of human cardiac stem/progenitor cells orchestrated by programmed death ligand 1. Circ. Res. 112, 451-464 (2013).
36. + embryonic-stem-cell-derived population. Nature 453, 524-528 (2008).
37. Strauer, B.E. & Steinhoff, G. 10 years of intracoronary and intramyocardial bone marrow stem cell therapy of the heart: from the methodological origin to clinical practice. J. Am. Coll. Cardiol. 58, 1095-1104 (2011).
38. Matsuura, K. et al. Cardiomyocytes fuse with surrounding non cardiomyocytes and reenter the cell cycle. J. Cell Biol. 167, 351-363 (2004).
39. + cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ. Res. 97, 52-61 (2005).
40. Oyama, T. et al. Cardiac side population cells have a potential to migrate and differentiate into cardiomyocytes in vitro and in vivo. J. Cell Biol. 176, 329-341 (2007).
41. Smith, R.R. et al. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115, 896-908 (2007).
42. Carr, C.A. et al. Cardiosphere-derived cells improve function in the infarcted rat heart for at least 16 weeks: an MRI study. PLoS ONE 6, e25669 (2011).
43. Bolli, R. et al. Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 378, 1847-1857 (2011).
44. Malliaras, K. et al. Intracoronary cardiosphere-derived cells after myocardial infarction: evidence for therapeutic regeneration in the fnal 1-year results of the CADUCEUS trial. J. Am. Coll. Cardiol. 63, 110-122 (2014).
45. Zhang, J. et al. Functional cardiomyocytes derived from human induced pluripotent cells. Circ. Res. 104, e30-e41 (2009).