Sca-1+cardiac progenitor cells and heart-making: A critical synopsis

Stem Cells and Development

Volumn 23, Issue 19, 2014, Pages 2263-2273

  Valente, Mariana ^a,b   Nascimento, Diana Santos ^a   Cumano, Ana ^b   Pinto Do Ó, Perpétua ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b Cellule Pasteur INSERM U1223   (France)

Author keywords

[No Author keywords available]

Indexed keywords

STEM CELL ANTIGEN 1; LY ANTIGEN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; CARDIAC STEM CELL; CELL DIFFERENTIATION; CELL LEVEL; CELL POPULATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FIBROBLAST; IN VITRO STUDY; INTRACELLULAR SPACE; MESENCHYMAL STEM CELL; MESODERM; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; REVIEW; STEM CELL; ANIMAL; CYTOLOGY; HEART; HEART MUSCLE CELL; HUMAN; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTIGENS, LY; CELL DIFFERENTIATION; HEART; HUMANS; MYOCYTES, CARDIAC; STEM CELLS;

EID: 84907432293     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0197     Document Type: Review

References (109)

1. Hsieh PC, VF Segers, ME Davis, C MacGillivray, J Gannon, JD Molkentin, J Robbins and RT Lee. (2007). Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med 13:970-974.
2. Senyo SE, ML Steinhauser, CL Pizzimenti, VK Yang, L Cai, M Wang, TD Wu, JL Guerquin-Kern, CP Lechene and RT Lee. (2013). Mammalian heart renewal by preexisting cardiomyocytes. Nature 493:433-436.
3. Bergmann O, RD Bhardwaj, S Bernard, S Zdunek, F Barnabe-Heider, S Walsh, J Zupicich, K Alkass, BA Buchholz et al. (2009). Evidence for cardiomyocyte renewal in humans. Science 324:98-102.
4. Kajstura J, K Urbanek, S Perl, T Hosoda, H Zheng, B Ogorek, J Ferreira-Martins, P Goichberg, C Rondon-Cla-vo et al. (2010). Cardiomyogenesis in the adult human heart. Circ Res 107:305-315.
5. Malliaras K, Y Zhang, J Seinfeld, G Galang, E Tseliou, K Cheng, B Sun, M Aminzadeh and E Marban. (2013). Car-diomyocyte proliferation and progenitor cell recruitment underlie therapeutic regeneration after myocardial infarction in the adult mouse heart. EMBO Mol Med 5:191-209.
6. Porrello ER, AI Mahmoud, E Simpson, JA Hill, JA Richardson, EN Olson and HA Sadek. (2011). Transient regenerative potential of the neonatal mouse heart. Science 331:1078-1080.
7. Porrello ER, AI Mahmoud, E Simpson, BA Johnson, D Grinsfelder, D Canseco, PP Mammen, BA Rothermel, EN Olson and HA Sadek. (2013). Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family. Proc Natl Acad Sci USA 110:187-192.
8. Clubb FJ, Jr. and SP Bishop. (1984). Formation of binu-cleated myocardial cells in the neonatal rat. An index for growth hypertrophy. Lab Invest 50:571-577.
9. Soonpaa MH, KK Kim, L Pajak, M Franklin and LJ Field. (1996). Cardiomyocyte DNA synthesis and binucleation during murine development. Am J Physiol 271:H2183-H2189.
10. Goldman S. (2005). Stem and progenitor cell-based therapy of the human central nervous system. Nat Biotechnol 23:862-871.
11. Warejcka DJ, R Harvey, BJ Taylor, HE Young and PA Lucas. (1996). A Population of cells isolated from rat heart capable of differentiating into several mesodermal phenotypes. J Surg Res 62:233-242.
12. Smith RR, L Barile, HC Cho, MK Leppo, JM Hare, E Messina, A Giacomello, MR Abraham and E Marban. (2007). Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115:896-908.
13. Hierlihy AM, P Seale, CG Lobe, MA Rudnicki and LA Megeney. (2002). The post-natal heart contains a myo-cardial stem cell population. FEBS Lett 530:239-243.
14. Martin CM, AP Meeson, SM Robertson, TJ Hawke, JA Richardson, S Bates, SC Goetsch, TD Gallardo and DJ Garry. (2004). Persistent expression of the ATP-binding cassette transporter, Abcg2, identifies cardiac SP cells in the developing and adult heart. Dev Biol 265:262-275.
15. Pfister O, F Mouquet, M Jain, R Summer, M Helmes, A Fine, WS Colucci and R Liao. (2005). CD31-but not CD31 + cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ Res 97:52-61.
16. Oyama T, T Nagai, H Wada, AT Naito, K Matsuura, K Iwanaga, T Takahashi, M Goto, Y Mikami et al. (2007). Cardiac side population cells have a potential to migrate and differentiate into cardiomyocytes in vitro and in vivo. J Cell Biol 176:329-341.
17. Yamahara K, S Fukushima, SR Coppen, LE Felkin, A Varela-Carver, PJR Barton, MH Yacoub and K Suzuki. (2008). Heterogeneic nature of adult cardiac side population cells. Biochem Biophys Res Commun 371:615-620.
18. Messina E, L De Angelis, G Frati, S Morrone, S Chimenti, F Fiordaliso, M Salio, M Battaglia, MVG Latronico et al. (2004). Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 95:911-921.
19. Ye J, A Boyle, H Shih, RE Sievers, Y Zhang, M Prasad, H Su, Y Zhou, W Grossman, HS Bernstein and Y Yeghiazar-ians. (2012). Sca-1 + cardiosphere-derived cells are enriched for Isl1-expressing cardiac precursors and improve cardiac function after myocardial injury. PLoS One 7:e30329.
20. Beltrami AP, L Barlucchi, D Torella, M Baker, F Limana, S Chimenti, H Kasahara, M Rota, E Musso et al. (2003). Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114:763-776.
21. Gambini E, G Pompilio, A Biondi, F Alamanni, MC Ca-pogrossi, M Agrifoglio and M Pesce. (2011). C-kit + cardiac progenitors exhibit mesenchymal markers and preferential cardiovascular commitment. Cardiovasc Res 89:362-373.
22. Tateishi K, E Ashihara, N Takehara, T Nomura, S Honsho, T Nakagami, S Morikawa, T Takahashi, T Ueyama, H Matsubara and H Oh. (2007). Clonally amplified cardiac stem cells are regulated by Sca-1 signaling for efficient cardiovascular regeneration. J Cell Sci 120:1791-1800.
23. Chong JJ, V Chandrakanthan, M Xaymardan, NS Asli, J Li, I Ahmed, C Heffernan, MK Menon, CJ Scarlett et al. (2011). Adult cardiac-resident MSC-like stem cells with a proepicardial origin. Cell 9:527-540.
24. Takamiya M, KH Haider and M Ashraf. (2011). Identification and characterization of a novel multipotent sub-population of Sca-1(+) cardiac progenitor cells for myocardial regeneration. PLoS One 6:e25265.
25. Oh H, SB Bradfute, TD Gallardo, T Nakamura, V Gaus-sin, Y Mishina, J Pocius, LH Michael, RR Behringer et al. (2003). Cardiac progenitor cells from adult myocardium: Homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 100:12313-12318.
26. Balsam LB, AJ Wagers, JL Christensen, T Kofidis, IL Weissman and RC Robbins. (2004). Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428:668-673.
27. Wagers AJ and IL Weissman. (2004). Plasticity of adult stem cells. Cell 116:639-648.
28. Lyngbæk S, M Schneider, J Hansen and S Sheikh. (2007). Cardiac regeneration by resident stem and progenitor cells in the adult heart. Basic Res Cardiol 102:101-114.
29. Segers VF and RT Lee. (2008). Stem-cell therapy for cardiac disease. Nature 451:937-942.
30. Bearzi C, M Rota, T Hosoda, J Tillmanns, A Nascimbene, A De Angelis, S Yasuzawa-Amano, I Trofimova, RW Siggins et al. (2007). Human cardiac stem cells. Proc Natl Acad Sci USA 104:14068-14073.
31. Ferreira-Martins J, B Ogorek, D Cappetta, A Matsuda, S Signore, D D'Amario, J Kostyla, E Steadman, N Ide-Iwata et al. (2012). Cardiomyogenesis in the developing heart is regulated by c-kit-positive cardiac stem cells. Circ Res 110:701-715.
32. Eberhard D and H Jockusch. (2005). Patterns of myocar-dial histogenesis as revealed by mouse chimeras. Dev Biol 278:336-346.
33. Orlic D, J Kajstura, S Chimenti, F Limana, I Jakoniuk, F Quaini, B Nadal-Ginard, DM Bodine, A Leri and P An-versa. (2001). Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci USA 98:10344-10349.
34. Quaini F, K Urbanek, AP Beltrami, N Finato, CA Bel-trami, B Nadal-Ginard, J Kajstura, A Leri and P Anversa. (2002). Chimerism of the transplanted heart. N Engl J Med 346:5-15.
35. Fazel S, M Cimini, L Chen, S Li, D Angoulvant, P Fedak, S Verma, RD Weisel, A Keating and R-K Li. (2006). Cardioprotective c-kit+ cells are from the bone marrow and regulate the myocardial balance of angiogenic cyto-kines. J Clin Invest 116:1865-1877.
36. Dimmeler S, AM Zeiher and MD Schneider. (2005). Unchain my heart: the scientific foundations of cardiac repair. J Clin Invest 115:572-583.
37. Wang X, Q Hu, Y Nakamura, J Lee, G Zhang, AH From and J Zhang. (2006). The role of the sca-1+/CD31-cardiac progenitor cell population in postinfarction left ventricular remodeling. Stem cells 24:1779-1788.
38. van Vliet P, M Roccio, A Smits, A van Oorschot, C Metz, T van Veen, J Sluijter, P Doevendans and MJ Goumans. (2008). Progenitor cells isolated from the human heart: a potential cell source for regenerative therapy. Neth Heart J 16:163-169.
39. Freire AG, DS Nascimento, G Forte, M Valente, TP Re-sende, S Pagliari, C Abreu, I Carvalho, P Di Nardo and P Pinto-do-O. (2014). Stable phenotype and function of immortalized Lin-Sca-1 + cardiac progenitor cells in long-term culture: a step closer to standardization. Stem Cells Dev 23:1012-1026.
40. Reinecke H, E Minami, WZ Zhu and MA Laflamme. (2008). Cardiogenic differentiation and transdifferentia-tion of progenitor cells. Circ Res 103:1058-1071.
41. Gonzales C and T Pedrazzini. (2009). Progenitor cell therapy for heart disease. Exp Cell Res 315:3077-3085.
42. Bolli R, AR Chugh, D D'Amario, JH Loughran, MF Stoddard, S Ikram, GM Beache, SG Wagner, A Leri et al. (2011). Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 378:1847-1857.
43. Makkar RR, RR Smith, K Cheng, K Malliaras, LE Thomson, D Berman, LS Czer, L Marban, A Mendizabal et al. (2012). Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADU-CEUS): a prospective, randomised phase 1 trial. Lancet 379:895-904.
44. van de Rijn M, S Heimfeld, GJ Spangrude and IL Weissman. (1989). Mouse hematopoietic stem-cell antigen Sca-1 is a member of the Ly-6 antigen family. Proc Natl Acad Sci USA 86:4634-4638.
45. Kotton DN, RS Summer, X Sun, BY Ma and A Fine. (2003). Stem cell antigen-1 expression in the pulmonary vascular endothelium. Am J Physiol Lung Cell Mol Physiol 284:L990-L996.
46. Luna G, J Paez and JE Cardier. (2004). Expression of the hematopoietic stem cell antigen Sca-1 (LY-6A/E) in liver sinusoidal endothelial cells: possible function of Sca-1 in endothelial cells. Stem Cells Dev 13:528-535.
47. +endothelial cells (SPECs) reside in the portal area of the liver and contribute to rapid recovery from acute liver disease. Biochem Biophys Res Commun 365:595-601.
48. Kang SG, N Shinojima, A Hossain, J Gumin, RL Yong, H Colman, F Marini, M Andreeff and FF Lang. (2010). Isolation and perivascular localization of mesenchymal stem cells from mouse brain. Neurosurgery 67:711-720.
49. Smits AM, P van Vliet, CH Metz, T Korfage, JP Sluijter, PA Doevendans and MJ Goumans. (2009). Human car-diomyocyte progenitor cells differentiate into functional mature cardiomyocytes: an in vitro model for studying human cardiac physiology and pathophysiology. Nat Protoc 4:232-243.
50. Asakura A and MA Rudnicki. (2002). Side population cells from diverse adult tissues are capable of in vitro hemato-poietic differentiation. Exp Hematol 30:1339-1345.
51. Challen GA and MH Little. (2006). A side order of stem cells: the SP phenotype. Stem Cells 24:3-12.
52. Oh H, X Chi, SB Bradfute, Y Mishina, J Pocius, LH Michael, RR Behringer, RJ Schwartz, ML Entman and MD Schneider. (2004). Cardiac muscle plasticity in adult and embryo by heart-derived progenitor cells. Ann N Y Acad Sci 1015:182-189.
53. Uchida S, P De Gaspari, S Kostin, K Jenniches, A Kilic, Y Izumiya, I Shiojima, K Grosse Kreymborg, H Renz, K Walsh and T Braun. (2013). Sca1-derived cells are a source of myocardial renewal in the murine adult heart. Stem Cell Reports 1:397-410.
54. Bailey B, J Fransioli, NA Gude, R Alvarez, X Zhan, AB Gustafsson and MA Sussman. (2012). Sca-1 knockout impairs myocardial and cardiac progenitor cell function. Circ Res 111:750-760.
55. Rosenblatt-Velin N, S Ogay, A Felley, WL Stanford and T Pedrazzini. (2012). Cardiac dysfunction and impaired compensatory response to pressure overload in mice deficient in stem cell antigen-1. FASEB J 26:229-239.
56. Zhou H, Z-Y Bian, J Zong, W Deng, L Yan, D-F Shen, H Guo, J Dai, Y Yuan et al. (2012). Stem cell antigen 1 protects against cardiac hypertrophy and fibrosis after pressure overload. Hypertension 60:802-809.
57. Matsuura K, A Honda, T Nagai, N Fukushima, K Iwanaga, M Tokunaga, T Shimizu, T Okano, H Kasanuki, N Hagi-wara and I Komuro. (2009). Transplantation of cardiac progenitor cells ameliorates cardiac dysfunction after myo-cardial infarction in mice. J Clin Invest 119:2204-2217.
58. Huang C, H Gu, Q Yu, MC Manukyan, JA Poynter and M Wang. (2011). Sca-1+ cardiac stem cells mediate acute cardioprotection via paracrine factor SDF-1 following myocardial ischemia/reperfusion. PLoS One 6:e29246.
59. Maxeiner H, N Krehbiehl, A Muller, N Woitasky, H Akinturk, M Muller, MA Weigand, Y Abdallah, S Kas-seckert et al. (2010). New insights into paracrine mechanisms of human cardiac progenitor cells. Eur J Heart Fail 12:730-737.
60. Ryzhov S, AE Goldstein, SV Novitskiy, MR Blackburn, I Biaggioni and I Feoktistov. (2012). Role of A2B adenosine receptors in regulation of paracrine functions of stem cell antigen 1-positive cardiac stromal cells. J Pharmacol Exp Ther 341:764-774.
61. Gnecchi M, Z Zhang, A Ni and VJ Dzau. (2008). Para-crine mechanisms in adult stem cell signaling and therapy. Circ Res 103:1204-1219.
62. Burchfield JS and S Dimmeler. (2008). Role of paracrine factors in stem and progenitor cell mediated cardiac repair and tissue fibrosis. Fibrogenesis Tissue Repair 1:4.
63. Nascimento DS, D Mosqueira, LM Sousa, M Teixeira, M Filipe, TP Resende, AF Araujo, M Valente, J Almeida et al. (2014). Human umbilical cord tissue-derived mes-enchymal stromal cells attenuate remodeling following myocardial infarction by pro-angiogenic, anti-apoptotic and endogenous cell activation mechanisms. Stem Cell Res Ther 5:5.
64. Bax NA, MH van Marion, B Shah, MJ Goumans, CV Bouten and DW van der Schaft. (2012). Matrix production and remodeling capacity of cardiomyocyte progenitor cells during in vitro differentiation. J Mol Cell Cardiol 53:497-508.
65. Thannickal VJ, DY Lee, ES White, Z Cui, JM Larios, R Chacon, JC Horowitz, RM Day and PE Thomas. (2003). Myofibroblast differentiation by transforming growth factor-beta1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase. J Biol Chem 278: 12384-12389.
66. Forte G, F Carotenuto, F Pagliari, S Pagliari, P Cossa, R Fiaccavento, A Ahluwalia, G Vozzi, B Vinci et al. (2008). Criticality of the biological and physical stimuli array inducing resident cardiac stem cell determination. Stem Cells 26:2093-2103.
67. Mosqueira D, S Pagliari, K Uto, M Ebara, S Romanazzo, C Escobedo-Lucea, J Nakanishi, A Taniguchi, O Franzese et al. (2014). Hippo pathway effectors control cardiac progenitor cell fate by acting as dynamic sensors of substrate mechanics and nanostructure. ACS Nano 8:2033-2047.
68. Navaratnam V, MH Kaufman, JN Skepper, S Barton and KM Guttridge. (1986). Differentiation of the myocardial rudiment of mouse embryos: an ultrastructural study including freeze-fracture replication. J Anat 146:65-85.
69. Moretti A, L Caron, A Nakano, JT Lam, A Bernshausen, Y Chen, Y Qyang, L Bu, M Sasaki et al. (2006). Multi-potent embryonic Isl1 + progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 127:1151-1165.
70. Kattman SJ, ED Adler and GM Keller. (2007). Specification of multipotential cardiovascular progenitor cells during embryonic stem cell differentiation and embryonic development. Trends Cardiovasc Med 17:240-246.
71. Prall OW, MK Menon, MJ Solloway, Y Watanabe, S Zaffran, F Bajolle, C Biben, JJ McBride, BR Robertson et al. (2007). An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell 128:947-959.
72. Sassoon DA, I Garner and M Buckingham. (1988). Transcripts of alpha-cardiac and alpha-skeletal actins are early markers for myogenesis in the mouse embryo. Development 104:155-164.
73. Nishii K and Y Shibata. (2006). Mode and determination of the initial contraction stage in the mouse embryo heart. Anat Embryol (Berl) 211:95-100.
74. Lints TJ, LM Parsons, L Hartley, I Lyons and RP Harvey. (1993). Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development 119:419-431.
75. Kubalak SW, WC Miller-Hance, TX O'Brien, E Dyson and KR Chien. (1994). Chamber specification of atrial myosin light chain-2 expression precedes septation during murine cardiogenesis. J Biol Chem 269:16961-16970.
76. Bu L, X Jiang, S Martin-Puig, L Caron, S Zhu, Y Shao, DJ Roberts, PL Huang, IJ Domian and KR Chien. (2009). Human ISL1 heart progenitors generate diverse multi-potent cardiovascular cell lineages. Nature 460:113-117.
77. Cai CL, X Liang, Y Shi, PH Chu, SL Pfaff, J Chen and S Evans. (2003). Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell 5:877-889.
78. Kelly RG, NA Brown and ME Buckingham. (2001). The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev Cell 1:435-440.
79. de Boer BA, G van den Berg, PA de Boer, AF Moorman and JM Ruijter. (2012). Growth of the developing mouse heart: an interactive qualitative and quantitative 3D atlas. Dev Biol 368:203-213.
80. Sedmera D, M Reckova, A DeAlmeida, SR Coppen, SW Kubalak, RG Gourdie and RP Thompson. (2003). Spa-tiotemporal pattern of commitment to slowed proliferation in the embryonic mouse heart indicates progressive differentiation of the cardiac conduction system. Anat Rec A Discov Mol Cell Evol Biol 274:773-777.
81. Moorman A, S Webb, NA Brown, W Lamers and RH Anderson. (2003). Development of the heart: (1) formation of the cardiac chambers and arterial trunks. Heart 89: 806-814.
82. Wu SM, Y Fujiwara, SM Cibulsky, DE Clapham, C-L Lien, TM Schultheiss and SH Orkin. (2006). Developmental origin of a bipotential myocardial and smooth muscle cell precursor in the mammalian heart. Cell 127: 1137-1150.
83. Bersell K, S Arab, B Haring and B Kuhn. (2009). Neur-egulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury. Cell 138:257-270.
84. Manasek FJ. (1969). Embryonic development of the heart. II. Formation of the epicardium. J Embryol Exp Morphol 22:333-348.
85. Vincent SD and ME Buckingham. (2010). How to make a heart: the origin and regulation of cardiac progenitor cells. Curr Top Dev Biol 90:1-41.
86. Dettman RW, W Denetclaw, Jr., CP Ordahl and J Bristow. (1998). Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and inter-myocardial fibroblasts in the avian heart. Dev Biol 193: 169-181.
87. Rosenthal N and RP Harvey. (2010). Heart Development and Regeneration. Elsevier, Inc., London, United Kingdom.
88. Cai CL, JC Martin, Y Sun, L Cui, L Wang, K Ouyang, L Yang, L Bu, X Liang et al. (2008). A myocardial lineage derives from Tbx18 epicardial cells. Nature 454:104-108.
89. Zhou B, Q Ma, S Rajagopal, SM Wu, I Domian, J Rivera-Feliciano, D Jiang, A von Gise, S Ikeda, KR Chien and WT Pu. (2008). Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454:109-113.
90. Ieda M, T Tsuchihashi, KN Ivey, RS Ross, TT Hong, RM Shaw and D Srivastava. (2009). Cardiac fibroblasts regulate myocardial proliferation through beta1 integrin signaling. Dev Cell 16:233-244.
91. Wu SM, KR Chien and C Mummery. (2008). Origins and fates of cardiovascular progenitor cells. Cell 132:537-543.
92. Smart N, S Bollini, KN Dube, JM Vieira, B Zhou, S Davidson, D Yellon, J Riegler, AN Price et al. (2011). De novo cardiomyocytes from within the activated adult heart after injury. Nature 474:640-644.
93. Zhou B, LB Honor, Q Ma, JH Oh, RZ Lin, JM Melero-Martin, A von Gise, P Zhou, T Hu et al. (2012). Thymosin beta 4 treatment after myocardial infarction does not re-program epicardial cells into cardiomyocytes. J Mol Cell Cardiol 52:43-47.
94. Chong JJ, H Reinecke, M Iwata, B Torok-Storb, A Stempien-Otero and CE Murry. (2013). Progenitor cells identified by PDGFR-alpha expression in the developing and diseased human heart. Stem Cells Dev 22:1932-1943.
95. Holmes C and WL Stanford. (2007). Concise review: stem cell antigen-1: expression, function, and enigma. Stem Cells 25:1339-1347.
96. Asakura A, P Seale, A Girgis-Gabardo and MA Rudnicki. (2002). Myogenic specification of side population cells in skeletal muscle. J Cell Biol 159:123-134.
97. Welm BE, SB Tepera, T Venezia, TA Graubert, JM Rosen and MA Goodell. (2002). Sca-1(pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Dev Biol 245:42-56.
98. Dekel B, L Zangi, E Shezen, S Reich-Zeliger, S Eventov-Friedman, H Katchman, J Jacob-Hirsch, N Amariglio, G Rechavi, R Margalit and Y Reisner. (2006). Isolation and characterization of nontubular sca-1 + lin-multipotent stem/progenitor cells from adult mouse kidney. J Am Soc Nephrol 17:3300-3314.
99. Clayton E and SJ Forbes. (2009). The isolation and in vitro expansion of hepatic Sca-1 progenitor cells. Bio-chem Biophys Res Commun 381:549-553.
100. Xin L, DA Lawson and ON Witte. (2005). The Sca-1 cell surface marker enriches for a prostate-regenerating cell subpopulation that can initiate prostate tumorigenesis. Proc Natl Acad Sci USA 102:6942-6947.
101. Driskell RR, BM Lichtenberger, E Hoste, K Kretzschmar, BD Simons, M Charalambous, SR Ferron, Y Herault, G Pavlovic, AC Ferguson-Smith and FM Watt. (2013). Distinct fibroblast lineages determine dermal architecture in skin development and repair. Nature 504:277-281.
102. McQualter JL, N Brouard, B Williams, BN Baird, S Sims-Lucas, K Yuen, SK Nilsson, PJ Simmons and I Berton-cello. (2009). Endogenous fibroblastic progenitor cells in the adult mouse lung are highly enriched in the Sca-1 positive cell fraction. Stem Cells 27:623-633.
103. Akamatsu T, Y Arai, I Kosugi, H Kawasaki, S Meguro, M Sakao, K Shibata, T Suda, K Chida and T Iwashita. (2013). Direct isolation of myofibroblasts and fibroblasts from bleomycin-injured lungs reveals their functional similarities and differences. Fibrogenesis Tissue Repair 6:15.
104. Ito CY, CYJ Li, A Bernstein, JE Dick and WL Stanford. (2003). Hematopoietic stem cell and progenitor defects in Sca-1/Ly-6A-null mice. Blood 101:517-523.
105. Kafadar KA, L Yi, Y Ahmad, L So, F Rossi and GK Pavlath. (2009). Sca-1 expression is required for efficient remodeling of the extracellular matrix during skeletal muscle regeneration. Dev Biol 326:47-59.
106. Lajiness JD and SJ Conway. (2013). Origin, development, and differentiation of cardiac fibroblasts. J Mol Cell Cardiol 70:2-8.
107. Chang HY, JT Chi, S Dudoit, C Bondre, M van de Rijn, D Botstein and PO Brown. (2002). Diversity, topographic differentiation, and positional memory in human fibro-blasts. Proc Natl Acad Sci USA 99:12877-12882.
108. Wang J, H Bo, X Meng, Y Wu, Y Bao and Y Li. (2006). A simple and fast experimental model of myocardial infarction in the mouse. Tex Heart Inst J 33:290-293.
109. Paylor B, J Fernandes, B McManus and F Rossi. (2013). Tissue-resident Sca1+ PDGFRalpha+ mesenchymal progenitors are the cellular source of fibrofatty infiltration in arrhythmogenic cardiomyopathy. F1000Res 2:141.