Harnessing the potential of adult cardiac stem cells: Lessons from haematopoiesis, the embryo and the niche

Journal of Cardiovascular Translational Research

Volumn 5, Issue 5, 2012, Pages 631-640

  Balmer, Gemma M ^a,b   Riley, Paul R ^c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cardiac regeneration; Cardiac stem cells; Haematopoiesis; Stem cell niche

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CHEMOKINE RECEPTOR CXCR4; FIBROBLAST GROWTH FACTOR 2; NERVE CELL ADHESION MOLECULE; NOTCH RECEPTOR; SONIC HEDGEHOG PROTEIN; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR RUNX1; VASCULOTROPIN A; BIOLOGICAL MARKER;

ADULT CARDIAC STEM CELL; ADULT CARDIAC STEM CELL TRANSPLANTATION; ADULT STEM CELL; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; FGF2 GENE; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INTERACTION; GENETIC MARKER; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; ISCHEMIC HEART DISEASE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RALDH2 GENE; SCX GENE; SEMA3D GENE; SIGNAL TRANSDUCTION; STEM CELL NICHE; STEM CELL RESEARCH; STEM CELL TRANSPLANTATION; TBX18 GENE; TISSUE REGENERATION; VEGFA GENE; WT1 GENE; ANIMAL; CELL PROLIFERATION; EMBRYONIC STEM CELL; GENOTYPE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; PHYSIOLOGY; REGENERATION; REGENERATIVE MEDICINE; REVIEW; TRANSPLANTATION;

ADULT STEM CELLS; ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOTYPE; HEMATOPOIETIC STEM CELLS; HUMANS; MYOCARDIAL ISCHEMIA; MYOCYTES, CARDIAC; PHENOTYPE; REGENERATION; REGENERATIVE MEDICINE; SIGNAL TRANSDUCTION; STEM CELL NICHE;

EID: 84874171344     PISSN: 19375387     EISSN: 19375395     Source Type: Journal    
DOI: 10.1007/s12265-012-9386-3     Document Type: Article

References (117)

1. Mimeault, M.; Hauke, R.; Batra, S. K. (2007). Stem cells: a revolution in therapeutics - recent advances in stem cell biology and their therapeutic applications in regenerative medicine and cancer therapies. Clin Pharmacol Ther, 82, 252-264.
2. Johnson, F. L.; Look, A. T.; Gockerman, J.; Ruggiero, M. R.; Dalla-Pozza, L.; Billings, F. T. (1984). Bone-marrow transplantation in a patient with sickle-cell anemia. N Engl J Med, 311, 780-783.
3. Vermylen, C.; Ninane, J.; Fernandez Robles, E.; Cornu, G. (1988). Bone marrow transplantation in five children with sickle cell anaemia. The Lancet, 331, 1427-1428.
4. Hansbury, E. N.; Schultz, W. H.; Ware, R. E.; Aygun, B. (2012). Bone marrow transplant options and preferences in a sickle cell anemia cohort on chronic transfusions. Pediatr. Blood Cancer, 58, 611-615.
5. Clifford, D. M.; Fisher, S. A.; Brunskill, S. J.; Doree, C.; Mathur, A.; Watt, S.; et al. (2012). Stem cell treatment for acute myocardial infarction. Cochrane Database Systematic Review, 2, CD006536.
6. Quaini, F.; Urbanek, K.; Beltrami, A. P.; Finato, N.; Beltrami, C. A.; Nadal-Ginard, B.; et al. (2002). Chimerism of the transplanted heart. N Engl J Med, 346, 5-15.
7. Beltrami, A. P.; Barlucchi, L.; Torella, D.; Baker, M.; Limana, F.; Chimenti, S.; et al. (2003). Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell, 114, 763-776.
8. Oh, H.; Bradfute, S. B.; Gallardo, T. D.; Nakamura, T.; Gaussin, V.; Mishina, Y.; et al. (2003). Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proceedings of the National Academy of Sciences, 100, 12313-12318.
9. Matsuura, K.; Nagai, T.; Nishigaki, N.; Oyama, T.; Nishi, J.; Wada, H.; et al. (2004). Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. Journal of Biological Chemistry, 279, 11384-11391.
10. Martin, C. M.; Meeson, A. P.; Robertson, S. M.; Hawke, T. J.; Richardson, J. A.; Bates, S.; et al. (2004). Persistent expression of the ATP-binding cassette transporter, Abcg2, identifies cardiac SP cells in the developing and adult heart. Developmental Biology, 265, 262-275.
11. Pfister, O.; Mouquet, F.; Jain, M.; Summer, R.; Helmes, M.; Fine, A.; et al. (2005). CD31- but not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation. Circulation Research, 97, 52-61.
12. Messina, E.; De Angelis, L.; Frati, G.; Morrone, S.; Chimenti, S.; Fiordaliso, F.; et al. (2004). Isolation and expansion of adult cardiac stem cells from human and murine heart. Circulation Research, 95, 911-921.
13. Bergmann, O.; Bhardwaj, R. D.; Bernard, S.; Zdunek, S.; Barnabé-Heider, F.; Walsh, S.; et al. (2009). Evidence for cardiomyocyte renewal in humans. Science, 324, 98-102.
14. Smart, N.; Risebro, C. A.; Melville, A. A.; Moses, K.; Schwartz, R. J.; Chien, K. R.; et al. (2007). Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization. Nature, 445, 177-182.
15. Zhou, B.; Ma, Q.; Rajagopal, S.; Wu, S. M.; Domian, I.; Rivera-Feliciano, J.; et al. (2008). Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature, 454, 109-113.
16. Smart, N.; Bollini, S.; Dube, K. N.; Vieira, J. M.; Zhou, B.; Davidson, S.; et al. (2011). De novo cardiomyocytes from within the activated adult heart after injury. Nature, 474, 640-644.
17. Lepilina, A.; Coon, A. N.; Kikuchi, K.; Holdway, J. E.; Roberts, R. W.; Burns, C. G.; et al. (2006). A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell, 127, 607-619.
18. Zhou, B.; Honor, L. B.; He, H.; Ma, Q.; Oh, J. H.; Butterfield, C.; et al. (2011). Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J. Clin. Invest, 121, 1894-1904.
19. Spradling, A.; Drummond-Barbosa, D.; Kai, T. (2001). Stem cells find their niche. Nature, 414, 98-104.
20. Scadden, D. T. (2006). The stem-cell niche as an entity of action. Nature, 441, 1075-1079.
21. Schofield, R. (1978). The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells, 4, 7-25.
22. Lander, A. D.; Kimble, J.; Clevers, H.; Fuchs, E.; Montarras, D.; Buckingham, M.; et al. (2012). What does the concept of the stem cell niche really mean today? BMC Biol, 10, 19.
23. Jones, D. L.; Wagers, A. J. (2008). No place like home: anatomy and function of the stem cell niche. Nat. Rev. Mol. Cell Biol.; 9, 11-21.
24. Ohta, M.; Sakai, T.; Saga, Y.; Aizawa, S.; Saito, M. (1998). Suppression of hematopoietic activity in tenascin-C-deficient mice. Blood, 91, 4074-4083.
25. Tsai, S.; Patel, V.; Beaumont, E.; Lodish, H. F.; Nathan, D. G.; Sieff, C. A. (1987). Differential binding of erythroid and myeloid progenitors to fibroblasts and fibronectin. Blood, 69, 1587-1594.
26. Weinstein, R.; Riordan, M. A.; Wenc, K.; Kreczko, S.; Zhou, M.; Dainiak, N. (1989). Dual role of fibronectin in hematopoietic differentiation. Blood, 73, 111-116.
27. St-Jacques, B.; Dassule, H. R.; Karavanova, I.; Botchkarev, V. A.; Li, J.; Danielian, P. S.; et al. (1998). Sonic hedgehog signaling is essential for hair development. Current Biology, 8, 1058-1069.
28. Levy, V.; Lindon, C.; Harfe, B. D.; Morgan, B. A. (2005). Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Dev Cell, 9, 855-861.
29. Madison, B. B.; Braunstein, K.; Kuizon, E.; Portman, K.; Qiao, X. T.; Gumucio, D. L. (2005). Epithelial hedgehog signals pattern the intestinal crypt-villus axis. Development, 132, 279-289.
30. Durand, C.; Dzierzak, E. (2005). Embryonic beginnings of adult hematopoietic stem cells. Haematologica, 90, 100-108.
31. Gratwohl, A.; Niederwieser, D. (2012). History of hematopoietic stem cell transplantation: evolution and perspectives. Curr. Probl. Dermatol.; 43, 81-90.
32. Costa, G.; Kouskoff, V.; Lacaud, G. (2012). Origin of blood cells and HSC production in the embryo. Trends in Immunology, 33, 215-223.
33. Kyba, M.; Perlingeiro, R. C. R.; Daley, G. Q. (2002). HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell, 109, 29-37.
34. Matsumoto, K.; Isagawa, T.; Nishimura, T.; Ogaeri, T.; Eto, K.; Miyazaki, S.; et al. (2009). Stepwise development of hematopoietic stem cells from embryonic stem cells. PLoS One, 4, e4820.
35. Wang, Y.; Yates, F.; Naveiras, O.; Ernst, P.; Daley, G. Q. (2005). Embryonic stem cell-derived hematopoietic stem cells. Proceedings of the National Academy of Sciences of the United States of America, 102, 19081-19086.
36. Ledran, M. H.; Krassowska, A.; Armstrong, L.; Dimmick, I.; Renström, J.; Lang, R.; et al. (2008). Efficient hematopoietic differentiation of human embryonic stem cells on stromal cells derived from hematopoietic niches. Cell Stem Cell, 3, 85-98.
37. PF, Dieterlen-Lievre. (1975). On the origin of haemopoietic stem cells in the avian embryo: an experimental approach. Journal of Embryology and Experimental Morphology, 33, 607-619.
38. Turpen, J. B.; Knudson, C. M.; Hoefen, P. S. (1981). The early ontogeny of hematopoietic cells studied by grafting cytogenetically labeled tissue anlagen: localization of a prospective stem cell compartment. Developmental Biology, 85, 99-112.
39. Ciau-Uitz, A.; Walmsley, M.; Patient, R. (2000). Distinct origins of adult and embryonic blood in Xenopus. Cell, 102, 787-796.
40. Winnier, G.; Blessing, M.; Labosky, P. A.; Hogan, B. L. (1995). Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev.; 9, 2105-2116.
41. Kumano, K.; Chiba, S.; Kunisato, A.; Sata, M.; Saito, T.; Nakagami-Yamaguchi, E.; et al. (2003). Notch1 but not notch2 is essential for generating hematopoietic stem cells from endothelial cells. Immunity, 18, 699-711.
42. Dyer, M. A.; Farrington, S. M.; Mohn, D.; Munday, J. R.; Baron, M. H. (2001). Indian hedgehog activates hematopoiesis and vasculogenesis and can respecify prospective neurectodermal cell fate in the mouse embryo. Development, 128, 1717-1730.
43. Speck, N. A.; Gilliland, D. G. (2002). Core-binding factors in haematopoiesis and leukaemia. Nat Rev Cancer, 2, 502-513.
44. Yokomizo, T.; Ogawa, M.; Osato, M.; Kanno, T.; Yoshida, H.; Fujimoto, T.; et al. (2001). Requirement of Runx1/AML1/PEBP2+B for the generation of haematopoietic cells from endothelial cells. Genes to Cells, 6, 13-23.
45. Chen, M. J.; Yokomizo, T.; Zeigler, B. M.; Dzierzak, E.; Speck, N. A. (2009). Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature, 457, 887-891.
46. Calvi, L. M.; Adams, G. B.; Weibrecht, K. W.; Weber, J. M.; Olson, D. P.; Knight, M. C.; et al. (2003). Osteoblastic cells regulate the haematopoietic stem cell niche. Nature, 425, 841-846.
47. Zhang, J.; Niu, C.; Ye, L.; Huang, H.; He, X.; Tong, W. G.; et al. (2003). Identification of the haematopoietic stem cell niche and control of the niche size. Nature, 425, 836-841.
48. Visnjic, D.; Kalajzic, I.; Gronowicz, G.; Aguila, H. L.; Clark, S. H.; Lichtler, A. C.; et al. (2001). Conditional ablation of the osteoblast lineage in Col2.3+ötk transgenic mice. J Bone Miner Res, 16, 2222-2231.
49. Kiel, M. J.; Yilmaz, O. H.; Iwashita, T.; Yilmaz, O. H.; Terhorst, C.; Morrison, S. J. (2005). SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell, 121, 1109-1121.
50. Liu, F.; Poursine-Laurent, J.; Link, D. C. (2000). Expression of the G-CSF receptor on hematopoietic progenitor cells is not required for their mobilization by G-CSF. Blood, 95, 3025-3031.
51. Nagasawa, T.; Hirota, S.; Tachibana, K.; Takakura, N.; Nishikawa, Si, Kitamura, Y.; et al. (1996). Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature, 382, 635-638.
52. Ma, Q.; Jones, D.; Springer, T. A. (1999). The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity, 10, 463-471.
53. Semerad, C. L.; Christopher, M. J.; Liu, F.; Short, B.; Simmons, P. J.; Winkler, I.; et al. (2005). G-CSF potently inhibits osteoblast activity and CXCL12 mRNA expression in the bone marrow. Blood, 106, 3020-3027.
54. Greenbaum, A. M.; Link, D. C. (2011). Mechanisms of G-CSF-mediated hematopoietic stem and progenitor mobilization. Leukemia, 25, 211-217.
55. Orlic, D.; Kajstura, J.; Chimenti, S.; Jakoniuk, I.; Anderson, S. M.; Li, B.; et al. (2001). Bone marrow cells regenerate infarcted myocardium. Nature, 410, 701-705.
56. Murry, C. E.; Soonpaa, M. H.; Reinecke, H.; Nakajima, H.; Nakajima, H. O.; Rubart, M.; et al. (2004). Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature, 428, 664-668.
57. Usas, A.; Maciulaitis, J.; Maciulaitis, R.; Jakuboniene, N.; Milasius, A.; Huard, J. (2011). Skeletal muscle-derived stem cells: implications for cell-mediated therapies. Medicina (Kaunas.), 47, 469-479.
58. Toma, C.; Pittenger, M. F.; Cahill, K. S.; Byrne, B. J.; Kessler, P. D. (2002). Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation, 105, 93-98.
59. Uemura, R.; Xu, M.; Ahmad, N.; Ashraf, M. (2006). Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling. Circulation Research, 98, 1414-1421.
60. Bolli, R.; Chugh, A. R.; D'Amario, D.; Loughran, J. H.; Stoddard, M. F.; Ikram, S.; et al. (1926). Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. The Lancet, 378, 1847-1857.
61. Makkar, R. R.; Smith, R. R.; Cheng, K.; Malliaras, K.; Thomson, L. E.; Berman, D.; et al. (2010). Intracoronary cardiosphere-derived cells for heart regeneration after myocardial infarction (CADUCEUS): a prospective, randomised phase 1 trial. The Lancet, 379, 895-904.
62. Bollini, S.; Smart, N.; Riley, P. R. (2011). Resident cardiac progenitor cells: at the heart of regeneration. Journal of Molecular and Cellular Cardiology, 50, 296-303.
63. Viragh, S.; Challice, C. E. (1981). The origin of the epicardium and the embryonic myocardial circulation in the mouse. Anat. Rec.; 201, 157-168.
64. Tomanek, R. J. (2005). Formation of the coronary vasculature during development. Angiogenesis.; 8, 273-284.
65. Chen, T. H.; Chang, T. C.; Kang, J. O.; Choudhary, B.; Makita, T.; Tran, C. M.; et al. (2002). Epicardial induction of fetal cardiomyocyte proliferation via a retinoic acid-inducible trophic factor. Dev. Biol.; 250, 198-207.
66. Katz, T.; Singh, M.; Degenhardt, K.; Rivera-Feliciano, J.; Johnson, R.; Epstein, J.; et al. (2012). Distinct compartments of the proepicardial organ give rise to coronary vascular endothelial cells. Dev Cell, 22, 639-650.
67. Limana, F.; Bertolami, C.; Mangoni, A.; Di, C. A.; Avitabile, D.; Mocini, D.; et al. (2010). Myocardial infarction induces embryonic reprogramming of epicardial c-kit(+) cells: role of the pericardial fluid. J. Mol. Cell Cardiol.; 48, 609-618.
68. Smart, N.; Bollini, S.; Dube, K. N.; Vieira, J. M.; Zhou, B.; Davidson, S.; et al. (2011b). De novo cardiomyocytes from within the activated adult heart after injury. Nature. advance online publication.
69. Cai, C. L.; Martin, J. C.; Sun, Y.; Cui, L.; Wang, L.; Ouyang, K.; et al. (2008). A myocardial lineage derives from Tbx18 epicardial cells. Nature, 454, 104-108.
70. Red-Horse, K.; Ueno, H.; Weissman, I. L.; Krasnow, M. A. (2010). Coronary arteries form by developmental reprogramming of venous cells. Nature, 464, 549-553.
71. Katz, T. C, Singh, M. K, Degenhardt, K.; Rivera-Feliciano, J.; Johnson, R. L.; Epstein, J. A.; et al. Distinct Compartments of the Proepicardial Organ Give Rise to Coronary Vascular Endothelial Cells. Developmental Cell, 22(3), 639-650. 13-3-2012b.
72. Christoffels, V. M.; Grieskamp, T.; Norden, J.; Mommersteeg, M. T. M.; Rudat, C.; Kispert, A. (2009). Tbx18 and the fate of epicardial progenitors. Nature, 458, E8-E9.
73. Riley, P. R.; Smart, N. (2011). Vascularizing the heart. Cardiovascular Research, 91, 260-268.
74. Zhou, B.; Honor, L. B.; Ma, Q.; Oh, J. H.; Lin, R. Z.; Melero-Martin, J. M.; et al. (2012). Thymosin beta 4 treatment after myocardial infarction does not reprogram epicardial cells into cardiomyocytes. Journal of Molecular and Cellular Cardiology, 52, 43-47.
75. Hannappel, E.; Wartenberg, F. (1993). Actin-sequestering ability of thymosin beta 4, thymosin beta 4 fragments, and thymosin beta 4-like peptides as assessed by the DNase I inhibition assay. Biol Chem. Hoppe Seyler, 374, 117-122.
76. Duan, J.; Gherghe, C.; Liu, D.; Hamlett, E.; Srikantha, L.; Rodgers, L.; et al. (2012). Wnt1/[beta]catenin injury response activates the epicardium and cardiac fibroblasts to promote cardiac repair. EMBO J, 31, 429-442.
77. Jopling, C.; Sleep, E.; Raya, M.; Marti, M.; Raya, A.; Belmonte, J. C. I. (2010). Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature, 464, 606-609.
78. Kikuchi, K.; Holdway, J. E.; Werdich, A. A.; Anderson, R. M.; Fang, Y.; Egnaczyk, G. F.; et al. (2010). Primary contribution to zebrafish heart regeneration by gata4+ cardiomyocytes. Nature, 464, 601-605.
79. Laugwitz, K. L.; Moretti, A.; Caron, L.; Nakano, A.; Chien, K. R. (2008). Islet1 cardiovascular progenitors: a single source for heart lineages? Development, 135, 193-205.
80. Tomita, Y.; Matsumura, K.; Wakamatsu, Y.; Matsuzaki, Y.; Shibuya, I.; Kawaguchi, H.; et al. (2005). Cardiac neural crest cells contribute to the dormant multipotent stem cell in the mammalian heart. The Journal of Cell Biology, 170, 1135-1146.
81. Takashima, Y.; Era, T.; Nakao, K.; Kondo, S.; Kasuga, M.; Smith, A. G.; et al. (2007). Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell, 129, 1377-1388.
82. Mouquet, Fdr, Pfister, O.; Jain, M.; Oikonomopoulos, A.; Ngoy, S.; Summer, R.; et al. (2005). Restoration of cardiac progenitor cells after myocardial infarction by self-proliferation and selective homing of bone marrow-derived stem cells. Circulation Research, 97, 1090-1092.
83. Laugwitz, K. L.; Moretti, A.; Lam, J.; Gruber, P.; Chen, Y.; Woodard, S.; et al. (2005). Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature, 433, 647-653.
84. Chong, J.; Chandrakanthan, V.; Xaymardan, M.; Asli, N.; Li, J.; Ahmed, I.; et al. (2011). Adult cardiac-resident MSC-like stem cells with a proepicardial origin. Cell Stem Cell, 9, 527-540.
85. Wilm, B.; Ipenberg, A.; Hastie, N. D.; Burch, J. B. E.; Bader, D. M. (2005). The serosal mesothelium is a major source of smooth muscle cells of the gut vasculature. Development, 132, 5317-5328.
86. Dettman, R. W.; Denetclaw, J.; Ordahl, C. P.; Bristow, J. (1998). Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart. Developmental Biology, 193, 169-181.
87. Urbanek, K.; Cesselli, D.; Rota, M.; Nascimbene, A.; De Angelis, A.; Hosoda, T.; et al. (2006). Stem cell niches in the adult mouse heart. Proc. Natl. Acad. Sci. U. S. A.; 103, 9226-9231.
88. Tumbar, T.; Guasch, G.; Greco, V.; Blanpain, C.; Lowry, W. E.; Rendl, M.; et al. (2004). Defining the epithelial stem cell niche in skin. Science, 303, 359-363.
89. Sato, T.; van Es, J. H.; Snippert, H. J.; Stange, D. E.; Vries, R. G.; van den Born, M.; et al. (2011). Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature, 469, 415-418.
90. Collins, C. A.; Olsen, I.; Zammit, P. S.; Heslop, L.; Petrie, A.; Partridge, T. A.; et al. (2005). Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell, 122, 289-301.
91. Kuang, S.; Rudnicki, M. A. (2008). The emerging biology of satellite cells and their therapeutic potential. Trends in Molecular Medicine, 14, 82-91.
92. Mauro, A. (1961). Satellite cell of skeletal muscle fibers. The Journal of Biophysical and Biochemical Cytology, 9, 493-495.
93. Hsu, Y. C.; Pasolli, H. A.; Fuchs, E. (2011). Dynamics between stem cells, niche, and progeny in the hair follicle. Cell, 144, 92-105.
94. Hsieh, P. C. H.; Segers, V. F. M.; Davis, M. E.; MacGillivray, C.; Gannon, J.; Molkentin, J. D.; et al. (2007). Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med, 13, 970-974.
95. Rudnicki, M. A.; Le Grand, F.; McKinnell, I.; Kuang, S. (2008). The molecular regulation of muscle stem cell function. Cold Spring Harbor Symposia on Quantitative Biology.
96. Sanes, J. R. (2003). The basement membrane/basal lamina of skeletal muscle. Journal of Biological Chemistry, 278, 12601-12604.
97. Burkin, D. J.; Kaufman, S. J. (1999). The α7β1 integrin in muscle development and disease. Cell and Tissue Research, 296, 183-190.
98. DiMario, J.; Buffinger, N.; Yamada, S.; Strohman, R. C. (1989). Fibroblast growth factor in the extracellular matrix of dystrophic (mdx) mouse muscle. Science, 244, 688-690.
99. Tatsumi, R.; Anderson, J. E.; Nevoret, C. J.; Halevy, O.; Allen, R. E. (1998). HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Developmental Biology, 194, 114-128.
100. Brack, A. S.; Conboy, I. M.; Conboy, M. J.; Shen, J.; Rando, T. A. (2008). A temporal switch from notch to wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell, 2, 50-59.
101. Cosgrove, B. D.; Sacco, A.; Gilbert, P. M.; Blau, H. M. (2009). A home away from home: challenges and opportunities in engineering in vitro muscle satellite cell niches. Differentiation, 78, 185-194.
102. Ratajczak, M. Z.; Majka, M.; Kucia, M.; Drukala, J.; Pietrzkowski, Z.; Peiper, S.; et al. (2003). Expression of functional CXCR4 by muscle satellite cells and secretion of SDF-1 by muscle-derived fibroblasts is associated with the presence of both muscle progenitors in bone marrow and hematopoietic stem/progenitor cells in muscles. STEM CELLS, 21, 363-371.
103. Sherwood, R. I.; Christensen, J. L.; Conboy, I. M.; Conboy, M. J.; Rando, T. A.; Weissman, I. L.; et al. (2004). Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle. Cell, 119, 543-554.
104. Riquelme, P. A.; Drapeau, E.; Doetsch, F. (2008). Brain micro-ecologies: neural stem cell niches in the adult mammalian brain. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 123-137.
105. Miller, F. D.; Gauthier-Fisher, Ae. (2009). Home at last: neural stem cell niches defined. Cell Stem Cell, 4, 507-510.
106. Mirzadeh, Z.; Merkle, F. T.; Soriano-Navarro, M.; Garcia-Verdugo, J. M.; Alvarez-Buylla, A. (2008). Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell, 3, 265-278.
107. Tavazoie, M.; Van der Veken, L.; Silva-Vargas, V.; Louissaint, M.; Colonna, L.; Zaidi, B.; et al. (2008). A specialized vascular niche for adult neural stem cells. Cell Stem Cell, 3, 279-288.
108. Kazanis, I.; ffrench-Constant, C. (2011). Extracellular matrix and the neural stem cell niche. Devel Neurobio, 71, 1006-1017.
109. Lathia, J. D.; Patton, B.; Eckley, D. M.; Magnus, T.; Mughal, M. R.; Sasaki, T.; et al. (2007). Patterns of laminins and integrins in the embryonic ventricular zone of the CNS. J. Comp. Neurol.; 505, 630-643.
110. Kazanis, I.; Lathia, J. D.; Vadakkan, T. J.; Raborn, E.; Wan, R.; Mughal, M. R.; et al. (2010). Quiescence and activation of stem and precursor cell populations in the subependymal zone of the mammalian brain are associated with distinct cellular and extracellular matrix signals. The Journal of Neuroscience, 30, 9771-9781.
111. Loulier, K.; Lathia, J. D.; Marthiens, V.; Relucio, J.; Mughal, M. R.; Tang, S. C.; et al. (2009). β1 integrin maintains integrity of the embryonic neocortical stem cell niche. PLoS Biol, 7, e1000176.
112. Li, L.; Xie, T. (2005). Stem cell niche: structure and function. Annu. Rev. Cell Dev. Biol.; 21, 605-631.
113. Zahn, J.; Doormann, P.; Dorn, A.; Dorn, D. C. (2007). Apoptosis of male germ-line stem cells after laser ablation of their niche. Stem Cell Research, 1, 75-85.
114. Blanpain, C.+.; Fuchs, E. (2006). Epidermal stem cells of the skin. Annual Review of Cell and Developmental Biology, 22, 339-373.
115. Dellatore, S. M.; Garcia, A. S.; Miller, W. M. (2008). Mimicking stem cell niches to increase stem cell expansion. Current Opinion in Biotechnology, 19, 534-540.
116. Cheema, F. H.; Polvani, G.; Caglar, M. A.; Pesce, M. (2012). Combining stem cells and tissue engineering in cardiovascular repair - a step forward to derivation of novel implants with enhanced function and self-renewal characteristics. Recent Patents on Cardiovascular Drug Discovery.
117. Jawad, H.; Lyon, A. R.; Harding, S. E.; Ali, N. N.; Boccaccini, A. R. (2008). Myocardial tissue engineering. British Medical Bulletin, 87, 31-47.