Placenta as a reservoir of stem cells: An underutilized resource?

British Medical Bulletin

Volumn 105, Issue 1, 2013, Pages 43-67

  Pipino, Caterina ^a   Shangaris, Panicos ^a,b   Resca, Elisa ^a,f   Zia, Silvia ^c   Deprest, Jan ^c   Sebire, Neil J ^d   David, Anna L ^b   Guillot, Pascale V ^e   De Coppi, Paolo ^a,d  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^d GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

amniotic epithelial cells; haematopoietic stem cells; mesenchymal stem cells; placenta

Indexed keywords

ARTICLE; CELL PROLIFERATION; EPITHELIUM CELL; HEMATOPOIETIC STEM CELL; HUMAN; INFLAMMATION; MESENCHYMAL STEM CELL; PLACENTA; PLASTICITY; PRIORITY JOURNAL; SAFETY; STEM CELL; AMNION; CELL DIFFERENTIATION; CELL POPULATION; CELL SUBPOPULATION; CELLULAR IMMUNITY; CEREBROVASCULAR ACCIDENT; CHORION; DIABETES MELLITUS; EMBRYONIC STEM CELL; ENTEROPATHY; EPITHELIUM; EXPERIMENTAL MODEL; FETUS MEMBRANE; IMMUNOMODULATION; IN VIVO STUDY; LUNG; MEDICAL ETHICS; MUSCLE; NONHUMAN; PLURIPOTENT STEM CELL; PREGNANCY; PROTEIN EXPRESSION; RESERVOIR; TISSUE ENGINEERING; VASCULAR DISEASE;

ADULT; ANIMALS; CELL DIFFERENTIATION; EPITHELIAL CELLS; FEMALE; HEALTH RESOURCES; HUMANS; MESENCHYMAL STROMAL CELLS; MICE; PLACENTA; PLURIPOTENT STEM CELLS; PREGNANCY; RATS; STEM CELLS;

PROTEIN; STAGE SPECIFIC EMBRYO ANTIGEN 3; TRA 1 60 PROTEIN; TRA 1 81 PROTEIN; UNCLASSIFIED DRUG;

EID: 84876242777     PISSN: 00071420     EISSN: 14718391     Source Type: Journal    
DOI: 10.1093/bmb/lds033     Document Type: Article

References (141)

1. Rossant J, Cross JC. Placental development: lessons from mouse mutants. Nat Rev Genet 2001;2:538-48.
2. Regnault TRH, Galan HL, Parker TA et al. Placental development in normal and compromised pregnancies - a review. Placenta 2002;23(Suppl A):S119-29.
3. Gude NM, Roberts CT, Kalionis B et al. Growth and function of the normal human placenta. Thrombosis Res 2004;114:397-407.
4. Maltepe E, Bakardjiev AI, Fisher SJ. Review series the placenta: transcriptional, epigenetic, and physiological integration during development. Comp Gen Pharmacol 2010; 120:1016-25.
5. Sood R, Zehnder JL, Druzin ML et al. Gene expression patterns in human placenta. Proc Natl Acad Sci USA 2006;103:5478-83.
6. Sadler TW. Langman's medical embryology. In: Sun B (ed). Langman's Medical Embryology. 9th edn. Philadelphia, PA, USA: Lippincott Williams & Wilkins, 2009,385.
7. Parolini O, Soncini M. Human placenta: a source of progenitor/Stem Cells? J Reprod Med Endocrinol 2006;3:117-26.
8. Pera MF, Reubinoff B, Trounson A. Human embryonic stem cells. J Cell Sci 2000;113(Pt 1):5-10.
9. Abdulrazzak H, Moschidou D, Jones G et al. Biological characteristics of stem cells from foetal, cord blood and extraembryonic tissues. J R Soc Interface 2010;7(Suppl 6): S689-706.
10. Castellucci M, Kosanke G, Verdenelli F et al. Villous sprouting: fundamental mechanisms of human placental development. Hum Reprod Update 2000;6:485-94.
11. Cross J. Genes, development and evolution of the placenta. Placenta 2003;24:123-30.
12. Ilancheran S, Moodley Y, Manuelpillai U. Human fetal membranes: a source of stem cells for tissue regeneration and repair? Placenta 2009;30:2-10.
13. Johnson KL, Bianchi DW. Fetal cells in maternal tissue following pregnancy: what are the consequences? Hum Reprod Update 2004;10:497-502.
14. Bianchi DW, Zickwolf GK, Weil GJ et al. Male fetal progenitor cells persist in maternal blood for as long as 27 years postpartum. Proc Natl Acad Sci USA 1996;93:705-8.
15. Bou-Gharios G, Amin F, Hill P et al. Microchimeric fetal cells are recruited to maternal kidney following injury and activate collagen type I transcription. Cells Tissues Organs 2011;193:379-92.
16. Bianchi DW. Fetal cells in the mother: from genetic diagnosis to diseases associated with fetal cell microchimerism. Euro J Obstet Gynecol Reprod Biol 2000;92:103-8.
17. Khosrotehrani K, Johnson KL, Lau J et al. The influence of fetal loss on the presence of fetal cell microchimerism: a systematic review. Arthritis Rheum 2003;48:3237-41.
18. Parolini O, Alviano F, Bagnara GP et al. Concise review: isolation and characterization of cells from human term placenta: outcome of the first international Workshop on Placenta Derived Stem Cells. Stem Cells 2008;26:300-11.
19. Yen BL, Huang H-I, Chien C-C et al. Isolation of multipotent cells from human term placenta. Stem Cells 2005;3-9.
20. Tsagias N, Koliakos I, Lappa M et al. Placenta perfusion has hematopoietic and mesenchymal progenitor stem cell potential. Transfusion 2011;51:976-85.
21. Shin D-M, Liu R, Klich I et al. Molecular signature of adult bone marrow-purified very small embryonic-like stem cells supports their developmental epiblast/germ line origin. Leukemia 2010;24:1450-61.
22. Miki T, Strom SC. Amnion-derived pluripotent/multipotent stem cells. Stem Cell Rev 2006;2:133-42.
23. Delo DM, De Coppi P, Bartsch G et al. Amniotic fluid and placental stem cells. Methods Enzymol 2006;419:426-38.
24. Fukuchi Y, Nakajima H, Sugiyama D et al. Human placental derived cells have mesenchymal stem/progenitor cell potential. Cells 2004;649-58.
25. Bá rcena A, Muench MO, Kapidzic M et al. A new role for the human placenta as a hematopoietic site throughout gestation. Reprod Sci 2009;16:178-87.
26. Miki T, Lehmann T, Cai H et al. Stem cell characteristics of amniotic epithelial cells. Stem Cells 2005;23:1549-59.
27. Parry S, Strauss JF. Premature rupture of the fetal membranes. N Engl J Med 1998; 338:663-70.
28. Wolbank S, van Griensven M, Grillari-Voglauer R et al. Alternative sources of adult stem cells: human amniotic membrane. Adv Biochem Eng Biotechnol 2010;123:1-27.
29. Miyamoto K, Hayashi K, Suzuki T et al. Human placenta feeder layers support undifferentiated growth of primate embryonic stem cells. Stem Cells 2004;22:433-40.
30. Uchida S, Inanaga Y, Kobayashi M et al. Neurotrophic function of conditioned medium from human amniotic epithelial cells. J Neurosci Res 2000;62:585-90.
31. Koyano S, Fukui A, Uchida S et al. Synthesis and release of activin and noggin by cultured human amniotic epithelial cells. Dev Growth Differ 2002;44:103-12.
32. Ilancheran S, Michalska A, Peh G et al. Stem cells derived from human fetal membranes display multilineage differentiation potential. Biol Reprod 2007;77:577-88.
33. Murphy S, Rosli S, Acharya R et al. Amnion epithelial cell isolation and characterization for clinical use. Curr Protoc Stem Cell Biol 2010;13:1E.6.1-6.
34. Miki T, Marongiu F, Dorko K et al. Isolation of amniotic epithelial stem cells. Curr Protoc Stem Cell Biol 2010;12:1E.3.1-3.
35. Pratama G, Vaghjiani V, Tee JY et al. Changes in culture expanded human amniotic epithelial cells: implications for potential therapeutic applications. PLoS One 2011;6:e26136.
36. Dua H, Gomes J, King A et al. The amniotic membrane in ophthalmology1. Surv Ophthalmol 2004;49:51-77.
37. Ishino Y, Sano Y, Nakamura T et al. Amniotic membrane as a carrier for cultivated human corneal endothelial cell transplantation. Invest Ophthalmol Vis Sci 2004;45:800-6.
38. Mi S, David AL, Chowdhury B et al. Tissue engineering a fetal membrane. Tissue Eng A 2011;18:373-81.
39. Vosdoganes P, Hodges RJ, Lim R et al. Human amnion epithelial cells as a treatment for inflammation-induced fetal lung injury in sheep. Am J Obstet Gynecol 2011; 205:156.e26-33.
40. Murphy S, Lim R, Dickinson H et al. Human amnion epithelial cells prevent bleomycin-induced lung injury and preserve lung function. Cell Transplant 2011; 20:909-23.
41. Moodley Y, Ilancheran S, Samuel C et al. Human amnion epithelial cell transplantation abrogates lung fibrosis and augments repair. Am J Respir Crit Care Med 2010;182:643-51.
42. Parolini O, Alviano F, Bergwerf I et al. Toward cell therapy using placenta-derived cells: disease mechanisms, cell biology, preclinical studies, and regulatory aspects at the round table. Stem Cells Dev 2010;19:143-54.
43. Sakuragawa N, Thangavel R, Mizuguchi M et al. Expression of markers for both neuronal and glial cells in human amniotic epithelial cells. Neurosci Lett 1996;209:9-12.
44. Kakishita K, Elwan MA, Nakao N et al. Human amniotic epithelial cells produce dopamine and survive after implantation into the striatum of a rat model of Parkinson's disease: a potential source of donor for transplantation therapy. Exp Neurol 2000;165:27-34.
45. Sankar V. Role of human amniotic epithelial cell transplantation in spinal cord injury repair research. Neuroscience 2003;118:11-7.
46. Wu Z-yuan, Hui G-zhen, Lu Y et al. Transplantation of human amniotic epithelial cells improves hindlimb function in rats with spinal cord injury. Chin Med J 2006;119:2101-7.
47. Meng X-T, Li C, Dong Z-Y et al. Co-transplantation of bFGF-expressing amniotic epithelial cells and neural stem cells promotes functional recovery in spinal cord-injured rats. Cell Biol Int 2008;32:1546-58.
48. Sakuragawa N, Misawa H, Ohsugi K et al. Evidence for active acetylcholine metabolism in human amniotic epithelial cells: applicable to intracerebral allografting for neurologic disease. Neurosci Lett 1997;232:53-6.
49. Liu T, Wu J, Huang Q et al. Human amniotic epithelial cells ameliorate behavioral dysfunction and reduce infarct size in the rat middle cerebral artery occlusion model. Shock 2008;29:603-11.
50. Sakuragawa N, Enosawa S, Ishii T et al. Human amniotic epithelial cells are promising transgene carriers for allogeneic cell transplantation into liver. J Hum Genet 2000;45:171-6.
51. Marongiu F, Gramignoli R, Dorko K et al. Hepatic differentiation of amniotic epithelial cells. Hepatology 2011;53:1719-29.
52. Wei JP, Zhang TS, Kawa S et al. Human amnion-isolated cells normalize blood glucose in streptozotocin-induced diabetic mice. Cell Transplant 2003;12:545-52.
53. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006;8:315-7.
54. Afanasyev BV, Elstner EE, Zander AR et al. A. J. Friedenstein, founder of the mesenchymal stem cell concept. Transplantation 2010;1:35-8.
55. Heey O, Paulal U. A population of cells isolated from rat heart capable of differentiating into several mesodermal phenotypes. J Surg Res 1996;62:233-42.
56. Campagnoli C. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 2001;98:2396-402.
57. Bieback K, Kern S, Kluter H et al. Critical parameters for the isolation of mesenchymal stem cells from umbilical cord blood. Stem Cells 2004;22:625-34.
58. Pasquinelli G, Tazzari P, Ricci F et al. Ultrastructural characteristics of human mesenchymal stromal (stem) cells derived from bone marrow and term placenta. Ultrastruct Pathol 2007;31:23-31.
59. Baksh D, Song L, Tuan RS. Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy. J Cell Mol Med 2004;8:301-16.
60. Dzierzak E, Robin C. Placenta as a source of hematopoietic stem cells. Trends Mol Med 2010;16:361-7.
61. Amos T, Gordon M. Sources of human hematopoietic stem cells for transplantation - a review. Cell Transplant 1995;4:547-69.
62. Matikainen T, Laine J. Placenta - an alternative source of stem cells. Toxicol Appl Pharmacol 2005;207(2 Suppl):544-9.
63. Kaviani A. The placenta as a cell source in fetal tissue engineering. J Pediatr Surg 2002;37:995-9.
64. Gucciardo L, Lories R, Ochsenbein-Kolble N et al. Fetal mesenchymal stem cells: isolation, properties and potential use in perinatology and regenerative medicine. BJOG 2009;116:166-72.
65. Anker PS In't, Scherjon SA, Kleijburg-van der Keur C et al. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 2004;22:1338-45.
66. Igura K, Zhang X, Takahashi K et al. Isolation and characterization of mesenchymal progenitor cells from chorionic villi of human placenta. Cytotherapy 2004;6:543-53.
67. Sudo K, Kanno M, Miharada K et al. Mesenchymal progenitors able to differentiate into osteogenic, chondrogenic, and/or adipogenic cells in vitro are present in most primary fibroblast-like cell populations. Stem Cells 2007;25:1610-7.
68. Battula VL, Bareiss PM, Treml S et al. Human placenta and bone marrow derived MSC cultured in serum-free, b-FGF-containing medium express cell surface frizzled-9 and SSEA-4 and give rise to multilineage differentiation. Differentiation 2007;75:279-91.
69. Portmann-lanz CB, Schoeberlein A, Huber A et al. Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregeneration. Am J Obstet Gynecol 2006;664-73.
70. Soncini M, Vertua E, Gibelli L et al. Isolation and characterization of mesenchymal cells from human fetal membranes. J Tissue Eng Regen Med 2007;1:296-305.
71. Poloni A, Rosini V, Mondini E et al. Characterization and expansion of mesenchymal progenitor cells from first-trimester chorionic villi of human placenta. Cytotherapy 2008;10:690-7.
72. Zhang Y, Li C, Jiang X. Human placenta-derived mesenchymal progenitor cells support culture expansion of long-term culture-initiating cells from cord blood CD34+ cells. Exp Hematol 2004;32:657-64.
73. Alviano F, Fossati V, Marchionni C et al. Term amniotic membrane is a high throughput source for multipotent mesenchymal stem cells with the ability to differentiate into endothelial cells in vitro. BMC Dev Biol 2007;7:11.
74. Marcus AJ, Coyne TM, Rauch J et al. Isolation, characterization, and differentiation of stem cells derived from the rat amniotic membrane. Differentiation 2008;76:130-44.
75. Tamagawa T, Oi S, Ishiwata I et al. Differentiation of mesenchymal cells derived from human amniotic membranes into hepatocyte-like cells in vitro. Hum Cell 2007;20:77-84.
76. Chang C-M, Kao C-L, Chang Y-L et al. Placenta-derived multipotent stem cells induced to differentiate into insulin-positive cells. Biochem Biophys Res Commun 2007; 357:414-20.
77. Okamoto K, Miyoshi S, Toyoda M et al. 'Working' cardiomyocytes exhibiting plateau action potentials from human placenta-derived extraembryonic mesodermal cells. Exp Cell Res 2007;313:2550-62.
78. Sarugaser R, Lickorish D, Baksh D et al. Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells 2005;23:220-9.
79. Fong C, Richards M, Manasi N et al. Comparative growth behaviour and characterization of stem cells from human Wharton's jelly. Reprod Biomed Online 2007;15:708-18.
80. Guillot PV, Gotherstrom C, Chan J et al. Human first-trimester fetal MSC express pluripotency markers and grow faster and have longer telomeres than adult MSC. Stem Cells 2007;25:646-54.
81. Crane JP, Cheung SW. An embryogenic model to explain cytogenetic inconsistencies observed in chorionic villus versus fetal tissue. Prenat Diagn 1988;8:119-29.
82. Wolbank S, Peterbauer A, Fahrner M et al. Dose-dependent immunomodulatory effect of human stem cells from amniotic membrane: a comparison with human mesenchymal stem cells from adipose tissue. Tissue Eng 2007;13:1173-83.
83. Kawamichi Y, Cui C-H, Toyoda M et al. Cells of extraembryonic mesodermal origin confer human dystrophin in the mdx model of Duchenne muscular dystrophy. J Cell Physiol 2010;223:695-702.
84. Wei JP, Nawata M, Wakitani S et al. Human amniotic mesenchymal cells differentiate into chondrocytes. Cloning Stem Cells 2009;11:19-26.
85. Sakuragawa N, Kakinuma K, Kikuchi A et al. Human amnion mesenchyme cells express phenotypes of neuroglial progenitor cells. J Neurosci Res 2004;78:208-14.
86. Hennerbichler S, Griensven MVAN. Dose-dependent immunomodulatory effect of human stem cells mesenchymal stem cells from adipose tissue. Tissue Eng 2007;13:1173-83.
87. Zhang X, Mitsuru A, Igura K et al. Mesenchymal progenitor cells derived from chorionic villi of human placenta for cartilage tissue engineering. Biochemical and Biophys Res Commun 2006;340:944-52.
88. Bacenková D, Rosocha J, Tó thová T et al. Isolation and basic characterization of human term amnion and chorion mesenchymal stromal cells. Cytotherapy 2011;13:1047-56.
89. Trimester F, Villi C, Spitalieri P et al. Identification of multipotent cytotrophoblast cells from human first trimester chorionic villi. Cloning Stem Cells 2009;11:535-56.
90. Chien C-C, Yen BL, Lee F-K et al. In vitro differentiation of human placenta-derived multipotent cells into hepatocyte-like cells. Stem Cells 2006;24:1759-68.
91. Huang H-I. Isolation of human placenta-derived multipotent cells and in vitro differentiation into hepatocyte-like cells. Curr Protoc Stem Cell Biol 2007;1:1E.1.1-1.
92. Miki T, Mitamura K, Ross MA et al. Identification of stem cell marker-positive cells by immunofluorescence in term human amnion. J Reprod Immunol 2007;75:91-6.
93. Fariha M-MN, Chua K-H, Tan G-C et al. Human chorion-derived stem cells: changes in stem cell properties during serial passage. Cytotherapy 2011;13:582-93.
94. Bailo M, Soncini M, Vertua E et al. Engraftment potential of human amnion and chorion cells derived from term placenta. Transplantation 2004;78:1439-48.
95. Banas A, Teratani T, Yamamoto Y et al. IFATS collection: in vivo therapeutic potential of human adipose tissue mesenchymal stem cells after transplantation into mice with liver injury. Stem Cells 2008;26:2705-12.
96. Magatti M, De Munari S, Vertua E et al. Human amnion mesenchyme harbors cells with allogeneic T-cell suppression and stimulation capabilities. Stem Cells 2008;26:182-92.
97. Kong X-Y, Cai Z, Pan L et al. Transplantation of human amniotic cells exerts neuroprotection in MPTP-induced Parkinson disease mice. Brain Res 2008;1205:108-15.
98. Zhao P, Ise H, Hongo M et al. Human amniotic mesenchymal cells have some characteristics of cardiomyocytes. Transplantation 2005;79:528-35.
99. Prather WR, Toren A, Meiron M. Placental-derived and expanded mesenchymal stromal cells (PLX-I) to enhance the engraftment of hematopoietic stem cells derived from umbilical cord blood. Expert Opin Biol Ther 2008;8:1241-50.
100. Hiwase SD, Dyson PG, To LB et al. Cotransplantation of placental mesenchymal stromal cells enhances single and double cord blood engraftment in nonobese diabetic/severe combined immune deficient mice. Stem Cells 2009;27:2293-300.
101. Chen C-P, Liu S-H, Huang J-P et al. Engraftment potential of human placenta-derived mesenchymal stem cells after in utero transplantation in rats. Hum Reprod 2009; 24:154-65.
102. Ventura C, Cantoni S, Bianchi F et al. Hyaluronan mixed esters of butyric and retinoic acid drive cardiac and endothelial fate in term placenta human mesenchymal stem cells and enhance cardiac repair in infarcted rat hearts. J Biol Chem 2007;282:14243-52.
103. Fujimoto KL, Miki T, Liu LJ et al. Naive rat amnion-derived cell transplantation improved left ventricular function and reduced myocardial scar of postinfarcted heart. Cell Transplant 2009;18:477-86.
104. Schmidt D, Mol A, Breymann C et al. Living autologous heart valves engineered from human prenatally harvested progenitors. Circulation 2006;114(1 Suppl):I125-31.
105. Cargnoni A, Gibelli L, Tosini A et al. Transplantation of allogeneic and xenogeneic placenta-derived cells reduces bleomycin-induced lung fibrosis. Cell Transplant 2009;18:405-22.
106. Kranz A, Wagner D-C, Kamprad M et al. Transplantation of placenta-derived mesenchymal stromal cells upon experimental stroke in rats. Brain Res 2010;1315:128-36.
107. Yarygin KN, Kholodenko IV, Konieva AA et al. Mechanisms of positive effects of transplantation of human placental mesenchymal stem cells on recovery of rats after experimental ischemic stroke. Bull Exp Biol Med 2009;148:862-8.
108. Yu LC, Wall DA, Sandler E et al. Unrelated cord blood transplant experience by the pediatric blood and marrow transplant consortium. Pediatr Hematol Oncol 2001; 18:235-45.
109. Schoeberlein A, Mueller M, Reinhart U et al. Homing of placenta-derived mesenchymal stem cells after perinatal intracerebral transplantation in a rat model. Am J Obstet Gynecol 2011;205:277.e1-6.
110. Kadam S, Muthyala S, Nair P et al. Human placenta-derived mesenchymal stem cells and islet-like cell clusters generated from these cells as a novel source for stem cell therapy in diabetes. RDS 2010;7:168-82.
111. Soon-Shiong P, Feldman E, Nelson R et al. Long-term reversal of diabetes by the injection of immunoprotected islets. Proc Natl Acad Sci USA 1993;90:5843-7.
112. Lanzoni G, Alviano F, Marchionni C et al. Isolation of stem cell populations with trophic and immunoregulatory functions from human intestinal tissues: potential for cell therapy in inflammatory bowel disease. Cytotherapy 2009;11:1020-31.
113. Ishikane S, Ohnishi S, Yamahara K et al. Allogeneic injection of fetal membrane-derived mesenchymal stem cells induces therapeutic angiogenesis in a rat model of hind limb ischemia. Stem Cells 2008;26:2625-33.
114. Hwang JH, Shim SS, Seok OS et al. Comparison of cytokine expression in mesenchymal stem cells from human placenta, cord blood, and bone marrow. J Korean Med Sci 2009;24:547.
115. Prather WR, Toren A, Meiron M et al. The role of placental-derived adherent stromal cell (PLX-PAD) in the treatment of critical limb ischemia. Cytotherapy 2009;11:427-34.
116. Parolini O, Caruso M. Review: preclinical studies on placenta-derived cells and amniotic membrane: an update. Placenta 2011;32(Suppl 2):S186-95.
117. Sant'Anna LB, Cargnoni A, Ressel L et al. Amniotic membrane application reduces liver fibrosis in a bile duct ligation rat model. Cell Transplant 2011;20:441-53.
118. Ismail A, Ramsis R, Sherif A et al. Use of human amniotic stem cells for common bile duct reconstruction: vascularized support of a free amnion graft. Med Sci Monit 2009;15:BR243-7.
119. Ueno H, Weissman IL. The origin and fate of yolk sac hematopoiesis: application of chimera analyses to developmental studies. Int J Dev Biol 2010;54:1019-31.
120. Gekas C, Rhodes KE, Van Handel B et al. Hematopoietic stem cell development in the placenta. Int J Dev Biol 2010;54:1089-98.
121. Weissman IL. Stem cells: units of development, units of regeneration, and units in evolution. Evolution 2000;100:157-68.
122. Weissman IL, Shizuru JA. The origins of the identification and isolation of hematopoietic stem cells, and their capability to induce donor-specific transplantation tolerance and treat autoimmune diseases. Blood 2008;112:3543-53.
123. McGrath KE, Palis J. Hematopoiesis in the yolk sac: more than meets the eye. Exp Hematol 2005;33:1021-8.
124. Ottersbach K, Dzierzak E. The placenta as a haematopoietic organ. Int J Dev Biol 2010;54:1099-106.
125. Broxmeyer HE, Douglas GW, Hangoc G et al. Human umbilical cord blood as a potential source of transplantable hematopoietic stem/progenitor cells. Proc Natl Acad Sci USA 1989;86:3828-32.
126. Ditadi A, de Coppi P, Picone O et al. Human and murine amniotic fluid c-Kit+Lin-cells display hematopoietic activity. Blood 2009;113:3953-60.
127. Gekas C, Dieterlen-Lievre F, Orkin SH et al. Hematopoietic stem cells. Dev Cell 2005;8: 365-75.
128. Alvarez-Silva M, Belo-Diabangouaya P, Salau?n J et al. Mouse placenta is a major hematopoietic organ. Development 2003;130:5437-44.
129. Ottersbach K, Dzierzak E. The murine placenta contains hematopoietic stem cells within the vascular labyrinth region. Developmental Cell 2005;8:377-87.
130. Caprioli A, Jaffredo T, Gautier R et al. Blood-borne seeding by hematopoietic and endothelial precursors from the allantois. Proc Natl Acad Sci USA 1998;95:1641-6.
131. Tavian M, Robin C, Coulombel L et al. The human embryo, but not its yolk sac, generates lympho-myeloid stem cells: mapping multipotent hematopoietic cell fate in intraembryonic mesoderm. Immunity 2001;15:487-95.
132. Robin C, Bollerot K, Mendes S et al. Human placenta is a potent hematopoietic niche containing hematopoietic stem and progenitor cells throughout development. Stem Cell 2009;5:385-95.
133. Coulombel L. Identification of hematopoietic stem/progenitor cells: strength and drawbacks of functional assays. Oncogene 2004;23:7210-22.
134. De Coppi P, Bartsch G, Siddiqui MM et al. Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 2007;25:100-6.
135. Barlow S, Brooke G, Chatterjee K. Comparison of human placenta-and bone marrowderived multipotent mesenchymal stem cells. Stem Cell 2008;1108:1095-108.
136. Mihu CM, Mihu D, Costin N et al. Isolation and characterization of stem cells from the placenta and the umbilical cord. Rom J Morphol Embryol 2008;49:441-6.
137. Rao MS, Mattson MP. Stem cells and aging: expanding the possibilities. Mech Ageing Dev 2001;122:713-34.
138. Hass R, Kasper C, Bohm S et al. Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal 2011;9:12.
139. Brooke G, Tong H, Levesque J-P et al. Molecular trafficking mechanisms of multipotent mesenchymal stem cells derived from human bone marrow and placenta. Stem Cells Dev 2008;17:929-40.
140. Strakova Z, Livak M, Krezalek M et al. Multipotent properties of myofibroblast cells derived from human placenta. Cell Tissue Res 2008;332:479-88.
141. Cavallo C, Cuomo C, Fantini S et al. Comparison of alternative mesenchymal stem cell sources for cell banking and musculoskeletal advanced therapies. J Cell Biochem 2011;112:1418-30.