Human Placenta Is a Potent Hematopoietic Niche Containing Hematopoietic Stem and Progenitor Cells throughout Development

Cell Stem Cell

Volumn 5, Issue 4, 2009, Pages 385-395

  Robin, Catherine ^a   Bollerot, Karine ^a   Mendes, Sandra ^a   Haak, Esther ^a   Crisan, Mihaela ^a   Cerisoli, Francesco ^a   Lauw, Ivoune ^a   Kaimakis, Polynikis ^a   Jorna, Ruud ^a   Vermeulen, Mark ^a   Kayser, Manfred ^a   van der Linden, Reinier ^a   Imanirad, Parisa ^a   Verstegen, Monique ^a   Nawaz Yousaf, Humaira ^a   Papazian, Natalie ^a   Steegers, Eric ^a   Cupedo, Tom ^a   Dzierzak, Elaine ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

STEMCELL

Indexed keywords

CD34 ANTIGEN; DNA;

ANIMAL EXPERIMENT; ARTICLE; CELL POPULATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; FEMALE; FETUS; FLOW CYTOMETRY; GESTATION PERIOD; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MOUSE; NONHUMAN; PERICYTE; PLACENTA DEVELOPMENT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SCID MOUSE; STROMA CELL; VASCULARIZATION;

ANIMALS; CELL TRANSPLANTATION; FEMALE; FLOW CYTOMETRY; GESTATIONAL AGE; HEMATOPOIETIC STEM CELLS; HEMATOPOIETIC SYSTEM; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; PLACENTA; POLYMERASE CHAIN REACTION; PREGNANCY;

EID: 70349308500     PISSN: 19345909     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stem.2009.08.020     Document Type: Article

References (52)

1. Alvarez-Silva M., Belo-Diabangouaya P., Salaun J., and Dieterlen-Lievre F. Mouse placenta is a major hematopoietic organ. Development 130 (2003) 5437-5444
2. Bailo M., Soncini M., Vertua E., Signoroni P.B., Sanzone S., Lombardi G., Arienti D., Calamani F., Zatti D., Paul P., et al. Engraftment potential of human amnion and chorion cells derived from term placenta. Transplantation 78 (2004) 1439-1448
3. Barcena A., Kapidzic M., Muench M.O., Gormley M., Scott M.A., Weier J.F., Ferlatte C., and Fisher S.J. The human placenta is a hematopoietic organ during the embryonic and fetal periods of development. Dev. Biol. 327 (2009) 24-33
4. Becker M., Nitsche A., Neumann C., Aumann J., Junghahn I., and Fichtner I. Sensitive PCR method for the detection and real-time quantification of human cells in xenotransplantation systems. Br. J. Cancer 87 (2002) 1328-1335
5. Bhatia M., Bonnet D., Murdoch B., Gan O.I., and Dick J.E. A newly discovered class of human hematopoietic cells with SCID-repopulating activity. Nat. Med. 4 (1998) 1038-1045
6. Bhatia M., Wang J.C., Kapp U., Bonnet D., and Dick J.E. Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc. Natl. Acad. Sci. USA 94 (1997) 5320-5325
7. Cashman J., Bockhold K., Hogge D.E., Eaves A.C., and Eaves C.J. Sustained proliferation, multi-lineage differentiation and maintenance of primitive human haemopoietic cells in NOD/SCID mice transplanted with human cord blood. Br. J. Haematol. 98 (1997) 1026-1036
8. Challier J.C., Galtier M., Cortez A., Bintein T., Rabreau M., and Uzan S. Immunocytological evidence for hematopoiesis in the early human placenta. Placenta 26 (2005) 282-288
9. Chen Y., Zhang H., Gou X., Horikawa Y., Xing J., and Chen Z. Upregulation of HAb18G/CD147 in activated human umbilical vein endothelial cells enhances the angiogenesis. Cancer Lett. 278 (2009) 113-121
10. Corbel C., Salaun J., Belo-Diabangouaya P., and Dieterlen-Lievre F. Hematopoietic potential of the pre-fusion allantois. Dev. Biol. 301 (2007) 478-488
11. Coulombel L. Identification of hematopoietic stem/progenitor cells: strength and drawbacks of functional assays. Oncogene 23 (2004) 7210-7222
12. Crisan M., Yap S., Casteilla L., Chen C.W., Corselli M., Park T.S., Andriolo G., Sun B., Zheng B., Zhang L., et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3 (2008) 301-313
13. Cumano A., Dieterlen-Lievre F., and Godin I. Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura. Cell 86 (1996) 907-916
14. de Bruijn M.F., Speck N.A., Peeters M.C., and Dzierzak E. Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. EMBO J. 19 (2000) 2465-2474
15. Durand C., Robin C., and Dzierzak E. Mesenchymal lineage potentials of aorta-gonad-mesonephros stromal clones. Haematologica 91 (2006) 1172-1179
16. Dzierzak E., and Speck N.A. Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat. Immunol. 9 (2008) 129-136
17. Ferkowicz M.J., Starr M., Xie X., Li W., Johnson S.A., Shelley W.C., Morrison P.R., and Yoder M.C. CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo. Development 130 (2003) 4393-4403
18. Fukuchi Y., Nakajima H., Sugiyama D., Hirose I., Kitamura T., and Tsuji K. Human placenta-derived cells have mesenchymal stem/progenitor cell potential. Stem Cells 22 (2004) 649-658
19. Gekas C., Dieterlen-Lievre F., Orkin S.H., and Mikkola H.K. The placenta is a niche for hematopoietic stem cells. Dev. Cell 8 (2005) 365-375
20. Gude N.M., Roberts C.T., Kalionis B., and King R.G. Growth and function of the normal human placenta. Thromb. Res. 114 (2004) 397-407
21. Hann I.M., Bodger M.P., and Hoffbrand A.V. Development of pluripotent hematopoietic progenitor cells in the human fetus. Blood 62 (1983) 118-123
22. Igura K., Zhang X., Takahashi K., Mitsuru A., Yamaguchi S., and Takashi T.A. Isolation and characterization of mesenchymal progenitor cells from chorionic villi of human placenta. Cytotherapy 6 (2004) 543-553
23. In't Anker P.S., Scherjon S.A., Kleijburg-van der Keur C., de Groot-Swings G.M., Claas F.H., Fibbe W.E., and Kanhai H.H. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 22 (2004) 1338-1345
24. Kim S.J., Song C.H., Sung H.J., Yoo Y.D., Geum D.H., Park S.H., Yoo J.H., Oh J.H., Shin H.J., Kim S.H., et al. Human placenta-derived feeders support prolonged undifferentiated propagation of a human embryonic stem cell line, SNUhES3: comparison with human bone marrow-derived feeders. Stem Cells Dev. 16 (2007) 421-428
25. Kumaravelu P., Hook L., Morrison A.M., Ure J., Zhao S., Zuyev S., Ansell J., and Medvinsky A. Quantitative developmental anatomy of definitive haematopoietic stem cells/long-term repopulating units (HSC/RUs): role of the aorta-gonad-mesonephros (AGM) region and the yolk sac in colonisation of the mouse embryonic liver. Development 129 (2002) 4891-4899
26. Larochelle A., Vormoor J., Hanenberg H., Wang J.C., Bhatia M., Lapidot T., Moritz T., Murdoch B., Xiao X.L., Kato I., et al. Identification of primitive human hematopoietic cells capable of repopulating NOD/SCID mouse bone marrow: implications for gene therapy. Nat. Med. 2 (1996) 1329-1337
27. Li C.D., Zhang W.Y., Li H.L., Jiang X.X., Zhang Y., Tang P., and Mao N. Isolation and identification of a multilineage potential mesenchymal cell from human placenta. Placenta (2005) in press. Published online September 17, 2005
28. Medvinsky A., and Dzierzak E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86 (1996) 897-906
29. Miao Z., Jin J., Chen L., Zhu J., Huang W., Zhao J., Qian H., and Zhang X. Isolation of mesenchymal stem cells from human placenta: comparison with human bone marrow mesenchymal stem cells. Cell Biol. Int. 30 (2006) 681-687
30. Miyamoto K., Hayashi K., Suzuki T., Ichihara S., Yamada T., Kano Y., Yamabe T., and Ito Y. Human placenta feeder layers support undifferentiated growth of primate embryonic stem cells. Stem Cells 22 (2004) 433-440
31. Oberlin E., Tavian M., Blazsek I., and Peault B. Blood-forming potential of vascular endothelium in the human embryo. Development 129 (2002) 4147-4157
32. Ottersbach K., and Dzierzak E. The murine placenta contains hematopoietic stem cells within the vascular labyrinth region. Dev. Cell 8 (2005) 377-387
33. Palis J., Robertson S., Kennedy M., Wall C., and Keller G. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 126 (1999) 5073-5084
34. Parolini O., Alviano F., Bagnara G.P., Bilic G., Buhring H.J., Evangelista M., Hennerbichler S., Liu B., Magatti M., Mao N., 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 26 (2008) 300-311
35. Pflumio F., Izac B., Katz A., Shultz L.D., Vainchenker W., and Coulombel L. Phenotype and function of human hematopoietic cells engrafting immune-deficient CB17-severe combined immunodeficiency mice and nonobese diabetic-severe combined immunodeficiency mice after transplantation of human cord blood mononuclear cells. Blood 88 (1996) 3731-3740
36. Portmann-Lanz C.B., Schoeberlein A., Huber A., Sager R., Malek A., Holzgreve W., and Surbek D.V. Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregeneration. Am. J. Obstet. Gynecol. 194 (2006) 664-673
37. Rhodes K.E., Gekas C., Wang Y., Lux C.T., Francis C.S., Chan D.N., Conway S., Orkin S.H., Yoder M.C., and Mikkola H.K. The emergence of hematopoietic stem cells is initiated in the placental vasculature in the absence of circulation. Cell Stem Cell 2 (2008) 252-263
38. Sullivan K.M., Mannucci A., Kimpton C.P., and Gill P. A rapid and quantitative DNA sex test: fluorescence-based PCR analysis of X-Y homologous gene amelogenin. BioTechniques 15 (1993) 636-638 640-641
39. Tavian M., Coulombel L., Luton D., Clemente H.S., Dieterlen-Lievre F., and Peault B. Aorta-associated CD34+ hematopoietic cells in the early human embryo. Blood 87 (1996) 67-72
40. Tavian M., Hallais M.F., and Peault B. Emergence of intraembryonic hematopoietic precursors in the pre-liver human embryo. Development 126 (1999) 793-803
41. Tavian M., and Peault B. Embryonic development of the human hematopoietic system. Int. J. Dev. Biol. 49 (2005) 243-250
42. Tavian M., Robin C., Coulombel L., and Peault B. The human embryo, but not its yolk sac, generates lympho-myeloid stem cells: mapping multipotent hematopoietic cell fate in intraembryonic mesoderm. Immunity 15 (2001) 487-495
43. Tse W., Bunting K.D., and Laughlin M.J. New insights into cord blood stem cell transplantation. Curr. Opin. Hematol. 15 (2008) 279-284
44. Wang J., Kimura T., Asada R., Harada S., Yokota S., Kawamoto Y., Fujimura Y., Tsuji T., Ikehara S., and Sonoda Y. SCID-repopulating cell activity of human cord blood-derived CD34- cells assured by intra-bone marrow injection. Blood 101 (2003) 2924-2931
45. Wang J.C., Doedens M., and Dick J.E. Primitive human hematopoietic cells are enriched in cord blood compared with adult bone marrow or mobilized peripheral blood as measured by the quantitative in vivo SCID-repopulating cell assay. Blood 89 (1997) 3919-3924
46. Weir B.S. Forensics. In: Balding D.J., Bishop M., and Cannings C. (Eds). Handbook of Statistical Genetics (2003), Wiley and Sons, Hoboken, NJ 830-850
47. Wulf G.G., Viereck V., Hemmerlein B., Haase D., Vehmeyer K., Pukrop T., Glass B., Emons G., and Trumper L. Mesengenic progenitor cells derived from human placenta. Tissue Eng. 10 (2004) 1136-1147
48. Yen B.L., Huang H.I., Chien C.C., Jui H.Y., Ko B.S., Yao M., Shun C.T., Yen M.L., Lee M.C., and Chen Y.C. Isolation of multipotent cells from human term placenta. Stem Cells 23 (2005) 3-9
49. Zambidis E.T., Oberlin E., Tavian M., and Peault B. Blood-forming endothelium in human ontogeny: lessons from in utero development and embryonic stem cell culture. Trends Cardiovasc. Med. 16 (2006) 95-101
50. Zeigler B.M., Sugiyama D., Chen M., Guo Y., Downs K.M., and Speck N.A. The allantois and chorion, when isolated before circulation or chorio-allantoic fusion, have hematopoietic potential. Development 133 (2006) 4183-4192
51. Zhang X., Mitsuru A., Igura K., Takahashi K., Ichinose S., Yamaguchi S., and Takahashi T.A. Mesenchymal progenitor cells derived from chorionic villi of human placenta for cartilage tissue engineering. Biochem. Biophys. Res. Commun. 340 (2006) 944-952
52. Zhang Y., Li C., Jiang X., Zhang S., Wu Y., Liu B., Tang P., and Mao N. Human placenta-derived mesenchymal progenitor cells support culture expansion of long-term culture-initiating cells from cord blood CD34+ cells. Exp. Hematol. 32 (2004) 657-664