Expression of angiotensin-converting enzyme (CD143) identifies and regulates primitive hemangioblasts derived from human pluripotent stem cells

Blood

Volumn 112, Issue 9, 2008, Pages 3601-3614

  Zambidis, Elias T ^a,b   Park, Tea Soon ^c   Yu, Wayne ^b   Tam, Ada ^a   Levine, Michal ^a   Yuan, Xuan ^a,b   Pryzhkova, Marina ^a   Péault, Bruno ^c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN RECEPTOR; CD34 ANTIGEN; CD45 ANTIGEN; DIPEPTIDYL CARBOXYPEPTIDASE; FIBROBLAST GROWTH FACTOR; THROMBOPOIETIN; BIOLOGICAL MARKER; GROWTH PROMOTOR;

ARTICLE; BLAST CELL; CELL DIFFERENTIATION; CELL EXPANSION; CONTROLLED STUDY; ENDOTHELIUM; ENZYME ACTIVITY; GESTATIONAL AGE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SIGNAL TRANSDUCTION; YOLK SAC; CELL LINE; CLONOGENIC ASSAY; CYTOLOGY; DRUG EFFECT; DRUG POTENTIATION; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; ENZYMOLOGY; IMMUNOLOGY; METABOLISM;

BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE; COLONY-FORMING UNITS ASSAY; DRUG SYNERGISM; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; GROWTH SUBSTANCES; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; PEPTIDYL-DIPEPTIDASE A; PLURIPOTENT STEM CELLS; RENIN-ANGIOTENSIN SYSTEM; THROMBOPOIETIN; YOLK SAC;

EID: 55749104551     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-03-144766     Document Type: Article

References (64)

1. Migliaccio G, Migliaccio AR, Petti S, et al. Human embryonic hemopoiesis. Kinetics of progenitors and precursors underlying the yolk sac-liver transition. J Clin Invest. 1986;78:51-60.
2. Tavian M, Hallais MF, and BPeault. Emergence of intraembryonic hematopoietic precursors in the pre-liver human embryo. Development. 1999; 126:793-803.
3. Bloom W, Bartelmez GW. Hematopoiesis in young human embryos. Am J Anat. 1940;67: 21-53.
4. Rowley RT, Ohisson-Wilhelm BM, Farley B. Erythroid colony formation from human fetal liver. Proc Natl Acad Sci U S A. 1978;75:984-988.
5. Peschle C, Migliaccio AR, Migliaccio G, et al. Embryonic3fetal Hb switch in humans: studies on erythroid bursts generated by embryonic progenitors from yolk sac and liver. Proc Natl Acad Sci U S A. 1984;81:2416-2420.
6. Peschle C, Mavilio F, Care A, et al. Haemoglobin switching in human embryos: asynchrony of ζ-α and ζ-α-globin switches in primitive and definite erythropoietic lineage. Nature. 1985;313:235-238.
7. Thomas DB, Yoffey JM. Human foetal haematopoiesis. II. Hepatic haematopoiesis in the human foetus. Br J Haematol. 1964;10:193-197.
8. Moore MA, Metcalf D. Ontogeny of the haemopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br J Haematol. 1970;18:279-296.
9. Palis J, Robertson S, Kennedy M, Wall C, Keller G. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development. 1999;126:5073-5084.
10. Stamatoyannopoulos G, Constantoulakis M, Brice M, Kurachi S, Papayannopoulos T. Coexpression of embryonic, fetal, and adult globins in erythroid cells of human embryos: relevance to the cell lineage models of globin switching. Dev Biol. 1987;123:191-197.
11. Medvinsky A, Dzierzak E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell. 1996;86:897-906.
12. Cumano A, Ferraz JC, Klaine M, Di Santo JP, Godin I. Intraembryonic, but not yolk sac hematopoietic precursors, isolated before circulation, provide long-term multilineage reconstitution. Immunity. 2001;15:477-485.
13. Toles JF, Chui DH, Belbeck LW, Starr E, Barker JE. Hemopoietic stem cells in murine embryonic yolk sac and peripheral blood. Proc Natl Acad Sci U S A. 1989;86:7456-7459.
14. Yoder MC, Hiatt K. Engraftment of embryonic hematopoietic cells in conditioned newborn recipients. Blood. 1997;89:2176-2183.
15. Yoder MC, Hiatt K, Mukherjee P. In vivo repopulating hematopoietic stem cells are present in the murine yolk sac at day 9.0 postcoitus. Proc Natl Acad Sci U S A. 1997;94:6776-6780.
16. Samokhvalov IM, Samakhvalova NI, Nishikawa SI. Cell tracing shows the contribution of the yolk sac to adult hematopoiesis. Nature. 2007;446: 1056-1061.
17. Sabin FR. Studies on the origin of blood vessels and of red blood corpuscles as seen in the living blastoderm of checks during the second day of incubation. Carnegie Inst. Wash. Pub. no. 272. Contrib Embryol. 1920;9:214.
18. Nishikawa SI, Nishikawa S, Kawamoto H, et al. In vitro generation of lymphohematopoietic cells from endothelial cells purified from murine embryos. Immunity. 1998;8:761-769.
19. Cortés F, Debacker C, Peault B, Labastie MC. Differential expression of KDR/VEGFR-2 and CD34 during mesoderm development of the early human embryo. Mech Dev. 1999;83:161-164.
20. Tavian M, Robin C, Coulombel L, Peault B. The human embryo, but not its yolk sac, generates lymphomyeloid stem cells: mapping multipotent hematopoietic cell fate in intraembryonic mesoderm. Immunity. 2001;15:487-495.
21. Oberlin E, Tavian M, Blazsek I, Peault B. Bloodforming potential of vascular endothelium in the human embryo. Development. 2002;129:4147-4157.
22. de Bruijn MF, Ma X, Robin C, Ottersbach K, Sanchez MJ, Dzierzak E. Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity. 2002;16: 673-683.
23. Kaufman DS, Hanson ET, Lewis RL, Auerbach R, Thomson JA. Hematopoietic colony-forming cells derived from human embryonic stem cells. Proc Natl Acad Sci U S A. 2001;98:10716-10721.
24. Wang L, Li L, Shojaei F, et al. Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity. 2004;21: 31-41.
25. Zambidis E, Peault B, Park TS, Bunz F, Civin CI. Hematopoietic differentiation of human embryonic stem cells progresses through sequential hemato-endothelial, primitive, and definitive stages resembling human yolk sac development. Blood. 2005;106:860-870.
26. Ng E, Davis RP, Azzola L, Stanley EG, Elefanty AG. Forced aggregation of defined numbers of human embryonic stem cells into embryoid bodies fosters robust, reproducible hematopoietic differentiation. Blood. 2005;106:1601-1603.
27. Chang KH, Nelson AM, Cao H, et al. Definitivelike erythroid cells derived from human embryonic stem cells co-express high levels of embryonic and fetal with little or no adult globin. Blood. 2006; 108:1515-1523.
28. Kennedy M, D'Souza S, Lynch-Kattman M, Schwantz S, Keller G. Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood. 2007;109:2679-2687.
29. Lu SJ, Feng Q, Caballero S, et al. Generation of functional hemangioblasts from human embryonic stem cells. Nature Methods. 2007;4:501-509.
30. Kabrun N, Buhring HJ, Choi K, Ullrich A, Risau W, Keller G. Flk-1 expression defines a population of early embryonic hematopoietic precursors. Development. 1997;124:2039-2048.
31. Shalaby F, Ho J, Stanford WL, et al. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell. 1997;89:981-990.
32. Chung YS, Zhang WJ, Arentson E, Kingsley PD, Palis J, Choi K. Lineage analysis of the hemangioblast as defined by FLK1 and SCL expression. Development. 2002;129:5511-5520.
33. Ramshaw HS, Haylock D, Swart B, et al. Monoclonal antibody BB9 raised against bone marrow stromal cells identifies a cell-surface glycoprotein expressed by primitive human hemopoietic progenitors. Exp Hematol. 2001;29:981-992.
34. Jokubaitis V, Sinka L, Driessen R, et al. Angioten-sinconverting enzyme (CD143) marks human embryonic, fetal, and adult primitive hematopoietic cells. Blood. 2008;111:4055-4063.
35. Savary K, Michaud A, Favier J, Larger E, Corvol P, Gasc JM. Role of the renin-angiotensin system in primitive erythropoiesis in the chick embryo. Blood. 2005;105:103-110.
36. Nakano T, Kodama H, T. Honjo. In vitro development of primitive and definitive erythrocytes from different precursors. Science. 1996;272:722-724.
37. Kennedy M, Firpo M, Choi K, et al. A common precursor for primitive erythropoiesis and definitive haematopoiesis. Nature. 1997;386:488-493.
38. Vodyanik MA, Thomson JA, Slukvin II. Leukosialin (CD43) defines hematopoietic progenitors in human embryonic stem cell differentiation cultures. Blood. 2006;108:2095-2105.
39. Timens W, Kamps WA. Hemopoiesis in human fetal and embryonic liver. Microsc Res Tech. 1997;39:387-397.
40. Schuh AC, Faloon P, Hu QL, Bhimani M, Choi KC. In vitro hematopoietic and endothelial potential of flk-1(-/-) embryonic stem cells and embryos. Proc Natl Acad Sci U S A. 1999;96:2159-2164.
41. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G. A common precursor for hematopoietic and endothelial cells. Development. 1998; 125:725-732.
42. Vodyanik MA, Bork JA, Thomson JA, Slukvin II. Human embryonic stem cell-derived CD34+ cells: efficient production in the co-culture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood. 2005;105:617-625.
43. Goodell MA, Rosenzweig M, Kim H, et al. Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nature Med. 1997;3:1337-1345.
44. Bhatia M, Bonnet D, Murdoch B, Gan OI, Dick JE. A newly discovered class of human hematopoietic cells with SCID-repopulating activity. Nat Med. 1998;4:1038-1045.
45. Grady EF, Sechi LA, Griffin C, Schambelan M, Kalinyak JE. Expression of AT2 Receptors in the developing rat fetus. J Clin Invest. 1991;88:921-929.
46. Schü tz S, Moullec JM, Corvol P, and Gasc JM Early expression of all the components of the reninangiotensin system in human development. Am J Pathol. 1996;149:2067-2079.
47. Akishita M, Ito M, Lehtonene J, Daviet L, Dzau V, Horiuchi M. Expression of the AT2 receptor developmentally programs extracellular signal-regulated kinase activity and influences fetal vascular growth. J Clin Invest. 1999;103:63-71.
48. Nakajima M, Hutchinson HG, Fujinaga M, et al. The angiotensin II type 2 (AT2) receptor antagonizes the growth effects of the AT1 receptor: gainoffunction study using gene transfer. Proc Natl Acad Sci U S A. 1995;92:10663-10667.
49. Luckett WP. Origin and differentiation of the yolk sac and extraembryonic mesoderm in presomite human and rhesus monkey embryos. Am J Anat. 1978;152:59-97.
50. Huber TL, Kouskoff V, Fehling HJ, Pali J, Keller G. Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature. 2004;432:625-630.
51. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282:1145-1147.
52. Osawa M, Hanada KI, Hamada H, Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science. 1996;273:242-245.
53. Chisi J, Wdzieczak-Bakala J, Thierry J, Briscoe C, Riches AC. Captopril inhibits the proliferation of hematopoietic stem and progenitor cells in murine long-term bone marrow cultures. Stem Cells. 1999;17:339-344.
54. Egami K, Murohara T, Shimada T, et al. Role of host angiotensin II type 1 receptor in tumor angiogenesis and growth. J Clin Invest. 2003;112:67-75.
55. Hubert C, Savary K, Gasc JM, Corvol P. The hematopoietic system: a new niche for the reninangiotensin system. Nat Clin Pract Cardiovasc Med. 2006;3:80-85.
56. Heffelfinger SC. The renin angiotensin system in the regulation of angiogenesis. Curr Pharm Des. 2007;13:1215-1229.
57. Rousseau A, Michaud A, Chauvet M-T, Lenfant M, Corvol P. The homoregulatory peptide N-acetyl-ser-asp-lys-pro is a natural and specific substrate of the N-terminal active site of human angiotensin-converting enzyme. J Biol Chem. 1995;270:3656-3661.
58. Bogden A, Moreau J-P, Gamba-Vitalo C, et al. Goralatide (AcSDKP), a negative growth regulator, protects the stem cell compartment during chemotherapy enhancing the myelopoietic response to GM-CSF. Int J Cancer. 1998;76:38-46.
59. Mrug M, Stopka T, Julian BA, Prchal J, Prchal J. Angiotensin II stimulates proliferation of normal early erythroid progenitors. J Clin Invest. 1997; 100:2310-2314.
60. Rodgers KE, Xiong S, Steer R, diZerega GS. Effect of angiotensin II on hematopoietic progenitor cell proliferation. Stem Cells. 2000;18:287-294.
61. Charrier S, Michaud A, Badaoui S, et al. Inhibition of angiotensin I-converting enzyme induces radioprotection by preserving murine hematopoietic short-term reconstituting cells (2004). Blood. 2004;104:978-985.
62. Cohn RD, van Erp C, Habashi JP, et al. Angiotensin II type 1 receptor blockade attenuates TGF-binduced failure of muscel regeneration in multiple myopathic states. Nat Med. 2007;13:204-210.
63. Grammatopoulos TN, Ahmedi F, Jones SM, Fariss MW, Wehenmeyer JA, Zawada WM. Angiotensin II protects cultured midbrain dopaminergic neurons against rotenone-induced cell death. Brain Res. 2005;1045:64-71.
64. Vervoort VS, Beacham MA, Edwards PS, et al. AGTR2 mutations in X-linked mental retardation. Science. 2002;296:2401-2403.