The endothelial antigen ESAM marks primitive hematopoietic progenitors throughout life in mice

Blood

Volumn 113, Issue 13, 2009, Pages 2914-2923

  Yokota, Takafumi ^a   Oritani, Kenji ^a   Butz, Stefan ^b   Kokame, Koichi ^c   Kincade, Paul W ^d   Miyata, Toshiyuki ^c   Vestweber, Dietmar ^b   Kanakura, Yuzuru ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^c NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^d OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN RECEPTOR; ATAXIN 1; CD31 ANTIGEN; CD34 ANTIGEN; CELL ANTIGEN; ENDOGLIN; ENDOTHELIAL CELL SELECTIVE ADHESION MOLECULE ANTIGEN; RAG1 PROTEIN; UNCLASSIFIED DRUG;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL ACTIVITY; CELL CULTURE; CELL SELECTION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ERYTHROID PRECURSOR CELL; FEMALE; FETUS; FETUS LIVER; FLOW CYTOMETRY; GENE ACTIVATION; GENE EXPRESSION; GENE LOCUS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; LYMPHOID PROGENITOR CELL; LYMPHOPOIESIS; MALE; MICROARRAY ANALYSIS; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; PRIORITY JOURNAL; UPREGULATION;

EID: 63849111505     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-07-167106     Document Type: Article

References (47)

1. Osawa M, Hanada K, Hamada H, Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science. 1996;273:242-245.
2. Spangrude GJ, Brooks DM. Mouse strain variability in the expression of the hematopoietic stem cell antigen Ly-6A/E by bone marrow cells. Blood. 1993;82:3327-3332.
3. Ogawa M. Changing phenotypes of hematopoi- etic stem cells. Exp Hematol. 2002;30:3-6.
4. Chambers SM, Shaw CA, Gatza C, Fisk CJ, Donehower LA, Goodell MA. Aging hematopoietic stem cells decline in function and exhibit epigenetic dysregulation. PLoS Biol. 2007;5:e201.
5. Yilmaz OH, Kiel MJ, Morrison SJ. SLAM family markers are conserved among hematopoietic stem cells from old and reconstituted mice and markedly increase their purity. Blood. 2006;107:924-930.
6. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861-872.
7. Hanna J, Wernig M, Markoulaki S, et al. Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science. 2007;318:1920-1923.
8. 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.
9. Oberlin E, Tavian M, Blazsek I, Péault B. Blood- forming potential of vascular endothelium in the human embryo. Development. 2002;129:4147-4157.
10. Yoder MC, Hiatt K, Dutt P, Mukherjee P, Bodine DM, Orlic D. Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity. 1997;7:335-344.
11. Takakura N, Huang XL, Naruse T, et al. Critical role of the TIE2 endothelial cell receptor in the development of definitive hematopoiesis. Immunity. 1998;9:677-686.
12. Cho SK, Bourdeau A, Letarte M, Zúñiga-Pflücker JC. Expression and function of CD105 during the onset of hematopoiesis from Flk1(+) precursors. Blood. 2001;98:3635-3642.
13. Matsuoka S, Ebihara Y, Xu M, et al. CD34ex- pression on long-term repopulating hematopoietic stem cells changes during developmental stages. Blood. 2001;97:419-425.
14. Sato T, Laver JH, Ogawa M. Reversible expression of CD34 by murine hematopoietic stem cells. Blood. 1999;94:2548-2554.
15. Tajima F, Sato T, Laver JH, Ogawa M. CD34 expression by murine hematopoietic stem cells mobilized by granulocyte colony-stimulating factor. Blood. 2000;96:1989-1993.
16. Randall TD, Weissman IL. Phenotypic and functional changes induced at the clonal level in he- matopoietic stem cells after 5-fluorouracil treatment. Blood. 1997;89:3596-3606.
17. Matsubara A, IwamaA, Yamazaki S, et al. Endo- mucin, a CD34-like sialomucin, marks hematopoi- etic stem cells throughout development. J Exp Med. 2005;202:1483-1492.
18. Yokota T, Kouro T, Hirose J, et al. Unique properties of fet al lymphoid progenitors identified according to RAG1 gene expression. Immunity. 2003;19:365-375.
19. Yokota T, Huang J, Tavian M, et al. Tracing the first waves of lymphopoiesis in mice. Development. 2006;133:2041-2051.
20. Kuwata N, Igarashi H, Ohmura T, Aizawa S, Sakaguchi N. Cutting edge: absence of expression of RAG1 in peritoneal B-1 cells detected by knocking into RAG1 locus with green fluorescent protein gene. J Immunol. 2001;163:6355-6359.
21. Igarashi H, Gregory SC, Yokota T, Sakaguchi N, Kincade PW. Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity. 2002;17:117-130.
22. Nasdala I, Wolburg-Buchholz K, Wolburg H, et al. A transmembrane tight junction protein selectively expressed on endothelial cells and platelets. J Biol Chem. 2002;277:16294-16303.
23. Yuasa H, Oike Y, Iwama A, et al. Oncogenic transcription factor Evi1 regulates hematopoietic stem cell proliferation through GATA-2 expression. EMBO J. 2005;24:1976-1987.
24. Mikkola HK, Fujiwara Y, Schlaeger TM, Traver D, Orkin SH. Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo. Blood. 2003;101:508-516.
25. Akashi K, Traver D, Miyamoto T, Weissman IL. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature. 2000;404:193-197.
26. Kim I, He S, Yilmaz OH, Kiel MJ, Morrison SJ. Enhanced purification of fet al liver hematopoietic stem cells using SLAM family receptors. Blood. 2006;108:737-744.
27. Cumano A, Dieterlen-Lievre F, Godin I. Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchno- pleura. Cell. 1996;86:907-916.
28. Medvinsky A, Dzierzak E. Definitive hematopoi- esis is autonomously initiated by the AGM region. Cell. 1996;86:897-906.
29. 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.
30. Forsberg EC, Prohaska SS, Katzman S, Heffner GC, Stuart JM, Weissman IL. Differential expression of novel potential regulators in hematopoietic stem cells. PLoS Genet. 2005;1:e28.
31. Hirata Ki, IshidaT, Penta K, et al. Cloning of an immunoglobulin family adhesion molecule selectively expressed by endothelial cells. J Biol Chem. 2001;276:16223-16231.
32. Kincade PW, Owen JJ, Igarashi H, Kouro T Yokota T, Rossi MI. Nature or nurture? Steady- state lymphocyte formation in adults does not recapitulate ontogeny. Immunol Rev. 2002;187:116-125.
33. Samokhvalov IM, Samokhvalova NI, Nishikawa SI. Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature. 2007;446:1056-1061.
34. Yao L, Yokota T, Xia L, Kincade PW, McEver RP. Bone marrow dysfunction in mice lacking the cy- tokine receptor gp130 in endothelial cells. Blood. 2005;106:4093-4101.
35. Wegmann F, Petri B, Khandoga AG, et al. ESAM supports neutrophil extravasation, activation of Rho, and VEGF-induced vascular permeability. J Exp Med. 2006;203:1671-1677.
36. Brass LF, Zhu L, Stalker TJ. Novel therapeutic targets at the platelet vascular interface. Arterio- scler Thromb Vasc Biol. 2008;28[suppl]:S43-S50.
37. Zhang J, Niu C, Ye L, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003;425:836-841.
38. Calvi LM, Adams GB, Weibrecht KW, et al. Os- teoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003;425:841-846.
39. Kiel MJ, Yilmaz OH, IwashitaT, Yilmaz OH, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005;121:1109-1121.
40. Sugiyama T, Kohara H, Noda M, Nagasawa T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity. 2006;25:977-988.
41. Yin T, Li L. The stem cell niches in bone. J Clin Invest. 2006;116:1195-1201.
42. Orford KW, Scadden DT. Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat Rev Genet. 2008;9:115-128.
43. Balazs AB, Fabian AJ, Esmon CT, Mulligan RC. Endothelial protein C receptor (CD201) explicitly identifies hematopoietic stem cells in murine bone marrow. Blood. 2006;107:2317-2321.
44. Jokubaitis VJ, Sinka L, Driessen R, et al. Angio- tensin-converting enzyme (CD143) marks hema- topoietic stem cells in human embryonic, fet al, and adult hematopoietic tissues. Blood. 2008;111:4055-4063.
45. Massberg S, Schaerli P, Knezevic-Maramica I, et al. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell. 2007;131:994-1008.
46. Welner RS, Kincade PW. Stem cells on patrol. Cell. 2007;131:842-844.
47. Massberg S, Konrad I, Schurzinger K, et al. Platelets secrete stromal cell-derived factor 1al- pha and recruit bone marrow-derived progenitor cells to arterial thrombi in vivo. J Exp Med. 2006;203:1221-1233.