Novel roles for Notch, Wnt and Hedgehog in hematopoesis derived from human pluripotent stem cells

International Journal of Developmental Biology

Volumn 54, Issue 6-7, 2010, Pages 955-964

  Cerdan, Chantal ^a   Bhatia, Mickie ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Hedgehog; Hematopoiesis; Human pluripotent stem cell; Notch; Wnt

Indexed keywords

FRIZZLED PROTEIN; LIPOPROTEIN RECEPTOR; NOTCH RECEPTOR; NOTCH1 RECEPTOR; NOTCH2 RECEPTOR; NOTCH3 RECEPTOR; NOTCH4 RECEPTOR; SONIC HEDGEHOG PROTEIN; WNT PROTEIN;

ADULT STEM CELL; CELL DIFFERENTIATION; CELL FUNCTION; CELL RENEWAL; CELL SPECIFICITY; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; EX VIVO STUDY; GENE EXPRESSION REGULATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; LIGAND BINDING; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SPECIES COMPARISON;

ANIMALS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; HEDGEHOG PROTEINS; HUMANS; MODELS, BIOLOGICAL; PLURIPOTENT STEM CELLS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; WNT PROTEINS;

ERINACEIDAE; MUS;

EID: 77954844712     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.103067cc     Document Type: Review

References (151)

1. ALCEDO, J. and NOLL, M. (1997) Hedgehog and its patched-smoothened receptor complex: a novel signalling mechanism at the cell surface. Biol Chem 378: 583-590.
2. ASTER, J.C., PEAR, W.S. and BLACKLOW, S.C. (2008) Notch signaling in leukemia. Annu Rev Pathol 3: 587-613.
3. ATTAR, E.C. and SCADDEN, D.T. (2004) Regulation of hematopoietic stem cell growth. Leukemia 18: 1760-1768.
4. AVERY, S., INNISS, K. and MOORE, H. (2006) The regulation of self-renewal in human embryonic stem cells. Stem Cells Dev 15: 729-740.
5. AZA-BLANC, P. and KORNBERG, T.B. (1999) Ci: a complex transducer of the hedgehog signal. Trends Genet 15: 458-462.
6. BAI, L.Y., CHIU, C.F., LIN, C.W., HSU, N.Y., LIN, C.L., LO, W.J. and KAO, M.C. (2008) Differential expression of Sonic hedgehog and Gli1 in hematological malignancies. Leukemia 22: 226-228.
7. BARON, M.H. (2001) Molecular regulation of embryonic hematopoiesis and vascular development: a novel pathway. J Hematother Stem Cell Res 10: 587-594.
8. BARON, M.H. (2003) Embryonic origins of mammalian hematopoiesis. Exp Hematol 31: 1160-1169.
9. BENDALL, S.C., STEWART, M.H., MENENDEZ, P., GEORGE, D., VIJAYARAGAVAN, K., WERBOWETSKI-OGILVIE, T., RAMOS-MEJIA, V., ROULEAU, A., YANG, J., BOSSE, M., LAJOIE, G. and BHATIA, M. (2007) IGF and FGF cooperatively establish the regulatory stem cell niche of pluripotent human cells in vitro. Nature 448: 1015-1021.
10. BHARDWAJ, G., MURDOCH, B., WU, D., BAKER, D.P., WILLIAMS, K.P., CHADWICK, K., LING, L.E., KARANU, F.N. and BHATIA, M. (2001) Sonic hedgehog induces the proliferation of primitive human hematopoietic cells via BMP regulation. Nat Immunol 2: 172-180.
11. BIANCHI, D.W., WILKINS-HAUG, L.E., ENDERS, A.C. and HAY, E.D. 1993. Origin of extraembryonic mesoderm in experimental animals: relevance to chorionic mosaicism in humans. Am J Med Genet 46: 542-550.
12. BIGAS, A., MARTIN, D.I. and MILNER, L.A. (1998) Notch1 and Notch2 inhibit myeloid differentiation in response to different cytokines. Mol Cell Biol 18: 2324-2333.
13. BRAY, S.J. (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7: 678-689.
14. BYRD, N., BECKER, S., MAYE, P., NARASIMHAIAH, R., ST-JACQUES, B., ZHANG, X., MCMAHON, J., MCMAHON, A. and GRABEL, L. (2002) Hedgehog is required for murine yolk sac angiogenesis. Development 129: 361-372.
15. CARLESSO, N., ASTER, J.C., SKLAR, J. and SCADDEN, D.T. (1999) Notch1-induced delay of human hematopoietic progenitor cell differentiation is associated with altered cell cycle kinetics. Blood 93: 838-848.
16. CERDAN, C., ROULEAU, A. and BHATIA, M. (2004) VEGF-A165 augments erythropoietic development from human embryonic stem cells. Blood 103: 2504-2512.
17. CHADWICK, K., WANG, L., LI, L., MENENDEZ, P., MURDOCH, B., ROULEAU, A. and BHATIA, M. (2003) Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood 102: 906-915.
18. CHEN, X., XU, H., YUAN, P., FANG, F., HUSS, M., VEGA, V.B., WONG, E., ORLOV, Y.L., ZHANG, W., JIANG, J., LOH, Y.H., YEO, H.C., YEO, Z.X., NARANG, V., GOVINDARAJAN, K.R., LEONG, B., SHAHAB, A., RUAN, Y., BOURQUE, G., SUNG, W.K., CLARKE, N.D., WEI, C.L. and NG, H.H. (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133: 1106-1117.
19. CHENG, X., HUBER, T.L., CHEN, V.C., GADUE, P. and KELLER, G.M. (2008) Numb mediates the interaction between Wnt and Notch to modulate primitive erythropoietic specification from the hemangioblast. Development 135: 3447-3458.
20. CHIANG, C., LITINGTUNG, Y., LEE, E., YOUNG, K.E., CORDEN, J.L., WESTPHAL, H. and BEACHY, P.A. (1996) Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383: 407-413.
21. CHIBA, S. (2006) Notch signaling in stem cell systems. Stem Cells 24: 2437-2447.
22. CHOI, K., KENNEDY, M., KAZAROV, A., PAPADIMITRIOU, J.C. and KELLER, G. (1998) A common precursor for hematopoietic and endothelial cells. Development 125: 725-732.
23. DAHLQVIST, C., BLOKZIJL, A., CHAPMAN, G., FALK, A., DANNAEUS, K., IBANEZ, C.F. and LENDAHL, U. (2003) Functional Notch signaling is required for BMP4-induced inhibition of myogenic differentiation. Development 130: 6089-6099.
24. DAI, P., AKIMARU, H., TANAKA, Y., MAEKAWA, T., NAKAFUKU, M. and ISHII, S. (1999) Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J Biol Chem 274: 8143-8152.
25. DANDO, J.S., TAVIAN, M., CATELAIN, C., POIRAULT, S., BENNACEURGRISCELLI, A., SAINTENY, F., VAINCHENKER, W., PEAULT, B. and LAURET, E. (2005) Notch/Delta4 interaction in human embryonic liver CD34+ CD38-cells: positive influence on BFU-E production and LTC-IC potential maintenance. Stem Cells 23: 550-560.
26. DAVIS, R.L. and TURNER, D.L. (2001) Vertebrate hairy and Enhancer of split related proteins: transcriptional repressors regulating cellular differentiation and embryonic patterning. Oncogene 20: 8342-8357.
27. DE STROOPER, B., ANNAERT, W., CUPERS, P., SAFTIG, P., CRAESSAERTS, K., MUMM, J.S., SCHROETER, E.H., SCHRIJVERS, V., WOLFE, M.S., RAY, W.J., GOATE, A. and KOPAN, R. (1999) A presenilin-1-dependent gammasecretase-like protease mediates release of Notch intracellular domain. Nature 398: 518-522.
28. DESHPANDE, A.J. and BUSKE, C. (2007) Knocking the Wnt out of the sails of leukemia stem cell development. Cell Stem Cell 1: 597-598.
29. DICK, J.E., BHATIA, M., GAN, O., KAPP, U. and WANG, J.C. (1997) Assay of human stem cells by repopulation of NOD/SCID mice. Stem Cells 15 Suppl 1: 199-203; discussion 204-197.
30. DUNCAN, A.W., RATTIS, F.M., DIMASCIO, L.N., CONGDON, K.L., PAZIANOS, G., ZHAO, C., YOON, K., COOK, J.M., WILLERT, K., GAIANO, N. and REYA, T. (2005) Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat Immunol 6: 314-322.
31. DYER, M.A., FARRINGTON, S.M., MOHN, D., MUNDAY, J.R. and 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.
32. FOX, V., GOKHALE, P.J., WALSH, J.R., MATIN, M., JONES, M. and ANDREWS, P.W. (2008) Cell-cell signaling through NOTCH regulates human embryonic stem cell proliferation. Stem Cells 26: 715-723.
33. GADUE, P., HUBER, T.L., PADDISON, P.J. and KELLER, G.M. (2006) Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc Natl Acad Sci USA 103: 16806-16811.
34. GERING, M. and PATIENT, R. (2005) Hedgehog signaling is required for adult blood stem cell formation in zebrafish embryos. Dev Cell 8: 389-400.
35. GIEBEL, B. and BRUNS, I. (2008) Self-renewal versus differentiation in hematopoietic stem and progenitor cells: a focus on asymmetric cell divisions. Curr Stem Cell Res Ther 3: 9-16.
36. GRABHER, C., VON BOEHMER, H. and LOOK, A.T. (2006) Notch 1 activation in the molecular pathogenesis of T-cell acute lymphoblastic leukaemia. Nat Rev Cancer 6: 347-359.
37. GREWAL, S.S., BARKER, J.N., DAVIES, S.M. and WAGNER, J.E. (2003) Unrelated donor hematopoietic cell transplantation: marrow or umbilical cord blood? Blood 101: 4233-4244.
38. HADLAND, B.K., HUPPERT, S.S., KANUNGO, J., XUE, Y., JIANG, R., GRIDLEY, T., CONLON, R.A., CHENG, A.M., KOPAN, R. and LONGMORE, G.D. (2004) A requirement for Notch1 distinguishes 2 phases of definitive hematopoiesis during development. Blood 104: 3097-3105.
39. HAYASHI, K., LOPES, S.M., TANG, F. and SURANI, M.A. (2008) Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 3: 391-401.
40. HING, H.K., SUN, X. and ARTAVANIS-TSAKONAS, S. (1994) Modulation of wingless signaling by Notch in Drosophila. Mech Dev 47: 261-268.
41. HOCHMAN, E., KINSTON, S., HARMELIN, A., GOTTGENS, B. and IZRAELI, S. (2006) The SCL 3' enhancer responds to Hedgehog signaling during hemangioblast specification. Exp Hematol 34: 1643-1650.
42. HOOPER, J.E. (1994) Distinct pathways for autocrine and paracrine Wingless signalling in Drosophila embryos. Nature 372: 461-464.
43. HUBER, T.L., KOUSKOFF, V., FEHLING, H.J., PALIS, J. and KELLER, G. (2004) Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432: 625-630.
44. HUELSKEN, J., VOGEL, R., BRINKMANN, V., ERDMANN, B., BIRCHMEIER, C. and BIRCHMEIER, W. (2000) Requirement for beta-catenin in anterior-posterior axis formation in mice. J Cell Biol 148: 567-578.
45. HUPPERT, S.S., LE, A., SCHROETER, E.H., MUMM, J.S., SAXENA, M.T., MILNER, L.A. and KOPAN, R. (2000) Embryonic lethality in mice homozygous for a processing-deficient allele of Notch1. Nature 405: 966-970.
46. INGHAM, P.W. and MCMAHON, A.P. (2001) Hedgehog signaling in animal development: paradigms and principles. Genes Dev 15: 3059-3087.
47. ITOH, F., ITOH, S., GOUMANS, M.J., VALDIMARSDOTTIR, G., ISO, T., DOTTO, G.P., HAMAMORI, Y., KEDES, L., KATO, M. and TEN DIJKE PT, P. (2004) Synergy and antagonism between Notch and BMP receptor signaling pathways in endothelial cells. EMBO J 23: 541-551.
48. JAFFREDO, T., GAUTIER, R., BRAJEUL, V. and DIETERLEN-LIEVRE, F. (2000) Tracing the progeny of the aortic hemangioblast in the avian embryo. Dev Biol 224: 204-214.
49. JI, J., VIJAYARAGAVAN, K., BOSSE, M., WEISEL, K. and BHATIA, M. (2008) OP9 Stroma augments survival of hematopoietic precursors and progenitors during hematopoietic differentiation from human embryonic stem cells. Stem Cells 26: 2485-2495.
50. JIA, J., AMANAI, K., WANG, G., TANG, J., WANG, B. and JIANG, J. (2002) Shaggy/ GSK3 antagonizes Hedgehog signalling by regulating Cubitus interruptus. Nature 416: 548-552.
51. KARANU, F.N., MURDOCH, B., GALLACHER, L., WU, D.M., KOREMOTO, M., SAKANO, S. and BHATIA, M. (2000) The notch ligand jagged-1 represents a novel growth factor of human hematopoietic stem cells. J Exp Med 192: 1365-1372.
52. KARANU, F.N., MURDOCH, B., MIYABAYASHI, T., OHNO, M., KOREMOTO, M., GALLACHER, L., WU, D., ITOH, A., SAKANO, S. and BHATIA, M. (2001) Human homologues of Delta-1 and Delta-4 function as mitogenic regulators of primitive human hematopoietic cells. Blood 97: 1960-1967.
53. KARANU, F.N., YUEFEI, L., GALLACHER, L., SAKANO, S. and BHATIA, M. (2003) Differential response of primitive human CD34- and CD34+ hematopoietic cells to the Notch ligand Jagged-1. Leukemia 17: 1366-1374.
54. KELLY, O.G., PINSON, K.I. and SKARNES, W.C. (2004) The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 131: 2803-2815.
55. KENNEDY, M., D'SOUZA, S.L., LYNCH-KATTMAN, M., SCHWANTZ, S. and KELLER, G. (2007) Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood 109: 2679-2687.
56. KIMELMAN, D. and GRIFFIN, K.J. (2000) Vertebrate mesendoderm induction and patterning. Curr Opin Genet Dev 10: 350-356.
57. KIRSTETTER, P., ANDERSON, K., PORSE, B.T., JACOBSEN, S.E. and NERLOV, C. (2006) Activation of the canonical Wnt pathway leads to loss of hematopoietic stem cell repopulation and multilineage differentiation block. Nat Immunol 7: 1048-1056.
58. KLUMP, H., SCHIEDLMEIER, B. and BAUM, C. (2005) Control of self-renewal and differentiation of hematopoietic stem cells: HOXB4 on the threshold. Ann N Y Acad Sci 1044: 6-15.
59. KOCH, U., WILSON, A., COBAS, M., KEMLER, R., MACDONALD, H.R. and RADTKE, F. (2008) Simultaneous loss of beta- and gamma-catenin does not perturb hematopoiesis or lymphopoiesis. Blood 111: 160-164.
60. KOEBERNICK, K. and PIELER, T. (2002) Gli-type zinc finger proteins as bipotential transducers of Hedgehog signaling. Differentiation 70: 69-76.
61. KOHN, A.D. and MOON, R.T. (2005) Wnt and calcium signaling: beta-cateninindependent pathways. Cell Calcium 38: 439-446.
62. KREBS, L.T., SHUTTER, J.R., TANIGAKI, K., HONJO, T., STARK, K.L. and GRIDLEY, T. (2004) Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev 18: 2469-2473.
63. KUHL, M. (2002) Non-canonical Wnt signaling in Xenopus: regulation of axis formation and gastrulation. Semin Cell Dev Biol 13: 243-249.
64. KUMANO, K., CHIBA, S., KUNISATO, A., SATA, M., SAITO, T., NAKAGAMIYAMAGUCHI, E., YAMAGUCHI, T., MASUDA, S., SHIMIZU, K., TAKAHASHI, T., OGAWA, S., HAMADA, Y. and HIRAI, H. (2003) Notch1 but not Notch2 is essential for generating hematopoietic stem cells from endothelial cells. Immunity 18: 699-711.
65. KYBA, M., PERLINGEIRO, R.C. and DALEY, G.Q. (2002) HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell 109: 29-37.
66. LAKO, M., LINDSAY, S., LINCOLN, J., CAIRNS, P.M., ARMSTRONG, L. and HOLE, N. (2001) Characterisation of Wnt gene expression during the differentiation of murine embryonic stem cells in vitro: role of Wnt3 in enhancing haematopoietic differentiation. Mech Dev 103: 49-59.
67. LEDRAN, M.H., KRASSOWSKA, A., ARMSTRONG, L., DIMMICK, I., RENSTROM, J., LANG, R., YUNG, S., SANTIBANEZ-COREF, M., DZIERZAK, E., STOJKOVIC, M., OOSTENDORP, R.A., FORRESTER, L. and LAKO, M. (2008) Efficient hematopoietic differentiation of human embryonic stem cells on stromal cells derived from hematopoietic niches. Cell Stem Cell 3: 85-98.
68. LEE, G.S., KIM, B.S., SHEIH, J.H. and MOORE, M. (2008) Forced expression of HoxB4 enhances hematopoietic differentiation by human embryonic stem cells. Mol Cells 25: 487-493.
69. LENGERKE, C., SCHMITT, S., BOWMAN, T.V., JANG, I.H., MAOUCHE-CHRETIEN, L., MCKINNEY-FREEMAN, S., DAVIDSON, A.J., HAMMERSCHMIDT, M., RENTZSCH, F., GREEN, J.B., ZON, L.I. and DALEY, G.Q. (2008) BMP and Wnt specify hematopoietic fate by activation of the Cdx-Hox pathway. Cell Stem Cell 2: 72-82.
70. LITINGTUNG, Y., DAHN, R.D., LI, Y., FALLON, J.F. and CHIANG, C. (2002) Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature 418: 979-983.
71. LIU, P., WAKAMIYA, M., SHEA, M.J., ALBRECHT, U., BEHRINGER, R.R. and BRADLEY, A. (1999) Requirement for Wnt3 in vertebrate axis formation. Nat Genet 22: 361-365.
72. LOGAN, C.Y. and NUSSE, R. (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20: 781-810.
73. LU, S.J., FENG, Q., CABALLERO, S., CHEN, Y., MOORE, M.A., GRANT, M.B. and LANZA, R. (2007b) Generation of functional hemangioblasts from human embryonic stem cells. Nat Methods 4: 501-509.
74. LU, S.J., FENG, Q., IVANOVA, Y., LUO, C., LI, T., LI, F., HONIG, G.R. and LANZA, R. (2007a) Recombinant HoxB4 fusion proteins enhance hematopoietic differentiation of human embryonic stem cells. Stem Cells Dev 16: 547-559.
75. LU, X., BORCHERS, A.G., JOLICOEUR, C., RAYBURN, H., BAKER, J.C. and TESSIERLA-VIGNE, M. (2004) PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 430: 93-98.
76. LUM, L. and BEACHY, P.A. (2004) The Hedgehog response network: sensors, switches, and routers. Science 304: 1755-1759.
77. MAILLARD, I., KOCH, U., DUMORTIER, A., SHESTOVA, O., XU, L., SAI, H., PROSS, S.E., ASTER, J.C., BHANDOOLA, A., RADTKE, F. and PEAR, W.S. (2008) Canonical notch signaling is dispensable for the maintenance of adult hematopoietic stem cells. Cell Stem Cell 2: 356-366.
78. MALOOF, J.N., WHANGBO, J., HARRIS, J.M., JONGEWARD, G.D. and KENYON, C. (1999) A Wnt signaling pathway controls hox gene expression and neuroblast migration in C. elegans. Development 126: 37-49.
79. MANCINI, S.J., MANTEI, N., DUMORTIER, A., SUTER, U., MACDONALD, H.R. and RADTKE, F. (2005) Jagged1-dependent Notch signaling is dispensable for hematopoietic stem cell self-renewal and differentiation. Blood 105: 2340-2342.
80. MAYE, P., BECKER, S., KASAMEYER, E., BYRD, N. and GRABEL, L. (2000) Indian hedgehog signaling in extraembryonic endoderm and ectoderm differentiation in ES embryoid bodies. Mech Dev 94: 117-132.
81. MAZURIER, F., DOEDENS, M., GAN, O.I. and DICK, J.E. (2003) Rapid myeloerythroid repopulation after intrafemoral transplantation of NOD-SCID mice reveals a new class of human stem cells. Nat Med 9: 959-963.
82. MCKINNEY-FREEMAN, S.L. and DALEY, G.Q. (2007) Towards hematopoietic reconstitution from embryonic stem cells: a sanguine future. Curr Opin Hematol 14: 343-347.
83. MCMAHON, A.P., INGHAM, P.W. and TABIN, C.J. (2003) Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol 53: 1-114.
84. MENENDEZ, P., WANG, L. and BHATIA, M. (2005) Genetic manipulation of human embryonic stem cells: a system to study early human development and potential therapeutic applications. Curr Gene Ther 5: 375-385.
85. MERCHER, T., CORNEJO, M.G., SEARS, C., KINDLER, T., MOORE, S.A., MAILLARD, I., PEAR, W.S., ASTER, J.C. and GILLILAND, D.G. (2008) Notch signaling specifies megakaryocyte development from hematopoietic stem cells. Cell Stem Cell 3: 314-326.
86. MURDOCH, B., CHADWICK, K., MARTIN, M., SHOJAEI, F., SHAH, K.V., GALLACHER, L., MOON, R.T. and BHATIA, M. (2003) Wnt-5A augments repopulating capacity and primitive hematopoietic development of human blood stem cells in vivo. Proc Natl Acad Sci USA 100: 3422-3427.
87. MURDOCH, B., GALLACHER, L., CHADWICK, K., FELLOWS, F. and BHATIA, M. (2002) Human embryonic-derived hematopoietic repopulating cells require distinct factors to sustain in vivo repopulating function. Exp Hematol 30: 598-605.
88. NAITO, A.T., SHIOJIMA, I., AKAZAWA, H., HIDAKA, K., MORISAKI, T., KIKUCHI, A. and KOMURO, I. (2006) Developmental stage-specific biphasic roles of Wnt/ beta-catenin signaling in cardiomyogenesis and hematopoiesis. Proc Natl Acad Sci USA 103: 19812-19817.
89. NARAYAN, A.D., CHASE, J.L., LEWIS, R.L., TIAN, X., KAUFMAN, D.S., THOMSON, J.A. and ZANJANI, E.D. (2006) Human embryonic stem cell-derived hematopoietic cells are capable of engrafting primary as well as secondary fetal sheep recipients. Blood 107: 2180-2183.
90. NEMIR, M., CROQUELOIS, A., PEDRAZZINI, T. and RADTKE, F. (2006) Induction of cardiogenesis in embryonic stem cells via downregulation of Notch1 signaling. Circ Res 98: 1471-1478.
91. NISHIKAWA, S.I., NISHIKAWA, S., HIRASHIMA, M., MATSUYOSHI, N. and KODAMA, H. (1998) Progressive lineage analysis by cell sorting and culture identifies FLK1+VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages. Development 125: 1747-1757.
92. NOBTA, M., TSUKAZAKI, T., SHIBATA, Y., XIN, C., MORIISHI, T., SAKANO, S., SHINDO, H. and YAMAGUCHI, A. (2005) Critical regulation of bone morphogenetic protein-induced osteoblastic differentiation by Delta1/Jagged1-activated Notch1 signaling. J Biol Chem 280: 15842-15848.
93. NOGGLE, S.A., WEILER, D. and CONDIE, B.G. (2006) Notch signaling is inactive but inducible in human embryonic stem cells. Stem Cells 24: 1646-1653.
94. NOSTRO, M.C., CHENG, X., KELLER, G.M. and GADUE, P. (2008) Wnt, activin, and BMP signaling regulate distinct stages in the developmental pathway from embryonic stem cells to blood. Cell Stem Cell 2: 60-71.
95. NUSSE, R. (2008) Wnt signaling and stem cell control. Cell Res 18: 523-527.
96. OHISHI, K., VARNUM-FINNEY, B. and BERNSTEIN, I.D. (2002) Delta-1 enhances marrow and thymus repopulating ability of human CD34(+)CD38(-) cord blood cells. J Clin Invest 110: 1165-1174.
97. ORKIN, S.H. and ZON, L.I. (2002) Hematopoiesis and stem cells: plasticity versus developmental heterogeneity. Nat Immunol 3: 323-328.
98. PALAPARTI, A., BARATZ, A. and STIFANI, S. (1997) The Groucho/transducin-like enhancer of split transcriptional repressors interact with the genetically defined amino-terminal silencing domain of histone H3. J Biol Chem 272: 26604-26610.
99. PALIS, J. and YODER, M.C. (2001) Yolk-sac hematopoiesis: the first blood cells of mouse and man. Exp Hematol 29: 927-936.
100. PARK, I.H., ZHAO, R., WEST, J.A., YABUUCHI, A., HUO, H., INCE, T.A., LEROU, P.H., LENSCH, M.W. and DALEY, G.Q. (2008) Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451: 141-146.
101. PEARSON, S., SROCZYNSKA, P., LACAUD, G. and KOUSKOFF, V. (2008) The stepwise specification of embryonic stem cells to hematopoietic fate is driven by sequential exposure to Bmp4, activin A, bFGF and VEGF. Development 135: 1525-1535.
102. PETROPOULOS, K., ARSENI, N., SCHESSL, C., STADLER, C.R., RAWAT, V.P., DESHPANDE, A.J., HEILMEIER, B., HIDDEMANN, W., QUINTANILLAMARTINEZ, L., BOHLANDER, S.K., FEURING-BUSKE, M. and BUSKE, C. (2008) A novel role for Lef-1, a central transcription mediator of Wnt signaling, in leukemogenesis. J Exp Med 205: 515-522.
103. QIAN, Z., CHEN, L., FERNALD, A.A., WILLIAMS, B.O. and LE BEAU, M.M. (2008) A critical role for Apc in hematopoietic stem and progenitor cell survival. J Exp Med 205: 2163-2175.
104. RADTKE, F., WILSON, A. and MACDONALD, H.R. (2005) Notch signaling in hematopoiesis and lymphopoiesis: lessons from Drosophila. Bioessays 27: 1117-1128.
105. RADTKE, F., WILSON, A., MANCINI, S.J. and MACDONALD, H.R. (2004) Notch regulation of lymphocyte development and function. Nat Immunol 5: 247-253.
106. RADTKE, F., WILSON, A., STARK, G., BAUER, M., VAN MEERWIJK, J., MACDONALD, H.R. and AGUET, M. (1999) Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 10: 547-558.
107. REUBINOFF, B.E., PERA, M.F., FONG, C.Y., TROUNSON, A. and BONGSO, A. (2000) Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol 18: 399-404.
108. REYA, T. and CLEVERS, H. (2005) Wnt signalling in stem cells and cancer. Nature 434: 843-850.
109. REYA, T., DUNCAN, A.W., AILLES, L., DOMEN, J., SCHERER, D.C., WILLERT, K., HINTZ, L., NUSSE, R. and WEISSMAN, I.L. (2003) A role for Wnt signaling in self-renewal of haematopoietic stem cells. Nature 423: 409-414.
110. ROBERT-MORENO, A., GUIU, J., RUIZ-HERGUIDO, C., LOPEZ, M.E., INGLESESTEVE, J., RIERA, L., TIPPING, A., ENVER, T., DZIERZAK, E., GRIDLEY, T., ESPINOSA, L. and BIGAS, A. (2008) Impaired embryonic haematopoiesis yet normal arterial development in the absence of the Notch ligand Jagged1. EMBO J 27: 1886-1895.
111. RODAWAY, A. and PATIENT, R. (2001) Mesendoderm. an ancient germ layer? Cell 105: 169-172.
112. SADLON, T.J., LEWIS, I.D. and D'ANDREA, R.J. (2004) BMP4: its role in development of the hematopoietic system and potential as a hematopoietic growth factor. Stem Cells 22: 457-474.
113. SAITO, T., CHIBA, S., ICHIKAWA, M., KUNISATO, A., ASAI, T., SHIMIZU, K., YAMAGUCHI, T., YAMAMOTO, G., SEO, S., KUMANO, K., NAKAGAMIYAMAGUCHI, E., HAMADA, Y., AIZAWA, S. and HIRAI, H. (2003) Notch2 is preferentially expressed in mature B cells and indispensable for marginal zone B lineage development. Immunity 18: 675-685.
114. SCHELLER, M., HUELSKEN, J., ROSENBAUER, F., TAKETO, M.M., BIRCHMEIER, W., TENEN, D.G. and LEUTZ, A. (2006) Hematopoietic stem cell and multilineage defects generated by constitutive beta-catenin activation. Nat Immunol 7: 1037-1047.
115. SCHROEDER, T., MEIER-STIEGEN, F., SCHWANBECK, R., EILKEN, H., NISHIKAWA, S., HASLER, R., SCHREIBER, S., BORNKAMM, G.W. and JUST, U. (2006) Activated Notch1 alters differentiation of embryonic stem cells into mesodermal cell lineages at multiple stages of development. Mech Dev 123: 570-579.
116. SENGUPTA, A., BANERJEE, D., CHANDRA, S., BANERJI, S.K., GHOSH, R., ROY, R. and BANERJEE, S. (2007) Deregulation and cross talk among Sonic hedgehog, Wnt, Hox and Notch signaling in chronic myeloid leukemia progression. Leukemia 21: 949-955.
117. SINHA, S. and CHEN, J.K. (2006) Purmorphamine activates the Hedgehog pathway by targeting Smoothened. Nat Chem Biol 2: 29-30.
118. STECCA, B. and RUIZIALTABA, A. (2002) The therapeutic potential of modulators of the Hedgehog-Gli signaling pathway. J Biol 1: 9.
119. STEWART, M.H., BOSSE, M., CHADWICK, K., MENENDEZ, P., BENDALL, S.C. and BHATIA, M. (2006) Clonal isolation of hESCs reveals heterogeneity within the pluripotent stem cell compartment. Nat Methods 3: 807-815.
120. SUMI, T., TSUNEYOSHI, N., NAKATSUJI, N. and SUEMORI, H. (2008) Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/beta-catenin, Activin/Nodal and BMP signaling. Development 135: 2969-2979.
121. TAIPALE, J., CHEN, J.K., COOPER, M.K., WANG, B., MANN, R.K., MILENKOVIC, L., SCOTT, M.P. and BEACHY, P.A. (2000) Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 406: 1005-1009.
122. TAIPALE, J., COOPER, M.K., MAITI, T. and BEACHY, P.A. (2002) Patched acts catalytically to suppress the activity of Smoothened. Nature 418: 892-897.
123. TAKAHASHI, K. and YAMANAKA, S. (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
124. TAKIZAWA, T., OCHIAI, W., NAKASHIMA, K. and TAGA, T. (2003) Enhanced gene activation by Notch and BMP signaling cross-talk. Nucleic Acids Res 31: 5723-5731.
125. TAVIAN, M., ROBIN, C., COULOMBEL, L. and PEAULT, B. (2001) The human embryo, but not its yolk sac, generates lympho-myeloid stem cells: mapping multipotent hematopoietic cell fate in intraembryonic mesoderm. Immunity 15: 487-495.
126. THOMSON, J.A., ITSKOVITZ-ELDOR, J., SHAPIRO, S.S., WAKNITZ, M.A., SWIERGIEL, J.J., MARSHALL, V.S. and JONES, J.M. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147.
127. TIAN, X. and KAUFMAN, D.S. (2008) Hematopoietic development of human embryonic stem cells in culture. Methods Mol Biol 430: 119-133.
128. TIAN, X., WOLL, P.S., MORRIS, J.K., LINEHAN, J.L. and KAUFMAN, D.S. (2006) Hematopoietic engraftment of human embryonic stem cell-derived cells is regulated by recipient innate immunity. Stem Cells 24: 1370-1380.
129. TROWBRIDGE, J.J., SCOTT, M.P. and BHATIA, M. (2006a) Hedgehog modulates cell cycle regulators in stem cells to control hematopoietic regeneration. Proc Natl Acad Sci USA 103: 14134-14139.
130. TROWBRIDGE, J.J., XENOCOSTAS, A., MOON, R.T. and BHATIA, M. (2006b) Glycogen synthase kinase-3 is an in vivo regulator of hematopoietic stem cell repopulation. Nat Med 12: 89-98.
131. UUSITALO, M., HEIKKILA, M. and VAINIO, S. (1999) Molecular genetic studies of Wnt signaling in the mouse. Exp Cell Res 253: 336-348.
132. VAN DEN BERG, D.J., SHARMA, A.K., BRUNO, E. and HOFFMAN, R. (1998) Role of members of the Wnt gene family in human hematopoiesis. Blood 92: 3189-3202.
133. VARNUM-FINNEY, B., PURTON, L.E., YU, M., BRASHEM-STEIN, C., FLOWERS, D., STAATS, S., MOORE, K.A., LE ROUX, I., MANN, R., GRAY, G., ARTAVANISTSAKONAS, S. and BERNSTEIN, I.D. (1998) The Notch ligand, Jagged-1, influences the development of primitive hematopoietic precursor cells. Blood 91: 4084-4091.
134. VIJAYARAGAVAN, K., SZABO, E., BOSSE, M., RAMOS-MEJIA, V., MOON, R.T. and BHATIA, M. (2009) Noncanonical Wnt signaling orchestrates early developmental events toward hematopoietic cell fate from human embryonic stem cells. Cell Stem Cell 4: 248-262.
135. VILLAVICENCIO, E.H., WALTERHOUSE, D.O. and IANNACCONE, P.M. (2000) The sonic hedgehog-patched-gli pathway in human development and disease. Am J Hum Genet 67: 1047-1054.
136. WANG, B., FALLON, J.F. and BEACHY, P.A. (2000) Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100: 423-434.
137. WANG, H., GILNER, J.B., BAUTCH, V.L., WANG, D.Z., WAINWRIGHT, B.J., KIRBY, S.L. and PATTERSON, C. (2007) Wnt2 coordinates the commitment of mesoderm to hematopoietic, endothelial, and cardiac lineages in embryoid bodies. J Biol Chem 282: 782-791.
138. WANG, L., LI, L., MENENDEZ, P., CERDAN, C. and BHATIA, M. (2005d) Human embryonic stem cells maintained in the absence of mouse embryonic fibroblasts or conditioned media are capable of hematopoietic development. Blood 105: 4598-4603.
139. WANG, L., LI, L., SHOJAEI, F., LEVAC, K., CERDAN, C., MENENDEZ, P., MARTIN, T., ROULEAU, A. and BHATIA, M. (2004) Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity 21: 31-41.
140. WANG, L., MENENDEZ, P., CERDAN, C. and BHATIA, M. (2005c) Hematopoietic development from human embryonic stem cell lines. Exp Hematol 33: 987-996.
141. WANG, L., MENENDEZ, P., SHOJAEI, F., LI, L., MAZURIER, F., DICK, J.E., CERDAN, C., LEVAC, K. and BHATIA, M. (2005b) Generation of hematopoietic repopulating cells from human embryonic stem cells independent of ectopic HOXB4 expression. J Exp Med 201: 1603-1614.
142. WANG, Y., YATES, F., NAVEIRAS, O., ERNST, P. and DALEY, G.Q. (2005a) Embryonic stem cell-derived hematopoietic stem cells. Proc Natl Acad Sci USA 102: 19081-19086.
143. WILLERT, K., BROWN, J.D., DANENBERG, E., DUNCAN, A.W., WEISSMAN, I.L., REYA, T., YATES, J.R.: 3RD and NUSSE, R. (2003) Wnt proteins are lipidmodified and can act as stem cell growth factors. Nature 423: 448-452.
144. WODARZ, A. and NUSSE, R. (1998) Mechanisms of Wnt signaling in development. Annu Rev Cell Dev Biol 14: 59-88.
145. WOLL, P.S., MORRIS, J.K., PAINSCHAB, M.S., MARCUS, R.K., KOHN, A.D., BIECHELE, T.L., MOON, R.T. and KAUFMAN, D.S. (2008) Wnt signaling promotes hematoendothelial cell development from human embryonic stem cells. Blood 111: 122-131.
146. WU, C.H. and NUSSE, R. (2002) Ligand receptor interactions in the Wnt signaling pathway in Drosophila. J Biol Chem 277: 41762-41769.
147. XUE, Y., GAO, X., LINDSELL, C.E., NORTON, C.R., CHANG, B., HICKS, C., GENDRON-MAGUIRE, M., RAND, E.B., WEINMASTER, G. and GRIDLEY, T. (1999) Embryonic lethality and vascular defects in mice lacking the Notch ligand Jagged1. Hum Mol Genet 8: 723-730.
148. YU, J. and THOMSON, J.A. (2008) Pluripotent stem cell lines. Genes Dev 22: 1987-1997.
149. YU, J., VODYANIK, M.A., SMUGA-OTTO, K., ANTOSIEWICZ-BOURGET, J., FRANE, J.L., TIAN, S., NIE, J., JONSDOTTIR, G.A., RUOTTI, V., STEWART, R., SLUKVIN, II and THOMSON, J.A. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
150. YU, X., ZOU, J., YE, Z., HAMMOND, H., CHEN, G., TOKUNAGA, A., MALI, P., LI, Y.M., CIVIN, C., GAIANO, N. and CHENG, L. (2008) Notch signaling activation in human embryonic stem cells is required for embryonic, but not trophoblastic, lineage commitment. Cell Stem Cell 2: 461-471.
151. ZAMBIDIS, E.T., PEAULT, B., PARK, T.S., BUNZ, F. and CIVIN, C.I. (2005) Hematopoietic differentiation of human embryonic stem cells progresses through sequential hematoendothelial, primitive, and definitive stages resembling human yolk sac development. Blood 106: 860-870.