Mapping mouse hemangioblast maturation from headfold stages

Developmental Biology

Volumn 365, Issue 1, 2012, Pages 1-13

  Rhee, Jerry M ^a   Iannaccone, Philip M ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Cross antagonism; GATA1; Hemangioblast; HoxB4; HSC; Posterior primitive streak

Indexed keywords

HOX PROTEIN; PROTEIN HOXB4; SMAD1 PROTEIN; SMAD5 PROTEIN; TRANSCRIPTION FACTOR GATA 1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; AORTA; BLOOD CELL; CELL ADHESION; CELL FATE; CELL MATURATION; DEVELOPMENTAL STAGE; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; FETUS LIVER; FETUS MEMBRANE; GONAD; HEADFOLD STAGE; HEMANGIOBLAST; HEMATOPOIETIC STEM CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MESONEPHROS; MOUSE; NEUROECTODERM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION;

EID: 84859431482     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.02.023     Document Type: Review

References (164)

1. Adelman C.A., Chattopadhyay S., Bieker J.J. The BMP/BMPR/Smad pathway directs expression of the erythroid-specific EKLF and GATA1 transcription factors during embryoid body differentiation in serum-free media. Development 2002, 129:539-549.
2. Allen G.E. A pact with the embryo: Viktor Hamburger, holistic and mechanistic philosophy in the development of neuroembryology, 1927-1955. J. Hist. Biol. 2004, 37:421-475.
3. Arinobu Y., Mizuno S., Chong Y., Shigematsu H., Iino T., Iwasaki H., Graf T., Mayfield R., Chan S., Kastner P., Akashi K. Reciprocal activation of GATA-1 and PU.1 marks initial specification of hematopoietic stem cells into myeloerythroid and myelolymphoid lineages. Cell Stem Cell 2007, 1:416-427.
4. Astorga J., Carlsson P. Hedgehog induction of murine vasculogenesis is mediated by Foxf1 and Bmp4. Development 2007, 134:3753-3761.
5. Bak P., Chen K. Self-organized criticality. Sci. Am. 1991, 264:46-53.
6. Beck R.N. Overview of imaging science. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:9746-9750.
7. Belaoussoff M., Farrington S.M., Baron M.H. Hematopoietic induction and respecification of A-P identity by visceral endoderm signaling in the mouse embryo. Development 1998, 125:5009-5018.
8. Belmont A.S., Dietzel S., Nye A.C., Strukov Y.G., Tumbar T. Large-scale chromatin structure and function. Curr. Opin. Cell Biol. 1999, 11:307-311.
9. Bertalanffy L.V. An essay on the relativity of categories. Philos. Sci. 1955, 22:243-263.
10. Boisset J.C., van Cappellen W., Andrieu-Soler C., Galjart N., Dzierzak E., Robin C. In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 2010, 464:116-120.
11. Bonnevie K. New facts on mesoderm formation and proamnion derivatives in the normal mouse embryo. J. Morphol. 1950, 86:495-545.
12. Borner K., Contractor N., Falk-Krzesinski H.J., Fiore S.M., Hall K.L., Keyton J., Spring B., Stokols D., Trochim W., Uzzi B. A multi-level systems perspective for the science of team science. Sci. Transl. Med. 2010, 2:49cm24.
13. Boyes J., Byfield P., Nakatani Y., Ogryzko V. Regulation of activity of the transcription factor GATA-1 by acetylation. Nature 1998, 396:594-598.
14. Brons I.G., Smithers L.E., Trotter M.W., Rugg-Gunn P., Sun B., de Sousa Chuva, Lopes S.M., Howlett S.K., Clarkson A., Ahrlund-Richter L., Pedersen R.A., Vallier L. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 2007, 448:191-195.
15. Burdsal C.A., Damsky C.H., Pedersen R.A. The role of E-cadherin and integrins in mesoderm differentiation and migration at the mammalian primitive streak. Development 1993, 118:829-844.
16. Byrd N., Becker S., Maye P., Narasimhaiah R., St-Jacques B., Zhang X., McMahon J., McMahon A., Grabel L. Hedgehog is required for murine yolk sac angiogenesis. Development 2002, 129:361-372.
17. Cantor A.B., Orkin S.H. Hematopoietic development: a balancing act. Curr. Opin. Genet. Dev. 2001, 11:513-519.
18. Carmeliet P., Ferreira V., Breier G., Pollefeyt S., Kieckens L., Gertsenstein M., Fahrig M., Vandenhoeck A., Harpal K., Eberhardt C., Declercq C., Pawling J., Moons L., Collen D., Risau W., Nagy A. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996, 380:435-439.
19. Chan R.J., Yoder M.C. The multiple facets of hematopoietic stem cells. Curr. Neurovasc. Res. 2004, 1:197-206.
20. Chang H., Huylebroeck D., Verschueren K., Guo Q., Matzuk M.M., Zwijsen A. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development 1999, 126:1631-1642.
21. Chen L., Yabuuchi A., Eminli S., Takeuchi A., Lu C.W., Hochedlinger K., Daley G.Q. Cross-regulation of the Nanog and Cdx2 promoters. Cell Res. 2009, 19:1052-1061.
22. Chen M.J., Li Y., De Obaldia M.E., Yang Q., Yzaguirre A.D., Yamada-Inagawa T., Vink C.S., Bhandoola A., Dzierzak E., Speck N.A. Erythroid/myeloid progenitors and hematopoietic stem cells originate from distinct populations of endothelial cells. Cell Stem Cell 2011, 9:541-552.
23. Choe S.K., Lu P., Nakamura M., Lee J., Sagerstrom C.G. Meis cofactors control HDAC and CBP accessibility at Hox-regulated promoters during zebrafish embryogenesis. Dev. Cell 2009, 17:561-567.
24. Ciruna B., Rossant J. FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Dev. Cell 2001, 1:37-49.
25. Coller B.S., Shattil S.J. The GPIIb/IIIa (integrin alphaIIbbeta3) odyssey: a technology-driven saga of a receptor with twists, turns, and even a bend. Blood 2008, 112:3011-3025.
26. Cook B.D., Liu S., Evans T. Smad1 signaling restricts hematopoietic potential after promoting hemangioblast commitment. Blood 2011, 117:6489-6497.
27. Corbel C., Salaun J., Belo-Diabangouaya P., Dieterlen-Lievre F. Hematopoietic potential of the pre-fusion allantois. Dev. Biol. 2007, 301:478-488.
28. Coultas L., Chawengsaksophak K., Rossant J. Endothelial cells and VEGF in vascular development. Nature 2005, 438:937-945.
29. Cremer T., Kupper K., Dietzel S., Fakan S. Higher order chromatin architecture in the cell nucleus: on the way from structure to function. Biol. Cell 2004, 96:555-567.
30. Daane J.M., Downs K.M. Hedgehog signaling in the posterior region of the mouse gastrula suggests manifold roles in the fetal-umbilical connection and posterior morphogenesis. Dev. Dyn. 2011, 240:2175-2193.
31. Daane J.M., Enders A.C., Downs K.M. Mesothelium of the murine allantois exhibits distinct regional properties. J. Morphol. 2011, 272:536-556.
32. Danchakoff V. Development of the haematopoetic organs and regeneration of the blood cells from the standpoint of the monophyletic school. Anat. Rec. 1916, 10:397-416.
33. de Sousa Lopes S.M., Roelen B.A., Monteiro R.M., Emmens R., Lin H.Y., Li E., Lawson K.A., Mummery C.L. BMP signaling mediated by ALK2 in the visceral endoderm is necessary for the generation of primordial germ cells in the mouse embryo. Genes Dev. 2004, 18:1838-1849.
34. Deng W., Blobel G.A. Do chromatin loops provide epigenetic gene expression states?. Curr. Opin. Genet. Dev. 2010, 20:548-554.
35. Deschamps J., van Nes J. Developmental regulation of the Hox genes during axial morphogenesis in the mouse. Development 2005, 132:2931-2942.
36. Dobreva M.P., Pereira P.N., Deprest J., Zwijsen A. On the origin of amniotic stem cells: of mice and men. Int. J. Dev. Biol. 2010, 54:761-777.
37. Downs K.M. Florence Sabin and the mechanism of blood vessel lumenization during vasculogenesis. Microcirculation 2003, 10:5-25.
38. Downs K.M. The enigmatic primitive streak: prevailing notions and challenges concerning the body axis of mammals. Bioessays 2009, 31:892-902.
39. Downs K.M. Lineage commitments: emphasis on embryonic-extraembryonic interfaces. EMBO Rep. 2011, 12:987-990.
40. Downs K.M., Davies T. Staging of gastrulating mouse embryos by morphological landmarks in the dissecting microscope. Development 1993, 118:1255-1266.
41. Downs K.M., Inman K.E., Jin D.X., Enders A.C. The allantoic core domain: new insights into development of the murine allantois and its relation to the primitive streak. Dev. Dyn. 2009, 238:532-553.
42. Dyer M.A., Farrington S.M., Mohn D., Munday J.R., Baron M.H. Indian hedgehog activates hematopoiesis and vasculogenesis and can respecify prospective neurectodermal cell fate in the mouse embryo. Development 2001, 128:1717-1730.
43. Dzierzak E., Speck N.A. Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat. Immunol. 2008, 9:129-136.
44. Eilken H.M., Nishikawa S., Schroeder T. Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature 2009, 457:896-900.
45. Ema M., Rossant J. Cell fate decisions in early blood vessel formation. Trends Cardiovasc. Med. 2003, 13:254-259.
46. Ema M., Faloon P., Zhang W.J., Hirashima M., Reid T., Stanford W.L., Orkin S., Choi K., Rossant J. Combinatorial effects of Flk1 and Tal1 on vascular and hematopoietic development in the mouse. Genes Dev. 2003, 17:380-393.
47. Ema M., Yokomizo T., Wakamatsu A., Terunuma T., Yamamoto M., Takahashi S. Primitive erythropoiesis from mesodermal precursors expressing VE-cadherin, PECAM-1, Tie2, endoglin, and CD34 in the mouse embryo. Blood 2006, 108:4018-4024.
48. Epstein J. Why model?. J. Artif. Soc. Soc. Simul. 2008, 11:12.
49. Ferkowicz M.J., Yoder M.C. Blood island formation: longstanding observations and modern interpretations. Exp. Hematol. 2005, 33:1041-1047.
50. Ferkowicz M.J., Starr M., Xie X., Li W., Johnson S.A., Shelley W.C., Morrison P.R., Yoder M.C. CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo. Development 2003, 130:4393-4403.
51. Forlani S., Lawson K.A., Deschamps J. Acquisition of Hox codes during gastrulation and axial elongation in the mouse embryo. Development 2003, 130:3807-3819.
52. Fox D.T., Morris L.X., Nystul T., Spradling A.C. Lineage analysis of stem cells. StemBook 2009.
53. Fujiwara T., Dunn N.R., Hogan B.L. Bone morphogenetic protein 4 in the extraembryonic mesoderm is required for allantois development and the localization and survival of primordial germ cells in the mouse. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:13739-13744.
54. Fukuda T., Scott G., Komatsu Y., Araya R., Kawano M., Ray M.K., Yamada M., Mishina Y. Generation of a mouse with conditionally activated signaling through the BMP receptor, ALK2. Genesis 2006, 44:159-167.
55. Gardner R.L. Clonal analysis of early mammalian development. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1985, 312:163-178.
56. Gilbert S.F. Epigenetic landscaping: Waddington's use of cell fate bifurcation diagrams. Biology and Philosophy 1991, 6:135-154.
57. Gilbert S.F. All I really needed to know I learned during gastrulation. CBE Life Sci. Educ. 2008, 7:12-13.
58. Gould A., Morrison A., Sproat G., White R.A., Krumlauf R. Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Genes Dev. 1997, 11:900-913.
59. Gould A., Itasaki N., Krumlauf R. Initiation of rhombomeric Hoxb4 expression requires induction by somites and a retinoid pathway. Neuron 1998, 21:39-51.
60. Graf T., Enver T. Forcing cells to change lineages. Nature 2009, 462:587-594.
61. Hamill K.J., Kligys K., Hopkinson S.B., Jones J.C. Laminin deposition in the extracellular matrix: a complex picture emerges. J. Cell Sci. 2009, 122:4409-4417.
62. Hemberger M., Dean W., Reik W. Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington's canal. Nat. Rev. Mol. Cell Biol. 2009, 10:526-537.
63. Hilliard J.E., Lawson L.R. Stereology and Stochastic Geometry 2003, Kluwer Academic Publishers.
64. Hills D., Gribi R., Ure J., Buza-Vidas N., Luc S., Jacobsen S.E., Medvinsky A. Hoxb4-YFP reporter mouse model: a novel tool for tracking HSC development and studying the role of Hoxb4 in hematopoiesis. Blood 2010, 13:3521-3528.
65. Hong S., Troyanovsky R.B., Troyanovsky S.M. Spontaneous assembly and active disassembly balance adherens junction homeostasis. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3528-3533.
66. Huang S. Reprogramming cell fates: reconciling rarity with robustness. Bioessays 2009, 31:546-560.
67. Huang S., Guo Y.P., May G., Enver T. Bifurcation dynamics in lineage-commitment in bipotent progenitor cells. Dev. Biol. 2007, 305:695-713.
68. Huber T.L., Kouskoff V., Fehling H.J., Palis J., Keller G. Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 2004, 432:625-630.
69. Jing H., Vakoc C.R., Ying L., Mandat S., Wang H., Zheng X., Blobel G.A. Exchange of GATA factors mediates transitions in looped chromatin organization at a developmentally regulated gene locus. Mol. Cell 2008, 29:232-242.
70. Joshi R., Passner J.M., Rohs R., Jain R., Sosinsky A., Crickmore M.A., Jacob V., Aggarwal A.K., Honig B., Mann R.S. Functional specificity of a Hox protein mediated by the recognition of minor groove structure. Cell 2007, 131:530-543.
71. Kan N.G., Stemmler M.P., Junghans D., Kanzler B., de Vries W.N., Dominis M., Kemler R. Gene replacement reveals a specific role for E-cadherin in the formation of a functional trophectoderm. Development 2007, 134:31-41.
72. Kattman S.J., Witty A.D., Gagliardi M., Dubois N.C., Niapour M., Hotta A., Ellis J., Keller G. Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell 2011, 8:228-240.
73. Kiel M.J., Yilmaz O.H., Iwashita T., Terhorst C., Morrison S.J. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 2005, 121:1109-1121.
74. Kim I., He S., Yilmaz O.H., Kiel M.J., Morrison S.J. Enhanced purification of fetal liver hematopoietic stem cells using SLAM family receptors. Blood 2006, 108:737-744.
75. Kinder S.J., Tsang T.E., Quinlan G.A., Hadjantonakis A.K., Nagy A., Tam P.P. The orderly allocation of mesodermal cells to the extraembryonic structures and the anteroposterior axis during gastrulation of the mouse embryo. Development 1999, 126:4691-4701.
76. Koestler A. Beyond atomism and holism - the concept of the holon. New Perspectives in the Life Sciences 1969, 192-232. The Macmillan Company. A. Smythies (Ed.).
77. Krumlauf R. Hox genes in vertebrate development. Cell 1994, 78:191-201.
78. Kumaravelu P., Hook L., Morrison A.M., Ure J., Zhao S., Zuyev S., Ansell J., 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 2002, 129:4891-4899.
79. Kurimoto K., Saitou M. Single-cell cDNA microarray profiling of complex biological processes of differentiation. Curr. Opin. Genet. Dev. 2010, 20:470-477.
80. Kyba M., Perlingeiro R.C., Daley G.Q. HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell 2002, 109:29-37.
81. Lancrin C., Sroczynska P., Stephenson C., Allen T., Kouskoff V., Lacaud G. The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage. Nature 2009, 457:892-895.
82. Laursen L. Computational biology: biological logic. Nature 2009, 462:408-410.
83. Lawson K.A., Meneses J.J., Pedersen R.A. Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 1991, 113:891-911.
84. Lawson K.A., Dunn N.R., Roelen B.A., Zeinstra L.M., Davis A.M., Wright C.V., Korving J.P., Hogan B.L. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 1999, 13:424-436.
85. Letting D.L., Rakowski C., Weiss M.J., Blobel G.A. Formation of a tissue-specific histone acetylation pattern by the hematopoietic transcription factor GATA-1. Mol. Cell. Biol. 2003, 23:1334-1340.
86. Lieberman-Aiden E., van Berkum N.L., Williams L., Imakaev M., Ragoczy T., Telling A., Amit I., Lajoie B.R., Sabo P.J., Dorschner M.O., Sandstrom R., Bernstein B., Bender M.A., Groudine M., Gnirke A., Stamatoyannopoulos J., Mirny L.A., Lander E.S., Dekker J. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009, 326:289-293.
87. Mann R.S., Affolter M. Hox proteins meet more partners. Curr. Opin. Genet. Dev. 1998, 8:423-429.
88. Massague J., Seoane J., Wotton D. Smad transcription factors. Genes Dev. 2005, 19:2783-2810.
89. Matsuoka S., Tsuji K., Hisakawa H., Xu M., Ebihara Y., Ishii T., Sugiyama D., Manabe A., Tanaka R., Ikeda Y., Asano S., Nakahata T. Generation of definitive hematopoietic stem cells from murine early yolk sac and paraaortic splanchnopleures by aorta-gonad-mesonephros region-derived stromal cells. Blood 2001, 98:6-12.
90. McLaren A. Primordial germ cells in the mouse. Dev. Biol. 2003, 262:1-15.
91. Medvinsky A., Rybtsov S., Taoudi S. Embryonic origin of the adult hematopoietic system: advances and questions. Development 2011, 138:1017-1031.
92. Mikedis M.M., Downs K.M. Collagen type IV and Perlecan exhibit dynamic localization in the allantoic core domain, a putative stem cell niche in the murine allantois. Dev. Dyn. 2009, 238:3193-3204.
93. Mikedis M.M., Downs K.M. STELLA-positive subregions of the primitive streak contribute to posterior tissues of the mouse gastrula. Dev. Biol. 2011, 363:201-218.
94. Mikkola H.K., Fujiwara Y., Schlaeger T.M., Traver D., Orkin S.H. Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo. Blood 2003, 101:508-516.
95. Miquerol L., Gertsenstein M., Harpal K., Rossant J., Nagy A. Multiple developmental roles of VEGF suggested by a LacZ-tagged allele. Dev. Biol. 1999, 212:307-322.
96. Misteli T. Higher-order genome organization in human disease. Cold Spring Harb. Perspect. Biol. 2010, 2:a000794.
97. Mitiku N., Baker J.C. Genomic analysis of gastrulation and organogenesis in the mouse. Dev. Cell 2007, 13:897-907.
98. Morita Y., Ema H., Nakauchi H. Heterogeneity and hierarchy within the most primitive hematopoietic stem cell compartment. J. Exp. Med. 2010, 207:1173-1182.
99. Murray P.D.F. The development in vitro of the blood of the early chick embryo. Proceedings of the Royal Society of London. Series B 1932, 111:497-521.
100. Newman P.J., Newman D.K. Signal transduction pathways mediated by PECAM-1: new roles for an old molecule in platelet and vascular cell biology. Arterioscler. Thromb. Vasc. Biol. 2003, 23:953-964.
101. Niwa H., Toyooka Y., Shimosato D., Strumpf D., Takahashi K., Yagi R., Rossant J. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 2005, 123:917-929.
102. Orkin S.H., Zon L.I. Genetics of erythropoiesis: induced mutations in mice and zebrafish. Annu. Rev. Genet. 1997, 31:33-60.
103. Ottino J. The art of mixing with an admixture of art: fluids, solids, and visual imagination. Physics of Fluids 2010, 22:12.
104. Park C., Afrikanova I., Chung Y.S., Zhang W.J., Arentson E., Fong Gh G., Rosendahl A., Choi K. A hierarchical order of factors in the generation of FLK1- and SCL-expressing hematopoietic and endothelial progenitors from embryonic stem cells. Development 2004, 131:2749-2762.
105. Pilat S., Carotta S., Schiedlmeier B., Kamino K., Mairhofer A., Will E., Modlich U., Steinlein P., Ostertag W., Baum C., Beug H., Klump H. HOXB4 enforces equivalent fates of ES-cell-derived and adult hematopoietic cells. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12101-12106.
106. Pineault N., Helgason C.D., Lawrence H.J., Humphries R.K. Differential expression of Hox, Meis1, and Pbx1 genes in primitive cells throughout murine hematopoietic ontogeny. Exp. Hematol. 2002, 30:49-57.
107. Plusa B., Piliszek A., Frankenberg S., Artus J., Hadjantonakis A.K. Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 2008, 135:3081-3091.
108. Powell K. Stem-cell niches: it's the ecology, stupid!. Nature 2005, 435:268-270.
109. Rakeman A.S., Anderson K.V. Axis specification and morphogenesis in the mouse embryo require Nap1, a regulator of WAVE-mediated actin branching. Development 2006, 133:3075-3083.
110. Rakic P. Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 2009, 10:724-735.
111. Riedl R. Order in Living Organisms: A Systems Analysis of Evolution. A Wiley-Interscience Publication 1978, 58-59. Wiley, Chichester; New York.
112. Robb L., Lyons I., Li R., Hartley L., Kontgen F., Harvey R.P., Metcalf D., Begley C.G. Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:7075-7079.
113. Robertson L., Joyner A. An interview with Alex Joyner and Liz Robertson: development editors at the helm of Developmental Biology Societies. Development 2010, 137:2075-2077.
114. Roeder I., Radtke F. Stem cell biology meets systems biology. Development 2009, 136:3525-3530.
115. Ronneberger O., Baddeley D., Scheipl F., Verveer P.J., Burkhardt H., Cremer C., Fahrmeir L., Cremer T., Joffe B. Spatial quantitative analysis of fluorescently labeled nuclear structures: problems, methods, pitfalls. Chromosome Res. 2008, 16:523-562.
116. Sabin F.R. On the origin of the cells of the blood. Physiol. Rev. 1922, 2:38-69.
117. Sabin F.R. Preliminary note on the differentiation of angioblasts and the method by which they produce blood-vessels, blood-plasma and red blood-cells as seen in the living chick. 1917. J. Hematother. Stem Cell Res. 2002, 11:5-7.
118. Saitou M., Yamaji M. Germ cell specification in mice: signaling, transcription regulation, and epigenetic consequences. Reproduction 2010, 139:931-942.
119. Schermelleh L., Carlton P.M., Haase S., Shao L., Winoto L., Kner P., Burke B., Cardoso M.C., Agard D.A., Gustafsson M.G., Leonhardt H., Sedat J.W. Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 2008, 320:1332-1336.
120. Scott M.P. Vertebrate homeobox gene nomenclature. Cell 1992, 71:551-553.
121. Segal E., Widom J. From DNA sequence to transcriptional behaviour: a quantitative approach. Nat. Rev. Genet. 2009, 10:443-456.
122. Serini G., Ambrosi D., Giraudo E., Gamba A., Preziosi L., Bussolino F. Modeling the early stages of vascular network assembly. EMBO J. 2003, 22:1771-1779.
123. Shalaby F., Ho J., Stanford W.L., Fischer K.D., Schuh A.C., Schwartz L., Bernstein A., Rossant J. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 1997, 89:981-990.
124. Shen W.F., Krishnan K., Lawrence H.J., Largman C. The HOX homeodomain proteins block CBP histone acetyltransferase activity. Mol. Cell. Biol. 2001, 21:7509-7522.
125. Shen W., Chrobak D., Krishnan K., Lawrence H.J., Largman C. HOXB6 protein is bound to CREB-binding protein and represses globin expression in a DNA binding-dependent, PBX interaction-independent process. J. Biol. Chem. 2004, 279:39895-39904.
126. Sidorenko S.P., Clark E.A. The dual-function CD150 receptor subfamily: the viral attraction. Nat. Immunol. 2003, 4:19-24.
127. Sinclair P., Bian Q., Plutz M., Heard E., Belmont A.S. Dynamic plasticity of large-scale chromatin structure revealed by self-assembly of engineered chromosome regions. J. Cell Biol. 2010, 190:761-776.
128. Smith K.K. Time's arrow: heterochrony and the evolution of development. Int. J. Dev. Biol. 2003, 47:613-621.
129. Stern C.D., Charite J., Deschamps J., Duboule D., Durston A.J., Kmita M., Nicolas J.F., Palmeirim I., Smith J.C., Wolpert L. Head-tail patterning of the vertebrate embryo: one, two or many unresolved problems?. Int. J. Dev. Biol. 2006, 50:3-15.
130. Tam P.P., Beddington R.S. The formation of mesodermal tissues in the mouse embryo during gastrulation and early organogenesis. Development 1987, 99:109-126.
131. Tesar P.J., Chenoweth J.G., Brook F.A., Davies T.J., Evans E.P., Mack D.L., Gardner R.L., McKay R.D. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 2007, 448:196-199.
132. Till J.E., McCulloch E.A., Siminovitch L. A stochastic model of stem cell proliferation, based on the growth of spleen colony-forming cells. Proc. Natl. Acad. Sci. U. S. A. 1964, 51:29-36.
133. Tremblay K.D., Dunn N.R., Robertson E.J. Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development 2001, 128:3609-3621.
134. Tsai S.F., Strauss E., Orkin S.H. Functional analysis and in vivo footprinting implicate the erythroid transcription factor GATA-1 as a positive regulator of its own promoter. Genes Dev. 1991, 5:919-931.
135. Tsien R.Y. Imagining imaging's future. Nat. Rev. Mol. Cell Biol. 2003, SS16-SS21. Suppl,.
136. Ueno H., Weissman I.L. Clonal analysis of mouse development reveals a polyclonal origin for yolk sac blood islands. Dev. Cell 2006, 11:519-533.
137. Unger C., Karner E., Treschow A., Stellan B., Felldin U., Concha H., Wendel M., Hovatta O., Aints A., Ahrlund-Richter L., Dilber M.S. Lentiviral-mediated HoxB4 expression in human embryonic stem cells initiates early hematopoiesis in a dose-dependent manner but does not promote myeloid differentiation. Stem Cells 2008, 26:2455-2466.
138. Vasiev B., Balter A., Chaplain M., Glazier J.A., Weijer C.J. Modeling gastrulation in the chick embryo: formation of the primitive streak. PLoS One 2010, 5:e10571.
139. Voiculescu O., Bertocchini F., Wolpert L., Keller R.E., Stern C.D. The amniote primitive streak is defined by epithelial cell intercalation before gastrulation. Nature 2007, 449:1049-1052.
140. Waddington C.H. Form and information. Biological Theory 2008, 3:267-283.
141. Wadman I.A., Osada H., Grutz G.G., Agulnick A.D., Westphal H., Forster A., Rabbitts T.H. The LIM-only protein Lmo2 is a bridging molecule assembling an erythroid, DNA-binding complex which includes the TAL1, E47, GATA-1 and Ldb1/NLI proteins. EMBO J. 1997, 16:3145-3157.
142. Wagner G.P. Characters, Units and Natural Kinds: An Introduction. The Character Concept in Evolutionary Biology 2000, Academic Press, San Diego, Calif, pp. 1-12.
143. Waldrip W.R., Bikoff E.K., Hoodless P.A., Wrana J.L., Robertson E.J. Smad2 signaling in extraembryonic tissues determines anterior-posterior polarity of the early mouse embryo. Cell 1998, 92:797-808.
144. Walls J.R., Coultas L., Rossant J., Henkelman R.M. Three-dimensional analysis of vascular development in the mouse embryo. PLoS One 2008, 3:e2853.
145. Wang L.D., Wagers A.J. Dynamic niches in the origination and differentiation of haematopoietic stem cells. Nat. Rev. Mol. Cell Biol. 2011, 12:643-655.
146. Wang L., Li L., Shojaei F., Levac K., Cerdan C., Menendez P., Martin T., Rouleau A., Bhatia M. Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity 2004, 21:31-41.
147. Warr M.R., Pietras E.M., Passegue E. Mechanisms controlling hematopoietic stem cell functions during normal hematopoiesis and hematological malignancies. Wiley Interdiscip. Rev. Syst. Biol. Med. 2011, 3:681-701.
148. Weissman I.L., Shizuru J.A. 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, 112:3543-3553.
149. Wilensky U. Netlogo 1999, http://ccl.northwestern.edu/netlogo/.
150. Wilensky U., Resnick M. Thinking in levels: a dynamic systems approach to making sense of the world. J. Sci. Educ. Technol. 1999, 8:3-19.
151. Winnier G., Blessing M., Labosky P.A., Hogan B.L. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 1995, 9:2105-2116.
152. Woodger J.H. The "concept of organism" and the relation between embryology and genetics part. II. Q. Rev. Biol. 1930, 5:438-463.
153. Xu C.R., Cole P.A., Meyers D.J., Kormish J., Dent S., Zaret K.S. Chromatin "prepattern" and histone modifiers in a fate choice for liver and pancreas. Science 2011, 332:963-966.
154. Yamashita J., Itoh H., Hirashima M., Ogawa M., Nishikawa S., Yurugi T., Naito M., Nakao K. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 2000, 408:92-96.
155. Ying Q.L., Wray J., Nichols J., Batlle-Morera L., Doble B., Woodgett J., Cohen P., Smith A. The ground state of embryonic stem cell self-renewal. Nature 2008, 453:519-523.
156. Yoder M.C. Generation of HSCs in the embryo and assays to detect them. Oncogene 2004, 23:7161-7163.
157. Yokomizo T., Dzierzak E. Three-dimensional cartography of hematopoietic clusters in the vasculature of whole mouse embryos. Development 2010, 137:3651-3661.
158. Yokomizo T., Takahashi S., Mochizuki N., Kuroha T., Ema M., Wakamatsu A., Shimizu R., Ohneda O., Osato M., Okada H., Komori T., Ogawa M., Nishikawa S., Ito Y., Yamamoto M. Characterization of GATA-1(+) hemangioblastic cells in the mouse embryo. EMBO J. 2007, 26:184-196.
159. Zafonte B.T., Liu S., Lynch-Kattman M., Torregroza I., Benvenuto L., Kennedy M., Keller G., Evans T. Smad1 expands the hemangioblast population within a limited developmental window. Blood 2007, 109:516-523.
160. Zamir E.A., Rongish B.J., Little C.D. The ECM moves during primitive streak formation - computation of ECM versus cellular motion. PLoS Biol. 2008, 6:e247.
161. Zeeb M., Strilic B., Lammert E. Resolving cell-cell junctions: lumen formation in blood vessels. Curr. Opin. Cell Biol. 2010, 22:626-632.
162. Zeigler B.M., Sugiyama D., Chen M., Guo Y., Downs K.M., Speck N.A. The allantois and chorion, when isolated before circulation or chorio-allantoic fusion, have hematopoietic potential. Development 2006, 133:4183-4192.
163. Zhang X.B., Schwartz J.L., Humphries R.K., Kiem H.P. Effects of HOXB4 overexpression on ex vivo expansion and immortalization of hematopoietic cells from different species. Stem Cells 2007, 25:2074-2081.
164. Zovein A.C., Turlo K.A., Ponec R.M., Lynch M.R., Chen K.C., Hofmann J.J., Cox T.C., Gasson J.C., Iruela-Arispe M.L. Vascular remodeling of the vitelline artery initiates extravascular emergence of hematopoietic clusters. Blood 2010, 116:3435-3444.