Inductive interactions mediated by interplay of asymmetric signalling underlie development of adult haematopoietic stem cells

Nature Communications

Volumn 7, Issue , 2016, Pages

  Souilhol, Céline ^a   Gonneau, Christèle ^a   Lendinez, Javier G ^a   Batsivari, Antoniana ^a   Rybtsov, Stanislav ^a   Wilson, Heather ^a   Morgado Palacin, Lucia ^a   Hills, David ^a   Taoudi, Samir ^b,c   Antonchuk, Jennifer ^d   Zhao, Suling ^a   Medvinsky, Alexander ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d StemCell Technologies Inc   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; SONIC HEDGEHOG PROTEIN; BMP4 PROTEIN, MOUSE; BONE MORPHOGENETIC PROTEIN 4; SHH PROTEIN, MOUSE;

ADULT; CELLS AND CELL COMPONENTS; EMBRYONIC DEVELOPMENT; EMERGENCE; MAMMAL;

ADULT; AORTA; ARTICLE; CELL INTERACTION; CELL LINEAGE; CELL MATURATION; CELLULAR DISTRIBUTION; GONAD; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MESONEPHROS; PROTEIN EXPRESSION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CYTOLOGY; EMBRYOLOGY; FEMALE; GENETICS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; MALE; METABOLISM;

MAMMALIA;

ANIMALS; AORTA; BONE MORPHOGENETIC PROTEIN 4; FEMALE; GONADS; HEDGEHOG PROTEINS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; MALE; MESONEPHROS; MICE, INBRED C57BL; SIGNAL TRANSDUCTION;

EID: 84960386356     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10784     Document Type: Article

References (70)

1. Medvinsky, A. & Dzierzak, E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86, 897-906 (1996).
2. de Bruijn, M. F., Speck, N. A., Peeters, M. C. & Dzierzak, E. Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. EMBO J. 19, 2465-2474 (2000).
3. Müller, A. M., Medvinsky, A., Strouboulis, J., Grosveld, F. & Dzierzak, E. Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1, 291-301 (1994).
4. Cumano, A., Dieterlen-Lievre, F. & Godin, I. Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura. Cell 86, 907-916 (1996).
5. Ivanovs, A., Rybtsov, S., Anderson, R. A., Turner, M. L. & Medvinsky, A. Identification of the niche and phenotype of the first human hematopoietic stem cells. Stem Cell Rep. 2, 449-456 (2014).
6. Taoudi, S. & Medvinsky, A. Functional identification of the hematopoietic stem cell niche in the ventral domain of the embryonic dorsal aorta. Proc. Natl Acad. Sci. USA 104, 9399-9403 (2007).
7. de Bruijn, M. F. et al. Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity 16, 673-683 (2002).
8. Bertrand, J. Y. et al. Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 464, 108-111 (2010).
9. Kissa, K. & Herbomel, P. Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464, 112-115 (2010).
10. Boisset, J. C. et al. In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464, 116-120 (2010).
11. Jaffredo, T., Gautier, R., Eichmann, A. & Dieterlen-Lievre, F. Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny. Development 125, 4575-4583 (1998).
12. Chen, M. J., Yokomizo, T., Zeigler, B. M., Dzierzak, E. & Speck, N. A. Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457, 887-891 (2009).
13. Yokomizo, T. & Dzierzak, E. Three-dimensional cartography of hematopoietic clusters in the vasculature of whole mouse embryos. Development 137, 3651-3661 (2010).
14. Ciau-Uitz, A., Walmsley, M. & Patient, R. Distinct origins of adult and embryonic blood in Xenopus. Cell 102, 787-796 (2000).
15. Taoudi, S. et al. Extensive hematopoietic stem cell generation in the AGM region via maturation of VE-cadherin+CD45+ pre-definitive HSCs. Cell Stem Cell 3, 99-108 (2008).
16. Rybtsov, S. et al. Hierarchical organization and early hematopoietic specification of the developing HSC lineage in the AGM region. J. Exp. Med. 208, 1305-1315 (2011).
17. Rybtsov, S. et al. Tracing the origin of the HSC hierarchy reveals an SCFdependent, IL-3-independent CD43(-) embryonic precursor. Stem Cell Rep. 3, 489-501 (2014).
18. Ferkowicz, M. J. et al. CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo. Development 130, 4393-4403 (2003).
19. Medvinsky, A., Rybtsov, S. & Taoudi, S. Embryonic origin of the adult hematopoietic system: advances and questions. Development 138, 1017-1031 (2011).
20. Kumano, K. et al. Notch1 but not Notch2 is essential for generating hematopoietic stem cells from endothelial cells. Immunity 18, 699-711 (2003).
21. Robin, C. et al. An unexpected role for IL-3 in the embryonic development of hematopoietic stem cells. Dev. Cell. 11, 171-180 (2006).
22. Ruiz-Herguido, C. et al. Hematopoietic stem cell development requires transient Wnt/beta-catenin activity. J. Exp. Med. 209, 1457-1468 (2012).
23. Chanda, B., Ditadi, A., Iscove, N. N. & Keller, G. Retinoic acid signaling is essential for embryonic hematopoietic stem cell development. Cell 155, 215-227 (2013).
24. Li, Y. et al. Inflammatory signaling regulates embryonic hematopoietic stem and progenitor cell production. Genes Dev. 28, 2597-2612 (2014).
25. Marcelo, K. L. et al. Hemogenic endothelial cell specification requires c-Kit, Notch signaling, and p27-mediated cell-cycle control. Dev. Cell 27, 504-515 (2013).
26. Espin-Palazon, R. et al. Proinflammatory signaling regulates hematopoietic stem cell emergence. Cell 159, 1070-1085 (2014).
27. Sawamiphak, S., Kontarakis, Z. & Stainier, D. Y. Interferon gamma signaling positively regulates hematopoietic stem cell emergence. Dev. Cell 31, 640-653 (2014).
28. Bigas, A., Guiu, J. & Gama-Norton, L. Notch and Wnt signaling in the emergence of hematopoietic stem cells. Blood Cells Mol. Dis. 51, 264-270 (2013).
29. Kim, P. G. et al. Signaling axis involving Hedgehog, Notch, and Scl promotes the embryonic endothelial-to-hematopoietic transition. Proc. Natl Acad. Sci. USA 110, E141-E150 (2013).
30. Jing, L. et al. Adenosine signaling promotes hematopoietic stem and progenitor cell emergence. J. Exp. Med. 212, 649-663 (2015).
31. Burns, C. E., Traver, D., Mayhall, E., Shepard, J. L. & Zon, L. I. Hematopoietic stem cell fate is established by the Notch-Runx pathway. Genes Dev. 19, 2331-2342 (2005).
32. Ding, L., Saunders, T. L., Enikolopov, G. & Morrison, S. J. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481, 457-462 (2012).
33. Ogawa, M. et al. Expression and function of c-kit in hemopoietic progenitor cells. J. Exp. Med. 174, 63-71 (1991).
34. Wilkinson, R. N. et al. Hedgehog and Bmp polarize hematopoietic stem cell emergence in the zebrafish dorsal aorta. Dev. Cell 16, 909-916 (2009).
35. Pouget, C. et al. FGF signalling restricts haematopoietic stem cell specification via modulation of the BMP pathway. Nat. Commun. 5, 5588 (2014).
36. Durand, C. et al. Embryonic stromal clones reveal developmental regulators of definitive hematopoietic stem cells. Proc. Natl Acad. Sci. USA 104, 20838-20843 (2007).
37. Peeters, M. et al. Ventral embryonic tissues and Hedgehog proteins induce early AGM hematopoietic stem cell development. Development 136, 2613-2621 (2009).
38. Nieuwkoop, P. D. The neural induction process; its morphogenetic aspects. Int. J. Dev. Biol. 43, 615-623 (1999).
39. Vainio, S. & Muller, U. Inductive tissue interactions, cell signaling, and the control of kidney organogenesis. Cell 90, 975-978 (1997).
40. Ashe, H. L. & Briscoe, J. The interpretation of morphogen gradients. Development 133, 385-394 (2006).
41. Clements, W. K. et al. A somitic Wnt16/Notch pathway specifies haematopoietic stem cells. Nature 474, 220-224 (2011).
42. Leung, A. et al. Uncoupling VEGFA functions in arteriogenesis and hematopoietic stem cell specification. Dev. Cell 24, 144-158 (2013).
43. Lee, Y. et al. FGF signalling specifies haematopoietic stem cells through its regulation of somitic Notch signalling. Nat. Commun. 5, 5583 (2014).
44. Nguyen, P. D. et al. Haematopoietic stem cell induction by somite-derived endothelial cells controlled by meox1. Nature 512, 314-318 (2014).
45. Murayama, E. et al. NACA deficiency reveals the crucial role of somitederived stromal cells in haematopoietic niche formation. Nat. Commun. 6, 8375 (2015).
46. Gilchrist, D. S., Ure, J., Hook, L. & Medvinsky, A. Labeling of hematopoietic stem and progenitor cells in novel activatable EGFP reporter mice. Genesis 36, 168-176 (2003).
47. Echelard, Y. et al. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417-1430 (1993).
48. Balaskas, N. et al. Gene regulatory logic for reading the Sonic Hedgehog signaling gradient in the vertebrate neural tube. Cell 148, 273-284 (2012).
49. Marshall, C. J., Kinnon, C. & Thrasher, A. J. Polarized expression of bone morphogenetic protein-4 in the human aorta-gonad-mesonephros region. Blood 96, 1591-1593 (2000).
50. Massague, J. & Wotton, D. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J. 19, 1745-1754 (2000).
51. Herrera, B. & Inman, G. J. A rapid and sensitive bioassay for the simultaneous measurement of multiple bone morphogenetic proteins. Identification and quantification of BMP4, BMP6 and BMP9 in bovine and human serum. BMC Cell Biol. 10, 20 (2009).
52. Pouget, C., Gautier, R., Teillet, M. A. & Jaffredo, T. Somite-derived cells replace ventral aortic hemangioblasts and provide aortic smooth muscle cells of the trunk. Development 133, 1013-1022 (2006).
53. Fitch, S. R. et al. Signaling from the sympathetic nervous system regulates hematopoietic stem cell emergence during embryogenesis. Cell Stem Cell 11, 554-566 (2012).
54. Gering, M. & Patient, R. Hedgehog signaling is required for adult blood stem cell formation in zebrafish embryos. Dev. Cell 8, 389-400 (2005).
55. Ribes, V. et al. Distinct Sonic Hedgehog signaling dynamics specify floor plate and ventral neuronal progenitors in the vertebrate neural tube. Genes Dev. 24, 1186-1200 (2010).
56. Goumans, M. J. & Mummery, C. Functional analysis of the TGFbeta receptor/Smad pathway through gene ablation in mice. Int. J. Dev. Biol. 44, 253-265 (2000).
57. Goldman, D. C. et al. BMP4 regulates the hematopoietic stem cell niche. Blood 114, 4393-4401 (2009).
58. Kim, P. G. et al. Flow-induced protein kinase A-CREB pathway acts via BMP signaling to promote HSC emergence. J. Exp. Med. 212, 633-648 (2015).
59. Crisan, M. et al. BMP signalling differentially regulates distinct haematopoietic stem cell types. Nat. Commun. 6, 8040 (2015).
60. Pimanda, J. E. et al. The SCL transcriptional network and BMP signaling pathway interact to regulate RUNX1 activity. Proc. Natl Acad. Sci. USA 104, 840-845 (2007).
61. Narula, J. et al. Mathematical model of a gene regulatory network reconciles effects of genetic perturbations on hematopoietic stem cell emergence. Dev. Biol. 379, 258-269 (2013).
62. Swiers, G. et al. Early dynamic fate changes in haemogenic endothelium characterized at the single-cell level. Nat. Commun. 4, 2924 (2013).
63. Knezevic, K. et al. A Runx1-Smad6 rheostat controls Runx1 activity during embryonic hematopoiesis. Mol. Cell. Biol. 31, 2817-2826 (2011).
64. Lan, Y. et al. Endothelial Smad4 restrains the transition to hematopoietic progenitors via suppression of ERK activation. Blood 123, 2161-2171 (2014).
65. Le Dréau, G. & Martí, E. Dorsal-ventral patterning of the neural tube: a tale of three signals. Dev. Neurobiol. 72, 1471-1481 (2012).
66. Botchkarev, V. A. et al. Noggin is required for induction of the hair follicle growth phase in postnatal skin. FASEB J. 15, 2205-2214 (2001).
67. Liem, K. F., Jessell, T. M. & Briscoe, J. Regulation of the neural patterning activity of sonic hedgehog by secreted BMP inhibitors expressed by notochord and somites. Development 127, 4855-4866 (2000).
68. McMahon, J. A. et al. Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev. 12, 1438-1452 (1998).
69. Taylor, E., Taoudi, S. & Medvinsky, A. Hematopoietic stem cell activity in the aorta-gonad-mesonephros region enhances after mid-day 11 of mouse development. Int. J. Dev. Biol. 54, 1055-1060 (2010).
70. Ohtsuka, S., Nishikawa-Torikai, S. & Niwa, H. E-cadherin promotes incorporation of mouse epiblast stem cells into normal development. PloS ONE 7, e45220 (2012).