Signaling from the sympathetic nervous system regulates hematopoietic stem cell emergence during embryogenesis

Cell Stem Cell

Volumn 11, Issue 4, 2012, Pages 554-566

  Fitch, Simon R ^a   Kimber, Gillian M ^a   Wilson, Nicola K ^a   Parker, Aimée ^a   Mirshekar Syahkal, Bahar ^a   Göttgens, Berthold ^a   Medvinsky, Alexander ^c   Dzierzak, Elaine ^b   Ottersbach, Katrin ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CATECHOLAMINE; TRANSCRIPTION FACTOR GATA 3;

ADRENERGIC SYSTEM; ANIMAL CELL; AORTA; ARTICLE; BLOOD FLOW; CELL POPULATION; EMBRYO; EMBRYO DEVELOPMENT; GONAD; HEMATOPOIETIC STEM CELL; MESONEPHROS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ADULT STEM CELLS; ANIMALS; AORTA; CATECHOLAMINES; CELL LINE; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; GATA3 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GONADS; HEMATOPOIETIC STEM CELLS; MESONEPHROS; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; STEM CELL NICHE; SYMPATHETIC NERVOUS SYSTEM;

EID: 84867353401     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2012.07.002     Document Type: Article

References (68)

1. L. Adamo, O. Naveiras, P.L. Wenzel, S. McKinney-Freeman, P.J. Mack, J. Gracia-Sancho, A. Suchy-Dicey, M. Yoshimoto, M.W. Lensch, and M.C. Yoder Biomechanical forces promote embryonic haematopoiesis Nature 459 2009 1131 1135
2. M.L. Asselin-Labat, K.D. Sutherland, H. Barker, R. Thomas, M. Shackleton, N.C. Forrest, L. Hartley, L. Robb, F.G. Grosveld, and J. van der Wees Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation Nat. Cell Biol. 9 2007 201 209
3. P. Benveniste, C. Frelin, S. Janmohamed, M. Barbara, R. Herrington, D. Hyam, and N.N. Iscove Intermediate-term hematopoietic stem cells with extended but time-limited reconstitution potential Cell Stem Cell 6 2010 48 58
4. J.Y. Bertrand, S. Giroux, R. Golub, M. Klaine, A. Jalil, L. Boucontet, I. Godin, and A. Cumano Characterization of purified intraembryonic hematopoietic stem cells as a tool to define their site of origin Proc. Natl. Acad. Sci. USA 102 2005 134 139
5. N. Buza-Vidas, S. Duarte, S. Luc, T. Bouriez-Jones, P.S. Woll, and S.E. Jacobsen GATA3 is redundant for maintenance and self-renewal of hematopoietic stem cells Blood 118 2011 1291 1293
6. M.J. Chen, T. Yokomizo, B.M. Zeigler, E. Dzierzak, and N.A. Speck Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter Nature 457 2009 887 891
7. P. Cserjesi, D. Brown, G.E. Lyons, and E.N. Olson Expression of the novel basic helix-loop-helix gene eHAND in neural crest derivatives and extraembryonic membranes during mouse development Dev. Biol. 170 1995 664 678
8. M.F. de Bruijn, X. Ma, C. Robin, K. Ottersbach, M.J. Sanchez, and E. Dzierzak Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta Immunity 16 2002 673 683
9. C. Durand, C. Robin, K. Bollerot, M.H. Baron, K. Ottersbach, and E. Dzierzak Embryonic stromal clones reveal developmental regulators of definitive hematopoietic stem cells Proc. Natl. Acad. Sci. USA 104 2007 20838 20843
10. D. Grote, A. Souabni, M. Busslinger, and M. Bouchard Pax 2/8-regulated Gata 3 expression is necessary for morphogenesis and guidance of the nephric duct in the developing kidney Development 133 2006 53 61
11. H. Hock, M.J. Hamblen, H.M. Rooke, J.W. Schindler, S. Saleque, Y. Fujiwara, and S.H. Orkin Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells Nature 431 2004 1002 1007
12. K. Huber The sympathoadrenal cell lineage: specification, diversification, and new perspectives Dev. Biol. 298 2006 335 343
13. T. Jaffredo, R. Gautier, A. Eichmann, and F. Dieterlen-Lièvre Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny Development 125 1998 4575 4583
14. T. Jaffredo, R. Gautier, V. Brajeul, and F. Dieterlen-Lièvre Tracing the progeny of the aortic hemangioblast in the avian embryo Dev. Biol. 224 2000 204 214
15. Y. Katayama, M. Battista, W.M. Kao, A. Hidalgo, A.J. Peired, S.A. Thomas, and P.S. Frenette Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow Cell 124 2006 407 421
16. C.K. Kaufman, P. Zhou, H.A. Pasolli, M. Rendl, D. Bolotin, K.C. Lim, X. Dai, M.L. Alegre, and E. Fuchs GATA-3: an unexpected regulator of cell lineage determination in skin Genes Dev. 17 2003 2108 2122
17. D.G. Kent, M.R. Copley, C. Benz, S. Wöhrer, B.J. Dykstra, E. Ma, J. Cheyne, Y. Zhao, M.B. Bowie, and Y. Zhao Prospective isolation and molecular characterization of hematopoietic stem cells with durable self-renewal potential Blood 113 2009 6342 6350
18. C. Khandanpour, E. Sharif-Askari, L. Vassen, M.C. Gaudreau, J. Zhu, W.E. Paul, T. Okayama, C. Kosan, and T. Möröy Evidence that growth factor independence 1b regulates dormancy and peripheral blood mobilization of hematopoietic stem cells Blood 116 2010 5149 5161
19. H. Kouros-Mehr, E.M. Slorach, M.D. Sternlicht, and Z. Werb GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland Cell 127 2006 1041 1055
20. C.J. Ku, T. Hosoya, I. Maillard, and J.D. Engel GATA-3 regulates hematopoietic stem cell maintenance and cell-cycle entry Blood 119 2012 2242 2251
21. P. Kumaravelu, L. Hook, A.M. Morrison, J. Ure, S. Zhao, S. Zuyev, J. Ansell, and A. Medvinsky 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 129 2002 4891 4899
22. D. Kurek, G.A. Garinis, J.H. van Doorninck, J. van der Wees, and F.G. Grosveld Transcriptome and phenotypic analysis reveals Gata3-dependent signalling pathways in murine hair follicles Development 134 2007 261 272
23. K.C. Lim, G. Lakshmanan, S.E. Crawford, Y. Gu, F. Grosveld, and J.D. Engel Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system Nat. Genet. 25 2000 209 212
24. K.W. Ling, K. Ottersbach, J.P. van Hamburg, A. Oziemlak, F.Y. Tsai, S.H. Orkin, R. Ploemacher, R.W. Hendriks, and E. Dzierzak GATA-2 plays two functionally distinct roles during the ontogeny of hematopoietic stem cells J. Exp. Med. 200 2004 871 882
25. A. Manaia, V. Lemarchandel, M. Klaine, I. Max-Audit, P. Romeo, F. Dieterlen-Lièvre, and I. Godin Lmo2 and GATA-3 associated expression in intraembryonic hemogenic sites Development 127 2000 643 653
26. M.I. Mascarenhas, A. Parker, E. Dzierzak, and K. Ottersbach Identification of novel regulators of hematopoietic stem cell development through refinement of stem cell localization and expression profiling Blood 114 2009 4645 4653
27. A. Medvinsky, and E. Dzierzak Definitive hematopoiesis is autonomously initiated by the AGM region Cell 86 1996 897 906
28. A.L. Medvinsky, N.L. Samoylina, A.M. Müller, and E.A. Dzierzak An early pre-liver intraembryonic source of CFU-S in the developing mouse Nature 364 1993 64 67
29. S.C. Mendes, C. Robin, and E. Dzierzak Mesenchymal progenitor cells localize within hematopoietic sites throughout ontogeny Development 132 2005 1127 1136
30. S. Méndez-Ferrer, D. Lucas, M. Battista, and P.S. Frenette Haematopoietic stem cell release is regulated by circadian oscillations Nature 452 2008 442 447
31. T. Moriguchi, N. Takako, M. Hamada, A. Maeda, Y. Fujioka, T. Kuroha, R.E. Huber, S.L. Hasegawa, A. Rao, and M. Yamamoto Gata3 participates in a complex transcriptional feedback network to regulate sympathoadrenal differentiation Development 133 2006 3871 3881
32. Y. Morikawa, and P. Cserjesi Extra-embryonic vasculature development is regulated by the transcription factor HAND1 Development 131 2004 2195 2204
33. A.M. Müller, A. Medvinsky, J. Strouboulis, F. Grosveld, and E. Dzierzak Development of hematopoietic stem cell activity in the mouse embryo Immunity 1 1994 291 301
34. T. North, T.L. Gu, T. Stacy, Q. Wang, L. Howard, M. Binder, M. Marín-Padilla, and N.A. Speck Cbfa2 is required for the formation of intra-aortic hematopoietic clusters Development 126 1999 2563 2575
35. T.E. North, M.F. de Bruijn, T. Stacy, L. Talebian, E. Lind, C. Robin, M. Binder, E. Dzierzak, and N.A. Speck Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo Immunity 16 2002 661 672
36. T.E. North, W. Goessling, M. Peeters, P. Li, C. Ceol, A.M. Lord, G.J. Weber, J. Harris, C.C. Cutting, and P. Huang Hematopoietic stem cell development is dependent on blood flow Cell 137 2009 736 748
37. O. Ohneda, K. Ohneda, H. Nomiyama, Z. Zheng, S.A. Gold, F. Arai, T. Miyamoto, B.E. Taillon, R.A. McIndoe, and R.A. Shimkets WECHE: a novel hematopoietic regulatory factor Immunity 12 2000 141 150
38. R.A. Oostendorp, C. Robin, C. Steinhoff, S. Marz, R. Bräuer, U.A. Nuber, E.A. Dzierzak, and C. Peschel Long-term maintenance of hematopoietic stem cells does not require contact with embryo-derived stromal cells in cocultures Stem Cells 23 2005 842 851
39. K. Ottersbach, and E. Dzierzak The murine placenta contains hematopoietic stem cells within the vascular labyrinth region Dev. Cell 8 2005 377 387
40. K. Ottersbach, A. Smith, A. Wood, and B. Göttgens Ontogeny of haematopoiesis: recent advances and open questions Br. J. Haematol. 148 2010 343 355
41. P.P. Pandolfi, M.E. Roth, A. Karis, M.W. Leonard, E. Dzierzak, F.G. Grosveld, J.D. Engel, and M.H. Lindenbaum Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis Nat. Genet. 11 1995 40 44
42. R.A. Panepucci, L.H. Oliveira, D.L. Zanette, R.D. Carrara, A.G. Araujo, M.D. Orellana, P.V. Palma, C.C. Menezes, D.T. Covas, and M.A. Zago Increased Levels of NOTCH1, NF-kappaB, and Other Interconnected Transcription Factors Characterize Primitive Sets of Hematopoietic Stem Cells Stem Cells and Development 19 2009 321 332
43. R.A. Panepucci, L.H. Oliveira, D.L. Zanette, Rde.C. Viu Carrara, A.G. Araujo, M.D. Orellana, P.V. Bonini de Palma, C.C. Menezes, D.T. Covas, and M.A. Zago Increased levels of NOTCH1, NF-kappaB, and other interconnected transcription factors characterize primitive sets of hematopoietic stem cells Stem Cells Dev. 19 2010 321 332
44. A. Pattyn, C. Goridis, and J.F. Brunet Specification of the central noradrenergic phenotype by the homeobox gene Phox2b Mol. Cell. Neurosci. 15 2000 235 243
45. M. Peeters, K. Ottersbach, K. Bollerot, C. Orelio, M. de Bruijn, M. Wijgerde, and E. Dzierzak Ventral embryonic tissues and Hedgehog proteins induce early AGM hematopoietic stem cell development Development 136 2009 2613 2621
46. J. Renström, R. Istvanffy, K. Gauthier, A. Shimono, J. Mages, A. Jardon-Alvarez, M. Kröger, M. Schiemann, D.H. Busch, and I. Esposito Secreted frizzled-related protein 1 extrinsically regulates cycling activity and maintenance of hematopoietic stem cells Cell Stem Cell 5 2009 157 167
47. C. Robin, K. Ottersbach, C. Durand, M. Peeters, L. Vanes, V. Tybulewicz, and E. Dzierzak An unexpected role for IL-3 in the embryonic development of hematopoietic stem cells Dev. Cell 11 2006 171 180
48. C. Robin, K. Ottersbach, J.C. Boisset, A. Oziemlak, and E. Dzierzak CD41 is developmentally regulated and differentially expressed on mouse hematopoietic stem cells Blood 117 2011 5088 5091
49. S. Rybtsov, M. Sobiesiak, S. Taoudi, C. Souilhol, J. Senserrich, A. Liakhovitskaia, A. Ivanovs, J. Frampton, S. Zhao, and A. Medvinsky Hierarchical organization and early hematopoietic specification of the developing HSC lineage in the AGM region J. Exp. Med. 208 2011 1305 1315
50. I.M. Samokhvalov, N.I. Samokhvalova, and S. Nishikawa Cell tracing shows the contribution of the yolk sac to adult haematopoiesis Nature 446 2007 1056 1061
51. M.J. Sánchez, A. Holmes, C. Miles, and E. Dzierzak Characterization of the first definitive hematopoietic stem cells in the AGM and liver of the mouse embryo Immunity 5 1996 513 525
52. A. Spiegel, S. Shivtiel, A. Kalinkovich, A. Ludin, N. Netzer, P. Goichberg, Y. Azaria, I. Resnick, I. Hardan, and H. Ben-Hur Catecholaminergic neurotransmitters regulate migration and repopulation of immature human CD34+ cells through Wnt signaling Nat. Immunol. 8 2007 1123 1131
53. Y. Tanaka, M. Hayashi, Y. Kubota, H. Nagai, G. Sheng, S. Nishikawa, and I.M. Samokhvalov Early ontogenic origin of the hematopoietic stem cell lineage Proc. Natl. Acad. Sci. USA 109 2012 4515 4520
54. S. Taoudi, and A. Medvinsky Functional identification of the hematopoietic stem cell niche in the ventral domain of the embryonic dorsal aorta Proc. Natl. Acad. Sci. USA 104 2007 9399 9403
55. S. Taoudi, C. Gonneau, K. Moore, J.M. Sheridan, C.C. Blackburn, E. Taylor, and A. Medvinsky Extensive hematopoietic stem cell generation in the AGM region via maturation of VE-cadherin+CD45+ pre-definitive HSCs Cell Stem Cell 3 2008 99 108
56. S.A. Thomas, A.M. Matsumoto, and R.D. Palmiter Noradrenaline is essential for mouse fetal development Nature 374 1995 643 646
57. C.N. Ting, M.C. Olson, K.P. Barton, and J.M. Leiden Transcription factor GATA-3 is required for development of the T-cell lineage Nature 384 1996 474 478
58. H. Toda, W.G. Ding, Y. Yasuda, F. Toyoda, M. Ito, H. Matsuura, and M. Horie Stimulatory action of protein kinase C(epsilon) isoform on the slow component of delayed rectifier K+ current in guinea-pig atrial myocytes Br. J. Pharmacol. 150 2007 1011 1021
59. Q. Tong, G. Dalgin, H. Xu, C.N. Ting, J.M. Leiden, and G.S. Hotamisligil Function of GATA transcription factors in preadipocyte-adipocyte transition Science 290 2000 134 138
60. K. Tsarovina, A. Pattyn, J. Stubbusch, F. Müller, J. van der Wees, C. Schneider, J.F. Brunet, and H. Rohrer Essential role of Gata transcription factors in sympathetic neuron development Development 131 2004 4775 4786
61. K. Tsarovina, T. Reiff, J. Stubbusch, D. Kurek, F.G. Grosveld, R. Parlato, G. Schütz, and H. Rohrer The Gata3 transcription factor is required for the survival of embryonic and adult sympathetic neurons J. Neurosci. 30 2010 10833 10843
62. J.H. van Doorninck, J. van Der Wees, A. Karis, E. Goedknegt, J.D. Engel, M. Coesmans, M. Rutteman, F. Grosveld, and C.I. De Zeeuw GATA-3 is involved in the development of serotonergic neurons in the caudal raphe nuclei J. Neurosci. 19 1999 RC12
63. C.A. Vosshenrich, M.E. García-Ojeda, S.I. Samson-Villéger, V. Pasqualetto, L. Enault, O. Richard-Le Goff, E. Corcuff, D. Guy-Grand, B. Rocha, and A. Cumano A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127 Nat. Immunol. 7 2006 1217 1224
64. E. Wei, W. Gao, and R. Lehner Attenuation of adipocyte triacylglycerol hydrolase activity decreases basal fatty acid efflux J. Biol. Chem. 282 2007 8027 8035
65. N.K. Wilson, R.T. Timms, S.J. Kinston, Y.H. Cheng, S.H. Oram, J.R. Landry, J. Mullender, K. Ottersbach, and B. Gottgens Gfi1 expression is controlled by five distinct regulatory regions spread over 100 kilobases, with Scl/Tal1, Gata2, PU.1, Erg, Meis1, and Runx1 acting as upstream regulators in early hematopoietic cells Mol. Cell. Biol. 30 2010 3853 3863
66. M. Wolkersdorfer, A. Laslop, C. Lazure, R. Fischer-Colbrie, and H. Winkler Processing of chromogranins in chromaffin cell culture: effects of reserpine and alpha-methyl-p-tyrosine Biochem. J. 316 1996 953 958
67. Q.Y. Zhou, C.J. Quaife, and R.D. Palmiter Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development Nature 374 1995 640 643
68. A.C. Zovein, J.J. Hofmann, M. Lynch, W.J. French, K.A. Turlo, Y. Yang, M.S. Becker, L. Zanetta, E. Dejana, and J.C. Gasson Fate tracing reveals the endothelial origin of hematopoietic stem cells Cell Stem Cell 3 2008 625 636