Hematopoiesis and stem cells during embryonic development

My lab focuses on the establishment of the hematopoietic system during embryonic development. We are particularly interested in the generation and regulation of the first hematopoietic stem cells, the very rare cells at the foundation of the entire adult blood system.

Catherine Robin

Catherine Robin received her PhD in 2000 at the Denis Diderot Paris VII University in Paris (France). She did her PhD research in the laboratory of Dr. W. Vainchenker in the group of Dr. L. Coulombel where she identified hematopoietic stem cells (HSCs) in cord blood, adult bone marrow and human embryos. She received a French fellowship (“La ligue nationale contre le cancer”) followed by a European Marie Curie long-term fellowship to join the laboratory of Prof. E. Dzierzak, in the Cell Biology Department of Prof. F. Grosveld at the Erasmus University Medical Center of Rotterdam (The Netherlands).

Her postdoctoral research focused on understanding the precise localization and regulation of the first HSCs emerging in the mid-gestation mouse embryo. She notably identified several signaling molecules involved in embryonic HSC survival and expansion. In 2006, she received a NWO (Vidi Award) Dutch young investigator grant to start her own research group at the Erasmus Stem Cell Institute for Regenerative Medicine (Rotterdam). By combining time-lapse confocal imaging and new dissection procedures she visualized, for the first time, the dynamic de novo emergence of the first HSCs from specialized endothelial cells (named hemogenic) directly inside the mouse embryonic aorta. This work was recognized as a major breakthrough discovery in 2010 and was broadcasted on TV and by several national and international newspapers. Images and movies generated in her lab were also exposed at the Museum Boymans van Beuningen in Rotterdam and at the MOTI museum in Breda (The Netherlands).

In 2013, she started as Associate Professor at the Hubrecht Institute and was awarded a ERC Consolidator Investigator award.

Other activities:

  • Associate professor at UMC Utrecht

c.robin(at)hubrecht.eu

Team membersRobin

Ismael Morin-Poulard

Postdoc

Ismael Morin-Poulard

Carla Kroon

Technician

Carla Kroon

Anna Klaus

PhD Student

Panagiota Giardoglou

PhD Student

Fanny Sage

Postdoc

Laurent Yvernogeau

Postdoc

Catherine Robin

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Research

Robin: Hematopoiesis and stem cells during embryonic development

Hematopoietic Stem Cells (HSCs) are self-renewing multipotent cells that produce all blood cell types during the entire life of an individual. They are the key cell type in transplantation protocols for patients with hematological malignancies. Adult HSCs are initially generated during embryonic development. We recently developed a novel experimental imaging set-up to visualize the mouse embryonic aorta. We have shown the dynamic formation of HSCs from specialized endothelial cells referred as hemogenic directly inside the aorta. The Robin group is developing novel approaches to uncover the cellular, molecular and biomechanical events implicated in embryonic HSC production and expansion in vivo.

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Key publications

  • GFI1 proteins orchestrate the emergence of haematopoietic stem cells through recruitment of LSD1. Thambyrajah, R., Mazan, M., Patel, R., Moignard, V., Stefanska, M., Marinopoulou, E., Li, Y., Lancrin, C., Clapes, T., Möröy, T., Robin, C., Miller, C., Cowley, S., Göttgens, B., Kouskoff, V., Lacaud, G. Nature Cell Biology 18, 21-32 (2016) Thambyrajah Nat Cell Biol 2016
  • Progressive maturation toward hematopoietic stem cells in the mouse embryo aorta. Boisset, J.C., Clapes, T., Klaus, A., Papazian, N., Onderwater, J., Mommaas-Kienhuis, M., Cupedo, T., Robin, C. Blood 125, 465-469 (2015) Boisset 2015 Blood
  • Ex vivo time-lapse confocal imaging of the mouse embryo aorta. Boisset, J.C., Andrieu-Soler, C., van Cappellen, W., Clapes, T., Robin, C. Nature Protocols 6: 1792-1805 (2011) Boisset Nat Prot 2011
  • In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Boisset, J.C., van Cappellen, W., Andrieu-Soler, C., Galjart, N., Dzierzak, E., Robin, C. Nature 464: 116-120 (2010) Boisset nature 2010
  • Human placenta is a potent hematopoietic niche containing hematopoietic stem and progenitor cells throughout development. Robin, C.*, Bollerot, K.*, Mendes, S.*, Haak, E., Crisan, M., Cerisoli, F., Lauw, I., Kaimakis, P., Jorna, R., Vermeulen, M., Kayser, M., van der Linden, R., Imanirad, P., Verstegen, M., Nawaz-Yousaf, M., Papazian, N., Steegers, E., Cupedo, T., Dzierzak, E. Cell Stem Cell 5: 385-395 (2009) Robin Cell stem cell 2009
  • An unexpected role for IL-3 in the embryonic development of hematopoietic stem cells. Robin, C., Ottersbach, K., Durand, C., Peeters, M., Vanes, L., Tybulewicz, V., Dzierzak, E. Developmental Cell 11: 171-180 (2006) Robin Dev cell 2006
  • Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. de Bruijn, M.F.*, Ma, X.*, Robin, C.*, Ottersbach, K., Sanchez, M.J., Dzierzak, E. Immunity 16: 673-683 (2002) deBruijn Immunity 2002

All publications

PDFs are for personal use only.

2016

  • GFI1 proteins orchestrate the emergence of haematopoietic stem cells through recruitment of LSD1. Thambyrajah, R., Mazan, M., Patel, R., Moignard, V., Stefanska, M., Marinopoulou, E., Li, Y., Lancrin, C., Clapes, T., Möröy, T., Robin, C., Miller, C., Cowley, S., Göttgens, B., Kouskoff, V., Lacaud, G. Nature Cell Biology 18, 21-32 (2016) Thambyrajah Nat Cell Biol 2016

2015

  • Development and trafficking function of haematopoietic stem cells and myeloid cells during fetal ontogeny. Heinig, K., Sage, F., Robin, C., Sperandio, M. Cardiovascular Research 107, 352-363 (2015) Heinig Cardio research 2015
  • Developmental biology of hematopoietic stem cells: cellular aspects. Yvernogeau, L., Boisset J.C., Robin, C. Stem cell biology and regenerative medicine. River publishers. 301-326 (2015)
  • Progressive maturation toward hematopoietic stem cells in the mouse embryo aorta. Boisset, J.C., Clapes, T., Klaus, A., Papazian, N., Onderwater, J., Mommaas-Kienhuis, M., Cupedo, T., Robin, C. Blood 125, 465-469 (2015) Boisset 2015 Blood

2013

  • Integrin αIIb (CD41) plays a role in the maintenance of hematopoietic stem cell activity in the mouse embryonic aorta. Boisset, J.C., Clapes, T., Van Der Linden, R., Dzierzak, E., Robin, C. Biology Open 2, 525-532 (2013) Boisset Biol Open 2013
  • Erythropoietic defect associated with reduced cell proliferation in mice lacking the 26S proteasome shuttling factor Rad23b. Bergink, S., Theil, A.F., Toussaint, W., De Cuyper, I.M., Kulu, D.I., Clapes, T., van der Linden, R., Demmers, J.A., Mul, E.P., van Alphen, F.P., Marteijn, J.A., van Gent, T., Maas, A., Robin, C., Philipsen, S., Vermeulen, W., Mitchell, J.R., Gutiérrez, L. Molecular and Cellular Biology 33, 3879-3892 (2013) Bergink Mol Cell Biol 2013

2012

  • The microtubule Plus-end tracking protein CLASP2 is required for hematopoiesis and hematopoietic stem cell maintenance. Drabek, K., Gutiérrez, L., Vermeij, M., Clapes, T., Patel, SR., Boisset, JC., van Haren, J., Pereira, AL., Liu, Z., Akinci, U., Nikolic, T., van Ijcken, W., van den Hout, M., Meinders, M., Melo, C., Sambade, C., Drabek, D., Hendriks, RW., Philipsen, S., Mommaas, M., Grosveld, F., Maiato, H., Italiano, JE. Jr., Robin, C., Galjart, N. Cell Reports 2, 781-788 (2012) Drabek + Suppl Cell reports 2012
  • Embryonic development of hematopoietic stem cells: implications for clinical use. Clapes, T. and Robin, C. Regenerative Medicine 7, 349-368 (2012) Clapes reg med 2012

2011

  • Ex vivo time-lapse confocal imaging of the mouse embryo aorta. Boisset, J.C., Andrieu-Soler, C., van Cappellen, W., Clapes, T., Robin, C. Nature Protocols 6, 1792-1805 (2011) Boisset Nat Prot 2011
  • Endothelial origin of hematopoietic stem cells: the proof in image | [Origine endothéliale des cellules souches hématopoïétiques: la preuve en image]. Boisset, J.C., and Robin, C. Médecine/Sciences 27, 875-81 (2011) Boisset med sci 2011
  • Fast-forward: The fourth dimension in development. Dzierzak, E., and Robin, C. Development 138, 3-5 (2011)
  • On the origin of hematopoietic stem cells: Progress and controversy. Boisset, J.C., and Robin, C. Stem Cell Research 8, 1–13 (2011) Boisset Stem cell research 2011
  • CD41 is developmentally regulated and differentially expressed on mouse hematopoietic stem cells. Robin, C.*, Ottersbach, K.*, Boisset, J.C., Oziemlak, A., Dzierzak, E. Blood 117, 5088-5091 (2011) Robin Blood 2011
  • Stem cell self-renewal: lessons from bone marrow, gut and iPS toward clinical applications. Staal, F.J., Baum, C., Cowan, C., Dzierzak, E., Hacein-Bey-Abina, S., Karlsson, S., Lapidot, T., Lemischka, I., Mendez-Ferrer, S., Mikkers, H., Moore, K., Moreno, E., Mummery, C.L., Robin, C., Suda, T., Van Pel, M., Vanden Brink, G., Zwaginga, J.J., Fibbe W.E. Leukemia 25, 1095-1102 (2011) Staal Leukemia 2011

2010

  • In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Boisset, J.C., van Cappellen, W., Andrieu-Soler, C., Galjart, N., Dzierzak, E., Robin, C. Nature 464, 116-120 (2010) Boisset nature 2010
  • Imaging the founder of adult hematopoiesis in the mouse embryo aorta. Boisset, J.C., and Robin, C. Cell Cycle 9, 2489-2490 (2010) Boisset Cell cycle 2010
  • Placenta as a source of hematopoietic stem cells. Dzierzak, E., and Robin, C. Trends in Molecular Medicine 16, 361-367 (2010) Dzierzak Trend in mol med 2010
  • The roles of BMP and IL-3 signaling pathways in the control of hematopoietic stem cells in the mouse embryo. Robin, C. and Durand, C. International Journal of Developmental Biology 54, 1189-1200 (2010) Robin int J Dev Biol 2010
  • Preparation of hematopoietic stem and progenitor cells from the human placenta. Robin, C., and Dzierzak, E. Current Protocols Stem Cell Biology Chapter 2, Unit 2A 9 (2010)

2009

  • Human placenta is a potent hematopoietic niche containing hematopoietic stem and progenitor cells throughout development. Robin, C.*, Bollerot, K.*, Mendes, S.*, Haak, E., Crisan, M., Cerisoli, F., Lauw, I., Kaimakis, P., Jorna, R., Vermeulen, M., Kayser, M., van der Linden, R., Imanirad, P., Verstegen, M., Nawaz-Yousaf, H., Papazian, N., Steegers, E., Cupedo, T., Dzierzak, E. Cell Stem Cell 5, 385-395 (2009) Robin Cell stem cell 2009

2008

  • The hematopoietic microenvironment of the AGM (Aorta-Gonads-Mesonephros) region: Molecular and cellular aspects | [Le microenvironnement hématopoïétique de la région AGM (Aorte-Gonade-Mésonephros): Aspects moléculaires et cellulaires]. Durand, C., Robin, C., Bollérot, K., Baron, M., Ottersbach, K., Dzierzak, E. Reproduction Humaine et Hormones 21, 246-250 (2008)

2007

  • Embryonic stromal clones reveal developmental regulators of definitive hematopoietic stem cells. Durand, C.*, Robin, C.*, Bollerot, K., Baron, M.H., Ottersbach, K., Dzierzak, E.  Proceedings of the National Academy of Sciences U S A 104, 20838-20843 (2007) Durand PNAS 2007

2006

  • Mesenchymal lineage potentials of aorta-gonad-mesonephros stromal clones. Durand, C., Robin, C., Dzierzak, E. Haematologica 91, 1172-1179 (2006) Durand Haematologica 2006
  • An unexpected role for IL-3 in the embryonic development of hematopoietic stem cells. Robin, C., Ottersbach, K., Durand, C., Peeters, M., Vanes, L., Tybulewicz, V., Dzierzak, E. Developmental Cell 11, 171-180 (2006) Robin Dev cell 2006

2005

  • Mesenchymal progenitor cells localize within hematopoietic sites throughout ontogeny. Mendes, S.C., Robin, C., Dzierzak, E. Development 132, 1127-1136 (2005) Mendes Dev 2005
  • Long-term maintenance of hematopoietic stem cells does not require contact with embryo-derived stromal cells in cocultures. Oostendorp, R.A., Robin, C., Steinhoff, C., Marz, S., Brauer, R., Nuber, U.A., Dzierzak, E.A., Peschel, C. Stem Cells 23, 842-851 (2005) Oostendorp Stem cells 2005
  • Multipotential hematopoietic progenitor cells from embryos developed in vitro engraft unconditioned W41/W41 neonatal miceB. Peeters, M., Ling, K.W., Oziemlak, A., Robin, C., Dzierzak, E. Haematologica 90, 734-739 (2005) Peeters Haematologica 2005
  • Hematopoietic stem cell enrichment from the AGM region of the mouse embryo. Robin, C., and Dzierzak, E. Methods in Molecular Medicine 105, 257-272 (2005)

2003

  • Developmental origins of hematopoietic stem cells. Robin, C., Ottersbach, K., de Bruijn, M., Ma, X., van der Horn, K., Dzierzak, E. Oncology Research 13, 315-321 (2003)

2002

  • Expression of the Ly-6A (Sca-1) lacZ transgene in mouse haematopoietic stem cells and embryos. Ma, X., de Bruijn, M., Robin, C., Peeters, M., Kong, A.S.J., de Wit, T., Snoijs, C., Dzierzak, E. British Journal of Haematology 116, 401-408 (2002) Ma Br J Haematol 2002
  • The Ly-6A (Sca-1) GFP transgene is expressed in all adult mouse hematopoietic stem cells. Ma, X., Robin, C., Ottersbach, K., Dzierzak, E. Stem Cells 20, 514-521 (2002) Ma Stem cell 2002
  • Successful transduction of human multipotent, lymphoid (T, B, NK) and myeloid, and transplantable CD34+CD38low cord blood cells using a murine oncoretroviral vector. Ravet, E., Dubart-Kupperschmitt, A., Robin, C., Titeux, M., Coulombel, L., Pflumio, F.  Journal of Hematotherapy and Stem Cell Research 11, 327-336 (2002)
  • Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. North, T.E., de Bruijn, M.F., Stacy, T., Talebian, L., Lind, E., Robin, C., Binder, M., Dzierzak, E., Speck, N.A. Immunity 16, 661-672 (2002) North Immunity 2002
  • Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. de Bruijn, M.F.*, Ma, X.*, Robin, C.*, Ottersbach, K., Sanchez, M.J., Dzierzak, E. Immunity 16, 673-683 (2002) deBruijn Immunity 2002

2001

  • Different expression of CD41 on human lymphoid and myeloid progenitors from adults and neonates. Debili, N., Robin, C., Schiavon, V., Letestu, R., Pflumio, F., Mitjavila-Garcia, M.T., Coulombel, L., Vainchenker, W. Blood 97, 2023-2030 (2001)
  • The human embryo, but not its yolk sac, generates lympho-myeloid stem cells: mapping multipotent hematopoietic cell fate in intraembryonic mesoderm. Tavian, M., Robin, C., Coulombel, L., Peault, B. Immunity 15, 487-495 (2001) Tavian Immunity 2001

2000

  • [The hemangioblast, common precursor of endothelial and hematopoietic cells]; L’hemangioblaste, precurseur commun des cellules endotheliales et hematopoietiques. Tavian, M., Cortes, F., Robin, C., Schiavon, V., Hallais, M.F., Coulombel, L., Charbord, P., Labastie, M.C., Peault, B. Transfusion Clinique et Biologique 7, 238-241 (2000)

1999

  • Identification of human T-lymphoid progenitor cells in CD34+CD38low and CD34+CD38+ subsets of human cord blood and bone marrow cells using NOD-SCID fetal thymus organ cultures. Robin, C., Bennaceur-Griscelli, A., Louache, F., Vainchenker, W., Coulombel, L. British Journal of Haematology 104, 809-819 (1999)
  • Identification of lymphomyeloid primitive progenitor cells in fresh human cord blood and in the marrow of nonobese diabetic-severe combined immunodeficient (NOD-SCID) mice transplanted with human CD34+ cord blood cells. Robin, C., Pflumio, F., Vainchenker, W., Coulombel, L. Journal of Experimental Medicine 189, 1601-1610 (1999) Robin J Exp Med 1999
  • The NOD-SCID model to assess human hematopoietic stem cell function | [Transplantation de cellules hematopoietiques humaines in vivo III – Qu’attendre du module de transplantation par voie intraveineuse chez les souris NOD-SCID?]. Pflumio, F., Tourino, C., Robin, C., Coulombel, L., Rouches, A., Ardouin, P. Hematologie 5, 20-30 (1999)

1998

  • NK cells differentiated from bone marrow, cord blood and peripheral blood stem cells exhibit similar phenotype and functions. Carayol, G., Robin, C., Bourhis, J.H., Bennaceur-Griscelli, A., Chouaib, S., Coulombel, L., Caignard, A. European Journal of Immunology 28, 1991-2002 (1998)