Robin: Hematopoiesis and stem cells during embryonic development

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The Robin group studies the cellular and molecular mechanisms that lead to the production and expansion of hematopoietic stem cells during embryonic development.

Figure 1: Intra-aortic hematopoietic clusters attached to the endothelial layer of the mouse embryonic aorta (Orange: CD31)

Hematopoietic stem cells (HSCs) are self-renewing multipotent cells that produce all blood cell types during the entire life of an individual. Hence, they are the only cell type that can be used to replenish the bone marrow in patients with blood-related disorders. One major challenge in the field of stem cell research is to generate large quantities of these very rare cells in vitro for research and clinical use. This is extremely difficult at present because all steps leading to HSC generation in vivo, and the precise role of the supportive surrounding microenvironment, are far from been elucidated yet. The overall research goal of the lab is to elucidate the cellular and molecular events leading to HSC production and expansion during embryonic development. We notably focus on understanding the origin of HSCs during embryonic development, the mechanisms implicated in HSC generation and expansion, the composition and function of the different HSC niches during ontogeny, and the cellular and molecular signature of HSCs and precursors.

Key publicationsView all publications

Progressive maturation toward hematopoietic stem cells in the mouse embryo aorta

Boisset JC, Clapes T, Klaus A, Papazian N, Onderwater J, Mommaas-Kienhuis M, Cupedo T, Robin C.

Blood 125, 465-469

Download|2015

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 Rep 2, 781-788

Download|2012

Ex vivo time-lapse confocal imaging of the mouse embryo aorta

Boisset JC, Andrieu-Soler C, van Cappellen W, Clapes T, Robin C.

Nature Protocols 6, 1792-1805

Download|2011

In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium

Boisset JC, van Cappellen W, Andrieu-Soler C, Galjart N, Dzierzak E, Robin C.

Nature 464, 116-120

Download|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 H, Papazian N, Steegers E, Cupedo T, Dzierzak E.

Cell Stem Cell 5, 385-395

Download|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.

Dev Cell 11, 171-180

Download|2006

Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta

de Bruijn MF*, Ma X*, Robin C*, Ottersbach K, Sanchez MJ, Dzierzak E.

Immunity 16, 673-683

Download|2002

Other publications

Single-cell sequencing reveals dissociation-induced gene expression in tissue subpopulations

van den Brink, S.C., Sage, F., Vértesy, Á., Spanjaard, B., Peterson-Maduro, J., Baron, C.S., Robin, C. , van Oudenaarden, A.

Nature Methods 14, 935-936

Download|2017

Developmental Biology 428, 318-327

Download|2017

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

Download|2016

Cardiovascular Research 107, 352-363

Download|2015

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

Download|2015

Biology Open 2, 525-532

Download|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

Download|2013

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

Download|2012

Regenerative Medicine 7, 349-368

2012

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

Download|2011

Médecine/Sciences 27, 875-81

2011

Development 138, 3-5

2011

Stem Cell Research 8, 1–13

Download|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

Download|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

Download|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

Download|2010

Cell Cycle 9, 2489-2490

Download|2010

Trends in Molecular Medicine 16, 361-367

Download|2010

International Journal of Developmental Biology 54, 1189-1200

Download|2010

Current Protocols Stem Cell Biology Chapter 2, Unit 2A 9

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, H., Papazian, N., Steegers, E., Cupedo, T., Dzierzak, E.

Cell Stem Cell 5, 385-395

Download|2009

The hematopoietic microenvironment of the AGM (Aorta-Gonads-Mesonephros) region: Molecular and cellular aspects

Durand, C., Robin, C., Bollérot, K., Baron, M., Ottersbach, K., Dzierzak, E.

Reproduction Humaine et Hormones 21, 246-250

2008

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

Download|2007

Haematologica 91, 1172-1179

Download|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

Download|2006

Development 132, 1127-1136

Download|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

Download|2005

Haematologica 90, 734-739

Download|2005

Methods in Molecular Medicine 105, 257-272

2005

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

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

Download|2002

Stem Cells 20, 514-521

Download|2002

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

Download|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

Download|2002

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

Download|2001

The hemangioblast, common precursor of endothelial and hematopoietic cells

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

Download|2000

British Journal of Haematology 104, 809-819

Download|1999

The NOD-SCID model to assess human hematopoietic stem cell function

Pflumio, F., Tourino, C., Robin, C., Coulombel, L., Rouches, A., Ardouin, P.

Hematologie 5, 20-30

1999

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

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Group leader

Catherine Robin

Catherine Robin is group leader at the Hubrecht Institute and is also appointed at the University Medical Center Utrecht. Her group focuses on the establishment of the hematopoietic system during embryonic development. They are particularly interested in better understanding how the first hematopoietic stem cells, the very rare cells at the foundation of the entire adult blood system, are generated and regulated during embryonic development. To answer these fundamental questions, the Robin group uses state-of-the-art technology and methods, including time-lapse live confocal imaging, in vivo transplantation and single-cell RNA sequencing.

Scientific training and positions

Current other activities


Group members

Catherine Robin

Principal Investigator

Carla Veenboer

Technician

Joris Maas

Technician

Laurent Yvernogeau

Postdoc

Ismael Morin-Poulard

Postdoc

Anna Klaus

PhD Student

Manon Molenaar

Student

Johnsons Sulter

Student

2018 – EMBL conference – Hematopoietic stem cells: From the embryo to the aging organism