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ZFIN ID: ZDB-LAB-970903-4
Herbomel Lab
PI/Director: Herbomel, Philippe
Co-PI / Senior
Colucci-Guyon, Emma
Levraud, Jean-Pierre
Murayama, Emi
Schmidt, Anne
Contact Person: Herbomel, Philippe
Address: 'Macrophages & Development of Immunity' Lab Department of Developmental & Stem Cell Biology Institut Pasteur 25 rue du Dr Roux Paris, 75724 cedex 15 France
Country: France
Phone: 33-1-44-38-95-29
Fax: 33-1-40-61-34-40
Line Designation: ip

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In vivo analysis of cell behaviours in embryogenesis; primitive macrophages, granulocytes; developmental hematopoiesis, from stem cell emergence to niches, to tissue leukocytes; microglia; innate immunity; phagocytes-microbes interactions; host responses to viral infection;

Demy, Doris-Lou Post-Doc Hernández-Cerda, Pedro Post-Doc Torcq, Léa Graduate Student
Touret, Anne-Lou Graduate Student Boucontet, Laurent Technical Staff Majello, Sara Technical Staff
Rolin, Yohann Technical Staff Vivier, Catherine Technical Staff Boutout, Laurence Administrative Staff
Laghi, Valerio

Blokzijl-Franke, S., Ponsioen, B., Schulte-Merker, S., Herbomel, P., Kissa, K., Choorapoikayil, S., den Hertog, J. (2021) Phosphatidylinositol-3 kinase signaling controls survival and stemness of hematopoietic stem and progenitor cells. Oncogene. 40(15):2741-2755
Rességuier, J., Levraud, J.P., Dal, N.K., Fenaroli, F., Primard, C., Wohlmann, J., Carron, G., Griffiths, G.W., Le Guellec, D., Verrier, B. (2021) Biodistribution of surfactant-free poly(lactic-acid) nanoparticles and uptake by endothelial cells and phagocytes in zebrafish: Evidence for endothelium to macrophage transfer. Journal of controlled release : official journal of the Controlled Release Society. 331:228-245
Colucci-Guyon, E., Rifflet, A., Saint-Auret, S., da Costa, A., Boucontet, L., Laval, T., Prehaud, C., Blanchard, N., Levraud, J.P., Boneca, I.G., Demangel, C., Guenin-Macé, L. (2020) Spatiotemporal analysis of mycolactone distribution in vivo reveals partial diffusion in the central nervous system. PLoS neglected tropical diseases. 14:e0008878
Widziolek, M., Janik, K., Mojzesz, M., Pooranachandran, N., Adamek, M., Pecio, A., Surachetpong, W., Levraud, J.P., Boudinot, P., Chadzinska, M., Rakus, K. (2020) Type I interferon-dependent response of zebrafish larvae during tilapia lake virus (TiLV) infection. Developmental and comparative immunology. 116:103936
Stressmann, F.A., Bernal-Bayard, J., Perez-Pascual, D., Audrain, B., Rendueles, O., Briolat, V., Bruchmann, S., Volant, S., Ghozlane, A., Häussler, S., Duchaud, E., Levraud, J.P., Ghigo, J.M. (2020) Mining zebrafish microbiota reveals key community-level resistance against fish pathogen infection. The ISME Journal. 15(3):702-719
Demy, D.L., Carrère, M., Noche, R., Tauzin, M., Le Bris, M., Baek, C., Leshchiner, I., Goessling, W., Herbomel, P. (2020) The cationic amino acid exporter Slc7a7 is induced and vital in tissue macrophages with sustained efferocytic activity. Journal of Cell Science. 133(20):
Demy, D.L., Campanari, M.L., Munoz-Ruiz, R., Durham, H.D., Gentil, B.J., Kabashi, E. (2020) Functional Characterization of Neurofilament Light Splicing and Misbalance in Zebrafish. Cells. 9(5):
Maarifi, G., Smith, N., Maillet, S., Moncorgé, O., Chamontin, C., Edouard, J., Sohm, F., Blanchet, F.P., Herbeuval, J.P., Lutfalla, G., Levraud, J.P., Arhel, N.J., Nisole, S. (2019) TRIM8 is required for virus-induced IFN response in human plasmacytoid dendritic cells. Science advances. 5:eaax3511
Bowes, C., Redd, M., Yousfi, M., Tauzin, M., Murayama, E., Herbomel, P. (2019) Coronin 1A depletion restores the nuclear stability and viability of Aip1/Wdr1-deficient neutrophils. The Journal of cell biology. 218(10):3258-3271
Levraud, J.P., Herbomel, P. (2019) Resident Macrophage Lookalikes of Unexpected Origin. Developmental Cell. 49:501-502
Lavalou, P., Eckert, H., Damy, L., Constanty, F., Majello, S., Bitetti, A., Graindorge, A., Shkumatava, A. (2019) Strategies for Genetic Inactivation of Long Noncoding RNAs in Zebrafish. RNA (New York, N.Y.). 25(8):897-904
Colucci-Guyon, E., Batista, A.S., Oliveira, S.D.S., Blaud, M., Bellettini, I.C., Marteyn, B.S., Leblanc, K., Herbomel, P., Duval, R. (2019) Ultraspecific live imaging of the dynamics of zebrafish neutrophil granules by a histopermeable fluorogenic benzochalcone probe. Chemical science. 10:3654-3670
Verweij, F.J., Revenu, C., Arras, G., Dingli, F., Loew, D., Pegtel, M.D., Follain, G., Allio, G., Goetz, J.G., Zimmermann, P., Herbomel, P., Del Bene, F., Raposo, G., van Niel, G. (2019) Live Tracking of Inter-organ Communication by Endogenous Exosomes In Vivo. Developmental Cell. 48(4):573-589.e4
Langevin, C., Levraud, J.P., Boudinot, P. (2018) Fish antiviral tripartite motif (TRIM) proteins. Fish & shellfish immunology. 86:724-733
Hernández, P.P., Strzelecka, P.M., Athanasiadis, E.I., Hall, D., Robalo, A.F., Collins, C.M., Boudinot, P., Levraud, J.P., Cvejic, A. (2018) Single-cell transcriptional analysis reveals ILC-like cells in zebrafish. Science immunology. 3(29):
Lancino, M., Majello, S., Herbert, S., De Chaumont, F., Tinevez, J.Y., Olivo-Marin, J.C., Herbomel, P., Schmidt, A. (2018) Anisotropic organization of circumferential actomyosin characterizes hematopoietic stem cells emergence in the zebrafish. eLIFE. 7:
Phan, Q.T., Sipka, T., Gonzalez, C., Levraud, J.P., Lutfalla, G., Nguyen-Chi, M. (2018) Neutrophils use superoxide to control bacterial infection at a distance. PLoS pathogens. 14:e1007157
Boucontet, L., Passoni, G., Thiry, V., Maggi, L., Herbomel, P., Levraud, J.P., Colucci-Guyon, E. (2018) A Model of Superinfection of Virus-Infected Zebrafish Larvae: Increased Susceptibility to Bacteria Associated With Neutrophil Death. Frontiers in immunology. 9:1084
Demy, D.L., Tauzin, M., Lancino, M., le Cabec, V., Redd, M., Murayama, E., Maridonneau-Parini, I., Trede, N., Herbomel, P. (2017) Trim33 / Tif1-γ is essential for macrophage and neutrophil mobilisation to developmental or inflammatory cues. Journal of Cell Science. 130(17):2797-2807
Passoni, G., Langevin, C., Palha, N., Mounce, B.C., Briolat, V., Affaticati, P., De Job, E., Joly, J.S., Vignuzzi, M., Saleh, M.C., Herbomel, P., Boudinot, P., Levraud, J.P. (2017) Imaging of viral neuroinvasion in the zebrafish reveals that Sindbis and chikungunya viruses favour different entry routes. Disease models & mechanisms. 10(7):847-857
Mazon-Moya, M.J., Willis, A.R., Torraca, V., Boucontet, L., Shenoy, A.R., Colucci-Guyon, E., Mostowy, S. (2017) Septins restrict inflammation and protect zebrafish larvae from Shigella infection. PLoS pathogens. 13:e1006467
Langevin, C., Aleksejeva, E., Houel, A., Briolat, V., Torhy, C., Lunazzi, A., Levraud, J.P., Boudinot, P. (2017) FTR83, a Member of the Large Fish-Specific finTRIM Family, Triggers IFN Pathway and Counters Viral Infection. Frontiers in immunology. 8:617
Rességuier, J., Delaune, E., Coolen, A.L., Levraud, J.P., Boudinot, P., Le Guellec, D., Verrier, B. (2017) Specific and Efficient Uptake of Surfactant-Free Poly(Lactic Acid) Nanovaccine Vehicles by Mucosal Dendritic Cells in Adult Zebrafish after Bath Immersion. Frontiers in immunology. 8:190
Delmaghani, S., Aghaie, A., Bouyacoub, Y., El Hachmi, H., Bonnet, C., Riahi, Z., Chardenoux, S., Perfettini, I., Hardelin, J.P., Houmeida, A., Herbomel, P., Petit, C. (2016) Mutations in CDC14A, Encoding a Protein Phosphatase Involved in Hair Cell Ciliogenesis, Cause Autosomal-Recessive Severe to Profound Deafness. American journal of human genetics. 98:1266-1270
Aleksejeva, E., Houel, A., Briolat, V., Levraud, J.P., Langevin, C., Boudinot, P. (2016) Zebrafish Plzf transcription factors enhance early type I IFN response induced by two non-enveloped RNA viruses. Developmental and comparative immunology. 57:48-56
Murayama, E., Sarris, M., Redd, M., Le Guyader, D., Vivier, C., Horsley, W., Trede, N., Herbomel, P. (2015) NACA deficiency reveals the crucial role of somite-derived stromal cells in haematopoietic niche formation. Nature communications. 6:8375
Kasher, P.R., Jenkinson, E.M., Briolat, V., Gent, D., Morrissey, C., Zeef, L.A., Rice, G.I., Levraud, J.P., Crow, Y.J. (2015) Characterization of samhd1 Morphant Zebrafish Recapitulates Features of the Human Type I Interferonopathy Aicardi-Goutières Syndrome. Journal of immunology (Baltimore, Md. : 1950). 194(6):2819-25
Mazon Moya, M.J., Colucci-Guyon, E., Mostowy, S. (2014) Use of Shigella flexneri to Study Autophagy-Cytoskeleton Interactions. Journal of visualized experiments : JoVE. (91):e51601
Levraud, J.P., Palha, N., Langevin, C., Boudinot, P. (2014) Through the looking glass: witnessing host-virus interplay in zebrafish. Trends in microbiology. 22(9):490-497
Nguyen-Chi, M., Phan, Q.T., Gonzalez, C., Dubremetz, J.F., Levraud, J.P., Lutfalla, G. (2014) Transient infection of the zebrafish notochord with E. coli induces chronic inflammation. Disease models & mechanisms. 7:871-882
Elks, P.M., van der Vaart, M., van Hensbergen, V., Schutz, E., Redd, M.J., Murayama, E., Spaink, H.P., Meijer, A.H. (2014) Mycobacteria Counteract a TLR-Mediated Nitrosative Defense Mechanism in a Zebrafish Infection Model. PLoS One. 9:e100928
Briolat, V., Jouneau, L., Carvalho, R., Palha, N., Langevin, C., Herbomel, P., Schwartz, O., Spaink, H.P., Levraud, J.P., Boudinot, P. (2014) Contrasted Innate Responses to Two Viruses in Zebrafish: Insights into the Ancestral Repertoire of Vertebrate IFN-Stimulated Genes. Journal of immunology (Baltimore, Md. : 1950). 192:4328-41
Choorapoikayil, S., Kers, R., Herbomel, P., Kissa, K., and den Hertog, J. (2014) Pivotal role of Pten in the balance between proliferation and differentiation of hematopoietic stem cells in zebrafish. Blood.
Langevin, C., Aleksejeva, E., Passoni, G., Palha, N., Levraud, J.P., and Boudinot, P. (2013) The Antiviral Innate Immune Response in Fish: Evolution and Conservation of the IFN System. Journal of molecular biology. 425(24):4904-20
Recher, G., Jouralet, J., Brombin, A., Heuzé, A., Mugniery, E., Hermel, J.M., Desnoulez, S., Savy, T., Herbomel, P., Bourrat, F., Peyriéras, N., Jamen, F., and Joly, J.S. (2013) Zebrafish midbrain slow-amplifying progenitors exhibit high levels of transcripts for nucleotide and ribosome biogenesis. Development (Cambridge, England). 140(24):4860-9
Langevin, C., van der Aa, L.M., Houel, A., Torhy, C., Briolat, V., Lunazzi, A., Harmache, A., Bremont, M., Levraud, J.P., and Boudinot, P. (2013) Zebrafish ISG15 exerts a strong anti-viral activity against RNA and DNA viruses and regulates the interferon response. Journal of virology. 87(18):10025-36
Deng, Q., Sarris, M., Bennin, D.A., Green, J.M., Herbomel, P., and Huttenlocher, A. (2013) Localized bacterial infection induces systemic activation of neutrophils through Cxcr2 signaling in zebrafish. Journal of Leukocyte Biology. 93(5):761-9
Demy, D.L., Ranta, Z., Giorgi, J.M., Gonzalez, M., Herbomel, P., and Kissa, K. (2013) Generating parabiotic zebrafish embryos for cell migration and homing studies. Nature Methods. 10(3):256-258
Mostowy, S., Boucontet, L., Mazon Moya, M.J., Sirianni, A., Boudinot, P., Hollinshead, M., Cossart, P., Herbomel, P., Levraud, J.P., and Colucci-Guyon, E. (2013) The Zebrafish as a New Model for the In Vivo Study of Shigella flexneri Interaction with Phagocytes and Bacterial Autophagy. PLoS pathogens. 9(9):e1003588
Palha, N., Guivel-Benhassine, F., Briolat, V., Lutfalla, G., Sourisseau, M., Ellett, F., Wang, C.H., Lieschke, G.J., Herbomel, P., Schwartz, O., and Levraud, J.P. (2013) Real-time whole-body visualization of chikungunya virus infection and host interferon response in zebrafish. PLoS pathogens. 9(9):e1003619
Prudent, J., Popgeorgiev, N., Bonneau, B., Thibaut, J., Gadet, R., Lopez, J., Gonzalo, P., Rimokh, R., Manon, S., Houart, C., Herbomel, P., Aouacheria, A., and Gillet, G. (2013) Bcl-wav and the mitochondrial calcium uniporter drive gastrula morphogenesis in zebrafish. Nature communications. 4:2330
Sarris, M., Masson, J.B., Maurin, D., Van der Aa, L.M., Boudinot, P., Lortat-Jacob, H., and Herbomel, P. (2012) Inflammatory Chemokines Direct and Restrict Leukocyte Migration within Live Tissues as Glycan-Bound Gradients. Current biology : CB. 22(24):2375-2382
van der Aa, L.M., Chadzinska, M., Derks, W., Scheer, M., Levraud, J.P., Boudinot, P., and Lidy Verburg-van Kemenade, B.M. (2012) Diversification of IFNγ-inducible CXCb chemokines in cyprinid fish. Developmental and comparative immunology. 38(2):243-253
Herbomel, P. (2012) Infection-induced hematopoiesis: a zebrafish perspective. Cell Stem Cell. 10(2):105-106
Rendueles, O., Ferrières, L., Frétaud, M., Bégaud, E., Herbomel, P., Levraud, J.P., and Ghigo, J.M. (2012) A new zebrafish model of Oro-intestinal pathogen colonization reveals a key role for adhesion in protection by probiotic bacteria. PLoS pathogens. 8(7):e1002815
Renaud, O., Herbomel, P., and Kissa, K. (2011) Studying cell behavior in whole zebrafish embryos by confocal live imaging: application to hematopoietic stem cells. Nature Protocols. 6(12):1897-1904
Colucci-Guyon, E., Tinevez, J.Y., Renshaw, S.A., and Herbomel, P. (2011) Strategies of professional phagocytes in vivo: unlike macrophages, neutrophils engulf only surface-associated microbes. Journal of Cell Science. 124(Pt 18):3053-9
Hamming, O.J., Lutfalla, G., Levraud, J.P., and Hartmann, R. (2011) Crystal structure of zebrafish Interferons 1 and 2 reveals a conservation of type I Interferon structure in vertebrates. Journal of virology. 85(16):8181-7
Kaneko, T., Iwamoto, S., Murayama, E., Kurio, H., Inai, T., Oda, S., and Iida, H. (2011) Immunolocalization of Spetex-1 at the Connecting Piece in Spermatozoa of the Musk Shrew (Suncus murinus). Zoological science. 28(6):444-452
Ludwig, M., Palha, N., Torhy, C., Briolat, V., Colucci-Guyon, E., Brémont, M., Herbomel, P., Boudinot, P., and Levraud, J.P. (2011) Whole-Body Analysis of a Viral Infection: Vascular Endothelium is a Primary Target of Infectious Hematopoietic Necrosis Virus in Zebrafish Larvae. PLoS pathogens. 7(2):e1001269
Boudinot, P., van der Aa, L.M., Jouneau, L., Du Pasquier, L., Pontarotti, P., Briolat, V., Benmansour, A., and Levraud, J.P. (2011) Origin and Evolution of TRIM Proteins: New Insights from the Complete TRIM Repertoire of Zebrafish and Pufferfish. PLoS One. 6(7):e22022
Aggad, D., Stein, C., Sieger, D., Mazel, M., Boudinot, P., Herbomel, P., Levraud, J.P., Lutfalla, G., and Leptin, M. (2010) In Vivo Analysis of Ifn-γ1 and Ifn-γ2 Signaling in Zebrafish. Journal of immunology (Baltimore, Md. : 1950). 185(11):6774-6782
Keller, P.J., Schmidt, A.D., Santella, A., Khairy, K., Bao, Z., Wittbrodt, J., and Stelzer, E.H. (2010) Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy. Nature Methods. 7(8):637-642
Kissa, K., and Herbomel, P. (2010) Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature. 464(7285):112-115
Aggad, D., Mazel, M., Boudinot, P., Mogensen, K.E., Hamming, O.J., Hartmann, R., Kotenko, S., Herbomel, P., Lutfalla, G., and Levraud, J.P. (2009) The two groups of zebrafish virus-induced interferons signal via distinct receptors with specific and shared chains. Journal of immunology (Baltimore, Md. : 1950). 183(6):3924-3931
Levraud, J.P., Disson, O., Kissa, K., Bonne, I., Cossart, P., Herbomel, P., and Lecuit, M. (2009) Real-time observation of Listeria-phagocyte interactions in the living zebrafish larva. Infection and Immunity. 77(9):3651-3660
van der Aa, L.M., Levraud, J.P., Yahmi, M., Lauret, E., Briolat, V., Herbomel, P., Benmansour, A., and Boudinot, P. (2009) A large new subset of TRIM genes highly diversified by duplication and positive selection in teleost fish. BMC Biology. 7:7
Olivari, F.A., Hernández, P.P., and Allende, M.L. (2008) Acute copper exposure induces oxidative stress and cell death in lateral line hair cells of zebrafish larvae. Brain research. 1244:1-12
Hernández, P.P., and Allende, M.L. (2008) Zebrafish (Danio rerio) as a model for studying the genetic basis of copper toxicity, deficiency, and metabolism. The American journal of clinical nutrition. 88(3):835S-839S
Kissa, K., Murayama, E., Zapata, A., Cortes, A., Perret, E., Machu, C., and Herbomel, P. (2008) Live imaging of emerging hematopoietic stem cells and early thymus colonization. Blood. 111(3):1147-1156
Le Guyader, D., Redd, M.J., Colucci-Guyon, E., Murayama, E., Kissa, K., Briolat, V., Mordelet, E., Zapata, A., Shinomiya, H., and Herbomel, P. (2008) Origins and unconventional behavior of neutrophils in developing zebrafish. Blood. 111(1):132-141
Levraud, J.P., Colucci-Guyon, E., Redd, M.J., Lutfalla, G., and Herbomel, P. (2008) In Vivo Analysis of Zebrafish Innate Immunity. Methods in molecular biology (Clifton, N.J.). 415:337-363
Lepiller, S., Laurens, V., Bouchot, A., Herbomel, P., Solary, E., and Chluba, J. (2007) Imaging of nitric oxide in a living vertebrate using a diaminofluorescein probe. Free radical biology & medicine. 43(4):619-627
Kissa, K., Murayama, E., and Herbomel, P. (2007) The zebrafish reveals the odyssey of hematopoietic precursors in developing vertebrate embryos. Medecine sciences : M/S. 23(8-9):698-700
Levraud, J.P., Boudinot, P., Colin, I., Benmansour, A., Peyriéras, N., Herbomel, P., and Lutfalla, G. (2007) Identification of the Zebrafish IFN Receptor: Implications for the Origin of the Vertebrate IFN System. Journal of immunology (Baltimore, Md. : 1950). 178(7):4385-4394
Murayama, E., Kissa, K., Zapata, A., Mordelet, E., Briolat, V., Lin, H.F., Handin, R.I., and Herbomel, P. (2006) Tracing Hematopoietic Precursor Migration to Successive Hematopoietic Organs during Zebrafish Development. Immunity. 25(6):963-975
Tohse, H., Murayama, E., Ohira, T., Takagi, Y., and Nagasawa, H. (2006) Localization and diurnal variations of carbonic anhydrase mRNA expression in the inner ear of the rainbow trout Oncorhynchus mykiss. Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology. 145(3-4):257-264
Murayama, E., Herbomel, P., Kawakami, A., Takeda, H., and Nagasawa H. (2005) Otolith matrix proteins OMP-1 and Otolin-1 are necessary for normal otolith growth and their correct anchoring onto the sensory maculae. Mechanisms of Development. 122(6):791-803
Herbomel, P., and Levraud, J.P. (2005) Imaging Early Macrophage Differentiation, Migration, and Behaviors in Live Zebrafish Embryos. Methods in molecular medicine. 105:199-214
Mathieu, J., Griffin, K., Herbomel, P., Dickmeis, T., Strähle, U., Kimelman, D., Rosa, F.M., and Peyriéras, N. (2004) Nodal and Fgf pathways interact through a positive regulatory loop and synergize to maintain mesodermal cell populations. Development (Cambridge, England). 131(3):629-641
Traver, D., Herbomel, P., Patton, E.E., Murphey, R.D., Yoder, J.A., Litman, G.W., Catic, A., Amemiya, C.T., Zon, L.I., and Trede, N.S. (2003) The zebrafish as a model organism to study development of the immune system. Advances in immunology. 81:253-330
Davis, J.M., Clay, H., Lewis, J.L., Ghori, N., Herbomel, P., and Ramakrishnan, L. (2002) Real-time visualization of mycobacterium-macrophage interactions leading to initiation of granuloma formation in zebrafish embryos. Immunity. 17(6):693-702
Herbomel, P., Thisse, B., and Thisse, C. (2001) Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Developmental Biology. 238(2):274-288
Herbomel, P. (1999) Spinning nuclei in the brain of the zebrafish embryo. Current biology : CB. 9(17):R627-R628
Herbomel, P., Thisse, B., and Thisse, C. (1999) Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development (Cambridge, England). 126(17):3735-3745