TNF signaling and macrophages govern fin regeneration in zebrafish larvae
Open accessAbstract
Macrophages are essential for appendage regeneration after amputation in regenerative species. The molecular mechanisms through which macrophages orchestrate blastema formation and regeneration are still unclear. Here, we use the genetically tractable and transparent zebrafish larvae to study the functions of polarized macrophage subsets during caudal fin regeneration. After caudal fin amputation, we show an early and transient accumulation of pro-inflammatory macrophages concomitant with the accumulation of non-inflammatory macrophages which, in contrast to pro-inflammatory macrophages, remain associated to the fin until the end of the regeneration. Chemical and genetic depletion of macrophages suggested that early recruited macrophages that express TNF α are critical for blastema formation. Combining parabiosis and morpholino knockdown strategies, we show that TNF α/TNFR1 signaling pathway is required for the fin regeneration. Our study reveals that TNFR1 has a necessary and direct role in blastema cell activation suggesting that macrophage subset balance provides the accurate TNF α signal to prime regeneration in zebrafish.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Death receptor signaling can also lead to NF-κB activation, generally resulting in cell survival associated with robust inflammatory response.
“Death receptor signaling can also lead to NF-κB activation, generally resulting in cell survival associated with a robust inflammatory response [272, 342].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [342]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Stages of embryonic development of the zebrafish
Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., & Schilling, T. F. (1995) · Developmental Dynamics · doi:10.1002/aja.1002030302 · Cited by 12,037 · see citing works
Macrophage plasticity and polarization: in vivo veritas
Sica, A., & Mantovani, A. (2012) · Journal of Clinical Investigation · doi:10.1172/jci59643 · Cited by 6,335 · see citing works
Alternative activation of macrophages
Gordon, S. (2003) · Nature Reviews Immunology · doi:10.1038/nri978 · Cited by 6,189 · see citing works
Macrophage biology in development, homeostasis and disease
Wynn, T. A., Chawla, A., & Pollard, J. W. (2013) · Nature · doi:10.1038/nature12034 · Cited by 4,684 · see citing works
Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm
Biswas, S. K., & Mantovani, A. (2010) · Nature Immunology · doi:10.1038/ni.1937 · Cited by 3,840 · see citing works
Arnold, L., Henry, A., Poron, F., Baba-Amer, Y., van Rooijen, N., Plonquet, A., Gherardi, R. K., & Chazaud, B. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20070075 · Cited by 2,002 · see citing works
Understanding the Mysterious M2 Macrophage through Activation Markers and Effector Mechanisms
Rőszer, T. (2015) · Mediators of Inflammation · doi:10.1155/2015/816460 · Cited by 1,762 · see citing works
A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish
Niethammer, P., Grabher, C., Look, A. T., & Mitchison, T. J. (2009) · Nature · doi:10.1038/nature08119 · Cited by 1,541 · see citing works
Inflammatory cells during wound repair: the good, the bad and the ugly
Martin, P., & Leibovich, S. J. (2005) · Trends in Cell Biology · doi:10.1016/j.tcb.2005.09.002 · Cited by 1,340 · cited 1× · see citing works
“Indeed, Pu.1 morpholino (MO) inhibiting the development of all myeloid lineage does not affect fin regeneration, whereas interferon regulatory factor 8 ( irf8 ) MO, which blocks the differentiation of macrophage lineage was reported to either delay or produce no effect on fin regeneration.”
mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish
Ellett, F. E., Pase, L. B., Hayman, J. W., Andrianopoulos, A., & Lieschke, G. J. (2010) · Blood · doi:10.1182/blood-2010-10-314120 · Cited by 1,085 · see citing works
A transgenic zebrafish model of neutrophilic inflammation
Renshaw, S. A., Loynes, C. A., Trushell, D. M. I., Elworthy, S., Ingham, P. W., & Whyte, M. K. B. (2006) · Blood · doi:10.1182/blood-2006-05-024075 · Cited by 1,013 · see citing works
Macrophages are required for adult salamander limb regeneration
Godwin, J. W., Pinto, A. R., & Rosenthal, N. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300290110 · Cited by 829 · see citing works
Regulation of Macrophage Polarization and Wound Healing
Ferrante, C., & Leibovich, S. (2012) · Advances in wound care · doi:10.1089/wound.2011.0307 · Cited by 578 · see citing works
The zebrafish as a model for complex tissue regeneration
Gemberling, M. P., Bailey, T. J., Hyde, D. R., & Poss, K. D. (2013) · Trends in Genetics · doi:10.1016/j.tig.2013.07.003 · Cited by 564 · see citing works
Bridging the regeneration gap: Genetic insights from diverse animal models
Alvarado, A. S., & Tsonis, P. A. (2006) · Nature Reviews Genetics · doi:10.1038/nrg1923 · Cited by 467 · see citing works
Davison, J. M., Akitake, C. M., Goll, M. G., Rhee, J. M., Gosse, N. J., Baier, H., Halpern, M. E., Leach, S. D., & Parsons, M. J. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.01.033 · Cited by 427 · see citing works
Saclier, M., Yacoub‐Youssef, H., Mackey, A. L., Arnold, L., Ardjoune, H., Magnan, M., Sailhan, F., Chelly, J., Pavlath, G. K., Mounier, R., et al. (2012) · Stem Cells · doi:10.1002/stem.1288 · Cited by 421 · see citing works
Recurrent turnover of senescent cells during regeneration of a complex structure
Yun, M. H., Davaapil, H., & Brockes, J. P. (2015) · eLife · doi:10.7554/elife.05505 · Cited by 385 · see citing works
Macrophages modulate adult zebrafish tail fin regeneration
Petrie, T. A., Strand, N. S., Tsung-Yang, C., Rabinowitz, J. S., & Moon, R. T. (2014) · Development · doi:10.1242/dev.098459 · Cited by 365 · see citing works
Li, L., Yan, B., Shi, Y.-Q., Zhang, W.-Q., & Wen, Z.-L. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.349126 · Cited by 353 · cited 3× · see citing works
“In our system TNF α promotes macrophage recruitment, presumably acting as an enhancing loop for macrophage accumulation to the wound (Figure 7).”
Old questions, new tools, and some answers to the mystery of fin regeneration
Akimenko, M., Marí‐Beffa, M., Becerra, J., & Géraudie, J. (2003) · Developmental Dynamics · doi:10.1002/dvdy.10248 · Cited by 316 · see citing works
Macrophages: Supportive cells for tissue repair and regeneration
Chazaud, B. (2013) · Immunobiology · doi:10.1016/j.imbio.2013.09.001 · Cited by 309 · see citing works
Pentoxifylline suppression of tumor necrosis factor gene transcription.
Doherty, G. M., Jensen, J. C., Alexander, H. R., Buresh, C. M., & Norton, J. A. (1991) · PubMed · Cited by 306 · see citing works
Identification of polarized macrophage subsets in zebrafish
Chi, M. N., Laplace-Builhe, B., Trávníčková, J., Luz‐Crawford, P., Téjédor, G., Phan, Q. T., Duroux-Richard, I., Levraud, J., Kissa, K., Lutfalla, G., et al. (2015) · eLife · doi:10.7554/elife.07288 · Cited by 295 · see citing works
Self-citationAggad, D., Mazel, M., Boudinot, P., Mogensen, K. E., Hamming, O. J., Hartmann, R., Kotenko, S. V., Herbomel, P., Lutfalla, G., & Levraud, J. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0901495 · Cited by 258 · see citing works
Self-citationMonocyte/macrophage interactions with myogenic precursor cells during skeletal muscle regeneration
Saclier, M., Cuvellier, S., Magnan, M., Mounier, R., & Chazaud, B. (2013) · FEBS Journal · doi:10.1111/febs.12166 · Cited by 248 · see citing works
Nelson, C. M., Ackerman, K. M., O’Hayer, P., Bailey, T. J., Gorsuch, R. A., & Hyde, D. R. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3838-12.2013 · Cited by 205 · see citing works
Palha, N., Guivel‐Benhassine, F., Briolat, V., Lutfalla, G., Sourisseau, M., Ellett, F. E., Wang, C., Lieschke, G. J., Herbomel, P., Schwartz, O., et al. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003619 · Cited by 202 · see citing works
Self-citationUnraveling Tissue Regeneration Pathways Using Chemical Genetics
Mathew, L. K., Sengupta, S., Kawakami, A., Andreasen, E. A., Löhr, C. V., Loynes, C. A., Renshaw, S. A., Peterson, R. T., & Tanguay, R. L. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m706640200 · Cited by 179 · see citing works
Notochord vacuoles are lysosome-related organelles that function in axis and spine morphogenesis
Ellis, K., Bagwell, J., & Bagnat, M. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201212095 · Cited by 175 · see citing works
Hasegawa, T., Hall, C. J., Crosier, P. S., Abe, G., Kawakami, K., Kudō, A., & Kawakami, A. (2017) · eLife · doi:10.7554/elife.22716 · Cited by 151 · see citing works
Matrix metalloproteinase 9 modulates collagen matrices and wound repair
LeBert, D. C., Squirrell, J. M., Rindy, J., Broadbridge, E., Lui, Y., Zakrzewska, A., Eliceiri, K. W., Meijer, A. H., & Anna Huttenlocher, A. (2015) · Development · doi:10.1242/dev.121160 · Cited by 148 · see citing works
Conner, C., Ackerman, K. M., Lahne, M., Hobgood, J. S., & Hyde, D. R. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0498-14.2014 · Cited by 146 · see citing works
Kawakami, A., Fukazawa, T., & Takeda, H. (2004) · Developmental Dynamics · doi:10.1002/dvdy.20181 · Cited by 145 · see citing works
Primitive macrophages control HSPC mobilization and definitive haematopoiesis
Travnickova, J., Chau, V. T., Julien, E., Mateos-Langerak, J., Gonzalez, C., Lelièvre, E., Lutfalla, G., Tavian, M., & Kissa, K. (2015) · Nature Communications · doi:10.1038/ncomms7227 · Cited by 119 · see citing works
Self-citationTransient infection of the zebrafish notochord with E. coli induces chronic inflammation
Chi, M. N., Phan, Q. T., Gonzalez, C., Dubremetz, J., Levraud, J., & Lutfalla, G. (2014) · Disease Models & Mechanisms · doi:10.1242/dmm.014498 · Cited by 116 · see citing works
Self-citationMolecular Steps of Tumor Necrosis Factor Receptor-Mediated Apoptosis
Gupta, S. (2001) · Current Molecular Medicine · doi:10.2174/1566524013363780 · Cited by 89 · see citing works
Tal, T. L., Franzosa, J. A., & Tanguay, R. L. (2009) · Gerontology · doi:10.1159/000259327 · Cited by 78 · see citing works
Espín, R., Roca, F. J., Candel, S., Sepulcre, M. P., González‐Rosa, J. M., Alcaraz‐Pérez, F., Meseguer, J., Cayuela, M. L., Mercader, N., & Mulero, V. (2012) · Disease Models & Mechanisms · doi:10.1242/dmm.010249 · Cited by 62 · see citing works
In Vivo Cell and Tissue Dynamics Underlying Zebrafish Fin Fold Regeneration
Mateus, R., Pereira, T., Sousa, S. H., de Lima, J. E., Pascoal, S., Saúde, L., & Jacinto, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051766 · Cited by 54 · see citing works
Chi, M. N., Bryson‐Richardson, R. J., Sonntag, C., Hall, T. E., Gibson, A., Sztal, T. E., Chua, W., Schilling, T. F., & Currie, P. D. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003014 · Cited by 48 · see citing works
Choudhury, A. R., Furuta, G. T., Lavigne, J. A., Galli, S. J., & Wershil, B. K. (1996) · Cellular Immunology · doi:10.1006/cimm.1996.0184 · Cited by 36 · see citing works
Hasegawa, T., Nakajima, T., Ishida, T., Kudō, A., & Kawakami, A. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.12.015 · Cited by 35 · see citing works
Pase, L. B., Nowell, C. J., & Lieschke, G. J. (2012) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-391856-7.00032-9 · Cited by 30 · see citing works
Generating parabiotic zebrafish embryos for cell migration and homing studies
Demy, D. L., Ranta, Z., Giorgi, J.-M., Gonzalez, M., Herbomel, P., & Kissa, K. (2013) · Nature Methods · doi:10.1038/nmeth.2362 · Cited by 28 · see citing works
Self-citationEl‐Ghoneimi, A., Cursio, R., Schmid‐Alliana, A., Tovey, M. G., Lasfar, A., Michiels, J., Rossi, B., & Gugenheim, J. (2007) · Transplantation Proceedings · doi:10.1016/j.transproceed.2007.05.017 · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Galluzzi, L., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Agostinis, P., Alnemri, E. S., Altucci, L., Amelio, I., Andrews, D. W., et al. (2018) · Cell Death & Differentiation · doi:10.1038/s41418-017-0012-4 · Cited by 6,680 · see citing works
Tsarouchas, T. M., Wehner, D., Cavone, L., Munir, T., Keatinge, M., Lambertus, M., Underhill, A., Barrett, T., Kassapis, E., Ogryzko, N. V., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07036-w · Cited by 294 · see citing works
The Macrophage in Cardiac Homeostasis and Disease
Lavine, K. J., Pinto, A. R., Epelman, S., Kopecky, B. J., Clemente-Casares, X., Godwin, J., Rosenthal, N., & Kovacic, J. C. (2018) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2018.08.2149 · Cited by 234 · see citing works
The zebrafish as a model for gastrointestinal tract–microbe interactions
Flores, E. M., Nguyen, A. T., Odem, M. A., Eisenhoffer, G. T., & Krachler, A. M. (2019) · Cellular Microbiology · doi:10.1111/cmi.13152 · Cited by 138 · see citing works
Morales, R. A., & Allende, M. L. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00253 · Cited by 99 · see citing works
Zebrafish as a model for inflammation and drug discovery
Zanandrea, R., Bonan, C. D., & Campos, M. M. (2020) · Drug Discovery Today · doi:10.1016/j.drudis.2020.09.036 · Cited by 101 · see citing works
Rougeot, J., Torraca, V., Zakrzewska, A., Kanwal, Z., Jansen, H. J., Sommer, F., Spaink, H. P., & Meijer, A. H. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00832 · Cited by 97 · see citing works
Determining macrophage versus neutrophil contributions to innate immunity using larval zebrafish
Rosowski, E. (2020) · Disease Models & Mechanisms · doi:10.1242/dmm.041889 · Cited by 82 · see citing works
Hu, D., Li, R., Li, Y., Wang, M., Wang, L., Wang, S., Cheng, H., Zhang, Q., Fu, C., Qian, Z., et al. (2024) · Advanced Science · doi:10.1002/advs.202308910 · Cited by 87 · see citing works
A matter of life and death: stem cell survival in tissue regeneration and tumour formation
Soteriou, D., & Fuchs, Y. (2018) · Nature Reviews Cancer · doi:10.1038/nrc.2017.122 · Cited by 87 · see citing works
Fernández, A., Vermeren, M., Humphries, D. C., Subirós‐Funosas, R., Barth, N. D., Campana, L., MacKinnon, A. C., Feng, Y., & Vendrell, M. (2017) · ACS Central Science · doi:10.1021/acscentsci.7b00262 · Cited by 81 · see citing works
Sanz-Morejón, A., García‐Redondo, A. B., Reuter, H., Marques, I. J., Bates, T. J. D., Galardi‐Castilla, M., Große, A., Manig, S., Langa, X., Ernst, A., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.091 · Cited by 81 · see citing works
The Macrophage Response Is Driven by Mesenchymal Stem Cell-Mediated Metabolic Reprogramming
Luque-Campos, N., Bustamante-Barrientos, F. A., Pradenas, C., García, C., Araya, M. J., Bohaud, C., Contreras-López, R., Elizondo-Vega, R., Djouad, F., Luz-Crawford, P., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.624746 · Cited by 82 · see citing works
Self-citationInflammation induces zebrafish regeneration
Iribarne, M. (2021) · Neural Regeneration Research · doi:10.4103/1673-5374.306059 · Cited by 73 · see citing works
Cellular diversity of the regenerating caudal fin
Hou, Y., Lee, H. J., Chen, Y., Ge, J., Osman, F. O. I., McAdow, A. R., Mokalled, M. H., Johnson, S. L., Zhao, G., & Wang, T. (2020) · Science Advances · doi:10.1126/sciadv.aba2084 · Cited by 72 · see citing works
Senescence and Apoptosis During in vitro Embryo Development in a Bovine Model
Ramos‐Ibeas, P., Gimeno, I., Cañón-Beltrán, K., Gutiérrez‐Adán, A., Rizos, D. V., & Gómez, E. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.619902 · Cited by 70 · see citing works
Iriawati, I., Vitasasti, S., Rahmadian, F. N. A., & Barlian, A. (2024) · PLoS ONE · doi:10.1371/journal.pone.0304335 · Cited by 65 · see citing works
When dying is not the end: Apoptotic caspases as drivers of proliferation
Pérez-Garijo, A. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.11.036 · Cited by 59 · see citing works
Iron regulates myeloma cell/macrophage interaction and drives resistance to bortezomib
Camiolo, G., Barbato, A., Giallongo, C., Vicario, N., Romano, A., Parrinello, N. L., Parenti, R., Cantón-Sandoval, J., García‐Moreno, D., Lazzarino, G., et al. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101611 · Cited by 60 · see citing works
Li, Y., Xiao, T., & Zou, J. (2020) · Science China Life Sciences · doi:10.1007/s11427-020-1712-4 · Cited by 60 · see citing works
The Evolving Roles of Cardiac Macrophages in Homeostasis, Regeneration, and Repair
Alvarez‐Argote, S., & O'Meara, C. C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22157923 · Cited by 56 · see citing works
Chemokine Receptors and Phagocyte Biology in Zebrafish
Sommer, F., Torraca, V., & Meijer, A. H. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00325 · Cited by 53 · see citing works
Blastemal progenitors modulate immune signaling during early limb regeneration
Tsai, S. L., Baselga‐Garriga, C., & Melton, D. A. (2019) · Development · doi:10.1242/dev.169128 · Cited by 52 · see citing works
Hippo-Yap/Taz signalling in zebrafish regeneration
Riley, S. E., Feng, Y., & Hansen, C. G. (2022) · npj Regenerative Medicine · doi:10.1038/s41536-022-00209-8 · Cited by 52 · see citing works
Miskolci, V., Tweed, K. E., Lasarev, M. R., Britt, E. C., Walsh, A. J., Zimmerman, L. J., McDougal, C. E., Cronan, M. R., Fan, J., Sauer, J., et al. (2022) · eLife · doi:10.7554/elife.66080 · Cited by 50 · see citing works
Molecular Actors of Inflammation and Their Signaling Pathways: Mechanistic Insights from Zebrafish
Leiba, J., Özbilgiç, R., Hernández, L., Demou, M., Lutfalla, G., Yatime, L., & Chi, M. N. (2023) · Biology · doi:10.3390/biology12020153 · Cited by 51 · see citing works
Self-citationSmits, A. I. P. M., & Bouten, C. V. C. (2018) · Current Opinion in Biomedical Engineering · doi:10.1016/j.cobme.2018.02.006 · Cited by 48 · see citing works
Role of Macrophages and Microglia in Zebrafish Regeneration
Var, S. R., & Byrd-Jacobs, C. A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21134768 · Cited by 48 · see citing works
Sipka, T., Peroceschi, R., Hassan-Abdi, R., Groß, M., Ellett, F., Begon-Pescia, C., Gonzalez, C., Lutfalla, G., & Nguyen-Chi, M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.636585 · Cited by 35 · see citing works
Self-citationIribarne, M., & Hyde, D. R. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.892271 · Cited by 45 · see citing works
Aztekin, C., Hiscock, T. W., Butler, R., Andino, F. D. J., Robert, J., Gurdon, J. B., & Jullien, J. (2020) · Development · doi:10.1242/dev.185496 · Cited by 43 · see citing works
Durant, F., & Whited, J. L. (2021) · Advanced Science · doi:10.1002/advs.202100407 · Cited by 41 · see citing works
The Macrophage Iron Signature in Health and Disease
Mertens, C., Marques, O., Horvat, N. K., Simonetti, M., Muckenthaler, M. U., & Jung, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22168457 · Cited by 43 · see citing works
Speirs, Z. C., Loynes, C. A., Mathiessen, H., Elks, P. M., Renshaw, S. A., & Jørgensen, L. V. G. (2024) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2024.109490 · Cited by 45 · see citing works
Parallels between vertebrate cardiac and cutaneous wound healing and regeneration
Richardson, R. J. (2018) · npj Regenerative Medicine · doi:10.1038/s41536-018-0059-y · Cited by 40 · see citing works
Immunity in salamander regeneration: Where are we standing and where are we headed?
Castro, L. A. B., Walters, H., Vázquez, R. O. G., & Yun, M. H. (2020) · Developmental Dynamics · doi:10.1002/dvdy.251 · Cited by 39 · see citing works
Injury-Induced Innate Immune Response During Segment Regeneration of the Earthworm, Eisenia andrei
Bodó, K., Kellermayer, Z., László, Z., Boros, Á., Kokhanyuk, B., Németh, P., & Engelmann, P. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052363 · Cited by 40 · see citing works
Zebrafish cardiac regeneration—looking beyond cardiomyocytes to a complex microenvironment
Ryan, R., Moyse, B., & Richardson, R. J. (2020) · Histochemistry and Cell Biology · doi:10.1007/s00418-020-01913-6 · Cited by 36 · see citing works
Tipping the Scales With Zebrafish to Understand Adaptive Tumor Immunity
Miao, K., Kim, G., Meara, G. K., Qin, X., & Feng, H. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.660969 · Cited by 35 · see citing works
Parallels between wound healing, epimorphic regeneration and solid tumors
Wong, A. Y. L., & Whited, J. L. (2020) · Development · doi:10.1242/dev.181636 · Cited by 31 · see citing works
Linking wound response and inflammation to regeneration in the zebrafish larval fin
Roehl, H. H. (2018) · The International Journal of Developmental Biology · doi:10.1387/ijdb.170331hr · Cited by 31 · see citing works
Tian, H., Xing, J., Tang, X., Sheng, X., Chi, H., & Zhan, W. (2022) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2022.104627 · Cited by 31 · see citing works
Macrophage–Neuroglia Interactions in Promoting Neuronal Regeneration in Zebrafish
Zeng, C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076483 · Cited by 29 · see citing works
A zebrafish model of granulin deficiency reveals essential roles in myeloid cell differentiation
Campbell, C. A., Fursova, O. V., Cheng, X., Snella, E. M., McCune, A., Li, L., Solchenberger, B., Schmid, B., Sahoo, D., Morton, M., et al. (2021) · Blood Advances · doi:10.1182/bloodadvances.2020003096 · Cited by 28 · see citing works
Bohaud, C., Johansen, M. D., Jørgensen, C., Ipseiz, N., Kremer, L., & Djouad, F. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.707824 · Cited by 31 · see citing works
Self-citationMacrophages undergo a behavioural switch during wound healing in zebrafish.
Sipka, T., Park, S.-A., Ozbilgic, R., Balas, L., Durand, T., Mikula, K., Lutfalla, G., & Nguyen-Chi, M. (2022) · Free Radical Biology & Medicine · doi:10.1016/j.freeradbiomed.2022.09.021 · Cited by 27 · see citing works
Self-citationMacrophages in tissue repair and regeneration: insights from zebrafish
Zhao, C., Yang, Z., Li, Y., & Wen, Z. (2024) · Cell Regeneration · doi:10.1186/s13619-024-00195-w · Cited by 30 · see citing works
12-Lipoxygenase governs the innate immune pathogenesis of islet inflammation and autoimmune diabetes
Kulkarni, A., Piñeros, A. R., Walsh, M. A., Casimiro, I., Ibrahim‐Shaikh, S., Hernández‐Pérez, M., Orr, K. S., Glenn, L. M., Nadler, J. L., Morris, M. A., et al. (2021) · JCI Insight · doi:10.1172/jci.insight.147812 · Cited by 29 · see citing works
Should we reconsider the apoptosis as a strategic player in tissue regeneration?
Codispoti, B., Im, M., Sied, J., Benincasa, C., Scacco, S., & Tatullo, M. (2019) · International Journal of Biological Sciences · doi:10.7150/ijbs.36362 · Cited by 28 · see citing works
Degen, A., Krynytska, І., & Kamyshnyi, O. (2020) · Endocrine Regulations · doi:10.2478/enr-2020-0019 · Cited by 29 · see citing works
Zebrafish ( Danio rerio ) as a Model for Understanding the Process of Caudal Fin Regeneration
Lebedeva, L., Zhumabayeva, B., Gebauer, T., Kisselev, I., & Aytasheva, Z. (2020) · Zebrafish · doi:10.1089/zeb.2020.1926 · Cited by 27 · see citing works
Laplace-Builhe, B., Barthelaix, A., Assou, S., Bohaud, C., Pratlong, M., Séverac, D., Téjédor, G., Luz‐Crawford, P., Chi, M. N., Mathieu, M. N., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-26422-5 · Cited by 27 · see citing works
Self-citationRoy, M., & Singh, R. K. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03900-z · Cited by 26 · see citing works
Chi, M. N., Luz‐Crawford, P., Balas, L., Sipka, T., Contreras-López, R. A., Barthelaix, A., Lutfalla, G., Durand, T., Jørgensen, C., & Djouad, F. (2020) · British Journal of Pharmacology · doi:10.1111/bph.15156 · Cited by 25 · see citing works
Self-citationPDX regulates inflammatory cell infiltration via resident macrophage in LPS‐induced lung injury
Yang, Y., Zhang, H., Mei, H., Xu, H., Xiang, S., Yang, Q., Zheng, S., Smith, F. G., Jin, S., & Wang, Q. (2020) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.15679 · Cited by 25 · see citing works
Diaz, O. E., Sorini, C., Morales, R. A., Luo, X., Frede, A., Krais, A. M., Chávez, M. N., Wincent, E., Das, S., & Villablanca, E. J. (2021) · Disease Models & Mechanisms · doi:10.1242/dmm.049104 · Cited by 25 · see citing works
Zhong, D., Jiang, H., Zhou, C., Ahmed, A., Li, H., Wei, X., Lian, Q., Tastemel, M., Xin, H., Ge, M., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112116 · Cited by 25 · see citing works
Kaveh, A., Bruton, F. A., Oremek, M. E. M., Tucker, C. S., Taylor, J. M., Mullins, J. J., Rossi, A. G., & Denvir, M. A. (2021) · Development · doi:10.1242/dev.199636 · Cited by 24 · see citing works
Understanding the Metabolic Profile of Macrophages During the Regenerative Process in Zebrafish
Paredes, L. C., Câmara, N. O. S., & Braga, T. T. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00617 · Cited by 23 · see citing works
Lactate metabolism coordinates macrophage response and regeneration in zebrafish
Bohaud, C., Cruz, J. D. L., Terraza, C., Barthelaix, A., Laplace-Builhe, B., Jørgensen, C., Arribat, Y., & Djouad, F. (2022) · Theranostics · doi:10.7150/thno.65235 · Cited by 22 · see citing works
Self-citationInflammation in Development and Aging: Insights from the Zebrafish Model
Mastrogiovanni, M., Martínez-Navarro, F. J., Bowman, T. V., & Cayuela, M. L. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25042145 · Cited by 22 · see citing works
Gence, L., Fernezelian, D., Bringart, M., Veeren, B., Christophe, A., Brion, F., Meilhac, O., Bascands, J., & Diotel, N. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.832928 · Cited by 21 · see citing works
Neutrophils facilitate the epicardial regenerative response after zebrafish heart injury
Peterson, E., Sun, J., Chen, X., & Wang, J. (2024) · Developmental Biology · doi:10.1016/j.ydbio.2024.01.011 · Cited by 21 · see citing works
Xu, C., Hutchins, E. D., Tokuyama, M. A., Wilson‐Rawls, J., & Kusumi, K. (2019) · Journal of Immunology and Regenerative Medicine · doi:10.1016/j.regen.2019.100025 · Cited by 21 · see citing works
Arkoudi, K., Yuan, Y., Cumine, A. P., Dyer, C., Busch‐Nentwich, E. M., Bravo, I. R., Feng, Y., & Knight, R. D. (2025) · npj Regenerative Medicine · doi:10.1038/s41536-025-00414-1 · Cited by 20 · see citing works
Nakamura, A., Wong, Y. F., Venturato, A., Michaut, M., Venkateswaran, S., Santra, M., Gonçalves, C., Larsen, M., Leuschner, M., Kim, Y. H., et al. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2022.03.013 · Cited by 20 · see citing works
Tissue Regeneration: The Dark Side of Opioids
Dromard, C., Rabiller, L., Jourdan, G., Cousin, B., Pénicaud, L., Casteilla, L., & Lorsignol, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147336 · Cited by 19 · see citing works
Bacterial lipopolysaccharides can initiate regeneration of the Xenopus tadpole tail
Bishop, T., & Beck, C. W. (2021) · iScience · doi:10.1016/j.isci.2021.103281 · Cited by 19 · see citing works
Macrophages modulate fibrosis during newt lens regeneration
Tsissios, G., Sallese, A., Pérez-Estrada, J. R., Tangeman, J. A., Chen, W., Smucker, B. J., Ratvasky, S. C., Grajales‐Esquivel, E., Martinez, A., Visser, K. J., et al. (2024) · Stem Cell Research & Therapy · doi:10.1186/s13287-024-03740-1 · Cited by 20 · see citing works
Cell death classification: A new insight based on molecular mechanisms
Dehghan, S., Kheshtchin, N., Hassannezhad, S., & Soleimani, M. (2023) · Experimental Cell Research · doi:10.1016/j.yexcr.2023.113860 · Cited by 18 · see citing works
Nitrite Improves Heart Regeneration in Zebrafish
Rochon, E. R., Missinato, M. A., Xue, J., Tejero, J., Tsang, M., Gladwin, M. T., & Corti, P. (2019) · Antioxidants and Redox Signaling · doi:10.1089/ars.2018.7687 · Cited by 18 · see citing works
Liu, L.-Z., Zhong, Y., Zheng, T., Zhao, J., Ding, S., Lv, J., Xu, Q., & Zhang, Y. (2024) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2024.109657 · Cited by 17 · see citing works
Rodriguez‐Duarte, J., Dapueto, R., Galliussi, G., Turell, L., Kamaid, A., Khoo, N. K. H., Schopfer, F. J., Freeman, B. Α., Escande, C., Batthyány, C., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-31218-7 · Cited by 17 · see citing works
Sawaki, R., Sato, D., Nakayama, H., Nakagawa, Y., & Shimada, Y. (2019) · Inventions · doi:10.3390/inventions4040072 · Cited by 17 · see citing works
Consequences of excessive glucosylsphingosine in glucocerebrosidase-deficient zebrafish.
Lelieveld, L., Gerhardt, S., Maas, S., Zwiers, K. C., de Wit, C. D., Beijk, E. H., Ferraz, M. J., Artola, M., Meijer, A., Tudorache, C., et al. (2022) · Journal of Lipid Research · doi:10.1016/j.jlr.2022.100199 · Cited by 11 · see citing works
Wound Healing Insights from Flies and FishPreprint
George, A., & Martin, P. B. (2022) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a041217 · Cited by 15 · see citing works
Begon‐Pescia, C., Boireau, S., Boyer-Clavel, M., Lutfalla, G., & Chi, M. N. (2022) · MethodsX · doi:10.1016/j.mex.2022.101651 · Cited by 16 · see citing works
Self-citationRabiller, L., Robert, V., Arlat, A., Labit, E., Ousset, M., Salon, M., Coste, A., Fernandes, L. D. C., Monsarrat, P., Ségui, B., et al. (2021) · npj Regenerative Medicine · doi:10.1038/s41536-021-00151-1 · Cited by 15 · see citing works
Martínez-López, M. F., de Almeida, C. R., Fontes, M., Mendes, R. V., Kaufmann, S. H. E., & Fior, R. (2024) · Disease Models & Mechanisms · doi:10.1242/dmm.050693 · Cited by 15 · see citing works
Du, L., Zhang, X., Huang, L., Yang, M., Zhang, W., Xu, J., Liu, J., Xie, W., Zhang, X., Liu, K., et al. (2025) · Materials Today Bio · doi:10.1016/j.mtbio.2025.101572 · Cited by 14 · see citing works
Expression analysis of Hsp90α and cytokines in zebrafish caudal fin regeneration
Li, J., Sultan, Y. Y., Sun, Y., Zhang, S., Liu, Y., & Li, X. (2020) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2020.103922 · Cited by 13 · see citing works
Occurrence of foamy macrophages during the innate response of zebrafish to trypanosome infections
Jacobs, S. H., Dóró, E., Hammond, F. R., Chi, M. N., Lutfalla, G., Wiegertjes, G. F., & Forlenza, M. (2021) · eLife · doi:10.7554/elife.64520 · Cited by 13 · see citing works
Self-citationWang, Y., Wei, S., Song, H., Zhang, X., Wang, W., Du, N., Song, T., Liang, H., Chen, X., & Wang, Y. (2019) · The FASEB Journal · doi:10.1096/fj.201801966rrr · Cited by 13 · see citing works
Gillies, S. L. J., Verdon, R., Stone, V., Brown, D. M., Henry, T. B., Tran, L., Tucker, C. S., Rossi, A. G., Tyler, C. R., & Johnston, H. J. (2022) · Nanotoxicology · doi:10.1080/17435390.2022.2088312 · Cited by 12 · see citing works
Shikonin Inhibits Fin Regeneration in Zebrafish Larvae
Cao, Z., Guo, C., Chen, G., Liu, J., Ni, H., Liu, F., Xiong, G., Liao, X., & Lu, H. (2022) · Cells · doi:10.3390/cells11203187 · Cited by 12 · see citing works
Liu, R., Imangali, N., Ethiraj, L. P., Carney, T. J., & Winkler, C. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.775512 · Cited by 12 · see citing works
Peds1 deficiency in zebrafish results in myeloid cell apoptosis and exacerbated inflammation
Arroyo, A. B., Tyrkalska, S. D., Bastida‐Martínez, E., Monera-Girona, A. J., Cantón-Sandoval, J., Bernal-Carrión, M., García‐Moreno, D., Arnanz, M. E., & Mulero, V. (2024) · Cell Death Discovery · doi:10.1038/s41420-024-02141-w · Cited by 11 · see citing works
Phan, Q., Liu, R.-R., Tan, W.-H., Imangali, N., Cheong, B., Schartl, M., & Winkler, C. (2020) · JBMR Plus · doi:10.1002/jbm4.10409 · Cited by 10 · see citing works
Secombes, C. J. (2022) · Springer eBooks · doi:10.1007/978-3-030-85420-1_10 · Cited by 11 · see citing works
Chen, Z., Li, N., Zhou, Z., Zhu, L., Wang, K., Chen, S., Gu, Q., Liu, Y., Zhai, K., & Xu, S. (2025) · BMC Complementary Medicine and Therapies · doi:10.1186/s12906-025-04978-9 · Cited by 10 · see citing works
Exploring Macrophage-Dependent Wound Regeneration During Mycobacterial Infection in Zebrafish
Bohaud, C., Johansen, M. D., Varga, B., Contreras-López, R. A., Barthelaix, A., Hamela, C., Sapède, D., Cloître, T., Gergely, C., Jørgensen, C., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.838425 · Cited by 11 · see citing works
Self-citationThe molecular interplay between progenitors and immune cells in tissue regeneration and homeostasis
Tsai, S. L. (2019) · Journal of Immunology and Regenerative Medicine · doi:10.1016/j.regen.2019.100024 · Cited by 10 · see citing works
Roscovitine Worsens Mycobacterium abscessus Infection by Reducing DUOX2-mediated Neutrophil Response
Moigne, V. L., Rincon, D. R., Glatigny, S., Dupont, C., Langevin, C., Said, A. A. A., Renshaw, S. A., Floto, R. A., Herrmann, J., & Bernut, A. (2022) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2021-0406oc · Cited by 10 · see citing works
Rumford, J. E., Grieshaber, A., Lewiston, S., Reed, J. L., Long, S. S., & Mitchell, D. M. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1495586 · Cited by 10 · see citing works
Sacchi, S., Malagoli, D., & Franchi, N. (2024) · Cells · doi:10.3390/cells13242106 · Cited by 9 · see citing works
Spencer, C. G., Hamilton, M., Bedsole, E., Wei, Y. N., Rojas, A. M., Burciu, A., Zhu, J., Sabin, K. Z., & Shiau, C. E. (2026) · Nature Communications · doi:10.1038/s41467-025-68204-3 · Cited by 9 · see citing works
Cavanah, P., Itou, J., Rusman, Y., Tahara, N., Williams, J. M., Salomon, C. E., & Kawakami, Y. (2020) · Developmental Dynamics · doi:10.1002/dvdy.244 · Cited by 9 · see citing works
Geurtzen, K., López-Delgado, A. C., Duseja, A., Kurzyukova, A., & Knopf, F. (2022) · Development · doi:10.1242/dev.199803 · Cited by 9 · see citing works
Non-traditional roles of immune cells in regeneration: an evolutionary perspective
Arinda, B. N., Innabi, Y. A., Grasis, J. A., & Oviedo, N. J. (2022) · Development · doi:10.1242/dev.199903 · Cited by 8 · see citing works
Diaz, O. E., Xue, S., Luo, X., Nava-Palacios, J., Appelblom, A., Morales, R. A., Das, S., & Villablanca, E. J. (2020) · Reproductive Toxicology · doi:10.1016/j.reprotox.2020.02.009 · Cited by 8 · see citing works
- Authors
- Nguyen-Chi, M., Laplace-Builhé, B., Travnickova, J., Luz-Crawford, P., Tejedor, G., Lutfalla, G., Kissa, K., Jorgensen, C., & Djouad, F.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Inserm (FR)
- Corresponding author
- Djouad, Farida
- Venue
- Cell Death & Disease
- Published
- 2017-08-10
- Volume
- 8
- Issue
- 8
- Pages
- e2979-e2979
- ISSN
- 2041-4889 (ISSN-L)
- PMC
- PMC5596562
- OpenAlex
- W2743154979
- Cited by
- 190
- References
- 46
- Citations by year
- 2026: 19 · 2025: 18 · 2024: 33 · 2023: 12 · 2022: 27 · 2021: 30 · 2020: 25 · 2019: 15 · 2018: 9 · 2017: 2
- FWCI
- 7.44
- Type
- journal article
- Language
- en
- Update notices
- correction (2018-06-13)
- Open access
- gold
- doi.org
- Locations
- Cell Death and Disease (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by)
- HAL (submittedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-10-MIDI-009, ANR-10-MIDI-0009, ANR-10)
- Institut National de la Santé et de la Recherche Médicale
- Université de Montpellier
- FP7 People: Marie-Curie Actions (PITN-GA-2011-289209, FP7-PEOPLE-2011-ITN)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Planarian Biology and Electrostimulation
- Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
- Keywords
- TNF signaling, macrophages, fin regeneration, blastema formation, macrophage polarization, inflammatory macrophages, macrophage depletion, parabiosis, zebrafish larvae, appendage regeneration
- MeSH terms
- Animals, Extremities, Larva, Macrophages, Regeneration, Tumor Necrosis Factor-alpha, Zebrafish, Signal Transduction, Zebrafish Proteins, Animals, Genetically Modified, Receptors, Tumor Necrosis Factor, Type I
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review