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Live Imaging Reveals Differing Roles of Macrophages and Neutrophils during Zebrafish Tail Fin Regeneration
Open accessAbstract
Macrophages and neutrophils are the pivotal immune phagocytes that enter the wound after tissue injury to remove the cell debris and invaded microorganisms, which presumably facilitate the regrowth of injured tissues. Taking advantage of the regeneration abilities of zebrafish and the newly generated leukocyte-specific zebrafish lines with labeling of both leukocyte lineages, we assessed the behaviors and functions of neutrophils and macrophages during tail fin regeneration. Live imaging showed that within 6 hours post amputation, the inflammatory stage, neutrophils were the primary cells scavenging apoptotic bodies and small cell debris, although they had limited phagocytic capacity and quickly underwent apoptosis. From 6 hours post amputation on, the resolution and regeneration stage, macrophages became the dominant scavengers, efficiently resolving inflammation and facilitating tissue remodeling and regrowth. Ablation of macrophages but not neutrophils severely impaired the inflammatory resolution and tissue regeneration, resulting in the formation of large vacuoles in the regenerated fins. In contrast, removal of neutrophils slightly accelerates the regrowth of injured fin. Our study documents the differing behaviors and functions of macrophages and neutrophils during tissue regeneration.
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“The zebrafish larval caudal fin regeneration model is a well-established system for studying the roles of the immune system in organ injury and regeneration [40]”
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Cites
Neutrophils and immunity: challenges and opportunities
Nathan, C. (2006) · Nature reviews. Immunology · doi:10.1038/nri1785 · Cited by 2,971
Recognition of microorganisms and activation of the immune response
Medzhitov, R. (2007) · Nature · doi:10.1038/nature06246 · Cited by 2,862 · cited 1×
“During this process, the immune cells play indispensable protective roles for removing dead cells, preventing invasion of microorganisms, and supporting regrowth of damaged tissues (2).”
BackgroundArnold, 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 · cited 2×
“Consistent with previous studies in mice (4, 7), we further document that the depletion of macrophages in zebrafish leads to the delay of the clearance of cell debris, decrease of regeneration speed, and formation of vacuoles in the regenerating fin.”
BackgroundResultHeart Regeneration in Zebrafish
Poss, K. D., Wilson, L. G., & Keating, M. T. (2002) · Science · doi:10.1126/science.1077857 · Cited by 1,938
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
The role of the macrophage in wound repair. A study with hydrocortisone and antimacrophage serum.
(1975) · PubMed Central · Cited by 1,437
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 4×
“Neutrophils and macrophages are two major immune system cells that participate in this process (3).”
BackgroundResultInfluentialWound Macrophages Express TGF-α and Other Growth Factors in Vivo: Analysis by mRNA Phenotyping
Rappolee, D. A., Mark, D., Banda, M. J., & Werb, Z. (1988) · Science · doi:10.1126/science.3041594 · Cited by 1,101
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
Phagocyte partnership during the onset and resolution of inflammation
Soehnlein, O., & Lindbom, L. (2010) · Nature Reviews Immunology · doi:10.1038/nri2779 · Cited by 1,054 · cited 2×
“Unexpectedly, we found that the regeneration speed of the fin is slightly faster in the neutrophil-deficient runx1 (44) (Fig.”
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Items 101–200 of 352
Real-time imaging and genetic dissection of host-microbe interactions in zebrafish
Meijer, A. H., van der Vaart, M., & Spaink, H. P. (2013) · Cellular Microbiology · doi:10.1111/cmi.12236 · Cited by 41
“To facilitate in vivo imaging, fluorescent reporter lines have been developed that mark different immune cell types of the zebrafish or subcellular compartments where pathogens reside (Mathias et al., 2006; Renshaw et al., 2006; Hall et al., 2009; He et al., 2009; Ellett and Lieschke, 2010; Gray et al., 2011; Wittamer…”
BackgroundCell migration during heart regeneration in zebrafish
Tahara, N., Brush, M. J. H., & Kawakami, Y. (2016) · Developmental Dynamics · doi:10.1002/dvdy.24411 · Cited by 40
“Immune cells, in particular macrophages, are involved in appendage regeneration, such as zebrafish fins (Li et al., 2012a; Petrie et al., 2014) and axolotl limbs (Godwin et al., 2013).”
BackgroundIkzf1 regulates embryonic T lymphopoiesis via Ccr9 and Irf4 in zebrafish
Huang, Y., Lu, Y., He, Y., Feng, Z. W., Zhan, Y., Huang, X. S., Liu, Q., Zhang, J., Li, H., Huang, H., et al. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.009883 · Cited by 40
“To generate Tg(coro1a:HA-ikzf1), Tg(coro1a: ccr9a), and Tg(coro1a:irf4a), their complementary DNA was amplified with specific primers (Table S1) and constructed into the pTol2 vector with the coro1a promoter (39).”
BackgroundMethodInfluentialChen, C., & Poss, K. D. (2017) · Annual Review of Genetics · doi:10.1146/annurev-genet-120116-024554 · Cited by 44
“Injury causes clotting and inflammation, and there are many recent studies that report evidence for pro-regenerative roles of immune cells like macrophages and T-cells (12; 67; 87; 135).”
BackgroundBernut, A., Loynes, C. A., Floto, R. A., & Renshaw, S. A. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01733 · Cited by 38
“In zebrafish larvae, tail amputation triggers leukocyte infiltration towards the wound, accurately mimicking the kinetics seen in mammalian inflammatory responses (17, 32, 33).”
BackgroundMüller glia–myeloid cell crosstalk accelerates optic nerve regeneration in the adult zebrafish
Dyck, A. V., Bollaerts, I., Beckers, A., Vanhunsel, S., Glorian, N., houcke, J. V., van Ham, T. J., Groef, L. D., Andries, L., & Moons, L. (2021) · Glia · doi:10.1002/glia.23972 · Cited by 39
“Hence, we are well aware that the observed increase in inflammatory cells may in part be attributed to infiltrating T-cells, especially at later time points after injury (Li et al., 2012).”
BackgroundEffects of 17α‑ethinylestradiol on caudal fin regeneration in zebrafish larvae
Sun, L., Gu, L., Tan, H., Liu, P., Gao, G. F., Tian, L., Chen, H., Lu, T., Qian, H., Fu, Z., et al. (2018) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2018.10.275 · Cited by 37
Wang, S.-F., He, Q.-P., Ma, D.-Y., Xue, Y.-F., & Liu, F. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.07.011 · Cited by 34
“…including wild-type, cloche mutant (Stainier et al., 1995), cmyb:EGFP (North et al., 2007), gata1:GFP (Long et al., 1997), mpo:EGFP (Renshaw et al., 2006), lyz:DsRed (Hall et al., 2007), and coro1a:EGFP (Li et al., 2012a) transgenic lines were raised and maintained in system water at 28.5 C.”
InfluentialFunctional and structural characterization of zebrafish ASC
Li, Y., Huang, Y., Cao, X., Yin, X., Jin, X., Liu, S., Jiang, J., Jiang, W., Xiao, T. S., Zhou, R., et al. (2018) · FEBS Journal · doi:10.1111/febs.14514 · Cited by 37
Xu, J., Qian, Q., Xia, M. H., Wang, X., & Wang, H. (2021) · Environmental Pollution · doi:10.1016/j.envpol.2021.116479 · Cited by 37
Interstitial leukocyte migration in vivo
Lam, P., & Huttenlocher, A. (2013) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2013.05.007 · Cited by 36
“Other cytokines are upregulated with wounding or infection, including Tumor Necrosis Factor (TNF) expression in zebrafish [53,54].”
Backgroundc-Myb acts in parallel and cooperatively with Cebp1 to regulate neutrophil maturation in zebrafish
Jin, H., Huang, Z., Chi, Y., Wu, M., Zhou, R., Zhao, L., Xu, J., Zhen, F., Lan, Y., Li, L., et al. (2016) · Blood · doi:10.1182/blood-2015-12-686147 · Cited by 34
Zhong, Y., Ye, Q., Chen, C., Wang, M., & Wang, H. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky101 · Cited by 36
“Wild-type zebrafish (Danio rerio), ezh2 heterozygous, per1b–/– mutant (41), rev-erbα–/– mutant (42), Tg(gata1:DsRED) (43), Tg(mpx:EGFP) (44), Tg(lyz:EGFP) (45), Tg(cmyb:EGFP) (46) and Tg(coro1a:EGFP) (47) zebrafish lines were maintained on a 14-h light/10-h dark cycle and fed three times daily at the Soochow Universit…”
MethodComparative Study in Zebrafish and Medaka Unravels the Mechanisms of Tissue Regeneration
Chowdhury, K., Lin, S., & Lai, S.-L. (2022) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2022.783818 · Cited by 37
Li, Y., Wang, C., Zhang, L., Chen, B., Mo, Y., & Zhang, J. (2022) · Fluids and Barriers of the CNS · doi:10.1186/s12987-022-00337-9 · Cited by 32
“Transgenic lines of Tg(kdrl:EGFP)s843 and Tg(coro1α:EGFP) were used to visualize the vasculature and microglia respectively [26, 27].”
MethodDesign, synthesis and anti-inflammatory effects of novel 9-O-substituted-berberine derivatives
Huang, M., Lin, J., Huang, Z., Xu, H., Hong, J., Sun, P., Guo, J., & Chen, W. (2016) · MedChemComm · doi:10.1039/c5md00577a · Cited by 33
Phagocyte dynamics in a highly regenerative urochordate: Insights into development and host defense
Lauzon, R. J., Brown, C., Kerr, L., & Tiozzo, S. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.11.006 · Cited by 32
“On the other hand, the in vivo behavior and function of different types of phagocytes during tissue and organ regeneration is not yet characterized (Li et al., 2012).”
BackgroundLin, Q., Zhang, Y., Zhou, R., Zheng, Y., Zhao, L., Huang, M., Zhang, X., Leung, A. Y. H., Zhang, W., & Zhang, Y. (2016) · Leukemia · doi:10.1038/leu.2016.320 · Cited by 32
Shi, Y., Zhang, Y., Zhao, F., Ruan, H., Huang, H., Luo, L., & Li, L. (2014) · Scientific Reports · doi:10.1038/srep05602 · Cited by 31
Simkin, J., & Seifert, A. W. (2017) · Stem Cells Translational Medicine · doi:10.1002/sctm.17-0213 · Cited by 29
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
“In contrast, another study that compared the individual roles for leucocytes by removing macrophages with an irf8 morpholino and neutrophils with a runx1 mutation found that loss of neutrophils increased regeneration and loss of macrophages slowed regeneration (Li et al., 2012).”
ResultHe, S., Tian, Y., Feng, S., Wu, Y., Shen, X., Chen, K., He, Y., Sun, Q., Li, X., Xu, J., et al. (2020) · eLife · doi:10.7554/elife.52024 · Cited by 31
“, 2005) and leukocytespecific coro1a promoter (Li et al., 2012), thus HEs and leukocytes (including myeloid and lymphoid cells) were marked by DsRedx (Figure 3A).”
BackgroundPossible Muscle Repair in the Human Cardiovascular System
Sommese, L., Zullo, A., Schiano, C., Mancini, F. P., & Claudio Napoli, A. (2017) · Stem Cell Reviews and Reports · doi:10.1007/s12015-016-9711-3 · Cited by 30
Bioelectric regulation of innate immune system function in regenerating and intact Xenopus laevis
Paré, J., Martyniuk, C. J., & Levin, M. G. (2017) · npj Regenerative Medicine · doi:10.1038/s41536-017-0019-y · Cited by 30
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
Simkin, J., Aloysius, A., Adam, M., Safaee, F., Donahue, R. R., Biswas, S. K., Lakhani, Z., Gensel, J. C., Thybert, D., Potter, S. S., et al. (2024) · Developmental Cell · doi:10.1016/j.devcel.2023.12.017 · Cited by 32
Macrophages 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 31
“These studies unveiled that neutrophils are the primary scavengers at the inflammatory stage, while macrophages become dominant phagocytes at the resolution stage (Li et al. 2012).”
BackgroundEvpP inhibits neutrophils recruitment via Jnk-caspy inflammasome signaling in vivo
Tan, J., Yang, D., Wang, Z., Zheng, X., Zhang, Y., & Liu, Q. (2019) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2019.05.051 · Cited by 28
Nlrc3-like is required for microglia maintenance in zebrafish
Wang, T., Yan, B., Lou, L., Lin, X., Yu, T., Wu, S., Lü, Q., Liu, W., Huang, Z., Zhang, M., et al. (2019) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2019.06.002 · Cited by 26
Zhu, Z., Chen, J., Xiong, J., & Peng, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096576 · Cited by 28
“label macrophages (green) and neutrophils (red), respectively [31].”
BackgroundZebrafish ( 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 32
“58 In contrast to previous studies showing that neutrophil ablation led to an elevated regeneration rate, inhibition of neutrophil recruitment to the site of injury by diphenyliodonium chloride did not affect the rate of tissue restoration.”
Application of the Zebrafish Traumatic Brain Injury Model in Assessing Cerebral Inflammation
Gan, D., Wu, S., Chen, B., & Zhang, J. (2019) · Zebrafish · doi:10.1089/zeb.2019.1793 · Cited by 26
mTOR activity is essential for retinal pigment epithelium regeneration in zebrafish
Lu, F., Leach, L. L., & Gross, J. M. (2022) · PLoS Genetics · doi:10.1371/journal.pgen.1009628 · Cited by 27
Miconazole protects blood vessels from matrix metalloproteinase 9-dependent rupture and hemorrhage
Yang, R., Zhang, Y., Huang, D., Luo, X., Zhang, L., Zhu, X., Zhang, X., Liu, Z., Han, J., & Xiong, J. (2017) · Disease Models & Mechanisms · doi:10.1242/dmm.027268 · Cited by 27
“, 2002), Tg(coro1a:eGFP) (Li et al., 2012), Tg( flk1:eGFP) (Beis et al.”
New function of zebrafish regulatory T cells in organ regeneration
Kikuchi, K. (2019) · Current Opinion in Immunology · doi:10.1016/j.coi.2019.10.001 · Cited by 25
Bertozzi, A., Wu, C. C., Nguyen, P. D., Vasudevarao, M. D., Mulaw, M. A., Koopman, C. D., de Boer, T. P., Bakkers, J., & Weidinger, G. (2020) · Developmental Biology · doi:10.1016/j.ydbio.2020.12.004 · Cited by 25
Vitamin D Enhances Neutrophil Generation and Function in Zebrafish (Danio rerio)
Liao, X., Lan, Y., Shao, R., Liu, J., Liang, S., Yin, Z., Gudmundsson, G. H., Bergman, P., & Wan, M. (2021) · Journal of Innate Immunity · doi:10.1159/000519183 · Cited by 25
Wang, K., Fang, X., Ma, N., Lin, Q., Huang, Z., Liu, W., Xu, M., Chen, X., Zhang, W., & Zhang, Y. (2015) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2015.01.038 · Cited by 25
“The construct pTol2-coronin1a:eGFP was generated as described previously [29].”
MethodZebrafish fin regeneration after cryoinjury-induced tissue damage
Chassot, B., Pury, D., & Jaźwińska, A. (2016) · Biology Open · doi:10.1242/bio.016865 · Cited by 25
“The transgenic lines were Tg(mpx:GFP) (Loynes et al., 2010); osterix(sp7):gfp (OlSp7: nlsGFPzf132) (Spoorendonk et al., 2008); Tg(osteocalcin:GFP) (Knopf et al., 2011); Tg(tie2:EGFP) (Motoike et al., 2000) and Tg(shh:GFP) 2.4shh: gfpABC#15 (Zhang et al., 2012).”
Prolonged neutrophil retention in the wound impairs zebrafish heart regeneration after cryoinjury
Xu, S., Xie, F., Tian, L., Manno, S. H. C., Manno, F. A. M., & Cheng, S. H. (2019) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2019.09.030 · Cited by 27
Schmidt, J. R., Geurtzen, K., von Bergen�, M., Schubert, K. A., & Knopf, F. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00674 · Cited by 25
“Soon after the injury neutrophils and macrophages are recruited to the resection site and into the forming regenerate where the latter are involved in the regeneration process (44, 45).”
BackgroundWu, X., Gu, R., Tang, M., Mu, X., He, W., & Nie, X. (2024) · Burns & Trauma · doi:10.1093/burnst/tkae061 · Cited by 28
“Macrophages are pivotal scavengers that resolve inflammation and stimulate tissue regeneration [98].”
Sheng, Y., Li, H., Liu, M., Xie, B., Wei, W. Z., Wu, J., Meng, F., Wang, H. Y., & Chen, D. (2019) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izz097 · Cited by 25
Ahi, E. P., Richter, F., Lecaudey, L. A., & Sefc, K. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-45599-w · Cited by 24
Zhao, F., Shi, Y., Huang, Y., Zhan, Y., Zhou, L., Li, Y., Wan, Y., Li, H., Huang, H., Ruan, H., et al. (2017) · Leukemia · doi:10.1038/leu.2017.189 · Cited by 24
Towards a gene regulatory network shaping the fins of the Princess cichlid
Ahi, E. P., & Sefc, K. M. (2018) · Scientific Reports · doi:10.1038/s41598-018-27977-y · Cited by 23
Nurani, F. S., Sukenda, S., & Nuryati, S. (2020) · Aquaculture Research · doi:10.1111/are.14499 · Cited by 22
Mandujano-Tinoco, E. A., Sultan, E., Ottolenghi, A., Gershoni‐Yahalom, O., & Rosental, B. (2021) · Cells · doi:10.3390/cells10081853 · Cited by 25
Zebrafish as an Experimental Model for Human Disease
Tonon, F., & Grassi, G. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24108771 · Cited by 22
“To study the interaction of the cancer cells with the innate immune response of zebrafish, the authors generated zebrafish xenograft models using the following zebrafish strains: (I) Tg(coro1a: GFP), where the innate immune cells (neutrophils, macrophages and thymus lymphocytes [15]) express the green fluorescence pro…”
MethodDing, C., Du, M., Xiong, Z., Wang, X., Li, H., He, E., Han, L., Dang, Y., Lü, Q., Li, S., et al. (2023) · Chemical Science · doi:10.1039/d3sc01896b · Cited by 23
Effects of neutrophil fate on inflammation
Xiao, Y., Yang, C. Z., Liu, W., Liu, K., Wang, Y., Xu, F., Wang, D., & Yang, Y. (2023) · Inflammation Research · doi:10.1007/s00011-023-01811-2 · Cited by 30
“However, neutrophil rTEM in the presence of tissue injury may hasten wound healing, thereby helping to reduce local inflammation [156, 174, 175].”
BackgroundThe innate immune regulator MyD88 dampens fibrosis during zebrafish heart regeneration
Goumenaki, P., Günther, S., Kikhi, K., Looso, M., Marín‐Juez, R., & Stainier, D. Y. R. (2024) · Nature Cardiovascular Research · doi:10.1038/s44161-024-00538-5 · Cited by 22
“Myeloid cells serve as key activators of the MyD88 signaling pathway in response to injury or infection 22,37–40 .”
BackgroundNeutrophils 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
Hou, Y., Sheng, Z., Mao, X., Li, C., Chen, J., Zhang, J., Huang, H., Ruan, H., Luo, L., & Li, L. (2016) · Scientific Reports · doi:10.1038/srep36853 · Cited by 21
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 22
Optimal combination of anti-inflammatory components from Chinese medicinal formula Liang-Ge-San
Lu, Z., Cao, H., Liu, D., Zheng, Y., Tian, C., Liu, S., Quan, J., Shi, L., Liu, J., & Yu, L. (2020) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2020.113747 · Cited by 21
Zhang, L., Er, J. C., Jiang, H., Li, X., Luo, Z., Ramezani, T., Feng, Y., Tang, M. K., Chang, Y., & Vendrell, M. (2016) · Chemical Communications · doi:10.1039/c6cc00095a · Cited by 20
Tissue regeneration effect of betulin via inhibition of ROS/MAPKs/NF-ĸB axis using zebrafish model
Ouyang, T., Yin, H., Yang, J., Liu, Y., & Ma, S. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.113420 · Cited by 20
Paredes‐Zúñiga, S., Morales, R. A., Muñoz‐Sánchez, S., Muñoz‐Montecinos, C., Parada, M., Tapia, K., Rubilar-Hernández, C., Allende, M. L., & Peña, O. A. (2017) · Immunogenetics · doi:10.1007/s00251-017-0975-9 · Cited by 20
“The CXCL12a/CXCR4b anti-inflammatory action could have a role limiting the amount of neutrophils responding to inflammatory signals, thus avoiding the detrimental consequences of excessive recruitment of neutrophils to wounds (Li et al. 2012).”
BackgroundMethodHu, W., van Steijn, L., Li, C., Verbeek, F. J., Cao, L., Merks, R. M. H., & Spaink, H. P. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.624571 · Cited by 21
Rac2 Regulates the Migration of T Lymphoid Progenitors to the Thymus during Zebrafish Embryogenesis
Lu, X., Zhang, Y., Liu, F., & Wang, L. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.1901494 · Cited by 21
“Transgenic lines including Tg(irf4a:KI-GFP) (3), Tg(runx1:en-GFP) (24), Tg(cmyb:EGFP) (25), Tg(coro1a:EGFP) (26), Tg(mpo:GFP) (27), Tg(CD41:GFP) (28), Tg(kdrl:mCherry) (29), Tg(rag2:dsRed) (30, 31), and Tg(lyz:mCherry) (32) were used for fluorescence imaging.”
BackgroundShimizu, Y., Kiyooka, M., & Ohshima, T. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.668408 · Cited by 19
“(2013) showed that IB4 staining colocalized with GFP-positive cells in other macrophage reporter line, Tg(cora1a:eGFP) (Li et al., 2012) and not with endothelial cell reporter line, Tg(flk:GFP) (Choi et al.”
BackgroundBacterial 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
Animal models of silicosis: fishing for new therapeutic targets and treatments
Martínez‐López, A., Candel, S., & Tyrkalska, S. D. (2023) · European Respiratory Review · doi:10.1183/16000617.0078-2023 · Cited by 20
Song, J., Pu, Q., Chen, C., Liu, X., Zhang, X., Wang, Z., Yan, J., Wang, X., Wang, H., & Qian, Q. (2025) · Environmental Health Perspectives · doi:10.1289/ehp14873 · Cited by 20
Yam, A. O. W., & Chtanova, T. (2019) · Cellular Immunology · doi:10.1016/j.cellimm.2019.01.003 · Cited by 19
Banu, S., Gaur, N., Nair, S., Ravikrishnan, T., Khan, S. A., Mani, S., Bharathi, S., Mandal, K., Kuram, N. A., Vuppaladadium, S., et al. (2022) · Genomics · doi:10.1016/j.ygeno.2022.110300 · Cited by 18
Xiong, Y., Halima, M., Che, X., Zhang, Y., Schaaf, M. J. M., Li, M., Gao, M., Guo, L., Huang, Y., Cui, X., et al. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.946900 · Cited by 18
Zhang, L., Chen, C., Li, X., Sun, S., Liu, J., Wan, M., Huang, L., Yang, D., Huang, B., Zhong, Z., et al. (2022) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2022.09.063 · Cited by 18
Abarca‐Buis, R. F., Martínez-Jiménez, A., Vera‐Gómez, E., Contreras-Figueroa, M. E., Garciadiego-Cázares, D., Paus, R., Robles‐Tenorio, A., & Krötzsch, E. (2017) · Differentiation · doi:10.1016/j.diff.2017.12.001 · Cited by 18
Bollaerts, I., houcke, J. V., Beckers, A., Lemmens, K., Vanhunsel, S., Groef, L. D., & Moons, L. (2019) · Mediators of Inflammation · doi:10.1155/2019/6135795 · Cited by 18
“red fluorescent protein (DsRed) is present in neutrophils only [24, 29].”
BackgroundTang, H., Ge, H., Chen, Z., Luo, X., Su, F., Liang, Y., Li, Z., Wu, J., Yang, Q., Zeng, L., et al. (2015) · Marine Drugs · doi:10.3390/md13095593 · Cited by 17
“Fish Lines—wild-type AB and the transgenic zebrafish line Tg (corola: eGFP), in which both macrophages and neutrophils express eGFP, was kindly provided by the Key Laboratory of Zebrafish Modeling and Drug Screening for Human Diseases of Guangdong Higher Education Institutes, Department of Cell Biology, Southern Medic…”
MethodOzone promotes regeneration by regulating the inflammatory response in zebrafish
Hao, K., Li, Y., Feng, J., Zhang, W., Zhang, Y., Ma, N., Zeng, Q., Pang, H., Wang, C., Xiao, L., et al. (2015) · International Immunopharmacology · doi:10.1016/j.intimp.2015.05.026 · Cited by 17
“2A) [25].”
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
Gilmore, N. J., Banach, M., Brown, E. B., Dawes, R. P., Edholm, E., Kim, M., & Robert, J. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.01.003 · Cited by 16
“To date this approach has been mainly developed in mouse and zebrafish models (Li et al., 2012; Nguyen et al., 2012; Painter and Ceol, 2014).”
MethodQian, Q., Song, J., Pu, Q., Chen, C., Yan, J., & Wang, H. (2023) · Aquatic Toxicology · doi:10.1016/j.aquatox.2023.106514 · Cited by 16
Kanagaraj, P., Chen, J. Y., Skaggs, K., Qadeer, Y., Connors, M., Cutler, N. S., Richmond, J., Kommidi, V., Poles, A., Affrunti, D., et al. (2023) · Glia · doi:10.1002/glia.24444 · Cited by 26
Zeng, Y., Yan, B., Sun, Q., He, S., Jiang, J., Wen, Z., & Qu, J. Y. (2014) · Biomedical Optics Express · doi:10.1364/boe.5.000653 · Cited by 16
Chen, Q., Chen, J., Chen, J., & Lu, X. (2016) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2016.08.007 · Cited by 16
Pericytes in Cutaneous Wound Healing
Morikawa, S., Iribar, H., Gutiérrez‐Rivera, A., Ezaki, T., & Izeta, A. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-16908-4_1 · Cited by 17
Bando, T., Okumura, M., Bando, Y., Hagiwara, M., Hamada, Y., Ishimaru, Y., Mito, T., Kawaguchi, E., Inoue, T., Agata, K., et al. (2021) · Development · doi:10.1242/dev.199916 · Cited by 16
Rapid orderly migration of neutrophils after traumatic brain injury depends on MMP9/13
Zou, D., Hu, W., Qin, J., Wei, Z., Wang, D., & Li, L. (2021) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2021.09.044 · Cited by 15
Qian, Q., Pu, Q., Li, X., Liu, X., Ni, A., Han, X., Wang, Z., Wang, X., Yan, J., & Wang, H. (2024) · Chemosphere · doi:10.1016/j.chemosphere.2024.141395 · Cited by 15
Wang, F., Wang, X., Gao, L., Meng, L.-Y., Xie, J.-M., Xiong, J., & Luo, Y. (2019) · Nanoscale · doi:10.1039/c9nr05758g · Cited by 16
Cannabidiol promotes fin regeneration and reduces apoptosis in zebrafish embryos
Xu, S., Zhang, H., Li, C.-Z., Lai, P., Wang, G., Chan, Y. S., Cheng, S. H., & Chen, X. (2021) · Journal of Functional Foods · doi:10.1016/j.jff.2021.104694 · Cited by 15
White, D. T., Saxena, M. T., & Mumm, J. S. (2019) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2019.01.011 · Cited by 15
Macrophage-Derived IL-1β Regulates Emergency Myelopoiesis via the NF-κB and C/ebpβ in Zebrafish
Wei, Z., Li, C., Zhang, Y., Lin, C., Zhang, Y., Shu, L., Luo, L., Zhuo, J., & Li, L. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.2000473 · Cited by 16
“AB, Tg(lyz:DsRed) and Tg(lyz:eGFP) (26), Tg(mpeg1:Gal4,UAS:NfsbmCherry) (27), Tg(runx1:GFP), Tg(NF-kB:GFP), Tg(CD41:GFP) (16), Tg(mpeg1:GFP) (28), Tg(hsp70:il1b-eGFP), Tg(kdrl:mCherry) (29), Tg(coro1a:dsred) (26), Tg(coro1a: C/ebpb), irf8 (30), myd88 (16), and C/ebpb strains were used, and their information is listed…”
BackgroundRampon, C., Gauron, C., Meda, F., Volovitch, M., & Vriz, S. (2014) · Purinergic Signalling · doi:10.1007/s11302-014-9420-9 · Cited by 15
“The infiltration of macrophages is required for blastema formation in newts regenerating their limbs [29], as well as in adult zebrafish regenerating their caudal fin and their heart [30, 31].”
BackgroundBrain milieu induces early microglial maturation through the BAX-Notch axis
Zhao, F., He, J., Tang, J., Cui, N., Shi, Y., Li, Z., Liu, S., Wang, Y., Ma, M., Zhao, C., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33836-2 · Cited by 14
“The mib ta52b mutant 48 , Tg ( coro1a:DsRed ) 31 , Tg ( coro1a:Kaede ) 49 , Tg ( mfap4:GFP ) 50 , Tg ( apoeb:GFP ) 30 , Tg(ubiq:secAnnexinV-mVenus) 51 ; Tg ( Tp1bglob:eGFP ) 52 , Tg ( Tp1bglob:hmgb1-mCherry ) 52 , Tg ( hsp70:DN-MAML-GFP ) 53 , Tg ( HuC:GCaMP6s ) 54 wereemployed.”
InfluentialMoon, H.-Y., Kim, O.-H., Kim, H.-T., Choi, J., Yeo, S., Kim, N.-S., Park, D., Oh, H.-W., You, K., Zoysa, M. D., et al. (2013) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2013.02.021 · Cited by 14
Zebrafish Xenograft Model for Studying Pancreatic Cancer-Instructed Innate Immune Microenvironment
Wang, X., Li, W., Jiang, H., Ma, C., Huang, M., Wei, X., Wang, W., & Jing, L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23126442 · Cited by 14
“To do that, we injected PANC1, BxPC3, and AsPC1 cells into Tg(coro1a: GFP) zebrafish hosts, which labels the innate immune cells including neutrophils and macrophages, and also marks the lymphocytes in the thymus [29].”
MethodSu, X., Li, K., Han, X., Wang, R., Yang, X. M., Wang, X., Yan, J., Qian, Q., Wang, Z., & Wang, H. (2025) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2025.179405 · Cited by 14
Zhan, Y., Huang, Y., Chen, J., Cao, Z., He, J., Zhang, J., Huang, H., Ruan, H., Luo, L., & Li, L. (2018) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2018.02.010 · Cited by 13
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
Zhang, G., Sun, J., Liu, M., Tian, Z., Ma, Z., Hao, B., Ning, J., Ren, X., Wang, M., Wang, P., et al. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114233 · Cited by 13
“Fishing” nano–bio interactions at the key biological barriers
Rong, J., He, Y., Tang, J., Qiao, R., & Lin, S. (2021) · Nanoscale · doi:10.1039/d1nr00328c · Cited by 12
The chromatin-remodeling enzyme Smarca5 regulates erythrocyte aggregation via Keap1-Nrf2 signaling
Ding, Y., Li, Y., Zhao, Z., Zhang, Q. C., & Liu, F. (2021) · eLife · doi:10.7554/elife.72557 · Cited by 13
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 11
“In the inflammatory phase after caudal fin amputation, neutrophils are the main scavengers of small dead cell debris, and macrophages are essential to alleviate inflammation and support the normal regeneration of the regenerated caudal fin [10].”
BackgroundHe, B., Wang, W., Wen, J., Zhang, R., Lin, W. X., Guo, Y., Xu, Y., Huser, T. R., Wei, X., & Yang, Z. (2024) · Journal of Biophotonics · doi:10.1002/jbio.202400026 · Cited by 12
Yam, A. O. W., Jakovija, A., Gatt, C., & Chtanova, T. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1458035 · Cited by 13
Metadata
- Authors
- Li, L., Yan, B., Shi, Y.-Q., Zhang, W.-Q., & Wen, Z.-L.
- Affiliations
- Southwest University (CN)
- Hong Kong University of Science and Technology (HK)
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2012-07
- Volume
- 287
- Issue
- 30
- Pages
- 25353-25360
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC3408142
- OpenAlex
- W1980758898
- Cited by
- 353
- References
- 49
- Citations by year
- 2026: 26 · 2025: 24 · 2024: 23 · 2023: 21 · 2022: 41 · 2021: 34 · 2020: 22 · 2019: 36 · 2018: 19 · 2017: 24 · 2016: 23 · 2015: 19 · 2014: 25 · 2013: 13 · 2012: 3
- FWCI
- 9.09
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Rare & Special e-Zone (The Hong Kong University of Science and Technology) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
- Health Sciences › Medicine › Surgery › Wound Healing and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Planarian Biology and Electrostimulation
- Keywords
- macrophages, neutrophils, tail fin regeneration, zebrafish, wound healing, phagocytosis, inflammation resolution, tissue remodeling, macrophage depletion, live imaging
- MeSH terms
- Animals, Macrophages, Neutrophils, Regeneration, Tail, Zebrafish, Animal Fins
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