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.
“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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“Similar findings have been reported in other regenerative species including zebrafish, where ablation of macrophages results in defects in fin regeneration following injury (21).”
ResultInfluentialEffects of inflammation on stem cells: together they strive?
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“During zebrafish fin regeneration, ablation of macrophages impairs regenerative outgrowth through reduced resolution of inflammation [36,124].”
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MethodModeling Inflammation in Zebrafish for the Development of Anti-inflammatory Drugs
Xie, Y., Meijer, A. H., & Schaaf, M. J. M. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.620984 · Cited by 164 · see citing works
“, 2015)], or by a promoter that marks both these cell types [coro1a (Li et al., 2012) and pu.”
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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
Zebrafish as a model for the study of neutrophil biology
Henry, K. M., Loynes, C. A., Whyte, M. K. B., & Renshaw, S. A. (2013) · Journal of Leukocyte Biology · doi:10.1189/jlb.1112594 · Cited by 143 · see citing works
“More recently, differing roles of macrophages and neutrophils during zebrafish tail-fin regeneration [54] have been discovered, using VE-DIC microscopy to distinguish between these two leukocytes based on their morphology at a wound site, confirming cell-specific transgene expression, and helping to elucidate macropha…”
BackgroundHydrogen peroxide primes heart regeneration with a derepression mechanism
Han, P., Zhou, X., Chang, N., Xiao, C., Yan, S., Ren, H., Yang, X., Zhang, M., Wu, Q., Tang, B., et al. (2014) · Cell Research · doi:10.1038/cr.2014.108 · Cited by 137 · see citing works
Tauzin, S., Starnes, T. W., Barros-Becker, F., Lam, P., & Anna Huttenlocher, A. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201408090 · Cited by 137 · see citing works
“In accordance with previous studies (Holmes et al., 2012; Li et al., 2012), we found that neutrophils and macrophages are recruited with different kinetics to tissue damage (Fig.”
Apoptosis in fish: environmental factors and programmed cell death
AnvariFar, H., Amirkolaie, A. K., Miandare, H. K., Ouraji, H., Jalali, M. A., & Üçüncü, S. İ. (2016) · Cell and Tissue Research · doi:10.1007/s00441-016-2548-x · Cited by 133 · see citing works
“The delay in the clearance of cell debris, a decrease of regeneration speed and formation of vacuoles in the regenerating fin were observed after the depletion of macrophages in the zebrafish model (Li et al. 2012).”
BackgroundBalic, A., García-Morales, C., Vervelde, L., Gilhooley, H., Sherman, A., Garceau, V., Gutowska, M., Burt, D., Kaiser, P., Hume, D., et al. (2014) · Development · doi:10.1242/dev.105593 · Cited by 112 · see citing works
“To date, there have been only limited reports of live imaging of macrophages in vertebrate embryos (Herbomel et al., 1999; Colucci-Guyon et al., 2011; Li et al., 2012; Al-Roubaie et al., 2012).”
BackgroundVriz, S., Reiter, S., & Galliot, B. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-391498-9.00002-4 · Cited by 111 · see citing works
“, 2013) as well as in adult zebrafish regenerating their caudal fin and their heart (Li et al., 2012; Huang et al., 2013).”
BackgroundMyocardial NF-κB activation is essential for zebrafish heart regeneration
Karra, R., Knecht, A. K., Kikuchi, K., & Poss, K. D. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1511209112 · Cited by 113 · 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
Ge, H., Tang, H., Liang, Y., Wu, J., Yang, Q., Zeng, L., & Ma, Z.-F. (2017) · Drug Design Development and Therapy · doi:10.2147/dddt.s133069 · Cited by 100 · see citing works
“Preparation of inflammation-induced zebrafish model by tail cutting and application of rhein The transgenic zebrafish line TG (corolla: enhanced green fluorescent protein [eGFP]), which expresses eGFP in both macrophages and neutrophils, was kindly provided by the Key Laboratory of Zebrafish Modeling and Drug Screenin…”
MethodYan, B., Han, P., Pan, L., Lü, W., Xiong, J., Zhang, M., Zhang, W., Li, L., & Wen, Z. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1301645 · Cited by 92 · see citing works
“2A–C, 2I) in Tg(coro1a:eGFP,lyz:DsRed2)hkz04t,nz50 transgenic zebrafish, in which macrophages and neutrophils can be labeled by different fluorescent colors (2).”
BackgroundMethodInfluentialRecent advances on the association of apoptosis in chronic non healing diabetic wound
Arya, A. K. (2014) · World Journal of Diabetes · doi:10.4239/wjd.v5.i6.756 · Cited by 92 · see citing works
Innate immune system and tissue regeneration in planarians: An area ripe for exploration
Peiris, T. H., Hoyer, K. K., & Oviedo, N. J. (2014) · Seminars in Immunology · doi:10.1016/j.smim.2014.06.005 · Cited by 86 · see citing works
“[80] Li L, Yan B, Shi YQ, Zhang WQ, Wen ZL.”
BackgroundDelineating the roles of neutrophils and macrophages in zebrafish regeneration models
Keightley, M.-C., Wang, C., Pazhakh, V., & Lieschke, G. J. (2014) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2014.07.010 · Cited by 82 · 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
“, 2016), fins (Li et al., 2012; Petrie et al., 2014), spinal cord, and the heart (Lai et al.”
BackgroundPei, W., Tanaka, K., Huang, S. C., Xu, L., Liu, B., Sinclair, J. W., Idol, J., Varshney, G. K., Huang, H., Lin, S., et al. (2016) · npj Regenerative Medicine · doi:10.1038/npjregenmed.2016.13 · Cited by 81 · see citing works
“27 47–51 In addition, transcriptional analysis has revealed that several immune response genes are associated with the regeneration of the heart and retina in zebrafish.”
Xiong, G., Deng, Y., Li, J., Cao, Z., Liao, X., Liu, Y., & Lu, H. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.124423 · Cited by 80 · see citing works
Inflammation induces zebrafish regeneration
Iribarne, M. (2021) · Neural Regeneration Research · doi:10.4103/1673-5374.306059 · Cited by 73 · see citing works
“Li and coworkers showed that cytokines IL-1β, TNF-β, and IL10 were increased during the inflammation phase, and were significantly reduced during the resolution phase (Li et al., 2012).”
BackgroundResultInfluentialMacrophages – sensors and effectors coordinating skin damage and repair
Willenborg, S., & Eming, S. A. (2014) · Journal der Deutschen Dermatologischen Gesellschaft = Journal of the German Society of Dermatology : JDDG · doi:10.1111/ddg.12290 · Cited by 80 · see citing works
White, D. T., & Mumm, J. S. (2013) · Methods · doi:10.1016/j.ymeth.2013.03.017 · Cited by 77 · see citing works
“Interestingly, ablation of macrophages (but not neutrophils) impaired resolution of the inflammatory response and inhibited regeneration – conversely, ablation of neutrophils (but not macrophages) accelerated regrowth of the injured fin [40].”
BackgroundMethodLeBert, D. C., & Huttenlocher, A. (2014) · Seminars in Immunology · doi:10.1016/j.smim.2014.04.007 · Cited by 77 · see citing works
Blood derivatives awaken in regenerative medicine strategies to modulate wound healing
Mendes, B. B., Gómez‐Florit, M., Babo, P. S., Domingues, R. M. A., Reis, R. L., & Gomes, M. E. (2017) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2017.12.018 · Cited by 75 · see citing works
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“In contrast, polymorphonuclear leukocytes, which are recruited by axonal degradation (54), were rarely seen in the many samples we have inspected.”
BackgroundResultRegeneration of the central nervous system-principles from brain regeneration in adult zebrafish
Zambusi, A., & Ninkovic, J. (2019) · World Journal of Stem Cells · doi:10.4252/wjsc.v12.i1.8 · Cited by 72 · see citing works
The Interaction between Joint Inflammation and Cartilage Repair
van der Kraan, P. M. (2019) · Tissue Engineering and Regenerative Medicine · doi:10.1007/s13770-019-00204-z · Cited by 71 · see citing works
Xue, Y., Lv, J., Zhang, C., Wang, L., Ma, D., & Liu, F. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.07.012 · Cited by 71 · see citing works
NF-κB Signaling Negatively Regulates Osteoblast Dedifferentiation during Zebrafish Bone Regeneration
Mishra, R., Sehring, I. M., Cederlund, M. L., Mulaw, M. A., & Weidinger, G. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.11.016 · Cited by 70 · see citing works
T6SS Mediated Stress Responses for Bacterial Environmental Survival and Host Adaptation
Yu, K., Xue, P., Fu, Y., & Yang, L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22020478 · Cited by 72 · see citing works
“The highly motile phagocytic cells, neutrophils and macrophages, can be recruited to the sites of tissue infection as the first-line of defence [98].”
BackgroundXu, S., Webb, S., Lau, T. C., & Cheng, S. H. (2018) · Scientific Reports · doi:10.1038/s41598-018-25490-w · Cited by 69 · see citing works
Development of a Zebrafish Sepsis Model for High-Throughput Drug Discovery
Philip, A. M., Wang, Y., Mauro, A., El‐Rass, S., Marshall, J. C., Lee, W. L., Slutsky, A. S., dos Santos, C. C., & Wen, X. (2017) · Molecular Medicine · doi:10.2119/molmed.2016.00188 · Cited by 66 · see citing works
Definitive hematopoietic stem cells minimally contribute to embryonic hematopoiesis
Ulloa, B. A., Habbsa, S. S., Potts, K. S., Lewis, A., McKinstry, M., Payne, S. G., Flores, J. C., Nizhnik, A., Norberto, M. F., Mosimann, C., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109703 · Cited by 63 · see citing works
“…(Gutiérrez et al., 2020; Galloway et al., 2005), ikzf1 (lymphoid) (Huang et al., 2019; Willett et al., 2001), and coro1a and csf1rb (myeloid) (Li et al., 2012; Carstanjen et al., 2005; Song et al., 2004); we consequently designated cluster C6 as hemogenic endothelial cells generating HSCs…”
In Vivo Imaging Reveals a Pioneer Wave of Monocyte Recruitment into Mouse Skin Wounds
Rodero, M., Licata, F., Poupel, L., Hamon, P., Khosrotehrani, K., Combadière, C., & Boissonnas, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108212 · Cited by 55 · see citing works
“resolution, Li et al showed that in newly injured zebrafish models, local resident macrophages and neutrophils are the first myeloid cells recruited, followed shortly after by circulating neutrophils, and later on by circulating monocytes [30].”
BackgroundLRH-1 agonism favours an immune-islet dialogue which protects against diabetes mellitus
Cobo‐Vuilleumier, N., Lorenzo, P. I., Rodríguez, N. G., Herrera-Gómez, I. D. G., Fuente-Martín, E., López–Noriega, L., Mellado‐Gil, J. M., Romero‐Zerbo, S., Baquié, M., Lachaud, C. C., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03943-0 · Cited by 65 · see citing works
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Zou, S., Tian, C., Ge, S., & Hu, B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057280 · Cited by 64 · see citing works
“AB/WT, Tg(coro1a:eGFP; lyz:DsRed) [32], Tg(olig2:eGFP) [33] and Tg(flk:GFP) transgenic lines were used for different aims.”
MethodAutophagy as a Therapeutic Target to Enhance Aged Muscle Regeneration
Lee, D. E., Bareja, A., Bartlett, D. B., & White, J. P. (2019) · Cells · doi:10.3390/cells8020183 · Cited by 64 · see citing works
Shan, Y., Fang, C., Cheng, C., Wang, Y., Peng, J., & Fang, W. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00373 · Cited by 59 · see citing works
“Received: 27 January 2015 Accepted: 12 April 2015 Published: 29 April 2015 Citation: Shan Y, Fang C, Cheng C, Wang Y, Peng J and Fang W (2015) Immersion infection of germ-free zebrafish with Listeria monocytogenes induces transient expression of innate immune response genes.”
BackgroundHoodless, L. J., Lucas, C. D., Duffin, R., Denvir, M. A., Haslett, C., Tucker, C. S., & Rossi, A. G. (2016) · Scientific Reports · doi:10.1038/srep36980 · Cited by 61 · see citing works
Lin, X., Zhou, Q., Zhao, C., Lin, G., Xu, J., & Wen, Z. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.03.028 · Cited by 61 · see citing works
Muscle wound healing in rainbow trout (Oncorhynchus mykiss)
Schmidt, J. G., Andersen, E. W., Ersbøll, B. K., & Nielsen, M. E. (2015) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2015.12.010 · Cited by 58 · see citing works
Torraca, V., Otto, N. A., Tavakoli-Tameh, A., & Meijer, A. (2017) · Developmental and Comparative Immunology · doi:10.1016/j.dci.2016.10.014 · Cited by 52 · see citing works
Redirecting cardiac growth mechanisms for therapeutic regeneration
Karra, R., & Poss, K. D. (2017) · Journal of Clinical Investigation · doi:10.1172/jci89786 · Cited by 59 · see citing works
“Although it is unclear whether macrophage recruitment is required for zebrafish heart regeneration, the macrophage response appears to be critical for regeneration in other tissues, such as fins (109, 110).”
Signals Orchestrating Peripheral Nerve Repair
Rigoni, M., & Negro, S. (2020) · Cells · doi:10.3390/cells9081768 · Cited by 57 · see citing works
Exogenous melatonin inhibits neutrophil migration through suppression of ERK activation
Ren, D., Sun, A.-A., Li, Y., Chen, M., Ge, S., & Hu, B. (2015) · Journal of Endocrinology · doi:10.1530/joe-15-0329 · Cited by 57 · see citing works
Johnston, H. J., Verdon, R., Gillies, S. L. J., Brown, D. M., Fernandes, T. F., Henry, T. B., Rossi, A. G., Tran, L., Tucker, C. S., Tyler, C. R., et al. (2017) · Critical Reviews in Toxicology · doi:10.1080/10408444.2017.1404965 · Cited by 54 · see citing works
“…injury (tail fin wound, which involves transection of the zebrafish embryo’s tail; e.g. Renshaw et al. 2006; de Oliveira et al. 2013; Lucas et al. 2013; Hoodless et al. 2016), and micro-organisms (e.g. Renshaw et al. 2006; Li et al. 2012; Nguyen-Chi et al. 2014, reviewed in Meeker and Trede 2008).”
BackgroundAdult zebrafish Langerhans cells arise from hematopoietic stem/progenitor cells
He, S., Chen, J., Jiang, Y., Wu, Y., Zhu, L., Jin, W., Zhao, C., Yu, T., Wang, T., Wu, S., et al. (2018) · eLife · doi:10.7554/elife.36131 · Cited by 52 · see citing works
Macrophages in Zebrafish Models of Liver Diseases
Shwartz, A., Goessling, W., & Yin, C. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02840 · Cited by 53 · see citing works
Li, Y., & Hu, B. (2012) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2012.07.006 · Cited by 52 · 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
“Monocyte-derived macrophages are necessary for successful appendage regeneration in the axolotl and other model systems, playing roles that include directing blastemal outgrowth, clearing senescent cells and modulating blastemal cell proliferation (Li et al., 2012; Godwin et al., 2013; Petrie et al., 2014; Yun et al.,…”
BackgroundRodgers, A. K., Smith, J. J., & Voss, S. R. (2020) · Experimental Cell Research · doi:10.1016/j.yexcr.2020.112149 · Cited by 45 · 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
“1:GFP) and Tg(coro1a:eGFP) are also commonly used to track all myeloid cells [41,42].”
BackgroundGodwin, J. W. (2014) · Bioessays · doi:10.1002/bies.201300144 · Cited by 53 · see citing works
“for macrophages, but not neutrophils, in epimorphic regeneration has recently been confirmed using conditional ablation in zebrafish fin regeneration, reinforcing the importance of innate immune signaling in epimorphic regeneration [49].”
BackgroundSok, C., Baker, N. F., McClain, C. A., Lim, H. S., Turner, T., Hymel, L. A., Ogle, M. E., Olingy, C. E., Palacios, J. I., García, J. R., et al. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.120475 · Cited by 50 · see citing works
He, M., Halima, M., Xie, Y., Schaaf, M. J. M., Meijer, A. H., & Wang, M. (2020) · Cells · doi:10.3390/cells9051107 · Cited by 52 · see citing works
“This conclusion is supported by a previous study using the zebrafish tail fin amputation assay in which ablation of the neutrophils did not affect regeneration of the fin, whereas ablation of macrophages did [49].”
ResultSmits, 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
Chen, Z., Yan, P., Zou, L., Zhao, M., Jiang, J., Liu, S., Zhang, K. Y., Huang, W., & Zhao, Q. (2018) · Advanced Healthcare Materials · doi:10.1002/adhm.201800309 · Cited by 48 · see citing works
Zhou, H., Cao, H., Zheng, Y., Lu, Z., Chen, Y., Liu, D., Yang, H., Quan, J., Huo, C., Liu, J., et al. (2019) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2019.112427 · Cited by 47 · 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
“In the zebrafish, with its high regenerative capacity, macrophages are also necessary for the regeneration of fins [87,97,100].”
BackgroundCalcineurin controls proximodistal blastema polarity in zebrafish fin regeneration
Cao, Z., Meng, Y., Gong, F., Xu, Z., Liu, F., Fang, M., Zou, L., Liao, X., Wang, X., Luo, L., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2009539118 · Cited by 46 · see citing works
The immune response is a critical regulator of zebrafish retinal pigment epithelium regeneration
Leach, L. L., Hanovice, N. J., George, S. M., Gabriel, A. E., & Gross, J. M. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2017198118 · Cited by 42 · see citing works
Iribarne, M., & Hyde, D. R. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.892271 · Cited by 45 · see citing works
“larvae and genetic ablation of macrophages affected fin growth in adult zebrafish (Li et al., 2012; Petrie et al., 2014).”
BackgroundChen, M., Luo, Y., Xu, J., Chang, M., & Liu, J. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02599 · Cited by 45 · see citing works
“In this study, red boxes for GFP-positive cell counting area were determined based on the wound loci in each larva as studies reported recently (7, 25), and”
BackgroundMethodResultInfluentialYang, X., Li, Y., Li, Y., Ye, D., Yuan, L., Sun, Y., Han, D., & Hu, Q. (2019) · Marine Drugs · doi:10.3390/md17040203 · Cited by 45 · see citing works
Using zebrafish as the model organism to understand organ regeneration
Shi, W., Fang, Z., Li, L., & Luo, L. (2015) · Science China Life Sciences · doi:10.1007/s11427-015-4838-z · Cited by 43 · see citing works
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Satarkar, D., & Patra, C. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.882017 · Cited by 42 · see citing works
“Like other vertebrates, neutrophils arrive first in zebrafish and scavenge debris, followed by macrophages in the resolution phase (Li et al., 2012).”
BackgroundSmarca5-mediated epigenetic programming facilitates fetal HSPC development in vertebrates
Ding, Y., Wang, W., Ma, D., Liang, G., Kang, Z., Xue, Y., Zhang, Y., Wang, L., Heng, J., Zhang, Y., et al. (2020) · Blood · doi:10.1182/blood.2020005219 · Cited by 41 · 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
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“These macrophages are the key scavengers for resolving inflammation and facilitating tissue regeneration (Li et al., 2012).”
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“They have also been shown to provide essential roles during the regeneration of various tissues, organs and appendages (Chazaud, 2014; Godwin et al., 2013; Li et al., 2012; Petrie et al., 2014; Tidball and WehlingHenricks, 2007).”
BackgroundCarrillo, S. A., Anguita-Salinas, C., Peña, O. A., Morales, R. A., Muñoz-Sánchez, S., Muñoz-Montecinos, C., Paredes-Zúñiga, S., Tapia, K., & Allende, M. (2016) · Journal of Cellular Biochemistry · doi:10.1002/jcb.25487 · Cited by 48 · see citing works
Anti-inflammatory properties of extracts from Chimonanthus nitens Oliv. leaf
Sun, Q., Zhu, J., Cao, F., & Chen, F. (2017) · PLoS ONE · doi:10.1371/journal.pone.0181094 · Cited by 41 · 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
de Oliveira, S., Boudinot, P., Calado, Â., & Mulero, V. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402386 · Cited by 41 · see citing works
“Regardless of their controversial role in wound healing, neutrophils are the first leukocytes to be recruited to wounds (4, 5).”
BackgroundChd7 Is Critical for Early T-Cell Development and Thymus Organogenesis in Zebrafish
Liu, Z., Wang, Z., Choi, T., Huang, W.-T., Wang, H.-T., Han, Y.-Y., Zhu, L., Kim, H.-T., Choi, J.-H., Lee, J. S., et al. (2018) · American Journal Of Pathology · doi:10.1016/j.ajpath.2017.12.005 · Cited by 40 · see citing works
- 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 › Rehabilitation › 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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