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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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Ogle, M. E., Segar, C. E., Sridhar, S., & Botchwey, E. A. (2016) · Experimental Biology and Medicine · doi:10.1177/1535370216650293 · Cited by 378
“The striking evolutionary examples of complex tissue regeneration in the salamander limb and zebrafish tailfin require the presence of myeloid cells and regeneration fails when macrophages are depleted prior to injury.(2,3) Increasing evidence suggests that division of labor among subpopulations of monocytes and macro…”
BackgroundMacrophages 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
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ResultZebrafish Regulatory T Cells Mediate Organ-Specific Regenerative Programs
Hui, S. P., Sheng, D. Z., Sugimoto, K., González-Rajal, Á., Nakagawa, S., Hesselson, D., & Kikuchi, K. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.11.010 · Cited by 272
Model systems for regeneration: zebrafish
Marques, I. J., Lupi, E., & Mercader, N. (2019) · Development · doi:10.1242/dev.167692 · Cited by 254
“Supporting these findings, genetic or chemical ablation of phagocytic macrophages during regeneration results in impaired fin (Li et al., 2012; Petrie et al., 2014), lateral line (Carrillo et al.”
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TNF signaling and macrophages govern fin regeneration in zebrafish larvae
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“In our system TNF α promotes macrophage recruitment, presumably acting as an enhancing loop for macrophage accumulation to the wound (Figure 7).”
A sensitive GRAB sensor for detecting extracellular ATP in vitro and in vivo
Wu, Z., He, K., Chen, Y., Li, H., Pan, S., Li, B., Liu, T., Xi, F., Deng, F., Wang, H., et al. (2022) · Neuron · doi:10.1016/j.neuron.2021.11.027 · Cited by 204
Tumor-Infiltrating Immune Cells Promoting Tumor Invasion and Metastasis: Existing Theories
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Godwin, J. W., & Rosenthal, N. A. (2014) · Differentiation · doi:10.1016/j.diff.2014.02.002 · Cited by 198
“…in regeneration has been confirmed in other regenerative animal models such as zebrafish: 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 (Li et al., 2012).”
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Macrophages are necessary for epimorphic regeneration in African spiny mice
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“…and tissue-specific macrophages are activated in response to injury and are recruited to the injury site at the outset of regenerative and scarring responses (Godwin et al., 2013; Li et al., 2012; Nguyen-Chi et al., 2015; reviewed in Novak and Koh, 2013; Petrie et al., 2014; Varga et al., 2016).”
BackgroundRethinking Regenerative Medicine: A Macrophage-Centered Approach
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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?
Kızıl, Ç., Kyritsis, N., & Brand, M. (2015) · EMBO Reports · doi:10.15252/embr.201439702 · Cited by 190
“During zebrafish fin regeneration, ablation of macrophages impairs regenerative outgrowth through reduced resolution of inflammation [36,124].”
Xu, J., Zhu, L., He, S., Wu, Y., Jin, W., Yu, T., Qu, J. Y., & Wen, Z. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.08.018 · Cited by 177
“Using Lcp1 as a microglia marker (Herbomel et al., 1999; Li et al., 2012a; Meijer et al., 2008), a significant number of GFP and Lcp1 double positive (GFP/Lcp1) microglia (on average 43%) were detected in the brains of 4 dpf RBI-labeled embryos by immunohistochemistry, whereas GFP cells were rarely seen in the brains…”
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
“, 2015)], or by a promoter that marks both these cell types [coro1a (Li et al., 2012) and pu.”
BackgroundInfluentialXu, J., Wang, T., Wu, Y., Jin, W., & Wen, Z. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.06.018 · Cited by 169
“8elavl3:eGFP;coro1a:DsRedx) embryos where neurons and leukocytes (mainly neutrophils and macrophages/microglia at early stages) are labeled by GFP and DsRed-Express (DsRedx), respectively (Li et al., 2012a; Zhao et al., 2006) and determined the distribution and number of microglia by direct observation under a confoca…”
MethodHasegawa, T., Hall, C. J., Crosier, P. S., Abe, G., Kawakami, K., Kudō, A., & Kawakami, A. (2017) · eLife · doi:10.7554/elife.22716 · Cited by 154
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“Besides their role in innate immunity, M F are also involved in tissue repair (108, 180, 201).”
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., & Huttenlocher, A. (2015) · Development · doi:10.1242/dev.121160 · Cited by 151
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
“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 143
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“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
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“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).”
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“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).”
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“, 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 117
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“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
“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
Innate immune system and tissue regeneration in planarians: An area ripe for exploration
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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
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“, 2016), fins (Li et al., 2012; Petrie et al., 2014), spinal cord, and the heart (Lai et al.”
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“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.”
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Inflammation induces zebrafish regeneration
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“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) · JDDG Journal der Deutschen Dermatologischen Gesellschaft · doi:10.1111/ddg.12290 · Cited by 81
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“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].”
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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
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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.”
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Zambusi, A., & Ninkovic, J. (2019) · World Journal of Stem Cells · doi:10.4252/wjsc.v12.i1.8 · Cited by 72
The Interaction between Joint Inflammation and Cartilage Repair
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Development of a Zebrafish Sepsis Model for High-Throughput Drug Discovery
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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 66
“…(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
“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
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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 65
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“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.”
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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
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
Redirecting cardiac growth mechanisms for therapeutic regeneration
Karra, R., & Poss, K. D. (2017) · Journal of Clinical Investigation · doi:10.1172/jci89786 · Cited by 60
“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
Exogenous melatonin inhibits neutrophil migration through suppression of ERK activation
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“…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 53
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 56
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
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 53
“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
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 53
“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 52
“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 51
He, M., Halima, M., Xie, Y., Schaaf, M. J. M., Meijer, A. H., & Wang, M. (2020) · Cells · doi:10.3390/cells9051107 · Cited by 53
“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
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
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
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 52
“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
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
Iribarne, M., & Hyde, D. R. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.892271 · Cited by 46
“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 44
“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
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
Yu, T., Guo, W., Tian, Y., Xu, J., Chen, J., Li, L., & Wen, Z. (2017) · Blood · doi:10.1182/blood-2016-07-727651 · Cited by 42
Satarkar, D., & Patra, C. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.882017 · Cited by 42
“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 42
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
Bardaa, S., Moalla, D., Khedir, S. B., Rebaï, T., & Sahnoun, Z. (2015) · Pharmaceutical Biology · doi:10.3109/13880209.2015.1067233 · Cited by 41
“These macrophages are the key scavengers for resolving inflammation and facilitating tissue regeneration (Li et al., 2012).”
BackgroundParedes, R., Ishibashi, S., Borrill, R. E., Robert, J., & Amaya, E. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.03.008 · Cited by 40
“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. L. (2016) · Journal of Cellular Biochemistry · doi:10.1002/jcb.25487 · Cited by 44
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 43
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 42
de Oliveira, S., Boudinot, P., Calado, Â., & Mulero, V. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402386 · Cited by 41
“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
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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