A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish
Open accessAbstract
Barrier structures (for example, epithelia around tissues and plasma membranes around cells) are required for internal homeostasis and protection from pathogens. Wound detection and healing represent a dormant morphogenetic program that can be rapidly executed to restore barrier integrity and tissue homeostasis. In animals, initial steps include recruitment of leukocytes to the site of injury across distances of hundreds of micrometres within minutes of wounding. The spatial signals that direct this immediate tissue response are unknown. Owing to their fast diffusion and versatile biological activities, reactive oxygen species, including hydrogen peroxide (H(2)O(2)), are interesting candidates for wound-to-leukocyte signalling. Here we probe the role of H(2)O(2) during the early events of wound responses in zebrafish larvae expressing a genetically encoded H(2)O(2) sensor. This reporter revealed a sustained rise in H(2)O(2) concentration at the wound margin, starting approximately 3 min after wounding and peaking at approximately 20 min, which extended approximately 100-200 microm into the tail-fin epithelium as a decreasing concentration gradient. Using pharmacological and genetic inhibition, we show that this gradient is created by dual oxidase (Duox), and that it is required for rapid recruitment of leukocytes to the wound. This is the first observation, to our knowledge, of a tissue-scale H(2)O(2) pattern, and the first evidence that H(2)O(2) signals to leukocytes in tissues, in addition to its known antiseptic role.
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?
ROS can serve as immediate damage attractants to draw immune cells to wounds in zebrafish.
“Currently, the most exciting insight from zebrafish studies of wound inflammation has been that ROS can serve as immediate damage attractants to draw immune cells to wounds (127).”
From Wound repair and regeneration: Mechanisms, signaling, and translation (2014) · cites this paper as [127]
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
The NOX Family of ROS-Generating NADPH Oxidases: Physiology and Pathophysiology
Bedard, K., & Krause, K.-H. (2007) · Physiological Reviews · doi:10.1152/physrev.00044.2005 · Cited by 6,989 · see citing works
Genetically encoded fluorescent indicator for intracellular hydrogen peroxide
Belousov, V. V., Fradkov, A. F., Lukyanov, K. A., Staroverov, D. B., Shakhbazov, K., Terskikh, A. V., & Lukyanov, S. (2006) · Nature Methods · doi:10.1038/nmeth866 · Cited by 1,260 · see citing works
Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-γ and PTEN
Zhao, M., Song, B., Pu, J., Wada, T., Reid, B., Tai, G., Wang, F., Guo, A., Walczysko, P., Gu, Y., et al. (2006) · Nature · doi:10.1038/nature04925 · Cited by 1,171 · see citing works
Membrane transport of hydrogen peroxide
Bienert, G. P., Schjoerring, J. K., & Jahn, T. P. (2006) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2006.02.015 · Cited by 1,079 · see citing works
A Direct Role for Dual Oxidase in Drosophila Gut Immunity
Ha, E.-M., Oh, C.-T., Bae, Y. S., & Lee, W. (2005) · Science · doi:10.1126/science.1117311 · Cited by 824 · see citing works
Kwon, J., Lee, S.-R., Yang, K.-S., Ahn, Y., Kim, Y. J., Stadtman, E. R., & Rhee, S. G. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407396101 · Cited by 631 · see citing works
(2002) · doi:10.1093/oso/9780199638086.001.0001 · Cited by 589 · see citing works
The zebrafish lysozyme C promoter drives myeloid-specific expression in transgenic fish
Hall, C. J., Flores, M. V., Storm, T., Crosier, K., & Crosier, P. S. (2007) · BMC Developmental Biology · doi:10.1186/1471-213x-7-42 · Cited by 582 · see citing works
Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish
Mathias, J. R., Perrin, B. J., Liu, T.-X., Kanki, J. P., Look, A. T., & Anna Huttenlocher, A. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.0506346 · Cited by 532 · see citing works
Self-citationDual oxidases represent novel hydrogen peroxide sources supporting mucosal surface host defense
Geiszt, M., Witta, J., Baff, J., Lekstrom, K. J., & Leto, T. L. (2003) · The FASEB Journal · doi:10.1096/fj.02-1104fje · Cited by 505 · see citing works
Redox signals in wound healing
Sen, C. K., & Roy, S. (2008) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2008.01.006 · Cited by 349 · see citing works
Molecular evolution of the reactive oxygen-generating NADPH oxidase (Nox/Duox) family of enzymes
Kawahara, T., Quinn, M. T., & Lambeth, J. D. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-109 · Cited by 336 · see citing works
Bertrand, J. Y., Kim, A. D., Violette, E. P., Stachura, D. L., Schwedler, J. L., & Traver, D. J. (2007) · Development · doi:10.1242/dev.012385 · Cited by 330 · see citing works
Wound healing and inflammation: embryos reveal the way to perfect repair
Redd, M. J., Cooper, L., Wood, W., Stramer, B., & Martin, P. (2004) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2004.1466 · Cited by 289 · see citing works
Control of cell polarity and motility by the PtdIns(3,4,5)P3 phosphatase SHIP1
Nishio, M., Watanabe, K., Sasaki, J., Taya, C., Takasuga, S., Iizuka, R., Balla, T., Yamazaki, M., Watanabe, H., Itoh, R., et al. (2006) · Nature Cell Biology · doi:10.1038/ncb1515 · Cited by 288 · see citing works
Fluorescent Probes for Hydrogen Peroxide Based on a Non‐Oxidative Mechanism
Maeda, H., Fukuyasu, Y., Yoshida, S., Fukuda, M., Saeki, K., Matsuno, H., Yamauchi, Y., Yoshida, K., Hirata, K., & Miyamoto, K. (2004) · Angewandte Chemie International Edition · doi:10.1002/anie.200452381 · Cited by 271 · see citing works
TENFREYHAUS, H., HUNTGEBURTH, M., WINGLER, K., SCHNITKER, J., BAUMER, A., VANTLER, M., BEKHITE, M., WARTENBERG, M., SAUER, H., & ROSENKRANZ, S. (2006) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.01.022 · Cited by 259 · see citing works
Redox Modulation of T-Type Calcium Channels in Rat Peripheral Nociceptors
Todorovic, S. M., Jevtović‐Todorović, V., Meyenburg, A., Mennerick, S. J., Perez‐Reyes, E., Romano, C., Olney, J. W., & Zorumski, C. F. (2001) · Neuron · doi:10.1016/s0896-6273(01)00338-5 · Cited by 253 · see citing works
Dual Oxidase-2 Has an Intrinsic Ca2+-dependent H2O2-generating Activity
Ameziane-El-Hassani, R., Morand, S., Boucher, J.-L., Frapart, Y.-M., Apostolou, D., Agnandji, D., Gnidehou, S., Ohayon, R., Noël-Hudson, M.-S., Francon, J., et al. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m500516200 · Cited by 248 · see citing works
Regulated Hydrogen Peroxide Production by Duox in Human Airway Epithelial Cells
Forteza, R., Salathe, M. A., Miot, F., Forteza, R., & Conner, G. E. (2005) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2004-0302oc · Cited by 240 · see citing works
Redox regulation of cellular functions
Oktyabrsky, O. N., & Smirnova, G. V. (2007) · Biochemistry (Moscow) · doi:10.1134/s0006297907020022 · Cited by 184 · see citing works
Chen, J., Ruan, H., Ng, S. M. E., Gao, C., Soo, H. M., Wu, W., Zhang, Z., Wen, Z., Lane, D. P., & Peng, J. (2005) · Genes & Development · doi:10.1101/gad.1366405 · Cited by 170 · see citing works
Airway Epithelial Cell Migration and Wound Repair by ATP-mediated Activation of Dual Oxidase 1
Wesley, U. V., Bove, P. F., Hristova, M., McCarthy, S. M., & van der Vliet, A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m606533200 · Cited by 139 · see citing works
Hydrogen peroxide-induced chemotaxis of mouse peritoneal neutrophils.
Klyubin, I. V., Kirpichnikova, K. M., & Gamaley, I. A. (1996) · PubMed · Cited by 137 · see citing works
Donkó, Á., Péterfi, Z., Sum, A., Leto, T. L., & Geiszt, M. (2005) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2005.1767 · Cited by 131 · see citing works
Novel Nox inhibitor of oxLDL-induced reactive oxygen species formation in human endothelial cells
Stielow, C., Catar, R. A., Müller, G. M., Wingler, K., Scheurer, P., Schmidt, H. H. H. W., & Morawietz, H. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.03.114 · Cited by 125 · see citing works
Tumor suppressor PTEN is a physiologic suppressor of chemoattractant-mediated neutrophil functions
Subramanian, K. K., Jia, Y., Zhu, D., Simms, B. T., Jo, H., Hattori, H., You, J., Mizgerd, J. P., & Luo, H. R. (2007) · Blood · doi:10.1182/blood-2006-10-055319 · Cited by 118 · see citing works
Lange, S., Heger, J., Euler, G., Wartenberg, M., Piper, H. M., & Sauer, H. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn258 · Cited by 96 · see citing works
Reverse leukocyte migration can be attractive or repulsive
Anna Huttenlocher, A., & Poznansky, M. C. (2008) · Trends in Cell Biology · doi:10.1016/j.tcb.2008.04.001 · Cited by 68 · see citing works
Birth and life of tissue macrophages and their migration in embryogenesis and inflammation in medaka
Grabher, C., Cliffe, A., Miura, K., Hayflick, J. S., Pepperkok, R., Rørth, P., & Wittbrodt, J. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.0806526 · Cited by 55 · see citing works
Self-citationShimohashi, N., Nakamuta, M., Uchimura, K., Sugimoto, R., Iwamoto, H., Enjoji, M., & Nawata, H. (2000) · Journal of Cellular Biochemistry · doi:10.1002/1097-4644(20000915)78:4 · Cited by 54 · see citing works
MODELING INFLAMMATION IN THE ZEBRAFISH: HOW A FISH CAN HELP US UNDERSTAND LUNG DISEASE
Renshaw, S. A., Loynes, C. A., Elworthy, S., et al. (2007) · Experimental Lung Research · doi:10.1080/01902140701756778 · Cited by 49 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [31]Nusslein-Volhard C Dahm R Zebrafish 2002 Oxford University Press NY
Cited by
Sorted by citations
Schroder, K., & Tschopp, J. (2010) · Cell · doi:10.1016/j.cell.2010.01.040 · Cited by 5,475 · see citing works
Wound repair and regeneration: Mechanisms, signaling, and translation
Eming, S. A., Martin, P., & Tomic-Canic, M. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3009337 · Cited by 3,562 · see citing works
Signal transduction by reactive oxygen species
Finkel, T. (2011) · Journal of Cell Biology · doi:10.1083/jcb.201102095 · Cited by 2,322 · see citing works
Sies, H. (2017) · Redox Biology · doi:10.1016/j.redox.2016.12.035 · Cited by 2,148 · see citing works
Chemistry and biology of reactive oxygen species in signaling or stress responses
Dickinson, B. C., & Chang, C. J. (2011) · Nature Chemical Biology · doi:10.1038/nchembio.607 · Cited by 1,821 · see citing works
Beyond oxidative stress: an immunologist's guide to reactive oxygen species
Nathan, C., & Cunningham-Bussel, A. (2013) · Nature Reviews Immunology · doi:10.1038/nri3423 · Cited by 1,619 · see citing works
Calcium and ROS: A mutual interplay
Görlach, A., Bertram, K., Hudecova, S., & Krizanova, O. (2015) · Redox Biology · doi:10.1016/j.redox.2015.08.010 · Cited by 1,546 · see citing works
Inflammation and metabolism in tissue repair and regeneration
Eming, S. A., Wynn, T. A., & Martin, P. (2017) · Science · doi:10.1126/science.aam7928 · Cited by 1,369 · see citing works
13 reasons why the brain is susceptible to oxidative stress
Cobley, J. N., Fiorello, M. L., & Bailey, D. M. (2018) · Redox Biology · doi:10.1016/j.redox.2018.01.008 · Cited by 1,215 · see citing works
Neutrophil migration in infection and wound repair: going forward in reverse
de Oliveira, S., Rosowski, E. E., & Huttenlocher, A. (2016) · Nature Reviews Immunology · doi:10.1038/nri.2016.49 · Cited by 1,058 · see citing works
Advances in skin grafting and treatment of cutaneous wounds
Sun, B. K., Siprashvili, Z., & Khavari, P. A. (2014) · Science · doi:10.1126/science.1253836 · Cited by 972 · see citing works
Tan, H.-Y., Wang, N., Li, S., Hong, M., Wang, X., & Feng, Y. (2016) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2016/2795090 · Cited by 657 · see citing works
Jones, D. P., & Sies, H. (2015) · Antioxidants & Redox Signaling · doi:10.1089/ars.2015.6247 · Cited by 647 · see citing works
Functions of ROS in Macrophages and Antimicrobial Immunity
Herb, M., & Schramm, M. (2021) · Antioxidants · doi:10.3390/antiox10020313 · Cited by 633 · see citing works
Evolution of nadph oxidase inhibitors: Selectivity and mechanisms for target engagement
Altenhöfer, S., Radermacher, K. A., Kleikers, P. W. M., Wingler, K., & Schmidt, H. H. H. W. (2015) · Antioxidants & Redox Signaling · doi:10.1089/ars.2013.5814 · Cited by 521 · see citing works
Nox enzymes and new thinking on reactive oxygen: A double-edged sword revisited
Lambeth, J. D., & Neish, A. S. (2014) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathol-012513-104651 · Cited by 495 · see citing works
Kleinschnitz, C., Grund, H., Wingler, K., Armitage, M. E., Jones, E., Mittal, M., Barit, D., Schwarz, T., Geis, C., Kraft, P., et al. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000479 · Cited by 447 · see citing works
NADPH oxidase in brain injury and neurodegenerative disorders
Ma, M. W., Wang, J., Zhang, Q., Wang, R., Dhandapani, K. M., Vadlamudi, R. K., & Brann, D. W. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-017-0150-7 · Cited by 432 · see citing works
The NOX toolbox: validating the role of NADPH oxidases in physiology and disease
Altenhöfer, S., Kleikers, P. W. M., Radermacher, K. A., Scheurer, P., Rob Hermans, J. J., Schiffers, P., Ho, H., Wingler, K., & Schmidt, H. H. H. W. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1010-9 · Cited by 371 · see citing works
Redox control of inflammation in macrophages
Brüne, B., Dehne, N., Grossmann, N., Jung, M., Namgaladze, D., Schmid, T., von Knethen, A., & Weigert, A. (2013) · Antioxidants & Redox Signaling · doi:10.1089/ars.2012.4785 · Cited by 377 · 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 · 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
Melatonin: A Pleiotropic Molecule Regulating Inflammation
Radogna, F., Diederich, M., & Ghibelli, L. (2010) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.07.041 · Cited by 342 · see citing works
The antioxidant paradox: less paradoxical now?
Halliwell, B. (2013) · British Journal of Clinical Pharmacology · doi:10.1111/j.1365-2125.2012.04272.x · Cited by 318 · see citing works
Redox regulation of protein kinases
Corcoran, A., & Cotter, T. G. (2013) · The FEBS Journal · doi:10.1111/febs.12224 · Cited by 306 · see citing works
Yang, C.-T., Cambier, C. J., Davis, J. M., Hall, C. J., Crosier, P. S., & Ramakrishnan, L. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.07.009 · Cited by 293 · see citing works
Redox regulation of cell migration and adhesion
Hurd, T. R., DeGennaro, M., & Lehmann, R. (2012) · Trends in Cell Biology · doi:10.1016/j.tcb.2011.11.002 · Cited by 263 · see citing works
Noninvasive Molecular Imaging of Neuroinflammation
Jacobs, A. H., Tavitian, B., & the INMiND consortium (2012) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2012.53 · Cited by 245 · see citing works
Comparative pharmacology of chemically distinct nadph oxidase inhibitors
Wind, S., Beuerlein, K., Eucker, T., Müller, H., Scheurer, P., Armitage, M., Ho, H., Schmidt, H., & Wingler, K. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00920.x · Cited by 241 · see citing works
Ulfig, A., & Leichert, L. I. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03591-y · Cited by 239 · see citing works
Changes in Regenerative Capacity through Lifespan
Yun, M. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161025392 · Cited by 216 · see citing works
Ramachandran, R., Zhao, X.-F., & Goldman, D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1107220108 · Cited by 206 · see citing works
TNF signaling and macrophages govern fin regeneration in zebrafish larvae
Nguyen-Chi, M., Laplace-Builhé, B., Travnickova, J., Luz-Crawford, P., Tejedor, G., Lutfalla, G., Kissa, K., Jorgensen, C., & Djouad, F. (2017) · Cell Death & Disease · doi:10.1038/cddis.2017.374 · Cited by 190 · see citing works
Ogrodnik, M., Salmonowicz, H., & Gladyshev, V. N. (2019) · Aging Cell · doi:10.1111/acel.12841 · Cited by 184 · see citing works
Haslund‐Vinding, J., McBean, G., Jaquet, V, & Vilhardt, F. (2017) · British Journal of Pharmacology · doi:10.1111/bph.13425 · Cited by 169 · see citing works
Receptor Activation of NADPH Oxidases
Petry, A., Weitnauer, M., & Görlach, A. (2010) · Antioxidants & Redox Signaling · doi:10.1089/ars.2009.3026 · Cited by 162 · see citing works
Hydrogen peroxide in inflammation: Messenger, guide, and assassin
Wittmann, C., Chockley, P., Singh, S. K., Pase, L., Lieschke, G. J., & Grabher, C. (2012) · Advances in Hematology · doi:10.1155/2012/541471 · Cited by 143 · see citing works
Self-citationZebrafish 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
Ncf1 polymorphism reveals oxidative regulation of autoimmune chronic inflammation
Holmdahl, R., Sareila, O., Olsson, L. M., Bäckdahl, L., & Wing, K. (2016) · Immunological Reviews · doi:10.1111/imr.12378 · Cited by 131 · see citing works
Hristova, M., Habibovic, A., Veith, C., Janssen-Heininger, Y. M. W., Dixon, A. E., Geiszt, M., & van der Vliet, A. (2016) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2015.10.003 · Cited by 141 · see citing works
Pase, L., Layton, J. E., Wittmann, C., Ellett, F., Nowell, C. J., Reyes-Aldasoro, C. C., Varma, S., Rogers, K. L., Hall, C. J., Keightley, M. C., et al. (2012) · Current Biology · doi:10.1016/j.cub.2012.07.060 · Cited by 118 · see citing works
Self-citationNox1, 2, 4, 5: Counting out oxidative stress
Wingler, K., Hermans, J., Schiffers, P., Moens, A., Paul, M., & Schmidt, H. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01249.x · Cited by 113 · see citing works
Characterization of aquaporin-driven hydrogen peroxide transport
Wang, H., Schoebel, S., Schmitz, F., Dong, H., & Hedfalk, K. (2020) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2019.183065 · Cited by 107 · see citing works
A tissue injury sensing and repair pathway distinct from host pathogen defense
Liu, S., Hur, Y. H., Cai, X., Cong, Q., Yang, Y., Xu, C., Bilate, A. M., Gonzales, K. A. U., Parigi, S. M., Cowley, C. J., et al. (2023) · Cell · doi:10.1016/j.cell.2023.03.031 · Cited by 108 · see citing works
Wiemann, P., Perevitsky, A., Lim, F. Y., Shadkchan, Y., Knox, B. P., Landero Figueora, J. A., Choera, T., Niu, M., Steinberger, A. J., Wüthrich, M., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.04.019 · Cited by 104 · see citing works
Antimicrobial actions of dual oxidases and lactoperoxidase
Sarr, D., Tóth, E., Gingerich, A., & Rada, B. (2018) · Journal of Microbiology · doi:10.1007/s12275-018-7545-1 · Cited by 98 · see citing works
The Quest for Selective Nox Inhibitors and Therapeutics: Challenges, Triumphs and Pitfalls
Cifuentes-Pagano, E., Meijles, D. N., & Pagano, P. J. (2014) · Antioxidants & Redox Signaling · doi:10.1089/ars.2013.5620 · Cited by 84 · see citing works
Sun, Q.-A., Hess, D. T., Wang, B., Miyagi, M., & Stamler, J. S. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.02.046 · Cited by 76 · see citing works
Srinivasan, N., Gordon, O., Ahrens, S., Franz, A., Deddouche, S., Chakravarty, P., Phillips, D., Yunus, A. A., Rosen, M. K., Valente, R. S., et al. (2016) · eLife · doi:10.7554/elife.19662 · Cited by 69 · see citing works
ROS-Activated Ratiometric Fluorescent Polymeric Nanoparticles for Self-Reporting Drug Delivery
Zhang, M., Song, C.-C., Su, S., Du, F.-S., & Li, Z.-C. (2018) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.7b18438 · Cited by 64 · see citing works
Abuaita, B. H., Burkholder, K. M., Boles, B. R., & O’Riordan, M. X. (2015) · mBio · doi:10.1128/mbio.00705-15 · Cited by 48 · see citing works
Bernardy, C. C. F., Zarpelon, A. C., Pinho-Ribeiro, F. A., Calixto-Campos, C., Carvalho, T. T., Fattori, V., Borghi, S. M., Casagrande, R., & Verri, W. A. (2017) · BioMed Research International · doi:10.1155/2017/9584819 · Cited by 40 · see citing works
Liepe, J., Taylor, H., Barnes, C. P., Huvet, M., Bugeon, L., Thorne, T., Lamb, J. R., Dallman, M. J., & Stumpf, M. P. H. (2012) · Integrative Biology · doi:10.1039/c2ib00175f · Cited by 33 · see citing works
The p-rpS6-zone delineates wounding responses and the healing process
Ring, N. A. R., Dworak, H., Bachmann, B., Schädl, B., Valdivieso, K., Rozmaric, T., Heimel, P., Fischer, I., Klinaki, E., Gutasi, A., et al. (2023) · Developmental Cell · doi:10.1016/j.devcel.2023.04.001 · Cited by 31 · see citing works
Cell resilience in species life spans: a link to inflammation?
Finch, C. E., Morgan, T. E., Longo, V. D., & De Magalhaes, J. P. (2010) · Aging Cell · doi:10.1111/j.1474-9726.2010.00578.x · Cited by 29 · see citing works
T cell tyrosine phosphorylation response to transient redox stress
Secchi, C., Carta, M., Crescio, C., Spano, A., Arras, M., Caocci, G., Galimi, F., La Nasa, G., Pippia, P., Turrini, F., et al. (2015) · Cellular Signalling · doi:10.1016/j.cellsig.2014.12.014 · Cited by 10 · see citing works
- Authors
- Niethammer, P., Grabher, C., Look, A. T., & Mitchison, T. J.
- Affiliations
- Harvard University (US)
- Karlsruhe Institute of Technology (DE)
- Corresponding author
- Niethammer, Philipp
- Venue
- Nature
- Published
- 2009-06
- Volume
- 459
- Issue
- 7249
- Pages
- 996-999
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2803098
- OpenAlex
- W2069463594
- Cited by
- 1,541
- References
- 32
- Citations by year
- 2026: 65 · 2025: 69 · 2024: 68 · 2023: 83 · 2022: 95 · 2021: 101 · 2020: 118 · 2019: 94 · 2018: 85 · 2017: 100 · 2016: 99 · 2015: 88 · 2014: 111 · 2013: 107 · 2012: 84
- FWCI
- 38.02
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institute of General Medical Sciences (GM-023928, R01GM023928)
- 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 › Redox biology and oxidative stress
- Keywords
- hydrogen peroxide, wound detection, dual oxidase, leukocyte recruitment, wound healing, inflammation, reactive oxygen species, zebrafish larvae, epithelium, barrier integrity
- MeSH terms
- Animals, Diffusion, Hydrogen Peroxide, Larva, Leukocytes, Wound Healing, Wounds and Injuries, Zebrafish, NADPH Oxidases, Zebrafish Proteins
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
