Wound healing recapitulates morphogenesis in Drosophila embryos
Abstract
The capacity to repair a wound is a fundamental survival mechanism that is activated at any site of damage throughout embryonic and adult life. To study the cell biology and genetics of this process, we have developed a wounding model in Drosophila melanogaster embryos that allows live imaging of rearrangements and changes in cell shape, and of the cytoskeletal machinery that draws closed an in vivo wound. Using embryos expressing green fluorescent protein (GFP) fusion proteins, we show that two cytoskeletal-dependent elements -- an actin cable and dynamic filopodial/lamellipodial protrusions -- are expressed by epithelial cells at the wound edge and are pivotal for repair. Modulating the activities of the small GTPases Rho and Cdc42 demonstrates that these actin-dependent elements have differing cellular functions, but that either alone can drive wound closure. The actin cable operates as a 'purse-string' to draw the hole closed, whereas filopodia are essential for the final 'knitting' together of epithelial cells at the end of repair. Our data suggest a more complex model for epithelial repair than previously envisaged and highlight remarkable similarities with the well-characterized morphogenetic movement of dorsal closure in Drosophila.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Fly epidermis live imaging reveals dynamic cytoskeletal machineries, including lamellipodial and filopodial protrusions, that enable bonding of epidermal wound edges at the end of healing.
“Although the advancing wound epidermis is hidden beneath a scab in mouse wounds, the simpler fly epidermis can be live-imaged, revealing dynamic cytoskeletal machineries, including lamellipodial and filopodial protrusions that enable bonding of epidermal wound edges together at the end of the healing process (120).”
From Wound repair and regeneration: Mechanisms, signaling, and translation (2014) · cites this paper as [120]
Cites
Targeted gene expression as a means of altering cell fates and generating dominant phenotypes
Brand, A. H., & Perrimon, N. (1993) · Development · doi:10.1242/dev.118.2.401 · Cited by 9,510 · see citing works
A formaldehyde - glutaraldehyde fixative of high osmolarity for use in electron microscopy
Karnovsky, M. J. (1965) · The Journal of Cell Biology · Cited by 5,882 · see citing works
Wound Healing--Aiming for Perfect Skin Regeneration
Martin, P. B. (1997) · Science · doi:10.1126/science.276.5309.75 · Cited by 4,814 · see citing works
Self-citationRidley, A. J., & Hall, A. (1992) · Cell · doi:10.1016/0092-8674(92)90163-7 · Cited by 4,469 · see citing works
Nobes, C. D., & Hall, A. (1995) · Cell · doi:10.1016/0092-8674(95)90370-4 · Cited by 4,414 · see citing works
The development of Drosophila melanogaster
Ingham, P. W. (1994) · Trends in Genetics · doi:10.1016/0168-9525(90)90017-z · Cited by 3,158 · see citing works
DEVELOPMENT IN DROSOPHILA MELANOGASTER
Li, J.-C. (1927) · Genetics · doi:10.1093/genetics/12.2.198 · Cited by 2,887 · see citing works
Luo, L.-Q., Liao, Y.-J., Jan, L., & Jan, Y. (1994) · Genes & Development · doi:10.1101/gad.8.15.1787 · Cited by 1,036 · see citing works
Multiple Forces Contribute to Cell Sheet Morphogenesis for Dorsal Closure in Drosophila
Kiehart, D. P., Galbraith, C. G., Edwards, K. A., Rickoll, W. L., & Montague, R. A. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.149.2.471 · Cited by 636 · see citing works
Mitotic domains reveal early commitment of cells in Drosophila embryos
Foe, V. E. (1989) · Trends in Genetics · doi:10.1016/0168-9525(89)90120-0 · Cited by 562 · see citing works
The role of RhoA in tissue polarity and Frizzled signalling
Strutt, D. I., Weber, U., & Mlodzik, M. (1997) · Nature · doi:10.1038/387292a0 · Cited by 560 · see citing works
Actin cables and epidermal movement in embryonic wound healing
Martin, P. B., & Lewis, J. (1992) · Nature · doi:10.1038/360179a0 · Cited by 515 · see citing works
Self-citationMitotic domains reveal early commitment of cells in Drosophila embryos
Foe, V. E. (1989) · Development · doi:10.1242/dev.107.1.1 · Cited by 431 · see citing works
Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function.Preprint
Young, P. E., Richman, A. M., Ketchum, A., & Kiehart, D. P. (1993) · Genes & Development · doi:10.1101/gad.7.1.29 · Cited by 427 · see citing works
Mechanisms of epithelial fusion and repair
Jacinto, A., Martínez-Arias, A., & Martin, P. B. (2001) · Nature Cell Biology · doi:10.1038/35074643 · Cited by 399 · see citing works
Self-citationRac function and regulation during Drosophila development
Hakeda‐Suzuki, S., Ng, J., Tzu, J., Dietzl, G., Sun, Y., Harms, M. B., Nardine, T. M., Luo, L., & Dickson, B. J. (2002) · Nature · doi:10.1038/416438a · Cited by 354 · see citing works
Dynamic actin-based epithelial adhesion and cell matching during Drosophila dorsal closure
Jacinto, A., Wood, W., Balayo, T., Turmaine, M., Martínez-Arias, A., & Martin, P. B. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00796-x · Cited by 341 · see citing works
Self-citationA novel cytoskeletal structure involved in purse string wound closure and cell polarity maintenance.
Bement, W. M., Forscher, P., & Mooseker, M. S. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.121.3.565 · Cited by 327 · see citing works
JNK Signaling Pathway Is Required for Efficient Wound Healing in Drosophila
Rämet, M., Lanot, R., Zachary, D., & Manfruelli, P. (2002) · Developmental Biology · doi:10.1006/dbio.2001.0502 · Cited by 313 · see citing works
Dynamic Analysis of Dorsal Closure in Drosophila
Jacinto, A., Woolner, S., & Martin, P. B. (2002) · Developmental Cell · doi:10.1016/s1534-5807(02)00208-3 · Cited by 235 · see citing works
Self-citationBrock, J., Midwinter, K., Lewis, J., & Martin, P. B. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.135.4.1097 · Cited by 232 · see citing works
Self-citationDanjo, Y., & Gipson, I. K. (1998) · Journal of Cell Science · doi:10.1242/jcs.111.22.3323 · Cited by 231 · see citing works
Dynamic Analysis of Actin Cable Function during Drosophila Dorsal Closure
Jacinto, A., Wood, W., Woolner, S., Hiley, C., Turner, L. J., WILSON, C. G., Martínez-Arias, A., & Martin, P. B. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00955-7 · Cited by 201 · see citing works
Self-citationHarden, N. (2002) · Differentiation · doi:10.1046/j.1432-0436.2002.700408.x · Cited by 184 · see citing works
Magie, C. R., Meyer, M. R., Gorsuch, M. S., & Parkhurst, S. M. (1999) · Development · doi:10.1242/dev.126.23.5353 · Cited by 160 · see citing works
Harden, N., Ricos, M. G., Ong, Y. M., Chia, W. N., & Lim, L. (1999) · Journal of Cell Science · doi:10.1242/jcs.112.3.273 · Cited by 129 · see citing works
Genova, J. L., Jong, S., Camp, J. T., & Fehon, R. G. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9671 · Cited by 120 · see citing works
Verkhusha, V. V., Tsukita, S., & Oda, H. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)00124-6 · Cited by 107 · see citing works
DrosophilaRhoA regulates the cytoskeleton and cell-cell adhesion in the developing epidermis
Bloor, J. W., & Kiehart, D. P. (2002) · Development · doi:10.1242/dev.129.13.3173 · Cited by 96 · see citing works
Drosophilamyosin phosphatase and its role in dorsal closure
Mizuno, T., Tsutsui, K., & Nishida, Y. (2002) · Development · doi:10.1242/dev.129.5.1215 · Cited by 94 · see citing works
Oda, H., & Tsukita, S. (1999) · Development, Genes and Evolution · doi:10.1007/s004270050246 · Cited by 72 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Gurtner, G. C., Werner, S., Barrandon, Y., & Longaker, M. T. (2008) · Nature · doi:10.1038/nature07039 · Cited by 6,542 · 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
Self-citationCellular and molecular mechanisms of skin wound healing
Peña, O. A., & Martin, P. (2024) · Nature reviews. Molecular cell biology · doi:10.1038/s41580-024-00715-1 · Cited by 1,637 · see citing works
Self-citationFilopodia: molecular architecture and cellular functions
Mattila, P. K., & Lappalainen, P. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2406 · Cited by 1,699 · see citing works
Cellular and molecular mechanisms of repair in acute and chronic wound healing
Martín, P., & Nunan, R. (2015) · British Journal of Dermatology · doi:10.1111/bjd.13954 · Cited by 1,021 · see citing works
Self-citationCollective migration of an epithelial monolayer in response to a model wound
Poujade, M., Grasland‐Mongrain, E., Hertzog, A., Jouanneau, J., Chavrier, P., Ladoux, B., Buguin, A., & Silberzan, P. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705062104 · Cited by 898 · see citing works
Mechanobiology of collective cell behaviours
Ladoux, B., & Mège, R.-M. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.98 · Cited by 749 · see citing works
Pérez‐Moreno, M., Jamora, C., & Fuchs, E. V. (2003) · Cell · doi:10.1016/s0092-8674(03)00108-9 · Cited by 717 · see citing works
Multicellular Rosette Formation Links Planar Cell Polarity to Tissue Morphogenesis
Blankenship, J. T., Backovic, S. T., Sanny, J., Weitz, O., & Zallen, J. A. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.09.007 · Cited by 693 · see citing works
Myosin II Dynamics Are Regulated by Tension in Intercalating Cells
Fernández‐González, R., Simões, S. D. M., Röper, J.-C., Eaton, S., & Zallen, J. A. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.09.003 · Cited by 644 · see citing works
Mechanisms, mechanics and function of epithelial–mesenchymal transitions in early development
Shook, D. R., & Keller, R. E. (2003) · Mechanisms of Development · doi:10.1016/j.mod.2003.06.005 · Cited by 577 · see citing works
Parallels between tissue repair and embryo morphogenesis
Martin, P. B., & Parkhurst, S. M. (2004) · Development · doi:10.1242/dev.01253 · Cited by 557 · see citing works
Self-citationFilopodia in cell adhesion, 3D migration and cancer cell invasion
Jacquemet, G., Hamidi, H., & Ivaska, J. (2015) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2015.06.007 · Cited by 515 · see citing works
Trepat, X., Chen, Z., & Jacobson, K. (2012) · Comprehensive physiology · doi:10.1002/cphy.c110012 · Cited by 475 · see citing works
Cell distribution of stress fibres in response to the geometry of the adhesive environment
Théry, M., Pépin, A., Dressaire, E., Chen, Y., & Bornens, M. (2006) · Cell Motility and the Cytoskeleton · doi:10.1002/cm.20126 · Cited by 452 · see citing works
Cellular and Genetic Analysis of Wound Healing in Drosophila Larvae
Galko, M. J., & Krasnow, M. A. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020239 · Cited by 423 · see citing works
Wiring through tunneling nanotubes--from electrical signals to organelle transfer
Abounit, S., & Zurzolo, C. (2012) · Journal of Cell Science · doi:10.1242/jcs.083279 · Cited by 386 · see citing works
Coagulation in arthropods: defence, wound closure and healing
Theopold, U., Schmidt, O., Söderhäll, K., & Dushay, M. S. (2004) · Trends in Immunology · doi:10.1016/j.it.2004.03.004 · Cited by 372 · see citing works
Hidalgo-Carcedo, C., Hooper, S., Chaudhry, S. I., Williamson, P., Harrington, K. J., Leitinger, B., & Sahai, E. A. (2010) · Nature Cell Biology · doi:10.1038/ncb2133 · Cited by 363 · see citing works
New insights into Drosophila larval haemocyte functions through genome-wide analysis
Irving, P., Ubeda, J.-M., Doucet, D., Troxler, L., Lagueux, M., Zachary, D., Hoffmann, J. A., Hétru, C., & Meister, M. F. (2005) · Cellular Microbiology · doi:10.1111/j.1462-5822.2004.00462.x · Cited by 360 · see citing works
Interplay of RhoA and mechanical forces in collective cell migration driven by leader cells
Reffay, M., Parrini, M. C., Cochet‐Escartin, O., Ladoux, B., Buguin, A., Coscoy, S., Amblard, F., Camonis, J., & Silberzan, P. (2014) · Nature Cell Biology · doi:10.1038/ncb2917 · Cited by 355 · see citing works
Myosin-X is a molecular motor that functions in filopodia formation
Bohil, A. B., Robertson, B. W., & Cheney, R. E. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602443103 · Cited by 337 · see citing works
Razzell, W., Evans, I. R., Martin, P. B., & Wood, W. (2013) · Current Biology · doi:10.1016/j.cub.2013.01.058 · Cited by 331 · see citing works
Self-citationWang, X., Veruki, M. L., Bukoreshtliev, N. V., Hartveit, E., & Gerdes, H. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1006785107 · Cited by 331 · see citing works
Wound Repair: Toward Understanding and Integration of Single-Cell and Multicellular Wound Responses
Sonnemann, K. J., & Bement, W. M. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-092910-154251 · Cited by 307 · see citing works
Shimizu, Y., Thumkeo, D., Keel, J., Ishizaki, T., Oshima, H., Oshima, M., Noda, Y., Matsumura, F., Taketo, M. M., & Narumiya, S. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200411179 · Cited by 302 · see citing works
Drosophila as a Genetic Model for Hematopoiesis
Banerjee, U. K., Girard, J. R., Goins, L. M., & Spratford, C. M. (2019) · Genetics · doi:10.1534/genetics.118.300223 · Cited by 299 · 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
Self-citationPhagocytosis and comparative innate immunity: learning on the fly
Stuart, L. M., & Ezekowitz, R. A. B. (2008) · Nature reviews. Immunology · doi:10.1038/nri2240 · Cited by 288 · see citing works
Stramer, B., Wood, W., Galko, M. J., Redd, M. J., Jacinto, A., Parkhurst, S. M., & Martin, P. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200405120 · Cited by 285 · see citing works
Self-citationThe role of transcription-independent damage signals in the initiation of epithelial wound healing
Cordeiro, J. V., & Jacinto, A. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3541 · Cited by 271 · see citing works
Self-citationFranke, J. D., Montague, R. A., & Kiehart, D. P. (2005) · Current Biology · doi:10.1016/j.cub.2005.11.064 · Cited by 264 · see citing works
Molecular Bases of Cell-Cell Junctions Stability and DynamicsPreprint
Cavey, M., & Lecuit, T. (2009) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a002998 · Cited by 257 · see citing works
Filopodia: The Fingers That Do the Walking
Gupton, S. L., & Gertler, F. B. (2007) · Science s STKE · doi:10.1126/stke.4002007re5 · Cited by 256 · see citing works
An Epidermal Barrier Wound Repair Pathway in Drosophila Is Mediated by grainy head
Mace, K. A., Pearson, J. C., & McGinnis, W. J. (2005) · Science · doi:10.1126/science.1107573 · Cited by 241 · see citing works
Haensel, D., & Dai, X. (2018) · Developmental Dynamics · doi:10.1002/dvdy.24561 · Cited by 232 · see citing works
Rho-dependent formation of epithelial “leader” cells during wound healing
Omelchenko, T., Vasiliev, J. M., Gelfand, I. M., Feder, H. H., & Bonder, E. M. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1834401100 · Cited by 228 · see citing works
Tissue fluidity promotes epithelial wound healing
Tetley, R. J., Staddon, M. F., Heller, D., Hoppe, A., Banerjee, S., & Mao, Y. (2019) · Nature Physics · doi:10.1038/s41567-019-0618-1 · Cited by 225 · see citing works
Cytonemes as specialized signaling filopodia
Kornberg, T. B., & Roy, S. (2014) · Development · doi:10.1242/dev.086223 · Cited by 216 · see citing works
Regulation of cell motile behavior by crosstalk between cadherin- and integrin-mediated adhesions
Borghi, N., Lowndes, M., Maruthamuthu, V., Gardel, M. L., & Nelson, W. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002662107 · Cited by 212 · see citing works
C. elegans Epidermal Wounding Induces a Mitochondrial ROS Burst that Promotes Wound Repair
Xu, S., & Chisholm, A. D. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.08.002 · Cited by 211 · see citing works
Membrane-induced bundling of actin filaments
Liu, A. P., Richmond, D., Maibaum, L., Pronk, S., Geissler, P. L., & Fletcher, D. A. (2008) · Nature Physics · doi:10.1038/nphys1071 · Cited by 207 · see citing works
Polyploidization and Cell Fusion Contribute to Wound Healing in the Adult Drosophila Epithelium
Losick, V. P., Fox, D. T., & Spradling, A. C. (2013) · Current Biology · doi:10.1016/j.cub.2013.09.029 · Cited by 204 · see citing works
The art of cellular communication: tunneling nanotubes bridge the divide
Gurke, S., Barroso, J. F., & Gerdes, H. (2008) · Histochemistry and Cell Biology · doi:10.1007/s00418-008-0412-0 · Cited by 199 · see citing works
JNK signaling pathway required for wound healing in regenerating Drosophila wing imaginal discs
Bosch, M., Serras, F., Martı́n-Blanco, E., & Baguñà, J. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.01.002 · Cited by 197 · see citing works
Cell death-induced regeneration in wing imaginal discs requires JNK signalling
Bergantiños, C., Corominas, M., & Serras, F. (2010) · Development · doi:10.1242/dev.045559 · Cited by 195 · see citing works
Dynamic analysis of filopodial interactions during the zippering phase of Drosophila dorsal closure
Millard, T. H., & Martin, P. B. (2008) · Development · doi:10.1242/dev.014001 · Cited by 189 · see citing works
Self-citationOscillatory behaviors and hierarchical assembly of contractile structures in intercalating cells
Fernández‐González, R., & Zallen, J. A. (2011) · Physical Biology · doi:10.1088/1478-3975/8/4/045005 · Cited by 182 · see citing works
A Gαq-Ca2+ Signaling Pathway Promotes Actin-Mediated Epidermal Wound Closure in C. elegans
Xu, S., & Chisholm, A. D. (2011) · Current Biology · doi:10.1016/j.cub.2011.10.050 · Cited by 179 · see citing works
Two distinct modes of myosin assembly and dynamics during epithelial wound closure
Tamada, M., Perez, T. D., Nelson, W. J., & Sheetz, M. P. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200609116 · Cited by 179 · see citing works
A common framework for EMT and collective cell migration
Campbell, K., & Casanova, J. (2016) · Development · doi:10.1242/dev.139071 · Cited by 177 · see citing works
The hallmarks of cancer are also the hallmarks of wound healing
MacCarthy-Morrogh, L., & Martin, P. (2020) · Science Signaling · doi:10.1126/scisignal.aay8690 · Cited by 158 · see citing works
Self-citationMiyake, Y., Inoue, N., Nishimura, K., Kinoshita, N., Hosoya, H., & Yonemura, S. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.01.031 · Cited by 172 · see citing works
Lin, L. M., Ricucci, D., Saoud, T. M. A., Sigurðsson, Á., & Kahler, B. (2019) · Australian Endodontic Journal · doi:10.1111/aej.12392 · Cited by 172 · see citing works
Quantitative structural mechanobiology of platelet-driven blood clot contraction
Kim, O. V., Игоревич, Л. Р., Alber, M., & Weisel, J. W. (2017) · Nature Communications · doi:10.1038/s41467-017-00885-x · Cited by 169 · see citing works
Coordinated cell-shape changes control epithelial movement in zebrafish and Drosophila
Köppen, M., Fernández, B. G., Carvalho, L., Jacinto, A., & Heisenberg, C. (2006) · Development · doi:10.1242/dev.02439 · Cited by 156 · see citing works
Self-citationMacrophages and cellular immunity in Drosophila melanogaster
Gold, K. S., & Brückner, K. (2015) · Seminars in Immunology · doi:10.1016/j.smim.2016.03.010 · Cited by 153 · see citing works
Abreu‐Blanco, M. T., Verboon, J. M., Liu, R., Watts, J. J., & Parkhurst, S. M. (2012) · Journal of Cell Science · doi:10.1242/jcs.109066 · Cited by 152 · see citing works
A secreted MMP is required for reepithelialization during wound healing
Stevens, L. J., & Page, A. W. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-09-0745 · Cited by 149 · see citing works
Coordinated waves of actomyosin flow and apical cell constriction immediately after wounding
Antunes, M., Pereira, T., Cordeiro, J. V., de Almeida, L. N., & Jacinto, A. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201211039 · Cited by 148 · see citing works
Self-citationAbreu‐Blanco, M. T., Verboon, J. M., & Parkhurst, S. M. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201011018 · Cited by 141 · see citing works
FiloQuant reveals increased filopodia density during breast cancer progression
Jacquemet, G., Paatero, I., Carisey, A. F., Padzik, A., Orange, J. S., Hamidi, H., & Ivaska, J. (2017) · The Journal of Cell Biology · doi:10.1083/jcb.201704045 · Cited by 141 · see citing works
Mechanical state transitions in the regulation of tissue form and function
Mao, Y., & Wickström, S. A. (2024) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-024-00719-x · Cited by 138 · see citing works
Wound healing and inflammation genes revealed by array analysis of 'macrophageless' PU.1 null mice
Cooper, L., Johnson, C. M., Burslem, F., & Martin, P. B. (2004) · Genome biology · doi:10.1186/gb-2004-6-1-r5 · Cited by 135 · see citing works
Self-citationLong-distance electrical coupling via tunneling nanotubes
Wang, X., & Gerdes, H. (2011) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2011.09.002 · Cited by 135 · see citing works
Rho GTPase activity zones and transient contractile arrays
Bement, W. M., Miller, A. L., & von Dassow, G. (2006) · BioEssays · doi:10.1002/bies.20477 · Cited by 134 · see citing works
Wounding Induces Motility in Sheets of Corneal Epithelial Cells through Loss of Spatial Constraints
Block, E. R., Matela, A. R., SundarRaj, N., Iszkula, E. R., & Klarlund, J. K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m401058200 · Cited by 132 · see citing works
Mechanics of epithelial tissues during gap closure
Begnaud, S., Chen, T., Delacour, D., Mège, R., & Ladoux, B. (2016) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2016.04.006 · Cited by 130 · see citing works
Cytoskeleton responses in wound repair
Abreu‐Blanco, M. T., Watts, J. J., Verboon, J. M., & Parkhurst, S. M. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-0928-2 · Cited by 129 · see citing works
The functions of insulin signaling: size isn't everything, even in Drosophila
Goberdhan, D. C. I., & WILSON, C. G. (2003) · Differentiation · doi:10.1046/j.1432-0436.2003.7107001.x · Cited by 128 · see citing works
Self-citationDamage signals in the insect immune response
Krautz, R., Arefin, B., & Theopold, U. (2014) · Frontiers in Plant Science · doi:10.3389/fpls.2014.00342 · Cited by 126 · see citing works
Integration of Single and Multicellular Wound Responses
Clark, A. G., Miller, A. L., Vaughan, E. M., Yu, H.-Y. E., Penkert, R. R., & Bement, W. M. (2009) · Current Biology · doi:10.1016/j.cub.2009.06.044 · Cited by 125 · see citing works
Cellular forces and matrix assembly coordinate fibrous tissue repair
Sakar, M. S., Eyckmans, J., Pieters, R., Eberli, D., Nelson, B. J., & Chen, C. S. (2016) · Nature Communications · doi:10.1038/ncomms11036 · Cited by 123 · see citing works
Wahedi, H. M., Jeong, M., Chae, J. K., Do, S. G., Yoon, H., & Kim, S. Y. (2017) · Phytomedicine · doi:10.1016/j.phymed.2017.02.005 · Cited by 122 · see citing works
Russo, J. M., Florian, P., Shen, L., Graham, W. V., Tretiakova, M., Gitter, A. H., Mrsny, R. J., & Turner, J. R. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.01.004 · Cited by 122 · see citing works
Border Forces and Friction Control Epithelial Closure Dynamics
Cochet‐Escartin, O., Ranft, J., Silberzan, P., & Marcq, P. (2014) · Biophysical Journal · doi:10.1016/j.bpj.2013.11.015 · Cited by 119 · see citing works
Decrease in Cell Volume Generates Contractile Forces Driving Dorsal Closure
Saïas, L., Swoger, J., D’Angelo, A., Hayes, P., Colombelli, J., Sharpe, J. A., Salbreux, G., & Solon, J. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.03.016 · Cited by 118 · see citing works
Live imaging of Drosophila imaginal disc development
Aldaz, S., Escudero, L. M., & Freeman, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1008623107 · Cited by 118 · see citing works
Filopodome Mapping Identifies p130Cas as a Mechanosensitive Regulator of Filopodia Stability
Jacquemet, G., Stubb, A., Saup, R., Miihkinen, M., Kremneva, E., Hamidi, H., & Ivaska, J. (2019) · Current Biology · doi:10.1016/j.cub.2018.11.053 · Cited by 117 · see citing works
Epithelial Cell Packing Induces Distinct Modes of Cell Extrusions
Kocgozlu, L., Saw, T. B., Le, A. P., Yow, I., Shagirov, M., Wong, E., Mège, R., Lim, C. T., Toyama, Y., & Ladoux, B. (2016) · Current Biology · doi:10.1016/j.cub.2016.08.057 · Cited by 113 · see citing works
Dushay, M. S. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-0036-0 · Cited by 110 · see citing works
Cao, R., Chen, J., Zhang, X., Zhai, Y., Qing, X., Xing, W., Zhang, L., Malik, Y. S., Yu, H., & Zhu, X. (2014) · British Journal of Cancer · doi:10.1038/bjc.2014.298 · Cited by 109 · see citing works
Chauhan, B. K., Disanza, A., Choi, S., Faber, S. C., Lou, M., Beggs, H. E., Scita, G., Zheng, Y., & Lang, R. A. (2009) · Development · doi:10.1242/dev.042242 · Cited by 101 · see citing works
Johnson, H. E., King, S. J., Asokan, S. B., Rotty, J. D., Bear, J. E., & Haugh, J. M. (2015) · The Journal of Cell Biology · doi:10.1083/jcb.201406102 · Cited by 100 · see citing works
Mattila, J., Omelyanchuk, L. V., Kyttala, S., Turunen, H., & Nokkala, S. (2005) · The International Journal of Developmental Biology · doi:10.1387/ijdb.052006jm · Cited by 100 · see citing works
Large-scale curvature sensing by directional actin flow drives cellular migration mode switching
Chen, T., Callan-Jones, A., Fedorov, E. G., Ravasio, A., Brugués, A., Ong, H. T., Toyama, Y., Low, B. C., Trepat, X., Shemesh, T., et al. (2019) · Nature Physics · doi:10.1038/s41567-018-0383-6 · Cited by 99 · see citing works
Drosophila as a model of wound healing and tissue regeneration in vertebrates
Belacortu, Y., & Paricio, N. (2011) · Developmental Dynamics · doi:10.1002/dvdy.22753 · Cited by 98 · see citing works
Schwayer, C., Sikora, M., Slováková, J., Kardos, R., & Heisenberg, C. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.05.024 · Cited by 95 · see citing works
Cell Sheet Morphogenesis: Dorsal Closure in Drosophila melanogaster as a Model System
Kiehart, D. P., Crawford, J. M., Aristotelous, A. C., Venakides, S., & Edwards, G. S. (2017) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-111315-125357 · Cited by 95 · see citing works
The Stochastic Dynamics of Filopodial Growth
Lan, Y., & Papoian, G. A. (2008) · Biophysical Journal · doi:10.1529/biophysj.107.123778 · Cited by 95 · see citing works
Drosophila as a model for the two myeloid blood cell systems in vertebrates
Gold, K. S., & Brückner, K. (2014) · Experimental Hematology · doi:10.1016/j.exphem.2014.06.002 · Cited by 94 · see citing works
Supracellular migration – beyond collective cell migration
Shellard, A., & Mayor, R. (2019) · Journal of Cell Science · doi:10.1242/jcs.226142 · Cited by 93 · see citing works
Swatting flies: modelling wound healing and inflammation in <i>Drosophila</i>
Razzell, W., Wood, W., & Martin, P. (2011) · Disease Models & Mechanisms · doi:10.1242/dmm.006825 · Cited by 92 · see citing works
Self-citationUpregulation of Forces and Morphogenic Asymmetries in Dorsal Closure during Drosophila Development
Peralta, X. G., Toyama, Y., Hutson, M. S., Montague, R. A., Venakides, S., Kiehart, D. P., & Edwards, G. S. (2007) · Biophysical Journal · doi:10.1529/biophysj.106.094110 · Cited by 92 · see citing works
Muliyil, S., & Narasimha, M. (2014) · Developmental Cell · doi:10.1016/j.devcel.2013.12.019 · Cited by 91 · see citing works
Drosophila as a model to study the role of blood cells in inflammation, innate immunity and cancer
Wang, L., Kounatidis, I., & Ligoxygakis, P. (2014) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00113 · Cited by 90 · see citing works
Computational models for mechanics of morphogenesis
Wyczalkowski, M. A., Chen, Z., Filas, B. A., Varner, V. D., & Taber, L. A. (2012) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.21013 · Cited by 90 · see citing works
Regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation
Jain, A., Ulman, V., Mukherjee, A., Prakash, M., Cuenca, M. B., Pimpale, L. G., Münster, S., Haase, R., Panfilio, K. A., Jug, F., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19356-x · Cited by 88 · see citing works
Lesch, C., Jo, J.-Y., Wu, Y., Fish, G. S., & Galko, M. J. (2010) · Genetics · doi:10.1534/genetics.110.121822 · Cited by 88 · see citing works
Genetic control of epidermis differentiation in Drosophila.
Payre, F. (2004) · The International Journal of Developmental Biology · doi:10.1387/ijdb.15272387 · Cited by 88 · see citing works
- Authors
- Wood, W., Jacinto, A., Grose, R., Woolner, S., Gale, J., Wilson, C., & Martin, P.
- Affiliations
- University College London (GB)
- University of Oxford (GB)
- Corresponding author
- Martin, Paul
- Venue
- Nature Cell Biology
- Published
- 2002-10-28
- Volume
- 4
- Issue
- 11
- Pages
- 907-912
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- OpenAlex
- W2073006837
- Cited by
- 435
- References
- 31
- Citations by year
- 2026: 11 · 2025: 14 · 2024: 17 · 2023: 23 · 2022: 18 · 2021: 20 · 2020: 17 · 2019: 24 · 2018: 12 · 2017: 17 · 2016: 25 · 2015: 23 · 2014: 28 · 2013: 22 · 2012: 21
- FWCI
- 16.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Bristol Research (University of Bristol) (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- Topics
- Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Keywords
- wound healing, epithelial repair, Drosophila embryo, actin cables, filopodia, lamellipodia, Rho GTPases, Cdc42, cytoskeleton, dorsal closure, morphogenesis, live imaging, cell shape changes
- MeSH terms
- Actins, Animals, Cytoskeleton, Drosophila melanogaster, Embryo, Nonmammalian, Epithelial Cells, Luminescent Proteins, Microscopy, Electron, Morphogenesis, Mutation, Pseudopodia, Recombinant Fusion Proteins, Time Factors, Wound Healing, rho GTP-Binding Proteins, cdc42 GTP-Binding Protein, Green Fluorescent 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
