Osmotic surveillance mediates rapid wound closure through nucleotide release

Journal of Cell Biology

Volumn 207, Issue 6, 2014, Pages 767-782

  Gault, William J ^a   Enyedi, Balázs ^a   Niethammer, Philipp ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; NUCLEOSIDE TRIPHOSPHATE;

ADULT; ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; EPITHELIUM BASAL CELL; EPITHELIUM CELL; FLUORESCENCE MICROSCOPY; HYDROLYSIS; IN VITRO STUDY; LARVA; LUMINESCENCE; MUSCLE HYPOTONIA; NONHUMAN; NUCLEOTIDE RELEASE; OSMOTIC PRESSURE; PARTICLE IMAGE VELOCIMETRY; PLASMID; PRIORITY JOURNAL; PROTEIN SECRETION; RAPID EPITHELIAL WOUND CLOSURE; TRANSGENIC ZEBRAFISH; ULTRAVIOLET RADIATION; WOUND CLOSURE; ANIMAL; CELL MOTION; EPIDERMIS; EXTRACELLULAR FLUID; METABOLISM; OSMOREGULATION; PATHOPHYSIOLOGY; PHYSIOLOGY; WOUND HEALING; ZEBRA FISH;

DANIO RERIO;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL MOVEMENT; EPIDERMIS; EPITHELIAL CELLS; EXTRACELLULAR FLUID; HYDROLYSIS; LARVA; OSMOREGULATION; WOUND HEALING; ZEBRAFISH;

EID: 84930439563     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201408049     Document Type: Article

References (44)

1. Abreu-Blanco, M.T., J.M. Verboon, and S.M. Parkhurst. 2011. Cell wound repair in Drosophila occurs through three distinct phases of membrane and cytoskeletal remodeling. J. Cell Biol. 193:455-464. http://dx.doi.org/10.1083/jcb.201011018
2. Beach, J.R., L.S. Licate, J.F. Crish, and T.T. Egelhoff. 2011. Analysis of the role of Ser1/Ser2/Thr9 phosphorylation on myosin II assembly and function in live cells. BMC Cell Biol. 12:52. http://dx.doi.org/10.1186/1471-2121-12-52
3. Beis, I., and E.A. Newsholme. 1975. The contents of adenine nucleotides, phosphagens and some glycolytic intermediates in resting muscles from vertebrates and invertebrates. Biochem. J. 152:23-32.
4. Belousov, V.V., A.F. Fradkov, K.A. Lukyanov, D.B. Staroverov, K.S. Shakhbazov, A.V. Terskikh, and S. Lukyanov. 2006. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods. 3:281-286. http://dx.doi.org/10.1038/nmeth866
5. Bement, W.M., P. Forscher, and M.S. Mooseker. 1993. A novel cytoskeletal structure involved in purse string wound closure and cell polarity maintenance. J. Cell Biol. 121:565-578. http://dx.doi.org/10.1083/jcb.121.3.565
6. Bertrand, J.Y., A.D. Kim, E.P. Violette, D.L. Stachura, J.L. Cisson, and D. Traver. 2007. Definitive hematopoiesis initiates through a committed erythromyeloid progenitor in the zebrafish embryo. Development. 134:4147-4156. http://dx.doi.org/10.1242/dev.012385
7. Block, E.R., and J.K. Klarlund. 2008. Wounding sheets of epithelial cells activates the epidermal growth factor receptor through distinct short- and long-range mechanisms. Mol. Biol. Cell. 19:4909-4917. http://dx.doi.org/10.1091/mbc.E08-01-0097
8. Boucher, I., C. Rich, A. Lee, M. Marcincin, and V. Trinkaus-Randall. 2010. The P2Y2 receptor mediates the epithelial injury response and cell migration. Am. J. Physiol. Cell Physiol. 299:C411-C421. http://dx.doi.org/10.1152/ajpcell.00100.2009
9. Burkel, B.M., G. von Dassow, and W.M. Bement. 2007. Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin. Cell Motil. Cytoskeleton. 64:822-832. http://dx.doi.org/10.1002/cm.20226
10. Choi, J., K. Tanaka, Y. Cao, Y. Qi, J. Qiu, Y. Liang, S.Y. Lee, and G. Stacey. 2014. Identification of a plant receptor for extracellular ATP. Science. 343:290-294. http://dx.doi.org/10.1126/science.343.6168.290
11. Enyedi, B., and P. Niethammer. 2013. H2O2: a chemoattractant? Methods Enzymol. 528:237-255. http://dx.doi.org/10.1016/B978-0-12-405881-1.00014-8
12. Enyedi, B., S. Kala, T. Nikolich-Zugich, and P. Niethammer. 2013. Tissue damage detection by osmotic surveillance. Nat. Cell Biol. 15:1123-1130. http://dx.doi.org/10.1038/ncb2818
13. Fuchigami, T., T. Matsuzaki, and S. Ihara. 2011. Exposure to external environment of low ion concentrations is the trigger for rapid wound closure in Xenopus laevis embryos. Zoolog. Sci. 28:633-641. http://dx.doi.org/10.2108/zsj.28.633
14. Geiger, J.A., L. Carvalho, I. Campos, A.C. Santos, and A. Jacinto. 2011. Holein-one mutant phenotypes link EGFR/ERK signaling to epithelial tissue repair in Drosophila. PLoS ONE. 6:e28349. http://dx.doi.org/10.1371/journal.pone.0028349
15. Goldfarb, A.J. 1907. Factors in the regeneration of a compound hydroid, Eudendrium ramosum. J. Exp. Zool. 4:317-356. http://dx.doi.org/10.1002/jez.1400040302
16. Goldfarb, A.J. 1914. Changes in salinity and their effects upon the regeneration of Cassiopea xamachana. In Papers from the Tortugas laboratory of the Carnegie Instiutiton of Washington. Vol. 6. D. Harold, editor. Carnegie Institution of Washington, Washington, D.C. 83-94.
17. Gong, Z., B. Ju, X. Wang, J. He, H. Wan, P.M. Sudha, and T. Yan. 2002. Green fluorescent protein expression in germ-line transmitted transgenic zebrafish under a stratified epithelial promoter from keratin8. Dev. Dyn. 223:204-215. http://dx.doi.org/10.1002/dvdy.10051
18. Higashijima, S., H. Okamoto, N. Ueno, Y. Hotta, and G. Eguchi. 1997. Highfrequency generation of transgenic zebrafish which reliably express GFP in whole muscles or the whole body by using promoters of zebrafish origin. Dev. Biol. 192:289-299. http://dx.doi.org/10.1006/dbio.1997.8779
19. Hoffmann, E.K., I.H. Lambert, and S.F. Pedersen. 2009. Physiology of cell volume regulation in vertebrates. Physiol. Rev. 89:193-277. http://dx.doi.org/10.1152/physrev.00037.2007
20. Huttenlocher, A., and M.C. Poznansky. 2008. Reverse leukocyte migration can be attractive or repulsive. Trends Cell Biol. 18:298-306. http://dx.doi.org/10.1016/j.tcb.2008.04.001
21. Johnson, R.G., Jr. 1988. Accumulation of biological amines into chromaffin granules: a model for hormone and neurotransmitter transport. Physiol. Rev. 68:232-307.
22. Kwan, K.M., E. Fujimoto, C. Grabher, B.D. Mangum, M.E. Hardy, D.S. Campbell, J.M. Parant, H.J. Yost, J.P. Kanki, and C.-B. Chien. 2007. The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236:3088-3099. http://dx.doi.org/10.1002/dvdy.21343
23. Kwon, Y., T. Hofmann, and C. Montell. 2007. Integration of phosphoinositideand calmodulin-mediated regulation of TRPC6. Mol. Cell. 25:491-503. http://dx.doi.org/10.1016/j.molcel.2007.01.021
24. Lavoie, E.G., B.D. Gulbransen, M. Martín-Satué, E. Aliagas, K.A. Sharkey, and J. Sévigny. 2011. Ectonucleotidases in the digestive system: focus on NTPDase3 localization. Am. J. Physiol. Gastrointest. Liver Physiol. 300:G608-G620. http://dx.doi.org/10.1152/ajpgi.00207.2010
25. Lazarowski, E.R., L. Homolya, R.C. Boucher, and T.K. Harden. 1997. Identification of an ecto-nucleoside diphosphokinase and its contribution to interconversion of P2 receptor agonists. J. Biol. Chem. 272:20402-20407. http://dx.doi.org/10.1074/jbc.272.33.20402
26. Loeb, J. 1891. Organization and growth. Wurtzburg.
27. Martin, P., and J. Lewis. 1992. Actin cables and epidermal movement in embryonic wound healing. Nature. 360:179-183. http://dx.doi.org/10.1038/360179a0
28. Moyer, J.D., and J.F. Henderson. 1983. Nucleoside triphosphate specificity of firefly luciferase. Anal. Biochem. 131:187-189. http://dx.doi.org/10.1016/0003-2697(83)90152-5
29. Müller, C.E., J. Iqbal, Y. Baqi, H. Zimmermann, A. Röllich, and H. Stephan. 2006. Polyoxometalates-a new class of potent ecto-nucleoside triphosphate diphosphohydrolase (NTPDase) inhibitors. Bioorg. Med. Chem. Lett. 16:5943-5947. http://dx.doi.org/10.1016/j.bmcl.2006.09.003
30. Niethammer, P., C. Grabher, A.T. Look, and T.J. Mitchison. 2009. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature. 459:996-999. http://dx.doi.org/10.1038/nature08119
31. Nusslein-Volhard, C., and R. Dahm. 2002. Zebrafish: A Practical Approach. Oxford University Press, Oxford. 322 pp.
32. Orriss, I.R., G.E. Knight, J.C. Utting, S.E.B. Taylor, G. Burnstock, and T.R. Arnett. 2009. Hypoxia stimulates vesicular ATP release from rat osteoblasts. J. Cell. Physiol. 220:155-162. http://dx.doi.org/10.1002/jcp.21745
33. Orriss, I.R., M.L. Key, M.O.R. Hajjawi, and T.R. Arnett. 2013. Extracellular ATP released by osteoblasts is a key local inhibitor of bone mineralisation. PLoS ONE. 8:e69057. http://dx.doi.org/10.1371/journal.pone.0069057
34. Praetorius, H.A., and J. Leipziger. 2009. ATP release from non-excitable cells. Purinergic Signal. 5:433-446. http://dx.doi.org/10.1007/s11302-009-9146-2
35. Radice, G.P. 1980. Locomotion and cell-substratum contacts of Xenopus epidermal cells in vitro and in situ. J. Cell Sci. 44:201-223.
36. Redd, M.J., L. Cooper, W. Wood, B. Stramer, and P. Martin. 2004. Wound healing and inflammation: embryos reveal the way to perfect repair. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359:777-784. http://dx.doi.org/10.1098/rstb.2004.1466
37. Reischauer, S., M.P. Levesque, C. Nüsslein-Volhard, and M. Sonawane. 2009. Lgl2 executes its function as a tumor suppressor by regulating ErbB signaling in the zebrafish epidermis. PLoS Genet. 5:e1000720. http://dx.doi.org/10.1371/journal.pgen.1000720
38. Richardson, R., K. Slanchev, C. Kraus, P. Knyphausen, S. Eming, and M. Hammerschmidt. 2013. Adult zebrafish as a model system for cutaneous wound-healing research. J. Invest. Dermatol. 133:1655-1665. http://dx.doi.org/10.1038/jid.2013.16
39. Rosemberg, D.B., E.P. Rico, A.S. Langoni, J.T. Spinelli, T.C. Pereira, R.D. Dias, D.O. Souza, C.D. Bonan, and M.R. Bogo. 2010. NTPDase family in zebrafish: Nucleotide hydrolysis, molecular identification and gene expression profiles in brain, liver and heart. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 155:230-240. http://dx.doi.org/10.1016/j.cbpb.2009.11.005
40. Schindelin, J., I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, et al. 2012. Fiji: an opensource platform for biological-image analysis. Nat. Methods. 9:676-682. http://dx.doi.org/10.1038/nmeth.2019
41. Sonawane, M., H. Martin-Maischein, H. Schwarz, and C. Nüsslein-Volhard. 2009. Lgl2 and E-cadherin act antagonistically to regulate hemidesmosome formation during epidermal development in zebrafish. Development. 136:1231-1240. http://dx.doi.org/10.1242/dev.032508
42. White, R.M., A. Sessa, C. Burke, T. Bowman, J. LeBlanc, C. Ceol, C. Bourque, M. Dovey, W. Goessling, C.E. Burns, and L.I. Zon. 2008. Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell. 2:183-189. http://dx.doi.org/10.1016/j.stem.2007.11.002
43. Yin, J., K. Xu, J. Zhang, A. Kumar, and F.-S.X. Yu. 2007. Wound-induced ATP release and EGF receptor activation in epithelial cells. J. Cell Sci. 120:815-825. http://dx.doi.org/10.1242/jcs.03389
44. Zimmermann, H., M. Zebisch, and N. Sträter. 2012. Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal. 8:437-502. http://dx.doi.org/10.1007/s11302-012-9309-4