C.elegans epidermal wounding induces a mitochondrial ROS burst that promotes wound repair

Developmental Cell

Volumn 31, Issue 1, 2014, Pages 48-60

  Xu, Suhong ^a   Chisholm, Andrew D ^a  

^a SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CALCIUM; CYCLOSPORIN A; ENHANCED GREEN FLUORESCENT PROTEIN; F ACTIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MYOSIN; REACTIVE OXYGEN METABOLITE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TERT BUTYL HYDROPEROXIDE; YELLOW FLUORESCENT PROTEIN; ANTIOXIDANT; CAENORHABDITIS ELEGANS PROTEIN; CARRIER PROTEIN; MCU-1 PROTEIN, C ELEGANS; RHO-1 PROTEIN, C ELEGANS;

ARTICLE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS SKIN WOUND; CELL PROTECTION; CONTROLLED STUDY; CYTOSOL; DISULFIDE BOND; ENZYME INHIBITION; EPIDERMIS; FLUORESCENCE; INNATE IMMUNITY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NONHUMAN; PHAGOCYTE; RNA INTERFERENCE; SKIN INJURY; WOUND CLOSURE; WOUND HEALING; ANIMAL; DRUG EFFECTS; GENETICS; METABOLISM; PHYSIOLOGY;

ACTINS; ANIMALS; ANTIOXIDANTS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM; EPIDERMIS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; REACTIVE OXYGEN SPECIES; RHO GTP-BINDING PROTEINS; WOUND HEALING;

EID: 84907980823     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.08.002     Document Type: Article

References (84)

1. Babior B.M. Oxygen-dependent microbial killing by phagocytes (first of two parts). N.Engl. J. Med. 1978, 298:659-668.
2. Balaban R.S., Nemoto S., Finkel T. Mitochondria, oxidants, and aging. Cell 2005, 120:483-495.
3. Baughman J.M., Perocchi F., Girgis H.S., Plovanich M., Belcher-Timme C.A., Sancak Y., Bao X.R., Strittmatter L., Goldberger O., Bogorad R.L., et al. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 2011, 476:341-345.
4. Belousov V.V., Fradkov A.F., Lukyanov K.A., Staroverov D.B., Shakhbazov K.S., Terskikh A.V., Lukyanov S. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods 2006, 3:281-286.
5. Bement W.M., Mandato C.A., Kirsch M.N. Wound-induced assembly and closure of an actomyosin purse string in Xenopus oocytes. Curr. Biol. 1999, 9:579-587.
6. Benink H.A., Bement W.M. Concentric zones of active RhoA and Cdc42 around single cell wounds. J.Cell Biol. 2005, 168:429-439.
7. Bernardi P. The permeability transition pore. Control points of a cyclosporin A-sensitive mitochondrial channel involved in cell death. Biochim. Biophys. Acta 1996, 1275:5-9.
8. Broekemeier K.M., Dempsey M.E., Pfeiffer D.R. Cyclosporin A is a potent inhibitor of the inner membrane permeability transition in liver mitochondria. J.Biol. Chem. 1989, 264:7826-7830.
9. Brookes P.S., Yoon Y., Robotham J.L., Anders M.W., Sheu S.S. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am. J. Physiol. Cell Physiol. 2004, 287:C817-C833.
10. Burridge K., Wennerberg K. Rho and Rac take center stage. Cell 2004, 116:167-179.
11. Bus J.S., Gibson J.E. Paraquat: model for oxidant-initiated toxicity. Environ. Health Perspect. 1984, 55:37-46.
12. Chandel N.S., Maltepe E., Goldwasser E., Mathieu C.E., Simon M.C., Schumacker P.T. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. USA 1998, 95:11715-11720.
13. Chávez V., Mohri-Shiomi A., Garsin D.A. Ce-Duox1/BLI-3 generates reactive oxygen species as a protective innate immune mechanism in Caenorhabditis elegans. Infect. Immun. 2009, 77:4983-4989.
14. Chen Q., Vazquez E.J., Moghaddas S., Hoppel C.L., Lesnefsky E.J. Production of reactive oxygen species by mitochondria: central role of complex III. J.Biol. Chem. 2003, 278:36027-36031.
15. Chisholm A.D., Hsiao T.I. The Caenorhabditis elegans epidermis as a model skin. I: development, patterning, and growth. Wiley Interdiscip. Rev. Dev. Biol. 2012, 1:861-878.
16. Clark A.G., Miller A.L., Vaughan E., Yu H.Y., Penkert R., Bement W.M. Integration of single and multicellular wound responses. Curr. Biol. 2009, 19:1389-1395.
17. Cordeiro J.V., Jacinto A. The role of transcription-independent damage signals in the initiation of epithelial wound healing. Nat. Rev. Mol. Cell Biol. 2013, 14:249-262.
18. De Stefani D., Raffaello A., Teardo E., Szabò I., Rizzuto R. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 2011, 476:336-340.
19. Dickinson B.C., Chang C.J. Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat. Chem. Biol. 2011, 7:504-511.
20. Doonan R., McElwee J.J., Matthijssens F., Walker G.A., Houthoofd K., Back P., Matscheski A., Vanfleteren J.R., Gems D. Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span in Caenorhabditis elegans. Genes Dev. 2008, 22:3236-3241.
21. Friedland A.E., Tzur Y.B., Esvelt K.M., Colaiácovo M.P., Church G.M., Calarco J.A. Heritable genome editing in C.elegans via a CRISPR-Cas9 system. Nat. Methods 2013, 10:741-743.
22. Frøkjaer-Jensen C., Davis M.W., Hopkins C.E., Newman B.J., Thummel J.M., Olesen S.P., Grunnet M., Jorgensen E.M. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 2008, 40:1375-1383.
23. Frøkjær-Jensen C., Davis M.W., Ailion M., Jorgensen E.M. Improved Mos1-mediated transgenesis in C.elegans. Nat. Methods 2012, 9:117-118.
24. Galko M.J., Krasnow M.A. Cellular and genetic analysis of wound healing in Drosophila larvae. PLoS Biol. 2004, 2:E239.
25. Gibson D.G., Young L., Chuang R.Y., Venter J.C., Hutchison C.A., Smith H.O. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 2009, 6:343-345.
26. Gurtner G.C., Werner S., Barrandon Y., Longaker M.T. Wound repair and regeneration. Nature 2008, 453:314-321.
27. Hekimi S., Lapointe J., Wen Y. Taking a "good" look at free radicals in the aging process. Trends Cell Biol. 2011, 21:569-576.
28. Heo J., Campbell S.L. Mechanism of redox-mediated guanine nucleotide exchange on redox-active Rho GTPases. J.Biol. Chem. 2005, 280:31003-31010.
29. Heo J., Raines K.W., Mocanu V., Campbell S.L. Redox regulation of RhoA. Biochemistry 2006, 45:14481-14489.
30. Honda Y., Tanaka M., Honda S. Modulation of longevity and diapause by redox regulation mechanisms under the insulin-like signaling control in Caenorhabditis elegans. Exp. Gerontol. 2008, 43:520-529.
31. Hou Y., Ouyang X., Wan R., Cheng H., Mattson M.P., Cheng A. Mitochondrial superoxide production negatively regulates neural progenitor proliferation and cerebral cortical development. Stem Cells 2012, 30:2535-2547.
32. Huang Z., Zhang W., Fang H., Zheng M., Wang X., Xu J., Cheng H., Gong G., Wang W., Dirksen R.T., Sheu S.S. Response to "A critical evaluation of cpYFP as a probe for superoxide". Free Radic. Biol. Med. 2011, 51:1937-1940.
33. Johnson D., Nehrke K. Mitochondrial fragmentation leads tointracellular acidification in Caenorhabditis elegans and mammalian cells. Mol. Biol. Cell 2010, 21:2191-2201.
34. Lambeth J.D. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 2004, 4:181-189.
35. Lambeth J.D., Neish A.S. Nox enzymes and new thinking on reactive oxygen: a double-edged sword revisited. Annu. Rev. Pathol. 2014, 9:119-145.
36. Lansdown A.B. Calcium: a potential central regulator in wound healing in the skin. Wound Repair Regen. 2002, 10:271-285.
37. Lee S.J., Hwang A.B., Kenyon C. Inhibition of respiration extends C.elegans life span via reactive oxygen species that increase HIF-1 activity. Curr. Biol. 2010, 20:2131-2136.
38. Love N.R., Chen Y., Ishibashi S., Kritsiligkou P., Lea R., Koh Y., Gallop J.L., Dorey K., Amaya E. Amputation-induced reactive oxygen species are required for successful Xenopus tadpole tail regeneration. Nat. Cell Biol. 2013, 15:222-228.
39. Mace K.A., Pearson J.C., McGinnis W. An epidermal barrier wound repair pathway in Drosophila is mediated by grainy head. Science 2005, 308:381-385.
40. 2 with expanded dynamic range. Bioorg. Med. Chem. 2011, 19:1079-1084.
41. Martin P. Wound healing-aiming for perfect skin regeneration. Science 1997, 276:75-81.
42. Melov S., Ravenscroft J., Malik S., Gill M.S., Walker D.W., Clayton P.E., Wallace D.C., Malfroy B., Doctrow S.R., Lithgow G.J. Extension of life-span with superoxide dismutase/catalase mimetics. Science 2000, 289:1567-1569.
43. Miki H., Funato Y. Regulation of intracellular signalling through cysteine oxidation by reactive oxygen species. J.Biochem. 2012, 151:255-261.
44. Mitchell L., Hobbs G.A., Aghajanian A., Campbell S.L. Redox regulation of Ras and Rho GTPases: mechanism and function. Antioxid. Redox Signal. 2013, 18:250-258.
45. Muliyil S., Narasimha M. Mitochondrial ROS regulates cytoskeletal and mitochondrial remodeling to tune cell and tissue dynamics in a model for wound healing. Dev. Cell 2014, 28:239-252.
46. Murawala P., Tanaka E.M., Currie J.D. Regeneration: the ultimate example of wound healing. Semin. Cell Dev. Biol. 2012, 23:954-962.
47. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
48. Niethammer P., Grabher C., Look A.T., Mitchison T.J. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 2009, 459:996-999.
49. Nimnual A.S., Taylor L.J., Bar-Sagi D. Redox-dependent downregulation of Rho by Rac. Nat. Cell Biol. 2003, 5:236-241.
50. Pujol N., Cypowyj S., Ziegler K., Millet A., Astrain A., Goncharov A., Jin Y., Chisholm A.D., Ewbank J.J. Distinct innate immune responses to infection and wounding in the C.elegans epidermis. Curr. Biol. 2008, 18:481-489.
51. 2+)-dependent apoptosis and necrosis. Cell Calcium 2011, 50:222-233.
52. Razzell W., Evans I.R., Martin P., Wood W. Calcium flashes orchestrate the wound inflammatory response through DUOX activation and hydrogen peroxide release. Curr. Biol. 2013, 23:424-429.
53. Razzell W., Wood W., Martin P. Recapitulation of morphogenetic cell shape changes enables wound re-epithelialisation. Development 2014, 141:1814-1820.
54. Rizzuto R., De Stefani D., Raffaello A., Mammucari C. Mitochondria as sensors and regulators of calcium signalling. Nat. Rev. Mol. Cell Biol. 2012, 13:566-578.
55. Roy S., Khanna S., Nallu K., Hunt T.K., Sen C.K. Dermal wound healing is subject to redox control. Mol. Ther. 2006, 13:211-220.
56. Schebesta M., Lien C.L., Engel F.B., Keating M.T. Transcriptional profiling of caudal fin regeneration in zebrafish. ScientificWorldJournal 2006, 6(Suppl1):38-54.
57. Schwarzländer M., Murphy M.P., Duchen M.R., Logan D.C., Fricker M.D., Halestrap A.P., Müller F.L., Rizzuto R., Dick T.P., Meyer A.J., Sweetlove L.J. Mitochondrial 'flashes': a radical concept repHined. Trends Cell Biol. 2012, 22:503-508.
58. Sen C.K. Wound healing essentials: let there be oxygen. Wound Repair Regen. 2009, 17:1-18.
59. Senoo-Matsuda N., Yasuda K., Tsuda M., Ohkubo T., Yoshimura S., Nakazawa H., Hartman P.S., Ishii N. A defect in the cytochrome b large subunit in complex II causes both superoxide anion overproduction and abnormal energy metabolism in Caenorhabditis elegans. J.Biol. Chem. 2001, 276:41553-41558.
60. Shen E.Z., Song C.Q., Lin Y., Zhang W.H., Su P.F., Liu W.Y., Zhang P., Xu J., Lin N., Zhan C., et al. Mitoflash frequency in early adulthood predicts lifespan in Caenorhabditis elegans. Nature 2014, 508:128-132.
61. Shyh-Chang N., Zhu H., Yvanka de Soysa T., Shinoda G., Seligson M.T., Tsanov K.M., Nguyen L., Asara J.M., Cantley L.C., Daley G.Q. Lin28 enhances tissue repair by reprogramming cellular metabolism. Cell 2013, 155:778-792.
62. Singer A.J., Clark R.A. Cutaneous wound healing. N.Engl. J. Med. 1999, 341:738-746.
63. Sipos P., Gyõry H., Hagymási K., Ondrejka P., Blázovics A. Special wound healing methods used in ancient egypt and the mythological background. World J. Surg. 2004, 28:211-216.
64. Sonnemann K.J., Bement W.M. Wound repair: toward understanding and integration of single-cell and multicellular wound responses. Annu. Rev. Cell Dev. Biol. 2011, 27:237-263.
65. Suzuki N., Mittler R. Reactive oxygen species-dependent wound responses in animals and plants. Free Radic. Biol. Med. 2012, 53:2269-2276.
66. Thom S.R. Oxidative stress is fundamental to hyperbaric oxygen therapy. J Appl. Physiol. (1985) 2009, 106:988-995.
67. Ting S.B., Caddy J., Hislop N., Wilanowski T., Auden A., Zhao L.L., Ellis S., Kaur P., Uchida Y., Holleran W.M., et al. A homolog of Drosophila grainy head is essential for epidermal integrity in mice. Science 2005, 308:411-413.
68. Tran P.O., Hinman L.E., Unger G.M., Sammak P.J. A wound-induced 'i increase and its transcriptional activation of immediate early genes is important in the regulation of motility. Exp. Cell Res. 1999, 246:319-326.
69. Tullet J.M., Hertweck M., An J.H., Baker J., Hwang J.Y., Liu S., Oliveira R.P., Baumeister R., Blackwell T.K. Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C.elegans. Cell 2008, 132:1025-1038.
70. van der Vliet A., Janssen-Heininger Y.M. Hydrogen peroxide as adamage signal in tissue injury and inflammation: murderer, mediator, or messenger?. J.Cell. Biochem. 2014, 115:427-435.
71. Van Raamsdonk J.M., Hekimi S. Superoxide dismutase is dispensable for normal animal lifespan. Proc. Natl. Acad. Sci. USA 2012, 109:5785-5790.
72. Ved R., Saha S., Westlund B., Perier C., Burnam L., Sluder A., Hoener M., Rodrigues C.M., Alfonso A., Steer C., et al. Similar patterns of mitochondrial vulnerability and rescue induced by genetic modification of alpha-synuclein, parkin, and DJ-1 in Caenorhabditis elegans. J.Biol. Chem. 2005, 280:42655-42668.
73. Wang W., Fang H., Groom L., Cheng A., Zhang W., Liu J., Wang X., Li K., Han P., Zheng M., et al. Superoxide flashes in single mitochondria. Cell 2008, 134:279-290.
74. Wei-LaPierre L., Gong G., Gerstner B.J., Ducreux S., Yule D.I., Pouvreau S., Wang X., Sheu S.S., Cheng H., Dirksen R.T., Wang W. Respective contribution of mitochondrial superoxide and pH to mitochondria-targeted circularly permuted yellow fluorescent protein (mt-cpYFP) flash activity. J.Biol. Chem. 2013, 288:10567-10577.
75. West A.P., Brodsky I.E., Rahner C., Woo D.K., Erdjument-Bromage H., Tempst P., Walsh M.C., Choi Y., Shadel G.S., Ghosh S. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 2011, 472:476-480.
76. Winterbourn C.C., Kettle A.J. Redox reactions and microbial killing in the neutrophil phagosome. Antioxid. Redox Signal. 2013, 18:642-660.
77. Wood W., Jacinto A., Grose R., Woolner S., Gale J., Wilson C., Martin P. Wound healing recapitulates morphogenesis in Drosophila embryos. Nat. Cell Biol. 2002, 4:907-912.
78. Wu Z., Ghosh-Roy A., Yanik M.F., Zhang J.Z., Jin Y., Chisholm A.D. Caenorhabditis elegans neuronal regeneration is influenced by life stage, ephrin signaling, and synaptic branching. Proc. Natl. Acad. Sci. USA 2007, 104:15132-15137.
79. 2' signaling pathway promotes actin-mediated epidermal wound closure in C. elegans. Curr. Biol. 2011, 21:1960-1967.
80. Yang W., Hekimi S. A mitochondrial superoxide signal triggers increased longevity in Caenorhabditis elegans. PLoS Biol. 2010, 8:e1000556.
81. Yang W., Li J., Hekimi S. A measurable increase in oxidative damage due to reduction in superoxide detoxification fails to shorten the lifespan of long-lived mitochondrial mutants of Caenorhabditis elegans. Genetics 2007, 177:2063-2074.
82. Yoo S.K., Starnes T.W., Deng Q., Huttenlocher A. Lyn is a redox sensor that mediates leukocyte wound attraction invivo. Nature 2011, 480:109-112.
83. Yoo S.K., Freisinger C.M., LeBert D.C., Huttenlocher A. Early redox, Src family kinase, and calcium signaling integrate wound responses and tissue regeneration in zebrafish. J.Cell Biol. 2012, 199:225-234.
84. Zhang Q., Raoof M., Chen Y., Sumi Y., Sursal T., Junger W., Brohi K., Itagaki K., Hauser C.J. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 2010, 464:104-107.