Hydrogen peroxide (H2O2) controls axon pathfinding during zebrafish development

Developmental Biology

Volumn 414, Issue 2, 2016, Pages 133-141

  Gauron, Carole ^a,e   Meda, Francesca ^a,b,e   Dupont, Edmond ^a,e   Albadri, Shahad ^d,e   Quenech'Du, Nicole ^a,e   Ipendey, Eliane ^a,b,e   Volovitch, Michel ^a,b,e   Del Bene, Filippo ^d,e   Joliot, Alain ^a,e   Rampon, Christine ^a,c,e   Vriz, Sophie ^a,c,e  

^a l'alimentation et l'Environnement   (France)

^b ECOLE NORMALE SUPÉRIEURE   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d CNRS   (France)

^e PSL RESEARCH UNIVERSITY   (France)

Author keywords

Axon pathfinding; Hedgehog; Hydrogen peroxide

Indexed keywords

HYDROGEN PEROXIDE; SONIC HEDGEHOG PROTEIN; CATALASE; CYSTEINE; PHOTOPROTEIN; SHHA PROTEIN, ZEBRAFISH; SUPEROXIDE DISMUTASE; ZEBRAFISH PROTEIN;

ANIMAL CELL; ARTICLE; AXON; BRAIN DEVELOPMENT; CONTROLLED STUDY; DEVELOPMENT; EMBRYO; ENZYME DEGRADATION; EX VIVO STUDY; MORPHOGENESIS; NERVE FIBER GROWTH; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN SECRETION; REGULATORY MECHANISM; RETINA GANGLION CELL; SOMITOGENESIS; ZEBRA FISH; ANIMAL; AXON GUIDANCE; DRUG EFFECTS; EMBRYOLOGY; HELA CELL LINE; HUMAN; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL; ULTRASTRUCTURE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXON GUIDANCE; AXONS; CATALASE; CYSTEINE; HEDGEHOG PROTEINS; HELA CELLS; HUMANS; HYDROGEN PEROXIDE; LUMINESCENT PROTEINS; NEUROGENESIS; PROTEIN TRANSPORT; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84975167827     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2016.05.004     Document Type: Article

References (55)

1. Bai, H., Zhang, W., Qin, X.J., Zhang, T., Wu, H., Liu, J.Z., Hai, C.X., Hydrogen peroxide modulates the proliferation/quiescence switch in the liver during embryonic development and posthepatectomy regeneration. Antioxid. Redox Signal. 22 (2015), 921–937.
2. 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 3 (2006), 281–286.
3. Bigarella, C.L., Liang, R., Ghaffari, S., Stem cells and the impact of ROS signaling. Development 141 (2014), 4206–4218.
4. Briscoe, J., Therond, P.P., The mechanisms of Hedgehog signalling and its roles in development and disease. Nat. Rev. Mol. Cell Biol. 14 (2013), 416–429.
5. Carney, T.J., Ingham, P.W., Drugging Hedgehog: signaling the pathway to translation. BMC Biol., 11, 2013, 37.
6. Chamberlain, C.E., Jeong, J., Guo, C., Allen, B.L., McMahon, A.P., Notochord-derived Shh concentrates in close association with the apically positioned basal body in neural target cells and forms a dynamic gradient during neural patterning. Development 135 (2008), 1097–1106.
7. Chen, J.K., Taipale, J., Young, K.E., Maiti, T., Beachy, P.A., Small molecule modulation of smoothened activity. Proc. Natl. Acad. Sci. USA 99 (2002), 14071–14076.
8. Covarrubias, L., Hernandez-Garcia, D., Schnabel, D., Salas-Vidal, E., Castro-Obregon, S., Function of reactive oxygen species during animal development: passive or active?. Dev. Biol. 320 (2008), 1–11.
9. Ertzer, R., Muller, F., Hadzhiev, Y., Rathnam, S., Fischer, N., Rastegar, S., Strahle, U., Cooperation of sonic hedgehog enhancers in midline expression. Dev. Biol. 301 (2007), 578–589.
10. Finkel, T., Signal transduction by reactive oxygen species. J. Cell Biol. 194 (2011), 7–15.
11. Funato, Y., Michiue, T., Asashima, M., Miki, H., The thioredoxin-related redox-regulating protein nucleoredoxin inhibits Wnt-beta-catenin signalling through dishevelled. Nat. Cell Biol. 8 (2006), 501–508.
12. Galang, C.K., Hauser, C.A., Cooperative DNA binding of the human HoxB5 (Hox-2.1) protein is under redox regulation in vitro. Mol. Cell Biol. 13 (1993), 4609–4617.
13. Gauron, C., Rampon, C., Bouzaffour, M., Ipendey, E., Teillon, J., Volovitch, M., Vriz, S., Sustained production of ROS triggers compensatory proliferation and is required for regeneration to proceed. Sci. Rep., 3, 2013, 2084.
14. Gordon, L., Mansh, M., Kinsman, H., Morris, A.R., Xenopus sonic hedgehog guides retinal axons along the optic tract. Dev. Dyn. 239 (2010), 2921–2932.
15. Guerrero, I., Kornberg, T.B., Hedgehog and its circuitous journey from producing to target cells. Semin. Cell Dev. Biol. 33 (2014), 52–62.
16. Guo, Y., Einhorn, L., Kelley, M., Hirota, K., Yodoi, J., Reinbold, R., Scholer, H., Ramsey, H., Hromas, R., Redox regulation of the embryonic stem cell transcription factor oct-4 by thioredoxin. Stem Cells 22 (2004), 259–264.
17. Hardy, R.Y., Resh, M.D., Identification of N-terminal residues of Sonic Hedgehog important for palmitoylation by Hedgehog acyltransferase. J. Biol. Chem. 287 (2012), 42881–42889.
18. Hernandez-Garcia, D., Wood, C.D., Castro-Obregon, S., Covarrubias, L., Reactive oxygen species: a radical role in development?. Free Radic. Biol. Med. 49 (2010), 130–143.
19. Higashijima, S., Hotta, Y., Okamoto, H., Visualization of cranial motor neurons in live transgenic zebrafish expressing green fluorescent protein under the control of the islet-1 promoter/enhancer. J. Neurosci. 20 (2000), 206–218.
20. Jeong, J., McMahon, A.P., Cholesterol modification of Hedgehog family proteins. J. Clin. Investig. 110 (2002), 591–596.
21. Knoefler, D., Thamsen, M., Koniczek, M., Niemuth, N.J., Diederich, A.K., Jakob, U., Quantitative in vivo redox sensors uncover oxidative stress as an early event in life. Mol. Cell 47 (2012), 767–776.
22. Kucenas, S., Soto, F., Cox, J.A., Voigt, M.M., Selective labeling of central and peripheral sensory neurons in the developing zebrafish using P2X(3) receptor subunit transgenes. Neuroscience 138 (2006), 641–652.
23. Lee, J.J., Ekker, S.C., Vonkessler, D.P., Porter, J.A., Sun, B.I., Beachy, P.A., Autoproteolysis in Hedgehog protein biogenesis. Science 266 (1994), 1528–1537.
24. Long, J., Tokhunts, R., Old, W.M., Houel, S., Rodgriguez-Blanco, J., Singh, S., Schilling, N., Capobianco, A.J., Ahn, N.G., Robbins, D.J., Identification of a family of fatty-acid-speciated sonic hedgehog proteins, whose members display differential biological properties. Cell Rep. 10 (2015), 1280–1287.
25. Loo, A.E., Wong, Y.T., Ho, R., Wasser, M., Du, T., Ng, W.T., Halliwell, B., Effects of hydrogen peroxide on wound healing in mice in relation to oxidative damage. PLoS One, 7, 2012, e49215.
26. 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. 15 (2013), 222–228.
27. Marinho, H.S., Cyrne, L., Cadenas, E., Antunes, F., H2O2 delivery to cells: steady-state versus bolus addition. Methods Enzymol. 526 (2013), 159–173.
28. Marinho, H.S., Real, C., Cyrne, L., Soares, H., Antunes, F., Hydrogen peroxide sensing, signaling and regulation of transcription factors. Redox Biol. 2 (2014), 535–562.
29. Meda, F., Gauron, C., Rampon, C., Teillon, J., Volovitch, M., Vriz, S., Nerves control Redox level in mature tissues through Schwann cells and Hedgehog signaling. Antioxid. Redox Signal. 24 (2016), 299–311.
30. Mishina, N.M., Markvicheva, K.N., Bilan, D.S., Matlashov, M.E., Shirmanova, M.V., Liebl, D., Schultz, C., Lukyanov, S., Belousov, V.V., Visualization of intracellular hydrogen peroxide with HyPer, a genetically encoded fluorescent probe. Methods Enzymol. 526 (2013), 45–59.
31. Mosimann, C., Kaufman, C.K., Li, P., Pugach, E.K., Tamplin, O.J., Zon, L.I., Ubiquitous transgene expression and Cre-based recombination driven by the ubiquitin promoter in zebrafish. Development 138 (2011), 169–177.
32. Niethammer, P., Grabher, C., Look, A.T., Mitchison, T.J., A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459 (2009), 996–999.
33. Pepinsky, R.B., Zeng, C.H., Wen, D.Y., Rayhorn, P., Baker, D.P., Williams, K.P., Bixler, S.A., Ambrose, C.M., Garber, E.A., Miatkowski, K., Taylor, F.R., Wang, E.A., Galdes, A., Identification of a palmitic acid-modified form of human Sonic hedgehog. J. Biol. Chem. 273 (1998), 14037–14045.
34. Petrova, R., Joyner, A.L., Roles for Hedgehog signaling in adult organ homeostasis and repair. Development 141 (2014), 3445–3457.
35. Pirotte, N., Stevens, A.S., Fraguas, S., Plusquin, M., Van Roten, A., Van Belleghem, F., Paesen, R., Ameloot, M., Cebria, F., Artois, T., Smeets, K., Reactive oxygen species in planarian regeneration: an upstream necessity for correct patterning and brain formation. Oxid. Med. Cell Longev., 2015, 2015, 392476.
36. Ray, P.D., Huang, B.W., Tsuji, Y., Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24 (2012), 981–990.
37. Reczek, C.R., Chandel, N.S., ROS-dependdent signal transduction. Curr. Opin. Cell Biol. 33 (2015), 8–13.
38. 2, a necessary evil for cell signaling. Science 312 (2006), 1882–1883.
39. Rieger, S., Sagasti, A., Hydrogen peroxide promotes injury-induced peripheral sensory axon regeneration in the zebrafish skin. PLoS Biol., 9, 2011, e1000621.
40. Sanchez-Camacho, C., Bovolenta, P., Autonomous and non-autonomous Shh signalling mediate the in vivo growth and guidance of mouse retinal ganglion cell axons. Development 135 (2008), 3531–3541.
41. Schieber, M., Chandel, N.S., ROS function in redox signaling and oxidative stress. Curr. Biol. 24 (2014), R453–R462.
42. Shkumatava, A., Fischer, S., Muller, F., Strahle, U., Neumann, C.J., Sonic hedgehog, secreted by amacrine cells, acts as a short-range signal to direct differentiation and lamination in the zebrafish retina. Development 131 (2004), 3849–3858.
43. Stuermer, C.A., Retinotopic organization of the developing retinotectal projection in the zebrafish embryo. J. Neurosci. 8 (1988), 4513–4530.
44. Suh, E., Chen, L., Taylor, J., Traber, P.G., A homeodomain protein related to caudal regulates intestine-specific gene transcription. Mol. Cell Biol. 14 (1994), 7340–7351.
45. Therond, P.P., Release and transportation of Hedgehog molecules. Curr. Opin. Cell Biol. 24 (2012), 173–180.
46. Thisse, C., Thisse, B., High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protoc. 3 (2008), 59–69.
47. Tighe, A., Staples, O., Taylor, S., Mps1 kinase activity restrains anaphase during an unperturbed mitosis and targets Mad2 to kinetochores. J. Cell Biol. 181 (2008), 893–901.
48. van der Vliet, A., Janssen-Heininger, Y.M., Hydrogen peroxide as a damage signal in tissue injury and inflammation: murderer, mediator, or messenger?. J. Cell Biochem. 115 (2014), 427–435.
49. Wang, P., Jin, T., Hydrogen peroxide stimulates nuclear import of the POU homeodomain protein Oct-1 and its repressive effect on the expression of Cdx-2. BMC Cell Biol., 11, 2010, 56.
50. Watson, J.D., Type 2 diabetes as a redox disease. Lancet 383 (2014), 841–843.
51. Wen, L., Wei, W., Gu, W., Huang, P., Ren, X., Zhang, Z., Zhu, Z., Lin, S., Zhang, B., Visualization of monoaminergic neurons and neurotoxicity of MPTP in live transgenic zebrafish. Dev. Biol. 314 (2008), 84–92.
52. Wong, J.L., Creton, R., Wessel, G.M., The oxidative burst at fertilization is dependent upon activation of the dual oxidase Udx1. Dev. Cell 7 (2004), 801–814.
53. Xiao, T., Baier, H., Lamina-specific axonal projections in the zebrafish tectum require the type IV collagen Dragnet. Nat. Neurosci. 10 (2007), 1529–1537.
54. Xu, L., Feng, Z., Sinha, D., Ducos, B., Ebenstein, Y., Tadmor, A.D., Gauron, C., Le Saux, T., Lin, S., Weiss, S., Vriz, S., Jullien, L., Bensimon, D., Spatiotemporal manipulation of retinoic acid activity in zebrafish hindbrain development via photo-isomerization. Development 139 (2012), 3355–3362.
55. Ye, Z.W., Zhang, J., Townsend, D.M., Tew, K.D., Oxidative stress, redox regulation and diseases of cellular differentiation. Biochim. Biophys. Acta 1850 (2014), 1607–1621.