Rapid and Permanent Neuronal Inactivation InVivo via Subcellular Generation of Reactive Oxygen with the Use of KillerRed

Cell Reports

Volumn 5, Issue 2, 2013, Pages 553-563

  Williams, Daniel C ^a   ElBejjani, Rachid ^a   Ramirez, PaulaMugno ^b   Coakley, Sean ^b   Kim, Shin Ae ^c   Lee, Hyewon ^c   Wen, Quan ^d   Samuel, Aravi ^d   Lu, Hang ^c   Hilliard, Massimo A ^b   Hammarlund, Marc ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c Georgia Institute of Technology   (United States)

^d HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CASPASE; FLUORESCENT DYE; KILLER RED; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; GREEN FLUORESCENT PROTEIN; KILLER RED PROTEIN, ANTHOMEDUSAE; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CAENORHABDITIS ELEGANS; CELL FUNCTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; IN VIVO STUDY; NERVE CELL DEGENERATION; NERVE CELL LESION; NERVE CELL MEMBRANE; NEUROTOXICITY; NONHUMAN; PERIKARYON; PHOTOSTIMULATION; PRIORITY JOURNAL; ANIMAL; APOPTOSIS; DRUG EFFECTS; GENETICS; LIGHT; METABOLISM; RADIATION RESPONSE; VIDEO MICROSCOPY;

ANIMALIA;

ANIMALS; APOPTOSIS; CAENORHABDITIS ELEGANS; GABAERGIC NEURONS; GREEN FLUORESCENT PROTEINS; LIGHT; MICROSCOPY, VIDEO; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 84887016927     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.09.023     Document Type: Article

References (45)

1. Alfonso A., Grundahl K., Duerr J.S., Han H.-P., Rand J.B. The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter. Science 1993, 261:617-619.
2. Avery L., Horvitz H.R. A cell that dies during wild-type C. elegans development can function as a neuron in a ced-3 mutant. Cell 1987, 51:1071-1078.
3. Avery L., Horvitz H.R. Pharyngeal pumping continues after laser killing of the pharyngeal nervous system of C. elegans. Neuron 1989, 3:473-485.
4. Barnham K.J., Masters C.L., Bush A.I. Neurodegenerative diseases and oxidative stress. Nat. Rev. Drug Discov. 2004, 3:205-214.
5. Bulina M.E., Chudakov D.M., Britanova O.V., Yanushevich Y.G., Staroverov D.B., Chepurnykh T.V., Merzlyak E.M., Shkrob M.A., Lukyanov S., Lukyanov K.A. A genetically encoded photosensitizer. Nat. Biotechnol. 2006, 24:95-99.
6. Campbell R.E., Tour O., Palmer A.E., Steinbach P.A., Baird G.S., Zacharias D.A., Tsien R.Y. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 2002, 99:7877-7882.
7. Carpentier P., Violot S., Blanchoin L., Bourgeois D. Structural basis for the phototoxicity of the fluorescent protein KillerRed. FEBS Lett. 2009, 583:2839-2842.
8. Catalá A. A synopsis of the process of lipid peroxidation since the discovery of the essential fatty acids. Biochem. Biophys. Res. Commun. 2010, 399:318-323.
9. Chow B.Y., Han X., Dobry A.S., Qian X., Chuong A.S., Li M., Henninger M.A., Belfort G.M., Lin Y., Monahan P.E., Boyden E.S. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 2010, 463:98-102.
10. DiMauro S., Schon E.A. Mitochondrial disorders in the nervous system. Annu. Rev. Neurosci. 2008, 31:91-123.
11. Edwards S.L., Charlie N.K., Milfort M.C., Brown B.S., Gravlin C.N., Knecht J.E., Miller K.G. A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans. PLoS Biol. 2008, 6:e198.
12. Ellis H.M., Horvitz H.R. Genetic control of programmed cell death in the nematode C. elegans. Cell 1986, 44:817-829.
13. Fang-Yen C., Gabel C.V., Samuel A.D.T., Bargmann C.I., Avery L. Laser microsurgery in Caenorhabditis elegans. Methods Cell Biol. 2012, 107:177-206.
14. Fatokun A.A., Stone T.W., Smith R.A. Oxidative stress in neurodegeneration and available means of protection. Front. Biosci. 2008, 13:3288-3311.
15. Fire A., Harrison S.W., Dixon D. A modular set of lacZ fusion vectors for studying gene expression in Caenorhabditis elegans. Gene 1990, 93:189-198.
16. Frøkjaer-Jensen C., Davis M.W., Hollopeter G., Taylor J., Harris T.W., Nix P., Lofgren R., Prestgard-Duke M., Bastiani M., Moerman D.G., Jorgensen E.M. Targeted gene deletions in C. elegans using transposon excision. Nat. Methods 2010, 7:451-453.
17. Gitai Z., Yu T.W., Lundquist E.A., Tessier-Lavigne M., Bargmann C.I. The netrin receptor UNC-40/DCC stimulates axon attraction and outgrowth through enabled and, in parallel, Rac and UNC-115/AbLIM. Neuron 2003, 37:53-65.
18. Hall D.H., Gu G., García-Añoveros J., Gong L., Chalfie M., Driscoll M. Neuropathology of degenerative cell death in Caenorhabditis elegans. J.Neurosci. 1997, 17:1033-1045.
19. Ichishita R., Tanaka K., Sugiura Y., Sayano T., Mihara K., Oka T. An RNAi screen for mitochondrial proteins required to maintain the morphology of the organelle in Caenorhabditis elegans. J.Biochem. 2008, 143:449-454.
20. Kanaji S., Iwahashi J., Kida Y., Sakaguchi M., Mihara K. Characterization of the signal that directs Tom20 to the mitochondrial outer membrane. J.Cell Biol. 2000, 151:277-288.
21. Keller J.N., Pang Z., Geddes J.W., Begley J.G., Germeyer A., Waeg G., Mattson M.P. Impairment of glucose and glutamate transport and induction of mitochondrial oxidative stress and dysfunction in synaptosomes by amyloid β-peptide: role of the lipid peroxidation product 4-hydroxynonenal. J.Neurochem. 1997, 69:273-284.
22. Landis G.N., Tower J. Superoxide dismutase evolution and life span regulation. Mech. Ageing Dev. 2005, 126:365-379.
23. Leifer A.M., Fang-Yen C., Gershow M., Alkema M.J., Samuel A.D.T. Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans. Nat. Methods 2011, 8:147-152.
24. Liu Q., Hollopeter G., Jorgensen E.M. Graded synaptic transmission at the Caenorhabditis elegans neuromuscular junction. Proc. Natl. Acad. Sci. USA 2009, 106:10823-10828.
25. Mark R.J., Hensley K., Butterfield D.A., Mattson M.P. Amyloid beta-peptide impairs ion-motive ATPase activities: evidence for a role in loss of neuronal Ca2+ homeostasis and cell death. J.Neurosci. 1995, 15:6239-6249.
26. McIntire S.L., Jorgensen E., Kaplan J., Horvitz H.R. The GABAergic nervous system of Caenorhabditis elegans. Nature 1993, 364:337-341.
27. McIntire S.L., Reimer R.J., Schuske K., Edwards R.H., Jorgensen E.M. Identification and characterization of the vesicular GABA transporter. Nature 1997, 389:870-876.
28. Mello C.C., Kramer J.M., Stinchcomb D., Ambros V. Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 1991, 10:3959-3970.
29. Nagel G., Brauner M., Liewald J.F., Adeishvili N., Bamberg E., Gottschalk A. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 2005, 15:2279-2284.
30. Neumann B., Nguyen K.C.Q., Hall D.H., Ben-Yakar A., Hilliard M.A. Axonal regeneration proceeds through specific axonal fusion in transected C. elegans neurons. Dev. Dyn. 2011, 240:1365-1372.
31. Okazaki A., Sudo Y., Takagi S. Optical silencing of C. elegans cells with arch proton pump. PLoS ONE 2012, 7:e35370.
32. Pletnev S., Gurskaya N.G., Pletneva N.V., Lukyanov K.A., Chudakov D.M., Martynov V.I., Popov V.O., Kovalchuk M.V., Wlodawer A., Dauter Z., Pletnev V. Structural basis for phototoxicity of the genetically encoded photosensitizer KillerRed. J.Biol. Chem. 2009, 284:32028-32039.
33. Qi Y.B., Garren E.J., Shu X., Tsien R.Y., Jin Y. Photo-inducible cell ablation in Caenorhabditis elegans using the genetically encoded singletoxygen generating protein miniSOG. Proc. Natl. Acad. Sci. USA 2012, 109:7499-7504.
34. Rand J.B. Genetic analysis of the cha-1-unc-17 gene complex in Caenorhabditis. Genetics 1989, 122:73-80.
35. Roy A., Carpentier P., Bourgeois D., Field M. Diffusion pathways of oxygen species in the phototoxic fluorescent protein KillerRed. Photochem. Photobiol. Sci. 2010, 9:1342-1350.
36. Serebrovskaya E.O., Edelweiss E.F., Stremovskiy O.A., Lukyanov K.A., Chudakov D.M., Deyev S.M. Targeting cancer cells by using an antireceptor antibody-photosensitizer fusion protein. Proc. Natl. Acad. Sci. USA 2009, 106:9221-9225.
37. Shaner N.C., Campbell R.E., Steinbach P.A., Giepmans B.N.G., Palmer A.E., Tsien R.Y. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 2004, 22:1567-1572.
38. Shu X., Lev-Ram V., Deerinck T.J., Qi Y., Ramko E.B., Davidson M.W., Jin Y., Ellisman M.H., Tsien R.Y. A genetically encoded tag for correlated light and electron microscopy of intact cells, tissues, and organisms. PLoS Biol. 2011, 9:e1001041.
39. Smith A.J., Smith R.A., Stone T.W. 5-Hydroxyanthranilic acid, a tryptophan metabolite, generates oxidative stress and neuronal death via p38 activation in cultured cerebellar granule neurones. Neurotox. Res. 2009, 15:303-310.
40. Stenico M., Lloyd A.T., Sharp P.M. Codon usage in Caenorhabditis elegans: delineation of translational selection and mutational biases. Nucleic Acids Res. 1994, 22:2437-2446.
41. Stirman J.N., Crane M.M., Husson S.J., Wabnig S., Schultheis C., Gottschalk A., Lu H. Real-time multimodal optical control of neurons and muscles in freely behaving Caenorhabditis elegans. Nat. Methods 2011, 8:153-158.
42. Teh C., Chudakov D.M., Poon K.-L., Mamedov I.Z., Sek J.-Y., Shidlovsky K., Lukyanov S., Korzh V. Optogenetic invivo cell manipulation in KillerRed-expressing zebrafish transgenics. BMC Dev. Biol. 2010, 10:110.
43. Uttara B., Singh A.V., Zamboni P., Mahajan R.T. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr. Neuropharmacol. 2009, 7:65-74.
44. White J.G., Southgate E., Thomson J.N., Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1986, 314:1-340.
45. Zhang F., Wang L.-P., Brauner M., Liewald J.F., Kay K., Watzke N., Wood P.G., Bamberg E., Nagel G., Gottschalk A., Deisseroth K. Multimodal fast optical interrogation of neural circuitry. Nature 2007, 446:633-639.