Hydrogen peroxide stimulates activity and alters behavior in Drosophila melanogaster

PLoS ONE

Volumn 4, Issue 10, 2009, Pages

  Grover, Dhruv ^a,b   Ford, Daniel ^a   Brown, Christopher ^a   Hoe, Nicholas ^a   Erdem, Aysen ^a   Tavaré, Simon ^a   Tower, John ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN PEROXIDE; SUPEROXIDE DISMUTASE; OXIDIZING AGENT;

ANIMAL BEHAVIOR; ANIMAL FOOD; ARTICLE; BODY MOVEMENT; CIRCADIAN RHYTHM; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENE ACTIVITY; GENE OVEREXPRESSION; LOCOMOTION; MALE; NONHUMAN; THREE DIMENSIONAL IMAGING; TIME; ANIMAL; BIOLOGICAL MODEL; CROSS BREEDING; DRUG EFFECT; FLUORESCENCE MICROSCOPY; FLYING; METABOLISM; METHODOLOGY; MOVEMENT (PHYSIOLOGY); OXIDATION REDUCTION REACTION; SEASON; TRANSGENIC ANIMAL;

ANIMALIA; DROSOPHILA MELANOGASTER;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; CROSSES, GENETIC; DROSOPHILA MELANOGASTER; FLIGHT, ANIMAL; HYDROGEN PEROXIDE; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MOVEMENT; OXIDANTS; OXIDATION-REDUCTION; SEASONS; SUPEROXIDE DISMUTASE; TIME FACTORS;

EID: 70449585209     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007580     Document Type: Article

References (67)

1. Szebenyi AL (1969) Cleaning behavior in Drosophila melanogaster. Animal Behaviour 17: 641-651.
2. Meunier N, Belgacem YH, Martin JR (2007) Regulation of feeding behaviour and locomotor activity by takeout in Drosophila. J Exp Biol 210: 1424-1434.
3. Vrontou E, Nilsen SP, Demir E, Kravitz EA, Dickson BJ (2006) fruitless regulates aggression and dominance in Drosophila. Nat Neurosci 9: 1469-1471.
4. Kadener S, Villella A, Kula E, Palm K, Pyza E, et al. (2006) Neurotoxic protein expression reveals connections between the circadian clock and mating behavior in Drosophila. Proc Natl Acad Sci U S A 103: 13537-13542.
5. Nishinokubi I, Shimoda M, Ishida N (2006) Mating rhythms of Drosophila: rescue of tim01 mutants by D. ananassae timeless. J Circadian Rhythms 4: 4.
6. Howlader G, Sharma VK (2006) Circadian regulation of egg-laying behavior in fruit flies Drosophila melanogaster. J Insect Physiol 52: 779-785.
7. Schibler U, Naef F (2005) Cellular oscillators: rhythmic gene expression and metabolism. Curr Opin Cell Biol 17: 223-229.
8. Boothroyd CE, Wijnen H, Naef F, Saez L, Young MW (2007) Integration of light and temperature in the regulation of circadian gene expression in Drosophila. PLoS Genet 3: e54.
9. Wijnen H, Young MW (2006) Interplay of circadian clocks and metabolic rhythms. Annu Rev Genet 40: 409-448.
10. Chen Z, Odstrcil EA, Tu BP, McKnight SL (2007) Restriction of DNA replication to the reductive phase of the metabolic cycle protects genome integrity. Science 316: 1916-1919.
11. King-Jones K, Horner MA, Lam G, Thummel CS (2006) The DHR96 nuclear receptor regulates xenobiotic responses in Drosophila. Cell Metab 4: 37-48.
12. Green CB, Takahashi JS (2006) Xenobiotic metabolism in the fourth dimension: PARtners in time. Cell Metab 4: 3-4.
13. Pletcher SD, Macdonald SJ, Marguerie R, Certa U, Stearns SC, et al. (2002) Genome-wide transcript profiles in aging and calorically restricted Drosophila melanogaster. Current Biology 12: 712-723.
14. Landis GN, Abdueva D, Skvortsov D, Yang J, Rabin BE, et al. (2004) Similar gene expression patterns characterize aging and oxidative stress in Drosophila melanogaster. Proc Natl Acad Sci U S A 101: 7663-7668.
15. Gems D, McElwee JJ (2005) Broad spectrum detoxification: the major longevity assurance process regulated by insulin/IGF-1 signaling? Mech Ageing Dev 126: 381-387.
16. Curtis C, Landis GN, Folk D, Wehr NB, Hoe N, et al. (2007) Transcriptional profiling of MnSOD-mediated lifespan extension in Drosophila reveals a species-general network of aging and metabolic genes. Genome Biol 8: R262.
17. Driver C, Georgiou A, Georgiou G (2004) The contribution by mitochondrially induced oxidative damage to aging in Drosophila melanogaster. Biogerontology 5: 185-192.
18. Koh K, Evans JM, Hendricks JC, Sehgal A (2006) A Drosophila model for age-associated changes in sleep:wake cycles. Proc Natl Acad Sci U S A 103: 13843-13847.
19. Shaw PJ, Tononi G, Greenspan RJ, Robinson DF (2002) Stress response genes protect against lethal effects of sleep deprivation in Drosophila. Nature 417: 287-291.
20. Landis GN, Tower J (2005) Superoxide dismutase evolution and life span regulation. Mech Ageing Dev 126: 365-379.
21. Yang J, Tower J (2009) Expression of hsp22 and hsp70 transgenes is partially predictive of Drosophila survival under normal and stress conditions. J Gerontol A Biol Sci Med Sci 64: 828-838.
22. Grover D, Yang J, Tavare S, Tower J (2008) Simultaneous tracking of fly movement and gene expression using GFP. BMC Biotechnol 8: 93.
23. Lee CC (2006) Tumor suppression by the mammalian Period genes. Cancer Causes Control 17: 525-530.
24. Tu BP, McKnight SL (2006) Metabolic cycles as an underlying basis of biological oscillations. Nat Rev Mol Cell Biol 7: 696-701.
25. Besson M, Martin JR (2005) Centrophobism/thigmotaxis, a new role for the mushroom bodies in Drosophila. J Neurobiol 62: 386-396.
26. Williams AE, Rose MR, Bradley TJ (2004) The respiratory pattern in Drosophila melanogaster selected for desiccation resistance is not associated with the observed evolution of decreased locomotory activity. Physiol Biochem Zool 77: 10-17.
27. Martin JR (2004) A portrait of locomotor behaviour in Drosophila determined by a video-tracking paradigm. Behav Processes 67: 207-219.
28. Valente D, Golani I, Mitra PP (2007) Analysis of the trajectory of Drosophila melanogaster in a circular open field arena. PLoS ONE 2: e1083.
29. Budick SA, Dickinson MH (2006) Free-flight responses of Drosophila melanogaster to attractive odors. J Exp Biol 209: 3001-3017.
30. Tammero LF, Dickinson MH (2002) The influence of visual landscape on the free flight behavior of the fruit fly Drosophila melanogaster. J Exp Biol 205: 327-343.
31. Branson K, Robie AA, Bender J, Perona P, Dickinson MH (2009) High-throughput ethomics in large groups of Drosophila. Nat Methods 6: 451-457.
32. Grover D, Tower J, Tavare S (2008) O fly, where art thou? J R Soc Interface 5: 1181-1191.
33. Grover D, Yang J, Ford D, Tavare S, Tower J (2009) Simultaneous tracking of movement and gene expression in multiple Drosophila melanogaster flies using GFP and DsRED fluorescent reporter transgenes. BMC Res Notes 2: 58.
34. Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120: 483-495.
35. Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59: 527-605.
36. Margoliash E, Novogrodsky A (1958) A study of the inhibition of catalase by 3-amino-1:2:4:-triazole. Biochem J 68: 468-475.
37. Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64: 97-112.
38. Bieschke ET, Wheeler JC, Tower J (1998) Doxycycline-induced transgene expression during Drosophila development and aging. Mol Gen Genet 258: 571-579.
39. Ford D, Hoe N, Landis GN, Tozer K, Luu A, et al. (2007) Alteration of Drosophila life span using conditional, tissue-specific expression of transgenes triggered by doxycycline or RU486/Mifepristone. Exp Gerontol 42: 483-497.
40. Cleveland RB, Cleveland WS, McRae JE, Terpenning I (1990) STL: A seasonal-trend decomposition procedure based on Loess. Journal of Official Statistics 6: 3-73.
41. Kaneuchi T, Togawa T, Matsuo T, Fuyama Y, Aigaki T (2003) Efficient measurement of H(2)O(2) resistance in Drosophila using an activity monitor. Biogerontology 4: 157-165.
42. Allegra M, Reiter RJ, Tan DX, Gentile C, Tesoriere L, et al. (2003) The chemistry of melatonin's interaction with reactive species. J Pineal Res 34: 1-10.
43. Tan DX, Reiter RJ, Manchester LC, Yan MT, El-Sawi M, et al. (2002) Chemical and physical properties and potential mechanisms: melatonin as a broad spectrum antioxidant and free radical scavenger. Curr Top Med Chem 2: 181-197.
44. Grzelak A, Macierzynska E, Bartosz G (2004) Melatonin does not react rapidly with hydrogen peroxide. Free Radic Res 38: 1155-1158.
45. Goncharova ND, Shmaliy AV, Bogatyrenko TN, Koltover VK (2006) Correlation between activity of antioxidant enzymes and circadian rhythms of corticosteroids in Macaca mulatta monkeys of different age. Exp Gerontol 41: 778-783.
46. Thomson SL, Garland Jr T, Swallow JG, Carter PA (2002) Response of Sod-2 enzyme activity to selection for high voluntary wheel running. Heredity 88: 52-61.
47. Liochev SI, Fridovich I (2007) The effects of superoxide dismutase on H2O2 formation. Free Radic Biol Med 42: 1465-1469.
48. Hanson GT, Aggeler R, Oglesbee D, Cannon M, Capaldi RA, et al. (2004) Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J Biol Chem 279: 13044-13053.
49. Dooley CT, Dore TM, Hanson GT, Jackson WC, Remington SJ, et al. (2004) Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J Biol Chem 279: 22284-22293.
50. Bjornberg O, Ostergaard H, Winther JR (2006) Measuring intracellular redox conditions using GFP-based sensors. Antioxid Redox Signal 8: 354-361.
51. Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, et al. (2007) Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 52: 973-86.
52. Niethammer P, Grabher C, Look AT, Mitchison TJ (2009) A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459: 996-999.
53. Krishnan N, Davis AJ, Giebultowicz JM (2008) Circadian regulation of response to oxidative stress in Drosophila melanogaster. Biochem Biophys Res Commun 374: 299-303.
54. Rutter J, Reick M, McKnight SL (2002) Metabolism and the control of circadian rhythms. Annu Rev Biochem 71: 307-331.
55. Rutter J, Reick M, Wu LC, McKnight SL (2001) Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science 293: 510-514.
56. Fridovich I (2004) Mitochondria: are they the seat of senescence? Aging Cell 3: 13-16.
57. Kondratov RV (2007) A role of the circadian system and circadian proteins in aging. Ageing Res Rev 6: 12-27.
58. Sun J, Folk D, Bradley TJ, Tower J (2002) Induced overexpression of mitochondrial Mn-superoxide dismutase extends the life span of adult Drosophila melanogaster. Genetics 161: 661-672.
59. Allikian MJ, Deckert-Cruz D, Rose MR, Landis GN, Tower J (2002) Doxycycline-induced expression of sense and inverted-repeat constructs modulates phosphogluconate mutase (Pgm) gene expression in adult Drosophila melanogaster. Genome Biol 3: research0021.
60. Brockwell PJ, Davis RA (1993) Time Series: Theory and Methods.: Springer-Verlag New York, Inc..
61. Levine JD, Funes P, Dowse HB, Hall JC (2002) Signal analysis of behavioral and molecular cycles. BMC Neurosci 3: 1.
62. de Gooijer JG, Abraham B, Gould A, Robinson L (1985) Methods for determining the order of an autoregressive-moving average process: A survey. International Statistical Review 53: 301-329.
63. RDevelopmentCore Team (2006) R: A language and environment for statistical computing.: R Foundation for Statistical Computing, Vienna, Austria.
64. Trapletti A, Hornik K (2007) tseries: Time Series Analysis and Computational Finance. R package version 010-11.
65. Montell C (1999) Visual transduction in Drosophila. Annu Rev Cell Dev Biol 15: 231-268.
66. Feldman A, Balch T (2004) Representing honey bee behavior for recognition using human trainable models. Adaptive Behavior - Animals, Animats, Software Agents, Robots, Adaptive Systems 12: 241-250.
67. Davis RA, Lee TCM, Rodriguez-Yam GA (2006) Structural break estimation for nonstationary time series models. Journal of the American Statistical Association 101: 223-239.