Insecticide resistance and glutathione S-transferases in mosquitoes: A review

African Journal of Biotechnology

Volumn 8, Issue 8, 2009, Pages 1386-1397

  Che Mendoza, Azael ^a   Penilla, R Patricia ^b   Rodriguez, D Américo ^b  

^a Servicios de Salud de Morelos   (Mexico)

^b INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

Author keywords

Glutathione s transferase; Gst based metabolic resistance; Insecticide resistance

Indexed keywords

CHLORPHENOTANE; GLUTATHIONE TRANSFERASE; ORGANOCHLORINE DERIVATIVE; ORGANOPHOSPHATE; PYRETHROID; XENOBIOTIC AGENT;

CHEMICAL STRUCTURE; DETOXIFICATION; ELIMINATION REACTION; ENZYME ACTIVITY; ENZYME PURIFICATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; GENE ISOLATION; INSECTICIDE RESISTANCE; LIPID PEROXIDATION; MOSQUITO; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW;

HEXAPODA;

EID: 66749191111     PISSN: None     EISSN: 16845315     Source Type: Journal    
DOI: None     Document Type: Review

References (99)

1. Abdollahi M, Ranjbar A, Shadnia S, Shekoufeh N, Rezaie A (2004). Pesticide and oxidative stress: a review. Med. Sci. Monit. 10:RA141- 147.
2. Adler V, Yin Z, Fuchs SY, Benezra M, Rosario L, Tew KD, et al (1999). Regulation of JNK signaling by GSTp. Embo J. 18: 1321 -1334.
3. Armstrong RN (1991). Glutathione S-transferases: reaction mechanism, structure, and function. Chem. Res. Toxicol. 4:131-140.
4. Beall C, Fyrberg C, Song S, Fyrberg E (1992). Isolation of a Drosophila gene encoding glutathione S-transferase. Biochem. Genet. 30: 515-527.
5. Bloomquist JR (1998). Chemistry and toxicology of the chlorinated cyclodienes and lindane. Rev. Pestic. Toxicol. 2: 333-355.
6. Bogwitz M (2005). The genetics resistance to lufenuron in Drosophila melanogaster. Ph.D. Thesis, University of Melbourne, Melbourne, Australia.
7. Brown AWA (1986). Insecticide resistance in mosquitoes: a pragmatic review. J. Am. Mosq. Control Assoc. 2: 123-140.
8. Chelvanayagam G, Parker MW, Board PG (2001). Fly fishing for GSTs: a unified nomenclature for mammalian and insect glutathione transferases. Chem. Biol. Interact. 133: 256-260.
9. Chen L, Hall PR, Zhou XE, Ranson H, Hemingway J, Meehan EJ (2003). Structure of an insect delta-class glutathione S-transferase from a DDT-resistant strain of the malaria vector Anopheles gambiae. Acta Cryst. D59: 2211 -2217.
10. Chiang, FM, Sun CN (1993). Glutathione transferase isozymes of diamondback moth larvae and their role in the degradation of some organophosphorus insecticides. Pestic. Biochem. Physiol. 45: 7-14.
11. Cho SG, Lee YH, Park HS, Ryoo K, Kang KW, Park J, Eom SJ, Kim MJ, Chang TS, Choi SY, Shim J, Kim Y, Dong MS, Lee MJ, Kim SG, Ichijo H, Choi EJ (2001). Glutathione S-transferase Mu modulates the stress-activated signals by suppressing apoptosis signal- regulating Kinase 1. Biol. Chem. 276:12749-12755.
12. Clark AG, Shamaan NA (1984). Evidence that DDT-dehydrochlorinase from the house fly is a glutathione S-transferase. Pestic. Biochem. Physiol. 22: 249-261.
13. Clark AG, Shamaan NA, Sinclair MD, Dauterman WC (1986). Insecticide metabolism by multiple glutathione S-transferases in two strains of the house fly, Musca domestica (L.). Pestic. Biochem. Physiol. 25: 169-175.
14. Danielson UH, Mannervik B (1985). Kinetic independence of the subunits of cytosolic glutathione transferase from the rat. Biochem. J. 231: 263-267.
15. David J-P, Strode C, Vontas J, Nikou D, Vaughan A, Pignatelli P, Christos L, Janet H, Hilary R (2005). The Anopheles gambiae detoxification chip: A highly specific microarray to study metabolic based insecticide resistance in malaria vectors. Proc. Natl. Acad. Sci. 102: 4080-4084.
16. Dimopoulos G, Christophides GK, Meister S, Schultz J, White KP, Barillas-Mury C, Kafatos FC (2002). Genome expression analysis of Anopheles gambiae: responses to injury, bacterial challenge, and malaria infection. Proc. Natl. Acad. Sci. 99: 8814-8819.
17. Ding Y, Ortelli F, Rossiter LC, Hemingway J, Ranson H (2003). The Anopheles gambiae glutathione transferase supergene family: annotation, phylogeny and expression profiles. BMC Genomics 4: 35.
18. Ding Y, Hawkes N, Meredith J, Eggleston P, Hemingway J, Ranson H (2005). Characterisation of the promoters of Epsilon glutathione transferases in the mosquito Anopheles gambiae and their response to oxidative stress. Biochem. J. 387: 879-888.
19. Enayati AA, Ranson H, Hemingway J (2005). Mini Review: Insect glutathione transferases and insecticide resistance. Insect. Mol. Biol. 14:3-8.
20. Feyereisen R (1995). Molecular biology of insecticide resistance. Toxicol. Lett. 82-83: 83-90.
21. Fournier D, Bride J-M, Poirie' M, Berge' J-B, Plapp FW (1992). Insect glutathione S-transferases. Biochemical characteristics of the major forms from houseflies susceptible and resistant to insecticides. J. Biol. Chem. 267: 1840-1845.
22. Grant DF, Matsumura F (1988). Glutathione S-transferase-1 in Aedes aegypti larvae. Purification and properties. Insect. Biochem. 18: 615-622.
23. Grant DF, Matsumura F (1989). Glutathione S-transferase 1 and 2 in susceptible and insecticide resistant Aedes aegypti. Pestic. Biochem. Physiol. 33: 132-143.
24. Grant DF, Dietze EC, Hammock BD (1991). Glutathione S-transferase isozymes in Aedes aegypti: purification, characterization, and isozyme specific regulation. Insect. Biochem. 4: 421-433.
25. Grant DF, Hammock BD (1992). Genetic and molecular evidence for a trans-acting regulatory locus controlling glutathiones transferase-2 expression in Aedes aegypti. Mol. Gen. Genet. 234: 169-176.
26. Ha EM, Oh CT, Bae YS, Lee WJ (2005a). A direct role for dual oxidase in Drosophila gut immunity. Science 310: 847-850.
27. Ha EM, Oh CT, Ryu JH, Bae YS, Kang SW, Jang IH, Brey PT, Lee WJ (2005b). An antioxidant system required for host protection against gut infection in Drosophila. Dev. Cell. 8: 125-132.
28. Habig WH, Pabst MJ, Jakoby WB (1974). Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249(22): 7130-7139.
29. Halliday WR, Feyereisen R (1987). Why does DDT toxicity change after a blood meal in adult female Culex pipiens? Pestic. Biochem. Physiol. 28: 172-181.
30. Harshman LG, James AA (1998). Differential gene expression in insects: transcriptional control. Annu. Rev. Entomol. 43: 671-700.
31. Hayes JD, Wolf CR (1988). Role of glutathione transferase in drug resistance. In: Sies H, Ketterer B (eds) Glutathione conjugation: Mechanisms and Biological Significance. Academic Press, London, pp. 315-355.
32. Hazelton GA, Lang CA (1983). Glutathione S-transferase activities in the yellow-fever mosquito [Aedes aegypti (Louisville)] during growth and aging. Biochem. J. 210: 281-287.
33. Hemingway J, Miyamoto J, Herath PRJ (1991). A possible novel link between organophosphorus and DDT insecticide resistance genes in Anopheles: supporting evidence from fenitrothion metabolism studies. Pestic. Biochem. Physiol. 39: 49-56.
34. Hemingway J (2000). Mini review: The molecular basis of two contrasting metabolic mechanisms of insecticide resistance. Insect. Biochem. Mol. Biol. 30: 1009-1015.
35. Hemingway J, Ranson H (2000). Insecticida resistance in insect vectors of human disease. Annu. Rev. Entomol. 45: 371-391.
36. Hemingway J, Hawkes NJ, McCarroll L, Ranson H (2004). The molecular basis of insecticide resistance in mosquitoes. Insect. Biochem. Mol. Biol. 34: 653-665.
37. Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JM, Wides R, Salzberg SL, Loftus B, Yandell M, Majoros WH, Rusch DB, Lai Z, Kraft CL, Abril JF, Anthouard V, Arensburger P, Atkinson PW, Baden H, de Berardinis V, Baldwin D, Benes V, Biedler J, Blass C, Bolanos R, Boscus D, Barnstead M, Cai S, Center A, Chaturverdi K, Christophides GK, Chrystal MA, Clamp M, Cravchik A, Curwen V, Dana A, Delcher A, Dew I, Evans CA, Flanigan M, Grundschober- Freimoser A, Friedli L, Gu Z, Guan P, Guigo R, Hillenmeyer ME, Hladun SL, Hogan JR, Hong YS, Hoover J, Jaillon O, Ke Z, Kodira C, Kokoza E, Koutsos A, Letunic I, Levitsky A, Liang Y, Lin JJ, Lobo NF, Lopez JR, Malek JA, McIntosh TC, Meister S, Miller J, Mobarry C, Mongin E, Murphy SD, O'Brochta DA, Pfannkoch C, Qi R, Regier MA, Remington K, Shao H, Sharakhova MV, Sitter CD, Shetty J, Smith TJ, Strong R, Sun J, Thomasova D, Ton LQ, Topalis P, Tu Z, Unger MF, Walenz B, Wang A, Wang J, Wang M, Wang X, Woodford KJ, Wortman JR, Wu M, Yao A, Zdobnov EM, Zhang H, Zhao Q, Zhao S, Zhu SC, Zhimulev I, Coluzzi M, della Torre A, Roth CW, Louis C, Kalush F, Mural RJ, Myers EW, Adams MD, Smith HO, Broder S, Gardner MJ, Fraser CM, Birney E, Bork P, Brey PT, Venter JC, Weissenbach J, Kafatos FC, Collins FH, Hoffman SL (2002). The genome sequence of the malaria mosquito Anopheles gambiae. Science 298(5591): 129-149.
38. Hooper GH (1967). The effect of larval density on mortality of Culex pipiens fatigans due to DDT and Dieldrin. Bull WHO 36: 179-80.
39. Hoy MA (1994). Comp. Insect molecular genetics: An introduction to principles and applications. Gainesville; Academic Press. http://www.uams.edu/ biochem/Hbenes.asp
40. Huang HS, Hu NT, Yao YE, Wu CY, Chiang SW, Sun CN (1998). Molecular cloning and heterologous expression of a glutathione S- transferase involved in insecticide resistance from the diamondback moth, Plutella xylostella. Insect. Biochem. Mol. Biol. 28: 651-658. Jakobsson PJ, Morgenstern R, Mancini J, Ford-Hutchinson A, Persson B (1999). Common structural features of MAPEG -- a widespread
41. superfamily of membrane associated proteins with highly divergent functions in eicosanoid and glutathione metabolism. Protein Sci. 8: 689-692.
42. Jakoby WB, Ziegler DM (1990). The enzymes of detoxication. Minireview. J. Biol. Chem. 265: 20715-20718.
43. Jirajaroenrat K, Pongjaroenkit S, Krittanai C, Prapanthadara L, Ketterman AJ (2001). Heterologous expression and characterization of alternatively spliced glutathione S-transferases from a single Anopheles gene. Insect Biochem. Mol. Biol. 31: 867-875.
44. Kostaropoulos I, Papadopoulos AI, Metaxakis A, Boukouvala E, Papadopoulou-Mourkidou E (2001). Glutathione S-transferase in the defence against pyrethroids in insects. Insect Biochem. Mol. Biol. 31: 313-319.
45. Kumar S, Christophides GK, Cantera R, Charles B, Han YS, Meister S, Dimopoulos G, Kafatos FC, Barillas-Mury C (2003). The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proc. Natl. Acad. Sci. 100(24): 14139-14144.
46. Lines JD, Nassor NS (1991). DDT resistance in Anopheles gambiae declines with mosquito age. Med. Vet. Entomol. 5: 261-265.
47. Lipke H, Chalkley J (1962). Glutathione, oxidized and reduced, in some dipterans treated with 1,1,1-trichloro-2,2-di-(p-chlorophenyl)ethane. Biochem. J. 85: 104-109.
48. Lipke H, Chalkley J (1964). The conversion of DDT to DDE by some Anophelines. Bull. WHO 30: 57-56.
49. Listowsky I, Abramovitz M, Homma H, Niitsu Y (1988). Intracellular binding and transport of hormones and xenobiotics by glutathione S- transferase. Drug Metab. Rev. 19: 305-318.
50. Lumjuan N (2005). Characterisation of Aedes aegypti glutathione S- transferase enzyme family. Ph.D. Thesis, Liverpool School of Tropical Medicine, Liverpool, UK.
51. Lumjuan N, McCarrol L, Prapanthadara L, Hemingway J, Ranson H (2005). Elevated activity of an Epsilon class glutathione transferase confers DDT resistance in the dengue vector, Aedes aegypti. Insect Biochem. Mol. Biol. 35: 861-871.
52. Mannervik B, Danielson UH (1988). Glutathione transferases--structure and catalytic activity. CRC Crit. Rev. Biochem. 23:283-337.
53. Marinotti O, Nguyen Q K, Calvo E, James AA, Ribeiro JMC (2005). Microarray analysis of genes showing variable expression following abloodmeal in Anopheles gambiae. Insect. Mol. Biol. 14: 365-374.
54. McCarroll L, Hemingway J (2002). Can insecticide resistance status affect parasite transmision in mosquitoes? Insect Biochem. Mol. Biol. 35: 1345-1351.
55. Morel F, Rauch C, Petit E, Piton A, Theret N, Coles B, Guillouzo A (2004). Gene and protein characterization of the human glutathione S-transferase kappa and evidence for a peroxisomal localization. J. Biol. Chem. 279: 16246-16253.
56. Oakley AJ, Harnnoi T, Udomsinprasert R, Jirajaroenrat K, Ketterman AJ, Wilce MCJ (2001). The crystal structures of glutathione S- transferases isozymes 1-3 and 1-4 from Anopheles dirus species B. Protein Sci. 10: 2176-2185.
57. Oppenoorth FJ, Van der Pas LJT, Houx NWH (1979). Glutathione S- transferases and hydrolytic activity in a tetrachlorvinphos-resistant strain of housefly and their influence on resistance. Pestic. Biochem. Physiol. 11: 176-188.
58. Ortelli F, Rossiter LC, Vontas J, Ranson H, Hemingway J (2003). Heterologous expression of four glutathione transferase genes genetically linked to a major insecticide-resistance locus from the malaria vector Anopheles gambiae. Biochem. J. 373: 957-963.
59. Parkes TL, Hilliker AJ, Phillips JP (1993). Genetic and biochemical analysis of glutathione S-transferases in the oxygen defence system of Drosophila melanogaster. Genome 36: 1007-1014.
60. Pearson WR (2005). Phylogenies of glutathione transferase families. Methods Enzymol. 401: 186-204.
61. Pemble SE, Wardle AF, Taylor JB (1996). Glutathione S-transferase class Kappa: characterization by the cloning of rat mitochondrial GST and identification of a human homologue. Biochem. J. 319: 749-754.
62. Penilla RP, Rodriguez AD, Hemingway J, Torres JL, Solis F. Rodriguez MH (2006). Changes in glutathione S-transferase levels in DDT resistant natural Mexican populations of Anopheles albimanus under different insecticide resistance management strategies. Pestic. Biochem. Physiol. 86: 63-71.
63. Pickett CB, Lu AY (1989). Glutathione S-transferases: gene structure, regulation, and biological function. Annu. Rev. Biochem. 58:743-764.
64. Pongjaroenkit S, Jirajaroenrat K, Boonchauy C, Chanama U, Leetachewa S, Prapanthadara L, Ketterman AJ (2001). Genomic organization and putative promoters of highly conserved glutathione S-transferases originating by alternative splicing in Anopheles dirus. Insect Biochem. Mol. Biol. 31:75-85.
65. Prapanthadara L, Hemingway J, Ketterman AJ (1993). Partial purification and characterization of glutathione S-transferases involved in DDT resistance from the mosquito Anopheles gambiae. Pestic. Biochem. Physiol. 47: 119-133.
66. Prapanthadara L, Hemingway J, Ketterman AJ (1995). DDT-resistance in Anopheles gambiae Giles from Zanzibar Tanzania, based on increased DDT-dehydrochlorinase activity of glutathione S transferases. Bull. Entomol. Res. 85: 267-274.
67. Prapanthadara L, Koottathep S, Promtet N, Hemingway J, Ketterman AJ (1996). Purification and characterization of a major glutathione S- tranferase from the mosquito Anopheles dirus (species B). Insect Biochem. Mol. Biol. 26: 277-285.
68. Prapanthadara L, Ranson H, Somboon P, Hemingway J (1998). Cloning, expression and characterization of an insect class I glutathione S-transferase from Anopheles dirus species B. Insect Biochem. Mol. Biol. 28: 321-329.
69. Prapanthadara L, Koottathep S, Promtet N, Suwonkerd W, Ketterman AJ, Somboon P (2000a). Correlation of glutathione S transferase and DDT dehydrochlorinase activities with DDT susceptibility in Anopheles and Culex mosquitos from northern Thailand. Southeast Asian J. Trop. Med. Public. Health. 31: 111-118.
70. Prapanthadara L, Promtet N, Koottathep S, Somboon P, Ketterman AJ (2000b). Isoenzymes of glutathione S-transferase from the mosquito Anopheles dirus species B: the purification, partial characterization and interaction with various insecticides. Insect Biochem. Mol. Biol. 30: 395-403.
71. Prapanthadara L, Promtet N, Koottathep S, Somboon P, Suwonkerd W, McCarroll L, Hemingway J (2002). Mechanisms of DDT and permethrin resistance in Aedes aegypti from Chiang Mai, Thailand. Dengue Bulletin 26: 185-189.
72. Ranson H, Cornel AJ, Fournier D, Vaughan A, Collins FH, Hemingway J (1997a). Cloning and localization of a glutathione S-transferase class I gene from Anopheles gambiae. J. Biol. Chem. 272: 5464-568.
73. Ranson H, Prapanthadara L, Hemingway J (1997b). Cloning and characterisation of two glutathione S-transferases from a DDT resistant strain of Anopheles gambiae. Biochem. J. 324: 97-102.
74. Ranson H, Collins FH, Hemingway J (1998). The role of alternative mRNA splicing in generating heterogeneity within the Anopheles gambiae class I glutathione S-transferase family. Proc. Natl. Acad. Sci. USA 95: 14284-14289.
75. Ranson H, Jensen B, Wang X, Hemingway J, Collins FH (2000). Genetic mapping of two loci affecting DDT resistance in the malaria vector Anopheles gambiae. Insect. Mol. Biol. 9: 499-507.
76. Ranson H, Rossiter L, Ortelli F, Jensen B, Wang X, Roth CW, Collins FH, Hemingway J (2001). Identification of a novel class of insect glutathione S-transferases involved in DDT resistance in the malaria vector, Anopheles gambiae. Biochem. J. 359: 295-304.
77. Ranson H, Claudianos C, Ortelli F, Abgrall C, Hemingway J, Sharakhova MV, Unger MF, Collins FH, Feyereisen R (2002). Evolution of supergene families associated with insecticide resistance. Science 298: 179-181.
78. Ranson H, Hemingway J (2005). Mosquito glutathione transferases. Review. Methods Enzymol. 401: 226-241.
79. Sawicki R, Singh SP, Mondal AK, Benes H, Zimniak P (2003). Cloning, expression and biochemical characterization of one Epsilon-class (GST-3) and ten Delta-class (GST-1) glutathione S-transferases from Drosophila melanogaster, and identification of additional nine members of the Epsilon class. Biochem. J. 370: 661-669.
80. Sheehan D, Meade G, Foley VM, Dowd CA (2001). Review article, Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem. J. 360: 1-16.
81. Singh SP, Coronella JA, Benes H, Cochrane BJ, Zimniak P (2001). Catalytic function of Drosophila melanogaster glutathione S- transferase DmGSTS1-1 (GST-2) in conjugation of lipid peroxidation end products. Eur. J. Biochem. 268: 2912-2923.
82. Tanaka K, Nakajima M, Kurihara N. (1981). The mechanism of resistance to lindane and hexadeuterated lindane in the third yumenoshima strain of house fly. Pestic. Biochem. Physiol. 16: 149-157.
83. Tang AH, Tu CP (1994). Biochemical caracterization of Drossophila glutathione S-transferase D1 and D2. J. Biol. Chem. 269: 27876-27884.
84. Tang AH, Tu CP (1995). Pentobarbital-induced changes in Drosophila glutathione S-transferase D21 mRNA stability. J. Biol. Chem. 270: 13819-13825.
85. Toung Y-PS, Hsieh T-S, Tu C-PD (1990). Drosophila glutathione S- transferase 1-1 shares a region of sequence homology with the maize glutathione S-transferase III. Proc. Natl. Acad. Sci. USA 87: 31-35.
86. Tu C-PD, Akgul B (2005). Drosophila glutathione S-transferases. Methods Enzymol. 401: 204-226.
87. Udomsinprasert R, Ketterman AJ (2002). Expression and characterization of a novel class of glutathione S-transferase from Anopheles dirus. Insect Biochem. Mol. Biol. 32: 425-433.
88. Udomsinprasert R, Pongjaroenkit S, Wongsantichon J, Oakley AJ, Prapanthadara L, Wilce MCJ, Ketterman AJ (2005). Identification, characterization and structure of a new Delta class glutathione transferase isoenzyme. Biochem. J. 388: 763-771.
89. Ugaki M, Shono T, Fukami J (1985). Metabolism of fenitrothion by organophosphorus-resistant and susceptible house flies, Musca domestica L. Pestic. Biochem. Physiol. 23: 33-40.
90. Vontas JG, Small GJ, Hemingway J (2001). Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochem. J. 357: 65-72.
91. Vontas JG, Small GJ, Nikou DC, Ranson H, Hemingway J (2002). Purification, molecular cloning and heterologous expression of a glutathione S-transferase involved in insecticide resistance from the rice brown planthopper, Nilaparvata lugens. Biochem. J. 362: 329-337.
92. Vontas J, Blass C, Koutsos AC, David JP, Kafatos FC, Louis C, Hemingway J, Christophides GK, Ranson H (2005). Gene expression in insecticide resistant and susceptible Anopheles gambiae strains constitutively or after insecticide exposure Insect Mol. Biol. 14(5): 509-521.
93. Wang J, McCommas S, Syvanen M (1991). Molecular cloning of a glutathione S-transferase overproduced in an insecticide resistant strain of the house fly (Musca domestica). Mol. Gen Genet. 227: 260-266.
94. Wei SH, Clark AG, Syvanen M (2001). Identification and cloning of a key insecticide-metabolizing glutathione S-transferase (MdGST-6A) from a hyper insecticide-resistant strain of the house-fly Musca domestica. Insect Biochem. Mol. Biol. 31: 1145-1153.
95. Wongsantichon J, Harnnoi T, Ketterman AJ (2003). A sensitive core region in the structure of glutathione S-tranferase. Biochem. J. 373:759-765.
96. Xu Q, Liu H, Zhang L, Liu N (2005). Resistance in the mosquito, Culex quinquefasciatus, and possible mechanisms for resistance. Pest. Manag. Sci. 61(11): 1096-1102.
97. Yang Y, Cheng J-Z, Singhal SS, Saini M, Pandya U, Awasthi S (2001). Role of glutathione S-transferases in protection against lipid peroxidation. J. Biol. Chem. 276(22): 19220-19230.
98. Yu SJ (1996). Insect glutathione S-transferases. Zool. Stud. 35(1): 9-19.
99. Zou S, Meadows S, Sharp L, Jan LY, Jan YN (2000). Genome-wide study of aging and oxidative stress response in Drosophila melanogaster. Proc. Natl. Acad. Sci. 97: 13726-13731.