Superoxide dismutase activities in the midgut of Helicoverpa armigera larvae: identification and biochemical properties of a manganese superoxide dismutase

References

• Felton GW, Summers CB. Antioxidant systems in insects. Arch Insect Biochem Physiol. 1995;29:187–197.
   PubMed Web of Science ®Google Scholar
• Aucoin RR, Philogene BJR, Arnason JT. Antioxidant enzymes as biochemical defenses against phototoxin-induced oxidative stress in three species of herbivorous Lepidoptera. Arch Insect Biochem Physiol. 1991;16:139–152.
   Web of Science ®Google Scholar
• Wang Y, Oberley LW, Murhammer DW. Antioxidant defense systems of two Lepidopteran insect cell lines. Free Radic Biol Med. 2001;30:1254–1262.
   PubMed Web of Science ®Google Scholar
• Weirich GF, Collins AM, Williams VP. Antioxidant enzymes in the honey bee, Apis mellifera. Apidologie. 2002;33:3–14.
   Web of Science ®Google Scholar
• Dubovskiy IM, Martemyanov VV, Vorontsova YL, Rantala MJ, Gryzanova EV, Glupov VV. Effect of bacterial infection on antioxidant activity and lipid peroxidation in the midgut of Galleria mellonella L. larvae (Lepidoptera, Pyralidae). Comp Biochem Physiol C. 2008;148:1–5.
   PubMed Web of Science ®Google Scholar
• Gujar GT, Kumar A, Kalia V, Chandrashekhar K. Spatial and temporal variation in susceptibility of American bollworm, Helicoverpa armigera (Hubner) to Bacillus thuringiensis var. Karstakin in India. Curr Sci. 2000;78:995–1001.
   Web of Science ®Google Scholar
• Rajapakse CNK, Walter GH. Polyphagy and primary host plants: oviposition preference versus larval performance in the lepidopteran pest Helicoverpa armigera. Arthropod Plant Interact. 2007;1:17–26.
   Web of Science ®Google Scholar
• Adamski Z, Ziemnicki K, Fila K, Zikic RV, Stajn A. Effects of long-term exposure to fenitrothion on Spodoptera exigua and Tenebrio molitor larval development and antioxidant enzyme activity. Biol Lett. 2003;40:43–52.
   Google Scholar
• Bagchi D, Bagchi M, Hassoun EA, Stohs SJ. In vitro and in vivo generation of reactive oxygen species, DNA damage and lactate dehydrogenase leakage by selected pesticides. Toxicology. 1995;104:129–140.
   PubMed Web of Science ®Google Scholar
• Vontas JG, Small GJ, Hemingway J. Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochem J. 2001;357:65–72.
   PubMed Web of Science ®Google Scholar
• Kannan K, Jain SK. Oxygen radical generation and endosulfan toxicity in Jurkat T-cells. Mol Cell Biochem. 2003;247:1–7.
   PubMed Web of Science ®Google Scholar
• Pritsos CA, Ahmad S, Elliott AJ, Pardini RS. Antioxidant enzyme level response to prooxidant allelochemicals in larvae of the southern armyworm moth, Spodoptera eridania. Free Radic Res Commun. 1990;9:127–133.
   PubMed Web of Science ®Google Scholar
• Ahmad S, Pardini RS. Mechanisms for regulating oxygen toxicity in phytophagous insects. Free Radic Biol Med. 1990;8:401–413.
   PubMed Web of Science ®Google Scholar
• Krishnan N, Kodrik D. Antioxidant enzymes in Spodoptera littoralis (Boisduval): are they enhanced to protect gut tissues during oxidative stress? J Insect Physiol. 2006;52:11–20.
   Google Scholar
• Datkhile KD, Mukhopadhyaya R, Dongre TK, Nath BB. Increased level of superoxide dismutase (SOD) activity in larvae of Chironomus ramosus (Diptera: Chironomidae) subjected to ionizing radiation. Comp Biochem Physiol C. 2009;149:500–506.
   PubMed Web of Science ®Google Scholar
• Yamamoto K, Zhang P, He N, et al. Molecular and biochemical characterization of manganese-containing superoxide dismutase from the silkworm, Bombyx mori. Comp Biochem Physiol B. 2005;142:403–409.
   Web of Science ®Google Scholar
• Choi YS, Lee KS, Yoon HJ, Kim I, Sohn HD, Jin BR. Bombus ignitus Cu, Zn superoxide dismutase (SOD1): cDNA cloning, gene structure, and up-regulation in response to paraquat, temperature stress, or lipopolysaccharide stimulation. Comp Biochem Physiol B. 2006;144:365–371.
   Web of Science ®Google Scholar
• Wang Y, Wang L, Zhu Z, Mab W, Lei C. The molecular characterization of antioxidant enzyme genes in Helicoverpa armigera adults and their involvement in response to ultraviolet-A stress. J Insect Physiol. 2012;58:1250–1258.
   PubMed Web of Science ®Google Scholar
• Nardini L, Christian RN, Coetzer N, Koekemoer LL. DDT and pyrethroid resistance in Anopheles arabiensis from South Africa. Parasit Vectors. 2013;6:229.
   Web of Science ®Google Scholar
• Mamidala P, Wijeratne AJ, Wijeratne S, et al. RNA-Seq and molecular docking reveal multi-level pesticide resistance in the bed bug. BMC Genomics. 2012;13:6.
   Web of Science ®Google Scholar
• Nagarkatti S, Prakash A. Rearing Helicoverpa armigera (Hubner) on an artificial diet, Volume 17; 1974. In: Technical Bulletin, Commonwealth Institute of Biological Control, Bangalore.
   Google Scholar
• Lomate PR, Jadhav BR, Giri AP, Hivrale VK. Alterations in the Helicoverpa armigera midgut digestive physiology after ingestion of pigeon pea inducible leucine aminopeptidase. PLoS One. 2013;8(9):e74889.
   Web of Science ®Google Scholar
• Pauchet A, Muck A, Svatos A, Heckel DG, Prelss S. Mapping the larval midgut lumen proteome of Helicoverpa armigera, a generalist herbivorous insect. J Proteome Res. 2007;7:1629–1639.
   Web of Science ®Google Scholar
• Lomate PR, Hivrale VK. Effect of Bacillus thuringiensis (Bt) Cry1Ac toxin and protease inhibitor on growth and development of Helicoverpa armigera (Hübner). Pest Biochem Physiol. 2013;105:77–83.
   Web of Science ®Google Scholar
• Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193:453–464.
   Web of Science ®Google Scholar
• Davis BJ. Disc electrophoresis II: methods and application to human serum. Ann N Y Acad Sci. 1964;12:404–427.
   Google Scholar
• Chen C, Pan S. Assay of superoxide dismutase activity by combining electrophoresis and densitometry. Bot Bull Acad Sin. 1996;37:107–111.
   Google Scholar
• Imanari T, Hirota M, Miyazaki M, Hayakawa K, Tamura Z. Improved assay method for superoxide dismutase. Igaku no ayumi. 1997;101:496–497.
   Google Scholar
• Hodgson EK, Fridovich I. The interaction of bovine erythrocyte superoxide dismutase with hydrogen peroxide: inactivation of the enzyme. Biochemistry. 1975;14:5294–5299.
   Web of Science ®Google Scholar
• Bannister JV, Bannister WH, Rotilio G. Aspects of the structure, function, and applications of superoxide dismutase. CRC Crit Rev Biochem. 1987;22:111–180.
   PubMed Web of Science ®Google Scholar
• Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–685.
   PubMed Web of Science ®Google Scholar
• Dawkar VV, Chikte YR, Lomate PR, Dholakia BB, Gupta VS, Giri AP. Molecular insights in to defense mechanisms of Lepidopteron insect pests against toxicants. J Proteome Res. 2013;12:4727–4737.
   Web of Science ®Google Scholar
• de la Paz Celorio-Mancera M, Wheat CW, Vogel H, Söderlind L, Janz N, Nylin S. Mechanisms of macroevolution: polyphagous plasticity in butterfly larvae revealed by RNA-Seq. Mol Ecol. 2013;22:4884–4895.
   Web of Science ®Google Scholar
• Fridovich I. Superoxide dismutase. Adv Enzymol. 1986;58:61–97.
   PubMedGoogle Scholar
• Lee YM, Ayala FJ, Misra HP. Purification and properties of superoxide dismutase from Drosophila melanogaster. J Biol Chem. 1981;256:8506–8509.
   PubMed Web of Science ®Google Scholar
• Asada K, Kanematsu S, Okada S, Hayakawa T. Phylogenetic distribution of three types of superoxide dismutase in organisms and in cell organelles. In: Bannister JV, Hill HAO, editors. Chemical and Biochemical Aspects of Superoxide and Superoxide Dismutase. Vol IIA. New York: Elsevier; 1980:136.
   Google Scholar
• Duttaroy A, Meidinger R, Kirby K, Carmichael S, Hilliker A, Phillips J. A manganese superoxide dismutase-encoding cDNA from Drosophila melanogaster. Gene. 1994;143:223–225.
   Google Scholar
• Gao XL, Li JM, Wang YL, et al. Cloning, expression and characterization of mitochondrial manganese superoxide dismutase from the whitefly, Bemisia tabaci. Int J Mol Sci. 2013;14:871–887.
   Web of Science ®Google Scholar
• Li JM, Su YL, Gao XL, He J, Liu SS, Wang XW. Molecular characterization and oxidative stress response of an intracellular Cu/Zn superoxide dismutase (CuZnSOD) of the whitefly, Bemisia tabaci. Arch Insect Biochem. 2011;77:118–133.
   Web of Science ®Google Scholar
• Appel HM.. The chewing herbivore gut lumen: physicochemical conditions and their impact on plant nutrients, allelochemicals and insect pathogens. In: Bernays EA, editor. Insect-Plant Interactions. Vol V. Boca Raton, FL: CRC Press; 1994:209–223.
   Google Scholar
• Rosen GM, Britigan BE, Halpern HJ, Pou S. Free Radicals: Biology and Detection by Spin Trapping. Oxford: Oxford University Press; 1999.
   Google Scholar