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Redox Metabolism During Tropical Diapause in a Lepidoptera Larva

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Living in a Seasonal World

Abstract

Many studies on metabolic rate depression and redox metabolism exist in the literature; however, virtually none focuses on tropical insect diapause. Thus, our aim was to evaluate peculiarities of the metabolism of reactive oxygen species (ROS) between diapausing and non-diapausing insects in a tropical region. The lepidopteran Chlosyne lacinia undergoes diapause as larva at the third instar prior to the dry season in middle-west Brazil. We measured the activity of metabolic and anti-oxidant enzymes at day 20 of diapause. The activity of citrate synthase decreased by 81% in whole-body extracts as compared with larvae sampled before diapause entry. Moreover, total-glutathione content and lipid peroxidation dropped significantly (by 82 and 24%, respectively) in diapausing insects. On the other hand, the activities of catalase and glucose 6-phosphate dehydrogenase (G6PDH) were unchanged. These results indicate a diminished oxidative metabolism and suggest important roles for catalase and G6PDH in ROS control in diapause and, possibly, during arousal. The diminished glutathione levels could be related to its depletion by glutathione-dependent systems or by its diminished biosynthesis.

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References

  • Augustyniak M, Babczynska A, Augustyniak M (2009) Does the grasshopper Chorthippus brunneus adapt to metal polluted habitats? A study of glutathione-dependent enzymes in grasshopper nymphs. Insect Sci 16:33–42

    Article  CAS  Google Scholar 

  • Augustyniak M, Babczynska A, Augustyniak M (2011) Oxidative stress in newly-hatched Chorthippus brunneus—the effects of zinc treatment during diapause, depending on the female’s age and its origins. Comp Biochem Physiol C 154:172–179

    CAS  Google Scholar 

  • Barbehenn RV (2002) Gut-based antioxidant enzymes in a polyphagous and a graminivorous grasshopper. J Chem Ecol 28:1329–1347

    Article  PubMed  CAS  Google Scholar 

  • Barbehenn RV, Maben RE, Knoester JJ (2008) Linking phenolic oxidation in the midgut lumen with oxidative stress in the midgut tissues of a tree-feeding caterpillar Malacosoma disstria (Lepidoptera: Lasiocampidae). Environ Entomol 37:1113–1118

    Article  PubMed  Google Scholar 

  • Barnhart MC, McMahon BR (1987) Discontinuous carbon dioxide release and metabolic depression in dormant land snails. J Exp Biol 128:123–138

    Google Scholar 

  • Benoit JB (2010) Water management by dormant insects: comparisons between dehydration resistance during summer aestivation and winter diapause. In: Navas CA, Carvalho JE (eds) Aestivation: molecular and physiological aspects. Progress in molecular and subcellular biology, vol 49. Springer, Heidelberg, pp 209–229

    Google Scholar 

  • Bickler PE, Buck LT (2007) Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69:145–170

    Article  PubMed  CAS  Google Scholar 

  • Boiça AL Jr, Vendramin JD (1993) Infestação de girassol pela lagarta Chlosyne lacinia saundersii em duas épocas de cultivo. Sci Agric 50:244–253

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    Article  PubMed  CAS  Google Scholar 

  • Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181

    PubMed  CAS  Google Scholar 

  • Cox AG, Winterbourn CC, Hampton MB (2010) Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochem J 425:313–325

    Article  CAS  Google Scholar 

  • Crozier AJG (1979) Diel oxygen uptake rhythms in diapausing pupae of Pieris brassicae and Papilio machaon. J Insect Physiol 25:647–652

    Article  CAS  Google Scholar 

  • Dalle-Donne I, Rossi R, Giustarini D, Colombo R, Milzani A (2007) S-glutathionylation in protein redox regulation. Free Radic Biol Med 43:883–898

    Article  PubMed  CAS  Google Scholar 

  • Denlinger DL (1979) Pupal diapause in tropical flesh flies: environmental and endocrine regulation, metabolic rate and genetic selection. Biol Bull 156:31–46

    Article  Google Scholar 

  • Denlinger DL (1986) Dormancy in tropical insects. Annu Rev Entomol 31:239–264

    Article  PubMed  CAS  Google Scholar 

  • Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122

    Article  PubMed  CAS  Google Scholar 

  • Droge W (2001) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95

    Google Scholar 

  • Drummond III BA, Bush GL, Emmel TC (1970) The biology and laboratory culture of Chlosyne lacinia Geyer (Nymphalidae). J Lep Soc 24:135–142

    Google Scholar 

  • Emerson KJ, Bradshaw WE, Holzapfel CM (2010) Microarrays reveal early transcriptional events during the termination of larval diapause in natural populations of the mosquito, Wyeomyia smithii. PLoS One 5:e9574

    Article  PubMed  Google Scholar 

  • Felton GW, Summers CB (1995) Antioxidant systems in insects. Arch Insect Biochem Physiol 29:187–197

    Article  PubMed  CAS  Google Scholar 

  • Feng QL, Davey KG, Pang ASD, Primavera M, Ladd TR, Zheng SC, Sohi SS, Retnakaran A, Palli SR (1999) Glutathione S-transferase from the spruce budworm, Choristoneura fumiferana: identification, characterization, localization, cDNA cloning, and expression. Insect Biochem Mol Biol 29:779–793

    Article  PubMed  CAS  Google Scholar 

  • Ferreira-Cravo M, Welker AF, Hermes-Lima M (2010) The connection between oxidative stress and estivation in gastropods and anurans. In: Navas CA, Carvalho JE (eds) Aestivation: molecular and physiological aspects. Progress in molecular and subcellular biology, vol 49. Springer, Heidelberg, pp 47–61

    Google Scholar 

  • Gorr TA, Wichmann D, Hu J, Hermes-Lima M, Welker AF, Terwilliger N, Wren JF, Viney M, Morris S, Nilsson GE, Deten A, Soliz J, Gassmann M (2010) Hypoxia tolerance in animals: biology and application. Physiol Biochem Zool 83:733–752

    Article  PubMed  CAS  Google Scholar 

  • Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212

    Article  PubMed  CAS  Google Scholar 

  • Grubor-Lajsic G, Block W, Telesmanic M, Jovanovic A, Stevanovic D, Baca F (1997) Effect of cold acclimation on the antioxidant defense system of two larval Lepidoptera (Noctuidae). Arch Insect Biochem Physiol 36:1–10

    Article  CAS  Google Scholar 

  • Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev Camb Philos Soc 74:1–40

    Article  PubMed  CAS  Google Scholar 

  • Hahn DA, Denlinger DL (2011) Energetics of insect diapause. Annu Rev Entomol 56:103–121

    Article  PubMed  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine. University Press, Oxford

    Google Scholar 

  • Hermes-Lima M (2004) Oxygen in biology and biochemistry: role of free radicals. In: Storey KB (ed) Functional metabolism: regulation and adaptation. Wiley, New York, pp 319–368

    Google Scholar 

  • Hermes-Lima M, Storey KB (1995) Antioxidant defenses and metabolic depression in a pulmonate land snail. Am J Physiol 268:R1386–R1393

    PubMed  CAS  Google Scholar 

  • Hermes-Lima M, Zenteno-Savin T (2002) Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comp Biochem Physiol C 133:537–556

    Article  Google Scholar 

  • Houthoofd K, Braeckman BP, Lenaerts I, Brys K, Vreese A, Eygen SV, Vanfleteren JR (2002) Ageing is reversed, and metabolism is reset to young levels in recovering dauer larvae of C. elegans. Exp Gerontol 37:1015–1021

    Article  PubMed  CAS  Google Scholar 

  • Hu Z, Lee KS, Choo YM, Yoon HJ, Lee SM, Lee JH, Kim DH, Sohn HD, Jin BR (2010) Molecular cloning and characterization of 1-Cys and 2-Cys peroxiredoxins from the bumblebee Bombus ignites. Comp Biochem Physiol B 155:272–280

    Article  PubMed  Google Scholar 

  • Joanisse DR, Storey KB (1998) Oxidative stress and antioxidants in stress and recovery of cold-hardy insects. Insect Biochem Mol Biol 28:23–30

    Article  CAS  Google Scholar 

  • Jones DP (2006) Redefining oxidative stress. Antioxid Redox Signal 8:1865–1879

    Article  PubMed  CAS  Google Scholar 

  • Jovanovic-Galovic A, Blagojevic DP, Grubor-Lajsic G, Worland R, Spasic MB (2004) Role of antioxidant defense during different stages of preadult life cycle in European corn borer (Ostrinia nubilalis, Hubn.): diapause and metamorphosis. Arch Insect Biochem Physiol 55:79–89

    Article  PubMed  CAS  Google Scholar 

  • Jovanovic-Galovic A, Blagojevic DP, Grubor-Lajsic G, Worland MR, Spasic MB (2007) Antioxidant defense in mitochondria during diapause and postdiapause development of European corn borer (Ostrinia nubilalis, Hubn.). Arch Insect Biochem Physiol 64:111–119

    Article  PubMed  CAS  Google Scholar 

  • Kim I, Lee KS, Hwang JS, Ahn MY, Li J, Sohn HD, Jin BR (2005) Molecular cloning and characterization of a peroxiredoxin gene from the mole cricket, Gryllotalpa orientalis. Comp Biochem Physiol B 140:579–587

    Article  PubMed  Google Scholar 

  • Kojic D, Spasojevic I, Mojovic M, Blagojevic D, Worland MR, Grubor-Lajsic G, Spasic MB (2009) Potential role of hydrogen peroxide and melanin in the cold hardiness of Ostrinia nubilalis (Lepidoptera: Pyralidae). Eur J Entomol 106:451–454

    Google Scholar 

  • Kostal V (2006) Eco-physiological phases of insect diapause. J Insect Physiol 52:113–127

    Article  PubMed  CAS  Google Scholar 

  • Kostal V, Sula J, Simek P (1998) Physiology of drought tolerance and cold hardiness of the Mediterranean tiger moth Cymbalophora pudica during summer diapause. J Insect Physiol 44:165–173

    Article  PubMed  CAS  Google Scholar 

  • Kostal V, Tollarova M, Sula J (2004) Adjustments of the enzymatic complement for polyol biosynthesis and accumulation in diapausing cold-acclimated adults of Pyrrhocoris apterus. J Insect Physiol 50:303–313

    Article  PubMed  CAS  Google Scholar 

  • Krishnan N, Kodrik D (2006) Antioxidant enzymes in Spodoptera littoralis (Boisduval): are they enhanced to protect gut tissues during oxidative stress. J Insect Physiol 52:11–20

    Article  PubMed  CAS  Google Scholar 

  • Ku C, Chiang F, Hsin C, Yao Y, Sun C (1994) Glutathione transferase isozymes involved in insecticide resistance of diamondback moth larvae. Pestic Biochem Physiol 50:191–197

    Article  CAS  Google Scholar 

  • Lee K, Iijima-Ando K, Iijima K, Lee W, Lee JH, Yu K, Lee D (2009) JNK/FOXO-mediated neuronal expression of fly homologue of peroxiredoxin II reduces oxidative stress and extends life span. J Biol Chem 284:29454–29461

    Article  PubMed  CAS  Google Scholar 

  • MacRae TH (2010) Gene expression, metabolic regulation and stress tolerance during diapause. Cell Mol Life Sci 67:2405–2424

    Article  PubMed  CAS  Google Scholar 

  • Meng G, Yao JM, Wang L, Zhao L (2011) Variation in glutathione status associated with induction and initiation of diapause in eggs of the bivoltine strain of the silkworm Bombyx mori. Physiol Entomol 36:173–179

    Article  CAS  Google Scholar 

  • Michaud MR, Denlinger DL (2007) Shifts in the carbohydrate, polyol, and amino acid pools during rapid cold-hardening and diapause-associated cold-hardening in flesh flies (Sarcophaga crassipalpis): a metabolomic comparison. J Comp Physiol B 177:753–763

    Article  PubMed  CAS  Google Scholar 

  • Pamplona R, Costantini D (2011) Molecular and structural antioxidant defenses against oxidative stress in animals. Am J Physiol Regul Integr Comp Physiol 301:R843–R863

    Article  PubMed  CAS  Google Scholar 

  • Pullin AS, Wolda H (1993) Glycerol and glucose accumulation during diapause in a tropical beetle. Physiol Entomol 18:75–78

    Article  CAS  Google Scholar 

  • Ragland GJ, Denlinger DL, Hahn DA (2010) Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly. Proc Natl Acad Sci U S A 107:14909–14914

    Article  PubMed  CAS  Google Scholar 

  • Ramos-Vasconcelos GR, Hermes-Lima M (2003) Hypometabolism, antioxidant defenses and free radical metabolism in the pulmonate land snail Helix aspersa. J Exp Biol 206:675–685

    Article  PubMed  CAS  Google Scholar 

  • Scott JA (1986) The butterflies of North America: a natural history and field guide. University Press, Stanford

    Google Scholar 

  • Sies H (1993) Strategies of antioxidant defense. Eur J Biochem 215:213–219

    Article  PubMed  CAS  Google Scholar 

  • Sim C, Denlinger DL (2011) Catalase and superoxide dismutase-2 enhance survival and protect ovaries during overwintering diapause in the mosquito Culex pipiens. J Insect Physiol 57:628–634

    Article  PubMed  CAS  Google Scholar 

  • Sima Y, Yao J, Hou Y, Wang L, Zhao L (2011) Variations of hydrogen peroxide and catalase expression in Bombyx eggs during diapause initiation and termination. Arch Insect Biochem Physiol 77:72–80

    Article  PubMed  CAS  Google Scholar 

  • Srere PA (1969) Citrate synthase. Methods Enzymol 13:3–11

    Article  CAS  Google Scholar 

  • Stanic B, Jovanovic-Galovic A, Blagojevic DP, Grubor-Lajsic G, Worland R, Spasic MB (2004) Cold hardiness in Ostrinia nubilalis (Lepidoptera: Pyralidae): glycerol content, hexose monophosphate shunt activity, and antioxidative defense system. Eur J Entomol 101:459–466

    CAS  Google Scholar 

  • Storey KB (2002) Life in the slow lane: molecular mechanisms of estivation. Comp Biochem Physiol A 133:733–754

    Article  Google Scholar 

  • Storey KB, Storey JM (1991) Glucose-6-phosphate dehydrogenase in cold hardy insects: kinetic properties, freezing stabilization, and control of hexose monophosphate shunt activity. Insect Biochem 21:157–164

    Article  CAS  Google Scholar 

  • Storey KB, Storey JM (2007) Tribute to P. L. Lutz: putting life on ‘pause’—molecular regulation of hypometabolism. J Exp Biol 210:1700–1714

    Article  PubMed  CAS  Google Scholar 

  • Zaman K, MacGill RS, Johnson JE, Ahmad S, Pardini RS (1995) An insect model for assessing oxidative stress related to arsenic toxicity. Arch Insect Biochem Physiol 29:199–209

    Article  PubMed  CAS  Google Scholar 

  • Zhao L, Shi L (2009) Metabolism of hydrogen peroxide in univoltine and polyvoltine strains of silkworm (Bombyx mori). Comp Biochem Physiol B 152:339–345

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants from FINATEC (Brasília, Brazil), Projeto Universal (CNPq, Brazil), and INCT-Processos Redox em Biomedicina (Redoxoma, CNPq). Daniel C. Moreira is a recipient of an undergraduate fellowship from CNPq. We thank graduate student Renata Timbó (UnB) for taking good care of our “sleeping” bugs and Prof. Élida G. Campos (UnB) for revising this manuscript. We also thank an anonymous reviewer for insightful comments. This study is in honor of Cláudio Mário Guimarães da Silva (Rio de Janeiro, Brazil), retired biology teacher and an inspiring mind.

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Correspondence to Marcelo Hermes-Lima .

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Moreira, D.C., Paula, D.P., Hermes-Lima, M. (2012). Redox Metabolism During Tropical Diapause in a Lepidoptera Larva. In: Ruf, T., Bieber, C., Arnold, W., Millesi, E. (eds) Living in a Seasonal World. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-28678-0_35

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