Redox Metabolism During Tropical Diapause in a Lepidoptera Larva

  • Daniel Carneiro Moreira
  • Débora Pires Paula
  • Marcelo Hermes-Lima
Chapter

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.

Keywords

Total Glutathione G6PDH Activity Metabolic Depression Redox Metabolism Hypometabolic State 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

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.

References

  1. 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 16:33–42CrossRefGoogle Scholar
  2. 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 154:172–179Google Scholar
  3. Barbehenn RV (2002) Gut-based antioxidant enzymes in a polyphagous and a graminivorous grasshopper. J Chem Ecol 28:1329–1347PubMedCrossRefGoogle Scholar
  4. 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 37:1113–1118PubMedCrossRefGoogle Scholar
  5. Barnhart MC, McMahon BR (1987) Discontinuous carbon dioxide release and metabolic depression in dormant land snails. J Exp Biol 128:123–138Google Scholar
  6. 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 209–229Google Scholar
  7. Bickler PE, Buck LT (2007) Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69:145–170PubMedCrossRefGoogle Scholar
  8. Boiça AL Jr, Vendramin JD (1993) Infestação de girassol pela lagarta Chlosyne lacinia saundersii em duas épocas de cultivo. Sci Agric 50:244–253CrossRefGoogle Scholar
  9. 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 72:248–254PubMedCrossRefGoogle Scholar
  10. Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310PubMedCrossRefGoogle Scholar
  11. Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181PubMedGoogle Scholar
  12. Cox AG, Winterbourn CC, Hampton MB (2010) Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochem J 425:313–325CrossRefGoogle Scholar
  13. Crozier AJG (1979) Diel oxygen uptake rhythms in diapausing pupae of Pieris brassicae and Papilio machaon. J Insect Physiol 25:647–652CrossRefGoogle Scholar
  14. Dalle-Donne I, Rossi R, Giustarini D, Colombo R, Milzani A (2007) S-glutathionylation in protein redox regulation. Free Radic Biol Med 43:883–898PubMedCrossRefGoogle Scholar
  15. Denlinger DL (1979) Pupal diapause in tropical flesh flies: environmental and endocrine regulation, metabolic rate and genetic selection. Biol Bull 156:31–46CrossRefGoogle Scholar
  16. Denlinger DL (1986) Dormancy in tropical insects. Annu Rev Entomol 31:239–264PubMedCrossRefGoogle Scholar
  17. Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122PubMedCrossRefGoogle Scholar
  18. Droge W (2001) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95Google Scholar
  19. Drummond III BA, Bush GL, Emmel TC (1970) The biology and laboratory culture of Chlosyne lacinia Geyer (Nymphalidae). J Lep Soc 24:135–142Google Scholar
  20. 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:e9574PubMedCrossRefGoogle Scholar
  21. Felton GW, Summers CB (1995) Antioxidant systems in insects. Arch Insect Biochem Physiol 29:187–197PubMedCrossRefGoogle Scholar
  22. 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 29:779–793PubMedCrossRefGoogle Scholar
  23. 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 47–61Google Scholar
  24. 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 83:733–752PubMedCrossRefGoogle Scholar
  25. Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212PubMedCrossRefGoogle Scholar
  26. 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 36:1–10CrossRefGoogle Scholar
  27. Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev Camb Philos Soc 74:1–40PubMedCrossRefGoogle Scholar
  28. Hahn DA, Denlinger DL (2011) Energetics of insect diapause. Annu Rev Entomol 56:103–121PubMedCrossRefGoogle Scholar
  29. Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine. University Press, OxfordGoogle Scholar
  30. 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 319–368Google Scholar
  31. Hermes-Lima M, Storey KB (1995) Antioxidant defenses and metabolic depression in a pulmonate land snail. Am J Physiol 268:R1386–R1393PubMedGoogle Scholar
  32. Hermes-Lima M, Zenteno-Savin T (2002) Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comp Biochem Physiol C 133:537–556CrossRefGoogle Scholar
  33. 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 37:1015–1021PubMedCrossRefGoogle Scholar
  34. 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 155:272–280PubMedCrossRefGoogle Scholar
  35. Joanisse DR, Storey KB (1998) Oxidative stress and antioxidants in stress and recovery of cold-hardy insects. Insect Biochem Mol Biol 28:23–30CrossRefGoogle Scholar
  36. Jones DP (2006) Redefining oxidative stress. Antioxid Redox Signal 8:1865–1879PubMedCrossRefGoogle Scholar
  37. 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 55:79–89PubMedCrossRefGoogle Scholar
  38. 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 64:111–119PubMedCrossRefGoogle Scholar
  39. 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 140:579–587PubMedCrossRefGoogle Scholar
  40. 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 106:451–454Google Scholar
  41. Kostal V (2006) Eco-physiological phases of insect diapause. J Insect Physiol 52:113–127PubMedCrossRefGoogle Scholar
  42. 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 44:165–173PubMedCrossRefGoogle Scholar
  43. 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 50:303–313PubMedCrossRefGoogle Scholar
  44. Krishnan N, Kodrik D (2006) Antioxidant enzymes in Spodoptera littoralis (Boisduval): are they enhanced to protect gut tissues during oxidative stress. J Insect Physiol 52:11–20PubMedCrossRefGoogle Scholar
  45. 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 50:191–197CrossRefGoogle Scholar
  46. 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 284:29454–29461PubMedCrossRefGoogle Scholar
  47. MacRae TH (2010) Gene expression, metabolic regulation and stress tolerance during diapause. Cell Mol Life Sci 67:2405–2424PubMedCrossRefGoogle Scholar
  48. 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 36:173–179CrossRefGoogle Scholar
  49. 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 177:753–763PubMedCrossRefGoogle Scholar
  50. Pamplona R, Costantini D (2011) Molecular and structural antioxidant defenses against oxidative stress in animals. Am J Physiol Regul Integr Comp Physiol 301:R843–R863PubMedCrossRefGoogle Scholar
  51. Pullin AS, Wolda H (1993) Glycerol and glucose accumulation during diapause in a tropical beetle. Physiol Entomol 18:75–78CrossRefGoogle Scholar
  52. 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 107:14909–14914PubMedCrossRefGoogle Scholar
  53. Ramos-Vasconcelos GR, Hermes-Lima M (2003) Hypometabolism, antioxidant defenses and free radical metabolism in the pulmonate land snail Helix aspersa. J Exp Biol 206:675–685PubMedCrossRefGoogle Scholar
  54. Scott JA (1986) The butterflies of North America: a natural history and field guide. University Press, StanfordGoogle Scholar
  55. Sies H (1993) Strategies of antioxidant defense. Eur J Biochem 215:213–219PubMedCrossRefGoogle Scholar
  56. 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 57:628–634PubMedCrossRefGoogle Scholar
  57. 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 77:72–80PubMedCrossRefGoogle Scholar
  58. Srere PA (1969) Citrate synthase. Methods Enzymol 13:3–11CrossRefGoogle Scholar
  59. 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 101:459–466Google Scholar
  60. Storey KB (2002) Life in the slow lane: molecular mechanisms of estivation. Comp Biochem Physiol A 133:733–754CrossRefGoogle Scholar
  61. 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 21:157–164CrossRefGoogle Scholar
  62. Storey KB, Storey JM (2007) Tribute to P. L. Lutz: putting life on ‘pause’—molecular regulation of hypometabolism. J Exp Biol 210:1700–1714PubMedCrossRefGoogle Scholar
  63. 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 29:199–209PubMedCrossRefGoogle Scholar
  64. Zhao L, Shi L (2009) Metabolism of hydrogen peroxide in univoltine and polyvoltine strains of silkworm (Bombyx mori). Comp Biochem Physiol B 152:339–345PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Daniel Carneiro Moreira
    • 1
  • Débora Pires Paula
    • 2
  • Marcelo Hermes-Lima
    • 1
  1. 1.Laboratório de Radicais Livres, Departamento de Biologia CelularUniversidade de BrasíliaBrasíliaBrazil
  2. 2.Laboratório de Ecologia MolecularEmbrapa Recursos Genéticos e BiotecnologiaBrasíliaBrazil

Personalised recommendations