Abstract
The activity of superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GSH-Px), glutathione reductase (GR), and glutathione S-transferase (GST), as well as the concentrations of sulfhydryl (SH) groups and glutathione (GSH) were analyzed in five age classes of the Mediterranean centipede Scolopendra cingulata as follows: embryo, adolescens, maturus junior, maturus, and maturus senior. The data obtained showed the presence of SOD, CAT, GSH-Px, GR, GST, and SH groups in embryos. The transition from embryo to adolescens was accompanied by an increase in the activities of all studied enzymes, in response to the increased production of ROS due to the increased metabolic activity of the centipede associated with growth and development. Our results show that trends in antioxidant enzyme (AOE) activities were not uniform among adult age classes, suggesting that maturus junior, maturus, and maturus senior differentially respond and/or have different susceptibility to ROS. On the other hand, GSH concentration in embryos was undetectable, highest in adolescens and decreased in the latter part of life. Pearson correlation analysis in embryos showed that the activities of the AOEs were strongly and positively correlated with each other but negatively correlated with GSH and SH groups. At later age classes, SOD, CAT, GSH-Px, GR, GSH, and SH groups were no longer significantly correlated with GST. In the discriminant analysis, the variables that separated the age classes were GR, GST, SH groups, and body length. Body length was directly related to the age of individuals, clearly indicating that development/aging affects the regulation of antioxidant defense in this species.
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The datasets generated and analyzed during the current study are available from the corresponding author upon reasonable request.
References
Aceto A, Amicarelli F, Sacchetta P, Dragani B, Bucciarelli T, Masciocco L, Miranda M, Di Ilio C (1994) Developmental aspects of detoxifying enzymes in fish (Salmo iridaeus). Free Radic Res 21(5):285–294. https://doi.org/10.3109/10715769409056581
Arthur W (2011) Evolution: a developmental approach. Wiley-Blackwell, Hoboken
Arun S, Subramanian P (1998) Antioxidant enzymes in freshwater prawn Macrobrachium malcolmsonii during embryonic and larval development. Comp Biochem Physiol B 121(3):273–277. https://doi.org/10.1016/S0305-0491(98)10100-1
Auten RL Jr (2014) Ontogeny of antioxidant systems. In: Dennery PA, Buonocore G, Saugstad OD (eds) Perinatal and prenatal disorders: oxidative stress in applied basic research and clinical practice. Humana Press, Totowa, pp 315–328
Barata C, Navarro JC, Varo I, Riva MC, Arun S, Porte C (2005) Changes in antioxidant enzyme activities, fatty acid composition and lipid peroxidation in Daphnia magna during the aging process. Comp Biochem Physiol B 140(1):81–90. https://doi.org/10.1016/j.cbpc.2004.09.025
Borković SS, Šaponjić JS, Pavlović SZ, Blagojević DP, Milošević SM, Kovačević TB, Radojičić RM, Spasić MB, Žikić RV, Saičić ZS (2005) The activity of antioxidant defence enzymes in the mussel Mytilus galloprovincialis from the Adriatic Sea. Comp Biochem Physiol C 141(4):366–374. https://doi.org/10.1016/j.cbpc.2005.08.001
Buttemer WA, Abele D, Costantini D (2010) From bivalves to birds: oxidative stress and longevity. Funct Ecol 24(5):971–983. https://doi.org/10.1111/j.1365-2435.2010.01740.x
Canesi L, Viarengo A (1997) Age-related differences in glutathione metabolism in mussel tissues (Mytilus edulis L.). Comp Biochem Physiol B 116(2):217–221. https://doi.org/10.1016/S0305-0491(96)00223-4
Carrillo M-C, Kitani K, Minami C, Maruyama W (2007) Age-related changes in antioxidant enzyme activities in the brain and liver of BN/Bi rats: striking differences from those in F344 rats emphasize the need for “public observations” for generating a general theory of aging. Geriatr Gerontol Int 7(3):279–284. https://doi.org/10.1111/j.1447-0594.2007.00404.x
Chainy GBN, Paital B, Dandapat J (2016) An overview of seasonal changes in oxidative stress and antioxidant defence parameters in some invertebrate and vertebrate species. Scientifica 2016:6126570. https://doi.org/10.1155/2016/6126570
Claiborne A (1985) Catalase activity. In: Greenwald RA (ed) CRC handbook of methods for oxygen radical research. CRC Press, Boca Raton, pp 283–284
Corona M, Hughes KA, Weaver DB, Robinson GE (2005) Gene expression patterns associated with queen honey bee longevity. Mech Ageing Dev 126(11):1230–1238. https://doi.org/10.1016/j.mad.2005.07.004
Correia AD, Costa MH, Luis OJ, Livingstone DR (2003) Age-related changes in antioxidant enzyme activities, fatty acid composition and lipid peroxidation in whole body Gammarus locusta (Crustacea: Amphipoda). J Exp Mar Biol Ecol 289(1):83–101. https://doi.org/10.1016/S0022-0981(03)00040-6
Dandapat J, Chainy GBN, Rao KJ (2003) Lipid peroxidation and antioxidant defence status during larval development and metamorphosis of giant prawn, Macrobrachium rosenbergii. Comp Biochem Physiol C 135:221–233. https://doi.org/10.1016/S1532-0456(03)00080-2
Dmochowska-Ślęzak K, Giejdasz K, Fliszkiewicz M, Żółtowska K (2015) Variations in antioxidant defense during the development of the solitary bee Osmia bicornis. Apidologie 46:432–444. https://doi.org/10.1007/s13592-014-0333-y
Edgecombe GD, Giribet G (2007) Evolutionary biology of centipedes (Myriapoda: Chilopoda). Annu Rev Entomol 52:151–170. https://doi.org/10.1146/annurev.ento.52.110405.091326
Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82(1):70–77. https://doi.org/10.1016/0003-9861(59)90090-6
Ferrari A, Anguiano L, Lascano C, Sotomayor V, Rosenbaum E, Venturino A (2008) Changes in the antioxidant metabolism in the embryonic development of the common South American toad Bufo arenarum: differential responses to pesticide in early embryos and autonomous-feeding larvae. J Biochem Mol Toxicol 22(4):259–267. https://doi.org/10.1002/jbt.20236
Gilbert SF, Epel D (2015) Ecological developmental biology: the environment regulation of development, health, and evolution, 2nd edn. Sinauer, Sunderland
Glatzle D, Vuilleumier JP, Weber F, Decker K (1974) Glutathione reductase test with whole blood, a convenient procedure for the assessment of the riboflavin status in humans. Experientia 30(6):665–667. https://doi.org/10.1007/BF01921531
Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106(1):207–212. https://doi.org/10.1016/0003-2697(80)90139-6
Habig WH, Pubst MJ, Jakoby WB (1974) Glutathione S-transferase. The first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139
Halliwell B, Gutteridge JMC (2015) Free radicals in biology and medicine, 5th edn. Oxford University Press, Oxford
Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11:298–300
Hermes-Lima M, Carreiro C, Moreira DC, Polcheira C, Machado DP, Campos ÉG (2012) Glutathione status and antioxidant enzymes in a crocodilian species from the swamps of the Brazilian Pantanal. Comp Biochem Physiol A 163(2):189–198. https://doi.org/10.1016/j.cbpa.2012.06.006
Jovanović-Galović A, Blagojević DP, Grubor-Lajšić G, Worland R, Spasić 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(2):79–89. https://doi.org/10.1002/arch.10126
Klichko VI, Radyuk SN, Orr WC (2004) Profiling catalase gene expression in Drosophila melanogaster during development and aging. Arch Insect Biochem Physiol 56(1):34–50. https://doi.org/10.1002/arch.10142
Lewis JGE (1981) The biology of centipedes. Cambridge University Press, Cambridge
Lionetto MG, Caricato R, Giordano M, Schettino T (2003) Acetylcholinesterase as biomarker in environmental biomonitoring. In: Parveen M, Kumar S (eds) Recent trends in the acetylcholinesterase system. IOS Press, Amsterdam, pp 91–102
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with Folin phenol reagent. J Biol Chem 193(1):265–725. https://doi.org/10.1016/S0021-9258(19)52451-6
Martínez-Álvarez RM, Morales AE, Sanz A (2005) Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fish 15:75–88. https://doi.org/10.1007/s11160-005-7846-4
Minelli A (2011) Chilopoda—reproduction. In: Minelli A (ed) Treatise on zoology—anatomy, taxonomy, biology. The Myriapoda, vol 1. Brill, Leiden, pp 279–294
Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and simple assay for superoxide dismutase. J Biol Chem 247(10):3170–3175. https://doi.org/10.1016/S0021-9258(19)45228-9
Mitić BM (2001) On some centipedes (Chilopoda, Myriapoda) in Serbia. Arch Biol Sci 53(1–2):21P-22P
Mitić BM (2002) On the diversity of centipedes (Chilopoda, Myriapoda) in Serbia. Part two. Arch Biol Sci 54(3–4):13P-14P. https://doi.org/10.2298/ABS0204133M
Mitić BM, Tomić VT (2002) On the fauna of centipedes (Chilopoda, Myriapoda) inhabiting Serbia and Montenegro. Arch Biol Sci 54(3–4):133–140. https://doi.org/10.2298/ABS0204133M
Mitić BM, Ilić BS, Tomić VT, Makarov SE, Ćurčić BPM (2010) Parental care in Clinopodes flavidus Koch (Chilopoda: Geophilomorpha: Geophilidae). Ann Zool 60(4):633–638. https://doi.org/10.3161/000345410X550490
Mitić BM, Antić DŽ, Ilić BS, Makarov SE, Lučić LR, Ćurčić BPM (2012) Parental care in Cryptops hortensis (Donovan) (Chilopoda: Scolopendromorpha) from Serbia, the Balkan Peninsula. Arch Biol Sci 64(3):1117–1121. https://doi.org/10.2298/ABS1203117M
Mitić BM, Stojanović DZ, Antić DŽ, Ilić BS, Gedged AM, Borković-Mitić SS, Ristić NM, Živić NV, Makarov SE (2016) Maternal care in epimorphic centipedes (Chilopoda: Phylactometria: Epimorpha) from the Balkan Peninsula. Invertebr Reprod Dev 60(1):81–86. https://doi.org/10.1080/07924259.2016.1143040
Montesano L, Carrì MT, Mariottini P, Amaldi F, Rotilio G (1989) Developmental expression of Cu, Zn superoxide dismutase in Xenopus. Constant level of the enzyme in oogenesis and embryogenesis. Eur J Biochem 186(1–2):421–426. https://doi.org/10.1111/j.1432-1033.1989.tb15226.x
Orr WC, Sohal RS (1994) Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster. Science 263(5150):1128–1130. https://doi.org/10.1126/science.8108730
Parolini M, Iacobuzio R, De Felice B, Bassano B, Pennati R, Saino N (2019) Age- and sex-dependent variation in the activity of antioxidant enzymes in the brown trout (Salmo trutta). Fish Physiol Biochem 45(1):145–154. https://doi.org/10.1007/s10695-018-0545-6
Pérez-Campo R, López-Torres M, Rojas C, Cadenas S, Barja G (1993) A comparative study of free radicals in vertebrates-I. Antioxidant enzymes. Comp Biochem Physiol B 105:749–755. https://doi.org/10.1016/0305-0491(93)90116-m
Peters LD, Livingstone DR (1996) Antioxidant enzyme activities in embryologic and early larval stages of turbot. J Fish Biol 49(5):986–997. https://doi.org/10.1111/j.1095-8649.1996.tb00095.x
Radl RC (1992) Brood care in Scolopendra cingulata Latreille (Chilopoda: Scolopendromorpha). Ber Nat-Med Ver Innsb Suppl 10:123–127
Ran Q, Liang H, Gu M, Qi W, Walter CA, Jackson Roberts II L, Herman B, Richardson A, Van Remmen H (2004) Transgenic mice overexpressing glutathione peroxidase 4 are protected against oxidative stress-induced apoptosis. J Biol Chem 279(53):55137–55146. https://doi.org/10.1074/jbc.M410387200
Rocha-e-Silva TAA, Rossa MM, Rantin FT, Matsumura-Tundisi T, Tundisi JG, Degterev IA (2004) Comparison of liver mixed-function oxygenase and antioxidant enzymes in vertebrates. Comp Biochem Physiol C 137:155–165. https://doi.org/10.1016/j.cca.2004.01.007
Rossi MA, Cecchini G, Dianzani MM (1983) Glutathione peroxidase, glutathione reductase and glutathione transferase in two different hepatomas and in normal liver. IRCS Med Sci Biochem 11:805
Rudneva II (1997) Blood antioxidant system of Black Sea elasmobranch and teleost. Comp Biochem Physiol C 118(2):255–260. https://doi.org/10.1016/S0742-8413(97)00111-4
Rudneva II (1999) Antioxidant system of Black Sea animals in early development. Comp Biochem Physiol C 122(2):265–271. https://doi.org/10.1016/s0742-8413(98)10121-4
Rudneva II, Skuratovskaya EN, Kuzminova NS, Kovyrshina TB (2010) Age composition and antioxidant enzyme activities in blood of Black Sea teleosts. Comp Biochem Physiol C 151(2):229–239. https://doi.org/10.1016/j.cbpc.2009.11.001
Schieber M, Chandel NS (2014) ROS function in redox signaling and oxidative stress. Curr Biol 24(10):R453–R462. https://doi.org/10.1016/j.cub.2014.03.034
Sohal RS, Arnold L, Orr WC (1990) Effect of age on superoxide dismutase, catalase, glutathione reductase, inorganic peroxides, TBA-reactive material, GSH/GSSG, NADPH/NADP+ and NADH/NAD+ in Drosophila melanogaster. Mech Ageing Dev 56(3):223–235. https://doi.org/10.1016/0047-6374(90)90084-s
Stanić B, Jovanović-Galović A, Blagojević D, Grubor-Lajšić G, Worland R, Spasić MB (2004) Cold hardiness in Ostrinia nubilalis (Lepidoptera: Pyralidae): glycerol content, hexose monophosphate shunt activity and antioxidative defense system. Eur J Entomol 101(3):459–466. https://doi.org/10.14411/eje.2004.065
Stojanović DZ, Vujić VD, Lučić LR, Tomić VT, Makarov SE, Mitić BM (2020) Life after the mother’s hug: late post-embryonic development of Cryptops parisi (Chilopoda: Scolopendromorpha: Cryptopidae). Arthropod Struct Dev 57:100948. https://doi.org/10.1016/j.asd.2020.100948
Surai PF (1999) Tissue-specific changes in the activities of antioxidant enzymes during the development of the chicken embryo. Br Poult Sci 40:397–405. https://doi.org/10.1080/00071669987511
Takada Y, Noguchi T, Okabe T, Kajiyama M (1982) Superoxide dismutase in various tissues from rabbits bearing the Vx-2 carcinoma in the maxillary sinus. Cancer Res 42(10):4233–4235
Tamura M, Oschino N, Chance B (1982) Some characteristics of hydrogen and alkyl-hydroperoxides metabolizing systems in cardiac tissue. J Biochem 92(4):1019–1031. https://doi.org/10.1093/oxfordjournals.jbchem.a134017
Tasaki E, Kobayashi K, Matsuura K, Iuchi Y (2017) An efficient antioxidant system in a long-lived termite queen. PLoS ONE 12:e0167412. https://doi.org/10.1371/journal.pone.0167412
Ufer C, Wang CC (2011) The roles of glutathione peroxidases during embryo development. Front Mol Neurosci 4:12. https://doi.org/10.3389/fnmol.2011.00012
Voigtländer K (2011) Chilopoda—ecology. In: Minelli A (ed) Treatise on zoology—anatomy, taxonomy, biology. The Myriapoda, vol 1. Brill, Leiden, pp 309–325
Vranković J (2016) Age-related changes in antioxidant and glutathione S-transferase enzyme activities in the Asian clam. Biochem (mosc) 81:224–232. https://doi.org/10.1134/S0006297916030044
Vranković J, Borković-Mitić S, Ilić B, Radulović M, Milošević S, Makarov S, Mitić B (2017) Bioaccumulation of metallic trace elements and antioxidant enzyme activities in Apfelbeckia insculpta (L. Koch, 1867) (Diplopoda: Callipodida) from the cave Hadži-Prodanova Pećina (Serbia). Int J Speleol 46(1):99–108. https://doi.org/10.5038/1827-806X.46.1.1981
Zhu Y, Carvey PM, Ling Z (2006) Age-related changes in glutathione and glutathione-related enzymes in rat brain. Brain Res 1090(1):35–44. https://doi.org/10.1016/j.brainres.2006.03.063
Zielinski S, Pörtner H-O (2000) Oxidative stress and antioxidative defense in cephalopods: a function of metabolic rate or age? Comp Biochem Physiol B 125(2):147–160. https://doi.org/10.1016/s0305-0491(99)00162-5
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This work was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia, Contract Nos. 451-03-47/2023-01/200007 and 451-03-47/2023-01/200178. The authors are grateful to Dr. Goran Poznanović for proofreading the manuscript.
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Mitić, B.M., Borković-Mitić, S.S., Vranković, J.S. et al. Age-related changes in antioxidant defenses of the Mediterranean centipede Scolopendra cingulata (Chilopoda). J Comp Physiol B 193, 249–260 (2023). https://doi.org/10.1007/s00360-023-01481-w
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DOI: https://doi.org/10.1007/s00360-023-01481-w