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Sexual alteration in antioxidant response and esterase profile in Hyalomma anatolicum anatolicum (Acari: Ixodidae) ticks

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Abstract

The objective of the study was to reveal physiological link between sex specific engorgement pattern and evading mechanism of ticks against oxidative stress as well as acaricides. Quantitative determination of nitric oxide radical scavenging, superoxide dismutase activity and reduced glutathione (GSH) concentrations in salivary gland and gut extracts of male and female Hyalomma anatolicum anatolicum (Acari: Ixodidae) ticks established significant variation in antioxidant responses between two sexes of the ticks. Higher activity of these antioxidants and GSH depletion in females clearly indicate stronger antioxidant defense in female ticks which is to combat host mediated oxidative assault during feeding for greater engorgement and reproductive stress. The females are also better equipped with the mechanism of acaricide resistance as evidenced by higher expression of esterases than males in unfed whole tick extracts in current study.

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References

  • Abbas RZ, Zamanb MR, Colwell DD, Gillearde J, Iqbal Z (2014) Acaricide resistance in cattle ticks and approaches to its management: The state of play. Vet Parasitol 203:6–20

    Article  CAS  PubMed  Google Scholar 

  • Al-Shammery KA, Fetoh BA (2011) Protein and esterase profile patterns of the camel tick Hyalomma (Hyalomma) dromedarii (Koch) (Acari: lxodidae) in Hail and Qassim Regions, Saudi Arabia. IJESE 2:53–60

    Google Scholar 

  • Baffi MA, Pereira CD, Souza GRL, Bonetti AM, de Ceron CR, Goulart Filho LR (2005) Esterase profile in a pyrethroid-resistant Brazilian strain of Boophilus microplus cattle ticks (Acari, Ixodidae). Genet Mol Biol 28:749–753

    Article  CAS  Google Scholar 

  • Baffi MA, Pereira CD, Souza GRL, de Ceron CR, Bonetti AM (2007) Esterase profile in the postembryonic development of Rhipicephalus microplus. Pesqui Agropecu Bras 42:1183–1188

    Article  Google Scholar 

  • Beutler E (1971) Red cell metabolism manual of biochemical methods. In: Beutler E (ed). Academic Press, London, pp. 68–70

  • 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  CAS  PubMed  Google Scholar 

  • Chen X, Yu Z, Guo L, Li L, Meng H, Wang D, Liu R, Liu J (2012) Life cycle of Haemaphysalis doenitzi (Acari: Ixodidae) under laboratory conditions and its phylogeny based on mitochondrial 16S rDNA. Exp Appl Acarol 56:143–150

    Article  PubMed  Google Scholar 

  • Devendra C (1995) Animal production system in South-East and East Asia: potential and challenges for research. In: Gardiner PR, Devendra C (eds) Global agenda for livestock research. Proceedings of a consultation, 18–20 January 1995. ILRI (International Livestock Research Institute), Nairobi, Kenya, pp 41–48

  • Devonshire AL, Williamson MS, Moores GD, Field LM (1993) Analysis of the esterase genes conferring insecticide resistance in peach-potato aphid, Myzus perspicae. Biochem J 294:569–574

    Article  PubMed  PubMed Central  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  CAS  PubMed  Google Scholar 

  • Francischetti IM, Sá-Nunes A, Mans BJ, Santos IM, Ribeiro JMC (2009) The role of saliva in tick feeding. Front Biosci 14:2051–2088

    Article  CAS  Google Scholar 

  • Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112

    Article  CAS  PubMed  Google Scholar 

  • Ghosh M, Sangwan N, Sangwan AK (2014) Variations in free radical scavenging activities and antioxidant responses in salivary glands of Hyalomma anatolicum anatolicum and Hyalomma dromedarii (Acari: Ixodidae) ticks. Vet World 7(10):876–881

    Article  CAS  Google Scholar 

  • Guillemaud T, Makate N, Raymond M, Hirst B, Callghan A (1997) Esterase gene amplification in Culex pipiensis. Insect Mol Biol 6:319–327

    CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1989) In: Free Radical in Biology and Medicine, 2nd edn. Clarendon Press, Oxford

  • Jamroz RC, Guerrero FD, Pruett JH, Oehler DD, Miller RJ (2000) Molecular and biochemical survey of acaricide resistance mechanisms in larvae from Mexican strains of southern cattle tick. J Insect Physiol 46:685–695

    Article  CAS  PubMed  Google Scholar 

  • Kemp DH, Stone BF, Binnington KC (1982) Tick attachment and feeding: role of the mouthparts, feeding apparatus, salivary gland secretions and host response. In: Obenchain FD, Galun R (eds) Physiology of ticks. Pergamon Press, Oxford, pp 119–168

    Chapter  Google Scholar 

  • Kort CA, Granger NA (1981) Regulation of the juvenile hormone titer. Annu Rev Entomol 26:1–28

    Article  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Ma M, Guan G, Chen Z, Liu Z, Liu A, Gou H, Ren Q, Li Y, Niu Q, Yang J, Yin H, Luo J (2013) The life cycle of Haemaphysalis qinghaiensis (Acari: Ixodidae) ticks under laboratory conditions. Exp Appl Acarol 59:493–500

    Article  PubMed  Google Scholar 

  • Madesh M, Balasubramanian KA (1998) Microtiter plate assay for superoxide dismutase using MTT reduction by superoxide. Indian J Biochem Biophys 35:184–188

    CAS  PubMed  Google Scholar 

  • Marklund S, Marklund G (1974) Involvement of the superoxyde anion radical in the auto oxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474

    Article  CAS  PubMed  Google Scholar 

  • Mutero A, Pralavorio M, Bride JM, Fournier D (1994) Resistance associated point mutations in insecticide-insensitive acetylcholinesterase. PNAS 91:5922–5926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richmond RC, Gilbert DG, Sheehan KB, Gromko MH, Butterworth FM (1980) Esterase 6 and reproduction in Drosophila melanogaster. Science 207:1483–1485

    Article  CAS  PubMed  Google Scholar 

  • Saeaue L, Morales NP, Komalamisra N, Vargas REM (2011) Antioxidative systems defense against oxidative stress induced by blood meal in Aedes aegypti. Southeast Asian J Trop Med Public Health 42(3):542–549

    CAS  PubMed  Google Scholar 

  • Shaw MK, Young AS (1994) The biology of Theileria species in ixodid ticks in relation to parasite transmission. In: Advances in Disease Vector Research, vol 10. Springer-Verlag, New York, pp 23–63 (1254)

  • Snedecor GW, Cochran WJ (1967) Statistical methods, 7th edn. Oxford and IBG Publishing Co., New Delhi

    Google Scholar 

  • Sreejayan N, Rao MNA (1997) Nitric oxide scavenging by curcuminoids. J Pharm Pharmacol 49:105–107

    Article  CAS  PubMed  Google Scholar 

  • Stauffer C, Leitinger R, Simsek Z, Schreiber JD, Führer E (1992) Allozyme variation among nine Austrian Ips typographus (L.) (Coleoptera, Scolytidae) populations. J Appl Entomol 114:17–25

    Article  Google Scholar 

  • Temeyer KB, Tuckow AP (2016) Tick Salivary Cholinesterase: A Probable Immunomodulator of Host–parasite Interactions. J Med Entomol 2016:1–5. doi:10.1093/jme/tjv252

    Google Scholar 

  • Villarino MA, Waghela SD, Wagner GG (2003) Biochemical detection of esterases in the adult female integument of organophosphate-resistant Boophilus microplus (Acari, Ixodidae). J Med Entomol 40:52–57

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Wang Y, Liu H, Yang H, Ma D, Li J, Li D, Lai R, Yu H (2010) Two immunoregulatory peptides with antioxidant activity from tick salivary glands. J Biol Chem 285:1–19

    Article  Google Scholar 

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Acknowledgments

This research was supported partly with grants from University Grant Commission (UGC), Govt. of India.

Authors’ contributions

MG and NS designed the experiment, data analyses and final corrections of the manuscript. MG and AKS collected the sample. AKS identified the tick species and contributed in dissection of ticks. MG, RK and RSG performed the dissection of ticks, wet lab analyses, and data analyses. All authors participated in manuscript preparation. All authors read and approved the final manuscript.

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Correspondence to Mayukh Ghosh.

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Ghosh, M., Sangwan, N., Sangwan, A.K. et al. Sexual alteration in antioxidant response and esterase profile in Hyalomma anatolicum anatolicum (Acari: Ixodidae) ticks. J Parasit Dis 41, 106–111 (2017). https://doi.org/10.1007/s12639-016-0758-5

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  • DOI: https://doi.org/10.1007/s12639-016-0758-5

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