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Mitochondrial P-Glycoprotein ATPase Contributes to Insecticide Resistance in the Cotton Bollworm, Helicoverpa armigera (Noctuidae: Lepidoptera)

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Abstract

Cotton bollworm, Helicoverpa armigera, is one of the most damaging polyphagous pests worldwide, which has developed high levels of resistance to commonly applied insecticides. Mitochondrial P-glycoprotein (Pgp) was detected in the insecticide-resistant strain of H. armigera using C219 antibodies, and its possible role was demonstrated in the efflux of xenobiotic compounds using spectrofluorometer. The TMR accumulated in mitochondria in the absence of ATP, and effluxed out in presence of ATP; the process of efflux was inhibited in the presence of ortho-vandate, an inhibitor of Pgp, in insecticide-resistant larvae of H. armigera. The mitochondria isolated from insecticide-resistant larvae were resistant to insecticide-induced inhibition of oxygen consumption and cytochrome c release. Membrane potential decreased in a dose-dependent manner in the presence of higher concentration of insecticides (>50 µM) in mitochondria of insecticide-resistant larvae. In conclusion, mitochondrial Pgp ATPase detected in the insecticide-resistant larvae influenced the efflux of xenobiotic compounds. Pgp might be involved in protecting the mitochondrial DNA and the components of the electron transport chain from damage due to insecticides, and contributing to the resistance to the deleterious effects of insecticides on the growth of insecticide-resistant H. armigera larvae.

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Abbreviations

FCCP:

Carbonyl cyanide p-(trifluoromethoxy) phenylhydrazone

MDR:

Multidrug resistance

Pgp:

P-glycoprotein

TMR:

Tetramethylrosamine

References

  1. Sharma, H. C. (2005). Heliothis/Helicoverpa management: Emerging trends and strategies for future research. New Delhi: Oxford and IBH Publishing Co.

    Google Scholar 

  2. Kranthi, K. R., Jadhav, D. R., Wanjari, R. R., Kranthi, S., & Russell, D. (2001). Pyrethroid resistance and mechanisms in field strains of Helicoverpa armigera Hubner (Lepidoptera: Noctuidae). Journal of Economic Entomology, 94, 253–263.

    Article  CAS  PubMed  Google Scholar 

  3. Srinivas, R., Udikeri, S. S., Jayalakshmi, S. K., & Sreeramulu, K. (2004). Identification of factors responsible for insecticide resistance in Helicoverpa armigera. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 137, 261–269.

    CAS  Google Scholar 

  4. Lanning, C. L., Fine, R. L., Sachs, C. W., Rao, U. S., Corcoran, J. J., & Abou-Donia, M. B. (1996). Chlorpyrifos oxon interacts with the mammalian multidrug resistance protein, P-glycoprotein. Journal of Toxicology and Environment Health, 47, 395–407.

    Article  CAS  Google Scholar 

  5. Leslie, E. M., Deeley, R. G., & Cole, S. P. C. (2005). Multidrug resistance proteins: Role of P glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicology and Applied Pharmacology, 204, 216–237.

    Article  CAS  PubMed  Google Scholar 

  6. Gottesman, M. M. (2002). Mechanisms of cancer drug resistance. Annual Review of Medicine, 53, 615–627.

    Article  CAS  PubMed  Google Scholar 

  7. Prasad, R., Murthy, S. K., Prasad, R., Gupta, V., & Lata, S. (1996). Multidrug resistance: An emerging threat. Current Science, 71, 205–213.

    CAS  Google Scholar 

  8. Murray, C. L., Quaglia, M., Arnason, J. T., & Morris, C. E. (1994). A putative nicotine pump at the metabolic blood–brain barrier of the tobacco hornworm. Journal of Neurobiology, 25, 23–34.

    Article  CAS  PubMed  Google Scholar 

  9. Bain, L. J., & LeBlanc, G. A. (1996). Interaction of structurally diverse pesticides with the human MDR1 gene product P-glycoprotein. Toxicology and Applied Pharmacology, 141, 288–298.

    CAS  PubMed  Google Scholar 

  10. Baldini, N., Scotlandi, K., Serra, M., Shikita, T., Zini, N., Ognibene, A., et al. (1995). Nuclear immunolocalization of P-glycoprotein in multidrug-resistant cell lines showing similar mechanisms of doxorubicin distribution. European Journal of Cell Biology, 68, 226–239.

    CAS  PubMed  Google Scholar 

  11. Molinari, A., Cianfriglia, M., Meschini, S., Calcabrini, A., & Arancia, G. (1994). P-glycoprotein expression in the Golgi apparatus of multidrug resistant cells. International Journal of Cancer, 9, 789–795.

    Article  Google Scholar 

  12. Munteanu, E., Verdier, M., Grandjean-Forestier, F., Stenger, G., Jayat-Vignoles, C., Huet, S., et al. (2006). Mitochondrial localization and activity of P-glycoprotein in doxorubicin-resistant K562 cells. Biochemical Pharmacology, 71, 1162–1174.

    Article  CAS  PubMed  Google Scholar 

  13. Solazzo, M., Fantappiè, O., Lasagna, N., Sassoli, C., Nosi, D., & Mazzanti, R. (2006). P-gp localization in mitochondria and its functional characterization in multiple drug-resistant cell lines. Experimental Cell Research, 312, 4070–4078.

    Article  CAS  PubMed  Google Scholar 

  14. Pullikuth, A. K., & Gill, S. S. (1997). Primary structure of an invertebrate dihydrolipoamide dehydrogenase with phylogenetic relationship to vertebrate and bacterial disulfide oxidoreductases. Gene, 200, 163–172.

    Article  CAS  PubMed  Google Scholar 

  15. Kaur, P., Radotra, B., Minz, R. W., & Gill, K. D. (2007). Impaired mitochondrial energy metabolism and neuronal apoptotic cell death after chronic dichlorvos (OP) exposure in rat brain. Neurotoxicology, 28(6), 1208–1219.

    Article  CAS  PubMed  Google Scholar 

  16. Armes, N. J., Jadhav, D. R., Bond, G. S., & King, A. B. S. (1992). Insecticide resistance in Helicoverpa armigera in South India. Pesticide Science, 34, 355–364.

    Article  CAS  Google Scholar 

  17. Chamberlin, M. E. (2004). Control of oxidative phosphorylation during insect metamorphosis. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 287, 314–321.

    Google Scholar 

  18. Akbar, S. Md, Sharma, H. C., Jayalakshmi, S. K., & Sreeramulu, K. (2012). Interaction of plant cell signaling molecules, salicylic acid and jasmonic acid, with the mitochondria of Helicoverpa armigera. Journal of Bioenergetics and Biomembranes, 44, 233–241.

    Article  CAS  PubMed  Google Scholar 

  19. Lowry, O. H., Rosenbrough, N. J., Farr, A. L., & Randal, A. J. (1951). Protein measurements with the folin phenol reagent. Journal of Biological Chemistry, 193, 265–275.

    CAS  PubMed  Google Scholar 

  20. Borgnia, M. J., Eytan, G. D., & Assaraf, Y. G. (1996). Competition of hydrophobic peptides, cytotoxic drugs, and chemosensitizers on a common P-glycoprotein pharmacophore as revealed by its ATPase activity. Journal of Biological Chemistry, 271, 3163–3171.

    Article  CAS  PubMed  Google Scholar 

  21. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London), 227, 680–685.

    Article  CAS  Google Scholar 

  22. Gerard, C. (1990). Purification of glycoproteins. Methods in Enzymology, 182, 529–539.

    Article  CAS  PubMed  Google Scholar 

  23. Aurade, R. M., Jayalakshmi, S. K., & Sreeramulu, K. (2010). P-glycoprotein ATPase from the resistant pest, Helicoverpa armigera: Purification, characterization and effect of various insecticides on its transport function. Biochimica et Biophysica Acta, 1798, 1135–1143.

    Article  CAS  PubMed  Google Scholar 

  24. Kim, M., Cooper, D. D., Hayes, S. F., & Spangrude, G. J. (1998). Rhodamine-123 staining in hematopoietic stem cells of young mice indicates mitochondrial activation rather than dye efflux. Blood, 91, 4106–4117.

    CAS  PubMed  Google Scholar 

  25. Braguini, W. L., Cadena, S. M. S. C., Carnieri, E. G. S., Rocha, M. E. M., & de Oliveira, M. B. M. (2004). Effect of deltamethrin on functions of rat liver mitochondria and on native and synthetic model membranes. Toxicology Letters, 152, 191–202.

    Article  CAS  PubMed  Google Scholar 

  26. Joshi, D. C., & Bakowska, J. C. (2011). Determination of mitochondrial membrane potential and reactive oxygen species in live rat cortical neurons. Journal of Visualized Experiments,. doi:10.3791/2704.

    Google Scholar 

  27. Sreeramulu, K., Liu, R., & Sharom, F. J. (2007). Interaction of insecticides with mammalian P-glycoprotein and their effect on its transport function. Biochimica et Biophysica Acta, 68, 1750–1757.

    Article  Google Scholar 

  28. Lu, P., Liu, R., & Sharom, F. J. (2001). Drug transport by reconstituted P-glycoprotein in proteoliposomes-effect of substrates and modulators, and dependence on bilayer phase state. European Journal of Biochemistry, 268, 1687–1697.

    Article  CAS  PubMed  Google Scholar 

  29. Ling, X., He, Y., Zhang, G., Zhou, Y., & Yan, B. (2012). Increased P-glycoprotein expression in mitochondria is related to acquired multidrug resistance in human hepatoma cells depleted of mitochondrial DNA. International Journal of Oncology, 40(1), 109–118.

    CAS  PubMed  Google Scholar 

  30. Bonnet, S., Archer, S. L., Allalunis-Turner, J., Haromy, A., Beaulieu, C., Thompson, R., et al. (2007). A mitochondria-k+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell, 11, 37–51.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported in part by UGC to S Md Akbar (under RFSMS scheme), UGC—SAP (DSR—I), New Delhi to KS and the Ministry of Agriculture, Government of India to HCS. We are indebted to Dr FJ Sharom, Professor, Department of Molecular and Cellular Biology, University of Guelph, Canada, for reading the manuscript before its submission and her helpful discussions in improving the manuscript.

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Authors and Affiliations

  1. Department of Biochemistry, Gulbarga University, Gulbarga, 585106, Karnataka, India

    S. Md Akbar, Ravindra M. Aurade & K. Sreeramulu

  2. International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, 502324, Andhra Pradesh, India

    S. Md Akbar & H. C. Sharma

Authors
  1. S. Md Akbar
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  2. Ravindra M. Aurade
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  4. K. Sreeramulu
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Correspondence to K. Sreeramulu.

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Akbar, S.M., Aurade, R.M., Sharma, H.C. et al. Mitochondrial P-Glycoprotein ATPase Contributes to Insecticide Resistance in the Cotton Bollworm, Helicoverpa armigera (Noctuidae: Lepidoptera). Cell Biochem Biophys 70, 651–660 (2014). https://doi.org/10.1007/s12013-014-9969-5

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