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Increased production of mitochondrial reactive oxygen species and reduced adult life span in an insecticide-resistant strain of Anopheles gambiae

Published online by Cambridge University Press:  21 February 2014

D. Otali*
Affiliation:
Department of Biology, University of Alabama at Birmingham, Campbell Hall 464, 1720 2ndAve. South, Birmingham, AL 35294-1170, USA
R.J. Novak
Affiliation:
Division of Infectious Diseases, Department of Medicine, William C Gorgas Center for Geographic Medicine, University of Alabama at Birmingham, 845 19th St. South, Birmingham, AL 35294-2170, USA Department of Global Health, University of South Florida, 13201 Bruce B. Downs Blvd., Tampa, FL 33612, USA
W. Wan
Affiliation:
Department of Biostatistics, Virginia Commonwealth University Medical Center, P.O. Box 980032, Richmond, VA 23298-0032, USA
S. Bu
Affiliation:
Department of Nutrition Sciences, University of Alabama at Birmingham, 1720 2ndAve. South, Birmingham, AL 35294-3360, USA
D.R. Moellering
Affiliation:
Department of Nutrition Sciences, University of Alabama at Birmingham, 1720 2ndAve. South, Birmingham, AL 35294-3360, USA
M. De Luca
Affiliation:
Department of Nutrition Sciences, University of Alabama at Birmingham, 1720 2ndAve. South, Birmingham, AL 35294-3360, USA
*
*Author for correspondence Phone: (+1) 205-975-6205 Fax: (+1) 205-975-7128 E-mail: otalid@uab.edu

Abstract

Control of the malaria vector An. gambiae is still largely obtained through chemical intervention using pyrethroids, such as permethrin. However, strains of An. gambiae that are resistant to the toxic effects of pyrethroids have become widespread in several endemic areas over the last decade. The objective of this study was to assess differences in five life-history traits (larval developmental time and the body weight, fecundity, hatch rate, and longevity of adult females) and energy metabolism between a strain of An. gambiae that is resistant to permethrin (RSP), due to knockdown resistance and enhanced metabolic detoxification, and a permethrin susceptible strain reared under laboratory conditions. We also quantified the expression levels of five antioxidant enzyme genes: GSTe3, CAT, GPXH1, SOD1, and SOD2. We found that the RSP strain had a longer developmental time than the susceptible strain. Additionally, RSP adult females had higher wet body weight and increased water and glycogen levels. Compared to permethrin susceptible females, RSP females displayed reduced metabolic rate and mitochondrial coupling efficiency and higher mitochondrial ROS production. Furthermore, despite higher levels of GSTe3 and CAT transcripts, RSP females had a shorter adult life span than susceptible females. Collectively, these results suggest that permethrin resistance alleles might affect energy metabolism, oxidative stress, and adult survival of An. gambiae. However, because the strains used in this study differ in their genetic backgrounds, the results need to be interpreted with caution and replicated in other strains to have significant implications for malaria transmission and vector control.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2014 

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References

Adasi, K. & Hemingway, J. (2008) Susceptibility to three pyrethroids and detection of knockdown resistance mutation in Ghanaian Anopheles gambiae sensu stricto. Journal of Vector Ecology 33, 255262.CrossRefGoogle ScholarPubMed
Affourtit, C., Quinlan, C.L. & Brand, M.D. (2012) Measurement of proton leak and electron leak in isolated mitochondria. Methods in Molecular Biology 810, 165182.CrossRefGoogle ScholarPubMed
Boveris, A., Oshino, N. & Chance, B. (1972) The cellular production of hydrogen peroxide. Biochemical Journal 128, 617630.CrossRefGoogle ScholarPubMed
Brooke, B.D. & Koekemoer, L.L. (2010) Major effect genes or loose confederations? The development of insecticide resistance in the malaria vector Anopheles gambiae . Parasities & Vectors 3, 74.CrossRefGoogle ScholarPubMed
Brown, Z.S., Dickinson, K.L. & Kramer, R.A. (2013) Insecticide resistance and malaria vector control: the importance of fitness cost mechanisms in determining economically optimal control trajectories. Journal of Economic Entomology 106, 366374.CrossRefGoogle ScholarPubMed
Cadenas, E., Boveris, A., Ragan, C.I. & Stoppani, A.O. (1977) Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria. Archives of Biochemistry and Biophysics 180, 248257.CrossRefGoogle ScholarPubMed
Casimiro, S., Coleman, M., Hemingway, J. & Sharp, B. (2006) Insecticide resistance in Anopheles arabiensis and Anopheles gambiae from Mozambique. Journal of Medical Entomology 43, 276282.CrossRefGoogle ScholarPubMed
Chown, S.L. & Gaston, K.J. (1999) Exploring links between physiology and ecology at macro-scales: the role of respiratory metabolism in insects. Biological Reviews of the Cambridge Philosophical Society 74, 87120.CrossRefGoogle Scholar
Coustau, C., Chevillon, C. & ffrench-Constant, R. (2000) Resistance to xenobiotics and parasites: can we count the cost? Trends in Ecology & Evolution 15, 378383.CrossRefGoogle ScholarPubMed
DeJong, R.J., Miller, L.M., Molina-Cruz, A., Gupta, L., Kumar, S. & Barillas-Mury, C. (2007) Reactive oxygen species detoxification by catalase is a major determinant of fecundity in the mosquito Anopheles gambiae . Proceedings of the National Academy of Sciences of the United States of America 104, 21212126.CrossRefGoogle ScholarPubMed
De Luca, M., Klimentidis, Y.C., Casazza, K., Chambers, M.M., Cho, R., Harbison, S.T., Jumbo-Lucioni, P., Zhang, S., Leips, J. & Fernandez, J.R. (2010) A conserved role for syndecan family members in the regulation of whole-body energy metabolism. PLoS One 5, e11286.CrossRefGoogle ScholarPubMed
Ding, Y., Hawkes, N., Meredith, J., Eggleston, P., Hemingway, J. & Ranson, H. (2005) Characterization of the promoters of Epsilon glutathione transferases in the mosquito Anopheles gambiae and their response to oxidative stress. Biochemical Journal 387, 879888.CrossRefGoogle ScholarPubMed
Djouaka, R.F., Bakare, A.A., Coulibaly, O.N., Akogbeto, M.C., Ranson, H., Hemingway, J. & Strode, C. (2008) Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae s.s. from Southern Benin and Nigeria. BMC Genomics 9, 538.CrossRefGoogle ScholarPubMed
Enayati, A.A. & Hemingway, J. (2006) Pyrethroid insecticide resistance and treated bednets efficacy in malaria control. Pesticide Biochemistry and Physiology 84, 116126.CrossRefGoogle Scholar
Félix, R. & Silveira, H. (2012) The role of Anopheles gambiae P450 Cytochrome in insecticide resistance and infection. pp. 503518 in Perveen, F. (Ed.) Insecticides – Pest Engineering, InTech – Open Access Company.Google Scholar
Ferguson, M., Mockett, R.J., Shen, Y., Orr, W.C. & Sohal, R.S. (2005) Age-associated decline in mitochondrial respiration and electron transport in Drosophila melanogaster . Biochemical Journal 390, 501511.CrossRefGoogle ScholarPubMed
Gibbs, A.G. & Matzkin, L.M. (2001) Evolution of water balance in the genus Drosophila . The Journal of Experimental Biology 204, 23312338.Google ScholarPubMed
Guzov, V.M., Houston, H.L., Murataliev, M.B., Walker, F.A. & Feyereisen, R. (1996) Molecular cloning, overexpression in Escherichia coli, structural and functional characterization of house fly cytochrome b5. Journal of Biological Chemistry 271, 2663726645.CrossRefGoogle ScholarPubMed
Hayes, J.D. & McLellan, L.I. (1999) Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radical Research 31, 273300.CrossRefGoogle ScholarPubMed
Hemingway, J. & Ranson, H. (2000) Insecticide resistance in insect vectors of human disease. Annual Review of Entomology 45, 371391.CrossRefGoogle ScholarPubMed
Hinkle, P.C., Butow, R.A., Racker, E. & Chance, B. (1967) Partial resolution of the enzymes catalyzing oxidative phosphorylation. XV. Reverse electron transfer in the flavin-cytochrome beta region of the respiratory chain of beef heart submitochondrial particles. The Journal of Biological Chemistry 242, 51695173.Google Scholar
Jumbo-Lucioni, P., Ayroles, J.F., Chambers, M.M., Jordan, K.W., Leips, J., Mackay, T.F. & De Luca, M. (2010) Systems genetics analysis of body weight and energy metabolism traits in Drosophila melanogaster . BMC Genomics 11, 297.CrossRefGoogle ScholarPubMed
Jumbo-Lucioni, P., Bu, S., Harbison, S.T., Slaughter, J.C., Mackay, T.F., Moellering, D.R. & De Luca, M. (2012) Nuclear genomic control of naturally occurring variation in mitochondrial function in Drosophila melanogaster . BMC Genomics 13, 659.CrossRefGoogle ScholarPubMed
Kawano, S., Kamataki, T., Yasumori, T., Yamazoe, Y. & Kato, R. (1987) Purification of human liver cytochrome P-450 catalyzing testosterone 6 beta-hydroxylation. Journal of Biochemistry 102, 493501.CrossRefGoogle ScholarPubMed
Kliot, A. & Ghanim, M. (2012) Fitness costs associated with insecticide resistance. Pest Management Science 68, 14311437.CrossRefGoogle ScholarPubMed
Kumar, S., Christophides, G.K., Cantera, R., Charles, B., Han, Y.S., Meister, S., Dimopoulos, G., Kafatos, F.C. & Barillas-Mury, C. (2003) The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae . Proceedings of the National Academy of Sciences of the United States of America 100, 1413914144.CrossRefGoogle ScholarPubMed
Li, X., Schuler, M.A. & Berenbaum, M.R. (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology 52, 231253.CrossRefGoogle ScholarPubMed
Lumjuan, N., Rajatileka, S., Changsom, D., Wicheer, J., Leelapat, P., Prapanthadara, L.A., Somboon, P., Lycett, G. & Ranson, H. (2011) The role of the Aedes aegypti Epsilon glutathione transferases in conferring resistance to DDT and pyrethroid insecticides. Insect Biochemistry and Molecular Biology 41, 203209.CrossRefGoogle ScholarPubMed
Marchi, S., Giorgi, C., Suski, J.M., Agnoletto, C., Bononi, A., Bonora, M., De Marchi, E., Missiroli, S., Patergnani, S., Poletti, F., Rimessi, A., Duszynski, J., Wieckowski, M.R. & Pinton, P. (2012) Mitochondria-ros crosstalk in the control of cell death and aging. Journal of Signal Transduction 2012, 329635.CrossRefGoogle ScholarPubMed
Melvin, R.G. & Ballard, J.W. (2006) Intraspecific variation in survival and mitochondrial oxidative phosphorylation in wild-caught Drosophila simulans . Aging Cell 5, 225233.CrossRefGoogle ScholarPubMed
Miwa, S., St-Pierre, J., Partridge, L. & Brand, M.D. (2003) Superoxide and hydrogen peroxide production by Drosophila mitochondria. Free Radical Biology & Medicine 35, 938948.CrossRefGoogle ScholarPubMed
Monaghan, P., Metcalfe, N.B. & Torres, R. (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecology Letters 12, 7592.CrossRefGoogle ScholarPubMed
Murataliev, M.B., Guzov, V.M., Walker, F.A. & Feyereisen, R. (2008) P450 reductase and cytochrome b5 interactions with cytochrome P450: effects on house fly CYP6A1 catalysis. Insect Biochemistry and Molecular Biology 38, 10081015.CrossRefGoogle ScholarPubMed
Okoye, P.N., Brooke, B.D., Hunt, R.H. & Coetzee, M. (2007) Relative developmental and reproductive fitness associated with pyrethroid resistance in the major southern African malaria vector, Anopheles funestus . Bulletin of Entomological Research 97, 599605.CrossRefGoogle ScholarPubMed
Raha, S., McEachern, G.E., Myint, A.T. & Robinson, B.H. (2000) Superoxides from mitochondrial complex III: the role of manganese superoxide dismutase. Free Radical Biology and Medicine 29, 170180.CrossRefGoogle ScholarPubMed
Ranson, H., Jensen, B., Vulule, J.M., Wang, X., Hemingway, J. & Collins, F.H. (2000) Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids. Insect Biochemistry and Molecular Biology 9, 491497.CrossRefGoogle ScholarPubMed
Ray, D.E. (2001) Pyrethroid insecticides: mechanisms of toxicity, systemic poisoning syndromes, paresthesia, and therapy. pp. 12891303 in Krieger, R. Doull, J. & Ecobichon, D. (Eds) Agents, San Diego, Academic Press.Google ScholarPubMed
Read, A.F., Lynch, P.A. & Thomas, M.B. (2009) How to make evolution-proof insecticides for malaria control. PLoS Biology 7, e1000058.CrossRefGoogle ScholarPubMed
Rigby, M.C., Hechinger, R.F. & Stevens, L. (2002) Why should parasite resistance be costly? Trends in Parasitology 18, 116120.CrossRefGoogle ScholarPubMed
Rivero, A., Vezilier, J., Weill, M., Read, A.F. & Gandon, S. (2010) Insecticide control of vector-borne diseases: when is insecticide resistance a problem? PLoS Pathogens 6, e1001000.CrossRefGoogle ScholarPubMed
Roberto, H.K. & Omoto, C. (2006) Fitness cost associated with carbosulfan resistance in Aphis gossypii Glover (Hemiptera: Aphididae). Neotropical Entomology 35, 246250.Google Scholar
Rose, M.R. & Charlesworth, B. (1981 a) Genetics of life history in Drosophila melanogaster. I. Sib analysis of adult females. Genetics 97, 173186.Google ScholarPubMed
Rose, M.R. & Charlesworth, B. (1981 b) Genetics of life history in Drosophila melanogaster. II. Exploratory selection experiments. Genetics 97, 187196.Google ScholarPubMed
Rowland, M. (1991) Behaviour and fitness of gamma HCH/dieldrin resistant and susceptible female Anopheles gambiae and An.stephensi mosquitoes in the absence of insecticide. Medical and Veterinary Entomology 5, 193206.CrossRefGoogle ScholarPubMed
Sacktor, B. & Sanborn, R. (1956) The effect of temperature on oxidative phosphorylation with insect flight muscle mitochondria. Journal of Biophysical and Biochemical Cytology 2, 105107.CrossRefGoogle ScholarPubMed
Santos, M., Fowler, K. & Partridge, L. (1994) Gene-environment interaction for body size and larval density in Drosophila melanogaster: an investigation of effects on development time, thorax length and adult sex ratio. Heredity (Edinb) 72 (Pt 5), 515521.CrossRefGoogle ScholarPubMed
Sanz, A. & Stefanatos, R.K. (2008) The mitochondrial free radical theory of aging: a critical view. Current Aging Science 1, 1021.CrossRefGoogle ScholarPubMed
Schimdt-Nielsen, K. (1997) Energy Metabolism. pp. 169216 in Schimdt-Nielsen, K. (Ed.) Animal Physiology: Adaptation and Environment, New York city, NY, Cambrigde University Press.Google Scholar
Shingleton, A. (2011) Evolution and the regulation of growth and body size. pp. 4355 in Flat, T. & Heyland, A. (Eds) Mechanisms of Life History Evolution. The Genetics and Physiology of Life History Traits and Trade-Offs, New York, Oxford University Press.CrossRefGoogle Scholar
Siegel, J.P., Novak, R.J. & Ruesink, W.G. (1994) Relationship between wing length and dry-weight of mosquitos. Journal of the American Mosquito Control Association 10, 186196.Google Scholar
Soderlund, D.M. (2008) Pyrethroids, knockdown resistance and sodium channels. Pest Management Science 64, 610616.CrossRefGoogle ScholarPubMed
Vulule, J.M., Beach, R.F., Atieli, F.K., McAllister, J.C., Brogdon, W.G., Roberts, J.M., Mwangi, R.W. & Hawley, W.A. (1999) Elevated oxidase and esterase levels associated with permethrin tolerance in Anopheles gambiae from Kenyan villages using permethrin-impregnated nets. Medical and Veterinary Entomology 13, 239244.CrossRefGoogle ScholarPubMed
Wheelock, G.D. & Scott, G.E. (1990) Immunological detection of cytochrome P450 from insecticide resistant and susceptible house flies. Pestic. Biochem. Physiol. 38, 130139.CrossRefGoogle Scholar
WHO (2007) Insecticide-Treated Mosquito Nets: A WHO Position Statement. World Health Organization. Retrieved from http://www.who.int/malaria/publications.Google Scholar
Wiley, R.H. (1974) Evolution of social organization and life-history patterns among grouse. Quaterly Review of Biology 49, 201227.CrossRefGoogle ScholarPubMed
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