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Differential induction of proteins in Anopheles gambiae sensu stricto (Diptera: Culicidae) larvae in response to heavy metal selection

Published online by Cambridge University Press:  01 December 2006

Paul Odhiambo Mireji ,
Joseph Keating ,
Eucharia Kenya ,
Charles Mbogo ,
Hudson Nyambaka ,
Ellie Osir ,
John Githure  and
John Beier
Paul Odhiambo Mireji*
Affiliation:
Department of Biochemistry, Kenyatta University, PO Box 43844, Nairobi, 00100, Kenya Molecular Biology and Biotechnology Division, International Centre of Insect Physiology and Ecology, PO Box 30772, Nairobi, 00100, Kenya
Joseph Keating
Affiliation:
International Health and Development, School of Public Health and Tropical Medicine, Tulane University, New Orleans, LA 70112 USA
Eucharia Kenya
Affiliation:
Department of Biochemistry, Kenyatta University, PO Box 43844, Nairobi, 00100, Kenya
Charles Mbogo
Affiliation:
Center for Geographic Medicine Research-Coast, Kenya Medical Research Institute (KEMRI), PO Box 4281, Kilifi, Kenya
Hudson Nyambaka
Affiliation:
Department of Chemistry, Kenyatta University, PO Box 43844, Nairobi, 00100, Kenya
Ellie Osir
Affiliation:
Molecular Biology and Biotechnology Division, International Centre of Insect Physiology and Ecology, PO Box 30772, Nairobi, 00100, Kenya
John Githure
Affiliation:
Human Health Division, International Centre of Insect Physiology and Ecology, PO Box 30772, Nairobi, 00100, Kenya
John Beier
Affiliation:
Department of Epidemiology and Public Health, University of Miami, Miami, FL 33177, USA
*
* E-mail: [email protected]
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Abstract

Investigations were conducted to establish the magnitude and pattern of differential expression of proteins due to generational selection of third instar Anopheles gambiae s.s. Giles larvae by cadmium, copper and lead heavy metals, the three possible common urban pollutants.

A susceptible strain of A. gambiae s.s. third instar larvae was separately placed under selection pressure with cadmium, copper and lead at LC30 and controls through five generations. First, third and fifth generation selection survivors were screened for differentially expressed proteins relative to non-exposed control by two-dimensional gel electrophoresis. Distribution patterns of the spots were analyzed by χ2 or Fishers' exact test and variations in expressions between and within generations by ANOVA. Most differentially expressed spots were acidic and of low molecular weight among all metals and generations. Type of heavy metal and generation were the main indicators of variations in differential expressions. Variation between generations was most significant among cadmium-selected populations of which the most number of spots were induced in the fifth generation. Most spots were induced in the copper-selected population in the third generation. The induced protein spots may be the products from respective genes that respond to heavy metals and counter their toxicity, thus building A. gambiae s.s. tolerance to these pollutants. The differential pattern and magnitude of expressed spots have potential application as molecular markers for assessment of anopheline adaptation status to heavy metals, and provide insight into the extent of environmental pollution.

Des études ont été menées afin d'estimer l'incidence de l'effet génération sur l'importance et les modalités d'expression différentielle des protéines sur des larves de 3ème stade d'Anopheles gambiae s.s. Giles élevées avec du cadmium, du cuivre et du plomb, qui sont des métaux lourds polluants, fréquemment rencontrés dans les zones urbaines. On a élevé pendant cinq générations une souche sensible de larves de 3ème stade d'A. gambiae séparément avec du cadmium, du cuivre et du plomb, à la dose DL30. Les survivants de la 1ère, 3ème et 5ème génération ont été testés par rapport aux témoins pour leur expression différentielle des protéines à l'aide d'une électrophorèse sur gel bidimensionnelle. Le mode de distribution des tâches a été analysé à l'aide des tests du χ2 et de Fisher et les variations de l'expression intra- et inter générations à l'aide d'une ANOVA. La plupart des tâches correspondent à des acides de faibles poids moléculaires pour tous les métaux et quelle que soit la génération. L'expression différentielle est fortement déterminée par le type de métal lourd et la génération. Les différences entre générations ont été les plus prononcées sur la population élevée avec du cadmium avec un plus grand nombre de tâches à la 5ème génération. La plupart des tâches ont été induites dès la 3ème génération pour la population élevée avec du cuivre. Les tâches de protéines induites peuvent être le résultat de l'expression de gènes spécifiques en réponse aux métaux lourds afin de contrecarrer leur toxicité, ce qui favorise la sélection de larves d'A. gambiae tolérantes aux polluants. Les modalités d'expression et l'importance des tâches ont une application potentielle comme marqueurs moléculaires pour l'estimation des capacités d'adaptation des anophèles aux métaux lourds. Elles permettent en outre d'apprécier l'étendue de la pollution environnementale.

Keywords

Métaux lourdsAnopheles gambiae sensu strictoadaptationtoléranceexpression différentielleheavy metalsAnopheles gambiae sensu strictoadaptationtolerancedifferential expression
Type
Research Paper
Information
International Journal of Tropical Insect Science , Volume 26 , Issue 4 , December 2006 , pp. 214 - 226
Copyright
Copyright © ICIPE 2006

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References

Abe, T., Konishi, T., Katoh, T., Hirano, H., Matsukuma, K., Kashimura, M. and Higashi, K. (1994) Induction of heat shock 70 mRNA by cadmium is mediated by glutathione suppressive and non-suppressive triggers. Biochimica et Biophysica Acta 1201, 29–36.CrossRefGoogle ScholarPubMed
Bagchi, D., Bagchi, M., Hassoun, E. A. and Stohs, S. J. (1996) Cadmium-induced excretion of urinary lipid metabolites, DNA damage, glutathione depletion, and hepatic lipid peroxidation in Sprague–Dawley rats. Biological Trace Element Research 52, 143–154.CrossRefGoogle ScholarPubMed
Beyersmann, D. and Hechtenberg, S. (1997) Cadmium, gene regulation and cellular signaling in mammalian cells. Toxicology and Applied Pharmacology 144, 247–261.CrossRefGoogle ScholarPubMed
Biney, C., Amazu, A. T., Calamari, D., Kaba, N., Mbome, I. L., Naeve, H., Ochumba, P. B. O., Osibanjo, O., Radegonde, V. and Saad, M. A. H. (1994) Review of heavy metals in the African aquatic environment. Ecotoxicology and Environmental Safety 28, 134–159.CrossRefGoogle ScholarPubMed
Bolnick, D. I. (2001) Intraspecific competition favours niche width expansion in Drosophila melanogaster. Nature 410, 463–466.CrossRefGoogle ScholarPubMed
Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
Busvine, J. R. (1971) A Critical Review of the Techniques for the Testing of Insecticides. Farnham Royal, Commonwealth Agricultural Bureaux, London. 345 pp.Google Scholar
Chin, T. A. and Templeton, D. M. (1993) Protective elevations of glutathione and metallothionein in cadmium-exposed mesangial cells. Toxicology 77, 145–156.CrossRefGoogle ScholarPubMed
Chinery, W. A. (1984) Effects of ecological changes on the malaria vectors Anopheles funestus and Anopheles gambiae complex of mosquitoes in Accra, Ghana. Journal of Tropical Medicine and Hygiene 87, 75–81.Google ScholarPubMed
Chinery, W. A. (1995) Impact of rapid urbanization on mosquitoes and their disease transmission potential in Accra and Tema, Ghana. African Journal of Medical Science 24, 179–188.Google ScholarPubMed
Clements, W. H. and Kifney, P. M. (1994) Integrated laboratory and field approach for assessing impact of heavy metals at the Arkansas River, Colorado. Environmental Toxicology and Chemistry 7, 715–722.CrossRefGoogle Scholar
Coene, J. (1993) Malaria in urban and rural Kinshasa: The entomological input. Medical and Veterinary Entomology 7, 127–137.CrossRefGoogle Scholar
Coluzzi, M. (1993) Advances in the study of Afrotropical malaria vectors. Parasitologia 35, 23–29.Google Scholar
Coluzzi, M. (1994) Malaria and the Afrotropical ecosystems: Impact of man-made environmental changes. Parasitologia 36, 223–227.Google ScholarPubMed
Coluzzi, M., Sabatini, A., Petrarca, V. and Di Deco, M. A. (1979) Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 483–497.CrossRefGoogle ScholarPubMed
Coogan, T. P., Bare, R. M., Bjornson, E. J. and Waalkes, M. P. (1994) Enhanced metallothionein gene expression is associated with protection from cadmium-induced genotoxicity in cultured rat liver cells. Journal of Toxicology and Environmental Health 41, 233–245.CrossRefGoogle ScholarPubMed
Finney, D. J. (1971) Probit Analysis. Cambridge University Press, London. 668 pp.Google Scholar
Goldstein, G. W. (1993) Evidence that lead acts as a calcium substitute in second messenger metabolism. Neurotoxicology 14, 97–101.Google ScholarPubMed
Gros, P., Croop, J. and Housman, D. (1986) Mammalian multi-drug resistance gene: Complete cDNA sequence indicates strong homology to bacterial transport proteins. Cell 47, 371–380.CrossRefGoogle Scholar
Hare, L. (1992) Aquatic insects and trace metals: Bio-availability, bio-accumulation and toxicity. Critical Reviews in Toxicology 22, 327–369.CrossRefGoogle Scholar
Hechtenberg, S., Schafer, T., Benters, J. and Beyersmann, D. (1996) Effects of cadmium on cellular calcium and proto-oncogene expression. Annals of Clinical and Laboratory Science 26, 512–521.Google ScholarPubMed
Hipfner, D. R., Deeley, R. G. and Cole, S. P. C. (1999) Structural, mechanistic and clinical aspects of MRP1. Biochimica et Biophysica Acta 1461, 359–376.CrossRefGoogle ScholarPubMed
Holt, R. A., Subramanian, G. M., Halpern, A., Sutton, G. G., Charlab, R., Nusskern, D. R., Wincker, P., Clark, A. G., Ribeiro, J. M., Wides, R., Salzberg, S. L., Loftus, B., Yandell, M., Majoros, W. H., Rusch, D. B., Lai, Z., Kraft, C. L., Abril, J. F., Anthouard, V., Arensburger, P., Atkinson, P. W., Baden, H., de Berardinis, V., Baldwin, D., Benes, V., Biedler, J., Blass, C., Bolanos, R., Boscus, D., Barnstead, M., Cai, S., Center, A., Chaturverdi, K., Christophides, G. K., Chrystal, M. A., Clamp, M., Cravchik, A., Curwen, V., Dana, A., Delcher, A., Dew, I., Evans, C. A., Flanigan, M., Grundschober-Freimoser, A., Friedli, L., Gu, Z., Guan, P., Guigo, R., Hillenmeyer, M. E., Hladun, S. L., Hogan, J. R., Hong, Y. S., Hoover, J., Jaillon, O., Ke, Z., Kodira, C., Kokoza, E., Koutsos, A., Letunic, I., Levitsky, A., Liang, Y., Lin, J. J., Lobo, N. F., Lopez, J. R., Malek, J. A., McIntosh, T. C., Meister, S., Miller, J., Mobarry, C., Mongin, E., Murphy, S. D., O'Brochta, D. A., Pfannkoch, C., Qi, R., Regier, M. A., Remington, K., Shao, H., Sharakhova, M. V., Sitter, C. D., Shetty, J., Smith, T. J., Strong, R., Sun, J., Thomasova, D., Ton, L. Q., Topalis, P., Tu, Z., Unger, M. F., Walenz, B., Wang, A., Wang, J., Wang, M., Wang, X., Woodford, K. J., Wortman, J. R., Wu, M., Yao, A., Zdobnov, E. M., Zhang, H., Zhao, Q., Zhao, S., Zhu, S. C., Zhimulev, I., Coluzzi, M., della Torre, A., Roth, C. W., Louis, C., Kalush, F., Mural, R. J., Myers, E. W., Adams, M. D., Smith, H. O., Broder, S., Gardner, M. J., Fraser, C. M., Birney, E., Bork, P., Brey, P. T., Venter, J. C., Weissenbach, J., Kafatos, F. C., Collins, F. H. and Hoffman, S. L. (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298, 129–149.CrossRefGoogle ScholarPubMed
Hurkman, W. J. and Tanaka, C. K. (1986) Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiology 81, 802–806.CrossRefGoogle ScholarPubMed
Jin, P. and Ringertz, N. R. (1990) Cadmium induces transcription of proto-oncogenes c-jun and c-myc in rat L6 myoblasts. Biological Chemistry 265, 14061–14064.CrossRefGoogle ScholarPubMed
Kaji, T., Suzuki, M., Yamamoto, C., Imaki, Y., Mishima, A., Fujiwara, Y., Sakamoto, M. and Kozuka, H. (1994) Induction of metallothionein synthesis by bismuth in cultured vascular endothelial cells. Research Communications in Molecular Pathology and Pharmacology 86, 25–35.Google ScholarPubMed
Kim, K. A., Chakraborti, T., Goldstein, G. W. and Bressler, J. P. (2000) Immediate early gene expression in PC12 cells exposed to lead: Requirement for protein kinase C. Journal of Neurochemistry 74, 1140–1146.CrossRefGoogle ScholarPubMed
Klerks, P. L. and Weis, J. S. (1987) Genetic adaptation to heavy metals in aquatic organisms: A review. Environmental Pollution 45, 173–205.CrossRefGoogle ScholarPubMed
König, J., Nies, A. T., Cui, Y., Leier, I. and Keppler, D. (1999) Conjugate export pumps of the multidrug resistance protein (MRP) family: Localization, substrate specificity, and MRP2-mediated drug resistance. Biochimica et Biophysica Acta 1461, 377–394.CrossRefGoogle ScholarPubMed
Kramer, K. K., Liu, J., Choudhuri, S. and Klaassen, C. D. (1996) Induction of metallothionein mRNA and protein in murine astrocyte cultures. Toxicology and Applied Pharmacology 136, 94–100.CrossRefGoogle ScholarPubMed
Krantzberg, G. and Stokes, P. M. (1990) Metal concentration and tissue distribution in larvae of Chironomus with reference to X-ray microprobe analysis. Archives of Environmental Contamination and Toxicology 19, 84–93.CrossRefGoogle Scholar
Liao, V. H. and Freedman, J. H. (1998) Cadmium-regulated genes from the nematode Caenorhabditis elegans. Identification and cloning of new cadmium-responsive genes by differential display. Journal of Biological Chemistry 273, 31962–31970.CrossRefGoogle ScholarPubMed
Maroni, G. and Watson, D. (1985) Uptake and binding of cadmium, copper and zinc by Drosophila melanogaster larvae. Insect Biochemistry 15, 55–63.CrossRefGoogle Scholar
Matsuoka, M. and Call, K. M. (1995) Cadmium-induced expression of immediate early genes in LLC-PK1 cells. Kidney International 48, 383–389.CrossRefGoogle ScholarPubMed
O'Farrell, P. H. (1975) High resolution two-dimensional electrophoresis of proteins. Journal of Biological Chemistry 250, 4007–4021.CrossRefGoogle ScholarPubMed
Ovelgonne, J. H., Souren, J. E., Wiegant, F. A. and Van Wijk, R. (1995) Relationship between cadmium-induced expression of heat-shock genes, inhibition of protein synthesis and cell death. Toxicology 99, 19–30.CrossRefGoogle ScholarPubMed
Rayms-Keller, A., Olson, K. E., McGaw, M., Oray, C., Carlson, J. O. and Beaty, B. J. (1998) Effect of heavy metals on Aedes aegypti (Diptera: Culicidae) larvae. Ecotoxicology and Environmental Safety 39, 41–47.CrossRefGoogle ScholarPubMed
Rayms-Keller, A., McGaw, M., Oray, C., Carlson, J. O. and Beaty, B. J. (2000) Molecular cloning and characterization of a metal responsive Aedes aegypti intestinal mucin cDNA. Insect Molecular Biology 9, 419–426.CrossRefGoogle ScholarPubMed
Salovsky, P., Shopova, V., Dancheva, V. and Marev, R. (1992) Changes in antioxidant lung protection after single intra-tracheal cadmium acetate instillation in rats. Human and Experimental Toxicology 11, 217–222.CrossRefGoogle ScholarPubMed
Shimizu, M., Hochadel, J. F. and Waalkes, M. P. (1997) Effects of glutathione depletion on cadmium-induced metallothionein synthesis, cytotoxicity, and proto-oncogene expression in cultured rat myoblasts. Journal of Toxicology and Environmental Health 51, 609–621.CrossRefGoogle ScholarPubMed
Singhal, R. K., Anderson, M. E. and Meister, A. (1987) Glutathione, a first line of defense against cadmium toxicity. FASEB Journal 1, 220–223.CrossRefGoogle ScholarPubMed
Stohs, S. J., Bagchi, D., Hassoun, E. and Bagchi, M. (2001) Oxidative mechanisms in the toxicity of chromium and cadmium ions. Journal of Environmental Pathology, Toxicology and Oncology 20, 77–88.CrossRefGoogle ScholarPubMed
Suzuki, K. T., Sunaga, H., Aoki, Y., Hatakeyama, S., Sugaya, Y., Sumi, Y. and Suzuki, T. (1988) Binding of cadmium and copper in the mayfly Baetis thermicus larvae that inhabit a river polluted with heavy metals. Comparative Biochemistry and Physiology 91C, 487–492.Google Scholar
Terracio, L. and Nachtigal, M. (1988) Oncogenicity of rat prostate cells transformed in vitro with cadmium chloride. Archives of Toxicology 61, 450–456.CrossRefGoogle ScholarPubMed
Toure, Y. T., Petrarca, V., Traore, S. F., Coulibaly, A., Maiga, H. M., Sankare, O., Sow, M., Di, D. M. A. and Coluzzi, M. (1998) The distribution and inversion polymorphism of chromosomally recognized taxa of the Anopheles gambiae complex in Mali, West Africa. Parasitologia 40, 477–511.Google ScholarPubMed
Trape, J. F. and Zoulani, A. (1987) Malaria and urbanization in central Africa: The example of Brazzaville. Part II: Results of entomological surveys and epidemiological analysis. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 10–18.CrossRefGoogle ScholarPubMed
Wentsel, R., McIntosh, A. and Atchinson, G. (1978) Evidence of resistance to metals in larvae of the midge Chironomus tentans in a metal contaminated lake. Bulletin of Environmental Contamination and Toxicology 20, 451–455.CrossRefGoogle Scholar
Zhang, B., Egli, D., Georgiev, O. and Schaffner, W. (2001) The Drosophila homolog of mammalian zinc finger factor MTF-1 activates transcription in response to heavy metals. Molecular and Cellular Biology 21, 4505–4514.CrossRefGoogle ScholarPubMed