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Neotropical Entomology

, Volume 48, Issue 4, pp 706–716 | Cite as

Detrimental Effects of Induced Antibodies on Aedes aegypti Reproduction

  • A N Lule-Chávez
  • E E Avila
  • L E González-de-la-Vara
  • M A Salas-Marina
  • J E IbarraEmail author
Medical and Veterinary Entomology

Abstract

Aedes aegypti (Linnaeus) (Diptera: Culicidae) is the main vector of viruses causing dengue, chikungunya, Zika, and yellow fever, worldwide. This report focuses on immuno-blocking four critical proteins in the female mosquito when fed on blood containing antibodies against ferritin, transferrin, one amino acid transporter (NAAT1), and acetylcholinesterase (AchE). Peptides from these proteins were selected, synthetized, conjugated to carrier proteins, and used as antigens to immunize New Zealand rabbits. After rabbits were immunized, a minimum of 20 female mosquitos were fed on each rabbit, per replicate. No effect in their viability was observed after blood-feeding; however, the number of infertile females was 20% higher than the control when fed on AchE-immunized rabbits. The oviposition period was significantly longer in females fed on immunized rabbits than those fed on control (non-immunized) rabbits. Fecundity (eggs/female) of treated mosquitoes was significantly reduced (about 50%) in all four treatments, as compared with the control. Fertility (hatched larvae) was also significantly reduced in all four treatments, as compared with the control, being the effect on AchE and transferrin the highest, by reducing hatching between 70 and 80%. Survival to the adult stage of the hatched larvae showed no significant effect, as more than 95% survival was observed in all treatments, including the control. In conclusion, immuno-blocking of these four proteins caused detrimental effects on the mosquito reproduction, being the effect on AchE the most significant.

Keywords

Immuno-blocking, fertility, ferritin, transferrin, amino acid transporter, acetylcholinesterase 

Notes

Acknowledgments

Authors express their gratitude to the excellent technical support of Javier Luévano-Borroel, Regina Basurto-Ríos, and Mayra Rodríguez-Solís.

Authors’ Contribution Statement

ANLC developed most of the experimental work as an MSc thesis under the technical supervision of JEI, EEA, and MASM. LGV contributed with some of the theoretical bases for the selection of critical proteins and active peptides. JEI was the leader of the group and contributed with the project design and general management and supervision. He also obtained the financial support for the project.

Funding Information

This work was supported by Consejo Nacional de Ciencia y Tecnología (CONACYT, Mexico), project number 258878.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. Abdeladhim M, Kamhawi S, Valenzuela JG (2014) What’s behind a sand fly bite? The profound effect of sand fly saliva on host hemostasis, inflammation and immunity. Infection Infect Genet Evol 28:691–703CrossRefGoogle Scholar
  2. Alger NE, Cabrera EJ (1972) An increase in death rate of Anopheles stephensi fed on rabbits immunized with mosquito antigen. J Econ Entomol 65:165–168CrossRefGoogle Scholar
  3. Ameku T, Niwa R (2016) Mating-induced increase in germline stem cells via the neuroendocrine system in female Drosophila. PLoS Genet 12:e1006123CrossRefGoogle Scholar
  4. Bartfeld NS, Law JW (1990) Isolation and molecular cloning of transferrin from the tobacco hornworm, Manduca sexta. Sequence similarity to the vertebrate transferrins. J Biol Chem 265:21684–21691Google Scholar
  5. Billingsley PF, Foy B, Rasgon JL (2008) Mosquitocidal vaccines: a neglected addition to malaria and dengue control strategies. Trends Parasitol 24:396–400CrossRefGoogle Scholar
  6. Bomford A, Munro H (1992) Ferritin gene expression in health and malignancy. PATHOBIOLOGY 60:10–18CrossRefGoogle Scholar
  7. Canals M (1996) Insectos hematófagos y sus enfermedades. TecnoVet 2:1–4Google Scholar
  8. Carlier PR, Bloomquist JR, Totrov M, Li J (2017) Discovery of species-selective and resistance-breaking anticholinesterase insecticides for the malaria mosquito. Curr Med Chem 24:2946–2958CrossRefGoogle Scholar
  9. Cole C, Barber JD, Barton GJ (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36:W197–W201CrossRefGoogle Scholar
  10. Diallo M, Dia I, Diallo D, Diagne CT, Ba Y, Yactayo S (2016) Perspectives and challenges in entomological risk assessment and vector control of chikungunya. J Infect Dis 214:S459–S465CrossRefGoogle Scholar
  11. Dunkov BC, Zhang D, Choumarov K, Winzerling JJ, Law JH (1995) Isolation and characterization of mosquito ferritin and cloning of a cDNA that encodes one subunit. Arch Insect Biochem Physiol 29:293–307CrossRefGoogle Scholar
  12. Evans AM, Aimanova KG, Gill SS (2009) Characterization of a blood-meal-responsive proton-dependent amino acid transporter in the disease vector, Aedes aegypti. J Exp Biol 212:3263–3271CrossRefGoogle Scholar
  13. Foy BD, Killeen GF, Magalhaes T, Beier JC (2002) Immunological targeting of critical insect antigens. J Econ Entomol 48:150–163Google Scholar
  14. Harizanova N, Georgieva T, Dunkov B, Yoshiga T, Law J (2005) Aedes aegypti transferrin. Gene structure, expression pattern, and regulation. Insect Mol Biol 14:79–88CrossRefGoogle Scholar
  15. Hatfield PR (1988) Anti-mosquito antibodies and their effects on feeding, fecundity and mortality of Aedes aegypti. Med Vet Entomol 2:331–338CrossRefGoogle Scholar
  16. Heifetz Y, Lindner M, Garini Y, Wolfner MF (2014) Mating regulates neuromodulator ensembles at nerve termini innervating the Drosophila reproductive tract. Curr Biol 24:731–737CrossRefGoogle Scholar
  17. Jacobs-Lorena M, Lemos FJA (1995) Immunological strategies for control of insect disease vectors: a critical assessment. Trends Parasitol 11:144–147Google Scholar
  18. Jin X, Aimanova K, Ross LS, Gill SS (2003) Identification, functional characterization and expression of a LAT type amino acid transporter from the mosquito Aedes aegypti. Insect Biochem Mol Biol 33:815–827CrossRefGoogle Scholar
  19. Johnston LAY, Kemp DH, Pearson RD (1986) Immunization of cattle against Boophilus microplus using extracts derived from adult female ticks: effects of induced immunity on tick populations. Int J Parasitol Parasites Wildl 16:27–34CrossRefGoogle Scholar
  20. Law JH (2002) Insects, oxygen, and iron. Biochem Biophys Res Commun 292:1191–1195CrossRefGoogle Scholar
  21. McDowell MA (2015) Vector-transmitted disease vaccines: targeting salivary proteins in transmission (SPIT). Trends Parasitol 31:363–372CrossRefGoogle Scholar
  22. Meyers JI, Foy BD (2017) Effect of host blood–derived antibodies targeting critical mosquito neuronal receptors and other proteins: disruption of vector physiology and potential for disease control. In: Arthropod vector: controller of disease transmission, vol 1. Wikel S, Aksoy S, Dimopoulos G, eds) Academic Press. New York, USA, pp 143–160CrossRefGoogle Scholar
  23. Meyers JI, Gray M, Foy BD (2015) Mosquitocidal properties of IgG targeting the glutamate-gated chloride channel in three mosquito disease vectors (Diptera: Culicidae). J Exp Biol 218:1487–1495CrossRefGoogle Scholar
  24. Nene V, Wortman JR, Lawson D, Haas B, Kodira C, Tu ZJ, Ren Q (2007) Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316:1718–1723CrossRefGoogle Scholar
  25. Ramasamy MS, Ramasamy R, Kay BH, Kidson C (1988) Anti-mosquito antibodies decrease the reproductive capacity of Aedes aegypti. Med Vet Entomol 2:87–93CrossRefGoogle Scholar
  26. Rey JR (2006) The mosquito. Entomology and Nematology Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida, ENY-727Google Scholar
  27. Rose G (2001) Sick individuals and sick populations. Int J Epidemiol 30:427–432CrossRefGoogle Scholar
  28. Sanders HR, Evans AM, Ross LS, Gill SS (2003) Blood meal induces global changes in midgut gene expression in the disease vector, Aedes aegypti. Insect Biochem Mol Biol 33:1105–1122CrossRefGoogle Scholar
  29. Shahabuddin M, Lemos F, Kaslow DC, Jacobs-Lorena M (1996) Antibody-mediated inhibition of Aedes aegypti midgut trypsins blocks sporogonic development of Plasmodium gallinaceum. Infect Immun 64:739–743Google Scholar
  30. Shen Z, Jacobs-Lorena M (1998) Nuclear factor recognition sites in the gut-specific enhancer region of an Anopheles gambiae trypsin gene. Insect Biochem Mol Biol 28:1007–1012CrossRefGoogle Scholar
  31. Sutherland GB, Ewen AB (1974) Fecundity decrease in mosquitoes ingesting blood from specifically sensitized mammals. J Insect Physiol 20:655–660CrossRefGoogle Scholar
  32. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  33. Toutant JP (1989) Insect acetylcholinesterase: catalytic properties, tissue distribution and molecular forms. Prog Neurobiol 32:423–446CrossRefGoogle Scholar
  34. Trager W (1939) Acquired immunity to ticks. J Parasitol 25:57–81CrossRefGoogle Scholar
  35. Vargas J (2003) Prevención y control de la malaria y otras enfermedades transmitidas por vectores en el Perú. Rev peru epidemiol 11:1–18Google Scholar
  36. Vaughan J, Azad A (1988) Passage of host immunoglobulin G from blood meal into hemolymph of selected mosquito species (Diptera: Culicidae). J Med Entomol 25:472–474CrossRefGoogle Scholar
  37. VenkatRao V, Kumar SK, Sridevi P, Muley V, Chaitanya RK (2017) Cloning, characterization and transmission blocking potential of midgut carboxypeptidase A in Anopheles stephensi. Acta Trop 168:21–28CrossRefGoogle Scholar
  38. Villalon J, Ghosh A, Jacobs-Lorena M (2003) The peritrophic matrix limits the rate of digestion in adult Anopheles stephensi and Aedes aegypti mosquitoes. J Insect Physiol 49:891–895CrossRefGoogle Scholar
  39. Wijffels G, Fitzgerald C, Gough J, Riding G, Elvin C, Kemp D, Willadsen P (1996) Cloning and characterisation of angiotensin-converting enzyme from the dipteran species, Haematobia irritans exigua, and its expression in the maturing male reproductive system. Eur J Biochem 237:414–423CrossRefGoogle Scholar
  40. Willadsen P (2001) The molecular revolution in the development of vaccines against ectoparasites. Vet Parasitol 101:353–368CrossRefGoogle Scholar
  41. Willadsen P, Riding GA, McKenna RV, Kemp DH, Tellam RL, Nielsen JN, Gough JM (1989) Immunologic control of a parasitic arthropod. Identification of a protective antigen from Boophilus microplus. J Immunol 143:1346–1351Google Scholar
  42. Womack M (1993) The yellow fever mosquito, Aedes aegypti. Wing Beats 5:4Google Scholar
  43. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40CrossRefGoogle Scholar

Copyright information

© Sociedade Entomológica do Brasil 2019

Authors and Affiliations

  1. 1.Depto de Biotecnología y BioquímicaCentro de Investigación y de Estudios Avanzados del IPNIrapuatoMexico
  2. 2.Depto de BiologíaUniv de GuanajuatoGuanajuatoMexico

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