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Identification and molecular analysis of mid-gut mucin gene in Anopheles stephensi (Diptera: Culicidae)

Published online by Cambridge University Press:  16 March 2016

Nahid Borhani Dizaji ,
Irene Ricci ,
Guido Favia ,
Claudia Damiani ,
Hamid Reza Basseri ,
Mansour Heidari ,
Saied Reza Naddaf  and
Fatemeh Fotouhi
Nahid Borhani Dizaji
Affiliation:
Department of Medical Entomology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran Department of Parasitology, Pasteur Institute of Iran, Tehran, Iran
Irene Ricci
Affiliation:
School of Biosciences and Biotechnology, University of Camerino, Camerino, Italy
Guido Favia
Affiliation:
School of Biosciences and Biotechnology, University of Camerino, Camerino, Italy
Claudia Damiani
Affiliation:
School of Biosciences and Biotechnology, University of Camerino, Camerino, Italy
Hamid Reza Basseri
Affiliation:
Department of Medical Entomology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
Mansour Heidari
Affiliation:
Department of Medical Genetics, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
Saied Reza Naddaf
Affiliation:
Department of Parasitology, Pasteur Institute of Iran, Tehran, Iran
Fatemeh Fotouhi*
Affiliation:
Influenza Research Lab, Pasteur Institute of Iran, Tehran, Iran
*
*E-mail: fotouhi@pasteur.ac.ir
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Abstract

Recognition of Anopheles mid-gut molecules interacting with the malaria parasite is important as they can potentially be targeted to interrupt the life cycle of the parasite in the mosquito's body. The mid-gut of mosquitoes is covered with the glycocalyx, which is composed of various glycoproteins. Pieces of evidence show that mucin proteins are one of the most frequent ingredients of the glycocalyx. In the present study, we isolated and identified the sequence of mucin from the mid-gut of Anopheles stephensi, Liston and Kazerun strains. Anopheles stephensi mucin (AsMuc) has two central core repeats with the consensus sequence TTTTVAP flanked with a hydrophobic N-terminus and a C-terminus which it seems are both necessary for cell surface expression. To show if this molecule is expressed on the surface of the cell, we cloned AsMuc in a baculovirus vector and tracked the expression of the protein in Sf9 insect cells. Immune assays showed the surface localization of the recombinant mucin. AsMuc expression on the surface of the cell suggests it could be a potential ligand for Plasmodium spp. attachment to the Anopheles mid-gut.

Keywords

Anopheles stephensimucin genemolecular analysislocalization
Type
Research Paper
Information
International Journal of Tropical Insect Science , Volume 36 , Issue 2 , June 2016 , pp. 60 - 69
Copyright
Copyright © icipe 2016 

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References

Abraham, E. G. and Jacobs-Lorena, M. (2004) Mosquito midgut barriers to malaria parasite development. Insect Biochemistry and Molecular Biology 34, 667–671.Google Scholar
Banerjea, A. C. (1930) Some observations on an unusual epidemic of malaria in the city of Lucknow. Indian Medical Gazette 65, 149–153.Google Scholar
Carraway, K. L., Ramsauer, V. P., Haq, B. and Carothers Carraway, C. A. (2003) Cell signaling through membrane mucins. Bioessays 25, 66–71.Google Scholar
Cavener, D. R. (1987) Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Research 15, 1353–1361.Google Scholar
Chaturvedi, P., Singh, A. P. and Batra, S. K. (2008) Structure, evolution, and biology of the MUC4 mucin. The FASEB Journal 22, 966–981.Google Scholar
Dinglasan, R., Fields, I., Shahabuddin, M., Azad, A. F. and Sacci, J. B. (2003) Monoclonal antibody MG96 completely blocks Plasmodium yoelii development in Anopheles stephensi . Infection and Immunity 71, 6995–7001.Google Scholar
Dinglasan, R. and Jacobs-Lorena, M. (2005) Insight into a conserved lifestyle, protein–carbohydrate adhesion strategies of vector-borne pathogens. Infection and Immunity 73, 7797–7807.Google Scholar
Dinglasan, R., Kalume, D. E., Kanzok, S. M., Ghosh, A. K., Muratova, O., Pandey, A. and Jacobs-Lorena, M. (2007) Disruption of Plasmodium falciparum development by antibodies against a conserved mosquito midgut antigen. Proceedings of the National Academy of Sciences 104, 13461–13466.Google Scholar
Hang, H. C. and Bertozzi, C. R. (2005) The chemistry and biology of mucin–type O-linked glycosylation. Bioorganic and Medicinal Chemistry 13, 5021–5034.CrossRefGoogle ScholarPubMed
Injera, E. W., Kabiru, E. W., Gicheru, M. M., Githure, J. I. and Beier, J. C. (2013) Immunopathological features developing in the mosquito midgut after feeding on Anopheles gambiae Mucin-1/Interleukin-12 cDNA immunized mice. Internatinal Journal of Morphology 31, 329–337.Google Scholar
Korgaonkar, N. S., Kumar, A., Yadav, R. S., Kabadi, D. and Dash, A. P. (2012) Mosquito biting activity on humans and detection of Plasmodium falciparum infection in Anopheles stephensi in Goa, India. Indian Journal of Medical Research 135, 120–126.Google Scholar
Kutzler, M. A. and Weiner, D. B. (2008) DNA vaccines, ready for prime time?. Nature Reviews Genetics 9, 776–788.Google Scholar
Lavazec, C. and Bourgouin, C. (2008) Mosquito-based transmission blocking vaccines for interrupting Plasmodium development. Microbes and Infection 10, 845–849.Google Scholar
Manouchehri, A. V., Javadian, E., Eshghy, N. and Motabar, M. (1976). Ecology of Anopheles stephensi in southern Iran. Tropical and Geographical Medicine 28, 228–232.Google Scholar
Morlais, I., Mori, A., Schneider, J. R. and Severson, D. W. (2003) A targeted approach to the identification of candidate genes determining susceptibility to Plasmodium gallinaceum in Aedes aegypti . Molecular Genetics and Genomics 269, 753–764.Google Scholar
Oshaghi, M. A., Yaaghoobi, F., Vatandoost, H., Abaei, M. R. and Akbarzadeh, K. (2006) Anopheles stephensi biological forms; geographical distribution and malaria transmission in malarious regions of Iran. Pakistan Journal of Biological Sciences 9, 294–298 doi. 10.3923.CrossRefGoogle Scholar
Patil, D. P., Atanur, S., Dhotre, D. P., Anantharam, D., Mahajan, V. S., Walujkar, S. A., Chandode, R. K., Kulkarni, G. J., Ghate, P. S., Srivastav, A., Dayananda, K. M., Gupta, N., Bhagwat, B., Joshi, R. R., Mourya, D. T., Patole, M. S. and Shouche, Y. S. (2009) Generation, annotation, and analysis of ESTs from midgut tissue of adult female Anopheles stephensi mosquitoes. BMC Genomics 10, 386. doi 10.1186/1471-2164-10-386.Google Scholar
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
Rudin, W. and Hecker, H. (1989) Lectin–binding sites in the midgut of the mosquitoes Anopheles stephensi Liston and Aedes aegypti L. (Diptera, Culicidae). Parasitology Research 75, 268–279.Google Scholar
Sheehan, J. K., Kesimer, M. and Pickles, R. (2006) Innate immunity and mucus structure and function. Novartis Foundation Symposia 279, 155–166; Discussion 167–169, 216–219.Google Scholar
Shen, Z., Dimopoulos, G., Kafatos, F. C. and Jacobs-Lorena, M. (1999) A cell surface mucin specifically expressed in the midgut of the malaria mosquito Anopheles gambiae . Proceedings of the National Academy of Sciences 96, 5610–5615.CrossRefGoogle ScholarPubMed
Singh, P. K. and Hollingsworth, M. A. (2006) Cell surface–associated mucins in signal transduction. Trends in Cell Biology 16, 467–476.Google Scholar
Subbarao, S. K., Vasantha, K., Adak, T., Sharma, V. P. and Curtis, C. F. (1987) Egg-float ridge number in Anopheles stephensi, ecological variation and genetic analysis. Medical and Veterinary Entomology 1, 265–271.Google Scholar
Sweet, W. C. and Rao, B. (1937) Races of Anopheles stephensi Liston 1901. Indian Medical Gazette 72, 665–674.Google Scholar
United Nations Development Programme/World Bank/World Health Organization. (2000) Malaria Transmission Blocking Vaccines, An Ideal Public Good. WHO, Geneva. 20 pp.Google Scholar
Wang, P. and Granados, R. R. (1997) Molecular cloning and sequencing of a novel invertebrate intestinal mucin cDNA. The Journal of Biological Chemistry 272, 16663–16669.CrossRefGoogle ScholarPubMed
Shi, X. and Jarvis, D. L. (2006) A new RACE method for extremely GC-rich genes. Analytical Biochemistry 356, 222–228.CrossRefGoogle Scholar
Zieler, H., Nawrocki, J. P. and Shahabuddin, M. (1999) Plasmodium gallinaceum ookinetes adhere specifically to the midgut epithelium of Aedes aegypti by interaction with a carbohydrate ligand. The Journal of Experimental Biology 202, 485–495.Google Scholar