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BioMed Research International
Volume 2013 (2013), Article ID 875958, 11 pages
Proteomic Identification of Dengue Virus Binding Proteins in Aedes aegypti Mosquitoes and Aedes albopictus Cells
1Department of Genetics and Molecular Biology, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, 07360 Mexico, DF, Mexico
2Coordinación Academica, Universidad Autónoma de la Ciudad de México, 06720 Mexico, DF, Mexico
3Department of Biochemestry, Faculty of Medicine, Universidad Nacional Autonoma de México, Edificio de Investigación, 04510 Mexico, DF, Mexico
4Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO 80523-0015, USA
Received 8 April 2013; Revised 19 September 2013; Accepted 25 September 2013
Academic Editor: Vittorio Sambri
Copyright © 2013 Maria de Lourdes Muñoz et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- P. Reiter, “Global-warming and vector-borne disease in temperate regions and at high altitude,” The Lancet, vol. 351, no. 9105, pp. 839–840, 1998.
- W. J. Tabachnick, “Challenges in predicting climate and environmental effects on vector-borne disease episystems in a changing world,” Journal of Experimental Biology, vol. 213, no. 6, pp. 946–954, 2010.
- R. Rico-Hesse, “Molecular evolution and distribution of dengue viruses type 1 and 2 in nature,” Virology, vol. 174, no. 2, pp. 479–493, 1990.
- J. A. Lewis, G.-J. Chang, R. S. Lanciotti, R. M. Kinney, L. W. Mayer, and D. W. Trent, “Phylogenetic relationships of Dengue-2 viruses,” Virology, vol. 197, no. 1, pp. 216–224, 1993.
- R. S. Lanciotti, J. G. Lewis, D. J. Gubler, and D. W. Trent, “Molecular evolution and epidemiology of dengue-3 viruses,” Journal of General Virology, vol. 75, no. 1, pp. 65–75, 1994.
- S. S. Twiddy, J. J. Farrar, N. V. Chau et al., “Phylogenetic relationships and differential selection pressures among genotypes of dengue-2 virus,” Virology, vol. 298, no. 1, pp. 63–72, 2002.
- M. G. Guzman, S. B. Halstead, H. Artsob et al., “Dengue: a continuing global threat,” Nature Reviews, vol. 8, 12, pp. S7–S16, 2010.
- M. de Lourdes Muñoz, A. Cisneros, J. Cruz, P. Das, R. Tovar, and A. Ortega, “Putative dengue virus receptors from mosquito cells,” FEMS Microbiology Letters, vol. 168, no. 2, pp. 251–258, 1998.
- R. F. Mercado-Curiel, W. C. Black IV, and M. D. L. Mũoz, “A dengue receptor as possible genetic marker of vector competence in Aedes aegypti,” BMC Microbiology, vol. 8, article 118, 2008.
- S. W. Gollins and J. S. Porterfield, “Flavivirus infection enhancement in macrophages: an electron microscopic study of viral cellular entry,” Journal of General Virology, vol. 66, no. 9, pp. 1969–1982, 1985.
- J. J. H. Chu and M. L. Ng, “Infectious entry of West Nile virus occurs through a clathrin-mediated endocytic pathway,” Journal of Virology, vol. 78, no. 19, pp. 10543–10555, 2004.
- C. Mosso, I. J. Galván-Mendoza, J. E. Ludert, and R. M. del Angel, “Endocytic pathway followed by dengue virus to infect the mosquito cell line C6/36 HT,” Virology, vol. 378, no. 1, pp. 193–199, 2008.
- H. M. Van der Schaar, M. J. Rust, C. Chen et al., “Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells,” PLoS Pathogens, vol. 4, no. 12, Article ID e1000244, 2008.
- H. Bielefeldt-Ohmann, “Analysis of antibody-independent binding of dengue viruses and dengue virus envelope protein to human myelomonocytic cells and B lymphocytes,” Virus Research, vol. 57, no. 1, pp. 63–79, 1998.
- J. Ramos-Castañeda, J. L. Imbert, B. L. Barrón, and C. Ramos, “A 65-kDa trypsin-sensible membrane cell protein as a possible receptor for dengue virus in cultured neuroblastoma cells,” Journal of NeuroVirology, vol. 3, no. 6, pp. 435–440, 1997.
- P. Hilgard and R. Stockert, “Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes,” Hepatology, vol. 32, no. 5, pp. 1069–1077, 2000.
- H. Ni, K. D. Ryman, H. Wang et al., “Interaction of yellow fever virus french neurotropic vaccine strain with monkey brain: characterization of monkey brain membrane receptor escape variants,” Journal of Virology, vol. 74, no. 6, pp. 2903–2906, 2000.
- M. M. B. Moreno-Altamirano, F. J. Sánchez-García, and M. L. Muñoz, “Non Fc receptor-mediated infection of human macrophages by dengue virus serotype 2,” Journal of General Virology, vol. 83, no. 5, pp. 1123–1130, 2002.
- B. Tassaneetrithep, T. H. Burgess, A. Granelli-Piperno et al., “DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells,” Journal of Experimental Medicine, vol. 197, no. 7, pp. 823–829, 2003.
- M. Y. Mendoza, J. S. Salas-Benito, H. Lanz-Mendoza, S. Hernández-Martinez, and R. M. Del Angel, “A putative receptor for dengue virus in mosquito tissues: localization of a 45-KDA glycoprotein,” The American Journal of Tropical Medicine and Hygiene, vol. 67, no. 1, pp. 76–84, 2002.
- H.-Y. Chee and S. AbuBakar, “Identification of a 48 kDa tubulin or tubulin-like C6/36 mosquito cells protein that binds dengue virus 2 using mass spectrometry,” Biochemical and Biophysical Research Communications, vol. 320, no. 1, pp. 11–17, 2004.
- B. K. Thaisomboonsuk, E. T. Clayson, S. Pantuwatana, D. W. Vaughn, and T. P. Endy, “Characterization of dengue-2 virus binding to surfaces of mammalian and insect cells,” The American Journal of Tropical Medicine and Hygiene, vol. 72, no. 4, pp. 375–383, 2005.
- R. F. Mercado-Curiel, H. A. Esquinca-Avilés, R. Tovar, Á. Díaz-Badillo, M. Camacho-Nuez, and M. D. L. Muñoz, “The four serotypes of dengue recognize the same putative receptors in Aedes aegypti midgut and Ae. albopictus cells,” BMC Microbiology, vol. 6, article 85, 2006.
- P. Sakoonwatanyoo, V. Boonsanay, and D. R. Smith, “Growth and production of the dengue virus in C6/36 cells and identification of a laminin-binding protein as a candidate serotype 3 and 4 receptor protein,” Intervirology, vol. 49, no. 3, pp. 161–172, 2006.
- J.-J. Hung, M.-T. Hsieh, M.-J. Young, C.-L. Kao, C.-C. King, and W. Chang, “An external loop region of domain III of dengue virus type 2 envelope protein is involved in serotype-specific binding to mosquito but not mammalian cells,” Journal of Virology, vol. 78, no. 1, pp. 378–388, 2004.
- F. A. Rey, F. X. Heinz, C. Mandl, C. Kunz, and S. C. Harrison, “The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution,” Nature, vol. 375, no. 6529, pp. 291–298, 1995.
- Y. Modis, S. Ogata, D. Clements, and S. C. Harrison, “A ligand-binding pocket in the dengue virus envelope glycoprotein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 12, pp. 6986–6991, 2003.
- Y. Modis, S. Ogata, D. Clements, and S. C. Harrison, “Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein,” Journal of Virology, vol. 79, no. 2, pp. 1223–1231, 2005.
- Y. Chen, T. Maguire, and R. M. Marks, “Demonstration of binding of dengue virus envelope protein to target cells,” Journal of Virology, vol. 70, no. 12, pp. 8765–8772, 1996.
- W. D. Crill and J. T. Roehrig, “Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are the most efficient blockers of virus adsorption to vero cells,” Journal of Virology, vol. 75, no. 16, pp. 7769–7773, 2001.
- J. J. H. Chu, R. Rajamanonmani, J. Li, R. Bhuvananakantham, J. Lescar, and M.-L. Ng, “Inhibition of West Nile virus entry by using a recombinant domain III from the envelope glycoprotein,” Journal of General Virology, vol. 86, no. 2, pp. 405–412, 2005.
- G. D. Gromowski and A. D. T. Barrett, “Characterization of an antigenic site that contains a dominant, type-specific neutralization determinant on the envelope protein domain III (ED3) of dengue 2 virus,” Virology, vol. 366, no. 2, pp. 349–360, 2007.
- J. F. L. Chin, J. J. H. Chu, and M. L. Ng, “The envelope glycoprotein domain III of dengue virus serotypes 1 and 2 inhibit virus entry,” Microbes and Infection, vol. 9, no. 1, pp. 1–6, 2007.
- K.-C. Huang, M.-C. Lee, C.-W. Wu, K.-J. Huang, H.-Y. Lei, and J.-W. Cheng, “Solution structure and neutralizing antibody binding studies of domain III of the dengue-2 virus envelope protein,” Proteins, vol. 70, no. 3, pp. 1116–1119, 2008.
- J. Abd-Jamil, C.-Y. Cheah, and S. AbuBakar, “Dengue virus type 2 envelope protein displayed as recombinant phage attachment protein reveals potential cell binding sites,” Protein Engineering, Design and Selection, vol. 21, no. 10, pp. 605–611, 2008.
- V. Huerta, G. Chinea, N. Fleitas et al., “Characterization of the interaction of domain III of the envelope protein of dengue virus with putative receptors from CHO cells,” Virus Research, vol. 137, no. 2, pp. 225–234, 2008.
- S. M. Erb, S. Butrapet, K. J. Moss et al., “Domain-III FG loop of the dengue virus type 2 envelope protein is important for infection of mammalian cells and Aedes aegypti mosquitoes,” Virology, vol. 406, no. 2, pp. 328–335, 2010.
- W. C. Black IV, K. E. Bennett, N. Gorrochótegui-Escalante et al., “Flavivirus susceptibility in Aedes aegypti,” Archives of Medical Research, vol. 33, no. 4, pp. 379–388, 2002.
- C. Gomez-Machorro, K. E. Bennett, M. D. L. Munoz, and W. C. Black IV, “Quantitative trait loci affecting dengue midgut infection barriers in an advanced intercross line of Aedes aegypti,” Insect Molecular Biology, vol. 13, no. 6, pp. 637–648, 2004.
- S. Butrapet, T. Childers, K. J. Moss et al., “Amino acid changes within the E protein hinge region that affect dengue virus type 2 infectivity and fusion,” Virology, vol. 413, no. 1, pp. 118–127, 2011.
- C. Delenda, I. Staropoli, M.-P. Frenkiel, L. Cabanie, and V. Deubel, “Analysis of C-terminally truncated dengue 2 and dengue 3 virus envelope glycoproteins: processing in insect cells and immunogenic properties in mice,” Journal of General Virology, vol. 75, no. 7, pp. 1569–1578, 1994.
- M. Simmons, W. M. Nelson, S. J. L. Wu, and C. G. Hayes, “Evaluation of the protective efficacy of a recombinant dengue envelope B domain fusion protein against dengue 2 virus infection in mice,” The American Journal of Tropical Medicine and Hygiene, vol. 58, no. 5, pp. 655–662, 1998.
- R. Ocazionez Jimenez and B. A. Lopes da Fonseca, “Recombinant plasmid expressing a truncated dengue-2 virus E protein without co-expression of prM protein induces partial protection in mice,” Vaccine, vol. 19, no. 6, pp. 648–654, 2000.
- M.-W. Chiu and Y.-L. Yang, “Blocking the dengue virus 2 infections on BHK-21 cells with purified recombinant dengue virus 2 E protein expressed in Escherichia coli,” Biochemical and Biophysical Research Communications, vol. 309, no. 3, pp. 672–678, 2003.
- G. Batra, R. Raut, S. Dahiya, N. Kamran, S. Swaminathan, and N. Khanna, “Pichia pastoris-expressed dengue virus type 2 envelope domain III elicits virus-neutralizing antibodies,” Journal of Virological Methods, vol. 167, no. 1, pp. 10–16, 2010.
- L.-C. Chen, T.-M. Yeh, Y.-Y. Lin et al., “The envelope glycoprotein domain III of dengue virus type 2 induced the expression of anticoagulant molecules in endothelial cells,” Molecular and Cellular Biochemistry, vol. 342, no. 1-2, pp. 215–221, 2010.
- G. W. Smith and P. J. Wright, “Synthesis of proteins and glycoproteins in Dengue type 2 virus-infected Vero and Aedes albopictus cells,” Journal of General Virology, vol. 66, no. 3, pp. 559–571, 1985.
- R. Putnak, D. A. Barvir, J. M. Burrous et al., “Development of a purified, inactivated, dengue-2 virus vaccine prototype in Vero cells: immunogenicity and protection in mice and rhesus monkeys,” Journal of Infectious Diseases, vol. 174, no. 6, pp. 1176–1184, 1996.
- A. K. Srivastava, Y. Aira, C. Mori, Y. Kobayashi, and A. Igarashi, “Antigenicity of Japanese encephalitis virus envelope glycoprotein V 3 (E) and its cyanogen bromide cleaved fragments examined by monoclonal antibodies and Western blotting,” Archives of Virology, vol. 96, no. 1-2, pp. 97–107, 1987.
- M. S. Ramasamy, M. Sands, B. H. Kay, I. D. Fanning, G. W. Lawrence, and R. Ramasamy, “Anti-mosquito antibodies reduce the susceptibility of Aedes aegypti to arbovirus infection,” Medical and Veterinary Entomology, vol. 4, no. 1, pp. 49–55, 1990.
- M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding,” Analytical Biochemistry, vol. 72, no. 1-2, pp. 248–254, 1976.
- U. K. Laemmli, “Cleavage of structural proteins during the assembly of the head of bacteriophage T4,” Nature, vol. 227, no. 5259, pp. 680–685, 1970.
- H. Towbin, T. Staehelin, and J. Gordon, “Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications,” Proceedings of the National Academy of Sciences of the United States of America, vol. 76, no. 9, pp. 4350–4354, 1979.
- J. G. Timmins, E. A. Petrovskis, C. C. Marchioli, and L. E. Post, “A method for efficient gene isolation from phage λgt11 libraries: use of antisera to denatured, acetone-precipitated proteins,” Gene, vol. 39, no. 1, pp. 89–93, 1985.
- C. R. Merril, D. Goldman, and M. L. Van Keuren, “Gel protein stains: silver stain,” Methods in Enzymology, vol. 104, pp. 441–447, 1983.
- C. F. Bosio, B. J. Beaty, and W. C. Black IV, “Quantitative genetics of vector competence for dengue-2 virus in Aedes aegypti,” The American Journal of Tropical Medicine and Hygiene, vol. 59, no. 6, pp. 965–970, 1998.
- D. J. Gubler, S. Nalim, R. Tan, H. Saipan, and J. Sulianti Saroso, “Variation in susceptibility to oral infection with dengue viruses among geographic strains of Aedes aegypti,” The American Journal of Tropical Medicine and Hygiene, vol. 28, no. 6, pp. 1045–1052, 1979.
- K. E. Bennett, K. E. Olson, M. D. L. Muñoz et al., “Variation in vector competence for dengue 2 virus among 24 collections of Aedes aegypti from Mexico and the United States,” The American Journal of Tropical Medicine and Hygiene, vol. 67, no. 1, pp. 85–92, 2002.
- D. L. Oliveira, C. G. Freire-de-Lima, J. D. Nosanchuk, A. Casadevall, M. L. Rodrigues, and L. Nimrichter, “Extracellular vesicles from Cryptococcus neoformans modulate macrophage functions,” Infection and Immunity, vol. 78, no. 4, pp. 1601–1609, 2010.
- D. L. Oliveira, E. S. Nakayasu, L. S. Joffe et al., “Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis,” PLoS ONE, vol. 5, no. 6, Article ID e11113, 2010.
- R. K. Swenerton, S. Zhang, M. Sajid et al., “The oligopeptidase B of Leishmania regulates parasite enolase and immune evasion,” Journal of Biological Chemistry, vol. 286, no. 1, pp. 429–440, 2011.
- J. T. Bechtel, R. C. Winant, and D. Ganem, “Host and viral proteins in the virion of kaposi's sarcoma-associated herpesvirus,” Journal of Virology, vol. 79, no. 8, pp. 4952–4964, 2005.
- E. Chertova, O. Chertov, L. V. Coren et al., “Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages,” Journal of Virology, vol. 80, no. 18, pp. 9039–9052, 2006.
- M. L. Shaw, K. L. Stone, C. M. Colangelo, E. E. Gulcicek, and P. Palese, “Cellular proteins in influenza virus particles,” PLoS Pathogens, vol. 4, no. 6, Article ID e1000085, 2008.
- T. Ogino, T. Yamadera, T. Nonaka, S. Imajoh-Ohmi, and K. Mizumoto, “Enolase, a cellular glycolytic enzyme, is required for efficient transcription of Sendai virus genome,” Biochemical and Biophysical Research Communications, vol. 285, no. 2, pp. 447–455, 2001.
- A. Popova-Butler and D. H. Dean, “Proteomic analysis of the mosquito Aedes aegypti midgut brush border membrane vesicles,” Journal of Insect Physiology, vol. 55, no. 3, pp. 264–272, 2009.
- T. M. Colpitts, J. Cox, A. Nguyen, F. Feitosa, M. N. Krishnan, and E. Fikrig, “Use of a tandem affinity purification assay to detect interactions between West Nile and dengue viral proteins and proteins of the mosquito vector,” Virology, vol. 417, no. 1, pp. 179–187, 2011.
- E. V. Gurevich, J. J. G. Tesmer, A. Mushegian, and V. V. Gurevich, “G protein-coupled receptor kinases: more than just kinases and not only for GPCRs,” Pharmacology and Therapeutics, vol. 133, no. 1, pp. 40–69, 2012.
- S. V. Naga Prasad, S. A. Laporte, D. Chamberlain, M. G. Caron, L. Barak, and H. A. Rockman, “Phosphoinositide 3-kinase regulates β2-adrenergic receptor endocytosis by AP-2 recruitment to the receptor/β-arrestin complex,” Journal of Cell Biology, vol. 158, no. 3, pp. 563–575, 2002.