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BioMed Research International
Volume 2013 (2013), Article ID 526069, 14 pages
http://dx.doi.org/10.1155/2013/526069
Research Article

Molecular and Immunogenic Properties of Apyrase SP01B and D7-Related SP04 Recombinant Salivary Proteins of Phlebotomus perniciosus from Madrid, Spain

Unidad de Entomología Médica, Servicio de Parasitología, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Carretera Majadahonda-Pozuelo s/n, Majadahonda, 28220 Madrid, Spain

Received 12 April 2013; Revised 26 July 2013; Accepted 16 August 2013

Academic Editor: Hirotaka Sakamoto

Copyright © 2013 Inés Martín-Martín 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.

Linked References

  1. WHO, Control of the Leishmaniases, Technical Report Series no. 949, World Health Organization, Geneva, Switzerland, 2010.
  2. J. M. C. Ribeiro and I. M. B. Francischetti, “Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives,” Annual Review of Entomology, vol. 48, pp. 73–88, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Kamhawi, “The biological and immunomodulatory properties of sand fly saliva and its role in the establishment of Leishmania infections,” Microbes and Infection, vol. 2, no. 14, pp. 1765–1773, 2000. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Barral, E. Honda, A. Caldas et al., “Human immune response to sand fly salivary gland antigens: a useful epidemiological marker?” American Journal of Tropical Medicine and Hygiene, vol. 62, no. 6, pp. 740–745, 2000. View at Scopus
  5. R. Gomes and F. Oliveira, “The immune response to sand fly salivary proteins and its influence on Leishmania immunity,” Frontiers in Immunology, vol. 3, article 110, 2012.
  6. I. Rohoušová and P. Volf, “Sand fly saliva: effects on host immune response and Leishmania transmission,” Folia Parasitologica, vol. 53, no. 3, pp. 161–171, 2006. View at Scopus
  7. M. Vlková, I. Rohoušová, J. Drahota et al., “Canine antibody response to Phlebotomus perniciosus bites negatively correlates with the risk of Leishmania infantum transmission,” PLoS Neglected Tropical Diseases, vol. 5, no. 10, article e1344, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Vlková, I. Rohoušová, J. Hostomská et al., “Kinetics of antibody response in BALB/c and C57BL/6 mice bitten by Phlebotomus papatasi,” PLoS Neglected Tropical Diseases, vol. 6, no. 7, article e1719, 2012.
  9. K. Gidwani, A. Picado, S. Rijal et al., “Serological markers of sand fly exposure to evaluate insecticidal nets against visceral leishmaniasis in India and Nepal: a cluster-randomized trial,” PLoS Neglected Tropical Diseases, vol. 5, no. 9, article e1296, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. C. Teixeira, R. Gomes, N. Collin et al., “Discovery of markers of exposure specific to bites of Lutzomyia longipalpis, the vector of Leishmania infantum chagasiin Latin America,” PLoS Neglected Tropical Diseases, vol. 4, no. 3, article e638, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. A. P. Souza, B. B. Andrade, D. Aquino et al., “Using recombinant proteins from Lutzomyia longipalpis saliva to estimate human vector exposure in visceral leishmaniasis endemic areas,” PLoS Neglected Tropical Diseases, vol. 4, no. 3, article e649, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. M. F. Clements, K. Gidwani, R. Kumar et al., “Measurement of recent exposure to Phlebotomus argentipes, the vector of indian visceral leishmaniasis, by using human antibody responses to sand fly saliva,” American Journal of Tropical Medicine and Hygiene, vol. 82, no. 5, pp. 801–807, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. J. G. Valenzuela, Y. Belkaid, E. Rowton, and J. M. C. Ribeiro, “The salivary apyrase of the blood-sucking sand fly Phlebotomus papatasi belongs to the novel Cimex family of apyrases,” Journal of Experimental Biology, vol. 204, no. 2, pp. 229–237, 2001. View at Scopus
  14. S. Marzouki, M. Abdeladhim, C. B. Abdessalem et al., “Salivary antigen SP32 is the immunodominant target of the antibody response to Phlebotomus papatasi bites in humans,” PLoS Neglected Tropical Diseases, vol. 6, no. 11, article e1911, 2012.
  15. R. Molina, M. I. Jiménez, I. Cruz et al., “The hare (Lepus granatensis) as potential sylvatic reservoir of Leishmania infantum in Spain,” Veterinary Parasitology, vol. 190, no. 1-2, pp. 268–271, 2012.
  16. M. Jiménez, E. González, A. Iriso et al., “Detection of Leishmania infantum and identification of blood meals in Phlebotomus perniciosus from a focus of human leishmaniasis in Madrid, Spain,” Parasitology Research, vol. 112, no. 7, pp. 2453–2459, 2013.
  17. I. Martín-Martín, R. Molina, and M. Jiménez, “An insight into the Phlebotomus perniciosus saliva by a proteomic approach,” Acta Tropica, vol. 123, no. 1, pp. 22–30, 2012.
  18. I. Martín-Martín, R. Molina, and M. Jiménez, “Identifying salivary antigens of Phlebotomus argentipes by a 2DE approach,” Acta Tropica, vol. 126, no. 1, pp. 229–239, 2013.
  19. J. M. Anderson, F. Oliveira, S. Kamhawi et al., “Comparative salivary gland transcriptomics of sandfly vectors of visceral leishmaniasis,” BMC Genomics, vol. 7, article 52, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. R. Molina, “Laboratory adaptation of an autochthonous colony of Phlebotomus perniciosus Newstead, 1911 (Diptera: Psychodidae),” Research and Reviews in Parasitology, vol. 51, no. 1–4, pp. 87–89, 1991.
  21. J. Sambrook and D. Russell, Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, New York, NY, USA, 2001.
  22. R. Gupta, E. Jung, and S. Brunak, “Prediction of N-glycosylation sites in human proteins,” in preparation, 2004, http://www.cbs.dtu.dk/services/NetNGlyc/.
  23. K. Julenius, A. Mølgaard, R. Gupta, and S. Brunak, “Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites,” Glycobiology, vol. 15, no. 2, pp. 153–164, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. N. Blom, S. Gammeltoft, and S. Brunak, “Sequence and structure-based prediction of eukaryotic protein phosphorylation sites,” Journal of Molecular Biology, vol. 294, no. 5, pp. 1351–1362, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. G. C. Lanzaro, A. H. C. S. Lopes, J. M. C. Ribeiro et al., “Variation in the salivary peptide, maxadilan, from species in the Lutzomyia longipalpis complex,” Insect Molecular Biology, vol. 8, no. 2, pp. 267–275, 1999. View at Scopus
  26. R. S. Milleron, J.-P. Mutebi, S. Valle et al., “Antigenic diversity in maxadilan, a salivary protein from the sand fly vector of American visceral leishmaniasis,” American Journal of Tropical Medicine and Hygiene, vol. 70, no. 3, pp. 286–293, 2004. View at Scopus
  27. H. Kato, J. M. Anderson, S. Kamhawi et al., “High degree of conservancy among secreted salivary gland proteins from two geographically distant Phlebotomus duboscqi sandflies populations (Mali and Kenya),” BMC Genomics, vol. 7, article 226, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Abdeladhim, R. C. Jochim, M. Ben Ahmed et al., “Updating the salivary gland transcriptome of Phlebotomus papatasi (Tunisian Strain): the search for sand fly-secreted immunogenic proteins for humans,” PLoS One, vol. 7, no. 11, Article ID e47347, 2012.
  29. S. S. Mahamdallie and P. D. Ready, “No recent adaptive selection on the apyrase of Mediterranean Phlebotomus: implications for using salivary peptides to vaccinate against canine leishmaniasis,” Evolutionary Applications, vol. 5, no. 3, pp. 293–305, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. D.-E. A. Elnalem, C. Meneses, M. Slotman, and G. C. Lanzaro, “Genetic variation in the sand fly salivary protein, SP-15, a potential vaccine candidate against Leishmania major,” Insect Molecular Biology, vol. 14, no. 2, pp. 145–150, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Oleaga, A. Escudero-Población, E. Camafeita, and R. Pérez-Sánchez, “A proteomic approach to the identification of salivary proteins from the argasid ticks Ornithodoros moubata and Ornithodoros erraticus,” Insect Biochemistry and Molecular Biology, vol. 37, no. 11, pp. 1149–1159, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. I. M. B. Francischetti, V. M. Pham, B. J. Mans et al., “The transcriptome of the salivary glands of the female western black-legged tick Ixodes pacificus (Acari: Ixodidae),” Insect Biochemistry and Molecular Biology, vol. 35, no. 10, pp. 1142–1161, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Patthy, “Alternative splicing: evolution,” eLS, 2008. View at Publisher · View at Google Scholar
  34. C. Walsh, M. Gangloff, T. Monie et al., “Elucidation of the MD-2/TLR4 interface required for signaling by lipid IVa,” Journal of Immunology, vol. 181, no. 2, pp. 1245–1254, 2008. View at Scopus
  35. J. M. C. Ribeiro, B. J. Mans, and B. Arcà, “An insight into the sialome of blood-feeding Nematocera,” Insect Biochemistry and Molecular Biology, vol. 40, no. 11, pp. 767–784, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. J. G. Valenzuela, R. Charlab, E. C. Gonzalez et al., “The D7 family of salivary proteins in blood sucking diptera,” Insect Molecular Biology, vol. 11, no. 2, pp. 149–155, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. A. A. James, K. Blackmer, O. Marinotti, C. R. Ghosn, and J. V. Racioppi, “Isolation and characterization of the gene expressing the major salivary gland protein of the female mosquito, Aedes aegypti,” Molecular and Biochemical Parasitology, vol. 44, no. 2, pp. 245–254, 1991. View at Publisher · View at Google Scholar · View at Scopus
  38. B. Arcà, F. Lombardo, A. Lanfrancotti et al., “A cluster of four D7-related genes is expressed in the salivary glands of the African malaria vector Anopheles gambiae,” Insect Molecular Biology, vol. 11, no. 1, pp. 47–55, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. R. Charlab, J. G. Valenzuela, E. D. Rowton, and J. M. C. Ribeiro, “Toward an understanding of the biochemical and pharmacological complexity of the saliva of a hematophagous sand fly Lutzomyia longipalpis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 26, pp. 15155–15160, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. E. Calvo, B. J. Mans, J. F. Andersen, and J. M. C. Ribeiro, “Function and evolution of a mosquito salivary protein family,” Journal of Biological Chemistry, vol. 281, no. 4, pp. 1935–1942, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. I. Rohoušová, S. Subrahmanyam, V. Volfová et al., “Salivary gland transcriptomes and proteomes of Phlebotomus tobbi and Phlebotomus sergenti, vectors of leishmaniasis,” PLoS Neglected Tropical Diseases, vol. 6, no. 5, article e1660, 2012.
  42. P. H. Alvarenga, I. M. B. Francischetti, E. Calvo, A. Sá-Nunes, J. M. C. Ribeiro, and J. F. Andersen, “The function and three-dimensional structure of a thromboxane A2/cysteinyl leukotriene-binding protein from the saliva of a mosquito vector of the malaria parasite,” PLoS Biology, vol. 8, no. 11, Article ID e1000547, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. E. Calvo, B. J. Mans, J. M. C. Ribeiro, and J. F. Andersen, “Multifunctionality and mechanism of ligand binding in a mosquito antiinflammatory protein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 10, pp. 3728–3733, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. J. Hostomská, V. Volfová, J. Mu et al., “Analysis of salivary transcripts and antigens of the sand fly Phlebotomus arabicus,” BMC Genomics, vol. 10, article 282, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. J. G. Valenzuela, Y. Belkaid, M. K. Garfield et al., “Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein,” Journal of Experimental Medicine, vol. 194, no. 3, pp. 331–342, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. P. K. Geyer, C. Spana, and V. G. Corces, “On the molecular mechanism of gypsy-induced mutations at the yellow locus of Drosophila melanogaster,” EMBO Journal, vol. 5, no. 10, pp. 2657–2662, 1986. View at Scopus
  47. X. Xu, F. Oliveira, B. W. Chang et al., “Structure and function of a “yellow” protein from saliva of the sand fly Lutzomyia longipalpis that confers protective immunity against Leishmania major infection,” Journal of Biological Chemistry, vol. 286, no. 37, pp. 32383–32393, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. F. Oliveira, S. Kamhawi, A. E. Seitz et al., “From transcriptome to immunome: identification of DTH inducing proteins from a Phlebotomus ariasi salivary gland cDNA library,” Vaccine, vol. 24, no. 3, pp. 374–390, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. N. Collin, T. C. Assumpcao, D. M. Mizurini et al., “Lufaxin, a novel factor Xa inhibitor from the salivary gland of the sand fly Lutzomyia longipalpis blocks protease-activated receptor 2 activation and inhibits inflammation and thrombosis in vivo,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 32, no. 9, pp. 2185–2198, 2012.
  50. T. R. de Moura, F. Oliveira, M. W. Carneiro et al., “Functional transcriptomics of wild-caught Lutzomyia intermedia salivary glands: identification of a protective salivary protein against Leishmania braziliensis infection,” PLoS Neglected Tropical Diseases, vol. 7, no. 5, article e2242, 2013. View at Publisher · View at Google Scholar
  51. H. Kato, R. C. Jochim, E. A. Gomez et al., “Analysis of salivary gland transcripts of the sand fly Lutzomyia ayacuchensis, a vector of Andean-type cutaneous leishmaniasis,” Infection, Genetics and Evolution, vol. 13, pp. 56–66, 2012. View at Publisher · View at Google Scholar
  52. J. Dai, J. Liu, Y. Deng, T. M. Smith, and M. Lu, “Structure and protein design of a human platelet function inhibitor,” Cell, vol. 116, no. 5, pp. 649–659, 2004. View at Publisher · View at Google Scholar · View at Scopus