1921
Volume 90, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

sand flies are among the primary vectors of parasites from Morocco to the Indian subcontinent and from southern Europe to central and eastern Africa. Antibody-based immunity to sand fly salivary gland proteins in human populations remains a complex contextual problem that is not yet fully understood. We profiled the immunoreactivities of plasma antibodies to sand fly salivary gland sonicates (SGSs) from 229 human blood donors residing in different regions of sand fly endemicity throughout Jordan and Egypt as well as 69 US military personnel, who were differentially exposed to bites and infections in Iraq. Compared with plasma from control region donors, antibodies were significantly immunoreactive to five salivary proteins (12, 26, 30, 38, and 44 kDa) among Jordanian and Egyptian donors, with immunoglobulin G4 being the dominant anti-SGS isotype. US personnel were significantly immunoreactive to only two salivary proteins (38 and 14 kDa). Using k-means clustering, donors were segregated into four clusters distinguished by unique immunoreactivity profiles to varying combinations of the significantly immunogenic salivary proteins. SGS-induced cellular proliferation was diminished among donors residing in sand fly-endemic regions. These data provide a clearer picture of human immune responses to sand fly vector salivary constituents.

[open-access] This is an Open Access article distributed under the terms of the American Society of Tropical Medicine and Hygiene's Re-use License which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.13-0130
2014-05-07
2017-09-23
Loading full text...

Full text loading...

/deliver/fulltext/14761645/90/5/923.html?itemId=/content/journals/10.4269/ajtmh.13-0130&mimeType=html&fmt=ahah

References

  1. Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, den Boer M, Team WHOLC, , 2012. Leishmaniasis worldwide and global estimates of its incidence. PLoS One 7: e35671.[Crossref]
  2. Konecny P, Stark DJ, , 2007. An Australian case of New World cutaneous leishmaniasis. Med J Aust 186: 315317.
  3. World Health Organization, 2012. Leishmaniasis: Burden of Disease. Available at: http://www.who.int/leishmaniasis/burden/en/. Accessed August 15, 2012.
  4. de Oliveira CI, Nascimento IP, Barral A, Soto M, Barral-Netto M, , 2009. Challenges and perspectives in vaccination against leishmaniasis. Parasitol Int 58: 319324.[Crossref]
  5. Kobets T, Grekov I, Lipoldova M, , 2012. Leishmaniasis: prevention, parasite detection and treatment. Curr Med Chem 19: 14431474.[Crossref]
  6. Aquino DM, Caldas AJ, Miranda JC, Silva AA, Barral-Netto M, Barral A, , 2010. Epidemiological study of the association between anti-Lutzomyia longipalpis saliva antibodies and development of delayed-type hypersensitivity to Leishmania antigen. Am J Trop Med Hyg 83: 825827.[Crossref]
  7. Barral A, Honda E, Caldas A, Costa J, Vinhas V, Rowton ED, Valenzuela JG, Charlab R, Barral-Netto M, Ribeiro JM, , 2000. Human immune response to sand fly salivary gland antigens: a useful epidemiological marker? Am J Trop Med Hyg 62: 740745.
  8. Clements MF, Gidwani K, Kumar R, Hostomska J, Dinesh DS, Kumar V, Das P, Muller I, Hamilton G, Volfova V, Boelaert M, Das M, Rijal S, Picado A, Volf P, Sundar S, Davies CR, Rogers ME, , 2010. Measurement of recent exposure to Phlebotomus argentipes, the vector of Indian visceral leishmaniasis, by using human antibody responses to sand fly saliva. Am J Trop Med Hyg 82: 801807.[Crossref]
  9. Gidwani K, Picado A, Rijal S, Singh SP, Roy L, Volfova V, Andersen EW, Uranw S, Ostyn B, Sudarshan M, Chakravarty J, Volf P, Sundar S, Boelaert M, Rogers ME, , 2011. Serological markers of sand fly exposure to evaluate insecticidal nets against visceral leishmaniasis in India and Nepal: a cluster-randomized trial. PLoS Negl Trop Dis 5: e1296.[Crossref]
  10. Gomes RB, Brodskyn C, de Oliveira CI, Costa J, Miranda JC, Caldas A, Valenzuela JG, Barral-Netto M, Barral A, , 2002. Seroconversion against Lutzomyia longipalpis saliva concurrent with the development of anti-Leishmania chagasi delayed-type hypersensitivity. J Infect Dis 186: 15301534.[Crossref]
  11. Marzouki S, Abdeladhim M, Abdessalem CB, Oliveira F, Ferjani B, Gilmore D, Louzir H, Valenzuela JG, Ben Ahmed M, , 2012. Salivary antigen SP32 is the immunodominant target of the antibody response to phlebotomus papatasi bites in humans. PLoS Negl Trop Dis 6: e1911.[Crossref]
  12. Marzouki S, Ben Ahmed M, Boussoffara T, Abdeladhim M, Ben Aleya-Bouafif N, Namane A, Hamida NB, Ben Salah A, Louzir H, , 2011. Characterization of the antibody response to the saliva of Phlebotomus papatasi in people living in endemic areas of cutaneous leishmaniasis. Am J Trop Med Hyg 84: 653661.[Crossref]
  13. Rohousova I, Ozensoy S, Ozbel Y, Volf P, , 2005. Detection of species-specific antibody response of humans and mice bitten by sand flies. Parasitology 130: 493499.[Crossref]
  14. de Moura TR, Oliveira F, Novais FO, Miranda JC, Clarencio J, Follador I, Carvalho EM, Valenzuela JG, Barral-Netto M, Barral A, Brodskyn C, de Oliveira CI, , 2007. Enhanced Leishmania braziliensis infection following pre-exposure to sandfly saliva. PLoS Negl Trop Dis 1: e84.[Crossref]
  15. Coutinho-Abreu IV, Mukbel R, Hanafi HA, Fawaz EY, El-Hossary SS, Wadsworth M, Stayback G, Pitts DA, Abo-Shehada M, Hoel DF, Kamhawi S, Ramalho-Ortigao M, McDowell MA, , 2011. Expression plasticity of Phlebotomus papatasi salivary gland genes in distinct ecotopes through the sand fly season. BMC Ecol 11: 24.[Crossref]
  16. Janini R, Saliba E, Kamhawi S, , 1995. Species composition of sand flies and population dynamics of Phlebotomus papatasi (Diptera: Psychodidae) in the southern Jordan Valley, an endemic focus of cutaneous leishmaniasis. J Med Entomol 32: 822826.[Crossref]
  17. Janini R, Saliba E, Khoury S, Oumeish O, Adwan S, Kamhawi S, , 1995. Incrimination of Phlebotomus papatasi as vector of Leishmania major in the southern Jordan Valley. Med Vet Entomol 9: 420422.[Crossref]
  18. Kamhawi S, Arbagi A, Adwan S, Rida M, , 1993. Environmental manipulation in the control of a zoonotic cutaneous leishmaniasis focus. Arch Inst Pasteur Tunis 70: 383390.
  19. Saliba EK, Pratlong F, Dedet JP, Saleh N, Khoury SA, Oumeish OY, Batayneh O, Al-Oran R, , 2004. Identification of Leishmania strains from Jordan. Ann Trop Med Parasitol 98: 677683.
  20. Schlein Y, Jacobson RL, , 1999. Sugar meals and longevity of the sandfly Phlebotomus papatasi in an arid focus of Leishmania major in the Jordan Valley. Med Vet Entomol 13: 6571.[Crossref]
  21. Schlein Y, Warburg A, Schnur LF, Gunders AE, , 1982. Leishmaniasis in the Jordan Valley II. Sandflies and transmission in the central endemic area. Trans R Soc Trop Med Hyg 76: 582586.[Crossref]
  22. Yuval B, , 1991. Populations of Phlebotomus papatasi (Diptera: Psychodidae) and the risk of Leishmania major transmission in three Jordan Valley habitats. J Med Entomol 28: 492495.[Crossref]
  23. Yuval B, Warburg A, Schlein Y, , 1988. Leishmaniasis in the Jordan Valley. V. Dispersal characteristics of the sandfly Phlebotomus papatasi . Med Vet Entomol 2: 391395.[Crossref]
  24. el Said SM, Kenawy MA, el Sawaf BM, Beier JC, el Sawy FM, , 1985. Seasonal abundance and distribution of Phlebotomus papatasi (Diptera: Psychodidae) inside houses in Aswan Governorate, Egypt. J Egypt Soc Parasitol 15: 371380.
  25. Fryauff DJ, Modi GB, Mansour NS, Kreutzer RD, Soliman S, Youssef FG, , 1993. Epidemiology of cutaneous leishmaniasis at a focus monitored by the multinational force and observers in the northeastern Sinai Desert of Egypt. Am J Trop Med Hyg 49: 598607.
  26. Hanafi HA, el Sawaf BM, Fryauff DJ, Beavers GM, Tetreault GE, , 1998. Susceptibility to Leishmania major of different populations of Phlebotomus papatasi (Diptera: Psychodidae) from endemic and non-endemic regions of Egypt. Ann Trop Med Parasitol 92: 5764.[Crossref]
  27. Hogsette JA, Hanafi HA, Bernier UR, Kline DL, Fawaz EY, Furman BD, Hoel DF, , 2008. Discovery of diurnal resting sites of phlebotomine sand flies in a village in southern Egypt. J Am Mosq Control Assoc 24: 601603.[Crossref]
  28. Morsy TA, Aboul Ela RG, Sarwat MA, Arafa MA, el Gozamy BM, , 1993. Some aspects of Phlebotomus papatasi (Scopoli) in greater Cairo, Egypt. J Egypt Soc Parasitol 23: 399416.
  29. Morsy TA, Shoukry A, Schnur LF, Sulitzeanu A, , 1987. Gerbillus pyramidum is a host of Leishmania major in the Sinai Peninsula. Ann Trop Med Parasitol 81: 741742.[Crossref]
  30. Prates DB, Santos LD, Miranda JC, Souza AP, Palma MS, Barral-Netto M, Barral A, , 2008. Changes in amounts of total salivary gland proteins of Lutzomyia longipallpis (Diptera: Psychodidae) according to age and diet. J Med Entomol 45: 409413.[Crossref]
  31. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M, , 2006. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1: 28562860.[Crossref]
  32. Champion MM, Williams EA, Kennedy GM, DiGiuseppe Champion PA, , 2012. Direct detection of bacterial protein secretion using whole colony proteomics. Mol Cell Proteomics 11: 596604.[Crossref]
  33. Information NCfB, 2012. Phlebotomine Sandfly Proteins. Available at: http://www.ncbi.nlm.nih.gov/protein/?term=txid29031[Organism:noexp]. Accessed December 4, 2012.
  34. Elias JE, Gygi SP, , 2007. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4: 207214.[Crossref]
  35. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG, , 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7: 539.[Crossref]
  36. Huang XQ, Hardison RC, Miller W, , 1990. A space-efficient algorithm for local similarities. Comput Appl Biosci 6: 373381.
  37. Belkaid Y, Kamhawi S, Modi G, Valenzuela J, Noben-Trauth N, Rowton E, Ribeiro J, Sacks DL, , 1998. Development of a natural model of cutaneous leishmaniasis: powerful effects of vector saliva and saliva preexposure on the long-term outcome of Leishmania major infection in the mouse ear dermis. J Exp Med 188: 19411953.[Crossref]
  38. de Hoon MJ, Imoto S, Nolan J, Miyano S, , 2004. Open source clustering software. Bioinformatics 20: 14531454.[Crossref]
  39. Saldanha AJ, , 2004. Java Treeview–extensible visualization of microarray data. Bioinformatics 20: 32463248.[Crossref]
  40. Reunala T, Brummer-Korvenkontio H, Palosuo T, , 1994. Are we really allergic to mosquito bites? Ann Med 26: 301306.[Crossref]
  41. Abdeladhim M, Jochim RC, Ben Ahmed M, Zhioua E, Chelbi I, Cherni S, Louzir H, Ribeiro JM, Valenzuela JG, , 2012. Updating the salivary gland transcriptome of Phlebotomus papatasi (Tunisian strain): the search for sand fly-secreted immunogenic proteins for humans. PLoS One 7: e47347.[Crossref]
  42. Hamarsheh O, Presber W, Yaghoobi-Ershadi MR, Amro A, Al-Jawabreh A, Sawalha S, Al-Lahem A, Das ML, Guernaoui S, Seridi N, Dhiman RC, Hashiguchi Y, Ghrab J, Hassan M, Schonian G, , 2009. Population structure and geographical subdivision of the Leishmania major vector Phlebotomus papatasi as revealed by microsatellite variation. Med Vet Entomol 23: 6977.[Crossref]
  43. Gazos-Lopes F, Mesquita RD, Silva-Cardoso L, Senna R, Silveira AB, Jablonka W, Cudischevitch CO, Carneiro AB, Machado EA, Lima LG, Monteiro RQ, Nussenzveig RH, Folly E, Romeiro A, Vanbeselaere J, Mendonca-Previato L, Previato JO, Valenzuela JG, Ribeiro JM, Atella GC, Silva-Neto MA, , 2012. Glycoinositolphospholipids from Trypanosomatids subvert nitric oxide production in Rhodnius prolixus salivary glands. PLoS One 7: e47285.[Crossref]
  44. Martin-Martin I, Molina R, Jimenez M, , 2013. Identifying salivary antigens of Phlebotomus argentipes by a 2DE approach. Acta Trop 126: 229239.[Crossref]
  45. Hostomska J, Volfova V, Mu J, Garfield M, Rohousova I, Volf P, Valenzuela JG, Jochim RC, , 2009. Analysis of salivary transcripts and antigens of the sand fly Phlebotomus arabicus . BMC Genomics 10: 282.[Crossref]
  46. Kane LP, , 2010. T cell Ig and mucin domain proteins and immunity. J Immunol 184: 27432749.[Crossref]
  47. Francischetti IM, , 2010. Platelet aggregation inhibitors from hematophagous animals. Toxicon 56: 11301144.[Crossref]
  48. Grespan R, Lemos HP, Carregaro V, Verri WA, Jr Souto FO, de Oliveira CJ, Teixeira C, Ribeiro JM, Valenzuela JG, Cunha FQ, , 2012. The protein LJM 111 from Lutzomyia longipalpis salivary gland extract (SGE) accounts for the SGE-inhibitory effects upon inflammatory parameters in experimental arthritis model. Int Immunopharmacol 12: 603610.[Crossref]
  49. Peng Z, Rasic N, Liu Y, Simons FE, , 2002. Mosquito saliva-specific IgE and IgG antibodies in 1059 blood donors. J Allergy Clin Immunol 110: 816817.[Crossref]
  50. Shan EZ, Taniguchi Y, Shimizu M, Ando K, Chinzei Y, Suto C, Ohtaki T, Ohtaki N, , 1995. Immunoglobulins specific to mosquito salivary gland proteins in the sera of persons with common or hypersensitive reactions to mosquito bites. J Dermatol 22: 411418.[Crossref]
  51. Rohousova I, Hostomska J, Vlkova M, Kobets T, Lipoldova M, Volf P, , 2011. The protective effect against Leishmania infection conferred by sand fly bites is limited to short-term exposure. Int J Parasitol 41: 481485.[Crossref]
  52. Abdeladhim M, Ben Ahmed M, Marzouki S, Belhadj Hmida N, Boussoffara T, Belhaj Hamida N, Ben Salah A, Louzir H, , 2011. Human cellular immune response to the saliva of Phlebotomus papatasi is mediated by IL-10-producing CD8+ T cells and Th1-polarized CD4+ lymphocytes. PLoS Negl Trop Dis 5: e1345.[Crossref]
  53. Carregaro V, Sa-Nunes A, Cunha TM, Grespan R, Oliveira CJ, Lima-Junior DS, Costa DL, Verri WA, Jr Milanezi CM, Pham VM, Brand DD, Valenzuela JG, Silva JS, Ribeiro JM, Cunha FQ, , 2011. Nucleosides from Phlebotomus papatasi salivary gland ameliorate murine collagen-induced arthritis by impairing dendritic cell functions. J Immunol 187: 43474359.[Crossref]
  54. Lopez Kostka S, Dinges S, Griewank K, Iwakura Y, Udey MC, von Stebut E, , 2009. IL-17 promotes progression of cutaneous leishmaniasis in susceptible mice. J Immunol 182: 30393046.[Crossref]
  55. Souza MA, Castro MC, Oliveira AP, Almeida AF, Reis LC, Silva CJ, Brito ME, Pereira VR, , 2012. American tegumentary leishmaniasis: cytokines and nitric oxide in active disease and after clinical cure, with or without chemotherapy. Scand J Immunol 76: 175180.[Crossref]
  56. Gupta G, Bhattacharjee S, Bhattacharyya S, Bhattacharya P, Adhikari A, Mukherjee A, Bhattacharyya Majumdar S, Majumdar S, , 2009. CXC chemokine-mediated protection against visceral leishmaniasis: involvement of the proinflammatory response. J Infect Dis 200: 13001310.[Crossref]
  57. de Moura TR, Oliveira F, Rodrigues GC, Carneiro MW, Fukutani KF, Novais FO, Miranda JC, Barral-Netto M, Brodskyn C, Barral A, de Oliveira CI, , 2010. Immunity to Lutzomyia intermedia saliva modulates the inflammatory environment induced by Leishmania braziliensis . PLoS Negl Trop Dis 4: e712.[Crossref]
  58. Ben Hadj Ahmed S, Chelbi I, Kaabi B, Cherni S, Derbali M, Zhioua E, , 2010. Differences in the salivary effects of wild-caught versus colonized Phlebotomus papatasi (Diptera: Psychodidae) on the development of zoonotic cutaneous leishmaniasis in BALB/c mice. J Med Entomol 47: 7479.[Crossref]
  59. Ben Hadj Ahmed S, Kaabi B, Chelbi I, Cherni S, Derbali M, Laouini D, Zhioua E, , 2011. Colonization of Phlebotomus papatasi changes the effect of pre-immunization with saliva from lack of protection towards protection against experimental challenge with Leishmania major and saliva. Parasit Vectors 4: 126.[Crossref]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.13-0130
Loading
/content/journals/10.4269/ajtmh.13-0130
Loading

Data & Media loading...

  • Received : 12 Mar 2013
  • Accepted : 05 Jan 2014

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error