Comparative Analysis of Salivary Gland Transcriptomes of Phlebotomus orientalis Sand Flies from Endemic and Non-endemic Foci of Visceral Leishmaniasis

PLoS Neglected Tropical Diseases

Volumn 8, Issue 2, 2014, Pages

  Vlkova, Michaela ^a   Sima, Michal ^a   Rohousova, Iva ^a   Kostalova, Tatiana ^a   Sumova, Petra ^a   Volfova, Vera ^a   Jaske, Erin L ^b   Barbian, Kent D ^b   Gebre Michael, Teshome ^c   Hailu, Asrat ^c   Warburg, Alon ^d   Ribeiro, Jose M C ^e   Valenzuela, Jesus G ^e   Jochim, Ryan C ^e,f   Volf, Petr ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c ADDIS ABABA UNIVERSITY   (Ethiopia)

^d HEBREW UNIVERSITY   (Israel)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^f WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APYRASE; COMPLEMENTARY DNA; HYALURONIDASE; MESSENGER RNA; PROTEOME; SALIVA PROTEIN; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGENICITY; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; CROSS REACTION; DISEASE TRANSMISSION; DNA SEQUENCE; ENZYME ACTIVITY; IMMUNOGENICITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHLEBOTOMUS LANGERONI; PHLEBOTOMUS PERNICIOSUS; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PSYCHODIDAE; VISCERAL LEISHMANIASIS; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; ENZYMES; ETHIOPIA; FEMALE; INSECT VECTORS; LEISHMANIASIS, VISCERAL; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; PHLEBOTOMUS; SALIVARY GLANDS; SALIVARY PROTEINS AND PEPTIDES; SEQUENCE ALIGNMENT; TRANSCRIPTOME;

EID: 84895772502     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002709     Document Type: Article

References (117)

1. Fontaine A, Diouf I, Bakkali N, Misse D, Pages F, et al. (2011) Implication of haematophagous arthropod salivary proteins in host-vector interactions. Parasit Vectors 4: 187.
2. Kamhawi S, Belkaid Y, Modi G, Roeton E, Sacks D, (2000) Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science 290: 1351-1354.
3. Souza AP, Andrade BB, Aquino D, Entringer P, Miranda JC, et al. (2010) Using recombinant proteins from Lutzomyia longipalpis saliva to estimate human vector exposure in visceral leishmaniasis endemic areas. PLoS Negl Trop Dis 4: e649.
4. Teixeira C, Gomes R, Collin N, Reynoso D, Jochim R, et al. (2010) Discovery of markers of exposure specific to bites of Lutzomyia longipalpis, the vector of Leishmania infantum chagasi in Latin America. PLoS Negl Trop Dis 4: e638.
5. Vlkova M, Rohousova I, Hostomska J, Pohankova L, Zidkova L, et al. (2012) Kinetics of antibody response in BALB/c and C57BL/6 mice bitten by Phlebotomus papatasi. PLoS Negl Trop Dis 6: e1719.
6. Morris RV, Shoemaker CB, David JR, Lanzaro GC, Titus RG, (2001) Sand fly maxadilan exacerbates infection with Leishmania major and vaccinating against it protects against L. major infection. J Immunol 167: 5226-5230.
7. Valenzuela JG, Belkaid Y, Garfield MK, Mendez S, Kamhawi S, et al. (2001) Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. J Exp Med 194: 331-342.
8. Gomes R, Teixeira C, Teixeira MJ, Oliveira F, Menezes MJ, et al. (2008) Immunity to a salivary protein of a sand fly vector protects against the fatal outcome of visceral leishmaniasis in a hamster model. Proc Natl Acad Sci U S A 105: 7845-7850.
9. Oliveira F, Lawyer PG, Kamhawi S, Valenzuela JG, (2008) Immunity to distinct sand fly salivary proteins primes the anti-Leishmania immune response towards protection or exacerbation of disease. PLOS Negl Trop Dis 2: e226.
10. da Silva RA, Tavares NM, Costa D, Pitombo M, Barbosa L, et al. (2011) DNA vaccination with KMP11 and Lutzomyia longipalpis salivary protein protects hamsters against visceral leishmaniasis. Acta Trop 120: 185-190.
11. Tavares NM, Silva RA, Costa DJ, Pitombo MA, Fukutani KF, et al. (2011) Lutzomyia longipalpis saliva or salivary protein LJM19 protects against Leishmania braziliensis and the saliva of its vector, Lutzomyia intermedia. PLoS Negl Trop Dis 5: e1169.
12. Xu X, Oliveira F, Chang BW, Collin N, Gomes R, et al. (2011) Structure and function of a "yellow" protein from saliva of the sand fly Lutzomyia longipalpis that confers protective immunity against Leishmania major infection. J Biol Chem 286: 32383-32393.
13. Gomes R, Oliveira F, Teixeira C, Meneses C, Gilmore DC, et al. (2012) Immunity to sand fly salivary protein LJM11 modulates host response to vector-transmitted Leishmania conferring ulcer-free protection. J Invest Dermatol 132: 2735-2743.
14. Volf P, Rohousova I, (2001) Species-specific antigens in salivary glands of phlebotomine sandflies. Parasitology 122: 37-41.
15. 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: 493-499.
16. Thiakaki M, Rohousova I, Volfova V, Volf P, Chang KP, et al. (2005) Sand fly specificity of saliva-mediated protective immunity in Leishmania amazonensis-BALB/c mouse model. Microbes Infect 7: 760-766.
17. Wahba M, Riera C, (2006) Salivary gland composition of some Old World vector sand fly. J Egypt Soc Parasitol 36: 289-296.
18. Drahota J, Lipoldova M, Volf P, Rohousova I, (2009) Specificity of anti-saliva immune response in mice repeatedly bitten by Phlebotomus sergenti. Parasite Immunol 31: 766-770.
19. Rohousova I, Volfova V, Nova S, Volf P, (2012a) Individual variability of salivary gland proteins in three Phlebotomus species. Acta Trop 122: 80-86.
20. Elnaiem DE, (2011) Ecology and control of the sand fly vectors of Leishmania donovani in East Africa, with special emphasis on Phlebotomus orientalis. J Vector Ecol 36: S23-31.
21. Doha SA, Samy AM, (2010) Bionomics of phlebotomine sand flies (Diptera: Psychodidae) in the province of Al-Baha, Saudi Arabia. Mem Inst Oswaldo Cruz 105: 850-856.
22. Daoud W, Rioux JA, Delalbre-Belmonte A, Dereure J, Rageh HA, (1989) Eco-epidemiology of visceral and cutaneous leishmaniasis in the Arab Republic of Yemen. III. Inventory and dynamics of Phlebotomus. Bull Soc Pathol Exot Filiales 82: 669-677.
23. Herrero M, Orfanos G, Argaw D, Mulugeta A, Aparicio P, et al. (2009) Natural history of a visceral leishmaniasis outbreak in highland Ethiopia. Am J Trop Med Hyg 81: 373-377.
24. Seblova V, Volfova V, Dvorak V, Pruzinova K, Votypka J, et al. (2013) Phlebotomus orientalis sand flies from two geographically distant Ethiopian localities: biology, genetic analyses and susceptibility to Leishmania donovani. PLoS Negl Trop Dis 7: e2187.
25. Warburg A, Saraiva E, Lanzaro GC, Titus RG, Neva F, (1994) Saliva of Lutzomyia longipalpis sibling species differs in its composition and capacity to enhance leishmaniasis. Philos Trans R Soc Lond B Biol Sci 345: 223-230.
26. Anderson JM, Oliveira F, Kamhawi S, Mans BJ, Reynoso D, et al. (2006) Comparative salivary gland transcriptomics of sandfly vectors of visceral leishmaniasis. BMC Genomics 7: a.n. 52.
27. Oliveira F, Kamhawi S, Seitz AE, Pham VM, Guigal PM, et al. (2006) From transcriptome to immunome: Identification of DTH inducing proteins from a Phlebotomus ariasi salivary gland cDNA library. Vaccine 24: 374-390.
28. Rohousova I, Subrahmanyam S, Volfova V, Mu J, Volf P, et al. (2012b) Salivary gland transcriptomes and proteomes of Phlebotomus tobbi and Phlebotomus sergenti, vectors of leishmaniasis. PLoS Negl Trop Dis 6: e1660.
29. Volf P, Volfova V, (2011) Establishment and maintenance of sand fly colonies. J Vector Ecol 36: S1-S9.
30. Chmelar J, Anderson JM, Mu J, Jochim RC, Valenzuela JG, et al. (2008) Insight into the sialome of the castor bean tick, Ixodes ricinus. BMC Genomics 9: 233.
31. Hostomska J, Volfova V, Mu JB, Garfield M, Rohousova I, et al. (2009) Analysis of salivary transcripts and antigens of the sand fly Phlebotomus arabicus. BMC Genomics 10: 282.
32. Ewing B, Hillier L, Wendl MC, Green P, (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8: 175-185.
33. Ewing B, Green P, (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8: 186-194.
34. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene Ontology: tool for the unification of biology. Nat Genet 25: 25-29.
35. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, et al. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 4.
36. Bateman A, Birney E, Durbin R, Eddy SR, Howe KL, et al. (2000) The Pfam protein families database. Nucleic Acids Res 28: 263-266.
37. Schultz J, Copley RR, Doerks T, Ponting CP, Bork P, (2000) SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res 28: 231-234.
38. Bendtsen JD, Nielsen H, von Heijne G, Brunak S, (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
39. Guo YJ, Ribeiro JMC, Anderson JM, Bour S, (2009) dCAS: a desktop application for cDNA sequence annotation. Bioinformatics 25: 1195-1196.
40. Julenius K, Mølgaard A, Gupta R, Brunak S, (2005) Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 15: 153-164.
41. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and clustal X version 2.0. Bioinformatics 23: 2947-2948.
42. Abascal F, Zardoya R, Posada D, (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105.
43. Schmidt HA, Strimmer K, Vingron M, von Haeseler, (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504.
44. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
45. Cerna P, Mikes L, Volf P, (2002) Salivary gland hyaluronidase in various species of phlebotomine sand flies (Diptera: Psychodidae). Insect Biochem Mol Biol 32: 1691-1697.
46. Frost GI, Stern R, (1997) A microtiter-based assay for hyaluronidase activity not requiring specialized reagents. Anal Biochem 251: 263-269.
47. Marinotti O, deBrito M, Moreira CK, (1996) Apyrase and alpha-glucosidase in the salivary glands of Aedes albopictus. Comp Biochem Physiol 113B: 675-679.
48. Ribeiro JMC, Modi GB, Tesh RB, (1989) Salivary apyrase activity of some Old World phlebotomine sand flies. Insect Biochemistry 19: 409-412.
49. Charlab R, Rowton ED, Ribeiro JM, (2000) The salivary adenosine deaminase from the sand fly Lutzomyia longipalpis. Exp Parasitol 95: 45-53.
50. Kato H, Anderson JM, Kamhawi S, Oliveira F, Lawyer PG, et al. (2006) High degree of conservancy among secreted salivary gland proteins from two geographically distant Phlebotomus duboscqi sandflies populations (Mali and Kenya). BMC Genomics 7: 226.
51. Kato H, Jochim RC, Lawyer PG, Valenzuela JG, (2007) Identification and characterization of a salivary adenosine deaminase from the sand fly Phlebotomus duboscqi, the vector of Leishmania major in sub-Saharan Africa. J Exp Biol 210: 733-740.
52. de Moura TR, Oliveira F, Carneiro MW, Miranda JC, Clarêncio J, et al. (2013) Functional transcriptomics of wild-caught Lutzomyia intermedia salivary glands: identification of a protective salivary protein against Leishmania braziliensis infection. PLoS Negl Trop Dis 7: e2242.
53. Charlab R, Valenzuela JG, Rowton ED, Ribeiro JMC, (1999) Toward an understanding of the biochemical and pharmacological complexity of the saliva of a hematophagous sand fly Lutzomyia longipalpis. Proc Natl Acad Sci U S A 96: 15155-15160.
54. Valenzuela JG, Garfield M, Rowton ED, Pham VM, (2004) Identification of the most abundant secreted proteins from the salivary glands of the sand fly Lutzomyia longipalpis, vector of Leishmania chagasi. J Exp Biol 207: 3717-3729.
55. Abdeladhim M, Jochim RC, Ben Ahmed M, Zhioua E, Chelbi I, et al. (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.
56. Kato H, Jochim RC, Gomez EA, Uezato H, Mimori T, et al. (2012) Analysis of salivary gland transcripts of the sand fly Lutzomyia ayacuchensis, a vector of Andean-type cutaneous leishmaniasis. Infect Genet Evol 13C: 56-66.
57. Volf P, Skarupova S, Man P, (2002) Characterization of the lectin from females of Phlebotomus duboscqi sand flies. Eur J Biochem 269: 6294-6301.
58. Johnson JK, Li J, Christensen BM, (2001) Cloning and characterization of a dopachrome conversion enzyme from the yellow fever mosquito, Aedes aegypti. Insect Biochem Mol Biol 31: 1125-1135.
59. Alves-Silva J, Ribeiro JMC, Van Den Abbeele J, Attardo G, Hao ZR, et al. (2010) An insight into the sialome of Glossina morsitans morsitans. BMC Genomics 11: 213.
60. Martin-Martin I, Molina R, Jimenez M, (2012) An insight into the Phlebotomus perniciosus saliva by a proteomic approach. Acta Trop 123: 22-30.
61. Bahia D, Gontijo NF, Leon IR, Perales J, Pereira MH, et al. (2007) Antibodies from dogs with canine visceral leishmaniasis recognise two proteins from the saliva of Lutzomyia longipalpis. Parasitol Res 100: 449-454.
62. Hostomska J, Rohousova I, Volfova V, Stanneck D, Mencke N, et al. (2008) Kinetics of canine antibody response to saliva of the sand fly Lutzomyia longipalpis. Vector Borne Zoonotic Dis 8: 443-450.
63. Vlkova M, Rohousova I, Drahota J, Stanneck D, Kruedewagen EM, et al. (2011) Canine antibody response to Phlebotomus perniciosus bites negatively correlates with the risk of Leishmania infantum transmission. PLoS Negl Trop Dis 5: e1344.
64. Gomes RB, Mendonça IL, Silva VC, Ruas J, Silva MB, et al. (2007) Antibodies against Lutzomyia longipalpis saliva in the fox Cerdocyon thous and the sylvatic cycle of Leishmania chagasi. Trans R Soc Trop Med Hyg 101: 127-133.
65. Gomes RB, Brodskyn U, de Oliveira CI, Costa J, Miranda JC, et al. (2002) Seroconversion against Lutzomyia longipalpis saliva concurrent with the development of anti-Leishmania chagasi delayed-type hypersensitivity. J Infect Dis 186: 1530-1534.
66. Vinhas V, Andrade BB, Paes F, Bomura A, Clarencio J, et al. (2007) Human anti-saliva immune response following experimental exposure to the visceral leishmaniasis vector, Lutzomyia longipalpis. Eur J Immunol 37: 3111-3121.
67. Marzouki S, Ahmed MB, Boussoffara T, Abdeladhim M, Aleya-Bouafif NB, et al. (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: 653-661.
68. Collin N, Gomes R, Teixeira C, Cheng L, Laughinghouse A, et al. (2009) Sand fly salivary proteins induce strong cellular immunity in a natural reservoir of visceral leishmaniasis with adverse consequences for Leishmania. PLoS Pathog 5: e1000441.
69. Santos A, Ribeiro JM, Lehane MJ, Gontijo NF, Veloso AB, et al. (2007) The sialotranscriptome of the blood-sucking bug Triatoma brasiliensis (Hemiptera: Triatominae). Insect Biochem Mol Biol 37: 702-712.
70. Jariyapan N, Roytrakul S, Paemanee A, Junkum A, Saeung A, et al. (2012) Proteomic analysis of salivary glands of female Anopheles barbirostris species A2 (Diptera: Culicidae) by two-dimensional gel electrophoresis and mass spectrometry. Parasitol Res 111: 1239-1249.
71. Andersen JF, Hinnebusch BJ, Lucas DA, Conrads TP, Veenstra TD, et al. (2007) An insight into the sialome of the oriental rat flea, Xenopsylla cheopis (Rots). BMC Genomics 8: 102.
72. Caljon G, De Ridder K, De Baetselier P, Coosemans M, Van Den Abbeele J, (2010) Identification of a tsetse fly salivary protein with dual inhibitory action on human platelet aggregation. PLoS One 5: e9671.
73. Perez de Leon AA, Tabachnick WJ, (1996) Apyrase activity and adenosine diphosphate induced platelet aggregation inhibition by the salivary gland proteins of Culicoides variipennis, the North American vector of bluetongue viruses. Vet Parasitol 61: 327-338.
74. Ma D, Wang Y, Yang H, Wu J, An S, et al. (2009) Anti-thrombosis repertoire of blood-feeding horsefly salivary glands. Mol Cell Proteomics 8: 2071-2079.
75. Wu S, Peiffer M, Luthe DS, Felton GW, (2012) ATP hydrolyzing salivary enzymes of caterpillars suppress plant defenses. PLoS One 7: e41947.
76. Fenckova M, Hobizalova R, Fric ZF, Dolezal T, (2011) Functional characterization of ecto-5′-nucleotidases and apyrases in Drosophila melanogaster. Insect Biochem Mol Biol 41: 956-967.
77. Ribeiro JM, Mans BJ, Arca B, (2010) An insight into the sialome of blood-feeding Nematocera. Insect Biochem Mol Biol 40: 767-784.
78. Valenzuela JG, Charlab R, Galperin MY, Ribeiro JM, (1998) Purification, cloning and expression of an apyrase from the bed bug Cimex lectularius. A new type of nucleotide-binding enzyme. J Biol Chem 273: 30583-30590.
79. Valenzuela JG, Belkaid Y, Rowton E, Ribeiro JM, (2001b) The salivary apyrase of the blood-sucking sand fly Phlebotomus papatasi belongs to the novel Cimex family of apyrases. J Exp Biol 204: 229-237.
80. Hamasaki R, Kato H, Terayama Y, Iwata H, Valenzuela JG, (2009) Functional characterization of a salivary apyrase from the sand fly, Phlebotomus duboscqi, a vector of Leishmania major. J Insect Physiol 55: 1044-1049.
81. Ribeiro JMC, Rossignol PA, Spielman A, (1986) Blood-finding strategy of a capillary-feeding sandfly, Lutzomyia longipalpis. Comp Biochem Physiol 83A: 683-686.
82. Martin-Martin I, Molina R, Jimenez M, (2013) Identifying salivary antigens of Phlebotomus argentipes by a 2DE approach. Acta Trop 126: 229-239.
83. Stern R, Jedrzejas MJ, (2006) Hyaluronidases: their genomics, structures, and mechanisms of action. Chem Rev 106: 818-839.
84. Muller UR, (2011) Hymenoptera venom proteins and peptides for diagnosis and treatment of venom allergic patients. Inflamm Allergy Drug Targets 10: 420-428.
85. Ribeiro JM, Charlab R, Rowton ED, Cupp EW, (2000a) Simulium vittatum (Diptera: Simuliidae) and Lutzomyia longipalpis (Diptera: Psychodidae) salivary gland hyaluronidase activity. J Med Entomol 37: 743-747.
86. Volfova V, Hostomska J, Cerny M, Votypka J, Volf P, (2008) Hyaluronidase of bloodsucking insects and its enhancing effect on Leishmania infection in mice. PLoS Negl Trop Dis 2: e294.
87. Ribeiro JM, Charlab R, Pham VM, Garfield M, Valenzuela JG, (2004) An insight into the salivary transcriptome and proteome of the adult female mosquito Culex pipiens quinquefasciatus. Insect Biochem Mol Biol 34: 543-563.
88. Calvo E, Ribeiro JM, (2006) A novel secreted endonuclease from Culex quinquefasciatus salivary glands. J Exp Biol 209: 2651-2659.
89. Jacobson RL, Schlein Y, Eisenberger CL, (2001) The biological function of sand fly and Leishmania glycosidases. Med Microbiol Immunol 190: 51-55.
90. Ribeiro JM, Rowton ED, Charlab R, (2000b) Salivary amylase activity of the phlebotomine sand fly, Lutzomyia longipalpis. Insect Biochem Mol Biol 30: 271-277.
91. Jacobson RL, Schlein Y, (2001) Phlebotomus papatasi and Leishmania major parasites express alpha-amylase and alpha-glucosidase. Acta Trop 78: 41-49.
92. Andersen JF, Pham VM, Meng Z, Champagne DE, Ribeiro JM, (2009) Insight into the sialome of the black fly, Simulium vittatum. J Proteome Res 8: 1474-1488.
93. Campbell CL, Vandyke KA, Letchworth GJ, Drolet BS, Hanekamp T, et al. (2005) Midgut and salivary gland transcriptomes of the arbovirus vector Culicoides sonorensis (Diptera:Ceratopogonidae). Insect Mol Biol 14: 121-136.
94. Valenzuela JG, Charlab R, Gonzalez EC, de Miranda-Santos IK, Marinotti O, et al. (2002) The D7 family of salivary proteins in blood sucking diptera. Insect Mol Biol 11: 149-55.
95. Gonzalez-Caballero N, Valenzuela JG, Ribeiro JM, Cuervo P, Brazil RP, (2013) Transcriptome exploration of the sex pheromone gland of Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae). Parasit Vectors 6: 56.
96. Calvo E, Mans BJ, Andersen JF, Ribeiro JMC, (2006) Function and evolution of a mosquito salivary protein family. J Biol Chem 281: 1935-1942.
97. Mans BJ, Calvo E, Ribeiro JM, Andersen JF, (2007) The crystal structure of D7r4, a salivary biogenic amine-binding protein from the malaria mosquito Anopheles gambiae. J Biol Chem 282: 36626-36633.
98. Isawa H, Yuda M, Orito Y, Chinzei Y, (2002) A mosquito salivary protein inhibits activation of the plasma contact system by binding to factor XII and high molecular weight kininogen. J Biol Chem 277: 27651-27658.
99. Alvarenga PH, Francischetti IMB, Calvo E, Sa-Nunes A, Ribeiro JMC, et al. (2010) The function and three-dimensional structure of a tromboxane A(2)/cysteinyl leukotriene-binding protein from the saliva of a mosquito vector of the malaria parasite. Plos Biol 8: e1000547.
100. Marzouki S, Abdeladhim M, Abdessalem CB, Oliveira F, Ferjani B, et al. (2012) Salivary antigen SP32 is the immunodominant target of the antibody response to Phlebotomus papatasi bites in humans. PLoS Negl Trop Dis 6: e1911.
101. Elnaiem DE, Meneses C, Slotman M, Lanzaro GC, (2005) Genetic variation in the sand fly salivary protein, SP-15, a potential vaccine candidate against Leishmania major. Insect Mol Biol 14: 145-150.
102. Milne TJ, Abbenante G, Tyndall JD, Halliday J, Lewis RJ, (2003) Isolation and characterization of a cone snail protease with homology to CRISP proteins of the Pathogenesis-related Protein Superfamily. J Biol Chem 278: 31105-31110.
103. Yeats C, Bentley S, Bateman A, (2003) New knowledge from old: In silico discovery of novel protein domains in Streptomyces coelicolor. BMC Microbiol 3: 3.
104. Hoffman DR, (1993) Allergens in Hymenoptera venom. XXV: The amino acid sequences of antigen 5 molecules and the structural basis of antigenic cross-reactivity. J Allergy Clin Immunol 92: 707-716.
105. Lu G, Villalba M, Coscia MR, Hoffman DR, King TP, (1993) Sequence analysis and antigenic cross-reactivity of a venom allergen, antigen 5, from hornets, wasps, and yellow jackets. J Immunol 150: 2823-2830.
106. King TP, Spangfort MD, (2000) Structure and biology of stinging insect venom allergens. Int Arch Allergy Immunol 123: 99-106.
107. Asojo OA, Goud G, Dhar K, Loukas A, Zhan B, et al. (2005) X-ray structure of Na-ASP-2, a pathogenesis-related-1 protein from the nematode parasite, Necator americanus, and a vaccine antigen for human hookworm infection. J Mol Biol 346: 801-814.
108. Assumpção TC, Ma D, Schwarz A, Reiter K, Santana JM, et al. (2013) Salivary antigen-5/CAP family members are Cu2+-dependent antioxidant enzymes that scavenge O2- and inhibit collagen-induced platelet aggregation and neutrophil oxidative burst. J Biol Chem 288: 14341-14361.
109. Collin N, Assumpção TC, Mizurini DM, Gilmore DC, Dutra-Oliveira A, et al. (2012) 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. Arterioscler Thromb Vasc Biol 32: 2185-2198.
110. Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, et al. (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS One 7: e35671.
111. Svobodova M, Alten B, Zidkova L, Dvorak V, Hlavackova J, et al. (2009) Cutaneous leishmaniasis caused by Leishmania infantum transmitted by Phlebotomus tobbi. Int J Parasitol 39: 251-256.
112. Di Muccio T, Marinucci M, Frusteri L, Maroli M, Pesson B, et al. (2000) Phylogenetic analysis of Phlebotomus species belonging to the subgenus Larroussius (Diptera, psychodidae) by ITS2 rDNA sequences. Insect Biochem Mol Biol 30: 387-393.
113. Esseghir S, Ready P, Ben-Ismail R, (2000) Speciation of Phlebotomus sandflies of the subgenus Larroussius coincided with the late Miocene-Pliocene aridification of the Mediterranean subregion. Biol J Linn Soc Lond 70: 189-219.
114. Clements MF, Gidwani K, Kumar R, Hostomska J, Dinesh DS, et al. (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: 801-807.
115. Barral A, Honda E, Caldas A, Costa J, Vinhas V, et al. (2000) Human immune response to sand fly salivary gland antigens: a useful epidemiological marker? Am J Trop Med Hyg 62: 740-745.
116. de Moura TR, Oliveira F, Novais FO, Miranda JC, Clarencio J, et al. (2007) Enhanced Leishmania braziliensis infection following pre-exposure to sandfly saliva. PLoS Negl Trop Dis 1: e84.
117. Aquino DM, Caldas AJ, Miranda JC, Silva AA, Barral-Netto M, et al. (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: 825-827.