Salivary gland transcriptomes and proteomes of phlebotomus tobbi and phlebotomus sergenti, vectors of leishmaniasis

PLoS Neglected Tropical Diseases

Volumn 6, Issue 5, 2012, Pages

  Rohoušová, Iva ^a   Subrahmanyam, Sreenath ^b   Volfová, Věra ^a   Mu, Jianbing ^b   Volf, Petr ^a   Valenzuela, Jesus G ^b   Jochim, Ryan C ^b  

^a CHARLES UNIVERSITY   (Czech Republic)

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

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN 5 RELATED PROTEIN; APYRASE; D7 RELATED PROTEIN; HYALURONIDASE; ODORANT BINDING RELATED PROTEIN; PARSP25 PROTEIN; PPSP15 PROTEIN; PPSP32 PROTEIN; SALIVA PROTEIN; UNCLASSIFIED DRUG; PROTEOME; TRANSCRIPTOME;

ARTICLE; BIOINFORMATICS; DNA LIBRARY; DNA SEQUENCE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; FEMALE; HIGH THROUGHPUT SCREENING; IMMUNOBLOTTING; LEISHMANIASIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHLEBOTOMUS; PHLEBOTOMUS SERGENTI; PHLEBOTOMUS TOBBI; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEOME; SALIVARY GLAND; SEQUENCE ALIGNMENT; TRANSCRIPTOME; UNINDEXED SEQUENCE; ANIMAL; BIOSYNTHESIS; CHEMISTRY; DISEASE CARRIER; GENETICS; MOLECULAR GENETICS;

ANIMALS; DISEASE VECTORS; FEMALE; MOLECULAR SEQUENCE DATA; PHLEBOTOMUS; PROTEOME; SALIVARY GLANDS; SALIVARY PROTEINS AND PEPTIDES; SEQUENCE ANALYSIS, DNA; TRANSCRIPTOME;

EID: 84863648527     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001660     Document Type: Article

References (93)

1. Titus RG, Ribeiro JMC, (1988) Salivary-Gland Lysates from the Sand Fly Lutzomyia-Longipalpis Enhance Leishmania Infectivity. Science 239: 1306-1308.
2. Rohousova I, Volf P, (2006) Sand fly saliva: effects on host immune response and Leishmania transmission. Folia Parasitol 53: 161-171.
3. Belkaid Y, Kamhawi S, Modi G, Valenzuela J, Noben-Trauth N, et al. (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: 1941-1953.
4. Kamhawi S, Belkaid Y, Modi G, Rowton E, Sacks D, (2000) Protection against cutaneous Leishmaniasis resulting from bites of uninfected sand flies. Science 290: 1351-1354.
5. Morris RV, Shoemaker CB, David JR, Lanzaro GC, Titus RG, (2001) Sandfly maxadilan exacerbates infection with Leishmania major and vaccinating against it protects against L-major infection. J Immunol 167: 5226-5230.
6. 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.
7. 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.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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.
14. Aquino DMC, Caldas AJM, Miranda JC, Silva AAM, Barral-Netto M, et al. (2010) Short report: 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.
15. 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.
16. 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.
17. Gidwani K, Picado A, Rijal S, Singh SP, Roy L, et al. (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.
18. Marzouki S, Ben Ahmed M, Boussoffara T, Abdeladhim M, Ben Aleya-Bouafif N, 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.
19. 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.
20. 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.
21. 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.
22. Volf P, Rohousova I, (2001) Species-specific antigens in salivary glands of phlebotomine sandflies. Parasitology 122: 37-41.
23. 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.
24. 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.
25. 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: 52.
26. 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.
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. 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.
29. Killick-Kendrick R, (1999) The biology and control of phlebotomine sand flies. Clin Dermatol 17: 279-289.
30. Svobodova M, Votypka J, (2003) Experimental transmission of Leishmania tropica to hamsters and mice by the bite of Phlebotomus sergenti. Microbes Infect 5: 471-4.
31. Svobodova M, Votypka J, Peckova J, Dvorak V, Nasereddin A, et al. (2006) Distinct transmission cycles of Leishmania tropica in 2 adjacent foci, Northern Israel. Emerg Infect Dis 12: 1860-8.
32. 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: 251-6.
33. Aransay AM, Scoulica E, Tselentis Y, Ready PD, (2000) Phylogenetic relationships of phlebotomine sandflies inferred from small subunit nuclear ribosomal DNA. Insect Mol Bio 9: 157-168.
34. Maia C, Afonso MO, Neto L, Dionisio L, Campino L, (2009) Molecular detection of Leishmania infantum in naturally infected Phlebotomus perniciosus from Algarve region, Portugal. J Vector Borne Dis 46: 268-272.
35. Volf P, Volfova V, (2011) Establishment and maintenance of sand fly colonies. J Vector Ecol 36: S1-S9.
36. 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.
37. Drastichova Z, Bourova L, Hejnova L, Jedelsky P, Svoboda P, et al. (2010) Protein alterations induced by long-term agonist treatment of HEK293 cells expressing thyrotropin-releasing hormone receptor and G(11)alpha protein. J Cell Biochem 109: 255-264.
38. Guo YJ, Ribeiro JMC, Anderson JM, Bour S, (2009) dCAS: a desktop application for cDNA sequence annotation. Bioinformatics 25: 1195-1196.
39. Huang XQ, Madan A, (1999) CAP3: A DNA sequence assembly program. Genome Res 9: 868-877.
40. 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.
41. Ewing B, Green P, (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8: 186-194.
42. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
43. 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.
44. 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.
45. Bateman A, Birney E, Durbin R, Eddy SR, Howe KL, et al. (2000) The Pfam protein families database. Nucleic Acids Res 28: 263-266.
46. 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.
47. Bendtsen JD, Nielsen H, von Heijne G, Brunak S, (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
48. NetNGlyc 1.0 Server. Available:http://www.cbs.dtu.dk/services/NetNGlyc/.
49. 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.
50. Abascal F, Zardoya R, Posada D, (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105.
51. Schmidt HA, Strimmer K, Vingron M, von Haeseler A, (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504.
52. 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.
53. 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.
54. Frost GI, Stern R, (1997) A microtiter-based assay for hyaluronidase activity not requiring specialized reagents. Anal Biochem 251: 263-269.
55. Ribeiro JMC, Arca B, (2009) From Sialomes to the Sialoverse: An Insight into Salivary Potion of Blood-Feeding Insects. Adv In Insect Phys 37: 59-118.
56. Ribeiro JMC, Mans BJ, Arca B, (2010) An insight into the sialome of blood-feeding Nematocera. Insect Biochem Mol Biol 40: 767-784.
57. 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.
58. Ameri M, Wang X, Wilkerson MJ, Kanost MR, Broce AB, (2008) An immunoglobulin binding protein (Antigen 5) of the stable fly (Diptera: Muscidae) salivary gland stimulates bovine immune responses. J Med Entomol 45: 94-101.
59. Ma DY, Gao L, An S, Song YZ, Wu J, et al. (2010) A horsefly saliva antigen 5-like protein containing RTS motif is an angiogenesis inhibitor. Toxicon 55: 45-51.
60. Xu XQ, Yang HL, Ma DY, Wu J, Wang YP, et al. (2008) Toward an understanding of the molecular mechanism for successful blood feeding by coupling proteomics analysis with pharmacological testing of horsefly salivary glands. Mol Cell Proteomics 7: 582-590.
61. Schaffartzik A, Weichel M, Crameri R, Bjornsdottir PS, Prisi C, et al. (2009) Cloning of IgE-binding proteins from Simulium vittatum and their potential significance as allergens for equine insect bite hypersensitivity. Vet Immunol Immunopathol 132: 68-77.
62. Schaffartzik A, Marti E, Crameri R, Rhyner C, (2010) Cloning, production and characterization of antigen 5 like proteins from Simulium vittatum and Culicoides nubeculosus, the first cross-reactive allergen associated with equine insect bite hypersensitivity. Vet Immunol Immunopathol 137: 76-83.
63. Caljon G, Broos K, De Goeyse I, De Ridder K, Sternberg JM, et al. (2009) Identification of a functional Antigen5-related allergen in the saliva of a blood feeding insect, the tsetse fly. Insect Biochem Mol Biol 39: 332-41.
64. Ribeiro JMC, Rossignol PA, Spielman A, (1986) Blood-Finding Strategy of A Capillary-Feeding Sandfly, Lutzomyia-Longipalpis. Comp Biochem Physiol A Comp Physiol 83: 683-686.
65. Ribeiro JMC, Modi GB, Tesh RB, (1989) Salivary apyrase activity of some Old World Phlebotomine sand flies. Insect Biochem 19: 409-412.
66. 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.
67. Valenzuela JG, Belkaid Y, Rowton E, Ribeiro JMC, (2001) 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.
68. Smith TM, Kirley TL, (2006) The calcium activated nucleotidases: A diverse family of soluble and membrane associated nucleotide hydrolyzing enzymes. Purinergic Signal 2: 327-333.
69. Yang MY, Kirley TL, (2004) Site-directed mutagenesis of human soluble calcium-activated nucleotidase 1 (hSCAN-1): Identification of residues essential for enzyme activity and the Ca2+-induced conformational change. Biochemistry 43: 9185-9194.
70. Dai JY, Liu J, Deng YQ, Smith TM, Lu M, (2004) Structure and protein design of a human platelet function inhibitor. Cell 116: 649-659.
71. Stern R, (2003) Devising a pathway for hyaluronan catabolism: are we there yet? Glycobiology 13: 105R-115R.
72. 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.
73. Ribeiro JMC, Charlab R, Rowton ED, Cupp EW, (2000) Simulium vittatum (Diptera: Simuliidae) and Lutzomyia longipalpis (Diptera: Psychodidae) salivary gland hyaluronidase activity. J Med Entomol 37: 743-747.
74. Stern R, Jedrzejas MJ, (2006) Hyaluronidases: Their genomics, structures, and mechanisms of action. Chem Rev 106: 818-839.
75. Markovic-Housley Z, Miglierini G, Soldatova L, Rizkallah PJ, Muller U, et al. (2000) Crystal structure of hyaluronidase, a major allergen of bee venom. Structure 8: 1025-1035.
76. Wilson AD, Heesom KJ, Mawby WJ, Mellor PS, Russell CL, (2008) Identification of abundant proteins and potential allergens in Culicoides nubeculosus salivary glands. Vet Immunol Immunopathol 122: 94-103.
77. 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.
78. Valenzuela JG, Charlab R, Gonzalez EC, de Miranda-Santos IKF, Marinotti O, et al. (2002) The D7 family of salivary proteins in blood sucking diptera. Insect Mol Bio 11: 149-155.
79. James AA, Blackmer K, Marinotti O, Ghosn CR, Racioppi JV, (1991) Isolation and Characterization of the Gene Expressing the Major Salivary-Gland Protein of the Female Mosquito, Aedes-Aegypti. Molecul Biochem Parasitol 44: 245-254.
80. Geng YJ, Gao ST, Huang DN, Zhao YR, Liu JP, et al. (2009) Differentially expressed genes between female and male adult Anopheles anthropophagus. Parasitol Res 105: 843-851.
81. Calvo E, Mans BJ, Andersen JF, Ribeiro JMC, (2006) Function and evolution of a mosquito salivary protein family. J Biol Chem 281: 1935-1942.
82. Isawa H, Orito Y, Iwanaga S, Jingushi N, Morita A, et al. (2007) Identification and characterization of a new kallikrein-kinin system inhibitor from the salivary glands of the malaria vector mosquito Anopheles stephensi. Insect Biochem Mol Biol 37: 466-477.
83. Alvarenga PH, Francischetti IMB, Calvo E, Sa-Nunes A, Ribeiro JMC, et al. (2010) The Function and Three-Dimensional Structure of a Thromboxane A(2)/Cysteinyl Leukotriene-Binding Protein from the Saliva of a Mosquito Vector of the Malaria Parasite. Plos Biol 8: e1000547.
84. 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.
85. 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.
86. Elnaiem DEA, 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 Bio 14: 145-150.
87. Coutinho-Abreu IV, Wadsworth M, Stayback G, Ramalho-Ortigao M, McDowell MA, (2010) Differential Expression of Salivary Gland Genes in the Female Sand Fly Phlebotomus papatasi (Diptera: Psychodidae). J Med Entomol 47: 1146-1155.
88. Schmitzova J, Klaudiny J, Albert S, Schroder W, Schreckengost W, et al. (1998) A family of major royal jelly proteins of the honeybee Apis mellifera L. Cell Mol Life Sci 54: 1020-1030.
89. Geyer PK, Spana C, Corces VG, (1986) On the Molecular Mechanism of Gypsy-Induced Mutations at the Yellow Locus of Drosophila-Melanogaster. EMBO J 5: 2657-2662.
90. Albert S, Bhattacharya D, Klaudiny J, Schmitzova J, Simuth J, (1999) The family of major royal jelly proteins and its evolution. J Mol Evol 49: 290-297.
91. 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.
92. 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.
93. Volf P, Skarupova S, Man P, (2002) Characterization of the lectin from females of Phlebotomus duboscqi sand flies. Eur J Biochem 269: 6294-6301.