Analysis of salivary gland transcripts of the sand fly Lutzomyia ayacuchensis, a vector of Andean-type cutaneous leishmaniasis

Infection, Genetics and Evolution

Volumn 13, Issue 1, 2013, Pages 56-66

  Kato, Hirotomo ^a   Jochim, Ryan C ^b   Gomez, Eduardo A ^c   Uezato, Hiroshi ^d   Mimori, Tatsuyuki ^e   Korenaga, Masataka ^f   Sakurai, Tatsuya ^a   Katakura, Ken ^a   Valenzuela, Jesus G ^b   Hashiguchi, Yoshihisa ^f,g,h  

^a HOKKAIDO UNIVERSITY   (Japan)

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

^c Servicio Nacional de Erradicacion de la Malaria (SNEM)   (Ecuador)

^d UNIVERSITY OF THE RYUKYUS   (Japan)

^e KUMAMOTO UNIVERSITY   (Japan)

^f KOCHI UNIVERSITY   (Japan)

^g Prometeo Secretaria Nacional de Educacion Superior   (Ecuador)

^h UNIVERSIDAD CENTRAL DEL ECUADOR   (Ecuador)

Author keywords

Bioinformatics; CDNA library; Lutzomyia ayacuchensis; Salivary gland; Transcript

Indexed keywords

ANTIGEN 5 RELATED PROTEIN; APYRASE; ARGINYLGLYCYLASPARTIC ACID; COMPLEMENTARY DNA; D7 FAMILY PROTEIN; INSECT PROTEIN; MAXADILAN; PROTEIN PPSP14; S1 LIKE PROTEIN; SALIVA PROTEIN; UNCLASSIFIED DRUG; YELLOW RELATED PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; DISEASE CARRIER; DNA BARCODING; DNA LIBRARY; ENZYME ACTIVITY; GENETIC TRANSCRIPTION; INSECT GENETICS; LUTZOMYIA; LUTZOMYIA AYACUCHENSIS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; SALIVARY GLAND; SKIN LEISHMANIASIS; UNINDEXED SEQUENCE;

AMINO ACID SEQUENCE; ANIMALS; GENE LIBRARY; GENES, ESSENTIAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; LEISHMANIASIS, CUTANEOUS; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; PSYCHODIDAE; SALIVARY GLANDS; SALIVARY PROTEINS AND PEPTIDES; SEQUENCE ALIGNMENT; TRANSCRIPTOME;

ARTHROPODA; HELCOCYRTOMYIA; HEXAPODA; LUTZOMYIA AYACUCHENSIS; LUTZOMYIA LONGIPALPIS; PHLEBOTOMINAE;

EID: 84870289003     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2012.08.024     Document Type: Article

References (68)

1. Aires J.M., Chociay M.F., Nascimento M.M., Figueiredo J.F., Roselino A.M. Maxadilan (MAX) - Salivaly protein of Lutzomyia longipalpis: detection of antibodies anti-MAX in American tegmentar leishmaniasis (ATL), and genetic and protein expression of MAX in Lutzomyia neivai. An. Bras. Dermatol. 2005, 80:S333-338.
2. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-4002.
3. Andersen J.F., Pham V.M., Meng Z., Champagne D.E., Ribeiro J.M.C. Insight into the sialome of the Black Fly, Simulium vittatum. J. Proteome Res. 2009, 8:1474-1488.
4. Anderson J.M., Oliveira F., Kamhawi S., Mans B.J., Reynoso D., Seitz A.E., Lawyer P., Garfield M., Pham M., Valenzuela J.G. Comparative salivary gland transcriptomics of sandfly vectors of visceral leishmaniasis. BMC Genomics 2006, 7:52.
5. Arcà B., Lombardo F., Francischetti I.M.B., Pham V.M., Mestres-Simon M., Andersen J.F., Ribeiro J.M.C. An insight into the sialome of the adult female mosquito Aedes albopictus. Insect Biochem. Mol. Biol. 2007, 37:107-127.
6. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., Davis A.P., Dolinski K., Dwight S.S., Eppig J.T., Harris M.A., Hill D.P., Issel-Tarver L., Kasarskis A., Lewis S., Matese J.C., Richardson J.E., Ringwald M., Rubin G.M., Sherlock G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 2000, 25:25-29.
7. Assumpção T.C., Francischetti I.M.B., Andersen J.F., Schwarz A., Santana J.M., Ribeiro J.M.C. An insight into the sialome of the blood-sucking bug Triatoma infestans, a vector of Chagas' disease. Insect Biochem. Mol. Biol. 2008, 38:213-232.
8. Bateman A., Birney E. Searching databases to find protein domain organization. Adv. Protein Chem. 2000, 54:137-157.
9. Belkaid Y., Kamhawi S., Modi G., Valenzuela J., Noben-Trauth N., Rowton E., Ribeiro J., Sacks D.L. 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. 1998, 188:1941-1953.
10. Belkaid Y., Valenzuela J.G., Kamhawi S., Rowton E., Sacks D.L., Ribeiro J.M.C. Delayed-type hypersensitivity to Phlebotomus papatasi sand fly bite: an adaptive response induced by the fly?. Proc. Natl. Acad. Sci. USA 2000, 97:6704-6709.
11. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004, 340:783-795.
12. Caceres A.G., Villaseca P., Dujardin J.C., Bañuls A.L., Inga R., Lopez M., Arana M., Le Ray D., Arevalo J. Epidemiology of Andean cutaneous leishmaniasis: incrimination of Lutzomyia ayacuchensis (Diptera: psychodidae) as a vector of Leishmania in geographically isolated, upland valleys of Peru. Am. J. Trop. Med. Hyg. 2004, 70:607-612.
13. Calvo E., Mans B.J., Andersen J.F., Ribeiro J.M.C. Function and evolution of a mosquito salivary protein family. J. Biol. Chem. 2006, 281:1935-1942.
14. Campbell C.L., Vandyke K.A., Letchworth G.J., Drolet B.S., Hanekamp T., Wilson W.C. Midgut and salivary gland transcriptomes of the arbovirus vector Culicoides sonorensis (Diptera: Ceratopogonidae). Insect Mol. Biol. 2005, 14:121-136.
15. Charlab R., Valenzuela J.G., Rowton E.D., Ribeiro J.M.C. Toward an understanding of the biochemical and pharmacological complexity of the saliva of a hematophagous sand fly Lutzomyia longipalpis. Proc. Natl. Acad. Sci. USA 1999, 96:15155-15160.
16. Charlab R., Rowton E.D., Ribeiro J.M.C. The salivary adenosine deaminase from the sand fly Lutzomyia longipalpis. Exp. Parasitol. 2000, 95:45-53.
17. Faudry E., Rocha P.S., Vernet T., Lozzi S.P., Teixeira A.R. Kinetics of expression of the salivary apyrases in Triatoma infestans. Insect Biochem. Mol. Biol. 2004, 34:1051-1058.
18. Francischetti I.M.B., Valenzuela J.G., Pham V.M., Garfield M.K., Ribeiro J.M.C. Toward a catalog for the transcripts and proteins (sialome) from the salivary gland of the malaria vector Anopheles gambiae. J. Exp. Biol. 2002, 205:2429-2451.
19. Gomes R., Teixeira C., Teixeira M.J., Oliveira F., Menezes M.J., Silva C., de Oliveira C.I., Miranda J.C., Elnaiem D.E., Kamhawi S., Valenzuela J.G., Brodskyn C.I. 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. USA 2008, 105:7845-7850.
20. Hamasaki R., Kato H., Terayama Y., Iwata H., Valenzuela J.G. Functional characterization of a salivary apyrase from the sand fly, Phlebotomus duboscqi, a vector of Leishmania major. J. Insect Physiol. 2009, 55:1044-1049.
21. Hoffman D.R. 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. 1993, 92:707-716.
22. Hostomská J., Volfová V., Mu J., Garfield M., Rohousová I., Volf P., Valenzuela J.G., Jochim R.C. Analysis of salivary transcripts and antigens of the sand fly Phlebotomus arabicus. BMC Genomics 2009, 10:282.
23. Huang X. A contig assembly program based on sensitive detection of fragment overlaps. Genomics 1992, 14:18-25.
24. Hynes R.O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992, 69:11-25.
25. Isawa H., Yuda M., Orito Y., Chinzei Y. A mosquito salivary protein inhibits activation of the plasma contact system by binding to factor XII and high molecular weight kininogen. J. Biol. Chem. 2002, 277:27651-27658.
26. James A.A., Blackmer K., Marinotti O., Ghosn C.R., Racioppi J.V. Isolation and characterization of the gene expressing the major salivary gland protein of the female mosquito, Aedes aegypti. Mol. Biochem. Parasitol. 1991, 44:245-253.
27. Kamhawi S., Belkaid Y., Modi G., Rowton E., Sacks D. Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science 2000, 290:1351-1354.
28. Kato H., Uezato H., Katakura K., Calvopiña M., Marco J.D., Barroso P.A., Gomez E.A., Mimori T., Korenaga M., Iwata H., Nonaka S., Hashiguchi Y. Detection and identification of Leishmania species within naturally infected sand flies in the andean areas of Ecuador by a polymerase chain reaction. Am. J. Trop. Med. Hyg. 2005, 72:87-93.
29. Kato H., Anderson J.M., Kamhawi S., Oliveira F., Lawyer P.G., Pham V.M., Sangare C.S., Samake S., Sissoko I., Garfield M., Sigutova L., Volf P., Doumbia S., Valenzuela J.G. High degree of conservancy among secreted salivary gland proteins from two geographically distant Phlebotomus duboscqi sandflies populations (Mali and Kenya). BMC Genomics 2006, 7:226.
30. Kato H., Cáceres A.G., Gomez E.A., Mimori T., Uezato H., Marco J.D., Barroso P.A., Iwata H., Hashiguchi Y. Molecular mass screening to incriminate sand fly vectors of Andean-type cutaneous leishmaniasis in Ecuador and Peru. Am. J. Trop. Med. Hyg. 2008, 79:719-721.
31. Kato H., Gomez E.A., Cáceres A.G., Uezato H., Mimori T., Hashiguchi Y. Molecular epidemiology for vector research on leishmaniasis. Int. J. Environ. Res. Public Health 2010, 7:814-826.
32. Kato H., Jochim R.C., Gomez E.A., Sakoda R., Iwata H., Valenzuela J.G., Hashiguchi Y. A repertoire of the dominant transcripts from the salivary glands of the blood-sucking bug, Triatoma dimidiata, a vector of Chagas disease. Infect. Genet. Evol. 2010, 10:184-191.
33. Katz O., Waitumbi J.N., Zer R., Warburg A. Adenosine, AMP, and protein phosphatase activity in sandfly saliva. Am. J. Trop. Med. Hyg. 2000, 62:145-150.
34. King T.P., Spangfort M.D. Structure and biology of stinging insect venom allergens. Int. Arch. Allergy Immunol. 2000, 123:99-106.
35. Lerner E.A., Ribeiro J.M.C., Nelson R.J., Lerner M.R. Isolation of maxadilan, a potent vasodilatory peptide from the salivary glands of the sand fly Lutzomyia longipalpis. J. Biol. Chem. 1991, 266:11234-11236.
36. Lima H.C., Titus R.G. Effects of sand fly vector saliva on development of cutaneous lesions and the immune response to Leishmania braziliensis in BALB/c mice. Infect. Immun. 1996, 64:5442-5445.
37. Lu X., Deadman J.J., Williams J.A., Kakkar V.V., Rahman S. Synthetic RGD peptides derived from the adhesive domains of snake-venom proteins: evaluation as inhibitors of platelet aggregation. Biochem. J. 1993, 296:21-24.
38. Marchler-Bauer A., Panchenko A.R., Ariel N., Bryant S.H. Comparison of sequence and structure alignments for protein domains. Proteins 2002, 48:439-446.
39. Munstermann L.E. Phlebotomine sand flies, the Psychodidae. Biology of Disease Vectors 2005, 41-151. Elsevier, San Diego, CA. second ed. W.C. Marquardt, W.C. Black, J.E. Freier, H.H. Hagedorn, J. Hemingway, S. Higgs, A.A. James, B. Kondratieff, C.G. Moore (Eds.).
40. Oliveira F., Kamhawi S., Seitz A.E., Pham V.M., Guigal P.M., Fischer L., Ward J., Valenzuela J.G. From transcriptome to immunome: identification of DTH inducing proteins from a Phlebotomus ariasi salivary gland cDNA library. Vaccine 2006, 24:374-390.
41. Oliveira F., Lawyer P.G., Kamhawi S., Valenzuela J.G. Immunity to distinct sand fly salivary proteins primes the anti-Leishmania immune response towards protection or exacerbation of disease. PLoS Negl. Trop. Dis. 2008, 2:e226.
42. Oliveira F., Jochim R.C., Valenzuela J.G., Kamhawi S. Sand flies, Leishmania, and transcriptome-borne solutions. Parasitol. Int. 2009, 58:1-5.
43. Ribeiro J.M.C. Blood-feeding arthropods: live syringes or invertebrate pharmacologists?. Infect. Agents Dis. 1995, 4:143-152.
44. Ribeiro J.M.C., Francischetti I.M.B. Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annu. Rev. Entomol. 2003, 48:73-88.
45. Ribeiro J.M.C., Modi G. The salivary adenosine/AMP content of Phlebotomus argentipes Annandale and Brunetti, the main vector of human kala-azar. J. Parasitol. 2001, 87:915-917.
46. Ribeiro J.M.C., Vachereau A., Modi G.B., Tesh R.B. A novel vasodilatory peptide from the salivary glands of the sand fly Lutzomyia longipalpis. Science 1989, 243:212-214.
47. Ribeiro J.M.C., Katz O., Pannell L.K., Waitumbi J., Warburg A. Salivary glands of the sand fly Phlebotomus papatasi contain pharmacologically active amounts of adenosine and 5'-AMP. J. Exp. Biol. 1999, 202:1551-1559.
48. Ribeiro J.M.C., Andersen J., Silva-Neto M.A., Pham V.M., Garfield M.K., Valenzuela J.G. Exploring the sialome of the blood-sucking bug Rhodnius prolixus. Insect Biochem. Mol. Biol. 2004, 34:61-79.
49. RohouŠová I., Volf P. Sand fly saliva: effects on host immune response and Leishmania transmission. Folia Parasitol. 2006, 53:161-171.
50. RohouŠová I., Subrahmanyam S., Volfová V., Mu J., Volf P., Valenzuela J.G., Jochim R.C. Salivary gland transcriptomes and proteomes of Phlebotomus tobbi and Phlebotomus sergenti, vectors of leishmaniasis. PLoS Negl. Trop. Dis. 2012, 6:e1660.
51. Santos A., Ribeiro J.M.C., Lehane M.J., Gontijo N.F., Veloso A.B., Sant'Anna M.R., Nascimento Araujo R., Grisard E.C., Pereira M.H. The sialotranscriptome of the blood-sucking bug Triatoma brasiliensis (Hemiptera, Triatominae). Insect Biochem. Mol. Biol. 2007, 37:702-712.
52. Schultz J., Milpetz F., Bork P., Ponting C.P. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. USA 1998, 95:5857-5864.
53. Singh H., Raghava G.P. ProPred: prediction of HLA-DR binding sites. Bioinformatics 2001, 17:1236-1237.
54. Takaoka H., Gomez E.A., Alexander J.B., Hashiguchi Y. Natural infections with Leishmania promastigotes in Lutzomyia ayacuchensis (Diptera: Psychodidae) in an Andean focus of Ecuador. J. Med. Entomol. 1990, 27:701-702.
55. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
56. Tavares N.M., Silva R.A., Costa D.J., Pitombo M.A., Fukutani K.F., Miranda J.C., Valenzuela J.G., Barral A., de Oliveira C.I., Barral-Netto M., Brodskyn C. Lutzomyia longipalpis saliva or salivary protein LJM19 protects against Leishmania braziliensis and the saliva of its vector, Lutzomyia intermedia. PLoS Negl. Trop. Dis. 2011, 5:e1169.
57. Teixeira C., Gomes R., Collin N., Reynoso D., Jochim R., Oliveira F., Seitz A., Elnaiem D.E., Caldas A., de Souza A.P., Brodskyn C.I., de Oliveira C.I., Mendonca I., Costa C.H., Volf P., Barral A., Kamhawi S., Valenzuela J.G. Discovery of markers of exposure specific to bites of Lutzomyia longipalpis, the vector of Leishmania infantum chagasi in Latin America. PLoS Negl. Trop. Dis. 2010, 4:e638.
58. Theodos C.M., Ribeiro J.M.C., Titus R.G. Analysis of enhancing effect of sand fly saliva on Leishmania infection in mice. Infect. Immun. 1991, 59:1592-1598.
59. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22:4673-4680.
60. Titus R.G., Ribeiro J.M.C. Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 1988, 239:1306-1308.
61. Valenzuela J.G. Blood-feeding arthropod salivary glands and saliva. Biology of Disease Vectors 2005, 377-386. Elsevier, San Diego, CA. second ed. W.C. Marquardt, W.C. Black, J.E. Freier, H.H. Hagedorn, J. Hemingway, S. Higgs, A.A. James, B. Kondratieff, C.G. Moore (Eds.).
62. Valenzuela J.G., Belkaid Y., Garfield M.K., Mendez S., Kamhawi S., Rowton E.D., Sacks D.L., Ribeiro J.M.C. Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. J. Exp. Med. 2001, 194:331-342.
63. Valenzuela J.G., Charlab R., Gonzalez E.C., de Miranda-Santos I.K., Marinotti O., Francischetti I.M.B., Ribeiro J.M.C. The D7 family of salivary proteins in blood sucking diptera. Insect Mol. Biol. 2002, 11:149-155.
64. Valenzuela J.G., Garfield M., Rowton E.D., Pham V.M. Identification of the most abundant secreted proteins from the salivary glands of the sand fly Lutzomyia longipalpis, vector of Leishmania chagasi. J. Exp. Biol. 2004, 207:3717-3729.
65. Vlkova M., Rohousova I., Drahota J., Stanneck D., Kruedewagen E.M., Mencke N., Otranto D., Volf P. Canine antibody response to Phlebotomus perniciosus bites negatively correlates with the risk of Leishmania infantum transmission. PLoS Negl. Trop. Dis. 2011, 5:e1344.
66. Weis W.I., Taylor M.E., Drickamer K. The C-type lectin superfamily in the immune system. Immunol. Rev. 1998, 163:19-34.
67. Xu X., Oliveira F., Chang B.W., Collin N., Gomes R., Teixeira C., Reynoso D., My Pham V., Elnaiem D.E., Kamhawi S., Ribeiro J.M.C., Valenzuela J.G., Andersen J.F. 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. 2011, 286:32383-32393.
68. Young, D.G., Duncan, M.A., 1994. Guide to the Identification and Geographic Distribution of Lutzomyia Sand Flies in Mexico, the West Indies, Central and South America (Diptera: Psychodidae), Memoirs of the American Entomological Institute, 54, Associated Publishers-American Entomological Institute, Gainsville, FL.