GP35 ANOAL, an abundant acidic glycoprotein of female Anopheles albimanus saliva

Insect Molecular Biology

Volumn 16, Issue 2, 2007, Pages 187-198

  Cazares Raga F E ^a,d   Gonzalez Lazaro M ^d   Montero Solis C ^b,d   Gonzalez Ceron L ^b   Zamudio, F ^c   Martinez Barnetche J ^a   Torres Monzon J A ^b,d   Ovilla Munoz M ^b   Aguilar Fuentes, J ^b   Rodriguez M H ^a   De La Cruz Hernandez Hernandez, Fidel ^d  

^a INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^b INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^c INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^d DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

Anopheles albimanus; Glycoprotein; GP35; Mosquito; Salivary glands; Sex specific

Indexed keywords

GLYCOPROTEIN; INSECT PROTEIN; MESSENGER RNA;

AMINO ACID SEQUENCE; ANIMAL; ANOPHELES; ARTICLE; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SALIVARY GLAND;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES; BASE SEQUENCE; FEMALE; GLYCOPROTEINS; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; RNA, MESSENGER; SALIVARY GLANDS;

AEDES AEGYPTI; ANOPHELES ALBIMANUS; CULEX PIPIENS; CULEX PIPIENS QUINQUEFASCIATUS;

EID: 33847700955     PISSN: 09621075     EISSN: 13652583     Source Type: Journal    
DOI: 10.1111/j.1365-2583.2006.00712.x     Document Type: Article

References (81)

1. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search Programs. Nucleic Acids Res 25: 3389-3402.
2. Andrews, L., Laughinghouse, A. and Sina, B.J. (1997) Lectin binding characteristics of male and female salivary gland proteins of Anopheles gambiae: identification and characterization of female specific glycoproteins. Insect Biochem Mol Biol 27: 159-166.
3. Arcà, B., Lombardo, F., de Lara Capurro, M., della Torre, A., Dimopoulos, G., James, A.A. and Coluzzi, M. (1999a) Trapping cDNAs encoding secreted proteins from the salivary glands of the malaria vector Anopheles gambiae. Proc Natl Acad Sci USA 96: 1516-1521.
4. Arcà, B., Lombardo, F., de Lara Capurro, M., della Torre, A., Spanos, L., Dimopoulos, G., et al. (1999b) Salivary glandspecific gene expression in the malaria vector Anopheles gambiae. Parassitologia 41: 483-487.
5. Arcà, B., Lombardo, F., Valenzuela, J.G., Francischetti, I.M., Marinotti, O., Coluzzi, M. and Ribeiro, J.M. (2005) An updated catalogue of salivary gland transcripts in the adult female mosquito, Anopheles gambiae. J Exp Biol 208: 3971-3986.
6. Barja-Fidalgo, C., Coelho, A., Saldanha-Gama, R., Helal-Neto, E., Mariano-Oliveira, A. and de Freitas, M. (2005) Disintegrins: integrin selective ligands which modulate leukocyte functions. Braz J Med Biol Res 38: 1513-1520.
7. Bendtsen, J.D., Nielsen, H., von Heijne, G. and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
8. Billingsley, P.F., Hodivala, K.J., Winger, L.A. and Sinden, R.E. (1991) Detection of mature malaria infections in live mosquitoes. Trans R Soc Trop Med Hyg 85: 450-453.
9. Blom, N., Gammeltoft, S. and Brunak, S. (1999) Sequence- and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294: 1351-1362.
10. Blom, N., Sicheritz-Ponten, T., Gupta, R., Gammeltoft, S. and Brunak, S. (2004) Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4: 1633-1649.
11. Brummer-Korvenkontio, H., Palosuo, T., Francois, G. and Reunala, T. (1997) Characterization of Aedes communis, Aedes aegypti and Anopheles stephensi mosquito saliva antigens by immunoblotting. Int Arch Allergy Immunol 112: 169-174.
12. Calvo, E., Andersen, J., Francischetti, I.M., de Lara Capurro, M., de Bianchi, A.G., James, A.A., Ribeiro, J.M. and Marinotti, O. (2004) The transcriptome of adult female Anopheles darlingi salivary glands. Insect Mol Biol 13: 73-88.
13. Cázares-Raga, F.E. (2000) Identificación de moléculas que se expresan en el estómago de mosquitos hembras de. Anopheles Albimanus. PhD Thesis. Centro de Investigación y de Estudios Avanzados del IPN, Mexico, D.F., Mexico.
14. Cázares-Raga, F.E., Sánchez-Contreras, M.E., Rodríguez, M.H. and Hernández-Hernández, F.C. (1998) Sex specific proteins and proteases present in the midguts of Anopheles albimanus (Diptera: Culicidae). J Med Entomol 35: 184-186.
15. Chan, A.S.T., Rodríguez, M.H., Torres, J.A., Rodríguez, M.C. and Villarreal, C. (1994) Susceptibility of three laboratory strains of Anopheles albimanus (Diptera: Culicidae) to coindigenous Plasmodium vivax. Southern Mexico. J Med Entomol 31: 400-403.
16. Dana, A.N., Hong, Y.S., Kern, M.I., Hillenmeyer, M., Harker, B., Lobo, N., et al. (2005) Gene expression patterns associated with blood-feeding in the malaria mosquito Anopheles gambiae. BMC Genomics 6(5): 1-24.
17. Emmanuelsson, O., Nielsen, H., Brunak, S. and von Heijne, G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016.
18. Feinberg, A.P. and Vogelstein, B. (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6-13.
19. Felsenstein, J. (1988) Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet 22: 521-565.
20. Fourney, R.M., Miyakoshi, J., Day, R.S. III and Paterson, M.C. (1988) Northern blotting: efficient RNA staining and transfer. Focus 10: 5-7.
21. Francischetti, I.M., Valenzuela, J.G., Pham, V.M., Garfield, M.K. and Ribeiro, J.M. (2002) Toward a catalog for the transcripts and proteins (sialome) from the salivary gland of the malaria vector Anopheles gambiae. J Exp Biol 205: 2429-2451.
22. Francischetti, I.M., Valenzuela, J.G. and Ribeiro, J.M. (1999) Anophelin: kinetics and mechanism of thrombin inhibition. Biochemistry 38: 16678-16685.
23. Frohman, M.A., Dush, M.K. and Martin, G.R. (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85: 8998-9002.
24. Gasmi, A., Srairi, N., Guermazi, S., Dkhil, H., Karoui, H. and El Ayeb, M. (2001) Amino acid structure and characterization of a heterodimeric disintegrin from Vipera lebetina venom. Biochim Biophys Acta 1547: 51-56.
25. Hansen, J.E., Lund, O., Tolstrup, N., Gooley, A.A., Williams, K.L. and Brunak, S. (1998) NetOglyc: prediction of mucin type Oglycosylation sites based on sequence context and surface accessibility. Glycoconjugate J 15: 115-130.
26. Higgins, D.G., Fuchs, R., Stoehr, P.J. and Cameron, G.N. (1992) The EMBL Data Library. Nucleic Acids Res 20(Suppl.): 2071-2074.
27. Isawa, H., Yuda, M., Orito, Y. and 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.
28. James, A.A. (1994) Molecular and biochemical analysis of the salivary glands of vector mosquitoes. Bull Inst Pasteur 92: 133-150.
29. James, A.A., Blackner, K., Marinotti, O., Ghosn, C.R. and Racioppi, J.V. (1991) Isolation and characterization of the gene expressing the major salivary gland protein of the female mosquito, Aedes aegypti. Mol Biochem Parasitol 44: 245-254.
30. Julenius, K., Mølgaard, A., Gupta, R. and Brunak, S. (2005) Prediction, conservation analysis and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 15: 153-164.
31. Kalume, D.E., Okulate, M., Zhong, J., Reddy, R., Suresh, S., Deshpande, N., et al. (2005b) A proteomic analysis of salivary glands of female Anopheles gambiae mosquito. Proteomics 5: 3765-3777.
32. Kalume, D.E., Peri, S., Reddy, R., Zhong, J., Okulate, M., Kumar, N. and Pandey, A. (2005a) Genome annotation of Anopheles gambiae using mass spectrometry-derived data. BMC Genomics 6: 128-121-11.
33. Korayem, A.M., Fabbri, M., Takahashi, K., Scherfer, C., Lindgren, M., Schmidt, O., et al. (2004) A Drosophila salivary gland mucin is also expressed in immune tissues: evidence for a function in coagulation and the entrapment of bacteria. Insect Biochem Mol Biol 34: 1297-1304.
34. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
35. Lanfrancotti, A., Lombardo, F., Santolamazza, F., Veneri, M., Castrignano, T., Coluzzi, M. and Arcà, B. (2002) Novel cDNAs encoding salivary proteins from the malaria vector Anopheles gambiae. FEBS Lett 517: 67-71.
36. Law, J.H., Ribeiro, J.M.C. and Wells, M.A. (1992) Biochemical insights derived from insect diversity. Annu Rev Biochem 61: 87-111.
37. Li, Z., Rossi, E.A., Hoheisel, J.D., Kalderon, D. and Rubin, C.S. (1999) Generation of a novel A kinase anchor protein and a myristoylated alanine-rich C kinase substrate-like analog from a single gene. J Biol Chem 274: 27191-27200.
38. Malandain, H. (2005) IgE-reactive carbohydrate epitopesclassification, cross-reactivity, and clinical impact. Allerg Immunol (Paris) 37: 122-128.
39. Marcinkiewicz, C., Calvete, J.J., Vijay-Kumar, S., Marcinkiewicz, M.M., Raida, M., Schick, P., et al. (1999) Structural and functional characterization of EMF10, a heterodimeric disintegrin from Eristocophis macmahoni venom that selectively inhibits alpha 5 beta 1 integrin. Biochemistry 38: 13302-13309.
40. Matsudaira, P. (1997) Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J Biol Chem 262: 10035-10038.
41. Montero-Solís, C., Gonzalez-Cerón, L., Rodríguez, M.H., Cirerol, B.E., Zamudio, F., Possani, L.D., et al. (2004) Identification and characterization of gp65, a salivary-gland-specific molecule expressed in the malaria vector Anopheles albimanus. Insect Mol Biol 13: 155-164.
42. Moreira, C.K., Marrelli, M.T., Lima, S.P. and Marinotti, O. (2001) Analysis of salivary gland proteins of the mosquito Anopheles darlingi (Diptera: Culicidae). J Med Entomol 38: 763-767.
43. Moreira-Ferro, C.K., Marinotti, O. and Bijovsky, A.T. (1999) Morphological and biochemical analyses of the salivary glands of the malaria vector, Anopheles darlingi. Tissue Cell 31: 264-273.
44. Mulder, N., Apweiler, J., Attwood, T.K., Bairoch, A., Barrell, D., Bateman, A., et al. (2003) The InterPro Database, 2003 brings increased coverage and new features. Nucleic Acids Res 31: 315-318.
45. Nielsen, B.L. and Brown, L.R. (1984) The basis for colored silverprotein complex formation in stained polyacrylamide gels. Anal Biochem 141: 311-315.
46. Nielsen, H., Engelbrecht, J., Brunak, S. and von Heijne, G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10: 1-6.
47. Nirmala, X., Marinotti, O. and James, A.A. (2005) The accumulation of specific mRNAs following multiple blood meals in Anopheles gambiae. Insect Mol Biol 14: 95-103.
48. North, M.J. (1989) Prevention of unwanted proteolysis. In Proteolytic Enzymes, a Practical Approach (eds Beynond, R.J. and Bond, J.S.), pp. 105-124. IRL Press at Oxford University Press, Oxford.
49. O'Farrell, P.H. (1975) High resolution two dimensional electrophoresis of proteins. J Biol Chem 250: 4007-4021.
50. Palosuo, K., Brummer-Korvenkontio, H., Mikkola, J., Sahi, T. and Reunala, T. (1997) Seasonal increase in human IgE and IgG4 antisaliva antibodies to Aedes mosquito bites. Int Arch Allergy Immunol 114: 367-372.
51. Peng, Z. and Simons, F.E. (1997) Cross-reactivity of skin and serum specific IgE responses and allergen analysis for three mosquito species with worldwide distribution. J Allergy Clin Immunol 100: 192-198.
52. Peng, Z. and Simons, F.E. (2004) Mosquito allergy: immune mechanisms and recombinant salivary allergens. Int Arch Allergy Immunol 133: 198-209.
53. Peng, Z., Xu, W., James, A.A., Lam, H., Sun, D., Cheng, L. and Simons, F.E. (2001) Expression, purification, characterization and clinical relevance of rAed a 1-a 68-kDa recombinant mosquito Aedes aegypti salivary allergen. Int Immunol 13: 1445-1452.
54. Perrone, J.B., De Maio, J. and Spielman, A. (1986) Regions of mosquito salivary glands distinguished by surface lectin binding characteristics. Insect Biochem 16: 313-318.
55. Poehling, H.M. (1979) Distribution of specific proteins in the salivary gland lobes of culicidae and their relation to age and blood sucking. J Insect Physiol 25: 3-8.
56. Ribeiro, J.M.C. (1987) Role of saliva in blood-feeding by arthropods. Annu Rev Entomol 32: 463-478.
57. Ribeiro, J.M. (1995) Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Infect Agents Dis 4: 143-152.
58. Ribeiro, J.M. and Valenzuela, J.G. (1999) Purification and cloning of the salivary peroxidase/catechol oxidase of the mosquito Anopheles albimanus. J Exp Biol 202: 809-816.
59. Ribeiro, J.M. and Valenzuela, J.G. (2003) The salivary purine nucleosidase of the mosquito, Aedes aegypti. Insect Biochem Mol Biol 33: 13-22.
60. Ribeiro, J.M., Charlab, R., Pham, V.M., Garfield, M. and Valenzuela, J.G. (2004) An insight into the salivary transcriptome and proteome of the adult female mosquito, Culex pipiens quinquefasciatus. Insect Biochem Mol Biol 34: 543-563.
61. Rodríguez, M.H. (2005) Malaria and dengue vector biology and control in Latin America. In Bridging Laboratory and Field Research for Genetic Control of Disease Vectors. Series Wageningen U.R. Frontis Series, Vol. 11 (Knols, B.G.J., Loius, C. and Bogers, R.J., eds), pp. 129-141. Springer, Dordrecht. The Netherlands.
62. Rodríguez, M.H. and Hernández-Hernández, F.C. (2004) Insect-malaria parasites interactions: the salivary gland. Insect Biochem Mol Biol 34: 615-624.
63. Rosewell, D.F. and White, E.H. (1978) The chemiluminescence of luminal and related hydrazides. Methods Enzymol LVII: 409-423.
64. Rossignol, P.A., Ribeiro, J.M.C. and Spielman, A. (1984) Increased intradermal probing time in sporozoite-infected mosquitoes. Am J Trop Med Hyg 33: 17-20.
65. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning a Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
66. Simons, F.E.R. and Peng, Z. (2001) Mosquito allergy: recombinant mosquito salivary antigens for new diagnostic tests. Int Arch Allergy Immunol 124: 403-405.
67. Smartt, C.T., Kim, A.P., Grossman, G.L. and James, A.A. (1995) The apyrase gene of the mosquito vector Aedes aegypti is expressed specifically in the adult female salivary glands. Exp Parasitol 81: 239-248.
68. Stark, K.R. and James, A.A. (1996) Salivary gland anticoagulants in culicine and anopheline mosquitoes (Diptera: Culicidae). J Med Entomol 33: 645-650.
69. Sterling, C.R., Aikawa, M. and Vanderberg, J.P. (1973) The passage of Plasmodium berghei sporozoites through the salivary glands of Anopheles stephensi: an electron microscopy study. J Parasitol 59: 593-605.
70. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
71. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Biotechnology 24: 145-149.
72. Valenzuela, J.G., Francischetti, I.M. and Ribeiro, J.M. (1999) Purification, cloning, and synthesis of a novel salivary anti-thrombin from the mosquito Anopheles albimanus. Biochemistry 38: 11209-11215.
73. Valenzuela, J.G., Charlab, R., Gonzalez, E.C., de Miranda-Santos, I.K., Marinotti, O., Francischetti, I.M. and Ribeiro, J.M. (2002a) The D7 family of salivary proteins in blood sucking diptera. Insect Mol Biol 11: 149-155.
74. Valenzuela, J.G., Pham, V.M., Garfield, M.K., Francischetti, I.M. and Ribeiro, J.M. (2002b) Toward a description of the sialome of the adult female mosquito Aedes aegypti. Insect Biochem Mol Biol 32: 1101-1122.
75. Valenzuela, J.G., Francischetti, I.M., Pham, V.M., Garfield, M.K. and Ribeiro, J.M. (2003) Exploring the salivary gland transcriptome and proteome of the Anopheles stephensi mosquito. Insect Biochem Mol Biol 33: 717-732.
76. Wal, J.M. (2001) Structure and function of milk allergens. Allergy 56(Suppl. 67): 35-38.
77. Williams, J., Rucinski, B., Holt, J. and Niewiarowski, S. (1990) Elegantin and albolabrin purified from viper venoms; homologies with the RGDS domain of fibrinogen and von Willebrand factor. Biochim Biophys Acta 1039: 81-89.
78. Wray, W., Boulikas, T., Wray, V.P. and Hancock, R. (1981) Silver staining of proteins in polyacrylamide gels. Anal Biochem 118: 197-203.
79. Wright, K.A. (1969) The anatomy of salivary glands of Anopheles stephensi Liston. Can J Zool 47: 579-587.
80. Yoshida, S. and Watanabe, H. (2006) Robust salivary gland-specific transgene expression in Anopheles stephensi mosquito. Insect Mol Biol 15: 403-410.
81. Zhou, Q., Hu, P., Ritter, R.M., Swenson, S.D., Argounova, S., Epstein, A.L. and Markland, F.S. Jr (2000) Molecular cloning and functional expression of contortrostatin, a homodimeric disintegrin from southern copperhead snake venom. Arch Biochem Biophys 375: 278-288.