A mosquito-specific protein family includes candidate receptors for malaria sporozoite invasion of salivary glands

Cellular Microbiology

Volumn 8, Issue 1, 2006, Pages 163-175

  Korochkina, Svetlana ^a,d   Barreau, Catherine ^a   Pradel, Gabriele ^a,e   Jeffery, Erin ^b   Li, Jun ^a   Natarajan, Ramya ^c   Shabanowitz, Jeffrey ^b   Hunt, Donald ^b   Frevert, Ute ^c   Vernick, Kenneth D ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; HEPARIN BINDING PROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; PROTEIN ANTIBODY; TYROSINE SULFATE;

AEDES AEGYPTI; ANIMAL CELL; ANOPHELES GAMBIAE; ARTICLE; BASEMENT MEMBRANE; BIOINFORMATICS; CELL INVASION; CONTROLLED STUDY; DROSOPHILA; EUKARYOTE; FEMALE; GENE TRANSFER; GENETIC COMPLEMENTATION; GENETIC IDENTIFICATION; GENUS; IN VIVO STUDY; LIVER CELL; MALARIA; MOSQUITO; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PREDICTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SALIVARY GLAND; SEQUENCE HOMOLOGY; SPOROZOITE; VERTEBRATE;

AEDES; AMINO ACID SEQUENCE; ANIMALS; ANOPHELES GAMBIAE; ANTIBODIES, MONOCLONAL; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; PLASMODIUM GALLINACEUM; RECEPTORS, CELL SURFACE; SALIVARY GLANDS; SALIVARY PROTEINS; SPOROZOITES;

AEDES AEGYPTI; ANIMALIA; ANOPHELES (GENUS); ANOPHELES GAMBIAE; EUKARYOTA; VERTEBRATA;

EID: 33644818992     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2005.00611.x     Document Type: Article

References (67)

1. Ancsin, J. B., Kisilevsky, R. (2004) A binding site for highly sulfated heparan sulfate is identified in the N terminus of the circumsporozoite protein: Significance for malarial sporozoite attachment to hepatocytes. J Biol Chem 279: 21824-21832
2. Andrei, C., Dazzi, C., Lotti, L., Torrisi, M. R., Chimini, G., Rubartelli, A. (1999) The secretory route of the leaderless protein interleukin 1beta involves exocytosis of endolysosome-related vesicles. Mol Biol Cell 10 1463-1475
3. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., Struhl, K. (eds) (2003) Current Protocols in Molecular Biology. New York: John Wiley & Sons.
4. Barreau, C., Touray, M., Pimenta, P. F., Miller, L. H., Vernick, K. D. (1995) Plasmodium gallinaceum: Sporozoite invasion of Aedes aegypti salivary glands is inhibited by anti-gland antibodies and by lectins. Exp Parasitol 81: 332-343
5. Barreau, C., Conrad, J., Fischer, E., Lujan, H. D., Vernick, K. D. (1999) Identification of surface molecules on salivary glands of the mosquito, Aedes aegypti, by a panel of monoclonal antibodies. Insect Biochem Mol Biol 29:515-526
6. Bendtsen, J. D., Nielsen, H., von Heijne, G., Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795
7. Birney, E., Clamp, M., Durbin, R. (2004) GeneWise and Genomewise. Genome Res 14: 988-995
8. Brennan, J. D. G., Kent, M., Dhar, R., Fujioka, H., Kumar, N. (2000) Anopheles gambiae salivary gland proteins as putative targets for blocking transmission of malaria parasites. Proc Natl Acad Sci USA 97: 13859-13864
9. Cerami, C., Frevert, U., Sinnis, P., Takacs, B., Clavijo, P., Santos, M. J., Nussenzweig, V. (1992) The basolateral domain of the hepatocyte plasma membrane bears receptors for the circumsporozoite protein of Plasmodium falciparum sporozoites. Cell 70: 1021-1033
10. Choe, H., Moore, M. J., Owens, C. M., Wright, P. L., Vasilieva, N., Li, W., et al. (2005) Sulphated tyrosines mediate association of chemokines and Plasmodium vivax Duffy binding protein with the Duffy antigen/ receptor for chemokines (DARC). Mol Microbiol 55: 1413-1422
11. Cleves, A. E., Cooper, D. N., Barondes, S. H., Kelly, R. B. (1996) A new pathway for protein export in Saccharomyces cerevisiae. J Cell Biol 133: 1017-1026
12. Farzan, M., Mirzabekov, T., Kolchinsky, P., Wyatt, R., Cayabyab, M., Gerard, N. P., et al. (1999) Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 96: 667-676
13. Frevert, U., Sinnis, P., Cerami, C., Shreffler, W., Takacs, B., Nussenzweig, V. (1993) Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med 177: 1287-1298
14. Fuhrmann, M., Hausherr, A., Ferbitz, L., Schodl, T., Heitzer, M., Hegemann, P. (2004) Monitoring dynamic expression of nuclear genes in Chlamydomonas reinhardtii by using a synthetic luciferase reporter gene. Plant Mol Biol 55: 869-881
15. Gardella, S., Andrei, C., Ferrera, D., Lotti, L. V., Torrisi, M. R., Bianchi, M. E., Rubartelli, A. (2002) The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep 3: 995-1001
16. Glantz, S. A. (2002) Primer of Biostatistics. New York: McGraw-Hill.
17. Grossman, G. L., James, A. A. (1993) The salivary glands of the vector mosquito, Aedes aegypti, express a novel member of the amylase gene family. Insect Mol Biol 1: 223-232
18. Harlow, E., Lane, D. (1999) Using Antibodies: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratories.
19. Hileman, R. E., Fromm, J. R., Weiler, J. M., Linhardt, R. J. (1998) Glycosaminoglycan-protein interactions: Definition of consensus sites in glycosaminoglycan binding proteins. Bioessays 20: 156-167
20. Hugel, F. U., Pradel, G., Frevert, U. (1996) Release of malaria circumsporozoite protein into the host cell cytoplasm and interaction with ribosomes. Mol Biochem Parasitol 81: 151-170
21. Ito, J., Ghosh, A., Moreira, L. A., Wimmer, E. A., Jacobs-Lorena, M. (2002) Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 417: 452-455
22. James, A. A. (1994) Molecular and biochemical analyses of the salivary glands of vector mosquitoes. Bull Inst Pasteur 92: 133-150
23. James, A. A., Rossignol, P. A. (1991) Mosquito salivary glands: parasitological and molecular aspects. Parasitol Today 7: 267-271
24. James, A. A., Blackmer, K., Racioppi, J. V. (1989) A salivary gland-specific, maltase-like gene of the vector mosquito, Aedes aegypti. Gene 75: 73-83
25. Kariu, T., Yuda, M., Yano, K., Chinzei, Y. (2002) MAEBL is essential for malarial sporozoite infection of the mosquito salivary gland. J Exp Med 195: 1317-1323
26. Kondo, N., Nikoh, N., Ijichi, N., Shimada, M., Fukatsu, T. (2002) Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proc Natl Acad Sci USA 99: 14280-14285.
27. Krogh, A., Larsson, B., von Heijne, G., Sonnhammer, E. L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580
28. Lanfrancotti, A., Lombardo, F., Santolamazza, F., Veneri, M., Castrignano, T., Coluzzi, M., Arca, B. (2002) Novel cDNAs encoding salivary proteins from the malaria vector Anopheles gambiae. Febs Lett 517: 67-71
29. MacCoss, M. J., Wu, C. C., Yates, J. R., 3rd. (2002) Probability-based validation of protein identifications using a modified SEQUEST algorithm. Anal Chem 74: 5593-5599
30. Marinotti, O., James, A. A. (1990) An a-glucosidase in the salivary glands of the vector mosquito, Aedes aegypti. Insect Biochem 20 619-623
31. Medeiros, G. F., Mendes, A., Castro, R. A., Bau, E. C., Nader, H. B., Dietrich, C. P. (2000) Distribution of sulfated glycosaminoglycans in the animal kingdom: Widespread occurrence of heparin-like compounds in invertebrates. Biochim Biophys Acta 1475: 287-294
32. Minet, A. D., Chiquet-Ehrismann, R. (2000) Phylogenetic analysis of teneurin genes and comparison to the rearrangement hot spot elements of E. coli. Gene 257: 87-97
33. Minet, A. D., Rubin, B. P., Tucker, R. P., Baumgartner, S., Chiquet-Ehrismann, R. (1999) Teneurin-1, a vertebrate homologue of the Drosophila pair-rule gene ten-m, is a neuronal protein with a novel type of heparin-binding domain. J Cell Sci 112:
34. Moore, K. L. (2003) The biology and enzymology of protein tyrosine O-sulfation. J Biol Chem 278: 24243-24246
35. Morris, A. C., Pott, G. B., Chen, J., James, A. A. (1995) Transient expression of a promoter-reporter construct in differentiated adult salivary glands and embryos of the mosquito Aedes aegypti. Am J Trop Med Hyg 52: 456-460
36. Myung, J. M., Marshall, P., Sinnis, P. (2004) The Plasmodium circumsporozoite protein is involved in mosquito salivary gland invasion by sporozoites. Mol Biochem Parasitol 133: 53-59
37. Nadershahi, A., Fahrenkrug, S., Ellis, L. (2004) Comparison of computational methods for identifying translation initiation sites in EST data. BMC Bioinformatics 5: 14.
38. Nakai, K., Horton, P. (1999) PSORT: A program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24: 34-36
39. Nicholas, H. B., Jr, Chan, S. S., Rosenquist, G. L. (1999) Reevaluation of the determinants of tyrosine sulfation. Endocrine 11: 285-292.
40. Niehrs, C., Kraft, M., Lee, R. W., Huttner, W. B. (1990) Analysis of the substrate specificity of tyrosylprotein sulfotransferase using synthetic peptides. J Biol Chem 265: 8525-8532
41. Pancake, S. J., Holt, G. D., Mellouk, S., Hoffman, S. L. (1992) Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates. J Cell Biol 117: 1351-1357
42. Pearson, W. R., Lipman, D. J. (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85: 2444-2448
43. Peng, Z. K., Yang, J., Wang, H. S., Simons, F. E. R. (1999) Production and characterization of monoclonal antibodies to two new mosquito Aedes aegypti salivary proteins. Insect Biochem Mol Biol 29: 909-914
44. Pimenta, P. F., Touray, M., Miller, L. (1994) The journey of malaria sporozoites in the mosquito salivary gland. J Eukaryot Microbiol 41: 608-624
45. Pinzon-Ortiz, C., Friedman, J., Esko, J., Sinnis, P. (2001) The binding of the circumsporozoite protein to cell surface heparan sulfate proteoglycans is required for plasmodium sporozoite attachment to target cells. J Biol Chem 276 26784-26791
46. Pradel, G., Garapaty, S., Frevert, U. (2002) Proteoglycans mediate malaria sporozoite targeting to the liver. Mol Microbiol 45: 637-651
47. Rathore, D., McCutchan, T. F. (2000) Role of cysteines in Plasmodium falciparum circumsporozoite protein: Interactions with heparin can rejuvenate inactive protein mutants. Proc Natl Acad Sci USA 97: 8530-8535
48. Rathore, D., McCutchan, T. F., Garboczi, D. N., Toida, T., Hernaiz, M. J., LeBrun, L. A., et al. (2001) Direct measurement of the interactions of glycosaminoglycans and a heparin decasaccharide with the malaria circumsporozoite protein. Biochemistry 40: 11518-11524
49. Retief, J. D., Lynch, K. R., Pearson, W. R. (1999) Panning for genes - a visual strategy for identifying novel gene orthologs and paralogs. Genome Res 9: 373-382
50. Ribeiro, J. M., Sarkis, J. J., Rossignol, P. A., Spielman, A. (1984) Salivary apyrase of Aedes aegypti: Characterization and secretory fate. Comp Biochem Physiol B 79: 81-86
51. Ribeiro, J. M., Topalis, P., Louis, C. (2004) AnoXcel: An Anopheles gambiae protein database. Insect Mol Biol 13: 449-457.
52. Robson, K. J., Frevert, U., Reckmann, I., Cowan, G., Beier, J., Scragg, I. G., et al. (1995) Thrombospondin-related adhesive protein (TRAP) of Plasmodium falciparum: Expression during sporozoite ontogeny and binding to human hepatocytes. EMBO J 14: 3883-3894
53. Rosenberg, R. (1985) Inability of Plasmodium knowlesi sporozoites to invade Anopheles freeborni salivary glands. Am J Trop Med Hyg 34: 687-691
54. Rosenberg, R., Rungsiwongse, J. (1991) The number of sporozoites produced by individual malaria oocysts. Am J Trop Med Hyg 45: 574-577
55. Rosenquist, G. L., Nicholas, H. B., Jr. (1993) Analysis of sequence requirements for protein tyrosine sulfation. Protein Sci 2: 215-222
56. Salamov, A., Nishikawa, T., Swindells, M. (1998) Assessing protein coding region integrity in cDNA sequencing projects. Bioinformatics 14: 384-390
57. Salzberg, S., Hotopp, J., Delcher, A., Pop, M., Smith, D., Eisen, M., Nelson, W. (2005) Serendipitous discovery of Wolbachia genomes in multiple Drosophila species. Genome Biol 6: R23.
58. Sambrook, J., Russell, D. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Press.
59. Sidjanski, S. P., Vanderberg, J. P., Sinnis, P. (1997) Anopheles stephensi salivary glands bear receptors for region I of the circumsporozoite protein of Plasmodium falciparum. Mol Biochem Parasitol 90: 33-41
60. Staatz, W. D., Toyoda, H., Kinoshita-Toyoda, A., Chhor, K., Selleck, S. B. (2001) Analysis of proteoglycans and glycosaminoglycans from Drosophila. Methods Mol Biol 171: 41-52
61. Sterling, C. R., Aikawa, M., Vanderberg, J. P. (1973) The passage of Plasmodium berghei sporozoites through the salivary glands of Anopheles stephensi: An electron microscope study. J Parasitol 59: 593-605
62. Touray, M. G., Warburg, A., Laughinghouse, A., Krettli, A. U., Miller, L. H. (1992) Developmentally regulated infectivity of malaria sporozoites for mosquito salivary glands and the vertebrate host. J Exp Med 175: 1607-1612
63. Toyoda, H., Kinoshita-Toyoda, A., Selleck, S. B. (2000) Structural analysis of glycosaminoglycans in Drosophila and Caenorhabditis elegans and demonstration that tout-velu, a Drosophila gene related to EXT tumor suppressors, affects heparan sulfate in vivo. J Biol Chem 275: 2269-2275
64. Valenzuela, J. G., Charlab, R., de Gonzalez, E. C., de Miranda-Santos, I. K., Marinotti, O., Francischetti, I. M. B., Ribeiro, J. M. C. (2002) The D7 family of salivary proteins in blood sucking diptera. Insect Mol Biol 11: 149-155
65. Wang, Y. D., Zhao, S., Hill, C. W. (1998) Rhs elements comprise three subfamilies which diverged prior to acquisition by Escherichia coli. J Bacteriol 180: 4102-4110
66. Wu, M., Sun, L. V., Vamathevan, J., Riegler, M., Deboy, R., Brownlie, J. C., et al. (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: A streamlined genome overrun by mobile genetic elements. PLoS Biol 2: E69.
67. Ying, P., Shakibaei, M., Patankar, M. S., Clavijo, P., Beavis, R. C., Clark, G. F., Frevert, U. (1997) The malaria circumsporozoite protein: interaction of the conserved regions I and II-plus with heparin-like oligosaccharides in heparan sulfate. Exp Parasitol 85: 168-182.