A novel lectin with a fibrinogen-like domain and its potential involvement in the innate immune response of Armigeres subalbatus against bacteria

Insect Molecular Biology

Volumn 13, Issue 3, 2004, Pages 273-282

  Wang, X ^a   Rocheleau, T A ^a   Fuchs, J F ^a   Hillyer, J F ^a   Chen, C C ^b   Christensen, B M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

Armigeres subalbatus; Haemocyte; Innate immunity; Lectin; Mosquito; Pattern recognition receptor

Indexed keywords

COMPLEMENTARY DNA; LECTIN; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CLUSTER ANALYSIS; COMPARATIVE STUDY; DNA SEQUENCE; FEMALE; GENE EXPRESSION REGULATION; GENE LIBRARY; GENE STRUCTURE; GENETIC PROCEDURES; GENETICS; HEMOLYMPH; INNATE IMMUNITY; METABOLISM; MOLECULAR GENETICS; MOSQUITO; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CLUSTER ANALYSIS; CULICIDAE; DNA, COMPLEMENTARY; FEMALE; GENE COMPONENTS; GENE EXPRESSION REGULATION; GENE LIBRARY; HEMOLYMPH; IMMUNITY, NATURAL; LECTINS; MOLECULAR PROBE TECHNIQUES; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS;

ANIMALIA; ARMIGERES SUBALBATUS; ESCHERICHIA COLI; MICROCOCCUS; MICROCOCCUS LUTEUS;

EID: 2942718954     PISSN: 09621075     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0962-1075.2004.00484.x     Document Type: Article

References (44)

1. Adema, C.M., Hertel, L.A., Miller, R.D. and Loker, E.S. (1997) A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proc Natl Acad Sci USA 94: 8691-8696.
2. Beerntsen, B.T., James, A.A. and Christensen, B.M. (2000) Genetics of mosquito vector competence. Microbiol Mol Biol Rev 64: 115-137.
3. Beerntsen, B.T., Luckhart, S. and Christensen, B.M. (1989) Brugia malayi and Brugia pahangi: inherent difference in immune activation in the mosquitoes Armigeres subalbatus and Aedes aegypti. J Parasitol 75: 76-81.
4. Chen, C.C. and Chen, C.S. (1995) Brugia pahangi: effects of melanization on the uptake of nutrients by microfilariae in vitro. Exp Parasitol 81: 72-78.
5. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159.
6. Christensen, B.M. (1981) Observations on the immune response of Aedes trivittatus against Dirofilaria immitis. Trans R Soc Trop Med Hyg 75: 439-443.
7. Christensen, B.M., Sutherland, D.R. and Gleason, L.N. (1984) Defense reactions of mosquitoes to filarial worms: comparative studies on the response of three different mosquitoes to inoculated Brugia pahangi and Dirofilaria immitis microfilariae. J Invertebr Pathol 44: 267-274.
8. Christophides, G.K., Zdobnov, E., Barillas-Mury, C., Birney, E., Blandin, S., Blass, C., Brey, P.T., Collins, F.H., Danielli, A., Dimopoulos, G., Hetru, C., Hoa, N.T., Hoffmann, J.A., Kanzok, S.M., Letunic, I., Levashina, E.A., Loukeris, T.G., Lycett, G., Meister, S., Michel, K., Moita, L.F., Muller, H.M., Osta, M.A., Paskewitz, S.M., Reichhart, J.M., Rzhetsky, A., Troxler, L., Vernick, K.D., Vlachou, D., Volz, J., von Mering, C., Xu, J., Zheng, L., Bork, P. and Kafatos, F.C. (2002) Immunity-related genes and gene families in Anopheles gambiae. Science 298: 159-165.
9. Cseh, S., Vera, L., Matsushita, M., Fujita, T., Arlaud, G.J. and Thielens, N.M. (2002) Characterization of the interaction between 1-ficolin/p35 and mannan-binding lectin-associated serine proteases-1 and -2. J Immunol 169: 5735-5743.
10. Dimopoulos, G. (2003) Insect immunity and its implication in mosquito-malaria interactions. Cell Microbiol 5: 3-14.
11. Dimopoulos, G., Casavant, T.L., Chang, S., Scheetz, T., Roberts, C., Donohue, M., Schultz, J., Benes, V., Bork, P., Ansorge, W., Soares, M.B. and Kafatos, F.C. (2000) Anopheles gambiae pilot gene discovery project: identification of mosquito innate immunity genes from expressed sequence tags generated from immune-competent cell lines. Proc Natl Acad Sci USA 97: 6619-6624.
12. Dimopoulos, G., Christophides, G.K., Meister, S., Schultz, J., White, K.P., Barillas-Mury, C. and Kafatos, F.C. (2002) Genome expression analysis of Anopheles gambiae: responses to injury, bacterial challenge, and malaria infection. Proc Natl Acad Sci USA 99: 8814-8819.
13. Durbin, J.E., Swerdel, M.R. and Fallon, A.M. (1988) Identification of cDNAs corresponding to mosquito ribosomal protein genes. Biochim Biophys Acta 950: 182-192.
14. Endo, Y., Sato, Y., Matsushita, M. and Fujita, T. (1996) Cloning and characterization of the human lectin P35 gene and its related gene. Genomics 36: 515-521.
15. Fujita, T. (2002) Evolution of the lectin-complement pathway and its role in innate immunity. Nat Rev Immunol 2: 346-353.
16. Gokudan, S., Muta, T., Tsuda, R., Koori, K., Kawahara, T., Seki, N., Mizunoe, Y., Wai, S.N., Iwanaga, S. and Kawabata, S. (1999) Horseshoe crab acetyl group-recognizing lectins involved in innate immunity are structurally related to fibrinogen. Proc Natl Acad Sci USA 96: 10086-10091.
17. Grilli, M., Chiu, J.J. and Lenardo, M.J. (1993) NF-kappa B and Rel: participants in a multiform transcriptional regulatory system. Int Rev Cytol 143: 1-62.
18. Herrscher, R.F., Kaplan, M.H., Lelsz, D.L., Das, C., Scheuermann, R. and Tucker, P.W. (1995) The immunoglobulin heavy-chain matrix-associating regions are bound by Bright: a B cell-specific trans-activator that describes a new DNA-binding protein family. Genes Dev 9: 3067-3082.
19. Hillyer, J.F., Schmidt, S.L. and Christensen, B.M. (2003a) Hemocyte-mediated phagocytosis and melanization in the mosquito Armigeres subalbatus following immune challenge by bacteria. Cell Tissue Res 313: 117-127.
20. Hillyer, J.F., Schmidt, S.L. and Christensen, B.M. (2003b) Rapid phagocytosis and melanization of bacteria and Plasmodium sporozoites by hemocytes of the mosquito Aedes aegypti. J Parasitol 89: 62-69.
21. Hoffmann, J.A., Kafatos, F.C., Janeway, C.A. and Ezekowitz, R.A. (1999) Phylogenetic perspectives in innate immunity. Science 284: 1313-1318.
22. Holmskov, U., Thiel, S., Jensenius, J.C. and Wallis, R. (2003) Collections and ficolins: humoral lectins of the innate immune defense. Annu Rev Immunol 21: 547-578.
23. Ichijo, H., Hellman, U., Wernstedt, C., Gonez, L.J., Claesson-Welsh, L., Heldin, C.H. and Miyazono, K. (1993) Molecular cloning and characterization of ficolin, a multimeric protein with fibrinogen- and collagen-like domains. J Biol Chem 268: 14505-14513.
24. Inamori, K., Saito, T., Iwaki, D., Nagira, T., Iwanaga, S., Arisaka, F. and Kawabata, S. (2001) Horseshoe crab hemocyte-derived lectin recognizing specific O-antigens of lipopolysaccharides. Adv Exp Med Biol 484: 185-190.
25. Jack, D.L., Klein, N.J. and Turner, M.W. (2001) Mannose-binding lectin: targeting the microbial world for complement attack and opsonophagocytosis. Immunol Rev 180: 86-99.
26. Kenjo, A., Takahashi, M., Matsushita, M., Endo, Y., Nakata, M., Mizuochi, T. and Fujita, T. (2001) Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi. J Biol Chem 276: 19959-19965.
27. Kim, Y.S., Ryu, J.H., Han, S.J., Choi, K.H., Nam, K.B., Jang, I.H., Lemaitre, B., Brey, P.T. and Lee, W.J. (2000) Gram-negative bacteria-binding protein, a pattern recognition receptor for lipopolysaccharide and beta-1,3-glucan that mediates the signaling for the induction of innate immune genes in Drosophila melanogaster cells. J Biol Chem 275: 32721-32727.
28. Kuraya, M., Matsushita, M., Endo, Y., Thiel, S. and Fujita, T. (2003) Expression of H-ficolin/Hakata antigen, mannose-binding lectin-associated serine protease (MASP)-1 and MASP-3 by human glioma cell line T98G. Int Immunol 15: 109-117.
29. Le, Y., Lee, S.H., Kon, O.L. and Lu, J. (1998) Human 1-ficolin: plasma levels, sugar specificity, and assignment of its lectin activity to the fibrinogen-like (FBG) domain. FEBS Lett 425: 367-370.
30. Lecourtois, M. and Schweisguth, F. (1995) The activity of Drosophila Hairless is required in pupae but not in embryos to inhibit Notch signal transduction. Genes Dev 9: 2598-2608.
31. Leonard, P.M., Adema, C.M., Zhang, S.M. and Loker, E.S. (2001) Structure of two FREP genes that combine IgSF and fibrinogen domains, with comments on diversity of the FREP gene family in the snail Biomphalaria glabrata. Gene 269: 155-165.
32. Levashina, E.A., Moita, L.F., Blandin, S., Vriend, G., Lagueux, M. and Kafatos, F.C. (2001) Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104: 709-718.
33. Lowenberger, C.A., Ferdig, M.T., Bulet, P., Khalili, S., Hoffmann, J.A. and Christensen, B.M. (1996) Aedes aegypti: induced antibacterial proteins reduce the establishment and development of Brugia malayi. Exp Parasitol 83: 191-201.
34. Lowenberger, C.A., Smartt, C.T., Bulet, P., Ferdig, M.T., Severson, D.W., Hoffmann, J.A. and Christensen, B.M. (1999) Insect immunity: molecular cloning, expression, and characterization of cDNAs and genomic DNA encoding three isoforms of insect defensin in Aedes aegypti. Insect Mol Biol 8: 107-118.
35. Matsushita, M., Endo, Y., Taira, S., Sato, Y., Fujita, T., Ichikawa, N., Nakata, M. and Mizuochi, T. (1996) A novel human serum lectin with collagen- and fibrinogen-like domains that functions as an opsonin. J Biol Chem 271: 2448-2454.
36. Matsushita, M., Kuraya, M., Hamasaki, N., Tsujimura, M., Shiraki, H. and Fujita, T. (2002) Activation of the lectin complement pathway by H-ficolin (Hakata antigen). J Immunol 168: 3502-3506.
37. Medzhitov, R. and Janeway, C.A. Jr (2002) Decoding the patterns of self and nonself by the innate immune system. Science 296: 298-300.
38. Polson, A., von Wechmar, M.B. and Fazakerley, G. (1980) Isolation of viral IgY antibodies from yolks of immunized hens. Immunol Commun 9: 495-514.
39. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
40. Severson, D.W., Mori, A., Zhang, Y. and Christensen, B.M. (1993) Comparative linkage maps for the mosquitoes, Aedes albopictus and Ae. aegypti, based on common RFLP loci. J Hered 84: 241-247.
41. Shaw, J.P., Utz, P.J., Durand, D.B., Toole, J.J., Emmel, E.A. and Crabtree, G.R. (1998) Identification of a putative regulator of early T cell activation genes. Science 241: 202-205.
42. Sugimoto, R., Yae, Y., Akaiwa, M., Kitajima, S., Shibata, Y., Sato, H., Hirata, J., Okochi, K., Izuhara, K. and Hamasaki, N. (1998) Cloning and characterization of the Hakata antigen, a member of the ficolin/opsonin p35 lectin family. J Biol Chem 273: 20721-20727.
43. Teh, C., Le, Y., Lee, S.H. and Lu, J. (2000) M-ficolin is expressed on monocytes and is a lectin binding to N-acetyl-D-glucosamine and mediates monocyte adhesion and phagocytosis of Escherichia coli. Immunology 101: 225-232.
44. Zdobnov, E.M., von Mering, C., Letunic, I., Torrents, D., Suyama, M., Copley, R.R., Christophides, G.K., Thomasova, D., Holt, R.A., Subramanian, G.M., Mueller, H.M., Dimopoulos, G., Law, J.H., Wells, M.A., Birney, E., Charlab, R., Halpern, A.L., Kokoza, E., Kraft, C.L., Lai, Z., Lewis, S., Louis, C., Barillas-Mury, C., Nusskern, D., Rubin, G.M., Salzberg, S.L., Sutton, G.G., Topalis, P., Wides, R., Wincker, P., Yandell, M., Collins, F.H., Ribeiro, J., Gelbart, W.M., Kafatos, F.C. and Bork, P. (2002) Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster. Science 298: 149-159.