Mosquito immune responses and malaria transmission: Lessons from insect model systems and implications for vertebrate innate immunity and vaccine development

Insect Biochemistry and Molecular Biology

Volumn 30, Issue 6, 2000, Pages 429-442

  Barillas Mury, Carolina ^a   Wizel, Benjamin ^b   Soo Han, Yeon ^a  

^a Immunology and Pathology   (United States)

^b UNIVERSITY OF TEXAS HEALTH CENTER   (United States)

Author keywords

Innate immunity; Insect; Malaria; Mosquito; Vaccine

Indexed keywords

MALARIA VACCINE; MONOPHENOL MONOOXYGENASE; TRANSCRIPTION FACTOR;

ADIPOCYTE; ANIMAL; ANTIBACTERIAL ACTIVITY; BIOLOGICAL MODEL; DISEASE CARRIER; DISEASE TRANSMISSION; EPITHELIUM CELL; GENE EXPRESSION REGULATION; HUMAN; IMMUNE RESPONSE; IMMUNOLOGY; INFECTION RESISTANCE; MALARIA; MOLECULAR RECOGNITION; MOSQUITO; NONHUMAN; PARASITOLOGY; SHORT SURVEY; SIGNAL TRANSDUCTION; SPOROZOITE; VERTEBRATE;

ANIMALS; CULICIDAE; HUMANS; INSECT VECTORS; MALARIA; MALARIA VACCINES; MODELS, BIOLOGICAL; VERTEBRATES;

EID: 0034040939     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0965-1748(00)00018-7     Document Type: Short Survey

References (124)

1. Aliprantis A.O., Yang R.B., Mark M.R., Suggett S., Devaux B., Radolf J.D., Klimpel G.R., Godowski P., Zychlinsky A. Cell activation and apoptosis by bacterial lipoproteins through toll-like receptor-2. Science. 285(5428):1999;736-739.
2. Barillas-Mury C., Charlesworth A., Gross I., Richman A., Hoffmann J.A., Kafatos F.C. Immune factor Gambif1, a new rel family member from the human malaria vector, Anopheles gambiae. Embo J. 15(17):1996;4691-4701.
3. Barillas-Mury C., Han Y.S., Seeley D., Kafatos F.C. Anopheles gambiae Ag-STAT, a new insect member of the STAT family, is activated in response to bacterial infection. Embo J. 18(4):1999;959-967.
4. Binari R., Perrimon N. Stripe-specific regulation of pair-rule genes by hopscotch, a putative Jak family tyrosine kinase in Drosophila. Genes Dev. 8(3):1994;300-312.
5. Böhnlein E., Lowenthal J.W., Siekevitz M., Ballard D.W., Franza B.R., Greene W.C. The same inducible nuclear proteins regulates mitogen activation of both the interleukin-2 receptor-alpha gene and type 1 HIV. Cell. 53(5):1988;827-836.
6. Brightbill H.D., Libraty D.H., Krutzik S.R., Yang R.B., Belisle J.T., Bleharski J.R., Maitland M., Norgard M.V., Plevy S.E., Smale S.T., Brennan P.J., Bloom B.R., Godowski P.J., Modlin R.L. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science. 285(5428):1999;732-736.
7. Chalk R., Townson H., Natori S., Desmond H., Ham P.J. Purification of an insect defensin from the mosquito, Aedes aegypti. Insect Biochem. Mol. Biol. 24(4):1994;403-410.
8. Chiou J.Y., Huang S.J., Huang S.T., Cho W.L. Identification of immune-related protein kinases from mosquitoes (Aedes aegypti). J. Biomed. Sci. 5(2):1998;120-126.
9. Cho W.L., Fu T.F., Chiou J.Y., Chen C.C. Molecular characterization of a defensin gene from the mosquito, Aedes aegypti. Insect Biochem. Mol. Biol. 27(5):1997;351-358.
10. Cho W.L., Fu Y.C., Chen C.C., Ho C.M. Cloning and characterization of cDNAs encoding the antibacterial peptide, defensin A, from the mosquito, Aedes aegypti. Insect Biochem. Mol. Biol. 26(4):1996;395-402.
11. Chow J.C., Young D.W., Golenbock D.T., Christ W.J., Gusovsky F. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem. 274(16):1999;10689-10692.
12. Coates C.J., Jasinskiene N., Miyashiro L., James A.A. Mariner transposition and transformation of the yellow fever mosquito, Aedes aegypti. Proc. Natl. Acad. Sci. USA. 95(7):1998;3748-3751.
13. Cociancich S.O., Park S.S., Fidock D.A., Shahabuddin M. Vesicular ATPase-overexpressing cells determine the distribution of malaria parasite oocysts on the midguts of mosquitoes. J. Biol. Chem. 274(18):1999;12650-12655.
14. Collins F.H., Sakai R.K., Vernick K.D., Paskewitz S., Seeley D.C., Miller L.H., Collins W.E., Campbell C.C., Gwadz R.W. Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science. 234(4776):1986;607-610.
15. Collins F.H., Zheng L., Paskewitz S.M., Kafatos F.C. Progress in the map-based cloning of the Anopheles gambiae genes responsible for the encapsulation of malarial parasites. Ann. Trop. Med. Parasitol. 91(5):1997;517-521.
16. Cramer P., Varrot A., Barillas-Mury C., Kafatos F.C., Muller C.W. Structure of the specificity domain of the Dorsal homologue Gambif1 bound to DNA. Structure Fold. Des. 7(7):1999;841-852.
17. Darnell J.E. Jr. STATs and gene regulation. Science. 277(5332):1997;1630-1635.
18. Diefenbach A., Schindler H., Rollinghoff M., Yokoyama W.M., Bogdan C. Requirement for type 2 NO synthase for IL-12 signaling in innate immunity. Science. 284(5416):1999;951-955.
19. Dimopoulos G., Richman A., Muller H.M., Kafatos F.C. Molecular immune responses of the mosquito Anopheles gambiae to bacteria and malaria parasites. Proc. Natl. Acad. Sci. USA. 94(21):1997;11508-11513.
20. Dimopoulos G., Seeley D., Wolf A., Kafatos F.C. Malaria infection of the mosquito Anopheles gambiae activates immune-responsive genes during critical transition stages of the parasite life cycle. Embo J. 17(21):1998;6115-6123.
21. Doolan D.L., Hoffman S.L. IL-12 and NK cells are required for antigen-specific adaptive immunity against malaria initiated by CD8+ T cells in the Plasmodium yoelii model. J. Immunol. 163(2):1999;884-892.
22. Engström Y., Kadalayil L., Sun S.C., Samakovlis C., Hultmark D., Faye I. kappa B-like motifs regulate the induction of immune genes in Drosophila. J. Mol. Biol. 232(2):1993;327-333.
23. Fearon D.T., Locksley R.M. The instructive role of innate immunity in the acquired immune response. Science. 272(5258):1996;50-53.
24. Frevert U., Galinski M.R., Hugel F.U., Allon N., Schreier H., Smulevitch S., Shakibaei M., Clavijo P. Malaria circumsporozoite protein inhibits protein synthesis in mammalian cells. Embo J. 17(14):1998;3816-3826.
25. Fujimoto K., Okino N., Kawabata S., Iwanaga S., Ohnishi E. Nucleotide sequence of the cDNA encoding the proenzyme of phenol oxidase A1 of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA. 92(17):1995;7769-7773.
26. Ganz T., Lehrer R.I. Antimicrobial peptides of vertebrates. Curr. Opin. Immunol. 10(1):1998;41-44.
27. Gorman M.J., Andreeva O.V., Paskewitz S.M. Molecular characterization of five serine protease genes cloned from Anopheles gambiae hemolymph. Insect Biochem. Mol. Biol. 30:2000;35-46.
28. Gorman M.J., Paskewitz S.M. A genetic study of a melanization response to Sephadex beads in Plasmodium-refractory and -susceptible strains of Anopheles gambiae. Am. J. Trop. Med. Hyg. 56(4):1997;446-451.
29. Gorman M.J., Severson D.W., Cornel A.J., Collins F.H., Paskewitz S.M. Mapping a quantitative trait locus involved in melanotic encapsulation of foreign bodies in the malaria vector, Anopheles gambiae. Genetics. 146(3):1997;965-971.
30. Hall M., Scott T., Sugumaran M., Söderhäll K., Law J.H. Proenzyme of Manduca sexta phenol oxidase: purification, activation, substrate specificity of the active enzyme, and molecular cloning. Proc. Natl. Acad. Sci. USA. 92(17):1995;7764-7768.
31. Hanratty W.P., Dearolf C.R. The Drosophila Tumorous-lethal hematopoietic oncogene is a dominant mutation in the hopscotch locus. Mol. Gen. Genet. 238(1-2):1993;33-37.
32. Harrison D.A., Binari R., Nahreini T.S., Gilman M., Perrimon N. Activation of a Drosophila Janus kinase (JAK) causes hematopoietic neoplasia and developmental defects. Embo J. 14(12):1995;2857-2865.
33. Hedengren M., Asling B., Dushay M.S., Ando I., Ekengren S., Wihlborg M., Hultmark D. Relish, a central factor in the control of humoral but not cellular immunity in Drosophila. Mol. Cell. 4(5):1999;827-837.
34. Hoffman S.L., Franke E.D., Hollingdale M.R., Druilhe P. Attacking the infected hepatocyte. Hoffman S.L. Malaria Vaccine Development. 1996;35 ASM Press, Washington, DC. (Chapter 3).
35. Hoffmann J.A., Kafatos F.C., Janeway C.A., Ezekowitz R.A. Phylogenetic perspectives in innate immunity. Science. 284(5418):1999;1313-1318.
36. Hoffmann J.A., Reichhart J.-M. Drosophila immunity. Trends in Cell Biology. 7(8):1997;309-316.
37. Hoshino K., Takeuchi O., Kawai T., Sanjo H., Ogawa T., Takeda Y., Takeda K., Akira S. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 162(7):1999;3749-3752.
38. Hou X.S., Melnick M.B., Perrimon N. Marelle acts downstream of the Drosophila HOP/JAK kinase and encodes a protein similar to the mammalian STATs. Cell. 84(3):1996;411-419.
39. Hoyos B., Ballard D.W., Bohnlein E., Siekevitz M., Greene W.C. Kappa B-specific DNA binding proteins: role in the regulation of human interleukin-2 gene expression. Science. 244(4903):1989;457-460.
40. Ihle J.N. STATs: Signal Transducers and Activators of Transcription. Cell. 84:1996;331-334.
41. Ip Y.T., Reach M., Engstrom Y., Kadalayil L., Cai H., Gonzalez-Crespo S., Tatei K., Levine M. Dif, a dorsal-related gene that mediates an immune response in Drosophila. Cell. 75(4):1993;753-763.
42. Janeway C.A. Jr. Presidential Address to The American Association of Immunologists. The road less traveled by: the role of innate immunity in the adaptive immune response. J. Immunol. 161(2):1998;539-544.
43. Jasinskiene N., Coates C.J., Benedict M.Q., Cornel A.J., Rafferty C.S., James A.A., Collins F.H. Stable transformation of the yellow fever mosquito, Aedes aegypti, with the Hermes element from the housefly. Proc. Natl. Acad. Sci. USA. 95(7):1998;3743-3747.
44. Jiang H., Wang Y., Kanost M.R. Pro-phenol oxidase activating proteinase from an insect, Manduca sexta: a bacteria-inducible protein similar to Drosophila easter. Proc. Natl. Acad. Sci. USA. 95(21):1998;12220-12225.
45. Jiang H., Wang Y., Korochkina S.E., Benes H., Kanost M.R. Molecular cloning of cDNAs for two pro-phenol oxidase subunits from the malaria vector, Anopheles gambiae. Insect Biochem. Mol. Biol. 27(7):1997;693-699.
46. Jiang H., Wang Y., Ma C., Kanost M.R. Subunit composition of pro-phenol oxidase from Manduca sexta: molecular cloning of subunit ProPO-P1. Insect Biochem. Mol. Biol. 27(10):1997;835-850.
47. Kang D., Romans P., Lee J.Y. Analysis of a lysozyme gene from the malaria vector mosquito, Anopheles gambiae. Gene. 174(2):1996;239-244.
48. Kanost M.R. Serine proteinase inhibitors in arthropod immunity. Dev. Comp. Immunol. 23(4-5):1999;291-301.
49. Kaplan M.H., Sun Y.L., Hoey T., Grusby M.J. Impaired IL-12 responses and enhanced development of Th2 cells in Stat4- deficient mice. Nature. 382(6587):1996;174-177.
50. Kappler C., Meister M., Lagueux M., Gateff E., Hoffmann J.A., Reichhart J.M. Insect immunity. Two 17 bp repeats nesting a kappa B-related sequence confer inducibility to the diptericin gene and bind a polypeptide in bacteria-challenged Drosophila. Embo J. 12(4):1993;1561-1568.
51. Kawabata T., Yasuhara Y., Ochiai M., Matsuura S., Ashida M. Molecular cloning of insect pro-phenol oxidase: a copper-containing protein homologous to arthropod hemocyanin. Proc. Natl. Acad. Sci. USA. 92(17):1995;7774-7778.
52. Kirschning C.J., Wesche H., Merrill Ayres T., Rothe M. Human toll-like receptor 2 confers responsiveness to bacterial lipopolysaccharide. J. Exp. Med. 188(11):1998;2091-2097.
53. Klotz F.W., Scheller L.F., Seguin M.C., Kumar N., Marletta M.A., Green S.J., Azad A.F. Co-localization of inducible-nitric oxide synthase and Plasmodium berghei in hepatocytes from rats immunized with irradiated sporozoites. J. Immunol. 154(7):1995;3391-3395.
54. Leaman D.W., Leung S., Li X., Stark G.R. Regulation of STAT-dependent pathways by growth factors and cytokines. Faseb J. 10(14):1996;1578-1588.
55. Lee S.Y., Cho M.Y., Hyun J.H., Lee K.M., Homma K.I., Natori S., Kawabata S.I., Iwanaga S., Lee B.L. Molecular cloning of cDNA for pro-phenol-oxidase-activating factor I, a serine protease is induced by lipopolysaccharide or 1,3-beta-glucan in coleopteran insect, Holotrichia diomphalia larvae. Eur. J. Biochem. 257(3):1998;615-621.
56. Lee W.J., Ahmed A., della Torre A., Kobayashi A., Ashida M., Brey P.T. Molecular cloning and chromosomal localization of a prophenoloxidase cDNA from the malaria vector Anopheles gambiae. Insect. Mol. Biol. 7(1):1998;41-50.
57. Lee W.J., Lee J.D., Kravchenko V.V., Ulevitch R.J., Brey P.T. Purification and molecular cloning of an inducible gram-negative bacteria-binding protein from the silkworm, Bombyx mori. Proc. Natl. Acad. Sci. USA. 93(15):1996;7888-7893.
58. Lehrer R.I., Ganz T. Antimicrobial peptides in mammalian and insect host defence. Curr. Opin. Immunol. 11(1):1999;23-27.
59. Lemaitre B., Kromer-Metzger E., Michaut L., Nicolas E., Meister M., Georgel P., Reichhart J.M., Hoffmann J.A. A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc. Natl. Acad. Sci. USA. 92(21):1995;9465-9469.
60. Lemaitre B., Meister M., Govind S., Georgel P., Steward R., Reichhart J.M., Hoffmann J.A. Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila. Embo J. 14(3):1995;536-545.
61. Lemaitre B., Nicolas E., Michaut L., Reichhart J.M., Hoffmann J.A. The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell. 86(6):1996;973-983.
62. Lenardo M.J., Baltimore D. NF-kappa B: a pleiotropic mediator of inducible and tissue-specific gene control. Cell. 58(2):1989;227-229.
63. Levashina E.A., Ohresser S., Lemaitre B., Imler J.L. Two distinct pathways can control expression of the gene encoding the Drosophila antimicrobial peptide metchnikowin. J. Mol. Biol. 278(3):1998;515-527.
64. Levashina E.A., Langley E., Green C., Gubb D., Ashburner M., Hoffmann J.A., Reichhart J.M. Constitutive activation of toll-mediated antifungal defense in serpin-deficient drosophila. Science. 285(5435):1999;1917-1919.
65. Lowenberger C., Charlet M., Vizioli J., Kamal S., Richman A., Christensen B.M., Bulet P. Antimicrobial activity spectrum, cDNA cloning, and mRNA expression of a newly isolated member of the cecropin family from the mosquito vector Aedes aegypti. J. Biol. Chem. 274(29):1999;20092-20097.
66. Lowenberger C.A., Kamal S., Chiles J., Paskewitz S., Bulet P., Hoffmann J.A., Christensen B.M. Mosquito-Plasmodium interactions in response to immune activation of the vector. Exp. Parasitol. 91(1):1999;59-69.
67. Lowenberger C.A., Smartt C.T., Bulet P., Ferdig M.T., Severson D.W., Hoffmann J.A., Christensen B.M. 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(1):1999;107-118.
68. Lowenberger C., Bulet P., Charlet M., Hetru C., Hodgeman B., Christensen B.M., Hoffmann J.A. Insect immunity: isolation of three novel inducible antibacterial defensins from the vector mosquito, Aedes aegypti. Insect Biochem. Mol. Biol. 25(7):1995;867-873.
69. Luckhart S., Rosenberg R. Gene structure and polymorphism of an invertebrate nitric oxide synthase gene. Gene. 232(1):1999;25-34.
70. Luckhart S., Vodovotz Y., Cui L., Rosenberg R. The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc. Natl. Acad. Sci., USA. 95(10):1998;5700-5705.
71. Ma, C., Kanost, M.R., 2000. A beta,1-3-glucan-recognition protein from an insect, Manduca sexta, agglutinates microorganisms and activates the phenoloxidase cascade. J. Biol. Chem., In press.
72. Manfruelli P., Reichhart J.M., Steward R., Hoffmann J.A., Lemaitre B. A mosaic analysis in Drosophila fat body cells of the control of antimicrobial peptide genes by the Rel proteins Dorsal and DIF. Embo J. 18(12):1999;3380-3391.
73. McDonald N.Q., Hendrickson W.A. A structural superfamily of growth factors containing a cystine knot motif. Cell. 73(3):1993;421-424.
74. Medzhitov R., Janeway C.A. Jr. Innate immunity: impact on the adaptive immune response. Curr. Opin. Immunol. 9(1):1997;4-9.
75. Medzhitov R., Janeway C.A. Jr. Innate immunity: the virtues of a nonclonal system of recognition. Cell. 91(3):1997;295-298.
76. Medzhitov R., Preston-Hurlburt P., Janeway C.A. Jr. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature. 388(6640):1997;394-397.
77. Mellouk S., Maheshwari R.K., Rhodes-Feuillette A., Beaudoin R.L., Berbiguier N., Matile H., Miltgen F., Landau I., Pied S., Chigot J.P.et al. Inhibitory activity of interferons and interleukin 1 on the development of Plasmodium falciparum in human hepatocyte cultures. J. Immunol. 139(12):1987;4192-4195.
78. Meng X., Khanuja B.S., Ip Y.T. Toll receptor-mediated Drosophila immune response requires Dif, an NF-kappaB factor. Genes Dev. 13(7):1999;792-797.
79. Meraz M.A., White J.M., Sheehan K.C., Bach E.A., Rodig S.J., Dighe A.S., Kaplan D.H., Riley J.K., Greenlund A.C., Campbell D., Carver-Moore K., DuBois R.N., Clark R., Aguet M., Schreiber R.D. Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell. 84(3):1996;431-442.
80. Moreira-Ferro C.K., Daffre S., James A.A., Marinotti O. A lysozyme in the salivary glands of the malaria vector Anopheles darlingi. Insect Mol. Biol. 7(3):1998;257-264.
81. Müller H.M., Dimopoulos G., Blass C., Kafatos F.C. A hemocyte-like cell line established from the malaria vector Anopheles gambiae expresses six prophenoloxidase genes. J. Biol. Chem. 274(17):1999;11727-11735.
82. Muta T., Iwanaga S. The role of hemolymph coagulation in innate immunity. Curr. Opin. Immunol. 8(1):1996;41-47.
83. Nussler A., Drapier J.C., Renia L., Pied S., Miltgen F., Gentilini M., Mazier D. L-Arginine-dependent destruction of intrahepatic malaria parasites in response to tumor necrosis factor and/or interleukin 6 stimulation. Eur. J. Immunol. 21(1):1991;227-230.
84. Nussler A., Pied S., Goma J., Renia L., Miltgen F., Grau G.E., Mazier D. TNF inhibits malaria hepatic stages in vitro via synthesis of IL-6. Int. Immunol. 3(4):1991;317-321.
85. Olson K.E., Beaty B.J., Higgs S. RNA virus expression systems. Miller L.K., Ball L.A. The Insect Viruses. 1998;Plenum, New York.
86. O'Shea J.J. Jaks, STATs, cytokine signal transduction, and immunoregulation: are we there yet? Immunity. 7(1):1997;1-11.
87. Paskewitz S.M., Gorman M.J. Mosquito immunity and malaria parasites. American Entomologist. 45(2):1999;81-94.
88. Paskewitz S.M., Reese-Stardy S., Gorman M.J. An easter-like serine protease from Anopheles gambiae exhibits changes in transcript abundance following immune challenge. Insect Mol. Biol. 8(3):1999;329-337.
89. Perrimon N., Mahowald A.P. Hopscotch, a larval-pupal zygotic lethal with a specific maternal effect on segmentation in Drosophila. Dev. Biol. 118(1):1986;28-41.
90. Pied S., Civas A., Berlot-Picard F., Renia L., Miltgen F., Gentilini M., Doly J., Mazier D. IL-6 induced by IL-1 inhibits malaria pre-erythrocytic stages but its secretion is down-regulated by the parasite. J. Immunol. 148(1):1992;197-201.
91. Poltorak A., He X., Smirnova I., Liu M.Y., Huffel C.V., Du X., Birdwell D., Alejos E., Silva M., Galanos C., Freudenberg M., Ricciardi-Castagnoli P., Layton B., Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 282(5396):1998;2085-2088.
92. Richman A.M., Bulet P., Hetru C., Barillas-Mury C., Hoffmann J.A., Kafalos F.C. Inducible immune factors of the vector mosquito Anopheles gambiae: biochemical purification of a defensin antibacterial peptide and molecular cloning of preprodefensin cDNA. Insect Mol. Biol. 5(3):1996;203-210.
93. Richman A.M., Dimopoulos G., Seeley D., Kafatos F.C. Plasmodium activates the innate immune response of Anopheles gambiae mosquitoes. Embo J. 16(20):1997;6114-6119.
94. Rock F.L., Hardiman G., Timans J.C., Kastelein R.A., Bazan J.F. A family of human receptors structurally related to Drosophila Toll. Proc. Natl. Acad. Sci. USA. 95(2):1998;588-593.
95. Satoh D., Horii A., Ochiai M., Ashida M. Prophenoloxidase-activating enzyme of the silkworm, Bombyx mori. Purification, characterization, and cDNA cloning. J. Biol. Chem. 274(11):1999;7441-7453.
96. Schletter J., Heine H., Ulmer A.J., Rietschel E.T. Molecular mechanisms of endotoxin activity. Arch. Microbiol. 164(6):1995;383-389.
97. Sedegah M., Finkelman F., Hoffman S.L. Interleukin 12 induction of interferon gamma-dependent protection against malaria. Proc. Natl. Acad. Sci. USA. 91(22):1994;10700-10702.
98. Sen R., Baltimore D. Multiple immune factors interact with the immunoglobulin enhancer sequences. Cell. 330:1986;583-586.
99. Shahabuddin M., Pimenta P.F. Plasmodium gallinaceum preferentially invades vesicular ATPase-expressing cells in Aedes aegypti midgut. Proc. Natl. Acad. Sci. USA. 95(7):1998;3385-3389.
100. Söderhäll K., Cerenius L. Role of the prophenoloxidase-activating system in invertebrate immunity. Curr. Opin. Immunol. 10(1):1998;23-28.
101. Steiner H., Hultmark D., Engstrom A., Bennich H., Boman H.G. Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature. 292(5820):1981;246-248.
102. Steward R. Dorsal, an embryonic polarity gene in Drosophila, is homologous to the vertebrate proto-oncogene, c-rel. Science. 238(4827):1987;692-694.
103. Steward R. Relocalization of the dorsal protein from the cytoplasm to the nucleus correlates with its function. Cell. 59(6):1989;1179-1188.
104. Sun D., Eccleston E.D., Fallon A.M. Peptide sequence of an antibiotic cecropin from the vector mosquito, Aedes albopictus. Biochem. Biophys. Res. Commun. 249(2):1998;410-415.
105. Sun D., Eccleston E.D., Fallon A.M. Cloning and expression of three cecropin cDNAs from a mosquito cell line. FEBS Lett. 454(1-2):1999;147-151.
106. Sun S.C., Faye I. Affinity purification and characterization of CIF, an insect immunoresponsive factor with NF-kappa B-like properties. Comp. Biochem. Physiol. B. 103(1):1992;225-233.
107. Takeda K., Tanaka T., Shi W., Matsumoto M., Minami M., Kashiwamura S., Nakanishi K., Yoshida N., Kishimoto T., Akira S. Essential role of Stat6 in IL-4 signalling. Nature. 380(6575):1996;627-630.
108. Takeuchi O., Hoshino K., Kawai T., Sanjo H., Takada H., Ogawa T., Takeda K., Akira S. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity. 11(4):1999;443-451.
109. Takeuchi O., Kawai T., Sanjo H., Copeland N.G., Gilbert D.J., Jenkins N.A., Takeda K., Akira S. TLR6: A novel member of an expanding toll-like receptor family. Gene. 231(1-2):1999;59-65.
110. Ulevitch R.J. Endotoxin opens the Tollgates to innate immunity. Nat. Med. 5(2):1999;144-145.
111. Ulevitch R.J., Tobias P.S. Recognition of gram-negative bacteria and endotoxin by the innate immune system. Curr. Opin. Immunol. 11(1):1999;19-22.
112. Underhill D.M., Ozinsky A., Hajjar A.M., Stevens A., Wilson C.B., Bassetti M., Aderem A. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature. 401(6755):1999;811-815.
113. Wasserman S.A. A conserved signal transduction pathway regulating the activity of the rel-like proteins dorsal and NF-kappa B. Mol. Biol. Cell. 4(8):1993;767-771.
114. Williams M.J., Rodriguez A., Kimbrell D.A., Eldon E.D. The 18-wheeler mutation reveals complex antibacterial gene regulation in Drosophila host defense. Embo J. 16(20):1997;6120-6130.
115. Wu L.P., Anderson K.V. Regulated nuclear import of Rel proteins in the Drosophila immune response. Nature. 392(6671):1998;93-97.
116. Xie Q.W., Whisnant R., Nathan C. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J. Exp. Med. 177(6):1993;1779-1784.
117. Yan R., Small S., Desplan C., Dearolf C.R., Darnell J.E. Jr. Identification of a Stat gene that functions in Drosophila development. Cell. 84(3):1996;421-430.
118. Yang R.B., Mark M.R., Gray A., Huang A., Xie M.H., Zhang M., Goddard A., Wood W.I., Gurney A.L., Godowski P.J. Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature. 395(6699):1998;284-288.
119. Yoshiga T., Hernandez V.P., Fallon A.M., Law J.H. Mosquito transferrin, an acute-phase protein that is up-regulated upon infection. Proc. Natl. Acad. Sci. USA. 94(23):1997;12337-12342.
120. Yoshimura A., Lien E., Ingalls R.R., Tuomanen E., Dziarski R., Golenbock D. Cutting edge: recognition of Gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J. Immunol. 163(1):1999;1-5.
121. Yu X.Q., Gan H., Kanost M.R. Immulectin, an inducible C-type lectin from an insect, Manduca sexta, stimulates activation of plasma prophenol oxidase. Insect Biochem. Mol. Biol. 29(7):1999;585-597.
122. Zanetti M., Gennaro R., Romeo D. Cathelicidins: a novel protein family with a common proregion and a variable C-terminal antimicrobial domain. FEBS Lett. 374(1):1995;1-5.
123. Zheng L., Benedict M.Q., Cornel A.J., Collins F.H., Kafatos F.C. An integrated genetic map of the African human malaria vector mosquito, Anopheles gambiae. Genetics. 143(2):1996;941-952.
124. Zheng L., Cornel A.J., Wang R., Erfle H., Voss H., Ansorge W., Kafatos F.C., Collins F.H. Quantitative trait loci for refractoriness of Anopheles gambiae to Plasmodium cynomolgi B. Science. 276(5311):1997;425-428.