The STAT Pathway Mediates Late-Phase Immunity against Plasmodium in the Mosquito Anopheles gambiae

Cell Host and Microbe

Volumn 5, Issue 5, 2009, Pages 498-507

  Gupta, Lalita ^a   Molina Cruz, Alvaro ^a   Kumar, Sanjeev ^a   Rodrigues, Janneth ^a   Dixit, Rajnikant ^a   Zamora, Rodolfo E ^a   Barillas Mury, Carolina ^a  

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

Author keywords

CELLBIO; MICROBIO; SIGNALING

Indexed keywords

MESSENGER RNA; NITRIC OXIDE SYNTHASE; STAT PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING;

ANIMAL CELL; ANIMAL TISSUE; ANOPHELES GAMBIAE; ARTICLE; BACTERIAL INFECTION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; GENE ACTIVATION; GENE DUPLICATION; GENE EXPRESSION; GENE SILENCING; IMMUNE RESPONSE; MIDGUT; NONHUMAN; OOCYST; PLASMODIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTOZOAL INFECTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES GAMBIAE; BASE SEQUENCE; CELL LINE; FEMALE; HOST-PARASITE INTERACTIONS; INSECT PROTEINS; MALARIA; MALE; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; NITRIC OXIDE SYNTHASE; OOCYSTS; PHYLOGENY; PLASMODIUM; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS;

ANOPHELES GAMBIAE; BACTERIA (MICROORGANISMS); VERTEBRATA;

EID: 65549140168     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2009.04.003     Document Type: Article

References (36)

1. Abraham E.G., Pinto S.B., Ghosh A., Vanlandingham D.L., Budd A., Higgs S., Kafatos F.C., Jacobs-Lorena M., and Michel K. An immune-responsive serpin, SRPN6, mediates mosquito defense against malaria parasites. Proc. Natl. Acad. Sci. USA 102 (2005) 16327-16332
2. Agaisse H., and Perrimon N. The roles of JAK/STAT signaling in Drosophila immune responses. Immunol. Rev. 198 (2004) 72-82
3. Alavi Y., Arai M., Mendoza J., Tufet-Bayona M., Sinha R., Fowler K., Billker O., Franke-Fayard B., Janse C.J., Waters A., et al. The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti. Int. J. Parasitol. 33 (2003) 933-943
4. Arbouzova N.I., and Zeidler M.P. JAK/STAT signalling in Drosophila: insights into conserved regulatory and cellular functions. Development 133 (2006) 2605-2616
5. Barillas-Mury C., Han Y.S., Seeley D., and 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 (1999) 959-967
6. Betz A., Lampen N., Martinek S., Young M.W., and Darnell Jr. J.E. A Drosophila PIAS homologue negatively regulates stat92E. Proc. Natl. Acad. Sci. USA 98 (2001) 9563-9568
7. Billker O., Shaw M.K., Margos G., and Sinden R.E. The roles of temperature, pH and mosquito factors as triggers of male and female gametogenesis of Plasmodium berghei in vitro. Parasitology 115 (1997) 1-7
8. Blandin S., Shiao S.H., Moita L.F., Janse C.J., Waters A.P., Kafatos F.C., and Levashina E.A. Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116 (2004) 661-670
9. Callus B.A., and Mathey-Prevot B. SOCS36E, a novel Drosophila SOCS protein, suppresses JAK/STAT and EGF-R signalling in the imaginal wing disc. Oncogene 21 (2002) 4812-4821
10. Castillo J.C., Robertson A.E., and Strand M.R. Characterization of hemocytes from the mosquitoes Anopheles gambiae and Aedes aegypti. Insect Biochem. Mol. Biol. 36 (2006) 891-903
11. Christophides G.K., Zdobnov E., Barillas-Mury C., Birney E., Blandin S., Blass C., Brey P.T., Collins F.H., Danielli A., Dimopoulos G., et al. Immunity-related genes and gene families in Anopheles gambiae. Science 298 (2002) 159-165
12. Collins F.H., Sakai R.K., Vernick K.D., Paskewitz S., Seeley D.C., Miller L.H., Collins W.E., Campbell C.C., and Gwadz R.W. Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science 234 (1986) 607-610
13. Dostert C., Jouanguy E., Irving P., Troxler L., Galiana-Arnoux D., Hetru C., Hoffmann J.A., and Imler J.L. The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of drosophila. Nat. Immunol. 6 (2005) 946-953
14. Ekengren S., and Hultmark D. A family of Turandot-related genes in the humoral stress response of Drosophila. Biochem. Biophys. Res. Commun. 284 (2001) 998-1003
15. Foley E., and O'Farrell P.H. Nitric oxide contributes to induction of innate immune responses to gram-negative bacteria in Drosophila. Genes Dev. 17 (2003) 115-125
16. Franke-Fayard B., Trueman H., Ramesar J., Mendoza J., van der Keur M., van der Linden R., Sinden R.E., Waters A.P., and Janse C.J. A Plasmodium berghei reference line that constitutively expresses GFP at a high level throughout the complete life cycle. Mol. Biochem. Parasitol. 137 (2004) 23-33
17. Garver L.S., Xi Z., and Dimopoulos G. Immunoglobulin superfamily members play an important role in the mosquito immune system. Dev. Comp. Immunol. 32 (2008) 519-531
18. Han Y.S., Thompson J., Kafatos F.C., and Barillas-Mury C. Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinete invasion of mosquitoes. EMBO J. 19 (2000) 6030-6040
19. Hanratty W.P., and Dearolf C.R. The Drosophila Tumorous-lethal hematopoietic oncogene is a dominant mutation in the hopscotch locus. Mol. Gen. Genet. 238 (1993) 33-37
20. Harrison D.A., Binari R., Nahreini T.S., Gilman M., and Perrimon N. Activation of a Drosophila Janus kinase (JAK) causes hematopoietic neoplasia and developmental defects. EMBO J. 14 (1995) 2857-2865
21. Hoffmann J.A., and Reichhart J.M. Drosophila innate immunity: an evolutionary perspective. Nat. Immunol. 3 (2002) 121-126
22. Ifediba T., and Vanderberg J.P. Complete in vitro maturation of Plasmodium falciparum gametocytes. Nature 294 (1981) 364-366
23. Kim L.K., Choi U.Y., Cho H.S., Lee J.S., Lee W.B., Kim J., Jeong K., Shim J., Kim-Ha J., and Kim Y.J. Down-regulation of NF-kappaB target genes by the AP-1 and STAT complex during the innate immune response in Drosophila. PLoS Biol. 5 (2007) e238
24. Krzemien J., Dubois L., Makki R., Meister M., Vincent A., and Crozatier M. Control of blood cell homeostasis in Drosophila larvae by the posterior signalling centre. Nature 446 (2007) 325-328
25. Levashina E.A., Moita L.F., Blandin S., Vriend G., Lagueux M., and Kafatos F.C. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104 (2001) 709-718
26. Luckhart S., and Rosenberg R. Gene structure and polymorphism of an invertebrate nitric oxide synthase gene. Gene 232 (1999) 25-34
27. Luckhart S., Vodovotz Y., Cui L., and Rosenberg R. The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc. Natl. Acad. Sci. USA 95 (1998) 5700-5705
28. Muller H.M., Dimopoulos G., Blass C., and Kafatos F.C. A hemocyte-like cell line established from the malaria vector Anopheles gambiae expresses six prophenoloxidase genes. J. Biol. Chem. 274 (1999) 11727-11735
29. Nappi A.J., Vass E., Frey F., and Carton Y. Nitric oxide involvement in Drosophila immunity. Nitric Oxide 4 (2000) 423-430
30. Osta M.A., Christophides G.K., and Kafatos F.C. Effects of mosquito genes on Plasmodium development. Science 303 (2004) 1984-1985
31. Schindler C., Levy D.E., and Decker T. JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 282 (2007) 20059-20063
32. Tanji T., and Ip Y.T. Regulators of the Toll and Imd pathways in the Drosophila innate immune response. Trends Immunol. 26 (2005) 193-198
33. Trager W., and Jensen J.B. Human malaria parasites in continuous culture. Science 193 (1976) 673-675
34. Vlachou D., Schlegelmilch T., Christophides G.K., and Kafatos F.C. Functional genomic analysis of midgut epithelial responses in Anopheles during Plasmodium invasion. Curr. Biol. 15 (2005) 1185-1195
35. Wormald S., and Hilton D.J. Inhibitors of cytokine signal transduction. J. Biol. Chem. 279 (2004) 821-824
36. Zolg J.W., MacLeod A.J., Dickson I.H., and Scaife J.G. Plasmodium falciparum: modifications of the in vitro culture conditions improving parasitic yields. J. Parasitol. 68 (1982) 1072-1080