Mosquito immune defenses against Plasmodium infection

Developmental and Comparative Immunology

Volumn 34, Issue 4, 2010, Pages 387-395

  Cirimotich, Chris M ^a   Dong, Yuemei ^a   Garver, Lindsey S ^a   Sim, Shuzhen ^a   Dimopoulos, George ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Anopheles; Innate immunity; Malaria; Mosquito; Plasmodium

Indexed keywords

C TYPE LECTIN; FIBRINOGEN RELATED PROTEIN; JANUS KINASE; LECTIN; LEUCINE RICH REPEAT DOMAIN CONTAINING PROTEIN; PROTEIN SERINE THREONINE KINASE; STAT PROTEIN; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

BACTERIAL FLORA; DROSOPHILA; GASTROINTESTINAL INFECTION; GASTROINTESTINAL TRACT FUNCTION; HOST PARASITE INTERACTION; IMMUNE RESPONSE; INFECTION PREVENTION; INNATE IMMUNITY; INTESTINE FLORA; MOSQUITO; NONHUMAN; PLASMODIUM; PLASMODIUM MALARIAE INFECTION; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; SIGNAL TRANSDUCTION;

PLASMODIUM PARASITES;

EID: 74449090116     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2009.12.005     Document Type: Review

References (104)

1. Lemaitre B., and Hoffmann J. The host defense of Drosophila melanogaster. Annual Review of Immunology 25 (2007) 697-743
2. Christophides G.K., Zdobnov E., Barillas-Mury C., Birney E., Blandin S., Blass C., et al. Immunity-related genes and gene families in Anopheles gambiae. Science (New York, NY) 298 5591 (2002) 159-165
3. Zambon R.A., Nandakumar M., Vakharia V.N., and Wu L.P. The Toll pathway is important for an antiviral response in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 102 20 (2005) 7257-7262
4. Xi Z., Ramirez J.L., and Dimopoulos G. The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathogens 4 7 (2008) e1000098
5. Frolet C., Thoma M., Blandin S., Hoffmann J.A., and Levashina E.A. Boosting NF-kappaB-dependent basal immunity of Anopheles gambiae aborts development of Plasmodium berghei. Immunity 25 4 (2006) 677-685
6. Barillas-Mury C., Charlesworth A., Gross I., Richman A., Hoffmann J.A., and Kafatos F.C. Immune factor Gambif1, a new rel family member from the human malaria vector, Anopheles gambiae. The EMBO Journal 15 17 (1996) 4691-4701
7. Han Z.S., and Ip Y.T. Interaction and specificity of Rel-related proteins in regulating Drosophila immunity gene expression. The Journal of Biological Chemistry 274 30 (1999) 21355-21361
8. Ip Y.T., Reach M., Engstrom Y., Kadalayil L., Cai H., González-Crespo S., et al. Dif., a dorsal-related gene that mediates an immune response in Drosophila. Cell 75 4 (1993) 753-763
9. Manfruelli P., Reichhart J.M., Steward R., Hoffmann J.A., and Lemaitre B. A mosaic analysis in Drosophila fat body cells of the control of antimicrobial peptide genes by the Rel proteins Dorsal and DIF. The EMBO Journal 18 12 (1999) 3380-3391
10. Meng X., Khanuja B.S., and Ip Y.T. Toll receptor-mediated Drosophila immune response requires Dif, an NF-kappaB factor. Genes & Development 13 7 (1999) 792-797
11. Bergmann A., Stein D., Geisler R., Hagenmaier S., Schmid B., Fernandez N., et al. A gradient of cytoplasmic Cactus degradation establishes the nuclear localization gradient of the dorsal morphogen in Drosophila. Mechanisms of Development 60 1 (1996) 109-123
12. Edwards D.N., Towb P., and Wasserman S.A. An activity-dependent network of interactions links the Rel protein Dorsal with its cytoplasmic regulators. Development (Cambridge, England) 124 19 (1997) 3855-3864
13. Nicolas E., Reichhart J.M., Hoffmann J.A., and Lemaitre B. In vivo regulation of the IkappaB homologue cactus during the immune response of Drosophila. The Journal of Biological Chemistry 273 17 (1998) 10463-10469
14. Yang J., and Steward R. A multimeric complex and the nuclear targeting of the Drosophila Rel protein Dorsal. Proceedings of the National Academy of Sciences of the United States of America 94 26 (1997) 14524-14529
15. Belvin M.P., Jin Y., and Anderson K.V. Cactus protein degradation mediates Drosophila dorsal-ventral signaling. Genes & Development 9 7 (1995) 783-793
16. Wu L.P., and Anderson K.V. Regulated nuclear import of Rel proteins in the Drosophila immune response. Nature 392 6671 (1998) 93-97
17. Garver L.S., Dong Y., and Dimopoulos G. Caspar controls resistance to Plasmodium falciparum in diverse anopheline species. PLoS Pathogens 5 3 (2009) e1000335
18. Zou Z., Shin S.W., Alvarez K.S., Bian G., Kokoza V., and Raikhel A.S. Mosquito RUNX4 in the immune regulation of PPO gene expression and its effect on avian malaria parasite infection. Proceedings of the National Academy of Sciences of the United States of America 105 47 (2008) 18454-18459
19. Aggarwal K., and Silverman N. Positive and negative regulation of the Drosophila immune response. BMB Reports 41 4 (2008) 267-277
20. Kaneko T., and Silverman N. Bacterial recognition and signalling by the Drosophila IMD pathway. Cellular Microbiology 7 4 (2005) 461-469
21. Choe K., Werner T., Stöven S., Hultmark D., and Anderson K.V. Requirement for a peptidoglycan recognition protein (PGRP) in Relish activation and antibacterial immune responses in Drosophila. Science (New York, NY) 296 5566 (2002) 359-362
22. Choe K., Lee H., and Anderson K.V. Drosophila peptidoglycan recognition protein LC (PGRP-LC) acts as a signal-transducing innate immune receptor. Proceedings of the National Academy of Sciences of the United States of America 102 4 (2005) 1122-1126
23. Georgel P., Naitza S., Kappler C., Ferrandon D., Zachary D., Swimmer C., et al. Drosophila immune deficiency (IMD) is a death domain protein that activates antibacterial defense and can promote apoptosis. Developmental Cell 1 4 (2001) 503-514
24. Leulier F., Vidal S., Saigo K., Ueda R., and Lemaitre B. Inducible expression of double-stranded RNA reveals a role for dFADD in the regulation of the antibacterial response in Drosophila adults. Current Biology: CB 12 12 (2002) 996-1000
25. Leulier F., Parquet C., Pili-Floury S., Ryu J., Caroff M., Lee W., et al. The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nature Immunology 4 5 (2003) 478-484
26. Kleino A., Valanne S., Ulvila J., Kallio J., Myllymäki H., Enwald H., et al. Inhibitor of apoptosis 2 and TAK1-binding protein are components of the Drosophila Imd pathway. The EMBO Journal 24 19 (2005) 3423-3434
27. Rutschmann S., Jung A.C., Zhou R., Silverman N., Hoffmann J.A., and Ferrandon D. Role of Drosophila IKK gamma in a toll-independent antibacterial immune response. Nature Immunology 1 4 (2000) 342-347
28. Tanji T., and Ip Y.T. Regulators of the Toll and Imd pathways in the Drosophila innate immune response. Trends in Immunology 26 4 (2005) 193-198
29. Meister S., Kanzok S.M., Zheng X., Luna C., Li T., Hoa N.T., et al. Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae. Proceedings of the National Academy of Sciences of the United States of America 102 32 (2005) 11420-11425
30. Stoven S., Silverman N., Junell A., Hedengren-Olcott M., Erturk D., Engstrom Y., et al. Caspase-mediated processing of the Drosophila NF-kappaB factor Relish. Proceedings of the National Academy of Sciences of the United States of America 100 10 (2003) 5991-5996
31. Boutros M., Agaisse H., and Perrimon N. Sequential activation of signaling pathways during innate immune responses in Drosophila. Developmental Cell 3 5 (2002) 711-722
32. Dushay M.S., Asling B., and Hultmark D. Origins of immunity: Relish, a compound Rel-like gene in the antibacterial defense of Drosophila. Proceedings of the National Academy of Sciences of the United States of America 93 19 (1996) 10343-10347
33. Hedengren M., Asling B., Dushay M.S., Ando I., Ekengren S., Wihlborg M., et al. Relish, a central factor in the control of humoral but not cellular immunity in Drosophila. Molecular Cell 4 5 (1999) 827-837
34. Hoa N., and Zheng L. Functional characterization of the NF-κB transcription factor gene rel2 from Anopheles gambiae. Insect Science 14 3 (2007) 175-184
35. Kallio J., Leinonen A., Ulvila J., Valanne S., Ezekowitz R.A., and Rämet M. Functional analysis of immune response genes in Drosophila identifies JNK pathway as a regulator of antimicrobial peptide gene expression in S2 cells. Microbes and Infection/Institut Pasteur 7 5-6 (2005) 811-819
36. Silverman N., Zhou R., Stöven S., Pandey N., Hultmark D., and Maniatis T. A Drosophila IkappaB kinase complex required for Relish cleavage and antibacterial immunity. Genes & Development 14 19 (2000) 2461-2471
37. Sluss H.K., Han Z., Barrett T., Goberdhan D.C., Wilson C., Davis R.J., et al. A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes & Development 10 21 (1996) 2745-2758
38. Stöven S., Ando I., Kadalayil L., Engström Y., and Hultmark D. Activation of the Drosophila NF-kappaB factor Relish by rapid endoproteolytic cleavage. EMBO Reports 1 4 (2000) 347-352
39. Luna C., Hoa N.T., Lin H., Zhang L., Nguyen H.L.A., Kanzok S.M., et al. Expression of immune responsive genes in cell lines from two different Anopheline species. Insect Molecular Biology 15 6 (2006) 721-729
40. Leulier F., Rodriguez A., Khush R.S., Abrams J.M., and Lemaitre B. The Drosophila caspase Dredd is required to resist gram-negative bacterial infection. EMBO Reports 1 4 (2000) 353-358
41. Kim M., Lee J.H., Lee S.Y., Kim E., Chung J., and Caspar. A suppressor of antibacterial immunity in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 103 44 (2006) 16358-16363
42. Meister S., Agianian B., Turlure F., Relógio A., Morlais I., Kafatos F.C., et al. Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites. PLoS Pathogens 5 8 (2009) e1000542
43. Povelones M., Waterhouse R.M., Kafatos F.C., and Christophides G.K. Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites. Science (New York, NY) 324 5924 (2009) 258-261
44. Buchon N., Broderick N.A., Poidevin M., Pradervand S., and Lemaitre B. Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host & Microbe 5 2 (2009) 200-211
45. Cronin S.J.F., Nehme N.T., Limmer S., Liegeois S., Pospisilik J.A., Schramek D., et al. Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science (New York, NY) 325 5938 (2009) 340-343
46. Dostert C., Jouanguy E., Irving P., Troxler L., Galiana-Arnoux D., Hetru C., et al. The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of drosophila. Nature Immunology 6 9 (2005) 946-953
47. Souza-Neto J.A., Sim S., and Dimopoulos G. An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proceedings of the National Academy of Sciences of the United States of America (2009)
48. Gupta L., Molina-Cruz A., Kumar S., Rodrigues J., Dixit R., Zamora R.E., et al. The STAT pathway mediates late-phase immunity against Plasmodium in the mosquito Anopheles gambiae. Cell Host & Microbe 5 5 (2009) 498-507
49. Brandt S.M., Jaramillo-Gutierrez G., Kumar S., Barillas-Mury C., and Schneider D.S. Use of a Drosophila model to identify genes regulating Plasmodium growth in the mosquito. Genetics 180 3 (2008) 1671-1678
50. Surachetpong W., Singh N., Cheung K.W., and Luckhart S. MAPK ERK signaling regulates the TGF-beta1-dependent mosquito response to Plasmodium falciparum. PLoS Pathogens 5 4 (2009) e1000366
51. Dimopoulos G., Christophides G.K., Meister S., Schultz J., White K.P., Barillas-Mury C., et al. Genome expression analysis of Anopheles gambiae: responses to injury, bacterial challenge, and malaria infection. Proceedings of the National Academy of Sciences of the United States of America 99 13 (2002) 8814-8819
52. Dong Y., Aguilar R., Xi Z., Warr E., Mongin E., and Dimopoulos G. Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathogens 2 6 (2006) e52
53. Osta M.A., Christophides G.K., and Kafatos F.C. Effects of mosquito genes on Plasmodium development. Science (New York, NY) 303 5666 (2004) 2030-2032
54. Riehle M.M., Markianos K., Niaré O., Xu J., Li J., Touré A.M., et al. Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science (New York, NY) 312 5773 (2006) 577-579
55. Riehle M.M., Xu J., Lazzaro B.P., Rottschaefer S.M., Coulibaly B., Sacko M., et al. Anopheles gambiae APL1 is a family of variable LRR proteins required for Rel1-mediated protection from the malaria parasite, Plasmodium berghei. PloS One 3 11 (2008) e3672
56. Habtewold T., Povelones M., Blagborough A.M., and Christophides G.K. Transmission blocking immunity in the malaria non-vector mosquito Anopheles quadriannulatus species A. PLoS Pathogens 4 5 (2008) e1000070
57. Warr E., Lambrechts L., Koella J.C., Bourgouin C., and Dimopoulos G. Anopheles gambiae immune responses to Sephadex beads: involvement of anti-Plasmodium factors in regulating melanization. Insect Biochemistry and Molecular Biology 36 10 (2006) 769-778
58. Fraiture M., Baxter R.H.G., Steinert S., Chelliah Y., Frolet C., Quispe-Tintaya W., et al. Two mosquito LRR proteins function as complement control factors in the TEP1-mediated killing of Plasmodium. Cell Host & Microbe 5 3 (2009) 273-284
59. Mitri C., Jacques J., Thiery I., Riehle M.M., Xu J., Bischoff E., et al. Fine pathogen discrimination within the APL1 gene family protects anopheles gambiae against human and rodent malaria species. PLoS Pathogens 5 9 (2009) e1000576
60. Dong Y., and Dimopoulos G. Anopheles fibrinogen-related proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. The Journal of Biological Chemistry 284 15 (2009) 9835-9844
61. Fujita T. Evolution of the lectin-complement pathway and its role in innate immunity. Nature Reviews. Immunology 2 5 (2002) 346-353
62. Gokudan S., Muta T., Tsuda R., Koori K., Kawahara T., Seki N., et al. Horseshoe crab acetyl group-recognizing lectins involved in innate immunity are structurally related to fibrinogen. Proceedings of the National Academy of Sciences of the United States of America 96 18 (1999) 10086-10091
63. Wang X., Zhao Q., and Christensen B.M. Identification and characterization of the fibrinogen-like domain of fibrinogen-related proteins in the mosquito, Anopheles gambiae, and the fruitfly, Drosophila melanogaster, genomes. BMC Genomics 6 (2005) 114
64. Middha S., and Wang X. Evolution and potential function of fibrinogen-like domains across twelve Drosophila species. BMC Genomics 9 (2008) 260
65. Waterhouse R.M., Kriventseva E.V., Meister S., Xi Z., Alvarez K.S., Bartholomay L.C., et al. Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science (New York, NY) 316 5832 (2007) 1738-1743
66. Dimopoulos G., Casavant T.L., Chang S., Scheetz T., Roberts C., Donohue M., et al. Anopheles gambiae pilot gene discovery project: identification of mosquito innate immunity genes from expressed sequence tags generated from immune-competent cell lines. Proceedings of the National Academy of Sciences of the United States of America 97 12 (2000) 6619-6624
67. Holmskov U., Thiel S., and Jensenius J.C. Collections and ficolins: humoral lectins of the innate immune defense. Annual Review of Immunology 21 (2003) 547-578
68. Kuhlman M., Joiner K., and Ezekowitz R.A. The human mannose-binding protein functions as an opsonin. The Journal of Experimental Medicine 169 5 (1989) 1733-1745
69. Matsushita M., and Fujita T. Activation of the classical complement pathway by mannose-binding protein in association with a novel C1s-like serine protease. The Journal of Experimental Medicine 176 6 (1992) 1497-1502
70. Schnitger A.K.D., Yassine H., Kafatos F.C., and Osta M.A. Two C-type lectins cooperate to defend Anopheles gambiae against Gram-negative bacteria. The Journal of Biological Chemistry 284 26 (2009) 17616-17624
71. Luckhart S., Li K., Dunton R., Lewis E.E., Crampton A.L., Ryan J.R., et al. Anopheles gambiae immune gene variants associated with natural Plasmodium infection. Molecular and Biochemical Parasitology 128 1 (2003) 83-86
72. Vizioli J., Bulet P., Hoffmann J.A., Kafatos F.C., Müller H.M., and Dimopoulos G. Gambicin: a novel immune responsive antimicrobial peptide from the malaria vector Anopheles gambiae. Proceedings of the National Academy of Sciences of the United States of America 98 22 (2001) 12630-12635
73. Dong Y., Taylor H.E., Dimopoulos G., and AgDscam. A hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biology 4 7 (2006) e229
74. Garver L.S., Xi Z., and Dimopoulos G. Immunoglobulin superfamily members play an important role in the mosquito immune system. Developmental and Comparative Immunology 32 5 (2008) 519-531
75. Warr E., Das S., Dong Y., and Dimopoulos G. The Gram-negative bacteria-binding protein gene family: its role in the innate immune system of anopheles gambiae and in anti-Plasmodium defence. Insect Molecular Biology 17 1 (2008) 39-51
76. Dimopoulos G., Richman A., Müller H.M., and Kafatos F.C. Molecular immune responses of the mosquito Anopheles gambiae to bacteria and malaria parasites. Proceedings of the National Academy of Sciences of the United States of America 94 21 (1997) 11508-11513
77. Pumpuni C.B., Demaio J., Kent M., Davis J.R., and Beier J.C. Bacterial population dynamics in three anopheline species: the impact on Plasmodium sporogonic development. The American Journal of Tropical Medicine and Hygiene 54 2 (1996) 214-218
78. Dong Y., Manfredini F., and Dimopoulos G. Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathogens 5 5 (2009) e1000423
79. Beier M.S., Pumpuni C.B., Beier J.C., and Davis J.R. Effects of para-aminobenzoic acid, insulin, and gentamicin on Plasmodium falciparum development in anopheline mosquitoes (Diptera: Culicidae). Journal of Medical Entomology 31 4 (1994) 561-565
80. Ryu J., Kim S., Lee H., Bai J.Y., Nam Y., Bae J., et al. Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science (New York, NY) 319 5864 (2008) 777-782
81. Ha E., Oh C., Bae Y.S., and Lee W. A direct role for dual oxidase in Drosophila gut immunity. Science (New York, NY) 310 5749 (2005) 847-850
82. Ha E., Lee K., Seo Y.Y., Kim S., Lim J., Oh B., et al. Coordination of multiple dual oxidase-regulatory pathways in responses to commensal and infectious microbes in drosophila gut. Nature Immunology 10 9 (2009) 949-957
83. Molina-Cruz A., DeJong R.J., Charles B., Gupta L., Kumar S., Jaramillo-Gutierrez G., et al. Reactive oxygen species modulate Anopheles gambiae immunity against bacteria and Plasmodium. The Journal of Biological Chemistry 283 6 (2008) 3217-3223
84. Gonzalez-Ceron L., Santillan F., Rodriguez M.H., Mendez D., and Hernandez-Avila J.E. Bacteria in midguts of field-collected Anopheles albimanus block Plasmodium vivax sporogonic development. Journal of Medical Entomology 40 3 (2003) 371-374
85. Pumpuni C.B., Beier M.S., Nataro J.P., Guers L.D., and Davis J.R. Plasmodium falciparum: inhibition of sporogonic development in Anopheles stephensi by gram-negative bacteria. Experimental Parasitology 77 2 (1993) 195-199
86. Arrighi R.B.G., Debierre-Grockiego F., Schwarz R.T., and Faye I. The immunogenic properties of protozoan glycosylphosphatidylinositols in the mosquito Anopheles gambiae. Developmental and Comparative Immunology 33 2 (2009) 216-223
87. Akman-Anderson L., Olivier M., and Luckhart S. Induction of nitric oxide synthase and activation of signaling proteins in Anopheles mosquitoes by the malaria pigment, hemozoin. Infection and Immunity 75 8 (2007) 4012-4019
88. Lim J., Gowda D.C., Krishnegowda G., and Luckhart S. Induction of nitric oxide synthase in Anopheles stephensi by Plasmodium falciparum: mechanism of signaling and the role of parasite glycosylphosphatidylinositols. Infection and Immunity 73 5 (2005) 2778-2789
89. Abraham E.G., and Jacobs-Lorena M. Mosquito midgut barriers to malaria parasite development. Insect Biochemistry and Molecular Biology 34 7 (2004) 667-671
90. 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. The EMBO Journal 19 22 (2000) 6030-6040
91. Billingsley P.F., and Rudin W. The role of the mosquito peritrophic membrane in bloodmeal digestion and infectivity of Plasmodium species. The Journal of Parasitology 78 3 (1992) 430-440
92. Kato N., Mueller C.R., Fuchs J.F., McElroy K., Wessely V., Higgs S., et al. Evaluation of the function of a type I peritrophic matrix as a physical barrier for midgut epithelium invasion by mosquito-borne pathogens in Aedes aegypti. Vector Borne and Zoonotic Diseases (Larchmont, NY) 8 5 (2008) 701-712
93. Dinglasan R.R., Devenport M., Florens L., Johnson J.R., McHugh C.A., Donnelly-Doman M., et al. The Anopheles gambiae adult midgut peritrophic matrix proteome. Insect Biochemistry and Molecular Biology 39 2 (2009) 125-134
94. Kadota K., Ishino T., Matsuyama T., Chinzei Y., and Yuda M. Essential role of membrane-attack protein in malarial transmission to mosquito host. Proceedings of the National Academy of Sciences of the United States of America 101 46 (2004) 16310-16315
95. Dessens J.T., Beetsma A.L., Dimopoulos G., Wengelnik K., Crisanti A., Kafatos F.C., et al. CTRP is essential for mosquito infection by malaria ookinetes. The EMBO Journal 18 22 (1999) 6221-6227
96. Dessens J.T., Sidén-Kiamos I., Mendoza J., Mahairaki V., Khater E., Vlachou D., et al. SOAP, a novel malaria ookinete protein involved in mosquito midgut invasion and oocyst development. Molecular Microbiology 49 2 (2003) 319-329
97. Baker R.P., Wijetilaka R., and Urban S. Two Plasmodium rhomboid proteases preferentially cleave different adhesins implicated in all invasive stages of malaria. PLoS Pathogens 2 10 (2006) e113
98. Srinivasan P., Coppens I., and Jacobs-Lorena M. Distinct roles of Plasmodium rhomboid 1 in parasite development and malaria pathogenesis. PLoS Pathogens 5 1 (2009) e1000262
99. González-Lázaro M., Dinglasan R.R., Hernández-Hernández F.D.L.C., Rodríguez M.H., Laclaustra M., Jacobs-Lorena M., et al. Anopheles gambiae Croquemort SCRBQ2, expression profile in the mosquito and its potential interaction with the malaria parasite Plasmodium berghei. Insect Biochemistry and Molecular Biology 39 5-6 (2009) 395-402
100. Kariu T., Ishino T., Yano K., Chinzei Y., and Yuda M. CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts. Molecular Microbiology 59 5 (2006) 1369-1379
101. Vlachou D., Zimmermann T., Cantera R., Janse C.J., Waters A.P., and Kafatos F.C. Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion. Cellular Microbiology 6 7 (2004) 671-685
102. Vlachou D., Schlegelmilch T., Christophides G.K., and Kafatos F.C. Functional genomic analysis of midgut epithelial responses in Anopheles during Plasmodium invasion. Current Biology: CB 15 13 (2005) 1185-1195
103. Mendes A.M., Schlegelmilch T., Cohuet A., Awono-Ambene P., De Iorio M., Fontenille D., et al. Conserved mosquito/parasite interactions affect development of Plasmodium falciparum in Africa. PLoS Pathogens 4 5 (2008) e1000069
104. Ghosh A.K., and Jacobs-Lorena M. Plasmodium sporozoite invasion of the mosquito salivary gland. Current Opinion in Microbiology 12 4 (2009) 394-400