Characterization of the Rel2-regulated transcriptome and proteome of Anopheles stephensi identifies new anti-Plasmodium factors

Insect Biochemistry and Molecular Biology

Volumn 52, Issue 1, 2014, Pages 82-93

  Pike, Andrew ^a   Vadlamani, Alekhya ^a   Sandiford, Simone L ^a   Gacita, Anthony ^a   Dimopoulos, George ^a  

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

Author keywords

Innate immunity; Mosquitoes; Plasmodium; Proteome; Rel2; Transcriptome; Transgenesis

Indexed keywords

INSECT PROTEIN; PROTEOME; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ANIMAL; ANOPHELES; BIOSYNTHESIS; DISEASE CARRIER; DNA MICROARRAY; FEMALE; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; PARASITOLOGY; PHYSIOLOGY; PLASMODIUM FALCIPARUM; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL; UPREGULATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANOPHELES; FEMALE; GENE EXPRESSION PROFILING; IMMUNITY, INNATE; INSECT PROTEINS; INSECT VECTORS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLASMODIUM FALCIPARUM; PROTEOME; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTOME; UP-REGULATION;

EID: 84904480186     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2014.06.005     Document Type: Article

References (59)

1. Abraham E.G., Pinto S.B., Ghosh A., Vanlandingham D.L., Budd A., Higgs S., Kafatos F.C., Jacobs-Lorena M., Michel K. An immune-responsive serpin, SRPN6, mediates mosquito defense against malaria parasites. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:16327-16332.
2. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J.Mol. Biol. 1990, 215:403-410.
3. An C., Jiang H., Kanost M.R. Proteolytic activation and function of the cytokine Spatzle in the innate immune response of a lepidopteran insect, Manduca sexta. FEBS J. 2010, 277:148-162.
4. Armstrong P.B., Quigley J.P. Alpha2-macroglobulin: an evolutionarily conserved arm of the innate immune system. Dev. Comp. Immunol. 1999, 23:375-390.
5. Bano N., Romano J.D., Jayabalasingham B., Coppens I. Cellular interactions of Plasmodium liver stage with its host mammalian cell. Int. J. Parasitol. 2007, 37:1329-1341.
6. Blandin S., Shiao S.H., Moita L.F., Janse C.J., Waters A.P., Kafatos F.C., Levashina E.A. Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 2004, 116:661-670.
7. Blandin S.A., Levashina E.A. Phagocytosis in mosquito immune responses. Immunol. Rev. 2007, 219:8-16.
8. Blumberg B.J., Trop S., Das S., Dimopoulos G. Bacteria- and IMD pathway-independent immune defenses against Plasmodium falciparum in Anopheles gambiae. PLoS One 2013, 8:e72130.
9. Buchon N., Broderick N.A., Lemaitre B. Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nat. Rev. Microbiol. 2013, 11:615-626.
10. Burnham S., Smith J.A., Lee A.J., Isaac R.E., Shirras A.D. The angiotensin-converting enzyme (ACE) gene family of Anopheles gambiae. BMC Genomics 2005, 6:172.
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., 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., Kafatos F.C. Immunity-related genes and gene families in Anopheles gambiae. Science 2002, 298:159-165.
12. Cirimotich C.M., Dong Y., Garver L.S., Sim S., Dimopoulos G. Mosquito immune defenses against Plasmodium infection. Dev. Comp. Immunol. 2009, 34:387-395.
13. Clayton A.M., Cirimotich C.M., Dong Y., Dimopoulos G. Caudal is a negative regulator of the Anopheles IMD pathway that controls resistance to Plasmodium falciparum infection. Dev. Comp. Immunol. 2012, 39:323-332.
14. Danielli A., Barillas-Mury C., Kumar S., Kafatos F.C., Loukeris T.G. Overexpression and altered nucleocytoplasmic distribution of Anopheles ovalbumin-like SRPN10 serpins in Plasmodium-infected midgut cells. Cell Microbiol. 2005, 7:181-190.
15. David J.P., Ismail H.M., Chandor-Proust A., Paine M.J. Role of cytochrome P450s in insecticide resistance: impact on the control of mosquito-borne diseases and use of insecticides on Earth. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368:20120429.
16. de Sousa Abreu R., Penalva L.O., Marcotte E.M., Vogel C. Global signatures of protein and mRNA expression levels. Mol. Biosyst. 2009, 5:1512-1526.
17. Dong Y., Aguilar R., Xi Z., Warr E., Mongin E., Dimopoulos G. Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog. 2006, 2:e52.
18. Dong Y., Das S., Cirimotich C., Souza-Neto J.A., McLean K.J., Dimopoulos G. Engineered anopheles immunity to Plasmodium infection. PLoS Pathog. 2011, 7:e1002458.
19. Dong Y., Manfredini F., Dimopoulos G. Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog. 2009, 5:e1000423.
20. Dong Y., Cirimotich C., Pike A., Chandra R., Dimopoulos G. Anopheles NF-κB -regulated splicing factors direct pathogen-specific repertoires of the hypervariable pattern recognition receptor AgDscam. Cell Host Microbe 2012, 12:521-530.
21. Dudoit S., Gentleman R.C., Quackenbush J. Open source software for the analysis of microarray data. Biotech. Suppl. 2003, 45-51.
22. Franc N.C., Dimarcq J.L., Lagueux M., Hoffmann J., Ezekowitz R.A. Croquemort, a novel Drosophila hemocyte/macrophage receptor that recognizes apoptotic cells. Immunity 1996, 4:431-443.
23. Franc N.C., Heitzler P., Ezekowitz R.A., White K. Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila. Science 1999, 284:1991-1994.
24. Garver L.S., de Almeida Oliveira G., Barillas-Mury C. The JNK pathway is a key mediator of Anopheles gambiae antiplasmodial immunity. PLoS Pathog. 2013, 9:e1003622.
25. Garver L.S., Dong Y., Dimopoulos G. Caspar controls resistance to Plasmodium falciparum in diverse anopheline species. PLoS Pathog. 2009, 5:e1000335.
26. Gedeon T., Bokes P. Delayed protein synthesis reduces the correlation between mRNA and protein fluctuations. Biophys. J. 2012, 103:377-385.
27. Goncalves R.L., Oliveira J.H., Oliveira G.A., Andersen J.F., Oliveira M.F., Oliveira P.L., Barillas-Mury C. Mitochondrial reactive oxygen species modulate mosquito susceptibility to Plasmodium infection. PLoS One 2012, 7:e41083.
28. Guo Y., Singleton P.A., Rowshan A., Gucek M., Cole R.N., Graham D.R., Van Eyk J.E., Garcia J.G. Quantitative proteomics analysis of human endothelial cell membrane rafts: evidence of MARCKS and MRP regulation in the sphingosine 1-phosphate-induced barrier enhancement. Mol. Cell Proteomics 2007, 6:689-696.
29. Han Y.S., Barillas-Mury C. Implications of Time Bomb model of ookinete invasion of midgut cells. Insect Biochem. Mol. Biol. 2002, 32:1311-1316.
30. Hurd H., Grant K.M., Arambage S.C. Apoptosis-like death as a feature of malaria infection in mosquitoes. Parasitology 2006, 132(Suppl.):S33-S47.
31. Imroze K., Prasad N.G. Mating with large males decreases the immune defence of females in Drosophila melanogaster. J.Genet. 2012, 90:427-434.
32. Ioannou Y.A. Niemann-Pick C proteins in sterol transport and absorption: flies in the ointment. Dev. Cell 2007, 12:481-483.
33. Ito J., Ghosh A., Moreira L.A., Wimmer E.A., Jacobs-Lorena M. Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 2002, 417:452-455.
34. Jupatanakul N., Sim S., Dimopoulos G. Aedes aegypti ML and Niemann-Pick type C family members are agonists of dengue virus infection. Dev. Comp. Immunol. 2013, 43:1-9.
35. Ligoxygakis P., Pelte N., Hoffmann J.A., Reichhart J.M. Activation of Drosophila Toll during fungal infection by a blood serine protease. Science 2002, 297:114-116.
36. Ligoxygakis P., Roth S., Reichhart J.M. Aserpin regulates dorsal-ventral axis formation in the Drosophila embryo. Curr. Biol. 2003, 13:2097-2102.
37. Maier T., Guell M., Serrano L. Correlation of mRNA and protein in complex biological samples. FEBS Lett. 2009, 583:3966-3973.
38. Martin B., Brenneman R., Becker K.G., Gucek M., Cole R.N., Maudsley S. iTRAQ analysis of complex proteome alterations in 3xTgAD Alzheimer's mice: understanding the interface between physiology and disease. PLoS One 2008, 3:e2750.
39. McKean K.A., Yourth C.P., Lazzaro B.P., Clark A.G. The evolutionary costs of immunological maintenance and deployment. BMC Evol. Biol. 2008, 8:76.
40. Meister S., Kanzok S.M., Zheng X.L., Luna C., Li T.R., Hoa N.T., Clayton J.R., White K.P., Kafatos F.C., Christophides G.K., Zheng L. Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:11420-11425.
41. Oliveira J.H., Goncalves R.L., Lara F.A., Dias F.A., Gandara A.C., Menna-Barreto R.F., Edwards M.C., Laurindo F.R., Silva-Neto M.A., Sorgine M.H., Oliveira P.L. Blood meal-derived heme decreases ROS levels in the midgut of Aedes aegypti and allows proliferation of intestinal microbiota. PLoS Pathog. 2011, 7:e1001320.
42. Pierce A., Unwin R.D., Evans C.A., Griffiths S., Carney L., Zhang L., Jaworska E., Lee C.F., Blinco D., Okoniewski M.J., Miller C.J., Bitton D.A., Spooncer E., Whetton A.D. Eight-channel iTRAQ enables comparison of the activity of six leukemogenic tyrosine kinases. Mol. Cell Proteomics 2008, 7:853-863.
43. Povelones M., Upton L.M., Sala K.A., Christophides G.K. Structure-function analysis of the Anopheles gambiae LRIM1/APL1C complex and its interaction with complement C3-like protein TEP1. PLoS Pathog. 2011, 7:e1002023.
44. Povelones M., Waterhouse R.M., Kafatos F.C., Christophides G.K. Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites. Science 2009, 324:258-261.
45. Provost-Javier K.N., Chen S., Rasgon J.L. Vitellogenin gene expression in autogenous Culex tarsalis. Insect Mol. Biol. 2010, 19:423-429.
46. Pumpuni C.B., Demaio J., Kent M., Davis J.R., Beier J.C. Bacterial population dynamics in three anopheline species: the impact on Plasmodium sporogonic development. Am. J. Trop. Med. Hyg. 1996, 54:214-218.
47. Riehle M.M., Xu J., Lazzaro B.P., Rottschaefer S.M., Coulibaly B., Sacko M., Niare O., Morlais I., Traore S.F., Vernick K.D. Anopheles gambiae APL1 is a family of variable LRR proteins required for Rel1-mediated protection from the malaria parasite, Plasmodium berghei. PLoS One 2008, 3:e3672.
48. Riordan J.F. Angiotensin-I-converting enzyme and its relatives. Genome Biol. 2003, 4:225.
49. Ross P.L., Huang Y.N., Marchese J.N., Williamson B., Parker K., Hattan S., Khainovski N., Pillai S., Dey S., Daniels S., Purkayastha S., Juhasz P., Martin S., Bartlet-Jones M., He F., Jacobson A., Pappin D.J. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell Proteomics 2004, 3:1154-1169.
50. Straif S.C., Mbogo C.N., Toure A.M., Walker E.D., Kaufman M., Toure Y.T., Beier J.C. Midgut bacteria in Anopheles gambiae and An. funestus (Diptera: Culicidae) from Kenya and Mali. J.Med. Entomol. 1998, 35:222-226.
51. Vogel C., Marcotte E.M. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 2012, 13:227-232.
52. Volz J., Osta M.A., Kafatos F.C., Muller H.M. The roles of two clip domain serine proteases in innate immune responses of the malaria vector Anopheles gambiae. J.Biol. Chem. 2005, 280:40161-40168.
53. Weber A.N., Tauszig-Delamasure S., Hoffmann J.A., Lelievre E., Gascan H., Ray K.P., Morse M.A., Imler J.L., Gay N.J. Binding of the Drosophila cytokine Spatzle to Toll is direct and establishes signaling. Nat. Immunol. 2003, 4:794-800.
54. Xi Z., Ramirez J.L., Dimopoulos G. The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog. 2008, 4:e1000098.
55. Yang Y.J., Davies D.M. Trypsin and chymotrypsin during metamorphosis in Aedes aegypti and properties of the chymotrypsin. J.Insect Physiol. 1971, 17:117-131.
56. Ye T., Zhang X. Involvement of Ran in the regulation of phagocytosis against virus infection in S2 cells. Dev. Comp. Immunol. 2013, 41:491-497.
57. You L., Yin J. Patterns of regulation from mRNA and protein time series. Metab. Eng. 2000, 2:210-217.
58. Zerofsky M., Harel E., Silverman N., Tatar M. Aging of the innate immune response in Drosophila melanogaster. Aging Cell 2005, 4:103-108.
59. Zou Z., Souza-Neto J., Xi Z., Kokoza V., Shin S.W., Dimopoulos G., Raikhel A. Transcriptome analysis of Aedes aegypti transgenic mosquitoes with altered immunity. PLoS Pathog. 2011, 7:e1002394.