Engineered Aedes aegypti JAK/STAT Pathway-Mediated Immunity to Dengue Virus

PLoS Neglected Tropical Diseases

Volumn 11, Issue 1, 2017, Pages

  Jupatanakul, Natapong ^a,c   Sim, Shuzhen ^a,d   Angleró Rodríguez, Yesseinia I ^a   Souza Neto, Jayme ^a   Das, Suchismita ^a   Poti, Kristin E ^a   Rossi, Shannan L ^b   Bergren, Nicholas ^b   Vasilakis, Nikos ^b   Dimopoulos, George ^a  

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

^b University of Texas Medical Branch School of Medicine   (United States)

^c NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

^d GENOME INSTITUTE OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

JANUS KINASE; STAT PROTEIN; VITELLOGENIN; INSECT PROTEIN;

AEDES AEGYPTI; ARTICLE; CONTROLLED STUDY; DENGUE VIRUS; GENE OVEREXPRESSION; GENE SILENCING; GENETIC ENGINEERING; IMMUNITY; NONHUMAN; PROTEIN INTERACTION; PROTEIN MICROARRAY; SEROTYPE; TRANSCRIPTOMICS; VIRUS INHIBITION; VIRUS TITRATION; AEDES; ANIMAL; DENGUE; FAT PAD; GENETICS; HUMAN; IMMUNOLOGY; INSECT VECTOR; MOUSE; PHYSIOLOGY; TRANSMISSION; VIROLOGY;

AEDES; ANIMALS; DENGUE; DENGUE VIRUS; FAT BODY; GENETIC ENGINEERING; HUMANS; INSECT PROTEINS; INSECT VECTORS; JANUS KINASES; MICE; STAT TRANSCRIPTION FACTORS;

EID: 85012918899     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0005187     Document Type: Article

References (63)

1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, et al. The global distribution and burden of dengue. Nature. 2013;496: 504–507. doi: 10.1038/nature1206023563266
2. Black WC, Bennett KE, Gorrochótegui-Escalante N, Barillas-Mury CV, Fernández-Salas I, de Lourdes Muñoz M, et al. Flavivirus susceptibility in Aedes aegypti. Arch Med Res. 2002;33: 379–388. 12234528
3. Alto BW, Bettinardi D, Temperature and dengue virus infection in mosquitoes: independent effects on the immature and adult stages. Am J Trop Med Hyg. 2013;88: 497–505. doi: 10.4269/ajtmh.12-042123382163
4. Salazar MI, Richardson JH, Sánchez-Vargas I, Olson KE, Beaty BJ, Dengue virus type 2: replication and tropisms in orally infected Aedes aegypti mosquitoes. BMC Microbiol. 2007;7: 9. doi: 10.1186/1471-2180-7-917263893
5. Sim S, Jupatanakul N, Ramirez JL, Kang S, Romero-Vivas CM, Mohammed H, et al. Transcriptomic profiling of diverse Aedes aegypti strains reveals increased basal-level immune activation in dengue virus-refractory populations and identifies novel virus-vector molecular interactions. Plos Neglect Trop D. 2013;7: e2295–e2295.
6. Murdock CC, Paaijmans KP, Cox-Foster D, Read AF, Thomas MB, Rethinking vector immunology: the role of environmental temperature in shaping resistance. Nat Rev Microbiol. 2012;10: 869–876. doi: 10.1038/nrmicro290023147703
7. Tjaden NB, Thomas SM, Fischer D, Beierkuhnlein C, Extrinsic incubation period of dengue: knowledge, backlog, and applications of temperature dependence. Plos Neglect Trop D. 2013;7: e2207.
8. Souza-Neto JA, Sim S, Dimopoulos G, An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. P Natl Acad Sci Usa. 2009;106: 17841–17846.
9. Arbouzova NI, Zeidler MP, JAK/STAT signalling in Drosophila: insights into conserved regulatory and cellular functions. Development. 2006;133: 2605–2616. doi: 10.1242/dev.0241116794031
10. Shuai K, Liu B, Regulation of JAK–STAT signalling in the immune system. Nature Reviews Immunology. Nature Publishing Group; 2003;3: 900–911. doi: 10.1038/nri122614668806
11. Romans P, Tu Z, Ke Z, Hagedorn HH, Analysis of a vitellogenin gene of the mosquito, Aedes aegypti and comparisons to vitellogenins from other organisms. Insect Biochem Mol Biol. 1995;25: 939–958. 7550249
12. Dong Y, Das S, Cirimotich C, Souza-Neto JA, McLean KJ, Dimopoulos G, Engineered Anopheles immunity to Plasmodium infection. PLoS Pathogens. 2011;7: e1002458–. doi: 10.1371/journal.ppat.100245822216006
13. Yoshida S, Shimada Y, Kondoh D, Kouzuma Y, Ghosh AK, Jacobs-Lorena M, et al. Hemolytic C-type lectin CEL-III from sea cucumber expressed in transgenic mosquitoes impairs malaria parasite development. PLoS Pathogens. 2007;3: e192. doi: 10.1371/journal.ppat.003019218159942
14. Kokoza V, Ahmed A, Wimmer EA, Raikhel AS, Efficient transformation of the yellow fever mosquito Aedes aegypti using the piggyBac transposable element vector pBac[3xP3-EGFP afm]. Insect Biochem Mol Biol. 2001;31: 1137–1143. 11583926
15. Xi Z, Ramirez JL, Dimopoulos G, The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathogens. 2008;4: e1000098. doi: 10.1371/journal.ppat.100009818604274
16. Nawa M, Takasaki T, Yamada KI, Akatsuka T, Kurane I, Development of dengue IgM-capture enzyme-linked immunosorbent assay with higher sensitivity using monoclonal detection antibody. Journal of Virological Methods. 2001;92: 65–70. 11164919
17. Yang IV, Chen E, Hasseman JP, Liang W, Frank BC, Wang S, et al. Within the fold: assessing differential expression measures and reproducibility in microarray assays. Genome Biol. 2002;3: research0062.
18. Falcon S, Gentleman R, Using GOstats to test gene lists for GO term association. Bioinformatics. 2007;23: 257–258. doi: 10.1093/bioinformatics/btl56717098774
19. Rivals I, Personnaz L, Taing L, Potier M- C, Enrichment or depletion of a GO category within a class of genes: which test?Bioinformatics. 2007;23: 401–407. doi: 10.1093/bioinformatics/btl63317182697
20. Cirimotich CM, Dong Y, Clayton AM, Sandiford SL, Souza-Neto JA, Mulenga M, et al. Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science. 2011;332: 855–858. doi: 10.1126/science.120161821566196
21. Raikhel AS, Kokoza VA, Zhu J, Martin D, Wang S- F, Li C, et al. Molecular biology of mosquito vitellogenesis: from basic studies to genetic engineering of antipathogen immunity. Insect Biochem Mol Biol. 2002;32: 1275–1286. 12225918
22. Delatte H, Desvars A, Bouétard A, Bord S, Gimonneau G, Vourc'h G, et al. Blood-feeding behavior of Aedes albopictus, a vector of Chikungunya on La Réunion. Vector Borne Zoonotic Dis. 2010;10: 249–258. doi: 10.1089/vbz.2009.002619589060
23. Klowden MJ, Briegel H, Mosquito gonotrophic cycle and multiple feeding potential: contrasts between Anopheles and Aedes (Diptera: Culicidae). Journal of Medical Entomology. 1994;31: 618–622. 7932610
24. Scott TW, Amerasinghe PH, Morrison AC, Lorenz LH, Clark GG, Strickman D, et al. Longitudinal studies of Aedes aegypti (Diptera: Culicidae) in Thailand and Puerto Rico: blood feeding frequency. Journal of Medical Entomology. 2000;37: 89–101. 15218911
25. Dong Y, Morton JC, Ramirez JL, Souza-Neto JA, Dimopoulos G, The entomopathogenic fungus Beauveria bassiana activate toll and JAK-STAT pathway-controlled effector genes and anti-dengue activity in Aedes aegypti. Insect Biochem Mol Biol. 2012;42: 126–132. doi: 10.1016/j.ibmb.2011.11.00522198333
26. Moreira LA, Wang J, Collins FH, Jacobs-Lorena M, Fitness of anopheline mosquitoes expressing transgenes that inhibit Plasmodium development. Genetics. 2004;166: 1337–1341. 15082552
27. Libert S, Chao Y, Chu X, Pletcher SD, Trade-offs between longevity and pathogen resistance in Drosophila melanogaster are mediated by NFkappaB signaling. Aging Cell. 2006;5: 533–543. doi: 10.1111/j.1474-9726.2006.00251.x17129215
28. Nüsslein-Volhard C, Wieschaus E, Mutations affecting segment number and polarity in Drosophila. Nature. 1980;287: 795–801. 6776413
29. Luo H, Asha H, Kockel L, Parke T, Mlodzik M, Dearolf CR, The Drosophila Jak kinase hopscotch is required for multiple developmental processes in the eye. Dev Biol. 1999;213: 432–441. doi: 10.1006/dbio.1999.939010479459
30. Yan R, Small S, Desplan C, Dearolf CR, Darnell JE, Identification of a Stat gene that functions in Drosophila development. Cell. 1996;84: 421–430. 8608596
31. Ihaka R, Gentleman R, R: A Language for Data Analysis and Graphics. Journal of Computational and Graphical Statistics. Taylor & Francis Group; 1996;5: 299–314.
32. Wang Y-H, Hu Y, Xing L-S, Jiang H, Hu S-N, Raikhel AS, et al. A Critical Role for CLSP2 in the Modulation of Antifungal Immune Response in Mosquitoes. PLoS Pathogens. 2015;11: e1004931. doi: 10.1371/journal.ppat.100493126057557
33. Middha S, Wang X, Evolution and potential function of fibrinogen-like domains across twelve Drosophila species. BMC Genomics. 2008;9: 260. doi: 10.1186/1471-2164-9-26018513432
34. Zou Z, Souza-Neto J, Xi Z, Kokoza V, Shin SW, Dimopoulos G, et al. Transcriptome analysis of Aedes aegypti transgenic mosquitoes with altered immunity. PLoS Pathogens. 2011;7: e1002394. doi: 10.1371/journal.ppat.100239422114564
35. Dong Y, Dimopoulos G, Anopheles fibrinogen-related proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. J Biol Chem. 2009;284: 9835–9844. doi: 10.1074/jbc.M80708420019193639
36. Xu D, Yin C, Wang S, Xiao Y, JAK-STAT in lipid metabolism of adipocytes. JAK-STAT. Taylor & Francis; 2014;2: e27203.
37. Richard AJ, Stephens JM, The role of JAK-STAT signaling in adipose tissue function. Biochim Biophys Acta. 2014;1842: 431–439. doi: 10.1016/j.bbadis.2013.05.03023735217
38. Luplertlop N, Surasombatpattana P, Patramool S, Dumas E, Wasinpiyamongkol L, Saune L, et al. Induction of a peptide with activity against a broad spectrum of pathogens in the Aedes aegypti salivary gland, following infection with dengue virus. PLoS Pathogens. Public Library of Science; 2011;7: e1001252. doi: 10.1371/journal.ppat.100125221249175
39. Pan X, Zhou G, Wu J, Bian G, Lu P, Raikhel AS, et al. Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti. P Natl Acad Sci Usa. 2012;109: E23–31.
40. Kang S, Shields AR, Jupatanakul N, Dimopoulos G, Suppressing dengue-2 infection by chemical inhibition of Aedes aegypti host factors. Plos Neglect Trop D. 2014;8: e3084.
41. Perera R, Riley C, Isaac G, Hopf-Jannasch AS, Moore RJ, Weitz KW, et al. Dengue virus infection perturbs lipid homeostasis in infected mosquito cells. PLoS Pathogens. 2012;8: e1002584. doi: 10.1371/journal.ppat.100258422457619
42. Jupatanakul N, Sim S, Dimopoulos G, Aedes aegypti ML and Niemann-Pick type C family members are agonists of dengue virus infection. Developmental and Comparative Immunology. 2014;43: 1–9. doi: 10.1016/j.dci.2013.10.00224135719
43. Scheller N, Mina LB, Galão RP, Chari A, Giménez-Barcons M, Noueiry A, et al. Translation and replication of hepatitis C virus genomic RNA depends on ancient cellular proteins that control mRNA fates. P Natl Acad Sci Usa. 2009;106: 13517–13522.
44. Ariumi Y, Kuroki M, Abe K-I, Dansako H, Ikeda M, Wakita T, et al. DDX3 DEAD-box RNA helicase is required for hepatitis C virus RNA replication. J Virol. 2007;81: 13922–13926. doi: 10.1128/JVI.01517-0717855521
45. Yu SF, Lujan P, Jackson DL, Emerman M, Linial ML, The DEAD-box RNA helicase DDX6 is required for efficient encapsidation of a retroviral genome. PLoS Pathogens. 2011;7: e1002303. doi: 10.1371/journal.ppat.100230322022269
46. Ariumi Y, Multiple functions of DDX3 RNA helicase in gene regulation, tumorigenesis, and viral infection. Front Genet. 2014;5: 423. doi: 10.3389/fgene.2014.0042325538732
47. Li C, Ge L-L, Li P-P, Wang Y, Sun M-X, Huang L, et al. The DEAD-box RNA helicase DDX5 acts as a positive regulator of Japanese encephalitis virus replication by binding to viral 3' UTR. Antiviral Res. 2013;100: 487–499. doi: 10.1016/j.antiviral.2013.09.00224035833
48. Xu C, Min J, Structure and function of WD40 domain proteins. Protein Cell. 2011;2: 202–214. doi: 10.1007/s13238-011-1018-121468892
49. Daly NL, Scanlon MJ, Djordjevic JT, Kroon PA, Smith R, Three-dimensional structure of a cysteine-rich repeat from the low-density lipoprotein receptor. Proc Natl Acad Sci USA. 1995;92: 6334–6338. 7603991
50. Hohenester E, Sasaki T, Timpl R, Crystal structure of a scavenger receptor cysteine-rich domain sheds light on an ancient superfamily. Nat Struct Biol. Nature Publishing Group; 1999;6: 228–232. doi: 10.1038/666910074941
51. Ericksen B, Wu Z, Lu W, Lehrer RI, Antibacterial activity and specificity of the six human alpha-defensins. Antimicrob Agents Chemother. 2005;49: 269–275. doi: 10.1128/AAC.49.1.269-275.200515616305
52. Paradkar PN, Trinidad L, Voysey R, Duchemin J- B, Walker PJ, Secreted Vago restricts West Nile virus infection in Culex mosquito cells by activating the Jak-STAT pathway. Proc Natl Acad Sci USA. 2012;109: 18915–18920. doi: 10.1073/pnas.120523110923027947
53. 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. Nat Immunol. 2005;6: 946–953. doi: 10.1038/ni123716086017
54. Morin-Poulard I, Vincent A, Crozatier M, The Drosophila JAK-STAT pathway in blood cell formation and immunity. JAK-STAT. 2014;2: e25700.
55. Ivashkiv LB, Donlin LT, Regulation of type I interferon responses. Nature Reviews Immunology. 2014;14: 36–49. doi: 10.1038/nri358124362405
56. Chakrabarti S, Dudzic JP, Li X, Collas EJ, Boquete J-P, Lemaitre B, Remote Control of Intestinal Stem Cell Activity by Haemocytes in Drosophila. PLoS Genet. 2016;12: e1006089. doi: 10.1371/journal.pgen.100608927231872
57. Molina-Cruz A, Gupta L, Richardson J, Bennett K, Black W, Barillas-Mury C, Effect of mosquito midgut trypsin activity on dengue-2 virus infection and dissemination in Aedes aegypti. Am J Trop Med Hyg. 2005;72: 631–637. 15891140
58. Kambris Z, Cook PE, Phuc HK, Sinkins SP, Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science. 2009;326: 134–136. doi: 10.1126/science.117753119797660
59. Radek JT, Dyer DH, Lan Q, Effects of mutations in Aedes aegypti sterol carrier protein-2 on the biological function of the protein. Biochemistry. 2010;49: 7532–7541. doi: 10.1021/bi902026v20681612
60. Fu Q, Inankur B, Yin J, Striker R, Lan Q, Sterol Carrier Protein 2, a Critical Host Factor for Dengue Virus Infection, Alters the Cholesterol Distribution in Mosquito Aag2 Cells. Journal of Medical Entomology. 2015;: tjv101.
61. McFarlane M, Arias-Goeta C, Martin E, O'Hara Z, Lulla A, Mousson L, et al. Characterization of Aedes aegypti Innate-Immune Pathways that Limit Chikungunya Virus Replication. Plos Neglect Trop D. 2014;8: e2994.
62. Hammond A, Galizi R, Kyrou K, Simoni A, Siniscalchi C, Katsanos D, et al. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nat Biotechnol. 2016;34: 78–83. doi: 10.1038/nbt.343926641531
63. Gantz VM, Jasinskiene N, Tatarenkova O, Fazekas A, Macias VM, Bier E, et al. Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. P Natl Acad Sci Usa. 2015;112: E6736–43.