Response of the Mosquito Protein Interaction Network to Dengue Infection

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2010 Jun 18

PMID 20553610

Citations 28

Authors

Xiang Guo

Yao Xu

Guowu Bian

Andrew D Pike

Yan Xie

Zhiyong Xi

Affiliations

Soon will be listed here.

Abstract

Background: Two fifths of the world's population is at risk from dengue. The absence of effective drugs and vaccines leaves vector control as the primary intervention tool. Understanding dengue virus (DENV) host interactions is essential for the development of novel control strategies. The availability of genome sequences for both human and mosquito host greatly facilitates genome-wide studies of DENV-host interactions.

Results: We developed the first draft of the mosquito protein interaction network using a computational approach. The weighted network includes 4,214 Aedes aegypti proteins with 10,209 interactions, among which 3,500 proteins are connected into an interconnected scale-free network. We demonstrated the application of this network for the further annotation of mosquito proteins and dissection of pathway crosstalk. Using three datasets based on physical interaction assays, genome-wide RNA interference (RNAi) screens and microarray assays, we identified 714 putative DENV-associated mosquito proteins. An integrated analysis of these proteins in the network highlighted four regions consisting of highly interconnected proteins with closely related functions in each of replication/transcription/translation (RTT), immunity, transport and metabolism. Putative DENV-associated proteins were further selected for validation by RNAi-mediated gene silencing, and dengue viral titer in mosquito midguts was significantly reduced for five out of ten (50.0%) randomly selected genes.

Conclusions: Our results indicate the presence of common host requirements for DENV in mosquitoes and humans. We discuss the significance of our findings for pharmacological intervention and genetic modification of mosquitoes for blocking dengue transmission.

Citing Articles

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References

Ishizuka A, Siomi M, Siomi H . A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev. 2002; 16(19):2497-508. PMC: 187455. DOI: 10.1101/gad.1022002. View

Petersen J, Her L, Varvel V, Lund E, Dahlberg J . The matrix protein of vesicular stomatitis virus inhibits nucleocytoplasmic transport when it is in the nucleus and associated with nuclear pore complexes. Mol Cell Biol. 2000; 20(22):8590-601. PMC: 102164. DOI: 10.1128/MCB.20.22.8590-8601.2000. View

Krishnan M, Ng A, Sukumaran B, Gilfoy F, Uchil P, Sultana H . RNA interference screen for human genes associated with West Nile virus infection. Nature. 2008; 455(7210):242-5. PMC: 3136529. DOI: 10.1038/nature07207. View

Guo X, Liu R, Shriver C, Hu H, Liebman M . Assessing semantic similarity measures for the characterization of human regulatory pathways. Bioinformatics. 2006; 22(8):967-73. DOI: 10.1093/bioinformatics/btl042. View

Chee H, AbuBakar S . Identification of a 48kDa tubulin or tubulin-like C6/36 mosquito cells protein that binds dengue virus 2 using mass spectrometry. Biochem Biophys Res Commun. 2004; 320(1):11-7. DOI: 10.1016/j.bbrc.2004.05.124. View

Foley E, OFarrell P . Functional dissection of an innate immune response by a genome-wide RNAi screen. PLoS Biol. 2004; 2(8):E203. PMC: 434151. DOI: 10.1371/journal.pbio.0020203. View

Garcia-Montalvo B, Medina F, Del Angel R . La protein binds to NS5 and NS3 and to the 5' and 3' ends of Dengue 4 virus RNA. Virus Res. 2004; 102(2):141-50. DOI: 10.1016/j.virusres.2004.01.024. View

Bogachek M, Protopopova E, Loktev V, Zaitsev B, Favre M, Sekatskii S . Immunochemical and single molecule force spectroscopy studies of specific interaction between the laminin binding protein and the West Nile virus surface glycoprotein E domain II. J Mol Recognit. 2007; 21(1):55-62. DOI: 10.1002/jmr.866. View

Hoffmann J . The immune response of Drosophila. Nature. 2003; 426(6962):33-8. DOI: 10.1038/nature02021. View

10.

Ideker T, Lauffenburger D . Building with a scaffold: emerging strategies for high- to low-level cellular modeling. Trends Biotechnol. 2003; 21(6):255-62. DOI: 10.1016/S0167-7799(03)00115-X. View

11.

Chu J, Leong P, Ng M . Characterization of plasma membrane-associated proteins from Aedes albopictus mosquito (C6/36) cells that mediate West Nile virus binding and infection. Virology. 2005; 339(2):249-60. DOI: 10.1016/j.virol.2005.05.026. View

12.

Li S, Armstrong C, Bertin N, Ge H, Milstein S, Boxem M . A map of the interactome network of the metazoan C. elegans. Science. 2004; 303(5657):540-3. PMC: 1698949. DOI: 10.1126/science.1091403. View

13.

Remm M, Storm C, Sonnhammer E . Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J Mol Biol. 2001; 314(5):1041-52. DOI: 10.1006/jmbi.2000.5197. View

14.

Fernandez-Garcia M, Mazzon M, Jacobs M, Amara A . Pathogenesis of flavivirus infections: using and abusing the host cell. Cell Host Microbe. 2009; 5(4):318-28. DOI: 10.1016/j.chom.2009.04.001. View

15.

Sanders H, Foy B, Evans A, Ross L, Beaty B, Olson K . Sindbis virus induces transport processes and alters expression of innate immunity pathway genes in the midgut of the disease vector, Aedes aegypti. Insect Biochem Mol Biol. 2005; 35(11):1293-307. DOI: 10.1016/j.ibmb.2005.07.006. View

16.

Sim C, Hong Y, Tsetsarkin K, Vanlandingham D, Higgs S, Collins F . Anopheles gambiae heat shock protein cognate 70B impedes o'nyong-nyong virus replication. BMC Genomics. 2007; 8:231. PMC: 1963456. DOI: 10.1186/1471-2164-8-231. View

17.

Calderwood M, Venkatesan K, Xing L, Chase M, Vazquez A, Holthaus A . Epstein-Barr virus and virus human protein interaction maps. Proc Natl Acad Sci U S A. 2007; 104(18):7606-11. PMC: 1863443. DOI: 10.1073/pnas.0702332104. View

18.

Nene V, Wortman J, Lawson D, Haas B, Kodira C, Tu Z . Genome sequence of Aedes aegypti, a major arbovirus vector. Science. 2007; 316(5832):1718-23. PMC: 2868357. DOI: 10.1126/science.1138878. View

19.

Lindenbach B, Rice C . Molecular biology of flaviviruses. Adv Virus Res. 2003; 59:23-61. DOI: 10.1016/s0065-3527(03)59002-9. View

20.

Brohee S, van Helden J . Evaluation of clustering algorithms for protein-protein interaction networks. BMC Bioinformatics. 2006; 7:488. PMC: 1637120. DOI: 10.1186/1471-2105-7-488. View