Gene expression changes in the salivary glands of Anopheles coluzzii elicited by Plasmodium berghei infection
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
26395987
PubMed Central
PMC4580310
DOI
10.1186/s13071-015-1079-8
PII: 10.1186/s13071-015-1079-8
Knihovny.cz E-zdroje
- MeSH
- Anopheles fyziologie MeSH
- interakce hostitele a patogenu MeSH
- kvantitativní polymerázová řetězová reakce MeSH
- myši MeSH
- Plasmodium berghei růst a vývoj MeSH
- proteiny usnadňující transport glukosy antagonisté a inhibitory MeSH
- receptory buněčného povrchu antagonisté a inhibitory MeSH
- sekvenční analýza RNA MeSH
- slinné žlázy parazitologie MeSH
- stanovení celkové genové exprese * MeSH
- umlčování genů MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- proteiny usnadňující transport glukosy MeSH
- receptory buněčného povrchu MeSH
BACKGROUND: Malaria is a devastating infectious disease caused by Plasmodium parasites transmitted through the bites of infected Anopheles mosquitoes. Salivary glands are the only mosquito tissue invaded by Plasmodium sporozoites, being a key stage for the effective parasite transmission, making the study of Anopheles sialome highly relevant. METHODS: RNA-sequencing was used to compare differential gene expression in salivary glands of uninfected and Plasmodium berghei-infected Anopheles coluzzii mosquitoes. RNA-seq results were validated by quantitative RT-PCR. The transmembrane glucose transporter gene AGAP007752 was selected for functional analysis by RNA interference. The effect of gene silencing on infection level was evaluated. The putative function and tertiary structure of the protein was assessed. RESULTS: RNA-seq data showed that 2588 genes were differentially expressed in mosquitoes salivary glands in response to P. berghei infection, being 1578 upregulated and 1010 downregulated. Metabolism, Immunity, Replication/Transcription/Translation, Proteolysis and Transport were the mosquito gene functional classes more affected by parasite infection. Endopeptidase coding genes were the most abundant within the differentially expressed genes in infected salivary glands (P < 0.001). Based on its putative function and expression level, the transmembrane glucose transporter gene, AGAP007752, was selected for functional analysis by RNA interference. The results demonstrated that the number of sporozoites was 44.3% lower in mosquitoes fed on infected mice after AGAPP007752 gene knockdown when compared to control (P < 0.01). CONCLUSIONS: Our hypothesis is that the protein encoded by the gene AGAPP007752 may play a role on An. coluzzii salivary glands infection by Plasmodium parasite, working as a sporozoite receptor and/or promoting a favorable environment for the capacity of sporozoites.
Center for Infection and Immunity of Lille Institut Pasteur de Lille Lille France
Global Health and Tropical Medicine Lisbon Portugal
Instituto de Higiene e Medicina Tropical Lisbon Portugal
SaBio Instituto de Investigación de Recursos Cinegéticos IREC CSIC UCLM JCCM Ciudad Real Spain
Unidade de Biofísica e Expressão Genética Instituto de Medicina Molecular Lisbon Portugal
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WHO (World Health Organization). Fact sheet N°94 Updated December 2013. http://www.who.int/malaria/publications/world_malaria_report_2013/en/. Acessed 10 Ago 2015.
Ghosh AK, Devenport M, Jethwaney D, Kalume DE, Pandey A, Vernon E, et al. Malaria Parasite Invasion of the Mosquito Salivary Gland Requires Interaction between the Plasmodium TRAP and the Anopheles Saglin Proteins. PloS Pathog. 2009;1 doi: 10.1371/journal.ppat.1000265. PubMed DOI PMC
Kappe SH, Gardner MJ, Brown SM, Ross J, Matuschewski K, Ribeiro JM, et al. Exploring the transcriptome of the malaria sporozoite stage. Proc Natl Acad Sci U S A. 2001;98:9895–9900. doi: 10.1073/pnas.171185198. PubMed DOI PMC
Mueller A-K, Kohlhepp F, Hammerschmidt C, Michel K. Invasion of mosquito salivary glands by malaria parasites: Prerequisites and defense strategies. Int J Parasitol. 2011;40:1229–1235. doi: 10.1016/j.ijpara.2010.05.005. PubMed DOI PMC
Brennan JD, Kent M, Dhar R, Fujioka H, Kumar N. Anopheles gambiae salivary gland proteins as putative targets for blocking transmission of malaria parasites. Proc Natl Acad Sci U S A. 2000;97:13859–64. doi: 10.1073/pnas.250472597. PubMed DOI PMC
Dinglasan RR, Valenzuela JG, Azad AF. Sugar epitopes as potential universal disease transmission blocking targets. Insect Biochem Mol Biol. 2005;35:1–10. doi: 10.1016/j.ibmb.2004.09.005. PubMed DOI
Zieler H, Nawrocki JP, Shahabuddin M. Plasmodium gallinaceum ookinetes adhere specifically to the midgut epithelium of Aedes aegypti by interaction with a carbohydrate ligand. J Exp Biol. 1999;202(Pt 5):485–95. PubMed
Liu K, Dong Y, Huang Y, Rasgon JL, Agre P. Impact of trehalose transporter knockdown on Anopheles gambiae stress adaptation and susceptibility to Plasmodium falciparum infection. Proc Natl Acad Sci U S A. 2013;110:17504–9. doi: 10.1073/pnas.1316709110. PubMed DOI PMC
Basseri HR, Doosti S, Akbarzadeh K, Nateghpour M, Whitten MM, Ladoni H. Competency of Anopheles stephensi mysorensis strain for Plasmodium vivax and the role of inhibitory carbohydrates to block its sporogonic cycle. Malar J. 2008;7:131. doi: 10.1186/1475-2875-7-131. PubMed DOI PMC
Wilhelm BT, Landry J-R. RNA-Seq-quantitative measurement of expression through massively parallel RNA-sequencing. Methods. 2009;48:249–57. doi: 10.1016/j.ymeth.2009.03.016. PubMed DOI
Crawford JE, Guelbeogo WM, Sanou A, Traoré A, Vernick KD, Sagnon N, et al. De novo transcriptome sequencing in Anopheles funestus using Illumina RNA-seq technology. PLoS One. 2010;5:e14202. doi: 10.1371/journal.pone.0014202. PubMed DOI PMC
Bonizzoni M, Afrane Y, Dunn WA, Atieli FK, Zhou G, Zhong D, et al. Comparative transcriptome analyses of deltamethrin-resistant and -susceptible Anopheles gambiae mosquitoes from Kenya by RNA-Seq. PLoS One. 2012;7:e44607. doi: 10.1371/journal.pone.0044607. PubMed DOI PMC
Antunes S, Galindo RC, Almazán C, Rudenko N, Golovchenko M, Grubhoffer L, et al. Functional genomics studies of Rhipicephalus (Boophilus) annulatus ticks in response to infection with the cattle protozoan parasite, Babesia bigemina. Int J Parasitol. 2012;42:187–95. doi: 10.1016/j.ijpara.2011.12.003. PubMed DOI
Deng Y, Wang CC, Choy KW, Du Q, Chen J, Wang Q, Li L, Chung TK, Tang T. Therapeutic potentials of gene silencing by RNA interference: Principles, challenges, and new strategies. Gene. 2014;217–27. PubMed
Blandin S, Shiao S-H, Moita LF, Janse CJ, Waters AP, Kafatos FC, et al. Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell. 2004;116:661–70. doi: 10.1016/S0092-8674(04)00173-4. PubMed DOI
Osta MA, Christophides GK, Kafatos FC. Effects of mosquito genes on Plasmodium development. Science. 2004;303:2030–2. doi: 10.1126/science.1091789. PubMed DOI
Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, et al. The genome sequence of the malaria mosquito Anopheles gambiae. Science. 2002;298:129–49. doi: 10.1126/science.1076181. PubMed DOI
Nene V, et al. Europe PMC Funders Group Genome sequence of Aedes aegypti, a major arbovirus vector. Science. 2007;316:1718–1723. doi: 10.1126/science.1138878. PubMed DOI PMC
Arcà B, Lombardo F, Valenzuela JG, Francischetti IMB, Marinotti O, Coluzzi M, et al. An updated catalogue of salivary gland transcripts in the adult female mosquito, Anopheles gambiae. J Exp Biol. 2005;208(Pt 20):3971–86. doi: 10.1242/jeb.01849. PubMed DOI
Calvo E, Dao A, Phan V, Ribeiro J. An insight into the sialome of Anopheles funestus reveals an emerging pattern in anopheline salivary protein families. Insect Biochem Mol Biol. 2007;37:164–175. doi: 10.1016/j.ibmb.2006.11.005. PubMed DOI PMC
Calvo E, Andersen J, Franscischetti A, de Capurro M, DeBianchi A, James A, et al. The transcriptome of adult female Anopheles darlingi salivary glands. Insect Mol Biol. 2004;13:73–88. doi: 10.1111/j.1365-2583.2004.00463.x. PubMed DOI
Ribeiro JMC. A catalogue of Anopheles gambiae transcripts significantly more or less expressed following a blood meal. Insect Biochem Mol Biol. 2003;33:865–882. doi: 10.1016/S0965-1748(03)00080-8. PubMed DOI
Valenzuela JG, Francischetti IMB, Pham VM, Garfield MK, Ribeiro JMC. Exploring the salivary gland transcriptome and proteome of the Anopheles stephensi mosquito. Insect Biochem Mol Biol. 2003;33:717–732. doi: 10.1016/S0965-1748(03)00067-5. PubMed DOI
Fontaine A, Fusaï T, Briolant S, Buffet S, Villard C, Baudelet E, et al. Anopheles salivary gland proteomes from major malaria vectors. BMC Genomics. 2012;13:614. doi: 10.1186/1471-2164-13-614. PubMed DOI PMC
Pinto SB, Kafatos FC, Michel K. The parasite invasion marker SRPN6 reduces sporozoite numbers in salivary glands of Anopheles gambiae. Cell Microbiol. 2008;10:891–8. doi: 10.1111/j.1462-5822.2007.01091.x. PubMed DOI
Chertemps T, Mitri C, Perrot S, Sautereau J, Jacques J-C, Thiery I, et al. Anopheles gambiae PRS1 modulates Plasmodium development at both midgut and salivary gland steps. PLoS One. 2010;5:e11538. doi: 10.1371/journal.pone.0011538. PubMed DOI PMC
Rodrigues J, Oliveira GA, Kotsyfakis M, Dixit R, Molina-Cruz A, Jochim R, et al. An epithelial serine protease, AgESP, is required for Plasmodium invasion in the mosquito Anopheles gambiae. PLoS One. 2012;7:e35210. doi: 10.1371/journal.pone.0035210. PubMed DOI PMC
Sokhna C, Ndiath MO, Rogier C. The changes in mosquito vector behaviour and the emerging resistance to insecticides will challenge the decline of malaria. Clin Microbiol Infect. 2013;19:902–7. doi: 10.1111/1469-0691.12314. PubMed DOI
Moreno-Cid JA, Pérez de la Lastra JM, Villar M, Jiménez M, Pinal R, Estrada-Peña A, et al. Control of multiple arthropod vector infestations with subolesin/akirin vaccines. Vaccine. 2013;31:1187–96. doi: 10.1016/j.vaccine.2012.12.073. PubMed DOI
De la Fuente J, Moreno-Cid JA, Galindo RC, Almazan C, Kocan KM, Merino O, et al. Subolesin/Akirin vaccines for the control of arthropod vectors and vectorborne pathogens. Transbound Emerg Dis. 2013;60(Suppl 2):172–8. doi: 10.1111/tbed.12146. PubMed DOI
Armada A, Gazarini ML, Gonçalves LM, Antunes S, Custódio A, Rodrigues A, et al. Generation of an antibody that recognizes Plasmodium chabaudi cysteine protease (chabaupain-1) in both sexual and asexual parasite life cycle and evaluation of chabaupain-1 vaccine potential. Exp Parasitol. 2013;135:166–74. doi: 10.1016/j.exppara.2013.06.009. PubMed DOI
Canales M, Ballesteros C, Moreno-Cid JA, Espinosa AM, Villar M, de la Fuente J. Extractive bioconversion to produce the Aedes albopictus akirin in an aqueous two-phase system supporting Pichia pastoris growth and protein secretion. Biochem Eng J. 2009;46:105–114. doi: 10.1016/j.bej.2009.04.014. DOI
De la Fuente J, Moreno-Cid JA, Canales M, Villar M, de la Lastra JMP, Kocan KM, et al. Targeting arthropod subolesin/akirin for the development of a universal vaccine for control of vector infestations and pathogen transmission. Vet Parasitol. 2011;181:17–22. doi: 10.1016/j.vetpar.2011.04.018. PubMed DOI
Janse C, Franke-Fayard B, Mair G, Ramesar J, Thiel C, Engelmann S, et al. High efficiency transfection of Plasmodium berghei facilitates novel selection procedures. Mol Biochem Parasitol. 2006;145:60–70. doi: 10.1016/j.molbiopara.2005.09.007. PubMed DOI
Ayllón N, Villar M, Galindo RC, Kocan KM, Šíma R, López JA, et al. Systems Biology of Tissue-Specific Response to Anaplasma phagocytophilum Reveals Differentiated Apoptosis in the Tick Vector Ixodes scapularis. PLOS Genet. 2015;11:e1005120. doi: 10.1371/journal.pgen.1005120. PubMed DOI PMC
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008;5:621–628. doi: 10.1038/nmeth.1226. PubMed DOI
Lee J, Ji Y, Liang S, Cai G, Müller P. On differential gene expression using RNA-Seq data. Cancer Inform. 2011;10:205–15. PubMed PMC
Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, et al. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 2007;35(Web Server issue):W585–7. doi: 10.1093/nar/gkm259. PubMed DOI PMC
Blum T, Briesemeister S, Kohlbacher O. MultiLoc2: integrating phylogeny and Gene Ontology terms improves subcellular protein localization prediction. BMC Bioinformatics. 2009;10:274. doi: 10.1186/1471-2105-10-274. PubMed DOI PMC
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods. 2001;25:402–8. doi: 10.1006/meth.2001.1262. PubMed DOI
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7. doi: 10.1093/nar/gkh340. PubMed DOI PMC
Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–52. doi: 10.1093/oxfordjournals.molbev.a026334. PubMed DOI
Anisimova M, Gascuel O. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol. 2006;55:539–52. doi: 10.1080/10635150600755453. PubMed DOI
Guindon S, Gascuel O. A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood. Syst Biol. 2003;52:696–704. doi: 10.1080/10635150390235520. PubMed DOI
Chevenet F, Brun C, Bañuls A-L, Jacq B, Christen R. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics. 2006;7:439. doi: 10.1186/1471-2105-7-439. PubMed DOI PMC
Cheng J, Baldi P. A machine learning information retrieval approach to protein fold recognition. Bioinformatics. 2006;22:1456–63. doi: 10.1093/bioinformatics/btl102. PubMed DOI
Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics. 2008;9:40. doi: 10.1186/1471-2105-9-40. PubMed DOI PMC
Vallat BK, Pillardy J, Májek P, Meller J, Cao B, Elber R. Building and assessing atomic models of proteins from structural templates: Learning and benchmarks. Proteins. 2010;76:930–945. doi: 10.1002/prot.22401. PubMed DOI PMC
Raman S, Vernon R, Thompson J, Tyka M, Pei J, Kim D, et al. Structure prediction for CASP8 with all-atom refinement using Rosetta. Proteins. 2009;77:89–99. doi: 10.1002/prot.22540. PubMed DOI PMC
Kelley LA, Sternberg MJE. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc. 2009;4:363–71. doi: 10.1038/nprot.2009.2. PubMed DOI
Arnold K, Bordoli L, Kopp J, Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics. 2006;22:195–201. doi: 10.1093/bioinformatics/bti770. PubMed DOI
Berjanskii M, Zhou J, Liang Y, Lin G, Wishart DS. Resolution-by-proxy: a simple measure for assessing and comparing the overall quality of NMR protein structures. J Biomol NMR. 2012;53:167–80. doi: 10.1007/s10858-012-9637-2. PubMed DOI
Benkert P, Künzli M, Schwede T. QMEAN server for protein model quality estimation. Nucleic Acids Res. 2009;37(Web Server issue):W510–4. doi: 10.1093/nar/gkp322. PubMed DOI PMC
McGuffin LJ, Buenavista MT, Roche DB. The ModFOLD4 server for the quality assessment of 3D protein models. Nucleic Acids Res. 2013;41(Web Server issue):W368–72. doi: 10.1093/nar/gkt294. PubMed DOI PMC
Li X, Jacobson MP, Zhu K, Zhao S, Friesner RA. Assignment of Polar States for Protein Amino Acid Residues Using an Interaction Cluster Decomposition Algorithm and its Application to High Resolution Protein Structure Modeling. Proteins Struct Funct Bioinforma. 2007;837(December 2006):824–37. PubMed
Padrón A, Molina-Cruz A, Quinones M, Ribeiro JMC, Ramphul U, Rodrigues J, et al. In depth annotation of the Anopheles gambiae mosquito midgut transcriptome. BMC Genomics. 2014;15:636. doi: 10.1186/1471-2164-15-636. PubMed DOI PMC
Martínez-Barnetche J, Gómez-Barreto RE, Ovilla-Muñoz M, Téllez-Sosa J, García López DE, Dinglasan RR, et al. Transcriptome of the adult female malaria mosquito vector Anopheles albimanus. BMC Genomics. 2012;13:207. doi: 10.1186/1471-2164-13-207. PubMed DOI PMC
Akbari OS, Antoshechkin I, Amrhein H, Williams B, Diloreto R, Sandler J, et al. The developmental transcriptome of the mosquito Aedes aegypti, an invasive species and major arbovirus vector. G3 (Bethesda) 2013;3:1493–509. doi: 10.1534/g3.113.006742. PubMed DOI PMC
Rosinski-Chupin I, Briolay J, Brouilly P, Perrot S, Gomez SM, Chertemps T, et al. SAGE analysis of mosquito salivary gland transcriptomes during Plasmodium invasion. Cell Microbiol. 2007;9:708–24. doi: 10.1111/j.1462-5822.2006.00822.x. PubMed DOI
Dixit R, Sharma A, Mourya DT, Kamaraju R, Patole MS, Shouche YS. Salivary gland transcriptome analysis during Plasmodium infection in malaria vector Anopheles stephensi. Int J Infect Dis. 2009;13:636–46. doi: 10.1016/j.ijid.2008.07.027. PubMed DOI
Waisberg M, Molina-Cruz A, Mizurini DM, Gera N, Sousa BC, Ma D, et al. Plasmodium falciparum Infection Induces Expression of a Mosquito Salivary Protein (Agaphelin) That Targets Neutrophil Function and Inhibits Thrombosis without Impairing Hemostasis. PLoS Pathog. 2014;10:e1004338. doi: 10.1371/journal.ppat.1004338. PubMed DOI PMC
Povelones M, Bhagavatula L, Yassine H, Tan LA, Upton LM, Osta MA, et al. The CLIP-domain serine protease homolog SPCLIP1 regulates complement recruitment to microbial surfaces in the malaria mosquito Anopheles gambiae. PLoS Pathog. 2013;9:e1003623. doi: 10.1371/journal.ppat.1003623. PubMed DOI PMC
Baxter RHG, Steinert S, Chelliah Y, Volohonsky G, Levashina EA, Deisenhofer J. A heterodimeric complex of the LRR proteins LRIM1 and APL1C regulates complement-like immunity in Anopheles gambiae. Proc Natl Acad Sci U S A. 2010;107:16817–22. doi: 10.1073/pnas.1010575107. PubMed DOI PMC
Povelones M, Upton LM, Sala KA, Christophides GK. Structure-function analysis of the Anopheles gambiae LRIM1/APL1C complex and its interaction with complement C3-like protein TEP1. PLoS Pathog. 2011;7:e1002023. doi: 10.1371/journal.ppat.1002023. PubMed DOI PMC
Le BV, Williams M, Logarajah S, Baxter RHG. Molecular basis for genetic resistance of Anopheles gambiae to Plasmodium: structural analysis of TEP1 susceptible and resistant alleles. PLoS Pathog. 2012;8:e1002958. doi: 10.1371/journal.ppat.1002958. PubMed DOI PMC
Dong Y, Taylor HE, Dimopoulos G. AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol. 2006;4:e229. doi: 10.1371/journal.pbio.0040229. PubMed DOI PMC
Lambrechts L, Vulule JM, Koella JC. Genetic correlation between melanization and antibacterial immune responses in a natural population of the malaria vector Anopheles gambiae. Evolution. 2004;58:2377–81. doi: 10.1111/j.0014-3820.2004.tb01611.x. PubMed DOI
Garver LS, Bahia AC, Das S, Souza-Neto JA, Shiao J, Dong Y, et al. Anopheles Imd Pathway Factors and Effectors in Infection Intensity-Dependent Anti-Plasmodium Action. PloS Pathog. 2012;8:7–9. doi: 10.1371/journal.ppat.1002737. PubMed DOI PMC
Yamazaki Y, Morita T. Structure and function of snake venom cysteine-rich secretory proteins. Toxicon. 2004;44:227–231. doi: 10.1016/j.toxicon.2004.05.023. PubMed DOI
Goulielmaki E, Siden-Kiamos I, Loukeris T. Functional characterization of Anopheles matrix metalloprotease 1 reveals its agonistic role during sporogonic development of malaria parasites. Infect Immun. 2014;82:4865–77. doi: 10.1128/IAI.02080-14. PubMed DOI PMC
Das S, Radtke A, Choi Y-J, Mendes AM, Valenzuela JG, Dimopoulos G. Transcriptomic and functional analysis of the Anopheles gambiae salivary gland in relation to blood feeding. BMC Genomics. 2010;11:566. doi: 10.1186/1471-2164-11-566. PubMed DOI PMC
Baker DA, Nolan T, Fischer B, Pinder A, Crisanti A, Russell S. A comprehensive gene expression atlas of sex- and tissue-specificity in the malaria vector, Anopheles gambiae. BMC Genomics. 2011;12:1–12. doi: 10.1186/1471-2164-12-296. PubMed DOI PMC
Aguilar R, Jedlicka AE, Mintz M, Mahairaki V, Scott AL, Dimopoulos G. Global gene expression analysis of Anopheles gambiae responses to microbial challenge. Insect Biochem Mol Biol. 2005;35:709–19. doi: 10.1016/j.ibmb.2005.02.019. PubMed DOI
Conway MJ, Watson AM, Colpitts TM, Dragovic SM, Li Z, Wang P, et al. Mosquito saliva serine protease enhances dissemination of dengue virus into the mammalian host. J Virol. 2014;88:164–75. doi: 10.1128/JVI.02235-13. PubMed DOI PMC
Sim S, Ramirez JL, Dimopoulos G. Dengue virus infection of the Aedes aegypti salivary gland and chemosensory apparatus induces genes that modulate infection and blood-feeding behavior. PLoS Pathog. 2012;8:e1002631. doi: 10.1371/journal.ppat.1002631. PubMed DOI PMC
Marquez AG, Pietri JE, Smithers HM, Nuss A, Antonova Y, Drexler AL, et al. Insulin-like peptides in the mosquito Anopheles stephensi: Identification and expression in response to diet and infection with Plasmodium falciparum. Gen Comp Endocrinol. 2011;173:303–312. doi: 10.1016/j.ygcen.2011.06.005. PubMed DOI PMC
Teets NM, Peyton JT, Colinet H, Renault D, Kelley JL, Kawarasaki Y, et al. Gene expression changes governing extreme dehydration tolerance in an Antarctic insect. Proc Natl Acad Sci U S A. 2012;109:20744–9. doi: 10.1073/pnas.1218661109. PubMed DOI PMC
Luckhart S, Vodovotz Y, Cui L, Rosenberg R. The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc Natl Acad Sci U S A. 1998;95:5700–5705. doi: 10.1073/pnas.95.10.5700. PubMed DOI PMC
Peterson TML, Gow AJ, Luckhart S. Malaria Parasite Infection. Free Radic Biol Med. 2007;42:132–142. doi: 10.1016/j.freeradbiomed.2006.10.037. PubMed DOI PMC
Lim J, Gowda DC, Luckhart S, Krishnegowda G. Induction of nitric oxide synthase in Anopheles stephensi by Plasmodium falciparum: mechanism of signaling and the role of parasite Glycosylphosphatidylinositols Induction of Nitric Oxide Synthase in Anopheles stephensi by Plasmodium falciparum : Mechanis. Infect Immun. 2005;73:2778–2789. doi: 10.1128/IAI.73.5.2778-2789.2005. PubMed DOI PMC
Mead EA, Li M, Tu Z, Zhu J. Translational regulation of Anopheles gambiae mRNAs in the midgut during Plasmodium falciparum infection. BMC Genomics. 2012;13:366. doi: 10.1186/1471-2164-13-366. PubMed DOI PMC
Baton LA, Robertson A, Warr E, Strand MR, Dimopoulos G. Genome-wide transcriptomic profiling of Anopheles gambiae hemocytes reveals pathogen-specific signatures upon bacterial challenge and Plasmodium berghei infection. BMC Genomics. 2009;10:257. doi: 10.1186/1471-2164-10-257. PubMed DOI PMC
Dimopoulos G, Christophides GK, Meister S, Schultz J, White KP, Barillas-Mury C, et al. Genome expression analysis of Anopheles gambiae: responses to injury, bacterial challenge, and malaria infection. Proc Natl Acad Sci U S A. 2002;99:8814–9. doi: 10.1073/pnas.092274999. PubMed DOI PMC
Kumar S, Christophides GK, Cantera R, Charles B, Han YS, Meister S, et al. The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proc Natl Acad Sci U S A. 2003;100:14139–14144. doi: 10.1073/pnas.2036262100. PubMed DOI PMC
Deng Y, Yan H, Gu J, Xu J, Wu K, Tu Z, et al. Molecular and Functional Characterization of Odorant-Binding Protein Genes in an Invasive Vector Mosquito. Aedes albopictus. PLoS One. 2013;8(7) doi: 10.1371/journal.pone.0068836. PubMed DOI PMC
Calvo E, Mans BJ, Andersen JF, Ribeiro JMC. Function and evolution of a mosquito salivary protein family. J Biol Chem. 2006;281:1935–1942. doi: 10.1074/jbc.M510359200. PubMed DOI
Drame PM, Poinsignon A, Besnard P, Cornelie S, le Mire J, Toto JC, et al. Human antibody responses to the Anopheles salivary gSG6-P1 peptide: A novel tool for evaluating the efficacy of ITNs in malaria vector control. PLoS One. 2010;5:1–8. doi: 10.1371/journal.pone.0015596. PubMed DOI PMC
King JG, Vernicks KD, Hillyer JF. Members of the salivary gland surface protein (SGS) family are major immunogenic components of mosquito saliva. J Biol Chem. 2011;286:40824–40834. doi: 10.1074/jbc.M111.280552. PubMed DOI PMC
Sun L, Zeng X, Yan C, Sun X, Gong X, Rao Y, et al. Crystal structure of a bacterial homologue of glucose transporters GLUT1-4. Nature. 2012;490:361–6. doi: 10.1038/nature11524. PubMed DOI
Overend G. Drosophila as a model for the Anopheles Malpighian tubule. PhD thesis. University of Glasgow; 2010.
Zollner GE, Ponsa N, Garman GW, Poudel S, Bell JA, Sattabongkot J, et al. Population dynamics of sporogony for Plasmodium vivax parasites from western Thailand developing within three species of colonized Anopheles mosquitoes. Malar J. 2006;5:68. doi: 10.1186/1475-2875-5-68. PubMed DOI PMC
Sato Y, Montagna GN, Matuschewski K. Plasmodium berghei sporozoites acquire virulence and immunogenicity during mosquito hemocoel transit. Infect Immun. 2014;82:1164–72. doi: 10.1128/IAI.00758-13. PubMed DOI PMC
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402. doi: 10.1093/nar/25.17.3389. PubMed DOI PMC
Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, et al. The Pfam protein families database. Nucleic Acids Res. 2002;30:276–80. doi: 10.1093/nar/30.1.276. PubMed DOI PMC
Kanamori Y, Saito A, Hagiwara-Komoda Y, Tanaka D, Mitsumasu K, Kikuta S, et al. The trehalose transporter 1 gene sequence is conserved in insects and encodes proteins with different kinetic properties involved in trehalose import into peripheral tissues. Insect Biochem Mol Biol. 2010;40:30–7. doi: 10.1016/j.ibmb.2009.12.006. PubMed DOI
Joost HG, Thorens B. The extended GLUT-family of sugar/polyol transport facilitators: nomenclature, sequence characteristics, and potential function of its novel members (review) Mol Membr Biol. 2001;18:247–56. doi: 10.1080/09687680110090456. PubMed DOI
Joost H, Bell GI, Best JD, Birnbaum MJ, Charron MJ, Chen YT, et al. Nomenclature of the GLUT/SLC2A family of sugar/polyol transport facilitators. Am J Physiol Endocrionl Metab. 2002;282:E974–E976. doi: 10.1152/ajpendo.00407.2001. PubMed DOI
Uldry M, Thorens B. The SLC2 family of facilitated hexose and polyol transporters. Pflugers Arch. 2004;447:480–9. doi: 10.1007/s00424-003-1085-0. PubMed DOI
Kikuta S, Kikawada T, Hagiwara-Komoda Y, Nakashima N, Noda H. Sugar transporter genes of the brown planthopper, Nilaparvata lugens: A facilitated glucose/fructose transporter. Insect Biochem Mol Biol. 2010;40:805–13. doi: 10.1016/j.ibmb.2010.07.008. PubMed DOI
Moller S, Croning M, Apweiler R. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics. 2001;17:646–653. doi: 10.1093/bioinformatics/17.7.646. PubMed DOI
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