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Rapid Evolution of Mosquito Anti-viral ncRNA Pathway Components

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Non-coding RNAs and Inter-kingdom Communication

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Abstract

Vector-host non-coding RNA (ncRNA) interactions are important for the maintenance of arthropod-borne virus (arbovirus) infection cycles in nature. A major anti-viral pathway in mosquitoes is the RNA interference (RNAi) pathway. Using high throughput sequencing (HTS) data, population genetics analysis was performed on major RNAi components from natural populations of the dengue and zika virus vector, Aedes aegypti. Pairwise comparisons of four geographically separated wild-caught collections (Senegal, Thailand, and Mexico) were analyzed for this study. Mutation rate ratios of siRNA/miRNA orthologs indicated rapid evolution of anti-viral siRNA pathway components, as had been reported previously. Polymorphisms were present in key amino acid residues of RNAi pathway components, which could contribute to variability in arbovirus infection rates, and thereby influence transmission cycles. Haplotype analysis of Argonaute-2 (Ago2), the RNAi slicer enzyme , revealed a hypervariable region in the predicted N-terminus that varied widely among the populations, as well as polymorphisms in the PAZ and PIWI domains. Dicer-2 showed selected coding changes near the DEAD/DEAH helicase , dimerization , and RNase III domains, which also varied among the collections. Senegal (PK10) showed the highest number of coding changes in Ago2 and Dicer-2. Rapid evolution of RNAi components may influence emergence of arbovirus genotypes and contribute to the inter-kingdom arms race of arbovirus pathogens and their hosts.

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References

  • Ambrose RL, Mackenzie JM (2015) Conserved amino acids within the N-terminus of the West Nile virus NS4A protein contribute to virus replication, protein stability and membrane proliferation. Virology 481:95–106. doi:10.1016/j.virol.2015.02.045

    Article  CAS  PubMed  Google Scholar 

  • Bean AG, Baker ML, Stewart CR, Cowled C, Deffrasnes C, Wang LF, Lowenthal JW (2013) Studying immunity to zoonotic diseases in the natural host—keeping it real. Nat Rev Immunol 13(12):851–861. doi:10.1038/nri3551

    Article  CAS  PubMed  Google Scholar 

  • Bennett KE, Olson KE, Munoz Mde L, Fernandez-Salas I, Farfan-Ale JA, Higgs S, Black WCt, Beaty BJ (2002) Variation in vector competence for dengue 2 virus among 24 collections of Aedes aegypti from Mexico and the United States. Am J Trop Med Hyg 67(1):85–92

    Google Scholar 

  • Bernhardt SA, Simmons MP, Olson KE, Beaty BJ, Blair CD, Black WC (2012) Rapid intraspecific evolution of miRNA and siRNA genes in the mosquito Aedes aegypti. PLoS ONE 7(9):e44198. doi:10.1371/journal.pone.0044198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, Wint GR, Simmons CP, Scott TW, Farrar JJ, Hay SI (2013) The global distribution and burden of dengue. Nature 496(7446):504–507. doi:10.1038/nature12060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bosio CF, Fulton RE, Salasek ML, Beaty BJ, Black WCT (2000) Quantitative trait loci that control vector competence for dengue-2 virus in the mosquito Aedes aegypti. Genetics 156(2):687–698

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brown JE, McBride CS, Johnson P, Ritchie S, Paupy C, Bossin H, Lutomiah J, Fernandez-Salas I, Ponlawat A, Cornel AJ, Black WCt, Gorrochotegui-Escalante N, Urdaneta-Marquez L, Sylla M, Slotman M, Murray KO, Walker C, Powell JR (2011) Worldwide patterns of genetic differentiation imply multiple ‘domestications’ of Aedes aegypti, a major vector of human diseases. Proc Biol Sci 278(1717):2446–2454. doi:10.1098/rspb.2010.2469

    Google Scholar 

  • Campbell CL, Black WCt, Hess AM, Foy BD (2008a) Comparative genomics of small RNA regulatory pathway components in vector mosquitoes. BMC Genomics 9:425. doi:10.1186/1471-2164-9-425

    Google Scholar 

  • Campbell CL, Keene KM, Brackney DE, Olson KE, Blair CD, Wilusz J, Foy BD (2008b) Aedes aegypti uses RNA interference in defense against Sindbis virus infection. BMC Microbiol 8:47. doi:10.1186/1471-2180-8-47

    Article  PubMed  PubMed Central  Google Scholar 

  • Campbell CL, Harrison T, Hess AM, Ebel GD (2014) MicroRNA levels are modulated in Aedes aegypti after exposure to Dengue-2. Insect Mol Biol 23(1):132–139. doi:10.1111/imb.12070

    Article  CAS  PubMed  Google Scholar 

  • Cummings DA, Irizarry RA, Huang NE, Endy TP, Nisalak A, Ungchusak K, Burke DS (2004) Travelling waves in the occurrence of dengue haemorrhagic fever in Thailand. Nature 427(6972):344–347. doi:10.1038/nature02225

    Article  CAS  PubMed  Google Scholar 

  • Dantes HG, Farfan-Ale JA, Sarti E (2014) Epidemiological trends of dengue disease in Mexico (2000–2011): a systematic literature search and analysis. PLoS Negl Trop Dis 8(11):e3158. doi:10.1371/journal.pntd.0003158

    Article  PubMed  PubMed Central  Google Scholar 

  • Diallo M, Ba Y, Faye O, Soumare ML, Dia I, Sall AA (2008) Vector competence of Aedes aegypti populations from Senegal for sylvatic and epidemic dengue 2 virus isolated in West Africa. Trans R Soc Trop Med Hyg 102(5):493–498. doi:10.1016/j.trstmh.2008.02.010

    Article  PubMed  Google Scholar 

  • Dickson LB, Sanchez-Vargas I, Sylla M, Fleming K, Black WCI (2014) Vector competence in West African Aedes aegypti is flavivirus species and genotype dependent. PLoS Negl Trop Dis 8(10):e3153. doi:10.1371/journal.pntd.0003153

    Article  PubMed  PubMed Central  Google Scholar 

  • Dickson LB, Campbell CL, Juneja P, Jiggins FM, Sylla M, Black WCI (2016a) Exon enriched libraries reveal large genetic differences on the sex autosome within and among Aedes aegypti from Senegal, West Africa. (Personal communication)

    Google Scholar 

  • Dickson LB, Sharakhova V, Timoshevskiy A, Fleming KL, Caspary A, Sylla M, Black WCI (2016b) Reproductive incompatibility involving Senegal Aedes aegypti (L) is associated with chromosome rearrangements. PLoS Negl Trop Dis 10(4):e0004626. doi: 10.1371/journal.pntd.0004626

    Google Scholar 

  • Franco L, Di Caro A, Carletti F, Vapalahti O, Renaudat C, Zeller H, Tenorio A (2010) Recent expansion of dengue virus serotype 3 in West Africa. Euro Surveill 15(7):578–583

    Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652. doi:10.1038/nbt.1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grun D, Wang YL, Langenberger D, Gunsalus KC, Rajewsky N (2005) microRNA target predictions across seven Drosophila species and comparison to mammalian targets. PLoS Comput Biol 1(1):e13. doi:10.1371/journal.pcbi.0010013

    Article  PubMed  PubMed Central  Google Scholar 

  • Gubler DJ (2002) The global emergence/resurgence of arboviral diseases as public health problems. Arch Med Res 33(4):330–342

    Article  PubMed  Google Scholar 

  • Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, Macmanes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, Leduc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the trinity platform for reference generation and analysis. Nat Protoc 8(8):1494–1512. doi:10.1038/nprot.2013.084

    Article  CAS  PubMed  Google Scholar 

  • Hess AM, Prasad AN, Ptitsyn A, Ebel GD, Olson KE, Barbacioru C, Monighetti C, Campbell CL (2011) Small RNA profiling of Dengue virus-mosquito interactions implicates the PIWI RNA pathway in anti-viral defense. BMC Microbiol 11:45. doi:10.1186/1471-2180-11-45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirano M, Yoshii K, Sakai M, Hasebe R, Ichii O, Kariwa H (2014) Tick-borne flaviviruses alter membrane structure and replicate in dendrites of primary mouse neuronal cultures. J Gen Virol 95(Pt 4):849–861. doi:10.1099/vir.0.061432-0

    Article  CAS  PubMed  Google Scholar 

  • Juneja P, Ariani CV, Ho YS, Akorli J, Palmer WJ, Pain A, Jiggins FM (2015) Exome and transcriptome sequencing of Aedes aegypti identifies a locus that confers resistance to Brugia malayi and alters the immune response. PLoS Pathog 11(3):e1004765. doi:10.1371/journal.ppat.1004765

    Article  PubMed  PubMed Central  Google Scholar 

  • Kakumani PK, Ponia SS, S RK, Sood V, Chinnappan M, Banerjea AC, Medigeshi GR, Malhotra P, Mukherjee SK, Bhatnagar RK (2013) Role of RNA interference (RNAi) in dengue virus replication and identification of NS4B as an RNAi suppressor. J Virol 87 (16):8870–8883. doi:10.1128/JVI.02774-12

    Google Scholar 

  • Keene KM, Foy BD, Sanchez-Vargas I, Beaty BJ, Blair CD, Olson KE (2004) RNA interference acts as a natural antiviral response to O’nyong-nyong virus (Alphavirus; Togaviridae) infection of Anopheles gambiae. Proc Natl Acad Sci USA 101(49):17240–17245. doi:10.1073/pnas.0406983101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD, Lin L, Miller CA, Mardis ER, Ding L, Wilson RK (2012) VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 22(3):568–576. doi:10.1101/gr.129684.111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lambrechts L, Chevillon C, Albright RG, Thaisomboonsuk B, Richardson JH, Jarman RG, Scott TW (2009) Genetic specificity and potential for local adaptation between dengue viruses and mosquito vectors. BMC Evol Biol 9:160. doi:10.1186/1471-2148-9-160

    Article  PubMed  PubMed Central  Google Scholar 

  • Lambrechts L, Paaijmans KP, Fansiri T, Carrington LB, Kramer LD, Thomas MB, Scott TW (2011) Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti. Proc Natl Acad Sci USA 108(18):7460–7465. doi:10.1073/pnas.1101377108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lambrechts L, Quillery E, Noel V, Richardson JH, Jarman RG, Scott TW, Chevillon C (2013) Specificity of resistance to dengue virus isolates is associated with genotypes of the mosquito antiviral gene Dicer-2. Proc Biol Sci 280(1751):20122437. doi:10.1098/rspb.2012.2437

    Article  PubMed  PubMed Central  Google Scholar 

  • Lawson D, Arensburger P, Atkinson P, Besansky NJ, Bruggner RV, Butler R, Campbell KS, Christophides GK, Christley S, Dialynas E, Emmert D, Hammond M, Hill CA, Kennedy RC, Lobo NF, MacCallum MR, Madey G, Megy K, Redmond S, Russo S, Severson DW, Stinson EO, Topalis P, Zdobnov EM, Birney E, Gelbart WM, Kafatos FC, Louis C, Collins FH (2007) VectorBase: a home for invertebrate vectors of human pathogens. Nucleic Acids Res 35 (Database issue):D503–505. doi:10.1093/nar/gkl960

    Google Scholar 

  • Lee YS, Nakahara K, Pham JW, Kim K, He Z, Sontheimer EJ, Carthew RW (2004) Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117(1):69–81

    Article  CAS  PubMed  Google Scholar 

  • Leger P, Lara E, Jagla B, Sismeiro O, Mansuroglu Z, Coppee JY, Bonnefoy E, Bouloy M (2013) Dicer-2- and Piwi-mediated RNA interference in Rift Valley fever virus-infected mosquito cells. J Virol 87(3):1631–1648. doi:10.1128/JVI.02795-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mattingly PF (1958) Genetical aspects of the Aedes aegypti problem. II. Disease relationships, genetics and control. Ann Trop Med Parasitol 52(1):5–17

    Article  CAS  PubMed  Google Scholar 

  • McBride CS, Baier F, Omondi AB, Spitzer SA, Lutomiah J, Sang R, Ignell R, Vosshall LB (2014) Evolution of mosquito preference for humans linked to an odorant receptor. Nature 515(7526):222–227. doi:10.1038/nature13964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miesen P, Girardi E, van Rij RP (2015) Distinct sets of PIWI proteins produce arbovirus and transposon-derived piRNAs in Aedes aegypti mosquito cells. Nucleic Acids Res 43(13):6545–6556. doi:10.1093/nar/gkv590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moncayo AC, Fernandez Z, Ortiz D, Diallo M, Sall A, Hartman S, Davis CT, Coffey L, Mathiot CC, Tesh RB, Weaver SC (2004) Dengue emergence and adaptation to peridomestic mosquitoes. Emerg Infect Dis 10(10):1790–1796. doi:10.3201/eid1010.030846

    Article  PubMed  PubMed Central  Google Scholar 

  • Moore DF (1979) Hybridization and mating behavior in Aedes aegypti (Diptera: Culicidae). J Med Entomol 16(3):223–226

    Article  CAS  PubMed  Google Scholar 

  • Morazzani EM, Wiley MR, Murreddu MG, Adelman ZN, Myles KM (2012) Production of virus-derived ping-pong-dependent piRNA-like small RNAs in the mosquito soma. PLoS Pathog 8(1):e1002470. doi:10.1371/journal.ppat.1002470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyet MN, Duong TH, Trung VT, Nguyen TH, Tran CN, Long VT, le Dui T, Nguyen HL, Farrar JJ, Holmes EC, Rabaa MA, Bryant JE, Nguyen TT, Nguyen HT, Nguyen LT, Pham MP, Luong TT, Wills B, Nguyen CV, Wolbers M, Simmons CP (2013) Host and viral features of human dengue cases shape the population of infected and infectious Aedes aegypti mosquitoes. Proc Natl Acad Sci USA 110(22):9072–9077. doi:10.1073/pnas.1303395110

    Article  PubMed  Google Scholar 

  • Obbard DJ, Jiggins FM, Halligan DL, Little TJ (2006) Natural selection drives extremely rapid evolution in antiviral RNAi genes. Curr Biol 16(6):580–585. doi:10.1016/j.cub.2006.01.065

    Article  CAS  PubMed  Google Scholar 

  • Pham JW, Sontheimer EJ (2005) Molecular requirements for RNA-induced silencing complex assembly in the Drosophila RNA interference pathway. J Biol Chem 280(47):39278–39283. doi:10.1074/jbc.M509202200

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg R, Johansson MA, Powers AM, Miller BR (2013) Search strategy has influenced the discovery rate of human viruses. Proc Natl Acad Sci USA 110(34):13961–13964. doi:10.1073/pnas.1307243110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roth A, Mercier A, Lepers C, Hoy D, Duituturaga S, Benyon E, Guillaumot L, Souares Y (2014) Concurrent outbreaks of dengue, chikungunya and Zika virus infections—an unprecedented epidemic wave of mosquito-borne viruses in the Pacific 2012–2014. Euro Surveill 19(41)

    Google Scholar 

  • Saito K, Nishida KM, Mori T, Kawamura Y, Miyoshi K, Nagami T, Siomi H, Siomi MC (2006) Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev 20(16):2214–2222. doi:10.1101/gad.1454806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanchez-Vargas I, Scott JC, Poole-Smith BK, Franz AW, Barbosa-Solomieu V, Wilusz J, Olson KE, Blair CD (2009) Dengue virus type 2 infections of Aedes aegypti are modulated by the mosquito’s RNA interference pathway. PLoS Pathog 5(2):e1000299. doi:10.1371/journal.ppat.1000299

    Article  PubMed  PubMed Central  Google Scholar 

  • Schirtzinger EE, Andrade CC, Devitt N, Ramaraj T, Jacobi JL, Schilkey F, Hanley KA (2015) Repertoire of virus-derived small RNAs produced by mosquito and mammalian cells in response to dengue virus infection. Virology 476:54–60. doi:10.1016/j.virol.2014.11.019

    Article  CAS  PubMed  Google Scholar 

  • Schnettler E, Sterken MG, Leung JY, Metz SW, Geertsema C, Goldbach RW, Vlak JM, Kohl A, Khromykh AA, Pijlman GP (2012) Noncoding flavivirus RNA displays RNA interference suppressor activity in insect and Mammalian cells. J Virol 86(24):13486–13500. doi:10.1128/JVI.01104-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schnettler E, Donald CL, Human S, Watson M, Siu RW, McFarlane M, Fazakerley JK, Kohl A, Fragkoudis R (2013) Knockdown of piRNA pathway proteins results in enhanced Semliki Forest virus production in mosquito cells. J Gen Virol 94(Pt 7):1680–1689. doi:10.1099/vir.0.053850-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schountz T, Acuna-Retamar M, Feinstein S, Prescott J, Torres-Perez F, Podell B, Peters S, Ye C, Black WCt, Hjelle B (2012) Kinetics of immune responses in deer mice experimentally infected with Sin Nombre virus. J Virol 86(18):10015–10027. doi:10.1128/JVI.06875-11

    Google Scholar 

  • Sigrist CJ, Cerutti L, Hulo N, Gattiker A, Falquet L, Pagni M, Bairoch A, Bucher P (2002) PROSITE: a documented database using patterns and profiles as motif descriptors. Brief Bioinform 3(3):265–274

    Article  CAS  PubMed  Google Scholar 

  • Sylla M, Bosio C, Urdaneta-Marquez L, Ndiaye M, Black WCt (2009) Gene flow, subspecies composition, and dengue virus-2 susceptibility among Aedes aegypti collections in Senegal. PLoS Negl Trop Dis 3(4):e408. doi:10.1371/journal.pntd.0000408

    Google Scholar 

  • Vagin VV, Sigova A, Li C, Seitz H, Gvozdev V, Zamore PD (2006) A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313(5785):320–324. doi:10.1126/science.1129333

    Article  CAS  PubMed  Google Scholar 

  • van Rij RP, Saleh MC, Berry B, Foo C, Houk A, Antoniewski C, Andino R (2006) The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev 20(21):2985–2995. doi:10.1101/gad.1482006

    Article  PubMed  PubMed Central  Google Scholar 

  • Weaver SC, Reisen WK (2010) Present and future arboviral threats. Antiviral Res 85(2):328–345. doi:10.1016/j.antiviral.2009.10.008

    Article  CAS  PubMed  Google Scholar 

  • Wu TD, Nacu S (2010) Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26(7):873–881. doi:10.1093/bioinformatics/btq057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xi Z, Ramirez JL, Dimopoulos G (2008) The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog 4(7):e1000098. doi:10.1371/journal.ppat.1000098

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was funded under RO1 NIH AI-83368 and R21 AI109463 to WCB4.

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  1. Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO, 80523, USA

    Corey L. Campbell, Laura B. Dickson & William C. Black IV

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Correspondence to Corey L. Campbell .

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  1. Universidade Nova de Lisboa, Caparica, Portugal

    Ana Lúcia Leitão

  2. Universidade de Lisboa, Lisboa, Portugal

    Francisco J. Enguita

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Campbell, C.L., Dickson, L.B., Black, W.C. (2016). Rapid Evolution of Mosquito Anti-viral ncRNA Pathway Components. In: Leitão, A., Enguita, F. (eds) Non-coding RNAs and Inter-kingdom Communication. Springer, Cham. https://doi.org/10.1007/978-3-319-39496-1_8

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