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A novel miRNA, miR-13664, targets CpCYP314A1 to regulate deltamethrin resistance in Culex pipiens pallens

Published online by Cambridge University Press:  03 July 2018

X. H. Sun ,
N. Xu Open the ORCID record for N. Xu [Opens in a new window] ,
Y. Xu ,
D. Zhou ,
Y. Sun ,
W. J. Wang ,
L. Ma ,
C. L. Zhu  and
B. Shen
X. H. Sun
Affiliation:
Department of Pathogen Biology, Nanjing Medical University, Nanjing, Jiangsu 211166, PR China Jiangsu Province Key Laboratory of Modern Pathogen Biology, Nanjing, Jiangsu 211166, PR China
N. Xu
Affiliation:
Department of Pathogen Biology, Nanjing Medical University, Nanjing, Jiangsu 211166, PR China Jiangsu Province Key Laboratory of Modern Pathogen Biology, Nanjing, Jiangsu 211166, PR China
Y. Xu
Affiliation:
Department of Pathogen Biology, Nanjing Medical University, Nanjing, Jiangsu 211166, PR China Jiangsu Province Key Laboratory of Modern Pathogen Biology, Nanjing, Jiangsu 211166, PR China
D. Zhou
Affiliation:
Department of Pathogen Biology, Nanjing Medical University, Nanjing, Jiangsu 211166, PR China Jiangsu Province Key Laboratory of Modern Pathogen Biology, Nanjing, Jiangsu 211166, PR China
Y. Sun
Affiliation:
Department of Pathogen Biology, Nanjing Medical University, Nanjing, Jiangsu 211166, PR China Jiangsu Province Key Laboratory of Modern Pathogen Biology, Nanjing, Jiangsu 211166, PR China
W. J. Wang
Affiliation:
Department of Pathogen Biology, Hebei Medical University, Shijiazhuang 050017, China
L. Ma
Affiliation:
Department of Pathogen Biology, Nanjing Medical University, Nanjing, Jiangsu 211166, PR China Jiangsu Province Key Laboratory of Modern Pathogen Biology, Nanjing, Jiangsu 211166, PR China
C. L. Zhu*
Affiliation:
Department of Pathogen Biology, Nanjing Medical University, Nanjing, Jiangsu 211166, PR China Jiangsu Province Key Laboratory of Modern Pathogen Biology, Nanjing, Jiangsu 211166, PR China
B. Shen*
Affiliation:
Department of Pathogen Biology, Nanjing Medical University, Nanjing, Jiangsu 211166, PR China Jiangsu Province Key Laboratory of Modern Pathogen Biology, Nanjing, Jiangsu 211166, PR China
*
Author for correspondence: B. Shen, E-mail: shenbo@njmu.edu.cn and C.L. Zhu, clzhu@njmu.edu.cn
Author for correspondence: B. Shen, E-mail: shenbo@njmu.edu.cn and C.L. Zhu, clzhu@njmu.edu.cn
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Abstract

Extensive insecticide use has led to the resistance of mosquitoes to these insecticides, posing a major barrier to mosquito control. Previous Solexa high-throughput sequencing of Culex pipiens pallens in the laboratory has revealed that the abundance of a novel microRNA (miRNA), miR-13664, was higher in a deltamethrin-sensitive (DS) strain than a deltamethrin-resistant (DR) strain. Real-time quantitative PCR revealed that the miR-13664 transcript level was lower in the DR strain than in the DS strain. MiR-13664 oversupply in the DR strain increased the susceptibility of these mosquitoes to deltamethrin, whereas inhibition of miR-13664 made the DS strain more resistant to deltamethrin. Results of bioinformatic analysis, quantitative reverse-transcriptase polymerase chain reaction, luciferase assay and miR mimic/inhibitor microinjection revealed CpCYP314A1 to be a target of miR-13664. In addition, downregulation of CpCYP314A1 expression in the DR strain reduced the resistance of mosquitoes to deltamethrin. Taken together, our results indicate that miR-13664 could regulate deltamethrin resistance by interacting with CpCYP314A1, providing new insights into mosquito resistance mechanisms.

Keywords

Culex pipiens pallensdeltamethrin resistanceCpCYP314A1miR-13664
Type
Research Article
Information
Parasitology , Volume 146 , Issue 2 , February 2019 , pp. 197 - 205
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Copyright
Copyright © Cambridge University Press 2018 

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References

Aizoun, N, Aikpon, R, Padonou, GG, Oussou, O, Oke-Agbo, F, Gnanguenon, V, Ossè, R and Akogbeto, M (2013) Mixed-function oxidases and esterases associated with permethrin, deltamethrin and bendiocarb resistance in Anopheles gambiae s.l. in the south-north transect Benin, West Africa. Parasites & Vectors 6, 223.10.1186/1756-3305-6-223Google Scholar
Blandin, S, Moita, LF, Kocher, T, Wilm, M, Kafatos, FC and Levashina, EA (2002) Reverse genetics in the mosquito Anopheles gambiae: targeted disruption of the Defensin gene. EMBO Reports 3, 852–856.10.1093/embo-reports/kvf180Google Scholar
Benelli, G (2015) Research in mosquito control: current challenges for a brighter future. Parasitology Research 114, 2801–2805.10.1007/s00436-015-4586-9Google Scholar
Benelli, G (2016) Green synthesized nanoparticles in the fight against mosquito-borne diseases and cancer-a brief review. Enzyme and Microbial Technology 95, 58–68.10.1016/j.enzmictec.2016.08.022Google 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, GRW, Simmons, CP, Scott, TW, Farrar, JJ and Hay, SI (2013) The global distribution and burden of dengue. Nature 496, 504–507.10.1038/nature12060Google Scholar
Breving, K and Esquela-Kerscher, A (2010) The complexities of microRNA regulation: mirandering around the rules. International Journal of Biochemistry & Cell Biology 42, 1316–1329.10.1016/j.biocel.2009.09.016Google Scholar
Campbell, CL, Black, WCT, Hess, AM and Foy, BD (2008) Comparative genomics of small RNA regulatory pathway components in vector mosquitoes. BMC Genomics 9, 425.10.1186/1471-2164-9-425Google Scholar
Carthew, RW (2006) Gene regulation by microRNAs. Current Opinion in Genetics & Development 16, 203–208.10.1016/j.gde.2006.02.012Google Scholar
Chen, L, Cao, H and Feng, Y (2017) MiR-199a suppresses prostate cancer paclitaxel resistance by targeting YES1. World Journal of Urology 36, 357–365.10.1007/s00345-017-2143-0Google Scholar
Chorostecki, U, Moro, B, Rojas, AML, Debernardi, JM, Schapire, AL, Notredame, C and Palatnik, JF (2017) Evolutionary footprints reveal insights into plant microRNA biogenesis. Plant Cell 29, 1248–1261.Google Scholar
Chiu, TL, Wen, Z, Rupasinghe, SG and Schuler, MA (2008) Comparative molecular modeling of Anopheles gambiae CYP6Z1, a mosquito P450 capable of metabolizing DDT. Proceedings of the National Academy of Sciences of the USA 105, 8855–886010.1073.10.1073/pnas.0709249105Google Scholar
Cui, J, Li, S, Zhao, P and Zou, F (2013) Flight capacity of adult Culex pipiens pallens (Diptera: Culicidae) in relation to gender and day-age. Journal of Medical Entomology 50, 1055–1058.10.1603/ME12078Google Scholar
Ding, N, Wang, S, Yang, Q, Li, Y, Cheng, H, Wang, J, Wang, D, Deng, Y, Yang, Y, Hua, S, Zhao, H and Fang, X (2015) Deep sequencing analysis of microRNA expression in human melanocyte and melanoma cell lines. Gene 572, 135–145.10.1016/j.gene.2015.07.013Google Scholar
Djouaka, RF, Bakare, AA, Coulibaly, ON, Akogbeto, MC, Ranson, H, Hemingway, J and Strode, C (2008) Expression of the cytochrome P450s, CYP6P3 and CYP6M2 are significantly elevated in multiple pyrethroid resistant populations of Anopheles gambiae s.s. from Southern Benin and Nigeria. BMC Genomics 9, 538.10.1186/1471-2164-9-538Google Scholar
Elzaki, MEA, Miah, MA, Wu, M, Zhang, H, Pu, J, Jiang, L and Han, Z (2017) Imidacloprid is degraded by CYP353D1v2, a cytochrome P450 overexpressed in a resistant strain of Laodelphax striatellus. Pest Management Science 73, 1358–1363.10.1002/ps.4570Google Scholar
Friedländer, MR, Chen, W, Adamidi, C, Maaskola, J, Einspanier, R, Knespel, S and Rajewsky, N (2008) Discovering microRNAs from deep sequencing data using miRDeep. Nature Biotechnology 26, 407–415.10.1038/nbt1394Google Scholar
Fu, X, Dimopoulos, G and Zhu, J (2017) Association of microRNAs with Argonaute proteins in the malaria mosquito Anopheles gambiae after blood ingestion. Scientific Reports 7, 6493.10.1038/s41598-017-07013-1Google Scholar
Gong, Y, Li, T, Feng, Y and Liu, N (2017) The function of two P450s, CYP9M10 and CYP6AA7, in the permethrin resistance of Culex quinquefasciatus. Scientific Reports 7, 587.10.1038/s41598-017-00486-0Google Scholar
Guo, Y, Wu, H, Zhang, X, Ma, E, Guo, Y, Zhu, KY and Zhang, J (2016) RNA interference of cytochrome P450 CYP6F subfamily genes affects susceptibility to different insecticides in Locusta migratoria. Pest Management Science 72, 2154–2165.10.1002/ps.4248Google Scholar
Guo, Q, Huang, Y, Zou, F, Liu, B, Tian, M, Ye, W, Guo, J, Sun, X, Zhou, D, Sun, Y, Ma, L, Shen, B and Zhu, C (2017) The role of miR-2~13~71 cluster in resistance to deltamethrin in Culex pipiens pallens. Insect Biochemistry and Molecular Biology 84, 15–22.10.1016/j.ibmb.2017.03.006Google Scholar
Han, J and Chen, Q (2015) MiR-16 modulate temozolomide resistance by regulating BCL-2 in human glioma cells. International Journal of Clinical and Experimental Pathology 8, 12698–12707.Google Scholar
Hemingway, J, Hawkes, NJ, McCarroll, L and Ranson, H (2004) The molecular basis of insecticide resistance in mosquitoes. Insect Biochemistry and Molecular Biology 34, 653–665.10.1016/j.ibmb.2004.03.018Google Scholar
Hong, S, Guo, Q, Wang, W, Hu, S, Fang, F, Lv, Y, Yu, J, Zou, F, Lei, Z, Ma, K, Ma, L, Zhou, D, Sun, Y, Zhang, D, Shen, B and Zhu, C (2014) Identification of differentially expressed microRNAs in Culex pipiens and their potential roles in pyrethroid resistance. Insect Biochemistry and Molecular Biology 55, 39–50.10.1016/j.ibmb.2014.10.007Google Scholar
Hussain, M, O'Neill, SL and Asgari, S (2013) Wolbachia interferes with the intracellular distribution of Argonaute 1 in the dengue vector Aedes aegypti by manipulating the host microRNAs. RNA Biology 10, 1868–1875.10.4161/rna.27392Google Scholar
Jiang, S, Wang, Z, Guo, X, Zhang, Y, Li, C, Dong, Y, Xing, D and Zhao, T (2014) Infection and dissemination of West Nile virus in China by the potential vector, Culex pipiens pallens. Journal of Vector Ecology 39, 78–82.10.1111/j.1948-7134.2014.12073.xGoogle Scholar
Kanokudom, S, Vilaivan, T, Wikan, N, Thepparit, C, Smith, DR and Assavalapsakul, W (2017) miR-21 promotes dengue virus serotype 2 replication in HepG2 cells. Antiviral Research 142, 169–177.10.1016/j.antiviral.2017.03.020Google Scholar
Lee, YR, Yeh, SF, Ruan, XM, Zhang, H, Hsu, SD, Huang, HD, Hsieh, CC, Lin, YS, Yeh, TM, Liu, HS and Gan, DD (2017) Honeysuckle aqueous extract and induced let-7a suppress dengue virus type 2 replication and pathogenesis. Journal of Ethnopharmacology 198, 109–121.10.1016/j.jep.2016.12.049Google Scholar
Letelier, P, Riquelme, I, Hernandez, AH, Guzman, N, Farias, JG and Roa, JC (2016) Circulating MicroRNAs as biomarkers in biliary tract cancers. International Journal of Molecular Sciences 17, 791–814.10.3390/ijms17050791Google Scholar
Lewis, SH, Salmela, H and Obbard, DJ (2016) Duplication and diversification of dipteran Argonaute genes, and the evolutionary divergence of Piwi and Aubergine. Genome Biology and Evolution 8, 507–518.10.1093/gbe/evw018Google Scholar
Li, X, Guo, L, Zhou, X, Gao, X and Liang, P (2015) miRNAs regulated overexpression of ryanodine receptor is involved in chlorantraniliprole resistance in Plutella xylostella (L.). Scientific Reports 5, 14095.10.1038/srep14095Google Scholar
Li, S, Zeng, A, Hu, Q, Yan, W, Liu, Y and You, Y (2017) miR-423-5p contributes to a malignant phenotype and temozolomide chemoresistance in glioblastomas. Journal of Neuro-oncology 19, 55–65.10.1093/neuonc/now129Google Scholar
Liang, G, Gao, X and Gould, EA (2015) Factors responsible for the emergence of arboviruses; strategies, challenges and limitations for their control. Emerging Microbes & Infections 4, e18.10.1038/emi.2015.18Google Scholar
Liu, Y, Zhang, H, Qiao, C, Lu, X and Cui, F (2011) Correlation between carboxylesterase alleles and insecticide resistance in Culex pipiens complex from China. Parasites & Vectors 4, 236.10.1186/1756-3305-4-236Google Scholar
Liu, YP, Yang, J and Liu, Y (2013) Research progress in microRNAs in insects. Acta Entomologica Sinica 56, 1026–1037.Google Scholar
Liu, B, Tian, M, Guo, Q, Ma, L, Zhou, D, Shen, B, Sun, Y and Zhu, C (2016) MiR-932 regulates pyrethroid resistance in Culex pipiens pallens (Diptera: Culicidae). Journal of Medical Entomology 53, 1205–1210.10.1093/jme/tjw083Google Scholar
Lucas, K and Raikhel, AS (2013) Insect microRNAs: biogenesis, expression profiling and biological functions. Insect Biochemistry and Molecular Biology 43, 24–38.10.1016/j.ibmb.2012.10.009Google Scholar
Luo, S and Lu, J (2017) Silencing of transposable elements by piRNAs in drosophila: an evolutionary perspective. Genomics, Proteomics & Bioinformatics 15, 164–176.10.1016/j.gpb.2017.01.006Google Scholar
Ma, K, Li, X, Hu, H, Zhou, D, Sun, Y, Ma, L, Zhu, C and Shen, B (2017) Pyrethroid-resistance is modulated by miR-92a by targeting CpCPR4 in Culex pipiens pallens. Comparative Biochemistry and Physiology – B Biochemistry and Molecular Biology 203, 20–24.10.1016/j.cbpb.2016.09.002Google Scholar
Muller, P, Warr, E, Stevenson, BJ, Pignatelli, PM, Morgan, JC, Steven, A, Yawson, AE, Mitchell, SN, Ranson, H, Hemingway, J, Paine, MJ and Donnelly, MJ (2008 a) Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. PLoS Genetics 4, e1000286.10.1371.10.1371/journal.pgen.1000286Google Scholar
Muller, P, Chouaibou, M, Pignatelli, P, Etang, J, Walker, ED, Donnelly, MJ, Simard, F and Ranson, H (2008 b) Pyrethroid tolerance is associated with elevated expression of antioxidants and agricultural practice in Anopheles arabiensis sampled from an area of cotton fields in Northern Cameroon. Molecular Ecology 17, 1145–115510.1111.10.1111/j.1365-294X.2007.03617.xGoogle Scholar
Pastula, DM, Smith, DE, Beckham, JD and Tyler, KL (2016) Four emerging arboviral diseases in North America: Jamestown Canyon, Powassan, chikungunya, and Zika virus diseases. Journal of Neurovirology 22, 257–260.Google Scholar
Rogers, AK, Situ, K, Perkins, EM and Toth, KF (2017) Zucchini-dependent piRNA processing is triggered by recruitment to the cytoplasmic processing machinery. Genes & Development 31, 1858–1869.Google Scholar
Salone, V and Rederstorff, M (2015) Stem-loop RT-PCR based quantification of small non-coding RNAs. Methods in Molecular Biology 1296, 103–108.Google Scholar
Schmittgen, TD and Livak, KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nature Protocols 3, 1101–1108.Google Scholar
Sebastiani, G, Po, A, Miele, E, Ventriglia, G, Ceccarelli, E, Bugliani, M, Marselli, L, Marchetti, P, Gulino, A, Ferretti, E and Dotta, F (2015) MicroRNA-124a is hyperexpressed in type 2 diabetic human pancreatic islets and negatively regulates insulin secretion. Acta Diabetologica 52, 523–530.Google Scholar
Shi, TF, Wang, YF, Liu, F, Qi, L and Yu, LS (2017) Influence of the neonicotinoid insecticide Thiamethoxam on miRNA expression in the Honey Bee (Hymenoptera: Apidae). Journal of Insect Science 17, 1–5.Google Scholar
Siegwart, M, Graillot, B, Blachere Lopez, C, Besse, S, Bardin, M, Nicot, PC and Lopez-Ferber, M (2015) Resistance to bio-insecticides or how to enhance their sustainability: a review. Frontiers in Plant Science 6, 381.Google Scholar
Stevenson, BJ, Bibby, J, Pignatelli, P, Muangnoicharoen, S, O'Neill, PM, Lian, LY, Müller, P, Nikou, D, Steven, A, Hemingway, J, Sutcliffe, MJ and Paine, MJ (2011) Cytochrome P450 6M2 from the malaria vector Anopheles gambiae metabolizes pyrethroids: sequential metabolism of deltamethrin revealed. Insect Biochemistry and Molecular Biology 41, 492–502101016.Google Scholar
Tang, F, Hajkova, P, Barton, SC, Lao, K and Surani, MA (2006) MicroRNA expression profiling of single whole embryonic stem cells. Nucleic Acids Research 34(2), e9.Google Scholar
Tian, M, Liu, B, Hu, H, Li, X, Guo, Q, Zou, F, Liu, X, Hu, M, Guo, J, Ma, L, Zhou, D, Sun, Y, Shen, B and Zhu, C (2016) MiR-285 targets P450 (CYP6N23) to regulate pyrethroid resistance in Culex pipiens pallens. Parasitology Research 115, 4511–4517.Google Scholar
Wang, Z, Li, C, Xing, D, Yu, Y, Liu, N, Xue, R, Dong, Y and Zhao, T (2012) Detection and widespread distribution of sodium channel alleles characteristic of insecticide resistance in Culex pipiens complex mosquitoes in China. Medical and Veterinary Entomology 26, 228–232.Google Scholar
White, MT, Lwetoijera, D, Marshall, J, Caron-Lormier, G, Bohan, DA, Denholm, I and Devine, GJ (2014) Negative cross resistance mediated by co-treated bed nets: a potential means of restoring pyrethroid-susceptibility to malaria vectors. PLoS ONE 9, e95640.Google Scholar
WHO (2017) World malaria report 2017. Available form http://www.who.int/malaria/publications/world-malaria-report-2017/report/en/Google Scholar
Yan, L, Yang, P, Jiang, F, Cui, N, Ma, E, Qiao, C and Cui, F (2012) Transcriptomic and phylogenetic analysis of Culex pipiens quinquefasciatus for three detoxification gene families. BMC Genomics 13, 609.Google Scholar
Zhang, Y, Meng, X, Yang, Y, Li, H, Wang, X, Yang, B, Zhang, J, Li, C, Millar, NS and Liu, Z (2016) Synergistic and compensatory effects of two point mutations conferring target-site resistance to fipronil in the insect GABA receptor RDL. Scientific Reports 6, 32335.Google Scholar
Zhu, Y, Zhang, R, Zhang, B, Zhao, T, Wang, P, Liang, G and Cheng, G (2017) Blood meal acquisition enhances arbovirus replication in mosquitoes through activation of the GABAergic system. Nature Communications 8, 1262.Google Scholar
Zou, F, Chen, C, Zhong, D, Shen, B, Zhang, D, Guo, Q, Wang, W, Yu, J, Lv, Y, Lei, Z, Ma, K, Ma, L, Zhu, C and Yan, G (2015) Identification of QTLs conferring resistance to deltamethrin in Culex pipiens pallens. PLoS ONE 10, e0140923.Google Scholar