CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES >

2020 , Vol. 38 >Issue 6: 742 - 748

DOI: https://doi.org/10.12140/j.issn.1000-7423.2020.06.011

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Functions and roles of miRNA during the infection of Anopheles by Plasmodium

  • Ling-qian ZHU ,
  • Xin-yu FENG ,
  • Wei HU ,
  • Shi-zhu LI
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  • National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention;Chinese Center for Tropical Diseases Research;WHO Collaborating Centre for Tropical Diseases;National Center for International Research on Tropical Diseases, Ministry of Science and Technology;Key Laboratory of Parasite and Vector Biology, Ministry of Health, Shanghai 200025, China

Received date: 2020-06-11

  Online published: 2021-01-12

Supported by

Youth Program of National Natural Science Foundation of China(81802039);National Key Program for Infectious Disease of China(2016ZX10004222-004)

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Abstract

miRNA is a type of single-stranded non-coding RNA with a length of 21-24 bases. miRNA may lead to mRNA degradation or translation inhibition by targeting the 3′-end untranslated region of mRNA, and plays an important role in the defense response of Anopheles against pathogen invasion among many other biological processes. This article reviews the possible functions, and target genes and signaling pathways involved of miRNAs, during Anopheles infection with Plasmodium.

Key words： miRNA; Anopheles; Plasmodium; Function; Regulation

Cite this article

Ling-qian ZHU , Xin-yu FENG , Wei HU , Shi-zhu LI . Functions and roles of miRNA during the infection of Anopheles by Plasmodium[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2020 , 38(6) : 742 -748 . DOI: 10.12140/j.issn.1000-7423.2020.06.011

References

[1] World Health Organization. World Malaria Report 2019[R]. Geneva: WHO, 2019.
[2] Ranson H, N’guessan R, Lines J, et al. Pyrethroid resistance in African anopheline mosquitoes: What are the implications for malaria control?[J]. Trends Parasitol, 2011,27(2):91-98.
[3] Chaturvedi N, Bharti PK, Tiwari A, et al. Strategies and recent development of transmission-blocking vaccines against Plasmodium falciparum[J]. Indian J Med Res, 2016,143(6):696-711.
[4] Zheng WQ, Wang JR, Wang H, et al. Truncated Plasmodium berghei putative secreted ookinete protein 7 induces transmission-blocking immunity[J]. Chin J Parasitol Parasit Dis, 2019,37(5):520-524, 531. (in Chinese)
[4] ( 郑文琪, 王俊瑞, 王华, 等. 伯氏疟原虫推测分泌动合子蛋白7截短片段传播阻断功能的研究[J]. 中国寄生虫学与寄生虫病杂志, 2019,37(5):520-524, 531.)
[5] Cirimotich CM, Dong Y, Garver LS, et al. Mosquito immune defenses against Plasmodium infection[J]. Dev Comp Immunol, 2010,34(4):387-395.
[6] Cai Z, Yu X, Cheng G. Progress towards mosquito microbiome on regulating the transmission of mosquito-borne diseases[J]. Chin J Parasitol Parasit Dis, 2019,37(5):603-608. (in Chinese)
[6] ( 蔡珍, 余茜, 程功. 蚊肠道微生物调节蚊媒传染病传播的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2019,37(5):603-608.)
[7] Vaughan JA, Noden BH, Beier JC. Sporogonic development of cultured Plasmodium falciparum in six species of laboratory-reared Anopheles mosquitoes[J]. Am J Trop Med Hyg, 1994,51(2):233-243.
[8] Hillyer JF, Barreau C, Vernick KD. Efficiency of salivary gland invasion by malaria sporozoites is controlled by rapid sporozoite destruction in the mosquito haemocoel[J]. Int J Parasitol, 2007,37(6):673-681.
[9] Bartel DP. MicroRNAs: target recognition and regulatory functions[J]. Cell, 2009,136(2):215-233.
[10] Liang H, Zen K, Zhang J, et al. New roles for microRNAs in cross-species communication[J]. RNA Biol, 2013,10(3):367-370.
[11] O’Connell RM, Rao DS, Baltimore D. microRNA regulation of inflammatory responses[J]. Annu Rev Immunol, 2012,30:295-312.
[12] Winter F, Edaye S, Hüttenhofer A, et al. Anopheles gambiae miRNAs as actors of defence reaction against Plasmodium invasion[J]. Nucleic Acids Res, 2007,35(20):6953-6962.
[13] Biryukova I, Ye T, Levashina E. Transcriptome-wide analysis of microRNA expression in the malaria mosquito Anopheles gambiae[J]. BMC Genom, 2014,15(1):1-19.
[14] Dennison NJ, BenMarzouk-Hidalgo OJ, Dimopoulos G. MicroRNA-regulation of Anopheles gambiae immunity to Plasmodium falciparum infection and midgut microbiota[J]. Dev Comp Immunol, 2015,49(1):170-178.
[15] Jain S, Rana V, Shrinet J, et al. Blood feeding and Plasmodium infection alters the miRNome of Anopheles stephensi[J]. PLoS One, 2014,9(5):e98402.
[16] Feng X, Zhou S, Wang J, et al. microRNA profiles and functions in mosquitoes[J]. PLoS Negl Trop Dis, 2018,12(5):e0006463.
[17] Liu S, Lucas KJ, Roy S, et al. Mosquito-specific microRNA-1174 targets serine hydroxymethyl transferase to control key functions in the gut[J]. Proc Natl Acad Sci USA, 2014,111(40):14460-14465.
[18] Jain S, Rana V, Tridibes A, et al. Dynamic expression of miRNAs across immature and adult stages of the malaria mosquito Anopheles stephensi[J]. Parasit Vectors, 2015,8:179.
[19] Jaramillo-Gutierrez G, Molina-Cruz A, Kumar S, et al. The Anopheles gambiae oxidation resistance 1 (OXR1) gene regulates expression of enzymes that detoxify reactive oxygen species[J]. PLoS One, 2010,5(6):e11168.
[20] Jain S, Shrinet J, Tridibes A, et al. miRNA-mRNA conflux regulating immunity and oxidative stress pathways in the midgut of blood-fed Anopheles stephensi[J]. Noncoding RNA, 2015,1(3):222-245.
[21] Lampe L, Jentzsch M, Levashina EA. Metabolic balancing by miR-276 shapes the mosquito reproductive cycle and Plasmodium falciparum development[J]. Nat Commun, 2019,10(1):5634.
[22] Liu W, Hao Z, Huang L, et al. Comparative expression profile of microRNAs in Anopheles anthropophagus midgut after blood-feeding and Plasmodium infection[J]. Parasit Vectors, 2017,10(1):86.
[23] Bryant B, Macdonald W, Raikhel AS. microRNA miR-275 is indispensable for blood digestion and egg development in the mosquito Aedes aegypti[J]. Proc Natl Acad Sci USA, 2010,107(52):22391-22398.
[24] Rutschmann S, Kilinc A, Ferrandon D. Cutting edge: The toll pathway is required for resistance to gram-positive bacterial infections in Drosophila[J]. J Immunol, 2002,168(4):1542-1546.
[25] Lemaitre B, Nicolas E, Michaut L, et al. The dorsoventral regulatory gene cassette sp?tzle/Toll/Cactus controls the potent antifungal response in Drosophila adults[J]. Cell, 1996,86(6):973-983.
[26] Zambon RA, Nandakumar M, Vakharia VN, et al. The toll pathway is important for an antiviral response in Drosophila[J]. Proc Natl Acad Sci USA, 2005,102(20):7257-7262.
[27] Xi Z, Ramirez JL, Dimopoulos G. The Aedes aegypti toll pathway controls dengue virus infection[J]. PLoS Pathog, 2008,4(7):e1000098.
[28] Frolet C, Thoma M, Blandin S, et al. Boosting NF-kappaB-dependent basal immunity of Anopheles gambiae aborts development of Plasmodium berghei[J]. Immunity, 2006,25(4):677-685.
[29] Fullaondo A, Lee SY. Identification of putative miRNA involved in Drosophila melanogaster immune response[J]. Dev Comp Immunol, 2012,36(2):267-273.
[30] Bayraktar R, Bertilaccio MTS, Calin GA. The interaction between two worlds: microRNAs and toll-like receptors[J]. Front Immunol, 2019,10:1053.
[31] Clayton AM, Dong Y, Dimopoulos G. The Anopheles innate immune system in the defense against malaria infection[J]. J Innate Immun, 2014,6(2):169-181.
[32] Garver LS, Dong YM, Dimopoulos G. Caspar controls resistance to Plasmodium falciparum in diverse anopheline species[J]. PLoS Pathog, 2009,5(3):e1000335.
[33] Gendrin M, Turlure F, Rodgers FH, et al. The peptidoglycan recognition proteins PGRPLA and PGRPLB regulate Anopheles immunity to bacteria and affect infection by Plasmodium[J]. J Innate Immun, 2017,9(4):333-342.
[34] Song X, Wang M, Dong L, et al. PGRP-LD mediates A. stephensi vector competency by regulating homeostasis of microbiota-induced peritrophic matrix synjournal[J]. PLoS Pathog, 2018,14(2):e1006899.
[35] Clayton AM, Cirimotich CM, Dong YM, et al. Caudal is a negative regulator of the Anopheles IMD pathway that controls resistance to Plasmodium falciparum infection[J]. Dev Comp Immunol, 2013,39(4):323-332.
[36] Souza-Neto JA, Sim S, Dimopoulos G. An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense[J]. Proc Natl Acad Sci USA, 2009,106(42):17841-17846.
[37] Gupta L, Molina-Cruz A, Kumar S, et al. The STAT pathway mediates late-phase immunity against Plasmodium in the mosquito Anopheles gambiae[J]. Cell Host Microbe, 2009,5(5):498-507.
[38] Bahia AC, Kubota MS, Tempone AJ, et al. The JAK-STAT pathway controls Plasmodium vivax load in early stages of Anopheles aquasalis infection[J]. PLoS Negl Trop Dis, 2011,5(11):e1317.
[39] Carissimo G, Pain A, Belda E, et al. Highly focused transcriptional response of Anopheles coluzziito O’nyongnyong arbovirus during the primary midgut infection[J]. BMC Genomics, 2018,19(1):526.
[40] Souvannaseng L, Hun LV, Baker H, et al. Inhibition of JNK signaling in the Asian malaria vector Anopheles stephensi extends mosquito longevity and improves resistance to Plasmodium falciparum infection[J]. PLoS Pathog, 2018,14(11):e1007418.
[41] Brenton AA, Souvannaseng L, Cheung K, et al. Engineered single nucleotide polymorphisms in the mosquito MEK docking site alter Plasmodium berghei development in Anopheles gambiae[J]. Parasit Vectors, 2014,7:287.
[42] Wang B, Pakpour N, Napoli E, et al. Anopheles stephensi p38 MAPK signaling regulates innate immunity and bioenergetics during Plasmodium falciparum infection[J]. Parasit Vectors, 2015,8:424.
[43] Feng XY. The role of microRNA in development and susceptibility to Plasmodium parasite in Chinese main malaria vector[D]. Beijing: Chinese Center for Disease Control and Prevention, 2018. (in Chinese)
[43] ( 冯欣宇. microRNA在我国主要传疟媒介按蚊发育及对疟原虫易感性中作用的研究[D]. 北京: 中国疾病预防控制中心, 2018.)
[44] Werling K, Shaw WR, Itoe MA, et al. Steroid hormone function controls non-competitive Plasmodium development in Anopheles[J]. Cell, 2019,177(2):315-325.
[45] Fu X, Liu P, Dimopoulos G, et al. Dynamic miRNA-mRNA interactions coordinate gene expression in adult Anopheles gambiae[J]. PLoS Genet, 2020,16(4):e1008765.
[46] Tarimo BB, Hritzo BA, Law HCH, et al. Ribosomal/nucleolar stress induction regulates tert-Butyl hydroperoxide (tBHP) mediated oxidative stress in Anopheles gambiae midguts[J]. BMC Res Notes, 2019,12(1):1-8.
[47] Sinden RE. Plasmodium differentiation in the mosquito[J]. Parassitologia, 1999,41(1/2/3):139-148.
[48] Dimopoulos G. Insect immunity and its implication in mosquito-malaria interactions[J]. Cell Microbiol, 2003,5(1):3-14.
[49] Allam M, Spillings BL, Abdalla H, et al. Identification and characterization of microRNAs expressed in the African malaria vector Anopheles funestus life stages using high throughput sequencing[J]. Malar J, 2016,15(1):542.
[50] Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene Lin-4 encodes small RNAs with antisense complementarity to Lin-14[J]. Cell, 1993,75(5):843-854.
[51] Mead EA, Tu Z. Cloning, characterization, and expression of microRNAs from the Asian malaria mosquito, Anopheles stephensi[J]. BMC Genomics, 2008,9:244.
[52] Jung CH, Hansen MA, Makunin IV, et al. Identification of novel non-coding RNAs using profiles of short sequence reads from next generation sequencing data[J]. BMC Genomics, 2010,11:77.
[53] Feng X, Zhou X, Zhou S, et al. Analysis of microRNA profile of Anopheles sinensis by deep sequencing and bioinformatic approaches[J]. Parasit Vectors, 2018,11(1):172.
[54] Bryant WB, Mills MK, Olson BJ, et al. Small RNA-seq analysis reveals miRNA expression dynamics across tissues in the malaria vector, Anopheles gambiae[J]. G3 (Bethesda), 2019,9(5):1507-1517.
[55] Zhang Y, Zhao B, Roy S, et al. microRNA-309 targets the Homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti[J]. Proc Natl Acad Sci USA, 2016,113(33):E4828-E4836.
[56] Arcà B, Colantoni A, Fiorillo C, et al. MicroRNAs from saliva of anopheline mosquitoes mimic human endogenous miRNAs and may contribute to vector-host-pathogen interactions[J]. Sci Rep, 2019,9(1):2955 .
[57] He X, Pan WQ. Research progress on miRNA-mediated schistosome-host interactions[J]. Chin J Parasitol Parasit Dis, 2020,38(3):259-262. (in Chinese)
[57] ( 何兴, 潘卫庆. miRNA介导血吸虫和宿主相互作用的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2020,38(3):259-262.)
[58] Seok H, Ham J, Jang ES, et al. MicroRNA target recognition: Insights from transcriptome-wide non-canonical interactions[J]. Mol Cells, 2016,39(5):375-381.
[59] Hussain M, Taft RJ, Asgari S. An insect virus-encoded microRNA regulates viral replication[J]. J Virol, 2008,82(18):9164-9170.
[60] Henke JI, Goergen D, Zheng J, et al. microRNA-122 stimulates translation of hepatitis C virus RNA[J]. Embo J, 2008,27(24):3300-3310.
[61] Lagos-Quintana M, Rauhut R, Lendeckel W, et al. Identification of novel genes coding for small expressed RNAs[J]. Science, 2001,294(5543):853-858.
[62] Bushati N, Cohen SM. microRNA functions[J]. Annu Rev Cell Dev Biol, 2007,23(1):175-205.
[63] Hussain M, Frentiu FD, Moreira LA, et al. Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti[J]. Proc Natl Acad Sci USA, 2011,108(22):9250-9255.
[64] Ma F, Liu X, Li D, et al. MicroRNA-466l upregulates IL-10 expression in TLR-triggered macrophages by antagonizing RNA-binding protein tristetraprolin-mediated IL-10 mRNA degradation[J]. J Immunol, 2010,184(11):6053-6059.
[65] Min H, Yoon S. Got target? Computational methods for microRNA target prediction and their extension[J]. Exp Mol Med, 2010,42(4):233-244.
[66] Ling L, Kokoza VA, Zhang C, et al. MicroRNA-277 targets insulin-like peptides 7 and 8 to control lipid metabolism and reproduction in Aedes aegypti mosquitoes[J]. Proc Natl Acad Sci USA, 2017,114(38):E8017-E8024.
[67] Zhao B, Lucas KJ, Saha TT, et al. MicroRNA-275 targets sarco/endoplasmic Reticulum Ca2+ adenosine triphosphatase (SERCA) to control key functions in the mosquito gut [J]. PLoS Genet, 2017,13(8):e1006943.
[68] Lampe L, Levashina EA. The role of microRNAs in Anopheles biology-an emerging research field[J]. Parasite Immunol, 2017,39(2):e12405.
[69] Kistler KE, Vosshall LB, Matthews BJ. Genome-engineering with CRISPR-Cas9 in the mosquito Aedes aegypti[J]. Cell Rep, 2015,11(1):51-60.
[70] Hammond A, Galizi R, Kyrou K, et al. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae[J]. Nat Biotechnol, 2016,34(1):78-83.
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