Identification and characterization of the expression profile of microRNAs in Anopheles anthropophagus

Particle and Fibre Toxicology

Shaohui Liang¹  Feng Tan¹  Chunxiang Li¹  Cuicui Xing¹  Huicong Huang¹  Wenquan Liu¹ 

[1] Department of Parasitology, Wenzhou Medical University, Wenzhou, Zhejiang Province 325035, PR China

关键词: Stage-specific;    Sexual differences;    Expression profile;    Anopheles anthropophagus;    MicroRNAs (miRNAs);   

Others  :  807409
DOI  :  10.1186/1756-3305-7-159

 received in 2013-12-26, accepted in 2014-03-25,  发布年份 2014

【 摘 要 】

Background

Anopheles anthropophagus, one of the most important mosquito-borne disease vectors in Asia, mainly takes blood meals from humans and transmits both malaria and filariae. MicroRNAs (miRNAs) are small non-coding RNAs, and play a critical role in many cellular processes, including development, differentiation, apoptosis and innate immunity.

Methods

We investigated the global miRNA expression profile of male and female adults of A. anthropophagus using illumina Hiseq2000 sequencing combined with Northern blot.

Results

By using the miRNAs of the closely-related species Anopheles gambiae and Aedes aegypti as reference, we obtained 102 miRNAs candidates out of 12.43 million raw sequencing reads for male and 16.51 million reads for female, with 81 of them found as known miRNAs in An. gambiae and/or Ae. aegypti, and the remaining 21 miRNAs were considered as novel. By analyzing the revised read count of miRNAs in male and female, 29 known miRNAs show sexual difference expression: >2-fold in the read count of the same miRNAs in male and female. Especially for miR-989, which is highly expressed in the female mosquitoes, but shows almost no detected expression in male mosquitoes, indicating that miR-989 may be involved in the physiological activity of female mosquito adults. The expression of four miRNAs in different growth stages of mosquito were further identified by Northern blot. Several miRNAs show the stage-specific expression, of which miR-2943 only expressed in the egg stage, suggesting that miR-2943 may be associated with the development of mosquito eggs.

Conclusions

The present study represents the first global characterization of An. anthropophagus miRNAs in sexual differences and stage-specific functions. A better understanding of the functions of these miRNAs will offer new insights in mosquito biology and has implications for the effective control of mosquito-borne infectious diseases.

【 授权许可】

   
2014 Liu et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Liu H, Gao X, Liang G: Newly recognized mosquito-associated viruses in mainland China, in the last two decades. Virol J 2011, 68:1-13.
• [2]Smith LD, Dushoff J, McKenzie EF: The risk of a mosquito-borne infection in a heterogeneous environment. PLoS Biol 2004, 11:e368.
• [3]Hancock AP, Sinkins PS, Godfray J, Charles H: Strategies for introducing wolbachia to reduce transmission of mosquito-borne diseases. PLoS Negl Trop Dis 2011, 4:e1024.
• [4]Gao Q, Beebe NW, Cooper RD: Molecular identification of the malaria vectors Anopheles anthropophagus and Anopheles sinensis (Diptera: Culicidae) in central China using polymerase chain reaction and appraisal of their position within the Hyrcanus group. J Med Entomol 2004, 1:5-11.
• [5]Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
• [6]Kim VN, Han J, Siomi MC: Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 2009, 10:126-139.
• [7]Zhang R, Wang YQ, Su B: Molecular evolution of a primate-specific microRNA family. Mol Biol Evol 2008, 25:1493-1502.
• [8]Kim YK, Kim VN: Processing of intronic microRNAs. EMBO J 2007, 26:775-783.
• [9]Bushati N: MicroRNA functions. Ann Rev Cell Dev Biol 2007, 23:175-205.
• [10]Miska EA: How microRNAs control cell division, differentiation and death. Curr Opin Genet Dev 2005, 15:563-568.
• [11]Liu N, Okamura K, Tyler DM, Phillips MD, Chung WJ, Lai EC: The evolution and functional diversification of animal microRNA genes. Cell Res 2008, 18:985-996.
• [12]Zhao GH, Xu MJ, Zhu XQ: Identification and characterization of microRNAs in Baylisascaris schroederi of the giant panda. Parasit Vectors 2013, 6:216. BioMed Central Full Text
• [13]Li S, Mead AE, Liang SH, Tu ZJ: Direct sequencing and expression analysis of a large number of miRNAs in Aedes aegypti and a multi-species survey of novel mosquito miRNAs. BMC Genomics 2009, 10:581. BioMed Central Full Text
• [14]Xu MJ, Zhou DH, Nisbet AJ, Huang SY, Fan YF, Zhu XQ: Characterization of mouse brain microRNAs after infection with cyst-forming Toxoplasma gondii. Parasit Vectors 2013, 1:154.
• [15]Skalsky LR, Vanlandingham LD, Scholle F, Higgs S, Cullen RB: Identification of microRNAs expressed in two mosquito vectors, Aedes albopictus and Culex quinquefasciatus. BMC Genomics 2010, 11:119. BioMed Central Full Text
• [16]Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ: miRBase: tools for microRNA genomics. Nucleic Acids Res 2008, 36:D154-D158.
• [17]Gu J, Hu W, Wu J, Zheng P, Chen M, James AA, Chen X, Tu Z: miRNA genes of an invasive vector mosquito, Aedes albopictus. PLoS One 2013, 7:e67638.
• [18]Winter F, Edaye S, Hüttenhofer A, Brune C: Anopheles gambiae miRNAs as actors of defence reaction against plasmodium invasion. Nucleic Acids Res 2007, 35:6953-6962.
• [19]Puthiyakunnon S, Yao Y, Li Y, Gu J, Peng H, Chen X: Functional characterization of three MicroRNAs of the Asian tiger mosquito, Aedes albopictus. Parasit Vectors 2013, 1:230.
• [20]Mead EA, Tu Z: Cloning, characterization, and expression of microRNAs from the Asian malaria mosquito, Anopheles stephensi. BMC Genomics 2008, 9:244. BioMed Central Full Text
• [21]Chatterjee R, Chaudhuri K: An approach for the identification of microRNA with an application to Anopheles gambiae. Acta Biochim Pol 2006, 2:303-309.
• [22]Geng YJ, Gao ST, Huang DN, Zhao YR, Liu JP, Li XH, Zhang RL: Differentially expressed genes between female and male adult Anopheles anthropophagus. Parasitol Res 2009, 105:843-851.
• [23]Friedlander MR, Chen W, Adamidi C, Maaskola J, Einspanier R, Knespel S, Rajewsky N: Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol 2008, 26:407-415.
• [24]Zuker M: Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003, 31:3406-3415.
• [25]Ruby JG, Stark A, Johnston WK, Kellis M, Bartel DP, Lai EC: Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res 2007, 17:1850-1864.
• [26]Léger P, Lara E, Jagla B, Sismeiro O, Mansuroglu Z, Coppée JY, Bonnefoy E, Bouloy M: Dicer-2- and piwi-mediated RNA interference in Rift Valley fever virus-infected mosquito cells. J Virol 2013, 3:1631-1648.
• [27]Morazzani EM, Wiley MR, Murreddu MG, Adelman ZN, Myles KM: Production of virus-derived ping-pong-dependent piRNA-like small RNAs in the mosquito soma. PLoS Pathog 2012, 1:e1002470.
• [28]Sinka ME, Bangs MJ, Manguin S, Coetzee M, Mbogo CM, Hemingway J, Patil AP, Temperley WH, Gething PW, Kabaria CW, Okara RM, Van Boeckel T, Godfray HC, Harbach RE, Hay SI: The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic précis. Parasit Vectors 2010, 3:117. BioMed Central Full Text
• [29]Xu MJ, Wang CR, Huang SY, Fu JH, Zhou DH, Chang QC, Zheng X, Zhu XQ: Identification and characterization of microRNAs in the pancreatic fluke Eurytrema pancreaticum. Parasit Vectors 2013, 6:25. BioMed Central Full Text
• [30]Iwakiri Y: A role of miR-33 for cell cycle progression and cell proliferation. Cell Cycle 2012, 6:1057-1058.
• [31]Valastyan S, Weinberg RA: miR-31: a crucial overseer of tumor metastasis and other emerging roles. Cell Cycle 2010, 11:2124-2129.
• [32]Augoff K, Das M, Bialkowska K, McCue B, Plow EF, Sossey-Alaoui K: miR-31 is a broad regulator of β1-integrin expression and function in cancer cells. Mol Cancer Res 2011, 11:1500-1508.
• [33]Ai L, Xu MJ, Chen MX, Zhang YN, Chen SH, Guo J, Cai YC, Zhou XN, Zhu XQ, Chen JX: Characterization of microRNAs in Taenia saginata of zoonotic significance by Solexa deep sequencing and bioinformatics analysis. Parasitol Res 2012, 6:2373-2378.
• [34]Kim YK, Yeo J, Kim B, Ha M, Kim VN: Short structured RNAs with low GC content are selectively lost during extraction from a small number of cells. Mol Cell 2012, 46:893-895.