期刊论文详细信息
BMC Genomics
In-depth profiling and analysis of host and viral microRNAs in Japanese flounder (Paralichthys olivaceus) infected with megalocytivirus reveal involvement of microRNAs in host-virus interaction in teleost fish
Li Sun2  Jian Zhang1  Bao-cun Zhang1 
[1] Graduate University of the Chinese Academy of Sciences, Beijing 100049, China;Collaborative Innovation Center of Deep Sea Biology, College of Life Sciences, Zhejiang University, Hangzhou 310058, China
关键词: Virus-host interaction;    Teleost;    Paralichthys olivaceus;    microRNA;    Iridovirus;   
Others  :  1128480
DOI  :  10.1186/1471-2164-15-878
 received in 2014-03-10, accepted in 2014-09-24,  发布年份 2014
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【 摘 要 】

Background

MicroRNAs (miRNAs) regulate gene expression by binding to mRNA transcripts in various biological processes. In mammals and birds, miRNAs are known to play vital parts in both host immune defense and viral infection. However, in lower vertebrates such as teleost, systematic investigations on host and viral miRNAs are lacking.

Results

In this study, we applied high-throughput sequencing technology to identify and analyze both host and viral miRNAs in Japanese flounder (Paralichthys olivaceus), an economically important teleost fish farmed widely in the world, infected with megalocytivirus at a timescale of 14 days divided into five different time points. The results showed that a total of 381 host miRNAs and 9 viral miRNAs were identified, the latter being all novel miRNAs that have no homologues in the currently available databases. Of the host miRNAs, 251 have been reported previously in flounder and other species, and 130 were discovered for the first time. The expression levels of 121 host miRNAs were significantly altered at 2 d to 14 d post-viral infection (pi), and these miRNAs were therefore classified as differentially expressed host miRNAs. The expression levels of all 9 viral miRNAs increased from 0 d pi to 10 d pi and then dropped from 10 d pi to 14 d pi. For the 121 differentially expressed host miRNAs and the 9 viral miRNAs, 243 and 48 putative target genes, respectively, were predicted in flounder. GO and KEGG enrichment analysis revealed that the putative target genes of both host and viral miRNAs were grouped mainly into the categories of immune response, signal transduction, and apoptotic process.

Conclusions

The results of our study provide the first evidences that indicate existence in teleost fish (i) infection-responsive host and viral miRNAs that exhibit dynamic changes in expression profiles during the course of viral infection, and (ii) potential involvement of miRNAs in host-viral interaction.

【 授权许可】

   
2014 Zhang et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Pritchard CC, Cheng HH, Tewari M: MicroRNA profiling: approaches and considerations. Nat Rev Genet 2012, 13(5):358-369.
  • [2]Boss IW, Renne R: Viral miRNAs and immune evasion. BBA-Gene Regul Mech 2011, 1809(11–12):708-714.
  • [3]Chen YT, Kitabayashi N, Zhou XK, Fahey TJ, Scognamiglio T: MicroRNA analysis as a potential diagnostic tool for papillary thyroid carcinoma. Mod Pathol 2008, 21(9):1139-1146.
  • [4]Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebet BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR, Golub TR: MicroRNA expression profiles classify human cancers. Nature 2005, 435(7043):834-838.
  • [5]Rosenfeld N, Aharonov R, Meiri E, Rosenwald S, Spector Y, Zepeniuk M, Benjamin H, Shabes N, Tabak S, Levy A, Lebanony D, Goren Y, Silberschein E, Targan N, Ben-Ari A, Gilad S, Sion-Vardy N, Tobar A, Feinmesser M, Kharenko O, Nativ O, Nass D, Perelman M, Yosepovich A, Shalmon B, Polak-Charcon S, Fridman E, Avniel A, Bentwich I, Bentwich Z, et al.: MicroRNAs accurately identify cancer tissue origin. Nat Biotechnol 2008, 26(4):462-469.
  • [6]Boeri M, Verri C, Conte D, Roz L, Modena P, Facchinetti F, Calabro E, Croce CM, Pastorino U, Sozzi G: MicroRNA signatures in tissues and plasma predict development and prognosis of computed tomography detected lung cancer. Proc Natl Acad Sci U S A 2011, 108(9):3713-3718.
  • [7]Tili E, Michaille JJ, Costinean S, Croce CM: MicroRNAs, the immune system and rheumatic disease. Nat Clin Pract Rheum 2008, 4(10):534-541.
  • [8]Hussain M, Torres S, Schnettler E, Funk A, Grundhoff A, Pijlman GP, Khromykh AA, Asgari S: West Nile virus encodes a microRNA-like small RNA in the 3' untranslated region which up-regulates GATA4 mRNA and facilitates virus replication in mosquito cells. Nucleic Acids Res 2012, 40(5):2210-2223.
  • [9]Singh CP, Singh J, Nagaraju J: A baculovirus-encoded microRNA (miRNA) suppresses its host miRNA biogenesis by regulating the exportin-5 cofactor ran. J Virol 2012, 86(15):7867-7879.
  • [10]Guo XK, Zhang Q, Gao L, Li N, Chen XX, Feng WH: Increasing expression of microRNA 181 inhibits porcine reproductive and respiratory syndrome virus replication and has implications for controlling virus infection. J Virol 2013, 87(2):1159-1171.
  • [11]Jopling CL, Yi MK, Lancaster AM, Lemon SM, Sarnow P: Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 2005, 309(5740):1577-1581.
  • [12]Song LP, Liu H, Gao SJ, Jiang W, Huang WL: Cellular microRNAs inhibit replication of the H1N1 influenza a virus in infected cells. J Virol 2010, 84(17):8849-8860.
  • [13]Pfeffer S, Zavolan M, Grasser FA, Chien MC, Russo JJ, Ju JY, John B, Enright AJ, Marks D, Sander C, Tuschl T: Identification of virus-encoded microRNAs. Science 2004, 304(5671):734-736.
  • [14]Skalsky RL, Cullen BR: Viruses, microRNAs, and host interactions. Annu Rev Microbiol 2010, 64:123-141.
  • [15]Stern-Ginossar N, Elefant N, Zimmermann A, Wolf DG, Saleh N, Biton M, Horwitz E, Prokocimer Z, Prichard M, Hahn G, Goldman-Wohl D, Greenfield C, Yagel S, Hengel H, Altuvia Y, Margalit H, Mandelboim O: Host immune system gene targeting by a viral miRNA. Science 2007, 317(5836):376-381.
  • [16]Sullivan CS: New roles for large and small viral RNAs in evading host defences. Nat Rev Gene 2008, 9(7):503-507.
  • [17]Gupta A, Gartner JJ, Sethupathy P, Hatzigeorgiou AG, Fraser NW: Anti-apoptotic function of a microRNA encoded by the HSV-1 latency-associated transcript. Nature 2006, 442(7098):82-85.
  • [18]Sullivan CS, Grundhoff AT, Tevethia S, Pipas JM, Ganem D: SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature 2005, 435(7042):682-686.
  • [19]Stark TJ, Arnold JD, Spector DH, Yeo GW: High-resolution profiling and analysis of viral and host small RNAs during human cytomegalovirus infection. J Virol 2012, 86(1):226-235.
  • [20]Wu ZH, Hao RZ, Li P, Zhang XA, Liu N, Qiu SF, Wang LG, Wang Y, Xue WZ, Liu K, Yang G, Cui JJ, Zhang CF, Song HB: MicroRNA expression profile of mouse lung infected with 2009 pandemic H1N1 influenza virus. Plos One 2013, 8(9):e74190.
  • [21]Wang Y, Brahmakshatriya V, Zhu HF, Lupiani B, Reddy SM, Yoon BJ, Gunaratne PH, Kim JH, Chen R, Wang JJ, Zhou H: Identification of differentially expressed miRNAs in chicken lung and trachea with avian influenza virus infection by a deep sequencing approach. BMC Genomics 2009, 10(1):512. BioMed Central Full Text
  • [22]Huang TZ, Xu DD, Zhang XB: Characterization of host microRNAs that respond to DNA virus infection in a crustacean. BMC Genomics 2012, 13(1):159. BioMed Central Full Text
  • [23]Ordas A, Kanwal Z, Lindenberg V, Rougeot J, Mink M, Spaink HP, Meijer AH: MicroRNA-146 function in the innate immune transcriptome response of zebrafish embryos to Salmonella typhimurium infection. BMC Genomics 2013, 14(1):696. BioMed Central Full Text
  • [24]Sha Z, Gong G, Wang S, Lu Y, Wang L, Wang Q, Chen S: Identification and characterization of Cynoglossus semilaevis microRNA response to Vibrio anguillarum infection through high-throughput sequencing. Dev Comp Immunol 2014, 44(1):59-69.
  • [25]Wu TH, Pan CY, Lin MC, Hsieh JC, Hui CF, Chen JY: In vivo screening of zebrafish microRNA responses to bacterial infection and their possible roles in regulating immune response genes after lipopolysaccharide stimulation. Fish Physiol Biochem 2012, 38(5):1299-1310.
  • [26]Ariel E, Jensen BB: Challenge studies of European stocks of redfin perch, Perca fluviatilis L., and rainbow trout, Oncorhynchus mykiss (Walbaum), with epizootic haematopoietic necrosis virus. J Fish Dis 2009, 32(12):1017-1025.
  • [27]Drennan JD, Ireland S, LaPatra SE, Grabowski L, Carrothers TK, Cain KD: High-density rearing of white sturgeon Acipenser transmontanus (Richardson) induces white sturgeon iridovirus disease among asymptomatic carriers. Aquac Res 2005, 36(8):824-827.
  • [28]Plumb JA, Noyes AD, Graziano S, Wang J, Mao JH, Chinchar VG: Isolation and identification of viruses from adult largemouth bass during a 1997–1998 survey in the southeastern United States. J Aquat Anim Health 1999, 11(4):391-399.
  • [29]Shi CY, Jia KT, Yang B, Huang J: Complete genome sequence of a Megalocytivirus (family Iridoviridae) associated with turbot mortality in China. Virol J 2010, 7(1):159. BioMed Central Full Text
  • [30]Tapiovaara H, Olesen NJ, Linden J, Rimaila-Parnanen E, von Bonsdorff CH: Isolation of an iridovirus from pike-perch Stizostedion lucioperca. Dis Aquat Organ 1998, 32(3):185-193.
  • [31]Zhang M, Sun K, Sun L: Regulation of autoinducer 2 production and luxS expression in a pathogenic Edwardsiella tarda strain. Microbiology 2008, 154(7):2060-2069.
  • [32]Zhang M, Xiao ZZ, Hu YH, Sun L: Characterization of a megalocytivirus from cultured rock bream, Oplegnathus fasciatus (Temminck & Schlege), in China. Aquac Res 2012, 43(4):556-564.
  • [33]Wang HR, Hu YH, Zhang WW, Sun L: Construction of an attenuated Pseudomonas fluorescens strain and evaluation of its potential as a cross-protective vaccine. Vaccine 2009, 27(30):4047-4055.
  • [34]Ambady S, Wu Z, Dominko T: Identification of novel microRNAs in Xenopus laevis metaphase II arrested eggs. Genesis 2012, 50(3):286-299.
  • [35]Fu YS, Shi ZY, Wu ML, Zhang JL, Jia L, Chen XW: Identification and differential expression of microRNAs during metamorphosis of the Japanese flounder (Paralichthys olivaceus). Plos One 2011, 6(7):e22957.
  • [36]Ding SW, Voinnet O: Antiviral immunity directed by small RNAs. Cell 2007, 130(3):413-426.
  • [37]Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, Chisari FV, David M: Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 2007, 449(7164):919-U913.
  • [38]Ghosh Z, Mallick B, Chakrabarti J: Cellular versus viral microRNAs in host-virus interaction. Nucleic Acids Res 2009, 37(4):1035-1048.
  • [39]Sisk JM, Witwer KW, Tarwater PM, Clements JE: SIV replication is directly downregulated by four antiviral miRNAs. Retrovirology 2013, 10(1):95. BioMed Central Full Text
  • [40]Cameron JE, Yin QY, Fewell C, Lacey M, McBride J, Wang X, Lin Z, Schaefer BC, Flemington EK: Epstein-Barr virus latent membrane protein 1 induces cellular MicroRNA miR-146a, a modulator of lymphocyte signaling pathways. J Virol 2008, 82(4):1946-1958.
  • [41]Jopling CL, Schuetz S, Sarnow P: Position-dependent function for a tandem microRNA miR-122-binding site located in the hepatitis C virus RNA genome. Cell Host Microbe 2008, 4(1):77-85.
  • [42]Yeung ML, Bennasser Y, Myers TG, Jiang GJ, Benkirane M, Jeang KT: Changes in microRNA expression profiles in HIV-1-transfected human cells. Retrovirology 2005, 2(1):81. BioMed Central Full Text
  • [43]Houzet L, Yeung ML, de Lame V, Desai D, Smith SM, Jeang KT: MicroRNA profile changes in human immunodeficiency virus type 1 (HIV-1) seropositive individuals. Retrovirology 2008, 5(1):181.
  • [44]Trobaugh DW, Gardner CL, Sun C, Haddow AD, Wang E, Chapnik E, Mildner A, Weaver SC, Ryman KD, Klimstra WB: RNA viruses can hijack vertebrate microRNAs to suppress innate immunity. Nature 2014, 506(7487):245-248.
  • [45]Anastasiadou E, Boccellato F, Vincenti S, Rosato P, Bozzoni I, Frati L, Faggioni A, Presutti C, Trivedi P: Epstein-Barr virus encoded LMP1 downregulates TCL1 oncogene through miR-29b. Oncogene 2010, 29(9):1316-1328.
  • [46]Nilsen TW: Mechanisms of microRNA-mediated gene regulation in animal cells. Trends Genet 2007, 23(5):243-249.
  • [47]Pezzolesi MG, Platzer P, Waite KA, Eng C: Differential expression of PTEN-targeting microRNAs miR-19a and miR-21 in Cowden Syndrome. Am J Hum Genet 2008, 82(5):1141-1149.
  • [48]Doebele C, Bonauer A, Fischer A, Scholz A, Reiss Y, Urbich C, Hofmann WK, Zeiher AM, Dimmeler S: Members of the microRNA-17-92 cluster exhibit a cell-intrinsic antiangiogenic function in endothelial cells. Blood 2010, 115(23):4944-4950.
  • [49]Chen B, She SF, Li DT, Liu ZH, Yang XJ, Zeng ZR, Liu FB: Role of miR-19a targeting TNF-alpha in mediating ulcerative colitis. Scand J Gastroenterol 2013, 48(7):815-824.
  • [50]Carotta S, Dakic A, D'Amico A, Pang SHM, Greig KT, Nutt SL, Wu L: The transcription factor pu.1 controls dendritic cell development and Flt3 cytokine receptor expression in a dose-dependent manner. Immunity 2010, 32(5):628-641.
  • [51]Chang HC, Sehra S, Goswami R, Yao WG, Yu Q, Stritesky GL, Jabeen R, McKinley C, Ahyi AN, Han L, Nguyen ET, Robertson MJ, Perumal NB, Tepper RS, Nutt SL, Kaplan MH: The transcription factor PU.1 is required for the development of IL-9-producing T cells and allergic inflammation. Nat Immunol 2010, 11(6):527-U598.
  • [52]Resnicoff M, Abraham D, Yutanawiboonchai W, Rotman HL, Kajstura J, Rubin R, Zoltick P, Baserga R: The insulin-like growth-factor-I receptor protects tumor-cells from apoptosis in-vivo. Cancer Res 1995, 55(11):2463-2469.
  • [53]Rubin R, Baserga R: Insulin-like growth-factor-I receptor - its role in cell-proliferation, apoptosis, and tumorigenicity. Lab Invest 1995, 73(3):311-331.
  • [54]Guicciardi ME, Deussing J, Miyoshi H, Bronk SF, Svingen PA, Peters C, Kaufmann SH, Gores GJ: Cathepsin B contributes to TNF-alpha-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c. J Clin Invest 2000, 106(9):1127-1137.
  • [55]Foghsgaard L, Wissing D, Mauch D, Lademann U, Bastholm L, Boes M, Elling F, Leist M, Jaattela M: Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J Cell Biol 2001, 153(5):999-1009.
  • [56]Everett H, McFadden G: Apoptosis: an innate immune response to virus infection. Trends Microbiol 1999, 7(4):160-165.
  • [57]Cuconati A, White E: Viral homologs of BCL-2: role of apoptosis in the regulation of virus infection. Genes Dev 2002, 16(19):2465-2478.
  • [58]Loveday EK, Svinti V, Diederich S, Pasick J, Jean F: Temporal- and strain-specific host microRNA molecular signatures associated with swine-origin H1N1 and avian-origin H7N7 influenza A virus infection. J Virol 2012, 86(11):6109-6122.
  • [59]Boldin MP, Taganov KD, Rao DS, Yang LL, Zhao JL, Kalwani M, Garcia-Flores Y, Luong M, Devrekanli A, Xu J, Sun G, Tay J, Linsley PS, Baltimore D: miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J Exp Med 2011, 208(6):1189-1201.
  • [60]Tang YJ, Luo XB, Cui HJ, Ni XM, Yuan M, Guo YZ, Huang XF, Zhou HB, de Vries N, Tak PP, Chen S, Shen N: MicroRNA-146a contributes to abnormal activation of the type I interferon pathway in human lupus by targeting the key signaling proteins. Arthritis Rheum 2009, 60(4):1065-1075.
  • [61]Fukami K, Inanobe S, Kanemaru K, Nakamura Y: Phospholipase C is a key enzyme regulating intracellular calcium and modulating the phosphoinositide balance. Prog Lipid Res 2010, 49(4):429-437.
  • [62]Bozym RA, Morosky SA, Kim KS, Cherry S, Coyne CB: Release of intracellular calcium stores facilitates coxsackievirus entry into polarized endothelial cells. PLoS Pathog 2010, 6(10):e1001135.
  • [63]Sullivan CS, Grundhoff A: Identification of viral microRNAs. Methods Enzymol 2007, 427:3-23.
  • [64]Jurak I, Silverstein LB, Sharma M, Coen DM: Herpes simplex virus is equipped with RNA- and protein-based mechanisms to repress expression of ATRX, an effector of intrinsic immunity. J Virol 2012, 86(18):10093-10102.
  • [65]Umbach JL, Wang K, Tang S, Krause PR, Mont EK, Cohen JI, Cullen BR: Identification of viral microRNAs expressed in human sacral ganglia latently infected with herpes simplex Virus 2. J Virol 2010, 84(2):1189-1192.
  • [66]Gurtan AM, Lu V, Bhutkar A, Sharp PA: In vivo structure-function analysis of human Dicer reveals directional processing of precursor miRNAs. RNA 2012, 18(6):1116-1122.
  • [67]Yan Y, Cui HC, Jiang SS, Huang YH, Huang XH, Wei SN, Xu WY, Qin QW: Identification of a novel marine fish virus, singapore grouper iridovirus-encoded microRNAs expressed in grouper cells by solexa sequencing. Plos One 2011, 6(4):e19148.
  • [68]Skalsky RL, Samols MA, Plaisance KB, Boss IW, Riva A, Lopez MC, Baker HV, Renne R: Kaposi's sarcoma-associated herpesvirus encodes an ortholog of miR-155. J Virol 2007, 81(23):12836-12845.
  • [69]Aoki T, Hikima J, Hwang SD, Jung TS: Innate immunity of finfish: primordial conservation and function of viral RNA sensors in teleosts. Fish Shellfish Immunol 2013, 35(6):1689-1702.
  • [70]Sato M, Suemori H, Hata N, Asagiri M, Ogasawara K, Nakao K, Nakaya T, Katsuki M, Noguchi S, Tanaka N, Taniguchi T: Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 2000, 13(4):539-548.
  • [71]Honda K, Yanai H, Negishi H, Asagiri M, Sato M, Mizutani T, Shimada N, Ohba Y, Takaoka A, Yoshida N, Taniguchi T: IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005, 434(7034):772-777.
  • [72]Reichlin A, Hu Y, Meffre E, Nagaoka H, Gong SC, Kraus M, Rajewsky K, Nussenzweig MC: B cell development is arrested at the immature B cell stage in mice carrying a mutation in the cytoplasmic domain of immunoglobulin beta. J Exp Med 2001, 193(1):13-23.
  • [73]Meffre E, Nussenzweig MC: Deletion of immunoglobulin β in developing B cells leads to cell death. Proc Natl Acad Sci U S A 2002, 99(17):11334-11339.
  • [74]Tsujimoto Y, Shimizu S: The voltage-dependent anion channel: an essential player in apoptosis. Biochimie 2002, 84(2–3):187-193.
  • [75]Osada M, Park HL, Park MJ, Liu JW, Wu GJ, Trink B, Sidransky D: A p53-type response element in the GDF15 promoter confers high specificity for p53 activation. Biochem Biophys Res Commun 2007, 354(4):913-918.
  • [76]Li PX, Wong J, Ayed A, Ngo D, Brade AM, Arrowsmith C, Austin RC, Klamut HJ: Placental transforming growth factor-beta is a downstream mediator of the growth arrest and apoptotic response of tumor cells to DNA damage and p53 overexpression. J Biol Chem 2000, 275(26):20127-20135.
  • [77]Balachandran S, Roberts PC, Brown LE, Truong H, Pattnaik AK, Archer DR, Barber GN: Essential role for the dsRNA-dependent protein kinase PKR in innate immunity to viral infection. Immunity 2000, 13(1):129-141.
  • [78]Gil J, Esteban M: Induction of apoptosis by the dsRNA-dependent protein kinase (PKR): Mechanism of action. Apoptosis 2000, 5(2):107-114.
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