Thermal plasticity of the miRNA transcriptome during Senegalese sole development

BMC Genomics

Jorge MO Fernandes²  Sofia Engrola⁴  Luis EC Conceição³  Luisa MP Valente¹  Arvind YM Sundaram²  Catarina Campos⁴ 

[1]CIIMAR/CIMAR, Centro Interdisciplinar de Investigação Marinha e Ambiental and ICBAS–Instituto de Ciências Biomédicas de Abel Salazar, Rua dos Bragas, Porto 289, 4050-123, Portugal

[2]Faculty of Biosciences and Aquaculture, University of Nordland, Bodø 8049, Norway

[3]Sparos Lda, CRIA, Universidade do Algarve, Campus de Gambelas, Faro 8005-139, Portugal

[4]CCMAR/CIMAR, Centro de Ciências do Mar, Faro 8005-139, Portugal

关键词: Epigenetics;    Growth;    Myogenesis;    Embryonic temperature;    miRNA;    Solea senegalensis;   

Others  :  857012
DOI  :  10.1186/1471-2164-15-525

 received in 2013-10-20, accepted in 2014-06-17,  发布年份 2014

【 摘 要 】

Background

Several miRNAs are known to control myogenesis in vertebrates. Some of them are specifically expressed in muscle while others have a broader tissue expression but are still involved in establishing the muscle phenotype. In teleosts, water temperature markedly affects embryonic development and larval growth. It has been previously shown that higher embryonic temperatures promoted faster development and increased size of Senegalese sole (Solea senegalensis) larvae relatively to a lower temperature. The role of miRNAs in thermal-plasticity of growth is hitherto unknown. Hence, we have used high-throughput SOLiD sequencing to determine potential changes in the miRNA transcriptome in Senegalese sole embryos that were incubated at 15°C or 21°C until hatching and then reared at a common temperature of 21°C.

Results

We have identified 320 conserved miRNAs in Senegalese sole, of which 48 had not been previously described in teleosts. mir-17a-5p, mir-26a, mir-130c, mir-206-3p, mir-181a-5p, mir-181a-3p and mir-199a-5p expression levels were further validated by RT- qPCR. The majority of miRNAs were dynamically expressed during early development, with peaks of expression at pre-metamorphosis or metamorphosis. Also, a higher incubation temperature (21°C) was associated with expression of some miRNAs positively related with growth (e.g., miR-17a, miR-181-5p and miR-206) during segmentation and at hatching. Target prediction revealed that these miRNAs may regulate myogenesis through MAPK and mTOR pathways. Expression of miRNAs involved in lipid metabolism and energy production (e.g., miR-122) also differed between temperatures. A miRNA that can potentially target calpain (miR-181-3p), and therefore negatively regulate myogenesis, was preferentially expressed during segmentation at 15°C compared to 21°C.

Conclusions

Temperature has a strong influence on expression of miRNAs during embryonic and larval development in fish. Higher expression levels of miR-17a, miR-181-5p and miR-206-3p and down-regulation of miR-181a-3p at 21°C may promote myogenesis and are in agreement with previous studies in Senegalese sole, which reported enhanced growth at higher embryonic temperatures compared to 15°C. Moreover, miRNAs involved in lipid metabolism and energy production may also contribute to increased larval growth at 21°C compared to 15°C. Taken together, our data indicate that miRNAs may play a role in temperature-induced phenotypic plasticity of growth in teleosts.

【 授权许可】

   
2014 Campos et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Chang TC, Mendell JT: microRNAs in vertebrate physiology and human disease. Annu Rev Genomics Hum Genet 2007, 8:215-239.
• [2]Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116(2):281-297.
• [3]Wood AW, Duan C, Bern HA: Insulin-like growth factor signaling in fish. Int Rev Cytol 2005, 243:215-285.
• [4]Nave BT, Ouwens M, Withers DJ, Alessi DR, Shepherd PR: Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J 1999, 344(Pt 2):427-431.
• [5]Jones NC, Fedorov YV, Rosenthal RS, Olwin BB: ERK1/2 is required for myoblast proliferation but is dispensable for muscle gene expression and cell fusion. J Cell Physiol 2001, 186(1):104-115.
• [6]Ren H, Accili D, Duan C: Hypoxia converts the myogenic action of insulin-like growth factors into mitogenic action by differentially regulating multiple signaling pathways. Proc Natl Acad Sci U S A 2010, 107(13):5857-5862.
• [7]Yecies JL, Zhang HH, Menon S, Liu S, Yecies D, Lipovsky AI, Gorgun C, Kwiatkowski DJ, Hotamisligil GS, Lee CH, Manning BD: Akt stimulates hepatic SREBP1c and lipogenesis through parallel mTORC1-dependent and independent pathways. Cell Metab 2011, 14(1):21-32.
• [8]Fornari F, Milazzo M, Chieco P, Negrini M, Calin GA, Grazi GL, Pollutri D, Croce CM, Bolondi L, Gramantieri L: MiR-199a-3p regulates mTOR and c-Met to influence the doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res 2010, 70(12):5184-5193.
• [9]Merkel O, Hamacher F, Laimer D, Sifft E, Trajanoski Z, Scheideler M, Egger G, Hassler MR, Thallinger C, Schmatz A, Turner SD, Greil R, Kenner L: Identification of differential and functionally active miRNAs in both anaplastic lymphoma kinase (ALK) + and ALK- anaplastic large-cell lymphoma. Proc Natl Acad Sci U S A 2010, 107(37):16228-16233.
• [10]Williams A, Henao-Mejia J, Harman CC, Flavell RA: miR-181 and Metabolic Regulation in the Immune System. Cold Spring Harb Symp Quant Biol 2013. doi:10.1101/sqb.2013.78.020024
• [11]Naguibneva I, Ameyar-Zazoua M, Polesskaya A, Ait-Si-Ali S, Groisman R, Souidi M, Cuvellier S, Harel-Bellan A: The microRNA miR-181 targets the homeobox protein Hox-A11 during mammalian myoblast differentiation. Nat Cell Biol 2006, 8(3):278-284.
• [12]Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang DZ: The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 2006, 38(2):228-233.
• [13]Johnston IA, Lee HT, Macqueen DJ, Paranthaman K, Kawashima C, Anwar A, Kinghorn JR, Dalmay T: Embryonic temperature affects muscle fibre recruitment in adult zebrafish: genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes. J Exp Biol 2009, 212(Pt 12):1781-1793.
• [14]Yan X, Ding L, Li Y, Zhang X, Liang Y, Sun X, Teng CB: Identification and profiling of microRNAs from skeletal muscle of the common carp. PLoS One 2012, 7(1):e30925.
• [15]Esau C, Davis S, Murray SF, Yu XX, Pandey SK, Pear M, Watts L, Booten SL, Graham M, McKay R, Subramaniam A, Propp S, Lollo BA, Freier S, Bennett CF, Bhanot S, Monia BP: miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab 2006, 3(2):87-98.
• [16]Rayner KJ, Suarez Y, Davalos A, Parathath S, Fitzgerald ML, Tamehiro N, Fisher EA, Moore KJ, Fernandez-Hernando C: MiR-33 contributes to the regulation of cholesterol homeostasis. Science 2010, 328(5985):1570-1573.
• [17]Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T: Identification of tissue-specific microRNAs from mouse. Curr Biol 2002, 12(9):735-739.
• [18]Mennigen JA, Panserat S, Larquier M, Plagnes-Juan E, Medale F, Seiliez I, Skiba-Cassy S: Postprandial regulation of hepatic microRNAs predicted to target the insulin pathway in rainbow trout. PLoS One 2012, 7(6):e38604.
• [19]Bizuayehu TT, Lanes CF, Furmanek T, Karlsen BO, Fernandes JM, Johansen SD, Babiak I: Differential expression patterns of conserved miRNAs and isomiRs during Atlantic halibut development. BMC Genomics 2012, 13:11.
• [20]Mennigen JA, Skiba-Cassy S, Panserat S: Ontogenesis of expression of metabolic genes and microRNAs in rainbow trout alevins during the transition from the endogenous to the exogenous feeding period. J Exp Biol 2013, 216:1597-1608.
• [21]Johnston IA: Environment and plasticity of myogenesis in teleost fish. J Exp Biol 2006, 209(Pt 12):2249-2264.
• [22]Imsland AK, Foss A, Conceição LEC, Dinis MT, Delbare D, Schram E, Kamstra A, Rema P, White P: A review of the culture potential of Solea solea and S. senegalensis. Rev Fish Biol Fisher 2003, 13(4):379-407.
• [23]Campos C, Valente LM, Conceicao LE, Engrola S, Sousa V, Rocha E, Fernandes JM: Incubation temperature induces changes in muscle cellularity and gene expression in Senegalese sole (Solea senegalensis). Gene 2013, 516(2):209-217.
• [24]Levy C, Khaled M, Iliopoulos D, Janas MM, Schubert S, Pinner S, Chen PH, Li S, Fletcher AL, Yokoyama S, Scott KL, Garraway LA, Song JS, Granter SR, Turley SJ, Fisher DE, Novina CD: Intronic miR-211 assumes the tumor suppressive function of its host gene in melanoma. Mol Cell 2010, 40(5):841-849.
• [25]Zhai Q, Zhou L, Zhao C, Wan J, Yu Z, Guo X, Qin J, Chen J, Lu R: Identification of miR-508-3p and miR-509-3p that are associated with cell invasion and migration and involved in the apoptosis of renal cell carcinoma. Biochem Biophys Res Commun 2012, 419(4):621-626.
• [26]Boulias K, Horvitz HR: The C. elegans microRNA mir-71 acts in neurons to promote germline-mediated longevity through regulation of DAF-16/FOXO. Cell Metab 2012, 15(4):439-450.
• [27]Guo L, Lu Z: The fate of miRNA* strand through evolutionary analysis: implication for degradation as merely carrier strand or potential regulatory molecule? PLoS One 2010, 5(6):e11387.
• [28]Heisenberg CP, Tada M, Rauch GJ, Saude L, Concha ML, Geisler R, Stemple DL, Smith JC, Wilson SW: Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 2000, 405(6782):76-81.
• [29]Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF: Stages of embryonic development of the zebrafish. Dev Dyn 1995, 203(3):253-310.
• [30]Stickney HL, Barresi MJ, Devoto SH: Somite development in zebrafish. Dev Dyn 2000, 219(3):287-303.
• [31]Trikic MZ, Monk P, Roehl H, Partridge LJ: Regulation of zebrafish hatching by tetraspanin cd63. PLoS One 2011, 6(5):e19683.
• [32]Funes V, Asensio E, Ponce M, Infante C, Canavate JP, Manchado M: Insulin-like growth factors I and II in the sole Solea senegalensis: cDNA cloning and quantitation of gene expression in tissues and during larval development. Gen Comp Endocrinol 2006, 149(2):166-172.
• [33]Darnell DK, Kaur S, Stanislaw S, Konieczka JH, Yatskievych TA, Antin PB: MicroRNA expression during chick embryo development. Dev Dyn 2006, 235(11):3156-3165.
• [34]Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S, Inoue K, Enright AJ, Schier AF: Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 2006, 312(5770):75-79.
• [35]Thatcher EJ, Flynt AS, Li N, Patton JR, Patton JG: MiRNA expression analysis during normal zebrafish development and following inhibition of the Hedgehog and Notch signaling pathways. Dev Dyn 2007, 236(8):2172-2180.
• [36]Pasquinelli AE, Reinhart BJ, Slack F, Martindale MQ, Kuroda MI, Maller B, Hayward DC, Ball EE, Degnan B, Muller P, Spring J, Srinivasan A, Fishman M, Finnerty J, Corbo J, Levine M, Leahy P, Davidson E, Ruvkun G: Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 2000, 408(6808):86-89.
• [37]Xie CX, Xu SL, Yang LL, Ke ZH, Xing JB, Gai JW, Gong XL, Xu LX, Bao BL: mRNA/microRNA Profile at the Metamorphic Stage of Olive Flounder (Paralichthys olivaceus). Comp Funct Genomics 2011, 2011:256038.
• [38]Fernández-Díaz C, Yúfera M, Cañavate JP, Moyano FJ, Alarcón FJ, Díaz M: Growth and physiological changes during metamorphosis of Senegal sole reared in the laboratory. J Fish Biol 2001, 58(4):1086-1097.
• [39]Schreiber AM: Asymmetric craniofacial remodeling and lateralized behavior in larval flatfish. J Exp Biol 2006, 209(Pt 4):610-621.
• [40]Fu YS, Shi ZY, Wang GY, Li WJ, Zhang JL, Jia L: Expression and regulation of miR-1, -133a, -206a, and MRFs by thyroid hormone during larval development in Paralichthys olivaceus. Comp Biochem Physiol B 2012, 161(3):226-232.
• [41]Yufera M, Parra G, Santiago R, Carrascosa M: Growth, carbon, nitrogen and caloric content of Solea senegalensis (Pisces: Soleidae) from egg fertilization to metamorphosis. Marine Biol 1999, 134:43-49.
• [42]Fu Y, Shi Z, Wu M, Zhang J, Jia L, Chen X: Identification and differential expression of microRNAs during metamorphosis of the Japanese flounder (Paralichthys olivaceus). PLoS One 2011, 6(7):e22957.
• [43]Mennigen JA, Martyniuk CJ, Seiliez I, Panserat S, Skiba-Cassy S: Metabolic consequences of microRNA-122 inhibition in rainbow trout: Oncorhynchus mykiss. BMC Genomics 2014, 15:70.
• [44]Wong CF, Tellam RL: MicroRNA-26a targets the histone methyltransferase Enhancer of Zeste homolog 2 during myogenesis. J Biol Chem 2008, 283(15):9836-9843.
• [45]Safdar A, Abadi A, Akhtar M, Hettinga BP, Tarnopolsky MA: miRNA in the regulation of skeletal muscle adaptation to acute endurance exercise in C57Bl/6 J male mice. PLoS One 2009, 4(5):e5610.
• [46]Kim HK, Lee YS, Sivaprasad U, Malhotra A, Dutta A: Muscle-specific microRNA miR-206 promotes muscle differentiation. J Cell Biol 2006, 174(5):677-687.
• [47]Campos C, Valente LMP, Conceição LEC, Engrola S, Fernandes JMO: Temperature affects methylation of the myogenin putative promoter, its expression and muscle cellularity in Senegalese sole larvae. Epigenetics 2013, 8(4):389-397.
• [48]Liu N, Williams AH, Kim Y, McAnally J, Bezprozvannaya S, Sutherland LB, Richardson JA, Bassel-Duby R, Olson EN: An intragenic MEF2-dependent enhancer directs muscle-specific expression of microRNAs 1 and 133. Proc Natl Acad Sci U S A 2007, 104(52):20844-20849.
• [49]Rosenberg MI, Georges SA, Asawachaicharn A, Analau E, Tapscott SJ: MyoD inhibits Fstl1 and Utrn expression by inducing transcription of miR-206. J Cell Biol 2006, 175(1):77-85.
• [50]Ason B, Darnell DK, Wittbrodt B, Berezikov E, Kloosterman WP, Wittbrodt J, Antin PB, Plasterk RH: Differences in vertebrate microRNA expression. Proc Natl Acad Sci U S A 2006, 103(39):14385-14389.
• [51]Juan AH, Kumar RM, Marx JG, Young RA, Sartorelli V: Mir-214-dependent regulation of the polycomb protein Ezh2 in skeletal muscle and embryonic stem cells. Mol Cell 2009, 36(1):61-74.
• [52]Maciotta S, Meregalli M, Cassinelli L, Parolini D, Farini A, Fraro GD, Gandolfi F, Forcato M, Ferrari S, Gabellini D, Bicciato S, Cossu G, Torrente Y: Hmgb3 is regulated by microrna-206 during muscle regeneration. PLoS One 2012, 7(8):e43464.
• [53]Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, Cobb MH: Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 2001, 22(2):153-183.
• [54]Gingras AC, Raught B, Gygi SP, Niedzwiecka A, Miron M, Burley SK, Polakiewicz RD, Wyslouch-Cieszynska A, Aebersold R, Sonenberg N: Hierarchical phosphorylation of the translation inhibitor 4E-BP1. Genes Dev 2001, 15(21):2852-2864.
• [55]Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK: Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol Cell 1999, 3(6):707-716.
• [56]Brugarolas J, Lei K, Hurley RL, Manning BD, Reiling JH, Hafen E, Witters LA, Ellisen LW, Kaelin WG Jr: Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev 2004, 18(23):2893-2904.
• [57]DeYoung MP, Horak P, Sofer A, Sgroi D, Ellisen LW: Hypoxia regulates TSC1/2-mTOR signaling and tumor suppression through REDD1-mediated 14-3-3 shuttling. Genes Dev 2008, 22(2):239-251.
• [58]Cloonan N, Brown MK, Steptoe AL, Wani S, Chan WL, Forrest AR, Kolle G, Gabrielli B, Grimmond SM: The miR-17-5p microRNA is a key regulator of the G1/S phase cell cycle transition. Genome Biol 2008, 9(8):R127.
• [59]Sabapathy K, Hochedlinger K, Nam SY, Bauer A, Karin M, Wagner EF: Distinct roles for JNK1 and JNK2 in regulating JNK activity and c-Jun-dependent cell proliferation. Mol Cell 2004, 15(5):713-725.
• [60]Budanov AV, Karin M: p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 2008, 134(3):451-460.
• [61]Chen CC, Jeon SM, Bhaskar PT, Nogueira V, Sundararajan D, Tonic I, Park Y, Hay N: FoxOs inhibit mTORC1 and activate Akt by inducing the expression of Sestrin3 and Rictor. Dev Cell 2010, 18(4):592-604.
• [62]Honda M, Masui F, Kanzawa N, Tsuchiya T, Toyo-oka T: Specific knockdown of m-calpain blocks myogenesis with cDNA deduced from the corresponding RNAi. Am J Physiol Cell Physiol 2008, 294(4):957-965.
• [63]Campos C, Valente LM, Borges P, Bizuayehu T, Fernandes JM: Dietary lipid levels have a remarkable impact on the expression of growth-related genes in Senegalese sole (Solea senegalensis Kaup). J Exp Biol 2010, 213(2):200-209.
• [64]Fernandes JM, Mackenzie MG, Wright PA, Steele SL, Suzuki Y, Kinghorn JR, Johnston IA: Myogenin in model pufferfish species: Comparative genomic analysis and thermal plasticity of expression during early development. Comp Biochem Physiol Part D Genomics Proteomics 2006, 1(1):35-45.
• [65]Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS: MicroRNA targets in Drosophila. Genome Biol 2003, 5(1):R1.
• [66]Kruger J, Rehmsmeier M: RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Res 2006, 34(Web Server issue):W451-454.