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Genes involved in miRNA biogenesis affect meiosis and fertility

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Abstract

MicroRNAs (miRNAs) are a class of small (containing about 22 nucleotides) single-stranded non-coding RNAs that regulate gene expression at the post-transcriptional level in plants and animals, being absent from unicellular organisms. They act on diverse key physiological and cellular processes, such as development and tissue differentiation, cell identity, cell cycle progression, and programmed cell death. They are also likely to be involved in a broad spectrum of human diseases. Particularly, this review examines and summarizes work characterizing the function of miRNAs in gametogenesis and fertility. Although numerous studies have elucidated the involvement of reproductive-specific small interfering RNAs (siRNAs) in regulating germ cell development and meiosis, less is known about the role of miRNAs in these processes. We focus on the study of hypomorphic and null alleles of genes encoding components of miRNA biogenesis in both plants (Arabidopsis thaliana) and mammals (Mus musculus). We compare the consequences of the presence of these mutations on male meiosis in both species.

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Abbreviations

AGO:

ARGONAUTE

ATM:

Ataxia-Telangiectasia Mutated

DCL1:

DICER-LIKE-1

DSB:

DNA double-strand break

HEN1:

HUA ENHANCER 1

HR:

Homologous recombination

HST:

HASTY

HYL1:

HYPONASTIC LEAVES 1

KO:

Knockout

miRNA:

MicroRNA

MMC:

Megaspore mother cell

MSCI:

Meiotic sex chromosome inactivation

phasiRNA:

Phased small interfering RNA

piRNA:

PIWI-interacting RNA

PMC:

Pollen mother cell

RISC:

RNA-induced silencing complex

SC:

Synaptonemal complex

SE:

SERRATE

SPO11:

SPORULATION DEFECTIVE 11

siRNA:

Small interfering RNA

SYCP1:

Synaptonemal complex protein 1

TRBP:

Human immunodeficiency virus trans-activating protein response RNA-binding protein

WT:

Wild-type

References

  • Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, Chien M, Russo JJ, Ju J, Sheridan R, Sander C, Zavolan M, Tuschl T (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442:203–207

    Article  CAS  PubMed  Google Scholar 

  • Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci U S A 102:11928–11933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–366

    Article  CAS  PubMed  Google Scholar 

  • Bollman KM, Aukerman MJ, Park MY, Hunter C, Berardini TZ, Poethig RS (2003) HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development 130:1493–1504

    Article  CAS  PubMed  Google Scholar 

  • Bologna NG, Voinnet O (2014) The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu Rev Plant Biol 65:473–503

    Article  CAS  PubMed  Google Scholar 

  • Borges F, Pereira PA, Slotkin RK (2011) MicroRNA activity in the Arabidopsis male germline. J Exp Bot 62:1611–1620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bukhari SI, Vasquez-Rifo A, Gagné D, Paquet ER, Zetka M, Robert C, Masson JY, Simard MJ (2012) The microRNA pathway controls germ cell proliferation and differentiation in C. elegans. Cell Res 22:1034–1045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chávez Montes RA, de Fátima Rosas-Cárdenas F, De Paoli E, Accerbi M, Rymarquis LA, Mahalingam G, Marsch-Martínez N, Meyers BC, Green PJ, de Folter S (2014) Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs. Nat Commun 5:3722

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Li X, Guo J, Zhang P, Zeng W (2017) The roles of microRNAs in regulation of mammalian spermatogenesis. J Anim Sci Biotechnol 8:35

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Choi K, Zhao X, Kelly KA, Venn O, Higgins JD, Yelina NE, Hardcastle TJ, Ziolkowski PA, Copenhaver GP, Franklin FC, McVean G, Henderson IR (2013) Arabidopsis meiotic crossover hot spots overlap with H2A.Z nucleosomes at gene promoters. Nat Genet 45:1327–1336

    Article  CAS  PubMed  Google Scholar 

  • D’Ario M, Griffiths-Jones S, Kim M (2017) Small RNAs: big impact on plant development. Trends Plant Sci 22:1056–1068

    Article  PubMed  CAS  Google Scholar 

  • Djami-Tchatchou AT, Sanan-Mistra N, Ntushelo K, Dubery IA (2017) Functional roles of microRNAs in agronomically important plants-potential as targets for crop improvement and protection. Frontiers Plant Sci 8:378

    Article  Google Scholar 

  • Dukowic-Schulze S, Sundararajan A, Ramaraj T, Kianian S, Pawlowski WP, Mudge J, Chen C (2016) Novel meiotic miRNAs and indications for a role of phasiRNAs in meiosis. Frontiers Plant Sci 7:762

  • Girard A, Sachidanandam R, Hannon GJ, Carmell MA (2006) A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442:199–202

    Article  PubMed  Google Scholar 

  • Greenlee AR, Shiao MS, Snyder E, Buaas FW, Gu T, Stearns TM, Sharma M, Murchison EP, Puente GC, Braun RE (2012) Deregulated sex chromosome gene expression with male germ cell-specific loss of Dicer1. PLoS One 7:e46359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grimson A, Srivastava M, Fahey B, Woodcroft BJ, Chiang HR, King N, Degnan BM, Rokhsar DS, Bartel DP (2008) Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455:1193–1197

    Article  CAS  PubMed  Google Scholar 

  • Grivna ST, Beyret E, Wang Z, Lin H (2006) A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 20:1709–1714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi K, Chuva de Sousa Lopes SM, Kaneda M, Tang F, Hajkova P, Lao K, O’Carroll D, Das P, Tarakhovsky A, Miska EA, Surani MA (2008) MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS One 3:e1738

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hilz S, Fogarty EA, Modzelewski AJ, Cohen PE, Grimson A (2017) Transcriptome profiling of the developing male germ line identifies the miR-29 family as a global regulator during meiosis. RNA Biol 14:219–235

    Article  PubMed  Google Scholar 

  • Huntzinger E, Izaurralde E (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12:99–110

    Article  CAS  PubMed  Google Scholar 

  • Iwakawa HO, Tomari Y (2015) The functions of MicroRNAs: mRNA decay and translational repression. Trends Cell Biol 25:651–665

    Article  CAS  PubMed  Google Scholar 

  • Jacobsen SE, Running MP, Meyerowitz EM (1999) Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development 126:5231–5243

    CAS  PubMed  Google Scholar 

  • Johnson C, Kasprzewska A, Tennessen K, Fernandes J, Nan GL, Walbot V, Sundaresan V, Vance V, Bowman LH (2009) Clusters and superclusters of phased small RNAs in the developing inflorescence of rice. Genome Res 19:1429–1440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones AM, Chory J, Dangl JL, Estelle M, Jacobsen SE, Meyerowitz EM, Nordborg M, Weigel D (2008) The impact of Arabidopsis on human health: diversifying our portfolio. Cell 133:939–943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Korhonen HM, Meikar O, Yadav RP, Papaioannou MD, Romero Y, Da Ros M, Herrera PL, Toppari J, Nef S, Kotaja N (2011) Dicer is required for haploid male germ cell differentiation in mice. PLoS One 6:e24821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lau NC, Seto AG, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel DP, Kingston RE (2006) Characterization of the piRNA complex from rat testes. Science 313:363–367

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Radmark O, Kim S (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425:415–419

    Article  CAS  PubMed  Google Scholar 

  • Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB (2003) Prediction of mammalian microRNA targets. Cell 115:787–798

    Article  CAS  PubMed  Google Scholar 

  • Lian H, Li X, Liu Z, He Y (2013) HYL1 is required for establishment of stamen architecture with four microsporangia in Arabidopsis. J Exp Bot (11):3307–3410

  • Lim LP, Glasner ME, Yekta S, Burge CB, Bartel DP (2003) Vertebrate miRNAs genes. Science 299:1540

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ, Hammond SM, Joshua-Tor L, Hannon GJ (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305:1437–1441

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Niu M, Yao C, Hai Y, Yuan Q, Liu Y, Guo Y, Li Z, He Z (2015) Fractionation of human spermatogenic cells using STA-PUT gravity sedimentation and their miRNA profiling. Sci Rep 5:8084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu YC, Chen WL, Kung WH (2017) Plant miRNAs found in human circulating system provide evidences of cross kingdom RNAi. BMC Genomics 18:112

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Llave C, Xie Z, Kasschau KD, Carrington JC (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297:2053–2056

    Article  CAS  PubMed  Google Scholar 

  • Lobbes D, Rallapalli G, Schmidt DD, Martin C, Clarke J (2006) SERRATE: a new player on the plant microRNA scene. EMBO Rep 7:1052–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma X, Cao X, Mo B, Chen X (2013) Trip to ER: MicroRNA-mediated translational repression in plants. RNA Biol 10:1586–1592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maatouk DM, Loveland KL, McManus MT, Moore K, Harfe BD (2008) Dicer1 is required for differentiation of the mouse male germline. Biol Reprod 79:696–703

    Article  CAS  PubMed  Google Scholar 

  • Mansoori B, Mohammadi A, Shirjang S, Baradaran B (2017) MicroRNAs in the diagnosis and treatment of cancer. Immunol Investig 46:880–897

    Article  CAS  Google Scholar 

  • McCreight JC, Schneider SE, Wilburn DB, Swanson WJ (2017) Evolution of miRNA in primates. PLoS One 12:e0176596

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T (2004) Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 15:185–197

    Article  CAS  PubMed  Google Scholar 

  • Meunier J, Lemoine F, Soumillon M, Liechti A, Weier M, Guschanski K, Hu H, Khaitovich P, Kaessmann H (2013) Birth and expression evolution of mammalian microRNAs. Genome Res 23:34–45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mishra A, Bohra A (2018) Non-coding RNAs and plant sterility: current knowledge and future prospects. Plant Cell Rep 37:177–191

    Article  CAS  PubMed  Google Scholar 

  • Mochizuki K, Gorovsky MA (2005) A Dicer-like protein in Tetrahymena has distinct functions in genome rearrangement, chromosome segregation, and meiotic prophase. Genes Dev 19:77–89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Modzelewski AJ, Holmes S, Hilz S, Grimson A, Cohen PE (2012) AGO4 regulates entry to meiosis and influences silencing of sex chromosomes in the male mouse germline. Dev Cell 23:251–264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Modzelewski AJ, Hilz S, Crate EA, Schweidenback CT, Fogarty EA, Grenier JK, Freire R, Cohen PE, Grimson A (2015) Dgcr8 and Dicer are essential for sex chromosome integrity during meiosis in males. J Cell Sci 128:2314–2327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murchison EP, Stein P, Xuan Z, Pan H, Zhang MQ, Schultz RM, Hannon GJ (2007) Critical roles for Dicer in the female germline. Genes Dev 21:682–693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliver C, Pradillo M, Jover-Gil S, Cuñado N, Ponce MR, Santos JL (2017) Loss of function of Arabidopsis micro-RNA machinery genes impairs fertility, and has effects on homologous recombination and meiotic chromosome dynamics. Sci Reports 7:9280

    Article  CAS  Google Scholar 

  • Papaioannou MD, Pitetti JL, Ro S, Park C, Aubry F, Schaad O, Vejnar CE, Kühne F, Descombes P, Zdobnov EM, McManus MT, Guillou F, Harfe BD, Yan W, Jégou B, Nef S (2009) Sertoli cell Dicer is essential for spermatogenesis in mice. Dev Biol 326:250–259

    Article  CAS  PubMed  Google Scholar 

  • Papp I, Mette MF, Aufsatz W, Daxinger L, Schauer SE, Ray A, van der Winden J, Matzke M, Matzke AJ (2003) Evidence for nuclear processing of plant micro RNA and short interfering RNA precursors. Plant Physiol 132:1382–1390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park MY, Wu G, Gonzalez-Sulser A, Vaucheret H, Poethig RS (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci U S A 102:3691–3696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520

    Article  CAS  PubMed  Google Scholar 

  • Romero Y, Meikar O, Papaioannou MD, Conne B, Grey C, Weier M, Pralong F, De Massy B, Kaessmann H, Vassalli JD, Kotaja N, Nef S (2011) Dicer1 depletion in male germ cells leads to infertility due to cumulative meiotic and spermiogenic defects. PLoS One 6:e25241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schnickel R, Boyerinas B, Park SM, Peter ME (2008) MicroRNAs: key players in the immune system, differentiation, tumorigenesis and cell death. Oncogene 27:5959–5974

    Article  CAS  Google Scholar 

  • Schott J, Stoecklin G (2010) Networks controlling mRNA decay in the immune system. Wiley Interdiscip Rev RNA 1:432–456

    Article  CAS  PubMed  Google Scholar 

  • Shabalina SA, Koonin EV (2016) Origins and evolution of eukaryotic RNA interference. Trends Ecol Evol 23:578–587

    Article  Google Scholar 

  • Song R, Hennig G, Wu Q, Jose C, Zheng H, Yan W (2011) Male germ cells express abundant endogenous siRNAs. Proc Natl Acad Sci U S A 108:13159–13164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song X, Li P, Zhai J, Zhou M, Ma L, Liu B, Jeong DH, Nakano M, Cao S, Liu C, Chu C, Wang XJ, Green PJ, Meyers BC, Cao X (2012) Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J 69:462–474

    Article  CAS  PubMed  Google Scholar 

  • Stein P, Rozhkov NV, Li F, Cárdenas FL, Davydenko O, Vandivier LE, Gregory BD, Hannon GJ, Schultz RM (2015) Essential role for endogenous siRNAs during meiosis in mouse oocytes. PLoS Genet 11:e1005013

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Suh N, Baehner L, Moltzahn F, Melton C, Shenoy A, Chen J, Blelloch R (2010) MicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr Biol 20:271–277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan T, Zhang Y, Ji W, Zheng P (2014) miRNA signature in mouse spermatogonial stem cells revealed by high-throughput sequencing. Biomed Res Int 154251:1–11

    Google Scholar 

  • Tang F, Kaneda M, O'Carroll D, Hajkova P, Barton SC, Sun YA, Lee C, Tarakhovsky A, Lao K, Surani MA (2007) Maternal microRNAs are essential for mouse zygotic development. Genes Dev 21:644–648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang G, Reinhart BJ, Bartel DP, Zamore PD (2003) A biochemical framework for RNA silencing in plants. Genes Dev 17:49–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tarver JE, Donoghue PCJ, Peterson KJ (2012) Do miRNAs have a deep evolutionary history? BioEssays 34:857–866

    Article  CAS  PubMed  Google Scholar 

  • Taylor RS, Tarver JE, Hiscock SJ, Donoghue PC (2014) Evolutionary history of plant microRNAs. Trends Plant Sci 19:175–182

    Article  CAS  PubMed  Google Scholar 

  • Telfer A, Bollman KM, Poethig RS (1997) Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development 124:645–654

    CAS  PubMed  Google Scholar 

  • Telfer A, Poethig RS (1998) HASTY: a gene that regulates the timing of shoot maturation in Arabidopsis thaliana. Development 125:1889–1898

    CAS  PubMed  Google Scholar 

  • Watanabe T, Takeda A, Tsukiyama T, Mise K, Okuno T, Sasaki H, Minami N, Imai H (2006) Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev 20:1732–1743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Q, Song R, Ortogero N, Zheng H, Evanoff R, Small CL, Griswold MD, Namekawa SH, Royo H, Turner JM, Yan W (2012) The RNase III enzyme DROSHA is essential for microRNA production and spermatogenesis. J Biol Chem 287:25173–25190

  • Xu XM, Møller SG (2011) The value of Arabidopsis research in understanding human disease states. Curr Opin Biotechnol 22:300–307

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Liu Z, Lu F, Dong A, Huang H (2006) SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant J 47:841–850

    Article  CAS  PubMed  Google Scholar 

  • Yelina NE, Choi K, Chelysheva L, Macaulay M, de Snoo B, Wijnker E, Miller N, Drouaud J, Grelon M, Copenhaver GP, Mezard C, Kelly KA, Henderson IR (2012) Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. PLoS Genet 8:e1002844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yi R, Qin Y, Macara IG, Cullen BR (2003) Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev 17:3011–3016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • You C, Cui J, Wang H, Qi X, Kuo LY, Ma H, Gao L, Mo B, Chen X (2017) Conservation and divergence of small RNA pathways and miRNAs in land plants. Genome Biol 18:158

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yu B, Yang Z, Li J, Minakhina S, Yang M, Padgett RW, Steward R, Chen X (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307:932–935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhai J, Zhang H, Arikit S, Huang K, Nan GL, Walbot V, Meyers BC (2015) Spatiotemporally dynamic, cell-type-dependent premeiotic and meiotic phasiRNAs in maize anthers. Proc Natl Acad Sci U S A 112:3146–3151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Cong L, Lukiw WJ (2017) Plant and animal microRNAs (miRNAs) and their potential for inter-kingdom communication. Cell Mol Neurobiol 38:133–140

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann C, Romero Y, Warnefors M, Bilican A, Borel C, Smith LB, Kotaja N, Kaessmann H, Nef S (2014) Germ cell-specific targeting of DICER or DGCR8 reveals a novel role for endo-siRNAs in the progression of mammalian spermatogenesis and male fertility. PLoS One 9:e107023

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Author contribution statement

JLS conceived the review. MP and JLS wrote the manuscript, contributed to revisions, and approved the final version. MP designed the figures.

Funding

The authors acknowledge the support of the Ministry of Economy and Competitiveness of Spain (by grants AGL2012-38852 and AGL2015-67349-P) and of the European Union (FP7: Meiosys-KBBE-2009-222883).

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Correspondence to Mónica Pradillo.

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Pradillo, M., Santos, J.L. Genes involved in miRNA biogenesis affect meiosis and fertility. Chromosome Res 26, 233–241 (2018). https://doi.org/10.1007/s10577-018-9588-x

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