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Go with the Flow: Fluid Roles for miRNAs in Vertebrate Osmoregulation

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Part of the Physiology in Health and Disease book series (PIHD)

Abstract

MicroRNAs are a family of small RNAs that regulate gene expression post-transcriptionally. By regulating the expression of multiple genes that mediate salt and water balance, miRNAs enable precise control over osmoregulatory processes in vertebrates. Differential expression of miRNAs and divergent mRNA targeting have allowed for adaptation of osmoregulatory tissues during vertebrate evolution. Interestingly, only a small number of mRNA target relationships have been maintained over the millennia, indicating that gain and loss of miRNA/mRNA networks have enabled species-specific osmoregulation.

Keywords

  • miRNA
  • Osmoregulation
  • Evolution
  • Kidney

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References

  • Aboobaker AA, Tomancak P, Patel N, Rubin GM, Lai EC (2005) Drosophila microRNAs exhibit diverse spatial expression patterns during embryonic development. Proc Natl Acad Sci USA 102(50):18017–18022. doi:10.1073/pnas.0508823102

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Agrawal R, Tran U, Wessely O (2009) The miR-30 miRNA family regulates Xenopus pronephros development and targets the transcription factor Xlim1/Lhx1. Development 136(23):3927–3936

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Anderson P, Kedersha N (2008) Stress granules: the Tao of RNA triage. Trends Biochem Sci 33(3):141–150

    CAS  CrossRef  PubMed  Google Scholar 

  • Arima H, Yamamoto N, Sobue K, Umenishi F, Tada T, Katsuya H, Asai K (2003) Hyperosmolar mannitol stimulates expression of aquaporins 4 and 9 through a p38 mitogen-activated protein kinase-dependent pathway in rat astrocytes. J Biol Chem 278(45):44525–44534

    CAS  CrossRef  PubMed  Google Scholar 

  • Bartel D (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    CAS  CrossRef  PubMed  Google Scholar 

  • Berezikov E, Chung W-J, Willis J, Cuppen E, Lai EC (2007) Mammalian mirtron genes. Mol Cell 28(2):328–336

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Betel D, Wilson M, Gabow A, Marks DS, Sander C (2008) The microRNA.org resource: targets and expression. Nucleic Acids Res 36:D149–D153

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Bhatt KM, Mi QS, Dong Z (2011) microRNAs in kidneys: biogenesis, regulation, and pathophysiological roles. Am J Physiol Ren Physiol 300(3):F602–F610

    CAS  CrossRef  Google Scholar 

  • Carmell MA, Xuan Z, Zhang MQ, Hannon GJ (2002) The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev 16(21):2733–2742

    CAS  CrossRef  PubMed  Google Scholar 

  • Chu JY, Sims-Lucas S, Bushnell DS, Bodnar AJ, Kreidberg JA, Ho J (2014) Dicer function is required in the metanephric mesenchyme for early kidney development. Am J Physiol Ren Physiol 306(7):F764–F772

    CAS  CrossRef  Google Scholar 

  • Darnell DK, Kaur S, Stanislaw S, Konieczka JK, Yatskievych TA, Antin PB (2006) MicroRNA expression during chick embryo development. Dev Dyn 235(11):3156–3165

    CAS  CrossRef  PubMed  Google Scholar 

  • Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS (2003) MicroRNA targets in drosophila. Genome Biol 5(1):R1

    PubMed Central  CrossRef  PubMed  Google Scholar 

  • Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: Dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177

    CAS  CrossRef  PubMed  Google Scholar 

  • Faehnle CR, Joshua-Tor L (2007) Argonautes confront new small RNAs. Curr Opin Chem Biol 11(5):569–577

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Farh KK, Grimson A, Jan C, Lewis BP, Johnston WK, Lim LP, Burge CB, Bartel DP (2005) The widespread impact of mammalian MicroRNAs on mRNA repression and evolution. Science 310(5755):1817–1821

    CAS  CrossRef  PubMed  Google Scholar 

  • Flynt AS, Lai EC (2008) Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat Rev Genet 9(11):831–842

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Flynt AS, Thatcher EJ, Burkewitz K, Li N, Liu Y, Patton JG (2009) miR-8 microRNAs regulate the response to osmotic stress in zebrafish embryos. J Cell Biol 185(1):115–127

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Friedman RC, Farh KK-H, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19(1):92–105

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, Shiekhattar R (2004) The microprocessor complex mediates the genesis of microRNAs. Nature 432(7014):235–240

    CAS  CrossRef  PubMed  Google Scholar 

  • Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34(Suppl 1):D140

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Grun D, Wang Y-L, Langenberger D, Gunsalus KC, Rajewsky N (2005) microRNA target predictions across seven drosophila species and comparison to mammalian targets. PLoS Comput Biol 1(1), e13

    PubMed Central  CrossRef  PubMed  Google Scholar 

  • Harvey SJ, Jarad G, Cunningham J, Goldberg S, Schermer B, Harfe BD, McManus MT, Benzing T, Miner JH (2008) Podocyte-specific deletion of dicer alters cytoskeletal dynamics and causes glomerular disease. J Am Soc Nephrol 19(11):2150–2158

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Hausser J, Syed AP, Selevsek N, van Nimwegen E, Jaskiewicz L, Aebersold R, Zavolan M (2013) Timescales and bottlenecks in miRNA-dependent gene regulation. Mol Syst Biol 9(1)

    Google Scholar 

  • Heimberg AM, Cowper-Sal lari R, Sémon M, Donoghue PCJ, Peterson KJ (2010) microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate. Proc Natl Acad Sci USA 107:19379–19383

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Hornstein E, Shomron N (2006) Canalization of development by microRNAs. Nat Genet 38(Suppl):S20–S24

    CAS  CrossRef  PubMed  Google Scholar 

  • Huang W, Liu H, Wang T, Zhang T, Kuang J, Luo Y, Chung SS, Yuan L, Yang JY (2011) Tonicity-responsive microRNAs contribute to the maximal induction of osmoregulatory transcription factor OREBP in response to high-NaCl hypertonicity. Nucleic Acids Res 39(2):475–485

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS (2004) Human microRNA targets. PLoS Biol 2(11), e363

    PubMed Central  CrossRef  PubMed  Google Scholar 

  • Ketting RF, Fischer S, Bernstein E, Sijen T, Hannon GJ, Plasterk R (2001) Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev 15:2654–2659

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Kim VN, Han J, Siomi MC (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10(2):126–139

    CAS  CrossRef  PubMed  Google Scholar 

  • Kiriakidou M, Nelson PT, Kouranov A, Fitziev P, Bouyioukos C, Mourelatos Z, Hatzigeorgiou A (2004) A combined computational-experimental approach predicts human microRNA targets. Genes Dev 18(10):1165–1178

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Kloosterman WP, Steiner FA, Berezikov E, de Bruijn E, van de Belt J, Verheul M, Cuppen E, Plasterk RHA (2006) Cloning and expression of new microRNAs from zebrafish. Nucleic Acids Res 34(9):2558–2569

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T (2001) Identification of novel genes coding for small expressed RNAs. Science 294(5543):853–858

    CAS  CrossRef  PubMed  Google Scholar 

  • Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T (2002) Identification of tissue-specific microRNAs from mouse. Curr Biol 12(9):735–739

    CAS  CrossRef  PubMed  Google Scholar 

  • Lai EC (2002) Micro RNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat Genet 30(4):363–364

    CAS  CrossRef  PubMed  Google Scholar 

  • Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, Lin C, Socci N, Hermida L, Fulci V, Chiaretti S, Foa R, Schliwka J, Fuchs U, Novosel A, Muller RU, Schermer B, Bissels U, Inman J, Phan Q, Chien M, Weir DB, Choksi R, De Vita G, Frezzetti D, Trompeter H-I, Hornung V, Teng G, Hartmann G, Palkovits M, Di Lauro R, Wernet P, Macino G, Rogler CE, Nagle JW, Ju J, Papavasiliou FN, Benzing T, Lichter P, Tam W, Brownstein MJ, Bosio A, Borkhardt A, Russo JJ, Sander C, Zavolan M, Tuschl T (2007) Mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129(7):1401–1414

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Radmark O, Kim VN (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425(6956):415–419

    CAS  CrossRef  PubMed  Google Scholar 

  • Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23(20):4051–4060

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Leung AKL, Calabrese JM, Sharp PA (2006) Quantitative analysis of Argonaute protein reveals microRNA-dependent localization to stress granules. PNAS 103(48):18125–18130

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Liu J, Valencia-Sanchez MA, Hannon GJ, Parker R (2005) MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat Cell Biol 7(7):719

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Martinez J, Tuschl T (2004) RISC is a 5′ phosphomonoester-producing RNA endonuclease. Genes Dev 18(9):975–980

    PubMed Central  CAS  CrossRef  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 microRNA genes. Genome Res 23(1):34–45

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Mignone F, Pesole G (2001) mRNA untranslated regions (UTRs). Wiley

    Google Scholar 

  • Miyakawa H, Woo SK, Dahl SC, Handler JS, Kwon HM (1999) Tonicity-responsive enhancer binding protein, a rel-like protein that stimulates transcription in response to hypertonicity. Proc Natl Acad Sci USA 96(5):2538–2542

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Mladinov D, Liu Y, Mattson DL, Liang M (2013) MicroRNAs contribute to the maintenance of cell-type-specific physiological characteristics: miR-192 targets Na+/K+-ATPase β1. Nucleic Acids Res 41(2):1273–1283

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Mohammed J, Flynt AS, Siepel A, Lai EC (2013) The impact of age, biogenesis, and genomic clustering on Drosophila microRNA evolution. RNA 19(9):1295–1308

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Murchison EP, Hannon GJ (2004) miRNAs on the move: miRNA biogenesis and the RNAi machinery. Curr Opin Cell Biol 16(3):223–229

    CAS  CrossRef  PubMed  Google Scholar 

  • Nishimura H, Fan Z (2003) Regulation of water movement across vertebrate renal tubules. Comp Biochem Physiol A Mol Integr Physiol 136(3):479–498

    CrossRef  PubMed  Google Scholar 

  • Perry SF, Shahsavarani A, Georgalis T, Bayaa M, Furimsky M, Thomas SLY (2003) Channels, pumps, and exchangers in the gill and kidney of freshwater fishes: their role in ionic and acid-base regulation. J Exp Zool A Comp Exp Biol 300A(1):53–62

    CAS  CrossRef  Google Scholar 

  • Pham JW, Pellino JL, Lee YS, Carthew RW, Sontheimer EJ (2004) A Dicer-2-dependent 80s complex cleaves targeted mRNAs during RNAi in Drosophila. Cell 117(1):83–94

    CAS  CrossRef  PubMed  Google Scholar 

  • Rehwinkel JAN, Behm-Ansmant I, Gatfield D, Izaurralde E (2005) A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 11(11):1640–1647

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Ruby JG, Stark A, Johnston WK, Kellis M, Bartel DP, Lai EC (2007) Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res 17(12):1850–1864

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Saal S, Harvey SJ (2009) MicroRNAs and the kidney: coming of age. Curr Opin Nephrol Hypertens 18(4):317–323

    CAS  CrossRef  PubMed  Google Scholar 

  • Sempere L, Cole C, McPeek M, Peterson K (2006) The phylogenetic distribution of Meazoan microRNAs: insights into evolutionary complexity and constraint. J Exp Zool 306(B):575–588

    CrossRef  Google Scholar 

  • Shi S, Yu L, Chiu C, Sun Y, Chen J, Khitrov G, Merkenschlager M, Holzman LB, Zhang W, Mundel P, Bottinger EP (2008) Podocyte-selective deletion of dicer induces proteinuria and glomerulosclerosis. J Am Soc Nephrol 19(11):2159–2169

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Smibert P, Yang J-S, Azzam G, Liu J-L, Lai EC (2013) Homeostatic control of Argonaute stability by microRNA availability. Nat Struct Mol Biol 20(7):789–795

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Sontheimer EJ, Carthew RW (2004) Molecular biology. Argonaute journeys into the heart of RISC. Science 305(5689):1409–1410

    CAS  CrossRef  PubMed  Google Scholar 

  • Varsamos S, Nebel C, Charmantier G (2005) Ontogeny of osmoregulation in postembryonic fish: a review. Comp Biochem Physiol A Mol Integr Physiol 141(4):401–429

    CrossRef  PubMed  Google Scholar 

  • Waterhouse R, Zdobnov E, Tegenfeldt F, Li J, Kriventseva E (2011) OrthoDB: the hierarchical catalog of eukaryotic orthologs in 2011. Nucleic Acids Res 39:D283–D288

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

  • Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E, de Bruijn E, Horvitz HR, Kauppinen S, Plasterk RHA (2005) MicroRNA expression in zebrafish embryonic development. Science 309(5732):310–311

    CAS  CrossRef  PubMed  Google Scholar 

  • Zamore PD, Tuschl T, Sharp PA, Bartel DP (2000) RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101(1):25–33

    CAS  CrossRef  PubMed  Google Scholar 

  • Zare H, Khodursky A, Sartorelli V (2014) An evolutionarily biased distribution of miRNA sites toward regulatory genes with high promoter-driven intrinsic transcriptional noise. BMC Evol Biol 14(1):74

    PubMed Central  CrossRef  PubMed  Google Scholar 

  • Zeng Y, Yi R, Cullen BR (2003) MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. PNAS 100(17):9779–9784

    PubMed Central  CAS  CrossRef  PubMed  Google Scholar 

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Correspondence to Alex S. Flynt or James G. Patton .

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Flynt, A.S., Patton, J.G. (2015). Go with the Flow: Fluid Roles for miRNAs in Vertebrate Osmoregulation. In: Hyndman, K., Pannabecker, T. (eds) Sodium and Water Homeostasis. Physiology in Health and Disease. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-3213-9_8

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