Skip to main content
Log in

Thinking about RNA? MicroRNAs in the brain

  • Published:
Mammalian Genome Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) are a recently discovered class of small RNA molecules implicated in a wide range of diverse gene regulatory mechanisms. Interestingly, numerous miRNAs are expressed in a spatially and temporally controlled manner in the nervous system. This suggests that gene regulation networks based on miRNA activities may be particularly relevant in neurons. Recent studies show the involvement of RNA-mediated gene silencing in neurogenesis, neural differentiation, synaptic plasticity, and neurologic and psychiatric diseases. This review focuses on the roles of miRNAs in the gene regulation of the nervous system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Abelson JF, Kwan KY, O’Roak BJ, Baek DY, Stillman AA et al (2005) Sequence variants in SLITRK1 are associated with Tourette’s syndrome. Science 310:317–320

    Article  CAS  PubMed  Google Scholar 

  • Anderson P, Kedersha N (2006) RNA granules. J Cell Biol 172:803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashraf SI, McLoon AL, Sclarsic SM, Kunes S (2006) Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 124:191–205

    Article  CAS  PubMed  Google Scholar 

  • Bak M, Silahtaroglu A, Møller M, Christensen M, Rath MF et al (2008) MicroRNA expression in the adult mouse central nervous system. RNA 14(3):432–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbato C, Ciotti MT, Serafino AL, Calissano P, Cogoni C (2007) Dicer expression and localization in post-mitotic neurons. Brain Res 1175:17–27

    Article  CAS  PubMed  Google Scholar 

  • Barbee SA, Estes PS, Cziko AM, Hillebrand J, Luedeman RA et al (2006) Staufen- and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies. Neuron 52:997–1009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Behm-Ansmant I, Rehwinkel J, Doerks T, Stark A, Bork P et al (2006) mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev 20(14):1885–1898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernstein E, Kim SY, Carmell MA, Murchison EP, Alcorn H et al (2003) Dicer is essential for mouse development. Nat Genet 35(3):215–217

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W (2006) Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125(6):1111–1124

    Article  CAS  PubMed  Google Scholar 

  • Bilen J, Liu N, Burnett BG, Pittman RN, Bonini NM (2006) MicroRNA pathways modulate polyglutamine-induced neurodegeneration. Mol Cell 24(1):157–163

    Article  CAS  PubMed  Google Scholar 

  • Bingol B, Schuman EM (2005) Synaptic protein degradation by the ubiquitin proteasome system. Curr Opin Neurobiol 15:536–541

    Article  CAS  PubMed  Google Scholar 

  • Bingol B, Schuman EM (2006) Activity-dependent dynamics and sequestration of proteasomes in dendritic spines. Nature 441:1144–1148

    Article  CAS  PubMed  Google Scholar 

  • Bohnsack MT, Czaplinski K, Gorlich D (2004) Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 10(2):185–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boutz PL, Chawla G, Stoilov P, Black DL (2007) MicroRNAs regulate the expression of the alternative splicing factor nPTB during muscle development. Genes Dev 21(1):71–84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caudy AA, Myers M, Hannon GJ, Hammond SM (2002) Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev 16:2491–2496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan JA, Krichevsky AM, Kosik KS (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65(14):6029–6033

    Article  CAS  PubMed  Google Scholar 

  • Chang S, Johnston RJ Jr, Frøkjaer-Jensen C, Lockery S, Hobert O (2004) MicroRNAs act sequentially and asymmetrically to control chemosensory laterality in the nematode. Nature 430(7001):785–789

    Article  CAS  PubMed  Google Scholar 

  • Chendrimada TP, Gregory RI, Kumaraswamy E, Norman J, Cooch N et al (2005) TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436(7051):740–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chendrimada TP, Finn KJ, Ji X, Baillat D, Gregory RI et al (2007) MicroRNA silencing through RISC recruitment of eIF6. Nature 447(7146):823–828

    Article  CAS  PubMed  Google Scholar 

  • Chu CY, Rana TM (2006) Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol 4(7):e210

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Conaco C, Otto S, Han JJ, Mandel G (2006) Reciprocal actions of REST and a microRNA promote neuronal identity. Proc Natl Acad Sci USA 103(7):2422–2427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Esquela-Kerscher A, Slack FJ (2006) Oncomirs—microRNAs with a role in cancer. Nat Rev Cancer (4):259-269

  • Eulalio A, Behm-Ansmant I, Schweizer D, Izaurralde E (2007) P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol Cell Biol 27(11):3970–3981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiore R, Siegel G, Schratt G (2008) MicroRNA function in neuronal development, plasticity and disease. Biochim Biophys Acta. doi:10.1016/j.bbagrm.2007.12.006

  • Giorgi C, Yeo GW, Stone ME, Katz DB, Burge C et al (2007) The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 130:179–191

    Article  CAS  PubMed  Google Scholar 

  • Giraldez AJ, Cinalli RM, Glasner ME, Enright AJ, Thomson JM et al (2005) MicroRNAs regulate brain morphogenesis in zebrafish. Science 308(5723):833–838

    Article  CAS  PubMed  Google Scholar 

  • Gregory RI, Yan KP, Amuthan G, Chendrimada TP, Doratotaj B et al (2004) The microprocessor complex mediates the genesis of microRNAs. Nature 432(7014):235–240

    Article  CAS  PubMed  Google Scholar 

  • Hansen T, Olsen L, Lindow M, Jakobsen KD, Ullum H et al (2007) Brain expressed microRNAs implicated in schizophrenia etiology. PLoS ONE 2(9):e873

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hébert SS, Horré K, Nicolaï L, Papadopoulou AS, Mandemakers W et al (2008) Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer’s disease correlates with increased BACE1/beta-secretase expression. Proc Natl Acad Sci USA 105(17):6415–6420

    Article  PubMed  PubMed Central  Google Scholar 

  • Hillebrand J, Barbee SA, Ramaswami M (2007) P-body components, microRNA regulation, and synaptic plasticity. ScientificWorldJournal 7:178–190

    Article  PubMed  PubMed Central  Google Scholar 

  • Hobert O (2006) Architecture of a microRNA-controlled gene regulatory network that diversifies neuronal cell fates. Cold Spring Harb Symp Quant Biol 71:181–188

    Article  CAS  PubMed  Google Scholar 

  • Hock J, Weinmann L, Ender C, Rüdel S, Kremmer E et al (2007) Proteomic and functional analysis of Argonaute-containing mRNA-protein complexes in human cells. EMBO Rep 8(11):1052–1060

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hohjoh H, Fukushima T (2007) Marked change in microRNA expression during neuronal differentiation of human teratocarcinoma NTera2D1 and mouse embryonal carcinoma P19 cells. Biochem Biophys Res Commun 362(2):360–367

    Article  CAS  PubMed  Google Scholar 

  • Humphreys DT, Westman BJ, Martin DI, Preiss T (2005) MicroRNAs control translation initiation by inhibiting eukaryotic initiation factor 4E/cap and poly(A) tail function. Proc Natl Acad Sci USA 102(47):16961–16966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huttelmaier S, Zenklusen D, Lederer M, Dictenberg J, Lorenz M et al (2005) Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1. Nature 438:512

    Article  PubMed  CAS  Google Scholar 

  • Hutvagner G, Simard MJ (2008) Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 9(1):22–32

    Article  CAS  PubMed  Google Scholar 

  • Ishizuka A, Siomi MC, Siomi H (2002) A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev 16:2497–2508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin P, Zarnescu DC, Ceman S, Nakamoto M, Mowrey J et al (2004) Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nat Neurosci 7:113–117

    Article  CAS  PubMed  Google Scholar 

  • Jing Q, Huang S, Guth S, Zarubin T, Motoyama A et al (2005) Involvement of microRNA in AU-rich element-mediated mRNA instability. Cell 120(5):623–634

    Article  CAS  PubMed  Google Scholar 

  • Johnston RJ, Hobert O (2003) A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature 426(6968):845–849

    Article  CAS  PubMed  Google Scholar 

  • Johnston RJ Jr, Chang S, Etchberger JF, Ortiz CO, Hobert O (2005) MicroRNAs acting in a double-negative feedback loop to control a neuronal cell fate decision. Proc Natl Acad Sci USA 102(35):12449–12454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kedde M, Strasser MJ, Boldajipour B, Vrielink JA, Slanchev K et al (2007) RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131(7):1273–1286

    Article  CAS  PubMed  Google Scholar 

  • Kiebler MA, Bassell GJ (2006) Neuronal RNA granules: movers and makers. Neuron 51:685–690

    Article  CAS  PubMed  Google Scholar 

  • Kim J, Krichevsky A, Grad Y, Hayes GD, Kosik KS et al (2004) Identification of many microRNAs that copurify with polyribosomes in mammalian neurons. Proc Natl Acad Sci USA 101(1):360–365

    Article  CAS  PubMed  Google Scholar 

  • Kim J, Inoue K, Ishii J, Vanti WB, Voronov SV et al (2007) A microRNA feedback circuit in midbrain dopamine neurons. Science 317(5842):1220–1224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6(5):376–385

    Article  CAS  PubMed  Google Scholar 

  • Kiriakidou M, Tan GS, Lamprinaki S, De Planell-Saguer M, Nelson PT et al (2007) An mRNA m7G cap binding-like motif within human Ago2 represses translation. Cell 129(6):1141–1151

    Article  CAS  PubMed  Google Scholar 

  • Krichevsky AM, King KS, Donahue CP, Khrapko K, Kosik KS (2003) A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 9(10):1274–1281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krichevsky AM, Sonntag KC, Isacson O, Kosik KS (2006) Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 24(4):857–864

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Laneve P, Di Marcotullio L, Gioia U, Fiori ME, Ferretti E et al (2007) The interplay between microRNAs and the neurotrophin receptor tropomyosin-related kinase C controls proliferation of human neuroblastoma cells. Proc Natl Acad Sci USA 104(19):7957–7962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5):843–854

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Ahn C, Han J, Choi H, Kim J et al (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425(6956):415–419

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Hur I, Park SY, Kim YK, Suh MR et al (2006) The role of PACT in the RNA silencing pathway. EMBO J 25(3):522–532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM et al (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433(7027):769–773

    Article  CAS  PubMed  Google Scholar 

  • Lindow M, Gorodkin J (2007) Principles and limitations of computational microRNA gene and target finding. DNA Cell Biol 26(5):339–351

    Article  CAS  PubMed  Google Scholar 

  • Lukiw WJ (2007) Micro-RNA speciation in fetal, adult and Alzheimer’s disease hippocampus. Neuroreport 18(3):297–300

    Article  CAS  PubMed  Google Scholar 

  • Makeyev EV, Zhang J, Carrasco MA, Maniatis T (2007) The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 27(3):435–448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maroney PA, Yu Y, Nilsen TW (2006) MicroRNAs, mRNAs, and translation. Cold Spring Harb Symp Quant Biol 71:531–535

    Article  CAS  PubMed  Google Scholar 

  • Mathonnet G, Fabian MR, Svitkin YV, Parsyan A, Huck L et al (2007) MicroRNA inhibition of translation initiation in vitro by targeting the cap-binding complex eIF4F. Science 317(5845):1764–1767

    Article  CAS  PubMed  Google Scholar 

  • Mathupala SP, Guthikonda M, Sloan AE (2006) RNAi based approaches to the treatment of malignant glioma. Technol Cancer Res Treat 5(3):261–269

    Article  CAS  PubMed  Google Scholar 

  • Meister G, Tuschl T (2004) Mechanisms of gene silencing by double-stranded RNA. Nature 431(7006):343–349

    Article  CAS  PubMed  Google Scholar 

  • Miska EA, Alvarez-Saavedra E, Townsend M, Yoshii A, Sestan N et al (2004) Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol 5(9):R68

    Article  PubMed  PubMed Central  Google Scholar 

  • Nottrott S, Simard MJ, Richter JD (2006) Human let-7a miRNA blocks protein production on actively translating polyribosomes. Nat Struct Mol Biol 13(12):1108–1114

    Article  CAS  PubMed  Google Scholar 

  • Olsen PH, Ambros V (1999) The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev Biol 216(2):671–680

    Article  CAS  PubMed  Google Scholar 

  • Penagarikano O, Mulle JG, Warren ST (2007) The pathophysiology of fragile X syndrome. Annu Rev Genomics Hum Genet 8:109–129

    Article  CAS  PubMed  Google Scholar 

  • Perkins DO, Jeffries CD, Jarskog LF, Thomson JM, Woods K et al (2007) MicroRNA expression in the prefrontal cortex of individuals with schizophrenia and schizoaffective disorder. Genome Biol 8(2):R27

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Petersen CP, Bordeleau ME, Pelletier J, Sharp PA (2006) Short RNAs repress translation after initiation in mammalian cells. Mol Cell 21(4):533–542

    Article  CAS  PubMed  Google Scholar 

  • Pillai RS, Artus CG, Filipowicz W (2004) Tethering of human Ago proteins to mRNA mimics the miRNA-mediated repression of protein synthesis. RNA 10(10):1518–1525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pillai RS, Bhattacharyya SN, Artus CG, Zoller T, Cougot N et al (2005) Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309(5740):1573–1576

    Article  CAS  PubMed  Google Scholar 

  • Rehwinkel J, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC et al (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403(6772):901–906

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez A, Griffiths-Jones S, Ashurst JL, Bradley A (2004) Identification of mammalian microRNA host genes and transcription units. Genome Res 14(10A):1902–1910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaefer A, O’Carroll D, Tan CL, Hillman D, Sugimori M et al (2007) Cerebellar neurodegeneration in the absence of microRNAs. J Exp Med 204(7):1553–1558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME et al (2006) A brain-specific microRNA regulates dendritic spine development. Nature 439(7074):283–289

    Article  CAS  PubMed  Google Scholar 

  • Sempere LF, Freemantle S, Pitha-Rowe I, Moss E, Dmitrovsky E et al (2004) Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol 5(3):R13

    Article  PubMed  PubMed Central  Google Scholar 

  • Sethupathy P, Megraw M, Hatzigeorgiou AG (2006) A guide through present computational approaches for the identification of mammalian microRNA targets. Nat Methods 3:881–886

    Article  CAS  PubMed  Google Scholar 

  • Smirnova L, Grafe A, Seiler A, Schumacher S, Nitsch R et al (2005) Regulation of miRNA expression during neural cell specification. Eur J Neurosci 21(6):1469–1477

    Article  PubMed  Google Scholar 

  • Sutton MA, Schuman EM (2005) Local translational control in dendrites and its role in long-term synaptic plasticity. J Neurobiol 64:116

    Article  CAS  PubMed  Google Scholar 

  • Thermann R, Hentze MW (2007) Drosophila miR2 induces pseudo-polysomes and inhibits translation initiation. Nature 447(7146):875–878

    Article  CAS  PubMed  Google Scholar 

  • Vanderklish PW, Edelman GM (2005) Differential translation and fragile × syndrome. Genes Brain Behav 4:360

    Article  CAS  PubMed  Google Scholar 

  • Vasudevan S, Steitz JA (2007) AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell 128(6):1105–1118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vasudevan S, Tong Y, Steitz JA (2007) Switching from repression to activation: microRNAs can up-regulate translation. Science 318(5858):1931–1934

    Article  CAS  PubMed  Google Scholar 

  • Visvanathan J, Lee S, Lee B, Lee JW, Lee SK (2007) The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev 21(7):744–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vo N, Klein ME, Varlamova O, Keller DM, Yamamoto T et al (2005) A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc Natl Acad Sci USA 102(45):16426–16431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A et al (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 103(7):2257–2261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang WX, Rajeev BW, Stromberg AJ, Ren N, Tang G et al (2008) The expression of microRNA miR-107 decreases early in Alzheimer’s disease and may accelerate disease progression through regulation of beta-site amyloid precursor protein-cleaving enzyme 1. J Neurosci 28(5):1213–1223

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wheeler G, Ntounia-Fousara S, Granda B, Rathjen T, Dalmay T (2006) Identification of new central nervous system specific mouse microRNAs. FEBS Lett 580(9):2195–2000

    Article  CAS  PubMed  Google Scholar 

  • Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E et al (2005) MicroRNA expression in zebrafish embryonic development. Science 309(5732):310–311

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Xie X (2006) Comparative sequence analysis reveals an intricate network among REST, CREB and miRNA in mediating neuronal gene expression. Genome Biol 7(9):R85

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu L, Belasco JG (2005) Micro-RNA regulation of the mammalian lin-28 gene during neuronal differentiation of embryonal carcinoma cells. Mol Cell Biol (21):9198–9208

  • Yekta S, Shih IH, Bartel DP (2004) MicroRNA-directed cleavage of HOXB8 mRNA. Science 304(5670):594–596

    Article  CAS  PubMed  Google Scholar 

  • Yoon S, De Micheli G (2006) Computational identification of microRNAs and their targets. Birth Defects Res C Embryo Today 78:118–128

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was partially funded by FIRB RBLA03FLJC-005 and FIRB RBIN04H5AS_002, PRIN prot. No. 2005055188-002 and TELETHON grant GGP05269 (to CC). This work was supported in part by ‘Fondazione Alazio Award 2007’ (to CB) (www.fondazionealazio.org, Via Torquato Tasso 22, 90144 Palermo). We thank Francesca Ruberti and Mauro Cozzolino for helpful discussions and comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christian Barbato.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barbato, C., Giorgi, C., Catalanotto, C. et al. Thinking about RNA? MicroRNAs in the brain. Mamm Genome 19, 541–551 (2008). https://doi.org/10.1007/s00335-008-9129-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00335-008-9129-6

Keywords

Navigation