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Evidence for Positive Selection on a Number of MicroRNA Regulatory Interactions during Recent Human Evolution


MicroRNA (miRNA)–mediated gene regulation is of critical functional importance in animals and is thought to be largely constrained during evolution. However, little is known regarding evolutionary changes of the miRNA network and their role in human evolution. Here we show that a number of miRNA binding sites display high levels of population differentiation in humans and thus are likely targets of local adaptation. In a subset we demonstrate that allelic differences modulate miRNA regulation in mammalian cells, including an interaction between miR-155 and TYRP1, an important melanosomal enzyme associated with human pigmentary differences. We identify alternate alleles of TYRP1 that induce or disrupt miR-155 regulation and demonstrate that these alleles are selected with different modes among human populations, causing a strong negative correlation between the frequency of miR-155 regulation of TYRP1 in human populations and their latitude of residence. We propose that local adaptation of microRNA regulation acts as a rheostat to optimize TYRP1 expression in response to differential UV radiation. Our findings illustrate the evolutionary plasticity of the microRNA regulatory network in recent human evolution.


Vyšlo v časopise: Evidence for Positive Selection on a Number of MicroRNA Regulatory Interactions during Recent Human Evolution. PLoS Genet 8(3): e32767. doi:10.1371/journal.pgen.1002578
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002578

Souhrn

MicroRNA (miRNA)–mediated gene regulation is of critical functional importance in animals and is thought to be largely constrained during evolution. However, little is known regarding evolutionary changes of the miRNA network and their role in human evolution. Here we show that a number of miRNA binding sites display high levels of population differentiation in humans and thus are likely targets of local adaptation. In a subset we demonstrate that allelic differences modulate miRNA regulation in mammalian cells, including an interaction between miR-155 and TYRP1, an important melanosomal enzyme associated with human pigmentary differences. We identify alternate alleles of TYRP1 that induce or disrupt miR-155 regulation and demonstrate that these alleles are selected with different modes among human populations, causing a strong negative correlation between the frequency of miR-155 regulation of TYRP1 in human populations and their latitude of residence. We propose that local adaptation of microRNA regulation acts as a rheostat to optimize TYRP1 expression in response to differential UV radiation. Our findings illustrate the evolutionary plasticity of the microRNA regulatory network in recent human evolution.


Zdroje

1. BartelDP 2009 MicroRNAs: target recognition and regulatory functions. Cell 136 215 233

2. FriedmanRCFarhKKBurgeCBBartelDP 2009 Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19 92 105

3. HeLHannonGJ 2004 MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5 522 531

4. CuiQYuZPurisimaEOWangE 2006 Principles of microRNA regulation of a human cellular signaling network. Mol Syst Biol 2 46

5. XieXLuJKulbokasEJGolubTRMoothaV 2005 Systematic discovery of regulatory motifs in human promoters and 3′ UTRs by comparison of several mammals. Nature 434 338 345

6. ChenKRajewskyN 2006 Deep conservation of microRNA-target relationships and 3′UTR motifs in vertebrates, flies, and nematodes. Cold Spring Harb Symp Quant Biol 71 149 156

7. ChenKRajewskyN 2006 Natural selection on human microRNA binding sites inferred from SNP data. Nat Genet 38 1452 1456

8. SaundersMALiangHLiWH 2007 Human polymorphism at microRNAs and microRNA target sites. Proc Natl Acad Sci U S A 104 3300 3305

9. SethupathyPCollinsFS 2008 MicroRNA target site polymorphisms and human disease. Trends Genet 24 489 497

10. KingMCWilsonAC 1975 Evolution at two levels in humans and chimpanzees. Science 188 107 116

11. GiladYOshlackASmythGKSpeedTPWhiteKP 2006 Expression profiling in primates reveals a rapid evolution of human transcription factors. Nature 440 242 245

12. HaygoodRFedrigoOHansonBYokoyamaKDWrayGA 2007 Promoter regions of many neural- and nutrition-related genes have experienced positive selection during human evolution. Nat Genet 39 1140 1144

13. KasowskiMGrubertFHeffelfingerCHariharanMAsabereA 2010 Variation in transcription factor binding among humans. Science 328 232 235

14. FrazerKABallingerDGCoxDRHindsDAStuveLL 2007 A second generation human haplotype map of over 3.1 million SNPs. Nature 449 851 861

15. GrimsonAFarhKKJohnstonWKGarrett-EngelePLimLP 2007 MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27 91 105

16. HolsingerKEWeirBS 2009 Genetics in geographically structured populations: defining, estimating and interpreting F(ST). Nat Rev Genet 10 639 650

17. BarreiroLBLavalGQuachHPatinEQuintana-MurciL 2008 Natural selection has driven population differentiation in modern humans. Nat Genet 40 340 345

18. CoopGPickrellJKNovembreJKudaravalliSLiJ 2009 The role of geography in human adaptation. PLoS Genet 5 e1000500 doi:10.1371/journal.pgen.1000500

19. PritchardJKPickrellJKCoopG 2010 The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr Biol 20 R208 215

20. VoightBFKudaravalliSWenXPritchardJK 2006 A map of recent positive selection in the human genome. PLoS Biol 4 e72 doi:10.1371/journal.pbio.0040072

21. FayJCWuCI 2000 Hitchhiking under positive Darwinian selection. Genetics 155 1405 1413

22. NielsenRWilliamsonSKimYHubiszMJClarkAG 2005 Genomic scans for selective sweeps using SNP data. Genome Res 15 1566 1575

23. SethupathyPMegrawMHatzigeorgiouAG 2006 A guide through present computational approaches for the identification of mammalian microRNA targets. Nat Methods 3 881 886

24. HalabanRMoellmannG 1990 Murine and human b locus pigmentation genes encode a glycoprotein (gp75) with catalase activity. Proc Natl Acad Sci U S A 87 4809 4813

25. KobayashiTImokawaGBennettDCHearingVJ 1998 Tyrosinase stabilization by Tyrp1 (the brown locus protein). J Biol Chem 273 31801 31805

26. SturmRA 2009 Molecular genetics of human pigmentation diversity. Hum Mol Genet 18 R9 17

27. RooryckCRoudautCRobineEMusebeckJArveilerB 2006 Oculocutaneous albinism with TYRP1 gene mutations in a Caucasian patient. Pigment Cell Res 19 239 242

28. SarangarajanRBoissyRE 2001 Tyrp1 and oculocutaneous albinism type 3. Pigment Cell Res 14 437 444

29. AlalufSBarrettKBlountMCarterN 2003 Ethnic variation in tyrosinase and TYRP1 expression in photoexposed and photoprotected human skin. Pigment Cell Res 16 35 42

30. FrudakisTThomasMGaskinZVenkateswarluKChandraKS 2003 Sequences associated with human iris pigmentation. Genetics 165 2071 2083

31. StokowskiRPPantPVDaddTFeredayAHindsDA 2007 A genomewide association study of skin pigmentation in a South Asian population. Am J Hum Genet 81 1119 1132

32. SulemPGudbjartssonDFStaceySNHelgasonARafnarT 2008 Two newly identified genetic determinants of pigmentation in Europeans. Nat Genet 40 835 837

33. IzagirreNGarciaIJunqueraCde la RuaCAlonsoS 2006 A scan for signatures of positive selection in candidate loci for skin pigmentation in humans. Mol Biol Evol 23 1697 1706

34. LaoOde GruijterJMvan DuijnKNavarroAKayserM 2007 Signatures of positive selection in genes associated with human skin pigmentation as revealed from analyses of single nucleotide polymorphisms. Ann Hum Genet 71 354 369

35. AlonsoSIzagirreNSmith-ZubiagaIGardeazabalJDiaz-RamonJL 2008 Complex signatures of selection for the melanogenic loci TYR, TYRP1 and DCT in humans. BMC Evol Biol 8 74

36. LandgrafPRusuMSheridanRSewerAIovinoN 2007 A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129 1401 1414

37. LiangYRidzonDWongLChenC 2007 Characterization of microRNA expression profiles in normal human tissues. BMC Genomics 8 166

38. PhilippidouDSchmittMMoserDMargueCNazarovPV 2010 Signatures of microRNAs and selected microRNA target genes in human melanoma. Cancer Res 70 4163 4173

39. MartonSGarciaMRRobelloCPerssonHTrajtenbergF 2008 Small RNAs analysis in CLL reveals a deregulation of miRNA expression and novel miRNA candidates of putative relevance in CLL pathogenesis. Leukemia 22 330 338

40. JiangSZhangHWLuMHHeXHLiY 2010 MicroRNA-155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene. Cancer Res 70 3119 3127

41. LouafiFMartinez-NunezRTSanchez-ElsnerT 2010 MicroRNA-155 targets SMAD2 and modulates the response of macrophages to transforming growth factor-{beta}. J Biol Chem 285 41328 41336

42. Martinez-NunezRTLouafiFSanchez-ElsnerT 2011 The interleukin 13 (IL-13) pathway in human macrophages is modulated by microRNA-155 via direct targeting of interleukin 13 receptor alpha1 (IL13Ralpha1). J Biol Chem 286 1786 1794

43. LuCHuangXZhangXRoenschKCaoQ 2011 miR-221 and miR-155 regulate human dendritic cell development, apoptosis, and IL-12 production through targeting of p27kip1, KPC1, and SOCS-1. Blood 117 4293 4303

44. FangDTsujiYSetaluriV 2002 Selective down-regulation of tyrosinase family gene TYRP1 by inhibition of the activity of melanocyte transcription factor, MITF. Nucleic Acids Res 30 3096 3106

45. SabetiPCReichDEHigginsJMLevineHZRichterDJ 2002 Detecting recent positive selection in the human genome from haplotype structure. Nature 419 832 837

46. SmigielskiEMSirotkinKWardMSherryST 2000 dbSNP: a database of single nucleotide polymorphisms. Nucleic Acids Res 28 352 355

47. ConsortiumGP 2010 A map of human genome variation from population-scale sequencing. Nature 467 1061 1073

48. LiJZAbsherDMTangHSouthwickAMCastoAM 2008 Worldwide human relationships inferred from genome-wide patterns of variation. Science 319 1100 1104

49. TsangJZhuJvan OudenaardenA 2007 MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol Cell 26 753 767

50. ShkumatavaAStarkASiveHBartelDP 2009 Coherent but overlapping expression of microRNAs and their targets during vertebrate development. Genes Dev 23 466 481

51. WuCIShenYTangT 2009 Evolution under canalization and the dual roles of microRNAs: a hypothesis. Genome Res 19 734 743

52. JablonskiNGChaplinG 2000 The evolution of human skin coloration. J Hum Evol 39 57 106

53. SiepelABejeranoGPedersenJSHinrichsASHouM 2005 Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15 1034 1050

54. QuachHBarreiroLBLavalGZidaneNPatinE 2009 Signatures of purifying and local positive selection in human miRNAs. Am J Hum Genet 84 316 327

55. ShinCNamJWFarhKKChiangHRShkumatavaA 2010 Expanding the microRNA targeting code: functional sites with centered pairing. Mol Cell 38 789 802

56. HafnerMLandthalerMBurgerLKhorshidMHausserJ 2010 Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141 129 141

57. ZlojutroMTarskaiaLASorensenMSnodgrassJJLeonardWR 2009 Coalescent simulations of Yakut mtDNA variation suggest small founding population. Am J Phys Anthropol 139 474 482

58. CaiJJ 2008 PGEToolbox: A Matlab toolbox for population genetics and evolution. J Hered 99 438 440

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Genetika Reprodukčná medicína

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PLOS Genetics


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