Species-specific exon loss in human transcriptomes

Molecular Biology and Evolution

Volumn 32, Issue 2, 2015, Pages 481-494

  Wang, Jinkai ^a   Lu, Zhi Xiang ^a   Tokheim, Collin J ^a   Miller, Sara E ^b   Xing, Yi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

evolution; exon loss; primate; RNA seq; splicing

Indexed keywords

AMINO ACID TRANSPORTER; GENOMIC DNA; MESSENGER RNA; SLC7A6 PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; SLC7A6 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ALU SEQUENCE; ARTICLE; CODON; EXON LOSS; GENE CONTROL; GENE DELETION; GENE LOSS; GENETIC RECOMBINATION; HUMAN; INTRON; LUCIFERASE ASSAY; MOLECULAR GENETICS; NONHUMAN; PHYLOGENY; PRIMATE; RNA SEQUENCE; RNA SPLICING; RNA TRANSLATION; SINGLE NUCLEOTIDE SUBSTITUTION; SPECIES DIFFERENCE; ANIMAL; EXON; GENETICS; MOLECULAR EVOLUTION;

PAN; PRIMATES;

AMINO ACID TRANSPORT SYSTEMS, BASIC; ANIMALS; EVOLUTION, MOLECULAR; EXONS; HUMANS; PRIMATES; TRANSCRIPTOME;

EID: 84988302662     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu317     Document Type: Article

References (60)

1. Alekseyenko AV, Kim N, Lee CJ. 2007. Global analysis of exon creation versus loss and the role of alternative splicing in 17 vertebrate genomes. RNA 13: 661-670
2. Arancibia-Garavilla Y, Toledo F, Casanello P, Sobrevia L. 2003. Nitric oxide synthesis requires activity of the cationic and neutral amino acid transport system y+L in human umbilical vein endothelium. Exp Physiol. 88:699-710
3. Barbosa C, Peixeiro I, Romao L. 2013. Gene expression regulation by upstream open reading frames and human disease. PLoS Genet. 9: e1003529
4. Barbosa-Morais NL, Irimia M, Pan Q, Xiong HY, Gueroussov S, Lee LJ, Slobodeniuc V, Kutter C, Watt S, Colak R., et al. 2012. The evolutionary landscape of alternative splicing in vertebrate species. Science 338:1587-1593
5. Black DL. 2000. Protein diversity from alternative splicing: a challenge for bioinformatics and post-genome biology. Cell 103:367-370
6. Blekhman R, Marioni JC, Zumbo P, Stephens M, Gilad Y. 2010. Sexspecific and lineage-specific alternative splicing in primates. Genome Res. 20:180-189
7. Boue S, Letunic I, Bork P. 2003. Alternative splicing and evolution. Bioessays 25:1031-1034
8. Brawand D, Soumillon M, Necsulea A, Julien P, Csardi G, Harrigan P, Weier M, Liechti A, Aximu-Petri A, Kircher M., et al. 2011. The evolution of gene expression levels in mammalian organs. Nature 478: 343-348
9. Broer A, Wagner CA, Lang F, Broer S. 2000. The heterodimeric amino acid transporter 4F2hc/y+LAT2mediates arginine efflux in exchange with glutamine. Biochem J. 349(Pt 3):787-795
10. Calvo SE, Pagliarini DJ,Mootha VK. 2009. Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans. Proc Natl Acad Sci USA. 106:7507-7512
11. Chatterjee S, Pal JK. 2009. Role of 5'-and 3'-untranslated regions of mRNAs in human diseases. Biol Cell. 101:251-262
12. Chimpanzee Sequencing and Analysis Consortium. 2005. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437:69-87
13. Chou HH, Hayakawa T, Diaz S, Krings M, Indriati E, Leakey M, Paabo S, Satta Y, Takahata N, Varki A. 2002. Inactivation of CMP-N-acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution. Proc Natl Acad Sci USA. 99:11736-11741
14. Chou HH, Takematsu H, Diaz S, Iber J, Nickerson E, Wright KL, Muchmore EA, Nelson DL, Warren ST, Varki A. 1998. A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc Natl Acad Sci USA. 95:11751-11756
15. Corvelo A, Eyras E. 2008. Exon creation and establishment in human genes. Genome Biol. 9:R141
16. Enard W, Przeworski M, Fisher SE, Lai CS, Wiebe V, Kitano T, Monaco AP, Paabo S. 2002. Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418:869-872
17. Feschotte C. 2008. Transposable elements and the evolution of regulatory networks. Nat Rev Genet. 9:397-405
18. Florea L, Di Francesco V, Miller J, Turner R, Yao A, Harris M, Walenz B, Mobarry C, Merkulov GV, Charlab R., et al. 2005. Gene and alternative splicing annotation with AIR. Genome Res. 15:54-66
19. Gerber A, O'Connell MA, Keller W. 1997. Two forms of human doublestranded RNA-specific editase 1 (hRED1) generated by the insertion of an Alu cassette. RNA 3:453-463
20. Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C., et al. 2010. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol. 28: 503-510
21. Hahn Y, Jeong S, Lee B. 2007. Inactivation of MOXD2 and S100A15A by exon deletion during human evolution. Mol Biol Evol. 24:2203-2212
22. Hayakawa T, Satta Y, Gagneux P, Varki A, Takahata N. 2001. Alu-mediated inactivation of the human CMP-N-acetylneuraminic acid hydroxylase gene. Proc Natl Acad Sci USA. 98:11399-11404
23. Haygood R, Fedrigo O, Hanson B, Yokoyama KD, Wray GA. 2007. Promoter regions of many neural-and nutrition-related genes have experienced positive selection during human evolution. Nat Genet. 39:1140-1144
24. Irie A, Koyama S, Kozutsumi Y, Kawasaki T, Suzuki A. 1998. The molecular basis for the absence of N-glycolylneuraminic acid in humans. J Biol Chem. 273:15866-15871
25. Kent WJ. 2002. BLAT-the BLAST-like alignment tool. Genome Res. 12: 656-664
26. Kim J, Zhao K, Jiang P, Lu ZX, Wang J, Murray JC, Xing Y. 2012. Transcriptome landscape of the human placenta. BMC Genomics 13:115
27. Knowles DG, McLysaght A. 2009. Recent de novo origin of human protein-coding genes. Genome Res. 19:1752-1759
28. Kondrashov FA, Koonin EV. 2001. Origin of alternative splicing by tandem exon duplication. Hum Mol Genet. 10:2661-2669
29. Letunic I, Copley RR, Bork P. 2002. Common exon duplication in animals and its role in alternative splicing. Hum Mol Genet. 11:1561-1567
30. Lewis BP, Green RE, Brenner SE. 2003. Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc Natl Acad Sci USA. 100:189-192
31. Lin L, Jiang P, Shen S, Sato S, Davidson BL, Xing Y. 2009. Large-scale analysis of exonized mammalian-wide interspersed repeats in primate genomes. Hum Mol Genet. 18:2204-2214
32. Lin L, Shen S, Tye A, Cai JJ, Jiang P, Davidson BL, Xing Y. 2008. Diverse splicing patterns of exonized Alu elements in human tissues. PLoS Genet. 4:e1000225
33. MacDonald JR, Ziman R, Yuen RK, Feuk L, Scherer SW. 2014. The Database of Genomic Variants: a curated collection of structural variation in the human genome. Nucleic Acids Res. 42: D986-D992
34. Maricic T, Gunther V, Georgiev O, Gehre S, Curlin M, Schreiweis C, Naumann R, Burbano HA, Meyer M, Lalueza-Fox C., et al. 2013. A recent evolutionary change affects a regulatory element in the human FOXP2 gene. Mol Biol Evol. 30:844-852
35. McLean CY, Reno PL, Pollen AA, Bassan AI, Capellini TD, Guenther C, Indjeian VB, Lim X, Menke DB, Schaar BT., et al. 2011. Humanspecific loss of regulatory DNA and the evolution of human-specific traits. Nature 471:216-219
36. Meijer HA, Thomas AA. 2003. Ribosomes stalling on uORF1 in the Xenopus Cx41 5' UTR inhibit downstream translation initiation. Nucleic Acids Res. 31:3174-3184
37. Merkin J, Russell C, Chen P, Burge CB. 2012. Evolutionary dynamics of gene and isoform regulation in mammalian tissues. Science 338: 1593-1599
38. Modrek B, Lee CJ. 2003. Alternative splicing in the human, mouse and rat genomes is associated with an increased frequency of exon creation and/or loss. Nat Genet. 34:177-180
39. Muotri AR, Marchetto MC, Coufal NG, Gage FH. 2007. The necessary junk: new functions for transposable elements. Hum Mol Genet. 16(Spec No. 2):R159-R167
40. Nilsen TW, Graveley BR. 2010. Expansion of the eukaryotic proteome by alternative splicing. Nature 463:457-463
41. Perry GH, Melsted P, Marioni JC,Wang Y, Bainer R, Pickrell JK, Michelini K, Zehr S, Yoder AD, Stephens M., et al. 2012. Comparative RNA sequencing reveals substantial genetic variation in endangered primates. Genome Res. 22:602-610
42. Qiao H, Lu N, Du E, Yao L, Xiao H, Lu S, Qi Y. 2011. Rare codons in uORFs of baculovirus p13 gene modulates downstream gene expression. Virus Res. 155:249-253
43. Schauer R. 2009. Sialic acids as regulators of molecular and cellular interactions. Curr Opin Struct Biol. 19:507-514
44. Sela N, Mersch B, Gal-Mark N, Lev-Maor G, Hotz-Wagenblatt A, Ast G. 2007. Comparative analysis of transposed element insertion within human andmouse genomes reveals Alu's unique role in shaping the human transcriptome. Genome Biol. 8:R127
45. Sen SK, Han K, Wang J, Lee J, Wang H, Callinan PA, Dyer M, Cordaux R, Liang P, Batzer MA. 2006. Human genomic deletions mediated by recombination between Alu elements. Am J Hum Genet. 79: 41-53
46. Shen S, Lin L, Cai JJ, Jiang P, Kenkel EJ, Stroik MR, Sato S, Davidson BL, Xing Y. 2011. Widespread establishment and regulatory impact of Alu exons in human genes. Proc Natl Acad Sci USA. 108: 2837-2842
47. Sorek R. 2007. The birth of new exons: mechanisms and evolutionary consequences. RNA 13:1603-1608
48. Sterne-Weiler T, Howard J,Mort M, Cooper DN, Sanford JR. 2011. Loss of exon identity is a common mechanism of human inherited disease. Genome Res. 21:1563-1571
49. Sterne-Weiler T, Martinez-Nunez RT, Howard JM, Cvitovik I, Katzman S, Tariq MA, Pourmand N, Sanford JR. 2013. Frac-seq reveals isoformspecific recruitment to polyribosomes. Genome Res. 23:1615-1623
50. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-1111
51. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 28:511-515
52. Varki A. 2001. Loss of N-glycolylneuraminic acid in humans: mechanisms, consequences, and implications for hominid evolution. Am J Phys Anthropol. 116(Suppl. 33), 54-69
53. Varki A. 2010. Colloquium paper: uniquely human evolution of sialic acid genetics and biology. Proc Natl Acad Sci USA. 107(Suppl. 2), 8939-8946
54. Wang HY, Chien HC, Osada N, Hashimoto K, Sugano S, Gojobori T, Chou CK, Tsai SF, Wu CI, Shen CK. 2007. Rate of evolution in brainexpressed genes in humans and other primates. PLoS Biol. 5:e13
55. Wang W, Zheng H, Yang S, Yu H, Li J, Jiang H, Su J, Yang L, Zhang J, McDermott J., et al. 2005. Origin and evolution of new exons in rodents. Genome Res. 15:1258-1264
56. Wang X, Grus WE, Zhang J. 2006. Gene losses during human origins. PLoS Biol. 4:e52
57. Wu DD, Irwin DM, Zhang YP. 2011. De novo origin of human proteincoding genes. PLoS Genet. 7:e1002379
58. Xing Y, Lee C. 2006. Alternative splicing and RNA selection pressure-evolutionary consequences for eukaryotic genomes. Nat Rev Genet. 7:499-509
59. Yeo G, Burge CB. 2004. Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J Comput Biol. 11: 377-394
60. Zhang XH, Chasin LA. 2006. Comparison of multiple vertebrate genomes reveals the birth and evolution of human exons. Proc Natl Acad Sci USA. 103:13427-13432