Noncoding origins of anthropoid traits and a new null model of transposon functionalization

Genome Research

Volumn 24, Issue 9, 2014, Pages 1469-1484

  Del Rosario, Ricardo C H ^a   Rayan, Nirmala Arul ^a   Prabhakar, Shyam ^a  

^a GENOME INSTITUTE OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; TRANSPOSON;

ADULT; ANIMAL EXPERIMENT; ANTHROPOID SPECIFIC CONSTRAINED ELEMENT; ARTICLE; BRAIN DEVELOPMENT; CALLITRICHINAE; CONTROLLED STUDY; ENHANCER REGION; FETUS; FETUS DEVELOPMENT; GENE LOCUS; GENE SEQUENCE; GENOME; HUMAN; IN VIVO STUDY; MOLECULAR GENETICS; MOTOR COORDINATION; MOUSE; NEUROTRANSMISSION; NONHUMAN; SEQUENCE ANALYSIS; TRANSPOSON; VALIDATION PROCESS; VISION; ANIMAL; ANTIBODY SPECIFICITY; BIOLOGICAL MODEL; BRAIN; GENETICS; GROWTH, DEVELOPMENT AND AGING; HAPLORHINI; METABOLISM; MOLECULAR EVOLUTION; NUCLEOTIDE REPEAT;

ANIMALS; BRAIN; DNA TRANSPOSABLE ELEMENTS; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; GENETIC LOCI; HAPLORHINI; HUMANS; MODELS, GENETIC; ORGAN SPECIFICITY; REPETITIVE SEQUENCES, NUCLEIC ACID;

EID: 84907217918     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.168963.113     Document Type: Article

References (85)

1. The 1000 Genomes Project Consortium. 2010. A map of human genome variation from population-scale sequencing. Nature 467: 1061-1073.
2. Anzai N, Endou H. 2011. Urate transporters: an evolving field. Semin Nephrol 31: 400-409.
3. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, LiWW, Noble WS. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202-W208.
4. Bejerano G, Lowe CB, Ahituv N, King B, Siepel A, Salama SR, Rubin EM, Kent WJ, Haussler D. 2006. A distal enhancer and an ultraconserved exon are derived from a novel retroposon. Nature 441: 87-90.
5. Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, Meissner A, Kellis M, Marra MA, Beaudet AL, Ecker JR, et al. 2010. The NIH Roadmap Epigenomics Mapping Consortium. Nat Biotechnol 28: 1045-1048.
6. Bharti K, Gasper M, Ou J, Brucato M, Clore-Gronenborn K, Pickel J, Arnheiter H. 2012. A regulatory loop involving PAX6, MITF, and WNT signaling controls retinal pigment epithelium development. PLoS Genet 8: e1002757.
7. Blanchette M, Kent WJ, Riemer C, Elnitski L, Smit AF, Roskin KM, Baertsch R, Rosenbloom K, Clawson H, Green ED, et al. 2004. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res 14: 708-715.
8. Boffelli D, McAuliffe J, Ovcharenko D, Lewis KD, Ovcharenko I, Pachter L, Rubin EM. 2003. Phylogenetic shadowing of primate sequences to find functional regions of the human genome. Science 299: 1391-1394.
9. Borja D, Manns F, Ho A, Ziebarth NM, Acosta AC, Arrieta-Quintera E, Augusteyn RC, Parel JM. 2010. Refractive power and biometric properties of the nonhuman primate isolated crystalline lens. Invest Ophthalmol Vis Sci 51: 2118-2125.
10. Britten RJ, Davidson EH. 1969. Gene regulation for higher cells: a theory. Science 165: 349-357.
11. Brudno M, Do CB, Cooper GM, Kim MF, Davydov E, Green ED, Sidow A, Batzoglou S. 2003. LAGAN and Multi-LAGAN: efficient tools for largescale multiple alignment of genomic DNA. Genome Res 13: 721-731.
12. Carroll SB. 2003. Genetics and the making of Homo sapiens. Nature 422: 849-857.
13. Cartmill M. 1974. Rethinking primate origins. Science 184: 436-443.
14. Chuong EB, Rumi MA, Soares MJ, Baker JC. 2013. Endogenous retroviruses function as species-specific enhancer elements in the placenta. Nat Genet 45: 325-329.
15. Cooper GM, Stone EA, Asimenos G, Program NCS, Green ED, Batzoglou S, Sidow A. 2005. Distribution and intensity of constraint in mammalian genomic sequence. Genome Res 15: 901-913.
16. De Koning APJ, Gu W, Castoe TA, Batzer MA, Pollock DD. 2011. Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 7: e1002384.
17. De Souza FS, Franchini LF, Rubinstein M. 2013. Exaptation of transposable elements into novel cis-regulatory elements: Is the evidence always strong? Mol Biol Evol 30: 1239-1251.
18. DoolittleWF. 2013. Is junkDNA bunk? A critique of ENCODE. Proc Natl Acad Sci 110: 5294-5300.
19. Doolittle WF, Sapienza C. 1980. Selfish genes, the phenotype paradigm and genome evolution. Nature 284: 601-603.
20. Eddy SR. 2012. The C-value paradox, junk DNA and ENCODE. Curr Biol 22: R898-R899.
21. Enard W, Khaitovich P, Klose J, Zollner S, Heissig F, Giavalisco P, Nieselt- Struwe K, Muchmore E, Varki A, Ravid R, et al. 2002. Intra- and interspecific variation in primate gene expression patterns. Science 296: 340-343.
22. Erhardt A, Czibere L, Roeske D, Lucae S, Unschuld PG, Ripke S, Specht M, Kohli MA, Kloiber S, Ising M, et al. 2011. TMEM132D, a new candidate for anxiety phenotypes: evidence from human and mouse studies. Mol Psychiatry 16: 647-663.
23. Feschotte C. 2008. Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9: 397-405.
24. Gupta S, Stamatoyannopoulos JA, Bailey TL, Noble WS. 2007. Quantifying similarity between motifs. Genome Biol 8: R24.
25. HagégeH, Klous P, Braem C, Splinter E, Dekker J, CathalaG, de LaatW, Forné T. 2007. Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat Protoc 2: 1722-1733.
26. 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.
27. Hedges SB, Dudley J, Kumar S. 2006. TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22: 2971-2972.
28. Hindorff LA, Sethupathy P, Junkins HA, Ramos EM, Mehta JP, Collins FS, Manolio TA. 2009. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci 106: 9362-9367.
29. Huntley S, Baggott DM, Hamilton AT, Tran-Gyamfi M, Yang S, Kim J, Gordon L, Branscomb E, Stubbs L. 2006. A comprehensive catalog of human KRAB-associated zinc finger genes: insights into the evolutionary history of a large family of transcriptional repressors. Genome Res 16: 669-677.
30. Jacques PE, Jeyakani J, Bourque G. 2013. The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet 9: e1003504.
31. Johnson R, Gamblin RJ, Ooi L, Bruce AW, Donaldson IJ, Westhead DR, Wood IC, Jackson RM, Buckley NJ. 2006. Identification of the REST regulon reveals extensive transposable element-mediated binding site duplication. Nucleic Acids Res 34: 3862-3877.
32. Kaas JH. 2006. Evolution of the neocortex. Curr Biol 16: R910-R914.
33. Kaas JH. 2008. The evolution of the complex sensory and motor systems of the human brain. Brain Res Bull 75: 384-390.
34. Kalin NH, Shelton SE, Davidson RJ, Kelley AE. 2001. The primate amygdala mediates acute fear but not the behavioral and physiological components of anxious temperament. J Neurosci 21: 2067-2074.
35. Kamal M, Xie X, Lander ES. 2006. A large family of ancient repeat elements in the human genome is under strong selection. Proc Natl Acad Sci 103: 2740-2745.
36. KelleyD, Rinn J. 2012. Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome Biol 13: R107.
37. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. 2002. The human genome browser at UCSC. Genome Res 12: 996-1006.
38. Khan H, Smit A, Boissinot S. 2006. Molecular evolution and tempo of amplification of human LINE-1 retrotransposons since the origin of primates. Genome Res 16: 78-87.
39. King MC, Wilson AC. 1975. Evolution at two levels in humans and chimpanzees. Science 188: 107-116.
40. Kirkwood BJ. 2009. Albinism and its implications with vision. Insight 34: 13-16.
41. Kiyota T, Kato A, Altmann CR, Kato Y. 2008. The POU homeobox protein Oct-1 regulates radial glia formation downstream of Notch signaling. Dev Biol 315: 579-592.
42. Kriegstein A, Noctor S, Martínez-Cerdeño V. 2006. Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 7: 883-890.
43. Kunarso G, Chia NY, Jeyakani J, Hwang C, Lu X, Chan YS, Ng HH, Bourque G. 2010. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet 42: 631-634.
44. Lidow MS, Goldman-Rakic PS, Rakic P. 1991. Synchronized overproduction of neurotransmitter receptors in diverse regions of the primate cerebral cortex. Proc Natl Acad Sci 88: 10218-10221.
45. Liu H, Thurig S, Mohamed O, Dufort D, Wallace VA. 2006. Mapping canonical Wnt signaling in the developing and adult retina. Invest Ophthalmol Vis Sci 47: 5088-5097.
46. Lowe CB, Bejerano G, Haussler D. 2007. Thousands of human mobile element fragments undergo strong purifying selection near developmental genes. Proc Natl Acad Sci 104: 8005-8010.
47. Lynch VJ, Leclerc RD, May G, Wagner GP. 2011. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat Genet 43: 1154-1159.
48. Mariño-Ramírez L, Jordan IK. 2006. Transposable element derived DNase Ihypersensitive sites in the human genome. Biol Direct 1: 20.
49. The Marmoset Genome Sequencing and Analysis Consortium. 2014. The common marmoset genome provides insight into primate biology and evolution. Nat Genet doi:10.1038/ng.3042.
50. Marsden CD. 1961. Pigmentation in the nucleus substantiae nigrae of mammals. J Anat 95: 256-261.
51. Martínez-Morales JR, Rodrigo I, Bovolenta P. 2004. Eye development: a view from the retina pigmented epithelium. Bioessays 26: 766-777.
52. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G. 2010. GREAT improves functional interpretation of cisregulatory regions. Nat Biotechnol 28: 495-501.
53. McLean CY, Reno PL, Pollen AA, Bassan AI, Capellini TD, Guenther C, Indjeian VB, Lim X, Menke DB, Schaar BT, et al. 2011. Human-specific loss of regulatory DNA and the evolution of human-specific traits. Nature 471: 216-219.
54. Meader S, Ponting CP, Lunter G. 2010. Massive turnover of functional sequence in human and other mammalian genomes. Genome Res 20: 1335-1343.
55. Mikkelsen TS, Wakefield MJ, Aken B, Amemiya CT, Chang JL, Duke S, Garber M, Gentles AJ, Goodstadt L, Heger A, et al. 2007. Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature 447: 167-177.
56. Nickla DL, Wallman J. 2010. The multifunctional choroid. Prog Retin Eye Res 29: 144-168.
57. Niu DK, Jiang L. 2013. Can ENCODE tell us how much junk DNAwe carry in our genome? Biochem Biophys Res Commun 430: 1340-1343.
58. Oda M, Satta Y, Takenaka O, Takahata N. 2002. Loss of urate oxidase activity in hominoids and its evolutionary implications. Mol Biol Evol 19: 640-653.
59. Oetting WS, King RA. 1999. Molecular basis of albinism: mutations and polymorphisms of pigmentation genes associated with albinism. Hum Mutat 13: 99-115.
60. Olsen GJ, Matsuda H, HagstromR, Overbeek R. 1994. fastDNAmL: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Comput Appl Biosci 10: 41-48.
61. Orgel LE, Crick FH. 1980. Selfish DNA: the ultimate parasite. Nature 284: 604-607.
62. Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA, Shoukry M, Minovitsky S, Dubchak I, Holt A, Lewis KD, et al. 2006. In vivo enhancer analysis of human conserved non-coding sequences. Nature 444: 499-502.
63. Pierron D, Wildman DE, Hüttemann M, Letellier T, Grossman LI. 2012. Evolution of the couple cytochrome c and cytochrome c oxidase in primates. Adv Exp Med Biol 748: 185-213.
64. Pollard KS, Salama SR, King B, Kern AD, Dreszer T, Katzman S, Siepel A, Pedersen JS, Bejerano G, Baertsch R, et al. 2006. Forces shaping the fastest evolving regions in the human genome. PLoS Genet 2: e168.
65. Prabhakar S, Noonan JP, Paabo S, Rubin EM. 2006a. Accelerated evolution of conserved noncoding sequences in humans. Science 314: 786.
66. Prabhakar S, Poulin F, Shoukry M, Afzal V, Rubin EM, Couronne O, Pennacchio LA. 2006b. Close sequence comparisons are sufficient to identify human cis-regulatory elements. Genome Res 16: 855-863.
67. Prabhakar S, Visel A, Akiyama JA, Shoukry M, Lewis KD, Holt A, Plajzer-Frick I, MorrisonH, Fitzpatrick DR, Afzal V, et al. 2008. Human-specific gain of function in a developmental enhancer. Science 321: 1346-1350.
68. Rebollo R, Romanish MT, Mager DL. 2012. Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annu Rev Genet 46: 21-42.
69. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, Maillard PV, Layard-Liesching H, Verp S, Marquis J, et al. 2010. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463: 237-240.
70. Schmidt D, Schwalie PC, Wilson MD, Ballester B, Goncalves A, Kutter C, Brown GD, Marshall A, Flicek P, Odom DT. 2012. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 148: 335-348.
71. Schwirtlich M, Kwakowsky A, Emri Z, Antal K, Lacza Z, Cselenyák A, Katarova Z, Szabó G. 2011. GABAergic signaling in primary lens epithelial and lentoid cells and its involvement in intracellular Ca2+ modulation. Cell Calcium 50: 381-392.
72. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, et al. 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050.
73. Tashiro K, Teissier A, Kobayashi N, Nakanishi A, Sasaki T, Yan K, Tarabykin V, Vigier L, Sumiyama K, Hirakawa M, et al. 2011. A mammalian conserved element derived from SINE displays enhancer properties recapitulating Satb2 expression in early-born callosal projection neurons. PLoS ONE 6: e28497.
74. Tay SK, Blythe J, Lipovich L. 2009. Global discovery of primate-specific genes in the human genome. Proc Natl Acad Sci 106: 12019-12024.
75. Theodorou E, Dalembert G, Heffelfinger C, White E, Weissman S, Corcoran L, Snyder M. 2009. A high throughput embryonic stem cell screen identifies Oct-2 as a bifunctional regulator of neuronal differentiation. Genes Dev 23: 575-588.
76. Thomas JH, Schneider S. 2011. Coevolution of retroelements and tandem zinc finger genes. Genome Res 21: 1800-1812.
77. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, Sheffield NC, Stergachis AB, Wang H, Vernot B, et al. 2012. The accessible chromatin landscape of the human genome. Nature 489: 75-82.
78. Tribioli C, Frasch M, Lufkin T. 1997. Bapx1: An evolutionary conserved homologue of the Drosophila bagpipe homeobox gene is expressed in splanchnic mesoderm and the embryonic skeleton. Mech Dev 65: 145-162.
79. Varki A, Geschwind DH, Eichler EE. 2008. Explaining human uniqueness: genome interactions with environment, behaviour and culture. Nat Rev Genet 9: 749-763.
80. Wang QF, Prabhakar S, Wang Q, Moses AM, Chanan S, Brown M, Eisen MB, Cheng JF, Rubin EM, Boffelli D. 2006. Primate-specific evolution of an LDLR enhancer. Genome Biol 7: R68.
81. Wang T, Zeng J, Lowe CB, Sellers RG, Salama SR, Yang M, Burgess SM, Brachmann RK, Haussler D. 2007. Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc Natl Acad Sci 104: 18613-18618.
82. Ward LD, Kellis M. 2013. Response to comment on ''Evidence of abundant purifying selection in humans for recently acquired regulatory functions''. Science 340: 682.
83. Williams BA, Kay RF, Kirk EC. 2010. New perspectives on anthropoid origins. Proc Natl Acad Sci 107: 4797-4804.
84. Xie M, Hong C, Zhang B, Lowdon RF, Xing X, Li D, Zhou X, Lee HJ, Maire CL, Ligon KL, et al. 2013. DNA hypomethylation within specific transposable element families associates with tissue-specific enhancer landscape. Nat Genet 45: 836-841.
85. Yasui DH, Peddada S, Bieda MC, Vallero RO, Hogart A, Nagarajan RP, Thatcher KN, Farnham PJ, Lasalle JM. 2007. Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes. Proc Natl Acad Sci 104: 19416-19421.