Decoding human gene expression signatures in the brain

Transcription

Volumn 4, Issue 3, 2013, Pages

  Wang, Guang Zhong ^a   Konopka, Genevieve ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Brain; Coexpression; Evolution; Gene expression; Genomics; Nervous system

Indexed keywords

MICRORNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXP2; ELAVL2 PROTEIN, HUMAN; HU ANTIGEN; RNA; TRANSCRIPTOME;

ARTICLE; BRAIN; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN REGION; COGNITION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENOME ANALYSIS; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; RNA SPLICING; SPECIES DIFFERENCE; ANIMAL; GENETICS; METABOLISM; PRIMATE;

ANIMALS; BRAIN; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; MICRORNAS; PRIMATES; RNA; RNA SPLICING; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84877907898     PISSN: 21541264     EISSN: 21541272     Source Type: Journal    
DOI: 10.4161/trns.24885     Document Type: Article

References (76)

1. King MC, Wilson AC. Evolution at two levels in humans and chimpanzees. Science 1975; 188:107-116; PMID:1090005; http://dx.doi.org/10.1126/sci-ence.1090005
2. Chimpanzee Sequencing and Analysis Consortium. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 2005; 437:69-87; PMID:16136131; http://dx.doi.org/10.1038/nature04072
3. Gazave E, Darré F, Morcillo-Suarez C, Petit-Marty N, Carreño A, Marigorta UM, et al. Copy number variation analysis in the great apes reveals species-specific patterns of structural variation. Genome Res 2011; 21:1626-1639; PMID:21824994; http://dx.doi.org/10.1101/gr.117242.110
4. Blekhman R, Oshlack A, Gilad Y. Segmental duplications contribute to gene expression differences between humans and chimpanzees. Genetics 2009; 182:627-630; PMID:19332884; http://dx.doi.org/10.1534/genetics.108.099960
5. Ventura M, Catacchio CR, Sajjadian S, Vives L, Sudmant PH, Marques-Bonet T, et al. The evolution of African great ape subtelomeric heterochromatin and the fusion of human chromosome 2. Genome Res 2012; 22:1036-1049; PMID:22419167; http://dx.doi.org/10.1101/gr.13 6556.111
6. Nowick K, Hamilton AT, Zhang H, Stubbs L. Rapid sequence and expression divergence suggest selection for novel function in primate-specific KRAB-ZNF genes. Mol Biol Evol 2010; 27:2606-2617; PMID:20573777; http://dx.doi.org/10.1093/mol-bev/msq157
7. Dunham I, Kundaje A, Aldred SF, Collins PJ, Davis CA, Doyle F, et al.; ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 2012; 489:57-74; PMID:22955616; http://dx.doi.org/10.1038/nature11247
8. Enard W, Przeworski M, Fisher SE, Lai CS, Wiebe V, Kitano T, et al. Molecular evolution of FOXP2, a gene involved in speech and language. Nature 2002; 418:869-872; PMID:12192408; http://dx.doi.org/10.1038/nature01025
9. Crow TJ. Schizophrenia as the price that homo sapiens pays for language: a resolution of the central paradox in the origin of the species. Brain Res Brain Res Rev 2000; 31:118-129; PMID:10719140; http://dx.doi.org/10.1016/S0165-0173(99)00029-6
10. Konopka G, Friedrich T, Davis-Turak J, Winden K, Oldham MC, Gao F, et al. Human-specific transcrip-tional networks in the brain. Neuron 2012; 75:601-617; PMID:22920253; http://dx.doi.org/10.1016/j. neuron.2012.05.034
11. Bragin A, Karsten SL, Almajano J, Wilson CL, Geschwind DH, Engel J Jr. Large-scale microarray gene expression analysis in discrete electrophysi-ologically identified neuronal clusters. J Neurosci Methods 2004; 133:49-55; PMID:14757344; http://dx.doi.org/10.1016/j.jneumeth.2003.09.016
12. Preuss TM, Cáceres M, Oldham MC, Geschwind DH. Human brain evolution: insights from microarrays. Nat Rev Genet 2004; 5:850-860; PMID:15520794; http: //dx.doi.org/10.1038/nrg1469
13. Oldham MC, Geschwind DH. Deconstructing language by comparative gene expression: from neu-robiology to microarray. Genes Brain Behav 2006; 5(Suppl 1):54-63; PMID:16417618; http://dx.doi.or g /10.1111/j.16 01-183X. 2006. 0019 5. x
14. Enard W, Khaitovich P, Klose J, Zöllner S, Heissig F, Giavalisco P, et al. Intra- and interspecific variation in primate gene expression patterns. Science 2002; 296:340-343; PMID:11951044; http://dx.doi.org/10.1126/science.1068996
15. Gu J, Gu X. Induced gene expression in human brain after the split from chimpanzee. Trends Genet 2003; 19:63-65; PMID:12547510; http://dx.doi.org/10.1016/S0168-9525(02)00040-9
16. Zhang YE, Landback P, Vibranovski MD, Long M. Accelerated recruitment of new brain development genes into the human genome. PLoS Biol 2011; 9:e1001179; PMID:22028629; http://dx.doi.org/10.1371/journal.pbio.1001179
17. Miller DJ, Duka T, Stimpson CD, Schapiro SJ, Baze WB, McArthur MJ, et al. Prolonged myelination in human neocortical evolution. Proc Natl Acad Sci U S A 2012; 109:16480-16485; PMID:23012402; http://dx.doi.org/10.1073/pnas.1117943109
18. Preuss TM. The human brain: rewired and running hot. Ann N Y Acad Sci 2011; 1225(Suppl 1):E182-E191; PMID:21599696; http://dx.doi.org/10.1111/j.1749-6632.2011.06001.x
19. Glasser MF, Goyal MS, Preuss TM, Raichle ME, Van Essen DC. Trends and properties of human cerebral cortex: Correlations with cortical myelin content. Neuroimage 2013; PMID:23567887; http://dx.doi.org/10.1016/j.neuroimage.2013.03.060
20. Cáceres M, Lachuer J, Zapala MA, Redmond JC, Kudo L, Geschwind DH, et al. Elevated gene expression levels distinguish human from non-human primate brains. Proc Natl Acad Sci U S A 2003; 100:13030-13035; PMID:14557539; http://dx.doi.org/10.1073/pnas.2135499100
21. Khaitovich P, Muetzel B, She X, Lachmann M, Hellmann I, Dietzsch J, et al. Regional patterns of gene expression in human and chimpanzee brains. Genome Res 2004; 14:1462-1473; PMID:15289471; http: //dx.doi.org/10.1101/gr.2538704
22. Liu X, Somel M, Tang L, Yan Z, Jiang X, Guo S, et al. Extension of cortical synaptic development distinguishes humans from chimpanzees and macaques. Genome Res 2012; 22:611-622; PMID:22300767; http: //d x.doi.org /10.1101/gr.127324.111
23. Colantuoni C, Lipska BK, Ye T, Hyde TM, Tao R, Leek JT, et al. Temporal dynamics and genetic control of transcription in the human prefrontal cortex. Nature 2011; 478:519-523; PMID:22031444; http://dx.doi.org/10.1038/nature10524
24. Kang HJ, Kawasawa YI, Cheng F, Zhu Y, Xu X, Li M, et al. Spatio-temporal transcriptome of the human brain. Nature 2011; 478:483-489; PMID:22031440; http://dx.doi.org/10.1038/nature10523
25. Calarco JA, Xing Y, Cáceres M, Calarco JP, Xiao X, Pan Q, et al. Global analysis of alternative splicing differences between humans and chimpanzees. Genes Dev 2007; 21:2963-2975; PMID:17978102; http://dx.doi.org/10.1101/gad.1606907
26. Lin L, Shen S, Jiang P, Sato S, Davidson BL, Xing Y. Evolution of alternative splicing in primate brain transcriptomes. Hum Mol Genet 2010; 19:2958-2973; PMID:20460271; http://dx.doi.org/10.1093/hmg/ddq201
27. Mazin P, Xiong J, Liu X, Yan Z, Zhang X, Li M, et al. Widespread splicing changes in human brain development and aging. Mol Syst Biol 2013; 9:633; PMID:23340839; http://dx.doi.org/10.1038/msb.2012.67
28. Shibata M, Nakao H, Kiyonari H, Abe T, Aizawa S. MicroRNA-9 regulates neurogenesis in mouse telen-cephalon by targeting multiple transcription factors. J Neurosci 2011; 31:3407-3422; PMID:21368052; http://dx.doi.org/10.1523/JNEUROSCI.5085-10.2011
29. Lai CS, Fisher SE, Hurst JA, Vargha-Khadem F, Monaco AP. A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 2001; 413:519-523; PMID:11586359; http://dx.doi.org/10.1038/35097076
30. MacDermot KD, Bonora E, Sykes N, Coupe AM, Lai CS, Vernes SC, et al. Identification of FOXP2 truncation as a novel cause of developmental speech and language deficits. Am J Hum Genet 2005; 76:1074-1080; PMID:15877281; http://dx.doi.org/10.1086/430841
31. Fisher SE, Scharff C. FOXP2 as a molecular window into speech and language. Trends Genet 2009; 25:166-177; PMID:19304338; http://dx.doi.org/10.1016/j.tig.2009.03.002
32. Zhang J, Webb DM, Podlaha O. Accelerated protein evolution and origins of human-specific features: Foxp2 as an example. Genetics 2002; 162:1825-1835; PMID:12524352
33. Krause J, Lalueza-Fox C, Orlando L, Enard W, Green RE, Burbano HA, et al. The derived FOXP2 variant of modern humans was shared with Neandertals. Curr Biol 2007; 17:1908-1912; PMID:17949978; http://dx.doi.org/10.1016/j.cub.2007.10.008
34. Maricic T, Günther V, Georgiev O, Gehre S, Curlin M, Schreiweis C, et al. A recent evolutionary change affects a regulatory element in the human FOXP2 gene. Mol Biol Evol 2013; 30:844-852; PMID:23197593; http://dx.doi.org/10.1093/molbev/mss271
35. Spiteri E, Konopka G, Coppola G, Bomar J, Oldham M, Ou J, et al. Identification of the transcriptional targets of FOXP2, a gene linked to speech and language, in developing human brain. Am J Hum Genet 2007; 81:1144-1157; PMID:17999357; http://dx.doi.org/10.1086/522237
36. Ayub Q, Yngvadottir B, Chen Y, Xue Y, Hu M, Vernes SC, et al. FOXP2 Targets Show Evidence of Positive Selection in European Populations. Am J Hum Genet 2013; PMID:23602712; http://dx.doi.org/10.1016 /j.ajhg.2013.03.019
37. Konopka G, Bomar JM, Winden K, Coppola G, Jonsson ZO, Gao F, et al. Human-specific tran-scriptional regulation of CNS development genes by FOXP2. Nature 2009; 462:213-217; PMID:19907493; http://dx.doi.org/10.1038/nature08549
38. Enard W, Gehre S, Hammerschmidt K, Hölter SM, Blass T, Somel M, et al. A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell 2009; 137:961-971; PMID:19490899; http://dx.doi.org/10.1016/j.cell.2009.03.041
39. Enard W. FOXP2 and the role of cortico-basal ganglia circuits in speech and language evolution. Curr Opin Neurobiol 2011; 21:415-424; PMID:21592779; http://dx.doi.org/10.1016/j.conb.2011.04.008
40. Somel M, Guo S, Fu N, Yan Z, Hu HY, Xu Y, et al. MicroRNA, mRNA, and protein expression link development and aging in human and macaque brain. Genome Res 2010; 20:1207-1218; PMID:20647238; http://dx.doi.org/10.1101/gr.106849.110
41. Hu HY, Guo S, Xi J, Yan Z, Fu N, Zhang X, et al. MicroRNA expression and regulation in human, chimpanzee, and macaque brains. PLoS Genet 2011; 7:e1002327; PMID:22022286; http://dx.doi.org/10.1371/journal.pgen.1002327
42. Fraser HB, Khaitovich P, Plotkin JB, Pääbo S, Eisen MB. Aging and gene expression in the primate brain. PLoS Biol 2005; 3:e274; PMID:16048372; http://dx.doi.org/10.1371/journal.pbio.0030274
43. Konopka G, Geschwind DH. Human brain evolution: harnessing the genomics (r)evolution to link genes, cognition, and behavior. Neuron 2010; 68:231-244; PMID:20955931; http://dx.doi.org/10.1016/j.neuron.2010.10.012
44. Oldham MC, Horvath S, Geschwind DH. Conservation and evolution of gene coexpression networks in human and chimpanzee brains. Proc Natl Acad Sci U S A 2006; 103:17973-17978; PMID:17101986; http://dx.doi.org/10.1073/pnas.0605938103
45. Oldham MC, Konopka G, Iwamoto K, Langfelder P, Kato T, Horvath S, et al. Functional organization of the transcriptome in human brain. Nat Neurosci 2008; 11:1271-1282; PMID:18849986; http://dx.doi.org/10.1038/nn.2207
46. Nowick K, Gernat T, Almaas E, Stubbs L. Differences in human and chimpanzee gene expression patterns define an evolving network of transcription factors in brain. Proc Natl Acad Sci U S A 2009; 106:22358-22363; PMID:20007773; http://dx.doi.org/10.1073/pnas.0911376106
47. Dumontheil I, Burgess PW, Blakemore SJ. Development of rostral prefrontal cortex and cognitive and behavioural disorders. Dev Med Child Neurol 2008; 50:168-181; PMID:18190537; http://dx.doi.org/10.1111/j.1469-8749.2008.02026.x
48. Semendeferi K, Teffer K, Buxhoeveden DP, Park MS, Bludau S, Amunts K, et al. Spatial organization of neurons in the frontal pole sets humans apart from great apes. Cereb Cortex 2011; 21:1485-1497; PMID:21098620; http://dx.doi.org/10.1093/cercor/bhq191
49. Wan L, Yan X, Chen T, Sun F. Modeling RNA degradation for RNA-Seq with applications. Biostatistics 2012; 13:734-747; PMID:22353193; http://dx.doi.org/10.1093/biostatistics/kxs001
50. Benjamini Y, Speed T P. Summarizing and correcting the GC content bias in high-throughput sequencing. Nucleic Acids Res 2012; 40:e72; PMID:22323520; http://dx.doi.org/10.1093/nar/gks001
51. DeLuca DS, Levin JZ, Sivachenko A, Fennell T, Nazaire MD, Williams C, et al. RNA-SeQC: RNA-seq metrics for quality control and process optimization. Bioinformatics 2012; 28:1530-1532; PMID:22539670; http://dx.doi.org/10.1093/bioin-formatics/bts196
52. Oshlack A, Robinson MD, Young MD. From RNA-seq reads to differential expression results. Genome Biol 2010; 11:220; PMID:21176179; http://dx.doi.org/10.1186/gb-2010-11-12-220
53. Wang L, Wang S, Li W. RSeQC: quality control of RNA-seq experiments. Bioinformatics 2012; 28:2184-2185; PMID:22743226; http://dx.doi.org/10.1093/bioinformatics/bts356
54. Planet E, Attolini CS, Reina O, Flores O, Rossell D. Htseqtools: high-throughput sequencing quality control, processing and visualization in R. Bioinformatics 2012; 28:589-590; PMID:22199381; http://dx.doi.org/10.1093/bioinformatics/btr700
55. García-Alcalde F, Okonechnikov K, Carbonell J, Cruz LM, Götz S, Tarazona S, et al. Qualimap: evaluating next-generation sequencing alignment data. Bioinformatics 2012; 28:2678-2679; PMID:22914218; http://dx.doi.org/10.1093/bioinformatics/bts503
56. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012; 7:562-578; PMID:22383036; http://dx.doi.org/10.1038/nprot.2012.016
57. Goecks J, Nekrutenko A, Taylor J; Galaxy Team. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 2010; 11:R86; PMID:20738864; http://dx.doi.org/10.1186/gb-2010-11-8-r86
58. Bardet AF, He Q, Zeitlinger J, Stark A. A computational pipeline for comparative ChIP-seq analyses. Nat Protoc 2012; 7:45-61; PMID:22179591; http://dx.doi.org/10.1038/nprot.2011.420
59. Zeng J, Konopka G, Hunt BG, Preuss TM, Geschwind D, Yi SV. Divergent whole-genome meth-ylation maps of human and chimpanzee brains reveal epigenetic basis of human regulatory evolution. Am J Hum Genet 2012; 91:455-465; PMID:22922032; http://dx.doi.org/10.1016/j.ajhg.2012.07.024
60. Cain CE, Blekhman R, Marioni JC, Gilad Y. Gene expression differences among primates are associated with changes in a histone epigenetic modification. Genetics 2011; 187:1225-1234; PMID:21321133; http://dx.doi.org/10.1534/genetics.110.126177
61. Shulha HP, Crisci JL, Reshetov D, Tushir JS, Cheung I, Bharadwaj R, et al. Human-specific histone meth-ylation signatures at transcription start sites in prefrontal neurons. PLoS Biol 2012; 10:e1001427; PMID:23185133; http://dx.doi.org/10.1371/journal. pbio.10014 27
62. Mattison JA, Roth GS, Beasley TM, Tilmont EM, Handy AM, Herbert RL, et al. Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 2012; 489:318-321; PMID:22932268; http://dx.doi.org/10.1038/nature11432
63. Hawrylycz MJ, Lein ES, Guillozet-Bongaarts AL, Shen EH, Ng L, Miller JA, et al. An anatomically comprehensive atlas of the adult human brain transcrip-tome. Nature 2012; 489:391-399; PMID:22996553; http://dx.doi.org/10.1038/nature11405
64. Bernard A, Lubbers LS, Tanis KQ, Luo R, Podtelezhnikov AA, Finney EM, et al. Transcriptional architecture of the primate neocortex. Neuron 2012; 73:1083-1099; PMID:22445337; http://dx.doi.org/10.1016/j.neuron.2012.03.002
65. Coskun MA, Loveland KA, Pearson DA, Papanicolaou AC, Sheth BR. Functional Assays of Local Connectivity in the Somatosensory Cortex of Individuals with Autism. Autism Res 2013; PMID:23427110; http://dx.doi.org/10.1002/aur.1276
66. Khan S, Gramfort A, Shetty NR, Kitzbichler MG, Ganesan S, Moran JM, et al. Local and long-range functional connectivity is reduced in concert in autism spectrum disorders. Proc Natl Acad Sci U S A 2013; 110:3107-3112; PMID:23319621; http://dx.doi.org/10.1073/pnas.1214533110
67. Shepherd GM. Corticostriatal connectivity and its role in disease. Nat Rev Neurosci 2013; 14:278-291; PMID:23511908; http://dx.doi.org/10.1038/nrn3469
68. Uhlhaas PJ. Dysconnectivity, large-scale networks and neuronal dynamics in schizophrenia. Curr Opin Neurobiol 2013; 23:283-290; PMID:23228430; http://dx.doi.org/10.1016/j.conb.2012.11.004
69. Anderson CN, Grant SG. High throughput protein expression screening in the nervous system-needs and limitations. J Physiol 2006; 575:367-372; PMID:16793899; http://dx.doi.org/10.1113/jphysi-o l. 2006.113795
70. Bayés A, van de Lagemaat LN, Collins MO, Croning MD, Whittle IR, Choudhary JS, et al. Characterization of the proteome, diseases and evolution of the human postsynaptic density. Nat Neurosci 2011; 14:19-21; PMID:21170055; http://dx.doi.org/10.1038/nn.2719
71. Carroll D. Genome engineering with zinc-finger nucleases. Genetics 2011; 188:773-782; PMID:21828278; http://dx.doi.org/10.1534/genet-ics.111.131433
72. Joung JK, Sander JD. TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 2013; 14:49-55; PMID:23169466; http://dx.doi.org/10.1038/nrm3486
73. Barrangou R. CRISPR-Cas systems and RNA-guided interference. Wiley Interdiscip Rev RNA 2013; http://dx.doi.org/10.1002/wrna.1159.
74. Charrier C, Joshi K, Coutinho-Budd J, Kim JE, Lambert N, de Marchena J, et al. Inhibition of SRGAP2 function by its human-specific paralogs induces neoteny during spine maturation. Cell 2012; 149:923-935; PMID:22559944; http://dx.doi.org/10.1016/j.cell.2012.03.034
75. Nithianantharajah J, Komiyama NH, McKechanie A, Johnstone M, Blackwood DH, St Clair D, et al. Synaptic scaffold evolution generated components of vertebrate cognitive complexity. Nat Neurosci 2013; 16:16-24; PMID:23201973; http://dx.doi.org/10.1038/nn.3276
76. Belgard TG, Geschwind DH. Retooling spare parts: gene duplication and cognition. Nat Neurosci 2013; 16:6-8; PMID:23257927; http://dx.doi.org/10.1038/nn.3292