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PMID: 17568002 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Pseudogenes in the ENCODE regions: consensus annotation, analysis of transcription, and evolution.

Genome research ·Vol. 17 ·No. 6 ·2007-06-00 ·Pages 839-51

Zheng D, Frankish A, Baertsch R, Kapranov P, Reymond A, Choo SW, Lu Y, Denoeud F, Antonarakis SE, Snyder M, Ruan Y, Wei CL, Gingeras TR, Guigó R, Harrow J, Gerstein MB

Abstract

Arising from either retrotransposition or genomic duplication of functional genes, pseudogenes are "genomic fossils" valuable for exploring the dynamics and evolution of genes and genomes. Pseudogene identification is an important problem in computational genomics, and is also critical for obtaining an accurate picture of a genome's structure and function. However, no consensus computational scheme for defining and detecting pseudogenes has been developed thus far. As part of the ENCyclopedia Of DNA Elements (ENCODE) project, we have compared several distinct pseudogene annotation strategies and found that different approaches and parameters often resulted in rather distinct sets of pseudogenes. We subsequently developed a consensus approach for annotating pseudogenes (derived from protein coding genes) in the ENCODE regions, resulting in 201 pseudogenes, two-thirds of which originated from retrotransposition. A survey of orthologs for these pseudogenes in 28 vertebrate genomes showed that a significant fraction ( approximately 80%) of the processed pseudogenes are primate-specific sequences, highlighting the increasing retrotransposition activity in primates. Analysis of sequence conservation and variation also demonstrated that most pseudogenes evolve neutrally, and processed pseudogenes appear to have lost their coding potential immediately or soon after their emergence. In order to explore the functional implication of pseudogene prevalence, we have extensively examined the transcriptional activity of the ENCODE pseudogenes. We performed systematic series of pseudogene-specific RACE analyses. These, together with complementary evidence derived from tiling microarrays and high throughput sequencing, demonstrated that at least a fifth of the 201 pseudogenes are transcribed in one or more cell lines or tissues.

MeSH Terms
Animals Cell Line Evolution, Molecular Gene Duplication Humans Primates/genetics Pseudogenes Retroelements Sequence Analysis, DNA Species Specificity Transcription, Genetic
Chemicals
Retroelements
Authors & Affiliations
16 authors, click to expand affiliations / ORCID
Zheng Deyou
Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520, USA. [email protected]
Frankish Adam
Baertsch Robert
Kapranov Philipp
Reymond Alexandre
Choo Siew Woh
Lu Yontao
Denoeud France
Antonarakis Stylianos E
Snyder Michael
Ruan Yijun
Wei Chia-Lin
Gingeras Thomas R
Guigó Roderic
Harrow Jennifer
Gerstein Mark B
References (78)
78 references, click to expand
  1. mRNA retroposition in human cells: processed pseudogene formation.
    EMBO J. 1995 Dec 15;14(24):6333-8 PMID: 8557053
  2. Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons.
    Proc Natl Acad Sci U S A. 1997 Mar 4;94(5):1872-7 PMID: 9050872
  3. PAML: a program package for phylogenetic analysis by maximum likelihood.
    Comput Appl Biosci. 1997 Oct;13(5):555-6 PMID: 9367129
  4. Comparison of DNA sequences with protein sequences.
    Genomics. 1997 Nov 15;46(1):24-36 PMID: 9403055
  5. A map of 75 human ribosomal protein genes.
    Genome Res. 1998 May;8(5):509-23 PMID: 9582194
  6. Toward a phylogenetic classification of Primates based on DNA evidence complemented by fossil evidence.
    Mol Phylogenet Evol. 1998 Jun;9(3):585-98 PMID: 9668008
  7. The mouse gene encoding the testis-specific isoform of Poly(A) binding protein (Pabp2) is an expressed retroposon: intimations that gene expression in spermatogenic cells facilitates the creation of new genes.
    J Mol Evol. 1998 Sep;47(3):275-81 PMID: 9732454
  8. The genomic record of Humankind's evolutionary roots.
    Am J Hum Genet. 1999 Jan;64(1):31-9 PMID: 9915940
  9. Identification of a novel cytokeratin 19 pseudogene that may interfere with reverse transcriptase-polymerase chain reaction assays used to detect micrometastatic tumor cells.
    Int J Cancer. 1999 Jan 5;80(1):119-25 PMID: 9935241
  10. Neuronal expression of neural nitric oxide synthase (nNOS) protein is suppressed by an antisense RNA transcribed from an NOS pseudogene.
    J Neurosci. 1999 Sep 15;19(18):7711-20 PMID: 10479675
  11. The Universal Protein Resource (UniProt).
    Nucleic Acids Res. 2005 Jan 1;33(Database issue):D154-9 PMID: 15608167
  12. HOPPSIGEN: a database of human and mouse processed pseudogenes.
    Nucleic Acids Res. 2005 Jan 1;33(Database issue):D59-66 PMID: 15608268
  13. Global identification of human transcribed sequences with genome tiling arrays.
    Science. 2004 Dec 24;306(5705):2242-6 PMID: 15539566
  14. Dark matter in the genome: evidence of widespread transcription detected by microarray tiling experiments.
    Trends Genet. 2005 Feb;21(2):93-102 PMID: 15661355
  15. PseudoPipe: an automated pseudogene identification pipeline.
    Bioinformatics. 2006 Jun 15;22(12):1437-9 PMID: 16574694
  16. TUF love for "junk" DNA.
    Cell. 2006 Jun 30;125(7):1215-20 PMID: 16814704
  17. A computational approach for identifying pseudogenes in the ENCODE regions.
    Genome Biol. 2006;7 Suppl 1:S13.1-10 PMID: 16925835
  18. EGASP: the human ENCODE Genome Annotation Assessment Project.
    Genome Biol. 2006;7 Suppl 1:S2.1-31 PMID: 16925836
  19. GENCODE: producing a reference annotation for ENCODE.
    Genome Biol. 2006;7 Suppl 1:S4.1-9 PMID: 16925838
  20. Integrated analysis of experimental data sets reveals many novel promoters in 1% of the human genome.
    Genome Res. 2007 Jun;17(6):720-31 PMID: 17567992
  21. Prominent use of distal 5' transcription start sites and discovery of a large number of additional exons in ENCODE regions.
    Genome Res. 2007 Jun;17(6):746-59 PMID: 17567994
  22. Analyses of deep mammalian sequence alignments and constraint predictions for 1% of the human genome.
    Genome Res. 2007 Jun;17(6):760-74 PMID: 17567995
  23. Finding cis-regulatory elements using comparative genomics: some lessons from ENCODE data.
    Genome Res. 2007 Jun;17(6):775-86 PMID: 17567996
  24. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project.
    Nature. 2007 Jun 14;447(7146):799-816 PMID: 17571346
  25. Estimation of average number of nucleotide substitutions when the rate of substitution varies with nucleotide.
    J Mol Evol. 1982;18(6):414-23 PMID: 7175958
  26. Nonrandomness of point mutation as reflected in nucleotide substitutions in pseudogenes and its evolutionary implications.
    J Mol Evol. 1984;21(1):58-71 PMID: 6442359
  27. Processed pseudogenes: characteristics and evolution.
    Annu Rev Genet. 1985;19:253-72 PMID: 3909943
  28. Retroposons--seeds of evolution.
    Science. 1991 Feb 15;251(4995):753 PMID: 1990437
  29. Vertebrate pseudogenes.
    FEBS Lett. 2000 Feb 25;468(2-3):109-14 PMID: 10692568
  30. Human LINE retrotransposons generate processed pseudogenes.
    Nat Genet. 2000 Apr;24(4):363-7 PMID: 10742098
  31. Initial sequencing and analysis of the human genome.
    Nature. 2001 Feb 15;409(6822):860-921 PMID: 11237011
  32. The complete human olfactory subgenome.
    Genome Res. 2001 May;11(5):685-702 PMID: 11337468
  33. Exclusive amplification of cDNA template (EXACT) RT-PCR to avoid amplifying contaminating genomic pseudogenes.
    Biotechniques. 2001 Oct;31(4):776-8, 780, 782 PMID: 11680707
  34. A maximum likelihood method for analyzing pseudogene evolution: implications for silent site evolution in humans and rodents.
    Mol Biol Evol. 2002 Jan;19(1):110-7 PMID: 11752196
  35. Molecular fossils in the human genome: identification and analysis of the pseudogenes in chromosomes 21 and 22.
    Genome Res. 2002 Feb;12(2):272-80 PMID: 11827946
  36. mRNA-specific reverse transcription-polymerase chain reaction from human tissue extracts.
    Anal Biochem. 2002 Aug 15;307(2):304-15 PMID: 12202248
  37. Human chromosome 21 gene expression atlas in the mouse.
    Nature. 2002 Dec 5;420(6915):582-6 PMID: 12466854
  38. LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA.
    Genome Res. 2003 Apr;13(4):721-31 PMID: 12654723
  39. Retroposed copies of the HMG genes: a window to genome dynamics.
    Genome Res. 2003 May;13(5):800-12 PMID: 12727900
  40. Patterns of nucleotide substitution, insertion and deletion in the human genome inferred from pseudogenes.
    Nucleic Acids Res. 2003 Sep 15;31(18):5338-48 PMID: 12954770
  41. Whole-genome screening indicates a possible burst of formation of processed pseudogenes and Alu repeats by particular L1 subfamilies in ancestral primates.
    Genome Biol. 2003;4(11):R74 PMID: 14611660
  42. Pseudogenes: are they "junk" or functional DNA?
    Annu Rev Genet. 2003;37:123-51 PMID: 14616058
  43. The origin of new genes: glimpses from the young and old.
    Nat Rev Genet. 2003 Nov;4(11):865-75 PMID: 14634634
  44. Millions of years of evolution preserved: a comprehensive catalog of the processed pseudogenes in the human genome.
    Genome Res. 2003 Dec;13(12):2541-58 PMID: 14656962
  45. A genome-wide survey of human pseudogenes.
    Genome Res. 2003 Dec;13(12):2559-67 PMID: 14656963
  46. Cap analysis gene expression for high-throughput analysis of transcriptional starting point and identification of promoter usage.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15776-81 PMID: 14663149
  47. MAVID: constrained ancestral alignment of multiple sequences.
    Genome Res. 2004 Apr;14(4):693-9 PMID: 15060012
  48. Aligning multiple genomic sequences with the threaded blockset aligner.
    Genome Res. 2004 Apr;14(4):708-15 PMID: 15060014
  49. GeneWise and Genomewise.
    Genome Res. 2004 May;14(5):988-95 PMID: 15123596
  50. A new role for expressed pseudogenes as ncRNA: regulation of mRNA stability of its homologous coding gene.
    J Mol Med (Berl). 2004 Jul;82(7):414-22 PMID: 15148580
  51. Improved techniques for the identification of pseudogenes.
    Bioinformatics. 2004 Aug 4;20 Suppl 1:i94-100 PMID: 15262786
  52. Large-scale analysis of pseudogenes in the human genome.
    Curr Opin Genet Dev. 2004 Aug;14(4):328-35 PMID: 15261647
  53. An X-to-autosome retrogene is required for spermatogenesis in mice.
    Nat Genet. 2004 Aug;36(8):872-6 PMID: 15258580
  54. A novel class of mammalian-specific tailless retropseudogenes.
    Genome Res. 2004 Oct;14(10A):1911-5 PMID: 15364902
  55. The ENCODE (ENCyclopedia Of DNA Elements) Project.
    Science. 2004 Oct 22;306(5696):636-40 PMID: 15499007
  56. A comparison of the human and chimpanzee olfactory receptor gene repertoires.
    Genome Res. 2005 Feb;15(2):224-30 PMID: 15687286
  57. Naturally occurring antisense: transcriptional leakage or real overlap?
    Genome Res. 2005 Mar;15(3):364-8 PMID: 15710751
  58. Transcribed processed pseudogenes in the human genome: an intermediate form of expressed retrosequence lacking protein-coding ability.
    Nucleic Acids Res. 2005;33(8):2374-83 PMID: 15860774
  59. Gene identification signature (GIS) analysis for transcriptome characterization and genome annotation.
    Nat Methods. 2005 Feb;2(2):105-11 PMID: 15782207
  60. Integrated pseudogene annotation for human chromosome 22: evidence for transcription.
    J Mol Biol. 2005 May 27;349(1):27-45 PMID: 15876366
  61. Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution.
    Science. 2005 May 20;308(5725):1149-54 PMID: 15790807
  62. Examples of the complex architecture of the human transcriptome revealed by RACE and high-density tiling arrays.
    Genome Res. 2005 Jul;15(7):987-97 PMID: 15998911
  63. Gene-breaking: a new paradigm for human retrotransposon-mediated gene evolution.
    Genome Res. 2005 Aug;15(8):1073-8 PMID: 16024818
  64. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes.
    Genome Res. 2005 Aug;15(8):1034-50 PMID: 16024819
  65. Initial sequence of the chimpanzee genome and comparison with the human genome.
    Nature. 2005 Sep 1;437(7055):69-87 PMID: 16136131
  66. Antisense transcription in the mammalian transcriptome.
    Science. 2005 Sep 2;309(5740):1564-6 PMID: 16141073
  67. Emergence of young human genes after a burst of retroposition in primates.
    PLoS Biol. 2005 Nov;3(11):e357 PMID: 16201836
  68. Genome sequence, comparative analysis and haplotype structure of the domestic dog.
    Nature. 2005 Dec 8;438(7069):803-19 PMID: 16341006
  69. Retroposition of processed pseudogenes: the impact of RNA stability and translational control.
    Trends Genet. 2006 Feb;22(2):69-73 PMID: 16356584
  70. Genomic fossils as a snapshot of the human transcriptome.
    Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1364-9 PMID: 16432206
  71. Evolutionary fate of retroposed gene copies in the human genome.
    Proc Natl Acad Sci U S A. 2006 Feb 28;103(9):3220-5 PMID: 16492757
  72. Iterative gene prediction and pseudogene removal improves genome annotation.
    Genome Res. 2006 May;16(5):678-85 PMID: 16651666
  73. Pseudo-messenger RNA: phantoms of the transcriptome.
    PLoS Genet. 2006 Apr;2(4):e23 PMID: 16683022
  74. Genome-wide identification of pseudogenes capable of disease-causing gene conversion.
    Hum Mutat. 2006 Jun;27(6):545-52 PMID: 16671097
  75. Genome-wide survey for biologically functional pseudogenes.
    PLoS Comput Biol. 2006 May;2(5):e46 PMID: 16680195
  76. Pseudogenes as a paradigm of neutral evolution.
    Nature. 1981 Jul 16;292(5820):237-9 PMID: 7254315
  77. Evolution of immunoglobulin VH pseudogenes in chickens.
    Mol Biol Evol. 1995 Jan;12(1):94-102 PMID: 7877500
  78. The size distribution of insertions and deletions in human and rodent pseudogenes suggests the logarithmic gap penalty for sequence alignment.
    J Mol Evol. 1995 Apr;40(4):464-73 PMID: 7769622
Article Info
Journal
Genome research
Abbr.
Genome Res
ISSN
1088-9051
Published
2007-06-00
Pages
839-51
Language
English
Region
United States
NLM ID
9518021
PMCID
PMC1891343
Subset
IM
Grants
NHGRI NIH HHS · U01 HG003147 · United States
NHGRI NIH HHS · U01HG03147 · United States
NHGRI NIH HHS · U01 HG003156 · United States
PHS HHS · N01C012400 · United States
NHGRI NIH HHS · U01HG03150 · United States
Wellcome Trust · 077198 · United Kingdom
NHGRI NIH HHS · U01HG03156 · United States
NCI NIH HHS · N01CO12400 · United States
NHGRI NIH HHS · U01 HG003150 · United States
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