Current topics in genome evolution: Molecular mechanisms of new gene formation

Cellular and Molecular Life Sciences

Volumn 64, Issue 5, 2007, Pages 542-554

  Babushok, D V ^a   Ostertag, E M ^a,b   Kazazian Jr , H H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Alternative splicing; Exon shuffling; Gene duplication; New gene formation; Retrotransposition

Indexed keywords

DNA; PROTEIN;

DNA DETERMINATION; EVOLUTIONARY ADAPTATION; GENE DUPLICATION; GENE STRUCTURE; GENOME ANALYSIS; MOLECULAR MECHANICS; REVIEW; RNA SPLICING; SPECIES DIFFERENTIATION; TANDEM REPEAT; VERTEBRATE; ALTERNATIVE RNA SPLICING; ANIMAL; EXON; EXPRESSED SEQUENCE TAG; GENETICS; GENOME; HUMAN; INTRON; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE;

EUKARYOTA;

ALTERNATIVE SPLICING; ANIMALS; CONSERVED SEQUENCE; DNA; EVOLUTION, MOLECULAR; EXONS; EXPRESSED SEQUENCE TAGS; GENE DUPLICATION; GENOME; HUMANS; INTRONS; PROTEINS; VERTEBRATES;

EID: 34247874698     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-006-6453-4     Document Type: Review

References (132)

1. Lander E. S., Linton L. M., Birren B., Nusbaum C., Zody M. C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W., Funke R., Gage D. et al. (2001) Initial sequencing and analysis of the human genome. Nature 409, 860-921.
2. Gibbs R. A., Weinstock G. M., Metzker M. L., Muzny D. M., Sodergren E. J., Scherer S., Scott G., Steffen D., Worley K. C., Burch P. E., Okwuonu G., Hines S. et al. (2004) Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428, 493-521.
3. Waterston R. H., Lindblad-Toh K., Birney E., Rogers J., Abril J. F., Agarwal P., Agarwala R., Ainscough R., Alexandersson M., An P., Antonarakis S. E., Attwood J. et al. (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520-562.
4. Lindblad-Toh K., Wade C. M., Mikkelsen T. S., Karlsson E. K., Jaffe D. B., Kamal M., Clamp M., Chang J. L., Kulbokas E. J., 3rd, Zody M. C., Mauceli E., Xie X. et al. (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438, 803-819.
5. The Chimpanzee Sequencing and Analysis Consortium (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437, 69-87.
6. Venter J. C., Adams M. D., Myers E. W., Li P. W., Mural R. J., Sutton G. G., Smith H. O., Yandell M., Evans C. A., Holt R. A., Gocayne J. D., Amanatides P. et al. (2001) The sequence of the human genome. Science 291, 1304-1351.
7. Hillier L. W., Miller W., Birney E., Warren W., Hardison R. C., Ponting C. P., Bork P., Burt D. W., Groenen M. A., Delany M. E., Dodgson J. B., Chinwalla A. T. et al. (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432, 695-716.
8. Aparicio S., Chapman J., Stupka E., Putnam N., Chia J. M., Dehal P., Christoffels A., Rash S., Hoon S., Smit A., Gelpke M. D., Roach J. et al. (2002) Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297, 1301-1310.
9. Liolios K., Tavernarakis N., Hugenholtz P. and Kyrpides N. C. (2006) The Genomes On Line Database (GOLD) v.2: a monitor of genome projects worldwide. Nucleic Acids Res. 34, D332-334.
10. Birney E., Andrews D., Caccamo M., Chen Y., Clarke L., Coates G., Cox T., Cunningham F., Curwen V., Cutts T., Down T., Durbin R. et al. (2006) Ensembl 2006. Nucleic Acids Res. 34, D556-561.
11. NCBI, http://www.ncbi.nlm.nih.gov/
12. Furey T. S. (2006) Comparison of human (and other) genome browsers. Hum. Genomics 2, 266-270.
13. Karolchik D., Baertsch R., Diekhans M., Furey T. S., Hinrichs A., Lu Y. T., Roskin K. M., Schwartz M., Sugnet C. W., Thomas D. J., Weber R. J., Haussler D. and Kent W. J. (2003) The UCSC Genome Browser Database. Nucleic Acids Res. 31, 51-54.
14. Lander E. S. (1996) The new genomics: global views of biology. Science 274, 536-539.
15. Thomas J. W., Touchman J. W., Blakesley R. W., Bouffard G. G., Beckstrom-Sternberg S. M., Margulies E. H., Blanchette M., Siepel A. C., Thomas P. J., McDowell J. C., Maskeri B., Hansen N. F. et al. (2003) Comparative analyses of multispecies sequences from targeted genomic regions. Nature 424, 788-793.
16. Margulies E. H., Maduro V. V., Thomas P. J., Tomkins J. P., Amemiya C. T., Luo M. and Green E. D. (2005) Comparative sequencing provides insights about the structure and conservation of marsupial and monotreme genomes. Proc. Natl. Acad. Sci. USA 102, 3354-3359.
17. Darwin C. (1859) By Means Of Natural Selection, Or The Preservation Of Favoured Races In The Struggle For Life. John Murray, London
18. Taylor J. S. and Raes J. (2004) Duplication and divergence: the evolution of new genes and old ideas. Annu. Rev. Genet. 38, 615-643.
19. Dorit R. L., Schoenbach L. and Gilbert W. (1990) How big is the universe of exons? Science 250, 1377-1382.
20. Li W. H., Gu Z., Wang H. and Nekrutenko A. (2001) Evolutionary analyses of the human genome. Nature 409, 847-849.
21. Long M., Rosenberg C. and Gilbert W. (1995) Intron phase correlations and the evolution of the intron/exon structure of genes. Proc. Natl. Acad. Sci. USA 92, 12495-12499.
22. de Souza S. J., Long M., Schoenbach L., Roy S. W. and Gilbert W. (1996) Intron positions correlate with module boundaries in ancient proteins. Proc. Natl. Acad. Sci. USA 93, 14632-14636.
23. Kaessmann H., Zollner S., Nekrutenko A. and Li W. H. (2002) Signatures of domain shuffling in the human genome. Genome Res. 12, 1642-1650.
24. Vibranovski M. D., Sakabe N. J., de Oliveira R. S. and de Souza S. J. (2005) Signs of ancient and modern exon-shuffling are correlated to the distribution of ancient and modern domains along proteins. J. Mol. Evol. 61, 341-350.
25. Patthy L. (1996) Exon shuffling and other ways of module exchange. Matrix Biol. 15, 301-310.
26. Patthy L. (2003) Modular assembly of genes and the evolution of new functions. Genetica 118, 217-231.
27. Claverie J. M. (2001) Gene number. What if there are only 30,000 human genes? Science 291, 1255-1257.
28. Long M., Betran E., Thornton K. and Wang W. (2003) The origin of new genes: glimpses from the young and old. Nat. Rev. Genet. 4, 865-875.
29. Salzberg S. L., White O., Peterson J. and Eisen J. A. (2001) Microbial genes in the human genome: Lateral transfer or gene loss? Science 292, 1903-1906.
30. Stanhope M. J., Lupas A., Italia M. J., Koretke K. K., Volker C. and Brown J. R. (2001) Phylogenetic analyses do not support horizontal gene transfers from bacteria to vertebrates. Nature 411, 940-944.
31. DeFilippis V., Villarreal; L. P., Salzberg S. L. and Eisen J. A. (2001) Lateral gene transfer or viral colonization? Science 293, 1048a
32. Roelofs J. and Van Haastert P. J. (2001) Genes lost during evolution. Nature 411, 1013-1014.
33. Andersson J. O. (2005) Lateral gene transfer in eukaryotes. Cell. Mol. Life Sci. 62, 1182-1197.
34. Modrek B., Resch A., Grasso C. and Lee C. (2001) Genome-wide detection of alternative splicing in expressed sequences of human genes. Nucleic Acids Res. 29, 2850-2859.
35. Johnson J. M., Castle J., Garrett-Engele P., Kan Z., Loerch P. M., Armour C. D., Santos R., Schadt E. E., Stoughton R. and Shoemaker D. D. (2003) Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302, 2141-2144.
36. Stolc V., Gauhar Z., Mason C., Halasz G., van Batenburg M. F., Rifkin S. A., Hua S., Herreman T., Tongprasit W., Barbano P. E., Bussemaker H. J. and White K. P. (2004) A gene expression map for the euchromatic genome of Drosophila melanogaster. Science 306, 655-660.
37. Blencowe B. J. (2006) Alternative splicing: new insights from global analyses. Cell 126, 37-47.
38. Resch A., Xing Y., Modrek B., Gorlick M., Riley R. and Lee C. (2004) Assessing the impact of alternative splicing on domain interactions in the human proteome. J. ProteomeRes. 3, 76-83.
39. Yeo G., Holste D., Kreiman G. and Burge C. B. (2004) Variation in alternative splicing across human tissues. Genome Biol. 5, R74.
40. Crawford J. B. and Patton J. G. (2006) Activation of alpha - tropomyosin exon 2 is regulated by the SR protein 9G8 and heterogeneous nuclear ribonucleoproteins H and F. Mol. Cell. Biol. 26, 8791-8802.
41. 2+ regulation associated with development. J. Mol. Biol. 352, 58-71.
42. Kogerman P., Krause D., Rahnama F., Kogerman L., Unden A. B., Zaphiropoulos P. G. and Toftgard R. (2002) Alternative first exons of PTCH1 are differentially regulated in vivo and may confer different functions to the PTCH1 protein. Oncogene 21, 6007-6016.
43. Zaphiropoulos P. G. (1999) RNA molecules containing exons originating from different members of the cytochrome P450 2C gene subfamily (CYP2C) in human epidermis and liver. Nucleic Acids Res. 27, 2585-2590.
44. Magrangeas F., Pitiot G., Dubois S., Bragado-Nilsson E., Cherel M., Jobert S., Lebeau B., Boisteau O., Lethe B., Mallet J., Jacques Y. and Minvielle S. (1998) Cotranscription and intergenic splicing of human galactose-1- phosphate uridylyltransferase and interleukin-11 receptor alpha-chain genes generate a fusion mRNA in normal cells. Implication for the production of multidomain proteins during evolution. J. Biol. Chem. 273, 16005-16010.
45. Akiva P., Toporik A., Edelheit S., Peretz Y., Diber A., Shemesh R., Novik A. and Sorek R. (2006) Transcription-mediated gene fusion in the human genome. Genome Res. 16, 30-36.
46. Parra G., Reymond A., Dabbouseh N., Dermitzakis E. T., Castelo R., Thomson T. M., Antonarakis S. E. and Guigo R. (2006) Tandem chimerism as a means to increase protein complexity in the human genome. Genome Res. 16, 37-44.
47. Fears S., Mathieu C., Zeleznik-Le N., Huang S., Rowley J. D. and Nucifora G. (1996) Intergenic splicing of MDS1 and EVI1 occurs in normal tissues as well as in myeloid leukemia and produces a new member of the PR domain family. Proc. Natl. Acad. Sci. USA 93, 1642-1647.
48. Pardigol A., Forssmann U., Zucht H. D., Loetscher P., Schulz-Knappe P., Baggiolini M., Forssmann W. G. and Magert H. J. (1998) HCC-2, a human chemokine: gene structure, expression pattern, and biological activity. Proc. Natl. Acad. Sci. USA 95, 6308-6313.
49. Upadhyaya A. B., Lee S. H. and DeJong J. (1999) Identification of a general transcription factor TFIIAalpha/beta homolog selectively expressed in testis. J. Biol. Chem. 274, 18040-18048.
50. Millar J. K., Christie S., Semple C. A. and Porteous D. J. (2000) Chromosomal location and genomic structure of the human translin-associated factor X gene (TRAX; TSNAX) revealed by intergenic splicing to DISC1, a gene disrupted by a translocation segregating with schizophrenia. Genomics 67, 69-77.
51. Thomson T. M., Lozano J. J., Loukili N., Carrio R., Serras F., Cormand B., Valeri M., Diaz V. M., Abril J., Burset M., Merino J., Macaya A., Corominas M. and Guigo R. (2000) Fusion of the human gene for the polyubiquitination coeffector UEV1 with Kua, a newly identified gene. Genome Res. 10, 1743-1756.
52. Communi D., Suarez-Huerta N., Dussossoy D., Savi P. and Boeynaems J. M. (2001) Cotranscription and intergenic splicing of human P2Y11 and SSF1 genes. J. Biol. Chem. 276, 16561-16566.
53. Cox P. R., Siddique T. and Zoghbi H. Y. (2001) Genomic organization of Tropomodulins 2 and 4 and unusual intergenic and intraexonic splicing of YL-1 and Tropomodulin 4. BMC Genomics 2, 7.
54. Kolfschoten G. M., Pradet-Balade B., Hahne M. and Medema J. P. (2003) TWE-PRIL; a fusion protein of TWEAK and APRIL. Biochem. Pharmacol. 66, 1427-1432.
55. Kato M., Khan S., Gonzalez N., O'Neill B. P., McDonald K. J., Cooper B. J., Angel N. Z. and Hart D. N. (2003) Hodgkin's lymphoma cell lines express a fusion protein encoded by intergenically spliced mRNA for the multilectin receptor DEC-205 (CD205) and a novel C-type lectin receptor DCL-1. J. Biol. Chem. 278, 34035-34041.
56. Poulin F., Brueschke A. and Sonenberg N. (2003) Gene fusion and overlapping reading frames in the mammalian genes for 4E-BP3 and MASK. J. Biol. Chem. 278, 52290-52297.
57. Maeda K., Horikoshi T., Nakashima E., Miyamoto Y., Mabuchi A. and Ikegawa S. (2005) MATN and LAPTM are parts of larger transcription units produced by intergenic splicing: Intergenic splicing may be a common phenomenon. DNA Res. 12, 365-372.
58. Roux M., Leveziel H. and Amarger V. (2006) Cotranscription and intergenic splicing of the PPARG and TSEN2 genes in cattle. BMC Genomics 7, 71.
59. Nekrutenko A. (2004) Identification of novel exons from rat-mouse comparisons. J. Mol. Evol. 59, 703-708.
60. Wang W., Zheng H., Yang S., Yu H., Li J., Jiang H., Su J., Yang L., Zhang J., McDermott J., Samudrala R., Wang J., Yang H., Yu J., Kristiansen K. and Wong G. K. (2005) Origin and evolution of new exons in rodents. Genome Res. 15, 1258-1264.
61. Makalowski W., Mitchell G. A. and Labuda D. (1994) Alu sequences in the coding regions of mRNA: a source of protein variability. Trends Genet. 10, 188-193.
62. Nekrutenko A. and Li W. H. (2001) Transposable elements are found in a large number of human protein-coding genes. Trends Genet. 17, 619-621.
63. Zhang X. H. and Chasin L. A. (2006) Comparison of multiple vertebrate genomes reveals the birth and evolution of human exons. Proc. Natl. Acad. Sci. USA 103, 13427-13432.
64. Gotea V. and Makalowski W. (2006) Do transposable elements really contribute to proteomes? Trends Genet. 22, 260-267.
65. Pavlicek A., Clay O. and Bernardi G. (2002) Transposable elements encoding functional proteins: pitfalls in unprocessed genomic data? FEBS Lett. 523, 252-253.
66. Belancio V. P., Hedges D. J. and Deininger P. (2006) LINE-1 RNA splicing and influences onmammalian gene expression. Nucleic Acids Res. 34, 1512-1521.
67. Lewis B. P., Green R. E. and Brenner S. E. (2003) Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc. Natl. Acad. Sci. USA 100, 189-192.
68. Nagy E. and Maquat L. E. (1998) A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem. Sci. 23, 198-199.
69. McLysaght A., Hokamp K. and Wolfe K. H. (2002) Extensive genomic duplication during early chordate evolution. Nat. Genet. 31, 200-204.
70. Blanc G. and Wolfe K. H. (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16, 1679-1691.
71. Jaillon O., Aury J. M., Brunet F., Petit J. L., Stange-Thomann N., Mauceli E., Bouneau L, Fischer C., Ozouf-Costaz C., Bernot A., Nicaud S., Jaffe D. et al. (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431, 946-957.
72. Samonte R. V. and Eichler E. E. (2002) Segmental duplications and the evolution of the primate genome. Nat. Rev. Genet. 3, 65-72.
73. Bailey J. A., Gu Z., Clark R. A., Reinert K., Samonte R. V., Schwartz S., Adams M. D., Myers E. W., Li P. W. and Eichler E. E. (2002) Recent segmental duplications in the human genome. Science 297, 1003-1007.
74. Zhang J. (2003) Evolution by gene duplication: an update. Trends Ecol. Evol. 18, 292-298.
75. Thompson L. H. and Schild D. (2001) Homologous recombinational repair of DNA ensures mammalian chromosome stability. Mutat Res. 477, 131-153.
76. Holland P. W. and Takahashi T. (2005) The evolution of homeobox genes: Implications for the study of brain development. Brain Res Bull. 66, 484-490.
77. Shen S. H., Slightom J. L. and Smithies O. (1981) A history of the human fetal globin gene duplication. Cell 26, 191-203.
78. Bailey J. A., Liu G. and Eichler E. E. (2003) An Alu transposition model for the origin and expansion of human segmental duplications. Am. J. Hum. Genet. 73, 823-834.
79. Babcock M., Pavlicek A., Spiteri E., Kashork C. D., Ioshikhes I., Shaffer L. G., Jurka J. and Morrow B. E. (2003) Shuffling of genes within low-copy repeats on 22q11 (LCR22) by Alu-mediated recombination events during evolution. Genome Res. 13, 2519-2532.
80. van Rijk A. and Bloemendal H. (2003) Molecular mechanisms of exon shuffling: illegitimate recombination. Genetica 118, 245-249.
81. van Rijk A. A., de Jong, W. W. and Bloemendal, H. (1999) Exon shuffling mimicked in cell culture. Proc. Natl. Acad. Sci. USA 96, 8074-8079.
82. Roth D. B., Porter T. N. and Wilson J. H. (1985) Mechanisms of nonhomologous recombination in mammalian cells. Mol. Cell. Biol. 5, 2599-2607.
83. Lynch M. and Conery J. S. (2000) The evolutionary fate and consequences of duplicate genes. Science 290, 1151-1155.
84. Eichler E. E. (2001) Recent duplication, domain accretion and the dynamic mutation of the human genome. Trends Genet. 17, 661-669.
85. Stankiewicz P., Shaw C. J., Withers M., Inoue K. and Lupski J. R. (2004) Serial segmental duplications during primate evolution result in complex human genome architecture. Genome Res. 14, 2209-2220.
86. Courseaux A., Richard F., Grosgeorge J., Ortola C., Viale A., Turc-Carel C., Dutrillaux B., Gaudray P. and Nahon J.-L. (2003) Segmental duplications in euchromatic regions of human chromosome 5: A source of evolutionary instability and transcriptional innovation. Genome Res. 13, 369-381.
87. Zhang Z., Harrison P. M., Liu Y. and Gerstein M. (2003) Millions of years of evolution preserved: a comprehensive catalog of the processed pseudogenes in the human genome. Genome Res. 13, 2541-2558.
88. Zhang Z., Carriero N. and Gerstein M. (2004) Comparative analysis of processed pseudogenes in the mouse and human genomes. Trends Genet. 20, 62-67.
89. Ohshima K., Hattori M., Yada T., Gojobori T., Sakaki Y. and Okada N. (2003) Whole-genome screening indicates a possible burst of formation of processed pseudogenes and Alu repeats by particular L1 subfamilies in ancestral primates. Genome Biol. 4, R74.
90. Marques A. C., Dupanloup I., Vinckenbosch N., Reymond A. and Kaessmann H. (2005) Emergence of young human genes after a burst of retroposition in primates. PLoS Biol. 3, e357.
91. Khelifi A., Duret L. and Mouchiroud D. (2005) HOPPSIGEN: a database of human and mouse processed pseudogenes. Nucleic Acids Res. 33, D59-66.
92. Ostertag E. M. and Kazazian H. H. Jr. (2001) Biology of mammalian L1 retrotransposons. Annu. Rev. Genet. 35, 501-538.
93. Wei W., Gilbert N., Ooi S. L., Lawler J. F., Ostertag E. M., Kazazian H. H., Boeke J. D. and Moran J. V. (2001) Human L1 retrotransposition: cis preference versus trans complementation. Mol. Cell. Biol. 21, 1429-1439.
94. Esnault C., Maestre J. and Heidmann T. (2000) Human LINE retrotransposons generate processed pseudogenes. Nat. Genet. 24, 363-367.
95. McCarrey J. R. and Thomas K. (1987) Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature 326, 501-505.
96. Mighell A. J., Smith N. R., Robinson P. A. and Markham A. F. (2000) Vertebrate pseudogenes. FEBS Lett. 468, 109-114.
97. Makeyev A. V., Chkheidze A. N. and Liebhaber S. A. (1999) A set of highly conserved RNA-binding proteins, alphaCP-1 and alphaCP-2, implicated in mRNA stabilization, are coexpressed from an intronless gene and its intron-containing paralog. J. Biol. Chem. 274, 24849-24857.
98. Bradley J., Baltus A., Skaletsky H., Royce-Tolland M., Dewar K. and Page D. C. (2004)An X-to-autosome retrogene is required for spermatogenesis in mice. Nat. Genet. 36, 872-876.
99. Vinckenbosch N., Dupanloup I. and Kaessmann H. (2006) Evolutionary fate of retroposed gene copies in the human genome. Proc. Natl. Acad. Sci. USA 103, 3220-3225.
100. Kleene K. C., Mulligan E., Steiger D., Donohue K. and Mastrangelo M. A. (1998) 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. 47, 275-281.
101. Betran E. and Long M. (2003) Dntf-2r, a young Drosophila retroposed gene with specific male expression under positive Darwinian selection. Genetics 164, 977-988.
102. Harrison P. M., Zheng D., Zhang Z., Carriero N. and Gerstein M. (2005) Transcribed processed pseudogenes in the human genome: an intermediate form of expressed retrosequence lacking protein-coding ability. Nucleic Acids Res. 33, 2374-2383.
103. Wang P. J. and Page D. C. (2002) Functional substitution for TAF(II)250 by a retroposed homolog that is expressed in human spermatogenesis. Hum. Mol. Genet. 11, 2341-2346.
104. Burki F. and Kaessmann H. (2004) Birth and adaptive evolution of a hominoid gene that supports high neurotransmitter flux. Nat. Genet. 36, 1061-1063.
105. Schmidt E. E. and Schibler U. (1995) High accumulation of components of the RNA polymerase II transcription machinery in rodent spermatids. Development 121, 2373-2383.
106. Schmidt E. E. and Schibler U. (1997) Developmental testis-specific regulation of mRNA levels and mRNA translational efficiencies for TATA-binding protein mRNA isoforms. Dev. Biol. 184, 138-149.
107. Schmidt E. E. (1996) Transcriptional promiscuity in testes. Curr. Biol. 6, 768-769.
108. Ossipow V., Tassan J. P., Nigg E. A. and Schibler U. (1995) A mammalian RNA polymerase II holoenzyme containing all components required for promoter-specific transcription initiation. Cell 83, 137-146.
109. Emerson J. J., Kaessmann H., Betran E. and Long M. (2004) Extensive gene traffic on the mammalian X chromosome. Science 303, 537-540.
110. Betran E., Thornton K. and Long M. (2002) Retroposed new genes out of the X in Drosophila. Genome Res. 12, 1854-1859.
111. Handel M. A., Park C. and Kot M. (1994) Genetic control of sex-chromosome inactivation during male meiosis. Cytogenet. Cell Genet. 66, 83-88.
112. Richler C., Soreq H. and Wahrman J. (1992) X inactivation in mammalian testis is correlated with inactive X-specific transcription. Nat. Genet. 2, 192-195.
113. Turner J. M., Mahadevaiah S. K., Elliott D. J., Garchon H. J., Pehrson J. R., Jaenisch R. and Burgoyne P. S. (2002) Meiotic sex chromosome inactivation in male mice with targeted disruptions of Xist. J. Cell Sci. 115, 4097-4105.
114. Sayah D. M., Sokolskaja E., Berthoux L. and Luban J. (2004) Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430, 569-573.
115. Goodier J. L., Ostertag E. M. and Kazazian H. H. Jr. (2000) Transduction of 3′-flanking sequences is common in L1 retrotransposition. Hum. Mol. Genet. 9, 653-657.
116. Moran J. V., DeBerardinis R. J. and Kazazian H. H. J. (1999) Exon shuffling by L1 retrotransposition. Science 283, 1530-1534.
117. Shemesh R., Novik A., Edelheit S. and Sorek R. (2006) Genomic fossils as a snapshot of the human transcriptome. Proc. Natl. Acad. Sci. USA 103, 1364-1369.
118. Finta C. and Zaphiropoulos P. G. (2002) Intergenic mRNA molecules resulting from trans-splicing. J. Biol. Chem. 277, 5882-5890.
119. Caudevilla C., Serra D., Miliar A., Codony C., Asins G., Bach M. and Hegardt F. G. (1998) Natural trans-splicing in carnitine octanoyltransferase pre-mRNAs in rat liver. Proc. Natl. Acad. Sci. USA. 95, 12185-12190.
120. Pasman Z. and Garcia-Blanco M. A. (1996) The 5′ and 3′ splice sites come together via a three dimensional diffusion mechanism. Nucleic Acids Res. 24, 1638-1645.
121. Chetverina H. V., Demidenko A. A., Ugarov V. I. and Chetverin A. B. (1999) Spontaneous rearrangements in RNA sequences. FEBS Lett. 450, 89-94.
122. Gmyl A. P., Belousov E. V., Maslova S. V., Khitrina E. V., Chetverin A. B. and Agol V. I. (1999) Nonreplicative RNA recombination in poliovirus. J. Virol. 73, 8958-8965.
123. Buzdin A., Ustyugova S., Gogvadze E., Vinogradova T., Lebedev Y. and Sverdlov E. (2002) A new family of chimeric retrotranscripts formed by a full copy of U6 small nuclear RNAfused to the 3′ terminus of l1. Genomics 80, 402-406.
124. Buzdin A., Gogvadze E., Kovalskaya E., Volchkov P., Ustyugova S., Illarionova A., Fushan A., Vinogradova T. and Sverdlov E. (2003) The human genome contains many types of chimeric retrogenes generated through in vivo RNA recombination. Nucleic Acids Res. 31, 4385-4390.
125. Gogvadze E. V., Buzdin A. A. and Sverdlov E. D. (2005) Multiple template switches on LINE-directed reverse transcription: the most probable formation mechanism for the double and triple chimeric retroelements in mammals. Bioorg. Khim. 31, 82-89.
126. Goodier J. L., Ostertag E. M., Engleka K. A., Seleme M. C. and Kazazian H. H. Jr (2004) A potential role for the nucleolus in L1 retrotransposition. Hum. Mol. Genet. 13, 1041-1048.
127. Britten R. J. (2004) Coding sequences of functioning human genes derived entirely from mobile element sequences. Proc. Natl. Acad. Sci. USA 101, 16825-16830.
128. Kimura M. (1983) The Neutral Theory of Molecular Evolution. Cambridge University Press, Cambridge
129. Jones C. D. and Begun D. J. (2005) Parallel evolution of chimeric fusion genes. Proc. Natl. Acad. Sci. USA 102, 11373-11378.
130. Rubin G. M., Yandell M. D., Wortman J. R., Gabor Miklos G. L., Nelson C. R., Hariharan I. K., Fortini M. E., Li P. W., Apweiler R., Fleischmann W., Cherry J. M., Henikoff S. et al. (2000) Comparative genomics of the eukaryotes. Science 287, 2204-2215.
131. Kim J. M., Vanguri S., Boeke J. D., Gabriel A. and Voytas D. F. (1998) Transposable elements and genome organization: A comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res. 8, 464-478.
132. Jones J. M., Huang J. D., Mermall V., Hamilton B. A., Mooseker M. S., Escayg A., Copeland N. G., Jenkins N. A. and Meisler M. H. (2000) The mouse neurological mutant flailer expresses a novel hybrid gene derived by exon shuffling between Gnb5 and Myo5a. Hum. Mol. Genet. 9, 821-828.