Natural selection drives the accumulation of amino acid tandem repeats in human proteins

Genome Research

Volumn 20, Issue 6, 2010, Pages 745-754

  Mularoni, Loris ^a,b   Ledda, Alice ^a   Toll Riera, Macarena ^a,c   Albà, M Mar ^a,c,d  

^a INST MUNIC D INVESTIGACIO MEDICA   (Spain)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; TRINUCLEOTIDE;

ARTICLE; CELLULAR DISTRIBUTION; DNA SEQUENCE; GENETIC TRANSCRIPTION; HUMAN; MUTATION RATE; NATURAL SELECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; TANDEM REPEAT; TRINUCLEOTIDE REPEAT;

AMINO ACID SEQUENCE; AMINO ACIDS; ANIMALS; HUMANS; MOLECULAR SEQUENCE DATA; PROTEINS; REPETITIVE SEQUENCES, AMINO ACID; SELECTION, GENETIC; SEQUENCE HOMOLOGY, AMINO ACID;

EUKARYOTA; VERTEBRATA;

EID: 77952977231     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.101261.109     Document Type: Article

References (63)

1. Albà MM, Guigo R. 2004. Comparative analysis of amino acid repeats in rodents and humans. Genome Res 14: 549-554. (Pubitemid 38500225)
2. Albà MM, Santibanez-Koref MF, Hancock JM. 1999a. Amino acid reiterations in yeast are overrepresented in particular classes of proteins and show evidence of a slippage-like mutational process. J Mol Evol 49: 789-797.
3. Albà MM, Santibanez-Koref MF, Hancock JM. 1999b. Conservation of polyglutamine tract size between mice and humans depends on codon interruption. Mol Biol Evol 16: 1641-1644.
4. Albà MM, Santibáñez-Koref MF, Hancock JM. 2001. The comparative genomics of polyglutamine repeats: Extreme differences in the codon organization of repeat-encoding regions between mammals and Drosophila. J Mol Evol 52: 249-259. (Pubitemid 32299607)
5. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402. (Pubitemid 27359211)
6. Alvarez M, Estivill X, de la Luna S. 2003. DYRK1A accumulates in splicing speckles through a novel targeting signal and induces speckle disassembly. J Cell Sci 116: 3099-3107. (Pubitemid 37038959)
7. Amiel J, Laudier B, Attie-Bitach T, Trang H, de Pontual L, Gener B, Trochet D, Etchevers H, Ray P, Simonneau M, et al. 2003. Polyalanine expansion and frameshift mutations of the paired-like homeobox gene PHOX2B in congenital central hypoventilation syndrome. Nat Genet 33: 459-461. (Pubitemid 36390004)
8. Amiel J, Trochet D, Clement-Ziza M, Munnich A, Lyonnet S. 2004. Polyalanine expansions in human. Hum Mol Genet 13: R235-R243.
9. Anan K, Yoshida N, Kataoka Y, Sato M, Ichise H, Nasu M, Ueda S. 2007. Morphological change caused by loss of the taxon-specific polyalanine tract in Hoxd-13. Mol Biol Evol 24: 281-287. (Pubitemid 46028506)
10. Brown LY, Brown SA. 2004. Alanine tracts: The expanding story of human illness and trinucleotide repeats. Trends Genet 20: 51-58.
11. Brown L, Paraso M, Arkell R, Brown S. 2005. In vitro analysis of partial loss-of-function ZIC2 mutations in holoprosencephaly: Alanine tract expansion modulates DNA binding and transactivation. Hum Mol Genet 14: 411-420.
12. Buchanan G, Yang M, Cheong A, Harris JM, Irvine RA, Lambert PF, Moore NL, Raynor M, Neufing PJ, Coetzee GA, et al. 2004. Structural and functional consequences of glutamine tract variation in the androgen receptor. Hum Mol Genet 13: 1677-1692. (Pubitemid 39173438)
13. Dalby AR. 2009. A comparative proteomic analysis of the simple amino acid repeat distributions in Plasmodia reveals lineage specific amino acid selection. PLoS One 4: e6231. doi: 10.1371/journal.pone.0006231.
14. Dunker AK, Silman I, Uversky VN, Sussman JL. 2008. Function and structure of inherently disordered proteins. Curr Opin Struct Biol 18: 756-764.
15. Faux NG, Bottomley SP, Lesk AM, Irving JA, Morrison JR, de la Banda MG, Whisstock JC. 2005. Functional insights from the distribution and role of homopeptide repeat-containing proteins. Genome Res 15: 537-551.
16. Faux NG, Huttley GA, Mahmood K, Webb GI, de la Banda MG, Whisstock JC. 2007. RCPdb: An evolutionary classification and codon usage database for repeat-containing proteins. Genome Res 17: 1118-1127. (Pubitemid 47026359)
17. Fondon JW III, Garner HR. 2004. Molecular origins of rapid and continuous morphological evolution. Proc Natl Acad Sci 101: 18058-18063.
18. Fondon JW III, Mele GM, Brezinschek RI, Cummings D, Pande A, Wren J, O'Brien KM, Kupfer KC,Wei MH, Lerman M, et al. 1998. Computerized polymorphic marker identification: Experimental validation and a predicted human polymorphism catalog. Proc Natl Acad Sci 95: 7514-7519. (Pubitemid 28293284)
19. Galant R, Carroll SB. 2002. Evolution of a transcriptional repression domain in an insect Hox protein. Nature 415: 910-913. (Pubitemid 34174752)
20. Gatchel JR, Zoghbi HY. 2005. Diseases of unstable repeat expansion: Mechanisms and common principles. Nat Rev Genet 6: 743-755.
21. Gerber HP, Seipel K, Georgiev O, Hofferer M, Hug M, Rusconi S, Schaffner W. 1994. Transcriptional activation modulated by homopolymeric glutamine and proline stretches. Science 263: 808-811. (Pubitemid 24093208)
22. Green H, Wang N. 1994. Codon reiteration and the evolution of proteins. Proc Natl Acad Sci 91: 4298-4302.
23. Haerty W, Golding GB. 2010. Genome-wide evidence for selection acting on single amino acid repeats. Genome Res (this issue). doi: 10.1101/ gr.101246.109.
24. Hancock JM, Worthey EA, Santibanez-Koref MF. 2001. A role for selection in regulating the evolutionary emergence of disease-causing and other coding CAG repeats in humans and mice. Mol Biol Evol 18: 1014-1023.
25. Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, Foulger R, Eilbeck K, Lewis S, Marshall B, Mungall C, et al. 2004. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32: D258-D261. (Pubitemid 38081651)
26. Hubbard TJ, Aken BL, Beal K, Ballester B, Caccamo M, Chen Y, Clarke L, Coates G, Cunningham F, Cutts T, et al. 2007. Ensembl 2007. Nucleic Acids Res 35: D610-D617.
27. Huntley MA, Clark AG. 2007. Evolutionary analysis of amino acid repeats across the genomes of 12 Drosophila species. Mol Biol Evol 24: 2598-2609.
28. Huntley M, Golding GB. 2000. Evolution of simple sequence in proteins. J Mol Evol 51: 131-140.
29. Huntley MA, Golding GB. 2002. Simple sequences are rare in the Protein Data Bank. Proteins 48: 134-140.
30. Huntley MA, Golding GB. 2006. Selection and slippage creating serine homopolymers. Mol Biol Evol 23: 2017-2025.
31. Igarashi S, Koide R, Shimohata T, Yamada M, Hayashi Y, Takano H, Date H, Oyake M, Sato T, Sato A, et al. 1998. Suppression of aggregate formation and apoptosis by transglutaminase inhibitors in cells expressing truncated DRPLA protein with an expanded polyglutamine stretch. Nat Genet 18: 111-117.
32. Janody F, Sturny R, Schaeffer V, Azou Y, Dostatni N. 2001. Two distinct domains of Bicoid mediate its transcriptional downregulation by the Torso pathway. Development 128: 2281-2290. (Pubitemid 32633361)
33. Karlin S, Brocchieri L, Bergman A, Mrazek J, Gentles AJ. 2002. Amino acid runs in eukaryotic proteomes and disease associations. Proc Natl Acad Sci 99: 333-338. (Pubitemid 34060363)
34. Karolchik D, Kuhn RM, Baertsch R, Barber GP, Clawson H, Diekhans M, Giardine B, Harte RA, Hinrichs AS, Hsu F, et al. 2008. The UCSC Genome Browser Database: 2008 update. Nucleic Acids Res 36: D773-D779. (Pubitemid 351149822)
35. Kashi Y, King DG. 2006. Simple sequence repeats as advantageous mutators in evolution. Trends Genet 22: 253-259.
36. Kasprzyk A, Keefe D, Smedley D, London D, Spooner W, Melsopp C, Hammond M, Rocca-Serra P, Cox T, Birney E. 2004. EnsMart: A generic system for fast and flexible access to biological data. Genome Res 14: 160-169. (Pubitemid 38088537)
37. Kruglyak S, Durrett RT, Schug MD, Aquadro CF. 1998. Equilibrium distributions of microsatellite repeat length resulting from a balance between slippage events and point mutations. Proc Natl Acad Sci 95: 10774-10778. (Pubitemid 28413144)
38. Lamond AI, Spector DL. 2003. Nuclear speckles: A model for nuclear organelles. Nat Rev Mol Cell Biol 4: 605-612.
39. Lanz RB, Wieland S, Hug M, Rusconi S. 1995. A transcriptional repressor obtained by alternative translation of a trinucleotide repeat. Nucleic Acids Res 23: 138-145.
40. Lavoie H, Debeane F, Trinh QD, Turcotte JF, Corbeil-Girard LP, Dicaire MJ, Saint-Denis A, Page M, Rouleau GA, Brais B. 2003. Polymorphism, shared functions and convergent evolution of genes with sequences coding for polyalanine domains. Hum Mol Genet 12: 2967-2979. (Pubitemid 37442025)
41. Lovell SC. 2003. Are non-functional, unfolded proteins ('junk proteins') common in the genome? FEBS Lett 554: 237-239.
42. Miller W, RosenbloomK, Hardison RC, Hou M, Taylor J, Raney B, Burhans R, King DC, Baertsch R, Blankenberg D, et al. 2007. 28-Way vertebrate alignment and conservation track in the UCSC Genome Browser. Genome Res 17: 1797-1808.
43. Mortlock DP, Sateesh P, Innis JW. 2000. Evolution of N-terminal sequences of the vertebrate HOXA13 protein. Mamm Genome 11: 151-158. (Pubitemid 30054419)
44. Mularoni L, Guigo R, Albà MM. 2006. Mutation patterns of amino acid tandem repeats in the human proteome. Genome Biol 7: R33. doi: 10.1186/gb-2006-7-4-r33. (Pubitemid 43871877)
45. Mularoni L, Veitia RA, Albà MM. 2007. Highly constrained proteins contain an unexpectedly large number of amino acid tandem repeats. Genomics 89: 316-325. (Pubitemid 46205127)
46. Mularoni L, Toll-Riera M, Albà MM. 2008. Comparative genetics of trinucleotide repeats in the human and ape genomes. In Handbook of human molecular evolution (ed. DN Cooper, H Kehrer-Sawatzki), pp. 677-686. Wiley, Chichester, UK.
47. Muragaki Y, Mundlos S, Upton J, Olsen BR. 1996. Altered growth and branching patterns in synpolydactyly caused by mutations in HOXD13. Science 272: 548-551. (Pubitemid 26138198)
48. Nakachi Y, Hayakawa T, Oota H, Sumiyama K, Wang L, Ueda S. 1997. Nucleotide compositional constraints on genomes generate alanine-, glycine-, and proline-rich structures in transcription factors. Mol Biol Evol 14: 1042-1049. (Pubitemid 27419240)
49. Notredame C, Higgins DG, Heringa J. 2000. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302: 205-217.
50. Panopoulou G, Poustka AJ. 2005. Timing and mechanism of ancient vertebrate genome duplications - the adventure of a hypothesis. Trends Genet 21: 559-567. (Pubitemid 41278461)
51. Ponting CP. 2008. The functional repertoires of metazoan genomes. Nat Rev Genet 9: 689-698.
52. R Development Core Team. 2007. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.r-project.org/
53. Salichs E, Ledda A, Mularoni L, Albà MM, de la Luna S. 2009. Genome-wide analysis of histidine repeats reveals their role in the localization of human proteins to the nuclear speckles compartment. PLoS Genet 5: e1000397. doi: 10.1371/journal.pgen.1000397.
54. Shimohata T, Nakajima T, Yamada M, Uchida C, Onodera O, Naruse S, Kimura T, Koide R, Nozaki K, Sano Y, et al. 2000. Expanded polyglutamine stretches interact with TAFII130, interfering with CREB-dependent transcription. Nat Genet 26: 29-36.
55. Simon M, Hancock JM. 2009. Tandem and cryptic amino acid repeats accumulate in disordered regions of proteins. Genome Biol 10: R59. doi: 10.1186/gb-2009-10-6-r59.
56. Sumiyama K, Washio-Watanabe K, Saitou N, Hayakawa T, Ueda S. 1996. Class III POU genes: Generation of homopolymeric amino acid repeats under GC pressure in mammals. J Mol Evol 43: 170-178. (Pubitemid 26315118)
57. Tompa P. 2003. Intrinsically unstructured proteins evolve by repeat expansion. BioEssays 25: 847-855. (Pubitemid 37081750)
58. Venkataraman S, Stevenson P, Yang Y, Richardson L, Burton N, Perry TP, Smith P, Baldock RA, Davidson DR, Christiansen JH. 2008. EMAGE - Edinburgh Mouse Atlas of Gene Expression: 2008 update. Nucleic Acids Res 36: D860-D865. (Pubitemid 351149836)
59. Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, Birney E. 2009. Ensembl Compara Gene Trees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19: 327-335.
60. Weber JL, Wong C. 1993. Mutation of human short tandem repeats. Hum Mol Genet 2: 1123-1128. (Pubitemid 23244988)
61. Wren JD, Forgacs E, Fondon JW III, Pertsemlidis A, Cheng SY, Gallardo T, Williams RS, Shohet RV, Minna JD, Garner HR. 2000. Repeat polymorphisms within gene regions: phenotypic and evolutionary implications. Am J Hum Genet 67: 345-356. (Pubitemid 30616740)
62. Wu HT, Su YN, Hung CC, Hsieh WS, Wu KJ. 2009. Interaction between PHOX2B and CREBBP mediates synergistic activation: Mechanistic implications of PHOX2B mutants. Hum Mutat 30: 655-660.
63. Xu X, Peng M, Fang Z. 2000. The direction of microsatellite mutations is dependent upon allele length. Nat Genet 24: 396-399. (Pubitemid 30187440)