Beyond junk-variable tandem repeats as facilitators of rapid evolution of regulatory and coding sequences

Genes

Volumn 3, Issue 3, 2012, Pages 461-480

  Gemayel, Rita ^a,b   Cho, Janice ^a,b   Boeynaems, Steven ^a,b   Verstrepen, Kevin J ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Evolvability; Microsatellites; Phenotype; Polyglutamine; Repeats

Indexed keywords

CELL SURFACE PROTEIN; MESSENGER RNA; POLYGLUTAMINE; RNA BINDING PROTEIN; SPACER DNA; TRANSCRIPTION FACTOR;

ADAPTATION; AMINO ACID SEQUENCE; BINDING SITE; CELL SURFACE; CHROMATIN STRUCTURE; CIRCADIAN RHYTHM; DEGENERATIVE DISEASE; DNA STRUCTURE; EUKARYOTE; FLY; GENE EXPRESSION; GENE SWITCHING; GENETIC POLYMORPHISM; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENOME ANALYSIS; GENOMIC INSTABILITY; HUMAN; INTRON; MAMMAL; MOLECULAR CLOCK; MOLECULAR EVOLUTION; MORPHOLOGICAL TRAIT; MUTATION RATE; NONHUMAN; NUCLEOSOME; PHENOTYPIC VARIATION; PROMOTER REGION; PROTEIN ASSEMBLY; PROTEIN INTERACTION; REGULATORY SEQUENCE; REVIEW; RNA SPLICING; TANDEM REPEAT; TRINUCLEOTIDE REPEAT; UNTRANSLATED REGION;

EID: 84865067382     PISSN: None     EISSN: 20734425     Source Type: Journal    
DOI: 10.3390/genes3030461     Document Type: Review

References (78)

1. Hartl, D.L. Molecular melodies in high and low C. Nat. Rev. Genet. 2000, 1, 145-149.
2. van Belkum, A.; Scherer, S.; van Alphen, L.; Verbrugh, H. Short-sequence DNA repeats in prokaryotic genomes. Microbiol. Mol. Biol. Rev. 1998, 62, 275-293.
3. Feschotte, C.; Keswani, U.; Ranganathan, N.; Guibotsy, M.L.; Levine, D. Exploring repetitive DNA landscapes using REPCLASS, a tool that automates the classification of transposable elements in eukaryotic genomes. Genome Biol. Evol. 2009, 1, 205-220.
4. Kit, S. Equilibrium sedimentation in density gradients of DNA preparations from animal tissues. J. Mol. Biol. 1961, 3, 711-716.
5. Verstrepen, K.J.; Jansen, A.; Lewitter, F.; Fink, G.R. Intragenic tandem repeats generate functional variability. Nat. Genet. 2005, 37, 986-990.
6. Paques, F.; Leung, W.Y.; Haber, J.E. Expansions and contractions in a tandem repeat induced by double-strand break repair. Mol. Cell. Biol. 1998, 18, 2045-2054.
7. Kokoska, R.J.; Stefanovic, L.; Tran, H.T.; Resnick, M.A.; Gordenin, D.A.; Petes, T.D. Destabilization of yeast micro-and minisatellite DNA sequences by mutations affecting a nuclease involved in Okazaki fragment processing (rad27) and DNA polymerase delta (pol3-t). Mol. Cell. Biol. 1998, 18, 2779-2788.
8. Richard, G.F.; Paques, F. Mini-and microsatellite expansions: The recombination connection. EMBO Rep. 2000, 1, 122-126.
9. Legendre, M.; Pochet, N.; Pak, T.; Verstrepen, K.J. Sequence-based estimation of minisatellite and microsatellite repeat variability. Genome Res. 2007, 17, 1787-1796.
10. Petes, T.D.; Greenwell, P.W.; Dominska, M. Stabilization of microsatellite sequences by variant repeats in the yeast Saccharomyces cerevisiae. Genetics 1997, 146, 491-498.
11. Gragg, H.; Harfe, B.D.; Jinks-Robertson, S. Base composition of mononucleotide runs affects DNA polymerase slippage and removal of frameshift intermediates by mismatch repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 2002, 22, 8756-8762.
12. Wierdl, M.; Greene, C.N.; Datta, A.; Jinks-Robertson, S.; Petes, T.D. Destabilization of simple repetitive DNA sequences by transcription in yeast. Genetics 1996, 143, 713-721.
13. Schmidt, A.L.; Mitter, V. Microsatellite mutation directed by an external stimulus. Mutat. Res. Fundam. Mol. Mech. Mutagen. 2004, 568, 233-243.
14. Rosenberg, S.M. Evolving responsively: Adaptive mutation. Nat. Rev. Genet. 2001, 2, 504-515.
15. Mittelman, D.; Sykoudis, K.; Hersh, M.; Lin, Y.; Wilson, J.H. Hsp90 modulates CAG repeat instability in human cells. Cell Stress Chaperones 2010, 15, 753-759.
16. Merkel, A.; Gemmell, N. Detecting short tandem repeats from genome data: Opening the software black box. Brief Bioinform. 2008, 9, 355-366.
17. Gemayel, R.; Vinces, M.D.; Legendre, M.; Verstrepen, K.J. Variable Tandem Repeats Accelerate Evolution of Coding and Regulatory Sequences. Annu. Rev. Genet. 2010, 44, 445-477.
18. Jansen, A.; Gemayel, R.; Verstrepen, K.J. Unstable microsatellite repeats facilitate rapid evolution of coding and regulatory sequences. Genome Dyn. 2012, 7, 108-125.
19. Young, E.T.; Sloan, J.S.; van Riper, K. Trinucleotide repeats are clustered in regulatory genes in Saccharomyces cerevisiae. Genetics 2000, 154, 1053-1068.
20. Metzgar, D.; Bytof, J.; Wills, C. Selection against frameshift mutations limits microsatellite expansion in coding DNA. Genome Res. 2000, 10, 72-80.
21. O'Dushlaine, C.T.; Edwards, R.J.; Park, S.D.; Shields, D.C. Tandem repeat copy-number variation in protein-coding regions of human genes. Genome Biol. 2005, 6, 12.
22. Mularoni, L.; Ledda, A.; Toll-Riera, M.; Alba, M.M. Natural selection drives the accumulation of amino acid tandem repeats in human proteins. Genome Res. 2010, 20, 745-754.
23. Legendre, M.; Verstrepen, K.J. Harvard University: Cambridge, MA, USA. Unpublished work, 2007.
24. Faux, N.G.; Bottomley, S.P.; Lesk, A.M.; Irving, J.A.; Morrison, J.R.; de la Banda, M.C.; Whisstock, J.C. Functional insights from the distribution and role of homopeptide repeat-containing proteins. Genome Res. 2005, 15, 537-551.
25. Doolittle, W.F.; Sapienza, C. Selfish genes, the phenotype paradigm and genome evolution. Nature 1980, 284, 601-603.
26. Ohno, S. So much "junk" DNA in our genome. Brookhaven Symp. Biol. 1972, 23, 366-370.
27. Orgel, L.E.; Crick, F.H. Selfish DNA: the ultimate parasite. Nature 1980, 284, 604-607.
28. King, M.C.; Wilson, A.C. Evolution at two levels in humans and chimpanzees. Science 1975, 188, 107-116.
29. Wray, G.A. The evolutionary significance of cis-regulatory mutations. Nat. Rev. Genet. 2007, 8, 206-216.
30. Rockman, M.V.; Wray, G.A. Abundant raw material for cis-regulatory evolution in humans. Mol. Biol. Evol. 2002, 19, 1991-2004.
31. Vinces, M.D.; Legendre, M.; Caldara, M.; Hagihara, M.; Verstrepen, K.J. Unstable tandem repeats in promoters confer transcriptional evolvability. Science 2009, 324, 1213-1216.
32. Martin, P.; Makepeace, K.; Hill, S.A.; Hood, D.W.; Moxon, E.R. Microsatellite instability regulates transcription factor binding and gene expression. Proc. Natl. Acad. Sci. USA 2005, 102, 3800-3804.
33. Johnson, A.C.; Jinno, Y.; Merlino, G.T. Modulation of epidermal growth factor receptor proto-oncogene transcription by a promoter site sensitive to S1 nuclease. Mol. Cell. Biol. 1988, 8, 4174-4184.
34. Whetstine, J.R.; Witt, T.L.; Matherly, L.H. The human reduced folate carrier gene is regulated by the AP2 and Sp1 transcription factor families and a functional 61-base pair polymorphism. J. Biol. Chem. 2002, 277, 43873-43880.
35. Iglesias, A.R.; Kindlund, E.; Tammi, M.; Wadelius, C. Some microsatellites may act as novel polymorphic cis-regulatory elements through transcription factor binding. Gene 2004, 341, 149-165.
36. Metruccio, M.M.E.; Pigozzi, E.; Roncarati, D.; Scorza, F.B.; Norais, N.; Hill, S.A.; Scarlato, V.; Delany, I. A Novel Phase Variation Mechanism in the Meningococcus Driven by a Ligand-Responsive Repressor and Differential Spacing of Distal Promoter Elements. PLoS Pathog. 2009, 5, e1000710.
37. van der Ende, A.; Hopman, C.T.; Zaat, S.; Essink, B.B.; Berkhout, B.; Dankert, J. Variable expression of class 1 outer membrane protein in Neisseria meningitidis is caused by variation in the spacing between the-10 and-35 regions of the promoter. J. Bacteriol. 1995, 177, 2475-2480.
38. van Ham, S.M.; van Alphen, L.; Mooi, F.R.; van Putten, J.P. Phase variation of H. influenzae fimbriae: Transcriptional control of two divergent genes through a variable combined promoter region. Cell 1993, 73, 1187-1196.
39. Willems, R.; Paul, A.; van der Heide, H.G.; ter Avest, A.R.; Mooi, F.R. Fimbrial phase variation in Bordetella pertussis: A novel mechanism for transcriptional regulation. EMBO J. 1990, 9, 2803-2809.
40. Yogev, D.; Rosengarten, R.; Watson-McKown, R.; Wise, K.S. Molecular basis of Mycoplasma surface antigenic variation: A novel set of divergent genes undergo spontaneous mutation of periodic coding regions and 5' regulatory sequences. EMBO J. 1991, 10, 4069-4079.
41. Saunders, N.J.; Jeffries, A.C.; Peden, P.F.; Hood, D.W.; Tettelin, H.; Rappuoli, R.; Moxon, E.R. Repeat-associated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol. Microbiol. 2000, 37, 207-215.
42. Iyer, V.; Struhl, K. Poly(dA:dT), a ubiquitous promoter element that stimulates transcription via its intrinsic DNA structure. EMBO J. 1995, 14, 2570-2579.
43. Kaplan, N.; Moore, I.K.; Fondufe-Mittendorf, Y.; Gossett, A.J.; Tillo, D.; Field, Y.; LeProust, E.M.; Hughes, T.R.; Lieb, J.D.; Widom, J.; et al. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 2009, 458, 362-366.
44. Yuan, G.C.; Liu, Y.J.; Dion, M.F.; Slack, M.D.; Wu, L.F.; Altschuler, S.J.; Rando, O.J. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 2005, 309, 626-630.
45. Naylor, L.H.; Clark, E.M. d(TG)n. d(CA)n sequences upstream of the rat prolactin gene form Z-DNA and inhibit gene transcription. Nucleic Acids Res. 1990, 18, 1595-1601.
46. Oh, D.B.; Kim, Y.G.; Rich, A. Z-DNA-binding proteins can act as potent effectors of gene expression in vivo. Proc. Natl. Acad. Sci. USA 2002, 99, 16666-16671.
47. Gatchel, J.R.; Zoghbi, H.Y. Diseases of unstable repeat expansion: Mechanisms and common principles. Nat. Rev. Genet. 2005, 6, 743-755.
48. Shang, E.; Cui, Q.; Wang, X.; Beseler, C.; Greenberg, D.A.; Wolgemuth, D.J. The Bromodomain-Containing Gene BRD2 Is Regulated at Transcription, Splicing, and Translation Levels. J. Cell. Biochem. 2011, 112, 2784-2793.
49. Pagani, F.; Buratti, E.; Stuani, C.; Romano, M.; Zuccato, E.; Niksic, M.; Giglio, L.; Faraguna, D.; Baralle, F.E. Splicing factors induce cystic fibrosis transmembrane regulator exon 9 skipping through a nonevolutionary conserved intronic element. J. Biol. Chem. 2000, 275, 21041-21047.
50. Rockman, M.V.; Hahn, M.W.; Soranzo, N.; Loisel, D.A.; Goldstein, D.B.; Wray, G.A. Positive selection on MMP3 regulation has shaped heart disease risk. Curr. Biol. 2004, 14, 1531-1539.
51. Fidalgo, M.; Barrales, R.R.; Ibeas, J.I.; Jimenez, J. Adaptive evolution by mutations in the FLO11 gene. Proc. Natl. Acad. Sci. USA 2006, 103, 11228-11233.
52. Hoyer, L.L. The ALS gene family of Candida albicans. Trends Microbiol. 2001, 9, 176-180.
53. Verstrepen, K.J.; Reynolds, T.B.; Fink, G.R. Origins of variation in the fungal cell surface. Nat. Rev. Microbiol. 2004, 2, 533-540.
54. Kita, E.; Katsui, N.; Emoto, M.; Sawaki, M.; Oku, D.; Nishikawa, F.; Hamuro, A.; Kashiba, S. Virulence of transparent and opaque colony types of Neisseria gonorrhoeae for the genital tract of mice. J. Med. Microbiol. 1991, 34, 355-362.
55. Stern, A.; Brown, M.; Nickel, P.; Meyer, T.F. Opacity genes in Neisseria gonorrhoeae: Control of phase and antigenic variation. Cell 1986, 47, 61-71.
56. Weiser, J.N.; Love, J.M.; Moxon, E.R. The molecular mechanism of phase variation of H. influenzae lipopolysaccharide. Cell 1989, 59, 657-665.
57. de Bolle, X.; Bayliss, C.D.; Field, D.; van de Ven, T.; Saunders, N.J.; Hood, D.W.; Moxon, E.R. The length of a tetranucleotide repeat tract in Haemophilus influenzae determines the phase variation rate of a gene with homology to type III DNA methyltransferases. Mol. Microbiol. 2000, 35, 211-222.
58. Srikhanta, Y.N.; Dowideit, S.J.; Edwards, J.L.; Falsetta, M.L.; Wu, H.J.; Harrison, O.B.; Fox, K.L.; Seib, K.L.; Maguire, T.L.; Wang, A.H.J.; et al. Phasevarions Mediate Random Switching of Gene Expression in Pathogenic Neisseria. PLoS Pathog. 2009, 5, e1000400.
59. Mrazek, J.; Guo, X.X.; Shah, A. Simple sequence repeats in prokaryotic genomes. Proc. Natl. Acad. Sci. USA 2007, 104, 8472-8477.
60. Lin, W.H.; Kussell, E. Evolutionary pressures on simple sequence repeats in prokaryotic coding regions. Nucleic Acids Res. 2012, 40, 2399-2413.
61. Orr, H.; Zoghbi, H. Trinucleotide repeat disorders. Annu. Rev. Neurosci. 2007, 30, 575-621.
62. Karlin, S.; Burge, C. Trinucleotide repeats and long homopeptides in genes and proteins associated with nervous system disease and development. Proc. Natl. Acad. Sci. USA 1996, 93, 1560-1565.
63. Froehlich, A.C.; Liu, Y.; Loros, J.J.; Dunlap, J.C. White collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 2002, 297, 815-819.
64. Michael, T.P.; Park, S.; Kim, T.S.; Booth, J.; Byer, A.; Sun, Q.; Chory, J.; Lee, K. Simple Sequence Repeats Provide a Substrate for Phenotypic Variation in the Neurospora crassa Circadian Clock. PLoS One 2007, 2, 10.
65. Johnsen, A.; Fidler, A.E.; Kuhn, S.; Carter, K.L.; Hoffmann, A.; Barr, I.R.; Biard, C.; Charmantier, A.; Eens, M.; Korsten, P.; et al. Avian Clock gene polymorphism: evidence for a latitudinal cline in allele frequencies. Mol. Ecol. 2007, 16, 4867-4880.
66. Fondon, J.W.; Garner, H.R. Molecular origins of rapid and continuous morphological evolution. Proc. Natl. Acad. Sci. USA 2004, 101, 18058-18063.
67. Sears, K.E.; Goswami, A.; Flynn, J.J.; Niswander, L.A. The correlated evolution of Runx2 tandem repeats, transcriptional activity, and facial length in Carnivora. Evol. Dev. 2007, 9, 555-565.
68. Gerber, H.P.; Seipel, K.; Georgiev, O.; Hofferer, M.; Hug, M.; Rusconi, S.; Schaffner, W. Transcriptional activation modulated by homopolymeric glutamine and proline stretches. Science 1994, 263, 808-811.
69. Friedman, M.J.; Shah, A.G.; Fang, Z.-H.; Ward, E.G.; Warren, S.T.; Li, S.; Li, X.-J. Polyglutamine domain modulates the TBP-TFIIB interaction: Implications for its normal function and neurodegeneration. Nat. Neurosci. 2007, 10, 1519-1528.
70. Jackson-Fisher, A.J.; Chitikila, C.; Mitra, M.; Pugh, B.F. A role for TBP dimerization in preventing unregulated gene expression. Mol. Cell 1999, 3, 717-727.
71. Bachtrog, D.; Weiss, S.; Zangerl, B.; Brem, G.; Schlotterer, C. Distribution of dinucleotide microsatellites in the Drosophila melanogaster genome. Mol. Biol. Evol. 1999, 16, 602-610.
72. Schroth, G.P.; Chou, P.J.; Ho, P.S. Mapping Z-DNA in the human genome. Computer-aided mapping reveals a nonrandom distribution of potential Z-DNA-forming sequences in human genes. J. Biol. Chem. 1992, 267, 11846-11855.
73. Riley, D.E.; Krieger, J.N. UTR dinucleotide simple sequence repeat evolution exhibits recurring patterns including regulatory sequence motif replacements. Gene 2009, 429, 80-86.
74. Riley, D.E.; Krieger, J.N. Embryonic nervous system genes predominate in searches for dinucleotide simple sequence repeats flanked by conserved sequences. Gene 2009, 429, 74-79.
75. Morgante, M.; Hanafey, M.; Powell, W. Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat. Genet. 2002, 30, 194-200.
76. Chen, M.; Tan, Z.; Jiang, J.; Li, M.; Chen, H.; Shen, G.; Yu, R. Similar distribution of simple sequence repeats in diverse completed Human Immunodeficiency Virus Type 1 genomes. FEBS Lett. 2009, 583, 2959-2963.
77. King, D.G.; Soller, M.; Kashi, Y. Evolutionary tuning knobs. Endeavour 1997, 21, 36-40.
78. Lo Sardo, V.; Zuccato, C.; Gaudenzi, G.; Vitali, B.; Ramos, C.; Tartari, M.; Myre, M.A.; Walker, J.A.; Pistocchi, A.; Conti, L.; et al. An evolutionary recent neuroepithelial cell adhesion function of huntingtin implicates ADAM10-Ncadherin. Nat. Neurosci. 2012, 15, 713-721.