Microsatellite Interruptions Stabilize Primate Genomes and Exist as Population-Specific Single Nucleotide Polymorphisms within Individual Human Genomes

PLoS Genetics

Volumn 10, Issue 7, 2014, Pages

  Ananda, Guruprasad ^a,c   Hile, Suzanne E ^b   Breski, Amanda ^b   Wang, Yanli ^a   Kelkar, Yogeshwar ^a,d   Makova, Kateryna D ^a   Eckert, Kristin A ^a,b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b PENN STATE CANCER INSTITUTE   (United States)

^c JACKSON LABORATORY   (United States)

^d UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE BETA; DNA DIRECTED DNA POLYMERASE ETA; DNA POLYMERASE; FAS ASSOCIATED DEATH DOMAIN PROTEIN; MELANOCORTIN 1 RECEPTOR; MELANOCORTIN 3 RECEPTOR; MELANOCORTIN 4 RECEPTOR; RHODOPSIN; SODIUM CHANNEL; SUCCINATE DEHYDROGENASE; MICROSATELLITE DNA;

AFRICAN; AIB1 GENE; AMERICAN; ARTICLE; ARX GENE; ATXN2 GENE; CBFA1 GENE; DISEASE ASSOCIATION; DNA STRAND; DNA SYNTHESIS; DRPLA GENE; EAST ASIAN; ETHNICITY; EUROPEAN; EVOLUTION; EXON; FMR1 GENE; FMR2 GENE; FOXL2 GENE; GENE EXPRESSION; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENE SEQUENCE; GENETIC VARIABILITY; HETEROZYGOSITY; HOXA13 GENE; HOXD13 GENE; HUMAN GENOME; MICROSATELLITE INSTABILITY; MUTAGENESIS; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; OPMD GENE; POPULATION GENETICS; PRIMATE; PROTEIN MOTIF; RECEPTOR BINDING; SCA1 GENE; SCA17 GENE; SCA2 GENE; SCA3 GENE; SEQUENCE ALIGNMENT; SHORT TANDEM REPEAT; SINGLE NUCLEOTIDE POLYMORPHISM; ZIC2 GENE; ALLELE; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; GENOMIC INSTABILITY; HUMAN; NUCLEOTIDE SEQUENCE; POPULATION;

ALLELES; ANIMALS; BASE SEQUENCE; GENE EXPRESSION REGULATION; GENOME, HUMAN; GENOMIC INSTABILITY; HUMANS; MICROSATELLITE REPEATS; POLYMORPHISM, SINGLE NUCLEOTIDE; POPULATION; PRIMATES;

EID: 84905457336     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004498     Document Type: Article

References (94)

1. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860-921.
2. Ellegren H, (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5: 435-445.
3. Pearson CE, Nichol Edamura K, Cleary JD, (2005) Repeat instability: mechanisms of dynamic mutations. Nat Rev Genet 6: 729-742.
4. Legendre M, Pochet N, Pak T, Verstrepen KJ, (2007) Sequence-based estimation of minisatellite and microsatellite repeat variability. Genome Res 17: 1787-1796.
5. Gemayel R, Vinces MD, Legendre M, Verstrepen KJ, (2010) Variable tandem repeats accelerate evolution of coding and regulatory sequences. Annu Rev Genet 44: 445-477.
6. Hui J, Hung LH, Heiner M, Schreiner S, Neumuller N, et al. (2005) Intronic CA-repeat and CA-rich elements: a new class of regulators of mammalian alternative splicing. EMBO J 24: 1988-1998.
7. Li YC, Korol AB, Fahima T, Nevo E, (2004) Microsatellites within genes: structure, function, and evolution. Mol Biol Evol 21: 991-1007.
8. Kashi Y, King DG, (2006) Simple sequence repeats as advantageous mutators in evolution. Trends Genet 22: 253-259.
9. Rockman MV, Wray GA, (2002) Abundant raw material for cis-regulatory evolution in humans. Mol Biol Evol 19: 1991-2004.
10. Nithianantharajah J, Hannan AJ, (2007) Dynamic mutations as digital genetic modulators of brain development, function and dysfunction. BioEssays 29: 525-535.
11. Fondon JW 3rd, Hammock EA, Hannan AJ, King DG, (2008) Simple sequence repeats: genetic modulators of brain function and behavior. Trends Neurosci 31: 328-334.
12. Hannan AJ, (2010) Tandem repeat polymorphisms: modulators of disease susceptibility and candidates for 'issing heritability'. Trends Genet 26: 59-65.
13. Matsuura T, Fang P, Pearson CE, Jayakar P, Ashizawa T, et al. (2006) Interruptions in the expanded ATTCT repeat of spinocerebellar ataxia type 10: repeat purity as a disease modifier? Am J Hum Genet 78: 125-129.
14. Matsuyama Z, Izumi Y, Kameyama M, Kawakami H, Nakamura S, (1999) The effect of CAT trinucleotide interruptions on the age at onset of spinocerebellar ataxia type 1 (SCA1). J Med Genet 36: 546-548.
15. Eichler EE, Holden JJ, Popovich BW, Reiss AL, Snow K, et al. (1994) Length of uninterrupted CGG repeats determines instability in the FMR1 gene. Nat Genet 8: 88-94.
16. Kunst CB, Warren ST, (1994) Cryptic and polar variation of the fragile X repeat could result in predisposing normal alleles. Cell 77: 853-861.
17. Braida C, Stefanatos RKA, Adam B, Mahajan N, Smeets HJM, et al. (2010) Variant CCG and GGC repeats within the CTG expansion dramatically modify mutational dynamics and likely contribute toward unusual symptoms in some myotonic dystrophy type 1 patients. Human Mol Genet 19: 1399-1412.
18. Leeflang EP, Arnheim N, (1995) A novel repeat structure at the myotonic dystrophy locus in a 37 repeat allele with unexpectedly high stability. Human MolGenet 4: 135-136.
19. Laken SJ, Petersen GM, Gruber SB, Oddoux C, Ostrer H, et al. (1997) Familial colorectal cancer in Ashkenazim due to a hypermutable tract in APC. Nat Genet 17: 79-83.
20. Yu Z, Zhu Y, Chen-Plotkin AS, Clay-Falcone D, McCluskey L, et al. (2011) PolyQ repeat expansions in ATXN2 associated with ALS are CAA interrupted repeats. PloS One 6: e17951.
21. Ramos EM, Martins S, Alonso I, Emmel VE, Saraiva-Pereira ML, et al. (2010) Common origin of pure and interrupted repeat expansions in spinocerebellar ataxia type 2 (SCA2). Am J Med Genet B Neuropsychiatr Genet 153B: 524-531.
22. Bachinski LL, Czernuszewicz T, Ramagli LS, Suominen T, Shriver MD, et al. (2009) Premutation allele pool in myotonic dystrophy type 2. Neurology 72: 490-497.
23. Buschiazzo E, Gemmell NJ, (2006) The rise, fall and renaissance of microsatellites in eukaryotic genomes. Bioessays 28: 1040-1050.
24. Kelkar YD, Strubczewski N, Hile SE, Chiaromonte F, Eckert KA, et al. (2010) What is a microsatellite: a computational and experimental definition based upon repeat mutational behavior at A/T and GT/AC repeats. Genome Biol Evol 2: 620-635.
25. Ananda G, Walsh E, Jacob KD, Krasilnikova M, Eckert KA, et al. (2013) Distinct Mutational Behaviors Differentiate Short Tandem Repeats from Microsatellites in the Human Genome. Genome Biol Evol 5: 606-620.
26. Baptiste BA, Ananda G, Strubczewski N, Lutzkanin A, Khoo SJ, et al. (2013) Mature microsatellites: mechanisms underlying dinucleotide microsatellite mutational biases in human cells. G3: Genes, Genomes, Genet (Bethesda) 3: 451-463.
27. Kelkar YD, Eckert KA, Chiaromonte F, Makova KD, (2011) A matter of life or death: how microsatellites emerge in and vanish from the human genome. Genome Res 21: 2038-2048.
28. Taylor JS, Durkin JM, Breden F, (1999) The death of a microsatellite: a phylogenetic perspective on microsatellite interruptions. Mol Biol Evol 16: 567-572.
29. Reza Shariflou M, Moran C, (2000) Conservation within artiodactyls of an AATA interrupt in the IGF-I microsatellite for 19-35 million years. Mol Biol Evol 17: 665-669.
30. Estoup A, Tailliez C, Cornuet JM, Solignac M, (1995) Size homoplasy and mutational processes of interrupted microsatellites in two bee species, Apis mellifera and Bombus terrestris (Apidae). Mol Biol Evol 12: 1074-1084.
31. Brandstrom M, Ellegren H, (2008) Genome-wide analysis of microsatellite polymorphism in chicken circumventing the ascertainment bias. Genome Res 18: 881-887.
32. Petes TD, Greenwell PW, Dominska M, (1997) Stabilization of microsatellite sequences by variant repeats in the yeast Saccharomyces cerevisiae. Genetics 146: 491-498.
33. Rolfsmeier ML, Lahue RS, (2000) Stabilizing effects of interruptions on trinucleotide repeat expansions in Saccharomyces cerevisiae. Mol Cell Biol 20: 173-180.
34. Brinkmann B, Klintschar M, Neuhuber F, Huhne J, Rolf B, (1998) Mutation rate in human microsatellites: influence of the structure and length of the tandem repeat. Am J Hum Genet 62: 1408-1415.
35. Webster MT, Smith NG, Ellegren H, (2002) Microsatellite evolution inferred from human-chimpanzee genomic sequence alignments. Proc Natl Acad Sci USA 99: 8748-8753.
36. Abecasis GR, Auton A, Brooks LD, DePristo MA, Durbin RM, et al. (2012) An integrated map of genetic variation from 1,092 human genomes. Nature 491: 56-65.
37. Marth G, Schuler G, Yeh R, Davenport R, Agarwala R, et al. (2003) Sequence variations in the public human genome data reflect a bottlenecked population history. Proc Natl Acad Sci USA 100: 376-381.
38. Lopez Castel A, Cleary JD, Pearson CE, (2010) Repeat instability as the basis for human diseases and as a potential target for therapy. Nat Rev Mol Cell Biol 11: 165-170.
39. Amiel J, Trochet D, Clement-Ziza M, Munnich A, Lyonnet S, (2004) Polyalanine expansions in human. Human Mol Genet 13 Spec No 2: R235-243.
40. Chelala C, Khan A, Lemoine NR, (2009) SNPnexus: a web database for functional annotation of newly discovered and public domain single nucleotide polymorphisms. Bioinformatics 25: 655-661.
41. Dayem Ullah AZ, Lemoine NR, Chelala C, (2012) SNPnexus: a web server for functional annotation of novel and publicly known genetic variants (2012 update). Nucl Acids Res 40: W65-70.
42. Dayem Ullah AZ, Lemoine NR, Chelala C, (2013) A practical guide for the functional annotation of genetic variations using SNPnexus. Brief Bioinform 14: 437-447.
43. Gryfe R, Di Nicola N, Lal G, Gallinger S, Redston M, (1999) Inherited colorectal polyposis and cancer risk of the APC I1307K polymorphism. Am J Hum Genet 64: 378-384.
44. Gryfe R, Di Nicola N, Gallinger S, Redston M, (1998) Somatic instability of the APC I1307K allele in colorectal neoplasia. Cancer Res 58: 4040-4043.
45. Eckert KA, Mowery A, Hile SE, (2002) Misalignment-mediated DNA polymerase beta mutations: comparison of microsatellite and frame-shift error rates using a forward mutation assay. Biochemistry 41: 10490-10498.
46. Hile SE, Wang X, Lee MY, Eckert KA, (2012) Beyond translesion synthesis: polymerase kappa fidelity as a potential determinant of microsatellite stability. Nucl Acids Res 40: 1636-1647.
47. Eckert KA, Hile SE, Vargo PL, (1997) Development and use of an in vitro HSV-tk forward mutation assay to study eukaryotic DNA polymerase processing of DNA alkyl lesions. Nucl Acids Res 25: 1450-1457.
48. Baptiste BA, Eckert KA, (2012) DNA polymerase kappa microsatellite synthesis: two distinct mechanisms of slippage-mediated errors. Environ Mol Mutagen 53: 787-796.
49. Eckert KA, Hile SE, (2009) Every microsatellite is different: Intrinsic DNA features dictate mutagenesis of common microsatellites present in the human genome. Mol Carcinog 48: 379-388.
50. Kelkar YD, Tyekucheva S, Chiaromonte F, Makova KD, (2008) The genome-wide determinants of human and chimpanzee microsatellite evolution. Genome Res 18: 30-38.
51. Bebenek K, Kunkel TA, (2004) Functions of DNA polymerases. Adv Protein Chem 69: 137-165.
52. Abdulovic AL, Hile SE, Kunkel TA, Eckert KA, (2011) The in vitro fidelity of yeast DNA polymerase delta and polymerase varepsilon holoenzymes during dinucleotide microsatellite DNA synthesis. DNA Repair (Amst) 10: 497-505.
53. Brohede J, Ellegren H, (1999) Microsatellite evolution: polarity of substitutions within repeats and neutrality of flanking sequences. Proc Biol Sci 266: 825-833.
54. Varela MA, Sanmiguel R, Gonzalez-Tizon A, Martinez-Lage A, (2008) Heterogeneous nature and distribution of interruptions in dinucleotides may indicate the existence of biased substitutions underlying microsatellite evolution. J Mol Evol 66: 575-580.
55. Bergstrom TF, Engkvist H, Erlandsson R, Josefsson A, Mack SJ, et al. (1999) Tracing the origin of HLA-DRB1 alleles by microsatellite polymorphism. Am J Hum Genet 64: 1709-1718.
56. Pearson CE, Eichler EE, Lorenzetti D, Kramer SF, Zoghbi HY, et al. (1998) Interruptions in the triplet repeats of SCA1 and FRAXA reduce the propensity and complexity of slipped strand DNA (S-DNA) formation. Biochemistry 37: 2701-2708.
57. Jarem DA, Huckaby LV, Delaney S, (2010) AGG interruptions in (CGG)(n) DNA repeat tracts modulate the structure and thermodynamics of non-B conformations in vitro. Biochemistry 49: 6826-6837.
58. Madsen BE, Villesen P, Wiuf C, (2008) Short tandem repeats in human exons: a target for disease mutations. BMC Genomics 9: 410.
59. Dai P, Wong LJ, (2003) Somatic instability of the DNA sequences encoding the polymorphic polyglutamine tract of the AIB1 gene. J Med Genet 40: 885-890.
60. Goodman FR, Mundlos S, Muragaki Y, Donnai D, Giovannucci-Uzielli ML, et al. (1997) Synpolydactyly phenotypes correlate with size of expansions in HOXD13 polyalanine tract. Proc Natl Acad Sci USA 94: 7458-7463.
61. Elden AC, Kim HJ, Hart MP, Chen-Plotkin AS, Johnson BS, et al. (2010) Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature 466: 1069-1075.
62. Sobczak K, Krzyzosiak WJ, (2004) Patterns of CAG repeat interruptions in SCA1 and SCA2 genes in relation to repeat instability. Hum Mutat 24: 236-247.
63. Choudhry S, Mukerji M, Srivastava AK, Jain S, Brahmachari SK, (2001) CAG repeat instability at SCA2 locus: anchoring CAA interruptions and linked single nucleotide polymorphisms. Human Mol Genet 10: 2437-2446.
64. Masutani C, Kusumoto R, Yamada A, Dohmae N, Yokoi M, et al. (1999) The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature 399: 700-704.
65. Lin Q, Clark AB, McCulloch SD, Yuan T, Bronson RT, et al. (2006) Increased susceptibility to UV-induced skin carcinogenesis in polymerase eta-deficient mice. Cancer Res 66: 87-94.
66. Masutani C, Kusumoto R, Iwai S, Hanaoka F, (2000) Mechanisms of accurate translesion synthesis by human DNA polymerase eta. EMBO J 19: 3100-3109.
67. Rey L, Sidorova JM, Puget N, Boudsocq F, Biard DS, et al. (2009) Human DNA polymerase eta is required for common fragile site stability during unperturbed DNA replication. Mol Cell Biol 29: 3344-3354.
68. Bergoglio V, Boyer AS, Walsh E, Naim V, Legube G, et al. (2013) DNA synthesis by Pol eta promotes fragile site stability by preventing under-replicated DNA in mitosis. J Cell Biol 201: 395-408.
69. Rogozin IB, Pavlov YI, Bebenek K, Matsuda T, Kunkel TA, (2001) Somatic mutation hotspots correlate with DNA polymerase eta error spectrum. Nat Immunol 2: 530-536.
70. Zeng X, Winter DB, Kasmer C, Kraemer KH, Lehmann AR, et al. (2001) DNA polymerase eta is an A-T mutator in somatic hypermutation of immunoglobulin variable genes. Nat Immunol 2: 537-541.
71. Masuda K, Ouchida R, Hikida M, Kurosaki T, Yokoi M, et al. (2007) DNA polymerases eta and theta function in the same genetic pathway to generate mutations at A/T during somatic hypermutation of Ig genes. J Biol Chem 282: 17387-17394.
72. Pumpernik D, Oblak B, Borstnik B, (2008) Replication slippage versus point mutation rates in short tandem repeats of the human genome. Mol Genet Genomics 279: 53-61.
73. Loire E, Higuet D, Netter P, Achaz G, (2013) Evolution of coding microsatellites in primate genomes. Genome Biol Evol 5: 283-295.
74. Harr B, Zangerl B, Schlotterer C, (2000) Removal of microsatellite interruptions by DNA replication slippage: phylogenetic evidence from Drosophila. Mol Biol Evol 17: 1001-1009.
75. Walsh E, Wang X, Lee MY, Eckert KA, (2013) Mechanism of replicative DNA polymerase delta pausing and a potential role for DNA polymerase kappa in common fragile site replication. J Mol Biol 425: 232-243.
76. Betous R, Pillaire MJ, Pierini L, van der Laan S, Recolin B, et al. (2013) DNA polymerase kappa-dependent DNA synthesis at stalled replication forks is important for CHK1 activation. EMBO J 32: 2172-2185.
77. Pena-Diaz J, Bregenhorn S, Ghodgaonkar M, Follonier C, Artola-Boran M, et al. (2012) Noncanonical mismatch repair as a source of genomic instability in human cells. Mol Cell 47: 669-680.
78. Abajian C (1994-2003) Sputnik. Available: http://espressosoftware.com/sputnik/index.html.
79. Lai Y, Sun F, (2003) The relationship between microsatellite slippage mutation rate and the number of repeat units. Mol Biol Evol 20: 2123-2131.
80. Rhead B, Karolchik D, Kuhn RM, Hinrichs AS, Zweig AS, et al. (2010) The UCSC Genome Browser database: update 2010. Nucl Acids Res 38: D613-619.
81. Karolchik D, Kuhn RM, Baertsch R, Barber GP, Clawson H, et al. (2008) The UCSC Genome Browser Database: 2008 update. Nucl Acids Res 36: D773-779.
82. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, et al. (2002) The human genome browser at UCSC. Genome Res 12: 996-1006.
83. Holsinger KE, Weir BS, (2009) Genetics in geographically structured populations: defining, estimating and interpreting F(ST). Nat Rev Genet 10: 639-650.
84. Jasjeet S, (2011) Multivariate and Propensity Score Matching Software with Automated Balance Optimization: The Matching Package for R. J Statist Software 42: 1-52.
85. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559-575.
86. Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, et al. (2010) Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol Chapter 19: Unit 19 10 11-21.
87. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, et al. (2005) Galaxy: a platform for interactive large-scale genome analysis. Genome Res 15: 1451-1455.
88. Goecks J, Nekrutenko A, Taylor J, (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11: R86.
89. Gray KA, Daugherty LC, Gordon SM, Seal RL, Wright MW, et al. (2013) Genenames.org: the HGNC resources in 2013. Nucleic Acids Res 41 (Database issue) (): D545-52.
90. Falcon S, Gentleman R, (2007) Using GOstats to test gene lists for GO term association. Bioinformatics 23: 257-258.
91. Opresko PL, Shiman R, Eckert KA, (2000) Hydrophobic interactions in the hinge domain of DNA polymerase beta are important but not sufficient for maintaining fidelity of DNA synthesis. Biochemistry 39: 11399-11407.
92. Xie B, Mazloum N, Liu L, Rahmeh A, Li H, et al. (2002) Reconstitution and characterization of the human DNA polymerase delta four-subunit holoenzyme. Biochemistry 41: 13133-13142.
93. Hile SE, Eckert KA, (2008) DNA polymerase kappa produces interrupted mutations and displays polar pausing within mononucleotide microsatellite sequences. Nucl Acids Res 36: 688-696.
94. Hile SE, Eckert KA, (2004) Positive correlation between DNA polymerase alpha-primase pausing and mutagenesis within polypyrimidine/polypurine microsatellite sequences. J Mol Biol 335: 745-759.