Every microsatellite is different: Intrinsic DNA features dictate mutagenesis of common microsatellites present in the human genome

Molecular Carcinogenesis

Volumn 48, Issue 4, 2009, Pages 379-388

  Eckert, Kristin A ^a   Hile, Suzanne E ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

DNA polymerase fidelity; Indel mutations; Interruptions; Microsatellite instability; Slipped strand mispairing

Indexed keywords

DINUCLEOTIDE MICROSATELLITE; DNA POLYMERASE; MICROSATELLITE DNA; MONONUCLEOTIDE MICROSATELLITE; TETRANUCLEOTIDE MICROSATELLITE; UNCLASSIFIED DRUG; DNA;

ALLELE; DNA BINDING MOTIF; DNA REPLICATION; DNA SEQUENCE; DNA STRAND; DNA STRUCTURE; DNA SYNTHESIS; EXPERIMENTAL MODEL; GENE FREQUENCY; GENE LOCUS; GENETIC STABILITY; GENETIC VARIABILITY; GENOME; HUMAN; INDEL MUTATION; MISMATCH REPAIR; MUTAGENESIS; MUTATION RATE; NUCLEIC ACID BASE SUBSTITUTION; PEDIGREE ANALYSIS; PRIORITY JOURNAL; REVIEW; GENETICS; HUMAN GENOME; MUTATION;

DNA; GENOME, HUMAN; HUMANS; MICROSATELLITE REPEATS; MUTAGENESIS; MUTATION;

EID: 65249153186     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20499     Document Type: Review

References (57)

1. Subramanian S, Mishra RK, Singh L. Genome-wide analysis of microsatellite repeats in humans: Their abundance and density in specific genomic regions. Genome Biol 2003;4: R13.
2. Li YC, Korol AB, Fahima T, Beiles A, Nevo E. Microsatellites: Genomic distribution, putative functions and mutational mechanisms: A review. Mol Ecol 2002;11: 2453-2465.
3. Katti MV, Ranjekar PK, Gupta VS. Differential distribution of simple sequence repeats in eukaryotic genome sequences. Mol Biol Evol 2001;18: 1161-1167.
4. Metzgar D, Bytof J, Wills C. Selection against frameshift mutations limits microsatellite expansion in coding DNA. Genome Res 2000;10: 72-80.
5. Bacolla A, Larson JE, Collins JR, et al. Abundance and length of simple repeats in vertebrate genomes are determined by their structural properties. Genome Res 2008;18: 1545-1553.
6. Chambers GK, MacAvoy ES. Microsatellites: Consensus and controversy. Comp Biochem Physiol B Biochem Mol Biol 2000;126: 455-476.
7. Waterson RH, Consortium MGS. Initial sequencing and comparative analysis of the mouse genome. Nature 2002; 420: 520-562.
8. Li YC, Korol AB, Fahima T, Nevo E. Microsatellites within genes: Structure, function, and evolution. Mol Biol Evol 2004;21: 991-1007.
9. Hui J, Hung LH, Heiner M, et al. Intronic CA-repeat and CA- rich elements: A new class of regulators of mammalian alternative splicing. EMBO J 2005; 24:1988-1998.
10. Rockman MV, Wray GA. Abundant raw material for cis- regulatory evolution in humans. Mol Biol Evol 2002; 19:1991 -2004.
11. Kashi Y, King DG. Simple sequence repeats as advantageous mutators in evolution. Trends Genet 2006;22: 253-259.
12. Chu CS, Trapnell BC, Curristin S, Cutting GR, Crystal RG. Genetic basis of variable exon 9 skipping in cystic fibrosis transmembrane conductance regulator mRNA. Nat Genet 1993;3: 151-156.
13. Cuppens H, Lin W, Jaspers M, et al. Polyvariant mutant cystic fibrosis transmembrane conductance regulator genes. The polymorphic (Tg)m locus explains the partial penetrance of the T5 polymorphism as a disease mutation. J Clin Invest 1998;101: 487-496.
14. Gebhardt F, Zanker KS, Brandt B. Modulation of epidermal growth factor receptor gene transcription by a polymorphic dinucleotide repeat in intron 1. J Biol Chem 1999;274: 13176-13180.
15. Buerger H, Packeisen J, Boecker A, et al. Allelic length of a CA dinucleotide repeat in the egfr gene correlates with the frequency of amplifications of this sequence-first results of an inter-ethnic breast cancer study. J Pathol 2004;203: 545-550.
16. Gangwal K, Sankar S, Hollenhorst PC, et al. Microsatellites as EWS/FLI response elements in Ewing's sarcoma. Proc Natl Acad Sci USA 2008;105: 10149-10154.
17. NikitinaTV, Nazarenko SA. Human microsatellites: Mutation and evolution. Russ J Genet 2004;40: 1064-1079.
18. Ellegren H. Microsatellites: Simple sequences with complex evolution. Nat Rev Genet 2004;5: 435-445.
19. Albertini RJ, NicklasJA, O'Neill JP, Robison SH. In vivo somatic mutations in humans: Measurement and analysis. Annu Rev Genet 1990;24: 305-326.
20. Brinkmann B, Klintschar M, Neuhuber F, Huhne J, Rolf B. Mutation rate in human microsatellites: Influence of the structure and length of the tandem repeat. Am J Hum Genet 1998;62: 1408-1415.
21. Dupuy BM, Stenersen M, Egeland T, Olaisen B. Y-chromo- somal microsatellite mutation rates: Differences in mutation rate between and within loci. Hum Mutat 2004;23: 117-124.
22. Kayser M, Roewer L, Hedman M, et al. Characteristics and frequency of germline mutations at microsatellite loci from the human Y chromosome, as revealed by direct observation in father/son pairs. Am J Hum Genet 2000;66: 1580-1588.
23. Lai Y, Sun F. The relationship between microsatellite slippage mutation rate and the number of repeat units. Mol Biol Evol 2003;20: 2123-2131.
24. Kelkar YD, Tyekucheva S, Chiaromonte F, Makova KD. The genome-wide determinants of human and chimpanzee microsatellite evolution. Genome Res 2008;18: 30-38.
25. Webster MT, Smith NG, Ellegren H. Microsatellite evolution inferred from human-chimpanzee genomic sequence alignments. Proc Natl Acad Sci USA 2002;99: 8748-8753.
26. Ellegren H. Heterogeneous mutation processes in human microsatellite DNA sequences. Nat Genet 2000;24: 400-402.
27. Xu X, Peng M, Fang Z, Xu X. The direction of microsatellite mutations is dependent upon allele length. Nat Genet 2000;24: 396-399.
28. Buschiazzo E, Gemmell NJ. The rise, fall and renaissance of microsatellites in eukaryotic genomes. Bioessays 2006;28: 1040-1050.
29. Kruglyak S, Durrett RT, Schug MD, Aquadro CF. Equilibrium distributions of microsatellite repeat length resulting from a balance between slippage events and point mutations. Proc Natl Acad Sci USA 1998;95: 10774-10778.
30. Jacob KD, Eckert KA. Escherichia coli DNA polymerase IV contributes to spontaneous mutagenesis at coding sequences but not microsatellite alleles. Mutat Res 2007;619: 93-103.
31. Sia EA, Kokoska RJ, Dominska M, Greenwell P, Petes TD. Microsatellite instability in yeast: Dependence on repeat unit size and mismatch repair genes. Mol Cell Biol 1997;17: 2851-2858.
32. Wierdl M, Dominska M, PetesTD. Microsatellite instability in yeast: Dependence on the length of the microsatellite. Genetics 1997;146: 769-779.
33. Petes TD, Greenwell PW, Dominska M. Stabilization of microsatellite sequences by variant repeats in the yeast Saccharomyces cerevisiae. Genetics 1997;146: 491-498.
34. Hawk JD, Stefanovic L, Boyer JC, Petes TD, Farber RA. Variation in efficiency of DNA mismatch repair at different sites in the yeast genome. Proc Natl Acad Sci USA 2005;102: 8639-8643.
35. Roques CN, Boyer JC, Farber RA. Microsatellite mutation rates are equivalent in normal and telomerase-immortalized human fibroblasts. Cancer Res 2001;61: 8405-8407.
36. Eckert KA, Yan G, Hile SE. Mutation rate and specificity analysis of tetranucleotide microsatellite DNA alleles in somatic human cells. Mol Carcinog 2002;34: 140-150.
37. Hile SE, Yan G, Eckert KA. Somatic mutation rates and specificities at TC/AG and GT/CA microsatellite sequences in nontumorigenic human lymphoblastoid cells. Cancer Res 2000;60: 1698-1703.
38. Eckert KA, Mowery A, Hile SE. Misalignment-mediated DNA polymerase beta mutations: Comparison of microsatellite and frame-shift error rates using a forward mutation assay. Biochemistry 2002;41: 10490-10498.
39. Hile SE, Eckert KA. Positive correlation between DNA polymerase alpha-primase pausing and mutagenesis within polypyrimidine/polypurine microsatellite sequences. J Mol Biol 2004;335: 745-759.
40. Hile SE, Eckert KA. DNA polymerase kappa produces interrupted mutations and displays polar pausing within mononucleotide microsatellite sequences. Nucleic Acids Res 2008;36: 688-696.
41. Sugden B. In the beginning: A viral origin exploits the cell. Trends Biochem Sci 2002;27: 1-3.
42. Levinson G, Gutman G. High frequencies of short frameshifts in poly-CA/TG tandem repeats borne by bacteriophage M13 in Escherichia coli K12. Nucleic Acids Res 1987;15: 5323-5338.
43. Weirdl M, Dominska M, PetesTD. Microsatellite instability in yeast: Dependence on the length of the microsatellite. Genetics 1997;146: 769-779.
44. Eckert KA, Yan G. Mutational analyses of dinucleotide and tetranucleotide microsatellites in Escherichia coli: Influence of sequence on expansion mutagenesis. Nucleic Acids Res 2000;28: 2831-2838.
45. Levinson G, Gutman GA. Slipped strand mispairing: A major mechanism for DNA sequence evolution. Mol Biol Evol 1987;4: 203-221.
46. Strand M, Prolla TA, Liskay RM, Petes TD. Destabilization of tracts of simple repetitve DNA in yeast by mutations affecting DNA mismatch repair. Nature (Lond) 1993;365: 274-276.
47. Narayanan L, Fritzell JA, Baker SM, Liskay RM, Glazer PM. Elevated levels of mutation in multiple tissues of mice deficient in the DNA mismatch repair gene PMS2. Proc Natl Acad Sci USA 1997;94: 3122-3127.
48. Vilkki S, Tsao JL, Loukola A, et al. Extensive somatic microsatellite mutations in normal human tissue. Cancer Res 2001;61: 4541-4544.
49. Gragg H, Harfe BD, 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.
50. Tran HT, Keen JD, Kricker M, Resnick MA, Gordenin DA. Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants. Mol Cell Biol 1997;17: 2859-2865.
51. Kunkel TA, Bebenek K. DNA replication fidelity. Annu Rev Biochem 2000;69: 497-529.
52. Sweasy JB, Lauper JM, Eckert KA. DNA polymerases and human diseases. Radiat Res 2006;166: 693-714.
53. Ripley LS. Frameshift mutation: Determinants of specificity. Ann Rev Genet 1990;24: 189-213.
54. Joshua-Tor L, Frolow F, Appella E, Hope H, Rabinovich D, Sussman JL. Three-dimensional structures of bulge-containing DNA fragments. J Mol Biol 1992;225: 397-431.
55. Wang G, Vasquez KM. Non-B DNA structure-induced genetic instability. Mutat Res 2006;598: 103-119.
56. Wells RD. Non-B DNA conformations, mutagenesis and disease. Trends Biochem Sci 2007;32: 271-278.
57. Raghuraman MK, Winzeler EA, Collingwood D, et al. Replication dynamics of the yeast genome. Science 2001; 294: 115-121.