Abstract
Various sequences in the mammalian genomes are unstable. One class of sequence arrangement is long inverted repeats, which are known to be unstable in bacteria and yeast. While in mammals some evidence suggests that short inverted repeats (<10 bp long) may show instability, nothing is known about the stability of long inverted repeats. Here we describe two unrelated multicopy transgenes in the mouse (loci 109 and OX1-5), each of which contains a long inverted repeat that shows substantial mitotic instability. This instability also occurs in the germline so that mutant transgenes appear within pedigrees at a high frequency. The mutation processes acting at these two inverted repeats are complex and can involve insertion or deletion, and can result in stabilization of the transgene. At transgene 109 mutational events range from very small rearrangements at the centre of the inverted repeat to complete transgene deletion. In addition we show that the rates of mutation at the inverted repeat of transgene OX1-5 can vary between the male and female germlines and between inbred strains of mice, suggesting the possibility of a genetic analysis to identify loci that modulate inverted repeat instability.
MeSH Terms
Animals
Base Sequence
DNA/genetics
DNA Primers/genetics
Female
Male
Mice
Mice, Inbred BALB C
Mice, Inbred DBA
Mice, Transgenic
Molecular Sequence Data
Mutagenesis, Insertional
Mutation
Polymerase Chain Reaction
Rats
Repetitive Sequences, Nucleic Acid
Sequence Deletion
Chemicals
DNA Primers
DNA
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Collick A
Department of Genetics, University of Leicester, United Kingdom.
Drew J
Penberth J
Bois P
Luckett J
Scaerou F
Jeffreys A
Reik W
References (29)
29 references, click to expand
-
A family of moderately repetitive sequences in mouse DNA.
Nucleic Acids Res. 1980 Sep 25;8(18):4075-90
PMID: 6253908
-
Rapid and efficient cosmid cloning.
Nucleic Acids Res. 1981 Jul 10;9(13):2989-98
PMID: 6269067
-
Identification and genetic analysis of sbcC mutations in commonly used recBC sbcB strains of Escherichia coli K-12.
J Bacteriol. 1985 Nov;164(2):836-44
PMID: 3932331
-
Spontaneous deletion formation at the aprt locus of hamster cells: the presence of short sequence homologies and dyad symmetries at deletion termini.
EMBO J. 1986 Jun;5(6):1199-204
PMID: 3015589
-
Germ-line transformation of mice.
Annu Rev Genet. 1986;20:465-99
PMID: 3545063
-
Recent progress in understanding mechanisms of mammalian DNA amplification.
Cell. 1989 Jun 16;57(6):901-8
PMID: 2661014
-
Lack of somatic mutation in a kappa light chain transgene.
Eur J Immunol. 1990 Jun;20(6):1379-85
PMID: 2115000
-
Imprinting by DNA methylation: from transgenes to endogenous gene sequences.
Dev Suppl. 1990;:99-106
PMID: 2090437
-
Development of the mammalian gonad: the fate of the supporting cell lineage.
Bioessays. 1991 Apr;13(4):151-6
PMID: 1859392
-
The role of inverted duplication in the generation of gene amplification in mammalian cells.
Biochim Biophys Acta. 1991 Oct 8;1090(2):143-55
PMID: 1932107
-
DNA rearrangement causes hepatocarcinogenesis in albumin-plasminogen activator transgenic mice.
Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11523-7
PMID: 1454842
-
Genetics and molecular biology of telomeres.
Adv Genet. 1992;30:185-249
PMID: 1456111
-
Tandemly repeated transgenes of the human minisatellite MS32 (D1S8), with novel mouse gamma satellite integration.
Nucleic Acids Res. 1994 Aug 11;22(15):2976-81
PMID: 8065909
-
Cruciform DNA binding protein in HeLa cell extracts.
Biochemistry. 1994 Nov 29;33(47):14185-96
PMID: 7947830
-
Variable germline and embryonic instability of the human minisatellite MS32 (D1S8) in transgenic mice.
EMBO J. 1994 Dec 1;13(23):5745-53
PMID: 7988570
-
Processing of intermediates in recombination and DNA repair: identification of a new endonuclease that specifically cleaves Holliday junctions.
EMBO J. 1994 Dec 15;13(24):6133-42
PMID: 7813450
-
Long DNA palindromes, cruciform structures, genetic instability and secondary structure repair.
Bioessays. 1994 Dec;16(12):893-900
PMID: 7840768
-
Hotspot for deletions in the CGG repeat region of FMR1 in fragile X patients.
Hum Mol Genet. 1995 Jan;4(1):45-9
PMID: 7711733
-
Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid.
Nature. 1953 Apr 25;171(4356):737-8
PMID: 13054692
-
The SbcCD protein of Escherichia coli is related to two putative nucleases in the UvrA superfamily of nucleotide-binding proteins.
Genetica. 1992;87(2):95-100
PMID: 1490631
-
Formation of large deletions by illegitimate recombination in the HPRT gene of primary human fibroblasts.
Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1392-6
PMID: 8433997
-
Mutations in POL1 increase the mitotic instability of tandem inverted repeats in Saccharomyces cerevisiae.
Genetics. 1993 May;134(1):43-56
PMID: 8514147
-
Instability of a plasmid-borne inverted repeat in Saccharomyces cerevisiae.
Genetics. 1993 May;134(1):57-62
PMID: 8514149
-
Inverted DNA repeats: a source of eukaryotic genomic instability.
Mol Cell Biol. 1993 Sep;13(9):5315-22
PMID: 8395002
-
Resolution of Holliday junctions by RuvC resolvase: cleavage specificity and DNA distortion.
Cell. 1993 Sep 24;74(6):1021-31
PMID: 8402879
-
The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer.
Cell. 1993 Dec 3;75(5):1027-38
PMID: 8252616
-
Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer.
Cell. 1993 Dec 17;75(6):1215-25
PMID: 8261515
-
Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary non-polyposis colon cancer.
Nature. 1994 Mar 17;368(6468):258-61
PMID: 8145827
-
Complex gene conversion events in germline mutation at human minisatellites.
Nat Genet. 1994 Feb;6(2):136-45
PMID: 8162067