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Region-Specific Genetic Marker in C57BL/6 Mice Using Genomic Representational Difference Analysis (X-Y Chromosome) IVETA D

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Region-Specific Genetic Marker in C57BL/6 Mice Using Genomic Representational Difference Analysis (X-Y Chromosome) IVETA D Proc. Natl. Acad. Sci. USA Vol. 92, pp. 12352-12356, December 1995 Genetics Isolation and characterization of a pseudoautosomal region-specific genetic marker in C57BL/6 mice using genomic representational difference analysis (X-Y chromosome) IVETA D. KALCHEVA*, YOICHI MATSUDAt, CHRISTOPH PLASS*, AND VERNE M. CHAPMAN** *Department of Molecular and Cellular Biology, Roswell Park Cancer Institute, Elm and Carlton Streets, Buffalo, NY 14263; and tNational Institute of Radiological Sciences, 9-1, Anagawa-4-chome Inage-ku, Chiba-shi 263, Japan Communicated by Stanley M. Gartler, University of Washington, Seattle, WA, August 14, 1995 (received for review April 11, 1995) ABSTRACT Representational difference analysis was recombination in male meiosis, this region provides an ideal used to identify strain-specific differences in the pseudoau- opportunity to study chromosome pairing, crossing-over, and tosomal region (PAR) of mouse X and Y chromosomes. One interference in a higher eukaryotic chromosome. second generation (C57BL/6 x Mus spretus) x Mus spretus In addition to these central issues in genetics and meiosis, an interspecific backcross male carrying the C57BL/6 (B6) PAR understanding of the physical structure of the PAR in mam- was used for tester DNA. DNA from five backcross males from mals is essential for understanding the molecular basis for the the same generation that were M. spretus-type for the PAR was failure of X and Y chromosome pairing that has been docu- pooled for the driver. A cloned probe designated B6-38 was mented in sterile, interspecific hybrid males (6-8). The failure recovered that is B6-specific in Southern analysis. Analysis of to pair is primarily a feature of the X and Y chromosomes in genomic DNA from several inbred strains of laboratory mice the laboratory mouse x Mus spretus hybrids in these studies, and diverse Mus species and subspecies identified a charac- but an elevated level of autosomal dissociation is also observed teristic Pst I pattern of fragment sizes that is present only in (6, 7). However, the subsequent development of C57BL-M. the C57BL family of strains. Hybridization was observed with spretus congenic mice for the PAR has shown that the X-Y in and to a limited extent with Mus dissociation and male sterility remain after 12 backcross sequences DBA/2J generations while the rest of the genotype is functionally musculus (PWK strain) and Mus castaneus DNA. No hybrid- C57BL and shows little autosomal dissociation (Y.M. and ization was observed in DNA of different Mus species, M. V.M.C., unpublished results). The occurrence of male sterility spretus, M. hortulanus, and M. caroli. Genetic analyses of B6-38 associated with a failure of X and Y chromosomes to pair was conducted using C57BL congenic males that carry M. during meiotic prophase provides a consistent mechanism that spretus alleles for distal X chromosome loci and the PAR and accounts for Haldane's rule: "When in the F1 offspring of two outcrosses of heterozygous congenic females with M. spretus. different animal races one sex is absent, rare, or sterile, that sex These analyses demonstrated that the B6-38 sequences were is the heterozygous sex" (9). inherited with both the X and Y chromosome. B6-38 sequences The X chromosome is highly conserved among eutherian were genetically mapped as a locus within the PAR using two mammals. However, there is little or no conservation of the interspecific backcrosses. The locus defined by B6-38 is des- genes that map within the PAR. For example, the CSF2RA ignated DXYRpl. Preliminary analyses of recombination be- locus of the human PAR maps to the distal end of chromosome tween the distal X chromosome gene amelogenin (Amg) and 19 in the mouse and to additional chromosomes in M. spretus the PAR loci for either TelXY or sex chromosome association (10). In addition, none of the other characterized human PAR (Sxa) suggest that the locus DXYRpl maps to the distal portion genes is localized to the mouse PAR. Similarly, the steroid of the PAR. sulfatase (Sts) gene in the mouse maps to the PAR, whereas in humans it maps to distal Xp outside of the PAR (11, 12). The mouse X and Y chromosomes pair and recombine during This suggests that there is a divergence between the PAR of meiosis in a short region of the distal telomeric ends of each mouse and human and it is necessary to characterize the of the chromosomes. This region has been termed the pseudo- physical and genetic makeup of the PAR of each mammalian autosomal region (PAR) because of the autosomal-like mode species as a unique entity. At present, there are relatively few of segregation and inheritance of the loci from this part of the loci that have been defined and mapped in the PAR of the genome The PAR has been mapped and char- laboratory mouse and its interbreeding species. These include (1). physically May15 (3, 13, 14) and a telomere-related fragment identified acterized in the human genome, and several studies have in the C57BL strains (15). We have used the genomic repre- demonstrated that the region is -2.7 Mb and contains a sentational difference analysis (RDA) to recover C57BL- limited number of genes that are expressed on both the X and specific sequences from the PAR against the M. spretus Y chromosome and that typically escape X chromosome genomic background (16). This paper demonstrates that the inactivation in females (2). Genetic analysis of the PAR in both cloned probe for one of these sequences identifies species mice and humans indicates that there is an obligate crossing- variation that is inherited as a locus on both the X and the Y over that occurs in this region in males such that the estimated chromosomes, and preliminary results indicate where it is genetic distance is 50 centimorgans (3-5). By contrast, the localized in the female genetic map. relative frequency of recombination within the PAR during female meiosis is similar to other regions on the X chromo- some (3). As a consequence, the relative genetic maps of PAR MATERIALS AND METHODS are about 7- to 10-fold greater in male meiosis as compared Mouse Strains and Genetic Crosses. The inbred mouse with female meiosis. Given the relatively high frequency of strains C57BL/6Ros (B6), C57BL/1OJ (BlO), and DBA/2J The publication costs of this article were defrayed in part by page charge Abbreviations: PAR, pseudoautosomal region; RDA, representa- payment. This article must therefore be hereby marked "advertisement" in tional difference analysis. accordance with 18 U.S.C. §1734 solely to indicate this fact. 4To whom reprint requests should be addressed. Downloaded by guest on September 30, 2021 12352 Genetics: Kalcheva et al. Proc. Natl. Acad. Sci. USA 92 (1995) 12353 (D2), which are representative of Mus domesticus, and PWK/ RESULTS Ros, which is representative of Mus musculus, were used. In Isolation of a C57BL/6-Specific Genetic Marker by Using addition, individuals from outbred colonies of M. spretus, Mus the RDA Method. Genomic DNA from a single second gen- castaneus, Mus hortulanus, Mus macedonicus, and Mus caroli eration BSS male that carried the C57BL/6 PAR (AmgB-SxaB) maintained at Roswell Park Cancer Institute were used in on its X chromosome and the M. spretus PAR on its Y these studies. A congenic C57BL strain (BSB) was produced chromosome was used as the RDA tester. DNA from five that carries the distal end of the M. spretus X chromosome and sibling males from the same backcross generation that carried the PAR on a C57BL background. The BSB strain was the M. spretus PAR on their X chromosomes and the M. spretus produced by selecting backcross females that were heterozy- PAR on the Y chromosome was pooled for the RDA driver. gous for the distal X gene amelogenin (Amg) and the distal The SxaB phenotype is characterized by a small testis weight telomere locus TelXY The selected females were mated with and a high frequency of X-Y dissociation that results from the either B6 or B10 in alternate generations using substrain allelic heterozygous combination of B6 X and M. spretus Y chromo- differences in TeiXY that distinguish the C57BL X chromo- somes (6). All of the males used for driver DNA wereAmgs and some PAR from the M. spretus X chromosome PAR. Congenic expressed the Sxas phenotype (all of these males had normal BSB females (generation N10-11) heterozygous for AmgB/S or large testis weight and low frequencies of X-Y dissociation). and TelXY B/S were mated with M. spretus to produce BSB x Three rounds of RDA subtraction and PCR amplification of S male progeny that were used to localize the B6-38 sequences the adaptor-ligated tester sequences were performed. The to the PAR of C57BL. The interspecific backcrosses from resulting PCR products were analyzed on agarose gels after Roswell Park Cancer Institute (BSS-RP; n = 59) (6) and from each round of RDA. After the third round of RDA, several The Jackson Laboratory (BSS-JAX) (17) used in this study distinctive bands from the subtracted tester DNA appeared on were produced by mating (B6 x M spretus) x M. spretus. a background smear upon ethidium bromide staining of the Probes. TeIXY probe was an oligonucleotide (TTATTG)5 agarose gel (data not shown). This DNA, ranging from 150 to containing the mammalian telomere consensus sequence (15). 400 bp, was digested with BamHI, gel purified, and cloned into Amg was characterized using the 170-bp Nco I-Xba I subfrag- the BamHI site of pBluescript II KS(+). The inserts from 15 ment excised from pMal6 (pMal6 is a pGEM-1 clone con- clones were independently used as hybridization probes on taining a 753-bp Pst I-Xba I fragment from the mouse Amg Southern blots containing C57BL/6 and M.
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