Molecular Analysis of Recombination in a Family with Duchenne Muscular Dystrophy and a Large Pericentric X Chromosome Inversion

Overview

Journal Am J Hum Genet

Publisher Cell Press

Specialty Genetics

Date 1996 Jun 1

PMID 8651300

Citations 8

Authors

V Shashi

W L Golden

P S Allinson

S H Blanton

C Von Kap-Herr

T E Kelly

Affiliations

Soon will be listed here.

Abstract

It has been demonstrated in animal studies that, in animals heterozygous for pericentric chromosomal inversions, loop formation is greatly reduced during meiosis. This results in absence of recombination within the inverted segment, with recombination seen only outside the inversion. A recent study in yeast has shown that telomeres, rather than centromeres, lead in chromosome movement just prior to meiosis and may be involved in promoting recombination. We studied by cytogenetic analysis and DNA polymorphisms the nature of meiotic recombination in a three-generation family with a large pericentric X chromosome inversion, inv(X)(p21.1q26), in which Duchenne muscular dystrophy (DMD) was cosegregating with the inversion. On DNA analysis there was no evidence of meiotic recombination between the inverted and normal X chromosomes in the inverted segment. Recombination was seen at the telomeric regions, Xp22 and Xq27-28. No deletion or point mutation was found on analysis of the DMD gene. On the basis of the FISH results, we believe that the X inversion is the mutation responsible for DMD in this family. Our results indicate that (1) pericentric X chromosome inversions result in reduction of recombination between the normal and inverted X chromosomes; (2) meiotic X chromosome pairing in these individuals is likely initiated at the telomeres; and (3) in this family DMD is caused by the pericentric inversion.

Citing Articles

Single variant, yet "double trouble": TSC and KBG syndrome because of a large de novo inversion.

Rodrigues Alves Barbosa V, Maroilley T, Diao C, Colvin-James L, Perrier R, Tarailo-Graovac M Life Sci Alliance. 2024; 7(4).

PMID: 38253421 PMC: 10803213. DOI: 10.26508/lsa.202302115.

Detection of pericentric inversion with breakpoint in DMD by whole genome sequencing.

Zaum A, Nanda I, Kress W, Rost S Mol Genet Genomic Med. 2022; 10(10):e2028.

PMID: 35912688 PMC: 9544221. DOI: 10.1002/mgg3.2028.

Haplotype-Based Noninvasive Prenatal Diagnosis of 21 Families With Duchenne Muscular Dystrophy: Real-World Clinical Data in China.

Kong L, Li S, Zhao Z, Feng J, Chen G, Liu L Front Genet. 2021; 12:791856.

PMID: 34970304 PMC: 8712857. DOI: 10.3389/fgene.2021.791856.

X-linked muscular dystrophy in a Labrador Retriever strain: phenotypic and molecular characterisation.

Barthelemy I, Calmels N, Weiss R, Tiret L, Vulin A, Wein N Skelet Muscle. 2020; 10(1):23.

PMID: 32767978 PMC: 7412789. DOI: 10.1186/s13395-020-00239-0.

A Girl with 10 Mb Distal Xp Deletion Arising from Maternal Pericentric Inversion: Clinical Data and Molecular Characterization.

Papoulidis I, Vetro A, Paspaliaris V, Ziegler M, Kreskowski K, Daskalakis G Curr Genomics. 2018; 19(3):240-246.

PMID: 29606911 PMC: 5850512. DOI: 10.2174/1389202918666170725102220.

References

Coyne J, Aulard S, Berry A . Lack of underdominance in a naturally occurring pericentric inversion in Drosophila melanogaster and its implications for chromosome evolution. Genetics. 1991; 129(3):791-802. PMC: 1204747. DOI: 10.1093/genetics/129.3.791. View

Chamberlain J, Gibbs R, Ranier J, Nguyen P, Caskey C . Deletion screening of the Duchenne muscular dystrophy locus via multiplex DNA amplification. Nucleic Acids Res. 1988; 16(23):11141-56. PMC: 339001. DOI: 10.1093/nar/16.23.11141. View

Huang T, Cottingham Jr R, Ledbetter D, Zoghbi H . Genetic mapping of four dinucleotide repeat loci, DXS453, DXS458, DXS454, and DXS424, on the X chromosome using multiplex polymerase chain reaction. Genomics. 1992; 13(2):375-80. DOI: 10.1016/0888-7543(92)90256-r. View

Lindberg L, Pelto K, Borgstrom G . Familial pericentric inversion (3)(p12q24). Hum Genet. 1992; 89(4):433-6. DOI: 10.1007/BF00194317. View

Reed K, Sites Jr J, Greenbaum I . Synapsis, recombination, and meiotic segregation in the mesquite lizard, Sceloporus grammicus, complex. I. Pericentric inversion heteromorphism of the F5 cytotype. Cytogenet Cell Genet. 1992; 61(1):40-5. DOI: 10.1159/000133366. View

Weissenbach J, Gyapay G, Dib C, Vignal A, Morissette J, Millasseau P . A second-generation linkage map of the human genome. Nature. 1992; 359(6398):794-801. DOI: 10.1038/359794a0. View

Hirsch B, Baldinger S . Pericentric inversion of chromosome 4 giving rise to dup(4p) and dup(4q) recombinants within a single kindred. Am J Med Genet. 1993; 45(1):5-8. DOI: 10.1002/ajmg.1320450104. View

Ashley T, Cacheiro N, Russell L, Ward D . Molecular characterization of a pericentric inversion in mouse chromosome 8 implicates telomeres as promoters of meiotic recombination. Chromosoma. 1993; 102(2):112-20. DOI: 10.1007/BF00356028. View

Coyne J, Meyers W, Crittenden A, Sniegowski P . The fertility effects of pericentric inversions in Drosophila melanogaster. Genetics. 1993; 134(2):487-96. PMC: 1205492. DOI: 10.1093/genetics/134.2.487. View

10.

Golden W, Von Kap-Herr C, Kurth B, Wright R, Flickinger C, Eddy R . Refinement of the localization of the gene for human intraacrosomal protein SP-10 (ACRV1) to the junction of bands q23-->q24 of chromosome 11 by nonisotopic in situ hybridization. Genomics. 1993; 18(2):446-9. DOI: 10.1006/geno.1993.1496. View

11.

Henke A, Fischer C, Rappold G . Genetic map of the human pseudoautosomal region reveals a high rate of recombination in female meiosis at the Xp telomere. Genomics. 1993; 18(3):478-85. DOI: 10.1016/s0888-7543(11)80003-0. View

12.

Chikashige Y, Ding D, Funabiki H, Haraguchi T, Mashiko S, Yanagida M . Telomere-led premeiotic chromosome movement in fission yeast. Science. 1994; 264(5156):270-3. DOI: 10.1126/science.8146661. View

13.

Van der Linden A, Pearson P, van de Kamp J . Cytological assessment of meiotic exchange in a human male with a pericentric inversion of chromosome No. 4. Cytogenet Cell Genet. 1975; 14(2):126-39. DOI: 10.1159/000130332. View

14.

Allderdice P, Browne N, Murphy D . Chromosome 3 duplication q21 leads to qter deletion p25 leads to pter syndrome in children of carriers of a pericentric inversion inv(3) (p25q21). Am J Hum Genet. 1975; 27(6):699-718. PMC: 1762887. View

15.

Sutherland G, GARDINER A, Carter R . Familial pericentric inversion of chromosome 19, inv(19) (p13q13) with a note on genetic counseling of pericentric inversion carriers. Clin Genet. 1976; 10(1):54-9. DOI: 10.1111/j.1399-0004.1976.tb00009.x. View

16.

Trunca C, Opitz J . Pericentric inversion of chromosome 14 and the risk of partial duplication of 14q (14q31 leads to 14qter). Am J Med Genet. 1977; 1(2):217-28. DOI: 10.1002/ajmg.1320010208. View

17.

de Perdigo A, Rumpler Y . Correlation between chromosomal breakpoint positions and synaptic behaviour in human males heterozygous for a pericentric inversion. Hum Genet. 1989; 83(3):274-6. DOI: 10.1007/BF00285171. View

18.

Disteche C, McConnell G, Grant S, Stephenson D, Chapman V, Gandy S . Comparison of the physical and recombination maps of the mouse X chromosome. Genomics. 1989; 5(2):177-84. DOI: 10.1016/0888-7543(89)90044-x. View

19.

Ashley T, Cacheiro N . Correlation between meiotic behavior and breakpoints with respect to G-bands in two X-4 mouse translocations: T(X;4)7R1 and T(X;4)8R1. Cytogenet Cell Genet. 1990; 53(4):178-84. DOI: 10.1159/000132926. View

20.

Beggs A, Koenig M, Boyce F, Kunkel L . Detection of 98% of DMD/BMD gene deletions by polymerase chain reaction. Hum Genet. 1990; 86(1):45-8. DOI: 10.1007/BF00205170. View