Meiotic pairing and gene expression disturbance in germ cells from an infertile boar with a balanced reciprocal autosome-autosome translocation

Abstract

Individuals carrying balanced constitutional reciprocal translocations generally have a normal phenotype, but often present reproductive disorders. The aim of our research was to analyze the meiotic process in an oligoasthenoteratospermic boar carrying an asymmetric reciprocal translocation involving chromosomes 1 and 14. Different multivalent structures (quadrivalent and trivalent plus univalent) were identified during chromosome pairing analysis. Some of these multivalents were characterized by the presence of unpaired autosomal segments with histone γH2AX accumulation sometimes associated with the XY body. Gene expression in spermatocytes was studied by RNA-DNA-FISH and microarray-based testis transcriptome analysis. Our results revealed a decrease in gene expression for chromosomes 1 and 14 and an up-regulated expression of X-chromosome genes for the translocated boar compared with normal individuals. We hypothesized that the observed meiotic arrest and reproductive failure in this boar might be due to silencing of crucial autosomal genes (MSUC) and disturbance of meiotic sex chromosome inactivation (MSCI). Further analysis revealed abnormal meiotic recombination (frequency and distribution) and the production of a high rate of unbalanced spermatozoa.Electronic supplementary materialThe online version of this article (doi:10.1007/s10577-016-9533-9) contains supplementary material, which is available to authorized users.

Genetic defects in human azoospermia

“…The second hypothesis relates to the silencing of crucial genes in segments close to the chromosome breakpoints (due to the frequent non-pairing of these autosomal segments) and thus asynapsis. This hypothesis has been confirmed in studies of male mice [73] and boars [74] bearing a translocation.…”

Cytogenetic screening in couples with recurrent pregnancy loss: A single-center study and review of literature

“…A likely explanation is that autosomal reciprocal translocations in male carriers may have a severe effect leading to the improper spermatogenetic function and resulting in reproductive failure (ranging from pregnancy loss to infertility). [ 11 12 ] In literature, there have been reports of reciprocal translocation carriers with varying combination of the involved chromosomes, resulting in RPL and reproductive failure. [ 4 13 ] The size of the chromosomal segment involved and the breakpoint positions have a vital role in meiosis.…”

Breeding and Economic Aspects of Cytogenetic Screening Studies of Pigs Qualified for Reproduction

“…The most prevalent type of structural rearrangements in pigs are reciprocal translocations, which are caused by the exchange of chromatid parts between two or more nonhomologous chromosomes. These heritable chromosomal mutations affect all autosomal chromosomes and sex chromosomes, and among almost 200 translocations that have been identified to date, no two identical cases have been found in unrelated animals [ 1 , 2 , 4 , 12 , 13 , 15 , 16 , 17 , 18 , 19 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 ]. The individual consequences of each translocation depend on the morphology of the chromosomes involved, size of the rearranged fragments, and location of centromere breakpoints and positions as factors determining the gametogenesis process (meiotic conjugation and segregation) and the proportion of aneuploid gametes produced (about 40% on average).…”