Can the partial deletion in the Y chromosome of male mice affect the reproductive efficiency of their daughters?

Abstract

It has been previously shown that cumuli oophori around ovulated oocytes of B10.BR-Y(del) female mice (sired by males with the deleted Y chromosome) are more resistant to enzymatic treatment than cumuli oophori around eggs of control B10.BR females (having fathers with the intact Y chromosome). This can imply that some genes which influence the establishment of the imprinting pattern in male gametes are located in the region covered by the deletion. We hypothesize that the Y-dependent imprinting pattern, inherited by female offspring, affects stability of periovum layers within them. In the present study, cumulus-oocyte complexes ovulated by females from consomic strains: DBA, DBA-Y(BR), DBA-Y(del), and CBA, CBA-Y(BR), CBA-Y(del) were tested for their susceptibility to hyaluronidase digestion. The mean times for dispersal of cumulus cells surrounding oocytes of females from the backcross lines were convergent with the times typical for oocytes from strains being the donors of the Y chromosome (B10.BR or B10.BR-Y(del)) and differed clearly from pure DBA and CBA strains. It confirmed previous findings that Y chromosomes of fathers influence the properties of cumulus-oocyte complexes ovulated by their daughters. This influence is definitely stronger than the influence of the genetic background. Additionally, it was demonstrated that the cumuli oophori surrounding oocytes of B10.BR-Y(del) females exhibit increased resistance to penetration by spermatozoa in vitro, in comparison to the control B10.BR strain. This regularity was reflected in the decreased proportion of fertilized ova recovered from oviducts of B10.BR-Y(del) females mated with B10.BR-Y(del) males and in the lower litter sizes recorded for these pairs. The excessive stability of cumuli oophori typical for oocytes of females having Y(del) fathers may negatively affect their fertility, if they have partners producing poor quality sperm.

Increased Progesterone Production in Cumulus—Oocyte Complexes of Female Mice Sired by Males With the Y-Chromosome Long Arm Deletion and its Potential Influence on Fertilization Efficiency

“…For spermatozoa produced by B10.BR-Y del males, the firm extracellular matrix of B10.BR(Y del ) COCs is, however, a serious obstacle that considerably reduces fertilization ratio. 15 We postulate that low availability of progesterone receptors on sperm of males with the Y-chromosome deletion contributes to the described regularity. B10.BR-Y del spermatozoa may be insufficiently stimulated and hence less effective in disintegration of resistant cumulus layer that surround oocytes of B10.BR(Y del ) females.…”

Aging deteriorates quality of sperm produced by male mice with partial Yq deletion

“…They are fertile, but produce sperm of lower quality than their B10.BR counterparts. Numerous past studies revealed frequent morphological and ultrastructural abnormalities [Styrna et al 1991a;Styrna et al 1991b;Styrna et al 2002], deterioration of movement parameters [Grzmil et al 2007], difficulties in crossing uterotubal junction [Kotarska and Lenartowicz 2011], aberrant expression of surface receptors [Kotarska et al 2015], and lower fertilization efficiency of B10.BR-Y del spermatozoa [Xian et al 1992;Styrna et al 2002; Kotarska and Styrna 2012]. All these studies were focused, however, only on young adult individuals.…”

Chromosome substitution strains: gene discovery, functional analysis, and systems studies

“…Because Y chromosome and mitochondrial substitutions are made so readily, they have been used for many years to study a variety of traits in many strain combinations (for recent examples, see Barrick et al 2009; Llamas et al 2009; Suto 2009; Nelson et al 2010; Hines et al 2011; Case et al 2012; Kotarska and Styrna 2012). In other instances, an autosomal CSS was made specifically to verify and in some cases localize QTLs with crosses and congenic strains (see, for example, Matin et al 1999; Ochiai et al 2003; Hollis-Moffatt et al 2005; Kumazawa et al 2007; Wang et al 2010; Anderson et al 2009; Trammell et al 2012).…”

“…Examples of environmental influences include folate effects on variation in coat color in agouti viable A vy mice (Cooney et al 2002), high-fat-diet effects on pancreatic β -cell function (Ng et al 2010), and low-protein-diet effects transmitted through the paternal germ lineage (Carone et al 2010). Genetic variants can also induce heritable epigenetic changes, with examples including white-spotting paramutation effects of some but not all Kit receptor mutants (Rassoulzadegan et al 2006), various modifier genes such as p53 in the parental generation and the Deadend1 (Dnd1) gene in the offspring generation on testicular cancer risk (Lam et al 2007), paternal Kit ligand effects on testicular cancer risk among wild-type male offspring (Heaney et al 2008), Cdk9 deficiency on heart development (Wagner et al 2008), miR-124-Sox9 effects on embryonic and adult growth (Grandjean et al 2009), susceptibility to diet-induced obesity and eating habits in subcongenic strains derived from B6-Chr6 A/J (Yazbek et al 2010), and paternal Y chromosome effects on daughters in host and CSS-Y strains (Nelson and Nadeau 2010; Kotarska and Styrna 2012). In each case, the same strains that led to these discoveries can also be used as test and control groups to search for the molecular basis for these novel inheritance patterns.…”