Chromosome Research 1994, 2, 147-152
DNA methylation changes during mouse
spermatogenesis
Jesüs del Mazo, Giorgio Prantera, Miguel Torres
& Marina Ferraro
Received 5 July 1993, received in revised form 9 November 1993;
Accepted for publication by H. C. Macgregor 23 November 1993
Genomic imprinting in mammals is thought to be
mediated by differences in the methylation level of
cytosine residues in the genome. These differences
in DNA methylation are thought to be generated during
the development of the germ line. To characterize the
profile of global methylation of the mouse genome
during male gametogenesis, we have quantified the
relative level of methylation in individual cells during
meiosis and spermatogenesis. A decrease in the level
of DNA methylation is observed from meiotic cells to
elongated spermatids. The erasure of the somatic
pattern of methylation during spermatogenesis sug-
gests the existence of a subsequent mechanism gen-
erating the parental specific methylation patterns
leading to genomic imprinting of specific alleles.
Key words: gametogenesis, imprinting, in situ nick-
translation, methylation, mouse, Mus musculus, sperma-
togenesis
Introduction
In mammals, genomic imprinting of maternal and
paternal chromosomes is a mechanism that generates
differential expression of aUeles in relation to their
parental origin. This phenomenon is thought to play
a crucial role in the embryonic development of mam-
mals (Solter 1988). Alteration of the genomic imprinting
pattern has also been identified as a possible cause of
genetic disorders, including some human diseases (Reik
1989, Clarke 1990, Hall 1990). The molecular basis for
this epigenetic inheritance has not been clearly deli-
neated. However, any proposed mechanism should
meet the following requisites: it should ensure the
inheritance of the imprinting pattern through subse-
quent rounds of DNA replication, and its reversal when
passing through the female or male gamete (Sapienza et
al. 1989).
Methylation of DNA at the cytosine residues is an
epigenetic phenomenon, which possesses the requisites
of heritability and reversibility (Razin et al. 1984).
Moreover, changes in DNA methylation have been
also associated with the regulation of gene expression
(Boyes & Bird 1991), and clinical manifestation of some
human diseases (Oberlé et al. 1991). For these reasons,
DNA methylation has been proposed as a possible
mechanism to imprint genes, chromosome regions, or
specific chromosomes (Swain et al. 1987, Prantera &
Ferraro 1990, Grant et al. 1992).
Although we cannot exclude fertilization as the mo-
ment when male and female pronuclei are differentially
imprinted, the most accepted hypothesis is that parental
imprinting takes place, or at least begins, during
the development of germ cells. Thus, changes in
the methylation pattern should occur during gameto-
genesis. In fact, different methylation patterns in ga-
mete cells versus somatic tissues have been described
for specific genes (Groudine & Conkin 1985, Driscoll &
Migeon 1990) or DNA sequences (Sandford et al. 1984).
In this work, we have applied a sensitive technique
that shows changes in the global methylation levels of
DNA in individual cells during mouse spermatogen-
esis. We have quantified the changes in DNA methyla-
tion for different cell types during the progression of
spermatogenesis. Our results suggest a model for the
participation of methylation in the generation of par-
ental imprinting.
Jesüs del Mazo (corresponding author) and Miguel Torres are at the Centro de Investigaciones Biolögicas (C.S.I.C.), Veläzquez 144,
28006- Madrid, Spain. Tel: ( + 34) 1 5644562 ext 4324; Fax: ( + 34) 15627518. Giorgio Prantera is at The Departimento di Agrobiologia
e Agrochimica, Universitd della Tuscia, Viterbo, Italy. Marina Ferraro is at the Departimento di Genetica e Biologia Molecolare,
Universitä La Sapienza, Roma, Italy.
© 1994 Rapid Communications of Oxford Ltd Chromosome Research Vol 2 1994 147