91
Article
doi:10.1006/geno.2001.6621, available online at http://www.idealibrary.com on IDEAL
INTRODUCTION
The two parental alleles of some mammalian genes are func-
tionally nonequivalent due to genomic imprinting, in which one
of the alleles is epigenetically modified and inactivated based on
parental origin. More than 30 imprinted genes have been isolated
from human and mouse (http://www.mgu.har.mrc.ac.uk/
imprinting/imprin-ref.html#impregs); most of these genes are
involved in controlling either fetal development or nurturing
behaviors [1]. The “genomic imprinting” phenomenon exists in
placental mammals and marsupials but not in monotremes (egg-
laying mammals) [2,3]. It is therefore believed that imprinting
may have coevolved with the unusual reproductive strategy of
these animals [1] to balance the potentially conflicting genetic
influences on fetal development that are contributed by the two
parents [4,5].
Besides monoallelic expression, there are a number of fea-
tures common to imprinted genes. Many imprinted genes are
associated with CpG islands that are hemi-methylated in a
manner specific to the parent of origin [6]. Some imprinted
Imprinting and Evolution of Two Kruppel-type Zinc-Finger
Genes, ZIM3 and ZNF264, Located in the PEG3/USP29
Imprinted Domain
Joomyeong Kim,
1,2,*
Anne Bergmann,
1
Edward Wehri,
1
Xiaochen Lu,
1
and Lisa Stubbs
1,2
1
Genomics Division, Biology and Biotechnology Research Program, L-441,
Lawrence Livermore National Laboratory, 7000 East Avenue, Livermore, California 94551, USA
2
DOE Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, California 94598, USA
*
To whom correspondence and reprint requests should be addressed. Fax: (925) 422-2282. E-mail: kim16@llnl.gov.
We have isolated Kruppel-type (C2H2) zinc-finger genes, ZIM3 (zinc-finger gene 3 from
imprinted domain) and ZNF264, located downstream of human and mouse USP29 genes
(encoding ubiquitin-specific processing protease 29). In human, both ZIM3 and ZNF264
encode zinc-finger proteins with Kruppel-associated box (KRAB) A and B domains at the
amino-terminal regions of the predicted proteins. In contrast, mouse Zim3 and Zfp264 seem
to have lost protein-coding capability based on the lack of open reading frames (ORFs) in
their cDNA sequences. In particular, the 3' end of the Zim3 transcript overlaps with the cod-
ing region of the adjacent gene Usp29 in an antisense orientation, indicating the conversion
of mouse Zim3 into an antisense transcript gene for Usp29. The expression patterns of ZIM3
and ZNF264 have been largely conserved between human and mouse, with testis-specific
expression of ZIM3 and ubiquitous expression of ZNF264, but high expression levels in adult
testes in both species. Our studies also demonstrate that both mouse genes are imprinted with
maternal expression of Zim3 in adult testes and paternal expression of Zfp264 in neonatal and
adult brain. The reciprocal imprinting of two neighboring mouse genes, Zim3 and Zfp264, is
consistent with a pattern observed frequently in other imprinted domains, and suggests that
the imprinting of these two genes might be coregulated.
genes (including Gnas1, Igf2, Igf2r, Ube3a, and Znf127) are
transcribed bidirectionally, resulting in both sense- and anti-
sense transcripts [7,8]. A number of imprinted genes, includ-
ing H19 and IPW, are expressed without any coding capabil-
ity; the final products of these genes are RNAs rather than
proteins [6]. Most imprinted genes are clustered with other
imprinted genes in discrete chromosomal regions, with recip-
rocally imprinted gene pairs often found closely juxtaposed;
well-known examples include Igf2/H19 and Dlk1/Meg3 [9].
Recent studies of the oppositely imprinted Igf2/H19 pair have
demonstrated that the CpG island located upstream of H19
functions as an enhancer-blocking element (insulator) or
boundary element, and that a conserved vertebrate zinc-fin-
ger gene, CTCF, binds to this boundary element and controls
the allele-specific expression of Igf2 and H19 [10,11].
Mouse chromosome 7 (Mmu7) contains three different
imprinted domains located in the proximal, central, and dis-
tal regions of the chromosome [12,13]. The central and distal
regions of Mmu7 are homologous to two human chromo-
some regions, 15q13–q11 and 11p15, respectively, which are
GENOMICS Vol. 77, Numbers 1–2, September 2001
Copyright © 2001 by Academic Press. All rights of reproduction in any form reserved.
0888-7543/01 $35.00