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http://dx.doi.org/10.5808/GI.2014.12.3.105

Regulation and Function of the Peg3 Imprinted Domain  

He, Hongzhi (Department of Biological Sciences, Louisiana State University)
Kim, Joomyeong (Department of Biological Sciences, Louisiana State University)
Abstract
A subset of mammalian genes differ functionally between two alleles due to genomic imprinting, and seven such genes (Peg3, Usp29, APeg3, Zfp264, Zim1, Zim2, Zim3) are localized within the 500-kb genomic interval of the human and mouse genomes, constituting the Peg3 imprinted domain. This Peg3 domain shares several features with the other imprinted domains, including an evolutionarily conserved domain structure, along with transcriptional co-regulation through shared cis regulatory elements, as well as functional roles in controlling fetal growth rates and maternal-caring behaviors. The Peg3 domain also displays some unique features, including YY1-mediated regulation of transcription and imprinting; conversion and adaptation of several protein-coding members as ncRNA genes during evolution; and its close connection to human cancers through the potential tumor suppressor functions of Peg3 and Usp29. In this review, we summarize and discuss these features of the Peg3 domain.
Keywords
genomic imprinting; ncRNA; Peg3; tumor suppressor genes; YY1 transcription factor;
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1 Kim J, Noskov VN, Lu X, Bergmann A, Ren X, Warth T, et al. Discovery of a novel, paternally expressed ubiquitin-specific processing protease gene through comparative analysis of an imprinted region of mouse chromosome 7 and human chromosome 19q13.4. Genome Res 2000;10:1138-1147.   DOI
2 Kim J, Bergmann A, Wehri E, Lu X, Stubbs L. Imprinting and evolution of two Kruppel-type zinc-finger genes, ZIM3 and ZNF264, located in the PEG3/USP29 imprinted domain. Genomics 2001;77:91-98.   DOI
3 Kim J, Bergmann A, Lucas S, Stone R, Stubbs L. Lineage-specific imprinting and evolution of the zinc-finger gene ZIM2. Genomics 2004;84:47-58.   DOI
4 Kim J, Lu X, Stubbs L. Zim1, a maternally expressed mouse Kruppel-type zinc-finger gene located in proximal chromosome 7. Hum Mol Genet 1999;8:847-854.   DOI
5 Choo JH, Kim JD, Kim J. Imprinting of an evolutionarily conserved antisense transcript gene APeg3. Gene 2008;409:28-33.   DOI
6 Kim J, Bergmann A, Choo JH, Stubbs L. Genomic organization and imprinting of the Peg3 domain in bovine. Genomics 2007;90:85-92.   DOI
7 Kim J, Gordon L, Dehal P, Badri H, Christensen M, Groza M, et al. Homology-driven assembly of a sequence-ready mouse BAC contig map spanning regions related to the 46-Mb gene-rich euchromatic segments of human chromosome 19. Genomics 2001;74:129-141.   DOI
8 Thiaville MM, Kim H, Frey WD, Kim J. Identification of an evolutionarily conserved cis-regulatory element controlling the Peg3 imprinted domain. PLoS One 2013;8:e75417.   DOI
9 Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, Kuan S, et al. A map of the cis-regulatory sequences in the mouse genome. Nature 2012;488:116-120.   DOI
10 Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci U S A 2010;107:21931-21936.   DOI
11 Chen MY, Liao WS, Lu Z, Bornmann WG, Hennessey V, Washington MN, et al. Decitabine and suberoylanilide hydroxamic acid (SAHA) inhibit growth of ovarian cancer cell lines and xenografts while inducing expression of imprinted tumor suppressor genes, apoptosis, G2/M arrest, and autophagy. Cancer 2011;117:4424-4438.   DOI
12 Buraschi S, Neill T, Goyal A, Poluzzi C, Smythies J, Owens RT, et al. Decorin causes autophagy in endothelial cells via Peg3. Proc Natl Acad Sci U S A 2013;110:E2582-E2591.   DOI
13 Broad KD, Keverne EB. Placental protection of the fetal brain during short-term food deprivation. Proc Natl Acad Sci U S A 2011;108:15237-15241.   DOI
14 Relaix F, Wei X, Li W, Pan J, Lin Y, Bowtell DD, et al. Pw1/Peg3 is a potential cell death mediator and cooperates with Siah1a in p53-mediated apoptosis. Proc Natl Acad Sci U S A 2000;97: 2105-2110.   DOI   ScienceOn
15 Schwarzkopf M, Coletti D, Sassoon D, Marazzi G. Muscle cachexia is regulated by a p53-PW1/Peg3-dependent pathway. Genes Dev 2006;20:3440-3452.   DOI
16 Yamaguchi A, Taniguchi M, Hori O, Ogawa S, Tojo N, Matsuoka N, et al. Peg3/Pw1 is involved in p53-mediated cell death pathway in brain ischemia/hypoxia. J Biol Chem 2002;277:623-629.   DOI
17 Martin Y, Cabrera E, Amoedo H, Hernandez-Perez S, Dominguez-Kelly R, Freire R. USP29 controls the stability of checkpoint adaptor Claspin by deubiquitination. Oncogene 2014 Mar 17 [Epub]. http://dx.doi.org/10.1038/onc.2014.38.
18 Thiaville MM, Huang JM, Kim H, Ekram MB, Roh TY, Kim J. DNA-binding motif and target genes of the imprinted transcription factor PEG3. Gene 2013;512:314-320.   DOI
19 Schultz DC, Ayyanathan K, Negorev D, Maul GG, Rauscher FJ 3rd. SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev 2002;16:919-932.   DOI   ScienceOn
20 Frietze S, O'Geen H, Blahnik KR, Jin VX, Farnham PJ. ZNF274 recruits the histone methyltransferase SETDB1 to the 3' ends of ZNF genes. PLoS One 2010;5:e15082.   DOI
21 Lucifero D, Mann MR, Bartolomei MS, Trasler JM. Gene-specific timing and epigenetic memory in oocyte imprinting. Hum Mol Genet 2004;13:839-849.   DOI
22 Huang JM, Kim J. DNA methylation analysis of the mammalian PEG3 imprinted domain. Gene 2009;442:18-25.   DOI
23 Kim J, Ekram MB, Kim H, Faisal M, Frey WD, Huang JM, et al. Imprinting control region (ICR) of the Peg3 domain. Hum Mol Genet 2012;21:2677-2687.   DOI
24 Kim J, Kollhoff A, Bergmann A, Stubbs L. Methylation-sensitive binding of transcription factor YY1 to an insulator sequence within the paternally expressed imprinted gene, Peg3. Hum Mol Genet 2003;12:233-245.   DOI
25 Kim JD, Hinz AK, Bergmann A, Huang JM, Ovcharenko I, Stubbs L, et al. Identification of clustered YY1 binding sites in imprinting control regions. Genome Res 2006;16:901-911.   DOI
26 Kim JD, Kim J. YY1's longer DNA-binding motifs. Genomics 2009;93:152-158.   DOI
27 Kim JD, Kang K, Kim J. YY1's role in DNA methylation of Peg3 and Xist. Nucleic Acids Res 2009;37:5656-5664.   DOI
28 Kim J, Kim JD. In vivo YY1 knockdown effects on genomic imprinting. Hum Mol Genet 2008;17:391-401.   DOI
29 Kim JD, Hinz AK, Choo JH, Stubbs L, Kim J. YY1 as a controlling factor for the Peg3 and Gnas imprinted domains. Genomics 2007;89:262-269.   DOI
30 Moore T, Haig D. Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet 1991;7:45-49.   DOI
31 Tilghman SM. The sins of the fathers and mothers: genomic imprinting in mammalian development. Cell 1999;96:185-193.   DOI   ScienceOn
32 Li L, Keverne EB, Aparicio SA, Ishino F, Barton SC, Surani MA. Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science 1999;284:330-333.   DOI
33 Bartolomei MS, Ferguson-Smith AC. Mammalian genomic imprinting. Cold Spring Harb Perspect Biol 2011;3:pii a002592.
34 Barlow DP, Bartolomei MS. Genomic imprinting in mammals. Cold Spring Harb Perspect Biol 2014;6:pii a018382.
35 Edwards CA, Ferguson-Smith AC. Mechanisms regulating imprinted genes in clusters. Curr Opin Cell Biol 2007;19:281-289.   DOI   ScienceOn
36 Spahn L, Barlow DP. An ICE pattern crystallizes. Nat Genet 2003;35:11-12.   DOI
37 Kuroiwa Y, Kaneko-Ishino T, Kagitani F, Kohda T, Li LL, Tada M, et al. Peg3 imprinted gene on proximal chromosome 7 encodes for a zinc finger protein. Nat Genet 1996;12:186-190.   DOI
38 Relaix F, Weng X, Marazzi G, Yang E, Copeland N, Jenkins N, et al. Pw1, a novel zinc finger gene implicated in the myogenic and neuronal lineages. Dev Biol 1996;177:383-396.   DOI
39 Kim J, Ashworth L, Branscomb E, Stubbs L. The human homolog of a mouse-imprinted gene, Peg3, maps to a zinc finger gene-rich region of human chromosome 19q13.4. Genome Res 1997;7:532-540.   DOI
40 Glasgow E, Ryu SL, Yamashita M, Zhang BJ, Mutsuga N, Gainer H. APeg3, a novel paternally expressed gene 3 antisense RNA transcript specifically expressed in vasopressinergic magnocellular neurons in the rat supraoptic nucleus. Brain Res Mol Brain Res 2005;137:143-151.   DOI
41 Ivanova E, Kelsey G. Imprinted genes and hypothalamic function. J Mol Endocrinol 2011;47:R67-R74.   DOI
42 Kim J, Frey WD, He H, Kim H, Ekram MB, Bakshi A, et al. Peg3 mutational effects on reproduction and placenta-specific gene families. PLoS One 2013;8:e83359.   DOI
43 Swaney WT, Curley JP, Champagne FA, Keverne EB. The paternally expressed gene Peg3 regulates sexual experience-dependent preferences for estrous odors. Behav Neurosci 2008;122:963-973.   DOI
44 Swaney WT, Curley JP, Champagne FA, Keverne EB. Genomic imprinting mediates sexual experience-dependent olfactory learning in male mice. Proc Natl Acad Sci U S A 2007;104:6084-6089.   DOI
45 Curley JP, Barton S, Surani A, Keverne EB. Coadaptation in mother and infant regulated by a paternally expressed imprinted gene. Proc Biol Sci 2004;271:1303-1309.   DOI
46 Flisikowski K, Venhoranta H, Nowacka-Woszuk J, McKay SD, Flyckt A, Taponen J, et al. A novel mutation in the maternally imprinted PEG3 domain results in a loss of MIMT1 expression and causes abortions and stillbirths in cattle (Bos taurus). PLoS One 2010;5:e15116.   DOI
47 Dowdy SC, Gostout BS, Shridhar V, Wu X, Smith DI, Podratz KC, et al. Biallelic methylation and silencing of paternally expressed gene 3 (PEG3) in gynecologic cancer cell lines. Gynecol Oncol 2005;99:126-134.   DOI
48 Feng W, Marquez RT, Lu Z, Liu J, Lu KH, Issa JP, et al. Imprinted tumor suppressor genes ARHI and PEG3 are the most frequently down-regulated in human ovarian cancers by loss of heterozygosity and promoter methylation. Cancer 2008;112:1489-1502.   DOI
49 Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, et al. High-resolution profiling of histone methylations in the human genome. Cell 2007;129:823-837.   DOI   ScienceOn
50 ENCODE Project Consortium, Birney E, Stamatoyannopoulos JA, Dutta A, Guigó R, Gingeras TR, et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007;447:799-816.   DOI   ScienceOn
51 Frey WD, Kim J. APeg3: regulation of Peg3 through an evolutionarily conserved ncRNA. Gene 2014;540:251-257.   DOI
52 Kim J. Multiple YY1 and CTCF binding sites in imprinting control regions. Epigenetics 2008;3:115-118.   DOI
53 Kim JD, Yu S, Choo JH, Kim J. Two evolutionarily conserved sequence elements for Peg3/Usp29 transcription. BMC Mol Biol 2008;9:108.   DOI
54 Calhoun VC, Levine M. Long-range enhancer-promoter interactions in the Scr-Antp interval of the Drosophila Antennapedia complex. Proc Natl Acad Sci U S A 2003;100:9878-9883.   DOI
55 Broad KD, Curley JP, Keverne EB. Increased apoptosis during neonatal brain development underlies the adult behavioral deficits seen in mice lacking a functional paternally expressed gene 3 (Peg3). Dev Neurobiol 2009;69:314-325.   DOI
56 Spengler D, Villalba M, Hoffmann A, Pantaloni C, Houssami S, Bockaert J, et al. Regulation of apoptosis and cell cycle arrest by Zac1, a novel zinc finger protein expressed in the pituitary gland and the brain. EMBO J 1997;16:2814-2825.   DOI
57 Varrault A, Gueydan C, Delalbre A, Bellmann A, Houssami S, Aknin C, et al. Zac1 regulates an imprinted gene network critically involved in the control of embryonic growth. Dev Cell 2006;11:711-722.   DOI
58 Duret L, Chureau C, Samain S, Weissenbach J, Avner P. The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 2006;312:1653-1655.   DOI