Szabó Laboratory

Selected Publications

Zhou W, Hinoue T, Barnes B, Mitchell O, Iqbal W, Lee SM, Foy KK, Lee KH, Moyer EJ, VanderArk A, Koeman JM, Ding W, Kalkat M, Spix NJ, Eagleson B, Pospisilik JA, Szabó PE, Bartolomei M, Vander Scaaf NA, Kang L, Wiseman AK, Jones PA, Krawczyk CM, Adams M, Porecha R, Chen BH, Shen H, Laird PW. Pre-print. DNA methylation dynamics and dysregulation delineated by high-throughput profiling in the mouse. bioRxiv.

Zeng TB, Pierce N, Liao J, Singh P, Lau K, Zhou W, Szabó P. 2022. EHMT2 suppresses the variation of transcriptional switches in the mouse embryo. PLOS Genet.

Liao J, Zeng TB, Pierce N, Tran DA, Singh P, Mann JR, Szabó PE. 2021. Prenatal correction of IGF2 to rescue the growth phenotypes in mouse models of Beckwith-Wiedemann and Silver-Russell syndromes. Cell Rep 34(6):108729.

Liao J, Szabó PE. 2020. Maternal DOT1L is dispensable for mouse development. Sci Rep 10(1):20636.

Zeng TB, Szabó PE. 2020.  Immunochemical detection of modified cytosine species in mammalian preimplantation embryos. Methods Mol Biol 2198:147–157.

Huang Z, Meng Y, Szabó PE, Kohli RM, Pfeifer GP. 2019.  High resolution analysis of 5-hydroxymethylcytosine by TET-assisted bisulfite sequencing.Methods Mol Bio 2198:321–331.

Pfeifer GP, Szabó PE, Song J. 2019.  Protein interactions at oxidized 5-methylcytosine bases. J Mol Biol.

Zeng TB, Han L, Pierce N, Pfeifer GP, Szabó PE. 2019. EHMT2 and SETDB1 protect the maternal pronucleus from 5mC oxidation. Proc Natl Acad Sci U S A. 116(22):10834-10841.

Pai S, Li P, Killinger B, Marshall L, Jia P, Liao J, Petronis A, Szabó P, Labrie V. 2019. Differential methylation of enhancer at IGF2 is associated with abnormal dopamine synthesis in major psychosis. Nat Comm.

Pfeifer GP, Szabó PE. 2018. Gene body profiles of 5-hydroxymethylcytosine: potential origin, function and use as a cancer biomarker. Epigenomics.

Jin SG, Zhang ZM, Dunwell TL, Harter MR, Wu X, Johnson J, Li Z, Liu J, Szabó PE, Lu Q, Xu GL, Song J, Pfeifer GP. 2016. Tet3 reads 5-carboxylcytosine through its CXXC domain and is a potential guardian against neurodegenerationCell Rep 14(3):493–505.  

Szabó PE. 2015. Response to: the nature of evidence for and against epigenetic inheritance. Genome Biol 16:138      PubMed

Iqbal K, Tran DA, Li AX, Warden C, Bai AY, Singh P, Wu X, Pfeifer GP, Szabó PE. 2015. Deleterious effects of endocrine disruptors are corrected in the mammalian germline by epigenome reprogramming. Genome Biol 16:59.    PubMed

Hahn M, Szabó PE, Pfeifer GP. 2014. 5-hydroxymethylcytosine: a stable or transient DNA modification? Genomics 104(5):314–323.     PubMed

Tran DA, Bai AY, Singh P, Wu X, Szabó PE. 2014. Characterization of the imprinting signature of mouse embryo fibroblasts by RNA deep sequencing. Nucleic Acids Res 42(3):1772–1783.     PubMed     

Liao J, He J, Szabó PE. 2013. The Pou5f1 distal enhancer is sufficient to drive Pou5f1 promoter-EGFP expression in embryonic stem cells. Int J Dev Biol 57(9-10):725–729.     PubMed

Singh P, Li AX, Tran, DA, Oates N, Kang E-R, Wu X, Szabó PE. 2013. De novo DNA methylation in the male germ line occurs by default but is excluded at sites of H3K4 methylation. Cell Rep 4(1):205–219.     PubMed

Singh P, Szabó PE. 2012. Chromatin immunoprecipitation to characterize the epigenetic profiles of imprinted domains. Methods Mol Biol 925:159–172.     PubMed

Singh P, Lee DH, Szabó PE. 2012. More than insulator: multiple roles of CTCF at the H19-Igf2 imprinted domain. Front Genet 3:214.     PubMed

Gu TP, Guo F, Yang H, Wu HP, Xu GF, Liu W, Xie ZG, Shi L, He X, Jin SG, Iqbal K, Shi YG, Deng Z, Szabó PE, Pfeifer GP, Li J, Xu GL. 2011. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477(7366):606–610.     PubMed

Abe M, Tsai SY, Jin SG, Pfeifer GP, Szabó PE. 2011. Sex-specific dynamics of global chromatin changes in fetal mouse germ cells. PLoS One 6(8):e23848.     PubMed

Kang ER, Iqbal K, Tran DA, Rivas GE, Singh P, Pfeifer GP, Szabó PE. 2011. Effects of endocrine disruptors on imprinted gene expression in the mouse embryo. Epigenetics 6(7):937–950.     PubMed

Iqbal K, Jin SG, Pfeifer GP*, Szabó PE*. 2011. Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc Natl Acad Sci USA 108(9):3642–3647.     PubMed 
*Equally contributing authors

Singh P, Wu X, Lee DH, Li AX, Rauch TA, Pfeifer GP, Mann JR, Szabó PE. 2011. Chromosome-wide analysis of parental allele-specific chromatin and DNA methylation. Mol Cell Biol 31(8):1757–1770.     PubMed
MCB Spotlight article

Lee DH, Tran D, Singh P, Oates N, Rivas GE, Larson GP, Pfeifer GP, Szabó PE. 2011. MIRA-SNuPE, a quantitative, multiplex method for measuring allele-specific DNA. Epigenetics 6(2):212–223.     PubMed

Lee DH, Singh P, Tsai, SY, Oates, N, Spalla A, Spalla C, Brown L, Rivas G, Larson G, Rauch AT, Pfeifer GP, Szabó PE. 2010. CTCF-dependent chromatin bias constitutes transient epigenetic memory of the mother at the H19-Igf2 imprinting control region in prospermatogonia. PLoS Genet 6(11):e1001224.     PubMed

Lee DH, Singh P, Tsark WM, Szabó PE. 2010. Complete biallelic insulation at the H19/Igf2 imprinting control region position results in fetal growth retardation and perinatal lethality. PLoS One 5(9):e12630.     PubMed

Singh P, Cho J, Tsai SY, Rivas GE, Larson GP, Szabó PE. 2010. Coordinated allele specific histone acetylation at the differentially methylated regions of imprinted genes. Nucleic Acids Res 38(22):7974–7990.     PubMed

Singh P, Han L, Rivas GE, Lee DH, Nicholson TB, Larson GP, Chen T, Szabó PE. 2010. Allele-specific H3K79 Di- versus trimethylation distinguishes opposite parental alleles at imprinted regions. Mol Cell Biol 30(11):2693–2707.     PubMed
MCB Spotlight article

Han L, Lee DH, Szabó PE. 2008. CTCF is the master organizer of domain-wide allele-specific chromatin at the H19/Igf2 imprinted region. Mol Cell Biol 28(3):1124–1135.     PubMed

Szabó PE, Han L, Hyo-Jung J, Mann JR. 2006. Mutagenesis in mice of nuclear hormone receptor binding sites in the Igf2/H19 imprinting control region. Cytogenet Genome Res 113(1-4):238–246.     PubMed

Szabó PE, Pfeifer GP, Mann JR. 2004. Parent-of-origin-specific binding of nuclear hormone receptor complexes in the H19-Igf2 imprinting control region. Mol Cell Biol 24(11):4858–4868.     PubMed

Szabó PE, Tang SH, Silva FJ, Tsark WM, Mann JR. 2004. Role of CTCF binding sites in the Igf2/H19 imprinting control region. Mol Cell Biol 24(11):4791–4800.     PubMed

Szabó PE, Hübner K, Schöler H, and Mann JR. 2002. Allele-specific expression of imprinted genes in mouse migratory primordial germ cells. Mech Dev115(1-2):157–160.     PubMed

Szabó PE, Tang SH, Reed MR, Silva FJ, Tsark WM, Mann JR. 2002. The chicken beta-globin insulator element conveys chromatin boundary activity but not imprinting at the Igf2 and H19 imprinted domain. Development 129(4):897–904.     PubMed

Szabó PE, Pfeifer GP, Miao F, O’Connor TR, Mann JR. 2000. Improved in vivo dimethyl sulfate footprinting using AlkA protein: DNA-protein interactions at the mouse H19 gene promoter in primary embryo fibroblasts. Anal Biochem 283(1):112–116.     PubMed

Szabó PE, Tang SH, Rentsendorj A, Pfeifer GP, Mann JR. 2000. Maternal-specific footprints at putative CTCF sites in the H19 imprinting control region give evidence for insulator function. Curr Biol 10(10):607–610.     PubMed

Szabó PE, Pfeifer GP, Mann JR. 1998. Characterization of novel parent-specific epigenetic modifications upstream of the imprinted mouse H19 gene. Mol Cell Biol 18(11):6767–6776.     PubMed

Szabó PE, Mann JR. 1996. Maternal and paternal genomes function independently in mouse ova in establishing expression of the imprinted genes Snrpn and Igf2r: no evidence for allelic trans-sensing and counting mechanisms. EMBO J 15(22):6018–6025.     PubMed

Szabó PE, Mann JR. 1995. Allele-specific expression and total expression levels of imprinted genes during early mouse development: implications for imprinting mechanisms. Genes Dev 9(24):3097–3108.     PubMed

Szabó PE, Mann JR. 1995. Biallelic expression of imprinted genes in the mouse germline: implications for erasure, establishment, and mechanisms of genomic imprinting. Genes Dev 9(15):1857–1868.     PubMed

Szabó P, Moitra J, Rencendorj A, Rákhely G, Rauch T, Kiss I. 1995. Identification of a nuclear factor-I family protein-binding site in the silencer region of the cartilage matrix protein gene. J Biol Chem 270(17):10212–10221.     PubMed

Szabó P, Mann JR. 1994. Expression and methylation of imprinted genes during in vitro differentiation of mouse parthenogenetic and androgenetic embryonic stem cell lines. Development 120(6):1651–1660.     PubMed

Kiss I, Bösze Z, Szabó P, Altanchimeg R, Barta E, Deák F. 1990. Identification of positive and negative regulatory regions controlling expression of the cartilage matrix protein gene. Mol Cell Biol 10(5):2432–2436.     PubMed