A novel imprinted locus on bovine chromosome 18 homologous with human chromosome 16q24.1.
Chromosome 18
Cow
DNA methylation
Genomic imprinting
Isoform-specific
Monoallelic expression
Journal
Molecular genetics and genomics : MGG
ISSN: 1617-4623
Titre abrégé: Mol Genet Genomics
Pays: Germany
ID NLM: 101093320
Informations de publication
Date de publication:
28 Mar 2024
28 Mar 2024
Historique:
received:
28
08
2023
accepted:
02
02
2024
medline:
28
3
2024
pubmed:
28
3
2024
entrez:
28
3
2024
Statut:
epublish
Résumé
Genomic imprinting is an epigenetic regulation mechanism in mammals resulting in the parentally dependent monoallelic expression of genes. Imprinting disorders in humans are associated with several congenital syndromes and cancers and remain the focus of many medical studies. Cattle is a better model organism for investigating human embryo development than mice. Imprinted genes usually cluster on chromosomes and are regulated by different methylation regions (DMRs) located in imprinting control regions that control gene expression in cis. There is an imprinted locus on human chromosome 16q24.1 associated with congenital lethal developmental lung disease in newborns. However, genomic imprinting on bovine chromosome 18, which is homologous with human chromosome 16 has not been systematically studied. The aim of this study was to analyze the allelic expressions of eight genes (CDH13, ATP2C2, TLDC1, COTL1, CRISPLD2, ZDHHC7, KIAA0513, and GSE1) on bovine chromosome 18 and to search the DMRs associated gene allelic expression. Three transcript variants of the ZDHHC7 gene (X1, X2, and X5) showed maternal imprinting in bovine placentas. In addition, the monoallelic expression of X2 and X5 was tissue-specific. Five transcripts of the KIAA0513 gene showed tissue- and isoform-specific monoallelic expression. The CDH13, ATP2C2, and TLDC1 genes exhibited tissue-specific imprinting, however, COTL1, CRISLPLD2, and GSE1 escaped imprinting. Four DMRs, established after fertilization, were found in this region. Two DMRs were located between the ZDHHC7 and KIAA0513 genes, and two were in exon 1 of the CDH13 and ATP2C2 genes, respectively. The results from this study support future studies on the molecular mechanism to regulate the imprinting of candidate genes on bovine chromosome 18.
Identifiants
pubmed: 38546894
doi: 10.1007/s00438-024-02123-8
pii: 10.1007/s00438-024-02123-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
40Subventions
Organisme : Earmarked Fund for China Agriculture Research System
ID : CARS36
Organisme : National Foreign Expert Project
ID : G2022003015L
Organisme : Hebei Province Agricultural Industry Technology System Innovation Team
ID : HBCT2024240206
Organisme : Hebei Province Agricultural Industry Technology System Innovation Team
ID : HBCT2024240202
Organisme : Hebei Province Natural Science Foundation
ID : C2023204145
Organisme : Hebei Province Natural Science Foundation
ID : C2022201058
Organisme : S&T Program of Hebei
ID : 22326321D
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Abril-Fornaguera J, Torrens L, Andreu-Oller C et al (2023) Identification of IGF2 as genomic driver and actionable therapeutic target in hepatoblastoma. Mol Cancer Ther 22(4):485–498. https://doi.org/10.1158/1535-7163
doi: 10.1158/1535-7163
pubmed: 36780225
pmcid: 10073300
Babak T, DeVeale B, Tsang EK et al (2015) Genetic conflict reflected in tissue-specific maps of genomic imprinting in human and mouse. Nat Genet 47(5):544–549. https://doi.org/10.1038/ng.3274
doi: 10.1038/ng.3274
pubmed: 25848752
pmcid: 4414907
Baran Y, Subramaniam M, Biton A et al (2015) The landscape of genomic imprinting across diverse adult human tissues. Genome Res 25(7):927–936. https://doi.org/10.1101/gr.192278.115
doi: 10.1101/gr.192278.115
pubmed: 25953952
pmcid: 4484390
Barlow DP, Bartolomei MS (2014) Genomic imprinting in mammals. Cold Spring Harb Perspect Biol 6(2):a018382. https://doi.org/10.1101/cshperspect.a018382
doi: 10.1101/cshperspect.a018382
pubmed: 24492710
pmcid: 3941233
Bartolomei MS, Ferguson-Smith AC (2011) Mammalian genomic imprinting. Cold Spring Harb Perspect Biol 3(7):a002592. https://doi.org/10.1101/cshperspect.a002592
doi: 10.1101/cshperspect.a002592
pubmed: 21576252
pmcid: 3119911
Bourneuf E, Otz P, Pausch H et al (2017) Rapid discovery of De Novo deleterious mutations in cattle enhances the value of livestock as model species. Sci Rep 7(1):11466. https://doi.org/10.1038/s41598-017-11523-3
doi: 10.1038/s41598-017-11523-3
pubmed: 28904385
pmcid: 5597596
Brideau CM, Eilertson KE, Hagarman JA et al (2010) Successful computational prediction of novel imprinted genes from epigenomic features. Mol Cell Biol 30(13):3357–3370. https://doi.org/10.1128/MCB.01355-09
doi: 10.1128/MCB.01355-09
pubmed: 20421412
pmcid: 2897571
Chen Z, Hagen DE, Wang J et al (2016) Global assessment of imprinted gene expression in the bovine conceptus by next generation sequencing. Epigenetics 11(7):501–516. https://doi.org/10.1080/15592294.2016.1184805
doi: 10.1080/15592294.2016.1184805
pubmed: 27245094
pmcid: 4939914
Dong Y, Jin L, Liu X et al (2022) IMPACT and OSBPL1A are two isoform-specific imprinted genes in bovines. Theriogenology 184:100–109. https://doi.org/10.1016/j.theriogenology.2022.02.023
doi: 10.1016/j.theriogenology.2022.02.023
pubmed: 35294861
Eggermann T, Curtis M, Zerres K et al (2004) Maternal uniparental disomy 16 and genetic counseling: new case and survey of published cases. Genet Couns 15(2):183–190
pubmed: 15287418
Eggermann T, Perez de Nanclares G, Maher ER et al (2015) Imprinting disorders: a group of congenital disorders with overlapping patterns of molecular changes affecting imprinted loci. Clin Epigenetics 7:123. https://doi.org/10.1186/s13148-015-0143-8
doi: 10.1186/s13148-015-0143-8
pubmed: 26583054
pmcid: 4650860
Ferguson-Smith AC, Cattanach BM, Barton SC et al (1991) Embryological and molecular investigations of parental imprinting on mouse chromosome 7. Nature 351(6328):667–670. https://doi.org/10.1038/351667a0
doi: 10.1038/351667a0
pubmed: 2052093
Ferguson-Smith AC (2011) Genomic imprinting: the emergence of an epigenetic paradigm]. Nat Rev Genet 12(8):565–575. https://doi.org/10.1038/nrg3032
doi: 10.1038/nrg3032
pubmed: 21765458
Finelli MJ, Sanchez-Pulido L, Liu KX et al (2016) The evolutionarily conserved Tre2/Bub2/Cdc16 (TBC), Lysin Motif (LysM), domain catalytic (TLDc) domain is neuroprotective against oxidative stress. J Biol Chem 291(6):2751–2763. https://doi.org/10.1074/jbc.M115.685222
doi: 10.1074/jbc.M115.685222
pubmed: 26668325
Hanna CW, Kelsey G (2014) The specification of imprints in mammals. Heredity (edinb) 113(2):176–183. https://doi.org/10.1038/hdy.2014.54
doi: 10.1038/hdy.2014.54
pubmed: 24939713
Hansen PJ (2014) Current and future assisted reproductive technologies for mammalian farm animals. Adv Exper Med Biol 752:1–22. https://doi.org/10.1007/978-1-4614-8887-3_1
doi: 10.1007/978-1-4614-8887-3_1
Hiver S, Shimizu-Mizuno N, Ikawa Y et al (2023) Gse1, a component of the CoREST complex, is required for placenta development in the mouse. Dev Biol 498:97–105. https://doi.org/10.1016/j.ydbio.2023.03.009
doi: 10.1016/j.ydbio.2023.03.009
pubmed: 37019373
Jadhav B, Monajemi R, Gagalova KK et al (2019) RNA-Seq in 296 phased trios provides a high-resolution map of genomic imprinting. BMC Biol 17(1):50. https://doi.org/10.1186/s12915-019-0674-0
doi: 10.1186/s12915-019-0674-0
pubmed: 31234833
pmcid: 6589892
John RM, Surani MA (1996) Imprinted genes and regulation of gene expression by epigenetic inheritance. Curr Opin Cell Biol 8(3):348–353. https://doi.org/10.1016/s0955-0674(96)80008-1
doi: 10.1016/s0955-0674(96)80008-1
pubmed: 8743885
Joshi RS, Garg P, Zaitlen N et al (2016) DNA methylation profiling of uniparental disomy subjects provides a map of parental epigenetic bias in the human genome. Am J Hum Genet 99(3):555–566. https://doi.org/10.1016/j.ajhg.2016.06.032
doi: 10.1016/j.ajhg.2016.06.032
pubmed: 27569549
pmcid: 5011056
Kerkenberg N, Wachsmuth L, Zhang M et al (2021) Brain microstructural changes in mice persist in adulthood and are modulated by the palmitoyl acyltransferase ZDHHC7. Eur J Neurosci 54(6):5951–5967. https://doi.org/10.1111/ejn.15415
doi: 10.1111/ejn.15415
pubmed: 34355442
Kim JY, Jelinek J, Lee YH et al (2023) Hypomethylation in MTNR1B: a novel epigenetic marker for atherosclerosis profiling using stenosis radiophenotype and blood inflammatory cells. Clin Epigenetics 15(1):11. https://doi.org/10.1186/s13148-023-01423-x
doi: 10.1186/s13148-023-01423-x
pubmed: 36658621
pmcid: 9854223
Koerner MV, Pauler FM, Huang R et al (2009) The function of non-coding RNAs in genomic imprinting. Development 136(11):1771–1783. https://doi.org/10.1242/dev.030403
doi: 10.1242/dev.030403
pubmed: 19429783
Lauriat TL, Dracheva S, Kremerskothen J et al (2006) Characterization of KIAA0513, a novel signaling molecule that interacts with modulators of neuroplasticity, apoptosis, and the cytoskeleton. Brain Res 1121(1):1–11. https://doi.org/10.1016/j.brainres.2006.08.099
doi: 10.1016/j.brainres.2006.08.099
pubmed: 17010949
Luedi PP, Dietrich FS, Weidman JR, Bosko JM, Jirtle RL, Hartemink AJ (2007) Computational and experimental identification of novel human imprinted genes. Genome Res 17(12):1723–1730. https://doi.org/10.1101/gr.6584707
doi: 10.1101/gr.6584707
pubmed: 18055845
pmcid: 2099581
Macartney-Coxson D, Benton MC, Blick R et al (2017) Genome-wide DNA methylation analysis reveals loci that distinguish different types of adipose tissue in obese individuals. Clin Epigenetics 9:48. https://doi.org/10.1186/s13148-017-0344-4
doi: 10.1186/s13148-017-0344-4
pubmed: 28473875
pmcid: 5415776
Morison IM, Paton CJ, Cleverley SD (2001) The imprinted gene and parent-of-origin effect database. Nucleic Acids Res 29(1):275–276. https://doi.org/10.1093/nar/29.1.275
doi: 10.1093/nar/29.1.275
pubmed: 11125110
pmcid: 29803
Mozaffari SV, Stein MM, Magnaye KM et al (2018) Parent of origin gene expression in a founder population identifies two new candidate imprinted genes at known imprinted regions. PLoS ONE 13(9):e0203906. https://doi.org/10.1371/journal.pone.0203906
doi: 10.1371/journal.pone.0203906
pubmed: 30204804
pmcid: 6133383
Pilvar D, Reiman M, Pilvar A et al (2019) Parent-of-origin-specific allelic expression in the human placenta is limited to established imprinted loci and it is stably maintained across pregnancy. Clin Epigenetics 11(1):94. https://doi.org/10.1186/s13148-019-0692-3
doi: 10.1186/s13148-019-0692-3
pubmed: 31242935
pmcid: 6595585
Sanchez-Delgado M, Court F, Vidal E et al (2016) Human oocyte-derived methylation differences persist in the placenta revealing widespread transient imprinting. PLoS Genet 12(11):e1006427. https://doi.org/10.1371/journal.pgen.1006427
doi: 10.1371/journal.pgen.1006427
pubmed: 27835649
pmcid: 5106035
Santoni FA, Stamoulis G, Garieri M et al (2017) Detection of imprinted genes by single-cell allele-specific gene expression. Am J Hum Genet 100(3):444–453. https://doi.org/10.1016/j.ajhg.2017.01.028
doi: 10.1016/j.ajhg.2017.01.028
pubmed: 28190458
pmcid: 5339288
Scheuvens R, Begemann M, Soellner L et al (2017) Maternal uniparental disomy of chromosome 16 [upd(16)mat]: clinical features are rather caused by (hidden) trisomy 16 mosaicism than by upd(16)mat itself. Clin Genet 92(1):45–51. https://doi.org/10.1111/cge.12958
doi: 10.1111/cge.12958
pubmed: 28032339
Schulze KV, Szafranski P, Lesmana H et al (2019) Novel parent-of-origin-specific differentially methylated loci on chromosome 16. Clin Epigenetics 11(1):60. https://doi.org/10.1186/s13148-019-0655-8
doi: 10.1186/s13148-019-0655-8
pubmed: 30961659
pmcid: 6454695
Shao Y, Li W, Zhang L et al (2022) CDH13 is a prognostic biomarker and a potential therapeutic target for patients with clear cell renal cell carcinoma. Am J Cancer Res 12(10):4520–4544
pubmed: 36381315
pmcid: 9641392
Soellner L, Begemann M, Mackay DJ et al (2017) Recent advances in imprinting disorders. Clin Genet 91(1):3–13. https://doi.org/10.1111/cge.12827
doi: 10.1111/cge.12827
pubmed: 27363536
Stelzer Y, Bar S, Bartok O et al (2015) Differentiation of human parthenogenetic pluripotent stem cells reveals multiple tissue- and isoform-specific imprinted transcripts. Cell Rep 11(2):308–320. https://doi.org/10.1016/j.celrep.2015.03.023
doi: 10.1016/j.celrep.2015.03.023
pubmed: 25843718
Wan J, Li R, Zhang Y et al (2018) Pregnancy outcome of autosomal aneuploidies other than common trisomies detected by noninvasive prenatal testing in routine clinical practice. Prenat Diagn 38(11):849–857. https://doi.org/10.1002/pd.5340
doi: 10.1002/pd.5340
pubmed: 30078205
Wang Y, Zhang L, Yang J et al (2018) CDH13 promoter methylation regulates cisplatin resistance of non-small cell lung cancer cells. Oncol Lett 16(5):5715–5722. https://doi.org/10.3892/ol.2018.9325
doi: 10.3892/ol.2018.9325
pubmed: 30344726
pmcid: 6176259
Yang J, Niu H, Huang Y et al (2016) A systematic analysis of the relationship of CDH13 promoter methylation and breast cancer risk and prognosis. PLoS ONE 11(5):e0149185. https://doi.org/10.1371/journal.pone.0149185
doi: 10.1371/journal.pone.0149185
pubmed: 27153114
pmcid: 4859545
Zhang H, Kho AT, Wu Q et al (2016) CRISPLD2 (LGL1) inhibits proinflammatory mediators in human fetal, adult, and COPD lung fibroblasts and epithelial cells. Physiol Rep 4(17):e12942. https://doi.org/10.14814/phy2.12942
doi: 10.14814/phy2.12942
pubmed: 27597766
pmcid: 5027350
Zhu M, Jia L, Li F, Jia J (2020) Identification of KIAA0513 and other hub genes associated with alzheimer disease using weighted gene coexpression network analysis. Front Genet 11:981. https://doi.org/10.3389/fgene.2020.00981
doi: 10.3389/fgene.2020.00981
pubmed: 33005179
pmcid: 7483929
Zink F, Magnusdottir DN, Magnusson OT et al (2018) Insights into imprinting from parent-of-origin phased methylomes and transcriptomes. Nat Genet 50(11):1542–1552. https://doi.org/10.1038/s41588-018-0232-7
doi: 10.1038/s41588-018-0232-7
pubmed: 30349119