The Imprinted Polycomb Group Gene Sfmbt2 is Required for Trophoblast Maintenance and Placenta Development

Overview

Journal Development

Specialty Biology

Date 2013 Oct 25

PMID 24154523

Citations 31

Authors

Kamelia Miri

Keith Latham

Barbara Panning

Zhisheng Zhong

Angela Andersen

Susannah Varmuza

Affiliations

Soon will be listed here.

Abstract

Imprinted genes play important roles in placenta development and function. Parthenogenetic embryos, deficient in paternally expressed imprinted genes, lack extra-embryonic tissues of the trophoblast lineage. Parthenogenetic trophoblast stem cells (TSCs) are extremely difficult to derive, suggesting that an imprinted gene(s) is necessary for TSC establishment or maintenance. In a candidate study, we were able to narrow the list to one known paternally expressed gene, Sfmbt2. We show that mouse embryos inheriting a paternal Sfmbt2 gene trap null allele have severely reduced placentae and die before E12.5 due to reduction of all trophoblast cell types. We infected early embryos with lentivirus vectors expressing anti-Sfmbt2 shRNAs and found that TSC derivation was significantly reduced. Together, these observations support the hypothesis that loss of SFMBT2 results in defects in maintenance of trophoblast cell types necessary for development of the extra-embryonic tissues, the placenta in particular.

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References

Lucifero D, Mann M, Bartolomei M, Trasler J . Gene-specific timing and epigenetic memory in oocyte imprinting. Hum Mol Genet. 2004; 13(8):839-49. DOI: 10.1093/hmg/ddh104. View

Wang Q, Chow J, Hong J, Smith A, Moreno C, Seaby P . Recent acquisition of imprinting at the rodent Sfmbt2 locus correlates with insertion of a large block of miRNAs. BMC Genomics. 2011; 12:204. PMC: 3110154. DOI: 10.1186/1471-2164-12-204. View

Grimm C, Matos R, Ly-Hartig N, Steuerwald U, Lindner D, Rybin V . Molecular recognition of histone lysine methylation by the Polycomb group repressor dSfmbt. EMBO J. 2009; 28(13):1965-77. PMC: 2693881. DOI: 10.1038/emboj.2009.147. View

Tiscornia G, Singer O, Verma I . Production and purification of lentiviral vectors. Nat Protoc. 2007; 1(1):241-5. DOI: 10.1038/nprot.2006.37. View

Rivera R, Stein P, Weaver J, Mager J, Schultz R, Bartolomei M . Manipulations of mouse embryos prior to implantation result in aberrant expression of imprinted genes on day 9.5 of development. Hum Mol Genet. 2007; 17(1):1-14. DOI: 10.1093/hmg/ddm280. View

Clarke H, Varmuza S, Prideaux V, Rossant J . The development potential of parthenogenetically derived cells in chimeric mouse embryos: implications for action of imprinted genes. Development. 1988; 104(1):175-82. DOI: 10.1242/dev.104.1.175. View

Goldberg A, Allis C, Bernstein E . Epigenetics: a landscape takes shape. Cell. 2007; 128(4):635-8. DOI: 10.1016/j.cell.2007.02.006. View

Park I, Qian D, Kiel M, Becker M, Pihalja M, Weissman I . Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature. 2003; 423(6937):302-5. DOI: 10.1038/nature01587. View

Nesterova T, Barton S, Surani M, Brockdorff N . Loss of Xist imprinting in diploid parthenogenetic preimplantation embryos. Dev Biol. 2001; 235(2):343-50. DOI: 10.1006/dbio.2001.0295. View

10.

Hancock D, OReilly N . Production of polyclonal antibodies in rabbits. Methods Mol Biol. 2004; 295:27-40. View

11.

Georgiades P, Cox B, Gertsenstein M, Chawengsaksophak K, Rossant J . Trophoblast-specific gene manipulation using lentivirus-based vectors. Biotechniques. 2007; 42(3):317-8, 320, 322-5. DOI: 10.2144/000112341. View

12.

Okae H, Hiura H, Nishida Y, Funayama R, Tanaka S, Chiba H . Re-investigation and RNA sequencing-based identification of genes with placenta-specific imprinted expression. Hum Mol Genet. 2011; 21(3):548-58. DOI: 10.1093/hmg/ddr488. View

13.

Renfree M, Ager E, Shaw G, Pask A . Genomic imprinting in marsupial placentation. Reproduction. 2008; 136(5):523-31. DOI: 10.1530/REP-08-0264. View

14.

Lefebvre L . The placental imprintome and imprinted gene function in the trophoblast glycogen cell lineage. Reprod Biomed Online. 2012; 25(1):44-57. PMC: 3819294. DOI: 10.1016/j.rbmo.2012.03.019. View

15.

Kuzmin A, Han Z, Golding M, Mann M, Latham K, Varmuza S . The PcG gene Sfmbt2 is paternally expressed in extraembryonic tissues. Gene Expr Patterns. 2007; 8(2):107-16. PMC: 2220043. DOI: 10.1016/j.modgep.2007.09.005. View

16.

Pfaffl M, Horgan G, Dempfle L . Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002; 30(9):e36. PMC: 113859. DOI: 10.1093/nar/30.9.e36. View

17.

Zeigler B, Sugiyama D, Chen M, Guo Y, Downs K, Speck N . The allantois and chorion, when isolated before circulation or chorio-allantoic fusion, have hematopoietic potential. Development. 2006; 133(21):4183-92. DOI: 10.1242/dev.02596. View

18.

Chuva de Sousa Lopes S, Hayashi K, Surani M . Proximal visceral endoderm and extraembryonic ectoderm regulate the formation of primordial germ cell precursors. BMC Dev Biol. 2007; 7:140. PMC: 2231376. DOI: 10.1186/1471-213X-7-140. View

19.

Ono R, Nakamura K, Inoue K, Naruse M, Usami T, Wakisaka-Saito N . Deletion of Peg10, an imprinted gene acquired from a retrotransposon, causes early embryonic lethality. Nat Genet. 2005; 38(1):101-6. DOI: 10.1038/ng1699. View

20.

Davis T, Yang G, McCarrey J, Bartolomei M . The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum Mol Genet. 2000; 9(19):2885-94. DOI: 10.1093/hmg/9.19.2885. View