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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Depletion of SMARCB1 and BRD7, two SWI/SNF chromatin remodelling complex subunits, differentially impact porcine embryo development

Yu-Chun Tseng A , Jennifer S. Crodian A and Ryan Cabot https://orcid.org/0000-0002-4790-9655 A *
+ Author Affiliations
- Author Affiliations

A Department of Animal Sciences, Purdue University, 270 South Russell Street, West Lafayette, IN 47907, USA.

* Correspondence to: rcabot@purdue.edu

Handling Editor: Ye Yuan

Reproduction, Fertility and Development 34(7) 549-559 https://doi.org/10.1071/RD21251
Published online: 17 March 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: SWI/SNF chromatin remodelling complexes are composed of multiple protein subunits and can be categorised into three sub-families, including the BAF, PBAF, and GBAF complexes. We hypothesised that depletion of SMARCB1 and BRD7, two subunits unique to different SWI/SNF sub-families, would differentially impact porcine embryo development.

Aim: The aim of these experiments was to determine the developmental requirements of two SWI/SNF subunits, SMARCB1 and BRD7.

Methods: RNA interference assays were used to determine the developmental requirements of SMARCB1 and BRD7 in porcine embryos.

Key results: Our findings indicate that knockdown of SMARCB1 dramatically reduces embryo developmental potential, with few embryos developing beyond the pronuclear stage. The knockdown of BRD7 had a less severe impact on developmental potential.

Conclusions: Our findings also demonstrate that knockdown of SMARCB1 alters the expression of NANOG and POU5F1 (also referred to as OCT4).

Implications: These findings highlight the unique developmental requirements for sub-families of SWI/SNF chromatin remodelling complexes. This new knowledge will enable us to determine how discrete genomic loci are differentially remodelled during key points in embryo development.

Keywords: BRD7, bromodomain, chromatin remodelling, embryo, epigenetics, SMARCB1, SNF5, SWI/SNF.


References

Abeydeera, LR, and Day, BN (1997). Fertilization and subsequent development in vitro of pig oocytes inseminated in a modified tris-buffered medium with frozen-thawed ejaculated spermatozoa. Biology of Reproduction 57, 729–734.
Fertilization and subsequent development in vitro of pig oocytes inseminated in a modified tris-buffered medium with frozen-thawed ejaculated spermatozoa.Crossref | GoogleScholarGoogle Scholar | 9314573PubMed |

Abeydeera, LR, Wang, WH, Prather, RS, and Day, BN (1998). Maturation in vitro of pig oocytes in protein-free media: fertilization and subsequent embryo development in vitro. Biology of Reproduction 58, 1316–1320.
Maturation in vitro of pig oocytes in protein-free media: fertilization and subsequent embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 9603270PubMed |

Alpsoy, A, and Dykhuizen, EC (2018). Glioma tumor suppressor candidate region gene 1 (GLTSCR1) and its paralog GLTSCR1-like form SWI/SNF chromatin remodeling subcomplexes. Journal of Biological Chemistry 293, 3892–3903.
Glioma tumor suppressor candidate region gene 1 (GLTSCR1) and its paralog GLTSCR1-like form SWI/SNF chromatin remodeling subcomplexes.Crossref | GoogleScholarGoogle Scholar |

Anderson, JE, Matteri, RL, Abeydeera, LR, Day, BN, and Prather, RS (1999). Cyclin B1 transcript quantitation over the maternal to zygotic transition in both in vivo- and in vitro-derived 4-cell porcine embryos. Biology of Reproduction 61, 1460–1467.
Cyclin B1 transcript quantitation over the maternal to zygotic transition in both in vivo- and in vitro-derived 4-cell porcine embryos.Crossref | GoogleScholarGoogle Scholar | 10569990PubMed |

Cabot, B, Tseng, YC, Crodian, JS, and Cabot, RA (2017). Differential expression of key subunits of SWI/SNF chromatin remodeling complexes in porcine embryos derived in vitro or in vivo. Molecular Reproduction and Development 84, 1238–1249.
Differential expression of key subunits of SWI/SNF chromatin remodeling complexes in porcine embryos derived in vitro or in vivo.Crossref | GoogleScholarGoogle Scholar | 29024220PubMed |

Chambers, I, Colby, D, Robertson, M, Nichols, J, Lee, S, Tweedie, S, and Smith, A (2003). Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113, 643–655.
Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 12787505PubMed |

Clapier, CR, and Cairns, BR (2009). The biology of chromatin remodeling complexes. Annual Review of Biochemistry 78, 273–304.
The biology of chromatin remodeling complexes.Crossref | GoogleScholarGoogle Scholar | 19355820PubMed |

Crodian, JS, Weldon, BM, Tseng, Y-C, Cabot, B, and Cabot, R (2019). Nuclear trafficking dynamics of Bromodomain-containing protein 7 (BRD7), a switch/sucrose non-fermentable (SWI/SNF) chromatin remodelling complex subunit, in porcine oocytes and cleavage-stage embryos. Reproduction, Fertility and Development 31, 1497–1506.
Nuclear trafficking dynamics of Bromodomain-containing protein 7 (BRD7), a switch/sucrose non-fermentable (SWI/SNF) chromatin remodelling complex subunit, in porcine oocytes and cleavage-stage embryos.Crossref | GoogleScholarGoogle Scholar |

Davis, DL (1985). Culture and storage of pig embryos. Journal of Reproduction and Fertility. Supplements 33, 115–124.

Euskirchen, G, Auerbach, RK, and Snyder, M (2012). SWI/SNF chromatin-remodeling factors: multiscale analyses and diverse functions. Journal of Biological Chemistry 287, 30897–30905.
SWI/SNF chromatin-remodeling factors: multiscale analyses and diverse functions.Crossref | GoogleScholarGoogle Scholar |

Fulka, J, Fulka, H, Slavik, T, and Okada, K (2006). DNA methylation pattern in pig in vivo produced embryos. Histochemistry and Cell Biology 126, 213–217.
DNA methylation pattern in pig in vivo produced embryos.Crossref | GoogleScholarGoogle Scholar | 16435122PubMed |

Gatchalian, J, Malik, S, Ho, J, Lee, DS, Kelso, TWR, Shokhirev, MN, Dixon, JR, and Hargreaves, DC (2018). A non-canonical BRD9-containing BAF chromatin remodeling comples regulates naive pluripotency in mouse embryonic stem cells. Nature Communications 9, 5139.
A non-canonical BRD9-containing BAF chromatin remodeling comples regulates naive pluripotency in mouse embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 30510198PubMed |

Guidi, CJ, Sands, AT, Zambrowicz, BP, Turner, TK, Demers, DA, Webster, W, Smith, TW, Imbalzano, AN, and Jones, SN (2001). Disruption of Ini1 leads to peri-implantation lethality and tumorigenesis in mice. Molecular and Cellular Biology 21, 3598–3603.
Disruption of Ini1 leads to peri-implantation lethality and tumorigenesis in mice.Crossref | GoogleScholarGoogle Scholar | 11313485PubMed |

Hochedlinger, K, and Plath, K (2009). Epigenetic reprogramming and induced pluripotency. Development 136, 509–523.
Epigenetic reprogramming and induced pluripotency.Crossref | GoogleScholarGoogle Scholar | 19168672PubMed |

Isakoff, MS, Sansam, CG, Tamayo, P, Subramanian, A, Evans, JA, and Fillmore, CM (2005). Inactivation of the Snf5 tumor suppressor stimulates cell cycle progression and cooperates with p53 loss in oncogenic transformation. Proceedings of the National Academy of Sciences of the United States of America 102, 17745–17750.
Inactivation of the Snf5 tumor suppressor stimulates cell cycle progression and cooperates with p53 loss in oncogenic transformation.Crossref | GoogleScholarGoogle Scholar | 16301525PubMed |

Kim, Y, Andrés Salazar Hernández, M, Herrema, H, Delibasi, T, and Park, SW (2016). The role of BRD7 in embryo development and glucose metabolism. Journal of Cellular and Molecular Medicine 20, 1561–1570.
The role of BRD7 in embryo development and glucose metabolism.Crossref | GoogleScholarGoogle Scholar | 27444544PubMed |

Klochendler-Yeivin, A, Fiette, L, Barra, J, Muchardt, C, Babinet, C, and Yaniv, M (2000). The murine SNF5/INI1 chromatin remodeling factor is essential for embryonic development and tumor suppression. EMBO Reports 1, 500–506.
The murine SNF5/INI1 chromatin remodeling factor is essential for embryonic development and tumor suppression.Crossref | GoogleScholarGoogle Scholar | 11263494PubMed |

Kuwahara, Y, Wei, D, Durand, J, and Weissman, BE (2013). SNF5 reexpression in malignant rhabdoid tumors regulates transcription of target genes by recruitment of SWI/SNF complexes and RNAPII to the transcription start site of their promoters. Molecular Cancer Research 11, 251–260.
SNF5 reexpression in malignant rhabdoid tumors regulates transcription of target genes by recruitment of SWI/SNF complexes and RNAPII to the transcription start site of their promoters.Crossref | GoogleScholarGoogle Scholar | 23364536PubMed |

Lonergan, P, Rizos, D, Gutiérrez-Adán, A, Fair, T, and Boland, MP (2003). Effect of culture environment on embryo quality and gene expression-experience from animal studies. Reproductive BioMedicine Online 7, 657–663.
Effect of culture environment on embryo quality and gene expression-experience from animal studies.Crossref | GoogleScholarGoogle Scholar | 14748964PubMed |

Magnani, L, and Cabot, RA (2008). In vitro and in vivo derived porcine embryos possess similar, but not identical, patterns of Oct4, Nanog, and Sox2 mRNA expression during cleavage development. Molecular Reproduction and Development 75, 1726–1735.
In vitro and in vivo derived porcine embryos possess similar, but not identical, patterns of Oct4, Nanog, and Sox2 mRNA expression during cleavage development.Crossref | GoogleScholarGoogle Scholar | 18425776PubMed |

Magnani, L, and Cabot, RA (2009). Manipulation of SMARCA2 and SMARCA4 transcript levels in porcine embryos differentially alters development and expression of SMARCA1, SOX2, NANOG, and EIF1. Reproduction 137, 23–33.
Manipulation of SMARCA2 and SMARCA4 transcript levels in porcine embryos differentially alters development and expression of SMARCA1, SOX2, NANOG, and EIF1.Crossref | GoogleScholarGoogle Scholar | 18845624PubMed |

Mitsui, K, Tokuzawa, Y, Itoh, H, Segawa, K, Murakami, M, Takahashi, K, Maruyama, M, Maeda, M, and Yamanaka, S (2003). The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113, 631–642.
The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells.Crossref | GoogleScholarGoogle Scholar | 12787504PubMed |

Monk, M, Boubelik, M, and Lehnert, S (1987). Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development 99, 371–382.
Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development.Crossref | GoogleScholarGoogle Scholar | 3653008PubMed |

Nagy, Z, and Tora, L (2007). Distinct GCN5/PCAF-containing complexes function as co-activators and are involved in transcription factor and global histone acetylation. Oncogene 26, 5341–5357.
Distinct GCN5/PCAF-containing complexes function as co-activators and are involved in transcription factor and global histone acetylation.Crossref | GoogleScholarGoogle Scholar | 17694077PubMed |

Nichols, J, Zevnik, B, Anastassiadis, K, Niwa, H, Klewe-Nebenius, D, Chambers, I, Schöler, H, and Smith, A (1998). Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379–391.
Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4.Crossref | GoogleScholarGoogle Scholar | 9814708PubMed |

Niwa, H, Miyazaki, J-I, and Smith, AG (2000). Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature Genetics 24, 372–376.
Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells.Crossref | GoogleScholarGoogle Scholar | 10742100PubMed |

Peng, C, Liu, HY, Zhou, M, Zhang, LM, Li, XL, Shen, SR, and Li, GY (2007). BRD7 suppresses the growth of Nasopharyngeal Carcinoma cells (HNE1) through negatively regulating beta-catenin and ERK pathways. Molecular and Cellular Biochemistry 303, 141–149.
BRD7 suppresses the growth of Nasopharyngeal Carcinoma cells (HNE1) through negatively regulating beta-catenin and ERK pathways.Crossref | GoogleScholarGoogle Scholar | 17458518PubMed |

Peterson, CL, Dingwall, A, and Scott, MP (1994). Five SWI/SNF gene products are components of a large multisubunit complex required for transcriptional enhancement. Proceedings of the National Academy of Sciences of the United States of America 91, 2905–2908.
Five SWI/SNF gene products are components of a large multisubunit complex required for transcriptional enhancement.Crossref | GoogleScholarGoogle Scholar | 8159677PubMed |

Prather, RS, and Rickords, LF (1992). Developmental regulation of a snRNP core protein epitope during pig embryogenesis and after nuclear transfer for cloning. Molecular Reproduction and Development 33, 119–123.
Developmental regulation of a snRNP core protein epitope during pig embryogenesis and after nuclear transfer for cloning.Crossref | GoogleScholarGoogle Scholar | 1384573PubMed |

Roberts, CW, and Biegel, JA (2009). The role of SMARCB1/INI1 in development of rhabdoid tumor. Cancer Biology & Therapy 8, 412–416.
The role of SMARCB1/INI1 in development of rhabdoid tumor.Crossref | GoogleScholarGoogle Scholar |

Roberts, CW, Galusha, SA, McMenamin, ME, Fletcher, CD, and Orkin, SH (2000). Haploinsufficiency of Snf5 (integrase interactor 1) predisposes to malignant rhabdoid tumors in mice. Proceedings of the National Academy of Sciences of the United States of America 97, 13796–13800.
Haploinsufficiency of Snf5 (integrase interactor 1) predisposes to malignant rhabdoid tumors in mice.Crossref | GoogleScholarGoogle Scholar | 11095756PubMed |

Roberts, CW, Leroux, MM, Fleming, MD, and Orkin, SH (2002). Highly penetrant, rapid tumorigenesis through conditional inversion of the tumor suppressor gene Snf5. Cancer Cell 2, 415–425.
Highly penetrant, rapid tumorigenesis through conditional inversion of the tumor suppressor gene Snf5.Crossref | GoogleScholarGoogle Scholar | 12450796PubMed |

Sohn, DH, Lee, KY, Lee, C, Oh, J, Chung, H, Jeon, SH, and Seong, RH (2007). SRG3 interacts directly with the major components of the SWI/SNF chromatin remodeling complex and protects them from proteasomal degradation. Journal of Biological Chemistry 282, 10614–10624.
SRG3 interacts directly with the major components of the SWI/SNF chromatin remodeling complex and protects them from proteasomal degradation.Crossref | GoogleScholarGoogle Scholar |

Tae, S, Karkhanis, V, Velasco, K, Yaneva, M, Erdjument-Bromage, H, Tempst, P, and Sif, S (2011). Bromodomain protein 7 interacts with PRMT5 and PRC2, and is involved in transcriptional repression of their target genes. Nucleic Acids Research 39, 5424–5438.
Bromodomain protein 7 interacts with PRMT5 and PRC2, and is involved in transcriptional repression of their target genes.Crossref | GoogleScholarGoogle Scholar | 21447565PubMed |

Teif, VB, and Rippe, K (2009). Predicting nucleosome positions on the DNA: combining intrinsic sequence preferences and remodeler activities. Nucleic Acids Research 37, 5641–5655.
Predicting nucleosome positions on the DNA: combining intrinsic sequence preferences and remodeler activities.Crossref | GoogleScholarGoogle Scholar | 19625488PubMed |

Telford, NA, Watson, AJ, and Schultz, GA (1990). Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Molecular Reproduction and Development 26, 90–100.
Transition from maternal to embryonic control in early mammalian development: a comparison of several species.Crossref | GoogleScholarGoogle Scholar | 2189447PubMed |

Tseng, YC, Cabot, B, and Cabot, RA (2017). ARID1A, a component of SWI/SNF chromatin remodeling complexes, is required for porcine embryo development. Molecular Reproduction and Development 84, 1250–1256.
ARID1A, a component of SWI/SNF chromatin remodeling complexes, is required for porcine embryo development.Crossref | GoogleScholarGoogle Scholar | 29178559PubMed |

van der Weijden, V, Schmidhauser, M, Kurome, M, Knubben, J, Flöter, VL, Wolf, E, and Ulbrich, SE (2021). Transcriptome dymanics in early in vivo developing in vitro produced porcine embryos. BCM Genomics 22, 139.
Transcriptome dymanics in early in vivo developing in vitro produced porcine embryos.Crossref | GoogleScholarGoogle Scholar |

Whitworth, KM, Agca, C, Kim, JG, Patel, RV, Springer, GK, Bivens, NJ, Forrester, LJ, Mathialagan, N, Green, JA, and Prather, RS (2005). Transcriptional profiling of pig embryogenesis by using a 15-K member unigene set specific for pig reproductive tissues and embryos. Biology of Reproduction 72, 1437–1451.
Transcriptional profiling of pig embryogenesis by using a 15-K member unigene set specific for pig reproductive tissues and embryos.Crossref | GoogleScholarGoogle Scholar | 15703372PubMed |

Yan, Z, Xie, S, Du, Y, and Qian, C (2017). Structural insights into BAF47 and BAF 155 complex formation. Journal of Molecular Biology 429, 1650–1660.
Structural insights into BAF47 and BAF 155 complex formation.Crossref | GoogleScholarGoogle Scholar |

Yoshioka, K, Suzuki, C, Tanaka, A, Anas, IM-K, and Iwamura, S (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biology of Reproduction 66, 112–119.
Birth of piglets derived from porcine zygotes cultured in a chemically defined medium.Crossref | GoogleScholarGoogle Scholar | 11751272PubMed |

You, JS, De Carvalho, DD, Dai, C, Liu, M, Pandiyan, K, and Zhou, XJ (2013). SNF5 is an essential executor of epigenetic regulation during differentiation. PLoS Genetics 9, 1003459.
SNF5 is an essential executor of epigenetic regulation during differentiation.Crossref | GoogleScholarGoogle Scholar |

Yu, X, Li, Z, and Shen, J (2016). BRD7: a novel tumor suppressor gene in different cancers. American Journal of Translational Research 8, 742–748.
| 27158366PubMed |

Yuan, Y, Spate, LD, Redel, BK, Tian, Y, Zhou, J, and Prather, RS (2017). Quadrupling efficiency in production of genetically modified pigs through improved oocyte maturation. Proceedings of the National Academy of Sciences of the United States of America 114, 5796–5804.
Quadrupling efficiency in production of genetically modified pigs through improved oocyte maturation.Crossref | GoogleScholarGoogle Scholar |