SMARCAD1 Contributes to the Regulation of Naive Pluripotency by Interacting with Histone Citrullination
Histone citrullination regulates diverse cellular processes. Here, we report that SMARCAD1 preferentially associates with H3 arginine 26 citrullination (H3R26Cit) peptides present on arrays composed of 384 histone peptides harboring distinct post-transcriptional modifications. Among ten histone modi...
| Main Authors: | , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2017-03-01
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| Series: | Cell Reports |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124717302887 |
| _version_ | 1828232199511474176 |
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| author | Shu Xiao Jia Lu Bharat Sridhar Xiaoyi Cao Pengfei Yu Tianyi Zhao Chieh-Chun Chen Darina McDee Laura Sloofman Yang Wang Marcelo Rivas-Astroza Bhanu Prakash V.L. Telugu Dana Levasseur Kang Zhang Han Liang Jing Crystal Zhao Tetsuya S. Tanaka Gary Stormo Sheng Zhong |
| author_facet | Shu Xiao Jia Lu Bharat Sridhar Xiaoyi Cao Pengfei Yu Tianyi Zhao Chieh-Chun Chen Darina McDee Laura Sloofman Yang Wang Marcelo Rivas-Astroza Bhanu Prakash V.L. Telugu Dana Levasseur Kang Zhang Han Liang Jing Crystal Zhao Tetsuya S. Tanaka Gary Stormo Sheng Zhong |
| author_sort | Shu Xiao |
| collection | DOAJ |
| description | Histone citrullination regulates diverse cellular processes. Here, we report that SMARCAD1 preferentially associates with H3 arginine 26 citrullination (H3R26Cit) peptides present on arrays composed of 384 histone peptides harboring distinct post-transcriptional modifications. Among ten histone modifications assayed by ChIP-seq, H3R26Cit exhibited the most extensive genomewide co-localization with SMARCAD1 binding. Increased Smarcad1 expression correlated with naive pluripotency in pre-implantation embryos. In the presence of LIF, Smarcad1 knockdown (KD) embryonic stem cells lost naive state phenotypes but remained pluripotent, as suggested by morphology, gene expression, histone modifications, alkaline phosphatase activity, energy metabolism, embryoid bodies, teratoma, and chimeras. The majority of H3R26Cit ChIP-seq peaks occupied by SMARCAD1 were associated with increased levels of H3K9me3 in Smarcad1 KD cells. Inhibition of H3Cit induced H3K9me3 at the overlapping regions of H3R26Cit peaks and SMARCAD1 peaks. These data suggest a model in which SMARCAD1 regulates naive pluripotency by interacting with H3R26Cit and suppressing heterochromatin formation. |
| first_indexed | 2024-04-12T19:17:32Z |
| format | Article |
| id | doaj.art-cd54b011fbc948e1ac2812682ba0b960 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-04-12T19:17:32Z |
| publishDate | 2017-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-cd54b011fbc948e1ac2812682ba0b9602022-12-22T03:19:42ZengElsevierCell Reports2211-12472017-03-0118133117312810.1016/j.celrep.2017.02.070SMARCAD1 Contributes to the Regulation of Naive Pluripotency by Interacting with Histone CitrullinationShu Xiao0Jia Lu1Bharat Sridhar2Xiaoyi Cao3Pengfei Yu4Tianyi Zhao5Chieh-Chun Chen6Darina McDee7Laura Sloofman8Yang Wang9Marcelo Rivas-Astroza10Bhanu Prakash V.L. Telugu11Dana Levasseur12Kang Zhang13Han Liang14Jing Crystal Zhao15Tetsuya S. Tanaka16Gary Stormo17Sheng Zhong18Department of Bioengineering, University of California, San Diego, La Jolla, CA 92093, USADepartment of Bioengineering, University of California, San Diego, La Jolla, CA 92093, USADepartment of Bioengineering, University of California, San Diego, La Jolla, CA 92093, USADepartment of Bioengineering, University of California, San Diego, La Jolla, CA 92093, USADepartment of Bioengineering, University of California, San Diego, La Jolla, CA 92093, USADepartment of Bioengineering, University of California, San Diego, La Jolla, CA 92093, USAInstitute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USADepartment of Bioengineering, University of California, San Diego, La Jolla, CA 92093, USAInstitute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USASanford Burnham Prebys Medical Discovery Institute, La Jolla, CA 92037, USADepartment of Bioengineering, University of California, San Diego, La Jolla, CA 92093, USADepartment of Animal and Avian Sciences, University of Maryland, College Park, MD 20742, USADepartment of Internal Medicine, Carver College of Medicine, University of Iowa, Iowa City, IA 52242, USADepartment of Ophthalmology, University of California, San Diego, La Jolla, CA 92093, USADepartment of Bioinformatics and Computational Biology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USASanford Burnham Prebys Medical Discovery Institute, La Jolla, CA 92037, USAInstitute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USADepartment of Genetics, Washington University at St. Louis, St. Louis, MO 63108, USADepartment of Bioengineering, University of California, San Diego, La Jolla, CA 92093, USAHistone citrullination regulates diverse cellular processes. Here, we report that SMARCAD1 preferentially associates with H3 arginine 26 citrullination (H3R26Cit) peptides present on arrays composed of 384 histone peptides harboring distinct post-transcriptional modifications. Among ten histone modifications assayed by ChIP-seq, H3R26Cit exhibited the most extensive genomewide co-localization with SMARCAD1 binding. Increased Smarcad1 expression correlated with naive pluripotency in pre-implantation embryos. In the presence of LIF, Smarcad1 knockdown (KD) embryonic stem cells lost naive state phenotypes but remained pluripotent, as suggested by morphology, gene expression, histone modifications, alkaline phosphatase activity, energy metabolism, embryoid bodies, teratoma, and chimeras. The majority of H3R26Cit ChIP-seq peaks occupied by SMARCAD1 were associated with increased levels of H3K9me3 in Smarcad1 KD cells. Inhibition of H3Cit induced H3K9me3 at the overlapping regions of H3R26Cit peaks and SMARCAD1 peaks. These data suggest a model in which SMARCAD1 regulates naive pluripotency by interacting with H3R26Cit and suppressing heterochromatin formation.http://www.sciencedirect.com/science/article/pii/S2211124717302887SMARCAD1histone modificationcitrullinationstem cellsnaive statepluripotencyChIP-seqprotein array |
| spellingShingle | Shu Xiao Jia Lu Bharat Sridhar Xiaoyi Cao Pengfei Yu Tianyi Zhao Chieh-Chun Chen Darina McDee Laura Sloofman Yang Wang Marcelo Rivas-Astroza Bhanu Prakash V.L. Telugu Dana Levasseur Kang Zhang Han Liang Jing Crystal Zhao Tetsuya S. Tanaka Gary Stormo Sheng Zhong SMARCAD1 Contributes to the Regulation of Naive Pluripotency by Interacting with Histone Citrullination Cell Reports SMARCAD1 histone modification citrullination stem cells naive state pluripotency ChIP-seq protein array |
| title | SMARCAD1 Contributes to the Regulation of Naive Pluripotency by Interacting with Histone Citrullination |
| title_full | SMARCAD1 Contributes to the Regulation of Naive Pluripotency by Interacting with Histone Citrullination |
| title_fullStr | SMARCAD1 Contributes to the Regulation of Naive Pluripotency by Interacting with Histone Citrullination |
| title_full_unstemmed | SMARCAD1 Contributes to the Regulation of Naive Pluripotency by Interacting with Histone Citrullination |
| title_short | SMARCAD1 Contributes to the Regulation of Naive Pluripotency by Interacting with Histone Citrullination |
| title_sort | smarcad1 contributes to the regulation of naive pluripotency by interacting with histone citrullination |
| topic | SMARCAD1 histone modification citrullination stem cells naive state pluripotency ChIP-seq protein array |
| url | http://www.sciencedirect.com/science/article/pii/S2211124717302887 |
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