Literature DB >> 27111767

Epigenetic Reprogramming in Naive CD4+ T Cells Favoring T Cell Activation and Non-Th1 Effector T Cell Immune Response as an Early Event in Lupus Flares.

Patrick Coit1, Mikhail G Dozmorov2, Joan T Merrill3, W Joseph McCune1, Kathleen Maksimowicz-McKinnon4, Jonathan D Wren5, Amr H Sawalha1.   

Abstract

OBJECTIVE: Systemic lupus erythematosus (SLE) is a relapsing autoimmune disease that affects multiple organ systems. T cells play an important role in the pathogenesis of lupus; however, early T cell events triggering disease flares are incompletely understood. This study was undertaken to examine DNA methylation in naive CD4+ T cells from lupus patients to determine if epigenetic remodeling in CD4+ T cells is an early event in lupus flares.
METHODS: A total of 74 lupus patients with an SLE Disease Activity Index score of 0-18 were included. Naive CD4+ T cells were isolated from peripheral blood samples, and DNA was extracted for genome-wide methylation assessment. RNA was also extracted from a subset of patients to determine the relationship between epigenetic changes and transcription activity using RNA sequencing and microRNA arrays.
RESULTS: We demonstrated that naive CD4+ T cells in lupus undergo an epigenetic proinflammatory shift, implicating effector T cell responses in lupus flare. This epigenetic landscape change occurs without changes in expression of the corresponding genes, poises naive CD4+ T cells for Th2, Th17, and follicular helper T cell immune responses, and opposes inhibitory transforming growth factor β signaling. Bioinformatics analyses indicate that the epigenetic modulator EZH2 might play an important role in shifting the epigenetic landscape, with increased disease activity in lupus naive CD4+ T cells. Further, the expression of microRNA-26a, which is sensitive to glucose availability and targets EZH2, was negatively correlated with disease activity in lupus patients.
CONCLUSION: An epigenetic landscape shift in naive CD4+ T cells that favors T cell activation and non-Th1 immune responses predates transcription activity and correlates with lupus activity. A role for EZH2 dysregulation in triggering lupus flares warrants further investigation.
© 2016, American College of Rheumatology.

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Year:  2016        PMID: 27111767      PMCID: PMC5001909          DOI: 10.1002/art.39720

Source DB:  PubMed          Journal:  Arthritis Rheumatol        ISSN: 2326-5191            Impact factor:   10.995


  31 in total

1.  The polycomb protein Ezh2 regulates differentiation and plasticity of CD4(+) T helper type 1 and type 2 cells.

Authors:  Damon J Tumes; Atsushi Onodera; Akane Suzuki; Kenta Shinoda; Yusuke Endo; Chiaki Iwamura; Hiroyuki Hosokawa; Haruhiko Koseki; Koji Tokoyoda; Yutaka Suzuki; Shinichiro Motohashi; Toshinori Nakayama
Journal:  Immunity       Date:  2013-11-14       Impact factor: 31.745

2.  Ezh2 regulates transcriptional and posttranslational expression of T-bet and promotes Th1 cell responses mediating aplastic anemia in mice.

Authors:  Qing Tong; Shan He; Fang Xie; Kazuhiro Mochizuki; Yongnian Liu; Izumi Mochizuki; Lijun Meng; Hongxing Sun; Yanyun Zhang; Yajun Guo; Elizabeth Hexner; Yi Zhang
Journal:  J Immunol       Date:  2014-04-23       Impact factor: 5.422

3.  Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus.

Authors:  M C Hochberg
Journal:  Arthritis Rheum       Date:  1997-09

4.  Renal involvement in lupus is characterized by unique DNA methylation changes in naïve CD4+ T cells.

Authors:  Patrick Coit; Paul Renauer; Matlock A Jeffries; Joan T Merrill; W Joseph McCune; Kathleen Maksimowicz-McKinnon; Amr H Sawalha
Journal:  J Autoimmun       Date:  2015-05-23       Impact factor: 7.094

5.  Genome-wide DNA methylation study suggests epigenetic accessibility and transcriptional poising of interferon-regulated genes in naïve CD4+ T cells from lupus patients.

Authors:  Patrick Coit; Matlock Jeffries; Nezam Altorok; Mikhail G Dozmorov; Kristi A Koelsch; Jonathan D Wren; Joan T Merrill; W Joseph McCune; Amr H Sawalha
Journal:  J Autoimmun       Date:  2013-04-24       Impact factor: 7.094

Review 6.  T cell signaling abnormalities contribute to aberrant immune cell function and autoimmunity.

Authors:  Vaishali R Moulton; George C Tsokos
Journal:  J Clin Invest       Date:  2015-05-11       Impact factor: 14.808

Review 7.  Autoimmune disease in the epigenetic era: how has epigenetics changed our understanding of disease and how can we expect the field to evolve?

Authors:  Matlock A Jeffries; Amr H Sawalha
Journal:  Expert Rev Clin Immunol       Date:  2015-01       Impact factor: 4.473

8.  The Polycomb group protein EZH2 directly controls DNA methylation.

Authors:  Emmanuelle Viré; Carmen Brenner; Rachel Deplus; Loïc Blanchon; Mario Fraga; Céline Didelot; Lluis Morey; Aleyde Van Eynde; David Bernard; Jean-Marie Vanderwinden; Mathieu Bollen; Manel Esteller; Luciano Di Croce; Yvan de Launoit; François Fuks
Journal:  Nature       Date:  2005-12-14       Impact factor: 49.962

9.  EZH2 is crucial for both differentiation of regulatory T cells and T effector cell expansion.

Authors:  Xiang-Ping Yang; Kan Jiang; Kiyoshi Hirahara; Golnaz Vahedi; Behdad Afzali; Giuseppe Sciume; Michael Bonelli; Hong-Wei Sun; Dragana Jankovic; Yuka Kanno; Vittorio Sartorelli; John J O'Shea; Arian Laurence
Journal:  Sci Rep       Date:  2015-06-19       Impact factor: 4.379

10.  High-density genotyping of immune-related loci identifies new SLE risk variants in individuals with Asian ancestry.

Authors:  Celi Sun; Julio E Molineros; Loren L Looger; Xu-Jie Zhou; Kwangwoo Kim; Yukinori Okada; Jianyang Ma; Yuan-Yuan Qi; Xana Kim-Howard; Prasenjeet Motghare; Krishna Bhattarai; Adam Adler; So-Young Bang; Hye-Soon Lee; Tae-Hwan Kim; Young Mo Kang; Chang-Hee Suh; Won Tae Chung; Yong-Beom Park; Jung-Yoon Choe; Seung Cheol Shim; Yuta Kochi; Akari Suzuki; Michiaki Kubo; Takayuki Sumida; Kazuhiko Yamamoto; Shin-Seok Lee; Young Jin Kim; Bok-Ghee Han; Mikhail Dozmorov; Kenneth M Kaufman; Jonathan D Wren; John B Harley; Nan Shen; Kek Heng Chua; Hong Zhang; Sang-Cheol Bae; Swapan K Nath
Journal:  Nat Genet       Date:  2016-01-25       Impact factor: 38.330

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  29 in total

1.  Coronavirus Disease-2019: Implication for the care and management of patients with systemic lupus erythematosus.

Authors:  Amr H Sawalha; Susan Manzi
Journal:  Eur J Rheumatol       Date:  2020-04-08

2.  Cell lineage-specific genome-wide DNA methylation analysis of patients with paediatric-onset systemic lupus erythematosus.

Authors:  Kit San Yeung; Tsz Leung Lee; Mo Yin Mok; Christopher Chun Yu Mak; Wanling Yang; Patrick Chun Yin Chong; Pamela Pui Wah Lee; Marco Hok Kung Ho; Sanaa Choufani; Chak Sing Lau; Yu Lung Lau; Rosanna Weksberg; Brian Hon Yin Chung
Journal:  Epigenetics       Date:  2019-03-16       Impact factor: 4.528

3.  Age-associated DNA methylation changes in naive CD4+ T cells suggest an evolving autoimmune epigenotype in aging T cells.

Authors:  Mikhail G Dozmorov; Patrick Coit; Kathleen Maksimowicz-McKinnon; Amr H Sawalha
Journal:  Epigenomics       Date:  2017-03-21       Impact factor: 4.778

Review 4.  Epigenetic Variability in Systemic Lupus Erythematosus: What We Learned from Genome-Wide DNA Methylation Studies.

Authors:  Maria Teruel; Amr H Sawalha
Journal:  Curr Rheumatol Rep       Date:  2017-06       Impact factor: 4.592

Review 5.  New insights into the immunopathogenesis of systemic lupus erythematosus.

Authors:  George C Tsokos; Mindy S Lo; Patricia Costa Reis; Kathleen E Sullivan
Journal:  Nat Rev Rheumatol       Date:  2016-11-22       Impact factor: 20.543

6.  New Perspectives in Rheumatology: May You Live in Interesting Times: Challenges and Opportunities in Lupus Research.

Authors:  Iñaki Sanz
Journal:  Arthritis Rheumatol       Date:  2017-06-16       Impact factor: 10.995

Review 7.  DNA methylation alterations in the pathogenesis of lupus.

Authors:  S H Chen; Q L Lv; L Hu; M J Peng; G H Wang; B Sun
Journal:  Clin Exp Immunol       Date:  2016-11-01       Impact factor: 4.330

8.  Modulation of EZH2 expression in T cells improves efficacy of anti-CTLA-4 therapy.

Authors:  Sangeeta Goswami; Irina Apostolou; Jan Zhang; Jill Skepner; Swetha Anandhan; Xuejun Zhang; Liangwen Xiong; Patrick Trojer; Ana Aparicio; Sumit K Subudhi; James P Allison; Hao Zhao; Padmanee Sharma
Journal:  J Clin Invest       Date:  2018-07-30       Impact factor: 14.808

Review 9.  New insights into the epigenetics of inflammatory rheumatic diseases.

Authors:  Esteban Ballestar; Tianlu Li
Journal:  Nat Rev Rheumatol       Date:  2017-09-14       Impact factor: 20.543

Review 10.  Clinical value of DNA methylation markers in autoimmune rheumatic diseases.

Authors:  Esteban Ballestar; Amr H Sawalha; Qianjin Lu
Journal:  Nat Rev Rheumatol       Date:  2020-08-05       Impact factor: 20.543

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