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Induction of a Long Noncoding RNA Transcript, NR_045064, Promotes Defense Gene Transcription and Facilitates Intestinal Epithelial Cell Responses against Cryptosporidium Infection

Min Li, Ai-Yu Gong, Xin-Tian Zhang, Yang Wang, Nicholas W. Mathy, Gislaine A. Martins, Juliane K. Strauss-Soukup and Xian-Ming Chen
J Immunol November 16, 2018, ji1800566; DOI: https://doi.org/10.4049/jimmunol.1800566
Min Li
*Department of Medical Microbiology and Immunology, Creighton University School of Medicine, Omaha, NE 68178;
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Ai-Yu Gong
*Department of Medical Microbiology and Immunology, Creighton University School of Medicine, Omaha, NE 68178;
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Xin-Tian Zhang
*Department of Medical Microbiology and Immunology, Creighton University School of Medicine, Omaha, NE 68178;
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Yang Wang
*Department of Medical Microbiology and Immunology, Creighton University School of Medicine, Omaha, NE 68178;
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Nicholas W. Mathy
*Department of Medical Microbiology and Immunology, Creighton University School of Medicine, Omaha, NE 68178;
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Gislaine A. Martins
†Research Division of Immunology, Department of Medicine, Cedars-Sinai Medical Center, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA 90048;
‡Research Division of Immunology, Department of Biomedical Sciences, Cedars-Sinai Medical Center, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA 90048; and
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Juliane K. Strauss-Soukup
§Department of Chemistry, Creighton University College of Arts and Sciences, Omaha, NE 68178
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Xian-Ming Chen
*Department of Medical Microbiology and Immunology, Creighton University School of Medicine, Omaha, NE 68178;
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Abstract

Cryptosporidium is an important opportunistic intestinal pathogen for immunocompromised individuals and a common cause of diarrhea in young children in developing countries. Gastrointestinal epithelial cells play a central role in activating and orchestrating host immune responses against Cryptosporidium infection, but underlying molecular mechanisms are not fully understood. We report in this paper that C. parvum infection causes significant alterations in long noncoding RNA (lncRNA) expression profiles in murine intestinal epithelial cells. Transcription of a panel of lncRNA genes, including NR_045064, in infected cells is controlled by the NF-κB signaling. Functionally, inhibition of NR_045064 induction increases parasite burden in intestinal epithelial cells. Induction of NR_045064 enhances the transcription of selected defense genes in host cells following C. parvum infection. Epigenetic histone modifications are involved in NR_045064-mediated transcription of associated defense genes in infected host cells. Moreover, the p300/MLL-associated chromatin remodeling is involved in NR_045064-mediated transcription of associated defense genes in intestinal epithelial cells following C. parvum infection. Expression of NR_045064 and associated genes is also identified in intestinal epithelium in C57BL/6J mice following phosphorothioate oligodeoxynucleotide or LPS stimulation. Our data demonstrate that lncRNAs, such as NR_045064, play a role in regulating epithelial defense against microbial infection.

Footnotes

  • This work was supported by the National Institutes of Health (AI116323 and AI136877) and the Nebraska Cancer and Smoking Disease Research Program (LB595) to X.-M.C. and by Grant G20RR024001 from the National Center for Research Resources.

  • The microarray data presented in this article have been submitted to the Gene Expression Omnibus (https://www.ncbi.nlm.nih.gov/geo) under accession number GSE112247.

  • The online version of this article contains supplemental material.

  • Received April 20, 2018.
  • Accepted October 20, 2018.
  • Copyright © 2018 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 208 (11)
The Journal of Immunology
Vol. 208, Issue 11
1 Jun 2022
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Induction of a Long Noncoding RNA Transcript, NR_045064, Promotes Defense Gene Transcription and Facilitates Intestinal Epithelial Cell Responses against Cryptosporidium Infection
Min Li, Ai-Yu Gong, Xin-Tian Zhang, Yang Wang, Nicholas W. Mathy, Gislaine A. Martins, Juliane K. Strauss-Soukup, Xian-Ming Chen
The Journal of Immunology November 16, 2018, ji1800566; DOI: 10.4049/jimmunol.1800566

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Induction of a Long Noncoding RNA Transcript, NR_045064, Promotes Defense Gene Transcription and Facilitates Intestinal Epithelial Cell Responses against Cryptosporidium Infection
Min Li, Ai-Yu Gong, Xin-Tian Zhang, Yang Wang, Nicholas W. Mathy, Gislaine A. Martins, Juliane K. Strauss-Soukup, Xian-Ming Chen
The Journal of Immunology November 16, 2018, ji1800566; DOI: 10.4049/jimmunol.1800566
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