Advertisement

Inflammation Research

, Volume 67, Issue 9, pp 757–764 | Cite as

Emerging role of lncRNAs in the normal and diseased intestinal barrier

  • Jie Chen
  • Jianhua Wan
  • Jianfang Ye
  • Liang Xia
  • Nonghua Lu
Review

Abstract

Objective

A significant effort has been made to understand the intestinal barrier, but the effective means to prevent, reduce, and restore intestinal mucosal damage remains unclear. Recently, a few of studies have explained the mechanism of the intestinal barrier in long noncoding RNAs (lncRNAs). This review aims to summarize recent views on the function of lncRNAs in the intestinal barrier and discuss the emerging role of lncRNAs in intestinal barrier diseases caused by inflammatory diseases.

Methods

Observations led us to believe that lncRNAs participate in inflammatory responses, cell proliferation, and control microbial susceptibility. In view of these, lncRNAs have been proved to involve in the intestinal barrier.

Results

lncRNAs directly or indirectly affect TJ mRNA translation and intestinal epithelial cells (IECs) paracellular permeability, as well as IECs proliferation and susceptibility to apoptosis, to modulate the function of the intestinal barrier. miRNAs play a pivotal role in this process.

Conclusions

lncRNAs have been shown to be fundamentally involved in intestinal mucosal regeneration, protection, and epithelial barrier function. It may emerge as new and potential factors to be evaluated in the intestinal barrier diseases caused by acute pancreatitis, inflammatory bowel diseases, and imbalance of intestinal flora.

Keywords

Long noncoding RNA Intestinal barrier Inflammation Intestinal epithelial cells 

Abbreviations

lncRNAs

Long noncoding RNAs

IECs

Intestinal epithelial cells

AP

Acute pancreatitis

TJ

Tight junction

ZO-1

Zonula occludin 1

E-cad

E-cadherin

VDR

Vitamin D receptor

3′UTR

3′-untranslated region

ceRNA

Competing endogenous RNA

AQP3

Aquaporin 3

UC

Ulcerative colitis

SPRY4-IT1

SPROUTY4 intronic transcript 1

PlncRNA1

Prostate cancer-upregulated long noncoding RNA 1

IBDs

Inflammatory bowel diseases

MAZ

Myc-associated zinc-finger protein

T-UCR

Transcribed ultra-conservative

Notes

Funding

This study is funded by the National Natural Science Foundation of China (no. 81760121); the Graduate Teaching Library Construction Project of Nanchang University (no. 9202-0210210802); the Graduate Innovation fund of Jiangxi Province (nos. YC2017-S094 and YC2017-B016).

Compliance with ethical standards

Conflict of interest

All authors read and approved the final manuscript. The authors declare no conflict of interest. The founding sponsors had no role in the writing of the manuscript and in the decision to publish the results.

References

  1. 1.
    Okumura R, Takeda K. Roles of intestinal epithelial cells in the maintenance of gut homeostasis. Exp Mol Med. 2017;49:e338.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Wang J, Ghosh SS, Ghosh S. Curcumin improves intestinal barrier function: modulation of intracellular signaling, and organization of tight junctions. Am J Physiol Cell Physiol. 2017;312:C438-45.Google Scholar
  3. 3.
    Mittal R, Coopersmith CM. Redefining the gut as the motor of critical illness. Trends Mol Med. 2014;20:214–23.CrossRefPubMedGoogle Scholar
  4. 4.
    Moraes F, Goes A. A decade of human genome project conclusion: scientific diffusion about our genome knowledge. Biochem Mol Biol Educ. 2016;44:215–23.CrossRefPubMedGoogle Scholar
  5. 5.
    Feng Y, Fan Y, Huiqing C, Zicai L, Quan D. The emerging landscape of long non-coding RNAs. Yi Chuan. 2014;36:456–68.PubMedGoogle Scholar
  6. 6.
    Chang CP, Han P. Epigenetic and lncRNA regulation of cardiac pathophysiology. Biochim Biophys Acta. 2016;1863:1767–71.CrossRefPubMedGoogle Scholar
  7. 7.
    Mele M, Rinn JL. “Cat’s Cradling” the 3D genome by the act of LncRNA transcription. Mol Cell. 2016;62:657–64.CrossRefPubMedGoogle Scholar
  8. 8.
    Wang JY, Xiao L, Wang JY. Posttranscriptional regulation of intestinal epithelial integrity by noncoding RNAs. Wiley Interdiscip Rev RNA. 2017;8:e1399.CrossRefGoogle Scholar
  9. 9.
    Jia Y, Li Z, Cai W, Xiao D, Han S, Han F, Bai X, Wang K, Liu Y, Li X, Guan H, Hu D. SIRT1 regulates inflammation response of macrophages in sepsis mediated by long noncoding RNA. Biochim Biophys Acta. 2018;1864:784–92.CrossRefPubMedGoogle Scholar
  10. 10.
    Chen H, Wang X, Yan X, Cheng X, He X, Zheng W. LncRNA MALAT1 regulates sepsis-induced cardiac inflammation and dysfunction via interaction with miR-125b and p38 MAPK/NFkappaB. Int Immunopharmacol. 2018;55:69–76.CrossRefPubMedGoogle Scholar
  11. 11.
    Liao B, Chen R, Lin F, Mai A, Chen J, Li H, Xu Z, Dong S. Long noncoding RNA HOTTIP promotes endothelial cell proliferation and migration via activation of the Wnt/beta-catenin pathway. J Cell Biochem. 2018;119:2797–805.CrossRefPubMedGoogle Scholar
  12. 12.
    Gomez JA, Wapinski OL, Yang YW, Bureau JF, Gopinath S, Monack DM, Chang HY, Brahic M, Kirkegaard K. The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-gamma locus. Cell. 2013;152:743–54.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Mowel WK, Kotzin JJ, McCright SJ, Neal VD, Henao-Mejia J. Control of immune cell homeostasis and function by lncRNAs. Trends Immunol. 2018;39:55–69.CrossRefPubMedGoogle Scholar
  14. 14.
    Gabory A, Ripoche MA, Yoshimizu T, Dandolo L. The H19 gene: regulation and function of a non-coding RNA. Cytogenet Genome Res. 2006;113:188–93.CrossRefPubMedGoogle Scholar
  15. 15.
    Raveh E, Matouk IJ, Gilon M, Hochberg A. The H19 Long non-coding RNA in cancer initiation, progression and metastasis—a proposed unifying theory. Mol Cancer. 2015;14:184.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Zhou X, Ye F, Yin C, Zhuang Y, Yue G, Zhang G. The interaction between MiR-141 and lncRNA-H19 in regulating cell proliferation and migration in gastric cancer. Cell Physiol Biochem. 2015;36:1440–52.CrossRefPubMedGoogle Scholar
  17. 17.
    Li X, Lin Y, Yang X, Wu X, He X. Long noncoding RNA H19 regulates EZH2 expression by interacting with miR-630 and promotes cell invasion in nasopharyngeal carcinoma. Biochem Biophys Res Commun. 2016;473:913–9.CrossRefPubMedGoogle Scholar
  18. 18.
    Su Z, Zhi X, Zhang Q, Yang L, Xu H, Xu Z. LncRNA H19 functions as a competing endogenous RNA to regulate AQP3 expression by sponging miR-874 in the intestinal barrier. FEBS Lett. 2016;590:1354–64.CrossRefPubMedGoogle Scholar
  19. 19.
    Wang SH, Ma F, Tang ZH, Wu XC, Cai Q, Zhang MD, Weng MZ, Zhou D, Wang JD, Quan ZW. Long non-coding RNA H19 regulates FOXM1 expression by competitively binding endogenous miR-342-3p in gallbladder cancer. J Exp Clin Cancer Res. 2016;35:160.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Zhang Q, Li X, Li X, Li X, Chen Z. LncRNA H19 promotes epithelial–mesenchymal transition (EMT) by targeting miR-484 in human lung cancer cells. J Cell Biochem. 2017;119:4447–57.CrossRefGoogle Scholar
  21. 21.
    Pan JX. LncRNA H19 promotes atherosclerosis by regulating MAPK and NF-kB signaling pathway. Eur Rev Med Pharmacol Sci. 2017;21:322–8.PubMedGoogle Scholar
  22. 22.
    Zou T, Jaladanki SK, Liu L, Xiao L, Chung HK, Wang J, Xu Y, Gorospe M, Wang J. H19 long noncoding RNA regulates intestinal epithelial barrier function via MicroRNA 675 by interacting with RNA-binding protein HuR. Mol Cell Biol. 2016;36:1332–41.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Chen S, Wang P, Liu Y, Sun L, Zhu J, Zuo S, Ma J, Li T, Zhang J, Chen G, Wang X, Zhu Q, Zheng Y, Chen Z, Yao Z, Pan Y. Effect of long noncoding RNA H19 overexpression on intestinal barrier function and its potential role in the pathogenesis of ulcerative colitis. Inflamm Bowel Dis. 2016;22:2582–92.CrossRefPubMedGoogle Scholar
  24. 24.
    Wang SH, Wu XC, Zhang MD, Weng MZ, Zhou D, Quan ZW. Long noncoding RNA H19 contributes to gallbladder cancer cell proliferation by modulated miR-194-5p targeting AKT2. Tumour Biol. 2016;37:9721–30.CrossRefPubMedGoogle Scholar
  25. 25.
    Zhi X, Tao J, Li Z, Jiang B, Feng J, Yang L, Xu H, Xu Z. MiR-874 promotes intestinal barrier dysfunction through targeting AQP3 following intestinal ischemic injury. FEBS Lett. 2014;588:757–63.CrossRefPubMedGoogle Scholar
  26. 26.
    Nathan C, Ding A. Nonresolving inflammation. Cell. 2010;140:871–82.CrossRefPubMedGoogle Scholar
  27. 27.
    Boshtam M, Asgary S, Kouhpayeh S, Shariati L, Khanahmad H. Aptamers against pro- and anti-inflammatory cytokines: a review. Inflammation. 2017;40:340–9.CrossRefPubMedGoogle Scholar
  28. 28.
    Zhu QN, Wang G, Guo Y, Peng Y, Zhang R, Deng JL, Li ZX, Zhu YS. LncRNA H19 is a major mediator of doxorubicin chemoresistance in breast cancer cells through a cullin4A-MDR1 pathway. Oncotarget. 2017;8:91990–2003.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Yoshimizu T, Miroglio A, Ripoche MA, Gabory A, Vernucci M, Riccio A, Colnot S, Godard C, Terris B, Jammes H, Dandolo L. The H19 locus acts in vivo as a tumor suppressor. Proc Natl Acad Sci USA. 2008;105:12417–22.CrossRefPubMedGoogle Scholar
  30. 30.
    Sun Y, Pan J, Zhang N, Wei W, Yu S, Ai L. Knockdown of long non-coding RNA H19 inhibits multiple myeloma cell growth via NF-kappaB pathway. Sci Rep. 2017;7:18079.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Lu D, Lan B, Din Z, Chen H, Chen G. A vitamin D receptor agonist converts CD4 + T cells to Foxp3 + regulatory T cells in patients with ulcerative colitis. Oncotarget. 2017;8:53552–62.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Zheng SZ, Zhang DG, Wu H, Jiang LJ, Jin J, Lin XQ, Ding R, Jiang Y. The association between vitamin D receptor polymorphisms and serum 25-hydroxyvitamin D levels with ulcerative colitis in Chinese Han population. Clin Res Hepatol Gastroenterol. 2017;41:110–7.CrossRefPubMedGoogle Scholar
  33. 33.
    Katoh Y, Katoh M. FGF signaling inhibitor, SPRY4, is evolutionarily conserved target of WNT signaling pathway in progenitor cells. Int J Mol Med. 2006;17:529–32.PubMedGoogle Scholar
  34. 34.
    Zhao XL, Zhao ZH, Xu WC, Hou JQ, Du XY. Increased expression of SPRY4-IT1 predicts poor prognosis and promotes tumor growth and metastasis in bladder cancer. Int J Clin Exp Pathol. 2015;8:1954–60.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Zhang HM, Yang FQ, Yan Y, Che JP, Zheng JH. High expression of long non-coding RNA SPRY4-IT1 predicts poor prognosis of clear cell renal cell carcinoma. Int J Clin Exp Pathol. 2014;7:5801–9.PubMedPubMedCentralGoogle Scholar
  36. 36.
    Shi Y, Li J, Liu Y, Ding J, Fan Y, Tian Y, Wang L, Lian Y, Wang K, Shu Y. The long noncoding RNA SPRY4-IT1 increases the proliferation of human breast cancer cells by upregulating ZNF703 expression. Mol Cancer. 2015;14:51.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Peng W, Wu G, Fan H, Wu J, Feng J. Long noncoding RNA SPRY4-IT1 predicts poor patient prognosis and promotes tumorigenesis in gastric cancer. Tumour Biol. 2015;36:6751–8.CrossRefPubMedGoogle Scholar
  38. 38.
    Jing W, Gao S, Zhu M, Luo P, Jing X, Chai H, Tu J. Potential diagnostic value of lncRNA SPRY4-IT1 in hepatocellular carcinoma. Oncol Rep. 2016;36:1085–92.CrossRefPubMedGoogle Scholar
  39. 39.
    Wen X, Han XR, Wang YJ, Fan SH, Zhuang J, Zhang ZF, Shan Q, Li MQ, Hu B, Sun CH, Wu Q, Tan JH, Wu DM, Lu J, Zheng YL. Effects of long noncoding RNA SPRY4-IT1-mediated EZH2 on the invasion and migration of lung adenocarcinoma. J Cell Biochem. 2018;119:1827–40.CrossRefPubMedGoogle Scholar
  40. 40.
    Xiao L, Rao JN, Cao S, Liu L, Chung HK, Zhang Y, Zhang J, Liu Y, Gorospe M, Wang JY. Long noncoding RNA SPRY4-IT1 regulates intestinal epithelial barrier function by modulating the expression levels of tight junction proteins. Mol Biol Cell. 2016;27:617–26.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Yu J, Han Q, Cui Y. Decreased long non-coding RNA SPRY4-IT1 contributes to ovarian cancer cell metastasis partly via affecting epithelial–mesenchymal transition. Tumour Biol. 2017;39:1393380535.Google Scholar
  42. 42.
    Zuo Q, Huang S, Zou Y, Xu Y, Jiang Z, Zou S, Xu H, Sun L. The Lnc RNA SPRY4-IT1 modulates trophoblast cell invasion and migration by affecting the epithelial–mesenchymal transition. Sci Rep. 2016;6:37183.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Sun M, Liu XH, Lu KH, Nie FQ, Xia R, Kong R, Yang JS, Xu TP, Liu YW, Zou YF, Lu BB, Yin R, Zhang EB, Xu L, De W, Wang ZX. EZH2-mediated epigenetic suppression of long noncoding RNA SPRY4-IT1 promotes NSCLC cell proliferation and metastasis by affecting the epithelial–mesenchymal transition. Cell Death Dis. 2014;5:e1298.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Cao D, Ding Q, Yu W, Gao M, Wang Y. Long noncoding RNA SPRY4-IT1 promotes malignant development of colorectal cancer by targeting epithelial–mesenchymal transition. Onco Targets Ther. 2016;9:5417–25.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Shen F, Cai WS, Feng Z, Chen JW, Feng JH, Liu QC, Fang YP, Li KP, Xiao HQ, Cao J, Xu B. Long non-coding RNA SPRY4-IT1 pormotes colorectal cancer metastasis by regulate epithelial–mesenchymal transition. Oncotarget. 2017;8:14479–86.PubMedGoogle Scholar
  46. 46.
    Zhang CY, Li RK, Qi Y, Li XN, Yang Y, Liu DL, Zhao J, Zhu DY, Wu K, Zhou XD, Zhao S. Upregulation of long noncoding RNA SPRY4-IT1 promotes metastasis of esophageal squamous cell carcinoma via induction of epithelial–mesenchymal transition. Cell Biol Toxicol. 2016;32:391–401.CrossRefPubMedGoogle Scholar
  47. 47.
    Levy L, Hill CS. Alterations in components of the TGF-beta superfamily signaling pathways in human cancer. Cytokine Growth Factor Rev. 2006;17:41–58.CrossRefPubMedGoogle Scholar
  48. 48.
    Wang H, Wang HS, Zhou BH, Li CL, Zhang F, Wang XF, Zhang G, Bu XZ, Cai SH, Du J. Epithelial–mesenchymal transition (EMT) induced by TNF-alpha requires AKT/GSK-3beta-mediated stabilization of snail in colorectal cancer. PLoS One. 2013;8:e56664.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Chen SL, Liu LL, Lu SX, Luo RZ, Wang CH, Wang H, Cai SH, Yang X, Xie D, Zhang CZ, Yun JP. HBx-mediated decrease of AIM2 contributes to hepatocellular carcinoma metastasis. Mol Oncol. 2017;11:1225–40.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Baratieh Z, Khalaj Z, Honardoost MA, Emadi-Baygi M, Khanahmad H, Salehi M, Nikpour P. Aberrant expression of PlncRNA-1 and TUG1: potential biomarkers for gastric cancer diagnosis and clinically monitoring cancer progression. Biomark Med. 2017;11:1077–90.CrossRefPubMedGoogle Scholar
  51. 51.
    Cui Z, Ren S, Lu J, Wang F, Xu W, Sun Y, Wei M, Chen J, Gao X, Xu C, Mao JH, Sun Y. The prostate cancer-up-regulated long noncoding RNA PlncRNA-1 modulates apoptosis and proliferation through reciprocal regulation of androgen receptor. Urol Oncol. 2013;31:1117–23.CrossRefPubMedGoogle Scholar
  52. 52.
    Dong L, Ni J, Hu W, Yu C, Li H. Upregulation of long non-coding RNA PlncRNA-1 promotes metastasis and induces epithelial–mesenchymal transition in hepatocellular carcinoma. Cell Physiol Biochem. 2016;38:836–46.CrossRefPubMedGoogle Scholar
  53. 53.
    Fang Z, Xu C, Li Y, Cai X, Ren S, Liu H, Wang Y, Wang F, Chen R, Qu M, Wang Y, Zhu Y, Zhang W, Shi X, Yao J, Gao X, Hou J, Xu C, Sun Y. A feed-forward regulatory loop between androgen receptor and PlncRNA-1 promotes prostate cancer progression. Cancer Lett. 2016;374:62–74.CrossRefPubMedGoogle Scholar
  54. 54.
    Wang CM, Wu QQ, Li SQ, Chen FJ, Tuo L, Xie HW, Tong YS, Ji L, Zhou GZ, Cao G, Wu M, Lv J, Shi WH, Cao XF. Upregulation of the long non-coding RNA PlncRNA-1 promotes esophageal squamous carcinoma cell proliferation and correlates with advanced clinical stage. Dig Dis Sci. 2014;59:591–7.CrossRefPubMedGoogle Scholar
  55. 55.
    Chen T, Xue H, Lin R, Huang Z. MiR-34c and PlncRNA1 mediated the function of intestinal epithelial barrier by regulating tight junction proteins in inflammatory bowel disease. Biochem Biophys Res Commun. 2017;486:6–13.CrossRefPubMedGoogle Scholar
  56. 56.
    Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell. 2011;146:353–8.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature. 2010;465:1033–8.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Zhao L, Wang P, Liu Y, Ma J, Xue Y. miR-34c regulates the permeability of blood-tumor barrier via MAZ-mediated expression changes of ZO-1, occludin, and claudin-5. J Cell Physiol. 2015;230:716–31.CrossRefPubMedGoogle Scholar
  59. 59.
    Nan A, Zhou X, Chen L, Liu M, Zhang N, Zhang L, Luo Y, Liu Z, Dai L, Jiang Y. A transcribed ultraconserved noncoding RNA, Uc.173, is a key molecule for the inhibition of lead-induced neuronal apoptosis. Oncotarget. 2016;7:112–24.CrossRefPubMedGoogle Scholar
  60. 60.
    Qin J, Ning H, Zhou Y, Hu Y, Huang B, Wu Y, Huang R. LncRNA Uc.173 is a key molecule for the regulation of lead-induced renal tubular epithelial cell apoptosis. Biomed Pharmacother. 2018;100:101–7.CrossRefPubMedGoogle Scholar
  61. 61.
    Xiao L, Wu J, Wang JY, Chung HK, Kalakonda S, Rao JN, Gorospe M, Wang JY. Long noncoding RNA uc.173 promotes renewal of the intestinal mucosa by inducing degradation of MicroRNA 195. Gastroenterology. 2018;154:599–611.CrossRefPubMedGoogle Scholar
  62. 62.
    Liz J, Portela A, Soler M, Gomez A, Ling H, Michlewski G, Calin GA, Guil S, Esteller M. Regulation of pri-miRNA processing by a long noncoding RNA transcribed from an ultraconserved region. Mol Cell. 2014;55:138–47.CrossRefPubMedGoogle Scholar
  63. 63.
    Wu F, Huang Y, Dong F, Kwon JH. Ulcerative colitis-associated long noncoding RNA, BC012900, regulates intestinal epithelial cell apoptosis. Inflamm Bowel Dis. 2016;22:782–95.CrossRefPubMedGoogle Scholar
  64. 64.
    Ofek P, Ben-Meir D, Kariv-Inbal Z, Oren M, Lavi S. Cell cycle regulation and p53 activation by protein phosphatase 2C alpha. J Biol Chem. 2003;278:14299–305.CrossRefPubMedGoogle Scholar
  65. 65.
    Carter SR, Zahs A, Palmer JL, Wang L, Ramirez L, Gamelli RL, Kovacs EJ. Intestinal barrier disruption as a cause of mortality in combined radiation and burn injury. Shock. 2013;40:281–9.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Zhang HJ, Wei QF, Wang SJ, Zhang HJ, Zhang XY, Geng Q, Cui YH, Wang XH. LncRNA HOTAIR alleviates rheumatoid arthritis by targeting miR-138 and inactivating NF-kappaB pathway. Int Immunopharmacol. 2017;50:283–90.CrossRefPubMedGoogle Scholar
  67. 67.
    Wu H, Liu J, Li W, Liu G, Li Z. LncRNA-HOTAIR promotes TNF-alpha production in cardiomyocytes of LPS-induced sepsis mice by activating NF-kappaB pathway. Biochem Biophys Res Commun. 2016;471:240–6.CrossRefPubMedGoogle Scholar
  68. 68.
    Viswanathan VK, Hecht G. Innate immunity and the gut. Curr Opin Gastroenterol. 2000;16:546–51.CrossRefPubMedGoogle Scholar
  69. 69.
    Yoon JH, Abdelmohsen K, Gorospe M. Functional interactions among microRNAs and long noncoding RNAs. Semin Cell Dev Biol. 2014;34:9–14.CrossRefPubMedGoogle Scholar
  70. 70.
    Loddo I, Romano C. Inflammatory bowel disease: genetics, epigenetics, and pathogenesis. Front Immunol. 2015;6:551.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Qiao YQ, Huang ML, Xu AT, Zhao D, Ran ZH, Shen J. LncRNA DQ786243 affects Treg related CREB and Foxp3 expression in Crohn’s disease. J Biomed Sci. 2013;20:87.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Mirza AH, Kaur S, Brorsson CA, Pociot F. Effects of GWAS-associated genetic variants on lncRNAs within IBD and T1D candidate loci. PLoS One. 2014;9:e105723.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Lucafo M, Di Silvestre A, Romano M, Avian A, Antonelli R, Martelossi S, Naviglio S, Tommasini A, Stocco G, Ventura A, Decorti G, De Iudicibus S. Role of the long non-coding RNA growth arrest-specific 5 in glucocorticoid response in children with inflammatory bowel disease. Basic Clin Pharmacol Toxicol. 2018;122:87–93.CrossRefPubMedGoogle Scholar
  74. 74.
    Chen D, Liu J, Zhao HY, Chen YP, Xiang Z, Jin X. Plasma long noncoding RNA expression profile identified by microarray in patients with Crohn’s disease. World J Gastroenterol. 2016;22:4716–31.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Harris J. Autophagy and cytokines. Cytokine. 2011;56:140–4.CrossRefPubMedGoogle Scholar
  76. 76.
    Wang J, Cao B, Han D, Sun M, Feng J. Long non-coding RNA H19 induces cerebral ischemia reperfusion injury via activation of autophagy. Aging Dis. 2017;8:71–84.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Guamer F. Role of intestinal flora in health and disease. Nutr Hosp. 2007;22(Suppl 2):14–9.PubMedGoogle Scholar
  78. 78.
    Spurlock CR, Crooke PR, Aune TM. Biogenesis and transcriptional regulation of long noncoding RNAs in the human immune system. J Immunol. 2016;197:4509–17.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of GastroenterologyThe First Affiliated Hospital of Nanchang UniversityNanchangPeople’s Republic of China

Personalised recommendations