Identification of the long noncoding RNA NEAT1 as a novel inflammatory regulator acting through MAPK pathway in human lupus

Journal of Autoimmunity

Volumn 75, Issue , 2016, Pages 96-104

  Zhang, Feifei ^a,b   Wu, Lingling ^a   Qian, Jie ^a   Qu, Bo ^a   Xia, Shiwei ^a   La, Ting ^b   Wu, Yanfang ^a   Ma, Jianyang ^a   Zeng, Jing ^a   Guo, Qiang ^a   Cui, Yong ^d   Yang, Wanling ^e   Huang, Jiaqi ^f   Zhu, Wei ^f   Yao, Yihong ^f   Shen, Nan ^a,b,c   Tang, Yuanjia ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d ANHUI MEDICAL UNIVERSITY   (China)

^e UNIVERSITY OF HONG KONG   (Hong Kong)

^f Cellular Biomedicine Group   (China)

Author keywords

Cytokines; Long noncoding RNA; NEAT1; Systemic lupus erythematosus; TLR4

Indexed keywords

CXCL1 CHEMOKINE; CXCL11 CHEMOKINE; CXCL9 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 12P40; INTERLEUKIN 29; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; LONG UNTRANSLATED RNA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 2; STRESS ACTIVATED PROTEIN KINASE 1; TOLL LIKE RECEPTOR 4; AUTACOID; CYTOKINE; NEAT1 LONG NON-CODING RNA, HUMAN;

ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE ACTIVITY; EARLY RESPONSE GENE; ENZYME ACTIVATION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; INFLAMMATION; MICROARRAY ANALYSIS; MONOCYTE; NEAT1 GENE; PATHOGENESIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; CLUSTER ANALYSIS; DNA MICROARRAY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETICS; IMMUNOLOGY; METABOLISM; PROCEDURES; RNA INTERFERENCE; TUMOR CELL LINE; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL LINE, TUMOR; CLUSTER ANALYSIS; CYTOKINES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ONTOLOGY; HUMANS; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; LUPUS ERYTHEMATOSUS, SYSTEMIC; MAP KINASE SIGNALING SYSTEM; MONOCYTES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA INTERFERENCE; RNA, LONG NONCODING;

EID: 84995646177     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2016.07.012     Document Type: Article

References (60)

1. [1] D'Cruz, D.P., Khamashta, M.A., Hughes, G.R.V., Systemic lupus erythematosus. Lancet 369:9561 (2007), 587–596.
2. [2] Kotzin, B.L., Systemic lupus erythematosus. Cell 85 (1996), 303–306.
3. [3] Waldner, H., The role of innate immune responses in autoimmune disease development. Autoimmun. Rev. 8:5 (2009), 400–404.
4. [4] Pisetsky, D.S., The role of innate immunity in the induction of autoimmunity. Autoimmun. Rev. 8:1 (2008), 69–72.
5. [5] Kontaki, E., Boumpas, D.T., Innate immunity in systemic lupus erythematosus: sensing endogenous nucleic acids. J. Autoimmun. 35:3 (2010), 206–211.
6. [6] Katsiari, C.G., Liossis, S.-N.C., Sfikakis, P.P., The pathophysiologic role of monocytes and macrophages in systemic lupus erythematosus: a reappraisal. Seminars Arthritis Rheumatism 39:6 (2010), 491–503.
7. [7] Steinbach, F., et al. Monocytes from systemic lupus erythematous patients are severely altered in phenotype and lineage flexibility. Ann. Rheumatic Dis. 59:4 (2000), 283–288.
8. [8] Li, Y., Lee, P., Reeves, W., Monocyte and macrophage abnormalities in systemic lupus erythematosus. Archivum Immunol. Ther. Exp. 58:5 (2010), 355–364.
9. [9] Dean, G.S., et al. Cytokines and systemic lupus erythematosus. Ann. Rheum. Dis. 59 (2000), 243–251.
10. [10] Ronnblom, L., Elkon, K.B., Cytokines as therapeutic targets in SLE. Nat. Rev. Rheumatol. 6:6 (2010), 339–347.
11. [11] Nockher, W.A., et al. Elevated levels of soluble CD 14 in serum of patients with systemic lupus erythematosus. Clin. Exp. Immunol. 96:1 (1994), 15–19.
12. [12] Granholm, N.A., Cavallo, T., Bacterial lipopolysaccharide enhances deposition of immune complexes and exacerbates nephritis in BXSB lupus-prone mice. Clin. Exp. Immunol. 85:2 (1991), 270–277.
13. [13] Granholm, N.A., Cavallo, T., Long-lasting Effects of bacterial lipopolysaccharide promote Progression of lupus Nephritis in NZB/W mice. Lupus 3:6 (1994), 507–514.
14. [14] Lartigue, A., et al. Critical role of TLR2 and TLR4 in autoantibody production and glomerulonephritis in lpr mutation-induced mouse lupus. J. Immunol. 183:10 (2009), 6207–6216.
15. [15] Summers, S.A., et al. TLR9 and TLR4 are required for the development of autoimmunity and lupus nephritis in pristane nephropathy. J. Autoimmun. 35:4 (2010), 291–298.
16. [16] Yu, L., Wang, L., Chen, S., Endogenous toll-like receptor ligands and their biological significance. J. Cell Mol. Med. 14:11 (2010), 2592–2603.
17. [17] Urbonaviciute, V., Voll, R.E., High-mobility group box 1 represents a potential marker of disease activity and novel therapeutic target in systemic lupus erythematosus. J. Intern Med. 270:4 (2011), 309–318.
18. [18] Guttman, M., et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458:7235 (2009), 223–227.
19. [19] Marques, A.C., Ponting, C.P., Catalogues of mammalian long noncoding RNAs: modest conservation and incompleteness. Genome Biol., 10(11), 2009, R124.
20. [20] Zhao, J., et al. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322 (2008), 750–756.
21. [21] Orom, U.A., et al. Long noncoding RNAs with enhancer-like function in human cells. Cell 143:1 (2010), 46–58.
22. [22] Ponting, C.P., Oliver, P.L., Reik, W., Evolution and functions of long noncoding RNAs. Cell 136:4 (2009), 629–641.
23. [23] Wang, K.C., Chang, H.Y., Molecular mechanisms of long noncoding RNAs. Mol. Cell 43:6 (2011), 904–914.
24. [24] Wapinski, O., Chang, H.Y., Long noncoding RNAs and human disease. Trends Cell Biol. 21:6 (2011), 354–361.
25. [25] Li, J., Xuan, Z., Liu, C., Long non-coding RNAs and complex human diseases. Int. J. Mol. Sci. 14:9 (2013), 18790–18808.
26. [26] Faghihi, M.A., et al. Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of beta-secretase. Nat. Med. 14 (2008), 723–730.
27. [27] Gupta, R.A., et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464:7291 (2010), 1071–1076.
28. [28] Shirasawa, S., et al. SNPs in the promoter of a B cell-specific antisense transcript, SAS-ZFAT, determine susceptibility to autoimmune thyroid disease. Hum. Mol. Genet. 13:19 (2004), 2221–2231.
29. [29] Song, J., et al. PBMC and exosome-derived Hotair is a critical regulator and potent marker for rheumatoid arthritis. Clin. Exp. Med. 15:1 (2015), 121–126.
30. [30] Hutchinson, J.N., et al. A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains. BMC Genomics, 8, 2007, 39.
31. [31] Sunwoo, H., et al. MEN epsilon/beta nuclear-retained non-coding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles. Genome Res. 19:3 (2008), 347–359.
32. [32] Sasaki, Y.T., et al. MENepsilon/beta noncoding RNAs are essential for structural integrity of nuclear paraspeckles. Proc. Natl. Acad. Sci. U. S. A. 106:8 (2009), 2525–2530.
33. [33] Chen, L.L., Carmichael, G.G., Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: functional role of a nuclear noncoding RNA. Mol. Cell 35:4 (2009), 467–478.
34. [34] Clemson, C.M., et al. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol. Cell 33:6 (2009), 717–726.
35. [35] Naganuma, T., et al. Alternative 3'-end processing of long noncoding RNA initiates construction of nuclear paraspeckles. EMBO J. 31:20 (2012), 4020–4034.
36. [36] Prasanth, K.V., et al. Regulating gene expression through RNA nuclear retention. Cell 123:2 (2005), 249–263.
37. [37] Saha, S., Murthy, S., Rangarajan, P.N., Identification and characterization of a virus-inducible non-coding RNA in mouse brain. J. Gen. Virol. 87:Pt 7 (2006), 1991–1995.
38. [38] Zhang, Q., et al. NEAT1 long noncoding RNA and paraspeckle bodies modulate HIV-1 posttranscriptional expression. MBio 4:1 (2013), e00596–e00612.
39. [39] Nakagawa, S., et al. Paraspeckles are subpopulation-specific nuclear bodies that are not essential in mice. J. Cell Biol. 193:1 (2011), 31–39.
40. [40] Baechler, E.C., et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc. Natl. Acad. Sci. U. S. A. 100:5 (2003), 2610–2615.
41. [41] Imamura, K., et al. Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Mol. Cell 53:3 (2014), 393–406.
42. [42] Marshak-Rothstein, A., Toll-like receptors in systemic autoimmune disease. Nat. Rev. Immunol. 6:11 (2006), 823–835.
43. [43] Hornung, V., et al. Quantitative expression of toll-like receptor 1–10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J. Immunol. 168:9 (2002), 4531–4537.
44. [44] Li, Z., et al. The long noncoding RNA THRIL regulates TNFα expression through its interaction with hnRNPL. Proc. Natl. Acad. Sci. U. S. A. 111:3 (2014), 1002–1007.
45. [45] Taganov, K.D., et al. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. U. S. A. 103:33 (2006), 12481–12486.
46. [46] Heinz, S., et al. Species-specific regulation of Toll-like receptor 3 genes in men and mice. J. Biol. Chem. 278:24 (2003), 21502–21509.
47. [47] Linker-Israeli, M., et al. Elevated levels of endogenous IL-6 in systemic lupus erythematosus. A putative role in pathogenesis. J. Immunol. Baltim. Md. 1950) 147:1 (1991), 117–123.
48. [48] Kim, W.U., Sreih, A., Bucala, R., Toll-like receptors in systemic lupus erythematosus; prospects for therapeutic intervention. Autoimmun. Rev. 8:3 (2009), 204–208.
49. [49] Christensen, S.R., Shlomchik, M.J., Regulation of lupus-related autoantibody production and clinical disease by Toll-like receptors. Semin. Immunol. 19:1 (2007), 11–23.
50. [50] Papadimitraki, E.D., Bertsias, G.K., Boumpas, D.T., Toll like receptors and autoimmunity: a critical appraisal. J. Autoimmun. 29:4 (2007), 310–318.
51. [51] Lang, K.S., et al. The role of the innate immune response in autoimmune disease. J. Autoimmun. 29:4 (2007), 206–212.
52. [52] Carpenter, S., et al. A long noncoding RNA mediates both activation and repression of immune response genes. Science 341 (2013), 789–792.
53. [53] Rapicavoli, N.A., et al. A mammalian pseudogene lncRNA at the interface of inflammation and anti-inflammatory therapeutics. Elife, 2, 2013, e00762.
54. [54] Masutani, K., et al. Predominance of Th1 immune response in diffuse proliferative lupus nephritis. Arthritis Rheum. 44 (2001), 2097–2106.
55. [55] Teramoto, K., et al. Microarray analysis of glomerular gene expression in murine lupus nephritis. J. Pharmacol. Sci. 106:1 (2008), 56–67.
56. [56] Steinmetz, O.M., et al. CXCR3 mediates renal Th1 and Th17 immune response in murine lupus nephritis. J. Immunol. 183:7 (2009), 4693–4704.
57. [57] Enghard, P., et al. CXCR3+CD4+ T cells are enriched in inflamed kidneys and urine and provide a new biomarker for acute nephritis flares in systemic lupus erythematosus patients. Arthritis Rheum. 60:1 (2009), 199–206.
58. [58] Crispin, J.C., Tsokos, G.C., Human TCR-alpha beta+ CD4- CD8- T cells can derive from CD8+ T cells and display an inflammatory effector phenotype. J. Immunol. 183:7 (2009), 4675–4681.
59. [59] Crispin, J.C., et al. Expanded double negative T cells in patients with systemic lupus erythematosus produce IL-17 and infiltrate the kidneys. J. Immunol. 181:12 (2008), 8761–8766.
60. [60] Molad, Y., et al. Increased ERK and JNK activities correlate with disease activity in patients with systemic lupus erythematosus. Ann. Rheum. Dis. 69:1 (2010), 175–180.