Genomics & Informatics

Korea Genome Organization (한국유전체학회)
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MicroRNAs in Autoimmune Sjögren's Syndrome

  • Cha, Seunghee (Department of Oral and Maxillofacial Diagnostic Sciences, College of Dentistry, University of Florida) ;
  • Mona, Mahmoud (Department of Oral and Maxillofacial Diagnostic Sciences, College of Dentistry, University of Florida) ;
  • Lee, Kyung Eun (Department of Oral Medicine, School of Dentistry, Chonbuk National University) ;
  • Kim, Dong Hee (Department of Anesthesiology and Pain Management, College of Medicine, Dankook University) ;
  • Han, Kyudong (Department of Nanobiomedical Science and BK21 PLUS NBM Global Research Center for Regenerative Medicine, Dankook University)
  • Received : 2018.07.24
  • Accepted : 2018.09.17
  • Published : 2018.12.31
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Abstract

MicroRNAs (miRNAs), small non-coding RNAs, have been implicated in various diseases and cellular functions as microregulators of gene expression. Although the history of miRNA investigation in autoimmune $Sj{\ddot{o}}gren^{\prime}s$ syndrome (SjS) is fairly short, a substantial amount of data has already been accumulated. These findings clearly indicate potential clinical implications of miRNAs, such as autoantigen expression and autoantibody production, viral miRNAs regulating the calcium signaling pathway, and aberrant immune cell regulation and cytokine production. Research endeavors in the field are currently underway to select disease-specific diagnostic and prognostic biomarkers by utilizing different types of tissues or biological specimens of SjS patients. Various techniques for miRNA analysis with different stringencies have been applied, with the most recent one being next-generation sequencing. This review compiles and highlights differentially-expressed miRNAs in various samples collected from SjS patients and their potential implications in the pathogenesis of SjS. To facilitate the development of miRNA-targeted personalized therapy in the future, we urge more follow-up studies that confirm these findings and elucidate the immunopathological roles of differentially-expressed miRNAs. Furthermore, improved diagnostic criteria for the disease itself will minimize sampling errors in patient recruitment, preventing the generation of inconsistent data.

Keywords

References

  1. Chen JQ, Papp G, Szodoray P, Zeher M. The role of microRNAs in the pathogenesis of autoimmune diseases. Autoimmun Rev 2016;15:1171-1180. https://doi.org/10.1016/j.autrev.2016.09.003
  2. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009;19:92-105.
  3. Ramos-Casals M, Brito-Zeron P, Seror R, Bootsma H, Bowman SJ, Dorner T, et al. Characterization of systemic disease in primary Sjogren's syndrome: EULAR-SS Task Force recommendations for articular, cutaneous, pulmonary and renal involvements. Rheumatology (Oxford) 2015;54:2230-2238. https://doi.org/10.1093/rheumatology/kev200
  4. Karageorgas T, Fragioudaki S, Nezos A, Karaiskos D, Moutsopoulos HM, Mavragani CP. Fatigue in primary Sjogren's syndrome: clinical, laboratory, psychometric, and biologic associations. Arthritis Care Res (Hoboken) 2016;68:123-131. https://doi.org/10.1002/acr.22720
  5. Kocer B, Tezcan ME, Batur HZ, Haznedaroglu S, Goker B, Irkec C, et al. Cognition, depression, fatigue, and quality of life in primary Sjogren's syndrome: correlations. Brain Behav 2016;6:e00586. https://doi.org/10.1002/brb3.586
  6. Vitali C, Bombardieri S, Jonsson R, Moutsopoulos HM, Alexander EL, Carsons SE, et al. Classification criteria for Sjogren's syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis 2002;61:554-558. https://doi.org/10.1136/ard.61.6.554
  7. Shiboski SC, Shiboski CH, Criswell L, Baer A, Challacombe S, Lanfranchi H, et al. American College of Rheumatology classification criteria for Sjogren's syndrome: a data-driven, expert consensus approach in the Sjogren's International Collaborative Clinical Alliance cohort. Arthritis Care Res (Hoboken) 2012;64:475-487. https://doi.org/10.1002/acr.21591
  8. Shiboski CH, Shiboski SC, Seror R, Criswell LA, Labetoulle M, Lietman TM, et al. 2016 American College of Rheumatology/European League Against Rheumatism classification criteria for primary Sjogren's syndrome: a consensus and data-driven methodology involving three international patient cohorts. Ann Rheum Dis 2017;76:9-16. https://doi.org/10.1136/annrheumdis-2016-210571
  9. Chouri E, Servaas NH, Bekker CP, Affandi AJ, Cossu M, Hillen MR, et al. Serum microRNA screening and functional studies reveal miR-483-5p as a potential driver of fibrosis in systemic sclerosis. J Autoimmun 2018;89:162-170. https://doi.org/10.1016/j.jaut.2017.12.015
  10. Chen JQ, Papp G, Poliska S, Szabo K, Tarr T, Balint BL, et al. MicroRNA expression profiles identify disease-specific alterations in systemic lupus erythematosus and primary Sjogren's syndrome. PLoS One 2017;12:e0174585. https://doi.org/10.1371/journal.pone.0174585
  11. Szabo K, Papp G, Szanto A, Tarr T, Zeher M. A comprehensive investigation on the distribution of circulating follicular T helper cells and B cell subsets in primary Sjogren's syndrome and systemic lupus erythematosus. Clin Exp Immunol 2016;183:76-89. https://doi.org/10.1111/cei.12703
  12. Murata K, Yoshitomi H, Tanida S, Ishikawa M, Nishitani K, Ito H, et al. Plasma and synovial fluid microRNAs as potential biomarkers of rheumatoid arthritis and osteoarthritis. Arthritis Res Ther 2010;12:R86. https://doi.org/10.1186/ar3013
  13. Filkova M, Aradi B, Senolt L, Ospelt C, Vettori S, Mann H, et al. Association of circulating miR-223 and miR-16 with disease activity in patients with early rheumatoid arthritis. Ann Rheum Dis 2014;73:1898-1904. https://doi.org/10.1136/annrheumdis-2012-202815
  14. Jiang Z, Tao JH, Zuo T, Li XM, Wang GS, Fang X, et al. The correlation between miR-200c and the severity of interstitial lung disease associated with different connective tissue diseases. Scand J Rheumatol 2017;46:122-129. https://doi.org/10.3109/03009742.2016.1167950
  15. Alevizos I, Alexander S, Turner RJ, Illei GG. MicroRNA expression profiles as biomarkers of minor salivary gland inflammation and dysfunction in Sjogren's syndrome. Arthritis Rheum 2011;63:535-544.
  16. Kapsogeorgou EK, Gourzi VC, Manoussakis MN, Moutsopoulos HM, Tzioufas AG. Cellular microRNAs (miRNAs) and Sjogren's syndrome: candidate regulators of autoimmune response and autoantigen expression. J Autoimmun 2011;37:129-135. https://doi.org/10.1016/j.jaut.2011.05.003
  17. Gallo A, Tandon M, Alevizos I, Illei GG. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One 2012;7:e30679. https://doi.org/10.1371/journal.pone.0030679
  18. Williams AE, Choi K, Chan AL, Lee YJ, Reeves WH, Bubb MR, et al. Sjogren's syndrome-associated microRNAs in CD14(+) monocytes unveils targeted $TGF{\beta}$ signaling. Arthritis Res Ther 2016;18:95. https://doi.org/10.1186/s13075-016-0987-0
  19. Pauley KM, Stewart CM, Gauna AE, Dupre LC, Kuklani R, Chan AL, et al. Altered miR-146a expression in Sjogren's syndrome and its functional role in innate immunity. Eur J Immunol 2011;41:2029-2039. https://doi.org/10.1002/eji.201040757
  20. Gourzi VC, Kapsogeorgou EK, Kyriakidis NC, Tzioufas AG. Study of microRNAs (miRNAs) that are predicted to target the autoantigens Ro/SSA and La/SSB in primary Sjogren's Syndrome. Clin Exp Immunol 2015;182:14-22. https://doi.org/10.1111/cei.12664
  21. Tandon M, Gallo A, Jang SI, Illei GG, Alevizos I. Deep sequencing of short RNAs reveals novel microRNAs in minor salivary glands of patients with Sjogren's syndrome. Oral Dis 2012;18:127-131. https://doi.org/10.1111/j.1601-0825.2011.01849.x
  22. Gallo A, Jang SI, Ong HL, Perez P, Tandon M, Ambudkar I, et al. Targeting the Ca(2+) sensor STIM1 by exosomal transfer of Ebv-miR-BART13-3p is associated with Sjogren's syndrome. EBioMedicine 2016;10:216-226. https://doi.org/10.1016/j.ebiom.2016.06.041
  23. Martini D, Gallo A, Vella S, Sernissi F, Cecchettini A, Luciano N, et al. Cystatin S-a candidate biomarker for severity of submandibular gland involvement in Sjogren's syndrome. Rheumatology (Oxford) 2017;56:1031-1038. https://doi.org/10.1093/rheumatology/kew501
  24. Peng L, Ma W, Yi F, Yang YJ, Lin W, Chen H, et al. MicroRNA profiling in Chinese patients with primary Sjogren syndrome reveals elevated miRNA-181a in peripheral blood mononuclear cells. J Rheumatol 2014;41:2208-2213. https://doi.org/10.3899/jrheum.131154
  25. Wang-Renault SF, Boudaoud S, Nocturne G, Roche E, Sigrist N, Daviaud C, et al. Deregulation of microRNA expression in purified T and B lymphocytes from patients with primary Sjogren's syndrome. Ann Rheum Dis 2018;77:133-140. https://doi.org/10.1136/annrheumdis-2017-211417
  26. Mariette X, Gozlan J, Clerc D, Bisson M, Morinet F. Detection of Epstein-Barr virus DNA by in situ hybridization and polymerase chain reaction in salivary gland biopsy specimens from patients with Sjogren's syndrome. Am J Med 1991;90:286-294. https://doi.org/10.1016/0002-9343(91)90567-H
  27. Maitland N, Flint S, Scully C, Crean SJ. Detection of cytomegalovirus and Epstein-Barr virus in labial salivary glands in Sjogren's syndrome and non-specific sialadenitis. J Oral Pathol Med 1995;24:293-298. https://doi.org/10.1111/j.1600-0714.1995.tb01187.x
  28. Perrot S, Calvez V, Escande JP, Dupin N, Marcelin AG. Prevalences of herpesviruses DNA sequences in salivary gland biopsies from primary and secondary Sjogren's syndrome using degenerated consensus PCR primers. J Clin Virol 2003;28:165-168. https://doi.org/10.1016/S1386-6532(02)00277-9
  29. Wen S, Shimizu N, Yoshiyama H, Mizugaki Y, Shinozaki F, Takada K. Association of Epstein-Barr virus (EBV) with Sjogren's syndrome: differential EBV expression between epithelial cells and lymphocytes in salivary glands. Am J Pathol 1996;149:1511-1517.
  30. Karameris A, Gorgoulis V, Iliopoulos A, Frangia C, Kontomerkos T, Ioakeimidis D, et al. Detection of the Epstein Barr viral genome by an in situ hybridization method in salivary gland biopsies from patients with secondary Sjogren's syndrome. Clin Exp Rheumatol 1992;10:327-332.
  31. Pauley KM, Satoh M, Chan AL, Bubb MR, Reeves WH, Chan EK. Upregulated miR-146a expression in peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Res Ther 2008;10:R101. https://doi.org/10.1186/ar2493
  32. Tang Y, Luo X, Cui H, Ni X, Yuan M, Guo Y, et al. MicroRNA-146A contributes to abnormal activation of the type I interferon pathway in human lupus by targeting the key signaling proteins. Arthritis Rheum 2009;60:1065-1075. https://doi.org/10.1002/art.24436
  33. Zilahi E, Tarr T, Papp G, Griger Z, Sipka S, Zeher M. Increased microRNA-146a/b, TRAF6 gene and decreased IRAK1 gene expressions in the peripheral mononuclear cells of patients with Sjogren's syndrome. Immunol Lett 2012;141:165-168. https://doi.org/10.1016/j.imlet.2011.09.006
  34. Jacob CO, Zhu J, Armstrong DL, Yan M, Han J, Zhou XJ, et al. Identification of IRAK1 as a risk gene with critical role in the pathogenesis of systemic lupus erythematosus. Proc Natl Acad Sci U S A 2009;106:6256-6261. https://doi.org/10.1073/pnas.0901181106
  35. Chung JW, Jeong SH, Lee SM, Pak JH, Lee GH, Jeong JY, et al. Expression of microRNA in host cells infected with Helicobacter pylori. Gut Liver 2017;11:392-400. https://doi.org/10.5009/gnl16265
  36. Palmer JD, Soule BP, Simone BA, Zaorsky NG, Jin L, Simone NL. MicroRNA expression altered by diet: can food be medicinal? Ageing Res Rev 2014;17:16-24. https://doi.org/10.1016/j.arr.2014.04.005
  37. Yang J, Zhang L, Yu C, Yang XF, Wang H. Monocyte and macrophage differentiation: circulation inflammatory monocyte as biomarker for inflammatory diseases. Biomark Res 2014;2:1. https://doi.org/10.1186/2050-7771-2-1
  38. Yoshimoto K, Tanaka M, Kojima M, Setoyama Y, Kameda H, Suzuki K, et al. Regulatory mechanisms for the production of BAFF and IL-6 are impaired in monocytes of patients of primary Sjogren's syndrome. Arthritis Res Ther 2011;13:R170. https://doi.org/10.1186/ar3493
  39. Brkic Z, Maria NI, van Helden-Meeuwsen CG, van de Merwe JP, van Daele PL, Dalm VA, et al. Prevalence of interferon type I signature in CD14 monocytes of patients with Sjogren's syndrome and association with disease activity and BAFF gene expression. Ann Rheum Dis 2013;72:728-735. https://doi.org/10.1136/annrheumdis-2012-201381
  40. Wildenberg ME, van Helden-Meeuwsen CG, van de Merwe JP, Drexhage HA, Versnel MA. Systemic increase in type I interferon activity in Sjogren's syndrome: a putative role for plasmacytoid dendritic cells. Eur J Immunol 2008;38:2024-2033. https://doi.org/10.1002/eji.200738008
  41. Lisi S, Sisto M, Lofrumento DD, D'Amore M. Altered $I{\kappa}B{\alpha}$ expression promotes $NF-{\kappa}B$ activation in monocytes from primary Sjogren's syndrome patients. Pathology 2012;44:557-561. https://doi.org/10.1097/PAT.0b013e3283580388
  42. Hauk V, Fraccaroli L, Grasso E, Eimon A, Ramhorst R, Hubscher O, et al. Monocytes from Sjogren's syndrome patients display increased vasoactive intestinal peptide receptor 2 expression and impaired apoptotic cell phagocytosis. Clin Exp Immunol 2014;177:662-670. https://doi.org/10.1111/cei.12378
  43. Wildenberg ME, Welzen-Coppens JM, van Helden-Meeuwsen CG, Bootsma H, Vissink A, van Rooijen N, et al. Increased frequency of CD16+ monocytes and the presence of activated dendritic cells in salivary glands in primary Sjogren syndrome. Ann Rheum Dis 2009;68:420-426. https://doi.org/10.1136/ard.2008.087874
  44. Chen W, Cao H, Lin J, Olsen N, Zheng SG. Biomarkers for primary Sjogren's syndrome. Genomics Proteomics Bioinformatics 2015;13:219-223. https://doi.org/10.1016/j.gpb.2015.06.002
  45. Deutsch O, Krief G, Konttinen YT, Zaks B, Wong DT, Aframian DJ, et al. Identification of Sjogren's syndrome oral fluid biomarker candidates following high-abundance protein depletion. Rheumatology (Oxford) 2015;54:884-890. https://doi.org/10.1093/rheumatology/keu405
  46. Delaleu N, Mydel P, Kwee I, Brun JG, Jonsson MV, Jonsson R. High fidelity between saliva proteomics and the biologic state of salivary glands defines biomarker signatures for primary Sjogren's syndrome. Arthritis Rheumatol 2015;67:1084-1095. https://doi.org/10.1002/art.39015
  47. Hamm-Alvarez SF, Janga SR, Edman MC, Madrigal S, Shah M, Frousiakis SE, et al. Tear cathepsin S as a candidate biomarker for Sjogren's syndrome. Arthritis Rheumatol 2014;66:1872-1881. https://doi.org/10.1002/art.38633
  48. Maria NI, Brkic Z, Waris M, van Helden-Meeuwsen CG, Heezen K, van de Merwe JP, et al. MxA as a clinically applicable biomarker for identifying systemic interferon type I in primary Sjogren's syndrome. Ann Rheum Dis 2014;73:1052-1059.
  49. Tobon GJ, Saraux A, Gottenberg JE, Quartuccio L, Fabris M, Seror R, et al. Role of Fms-like tyrosine kinase 3 ligand as a potential biologic marker of lymphoma in primary Sjogren's syndrome. Arthritis Rheum 2013;65:3218-3227. https://doi.org/10.1002/art.38129
  50. Kramer JM, Klimatcheva E, Rothstein TL. CXCL13 is elevated in Sjogren's syndrome in mice and humans and is implicated in disease pathogenesis. J Leukoc Biol 2013;94:1079-1089. https://doi.org/10.1189/jlb.0113036
  51. Brkic Z, Versnel MA. Type I IFN signature in primary Sjogren's syndrome patients. Expert Rev Clin Immunol 2014;10:457-467. https://doi.org/10.1586/1744666X.2014.876364
  52. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 1999;94:3791-3799.
  53. Ajit SK. Circulating microRNAs as biomarkers, therapeutic targets, and signaling molecules. Sensors (Basel) 2012;12:3359-3369. https://doi.org/10.3390/s120303359
  54. Natasha G, Gundogan B, Tan A, Farhatnia Y, Wu W, Rajadas J, et al. Exosomes as immunotheranostic nanoparticles. Clin Ther 2014;36:820-829. https://doi.org/10.1016/j.clinthera.2014.04.019
  55. Rekker K, Saare M, Roost AM, Kubo AL, Zarovni N, Chiesi A, et al. Comparison of serum exosome isolation methods for microRNA profiling. Clin Biochem 2014;47:135-138.
  56. Tan L, Wu H, Liu Y, Zhao M, Li D, Lu Q. Recent advances of exosomes in immune modulation and autoimmune diseases. Autoimmunity 2016;49:357-365. https://doi.org/10.1080/08916934.2016.1191477
  57. Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res 2011;39:7223-7233. https://doi.org/10.1093/nar/gkr254
  58. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A 2011;108:5003-5008. https://doi.org/10.1073/pnas.1019055108
  59. Shomron N, Levy C. MicroRNA-biogenesis and pre-mRNA splicing crosstalk. J Biomed Biotechnol 2009;2009:594678.
  60. Basyuk E, Suavet F, Doglio A, Bordonne R, Bertrand E. Human let-7 stem-loop precursors harbor features of RNase III cleavage products. Nucleic Acids Res 2003;31:6593-6597. https://doi.org/10.1093/nar/gkg855
  61. Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, et al. The Microprocessor complex mediates the genesis of microRNAs. Nature 2004;432:235-240. https://doi.org/10.1038/nature03120