657
Views
8
CrossRef citations to date
0
Altmetric
Reviews

Advances in applying of multi-omics approaches in the research of systemic lupus erythematosus

Summarization of biomarkers from different omics, and discussion of challenges and advances in integrative analysis of multi-omics in SLE studies

, , , , , , , , , , , & show all
Pages 163-173 | Received 28 Jun 2019, Accepted 24 Feb 2020, Published online: 06 Mar 2020

References

  • Lipsky PE. Systemic lupus erythematosus: an autoimmune disease of B cell hyperactivity. Nat Immunol 2001;2(9):764–766. doi:10.1038/ni0901-764.
  • Borchers AT, Naguwa SM, Shoenfeld Y, et al. The geoepidemiology of systemic lupus erythematosus. Autoimmun Rev 2010;9(5):A277–A287. doi:10.1016/j.autrev.2009.12.008.
  • Lau CS, Yin G, Mok MY. Ethnic and geographical differences in systemic lupus erythematosus: an overview. Lupus 2006;15(11):715–719. doi:10.1177/0961203306072311.
  • Lateef A, Petri M. Unmet medical needs in systemic lupus erythematosus. Arthritis Res Ther 2012;14:1–9. doi:10.1186/ar3919.
  • Liu J, Ni J, Li L, et al. Decreased UBASH3A mRNA expression levels in peripheral blood mononuclear cells from patients with systemic lupus erythematosus. Inflammation 2015;38(5):1903–1910. doi:10.1007/s10753-015-0170-9.
  • Xu W, Chen D, Li R, et al. Elevated plasma levels of TL1A in newly diagnosed systemic lupus erythematosus patients. Rheumatol Int 2015;35(8):1435–1437. doi:10.1007/s00296-015-3277-2.
  • Lu M, Wang J, Pan H, et al. Increased serum RANTES in patients with systemic lupus erythematosus. Rheumatol Int 2012;32(5):1231–1233. doi:10.1007/s00296-010-1761-2.
  • Akula SP, Miriyala RN, Thota H, et al. Techniques for integrating-omics data. Bioinformation 2009;3(6):284–286. doi:10.6026/97320630003284.
  • Mcgarry K, Garfield S, Morris NJ. Recent trends in knowledge and data integration for the life sciences. Expert Syst 2006;23(5):330–341. doi:10.1111/j.1468-0394.2006.00414.x.
  • Morris DL, Sheng Y, Zhang Y, et al. Genome-wide association meta-analysis in Chinese and European individuals identifies ten new loci associated with systemic lupus erythematosus. Nat Genet 2016;48(8):940–946. doi:10.1038/ng.3603.
  • Almlöf JC, Nystedt S, Leonard D, et al. Whole-genome sequencing identifies complex contributions to genetic risk by variants in genes causing monogenic systemic lupus erythematosus. Hum Genet 2019;138(2):141–150. doi:10.1007/s00439-018-01966-7.
  • Roberts AL, Thomas ER, Bhosle S, et al. Resequencing the susceptibility gene, ITGAM, identifies two functionally deleterious rare variants in systemic lupus erythematosus cases. Arthr Res Ther 2014;16(3):R114. doi:10.1186/ar4566.
  • Blalock ES, Barwick B, Jenks S, Neary B, Boss J, Sanz I. B cell subsets are epigenetically and transcriptionally dysregulated in systemic lupus erythematosus: abstract number: 1073. Arthr Rheumatol 2015;67:1400–1401.
  • Chung SA, Nititham J, Elboudwarej E, et al. Genome-wide assessment of differential DNA methylation associated with autoantibody production in systemic lupus erythematosus. PLoS One 2015;10(7):e0129813. doi:10.1371/journal.pone.0129813.
  • Mok A, Solomon O, Nayak RR, et al. Genome-wide profiling identifies associations between lupus nephritis and differential methylation of genes regulating tissue hypoxia and type 1 interferon responses. Lupus Sci Med 2016;3:e000183. doi:10.1136/lupus-2016-000183.
  • Imgenbergkreuz J, Almlof JC, Leonard D, et al. DNA methylation mapping identifies gene regulatory effects in patients with systemic lupus erythematosus. Ann Rheum Dis 2018;77:736–743. doi:10.1136/annrheumdis-2017-212379.
  • Barski A, Cuddapah S, Cui K, et al. High-resolution profiling of histone methylations in the human genome. Cell 2007;129(4):823–837. doi:10.1016/j.cell.2007.05.009.
  • Huiyuen J, Zhu L, Wong LP, et al. Chromatin landscapes and genetic risk in systemic lupus. Arthr Res Ther 2016;18:281–281. doi:10.1186/s13075-016-1169-9.
  • Zhe Z, Shi L, Song L, et al. Overall downregulation of mRNAs and enrichment of H3K4me3 change near genome-wide association study signals in systemic lupus erythematosus: cell-specific effects. Front Immunol 2018;9:497. doi:10.3389/fimmu.2018.00497.
  • Scharer CD, Blalock EL, Barwick BG, et al. ATAC-seq on biobanked specimens defines a unique chromatin accessibility structure in naïve SLE B cells. Sci Rep 2016;6(1):27030. doi:10.1038/srep27030.
  • Crow MK, Wohlgemuth J. Microarray analysis of gene expression in lupus. Arthr Res Ther 2003;5:279–287. doi:10.1186/ar1015.
  • Han GM, Chen SL, Shen N, et al. Analysis of gene expression profiles in human systemic lupus erythematosus using oligonucleotide microarray. Genes Immun 2003;4(3):177–186. doi:10.1038/sj.gene.6363966.
  • Odhams CA, Cortini A, Chen L, et al. Mapping eQTLs with RNA-seq reveals novel susceptibility genes, non-coding RNAs and alternative-splicing events in systemic lupus erythematosus . Hum Mol Genet 2017;26(5):1003–1017. doi:10.1093/hmg/ddw417.
  • Nicolaou O, Kousios A, Hadjisavvas A, et al. Biomarkers of systemic lupus erythematosus identified using mass spectrometry-based proteomics: a systematic review. J Cell Mol Med 2017;21(5):993–1012. doi:10.1111/jcmm.13031.
  • Li Q, Zhou J, Lian Y, et al. Interferon signature gene expression is correlated with autoantibody profiles in patients with incomplete lupus syndromes. Clin Exp Immunol 2010;159(3):281–291. doi:10.1111/j.1365-2249.2009.04057.x.
  • Fattal I, Shental N, Mevorach D, et al. An antibody profile of systemic lupus erythematosus detected by antigen microarray. Immunology 2010;130(3):337–343. doi:10.1111/j.1365-2567.2010.03245.x.
  • Yan B, Huang J, Zhang C, et al. Serum metabolomic profiling in patients with systemic lupus erythematosus by GC/MS. Mod Rheumatol 2016;26(6):914–922. doi:10.3109/14397595.2016.1158895.
  • Bengtsson AA, Trygg J, Wuttge DM, et al. Metabolic profiling of systemic lupus erythematosus and comparison with primary Sjögren’s syndrome and systemic sclerosis. PLoS One 2016;11(7):e0159384. doi:10.1371/journal.pone.0159384.
  • Chung CP, Oeser A, Raggi P, et al. Lipoprotein subclasses and particle size determined by nuclear magnetic resonance spectroscopy in systemic lupus erythematosus. Clin Rheumatol 2008;27(10):1227–1233. doi:10.1007/s10067-008-0890-4.
  • Xinghong D, Jinbo H, Chengping W, et al. Rapid resolution liquid chromatography coupled with quadrupole time-of-flight mass spectrometry-based metabolomics approach to study the effects of jieduquyuziyin prescription on systemic lupus erythematosus. PLoS One 2014;9:e88223.
  • Madda R, Lin SC, Sun WH, et al. Plasma proteomic analysis of systemic lupus erythematosus patients using liquid chromatography/tandem mass spectrometry with label-free quantification. PeerJ 2018;6:e4730. doi:10.7717/peerj.4730.
  • Koboldt DC, Steinberg KM, Larson DE, et al. The next-generation sequencing revolution and its impact on genomics. Cell 2013;155(1):27–38. doi:10.1016/j.cell.2013.09.006.
  • Fronek Z, Timmerman LA, Alper CA, et al. Major histocompatibility complex genes and susceptibility to systemic lupus erythematosus. Arthr Rheum 1990;33:1542–1553. doi:10.1002/art.1780331012.
  • Harley JB, Alarconriquelme ME, Criswell LA, et al. Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci. Nat Genet 2008;40(2):204–210. doi:10.1038/ng.81.
  • Fernando MMA, Freudenberg J, Lee AT, et al. Transancestral mapping of the MHC region in systemic lupus erythematosus identifies new independent and interacting loci at MSH5, HLA-DPB1 and HLA-G. Ann Rheum Dis 2012;71(5):777–784. doi:10.1136/annrheumdis-2011-200808.
  • Arriens C, Mohan C. Systemic lupus erythematosus diagnostics in the ‘omics’ era. Int J Clin Rheumtol 2013;8(6):671–687. doi:10.2217/ijr.13.59.
  • Teruel M, Chamberlain C, Alarcón-Riquelme ME. Omics studies: their use in diagnosis and reclassification of SLE and other systemic autoimmune diseases. Rheumatology 2017;56(suppl_1):i78–i87. doi:10.1093/rheumatology/kew339.
  • Chen L, Morris DL, Vyse TJ. Genetic advances in systemic lupus erythematosus: an update. Curr Opin Rheumatol 2017;29(5):423–433. doi:10.1097/BOR.0000000000000411.
  • Bengtsson AA, Ronnblom L. Systemic lupus erythematosus: still a challenge for physicians. J Intern Med 2017;281(1):52–64. doi:10.1111/joim.12529.
  • Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol 2010;28(10):1057–1068. doi:10.1038/nbt.1685.
  • Sui W, Tan Q, Yang M, et al. Genome-wide analysis of 5-hmC in the peripheral blood of systemic lupus erythematosus patients using an hMeDIP-chip. Int J Mol Med 2015;35:1467. doi:10.3892/ijmm.2015.2149.
  • Dai Y, Zhang L, Hu C, Zhang Y. Genome-wide analysis of histone H3 lysine 4 trimethylation by ChIP-chip in peripheral blood mononuclear cells of systemic lupus erythematosus patients. Clin Exp Rheumatol 2010;28(2):158–168.
  • Dai Y, Huang Y-S, Tang M, et al. Microarray analysis of microRNA expression in peripheral blood cells of systemic lupus erythematosus patients. Lupus 2007;16(12):939–946. doi:10.1177/0961203307084158.
  • Wang H, Peng W, Ouyang X, et al. Circulating microRNAs as candidate biomarkers in patients with systemic lupus erythematosus. Transl Res 2012;160(3):198–206. doi:10.1016/j.trsl.2012.04.002.
  • Wenbiao C, Kuibi T, Jianrong H. Analysis of microRNAs in patients with systemic lupus erythematosus, using Solexa deep sequencing. Connect Tissue Res 2014;55:187–196.
  • Dai Y, Sui W, Lan H, et al. Comprehensive analysis of microRNA expression patterns in renal biopsies of lupus nephritis patients. Rheumatol Int 2009;29(7):749–754. doi:10.1007/s00296-008-0758-6.
  • Richardson B. DNA methylation and autoimmune disease. Clin Immunol 2003;109(1):72–79. doi:10.1016/S1521-6616(03)00206-7.
  • Lee W-W, Yang Z-Z, Li G, et al. Unchecked CD70 expression on T cells lowers threshold for T cell activation in rheumatoid arthritis. J Immunol 2007;179(4):2609–2615. doi:10.4049/jimmunol.179.4.2609.
  • Lu Q, Wu A, Tesmer L, et al. Demethylation of CD40LG on the inactive X in t cells from women with lupus. J Immunol 2007;179(9):6352–6358. doi:10.4049/jimmunol.179.9.6352.
  • Ding S, Liang Y, Zhao M, et al. Decreased microRNA‐142‐3p/5p expression causes CD4+ T cell activation and B cell hyperstimulation in systemic lupus erythematosus. Arthr Rheum 2012;64:2953–2963. doi:10.1002/art.34505.
  • Stagakis E, Bertsias G, Verginis P, et al. Identification of novel microRNA signatures linked to human lupus disease activity and pathogenesis: miR-21 regulates aberrant T cell responses through regulation of PDCD4 expression. Ann Rheum Dis 2011;70(8):1496–1506. doi:10.1136/ard.2010.139857.
  • Zhao X, Tang Y, Qu B, et al. MicroRNA-125a contributes to elevated inflammatory chemokine RANTES levels via targeting KLF13 in systemic lupus erythematosus. Arthr Rheum 2010;62:3425–3435. doi:10.1002/art.27632.
  • Tang Y, Luo X, Cui H, et al. MicroRNA-146a contributes to abnormal activation of the type I interferon pathway in human lupus by targeting the key signaling proteins. Arthr Rheum 2009;60:1065–1075. doi:10.1002/art.24436.
  • Zhang X, Ma H, Huang J, et al. Characterization of the phosphoproteome in SLE patients. PLoS One 2012;7(12):e53129. doi:10.1371/journal.pone.0053129.
  • Mutz K, Heilkenbrinker A, Lonne M, et al. Transcriptome analysis using next-generation sequencing. Curr Opin Biotechnol 2013;24(1):22–30. doi:10.1016/j.copbio.2012.09.004.
  • Malone JH, Oliver B. Microarrays, deep sequencing and the true measure of the transcriptome. BMC Biol 2011;9(1):34–34. doi:10.1186/1741-7007-9-34.
  • Zhao M, Liu S, Luo S, et al. DNA methylation and mRNA and microRNA expression of SLE CD4+ T cells correlate with disease phenotype. J Autoimmun 2014;54:127–136. doi:10.1016/j.jaut.2014.07.002.
  • Wright HL, Thomas HB, Moots RJ, et al. Interferon gene expression signature in rheumatoid arthritis neutrophils correlates with a good response to TNFi therapy. Rheumatology 2015;54(1):188–193. doi:10.1093/rheumatology/keu299.
  • Frangou E, Grigorioy M, Banos A, et al. PS2:38 Comparative tissue transcriptome analysis by next-generation sequencing reveals novel pathways that characterise genetic susceptibility and developmental biology in systemic lupus erythematosus (sle). Lupus Sci Med 2018;5:A51. doi:10.1136/lupus-2018-abstract.86.
  • Rai R, Chauhan SK, Singh VV, et al. RNA-seq analysis reveals unique transcriptome signatures in systemic lupus erythematosus patients with distinct autoantibody specificities. PLoS One 2016;11(11):e0166312. doi:10.1371/journal.pone.0166312.
  • Sui W, Lin H, Chen J, et al. Comprehensive analysis of transcription factor expression patterns in peripheral blood mononuclear cell of systemic lupus erythematosus. Int J Rheum Dis 2012;15(2):212–219. doi:10.1111/j.1756-185X.2012.01718.x.
  • Dai Y, Hu C, Wang L, et al. Serum peptidome patterns of human systemic lupus erythematosus based on magnetic bead separation and MALDI-TOF mass spectrometry analysis. Scand J Rheumatol 2010;39(3):240–246. doi:10.3109/03009740903456292.
  • Mosley K, Tam FWK, Edwards RJ, et al. Urinary proteomic profiles distinguish between active and inactive lupus nephritis. Rheumatology 2006;45(12):1497–1504. doi:10.1093/rheumatology/kel351.
  • Fang S, Zeng F, Guo Q. Comparative proteomics analysis of cytokeratin and involucrin expression in lesions from patients with systemic lupus erythematosus. Acta Biochim Biophys Sin 2008;40(12):989–995. doi:10.1111/j.1745-7270.2008.00484.x.
  • Qi S, Chen Q, Xu D, et al. Clinical application of protein biomarkers in lupus erythematosus and lupus nephritis. Lupus 2018;27(10):1582–1590. doi:10.1177/0961203318773643.
  • Weiguo S, Donge T, Guimian Z, et al. Differential proteomic analysis of renal tissue in lupus nephritis using iTRAQ reagent technology. Rheumatol Int 2012;32:3537–3543.
  • Dai Y, Hu C, Huang Y, et al. A proteomic study of peripheral blood mononuclear cells in systemic lupus erythematosus. Lupus 2008;17(9):799–804. doi:10.1177/0961203308089444.
  • Wang L, Dai Y, Qi S, et al. Comparative proteome analysis of peripheral blood mononuclear cells in systemic lupus erythematosus with iTRAQ quantitative proteomics. Rheumatol Int 2012;32(3):585–593. doi:10.1007/s00296-010-1625-9.
  • Johnson CH, Ivanisevic J, Siuzdak G. Metabolomics: beyond biomarkers and towards mechanisms. Nat Rev Mol Cell Biol 2016;17(7):451–459. doi:10.1038/nrm.2016.25.
  • Chan ECY, Koh PK, Mal M, et al. Metabolic profiling of human colorectal cancer using high-resolution magic angle spinning nuclear magnetic resonance (HR-MAS NMR) spectroscopy and gas chromatography mass spectrometry (GC/MS). J Proteome Res 2009;8(1):352–361. doi:10.1021/pr8006232.
  • Giera M, Ioan-Facsinay A, Toes R, et al. Lipid and lipid mediator profiling of human synovial fluid in rheumatoid arthritis patients by means of LC-MS/MS. Biochim Biophys Acta 2012;1821(11):1415–1424. doi:10.1016/j.bbalip.2012.07.011.
  • Ouyang X, Dai Y, Wen J, et al. 1H NMR-based metabolomic study of metabolic profiling for systemic lupus erythematosus. Lupus 2011;20(13):1411–1420. doi:10.1177/0961203311418707.
  • Romickrosendale LE, Brunner HI, Bennett MR, et al. Identification of urinary metabolites that distinguish membranous lupus nephritis from proliferative lupus nephritis and focal segmental glomerulosclerosis. Arthr Res Ther 2011;13:1–10. doi:10.1186/ar3530.
  • Guleria A, Pratap A, Dubey D, et al. NMR based serum metabolomics reveals a distinctive signature in patients with lupus nephritis. Sci Rep 2016;6(1):35309. doi:10.1038/srep35309.
  • Yan B, Huang J, Dong F, et al. Urinary metabolomic study of systemic lupus erythematosus based on gas chromatography/mass spectrometry. Biomed Chromatogr 2016;30(11):1877–1881. doi:10.1002/bmc.3734.
  • Tianfu W, Chun X, Jie H, et al. Metabolic disturbances associated with systemic lupus erythematosus. PLoS One 2012;7:e37210. doi:10.1371/journal.pone.0037210.
  • Karczewski KJ, Snyder M. Integrative omics for health and disease. Nat Rev Genet 2018;19(5):299–310. doi:10.1038/nrg.2018.4.
  • Sui W, Lin H, Peng W, et al. Molecular dysfunctions in acute rejection after renal transplantation revealed by integrated analysis of transcription factor, microRNA and long noncoding RNA. Genomics 2013;102(4):310–322. doi:10.1016/j.ygeno.2013.05.002.
  • Tang D, Chen Y, He H, et al. Integrated analysis of mRNA, microRNA and protein in systemic lupus erythematosus-specific induced pluripotent stem cells from urine. BMC Genomics 2016;17(1):15. doi:10.1186/s12864-016-2809-9.
  • Liang Y, Xie S, Wu C, et al. Coagulation cascade and complement system in systemic lupus erythematosus. Oncotarget 2017;9:14862–14881. doi:10.18632/oncotarget.23206.
  • Vielhauer V, Anders H-J, Schlöndorff D. Chemokines and chemokine receptors as therapeutic targets in lupus nephritis. Semin Nephrol 2007;27(1):81–97. doi:10.1016/j.semnephrol.2006.09.010.
  • Linge P, Fortin PR, Lood C, et al. The non-haemostatic role of platelets in systemic lupus erythematosus. Nat Rev Rheumatol 2018;14(4):195–213. doi:10.1038/nrrheum.2018.38.
  • Kyttaris VC, Wang Y, Juang Y-T, et al. Increased levels of NF-ATc2 differentially regulate CD154 and IL-2 genes in t cells from patients with systemic lupus erythematosus. J Immunol 2007;178(3):1960–1966. doi:10.4049/jimmunol.178.3.1960.
  • Wang X, Huang W, Schiffer LE, et al. Effects of anti-CD154 treatment on B cells in murine systemic lupus erythematosus. Arthr Rheumatol 2003;48:495–506. doi:10.1002/art.10929.
  • Ohl K, Tenbrock K. Inflammatory cytokines in systemic lupus erythematosus. BioMed Res Int 2011;2011:432595. doi:10.1155/2011/432595.
  • Sun YV, Hu Y. Integrative analysis of multi-omics data for discovery and functional studies of complex human diseases. Adv Genet 2016;93:147–190. doi:10.1016/bs.adgen.2015.11.004.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.