Please wait a minute...
Shopping Cart Email List Chinese
Advanced Search Fig/Tab
Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Featured Articles  |  Most Downloaded  |  Most Reading
Online Submission Subscribe to Our RSS Content Feed
Front. Biol.    2018, Vol. 13 Issue (1) : 28-35    https://doi.org/10.1007/s11515-017-1477-8
REVIEW
Threatening biomarkers in lupus pregnancy: Biochemistry and genetic challenges
Karim Mowla1, Elham Rajaei1, Mohammad Taha Jalali2, Zeinab Deris Zayeri1()
1. Golestan Hospital Clinical Research Development Unit, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
2. Hyperlipidemia Research Center, Diabetes Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
 Download: PDF(146 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

OBJECTIVES: Using genetic markers and miRs work strongly beside other sensitive biomarkers in lupus management during sensitive period of pregnancy.

METHOD: PubMed and Google Scholar databases were searched from 2000 to 2017 using the terms “lupus,” “lupus pregnancy,” “biomarkers,” “micro-RNA,” “polymorphisms,” “anti-phospholipid antibodies,” and “cluster differentiation markers.”

DISCUSSION: Complement is a valuable biomarker in lupus pregnancy. However, the complement profile has ambiguous meaning because decreased levels of C3 and C4 reflect inflammation and because they are also prognostic biomarkers for abortion. Furthermore, increased C3 and C4 levels indicate hepatic protein synthesis in hepatocytes. Anti-phospholipid (APL) antibodies are present in 25% to 50% of lupus patients, and can lead to thrombotic and obstetric complications in some pregnancies and increase the risk of abortion, especially in a pregnant woman in the active phase of lupus. Several studies have associated APL with HELLP syndrome. However, other pregnancy complications have not been associated with APL. Autoantibodies against the major vault protein and anti-double strand DNA antibodies are valuable biomarkers in evaluating lupus activity. The expression pattern of micro-RNAs (miRs) differs in various diseases. Current studies have demonstrated the potential of miRs as diagnostic and prognostic biomarkers in various diseases; for example, the level of miR-126 is higher in lupus.

CONCLUSION: miR-223-3p and miR-451 are informative biomarkers in estimating disease activity. TWEAK, BAFF, and APOL1 genes, and their polymorphisms are informative in estimating disease activity, especially renal effects, and in monitoring higher-risk pregnant women. Further studies of these genes and their relevant polymorphisms are needed.
Keywords lupus      biomarker      genetic      micro-RNA      anti-phospholipid antibodies     
Corresponding Author(s): Zeinab Deris Zayeri   
Online First Date: 31 January 2018    Issue Date: 26 March 2018
 Cite this article:   
Karim Mowla,Elham Rajaei,Mohammad Taha Jalali, et al. Threatening biomarkers in lupus pregnancy: Biochemistry and genetic challenges[J]. Front. Biol., 2018, 13(1): 28-35.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-017-1477-8
https://academic.hep.com.cn/fib/EN/Y2018/V13/I1/28
miR Upregulation Downregulation Role Reference
miR-21 * Increased plasma miR-21 levels are associated with C3 and C4 levels in LN. Guo et al., 2016
miR-451 * Overexpression of miR-451 attenuates glomerular damage. Sun et al., 2016
miR-223-3p * Correlates with lupus anticoagulant Kim et al., 2016a
miR-16 * Associated with primary Sjögren's syndrome Papp et al., 2017
miR-125a-3p * * Disease activity, treatment response Zeng et al., 2017
miR-155 * Pathophysiology of lupus; might be used as a biomarker. Urinary level can be a potent biomarker for disease activity and therapeutic responses. Wang et al., 2010, 2012a; Testa et al., 2017
miR-210 * Regulating
the expression of HIF-1a and the differentiation of Th17 may be involved in the development and function of the immune response.		 Huang et al., 2017
miR-146a * Increases phagocytic activity and suppresses inflammatory cytokine production. Urinary level can be a potent biomarker for disease activity and therapeutic responses. Disease severity Pauley et al., 2011; Lu et al., 2012; Wang et al., 2012a
miR-185 * Contributes to DNA hypomethylation of CD4+ T cells in pregnancies. miR-185 may represent a potential therapeutic target in lupus. Liu et al., 2016
miR-26a, miR-
30b, miR-4286,		 * Decrease in lupus nephritis Costa Reis et al., 2014
Tab.1  miRs associated with lupus and lupus activities
Gene Polymorphism Role Reference
ANKRD44 rs1429411 Primary disease pathogenesis, involved in INF-a production, have a high correlation with European INF-a Kariuki et al.,2015; Qian and Nan, 2017
PLEKHF2 rs297573 Associated with DC and NK cell function, involved in INF-a production, primary pathogenesis, associated with IFN-a (however, secondary to the serological association) Kariuki et al.,2015; Qian and Nan, 2017
Ox40 &Ox40L rs4810485 Ox40 &Ox40 ligand (Ox40L) are associated with lupus risk, and the NL phenotype Perricone et al., 2016; Sitrin et al., 2017
APOL1 G1/G2 alleles LN who progress ESRD in African-American population Freedman et al., 2014
BAFF insertion–deletion variant, GCTGT→A (in which A is the risk allele) Increase lupus risk Abnormal form of BAFF may also be a pathogenic factor lupus & NL. Kang et al.,2017; Mackay, 2017; Steri et al., 2017
TWEAK TWEAK/Fn14 Increased risk of atherosclerosis and activation was found in the lesion of CLE. Badawi et al.,2017; Liu et al., 2017
HER2 - Increase in LN Reis et al., 2017
Tab.2  Genes and polymorphisms associated with lupus and lupus activities
1 Araki Y,Mimura T (2017). The histone modification code in the pathogenesis of autoimmune diseases. Mediators Inflamm, 2017:2608605
2 Badawi A I, El-Hamid A M A, Mohamed N K, Darwish E M M, Wassef M, Elfirgani H (2017). Serum tumor necrosis factor (TNF)-like weak inducer of apoptosis (TWEAK) and leptin as biomarkers of accelerated atherosclerosis in patients with systemic lupus erythematosus and antiphospholipid syndrome. Egyptian Rheumatologist, 39(2): 75–81
https://doi.org/10.1016/j.ejr.2016.07.001
3 Balada E, Castro-Marrero J, Felip L, Ordi-Ros J, Vilardell-Tarrés M (2014). Clinical and serological findings associated with the expression of ITGAL, PRF1, and CD70 in systemic lupus erythematosus. Clin Exp Rheumatol, 32(1): 113–116
pmid: 24238281
4 Ball E M, Gibson D S, Bell A L, Rooney M R (2014). Plasma IL-6 levels correlate with clinical and ultrasound measures of arthritis in patients with systemic lupus erythematosus. Lupus, 23(1): 46–56
https://doi.org/10.1177/0961203313512882 pmid: 24243775
5 Blomjous B, Abheiden C, Kroese S, van Laar J, Derksen R, Bultink I, Voskuyl A, Lely A , de Boer M, de Vries J, Fritsch-Stork R(2017). OP0310 Pregnancy outcome in women with systemic lupus erythematosus, a multicenter cohort-study. Ann Rheum Dis, 76:184
6 Boh E E (2004). Neonatal lupus erythematosus. Clin Dermatol, 22(2): 125–128
https://doi.org/10.1016/j.clindermatol.2003.12.019 pmid: 15234013
7 Bramham K, Hunt B J, Germain S, Calatayud I, Khamashta M, Bewley S, Nelson-Piercy C (2010). Pregnancy outcome in different clinical phenotypes of antiphospholipid syndrome. Lupus, 19(1): 58–64
https://doi.org/10.1177/0961203309347794 pmid: 19897518
8 Brkic Z, Corneth O B, van Helden-Meeuwsen C G, Dolhain R J, Maria N I, Paulissen S M, Davelaar N, van Hamburg J P, van Daele P L, Dalm V A, van Hagen P M, Hazes J M, Versnel M A, Lubberts E (2014). T-helper 17 cell cytokines and interferon type I: partners in crime in systemic lupus erythematosus? Arthritis Res Ther, 16(2): R62
https://doi.org/10.1186/ar4499 pmid: 24598455
9 Budde P, Zucht H D, Schulte-Pelkum J, Wirtz D, Rengers P, Vordenbäumen S, Schneider M, Schulz-Knappe P (2017). 267 Novel autoantibodies against the interferon-responsive major vault protein (mvp) in systemic lupus erythmatosus. Lupus Sci Med, 4: doi: 10.1136/lupus-2017-000215.267
10 Chakravarty E F, Colón I, Langen E S, Nix D A, El-Sayed Y Y, Genovese M C, Druzin M L (2005). Factors that predict prematurity and preeclampsia in pregnancies that are complicated by systemic lupus erythematosus. Am J Obstet Gynecol, 192(6): 1897–1904
https://doi.org/10.1016/j.ajog.2005.02.063 pmid: 15970846
11 Chakravarty E F, Nelson L, Krishnan E (2006). Obstetric hospitalizations in the United States for women with systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum, 54(3): 899–907
https://doi.org/10.1002/art.21663 pmid: 16508972
12 Chamberlain C, Colman P J, Ranger A M, Burkly L C, Johnston G I, Otoul C, Stach C,Zamacona M, Dörner T, Urowitz M, Hiepe F (2017). Repeated administration of dapirolizumab pegol in a randomised phase I study is well tolerated and accompanied by improvements in several composite measures of systemic lupus erythematosus disease activity and changes in whole blood transcriptomic profiles. Ann Rheum Dis, 76(11):1837–1844
13 Clowse M E (2007). Lupus activity in pregnancy. Rheum Dis Clin North Am, 33(2): 237–252, v
https://doi.org/10.1016/j.rdc.2007.01.002 pmid: 17499705
14 Clowse M E, Wallace D J, Weisman M, James A, Criscione-Schreiber L G, Pisetsky D S (2013). Predictors of preterm birth in patients with mild systemic lupus erythematosus. Ann Rheum Dis, 72(9):1536-1539
15 Clowse M E, Magder L S, Petri M (2011). The clinical utility of measuring complement and anti-dsDNA antibodies during pregnancy in patients with systemic lupus erythematosus. J Rheumatol, 38(6):1012–1016
https://doi.org/10.3899/jrheum.100746
16 Costa Reis A P, Russo P, Gallucci S, Sullivan K E (2014). A150: Control of Cell Proliferation in Lupus Nephritis: The Role of miRNAs and HER2. Arthritis Rheumatol, 66(S3): S194
https://doi.org/10.1002/art.38571
17 de Leeuw K, Bungener L, Roozendaal C, Bootsma H, Stegeman C A(2017). Comment on: Auto-antibodies to double-stranded DNA as biomarker in SLE: comparison of different assays during quiescent and active disease. Rheumatology, 56(11): 2039–2040
https://doi.org/10.1093/rheumatology/kex314
18 Flechsig A, Rose T, Barkhudarova F, Strauss R, Klotsche J, Dähnrich C, Schlumberger W, Enghard P, Burmester G R, Hiepe F, Biesen R (2017). What is the clinical significance of anti-Sm antibodies in systemic lupus erythematosus? A comparison with anti-dsDNA antibodies and C3. Clin Exp Rheumatol, 35(4): 598–606
pmid: 28281463
19 Font J, Pallares L, Martorell J, Martinez E, Gaya A, Vives J, Ingelmo M (1996). Elevated soluble CD27 levels in serum of patients with systemic lupus erythematosus. Clin Immunol Immunopathol, 81(3): 239–243
https://doi.org/10.1006/clin.1996.0184 pmid: 8938100
20 Förger F, Matthias T, Oppermann M, Becker H, Helmke K (2004). Clinical significance of anti-dsDNA antibody isotypes: IgG/IgM ratio of anti-dsDNA antibodies as a prognostic marker for lupus nephritis. Lupus, 13(1): 36–44
https://doi.org/10.1191/0961203304lu485oa pmid: 14870916
21 Freedman B I, Langefeld C D, Andringa K K, Croker J A, Williams A H, Garner N E, Birmingham D J, Hebert L A, Hicks P J, Segal M S, Edberg J C, Brown E E, Alarcón G S, Costenbader K H, Comeau M E, Criswell L A, Harley J B, James J A, Kamen D L, Lim S S, Merrill J T, Sivils K L, Niewold T B, Patel N M, Petri M, Ramsey-Goldman R, Reveille J D, Salmon J E, Tsao B P, Gibson K L, Byers J R, Vinnikova A K, Lea J P, Julian B A, Kimberly R P, and the Lupus Nephritis–End‐Stage Renal Disease Consortium (2014). End-stage renal disease in African Americans with lupus nephritis is associated with APOL1. Arthritis Rheumatol, 66(2): 390–396
https://doi.org/10.1002/art.38220 pmid: 24504811
22 Guimarães P M, Macedo Guimarães P, Miglioranza Acavuzzi B, Frizon Alfieri D, Perugini Stadtlober N, Batisti Lozovoy M A, Vissoci Reiche E M, Kaminami Morimoto H, Delicato de Almeida E R, Mayumi Veiga Iriyoda T, Tomimura Costa N, Dichi I, Maes M (2017). 459 Systemic lupus erythematosus and severity of illness are associated with t helper 1 and 17 cytokines profiles together with a lowered il-4 production. Lupus Sci Med, 4:
https://doi.org/10.1136/lupus-2017-000215.459
23 Guo S, Ge S, Ku M, Shang W, Zeng R, Han M, Xu G, Rong S (2016). Clinical correlation of plasma miR-21, miR-126 and miR-148a in patients with lupus nephritis. Int J Clin Exp Med, 9(2): 2905–U7186
24 Heelan K, Watson R, Collins S M (2013). Neonatal lupus syndrome associated with ribonucleoprotein antibodies. Pediatr Dermatol, 30(4): 416–423
https://doi.org/10.1111/pde.12088 pmid: 23432184
25 Ho A, Barr S G, Magder L S, Petri M (2001). A decrease in complement is associated with increased renal and hematologic activity in patients with systemic lupus erythematosus. Arthritis Rheum, 44(10): 2350–2357
https://doi.org/10.1002/1529-0131(200110)44:10<2350::AID-ART398>3.0.CO;2-A pmid: 11665976
26 Huang Q, Chen S S, Li J, Tao S S, Wang M, Leng R X, Pan H F, Ye D Q (2017). miR-210 expression in PBMCs from patients with systemic lupus erythematosus and rheumatoid arthritis. Ir J Med Sci,
https://doi.org/10.1007/s11845-017-1634-8
27 Izmirly P M, Halushka M K, Rosenberg A Z, Whelton S, Rais-Bahrami K, Nath D S, Parton H, Clancy R M, Rasmussen S, Saxena A, Buyon J P (2017). Clinical and pathologic implications of extending the spectrum of maternal autoantibodies reactive with ribonucleoproteins associated with cutaneous and now cardiac neonatal lupus from SSA/Ro and SSB/La to U1RNP. Autoimmun Rev, 16(9): 980–983
https://doi.org/10.1016/j.autrev.2017.07.013 pmid: 28709760
28 Kaifu T, Nakamura A (2017). Polymorphisms of immunoglobulin receptors and the effects on clinical outcome in cancer immunotherapy and other immune diseases: a general review. Int Immunol, 29(7): 319–325
https://doi.org/10.1093/intimm/dxx041 pmid: 28910969
29 Kang S, Fedoriw Y, Brenneman E K, Truong Y K, Kikly K, Vilen B J (2017). BAFF Induces Tertiary Lymphoid Structures and Positions T Cells within the Glomeruli during Lupus Nephritis. J Immunol, 198(7): 2602–2611
https://doi.org/10.4049/jimmunol.1600281 pmid: 28235864
30 Kariuki S N, Ghodke-Puranik Y, Dorschner J M, Chrabot B S, Kelly J A, Tsao B P, Kimberly R P, Alarcón-Riquelme M E, Jacob C O, Criswell L A, Sivils K L, Langefeld C D, Harley J B, Skol A D, Niewold T B (2015). Genetic analysis of the pathogenic molecular sub-phenotype interferon-alpha identifies multiple novel loci involved in systemic lupus erythematosus. Genes Immun, 16(1): 15–23
https://doi.org/10.1038/gene.2014.57 pmid: 25338677
31 Keisa L, Boka O, Vitina S, Rezeberga D (2016). New onset of systemic lupus erythematosus during pregnancy. Int J Reprod Contracept Obstet Gynecol, 5(4): 1221–1224
https://doi.org/10.18203/2320-1770.ijrcog20160889
32 Kim B S, Jung J Y, Jeon J Y, Kim H A, Suh C H (2016a). Circulating hsa-miR-30e-5p, hsa-miR-92a-3p, and hsa-miR-223-3p may be novel biomarkers in systemic lupus erythematosus. HLA, 88(4): 187–193
https://doi.org/10.1111/tan.12874 pmid: 27596248
33 Kim K J, Baek I W, Yoon C H, Kim W U, Cho C S (2017). Elevated levels of soluble CD40 ligand are associated with antiphospholipid antibodies in patients with systemic lupus erythematosus. Clin Exp Rheumatol, 35(5): 823–830
pmid: 28421990
34 Kim M Y, Buyon J P, Guerra M M, Rana S, Zhang D, Laskin C A, Petri M, Lockshin M D, Sammaritano L R,Branch D W, Porter T F, Merrill J T, Stephenson M D, Gao Q, Karumanchi S A, Salmon J E(2016b). Angiogenic factor imbalance early in pregnancy predicts adverse outcomes in patients with lupus and antiphospholipid antibodies: results of the PROMISSE study. Am J Obstet Gynecol, 214(1):108.e1–108.e14
35 La Paglia G M C, Leone M C, Lepri G, Vagelli R, Valentini E, Alunno A, Tani C (2017). One year in review 2017: systemic lupus erythematosus. Clin Exp Rheumatol, 35(4): 551–561
pmid: 28721860
36 Lateef A, Petri M (2013). Managing lupus patients during pregnancy. Best Pract Res Clin Rheumatol, 27(3): 435–447
https://doi.org/10.1016/j.berh.2013.07.005 pmid: 24238698
37 Lateef A, Petri M (2017). Systemic Lupus Erythematosus and Pregnancy. Rheum Dis Clin North Am, 43(2): 215–226
https://doi.org/10.1016/j.rdc.2016.12.009 pmid: 28390564
38 Lazzaroni M, Andreoli L, Lupoli F, Aggogeri E, Bettiga E , Zatti S, Lojacono A, Ramazzotto F, Fredi M,Tincani A(2016). THU0300 Risk Factors for Adverse Pregnancy Outcome in First-Line Treated Pregnancies in Antiphospholipid Antibodies-Positive Women According To Different Treatment Strategies: Results from Our 30 Years’ Experience Pregnancy Clinic. Ann Rheum Dis, 75:295
39 Lazzaroni M, Andreoli L, Chighizola C B, Ross T D, M Gerosa (2017). OP0046 Risk factors for adverse pregnancy outcome in antiphospholipid antibodies carriers: results from a multicenter italian cohort over 20 years of experience. European Congress of Rheumatology, 70:1–70
40 Le Thi Thuong D, Tieulié N, Costedoat N, Andreu M R, Wechsler B, Vauthier-Brouzes D, Aumaître O, Piette J C (2005). The HELLP syndrome in the antiphospholipid syndrome: retrospective study of 16 cases in 15 women. Ann Rheum Dis, 64(2): 273–278
https://doi.org/10.1136/ard.2003.019000 pmid: 15647435
41 Linnik M D, Hu J Z, Heilbrunn K R, Strand V, Hurley F L, Joh T, and the LJP 394 Investigator Consortium (2005). Relationship between anti-double-stranded DNA antibodies and exacerbation of renal disease in patients with systemic lupus erythematosus. Arthritis Rheum, 52(4): 1129–1137
https://doi.org/10.1002/art.20980 pmid: 15818711
42 Liu E, Zhou Y, Liu Z, Wang L, Zhang Y, Han B, Ma H, Li S (2016). MicroRNA-185 contributes to DNA hypomethylation of CD4+ T cells in pregnant patients with systemic lupus erythematosus by targeting DNA methyltransferase 1. Int J Clin Exp Pathol, 9(8): 8181–8189
43 Liu Y, Xu M, Min X, Wu K, Zhang T, Li K, Xiao S, Xia Y (2017). TWEAK/Fn14 Activation Participates in Ro52-Mediated Photosensitization in Cutaneous Lupus Erythematosus. Front Immunol, 8: 651
https://doi.org/10.3389/fimmu.2017.00651 pmid: 28620393
44 Lu J, Kwan B C, Lai F M, Tam L S, Li E K, Chow K M, Wang G, Li P K, Szeto C C (2012). Glomerular and tubulointerstitial miR-638, miR-198 and miR-146a expression in lupus nephritis. Nephrology (Carlton), 17(4): 346–351
https://doi.org/10.1111/j.1440-1797.2012.01573.x pmid: 22295894
45 Lyn-Cook B D, Xie C, Oates J, Treadwell E, Word B, Hammons G, Wiley K (2014). Increased expression of Toll-like receptors (TLRs) 7 and 9 and other cytokines in systemic lupus erythematosus (SLE) patients: ethnic differences and potential new targets for therapeutic drugs. Mol Immunol, 61(1): 38–43
https://doi.org/10.1016/j.molimm.2014.05.001 pmid: 24865418
46 Mackay F (2017). 345 Deletion of the baff receptor taci fully protects against sle without reduction of b cell numbers and function. Lupus Sci Med, 4: doi:10.1136/lupus-2017-000215.345
47 Mankee A, Petri M, Magder L S (2015). Lupus anticoagulant, disease activity and low complement in the first trimester are predictive of pregnancy loss. Lupus Sci Med, 2(1): e000095
https://doi.org/10.1136/lupus-2015-000095 pmid: 26688740
48 Massenkeil G, Alexander T, Rosen O, Dörken B, Burmester G, Radbruch A, Hiepe F, Arnold R (2016). Long-term follow-up of fertility and pregnancy in autoimmune diseases after autologous haematopoietic stem cell transplantation. Rheumatol Int, 36(11): 1563–1568
https://doi.org/10.1007/s00296-016-3531-2 pmid: 27522225
49 McCarthy E M, Smith S, Lee R Z, Cunnane G, Doran M F, Donnelly S, Howard D, O’Connell P, Kearns G, Ní Gabhann J, Jefferies C A (2014). The association of cytokines with disease activity and damage scores in systemic lupus erythematosus patients. Rheumatology (Oxford), 53(9): 1586–1594
https://doi.org/10.1093/rheumatology/ket428 pmid: 24706988
50 Medina G, Florez O I , Montiel Manzano G, Reyes Maldonado E , Cruz Domínguez P, Ortega L O, Saavedra M A, Salinas L J(2015). Jara6 AB0572 Antiphospholipid Antibodies Profile and Thrombosis Recurrence. Ann Rheum Dis, 74 (Suppl 2) :1091.2–1091
51 Mendez B, Saxena A, Buyon J P, Izmirly P M (2014). Neonatal lupus, In: Sammaritano L R, Bermas B L, eds. Contraception and Pregnancy in Patients with Rheumatic Disease. Berlin: Springer verlag. pp. 251–272
52 Molad Y, Borkowski T, Monselise A, Ben-Haroush A, Sulkes J, Hod M, Feldberg D, Bar J (2005). Maternal and fetal outcome of lupus
53 Moroni G, Ponticelli C (2016). Pregnancy in women with systemic lupus erythematosus (SLE). Eur J Intern Med, 32: 7–12
https://doi.org/10.1016/j.ejim.2016.04.005 pmid: 27142327
54 Nasef N, Hafez M, Bakr A (2014). Neonatal lupus erythematosus. J Neonatol Clin Pediatr, . 77(2): 82–86
55 Palatinus A, Adams M (2009).Thrombosis in systemic lupus erythematosus. Semin Thromb Hemost. 35(7): 621–629
56 Papp G, Chen J Q, Pόliska S, Szabό K, Tarr T, Bá lint B L, Szodoray P, Zeher M(2017). AB0137 Alterations in microrna expression profiles in primary sjÖgren9s syndrome and systemic lupus erythematosus. Ann Rheum Dis,76:1094–1095
57 Pauley K M, Stewart C M, Gauna A E, Dupre L C, Kuklani R, Chan A L, Pauley B A, Reeves W H, Chan E K, Cha S (2011). Altered miR-146a expression in Sjögren’s syndrome and its functional role in innate immunity. Eur J Immunol, 41(7): 2029–2039
https://doi.org/10.1002/eji.201040757 pmid: 21469088
58 Perez-Sanchez C, Aguirre M A, Ruiz-Limon P, Abalos-Aguilera M C, Arias-de la Rosa I, Barbarroja N, Jimenez-Gomez Y, Segui P,Collantes-Estevez E, Gonzalez-Reyes J A, Villalba J M, Cuadrado M J, Lopez-Pedrera C(2017). AB0127 ANTI-DS-DNA antibodies regulate atherothrombosis in systemic lupus erythematosus through the induction of netosis, inflammation and endothelial activation., BMJ Publishing Group Ltd.
59 Perricone C, Ciccacci C, Ceccarelli F, Cipriano E, Alessandri C, Spinelli F R, Rufini S,Politi C,Latini A, Novelli G, Valesini G, Borgiani P , Conti F (2016). AB0004 polymorphisms in genes in the IL-17 pathway and B cell mediated immune response modulate the development of specific autoimmune manifestations in systemic lupus erythematosus. Ann Rheum Dis,75: 898
60 Pickering M C, Walport M J (2000). Links between complement abnormalities and systemic lupus erythematosus. Rheumatology (Oxford), 39(2): 133–141
https://doi.org/10.1093/rheumatology/39.2.133 pmid: 10725062
61 Qian J, Nan ( S 2017). 307 The pathogenic mechanisms of systemic lupus erythematosus associated genes pnp, plekhf2 and ankrd44. Lupus Sci Med, 4: doi:10.1136/lupus-2017-000215.307
62 Ramezani M, Hashemi B S, Khazaei S, Rezaei M, Ebrahimi A, Sadeghi M (2017). Diagnostic value of immunohistochemistry staining of Bcl-2, CD34, CD20 and CD3 for distinction between discoid lupus erythematosus and lichen planus in the skin. Indian J Pathol Microbiol, 60(2): 172–176
https://doi.org/10.4103/0377-4929.208381 pmid: 28631630
63 Ray D, Hailow S, Strickland F, Orlowski R, Marder W, McCune W J, Somer E C, (2016). CD70 methylation of a regulatory region increases with age in lupus patients., J Immnol, 196(Suppl.): 1876
64 Reis P C, Maurer K, Schanberg L, Burnham J M , von Scheven E, O'Neil K, Klein Gitelman M ,Petri M ,Sullivan K E(2017). THU0490 Multicentre study of lupus nephritis urinary biomarkers in adult and paediatric patients. Ann Rheum Dis, 76: 391–392
65 Sammaritano L R (2017). Management of systemic lupus erythematosus during pregnancy. Annu Rev Med, 68(1): 271–285
https://doi.org/10.1146/annurev-med-042915-102658 pmid: 27686021
66 Sawalha A H, Wang L, Nadig A, Somers E C, McCune W J, Hughes T, Merrill J T, Scofield R H, Strickland F M, Richardson B, and the Michigan Lupus Cohort (2012). Sex-specific differences in the relationship between genetic susceptibility, T cell DNA demethylation and lupus flare severity. J Autoimmun, 38(2-3): J216–J222
https://doi.org/10.1016/j.jaut.2011.11.008 pmid: 22305513
67 Shimada H, Kanenishi K, Kameda T, Izumikawa M, Nakashima S, Ozaki H, Wakiya R, Kondo A ,Kadowaki N,H Dobashi(2017). FRI0704 Analysis of risk factor for pregnancy outcomes in 142 pregnancies complicated with connective tissue disease. Ann Rheum Dis, 76:757
68 Sitrin J, Suto E, Wuster A, Eastham-Anderson J, Kim J M, Austin C D, Lee W P, Behrens T W (2017). The Ox40/Ox40 Ligand Pathway Promotes Pathogenic Th Cell Responses, Plasmablast Accumulation, and Lupus Nephritis in NZB/W F1 Mice. J Immunol, 199(4): 1238–1249
https://doi.org/10.4049/jimmunol.1700608 pmid: 28696253
69 Steri M, Orrù V, Idda M L, Pitzalis M, Pala M, Zara I, Sidore C, Faà V, Floris M, Deiana M, Asunis I, Porcu E, Mulas A, Piras M G, Lobina M, Lai S, Marongiu M, Serra V, Marongiu M, Sole G, Busonero F, Maschio A, Cusano R, Cuccuru G, Deidda F, Poddie F, Farina G, Dei M, Virdis F, Olla S, Satta M A, Pani M, Delitala A, Cocco E, Frau J, Coghe G, Lorefice L, Fenu G, Ferrigno P, Ban M, Barizzone N, Leone M, Guerini F R, Piga M, Firinu D, Kockum I, Lima Bomfim I, Olsson T, Alfredsson L, Suarez A, Carreira P E, Castillo-Palma M J, Marcus J H, Congia M, Angius A, Melis M, Gonzalez A, Alarcón Riquelme M E, da Silva B M, Marchini M, Danieli M G, Del Giacco S, Mathieu A, Pani A, Montgomery S B, Rosati G, Hillert J, Sawcer S, D’Alfonso S, Todd J A, Novembre J, Abecasis G R, Whalen M B, Marrosu M G, Meloni A, Sanna S, Gorospe M, Schlessinger D, Fiorillo E, Zoledziewska M, Cucca F (2017). Overexpression of the cytokine BAFF and autoimmunity risk. N Engl J Med, 376(17): 1615–1626
https://doi.org/10.1056/NEJMoa1610528 pmid: 28445677
70 Sun Y, Peng R, Peng H, Liu H, Wen L, Wu T, Yi H, Li A, Zhang Z (2016). miR-451 suppresses the NF-kappaB-mediated proinflammatory molecules expression through inhibiting LMP7 in diabetic nephropathy. Mol Cell Endocrinol, 433: 75–86
https://doi.org/10.1016/j.mce.2016.06.004 pmid: 27264074
71 Tangtanatakul P, Thammasate B, Jacquet A, Reantragoon R, Pisitkun T,Avihingsanon Y, Leelahavanichkul A, Hirankarn N (2017). 322 Down-regulation of mir-10a induces il-8 in human mesangial cells stimulated with anti-dsdna igg antibodies. Lupus Sci Med, 4: doi:10.1136/lupus-2017-000215.322
72 Teh C L, Wan S A, Cheong Y K, Ling G R (2016). Systemic lupus erythematosus pregnancies: ten-year data from a single centre in Malaysia. Lupus, 26(2): 218–223
https://doi.org/10.1177/0961203316664996 pmid: 27522092
73 Testa U, Pelosi E, Castelli G, Labbaye C (2017). miR-146 and miR-155: Two Key Modulators of Immune Response and Tumor Development. Non-Coding RNA, 3(3): 22
https://doi.org/10.3390/ncrna3030022
74 Ünlü O, Zuily S, Erkan D ( 2016 ). The clinical significance of antiphospholipid antibodies in systemic lupus erythematosus. Euro J Rheum, 3(2): 75
75 Vinet É, Pineau C A, Clarke A E, Fombonne É, Platt R W, Bernatsky S (2014). Neurodevelopmental disorders in children born to mothers with systemic lupus erythematosus. Lupus, 23(11): 1099–1104
https://doi.org/10.1177/0961203314541691 pmid: 24969080
76 Wang G, Tam L S, Kwan B C, Li E K, Chow K M, Luk C C, Li P K, Szeto C C (2012a). Expression of miR-146a and miR-155 in the urinary sediment of systemic lupus erythematosus. Clin Rheumatol, 31(3): 435–440
https://doi.org/10.1007/s10067-011-1857-4 pmid: 21987229
77 Wang G, Tam L S, Li E K, Kwan B C, Chow K M, Luk C C, Li P K, Szeto C C (2010). Serum and urinary cell-free MiR-146a and MiR-155 in patients with systemic lupus erythematosus. J Rheumatol, 37(12): 2516–2522
https://doi.org/10.3899/jrheum.100308 pmid: 20952466
78 Wang H, Peng W, Ouyang X, Li W, Dai Y (2012b). Circulating microRNAs as candidate biomarkers in patients with systemic lupus erythematosus. Transl Res, 160(3): 198–206
https://doi.org/10.1016/j.trsl.2012.04.002 pmid: 22683424
79 Wang Z, Chang C, Peng M, Lu Q (2017). Translating epigenetics into clinic: focus on lupus. Clin Epigenetics, 9(1): 78
https://doi.org/10.1186/s13148-017-0378-7 pmid: 28785369
80 Yelnik C M, Laskin C A, Porter T F, Branch D W, Buyon J P, Guerra M M, Lockshin M D, Petri M, Merrill J T, Sammaritano L R, Kim M Y, Salmon J E (2016). Lupus anticoagulant is the main predictor of adverse pregnancy outcomes in aPL-positive patients: validation of PROMISSE study results. Lupus Sci Med, 3(1): e000131
https://doi.org/10.1136/lupus-2015-000131 pmid: 26835148
81 Yin H, Lu Q (2014). Histone Demethylase Jmjd3 Regulates Cd11a Expression In Lupus T Cells By Changing Histone H3k27 Tri-methylation Level. J Dermatol, 41: 29
pmid: 24438142
82 Zeng J, Wu H, Zhao M, Q Lu(2017). Novel biomarkers for systemic lupus erythematosus. Biomark Med,
83 Zhang Y, Zhao M, Sawalha A H, Richardson B, Lu Q (2013). Impaired DNA methylation and its mechanisms in CD4(+)T cells of systemic lupus erythematosus. J Autoimmun, 41: 92–99
https://doi.org/10.1016/j.jaut.2013.01.005 pmid: 23340289
84 Zola H, Swart B ( 2016). CD Markers. Encyclopedia of Immunotoxicology, 146–150
[1] Peyman Hadi, Karimeh Haghani, Ali Noori-Zadeh, Salar Bakhtiyari. Prevalence of fragile X syndrome among patients with mental retardation in the west of Iran[J]. Front. Biol., 2018, 13(6): 464-468.
[2] Ji-Song Guan, Hong Xie, San-Xiong Liu. Epigenetic regulators sculpt the plastic brain[J]. Front. Biol., 2017, 12(5): 317-332.
[3] Karim Mowla, Mohammad Amin Saki, Mohammad Taha Jalali, Zeinab Deris Zayeri. How to manage rheumatoid arthritis according to classic biomarkers and polymorphisms?[J]. Front. Biol., 2017, 12(3): 183-191.
[4] Pang-Kuo Lo,Benjamin Wolfson,Qun Zhou. Cellular, physiological and pathological aspects of the long non-coding RNA NEAT1[J]. Front. Biol., 2016, 11(6): 413-426.
[5] Liang Hu,Edward Trope,Qi-Long Ying. Metabolism of pluripotent stem cells[J]. Front. Biol., 2016, 11(5): 355-365.
[6] Shirin Ferdowsi,Shirin Azizidoost,Nasim Ghafari,Najmaldin Saki. Cytogenetic changes of mesenchymal stem cells in the neoplastic bone marrow niche in leukemia[J]. Front. Biol., 2016, 11(4): 305-310.
[7] Ying-Tao Zhao,Maria Fasolino,Zhaolan Zhou. Locus- and cell type-specific epigenetic switching during cellular differentiation in mammals[J]. Front. Biol., 2016, 11(4): 311-322.
[8] Joshua D. TOMPKINS,Arthur D. RIGGS. An epigenetic perspective on the failing heart and pluripotent-derived-cardiomyocytes for cell replacement therapy[J]. Front. Biol., 2015, 10(1): 11-27.
[9] Jamie K. WONG,Hongyan ZOU. Reshaping the chromatin landscape after spinal cord injury[J]. Front. Biol., 2014, 9(5): 356-366.
[10] Nidhi VISHNOI,Jie YAO. Gene positioning and genome function[J]. Front. Biol., 2014, 9(4): 255-268.
[11] Simon HIPPENMEYER. Dissection of gene function at clonal level using mosaic analysis with double markers[J]. Front Biol, 2013, 8(6): 557-568.
[12] Yiwei LIN, Binhua P. ZHOU. Histone mimics: digging down under[J]. Front Biol, 2013, 8(2): 228-233.
[13] Blanca E. BARRERA-FIGUEROA, Zhigang WU, Renyi LIU. Abiotic stress-associated microRNAs in plants: discovery, expression analysis, and evolution[J]. Front Biol, 2013, 8(2): 189-197.
[14] Pippa A. THOMSON, Elise L.V. MALAVASI, Ellen GRüNEWALD, Dinesh C. SOARES, Malgorzata BORKOWSKA, J. Kirsty MILLAR. DISC1 genetics, biology and psychiatric illness[J]. Front Biol, 2013, 8(1): 1-31.
[15] Iouri CHEPELEV, Xin CHEN. Alternative splicing switching in stem cell lineages[J]. Front Biol, 2013, 8(1): 50-59.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed