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Open Access 01-12-2024 | Human Cytomegalovirus | Research

Integrating clinical data and genetic susceptibility to elucidate the relationship between systemic lupus erythematosus and human cytomegalovirus infection

Authors: Xin Luo, Liuliu Quan, Qingting Lin, Huiteng Rong, Yue Liu, Jiaqi Meng, Xin You

Published in: Virology Journal | Issue 1/2024

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Abstract

Background

Viral infections are known to induce the occurrence and pathogenesis of systemic lupus erythematosus (SLE). Previous studies have indicated a possible relationship between SLE and human cytomegalovirus (HCMV) infection and have attributed HCMV to be associated with various autoantibodies; however, these studies were constrained by variations in sample size and potential selection bias. Therefore, in the present study, we aimed to elucidate the relationship between HCMV and autoantibodies in patients with SLE by integrating clinical data and genetic susceptibility.

Methods

Using various statistical methods, we conducted a retrospective analysis of the spectrum of SLE autoantibodies and HCMV infections among patients hospitalized at our center over the past 10 years. Machine learning modeling was used to predict active HCMV infections based on the antinuclear (ANA) spectrum. Moreover, Mendelian randomization (MR) was used to investigate the causal relationship between SLE and HCMV infection.

Results

In the HCMV group, the levels of ANA, anti-dsDNA, anti-histone antibody (AHA), and anti-nucleosome antibody (ANuA) were significantly increased (P < 0.001) and were linked to the presence of CMV-pp65-antigen-positive polymorphonuclear leukocytes (P < 0.001). A weak correlation was observed between the titers of anti-CMV IgM and ANA (P < 0.001). The ANA spectrum demonstrated a strong predictive performance for active HCMV infection based on principal component analysis (Adonis and ANOSIM P < 0.001) as well as support vector machine and extreme gradient boosting modeling. MR analyses of inverse-variance weighted, weighted mean, MR-Egger, and weighted mode revealed that patients with SLE were at a higher risk of developing HCMV infection (P < 0.05). However, HCMV infection did not have a causal effect on SLE (P > 0.05).

Conclusion

The ANA spectrum in patients with SLE can be used to predict HCMV infection status. Due to the inherent susceptibility of patients with SLE to HCMV infection, we propose for the first time that if a patient with SLE exhibits high serum titers of ANA, anti-dsDNA, ANuA, and AHA, caution should be exercised for HCMV infection, which can contribute to the clinical assessment of SLE and improve patient prognosis.
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Literature
1.
go back to reference Vina ER, Utset TO, Hannon MJ, Masi CM, Roberts N, Kwoh CK. Racial differences in treatment preferences among lupus patients: a two-site study. Clin Exp Rheumatol. 2014;32(5):680–8.PubMed Vina ER, Utset TO, Hannon MJ, Masi CM, Roberts N, Kwoh CK. Racial differences in treatment preferences among lupus patients: a two-site study. Clin Exp Rheumatol. 2014;32(5):680–8.PubMed
2.
go back to reference Silman AJ, MacGregor AJ, Thomson W, Holligan S, Carthy D, Farhan A, Ollier WE. Twin concordance rates for rheumatoid arthritis: results from a nationwide study. Br J Rheumatol. 1993;32(10):903–7.PubMedCrossRef Silman AJ, MacGregor AJ, Thomson W, Holligan S, Carthy D, Farhan A, Ollier WE. Twin concordance rates for rheumatoid arthritis: results from a nationwide study. Br J Rheumatol. 1993;32(10):903–7.PubMedCrossRef
3.
go back to reference Arbuckle MR, McClain MT, Rubertone MV, Scofield RH, Dennis GJ, James JA, Harley JB. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med. 2003;349(16):1526–33.PubMedCrossRef Arbuckle MR, McClain MT, Rubertone MV, Scofield RH, Dennis GJ, James JA, Harley JB. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med. 2003;349(16):1526–33.PubMedCrossRef
4.
go back to reference Akagi S, Ichikawa H, Suzuki J, Makino H. Systemic lupus erythematosus associated with cytomegalovirus infection. Scand J Rheumatol. 2004;33(1):58–9.PubMedCrossRef Akagi S, Ichikawa H, Suzuki J, Makino H. Systemic lupus erythematosus associated with cytomegalovirus infection. Scand J Rheumatol. 2004;33(1):58–9.PubMedCrossRef
5.
go back to reference Díaz F, Urkijo JC, Mendoza F, De la Viuda JM, Blanco M, Flores M, Berdonces P. Systemic lupus erythematosus associated with acute cytomegalovirus infection. J Clin Rheumatol. 2006;12(5):263–4.PubMedCrossRef Díaz F, Urkijo JC, Mendoza F, De la Viuda JM, Blanco M, Flores M, Berdonces P. Systemic lupus erythematosus associated with acute cytomegalovirus infection. J Clin Rheumatol. 2006;12(5):263–4.PubMedCrossRef
6.
go back to reference Rasmussen NS, Draborg AH, Nielsen CT, Jacobsen S, Houen G. Antibodies to early EBV, CMV, and HHV6 antigens in systemic lupus erythematosus patients. Scand J Rheumatol. 2015;44(2):143–9.PubMedPubMedCentralCrossRef Rasmussen NS, Draborg AH, Nielsen CT, Jacobsen S, Houen G. Antibodies to early EBV, CMV, and HHV6 antigens in systemic lupus erythematosus patients. Scand J Rheumatol. 2015;44(2):143–9.PubMedPubMedCentralCrossRef
7.
go back to reference Quaglia M, Merlotti G, De Andrea M, Borgogna C, Cantaluppi V. Viral infections and systemic Lupus Erythematosus: New players in an Old Story. Viruses 2021, 13(2). Quaglia M, Merlotti G, De Andrea M, Borgogna C, Cantaluppi V. Viral infections and systemic Lupus Erythematosus: New players in an Old Story. Viruses 2021, 13(2).
8.
go back to reference Stern-Ginossar N, Weisburd B, Michalski A, Le VT, Hein MY, Huang SX, Ma M, Shen B, Qian SB, Hengel H, et al. Decoding human cytomegalovirus. Sci (New York NY). 2012;338(6110):1088–93.CrossRef Stern-Ginossar N, Weisburd B, Michalski A, Le VT, Hein MY, Huang SX, Ma M, Shen B, Qian SB, Hengel H, et al. Decoding human cytomegalovirus. Sci (New York NY). 2012;338(6110):1088–93.CrossRef
9.
go back to reference Sinnott JT, Cancio MR. Cytomegalovirus. Infect Control Hosp Epidemiol. 1987;8(2):79–82.CrossRef Sinnott JT, Cancio MR. Cytomegalovirus. Infect Control Hosp Epidemiol. 1987;8(2):79–82.CrossRef
10.
go back to reference Cannon MJ, Schmid DS, Hyde TB. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev Med Virol. 2010;20(4):202–13.PubMedCrossRef Cannon MJ, Schmid DS, Hyde TB. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev Med Virol. 2010;20(4):202–13.PubMedCrossRef
11.
go back to reference Barber C, Gold WL, Fortin PR. Infections in the lupus patient: perspectives on prevention. Curr Opin Rheumatol. 2011;23(4):358–65.PubMedCrossRef Barber C, Gold WL, Fortin PR. Infections in the lupus patient: perspectives on prevention. Curr Opin Rheumatol. 2011;23(4):358–65.PubMedCrossRef
12.
go back to reference Qin L, Qiu Z, Hsieh E, Geng T, Zhao J, Zeng X, Wan L, Xie J, Ramendra R, Routy JP, et al. Association between lymphocyte subsets and cytomegalovirus infection status among patients with systemic lupus erythematosus: a pilot study. Med (Baltim). 2019;98(39):e16997.CrossRef Qin L, Qiu Z, Hsieh E, Geng T, Zhao J, Zeng X, Wan L, Xie J, Ramendra R, Routy JP, et al. Association between lymphocyte subsets and cytomegalovirus infection status among patients with systemic lupus erythematosus: a pilot study. Med (Baltim). 2019;98(39):e16997.CrossRef
13.
go back to reference Hung M, Huang DF, Chen WS, Lai CC, Chen MH, Liao HT, Tsai CY. The clinical features and mortality risk factors of cytomegalovirus infection in patients with systemic lupus erythematosus. J Microbiol Immunol Infect. 2019;52(1):114–21.PubMedCrossRef Hung M, Huang DF, Chen WS, Lai CC, Chen MH, Liao HT, Tsai CY. The clinical features and mortality risk factors of cytomegalovirus infection in patients with systemic lupus erythematosus. J Microbiol Immunol Infect. 2019;52(1):114–21.PubMedCrossRef
14.
go back to reference Yamazaki S, Endo A, Iso T, Abe S, Aoyagi Y, Suzuki M, Fujii T, Haruna H, Ohtsuka Y, Shimizu T. Cytomegalovirus as a potential trigger for systemic lupus erythematosus: a case report. BMC Res Notes. 2015;8:487.PubMedPubMedCentralCrossRef Yamazaki S, Endo A, Iso T, Abe S, Aoyagi Y, Suzuki M, Fujii T, Haruna H, Ohtsuka Y, Shimizu T. Cytomegalovirus as a potential trigger for systemic lupus erythematosus: a case report. BMC Res Notes. 2015;8:487.PubMedPubMedCentralCrossRef
16.
go back to reference Pan Q, Liu Z, Liao S, Ye L, Lu X, Chen X, Li Z, Li X, Xu YZ, Liu H. Current mechanistic insights into the role of infection in systemic lupus erythematosus. Biomed Pharmacother. 2019;117:109122.PubMedCrossRef Pan Q, Liu Z, Liao S, Ye L, Lu X, Chen X, Li Z, Li X, Xu YZ, Liu H. Current mechanistic insights into the role of infection in systemic lupus erythematosus. Biomed Pharmacother. 2019;117:109122.PubMedCrossRef
17.
go back to reference HoHsieh A, Wang CM, Wu YJ, Chen A, Chang MI, Chen JY. B cell epitope of human cytomegalovirus phosphoprotein 65 (HCMV pp65) induced anti-dsDNA antibody in BALB/c mice. Arthritis Res Therapy. 2017;19(1):65.CrossRef HoHsieh A, Wang CM, Wu YJ, Chen A, Chang MI, Chen JY. B cell epitope of human cytomegalovirus phosphoprotein 65 (HCMV pp65) induced anti-dsDNA antibody in BALB/c mice. Arthritis Res Therapy. 2017;19(1):65.CrossRef
18.
go back to reference Neo JYJ, Wee SYK, Bonne I, Tay SH, Raida M, Jovanovic V, Fairhurst A-M, Lu J, Hanson BJ, MacAry PA. Characterisation of a human antibody that potentially links cytomegalovirus infection with systemic lupus erythematosus. Sci Rep. 2019;9(1):1–9.CrossRef Neo JYJ, Wee SYK, Bonne I, Tay SH, Raida M, Jovanovic V, Fairhurst A-M, Lu J, Hanson BJ, MacAry PA. Characterisation of a human antibody that potentially links cytomegalovirus infection with systemic lupus erythematosus. Sci Rep. 2019;9(1):1–9.CrossRef
19.
go back to reference Liu Y, Mu R, Gao Y-P, Dong J, Zhu L, Ma Y, Li Y-H, Zhang H-Q, Han D, Zhang Y. A cytomegalovirus peptide-specific antibody alters natural killer cell homeostasis and is shared in several autoimmune diseases. Cell Host Microbe. 2016;19(3):400–8.PubMedCrossRef Liu Y, Mu R, Gao Y-P, Dong J, Zhu L, Ma Y, Li Y-H, Zhang H-Q, Han D, Zhang Y. A cytomegalovirus peptide-specific antibody alters natural killer cell homeostasis and is shared in several autoimmune diseases. Cell Host Microbe. 2016;19(3):400–8.PubMedCrossRef
20.
go back to reference Newkirk MM, van Venrooij WJ, Marshall GS. Autoimmune response to U1 small nuclear ribonucleoprotein (U1 snRNP) associated with cytomegalovirus infection. Arthritis Res. 2001;3(4):253–8.PubMedPubMedCentralCrossRef Newkirk MM, van Venrooij WJ, Marshall GS. Autoimmune response to U1 small nuclear ribonucleoprotein (U1 snRNP) associated with cytomegalovirus infection. Arthritis Res. 2001;3(4):253–8.PubMedPubMedCentralCrossRef
21.
go back to reference Xin L. Clinical characteristics of new-onset systemic lupus erythematosus patients with human cytomegalovirus infection. master’s thesis. Upublished: Chinese Academy of Medical Sciences & Peking Union Medical College; 2021. Xin L. Clinical characteristics of new-onset systemic lupus erythematosus patients with human cytomegalovirus infection. master’s thesis. Upublished: Chinese Academy of Medical Sciences & Peking Union Medical College; 2021.
22.
go back to reference Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997;40(9):1725.PubMedCrossRef Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997;40(9):1725.PubMedCrossRef
23.
go back to reference Aringer M, Costenbader K, Daikh D, Brinks R, Mosca M, Ramsey-Goldman R, Smolen JS, Wofsy D, Boumpas DT, Kamen DL, et al. 2019 European League Against Rheumatism/American College of Rheumatology Classification Criteria for systemic Lupus Erythematosus. Arthritis Rheumatol. 2019;71(9):1400–12.PubMedPubMedCentralCrossRef Aringer M, Costenbader K, Daikh D, Brinks R, Mosca M, Ramsey-Goldman R, Smolen JS, Wofsy D, Boumpas DT, Kamen DL, et al. 2019 European League Against Rheumatism/American College of Rheumatology Classification Criteria for systemic Lupus Erythematosus. Arthritis Rheumatol. 2019;71(9):1400–12.PubMedPubMedCentralCrossRef
24.
go back to reference Tan YT, Shi XC, Liu XQ, Zeng XF, Zhou BT. [Clinical features and risk factors of systemic Lupus Erythematosus complicated with cytomegalovirus infection]. Zhongguo Yi Xue Ke Xue Yuan Xue Bao. 2020;42(6):749–54.PubMed Tan YT, Shi XC, Liu XQ, Zeng XF, Zhou BT. [Clinical features and risk factors of systemic Lupus Erythematosus complicated with cytomegalovirus infection]. Zhongguo Yi Xue Ke Xue Yuan Xue Bao. 2020;42(6):749–54.PubMed
25.
go back to reference Ljungman P, Boeckh M, Hirsch HH, Josephson F, Lundgren J, Nichols G, Pikis A, Razonable RR, Miller V, Griffiths PD. Definitions of cytomegalovirus infection and disease in transplant patients for use in clinical trials. Clin Infect Dis. 2017;64(1):87–91.PubMedCrossRef Ljungman P, Boeckh M, Hirsch HH, Josephson F, Lundgren J, Nichols G, Pikis A, Razonable RR, Miller V, Griffiths PD. Definitions of cytomegalovirus infection and disease in transplant patients for use in clinical trials. Clin Infect Dis. 2017;64(1):87–91.PubMedCrossRef
26.
go back to reference Greenland S. An introduction to instrumental variables for epidemiologists. Int J Epidemiol. 2000;29(4):722–9.PubMedCrossRef Greenland S. An introduction to instrumental variables for epidemiologists. Int J Epidemiol. 2000;29(4):722–9.PubMedCrossRef
27.
go back to reference Burgess S, Thompson SG. Mendelian randomization: methods for causal inference using genetic variants. CRC; 2021. Burgess S, Thompson SG. Mendelian randomization: methods for causal inference using genetic variants. CRC; 2021.
28.
go back to reference Bowden J, Davey Smith G, Burgess S. Mendelian randomization with invalid instruments: effect estimation and bias detection through Egger regression. Int J Epidemiol. 2015;44(2):512–25.PubMedPubMedCentralCrossRef Bowden J, Davey Smith G, Burgess S. Mendelian randomization with invalid instruments: effect estimation and bias detection through Egger regression. Int J Epidemiol. 2015;44(2):512–25.PubMedPubMedCentralCrossRef
29.
go back to reference Bentham J, Morris DL, Graham DSC, Pinder CL, Tombleson P, Behrens TW, Martín J, Fairfax BP, Knight JC, Chen L, et al. Genetic association analyses implicate aberrant regulation of innate and adaptive immunity genes in the pathogenesis of systemic lupus erythematosus. Nat Genet. 2015;47(12):1457–64.PubMedPubMedCentralCrossRef Bentham J, Morris DL, Graham DSC, Pinder CL, Tombleson P, Behrens TW, Martín J, Fairfax BP, Knight JC, Chen L, et al. Genetic association analyses implicate aberrant regulation of innate and adaptive immunity genes in the pathogenesis of systemic lupus erythematosus. Nat Genet. 2015;47(12):1457–64.PubMedPubMedCentralCrossRef
30.
go back to reference Zhang M, Ming Y, Du Y, Xin Z. Two-sample mendelian randomization study does not reveal a significant relationship between cytomegalovirus (CMV) infection and autism spectrum disorder. BMC Psychiatry. 2023;23(1):559.PubMedPubMedCentralCrossRef Zhang M, Ming Y, Du Y, Xin Z. Two-sample mendelian randomization study does not reveal a significant relationship between cytomegalovirus (CMV) infection and autism spectrum disorder. BMC Psychiatry. 2023;23(1):559.PubMedPubMedCentralCrossRef
31.
go back to reference Kamat MA, Blackshaw JA, Young R, Surendran P, Burgess S, Danesh J, Butterworth AS, Staley JR. PhenoScanner V2: an expanded tool for searching human genotype–phenotype associations. Bioinformatics. 2019;35(22):4851–3.PubMedPubMedCentralCrossRef Kamat MA, Blackshaw JA, Young R, Surendran P, Burgess S, Danesh J, Butterworth AS, Staley JR. PhenoScanner V2: an expanded tool for searching human genotype–phenotype associations. Bioinformatics. 2019;35(22):4851–3.PubMedPubMedCentralCrossRef
32.
go back to reference Staley JR, Blackshaw J, Kamat MA, Ellis S, Surendran P, Sun BB, Paul DS, Freitag D, Burgess S, Danesh J. PhenoScanner: a database of human genotype–phenotype associations. Bioinformatics. 2016;32(20):3207–9.PubMedPubMedCentralCrossRef Staley JR, Blackshaw J, Kamat MA, Ellis S, Surendran P, Sun BB, Paul DS, Freitag D, Burgess S, Danesh J. PhenoScanner: a database of human genotype–phenotype associations. Bioinformatics. 2016;32(20):3207–9.PubMedPubMedCentralCrossRef
33.
go back to reference Lawlor DA, Harbord RM, Sterne JA, Timpson N, Davey Smith G. Mendelian randomization: using genes as instruments for making causal inferences in epidemiology. Stat Med. 2008;27(8):1133–63.PubMedCrossRef Lawlor DA, Harbord RM, Sterne JA, Timpson N, Davey Smith G. Mendelian randomization: using genes as instruments for making causal inferences in epidemiology. Stat Med. 2008;27(8):1133–63.PubMedCrossRef
34.
go back to reference Burgess S, Thompson SG. Avoiding bias from weak instruments in mendelian randomization studies. Int J Epidemiol. 2011;40(3):755–64.PubMedCrossRef Burgess S, Thompson SG. Avoiding bias from weak instruments in mendelian randomization studies. Int J Epidemiol. 2011;40(3):755–64.PubMedCrossRef
35.
go back to reference Shim H, Chasman DI, Smith JD, Mora S, Ridker PM, Nickerson DA, Krauss RM, Stephens M. A multivariate genome-wide association analysis of 10 LDL subfractions, and their response to statin treatment, in 1868 caucasians. PLoS ONE. 2015;10(4):e0120758.PubMedPubMedCentralCrossRef Shim H, Chasman DI, Smith JD, Mora S, Ridker PM, Nickerson DA, Krauss RM, Stephens M. A multivariate genome-wide association analysis of 10 LDL subfractions, and their response to statin treatment, in 1868 caucasians. PLoS ONE. 2015;10(4):e0120758.PubMedPubMedCentralCrossRef
36.
go back to reference Burgess S, Butterworth A, Thompson SG. Mendelian randomization analysis with multiple genetic variants using summarized data. Genet Epidemiol. 2013;37(7):658–65.PubMedPubMedCentralCrossRef Burgess S, Butterworth A, Thompson SG. Mendelian randomization analysis with multiple genetic variants using summarized data. Genet Epidemiol. 2013;37(7):658–65.PubMedPubMedCentralCrossRef
37.
go back to reference Bowden J, Davey Smith G, Haycock PC, Burgess S. Consistent estimation in mendelian randomization with some Invalid instruments using a weighted median estimator. Genet Epidemiol. 2016;40(4):304–14.PubMedPubMedCentralCrossRef Bowden J, Davey Smith G, Haycock PC, Burgess S. Consistent estimation in mendelian randomization with some Invalid instruments using a weighted median estimator. Genet Epidemiol. 2016;40(4):304–14.PubMedPubMedCentralCrossRef
38.
go back to reference Hemani G, Zheng J, Elsworth B, Wade KH, Haberland V, Baird D, Laurin C, Burgess S, Bowden J, Langdon R et al. The MR-Base platform supports systematic causal inference across the human phenome. Elife 2018, 7. Hemani G, Zheng J, Elsworth B, Wade KH, Haberland V, Baird D, Laurin C, Burgess S, Bowden J, Langdon R et al. The MR-Base platform supports systematic causal inference across the human phenome. Elife 2018, 7.
39.
go back to reference Hartwig FP, Davey Smith G, Bowden J. Robust inference in summary data mendelian randomization via the zero modal pleiotropy assumption. Int J Epidemiol. 2017;46(6):1985–98.PubMedPubMedCentralCrossRef Hartwig FP, Davey Smith G, Bowden J. Robust inference in summary data mendelian randomization via the zero modal pleiotropy assumption. Int J Epidemiol. 2017;46(6):1985–98.PubMedPubMedCentralCrossRef
41.
go back to reference Hemani G, Tilling K, Davey Smith G. Orienting the causal relationship between imprecisely measured traits using GWAS summary data. PLoS Genet. 2017;13(11):e1007081.PubMedPubMedCentralCrossRef Hemani G, Tilling K, Davey Smith G. Orienting the causal relationship between imprecisely measured traits using GWAS summary data. PLoS Genet. 2017;13(11):e1007081.PubMedPubMedCentralCrossRef
42.
go back to reference Greco MF, Minelli C, Sheehan NA, Thompson JR. Detecting pleiotropy in mendelian randomisation studies with summary data and a continuous outcome. Stat Med. 2015;34(21):2926–40.CrossRef Greco MF, Minelli C, Sheehan NA, Thompson JR. Detecting pleiotropy in mendelian randomisation studies with summary data and a continuous outcome. Stat Med. 2015;34(21):2926–40.CrossRef
43.
go back to reference Bowden J, Del Greco MF, Minelli C, Zhao Q, Lawlor DA, Sheehan NA, Thompson J, Davey Smith G. Improving the accuracy of two-sample summary-data mendelian randomization: moving beyond the NOME assumption. Int J Epidemiol. 2019;48(3):728–42.PubMedCrossRef Bowden J, Del Greco MF, Minelli C, Zhao Q, Lawlor DA, Sheehan NA, Thompson J, Davey Smith G. Improving the accuracy of two-sample summary-data mendelian randomization: moving beyond the NOME assumption. Int J Epidemiol. 2019;48(3):728–42.PubMedCrossRef
45.
go back to reference Chen T, Guestrin C. Xgboost: A scalable tree boosting system. In: Proceedings of the 22nd acm sigkdd international conference on knowledge discovery and data mining: 2016. 785–794. Chen T, Guestrin C. Xgboost: A scalable tree boosting system. In: Proceedings of the 22nd acm sigkdd international conference on knowledge discovery and data mining: 2016. 785–794.
46.
go back to reference Verbanck M, Chen C-Y, Neale B, Do R. Detection of widespread horizontal pleiotropy in causal relationships inferred from mendelian randomization between complex traits and diseases. Nat Genet. 2018;50(5):693–8.PubMedPubMedCentralCrossRef Verbanck M, Chen C-Y, Neale B, Do R. Detection of widespread horizontal pleiotropy in causal relationships inferred from mendelian randomization between complex traits and diseases. Nat Genet. 2018;50(5):693–8.PubMedPubMedCentralCrossRef
48.
go back to reference Rozenblyum EV, Levy DM, Allen U, Harvey E, Hebert D, Silverman ED. Cytomegalovirus in pediatric systemic lupus erythematosus: prevalence and clinical manifestations. Lupus. 2015;24(7):730–5.PubMedCrossRef Rozenblyum EV, Levy DM, Allen U, Harvey E, Hebert D, Silverman ED. Cytomegalovirus in pediatric systemic lupus erythematosus: prevalence and clinical manifestations. Lupus. 2015;24(7):730–5.PubMedCrossRef
49.
go back to reference Hsieh A-H, Kuo C-F, Chou IJ, Tseng W-Y, Chen Y-F, Yu K-H, Luo S-F. Human cytomegalovirus pp65 peptide-induced autoantibodies cross-reacts with TAF9 protein and induces lupus-like autoimmunity in BALB/c mice. Sci Rep. 2020;10(1):9662.PubMedPubMedCentralCrossRef Hsieh A-H, Kuo C-F, Chou IJ, Tseng W-Y, Chen Y-F, Yu K-H, Luo S-F. Human cytomegalovirus pp65 peptide-induced autoantibodies cross-reacts with TAF9 protein and induces lupus-like autoimmunity in BALB/c mice. Sci Rep. 2020;10(1):9662.PubMedPubMedCentralCrossRef
50.
go back to reference Rekvig OP. The dsDNA, Anti-dsDNA antibody, and Lupus Nephritis: what we agree on, what must be done, and what the best strategy Forward could be. Front Immunol. 2019;10:1104.PubMedPubMedCentralCrossRef Rekvig OP. The dsDNA, Anti-dsDNA antibody, and Lupus Nephritis: what we agree on, what must be done, and what the best strategy Forward could be. Front Immunol. 2019;10:1104.PubMedPubMedCentralCrossRef
51.
go back to reference Agmon-Levin N, Blank M, Paz Z, Shoenfeld Y. Molecular mimicry in systemic lupus erythematosus. Lupus. 2009;18(13):1181–5.PubMedCrossRef Agmon-Levin N, Blank M, Paz Z, Shoenfeld Y. Molecular mimicry in systemic lupus erythematosus. Lupus. 2009;18(13):1181–5.PubMedCrossRef
52.
go back to reference Poole BD, Scofield RH, Harley JB, James JA. Epstein-Barr virus and molecular mimicry in systemic lupus erythematosus. Autoimmunity. 2006;39(1):63–70.PubMedCrossRef Poole BD, Scofield RH, Harley JB, James JA. Epstein-Barr virus and molecular mimicry in systemic lupus erythematosus. Autoimmunity. 2006;39(1):63–70.PubMedCrossRef
53.
go back to reference Hsieh A-H, Jhou Y-J, Liang C-T, Chang M, Wang S-L. Fragment of tegument protein pp65 of human cytomegalovirus induces autoantibodies in BALB/c mice. Arthritis Res Therapy. 2011;13(5):1–15.CrossRef Hsieh A-H, Jhou Y-J, Liang C-T, Chang M, Wang S-L. Fragment of tegument protein pp65 of human cytomegalovirus induces autoantibodies in BALB/c mice. Arthritis Res Therapy. 2011;13(5):1–15.CrossRef
54.
go back to reference Chen J, Zhang H, Chen P, Lin Q, Zhu X, Zhang L, Xue X. Correlation between systemic lupus erythematosus and cytomegalovirus infection detected by different methods. Clin Rheumatol. 2015;34(4):691–8.PubMedCrossRef Chen J, Zhang H, Chen P, Lin Q, Zhu X, Zhang L, Xue X. Correlation between systemic lupus erythematosus and cytomegalovirus infection detected by different methods. Clin Rheumatol. 2015;34(4):691–8.PubMedCrossRef
55.
go back to reference Curtis HA, Singh T, Newkirk MM. Recombinant cytomegalovirus glycoprotein gB (UL55) induces an autoantibody response to the U1-70 kDa small nuclear ribonucleoprotein. Eur J Immunol. 1999;29(11):3643–53.PubMedCrossRef Curtis HA, Singh T, Newkirk MM. Recombinant cytomegalovirus glycoprotein gB (UL55) induces an autoantibody response to the U1-70 kDa small nuclear ribonucleoprotein. Eur J Immunol. 1999;29(11):3643–53.PubMedCrossRef
56.
go back to reference HoHsieh A, Wang CM, Wu Y-JJ, Chen A, Chang M-I, Chen J-Y. B cell epitope of human cytomegalovirus phosphoprotein 65 (HCMV pp65) induced anti-dsDNA antibody in BALB/c mice. Arthritis Res Therapy. 2017;19(1):1–14.CrossRef HoHsieh A, Wang CM, Wu Y-JJ, Chen A, Chang M-I, Chen J-Y. B cell epitope of human cytomegalovirus phosphoprotein 65 (HCMV pp65) induced anti-dsDNA antibody in BALB/c mice. Arthritis Res Therapy. 2017;19(1):1–14.CrossRef
57.
go back to reference Gladman DD, Ibañez D, Urowitz MB. Systemic lupus erythematosus disease activity index 2000. J Rheumatol. 2002;29(2):288–91.PubMed Gladman DD, Ibañez D, Urowitz MB. Systemic lupus erythematosus disease activity index 2000. J Rheumatol. 2002;29(2):288–91.PubMed
58.
go back to reference Lino K, Trizzotti N, Carvalho FR, Cosendey RI, Souza CF, Klumb EM, Silva AA, Almeida JR. Pp65 antigenemia and cytomegalovirus diagnosis in patients with lupus nephritis: report of a series. J Bras Nefrol. 2018;40(1):44–52.PubMedPubMedCentralCrossRef Lino K, Trizzotti N, Carvalho FR, Cosendey RI, Souza CF, Klumb EM, Silva AA, Almeida JR. Pp65 antigenemia and cytomegalovirus diagnosis in patients with lupus nephritis: report of a series. J Bras Nefrol. 2018;40(1):44–52.PubMedPubMedCentralCrossRef
59.
go back to reference Zeng P, Zhang F. Cytomegalovirus infection in systemic lupus erythematosus: an analysis of 121 cases. Chin J Rheumatol. 2011;15(4):249–51. Zeng P, Zhang F. Cytomegalovirus infection in systemic lupus erythematosus: an analysis of 121 cases. Chin J Rheumatol. 2011;15(4):249–51.
60.
go back to reference Odeberg J, Plachter B, Brandén L, Söderberg-Nauclér C. Human cytomegalovirus protein pp65 mediates accumulation of HLA-DR in lysosomes and destruction of the HLA-DR alpha-chain. Blood. 2003;101(12):4870–7.PubMedCrossRef Odeberg J, Plachter B, Brandén L, Söderberg-Nauclér C. Human cytomegalovirus protein pp65 mediates accumulation of HLA-DR in lysosomes and destruction of the HLA-DR alpha-chain. Blood. 2003;101(12):4870–7.PubMedCrossRef
61.
go back to reference Li H, Zheng Y, Chen L, Lin S. High titers of antinuclear antibody and the presence of multiple autoantibodies are highly suggestive of systemic lupus erythematosus. Sci Rep. 2022;12(1):1687.PubMedPubMedCentralCrossRef Li H, Zheng Y, Chen L, Lin S. High titers of antinuclear antibody and the presence of multiple autoantibodies are highly suggestive of systemic lupus erythematosus. Sci Rep. 2022;12(1):1687.PubMedPubMedCentralCrossRef
62.
go back to reference Bizzaro N, Villalta D, Giavarina D, Tozzoli R. Are anti-nucleosome antibodies a better diagnostic marker than anti-dsDNA antibodies for systemic lupus erythematosus? A systematic review and a study of metanalysis. Autoimmun Rev. 2012;12(2):97–106.PubMedCrossRef Bizzaro N, Villalta D, Giavarina D, Tozzoli R. Are anti-nucleosome antibodies a better diagnostic marker than anti-dsDNA antibodies for systemic lupus erythematosus? A systematic review and a study of metanalysis. Autoimmun Rev. 2012;12(2):97–106.PubMedCrossRef
63.
go back to reference Cohen MG, Pollard KM, Webb J. Antibodies to histones in systemic lupus erythematosus: prevalence, specificity, and relationship to clinical and laboratory features. Ann Rheum Dis. 1992;51(1):61–6.PubMedPubMedCentralCrossRef Cohen MG, Pollard KM, Webb J. Antibodies to histones in systemic lupus erythematosus: prevalence, specificity, and relationship to clinical and laboratory features. Ann Rheum Dis. 1992;51(1):61–6.PubMedPubMedCentralCrossRef
64.
go back to reference Zeng Y, Xiao Y, Zeng F, Jiang L, Yan S, Wang X, Lin Q, Yu L, Lu X, Zhang Y, et al. Assessment of anti-nucleosome antibody (ANuA) isotypes for the diagnosis and prediction of systemic lupus erythematosus and lupus nephritis activity. Clin Exp Med. 2023;23(5):1677–89.PubMedCrossRef Zeng Y, Xiao Y, Zeng F, Jiang L, Yan S, Wang X, Lin Q, Yu L, Lu X, Zhang Y, et al. Assessment of anti-nucleosome antibody (ANuA) isotypes for the diagnosis and prediction of systemic lupus erythematosus and lupus nephritis activity. Clin Exp Med. 2023;23(5):1677–89.PubMedCrossRef
65.
go back to reference Oliveira RC, Oliveira IS, Santiago MB, Sousa Atta ML, Atta AM. High Avidity dsDNA Autoantibodies in Brazilian Women with Systemic Lupus Erythematosus: Correlation with Active Disease and Renal Dysfunction. J Immunol Res 2015, 2015:814748. Oliveira RC, Oliveira IS, Santiago MB, Sousa Atta ML, Atta AM. High Avidity dsDNA Autoantibodies in Brazilian Women with Systemic Lupus Erythematosus: Correlation with Active Disease and Renal Dysfunction. J Immunol Res 2015, 2015:814748.
66.
go back to reference Chou S. Newer methods for diagnosis of cytomegalovirus infection. Rev Infect Dis. 1990;12(Suppl 7):727–36.CrossRef Chou S. Newer methods for diagnosis of cytomegalovirus infection. Rev Infect Dis. 1990;12(Suppl 7):727–36.CrossRef
Metadata
Title
Integrating clinical data and genetic susceptibility to elucidate the relationship between systemic lupus erythematosus and human cytomegalovirus infection
Authors
Xin Luo
Liuliu Quan
Qingting Lin
Huiteng Rong
Yue Liu
Jiaqi Meng
Xin You
Publication date
01-12-2024
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2024
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-024-02578-6

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