Relationship between anti-ENO1 antibody and systemic lupus erythematosus patients with retinopathy

  • Lin-qi ZHANG ,
  • Jing ZHAO ,
  • Hong-yan WANG ,
  • Zong-yi WANG ,
  • Ying-ni LI ,
  • Ji-yang TANG ,
  • Si-ying LI ,
  • Jin-feng QU ,
  • Ming-wei ZHAO
Expand
  • 1. Department of Ophthalmology, Peking University People's Hospital, Eye Diseases and Optometry Institute, Beijing Key Laboratory of Diagnosis and Therapy of Retinal and Choroid Disease, College of Optometry, Peking University Health and Science Center, Beijing, 100044
    2. Department of Rheumatology and Immunology, Peking University People's Hospital, Beijing, 100044

Received date: 2022-08-19

  Online published: 2022-12-19

Supported by

the National Key Research and Development Program of China(2020YFC20820);the Capital Clinical Diagnosis and Treatment Technology Research and Demonstration Application Project of China(Z191100006619029)

Abstract

Objective: To build bridges between anti-α enolase antibody (anti-enolase 1 antibody, anti-ENO1 antibody) and common clinical and laboratory characteristics of systemic lupus erythematosus (SLE) and to analyze the role of anti-ENO1 antibody in the evaluation of SLE disease activity. Methods: The SLE patients with retinopathy and without retinopathy were enrolled in the study, as well as healthy individuals whose gender and age matched with those of the SLE patients. Serum anti-ENO1 antibodies were measured using enzyme-linked immunosorbent assay (ELISA), presenting as intra-group positive rate and arbitrary units (AU) value. Clinical and laboratory data were obtained from medical records. Results: The SLE retinopathy patients represented various fundus abnormalities. Ranked by percentage, the top three retinopathies were retinal hemorrhage (14/32, 43.75%), cotton-wool spots (8/32, 25.00%) and retinal vein occlusion (3/32, 9.38%). Among the 32 SLE retinopathy patients, 13 (40.63%) suffered from two or more fundus abnormalities. The positive rate and AU value of the SLE patients were higher than of the SLE patients without retinopathy (68.75% vs. 46.00%, P=0.043; 16.11%±10.35% vs. 12.06%±6.47%, P=0.045). Besides, the positive rate and AU value of the two SLE groups were both significantly higher than those of the healthy control group (P < 0.001). Compared with the SLE-without-retinopathy group, the systemic lupus erythematosus disease activity index (SLEDAI)-2000 of the SLE retinopathy patients were significantly higher than those of the SLE patients without retinopathy (17.41±4.25 vs. 9.48±5.35, P < 0.001). Dividing all the SLE patients into an anti-ENO1-positive group and an anti-ENO1-negative group, we found that anti-ENO1-positive was more likely to be correlated to developing fever and positive result of urine occult blood (P=0.011, P=0.042). Comparing with the patients with negative anti-ENO1 antibodies, the patients with positive anti-ENO1 antibodies had significantly higher erythrocyte sedimentation rate (ESR) [the median (range) was 29.50 (1.52-110.00) mg/L vs. 12.00 (4.00-101.00) mg/L, P=0.001], higher immunoglobulin G (IgG) [the median (range) was 14.30 (4.02-37.80) g/L vs. 10.46 (2.50-25.73) g/L, P=0.000 3], and higher blood platelet count (PLT) [(205.87×109±67.98×109) /L vs. (164.57×109±69.57×109) /L, P=0.008], as well as higher immunoglobulin A (IgA) [the median (range) was 2.85 (0.07-27.00) g/L vs. 2.05 (0.42-4.36) g/L, P=0.014]. Conclusion: The positive rate and AU value of anti-ENO1 antibody suggested higher SLE disease activity and they were elevated in SLE and SLE retinopathy.

Cite this article

Lin-qi ZHANG , Jing ZHAO , Hong-yan WANG , Zong-yi WANG , Ying-ni LI , Ji-yang TANG , Si-ying LI , Jin-feng QU , Ming-wei ZHAO . Relationship between anti-ENO1 antibody and systemic lupus erythematosus patients with retinopathy[J]. Journal of Peking University(Health Sciences), 2022 , 54(6) : 1099 -1105 . DOI: 10.19723/j.issn.1671-167X.2022.06.007

References

1 Dammacco R . Systemic lupus erythematosus and ocular involvement: An overview[J]. Clin Exp Med, 2017, 18 (2): 135- 149.
2 Lanham JG , Barrie T , Kohner EM , et al. SLE retinopathy: Evaluation by fluorescein angiography[J]. Ann Rheu Dis, 1982, 41 (5): 473- 478.
3 Li M , Cheng G , Wang Z , et al. Anti-recoverin antibodies indicate fundus abnormalities in systemic lupus erythematosus[J]. Lupus, 2020, 29 (11): 1346- 1352.
4 Sharma SK , Sharma AL , Mahajan VK . Ophthalmic manifestations in patients with collagen vascular disorders: A hospital-based retrospective observational study[J]. Int Ophthalmol, 2021, 41 (8): 2765- 2775.
5 Bashiri H , Karimi N , Mostafaei S , et al. Retinopathy in newly-diagnosed systemic lupus erythematosus: Should we screen for ocular involvement[J]. BMC Rheumatol, 2021, 5 (1): 34.
6 Stafford-brady FJ , Urowitz MB , Gladman DD , et al. Lupus retinopathy: Patterns, associations, and prognosis[J]. Arthritis Rheum, 1988, 31 (9): 1105- 1110.
7 de Andrade FA , Guimar?es Moreira Balbi G , Bortoloti de Azevedo LG , et al. Neuro-ophthalmologic manifestations in systemic lupus erythematosus[J]. Lupus, 2017, 26 (5): 522- 528.
8 Nishiguchi KM , Ito Y , Terasaki H . Bilateral central retinal artery occlusion and vein occlusion complicated by severe choroidopathy in systemic lupus erythematosus[J]. Lupus, 2013, 22 (7): 733- 735.
9 Seth G , Chengappa KG , Misra DP , et al. Lupus retinopathy: A marker of active systemic lupus erythematosus[J]. Rheumatol Int, 2018, 38 (8): 1495- 1501.
10 Pratesi F , Moscato S , Sabbatini A , et al. Autoantibodies specific for alpha-enolase in systemic autoimmune disorders[J]. J Rheumatol, 2000, 27 (1): 109- 115.
11 Mosca M , Chimenti D , Pratesi F , et al. Prevalence and clinico-serological correlations of anti-alpha-enolase, anti-C1q, and anti-dsDNA antibodies in patients with systemic lupus erythematosus[J]. J Rheumatol, 2006, 33 (4): 695- 697.
12 Adamus G , Aptsiauri N , Guy J , et al. The occurrence of serum autoantibodies against enolase in cancer-associated retinopathy[J]. Clin Immunol Immunopathol, 1996, 78 (2): 120- 129.
13 Smith WC , Bolch S , Dugger DR , et al. Interaction of arrestin with enolase1 in photoreceptors[J]. Invest Ophthalmol Vis Sci, 2011, 52 (3): 1832- 1840.
14 Doyle MK . Vasculitis associated with connective tissue disorders[J]. Curr Rheumatol Rep, 2006, 8 (4): 312- 316.
15 Calle-Botero E , Abril A . Lupus vasculitis[J]. Curr Rheumatol Rep, 2020, 22 (10): 71.
16 Barile-Fabris L , Hernández-Cabrera MF , Barragan-Garfias JA . Vasculitis in systemic lupus erythematosus[J]. Curr Rheumatol Rep, 2014, 16 (9): 440.
17 Cies'lik P , Hrycek A , Kńuciński P . Vasculopathy and vasculitis in systemic lupus erythematosus[J]. Pol Arch Med Wewn, 2008, 118 (1/2): 57- 63.
18 Ramos-Casals M , Nardi N , Lagrutta M , et al. Vasculitis in systemic lupus erythematosus: Prevalence and clinical characteristics in 670 patients[J]. Medicine (Baltimore), 2006, 85 (2): 95- 104.
19 Terrier B , Degand N , Guilpain P , et al. Alpha-enolase: A target of antibodies in infectious and autoimmune diseases[J]. Autoimmun Rev, 2007, 6 (3): 176- 182.
20 Shimizu A , Suzuki F , Kato K . Characterization of alpha alpha, beta beta, gamma gamma and alpha gamma human enolase isozymes, and preparation of hybrid enolases (alpha gamma, beta gamma and alpha beta) from homodimeric forms[J]. Biochim Biophys Acta, 1983, 748 (2): 278- 284.
21 Moscato S , Pratesi F , Sabbatini A , et al. Surface expression of a glycolytic enzyme, alpha-enolase, recognized by autoantibodies in connective tissue disorders[J]. Eur J Immunol, 2000, 30 (12): 3575- 3584.
22 Redlitz A , Fowler BJ , Plow EF , et al. The role of an enolase-related molecule in plasminogen binding to cells[J]. Eur J Biochem, 1995, 227 (1/2): 407- 415.
23 Adamus G . Impact of autoantibodies against glycolytic enzymes on pathogenicity of autoimmune retinopathy and other autoimmune disorders[J]. Front Immunol, 2017, 8, 505.
24 Magrys A , Anekonda T , Ren G , et al. The role of anti-alpha-enolase autoantibodies in pathogenicity of autoimmune-mediated retinopathy[J]. J Clin Immunol, 2007, 27 (2): 181- 192.
25 Lu Y , He S , Jia L , et al. Two mouse models for recoverin-associated autoimmune retinopathy[J]. Mol Vis, 2010, 16, 1936- 1948.
26 Li M , Li J , Wang J , et al. Serum level of anti-α-enolase antibody in untreated systemic lupus erythematosus patients correlates with 24-hour urine protein and D-dimer[J]. Lupus, 2018, 27 (1): 139- 142.
27 Huang Y , Chen L , Chen K , et al. Anti-α-enolase antibody combined with β2 microglobulin evaluated the incidence of nephritis in systemic lupus erythematosus patients[J]. Lupus, 2019, 28 (3): 365- 370.
28 Bruschi M , Sinico RA , Moroni G , et al. Glomerular autoimmune multicomponents of human lupus nephritis in vivo: α-enolase and annexin AI[J]. J Am Soc Nephrol, 2014, 25 (11): 2483- 2498.
29 Bruschi M , Moroni G , Sinico RA , et al. Serum IgG2 antibody multicomposition in systemic lupus erythematosus and lupus nephritis (Part 1): Cross-sectional analysis[J]. Rheumatology (Oxford), 2021, 60 (7): 3176- 3188.
30 Bruschi M , Moroni G , Sinico RA , et al. Serum IgG2 antibody multi-composition in systemic lupus erythematosus and lupus nephritis (Part 2): Prospective study[J]. Rheumatology (Oxford), 2021, 60 (7): 3388- 3397.
Outlines

/