Journal of Peking University (Health Sciences) ›› 2022, Vol. 54 ›› Issue (6): 1099-1105. doi: 10.19723/j.issn.1671-167X.2022.06.007

Previous Articles     Next Articles

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

Lin-qi ZHANG1,Jing ZHAO2,Hong-yan WANG2,Zong-yi WANG1,Ying-ni LI2,Ji-yang TANG1,Si-ying LI1,Jin-feng QU1,*(),Ming-wei ZHAO1   

  1. 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:2022-08-19 Online:2022-12-18 Published:2022-12-19
  • Contact: Jin-feng QU E-mail:drbari@163.com
  • 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)

RICH HTML

  

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.

Key words: Systemic lupus erythematosus, Retinopathy, Autoantibody, α-enolase, Anti-ENO1 antibody

CLC Number: 

  • R593.24

Table 1

Demographic data of all the three groups"

Items SLE retinopathy SLE without retinopathy Healthy control P value
Age/years, ${\bar x}$±s 43.40±17.31 35.58±14.87 39.03±19.39 0.335
Range of age/years 18-73 17-70 19-74 -
Sample size, n 32 50 50 -
Gender, n (%)
  Male 7 (21.87) 7 (14.00) 6 (12.00) 0.458
  Female 25 (78.13) 43 (86.00) 44 (88.00)
Disease duration
  Median/years 10.5 6 - 0.156
  Range 20 days to 50 years 6 months to 42 years - -

Table 2

Clinical and laboratory characteristics of the two SLE groups"

Items SLE retinopathy, n=32 SLE without retinopathy, n=50 P value
SLEDAI-2000, ${\bar x}$±s 17.41±4.25 9.48±5.35 < 0.001#
Clinical Features
  Fever, n (%) 22 (68.75) 35 (70.00) 0.905
  Tmax/℃, ${\bar x}$±s 38.92±0.76 38.93±0.76 0.980
  Rash, n (%) 13 (40.62) 23 (46.00) 0.632
  Malar erythema, n (%) 15 (46.88) 20 (40.00) 0.539
  Arthralgia, n (%) 20 (62.50) 32 (64.00) 0.891
  Hair loss, n (%) 17 (53.12) 18 (36.00) 0.126
  Mucosal ulcer, n (%) 11 (34.38) 10 (20.00) 0.146
  Photosensitivity, n (%) 5 (15.62) 9 (18.00) 0.780
  Raynaud’s phenomenon, n (%) 5 (15.62) 11 (22.00) 0.477
  Urine occult blood, n (%) 13 (40.62) 11 (22.00) 0.071
  Urine protein, n (%) 19 (59.38) 25 (50.00) 0.406
  Pleurisy, n (%) 13 (40.62) 11 (22.00) 0.071
  Pericarditis, n (%) 9 (28.12) 10 (20.00) 0.395
Antibodies
  anti-dsDNA (+), n (%) 12 (37.50) 21 (42.00) 0.770
  ANA (+), n (%) 28 (87.50) 48 (96.00) 0.314
  anti-Sm (+), n (%) 3 (9.38) 12 (24.00) 0.095
  anti-U1 RNP (+), n (%) 10 (31.25) 19 (38.00) 0.533
  anti-SSA (+), n (%) 12 (37.50) 26 (52.00) 0.199
  anti-SSB (+), n (%) 2 (6.25) 4 (8.00) >0.999

Table 3

Prevalence of symptoms and laboratory abnormalities of SLE patients"

Items Anti-ENO1(+), n=45 Anti-ENO1(-), n=37 P value
SLEDAI-2000, ${\bar x}$±s 13.56±6.23 11.38±6.20 0.119
Fever, n (%) 26 (57.78) 31 (83.78) 0.011*
Tmax/℃, ${\bar x}$±s 38.88±0.69 38.96±0.79 0.705
Rash, n (%) 19 (42.22) 17 (45.95) 0.735
Malar erythema, n (%) 21 (46.67) 14 (37.84) 0.421
Arthralgia, n (%) 31 (68.89) 21 (56.76) 0.256
Hair loss, n (%) 20 (44.44) 15 (40.54) 0.722
Mucosal ulcer, n (%) 9 (20.00) 12 (32.43) 0.199
Photosensitivity, n (%) 6 (13.33) 8 (21.62) 0.301
Raynaud’s phenomenon, n (%) 9 (20.00) 7 (18.92) 0.902
Urine occult blood, n (%) 9 (20.00) 15 (40.54) 0.042*
Urine protein, n (%) 12 (46.67) 23 (62.16) 0.161
Pleurisy, n (%) 14 (31.11) 10 (27.03) 0.686
Pericarditis, n (%) 11 (24.44) 8 (21.62) 0.763
Anti-dsDNA (+), n (%) 21 (47.73) 12 (32.43) 0.163
ANA (+), n (%) 44 (97.78) 32 (86.49) 0.127
anti-Sm (+), n (%) 11 (24.44) 4 (10.81) 0.112
anti-U1 RNP (+), n (%) 19 (42.22) 10 (27.03) 0.152
anti-SSA (+), n (%) 21 (46.67) 17 (45.95) 0.948
anti-SSB (+), n (%) 6 (13.33) 0 0.060
ESR/(mm/h), M (range) 29.50 (1.52-110.00) 12.00 (4.00-101.00) 0.001#
CRP/(mg/L), M (range) 1.30 (0.30-52.40) 1.55 (0.39-101.71) 0.922
IgA/(g/L), M (range) 2.85 (0.07-27.00) 2.05 (0.42-4.36) 0.014*
IgG/(g/L), M (range) 14.30 (4.02-37.80) 10.46 (2.50-25.73) 0.0003#
IgM/(g/L), M (range) 0.90 (0.22-3.18) 0.69 (0.17-2.24) 0.148
C3/(g/L), ${\bar x}$±s 0.63±0.31 0.73±0.29 0.157
C4/(g/L), M (range) 0.14 (0.02-0.47) 0.16 (0.02-0.49) 0.245
WBC/(×109 /L), M (range) 6.40 (1.89-12.20) 5.00 (1.50-17.60) 0.132
HB/(g/L), ${\bar x}$±s 107.98±19.09 111.32±23.76 0.481
PLT/(×109 /L), ${\bar x}$±s 205.87±67.98 164.57±69.57 0.008#
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.
doi: 10.1136/ard.41.5.473
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.
doi: 10.1177/0961203320940780
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.
doi: 10.1007/s10792-021-01833-x
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.
doi: 10.1186/s41927-021-00203-5
6 Stafford-brady FJ , Urowitz MB , Gladman DD , et al. Lupus retinopathy: Patterns, associations, and prognosis[J]. Arthritis Rheum, 1988, 31 (9): 1105- 1110.
doi: 10.1002/art.1780310904
7 de Andrade FA , Guimarães Moreira Balbi G , Bortoloti de Azevedo LG , et al. Neuro-ophthalmologic manifestations in systemic lupus erythematosus[J]. Lupus, 2017, 26 (5): 522- 528.
doi: 10.1177/0961203316683265
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.
doi: 10.1177/0961203313490435
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.
doi: 10.1007/s00296-018-4083-4
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.
doi: 10.1006/clin.1996.0021
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.
doi: 10.1167/iovs.10-5724
14 Doyle MK . Vasculitis associated with connective tissue disorders[J]. Curr Rheumatol Rep, 2006, 8 (4): 312- 316.
doi: 10.1007/s11926-006-0015-5
15 Calle-Botero E , Abril A . Lupus vasculitis[J]. Curr Rheumatol Rep, 2020, 22 (10): 71.
doi: 10.1007/s11926-020-00937-0
16 Barile-Fabris L , Hernández-Cabrera MF , Barragan-Garfias JA . Vasculitis in systemic lupus erythematosus[J]. Curr Rheumatol Rep, 2014, 16 (9): 440.
doi: 10.1007/s11926-014-0440-9
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.
doi: 10.1097/01.md.0000216817.35937.70
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.
doi: 10.1016/j.autrev.2006.10.004
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.
doi: 10.1016/0167-4838(83)90305-9
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.
doi: 10.1002/1521-4141(200012)30:12<3575::AID-IMMU3575>3.0.CO;2-#
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.
doi: 10.3389/fimmu.2017.00505
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.
doi: 10.1007/s10875-006-9065-8
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.
doi: 10.1177/0961203317721752
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.
[1] Zhihui WU, Mingzhi HU, Qiaoying ZHAO, Fengfeng LV, Jingying ZHANG, Wei ZHANG, Yongfu WANG, Xiaolin SUN, Hui WANG. Immunomodulatory mechanism of umbilical cord mesenchymal stem cells modified by miR-125b-5p in systemic lupus erythematosus [J]. Journal of Peking University (Health Sciences), 2024, 56(5): 860-867.
[2] Limin REN,Chuchu ZHAO,Yi ZHAO,Huiqiong ZHOU,Liyun ZHANG,Youlian WANG,Lingxun SHEN,Wenqiang FAN,Yang LI,Xiaomei LI,Jibo WANG,Yongjing CHENG,Jiajing PENG,Xiaozhen ZHAO,Miao SHAO,Ru Li. Low disease activity and remission status of systemic lupus erythematosus in a real-world study [J]. Journal of Peking University (Health Sciences), 2024, 56(2): 273-278.
[3] Hai-hong YAO,Fan YANG,Su-mei TANG,Xia ZHANG,Jing HE,Yuan JIA. Clinical characteristics and diagnostic indicators of macrophage activation syndrome in patients with systemic lupus erythematosus and adult-onset Still's disease [J]. Journal of Peking University (Health Sciences), 2023, 55(6): 966-974.
[4] Zhi-jun LUO,Jia-jia WU,You SONG,Chun-li MEI,Rong DU. Systemic lupus erythematosus associated macrophage activation syndrome with neuropsychiatric symptoms: A report of 2 cases [J]. Journal of Peking University (Health Sciences), 2023, 55(6): 1111-1117.
[5] Xiang-ge ZHAO,Jia-qing LIU,Hui-na HUANG,Zhi-min LU,Zi-ran BAI,Xia LI,Jing-jing QI. Interferon-α mediating the functional damage of CD56dimCD57+natural killer cells in peripheral blood of systemic lupus erythematosuss [J]. Journal of Peking University (Health Sciences), 2023, 55(6): 975-981.
[6] Miao SHAO,Hui-fang GUO,Ling-yan LEI,Qing ZHAO,Yan-jie DING,Jin LIN,Rui WU,Feng YU,Yu-cui LI,Hua-li MIAO,Li-yun ZHANG,Yan DU,Rui-ying JIAO,Li-xia PANG,Li LONG,Zhan-guo LI,Ru LI. A multicenter study on the tolerance of intravenous low-dose cyclophosphamide in systemic lupus erythematosus [J]. Journal of Peking University (Health Sciences), 2022, 54(6): 1112-1116.
[7] Min LI,Lin-qing HOU,Yue-bo JIN,Jing HE. Clinical and immunological characteristics of systemic lupus erythematosus with retinopathy [J]. Journal of Peking University (Health Sciences), 2022, 54(6): 1106-1111.
[8] Jian-mei ZOU,Li-jun WU,Cai-nan LUO,Ya-mei SHI,Xue WU. Relationship of serum 25- hydroxy vitamin D and systemic lupus erythematosus [J]. Journal of Peking University (Health Sciences), 2021, 53(5): 938-941.
[9] XIA Fang-fang,LU Fu-ai,LV Hui-min,YANG Guo-an,LIU Yuan. Clinical characteristics and related factors of systemic lupus erythematosus with interstitial pneumonia [J]. Journal of Peking University (Health Sciences), 2021, 53(2): 266-272.
[10] ZHANG Qing-fen,ZHAO Hong,FENG Yi. Different anesthesia management in preterm infants undergoing surgeries for retinopathy of prematurity: A retrospective study [J]. Journal of Peking University (Health Sciences), 2021, 53(1): 195-199.
[11] Yu-zhou GAN,Yu-hui LI,Li-hua ZHANG,Lin MA,Wen-wen HE,Yue-bo JIN,Yuan AN,Zhan-guo LI,Hua YE. Comparison of clinical and immunological features between clinically amyopathic dermatomyositis and typical dermatomyositis [J]. Journal of Peking University (Health Sciences), 2020, 52(6): 1001-1008.
[12] Yan GENG,Bo-rui LI,Zhuo-li ZHANG. Musculoskeletal ultrasound findings of symptomatic joints in patients with systemic lupus erythematosus [J]. Journal of Peking University(Health Sciences), 2020, 52(1): 163-168.
[13] Yu-hua WANG,Guo-hua ZHANG,Ling-ling ZHANG,Jun-li LUO,Lan GAO. Adrenal hemorrhage in a patient with systemic lupus erythematosus [J]. Journal of Peking University(Health Sciences), 2019, 51(6): 1178-1181.
[14] Ying-ni LI,Xiao-hong XIANG,Jing ZHAO,Yun LI,Feng SUN,Hong-yan WANG,Ru-lin JIA,Fan-lei HU. Significance of anti-carbamylated fibrinogen antibodies in systemic lupus erythematosus [J]. Journal of Peking University(Health Sciences), 2019, 51(6): 1019-1024.
[15] Fan YANG,Yun-shan ZHOU,Yuan JIA. Systemic lupus erythematosus with acquired hemophilia A: a case report [J]. Journal of Peking University(Health Sciences), 2018, 50(6): 1108-1111.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!