Галектины, антитела к ним и галектин-3-связывающий белок при системной красной волчанке
https://doi.org/10.47360/1995-4484-2025-37-45
Аннотация
При системной красной волчанке (СКВ) изучение галектинов связано с поиском новых биомаркеров активности, клинических проявлений, исходов заболевания. В представленном обзоре литературы обобщены сведения по наиболее хорошо известным галектинам-1, -3, -9, а также по антителам к галектинам и галектин-3-связывающему белку, полученные при культуральных исследованиях, на моделях волчанки у животных и у пациентов с СКВ.
Ключевые слова
Об авторах
Л. В. КондратьеваРоссия
Кондратьева Любовь Валерьевна.
115522, Москва, Каширское шоссе, 34а
Конфликт интересов:
Нет
Т. В. Попкова
Россия
115522, Москва, Каширское шоссе, 34а
Конфликт интересов:
Нет
Е. Л. Насонов
Россия
115522, Москва, Каширское шоссе, 34а
Конфликт интересов:
Нет
Список литературы
1. Насонов ЕЛ, Соловьев СК, Аршинов АВ. Системная красная волчанка: история и современность. Научно-практическая ревматология. 2022;60(4):397-412. doi: 10.47360/1995-4484-2022-397-412
2. Tsokos GC. Systemic lupus erythematosus. N Engl J Med. 2011;365(22):2110-2121. doi: 10.1056/NEJMra1100359
3. Kaul A, Gordon C, Crow MK, Touma Z, Urowitz MB, van Vollenhoven R, et al. Systemic lupus erythematosus. Nat Rev Dis Primers. 2016;2:16039. doi: 10.1038/nrdp.2016.39
4. Capecchi R, Puxeddu I, Pratesi F, Migliorini P. New biomarkers in SLE: From bench to bedside. Rheumatology (Oxford). 2020;59(Suppl5):v12-v18. doi: 10.1093/rheumatology/keaa484
5. Johannes L, Jacob R, Leffler H. Galectins at a glance. J Cell Sci. 2018;131(9):jcs208884. doi: 10.1242/jcs.208884
6. Mariño KV, Cagnoni AJ, Croci DO, Rabinovich GA. Targeting galectin-driven regulatory circuits in cancer and fibrosis. Nat Rev Drug Discov. 2023;22(4):295-316. doi: 10.1038/s41573-023-00636-2
7. Liu FT, Stowell SR. The role of galectins in immunity and infection. Nat Rev Immunol. 2023;23(8):479-494. doi: 10.1038/s41577-022-00829-7
8. Giovannone N, Smith LK, Treanor B, Dimitroff CJ. Galectin-glycan interactions as regulators of B cell immunity. Front Immunol. 2018;9:2839. doi: 10.3389/fimmu.2018.02839
9. Thiemann S, Baum LG. Galectins and immune responses – Just how do they do those things they do? Annu Rev Immunol. 2016;34:243-264. doi: 10.1146/annurev-immunol-041015-055402
10. Montiel JL, Monsiváis-Urenda A, Figueroa-Vega N, Moctezuma JF, Burgos-Vargas R, González-Amaro R, et al. Anti-CD43 and anti-galectin-1 autoantibodies in patients with systemic lupus erythematosus. Scand J Rheumatol. 2010;39(1):50-57. doi: 10.3109/03009740903013213
11. Kang EH, Moon KC, Lee EY, Lee YJ, Lee EB, Ahn C, et al. Renal expression of galectin-3 in systemic lupus erythematosus patients with nephritis. Lupus. 2009;18(1):22-28. doi: 10.1177/0961203308094361
12. Gruszewska E, Cylwik B, Gińdzieńska-Sieśkiewicz E, Kowal-Bielecka O, Mroczko B, Chrostek L. Diagnostic power of galectin-3 in rheumatic diseases. J Clin Med. 2020;9(10):3312. doi: 10.3390/jcm9103312
13. Koca SS, Akbas F, Ozgen M, Yolbas S, Ilhan N, Gundogdu B, et al. Serum galectin-3 level in systemic sclerosis. Clin Rheumatol. 2014;33(2):215-220. doi: 10.1007/s10067-013-2346-8
14. Shi Z, Meng Z, Han Y, Cao C, Tan G, Wang L. The involvement of galectin-3 in skin injury in systemic lupus erythematosus patients. Lupus. 2018;27(4):621-627. doi: 10.1177/0961203317736144
15. Kalinska-Bienias A, Kowalczyk E, Bienias P, Gala K, Jagielski P, Kowalewski C. Serum galectin-3 and galectin-3 binding protein levels in systemic lupus erythematosus and cutaneous lupus erythematosus. Postepy Dermatol Alergol. 2021;38(2):274-280. doi: 10.5114/ada.2020.92320
16. Koletsos N, Lazaridis A, Triantafyllou A, Anyfanti P, Lamprou S, Stoimeni A, et al. Accumulation of microvascular target organ damage in systemic lupus erythematosus patients is associated with increased cardiovascular risk. J Clin Med. 2024;13(7):2140. doi: 10.3390/jcm13072140
17. Jiao Q, Qian Q, Zhao Z, Fang F, Hu X, An J, et al. Expression of human T cell immunoglobulin domain and mucin-3 (TIM-3) and TIM-3 ligands in peripheral blood from patients with systemic lupus erythematosus. Arch Dermatol Res. 2016;308(8):553-61. doi: 10.1007/s00403-016-1665-4
18. van den Hoogen LL, van Roon JAG, Mertens JS, Wienke J, Lopes AP, de Jager W, et al. Galectin-9 is an easy to measure biomarker for the interferon signature in systemic lupus erythematosus and antiphospholipid syndrome. Ann Rheum Dis. 2018;77(12):1810-1814. doi: 10.1136/annrheumdis-2018-213497
19. Enocsson H, Wetterö J, Eloranta ML, Gullstrand B, Svanberg C, Larsson M, et al. Comparison of surrogate markers of the type I interferon response and their ability to mirror disease activity in systemic lupus erythematosus. Front Immunol. 2021;12:688753. doi: 10.3389/fimmu.2021.688753
20. Matsuoka N, Fujita Y, Temmoku J, Furuya MY, Asano T, Sato S, et al. Galectin-9 as a biomarker for disease activity in systemic lupus erythematosus. PLoS One. 2020;15(1):e0227069. doi: 10.1371/journal.pone.0227069
21. Mehta P, Singh P, Aggarwal A. Serum and urinary galectin-9 and C-X-C motif chemokine ligand 10. Lupus. 2022;31(4):482-487. doi: 10.1177/09612033221082907
22. Gensous N, Vagner D, Barnetche T, Duffau P, Lazaro E, Richez C, et al. CXCL-10 and tumor necrosis factor receptor type II as biomarkers of disease activity in systemic lupus erythematosus. Joint Bone Spine. 2022;89(3):105311. doi: 10.1016/j.jbspin.2021.105311
23. Szabó E, Faragó A, Bodor G, Gémes N, Puskás LG, Kovács L, et al. Identification of immune subsets with distinct lectin binding signatures using multi-parameter flow cytometry: Correlations with disease activity in systemic lupus erythematosus. Front Immunol. 2024;15:1380481. doi: 10.3389/fimmu.2024.1380481
24. Szabó E, Hornung Á, Monostori É, Bocskai M, Czibula Á, Kovács L. Altered cell surface N-glycosylation of resting and activated T cells in systemic lupus erythematosus. Int J Mol Sci. 2019;20(18):4455. doi: 10.3390/ijms20184455
25. Jiang X, Xiao X, Li H, Gong Y, Wang M, Yang H, et al. Oxidized galectin-1 in SLE fails to bind the inhibitory receptor VSTM1 and increases reactive oxygen species levels in neutrophils. Cell Mol Immunol. 2023;20(11):1339-1351. doi: 10.1038/s41423-023-01084-z
26. Chen SY, Wang CT, Chen CY, Kuo PY, Wang CR, Shiau AL, et al. Galectin-3 mediates NETosis and acts as an autoantigen in systemic lupus erythematosus-associated diffuse alveolar haemorrhage. Int J Mol Sci. 2023;24(11):9493. doi: 10.3390/ijms24119493
27. Shi Z, Zhang YP, Hong D, Qiu X, Zheng L, Bian L, et al. Antigalectin-3 antibodies induce skin vascular inflammation via promoting local production of IL-1β in systemic lupus erythematosus. Int Immunopharmacol. 2022;112:109197. doi: 10.1016/j.intimp.2022.109197
28. Shi ZR, Tan GZ, Meng Z, Yu M, Li KW, Yin J, et al. Association of anti-acidic ribosomal protein P0 and anti-galectin 3 antibodies with the development of skin lesions in systemic lupus erythematosus. Arthritis Rheumatol. 2015;67(1):193-203. doi: 10.1002/art.38891
29. Nielsen CT, Lood C, Ostergaard O, Iversen LV, Voss A, Bengtsson A, et al. Plasma levels of galectin-3-binding protein reflect type I interferon activity and are increased in patients with systemic lupus erythematosus. Lupus Sci Med. 2014;1(1):e000026. doi: 10.1136/lupus-2014-000026
30. Østergaard O, Nielsen CT, Iversen LV, Tanassi JT, Knudsen S, Jacobsen S, et al. Unique protein signature of circulating microparticles in systemic lupus erythematosus. Arthritis Rheum. 2013;65(10):2680-2690. doi: 10.1002/art.38065
31. Ullal AJ, Reich CF 3rd, Clowse M, Criscione-Schreiber LG, Tochacek M, Monestier M, et al. Microparticles as antigenic targets of antibodies to DNA and nucleosomes in systemic lupus erythematosus. J Autoimmun. 2011;36(3-4):173-180. doi: 10.1016/j.jaut.2011.02.001
32. Liu SD, Lee S, La Cava A, Motran CC, Hahn BH, Miceli MC. Galectin-1-induced down-regulation of T lymphocyte activation protects (NZB x NZW) F1 mice from lupus-like disease. Lupus. 2011;20(5):473-484. doi: 10.1177/0961203310388444
33. Fava A, Buyon J, Magder L, Hodgin J, Rosenberg A, Demeke DS, et al. Urine proteomic signatures of histological class, activity, chronicity, and treatment response in lupus nephritis. JCI Insight. 2024;9(2):e172569. doi: 10.1172/jci.insight.172569
34. Насонов ЕЛ, Авдеева АС, Решетняк ТМ, Алексанкин АП, Рубцов ЮП. Роль нетоза в патогенезе иммуновоспалительных ревматических заболеваний. Научно-практическая ревматология. 2023;61(5):513-530. doi: 10.47360/1995-4484-2023-513-530
35. Beccaria CG, Amezcua Vesely MC, Fiocca Vernengo F, Gehrau RC, Ramello MC, Tosello Boari J, et al. Galectin-3 deficiency drives lupus-like disease by promoting spontaneous germinal centers formation via IFN-γ. Nat Commun. 2018;9(1):1628. doi: 10.1038/s41467-018-04063-5
36. Насонов ЕЛ, Авдеева АС. Иммуновоспалительные ревматические заболевания, связанные с интерфероном типа I: новые данные. Научно-практическая ревматология. 2019;55(4):452-461. doi: 10.14412/1995-4484-2019-452-461
37. Kuca-Warnawin E, Skalska U, Janicka I, Musiałowicz U, Bonek K, Głuszko P, et al. The phenotype and secretory activity of adipose-derived mesenchymal stem cells (ASCs) of patients with rheumatic diseases. Cells. 2019;8(12):1659. doi: 10.3390/cells8121659
38. Zhao CN, Mao YM, Liu LN, Wu Q, Dan YL, Pan HF. Plasma galectin-3 levels do not differ in systemic lupus erythematosus patients. Int J Rheum Dis. 2019;22(10):1820-1824. doi: 10.1111/1756-185X.13677
39. Faustini F, Idborg H, Fuzzi E, Larsson A, Lie WR, Pötzsch S, et al. Urine galectin-3 binding protein reflects nephritis activity in systemic lupus erythematosus. Lupus. 2023;32(2):252-262. doi: 10.1177/09612033221145534
40. Guo Y, Li L, Hu S. Circulating galectin-3 levels and diabetic nephropathy: A systematic review and meta-analysis. BMC Nephrol. 2023;24(1):163. doi: 10.1186/s12882-023-03226-x
41. Kikuchi Y, Kobayashi S, Hemmi N, Ikee R, Hyodo N, Saigusa T, et al. Galectin-3-positive cell infiltration in human diabetic nephropathy. Nephrol Dial Transplant. 2004;19(3):602-607. doi: 10.1093/ndt/gfg603
42. Li LC, Li J, Gao J. Functions of galectin-3 and its role in fibrotic diseases. J Pharmacol Exp Ther. 2014;351(2):336-343. doi: 10.1124/jpet.114.218370
43. Henderson NC, Mackinnon AC, Farnworth SL, Poirier F, Russo FP, Iredale JP, et al. Galectin-3 regulates myofibroblast activation and hepatic fibrosis. Proc Natl Acad Sci U S A. 2006;103(13):5060-5065. doi: 10.1073/pnas.0511167103
44. Jia Q, Yang Y, Yao S, Chen X, Hu Z. Emerging roles of galectin-3 in pulmonary diseases. Lung. 2024;202(4):385-403. doi: 10.1007/s00408-024-00709-y
45. Гямджян КА, Драпкина ОМ, Максимов МЛ. Галектин-3: клиническая и прогностическая ценность определения у пациентов с хронической сердечной недостаточностью. Журнал Cердечная недостаточность. 2014;82(1):51-55.
46. Анкудинов АС, Калягин АН. Применение галектина-3 в оценке тяжести хронической сердечной недостаточности, ассоциированной с ревматоидным артритом. Результаты анализа. Доктор.Ру. 2021;20(11):12-16. doi: 10.31550/1727-2378-2021-20-11-12-16
47. Gieseke F, Kruchen A, Tzaribachev N, Bentzien F, Dominici M, Müller I. Proinflammatory stimuli induce galectin-9 in human mesenchymal stromal cells to suppress T-cell proliferation. Eur J Immunol. 2013;43(10):2741-2749. doi: 10.1002/eji.201343335
48. Zeggar S, Watanabe KS, Teshigawara S, Hiramatsu S, Katsuyama T, Katsuyama E, et al. Role of Lgals9 deficiency in attenuating nephritis and arthritis in BALB/c mice in a pristane-induced lupus model. Arthritis Rheumatol. 2018;70(7):1089-1101. doi: 10.1002/art.40467
49. Panda SK, Facchinetti V, Voynova E, Hanabuchi S, Karnell JL, Hanna RN, et al. Galectin-9 inhibits TLR7-mediated autoimmunity in murine lupus models. J Clin Invest. 2018;128(5):1873-1887. doi: 10.1172/JCI97333
50. Moritoki M, Kadowaki T, Niki T, Nakano D, Soma G, Mori H, et al. Galectin-9 ameliorates clinical severity of MRL/lpr lupusprone mice by inducing plasma cell apoptosis independently of Tim-3. PLoS One. 2013;8(4):e60807. doi: 10.1371/journal.pone.0060807
51. Yuksel K, Sag E, Demir S, Özdel S, Kaya UA, Atalay E, et al. Plasma checkpoint protein levels and galectin-9 in juvenile systemic lupus erythematosus. Lupus. 2021;30(6):998-1004. doi: 10.1177/09612033211002275
52. van den Hoogen LL, van der Heijden EHM, Hillen MR, Mertens JS, Fritsch-Stork RDE, Radstake TRDJ, et al. Galectin-9 reflects the interferon signature and correlates with disease activity in systemic autoimmune diseases. Response to: ’Biomarkers: to be or not to be’ by Yavuz and Rönnblom. Ann Rheum Dis. 2020;79(1):e9. doi: 10.1136/annrheumdis-2018-214651
53. Wang Y, Song L, Sun J, Sui Y, Li D, Li G, et al. Expression of galectin-9 and correlation with disease activity and vascular endothelial growth factor in rheumatoid arthritis. Clin Exp Rheumatol. 2020;38(4):654-661.
54. Fujita Y, Asano T, Matsuoka N, Temmoku J, Sato S, Matsumoto H, et al. Differential regulation and correlation between galectin-9 and anti-CCP antibody (ACPA) in rheumatoid arthritis patients. Arthritis Res Ther. 2020;22(1):80. doi: 10.1186/s13075-020-02158-3
55. Wienke J, Bellutti Enders F, Lim J, Mertens JS, van den Hoogen LL, Wijngaarde CA, et al. Galectin-9 and CXCL10 as biomarkers for disease activity in juvenile dermatomyositis: A longitudinal cohort study and multicohort validation. Arthritis Rheumatol. 2019;71(8):1377-1390. doi: 10.1002/art.40881
56. Matsuoka N, Kozuru H, Koga T, Abiru S, Yamasaki K, Komori A, et al. Galectin-9 in autoimmune hepatitis: Correlation between serum levels of galectin-9 and M2BPGi in patients with autoimmune hepatitis. Medicine (Baltimore). 2019;98(35):e16924. doi: 10.1097/MD.0000000000016924
57. Sarter K, Janko C, André S, Muñoz LE, Schorn C, Winkler S, Rech J, et al. Autoantibodies against galectins are associated with antiphospholipid syndrome in patients with systemic lupus erythematosus. Glycobiology. 2013;23(1):12-22. doi: 10.1093/glycob/cws120
58. Janko C, André S, Munoz LE, Briand JP, Schorn C, Winkler S, et al. Autoantibodies against galectin-2 peptides as biomarkers for the antiphospholipid syndrome. Lupus. 2012;21(7):781-783. doi: 10.1177/0961203312443422
59. Lim Y, Lee DY, Lee S, Park SY, Kim J, Cho B, et al. Identification of autoantibodies associated with systemic lupus erythematosus. Biochem Biophys Res Commun. 2002;295(1):119-124. doi: 10.1016/s0006-291x(02)00637-x
60. Rasmussen NS, Nielsen CT, Houen G, Jacobsen S. Humoral markers of active Epstein – Barr virus infection associate with antiextractable nuclear antigen autoantibodies and plasma galectin-3 binding protein in systemic lupus erythematosus. Lupus. 2016;25(14):1567-1576. doi: 10.1177/0961203316644334
61. Rasmussen NS, Draborg AH, Houen G, Nielsen CT. Human herpesvirus infections and circulating microvesicles expressing galectin-3 binding protein in patients with systemic lupus erythematosus. Clin Exp Rheumatol. 2022;40(1):158-161. doi: 10.55563/clinexprheumatol/s364rt
62. Loimaranta V, Hepojoki J, Laaksoaho O, Pulliainen AT. Galectin-3-binding protein: A multitask glycoprotein with innate immunity functions in viral and bacterial infections. J Leukoc Biol. 2018; 104(4):777-786. doi: 10.1002/JLB.3VMR0118-036R
63. Capone E, Iacobelli S, Sala G. Role of galectin 3 binding protein in cancer progression: A potential novel therapeutic target. J Transl Med. 2021;19(1):405. doi: 10.1186/s12967-021-03085-w
64. Keinänen O, Sarrett SM, Delaney S, Rodriguez C, Dayts EJ, Capone E, et al. Visualizing galectin-3 binding protein expression with ImmunoPET. Mol Pharm. 2023;20(6):3241-3248. doi: 10.1021/acs.molpharmaceut.3c00241
65. Lee YJ, Kang SW, Song JK, Park JJ, Bae YD, Lee EY, et al. Serum galectin-3 and galectin-3 binding protein levels in Behçet’s disease and their association with disease activity. Clin Exp Rheumatol. 2007;25(4 Suppl 45):S41-S45.
66. Ohshima S, Kuchen S, Seemayer CA, Kyburz D, Hirt A, Klinzing S, et al. Galectin 3 and its binding protein in rheumatoid arthritis. Arthritis Rheum. 2003;48(10):2788-2795. doi: 10.1002/art.11287
67. Ahn SS, Park Y, Lee DD, Bothwell ALM, Jung SM, Song JJ, et al. Serum Wisteria floribunda agglutinin-positive Mac-2-binding protein can reflect systemic lupus erythematosus activity. Lupus. 2018;27(5):771-779. doi: 10.1177/0961203317747719
68. Peretz ASR, Rasmussen NS, Jacobsen S, Sjöwall C, Nielsen CT. Galectin-3-binding protein is a novel predictor of venous thromboembolism in systemic lupus erythematosus. Clin Exp Rheumatol. 2021;39(6):1360-1368. doi: 10.55563/clinexprheumatol/ol0vqj
69. DeRoo EP, Wrobleski SK, Shea EM, Al-Khalil RK, Hawley AE, Henke PK, et al. The role of galectin-3 and galectin-3-binding protein in venous thrombosis. Blood. 2015;125(11):1813-1821. doi: 10.1182/blood-2014-04-569939
70. Diaz JA, Hawley AE, Wrobleski SK, Shea E, DeRoo E, Al-Khalil R, et al. Galectin-3 binding protein and galectin-3: Novel factors promoting venous thrombosis. J Vasc Surg Venous Lymphat Disord. 2013;1(1):102. doi: 10.1016/j.jvsv.2012.10.012
71. Gleissner CA, Erbel C, Linden F, Domschke G, Akhavanpoor M, Doesch AO, et al. Galectin-3 binding protein plasma levels are associated with long-term mortality in coronary artery disease independent of plaque morphology. Atherosclerosis. 2016;251:94-100. doi: 10.1016/j.atherosclerosis.2016.06.002
72. Gleissner CA, Erbel C, Linden F, Domschke G, Akhavanpoor M, Helmes CM, et al. Galectin-3 binding protein, coronary artery disease and cardiovascular mortality: Insights from the LURIC study. Atherosclerosis. 2017;260:121-129. doi: 10.1016/j.atherosclerosis.2017.03.031
73. Nielsen CT, Østergaard O, Rekvig OP, Sturfelt G, Jacobsen S, Heegaard NH. Galectin-3 binding protein links circulating microparticles with electron dense glomerular deposits in lupus nephritis. Lupus. 2015;24(11):1150-1160. doi: 10.1177/0961203315580146
74. Ding H, Shen Y, Lin C, Qin L, He S, Dai M, et al. Urinary galectin-3 binding protein (G3BP) as a biomarker for disease activity and renal pathology characteristics in lupus nephritis. Arthritis Res Ther. 2022;24(1):77. doi: 10.1186/s13075-022-02763-4
Рецензия
Для цитирования:
Кондратьева Л.В., Попкова Т.В., Насонов Е.Л. Галектины, антитела к ним и галектин-3-связывающий белок при системной красной волчанке. Научно-практическая ревматология. 2025;63(1):37-45. https://doi.org/10.47360/1995-4484-2025-37-45
For citation:
Kondratyeva L.V., Popkova T.V., Nasonov E.L. Galectins, antibodies to them and galectin-3 binding protein in systemic lupus erythematosus. Rheumatology Science and Practice. 2025;63(1):37-45. (In Russ.) https://doi.org/10.47360/1995-4484-2025-37-45