Research progress on the regulatory mechanisms and influencing factors of blood-brain barrier permeability in optic neuromyelitis spectrum diseases_Chinese Journal of Ocular Fundus Diseases

Authors：

Chen Siqi ,  Yang Hui

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangdong Provincial Key Laboratory of Ophthalmology and Visual Science, Guangzhou 510060, China;

Corresponding author：

Yang Hui, Email: yanghui9@hotmail.com

Keywords：

Neuromyelitis optic spectrum disorders; Blood brain barrier; Aquaporin 4 antibody; Review

DOI：

10.3760/cma.j.cn511434-20230117-00026

Video：

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Abstract Full text Figures/Tables Video References Cited by

Neuromyelitis spectrum disease (NMOSD) is an immune-mediated inflammatory demyelinating disease of the central nervous system. The breakdown of the blood-brain barrier (BBB), as an important link in the pathogenesis of NMOSD, has an important impact on the occurrence, development and prognosis of the disease. It is generally believed that the aquaporin 4 antibody produced in the peripheral circulation crosses the BBB cause damage to the central nervous system, and there are components involved in the destruction of BBB in the occurrence and development of NMOSD disease. At present, little is known about the molecular mechanism of BBB destruction in NMOSD lesions and there is still a lack of systematic theory. Further research and exploration of the regulatory mechanism of BBB permeability and the manifestation of barrier destruction in NMOSD diseases are of great significance for understanding the pathogenesis of NMOSD, so as to achieve early diagnosis and discover new therapeutic and preventive targets.

Citation： Chen Siqi, Yang Hui. Research progress on the regulatory mechanisms and influencing factors of blood-brain barrier permeability in optic neuromyelitis spectrum diseases. Chinese Journal of Ocular Fundus Diseases, 2023, 39(11): 938-943. doi: 10.3760/cma.j.cn511434-20230117-00026 Copy

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1. Wingerchuk DM, Lucchinetti CF, et al. Neuromyelitis optica spectrum disorder[J]. N Engl J Med, 2022, 387(7): 631-639. DOI: 10.1056/NEJMra1904655.
2. Coisne C, Engelhardt B. Tight junctions in brain barriers during central nervous system inflammation[J]. Antioxid Redox Signal, 2011, 15(5): 1285-1303. DOI: 10.1089/ars.2011.3929.
3. Akaza M, Tanaka K, Tanaka M, et al. Can anti-AQP4 antibody damage the blood-brain barrier?[J]. Eur Neurol, 2014, 72(5-6): 273-277. DOI: 10.1159/000360619.
4. Hillebrand S, Schanda K, Nigritinou M, et al. Circulating AQP4-specific auto-antibodies alone can induce neuromyelitis optica spectrum disorder in the rat[J]. Acta Neuropathologica, 2019, 137(3): 467-485. DOI: 10.1007/s00401-018-1950-8.
5. Bennett JL, Lam C, Kalluri SR, et al. Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica[J]. Ann Neurol, 2009, 66(5): 617-629. DOI: 10.1002/ana.21802.
6. Cho S, Lee H, Jung M, et al. Neuromyelitis optica (NMO)-IgG-driven organelle reorganization in human iPSC-derived astrocytes[J/OL]. FASEB J, 2021, 35(10): e21894[2021-08-30]. https://pubmed.ncbi.nlm.nih.gov/34460995/. DOI: 10.1096/fj.202100637R.
7. Chen T, Lennon VA, Liu YU, et al. Astrocyte-microglia interaction drives evolving neuromyelitis optica lesion[J]. J Clin Invest, 2020, 130(8): 4025-4038. DOI: 10.1172/JCI134816.
8. Ganong WF. Circumventricular organs: definition and role in the regulation of endocrine and autonomic function[J]. Clin Exp Pharmacol Physiol, 2000, 27(5-6): 422-427. DOI: 10.1046/j.1440-1681.2000.03259.x.
9. Miyata S. New aspects in fenestrated capillary and tissue dynamics in the sensory circumventricular organs of adult brains[J/OL]. Front Neurosci, 2015, 9: 930[2015-10-27]. https://pubmed.ncbi.nlm.nih.gov/26578857/. DOI: 10.3389/fnins.2015.00390.
10. Popescu BF, Lennon VA, Parisi JE, et al. Neuromyelitis optica unique area postrema lesions: nausea, vomiting, and pathogenic implications[J]. Neurology, 2011, 76(14): 1229-1237. DOI: 10.1212/WNL.0b013e318214332c.
11. Ratelade J, Bennett JL, Verkman AS. Intravenous neuromyelitis optica autoantibody in mice targets aquaporin-4 in peripheral organs and area postrema[J/OL]. PLoS One, 2011, 6(11): e27412[2011-11-04]. https://pubmed.ncbi.nlm.nih.gov/22076159/. DOI: 10.1371/journal.pone.0027412.
12. Iliff JJ, Wang M, Liao Y, et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β[J/OL]. Sci Transl Med, 2012, 4(147): 147[2012-08-15]. https://pubmed.ncbi.nlm.nih.gov/22896675/. DOI: 10.1126/scitranslmed.3003748.
13. Klarica M, Radoš M, Orešković D. The movement of cerebrospinal fluid and its relationship with substances behavior in cerebrospinal and interstitial fluid[J]. Neuroscience, 2019, 414: 28-48. DOI: 10.1016/j.neuroscience.2019.06.032.
14. Marignier R, Ruiz A, Cavagna S, et al. Neuromyelitis optica study model based on chronic infusion of autoantibodies in rat cerebrospinal fluid[J]. J Neuroinflammation, 2016, 13(1): 111. DOI: 10.1186/s12974-016-0577-8.
15. Mogensen FL, Delle C, Nedergaard M. The glymphatic system (en)during inflammation[J/OL]. Int J Mol Sci, 2021, 22(14): 7491[2021-07-13]. https://pubmed.ncbi.nlm.nih.gov/34299111/. DOI: 10.3390/ijms22147491.
16. Zhang Y, Bao Y, Qiu W, et al. Structural and visual functional deficits in a rat model of neuromyelitis optica spectrum disorders related optic neuritis[J]. Exp Eye Res, 2018, 175: 124-132. DOI: 10.1016/j.exer.2018.06.011.
17. Guo Y, Weigand SD, Popescu BF, et al. Pathogenic implications of cerebrospinal fluid barrier pathology in neuromyelitis optica[J]. Acta Neuropathol, 2017, 133(4): 597-612. DOI: 10.1007/s00401-017-1682-1.
18. Propson NE, Roy ER, Litvinchuk A, et al. Endothelial C3a receptor mediates vascular inflammation and blood-brain barrier permeability during aging[J/OL]. J Clin Invest, 2021, 131(1): e140966[2021-01-04]. https://pubmed.ncbi.nlm.nih.gov/32990682/. DOI: 10.1172/JCI140966.
19. Nytrova P, Potlukova E, Kemlink D, et al. Complement activation in patients with neuromyelitis optica[J]. J Neuroimmunol, 2014, 274(1-2): 185-191. DOI: 10.1016/j.jneuroim.2014.07.001.
20. Haruwaka K, Ikegami A, Tachibana Y, et al. Dual microglia effects on blood brain barrier permeability induced by systemic inflammation[J/OL]. Nat Commun, 2019, 10(1): 5816[2019-12-20]. https://pubmed.ncbi.nlm.nih.gov/31862977/. DOI: 10.1038/s41467-019-13812-z.
21. Lin L, Wu Y, Hang H, et al. Plasma complement 3 and complement 4 are promising biomarkers for distinguishing NMOSD from mogad and are associated with the blood-brain-barrier disruption in NMOSD[J/OL]. Front Immunol, 2022, 13: 853891[2022-07-11]. https://pubmed.ncbi.nlm.nih.gov/35898513/. DOI: 10.3389/fimmu.2022.853891.
22. Zelek WM, Fathalla D, Morgan A, et al. Cerebrospinal fluid complement system biomarkers in demyelinating disease[J]. Mult Scler, 2020, 26(14): 1929-1937. DOI: 10.1177/1352458519887905.
23. Pan C, Zhao Y, Xie H, et al. Effect of low complement C4 on clinical characteristics of patients with first-episode neuromyelitis optica spectrum disorder[J]. Neuropsychiatr Dis Treat, 2021, 17: 2859-2866. DOI: 10.2147/NDT.S322789.
24. Gonzalez-Gronow M, Pizzo SV. Physiological roles of the autoantibodies to the 78-kilodalton glucose-regulated protein (GRP78) in cancer and autoimmune diseases[J/OL]. Biomedicines, 2022, 10(6): 1222[2022-05-24]. https://pubmed.ncbi.nlm.nih.gov/35740249/. DOI: 10.3390/biomedicines10061222.
25. Shimizu F, Schaller KL, Owens GP, et al. Glucose-regulated protein 78 autoantibody associates with blood-brain barrier disruption in neuromyelitis optica[J/OL]. Sci Transl Med, 2017, 9(397): e9111[2017-07-05]. https://pubmed.ncbi.nlm.nih.gov/28679661/. DOI: 10.1126/scitranslmed.aai9111.
26. Shimizu F, Takeshita Y, Hamamoto Y, et al. GRP 78 antibodies are associated with clinical phenotype in neuromyelitis optica[J]. Ann Clin Transl Neurol, 2019, 6(10): 2079-2087. DOI: 10.1002/acn3.50905.
27. Fujihara K, Bennett JL, De Seze J, et al. Interleukin-6 in neuromyelitis optica spectrum disorder pathophysiology[J/OL]. Neurol Neuroimmunol Neuroinflamm, 2020, 7(5): e841[2020-08-20]. https://pubmed.ncbi.nlm.nih.gov/32820020/. DOI: 10.1212/NXI.0000000000000841.
28. Erta M, Quintana A, Hidalgo J. Interleukin-6, a major cytokine in the central nervous system[J]. Int J Biol Sci, 2012, 8(9): 1254-1266. DOI: 10.7150/ijbs.4679.
29. Uzawa A, Mori M, Masuda H, et al. Interleukin-6 analysis of 572 consecutive CSF samples from neurological disorders: a special focus on neuromyelitis optica[J]. Clin Chim Acta, 2017, 469: 144-149. DOI: 10.1016/j.cca.2017.03.006.
30. Takeshita Y, Obermeier B, Cotleur AC, et al. Effects of neuromyelitis optica-IgG at the blood-brain barrier in vitro[J/OL]. Neurol Neuroimmunol Neuroinflamm, 2016, 4(1): e311[2016-12-19]. https://pubmed.ncbi.nlm.nih.gov/28018943/. DOI: 10.1212/NXI.0000000000000311.
31. Takeshita Y, Fujikawa S, Serizawa K, et al. New BBB model reveals that IL-6 blockade suppressed the BBB disorder, preventing onset of NMOSD[J/OL]. Neurol Neuroimmunol Neuroinflamm, 2021, 8(6): e1076[2021-10-19]. https://pubmed.ncbi.nlm.nih.gov/34667128/. DOI: 10.1212/NXI.0000000000001076.
32. Hosokawa T, Nakajima H, Doi Y, et al. Increased serum matrix metalloproteinase-9 in neuromyelitis optica: implication of disruption of blood-brain barrier[J]. J Neuroimmunol, 2011, 236(1-2): 81-86. DOI: 10.1016/j.jneuroim.2011.04.009.
33. Uchida T, Mori M, Uzawa A, et al. Increased cerebrospinal fluid metalloproteinase-2 and interleukin-6 are associated with albumin quotient in neuromyelitis optica: their possible role on blood-brain barrier disruption[J]. Mult Scler, 2017, 23(8): 1072-1084. DOI: 10.1177/1352458516672015.
34. Apte RS, Chen DS, Ferrara N. VEGF in signaling and disease: beyond discovery and development[J]. Cell, 2019, 176(6): 1248-1264. DOI: 10.1016/j.cell.2019.01.021.
35. Ferrara N, Adamis AP. Ten years of anti-vascular endothelial growth factor therapy[J]. Nat Rev Drug Discov, 2016, 15(6): 385-403. DOI: 10.1038/nrd.2015.17.
36. Shimizu F, Sano Y, Takahashi T, et al. Sera from neuromyelitis optica patients disrupt the blood-brain barrier[J]. J Neurol Neurosurg Psychiatry, 2012, 83(3): 288-297. DOI: 10.1136/jnnp-2011-300434.
37. Mealy MA, Shin K, John G, et al. Bevacizumab is safe in acute relapses of neuromyelitis optica[J]. Clin Exp Neuroimmunol, 2015, 6(4): 413-418. DOI: 10.1111/cen3.12239.
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Research progress on the regulatory mechanisms and influencing factors of blood-brain barrier permeability in optic neuromyelitis spectrum diseases

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