Роль нарушения целостности гематоэнцефалического барьера в развитии двигательных нарушений при аутоиммунных заболеваниях, сопровождающихся психопатологической симптоматикой
Рекомендуемое оформление библиографической ссылки:
Барканова В., Шмуклер А.Б. Роль нарушения целостности гематоэнцефалического барьера в развитии двигательных нарушений при аутоиммунных заболеваниях, сопровождающихся психопатологической симптоматикой // Российский психиатрический журнал. 2023. №3. С. 91-103.
В данном систематическом обзоре осуществлен анализ роли целостности гематоэнцефалического барьера в отношении развития двигательных нарушений у пациентов с аутоиммунными заболеваниями, проявляющимися широким спектром психических расстройств: от легких аффективных нарушений до психотической симптоматики с кататоническими включениями. Обзор выполнен по критериям PRISMA 2020 и включает в себя 19 исследований. Показано, что повреждения гематоэнцефалического барьера и высокого титра антител не всегда достаточно для возникновения развернутой клинической картины заболевания. Развитие кататонической симптоматики не во всех случаях сопровождается одновременным повреждением гематоэнцефалического барьера. Однако для тяжелого течения заболевания характерно такое повреждение. Подчеркивается важность других, сопутствующих факторов в развитии двигательных нарушений при аутоиммунных заболеваниях, клиническая картина которых включает психопатологическую симптоматику.
Ключевые слова психопатологическая симптоматика; кататония; двигательные нарушения; гематоэнцефалический барьер; аутоиммунные заболевания; анти-NMDA-рецепторный энцефалит; нейропсихиатрическая системная красная волчанка; антифосфолипидный синдром
1. Weiss DB, Dyrud J, House RM, Beresford TP. Psychiatric manifestations of autoimmune disorders. Curr Treat Options Neurol. 2005;7(5):413–7. DOI: https://doi.org/10.1007/s11940-005-0033-z 2. Cullen AE, Holmes S, Pollak TA, et al. Associations Between Non-neurological Autoimmune Disorders and Psychosis: A Meta-analysis. Biol Psychiatry. 2019;85(1):35–48. DOI: https://doi.org/10.1016/j.biopsych.2018.06.016 3. Benros ME, Mortensen PB, Eaton WW. Autoimmune diseases and infections as risk factors for schizophrenia. Ann N Y Acad Sci. 2012;1262:56–66. DOI: https://doi.org/10.1111/j.1749-6632.2012.06638.x 4. Benros ME, Waltoft BL, Nordentoft M, et al. Autoimmune diseases and severe infections as risk factors for mood disorders: a nationwide study. JAMA Psychiatry. 2013;70(8):812–20. DOI: https://doi.org/10.1001/jamapsychiatry.2013.1111 5. Lejuste F, Thomas L, Picard G, et al. Neuroleptic intolerance in patients with anti-NMDAR encephalitis. Neurol Neuroimmunol Neuroinflamm. 2016;3(5):e280. DOI: https://doi.org/10.1212/NXI.0000000000000280 6. Sarkis RA, Coffey MJ, Cooper JJ, et al. Anti-N-Methyl-D-Aspartate Receptor Encephalitis: A Review of Psychiatric Phenotypes and Management Considerations: A Report of the American Neuropsychiatric Association Committee on Research. J Neuropsychiatry Clin Neurosci. 2019;31(2):137–42. DOI: https://doi.org/10.1176/appi.neuropsych.18010005 7. Mané-Damas M, Hoffmann C, Zong S, et al. Autoimmunity in psychotic disorders. Where we stand, challenges and opportunities. Autoimmun Rev. 2019;18(9):102348. DOI: https://doi.org/10.1016/j.autrev.2019.102348 8. Lang K, Prüss H. Frequencies of neuronal autoantibodies in healthy controls: Estimation of disease specificity. Neurol Neuroimmunol Neuroinflamm. 2017;4(5):e386. DOI: https://doi.org/10.1212/NXI.0000000000000386 9. Mueller SH, Färber A, Prüss H, et al.; German Network for Research on Autoimmune Encephalitis (GENERATE). Genetic predisposition in anti-LGI1 and anti-NMDA receptor encephalitis. Ann Neurol. 2018;83(4):863–9. DOI: https://doi.org/10.1002/ana.25216 10. Prüss H, Finke C, Höltje M, et al. N-methyl-D-aspartate receptor antibodies in herpes simplex encephalitis. Ann Neurol. 2012;72(6):902–11. DOI: https://doi.org/10.1002/ana.23689 11. Armangue T, Moris G, Cantarín-Extremera V, et al; Spanish Prospective Multicentric Study of Autoimmunity in Herpes Simplex Encephalitis. Autoimmune post-herpes simplex encephalitis of adults and teenagers. Neurology. 2015;85(20):1736–43. DOI: https://doi.org/10.1212/WNL.0000000000002125 12. Galli J, Clardy SL, Piquet AL. NMDAR Encephalitis Following Herpes Simplex Virus Encephalitis. Curr Infect Dis Rep. 2017;19(1):1. DOI: https://doi.org/10.1007/s11908-017-0556-y 13. Armangue T, Spatola M, Vlagea A, et al.; Spanish Herpes Simplex Encephalitis Study Group. Frequency, symptoms, risk factors, and outcomes of autoimmune encephalitis after herpes simplex encephalitis: a prospective observational study and retrospective analysis. Lancet Neurol. 2018;17(9):760–72. DOI: https://doi.org/10.1016/S1474-4422(18)30244-8 14. Hou R, Wu J, He D, et al. Anti-N-methyl-D-aspartate receptor encephalitis associated with reactivated Epstein-Barr virus infection in pediatric patients: Three case reports. Medicine (Baltimore). 2019;98(20):e15726. DOI: https://doi.org/10.1097/MD.0000000000015726 15. Dalmau J, Gleichman AJ, Hughes EG, et al. Anti-NMDA-receptor encephalitis: case series and analysis of the effects of antibodies. Lancet Neurol. 2008;7(12):1091–8. DOI: https://doi.org/10.1016/S1474-4422(08)70224-2 16. Abu-Hashyeh A, Katabi A, Zeid F. Limbic Encephalitis as a Presenting Complication for Small Cell Lung Cancer. Cureus. 2020;12(8):e9623. DOI: https://doi.org/10.7759/cureus.9623 17. Mauermann ML. Neurologic Complications of Lymphoma, Leukemia, and Paraproteinemias. Continuum (Minneap Minn). 2017;23(3):669–90. DOI: https://doi.org/10.1212/CON.0000000000000468 18. Pan H, Steixner-Kumar AA, Seelbach A, et al. Multiple inducers and novel roles of autoantibodies against the obligatory NMDAR subunit NR1: a translational study from chronic life stress to brain injury. Mol Psychiatry. 2021;26(6):2471–82. DOI: https://doi.org/10.1038/s41380-020-0672-1 19. Jeppesen R, Benros ME. Autoimmune Diseases and Psychotic Disorders. Front Psychiatry. 2019;10:131. DOI: https://doi.org/10.3389/fpsyt.2019.00131 20. Hoffmann C, Zong S, Mané-Damas M, et al. Autoantibodies in Neuropsychiatric Disorders. Antibodies (Basel). 2016;5(2):9. DOI: https://doi.org/10.3390/antib5020009 21. Yu Y, Wu Y, Cao X, et al. The Clinical Features and Prognosis of Anti-NMDAR Encephalitis Depends on Blood Brain Barrier Integrity. Mult Scler Relat Disord. 2021;47:102604. DOI: https://doi.org/10.1016/j.msard.2020.102604 22. Platt MP, Agalliu D, Cutforth T. Hello from the Other Side: How Autoantibodies Circumvent the Blood-Brain Barrier in Autoimmune Encephalitis. Front Immunol. 2017;8:442. DOI: https://doi.org/10.3389/fimmu.2017.00442 23. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. DOI: https://doi.org/10.1136/bmj.n71 24. Wagnon I, Hélie P, Bardou I, et al. Autoimmune encephalitis mediated by B-cell response against N-methyl-d-aspartate receptor. Brain. 2020;143(10):2957–72. DOI: https://doi.org/10.1093/brain/awaa250 25. Arinrad S, Wilke JBH, Seelbach A, et al. NMDAR1 autoantibodies amplify behavioral phenotypes of genetic white matter inflammation: a mild encephalitis model with neuropsychiatric relevance. Mol Psychiatry. 2022;27(12):4974–83. DOI: https://doi.org/10.1038/s41380-021-01392-8 26. Wilke JBH, Hindermann M, Berghoff SA, et al. Autoantibodies against NMDA receptor 1 modify rather than cause encephalitis. Mol Psychiatry. 2021;26(12):7746–59. DOI: https://doi.org/10.1038/s41380-021-01238-3 27. García-Serra A, Radosevic M, Pupak A, et al. Placental transfer of NMDAR antibodies causes reversible alterations in mice. Neurol Neuroimmunol Neuroinflamm. 2020;8(1):e915. DOI: https://doi.org/10.1212/NXI.0000000000000915 28. Hammer C, Stepniak B, Schneider A, et al. Neuropsychiatric disease relevance of circulating anti-NMDA receptor autoantibodies depends on blood-brain barrier integrity. Mol Psychiatry. 2014;19(10):1143–9. DOI: https://doi.org/10.1038/mp.2013.110 29. Pan H, Oliveira B, Saher G, et al. Uncoupling the widespread occurrence of anti-NMDAR1 autoantibodies from neuropsychiatric disease in a novel autoimmune model. Mol Psychiatry. 2019;24(10):1489-1501. DOI: https://doi.org/10.1038/s41380-017-0011-3 30. Shu Y, Peng F, Zhao B, et al. Transfer of patient's peripheral blood mononuclear cells (PBMCs) disrupts blood-brain barrier and induces anti-NMDAR encephalitis: a study of novel humanized PBMC mouse model. J Neuroinflammation. 2023;20(1):164. DOI: https://doi.org/10.1186/s12974-023-02844-4 31. Cai L, Liang Y, Huang H, et al. Cerebral functional activity and connectivity changes in anti-N-methyl-D-aspartate receptor encephalitis: A resting-state fMRI study. Neuroimage Clin. 2020;25:102189. DOI: https://doi.org/10.1016/j.nicl.2020.102189 32. Endres D, Meixensberger S, Dersch R, et al. Cerebrospinal fluid, antineuronal autoantibody, EEG, and MRI findings from 992 patients with schizophreniform and affective psychosis. Transl Psychiatry. 2020;10(1):279. DOI: https://doi.org/10.1038/s41398-020-00967-3 33. Kothur K, Gill D, Wong M, et al. Cerebrospinal fluid cyto-/chemokine profile during acute herpes simplex virus induced anti-N-methyl-d-aspartate receptor encephalitis and in chronic neurological sequelae. Dev Med Child Neurol. 2017;59(8):806–14. DOI: https://doi.org/10.1111/dmcn.13431 34. Wen J, Doerner J, Chalmers S, et al. B cell and/or autoantibody deficiency do not prevent neuropsychiatric disease in murine systemic lupus erythematosus. J Neuroinflammation. 2016;13(1):73. DOI: https://doi.org/10.1186/s12974-016-0537-3 35. Katzav A, Menachem A, Maggio N, et al. IgG accumulates in inhibitory hippocampal neurons of experimental antiphospholipid syndrome. J Autoimmun. 2014;55:86–93. DOI: https://doi.org/10.1016/j.jaut.2014.07.006 36. Wen J, Xia Y, Stock A, et al. Neuropsychiatric disease in murine lupus is dependent on the TWEAK/Fn14 pathway. J Autoimmun. 2013;43:44–54. DOI: https://doi.org/10.1016/j.jaut.2013.03.002 37. Nikolopoulos D, Manolakou T, Polissidis A, et al. Microglia activation in the presence of intact blood-brain barrier and disruption of hippocampal neurogenesis via IL-6 and IL-18 mediate early diffuse neuropsychiatric lupus. Ann Rheum Dis. 2023;82(5):646–57. DOI: https://doi.org/10.1136/ard-2022-223506 38. Hirohata S, Sakuma Y, Matsueda Y, et al. Role of serum autoantibodies in blood brain barrier damages in neuropsychiatric systemic lupus erythematosus. Clin Exp Rheumatol. 2018;36(6):1003–7. DOI: https://doi.org/10.26226/morressier.56e174d7d462b8028d88aba5 39. Hirohata S, Arinuma Y, Yanagida T, Yoshio T. Blood-brain barrier damages and intrathecal synthesis of anti-N-methyl-D-aspartate receptor NR2 antibodies in diffuse psychiatric/neuropsychological syndromes in systemic lupus erythematosus. Arthritis Res Ther. 2014;16(2):R77. DOI: https://doi.org/10.1186/ar4518 40. Matsueda Y, Arinuma Y, Nagai T, Hirohata S. Elevation of serum anti-glucose-regulated protein 78 antibodies in neuropsychiatric systemic lupus erythematosus. Lupus Sci Med. 2018;5(1):e000281. DOI: https://doi.org/10.1136/lupus-2018-000281 41. Lauvsnes M, Tjensvoll A, Maroni S, et al. A permeable blood-brain barrier is not required for neuropsychatric manifestations in SLE and PSS. Annals of the Rheumatic Diseases. 2018;77:157–8 DOI: https://doi.org/10.1136/annrheumdis-2018-eular.3923 42. Spatola M, Nziza N, Jung W, et al. Neurologic sequelae of COVID-19 are determined by immunologic imprinting from previous coronaviruses. Brain. 2023;146(10):4292–305. DOI: https://doi.org/10.1093/brain/awad155 43. Planagumà J, Leypoldt F, Mannara F, et al. Human N-methyl D-aspartate receptor antibodies alter memory and behaviour in mice. Brain. 2015;138(1):94–109. DOI: https://doi.org/10.1093/brain/awu310 44. Malviya M, Barman S, Golombeck KS, et al. NMDAR encephalitis: passive transfer from man to mouse by a recombinant antibody. Ann Clin Transl Neurol. 2017;4(11):768–83. DOI: https://doi.org/10.1002/acn3.444 45. Taraschenko O, Fox HS, Eldridge E, et al. Monoclonal Antibodies From Anti-NMDA Receptor Encephalitis Patient as a Tool to Study Autoimmune Seizures. Front Neurosci. 2021;15:710650. DOI: https://doi.org/10.3389/fnins.2021.710650 46. Rosch RE, Wright S, Cooray G, et al. NMDA-receptor antibodies alter cortical microcircuit dynamics. Proc Natl Acad Sci U S A. 2018;115(42):E9916–25. DOI: https://doi.org/10.1073/pnas 47. Sharp FR, Hendren RL. Psychosis: atypical limbic epilepsy versus limbic hyperexcitability with onset at puberty? Epilepsy Behav. 2007;10(4):515–20. DOI: https://doi.org/10.1016/j.yebeh.2007.02.014 48. Kostrzewa RM. Neurotoxins. Reference Module in Neuroscience and Biobehavioral Psychology. Elsevier; 2017. DOI: https://doi.org/10.1016/B978-0-12-809324-5.02663-8 49. Lundgaard I, Luzhynskaya A, Stockley JH, et al. Neuregulin and BDNF induce a switch to NMDA receptor-dependent myelination by oligodendrocytes. PLoS Biol. 2013;11(12):e1001743. DOI: https://doi.org/10.1371/journal.pbio.1001743 50. Saab AS, Tzvetavona ID, Trevisiol A, et al. Oligodendroglial NMDA Receptors Regulate Glucose Import and Axonal Energy Metabolism. Neuron. 2016;91(1):119–32. DOI: https://doi.org/10.1016/j.neuron.2016.05.016 51. Manto M, Dalmau J, Didelot A, et al. Afferent facilitation of corticomotor responses is increased by IgGs of patients with NMDA-receptor antibodies. J Neurol. 2011;258(1):27–33. DOI: https://doi.org/10.1007/s00415-010-5674-5 52. Hansen SL, Sperling BB, Sánchez C. Anticonvulsant and antiepileptogenic effects of GABAA receptor ligands in pentylenetetrazole-kindled mice. Prog Neuropsychopharmacol Biol Psychiatry. 2004;28(1):105–13. DOI: https://doi.org/10.1016/j.pnpbp.2003.09.026 53. Fan J, Malik AB. Toll-like receptor-4 (TLR4) signaling augments chemokine-induced neutrophil migration by modulating cell surface expression of chemokine receptors. Nat Med. 2003;9(3):315–21. DOI: https://doi.org/10.1038/nm832 54. Danjo S, Ishihara Y, Watanabe M, et al. Pentylentetrazole-induced loss of blood-brain barrier integrity involves excess nitric oxide generation by neuronal nitric oxide synthase. Brain Res. 2013;1530:44–53. DOI: https://doi.org/10.1016/j.brainres.2013.06.043 55. Kim KS, Jeon MT, Kim ES, et al. Activation of NMDA receptors in brain endothelial cells increases transcellular permeability. Fluids Barriers CNS. 2022;19(1):70. DOI: https://doi.org/10.1186/s12987-022-00364-6 56. Yu Y, Wu Y, Wei J, et al. NMDA mediates disruption of blood-brain barrier permeability via Rho/ROCK signaling pathway. Neurochem Int. 2022;154:105278. DOI: https://doi.org/10.1016/j.neuint.2022.105278 57. Shlosberg D, Benifla M, Kaufer D, Friedman A. Blood-brain barrier breakdown as a therapeutic target in traumatic brain injury. Nat Rev Neurol. 2010;6(7):393–403. DOI: https://doi.org/10.1038/nrneurol.2010.74 58. Baburamani AA, Ek CJ, Walker DW, Castillo-Melendez M. Vulnerability of the developing brain to hypoxic-ischemic damage: contribution of the cerebral vasculature to injury and repair? Front Physiol. 2012;3:424. DOI: https://doi.org/10.3389/fphys.2012.00424 59. Biancardi VC, Son SJ, Ahmadi S, et al. Circulating angiotensin II gains access to the hypothalamus and brain stem during hypertension via breakdown of the blood-brain barrier. Hypertension. 2014;63(3):572–9. DOI: https://doi.org/10.1161/HYPERTENSIONAHA.113.01743 60. Fan Y, Yang X, Tao Y, et al. Tight junction disruption of blood-brain barrier in white matter lesions in chronic hypertensive rats. Neuroreport. 2015;26(17):1039–43. DOI: https://doi.org/10.1097/WNR.0000000000000464 61. Ma Y, Wang J, Guo S, et al. Cytokine/chemokine levels in the CSF and serum of anti-NMDAR encephalitis: A systematic review and meta-analysis. Front Immunol. 2023;13:1064007. DOI: https://doi.org/10.3389/fimmu.2022.1064007 62. Camdessanché JP, Streichenberger N, Cavillon G, et al. Brain immunohistopathological study in a patient with anti-NMDAR encephalitis. Eur J Neurol. 2011;18(6):929–31. DOI: https://doi.org/10.1111/j.1468-1331.2010.03180.x 63. Filatenkov A, Richardson TE, Daoud E, et al. Persistence of parenchymal and perivascular T-cells in treatment-refractory anti-N-methyl-D-aspartate receptor encephalitis. Neuroreport. 2017;28(14):890–5. DOI: https://doi.org/10.1097/WNR.0000000000000851 64. Blamire AM, Anthony DC, Rajagopalan B, et al. Interleukin-1beta -induced changes in blood-brain barrier permeability, apparent diffusion coefficient, and cerebral blood volume in the rat brain: a magnetic resonance study. J Neurosci. 2000;20(21):8153–9. DOI: https://doi.org/10.1523/JNEUROSCI.20-21-08153.2000 65. Labus J, Häckel S, Lucka L, Danker K. Interleukin-1β induces an inflammatory response and the breakdown of the endothelial cell layer in an improved human THBMEC-based in vitro blood-brain barrier model. J Neurosci Methods. 2014;228:35–45. DOI: https://doi.org/10.1016/j.jneumeth.2014.03.002 66. Argaw AT, Zhang Y, Snyder BJ, et al. IL-1beta regulates blood-brain barrier permeability via reactivation of the hypoxia-angiogenesis program. J Immunol. 2006;177(8):5574–84. DOI: https://doi.org/10.4049/jimmunol.177.8.5574 67. Melnikov PA, Valikhov MP, Kuznetsov II, et al. Analysis of the Effect of IL-1β on Blood-Brain Barrier Permeability in M6 Glioma Mouse Model Using Intravital Microscopy. Bull Exp Biol Med. 2019;168(1):118–24. DOI: https://doi.org/10.1007/s10517-019-04661-3 68. Wang Y, Jin S, Sonobe Y, et al. Interleukin-1β induces blood-brain barrier disruption by downregulating Sonic hedgehog in astrocytes. PLoS One. 2014;9(10):e110024. DOI: https://doi.org/10.1371/journal.pone.0110024 69. Ching S, He L, Lai W, Quan N. IL-1 type I receptor plays a key role in mediating the recruitment of leukocytes into the central nervous system. Brain Behav Immun. 2005;19(2):127–37. DOI: https://doi.org/10.1016/j.bbi.2004.06.001 70. Shaftel SS, Carlson TJ, Olschowka JA, et al. Chronic interleukin-1beta expression in mouse brain leads to leukocyte infiltration and neutrophil-independent blood brain barrier permeability without overt neurodegeneration. J Neurosci. 2007;27(35):9301–9. DOI: https://doi.org/10.1523/JNEUROSCI.1418-07.2007 71. Li Y, Yang K, Zhang F, et al. Identification of cerebrospinal fluid biomarker candidates for anti-N-methyl-D-aspartate receptor encephalitis: High-throughput proteomic investigation. Front Immunol. 2022;13:971659. DOI: https://doi.org/10.3389/fimmu.2022.971659 72. Faust TW, Chang EH, Kowal C, et al. Neurotoxic lupus autoantibodies alter brain function through two distinct mechanisms. Proc Natl Acad Sci U S A. 2010;107(43):18569–74. DOI: https://doi.org/10.1073/pnas.1006980107 73. Katzav A, Litvinjuk Y, Pick CG, et al. Genetic and immunological factors interact in a mouse model of CNS antiphospholipid syndrome. Behav Brain Res. 2006;169(2):289–93. DOI: https://doi.org/10.1016/j.bbr.2006.01.015 74. Katzav A, Pick CG, Korczyn AD, et al. Hyperactivity in a mouse model of the antiphospholipid syndrome. Lupus. 2001;10(7):496–9. DOI: https://doi.org/10.1191/096120301678416060 75. Ziporen L, Shoenfeld Y, Levy Y, Korczyn AD. Neurological dysfunction and hyperactive behavior associated with antiphospholipid antibodies. A mouse model. J Clin Invest. 1997;100(3):613–9. DOI: https://doi.org/10.1172/JCI119572 76. Kowal C, DeGiorgio LA, Nakaoka T, et al. Cognition and immunity; antibody impairs memory. Immunity. 2004;21(2):179–88. DOI: https://doi.org/10.1016/j.immuni.2004.07.011 77. Frauenknecht K, Katzav A, Grimm C, et al. Neurological impairment in experimental antiphospholipid syndrome is associated with increased ligand binding to hippocampal and cortical serotonergic 5-HT1A receptors. Immunobiology. 2013;218(4):517–26. DOI: https://doi.org/10.1016/j.imbio.2012.06.011 78. Muldoon MF, Mackey RH, Williams KV, et al. Low central nervous system serotonergic responsivity is associated with the metabolic syndrome and physical inactivity. J Clin Endocrinol Metab. 2004;89(1):266–71. DOI: https://doi.org/10.1210/jc.2003-031295 79. Uçeyler N, Schütt M, Palm F, et al. Lack of the serotonin transporter in mice reduces locomotor activity and leads to gender-dependent late onset obesity. Int J Obes (Lond). 2010;34(4):701–11. DOI: https://doi.org/10.1038/ijo.2009.289 80. Yoshio T, Okamoto H, Hirohata S, Minota S. IgG anti-NR2 glutamate receptor autoantibodies from patients with systemic lupus erythematosus activate endothelial cells. Arthritis Rheum. 2013;65(2):457–63. DOI: https://doi.org/10.1002/art.37745 81. Frampton G, Moriya S, Pearson JD, et al. Identification of candidate endothelial cell autoantigens in systemic lupus erythematosus using a molecular cloning strategy: a role for ribosomal P protein P0 as an endothelial cell autoantigen. Rheumatology (Oxford). 2000;39(10):1114–20. DOI: https://doi.org/10.1093/rheumatology/39.10.1114 82. Kent MN, Alvarez FJ, Ng AK, Rote NS. Ultrastructural localization of monoclonal antiphospholipid antibody binding to rat brain. Exp Neurol. 2000;163(1):173–9. DOI: https://doi.org/10.1006/exnr.2000.7358 83. Shimizu F, Schaller KL, Owens GP, et al. Glucose-regulated protein 78 autoantibody associates with blood-brain barrier disruption in neuromyelitis optica. Sci Transl Med. 2017;9(397):eaai9111. DOI: https://doi.org/10.1126/scitranslmed.aai9111 84. Diamond B, Huerta PT, Mina-Osorio P, et al. Losing your nerves? Maybe it's the antibodies. Nat Rev Immunol. 2009;9(6):449–56. DOI: https://doi.org/10.1038/nri2529 85. Sabharwal UK, Fong S, Hoch S, et al. Complement activation by antibodies to Sm in systemic lupus erythematosus. Clin Exp Immunol. 1983;51(2):317–24. PMID: 6601552 86. Jacob A, Hack B, Chen P, et al. C5a/CD88 signaling alters blood-brain barrier integrity in lupus through nuclear factor-κB. J Neurochem. 2011;119(5):1041–51. DOI: https://doi.org/10.1111/j.1471-4159.2011.07490.x 87. Jacob A, Hack B, Chiang E, et al. C5a alters blood-brain barrier integrity in experimental lupus. FASEB J. 2010;24(6):1682–8. DOI: https://doi.org/10.1096/fj.09-138834 88. Nagai T, Arinuma Y, Yanagida T, et al. Anti-ribosomal P protein antibody in human systemic lupus erythematosus up-regulates the expression of proinflammatory cytokines by human peripheral blood monocytes. Arthritis Rheum. 2005;52(3):847–55. DOI: https://doi.org/10.1002/art.20869 89. Katzav A, Shoenfeld Y, Chapman J. The pathogenesis of neural injury in animal models of the antiphospholipid syndrome. Clin Rev Allergy Immunol. 2010;38(2–3):196–200. DOI: https://doi.org/10.1007/s12016-009-8154-x 90. Haruwaka K, Ikegami A, Tachibana Y, et al. Dual microglia effects on blood brain barrier permeability induced by systemic inflammation. Nat Commun. 2019;10(1):5816. DOI: https://doi.org/10.1038/s41467-019-13812-z 91. Ainiala H, Hietaharju A, Dastidar P, et al. Increased serum matrix metalloproteinase 9 levels in systemic lupus erythematosus patients with neuropsychiatric manifestations and brain magnetic resonance imaging abnormalities. Arthritis Rheum. 2004;50(3):858–65. DOI: https://doi.org/10.1002/art.20045
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