nach oben

Erschienen in:

01.06.2024 | Original Paper

Stage-dependent immunity orchestrates AQP4 antibody-guided NMOSD pathology: a role for netting neutrophils with resident memory T cells in situ

verfasst von: Akihiro Nakajima, Fumihiro Yanagimura, Etsuji Saji, Hiroshi Shimizu, Yasuko Toyoshima, Kaori Yanagawa, Musashi Arakawa, Mariko Hokari, Akiko Yokoseki, Takahiro Wakasugi, Kouichirou Okamoto, Hirohide Takebayashi, Chihiro Fujii, Kyoko Itoh, Yo-ichi Takei, Shinji Ohara, Mitsunori Yamada, Hitoshi Takahashi, Masatoyo Nishizawa, Hironaka Igarashi, Akiyoshi Kakita, Osamu Onodera, Izumi Kawachi

Erschienen in: Acta Neuropathologica | Ausgabe 1/2024

Einloggen, um Zugang zu erhalten

Abstract

Neuromyelitis optica spectrum disorder (NMOSD) is an autoimmune disease of the CNS characterized by the production of disease-specific autoantibodies against aquaporin-4 (AQP4) water channels. Animal model studies suggest that anti-AQP4 antibodies cause a loss of AQP4-expressing astrocytes, primarily via complement-dependent cytotoxicity. Nonetheless, several aspects of the disease remain unclear, including: how anti-AQP4 antibodies cross the blood–brain barrier from the periphery to the CNS; how NMOSD expands into longitudinally extensive transverse myelitis or optic neuritis; how multiphasic courses occur; and how to prevent attacks without depleting circulating anti-AQP4 antibodies, especially when employing B-cell-depleting therapies. To address these knowledge gaps, we conducted a comprehensive ‘stage-dependent’ investigation of immune cell elements in situ in human NMOSD lesions, based on neuropathological techniques for autopsied/biopsied CNS materials. The present study provided three major findings. First, activated or netting neutrophils and melanoma cell adhesion molecule-positive (MCAM⁺) helper T (T_H) 17/cytotoxic T (T_C) 17 cells are prominent, and the numbers of these correlate with the size of NMOSD lesions in the initial or early-active stages. Second, forkhead box P3-positive (FOXP3⁺) regulatory T (T_reg) cells are recruited to NMOSD lesions during the initial, early-active or late-active stages, suggesting rapid suppression of proinflammatory autoimmune events in the active stages of NMOSD. Third, compartmentalized resident memory immune cells, including CD103⁺ tissue-resident memory T (T_RM) cells with long-lasting inflammatory potential, are detected under “standby” conditions in all stages. Furthermore, CD103⁺ T_RM cells express high levels of granzyme B/perforin-1 in the initial or early-active stages of NMOSD in situ. We infer that stage-dependent compartmentalized immune traits orchestrate the pathology of anti-AQP4 antibody-guided NMOSD in situ. Our work further suggests that targeting activated/netting neutrophils, MCAM⁺ T_H17/T_C17 cells, and CD103⁺ T_RM cells, as well as promoting the expansion of FOXP3⁺ T_reg cells, may be effective in treating and preventing relapses of NMOSD.

Nur mit Berechtigung zugänglich

Agasing AM, Wu Q, Khatri B, Borisow N, Ruprecht K, Brandt AU et al (2020) Transcriptomics and proteomics reveal a cooperation between interferon and T-helper 17 cells in neuromyelitis optica. Nat Commun 11:2856. https://doi.org/10.1038/s41467-020-16625-7CrossRefPubMedPubMedCentral

Behnen M, Leschczyk C, Möller S, Batel T, Klinger M, Solbach W et al (2014) Immobilized immune complexes induce neutrophil extracellular trap release by human neutrophil granulocytes via FcγRIIIB and Mac-1. J Immunol 193:1954–1965. https://doi.org/10.4049/jimmunol.1400478CrossRefPubMed

Beltran E, Gerdes LA, Hansen J, Flierl-Hecht A, Krebs S, Blum H et al (2019) Early adaptive immune activation detected in monozygotic twins with prodromal multiple sclerosis. J Clin Investig 129:4758–4768. https://doi.org/10.1172/JCI128475CrossRefPubMedPubMedCentral

Boeltz S, Amini P, Anders HJ, Andrade F, Bilyy R, Chatfield S et al (2019) To NET or not to NET:current opinions and state of the science regarding the formation of neutrophil extracellular traps. Cell Death Differ 26:395–408. https://doi.org/10.1038/s41418-018-0261-xCrossRefPubMedPubMedCentral

Brinkmann V, Zychlinsky A (2012) Neutrophil extracellular traps: is immunity the second function of chromatin? J Cell Biol 198:773–783. https://doi.org/10.1083/jcb.201203170CrossRefPubMedPubMedCentral

Brucklacher-Waldert V, Stuerner K, Kolster M, Wolthausen J, Tolosa E (2009) Phenotypical and functional characterization of T helper 17 cells in multiple sclerosis. Brain 132:3329–3341. https://doi.org/10.1093/brain/awp289CrossRefPubMed

Buggert M, Price DA, Mackay LK, Betts MR (2023) Human circulating and tissue-resident memory CD8(+) T cells. Nat Immunol 24:1076–1086. https://doi.org/10.1038/s41590-023-01538-6CrossRefPubMed

Carnero Contentti E, Correale J (2023) Association between infections, the microbiome, vaccination, and neuromyelitis optica spectrum disorder. Mult Scler 29:492–501. https://doi.org/10.1177/13524585221113272CrossRefPubMed

Cassinotto C, Deramond H, Olindo S, Aveillan M, Smadja D, Cabre P (2009) MRI of the spinal cord in neuromyelitis optica and recurrent longitudinal extensive myelitis. J Neuroradiol 36:199–205. https://doi.org/10.1016/j.neurad.2008.12.008CrossRefPubMed

10.

Charabati M, Zandee S, Fournier AP, Tastet O, Thai K, Zaminpeyma R et al (2023) MCAM+ brain endothelial cells contribute to neuroinflammation by recruiting pathogenic CD4+ T lymphocytes. Brain 146:1483–1495. https://doi.org/10.1093/brain/awac389CrossRefPubMed

11.

Cheuk S, Schlums H, Gallais Serezal I, Martini E, Chiang SC, Marquardt N et al (2017) CD49a Expression Defines Tissue-Resident CD8(+) T Cells Poised for Cytotoxic Function in Human Skin. Immunity 46:287–300. https://doi.org/10.1016/j.immuni.2017.01.009CrossRefPubMedPubMedCentral

12.

Cree BAC, Bennett JL, Kim HJ, Weinshenker BG, Pittock SJ, Wingerchuk DM et al (2019) Inebilizumab for the treatment of neuromyelitis optica spectrum disorder (N-MOmentum): a double-blind, randomised placebo-controlled phase 2/3 trial. Lancet 394:1352–1363. https://doi.org/10.1016/S0140-6736(19)31817-3CrossRefPubMed

13.

Daniel C, Leppkes M, Munoz LE, Schley G, Schett G, Herrmann M (2019) Extracellular DNA traps in inflammation, injury and healing. Nat Rev Nephrol 15:559–575. https://doi.org/10.1038/s41581-019-0163-2CrossRefPubMed

14.

Dean JW, Helm EY, Fu Z, Xiong L, Sun N, Oliff KN et al (2023) The aryl hydrocarbon receptor cell intrinsically promotes resident memory CD8(+) T cell differentiation and function. Cell Rep 42:111963. https://doi.org/10.1016/j.celrep.2022.111963CrossRefPubMedPubMedCentral

15.

Duan T, Verkman AS (2020) Experimental animal models of aquaporin-4-IgG-seropositive neuromyelitis optica spectrum disorders: progress and shortcomings. Brain Pathol 30:13–25. https://doi.org/10.1111/bpa.12793CrossRefPubMed

16.

Felix CM, Levin MH, Verkman AS (2016) Complement-independent retinal pathology produced by intravitreal injection of neuromyelitis optica immunoglobulin G. J Neuroinflammation 13:275. https://doi.org/10.1186/s12974-016-0746-9CrossRefPubMedPubMedCentral

17.

Flanagan K, Fitzgerald K, Baker J, Regnstrom K, Gardai S, Bard F et al (2012) Laminin-411 is a vascular ligand for MCAM and facilitates TH17 cell entry into the CNS. PLoS ONE 7:e40443. https://doi.org/10.1371/journal.pone.0040443CrossRefPubMedPubMedCentral

18.

Fousert E, Toes R, Desai J (2020) Neutrophil Extracellular Traps (NETs) Take the Central Stage in Driving Autoimmune Responses. Cells. https://doi.org/10.3390/cells9040915CrossRefPubMedPubMedCentral

19.

Fransen NL, Hsiao CC, van der Poel M, Engelenburg HJ, Verdaasdonk K, Vincenten MCJ et al (2020) Tissue-resident memory T cells invade the brain parenchyma in multiple sclerosis white matter lesions. Brain 143:1714–1730. https://doi.org/10.1093/brain/awaa117CrossRefPubMed

20.

Frieser D, Pignata A, Khajavi L, Shlesinger D, Gonzalez-Fierro C, Nguyen XH et al (2022) Tissue-resident CD8(+) T cells drive compartmentalized and chronic autoimmune damage against CNS neurons. Science translational medicine 14:6157. https://doi.org/10.1126/scitranslmed.abl6157CrossRef

21.

Garcia-Romo GS, Caielli S, Vega B, Connolly J, Allantaz F, Xu Z et al (2011) Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Science translational medicine 3:7320. https://doi.org/10.1126/scitranslmed.3001201CrossRef

22.

Geginat J, Vasco C, Gruarin P, Bonnal R, Rossetti G, Silvestri Y et al (2023) Eomesodermin-expressing type 1 regulatory (EOMES(+) Tr1)-like T cells: Basic biology and role in immune-mediated diseases. Eur J Immunol 53:e2149775. https://doi.org/10.1002/eji.202149775CrossRefPubMed

23.

Gredler V, Mader S, Schanda K, Hegen H, Di Pauli F, Kuenz B et al (2013) Clinical and immunological follow-up of B-cell depleting therapy in CNS demyelinating diseases. J Neurol Sci 328:77–82. https://doi.org/10.1016/j.jns.2013.02.024CrossRefPubMed

24.

Hametner S, Wimmer I, Haider L, Pfeifenbring S, Bruck W, Lassmann H (2013) Iron and neurodegeneration in the multiple sclerosis brain. Ann Neurol 74:848–861. https://doi.org/10.1002/ana.23974CrossRefPubMedPubMedCentral

25.

Herwerth M, Kalluri SR, Srivastava R, Kleele T, Kenet S, Illes Z et al (2016) In vivo imaging reveals rapid astrocyte depletion and axon damage in a model of neuromyelitis optica-related pathology. Ann Neurol 79:794–805. https://doi.org/10.1002/ana.24630CrossRefPubMedPubMedCentral

26.

Hinson SR, McKeon A, Fryer JP, Apiwattanakul M, Lennon VA, Pittock SJ (2009) Prediction of neuromyelitis optica attack severity by quantitation of complement-mediated injury to aquaporin-4-expressing cells. Arch Neurol 66:1164–1167. https://doi.org/10.1001/archneurol.2009.188CrossRefPubMed

27.

Hinson SR, Romero MF, Popescu BF, Lucchinetti CF, Fryer JP, Wolburg H et al (2012) Molecular outcomes of neuromyelitis optica (NMO)-IgG binding to aquaporin-4 in astrocytes. Proc Natl Acad Sci U S A 109:1245–1250. https://doi.org/10.1073/pnas.1109980108CrossRefPubMed

28.

Hokari M, Yokoseki A, Arakawa M, Saji E, Yanagawa K, Yanagimura F et al (2016) Clinicopathological features in anterior visual pathway in neuromyelitis optica. Ann Neurol 79:605–624. https://doi.org/10.1002/ana.24608CrossRefPubMed

29.

Hombrink P, Helbig C, Backer RA, Piet B, Oja AE, Stark R et al (2016) Programs for the persistence, vigilance and control of human CD8(+) lung-resident memory T cells. Nat Immunol 17:1467–1478. https://doi.org/10.1038/ni.3589CrossRefPubMed

30.

Horie M, Watanabe K, Bepari AK, Nashimoto J, Araki K, Sano H et al (2014) Disruption of actin-binding domain-containing Dystonin protein causes dystonia musculorum in mice. Eur J Neurosci 40:3458–3471. https://doi.org/10.1111/ejn.12711CrossRefPubMed

31.

Ikeguchi R, Shimizu Y, Kondo A, Kanda N, So H, Kojima H et al (2021) Melanoma Cell Adhesion Molecule Expressing Helper T Cells in CNS Inflammatory Demyelinating Diseases. Neurology(R) neuroimmunology & neuroinflammation 8: e1069. https://doi.org/10.1212/NXI.0000000000001069

32.

Ito M, Komai K, Mise-Omata S, Iizuka-Koga M, Noguchi Y, Kondo T et al (2019) Brain regulatory T cells suppress astrogliosis and potentiate neurological recovery. Nature 565:246–250. https://doi.org/10.1038/s41586-018-0824-5CrossRefPubMed

33.

Jarius S, Wildemann B (2013) Aquaporin-4 antibodies (NMO-IgG) as a serological marker of neuromyelitis optica: a critical review of the literature. Brain Pathol 23:661–683. https://doi.org/10.1111/bpa.12084CrossRefPubMedPubMedCentral

34.

Kawachi I, Lassmann H (2017) Neurodegeneration in multiple sclerosis and neuromyelitis optica. J Neurol Neurosurg Psychiatry 88:137–145. https://doi.org/10.1136/jnnp-2016-313300CrossRefPubMed

35.

Kebir H, Kreymborg K, Ifergan I, Dodelet-Devillers A, Cayrol R, Bernard M et al (2007) Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat Med 13:1173–1175. https://doi.org/10.1038/nm1651CrossRefPubMedPubMedCentral

36.

Kinoshita M, Nakatsuji Y, Kimura T, Moriya M, Takata K, Okuno T et al (2009) Neuromyelitis optica: Passive transfer to rats by human immunoglobulin. Biochem Biophys Res Commun 386:623–627. https://doi.org/10.1016/j.bbrc.2009.06.085CrossRefPubMed

37.

Kinoshita M, Ogawa Y, Hama N, Ujiie I, Hasegawa A, Nakajima S et al (2021) Neutrophils initiate and exacerbate Stevens-Johnson syndrome and toxic epidermal necrolysis. Science translational medicine. https://doi.org/10.1126/scitranslmed.aax2398CrossRefPubMedPubMedCentral

38.

Korn T, Kallies A (2017) T cell responses in the central nervous system. Nat Rev Immunol 17:179–194. https://doi.org/10.1038/nri.2016.144CrossRefPubMed

39.

Kuhlmann T, Ludwin S, Prat A, Antel J, Bruck W, Lassmann H (2017) An updated histological classification system for multiple sclerosis lesions. Acta Neuropathol 133:13–24. https://doi.org/10.1007/s00401-016-1653-yCrossRefPubMed

40.

Lande R, Ganguly D, Facchinetti V, Frasca L, Conrad C, Gregorio J et al (2011) Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Science translational medicine 3:7319. https://doi.org/10.1126/scitranslmed.3001180CrossRef

41.

Laridan E, Denorme F, Desender L, François O, Andersson T, Deckmyn H et al (2017) Neutrophil extracellular traps in ischemic stroke thrombi. Ann Neurol 82:223–232. https://doi.org/10.1002/ana.24993CrossRefPubMed

42.

Larochelle C, Cayrol R, Kebir H, Alvarez JI, Lecuyer MA, Ifergan I et al (2012) Melanoma cell adhesion molecule identifies encephalitogenic T lymphocytes and promotes their recruitment to the central nervous system. Brain 135:2906–2924. https://doi.org/10.1093/brain/aws212CrossRefPubMed

43.

Larochelle C, Lecuyer MA, Alvarez JI, Charabati M, Saint-Laurent O, Ghannam S et al (2015) Melanoma cell adhesion molecule-positive CD8 T lymphocytes mediate central nervous system inflammation. Ann Neurol 78:39–53. https://doi.org/10.1002/ana.24415CrossRefPubMed

44.

Leffler J, Martin M, Gullstrand B, Tyden H, Lood C, Truedsson L et al (2012) Neutrophil extracellular traps that are not degraded in systemic lupus erythematosus activate complement exacerbating the disease. J Immunol 188:3522–3531. https://doi.org/10.4049/jimmunol.1102404CrossRefPubMed

45.

Lennon VA, Kryzer TJ, Pittock SJ, Verkman AS, Hinson SR (2005) IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med 202:473–477. https://doi.org/10.1084/jem.20050304CrossRefPubMedPubMedCentral

46.

Lennon VA, Wingerchuk DM, Kryzer TJ, Pittock SJ, Lucchinetti CF, Fujihara K et al (2004) A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 364:2106–2112. https://doi.org/10.1016/S0140-6736(04)17551-XCrossRefPubMed

47.

Li J, Patil RV, Verkman AS (2002) Mildly abnormal retinal function in transgenic mice without Muller cell aquaporin-4 water channels. Invest Ophthalmol Vis Sci 43:573–579PubMed

48.

Lucchinetti CF, Mandler RN, McGavern D, Bruck W, Gleich G, Ransohoff RM et al (2002) A role for humoral mechanisms in the pathogenesis of Devic’s neuromyelitis optica. Brain 125:1450–1461. https://doi.org/10.1093/brain/awf151CrossRefPubMed

49.

Lucchinetti CF, Popescu BF, Bunyan RF, Moll NM, Roemer SF, Lassmann H et al (2011) Inflammatory cortical demyelination in early multiple sclerosis. N Engl J Med 365:2188–2197. https://doi.org/10.1056/NEJMoa1100648CrossRefPubMedPubMedCentral

50.

Machado-Santos J, Saji E, Troscher AR, Paunovic M, Liblau R, Gabriely G et al (2018) The compartmentalized inflammatory response in the multiple sclerosis brain is composed of tissue-resident CD8+ T lymphocytes and B cells. Brain 141:2066–2082. https://doi.org/10.1093/brain/awy151CrossRefPubMedPubMedCentral

51.

Magliozzi R, Howell O, Vora A, Serafini B, Nicholas R, Puopolo M et al (2007) Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain 130:1089–1104. https://doi.org/10.1093/brain/awm038CrossRefPubMed

52.

Merino-Vico A, Frazzei G, van Hamburg JP, Tas SW (2023) Targeting B cells and plasma cells in autoimmune diseases: From established treatments to novel therapeutic approaches. Eur J Immunol 53:e2149675. https://doi.org/10.1002/eji.202149675CrossRefPubMed

53.

Middleton EA, He XY, Denorme F, Campbell RA, Ng D, Salvatore SP et al (2020) Neutrophil extracellular traps contribute to immunothrombosis in COVID-19 acute respiratory distress syndrome. Blood 136:1169–1179. https://doi.org/10.1182/blood.2020007008CrossRefPubMed

54.

Murata H, Kinoshita M, Yasumizu Y, Motooka D, Beppu S, Shiraishi N et al (2022) Cell-Free DNA Derived From Neutrophils Triggers Type 1 Interferon Signature in Neuromyelitis Optica Spectrum Disorder. Neurology(R) neuroimmunology & neuroinflammation 9: e1149. https://doi.org/10.1212/NXI.0000000000001149

55.

Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP (1997) Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 17:171–180. https://doi.org/10.1523/JNEUROSCI.17-01-00171.1997CrossRefPubMedPubMedCentral

56.

Panduro M, Benoist C, Mathis D (2016) Tissue Tregs. Annu Rev Immunol 34:609–633. https://doi.org/10.1146/annurev-immunol-032712-095948CrossRefPubMedPubMedCentral

57.

Papayannopoulos V (2018) Neutrophil extracellular traps in immunity and disease. Nat Rev Immunol 18:134–147. https://doi.org/10.1038/nri.2017.105CrossRefPubMed

58.

Pohl M, Fischer MT, Mader S, Schanda K, Kitic M, Sharma R et al (2011) Pathogenic T cell responses against aquaporin 4. Acta Neuropathol 122:21–34. https://doi.org/10.1007/s00401-011-0824-0CrossRefPubMedPubMedCentral

59.

Pohl M, Kawakami N, Kitic M, Bauer J, Martins R, Fischer MT et al (2013) T cell-activation in neuromyelitis optica lesions plays a role in their formation. Acta Neuropathol Commun 1:85. https://doi.org/10.1186/2051-5960-1-85CrossRefPubMedPubMedCentral

60.

Radermecker C, Detrembleur N, Guiot J, Cavalier E, Henket M, d’Emal C et al (2020) Neutrophil extracellular traps infiltrate the lung airway, interstitial, and vascular compartments in severe COVID-19. J Exp Med. https://doi.org/10.1084/jem.20201012CrossRefPubMedPubMedCentral

61.

Radermecker C, Hego A, Vanwinge C, Marichal T (2022) Methods to Detect Neutrophil Extracellular Traps in Asthma. Methods Mol Biol 2506:281–295. https://doi.org/10.1007/978-1-0716-2364-0_20CrossRefPubMed

62.

Ratelade J, Asavapanumas N, Ritchie AM, Wemlinger S, Bennett JL, Verkman AS (2013) Involvement of antibody-dependent cell-mediated cytotoxicity in inflammatory demyelination in a mouse model of neuromyelitis optica. Acta Neuropathol 126:699–709. https://doi.org/10.1007/s00401-013-1172-zCrossRefPubMedPubMedCentral

63.

Roemer SF, Parisi JE, Lennon VA, Benarroch EE, Lassmann H, Bruck W et al (2007) Pattern-specific loss of aquaporin-4 immunoreactivity distinguishes neuromyelitis optica from multiple sclerosis. Brain 130:1194–1205. https://doi.org/10.1093/brain/awl371CrossRefPubMed

64.

Saadoun S, Bridges LR, Verkman AS, Papadopoulos MC (2012) Paucity of natural killer and cytotoxic T cells in human neuromyelitis optica lesions. NeuroReport 23:1044–1047. https://doi.org/10.1097/WNR.0b013e32835ab480CrossRefPubMedPubMedCentral

65.

Saadoun S, Waters P, MacDonald C, Bell BA, Vincent A, Verkman AS et al (2012) Neutrophil protease inhibition reduces neuromyelitis optica-immunoglobulin G-induced damage in mouse brain. Ann Neurol 71:323–333. https://doi.org/10.1002/ana.22686CrossRefPubMedPubMedCentral

66.

Saji E, Arakawa M, Yanagawa K, Toyoshima Y, Yokoseki A, Okamoto K et al (2013) Cognitive impairment and cortical degeneration in neuromyelitis optica. Ann Neurol 73:65–76. https://doi.org/10.1002/ana.23721CrossRefPubMed

67.

Serizawa K, Miyake S, Katsura Y, Yorozu K, Kurasawa M, Tomizawa-Shinohara H et al (2023) Intradermal AQP4 peptide immunization induces clinical features of neuromyelitis optica spectrum disorder in mice. J Neuroimmunol 380:578109. https://doi.org/10.1016/j.jneuroim.2023.578109CrossRefPubMed

68.

Shichita T, Sugiyama Y, Ooboshi H, Sugimori H, Nakagawa R, Takada I et al (2009) Pivotal role of cerebral interleukin-17-producing gammadeltaT cells in the delayed phase of ischemic brain injury. Nat Med 15:946–950. https://doi.org/10.1038/nm.1999CrossRefPubMed

69.

Tadie JM, Bae HB, Jiang S, Park DW, Bell CP, Yang H et al (2013) HMGB1 promotes neutrophil extracellular trap formation through interactions with Toll-like receptor 4. Am J Physiol Lung Cell Mol Physiol 304:L342-349. https://doi.org/10.1152/ajplung.00151.2012CrossRefPubMedPubMedCentral

70.

Tahara M, Oeda T, Okada K, Kiriyama T, Ochi K, Maruyama H et al (2020) Safety and efficacy of rituximab in neuromyelitis optica spectrum disorders (RIN-1 study): a multicentre, randomised, double-blind, placebo-controlled trial. Lancet Neurol 19:298–306. https://doi.org/10.1016/S1474-4422(20)30066-1CrossRefPubMed

71.

Thompson AJ, Banwell BL, Barkhof F, Carroll WM, Coetzee T, Comi G et al (2018) Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. The Lancet Neurology 17:162–173. https://doi.org/10.1016/s1474-4422(17)30470-2CrossRefPubMed

72.

Uzawa A, Masahiro M, Kuwabara S (2014) Cytokines and chemokines in neuromyelitis optica: pathogenetic and therapeutic implications. Brain Pathol 24:67–73. https://doi.org/10.1111/bpa.12097CrossRefPubMed

73.

Uzawa A, Mori M, Arai K, Sato Y, Hayakawa S, Masuda S et al (2010) Cytokine and chemokine profiles in neuromyelitis optica: significance of interleukin-6. Mult Scler 16:1443–1452. https://doi.org/10.1177/1352458510379247CrossRefPubMed

74.

Van Avondt K, van der Linden M, Naccache PH, Egan DA, Meyaard L (2016) Signal Inhibitory Receptor on Leukocytes-1 Limits the Formation of Neutrophil Extracellular Traps, but Preserves Intracellular Bacterial Killing. J Immunol 196:3686–3694. https://doi.org/10.4049/jimmunol.1501650CrossRefPubMed

75.

van Dam LS, Kraaij T, Kamerling SWA, Bakker JA, Scherer UH, Rabelink TJ et al (2019) Intrinsically Distinct Role of Neutrophil Extracellular Trap Formation in Antineutrophil Cytoplasmic Antibody-Associated Vasculitis Compared to Systemic Lupus Erythematosus. Arthritis Rheumatol 71:2047–2058. https://doi.org/10.1002/art.41047CrossRefPubMedPubMedCentral

76.

Vandereyken K, Sifrim A, Thienpont B, Voet T (2023) Methods and applications for single-cell and spatial multi-omics. Nat Rev Genet 24:494–515. https://doi.org/10.1038/s41576-023-00580-2CrossRefPubMed

77.

Varrin-Doyer M, Spencer CM, Schulze-Topphoff U, Nelson PA, Stroud RM, Cree BA et al (2012) Aquaporin 4-specific T cells in neuromyelitis optica exhibit a Th17 bias and recognize Clostridium ABC transporter. Ann Neurol 72:53–64. https://doi.org/10.1002/ana.23651CrossRefPubMedPubMedCentral

78.

Vincent T, Saikali P, Cayrol R, Roth AD, Bar-Or A, Prat A et al (2008) Functional consequences of neuromyelitis optica-IgG astrocyte interactions on blood-brain barrier permeability and granulocyte recruitment. J Immunol 181:5730–5737. https://doi.org/10.4049/jimmunol.181.8.5730CrossRefPubMed

79.

Vincenti I, Page N, Steinbach K, Yermanos A, Lemeille S, Nunez N et al (2022) Tissue-resident memory CD8(+) T cells cooperate with CD4(+) T cells to drive compartmentalized immunopathology in the CNS. Science translational medicine 14:6058. https://doi.org/10.1126/scitranslmed.abl6058CrossRef

80.

Wang H, Wang K, Wang C, Xu F, Zhong X, Qiu W et al (2013) Cerebrospinal fluid high-mobility group box protein 1 in neuromyelitis optica and multiple sclerosis. NeuroImmunoModulation 20:113–118. https://doi.org/10.1159/000345994CrossRefPubMed

81.

Wang HH, Dai YQ, Qiu W, Lu ZQ, Peng FH, Wang YG et al (2011) Interleukin-17-secreting T cells in neuromyelitis optica and multiple sclerosis during relapse. J Clin Neurosci 18:1313–1317. https://doi.org/10.1016/j.jocn.2011.01.031CrossRefPubMed

82.

Wang KC, Tsai CP, Lee CL, Chen SY, Chin LT, Chen SJ (2012) Elevated plasma high-mobility group box 1 protein is a potential marker for neuromyelitis optica. Neuroscience 226:510–516. https://doi.org/10.1016/j.neuroscience.2012.08.041CrossRefPubMed

83.

Warnatsch A, Ioannou M, Wang Q, Papayannopoulos V (2015) Inflammation. Neutrophil extracellular traps license macrophages for cytokine production in atherosclerosis. Science 349:316–320. https://doi.org/10.1126/science.aaa8064CrossRefPubMedPubMedCentral

84.

Wingerchuk DM, Banwell B, Bennett JL, Cabre P, Carroll W, Chitnis T et al (2015) International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology 85:177–189. https://doi.org/10.1212/WNL.0000000000001729CrossRefPubMedPubMedCentral

85.

Wingerchuk DM, Lennon VA, Pittock SJ, Lucchinetti CF, Weinshenker BG (2006) Revised diagnostic criteria for neuromyelitis optica. Neurology 66:1485–1489. https://doi.org/10.1212/01.wnl.0000216139.44259.74CrossRefPubMed

86.

Winkler A, Wrzos C, Haberl M, Weil MT, Gao M, Mobius W et al (2021) Blood-brain barrier resealing in neuromyelitis optica occurs independently of astrocyte regeneration. J Clin Investig. https://doi.org/10.1172/JCI141694CrossRefPubMedPubMedCentral

87.

Yamamura T, Kleiter I, Fujihara K, Palace J, Greenberg B, Zakrzewska-Pniewska B et al (2019) Trial of Satralizumab in Neuromyelitis Optica Spectrum Disorder. N Engl J Med 381:2114–2124. https://doi.org/10.1056/NEJMoa1901747CrossRefPubMed

88.

Yanagawa K, Kawachi I, Toyoshima Y, Yokoseki A, Arakawa M, Hasegawa A et al (2009) Pathologic and immunologic profiles of a limited form of neuromyelitis optica with myelitis. Neurology 73:1628–1637. https://doi.org/10.1212/WNL.0b013e3181c1deb9CrossRefPubMed

89.

Yipp BG, Petri B, Salina D, Jenne CN, Scott BN, Zbytnuik LD et al (2012) Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med 18:1386–1393. https://doi.org/10.1038/nm.2847CrossRefPubMedPubMedCentral

90.

Yokoseki A, Saji E, Arakawa M, Kosaka T, Hokari M, Toyoshima Y et al (2014) Hypertrophic pachymeningitis: significance of myeloperoxidase anti-neutrophil cytoplasmic antibody. Brain 137:520–536. https://doi.org/10.1093/brain/awt314CrossRefPubMed

91.

Zrzavy T, Hametner S, Wimmer I, Butovsky O, Weiner HL, Lassmann H (2017) Loss of “homeostatic” microglia and patterns of their activation in active multiple sclerosis. Brain 140:1900–1913. https://doi.org/10.1093/brain/awx113CrossRefPubMedPubMedCentral

92.

Zrzavy T, Machado-Santos J, Christine S, Baumgartner C, Weiner HL, Butovsky O et al (2018) Dominant role of microglial and macrophage innate immune responses in human ischemic infarcts. Brain Pathol 28:791–805. https://doi.org/10.1111/bpa.12583CrossRefPubMed

Titel: Stage-dependent immunity orchestrates AQP4 antibody-guided NMOSD pathology: a role for netting neutrophils with resident memory T cells in situ
verfasst von: Akihiro Nakajima
Fumihiro Yanagimura
Etsuji Saji
Hiroshi Shimizu
Yasuko Toyoshima
Kaori Yanagawa
Musashi Arakawa
Mariko Hokari
Akiko Yokoseki
Takahiro Wakasugi
Kouichirou Okamoto
Hirohide Takebayashi
Chihiro Fujii
Kyoko Itoh
Yo-ichi Takei
Shinji Ohara
Mitsunori Yamada
Hitoshi Takahashi
Masatoyo Nishizawa
Hironaka Igarashi
Akiyoshi Kakita
Osamu Onodera
Izumi Kawachi
Publikationsdatum: 01.06.2024
Verlag: Springer Berlin Heidelberg
Erschienen in: Acta Neuropathologica / Ausgabe 1/2024
Print ISSN: 0001-6322
Elektronische ISSN: 1432-0533
DOI: https://doi.org/10.1007/s00401-024-02725-x

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

Darf man die Behandlung eines Neonazis ablehnen?

08.05.2024 Gesellschaft Nachrichten

In einer Leseranfrage in der Zeitschrift Journal of the American Academy of Dermatology möchte ein anonymer Dermatologe bzw. eine anonyme Dermatologin wissen, ob er oder sie einen Patienten behandeln muss, der eine rassistische Tätowierung trägt.

Wartezeit nicht kürzer, aber Arbeit flexibler

Psychotherapie Medizin aktuell

Fünf Jahren nach der Neugestaltung der Psychotherapie-Richtlinie wurden jetzt die Effekte der vorgenommenen Änderungen ausgewertet. Das Hauptziel der Novellierung war eine kürzere Wartezeit auf Therapieplätze. Dieses Ziel wurde nicht erreicht, es gab jedoch positive Auswirkungen auf andere Bereiche.

„Restriktion auf vier Wochen Therapie bei Schlaflosigkeit ist absurd!“

06.05.2024 Insomnie Nachrichten

Chronische Insomnie als eigenständiges Krankheitsbild ernst nehmen und adäquat nach dem aktuellen Forschungsstand behandeln: Das forderte der Schlafmediziner Dr. Dieter Kunz von der Berliner Charité beim Praxis Update.

Stuhltransfusion könnte Fortschreiten von Parkinson-Symptomen bremsen

03.05.2024 Parkinson-Krankheit Nachrichten

Kann eine frühzeitige Stuhltransplantation das Fortschreiten von Parkinson-Symptomen verlangsamen? Die Ergebnisse einer randomisierten Phase-2-Studie scheinen dafür zu sprechen.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Klimawandel und Gesundheit: Was Sie in der Hausarztpraxis wissen müssen und tun können

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 1/2024

Characterization of NEB pathogenic variants in patients reveals novel nemaline myopathy disease mechanisms and omecamtiv mecarbil force effects

Physiological aging and inflammation-induced cellular senescence may contribute to oligodendroglial dysfunction in MS

A familial missense variant in the Alzheimer’s disease gene SORL1 impairs its maturation and endosomal sorting

RNA aptamer reveals nuclear TDP-43 pathology is an early aggregation event that coincides with STMN-2 cryptic splicing and precedes clinical manifestation in ALS

CSF p-tau205: a biomarker of tau pathology in Alzheimer’s disease