The neurotropic schistosome vs experimental autoimmune encephalomyelitis: are there any winners?
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
Cooperatio Biology
Univerzita Karlova v Praze
PROGRES Q43
Univerzita Karlova v Praze
SVV 260432/2018
Univerzita Karlova v Praze
SVV 260563/2020
Univerzita Karlova v Praze
UNCE/SCI/012-204072/2018
Univerzita Karlova v Praze
UNCE24/SCI/011
Univerzita Karlova v Praze
CZ.02.1.01/0.0/0.0/16_019/ 0000759: Centre for Res
Ministerstvo Školství, Mládeže a Tělovýchovy
18-11140S
Grantová Agentura České Republiky
580120
Grantová Agentura, Univerzita Karlova
PubMed
38443998
PubMed Central
PMC11044066
DOI
10.1017/s0031182024000210
PII: S0031182024000210
Knihovny.cz E-zdroje
- Klíčová slova
- EAE, IFN-γ, Trichobilharzia regenti, demyelination, eosinophilia, experimental autoimmune encephalomyelitis, neurotropic parasite, neurotropic schistosome,
- MeSH
- encefalomyelitida autoimunitní experimentální * imunologie patologie MeSH
- eozinofily imunologie MeSH
- interferon gama * metabolismus MeSH
- myši inbrední C57BL * MeSH
- myši MeSH
- roztroušená skleróza imunologie patologie MeSH
- Schistosomatidae fyziologie MeSH
- slezina patologie parazitologie imunologie MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- interferon gama * MeSH
The incidences of multiple sclerosis have risen worldwide, yet neither the trigger nor efficient treatment is known. Some research is dedicated to looking for treatment by parasites, mainly by helminths. However, little is known about the effect of helminths that infect the nervous system. Therefore, we chose the neurotropic avian schistosome Trichobilharzia regenti, which strongly promotes M2 polarization and tissue repair in the central nervous system, and we tested its effect on the course of experimental autoimmune encephalomyelitis (EAE) in mice. Surprisingly, the symptoms of EAE tended to worsen after the infection with T. regenti. The infection did not stimulate tissue repair, as indicated by the similar level of demyelination. Eosinophils heavily infiltrated the infected tissue, and the microglia number increased as well. Furthermore, splenocytes from T. regenti-infected EAE mice produced more interferon (IFN)-γ than splenocytes from EAE mice after stimulation with myelin oligodendrocyte glycoprotein. Our research indicates that the combination of increased eosinophil numbers and production of IFN-γ tends to worsen the EAE symptoms. Moreover, the data highlight the importance of considering the direct effect of the parasite on the tissue, as the migrating parasite may further tissue damage and make tissue repair even more difficult.
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Arellano G, Ottum PA, Reyes LI, Burgos PI and Naves R (2015) Stage-specific role of interferon-γ in experimental autoimmune encephalomyelitis and multiple sclerosis. Frontiers in Immunology 6, 1–9. PubMed PMC
Attfield KE, Jensen LT, Kaufmann M, Friese MA and Fugger L (2022) The immunology of multiple sclerosis. Nature Reviews Immunology 22, 734–750. PubMed
Charabati M, Donkers SJ, Kirkland MC and Osborne LC (2020) A critical analysis of helminth immunotherapy in multiple sclerosis. Multiple Sclerosis Journal 26, 1448–1458. PubMed
Che J, Li D, Hong W, Wang L, Guo Y, Wu M, Lu J, Tong L, Weng Q, Wang J and Dong X (2022) Discovery of new macrophage M2 polarization modulators as multiple sclerosis treatment agents that enable the inflammation microenvironment remodeling. European Journal of Medicinal Chemistry 243, 1–19. PubMed
Chu F, Shi M, Lang Y, Chao Z, Jin T, Cui L and Zhu J (2021) Adoptive transfer of immunomodulatory M2 macrophages suppresses experimental autoimmune encephalomyelitis in C57BL/6 mice via blockading NF-κB pathway. Clinical and Experimental Immunology 204, 199–211. PubMed PMC
Dendrou CA, Fugger L and Friese MA (2015) Immunopathology of multiple sclerosis. Nature Reviews Immunology 15, 545–558. PubMed
Dixit A, Tanaka A, Greer JM and Donnelly S (2017) Novel therapeutics for multiple sclerosis designed by parasitic worms. International Journal of Molecular Sciences 18, 1–17. PubMed PMC
Dolitzky A, Shapira G, Grisaru-Tal S, Hazut I, Avlas S, Gordon Y, Itan M, Shomron N and Munitz A (2021) Transcriptional profiling of mouse eosinophils identifies distinct gene signatures following cellular activation. Frontiers in Immunology 12, 1–15. PubMed PMC
Dolitzky A, Hazut I, Avlas S, Grisaru-Tal S, Itan M, Zaffran I, Levi-Schaffer F, Gerlic M and Munitz A (2022) Differential regulation of type 1 and type 2 mouse eosinophil activation by apoptotic cells. Frontiers in Immunology 13, 1–16. PubMed PMC
Finlay CM, Stefanska AM, Walsh KP, Kelly PJ, Boon L, Lavelle EC, Walsh PT and Mills KHG (2016) Helminth products protect against autoimmunity via innate type 2 cytokines IL-5 and IL-33, which promote eosinophilia. The Journal of Immunology 196, 703–714. PubMed
Furlan R, Brambilla E, Ruffini F, Poliani PL, Bergami A, Marconi PC, Franciotta DM, Penna G, Comi G, Adorini L and Martino G (2001) Intrathecal delivery of IFN-γ protects C57BL/6 mice from chronic-progressive experimental autoimmune encephalomyelitis by increasing apoptosis of central nervous system-infiltrating lymphocytes. Journal of Immunology 167, 1821–1829. PubMed
Ham DW, Kim SG, Seo SH, Shin JH, Lee SH and Shin EH (2021) Chronic Toxoplasma gondii infection alleviates experimental autoimmune encephalomyelitis by the immune regulation inducing reduction in IL-17A/Th17 via upregulation of SOCS3. Neurotherapeutics: The Journal of the American Society for Experimental NeuroTherapeutics 18, 430–447. PubMed PMC
Hauser SL and Cree BAC (2020) Treatment of multiple sclerosis: a review. The American Journal of Medicine 133, 1380–1390.e2. PubMed PMC
Hayes KS and Grencis RK (2021) Trichuris muris and comorbidities – within a mouse model context. Parasitology 148, 1774–1782. PubMed PMC
Hooke Laboratories (n.d.) Mouse EAE Scoring. Retrieved from Hooke Laboratories website: https://hookelabs.com/services/cro/eae/MouseEAEscoring.html (accessed 2 February 2024).
Horák P, Dvořák J, Kolářová L and Trefil L (1999) Trichobilharzia regenti, a pathogen of the avian and mammalian central nervous systems. Parasitology 119, 577–581. PubMed
Leontovyč R, Young ND, Korhonen PK, Hall RS, Tan P, Mikeš L, Kašný M, Horák P and Gasser RB (2016) Comparative transcriptomic exploration reveals unique molecular adaptations of neuropathogenic Trichobilharzia to invade and parasitize its avian definitive host. PLoS Neglected Tropical Diseases 10, 1–24. PubMed PMC
Lucarini V, Ziccheddu G, Macchia I, La Sorsa V, Peschiaroli F, Buccione C, Sistigu A, Sanchez M, Andreone S, D'Urso MT, Spada M, Macchia D, Afferni C, Mattei F and Schiavoni G (2017) IL-33 restricts tumor growth and inhibits pulmonary metastasis in melanoma-bearing mice through eosinophils. OncoImmunology 6, e1317420. PubMed PMC
Lund ME, Greer J, Dixit A, Alvarado R, McCauley-Winter P, To J, Tanaka A, Hutchinson AT, Robinson MW, Simpson AM, O’Brien BA, Dalton JP and Donnelly S (2016) A parasite-derived 68-mer peptide ameliorates autoimmune disease in murine models of Type 1 diabetes and multiple sclerosis. Scientific Reports 6, 1–11. PubMed PMC
Macháček T, Šmídová B, Pankrác J, Majer M, Bulantová J and Horák P (2020) Nitric oxide debilitates the neuropathogenic schistosome Trichobilharzia regenti in mice, partly by inhibiting its vital peptidases. Parasites & Vectors 13, 1–14. PubMed PMC
Macháček T, Leontovyč R, Šmídová B, Majer M, Vondráček O, Vojtěchová I, Petrásek T and Horák P (2022) Mechanisms of the host immune response and helminth-induced pathology during Trichobilharzia regenti (Schistosomatidae) neuroinvasion in mice. PLoS Pathogens 18, 1–34. PubMed PMC
Maizels RM (2013) Toxocara canis: molecular basis of immune recognition and evasion. Veterinary Parasitology 193, 365–374. PubMed PMC
Maizels RM, Smits HH and McSorley HJ (2018) Modulation of host immunity by helminths: the expanding repertoire of parasite effector molecules. Immunity 49, 801–818. PubMed PMC
Majer M, Macháček T, Súkeníková L, Hrdý J and Horák P (2020) The peripheral immune response of mice infected with a neuropathogenic schistosome. Parasite Immunology 42, 1–11. PubMed
Miron VE, Boyd A, Zhao J-W, Yuen TJ, Ruckh JM, Shadrach JL, van Wijngaarden P, Wagers AJ, Williams A and Franklin RJM and ffrench-Constant C. (2013) M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nature Neuroscience 16, 1211–1218. PubMed PMC
Novák J, Macháček T, Majer M, Kostelanská M, Skulinová K, Černý V, Kolářová L, Hrdý J and Horák P (2022) Toxocara canis infection worsens the course of experimental autoimmune encephalomyelitis in mice. Parasitology 149, 1720–1728. PubMed PMC
Reyes J, Espinoza-Jiménez A, González M, Verdin L and Terrazas LI (2011) Taenia crassiceps infection abrogates experimental autoimmune encephalomyelitis. Cellular Immunology 267, 77–87. PubMed
Sakkal S, Miller S, Apostolopoulos V and Nurgali K (2016) Eosinophils in cancer: favourable or unfavourable? Current Medicinal Chemistry 23, 650–666. PubMed
Tanasescu R, Tench CR, Constantinescu CS, Telford G, Singh S, Frakich N, Onion D, Auer DP, Gran B, Evangelou N, Falah Y, Ranshaw C, Cantacessi C, Jenkins TP and Pritchard DI (2020) Hookworm treatment for relapsing multiple sclerosis: a randomized double-blinded placebo-controlled trial. JAMA Neurology 77, 1089–1098. PubMed PMC
Tichauer JE, Arellano G, Acuña E, González LF, Kannaiyan NR, Murgas P, Panadero-Medianero C, Ibañez-Vega J, Burgos PI, Loda E, Miller SD, Rossner MJ, Gebicke-Haerter PJ and Naves R (2023) Interferon-gamma ameliorates experimental autoimmune encephalomyelitis by inducing homeostatic adaptation of microglia. Frontiers in Immunology 14, 1–22. PubMed PMC
Tintore M, Vidal-Jordana A and Sastre-Garriga J (2019) Treatment of multiple sclerosis – success from bench to bedside. Nature Reviews Neurology 15, 53–58. PubMed
Tran GT, Wilcox PL, Dent LA, Robinson CM, Carter N, Verma ND, Hall BM and Hodgkinson SJ (2017) Interleukin-5 mediates parasite-induced protection against experimental autoimmune encephalomyelitis: association with induction of antigen-specific CD4+CD25+ T regulatory cells. Frontiers in Immunology 8, 1–13. PubMed PMC
Walton C, King R, Rechtman L, Kaye W, Leray E, Marrie RA, Robertson N, La Rocca N, Uitdehaag B, Van der Mei I, Wallin M, Helme A, Angood Napier C, Rijke N and Baneke P (2020) Rising prevalence of multiple sclerosis worldwide: insights from the Atlas of MS, third edition. Multiple Sclerosis Journal 26, 1816–1821. PubMed PMC
Weng Q, Wang J, Wang J, Wang J, Sattar F, Zhang Z, Zheng J, Xu Z, Zhao M, Liu X, Yang L, Hao G, Fang L, Lu QR, Yang B and He Q (2018) Lenalidomide regulates CNS autoimmunity by promoting M2 macrophages polarization. Cell Death & Disease 9, 1–13. PubMed PMC
Wiendl H, Gold R, Berger T, Derfuss T, Linker R, Mäurer M, Aktas O, Baum K, Berghoff M, Bittner S, Chan A, Czaplinski A, Deisenhammer F, Di Pauli F, Du Pasquier R, Enzinger C, Fertl E, Gass A, Gehring K, Gobbi C, Goebels N, Guger M, Haghikia A, Hartung HP, Heidenreich F, Hoffmann O, Kallmann B, Kleinschnitz C, Klotz L, Leussink VI, Leutmezer F, Limmroth V, Lünemann JD, Lutterotti A, Meuth SG, Meyding-Lamadé U, Platten M, Rieckmann P, Schmidt S, Tumani H, Weber F, Weber MS, Zettl UK, Ziemssen T and Zipp F (2021) Multiple Sclerosis Therapy Consensus Group (MSTCG): position statement on disease-modifying therapies for multiple sclerosis (white paper). Therapeutic Advances in Neurological Disorders 14, 1–39. PubMed PMC