CXCL13/CXCR5 signalling is pivotal to preserve motor neurons in amyotrophic lateral sclerosis

EBioMedicine - Tập 62 - Trang 103097 - 2020
Maria Chiara Trolese1, Alessandro Mariani2, Mineko Terao3, Massimiliano de Paola2, Paola Fabbrizio1, Francesca Sironi1, Mami Kurosaki3, Silvia Bonanno4, Stefania Marcuzzo4, Pia Bernasconi4, Francesca Trojsi5, Eleonora Aronica6, Caterina Bendotti1, Giovanni Nardo1
1Laboratory of Molecular Neurobiology, Department of Neuroscience, Istituto di Ricerche Farmacologiche Mario Negri IRCCS, Via Mario Negri 2, Milan 20156, Italy
2Laboratory of Biology of Neurodegenerative Disorders, Department of Neuroscience, Istituto di Ricerche Farmacologiche Mario Negri IRCCS, Via Mario Negri 2, Milan 20156, Italy
3Laboratory of Molecular Biology, Department of Biochemistry and Molecular Pharmacology, Istituto di Ricerche Farmacologiche IRCCS, Via Mario Negri 2, Milan 20156, Italy
4Neurology IV-Neuroimmunology and Neuromuscular Diseases Unit, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Celoria 11, Milan 20133, Italy
5Department of Advanced Medical and Surgical Sciences, University of Campania "Luigi Vanvitelli”, P.zza Miraglia 2, Naples 80138, Italy
6Department of Pathology, Academic Medic\\\al Centre, University of Amsterdam, Meibergdreef 9, Amsterdam 1105 AZ, Netherlands

Tài liệu tham khảo

Hardiman, 2017, Amyotrophic lateral sclerosis, Nat Rev Dis Prim [Internet], 3, 17071, 10.1038/nrdp.2017.71 Hardiman, 2011, Clinical diagnosis and management of amyotrophic lateral sclerosis, Nat Rev Neurol [Internet], 7, 639, 10.1038/nrneurol.2011.153 Beghi, 2011, The epidemiology and treatment of ALS: focus on the heterogeneity of the disease and critical appraisal of therapeutic trials, Amyotroph Later Scler [Internet], 12, 1, 10.3109/17482968.2010.502940 Turner, 2013, Mechanisms, models and biomarkers in amyotrophic lateral sclerosis, Amyotroph Later Scler Front Degener [Internet], 14, 19, 10.3109/21678421.2013.778554 Boillée, 2006, ALS: a disease of motor neurons and their nonneuronal neighbors, Neuron [Internet], 52, 39, 10.1016/j.neuron.2006.09.018 Yamanaka, 2008, Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis, Nat Neurosci [Internet], 11, 251, 10.1038/nn2047 Thonhoff, 2018, Neuroinflammatory mechanisms in amyotrophic lateral sclerosis pathogenesis, Curr Opin Neurol [Internet], 31, 635, 10.1097/WCO.0000000000000599 Beers, 2008, CD4+ T cells support glial neuroprotection, slow disease progression, and modify glial morphology in an animal model of inherited ALS, Proc Natl Acad Sci U S A [Internet], 105, 15558, 10.1073/pnas.0807419105 Chiu, 2008, T lymphocytes potentiate endogenous neuroprotective inflammation in a mouse model of ALS, Proc Natl Acad Sci U S A [Internet], 105, 17913, 10.1073/pnas.0804610105 Boulanger, 2009, Immune proteins in brain development and synaptic plasticity, Neuron [Internet], 64, 93, 10.1016/j.neuron.2009.09.001 Nardo, 2016, Major histocompatibility complex I expression by motor neurons and its implication in amyotrophic lateral sclerosis, Front Neurol [Internet], 7 Kwon, 2015, CCL2 mediates neuron-macrophage interactions to drive proregenerative macrophage activation following preconditioning injury, J Neurosci [Internet], 35, 15934, 10.1523/JNEUROSCI.1924-15.2015 Charo, 2006, The many roles of chemokines and chemokine receptors in inflammation, N Engl J Med [Internet], 354, 610, 10.1056/NEJMra052723 de Haas, 2007, Neuronal chemokines: versatile messengers in central nervous system cell interaction, Mol Neurobiol [Internet], 36, 137, 10.1007/s12035-007-0036-8 Savarin-Vuaillat, 2007, Chemokines and chemokine receptors in neurological disease: raise, retain, or reduce?, Neurotherapeutics [Internet], 4, 590, 10.1016/j.nurt.2007.07.004 Kuhle, 2009, Increased levels of inflammatory chemokines in amyotrophic lateral sclerosis, Eur J Neurol [Internet], 16, 771, 10.1111/j.1468-1331.2009.02560.x Endo, 2016, Neuroinflammation in motor neuron disease, Clin Exp Neuroimmunol [Internet], 7, 126, 10.1111/cen3.12309 de Oliveira, 2013, Early gene expression changes in spinal cord from SOD1G93A amyotrophic lateral sclerosis animal model, Front Cell Neurosci [Internet], 7 Zhang, 2018, Dynamic changes of CX3CL1/CX3CR1 axis during microglial activation and motor neuron loss in the spinal cord of ALS mouse model, Transl Neurodegener [Internet], 7, 35, 10.1186/s40035-018-0138-4 Ansel, 2000, A chemokine-driven positive feedback loop organizes lymphoid follicles, Nature [Internet], 406, 309, 10.1038/35018581 Förster, 1996, A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen, Cell [Internet], 87, 1037, 10.1016/S0092-8674(00)81798-5 Bagaeva, 2006, CXC chemokine ligand 13 plays a role in experimental autoimmune encephalomyelitis, J Immunol [Internet], 176, 7676, 10.4049/jimmunol.176.12.7676 Magliozzi, 2004, Intracerebral expression of CXCL13 and BAFF is accompanied by formation of lymphoid follicle-like structures in the meninges of mice with relapsing experimental autoimmune encephalomyelitis, J Neuroimmunol [Internet], 148, 11, 10.1016/j.jneuroim.2003.10.056 Smith, 2003, Expression of B-cell-attracting chemokine 1 (CXCL13) by malignant lymphocytes and vascular endothelium in primary central nervous system lymphoma, Blood [Internet], 101, 815, 10.1182/blood-2002-05-1576 Irani, 2016, Regulated production of CXCL13 within the central nervous system, J Clin Cell Immunol [Internet], 7 Krumbholz, 2006, Chemokines in multiple sclerosis: CXCL12 and CXCL13 up-regulation is differentially linked to CNS immune cell recruitment, Brain [Internet], 129, 200, 10.1093/brain/awh680 Sellebjerg, 2009, Increased cerebrospinal fluid concentrations of the chemokine CXCL13 in active MS, Neurology [Internet], 73, 2003, 10.1212/WNL.0b013e3181c5b457 Fischer, 2009, CXCL13 and CXCL12 in central nervous system lymphoma patients, Clin Cancer Res [Internet], 15, 5968, 10.1158/1078-0432.CCR-09-0108 Jiang, 2016, CXCL13 drives spinal astrocyte activation and neuropathic pain via CXCR5, J Clin Invest [Internet], 126, 745, 10.1172/JCI81950 Esen, 2014, Type-I interferons suppress microglial production of the lymphoid chemokine, CXCL13, Glia [Internet], 62, 1452, 10.1002/glia.22692 Monson, 2014, Repetitive hypoxic preconditioning induces an immunosuppressed B cell phenotype during endogenous protection from stroke, J Neuroinflamm [Internet], 11, 22, 10.1186/1742-2094-11-22 Nardo, 2013, Transcriptomic indices of fast and slow disease progression in two mouse models of amyotrophic lateral sclerosis, Brain [Internet], 136, 3305, 10.1093/brain/awt250 Brooks, 1994, El escorial world federation of neurology criteria for the diagnosis of amyotrophic lateral sclerosis, J Neurol Sci [Internet], 124, 96, 10.1016/0022-510X(94)90191-0 Klimatcheva, 2015, CXCL13 antibody for the treatment of autoimmune disorders, BMC Immunol [Internet], 16, 6, 10.1186/s12865-015-0068-1 Nardo, 2018, Counteracting roles of MHCI and CD8+ T cells in the peripheral and central nervous system of ALS SOD1G93A mice, Mol Neurodegener [Internet], 13, 42, 10.1186/s13024-018-0271-7 De Paola, 2012, Neuroprotective effects of toll-like receptor 4 antagonism in spinal cord cultures and in a mouse model of motor neuron degeneration, Mol Med [Internet], 18, 971, 10.2119/molmed.2012.00020 Ludolph, 2010, Guidelines for preclinical animal research in ALS/MND: a consensus meeting, Amyotroph Later Scler [Internet], 11, 38, 10.3109/17482960903545334 Kilkenny, 2010, Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research, PLoS Biol [Internet], 8 Huang, 2017, Age-related macular degeneration phenotypes are associated with increased tumor necrosis-alpha and subretinal immune cells in aged Cxcr5 knockout mice. Boulton ME, editor, PLoS One [Internet], 12 Banerjee, 2008, Adaptive immune neuroprotection in G93A-SOD1 amyotrophic lateral sclerosis mice. McCabe BD, editor, PLoS One [Internet], 3, e2740, 10.1371/journal.pone.0002740 Noguchi, 2017, Pharmacokinetics of an intracerebroventricularly administered antibody in rats, MAbs [Internet], 9, 1210, 10.1080/19420862.2017.1345834 Hussain, 2019, CXCL13/CXCR5 signaling axis in cancer, Life Sci [Internet], 227, 175, 10.1016/j.lfs.2019.04.053 Waite, 2012, Th17 response and inflammatory autoimmune diseases, Int J Inflam [Internet], 2012, 1 Brettschneider, 2013, Stages of pTDP-43 pathology in amyotrophic lateral sclerosis, Ann Neurol [Internet], 74, 20, 10.1002/ana.23937 Marino, 2015, Differences in protein quality control correlate with phenotype variability in 2 mouse models of familial amyotrophic lateral sclerosis, Neurobiol Aging [Internet], 36, 492, 10.1016/j.neurobiolaging.2014.06.026 Nardo, 2016, New insights on the mechanisms of disease course variability in ALS from mutant SOD1 mouse models, Brain Pathol [Internet], 26, 237, 10.1111/bpa.12351 Ramesh, 2009, Possible role of glial cells in the onset and progression of Lyme neuroborreliosis, J Neuroinflamm [Internet], 6, 23, 10.1186/1742-2094-6-23 Narayan, 2005, The nervous system as ectopic germinal center: CXCL13 and IgG in lyme neuroborreliosis, Ann Neurol [Internet], 57, 813, 10.1002/ana.20486 Peviani, 2014, Specific induction of Akt3 in spinal cord motor neurons is neuroprotective in a mouse model of familial amyotrophic lateral sclerosis, Mol Neurobiol [Internet], 49, 136, 10.1007/s12035-013-8507-6 Vallarola, 2018, RNS60 exerts therapeutic effects in the SOD1 ALS mouse model through protective glia and peripheral nerve rescue, J Neuroinflamm [Internet], 15, 65, 10.1186/s12974-018-1101-0 Kowarik, 2012, CXCL13 is the major determinant for B cell recruitment to the CSF during neuroinflammation, J Neuroinflamm [Internet], 9, 624 Rupprecht, 2009, The chemokine CXCL13 is a key regulator of B cell recruitment to the cerebrospinal fluid in acute Lyme neuroborreliosis, J Neuroinflamm [Internet], 6, 42, 10.1186/1742-2094-6-42 Naor, 2009, Development of ALS-like disease in SOD-1 mice deficient of B lymphocytes, J Neurol [Internet], 256, 1228, 10.1007/s00415-009-5097-3 Rentzos, 2010, Interleukin-17 and interleukin-23 are elevated in serum and cerebrospinal fluid of patients with ALS: a reflection of Th17 cells activation?, Acta Neurol Scand [Internet], 122, 425, 10.1111/j.1600-0404.2010.01333.x Fiala, 2010, IL-17A is increased in the serum and in spinal cord CD8 and mast cells of ALS patients, J Neuroinflammation [Internet], 7, 76, 10.1186/1742-2094-7-76 Boulanger, 2004, Immune signalling in neural development, synaptic plasticity and disease, Nat Rev Neurosci [Internet], 5, 521, 10.1038/nrn1428 Pehar, 2005, Complexity of astrocyte-motor neuron interactions in amyotrophic lateral sclerosis, Neurodegen Dis [Internet], 2, 139, 10.1159/000089619 Song, 2016, Major histocompatibility complex class I molecules protect motor neurons from astrocyte-induced toxicity in amyotrophic lateral sclerosis, Nat Med [Internet], 22, 397, 10.1038/nm.4052 Nardo, 2016, Immune response in peripheral axons delays disease progression in SOD1G93A mice, J Neuroinflamm [Internet], 13, 261, 10.1186/s12974-016-0732-2 Allen, 2004, Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5, Nat Immunol [Internet], 5, 943, 10.1038/ni1100 Lazarini, 2003, Role of the ?-chemokine stromal cell-derived factor (SDF-1) in the developing and mature central nervous system, Glia [Internet], 42, 139, 10.1002/glia.10139 Klein, 2004, Immune and nervous system CXCL12 and CXCR4: parallel roles in patterning and plasticity, Trends Immunol [Internet], 25, 306, 10.1016/j.it.2004.04.002 Stumm, 2002, A dual role for the SDF-1/CXCR4 chemokine receptor system in adult brain: isoform-selective regulation of SDF-1 expression modulates CXCR4-dependent neuronal plasticity and cerebral leukocyte recruitment after focal ischemia, J Neurosci [Internet], 22, 5865, 10.1523/JNEUROSCI.22-14-05865.2002 Negro, 2017, <scp>CXCL</scp>12α/ <scp>SDF</scp>‐1 from perisynaptic Schwann cells promotes regeneration of injured motor axon terminals, EMBO Mol Med [Internet], 9, 1000, 10.15252/emmm.201607257 El Khoury, 2019, Serum-based differentiation between multiple sclerosis and amyotrophic lateral sclerosis by Random Forest classification of FTIR spectra, Analyst [Internet], 144, 4647, 10.1039/C9AN00754G Leypoldt, 2015, Investigations on CXCL13 in Anti - N -methyl- D - aspartate receptor encephalitis, JAMA Neurol [Internet], 72, 180, 10.1001/jamaneurol.2014.2956 Kim, 2019, Serum CXCL13 reflects local B-cell mediated inflammatory demyelinating peripheral neuropathy, Sci Rep [Internet], 9, 16535, 10.1038/s41598-019-52643-2 Alvarez, 2013, CXCL13 is a biomarker of inflammation in multiple sclerosis, neuromyelitis optica, and other neurological conditions, Mult Scler J [Internet], 19, 1204, 10.1177/1352458512473362 Nissen, 2019, Use of cerebrospinal fluid biomarkers in diagnosis and monitoring of rheumatoid meningitis, Front Neurol [Internet], 10