Allogeneic B cell immunomodulatory therapy in amyotrophic lateral sclerosis.
ALS
B cells
SOD1
immune modulation
neuroprotection
regulatory
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
15 Jul 2024
15 Jul 2024
Historique:
revised:
04
06
2024
received:
26
12
2023
accepted:
24
06
2024
medline:
5
7
2024
pubmed:
5
7
2024
entrez:
5
7
2024
Statut:
ppublish
Résumé
Amyotrophic lateral sclerosis (ALS) is an orphan neurodegenerative disease. Immune system dysregulation plays an essential role in ALS onset and progression. Our preclinical studies have shown that the administration of exogenous allogeneic B cells improves outcomes in murine models of skin and brain injury through a process termed pligodraxis, in which B cells adopt an immunoregulatory and neuroprotective phenotype in an injured environment. Here, we investigated the effects of B-cell therapy in the SOD1
Identifiants
pubmed: 38967302
doi: 10.1096/fj.202302659R
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e23796Subventions
Organisme : Ward Family Foundation
Organisme : Vaccine and Immunotherapy Center Innovation Fund
Organisme : Vaccine and Immunotherapy Center Education Fund
Organisme : Sean M. Healey and AMG Center for ALS
Informations de copyright
© 2024 Federation of American Societies for Experimental Biology.
Références
Brown RH, Al‐Chalabi A. Amyotrophic lateral sclerosis. N Engl J Med. 2017;377:162‐172.
Hardiman O, al‐Chalabi A, Chio A, et al. Amyotrophic lateral sclerosis. Nat Rev Dis Primers. 2017;3:17071.
Alexianu ME, Kozovska M, Appel SH. Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology. 2001;57:1282‐1289.
Beers DR, Appel SH. Immune dysregulation in amyotrophic lateral sclerosis: mechanisms and emerging therapies. Lancet Neurol. 2019;18:211‐220.
Rothstein JD, Van Kammen M, Levey AI, Martin LJ, Kuncl RW. Selective loss of glial glutamate transporter GLT‐1 in amyotrophic lateral sclerosis. Ann Neurol. 1995;38:73‐84.
Trotti D, Rolfs A, Danbolt NC, Brown RH Jr, Hediger MA. SOD1 mutants linked to amyotrophic lateral sclerosis selectively inactivate a glial glutamate transporter. Nat Neurosci. 1999;2:427‐433.
Engelhardt JI, Tajti J, Appel SH. Lymphocytic infiltrates in the spinal cord in amyotrophic lateral sclerosis. Arch Neurol. 1993;50:30‐36.
Zhao W, Beers DR, Hooten KG, et al. Characterization of gene expression phenotype in amyotrophic lateral sclerosis monocytes. JAMA Neurol. 2017;74:677‐685.
Gustafson MP, Staff NP, Bornschlegl S, et al. Comprehensive immune profiling reveals substantial immune system alterations in a subset of patients with amyotrophic lateral sclerosis. PLoS ONE. 2017;12:e0182002.
Henkel JS, Beers DR, Wen S, et al. Regulatory T‐lymphocytes mediate amyotrophic lateral sclerosis progression and survival. EMBO Mol Med. 2013;5:64‐79.
Garofalo S, Cocozza G, Porzia A, et al. Natural killer cells modulate motor neuron‐immune cell cross talk in models of Amyotrophic Lateral Sclerosis. Nat Commun. 2020;11:1773.
Butovsky O, Siddiqui S, Gabriely G, et al. Modulating inflammatory monocytes with a unique microRNA gene signature ameliorates murine ALS. J Clin Invest. 2012;122:3063‐3087.
Chiot A, Zaïdi S, Iltis C, et al. Modifying macrophages at the periphery has the capacity to change microglial reactivity and to extend ALS survival. Nat Neurosci. 2020;23:1339‐1351.
Coque E, Salsac C, Espinosa‐Carrasco G, et al. Cytotoxic CD8(+) T lymphocytes expressing ALS‐causing SOD1 mutant selectively trigger death of spinal motoneurons. Proc Natl Acad Sci USA. 2019;116:2312‐2317.
Jin M, Gunther R, Akgun K, Hermann A, Ziemssen T. Peripheral proinflammatory Th1/Th17 immune cell shift is linked to disease severity in amyotrophic lateral sclerosis. Sci Rep. 2020;10:5941.
Thonhoff JR, Beers DR, Zhao W, et al. Expanded autologous regulatory T‐lymphocyte infusions in ALS: a phase I, first‐in‐human study. Neurol Neuroimmunol Neuroinflamm. 2018;5:e465.
Beers DR, Zhao W, Wang J, et al. ALS patients' regulatory T lymphocytes are dysfunctional, and correlate with disease progression rate and severity. JCI Insight. 2017;2:e89530.
Giovannelli I, Heath P, Shaw PJ, Kirby J. The involvement of regulatory T cells in amyotrophic lateral sclerosis and their therapeutic potential. Amyotroph Lateral Scler Frontotemporal Degener. 2020;21:435‐444.
Sîrbulescu RF, Mamidi A, Chan SYC, et al. B cells support the repair of injured tissues by adopting MyD88‐dependent regulatory functions and phenotype. FASEB J. 2021;35:e22019.
Dwyer LJ, Maheshwari S, Levy E, Poznansky MC, Whalen MJ, Sîrbulescu RF. B cell treatment promotes a neuroprotective microenvironment after traumatic brain injury through reciprocal immunomodulation with infiltrating peripheral myeloid cells. J Neuroinflammation. 2023;20:133.
Mauri C, Menon M. Human regulatory B cells in health and disease: therapeutic potential. J Clin Invest. 2017;127:772‐779.
Goodchild TT, Robinson KA, Pang W, et al. Bone marrow‐derived B cells preserve ventricular function after acute myocardial infarction. JACC Cardiovasc Interv. 2009;2:1005‐1016.
Sîrbulescu RF, Boehm CK, Soon E, et al. Mature B cells accelerate wound healing after acute and chronic diabetic skin lesions. Wound Repair Regen. 2017;25:774‐791.
Sîrbulescu RF, Chung JY, Edmiston WJ III, Poznansky SA, Poznansky MC, Whalen MJ. Intraparenchymal application of mature B lymphocytes improves structural and functional outcome after contusion traumatic brain injury. J Neurotrauma. 2019;36:2579‐2589.
Hatzipetros T, Kidd JD, Moreno AJ, Thompson K, Gill A, Vieira FG. A quick phenotypic neurological scoring system for evaluating disease progression in the SOD1‐G93A mouse model of ALS. J Vis Exp. 2015;104:53257.
Turner BJ, Alfazema N, Sheean RK, et al. Overexpression of survival motor neuron improves neuromuscular function and motor neuron survival in mutant SOD1 mice. Neurobiol Aging. 2014;35:906‐915.
Cedarbaum JM, Stambler N, Malta E, et al. The ALSFRS‐R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci. 1999;169:13‐21.
Morbach H, Eichhorn EM, Liese JG, Girschick HJ. Reference values for B cell subpopulations from infancy to adulthood. Clin Exp Immunol. 2010;162:271‐279.
Winkler J, Tittlbach H, Schneider A, et al. Adoptive transfer of donor B lymphocytes: a phase 1/2a study for patients after allogeneic stem cell transplantation. Blood Adv. 2024;8:2373‐2383.
Lu CH, Macdonald‐Wallis C, Gray E, et al. Neurofilament light chain: a prognostic biomarker in amyotrophic lateral sclerosis. Neurology. 2015;84:2247‐2257.
Zhou YN, Chen YH, Dong SQ, et al. Role of blood neurofilaments in the prognosis of amyotrophic lateral sclerosis: a meta‐analysis. Front Neurol. 2021;12:712245.
Thonhoff JR, Berry JD, Macklin EA, et al. Combined regulatory T‐lymphocyte and IL‐2 treatment is safe, tolerable, and biologically active for 1 year in persons with amyotrophic lateral sclerosis. Neurol Neuroimmunol Neuroinflamm. 2022;9.
Gugliandolo A, Bramanti P, Mazzon E. Mesenchymal stem cells: a potential therapeutic approach for amyotrophic lateral sclerosis? Stem Cells Int. 2019;2019:3675627.
Magota H, Sasaki M, Kataoka‐Sasaki Y, et al. Repeated infusion of mesenchymal stem cells maintain the condition to inhibit deteriorated motor function, leading to an extended lifespan in the SOD1G93A rat model of amyotrophic lateral sclerosis. Mol Brain. 2021;14:76.
Ortega SB, Torres VO, Latchney SE, et al. B cells migrate into remote brain areas and support neurogenesis and functional recovery after focal stroke in mice. Proc Natl Acad Sci USA. 2020;117:4983‐4993.