Peripheral immunity relate to disease progression and prognosis in amyotrophic lateral sclerosis

References

• Brown RH, Al-Chalabi A. Amyotrophic lateral sclerosis. N Engl J Med. 2017;377:162–72.
   PubMed Web of Science ®Google Scholar
• Yang T, Wei Q, Li C, Cao B, Ou R, Hou Y, et al. Spatial-temporal pattern of propagation in amyotrophic lateral sclerosis and effect on survival: a cohort study. Eur J Neurol. 2022;29:3177–86.
   PubMed Web of Science ®Google Scholar
• Shefner J, Heiman-Patterson T, Pioro EP, Wiedau-Pazos M, Liu S, Zhang J, et al. Long-term edaravone efficacy in amyotrophic lateral sclerosis: post-hoc analyses of Study 19 (MCI186-19). Muscle Nerve. 2020;61:218–21.
   PubMed Web of Science ®Google Scholar
• Scott A. Drug therapy: on the treatment trail for ALS. Nature 2017;550:S120–S121.
   PubMedGoogle Scholar
• Feldman EL, Goutman SA, Petri S, Mazzini L, Savelieff MG, Shaw PJ, et al. Amyotrophic lateral sclerosis. Lancet. 2022;400:1363–80.
   PubMed Web of Science ®Google Scholar
• Huang J, Li C, Shang H. Astrocytes in neurodegeneration: inspiration from genetics. Front Neurosci. 2022;16:882316.
   PubMed Web of Science ®Google Scholar
• Theoharides TC, Tsilioni I. Amyotrophic lateral sclerosis, neuroinflammation, and cromolyn. Clin Ther. 2020;42:546–9.
   PubMed Web of Science ®Google Scholar
• Masrori P, Beckers J, Gossye H, Van Damme P. The role of inflammation in neurodegeneration: novel insights into the role of the immune system in C9orf72 HRE-mediated ALS/FTD. Mol Neurodegener. 2022;17:22.
   PubMed Web of Science ®Google Scholar
• Dutta K, Thammisetty SS, Boutej H, Bareil C, Julien JP. Mitigation of ALS pathology by neuron-specific inhibition of nuclear factor kappa B signaling. J Neurosci. 2020;40:5137–54.
   PubMed Web of Science ®Google Scholar
• Beers DR, Appel SH. Immune dysregulation in amyotrophic lateral sclerosis: mechanisms and emerging therapies. Lancet Neurol. 2019;18:211–20.
   PubMed Web of Science ®Google Scholar
• Mantovani S, Garbelli S, Pasini A, Alimonti D, Perotti C, Melazzini M, et al. Immune system alterations in sporadic amyotrophic lateral sclerosis patients suggest an ongoing neuroinflammatory process. J Neuroimmunol. 2009;210:73–9.
   PubMed Web of Science ®Google Scholar
• Murdock BJ, Zhou T, Kashlan SR, Little RJ, Goutman SA, Feldman EL. Correlation of peripheral immunity with rapid amyotrophic lateral sclerosis progression. JAMA Neurol. 2017;74:1446–54.
   PubMed Web of Science ®Google Scholar
• Wei QQ, Hou YB, Zhang LY, Ou RW, Cao B, Chen YP, et al. Neutrophil-to-lymphocyte ratio in sporadic amyotrophic lateral sclerosis. Neural Regen Res. 2022;17:875–80.
   PubMed Web of Science ®Google Scholar
• Apostolski S, Nikolić J, Bugarski‐Prokopljević C, Miletić V, Pavlović S, Filipović S. Serum and CSF immunological findings in ALS. Acta Neurol Scand. 1991;83:96–8.
   PubMed Web of Science ®Google Scholar
• Saleh IA, Zesiewicz T, Xie Y, Sullivan KL, Miller AM, Kuzmin-Nichols N, et al. Evaluation of humoral immune response in adaptive immunity in ALS patients during disease progression. J Neuroimmunol. 2009;215:96–101.
   PubMed Web of Science ®Google Scholar
• Chen X, Feng W, Huang R, Guo X, Chen Y, Zheng Z, et al. Evidence for peripheral immune activation in amyotrophic lateral sclerosis. J Neurol Sci. 2014;347:90–5.
   PubMed Web of Science ®Google Scholar
• Rentzos M, Evangelopoulos ME, Sereti E, Zouvelou V, Marmara S, Alexakis T, et al. Humoral immune activation in amyotrophic lateral sclerosis patients. Neurol Int. 2013;5:e3.
   PubMedGoogle Scholar
• Zhang R, Gascon R, Miller RG, Gelinas DF, Mass J, Hadlock K, et al. Evidence for systemic immune system alterations in sporadic amyotrophic lateral sclerosis (sALS). J Neuroimmunol. 2005;159:215–24.
   PubMed Web of Science ®Google Scholar
• Brooks BR, Miller RG, Swash M, Munsat TL, World Federation of Neurology Research Group on Motor Neuron Diseases. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord. 2000;1:293–9.
   PubMed Web of Science ®Google Scholar
• Roche JC, Rojas-Garcia R, Scott KM, Scotton W, Ellis CE, Burman R, et al. A proposed staging system for amyotrophic lateral sclerosis. Brain. 2012;135:847–52.
   PubMed Web of Science ®Google Scholar
• Hamilton M. A rating scale for depression. J Neurol Neurosurg Psychiat. 1960;23:56–62.
   PubMed Web of Science ®Google Scholar
• Hamilton M. The assessment of anxiety states by rating. Br J Med Psychol. 1959;32:50–5.
   PubMed Web of Science ®Google Scholar
• Chiò A, Calvo A, Moglia C, Mazzini L, Mora G, PARALS study group. Phenotypic heterogeneity of amyotrophic lateral sclerosis: a population based study. J Neurol Neurosurg Psychiatry. 2011;82:740–6.
   PubMed Web of Science ®Google Scholar
• Fan KQ, Li YY, Wang HL, Mao XT, Guo JX, Wang F, et al. Stress-induced metabolic disorder in peripheral CD4(+) T cells leads to anxiety-like behavior. Cell 2019;179:864–79.e19.
   PubMed Web of Science ®Google Scholar
• Gustafson MP, Staff NP, Bornschlegl S, Butler GW, Maas ML, Kazamel M, et al. Comprehensive immune profiling reveals substantial immune system alterations in a subset of patients with amyotrophic lateral sclerosis. PLoS One. 2017;12:e0182002.
   PubMed Web of Science ®Google Scholar
• Linton PJ, Dorshkind K. Age-related changes in lymphocyte development and function. Nat Immunol. 2004;5:133–9.
   PubMed Web of Science ®Google Scholar
• Coque E, Salsac C, Espinosa-Carrasco G, Varga B, Degauque N, Cadoux M, et al. Cytotoxic CD8(+) T lymphocytes expressing ALS-causing SOD1 mutant selectively trigger death of spinal motoneurons. Proc Natl Acad Sci USA. 2019;116:2312–7.
   PubMed Web of Science ®Google Scholar
• Nardo G, Trolese MC, Verderio M, Mariani A, de Paola M, Riva N, et al. Counteracting roles of MHCI and CD8(+) T cells in the peripheral and central nervous system of ALS SOD1(G93A) mice. Mol Neurodegener. 2018;13:42.
   PubMed Web of Science ®Google Scholar
• Holmøy T. T cells in amyotrophic lateral sclerosis. Eur J Neurol. 2008;15:360–6.
   PubMed Web of Science ®Google Scholar
• Caza T, Landas S. Functional and phenotypic plasticity of CD4(+) T cell subsets. Biomed Res Int. 2015;2015:521957–13.
   PubMed Web of Science ®Google Scholar
• Chiu IM, Chen A, Zheng Y, Kosaras B, Tsiftsoglou SA, Vartanian TK, et al. T lymphocytes potentiate endogenous neuroprotective inflammation in a mouse model of ALS. Proc Natl Acad Sci USA. 2008;105:17913–8.
   PubMed Web of Science ®Google Scholar
• Henkel JS, Beers DR, Wen S, Rivera AL, Toennis KM, Appel JE, et al. Regulatory T-lymphocytes mediate amyotrophic lateral sclerosis progression and survival. EMBO Mol Med. 2013;5:64–79.
   PubMed Web of Science ®Google Scholar
• Rentzos M, Evangelopoulos E, Sereti E, Zouvelou V, Marmara S, Alexakis T, et al. Alterations of T cell subsets in ALS: a systemic immune activation? Acta Neurol Scand. 2012;125:260–4.
   PubMed Web of Science ®Google Scholar
• Beers DR, Zhao W, Wang J, Zhang X, Wen S, Neal D, et al. ALS patients’ regulatory T lymphocytes are dysfunctional, and correlate with disease progression rate and severity. JCI Insight. 2017;2:e89530.
   PubMed Web of Science ®Google Scholar
• Sheean RK, McKay FC, Cretney E, Bye CR, Perera ND, Tomas D, et al. Association of regulatory T-cell expansion with progression of amyotrophic lateral sclerosis a study of humans and a transgenic mouse model. JAMA Neurol. 2018;75:681–9.
   PubMed Web of Science ®Google Scholar
• Engelhardt JI, Siklós L, Kömüves L, Smith RG, Appel SH. Antibodies to calcium channels from ALS patients passively transferred to mice selectively increase intracellular calcium and induce ultrastructural changes in motoneurons. Synapse. 1995;20:185–99.
   PubMed Web of Science ®Google Scholar
• Kimura F, Smith RG, Delbono O, Nyormoi O, Schneider T, Nastainczyk W, et al. Amyotrophic lateral sclerosis patient antibodies label Ca2+ channel α1 subunit. Ann Neurol. 1994;35:164–71.
   PubMed Web of Science ®Google Scholar
• Crayle J, Elmallah M, Sleasman J, Bedlack R. Total serum immunoglobulin A in ALS. Amyotroph Lateral Scler Frontotemporal Degener. 2021;22:61–5.
   PubMed Web of Science ®Google Scholar
• Buckley CE, 3rd, Dorsey FC. Serum immunoglobulin levels throughout the life-span of healthy man. Ann Intern Med. 1971;75:673–82.
   PubMed Web of Science ®Google Scholar
• De Waart FG, Portengen L, Doekes G, Verwaal CJ, Kok FJ. Effect of 3 months vitamin E supplementation on indices of the cellular and humoral immune response in elderly subjects. Br J Nutr. 1997;78:761–74.
   PubMed Web of Science ®Google Scholar
• Sun M, Yan Z, Sun R, Tian W, Yi W, Zhang J. Dynamic monitoring and a clinical correlation analysis of the serum vitamin A, D, and E levels in children with recurrent respiratory tract infections. Am J Transl Res. 2022;14:3533–8.
   PubMed Web of Science ®Google Scholar
• Tian W, Yi W, Zhang J, Sun M, Sun R, Yan Z. The correlation between the vitamin A, D, and E levels and recurrent respiratory tract infections in children of different ages. Am J Transl Res. 2021;13:5665–71.
   PubMed Web of Science ®Google Scholar
• Appel SH, Engelhardt JI, Henkel JS, Siklos L, Beers DR, Yen AA, et al. Hematopoietic stem cell transplantation in patients with sporadic amyotrophic lateral sclerosis. Neurology. 2008;71:1326–34.
   PubMed Web of Science ®Google Scholar
• Pullen AH, Demestre M, Howard RS, Orrell RW. Passive transfer of purified IgG from patients with amyotrophic lateral sclerosis to mice results in degeneration of motor neurons accompanied by Ca2+ enhancement. Acta Neuropathol. 2004;107:35–46.
   PubMed Web of Science ®Google Scholar
• Obál I, Nógrádi B, Meszlényi V, Patai R, Ricken G, Kovacs GG, et al. Experimental motor neuron disease induced in mice with long-term repeated intraperitoneal injections of serum from ALS patients. Int J Mol Sci. 2019;20:2573.
   PubMed Web of Science ®Google Scholar
• Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol. 2010;11:785–97.
   PubMed Web of Science ®Google Scholar
• Garred P, Genster N, Pilely K, Bayarri-Olmos R, Rosbjerg A, Ma YJ, et al. A journey through the lectin pathway of complement-MBL and beyond. Immunol Rev. 2016;274:74–97.
   PubMed Web of Science ®Google Scholar
• Thompson AG, Gray E, Verber N, Bobeva Y, Lombardi V, Shepheard SR, et al. Multicentre appraisal of amyotrophic lateral sclerosis biofluid biomarkers shows primacy of blood neurofilament light chain. Brain Commun. 2022;4:fcac029.
   PubMedGoogle Scholar
• Goldknopf IL, Sheta EA, Bryson J, Folsom B, Wilson C, Duty J, et al. Complement C3c and related protein biomarkers in amyotrophic lateral sclerosis and Parkinson’s disease. Biochem Biophys Res Commun. 2006;342:1034–9.
   PubMed Web of Science ®Google Scholar
• Ricklin D, Reis ES, Lambris JD. Complement in disease: a defence system turning offensive. Nat Rev Nephrol. 2016;12:383–401.
   PubMed Web of Science ®Google Scholar
• Vogt W, Schmidt G, Von Buttlar B, Dieminger L. A new function of the activated third component of complement: binding to C5, an essential step for C5 activation. Immunology. 1978;34:29–40.
   PubMed Web of Science ®Google Scholar
• Bahia El N, Idrissi K, Fluiter FG, Vieira FB. Complement component C6 inhibition decreases neurological disability in female transgenic SOD1G93A mouse model of amyotrophic lateral sclerosis. Ann Neurodegener Dis. 2016;1(3): 1015.
   Google Scholar
• Woodruff TM, Costantini KJ, Crane JW, Atkin JD, Monk PN, Taylor SM, et al. The complement factor C5a contributes to pathology in a rat model of amyotrophic lateral sclerosis. J Immunol. 2008;181:8727–34.
   PubMed Web of Science ®Google Scholar
• Lee JD, Kamaruzaman NA, Fung JNT, Taylor SM, Turner BJ, Atkin JD, et al. Dysregulation of the complement cascade in the hSOD1G93A transgenic mouse model of amyotrophic lateral sclerosis. J Neuroinflam. 2013;10:119.
   PubMed Web of Science ®Google Scholar
• Heurich B, el Idrissi NB, Donev RM, Petri S, Claus P, Neal J, et al. Complement upregulation and activation on motor neurons and neuromuscular junction in the SOD1 G93A mouse model of familial amyotrophic lateral sclerosis. J Neuroimmunol. 2011;235:104–9.
   PubMed Web of Science ®Google Scholar
• Lee JD, Levin SC, Willis EF, Li R, Woodruff TM, Noakes PG. Complement components are upregulated and correlate with disease progression in the TDP-43 Q331K mouse model of amyotrophic lateral sclerosis. J Neuroinflam. 2018;15:171.
   PubMed Web of Science ®Google Scholar
• Kjældgaard AL, Pilely K, Olsen KS, Øberg Lauritsen A, Wørlich Pedersen S, Svenstrup K, et al. Complement profiles in patients with amyotrophic lateral sclerosis: a prospective observational cohort study. J Inflamm Res. 2021;14:1043–53.
   PubMed Web of Science ®Google Scholar