Acute Exposure to the Food-Borne Pathogen Listeria monocytogenes Does Not Induce α-Synuclein Pathology in the Colonic ENS of Nonhuman Primates

References

• Vermilyea SC, Emborg ME. α-Synuclein and nonhuman primate models of Parkinson’s disease. J Neurosci Methods. 2015;255:38–51. doi:10.1016/j.jneumeth.2015.07.025
   PubMed Web of Science ®Google Scholar
• Bendor JT, Logan TP, Edwards RH. The function of α-synuclein. Neuron. 2013;79(6):1044–1066. doi:10.1016/j.neuron.2013.09.004
   PubMed Web of Science ®Google Scholar
• Hald A, Lotharius J. Oxidative stress and inflammation in Parkinson’s disease: is there a causal link? Exp Neurol. 2005;193(2):279–290. doi:10.1016/j.expneurol.2005.01.013
   PubMed Web of Science ®Google Scholar
• Matyszak MK. Inflammation in the CNS: balance between immunological privilege and immune responses. Prog Neurobiol. 1998;56(1):19–35. doi:10.1016/S0301-0082(98)00014-8
   PubMed Web of Science ®Google Scholar
• Rai SN, Singh P, Varshney R, et al. Promising drug targets and associated therapeutic interventions in Parkinson’s disease. Neural Regen Res. 2021;16(9):1730–1739. doi:10.4103/1673-5374.306066
   PubMed Web of Science ®Google Scholar
• Jankovic J. Parkinson’s disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry. 2008;79(4):368–376. doi:10.1136/jnnp.2007.131045
   PubMed Web of Science ®Google Scholar
• Braak H, Rob U, Gai WP, et al. Idiopathic Parkinson’s disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J Neural Transm (Vienna). 2003;110(5):517–536. doi:10.1007/s00702-002-0808-2
   PubMed Web of Science ®Google Scholar
• Braak H, Tredici KD, Rüb U, et al. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging. 2003;24(2):197–211. doi:10.1016/S0197-4580(02)00065-9
   PubMed Web of Science ®Google Scholar
• Braak H, de Vos RAI, Bohl J, et al. Gastric alpha-synuclein immunoreactive inclusions in Meissner’s and Auerbach’s plexuses in cases staged for Parkinson’s disease-related brain pathology. Neurosci Lett. 2006;396(1):67–72. doi:10.1016/j.neulet.2005.11.012
   PubMed Web of Science ®Google Scholar
• Liu B, Fang F, Pedersen NL, et al. Vagotomy and Parkinson disease: a Swedish register-based matched-cohort study. Neurology. 2017;88(21):1996–2002. doi:10.1212/WNL.0000000000003961
   PubMed Web of Science ®Google Scholar
• Svensson E, Horváth-Puhó E, Thomsen RW, et al. Vagotomy and subsequent risk of Parkinson’s disease. Ann Neurol. 2015;78(4):522–529. doi:10.1002/ana.24448
   PubMed Web of Science ®Google Scholar
• Tysnes OB, Kenborg L, Herlofson K, et al. Does vagotomy reduce the risk of Parkinson’s disease? Ann Neurol. 2015;78(6):1011–1012. doi:10.1002/ana.24531
   PubMed Web of Science ®Google Scholar
• Lohmann S, Bernis ME, Tachu BJ, et al. Oral and intravenous transmission of alpha-synuclein fibrils to mice. Acta Neuropathol. 2019;138(4):515–533. doi:10.1007/s00401-019-02037-5
   PubMed Web of Science ®Google Scholar
• Kim S, Kwon S-H, Kam T-I, et al. Transneuronal propagation of pathologic alpha-synuclein from the gut to the brain models Parkinson’s disease. Neuron. 2019;103(4):627–641e7. doi:10.1016/j.neuron.2019.05.035
   PubMed Web of Science ®Google Scholar
• Holmqvist S, Chutna O, Bousset L, et al. Direct evidence of Parkinson pathology spread from the gastrointestinal tract to the brain in rats. Acta Neuropathol. 2014;128(6):805–820. doi:10.1007/s00401-014-1343-6
   PubMed Web of Science ®Google Scholar
• Van Den Berge N, Ferreira N, Mikkelsen TW, et al. Ageing promotes pathological alpha-synuclein propagation and autonomic dysfunction in wild-type rats. Brain. 2021;144(6):1853–1868. doi:10.1093/brain/awab061
   PubMedGoogle Scholar
• Van Den Berge N, Ferreira N, Gram H, et al. Evidence for bidirectional and trans-synaptic parasympathetic and sympathetic propagation of alpha-synuclein in rats. Acta Neuropathol. 2019;138(4):535–550. doi:10.1007/s00401-019-02040-w
   PubMed Web of Science ®Google Scholar
• Pajares M, I Rojo A, Manda G, Boscá L, Cuadrado A. et al. Inflammation in Parkinson’s disease: mechanisms and therapeutic implications. Cells. 2020;9(7):1687.
   PubMed Web of Science ®Google Scholar
• Devos D, Lebouvier T, Lardeux B, et al. Colonic inflammation in Parkinson’s disease. Neurobiol Dis. 2013;50:42–48. doi:10.1016/j.nbd.2012.09.007
   PubMed Web of Science ®Google Scholar
• Houser MC, Chang J, Factor SA, et al. Stool Immune profiles evince gastrointestinal inflammation in Parkinson’s disease. Mov Disord. 2018;33(5):793–804. doi:10.1002/mds.27326
   PubMed Web of Science ®Google Scholar
• Kooij IA, Sahami S, Meijer SL, et al. The immunology of the vermiform appendix: a review of the literature. Clin Exp Immunol. 2016;186(1):1–9. doi:10.1111/cei.12821
   PubMed Web of Science ®Google Scholar
• Killinger BA, Madaj Z, Sikora JW, et al. The vermiform appendix impacts the risk of developing Parkinson’s disease. Sci Transl Med. 2018;10::465.
   Web of Science ®Google Scholar
• Roberts BN, Chakravarty D, Gardner JC, et al. Response to anaerobic environments. Pathogens. 2020;9(3):210.
   PubMed Web of Science ®Google Scholar
• Charlier C, Perrodeau É, Leclercq A, et al. Clinical features and prognostic factors of listeriosis: the MONALISA national prospective cohort study. Lancet Infect Dis. 2017;17(5):510–519. doi:10.1016/S1473-3099(16)30521-7
   PubMed Web of Science ®Google Scholar
• Lecuit M. Understanding how Listeria monocytogenes targets and crosses host barriers. Clin Microbiol Infect. 2005;11(6):430–436. doi:10.1111/j.1469-0691.2005.01146.x
   PubMed Web of Science ®Google Scholar
• Corr S, Hill C, Gahan CG. An in vitro cell-culture model demonstrates internalin- and hemolysin-independent translocation of Listeria monocytogenes across M cells. Microb Pathog. 2006;41(6):241–250. doi:10.1016/j.micpath.2006.08.003
   PubMed Web of Science ®Google Scholar
• Greiffenberg L, Goebel W, Kim KS, et al. Interaction of Listeria monocytogenes with human brain microvascular endothelial cells: inlB-dependent invasion, long-term intracellular growth, and spread from macrophages to endothelial cells. Infect Immun. 1998;66(11):5260–5267. doi:10.1128/IAI.66.11.5260-5267.1998
   PubMed Web of Science ®Google Scholar
• Drevets DA, Sawyer RT, Potter TA, et al. Listeria monocytogenes infects human endothelial cells by two distinct mechanisms. Infect Immun. 1995;63(11):4268–4276. doi:10.1128/iai.63.11.4268-4276.1995
   PubMed Web of Science ®Google Scholar
• Gaillard JL, Berche P, Sansonetti P. Transposon mutagenesis as a tool to study the role of hemolysin in the virulence of Listeria monocytogenes. Infect Immun. 1986;52(1):50–55. doi:10.1128/iai.52.1.50-55.1986
   PubMed Web of Science ®Google Scholar
• Kathariou S, Metz P, Hof H, et al. Tn916-induced mutations in the hemolysin determinant affecting virulence of Listeria monocytogenes. J Bacteriol. 1987;169(3):1291–1297. doi:10.1128/jb.169.3.1291-1297.1987
   PubMed Web of Science ®Google Scholar
• Tilney LG, Portnoy DA. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol. 1989;109(4 Pt 1):1597–1608. doi:10.1083/jcb.109.4.1597
   PubMed Web of Science ®Google Scholar
• Gabay C. Interleukin-6 and chronic inflammation. Arthritis Res Ther. 2006;8(Suppl 2):S3. doi:10.1186/ar1917
   PubMed Web of Science ®Google Scholar
• Ryan GB, Majno G. Acute inflammation. A review. Am J Pathol. 1977;86(1):183–276.
   PubMed Web of Science ®Google Scholar
• Freire MO, Van Dyke TE. Natural resolution of inflammation. Periodontol. 2000;63(1):149–164. doi:10.1111/prd.12034
   Google Scholar
• Creagh EM, O’Neill LA. TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity. Trends Immunol. 2006;27(8):352–357. doi:10.1016/j.it.2006.06.003
   PubMed Web of Science ®Google Scholar
• O’Neill LA, Bowie AG. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol. 2007;7(5):353–364. doi:10.1038/nri2079
   PubMed Web of Science ®Google Scholar
• Ranson T, Bregenholt S, Lehuen A, et al. Invariant Vα14+NKT cells participate in the early response to enteric Listeria monocytogenes Infection. J Immunol. 2005;175(2):1137–1144. doi:10.4049/jimmunol.175.2.1137
   PubMed Web of Science ®Google Scholar
• Wolfe B, Kerr AR, Mejia A, et al. Sequelae of fetal infection in a non-human primate model of listeriosis. Front Microbiol. 2019;10:2021. doi:10.3389/fmicb.2019.02021
   PubMed Web of Science ®Google Scholar
• Wolfe B, Wiepz GJ, Schotzko M, et al. Acute fetal demise with first trimester maternal infection resulting from. mBio. 2017;8(1):e01938.
   PubMed Web of Science ®Google Scholar
• Lancaster DP, Friedman DF, Chiotos K, et al. Blood volume required for detection of low levels and ultralow levels of organisms responsible for neonatal bacteremia by use of bactec peds Plus/F, Plus Aerobic/F Medium, and the BD Bactec FX system: an in vitro study. J Clin Microbiol. 2015;53(11):3609–3613. doi:10.1128/JCM.01706-15
   PubMed Web of Science ®Google Scholar
• Resnikoff H, Metzger JM, Lopez M, et al. Colonic inflammation affects myenteric alpha-synuclein in nonhuman primates. J Inflamm Res. 2019;12:113–126. doi:10.2147/JIR.S196552
   PubMed Web of Science ®Google Scholar
• Shultz JM, Resnikoff H, Bondarenko V, et al. Neurotoxin-induced catecholaminergic loss in the colonic myenteric plexus of rhesus monkeys. J Alzheimers Dis Parkinsonism. 2016;6:6.
   Google Scholar
• Harty JT, Lenz LL, Bevan MJ. Primary and secondary immune responses to Listeria monocytogenes. Curr Opin Immunol. 1996;8(4):526–530. doi:10.1016/S0952-7915(96)80041-0
   PubMed Web of Science ®Google Scholar
• Czuprynski CJ, Brown JF, Maroushek N, et al. Administration of anti-granulocyte mAb RB6-8C5 impairs the resistance of mice to Listeria monocytogenes infection. J Immunol. 1994;152(4):1836–1846.
   PubMed Web of Science ®Google Scholar
• Vázquez-Boland JA, Kuhn M, Berche P, et al. Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev. 2001;14(3):584–640.
   PubMed Web of Science ®Google Scholar
• Fisher RE. The primate appendix: a reassessment. Anat Rec. 2000;261(6):228–236. doi:10.1002/1097-0185(20001215)261:6<228::AID-AR1005>3.0.CO;2-O
   PubMedGoogle Scholar
• Zinnen AD, Jeanette JV, Metzger M, et al. Alpha-synuclein and Tau are abundantly expressed in the appendix of humans and the ceca of common marmosets and rhesus macaques. Society for Neuroscience Abst. 2021; 2021.
   Google Scholar
• Delic V, Chandra S, Abdelmotilib H, et al. Sensitivity and specificity of phospho-Ser129 alpha-synuclein monoclonal antibodies. J Comp Neurol. 2018;526(12):1978–1990. doi:10.1002/cne.24468
   PubMed Web of Science ®Google Scholar
• Wooten GF, Currie LJ, Bovbjerg VE, Lee JK, Patrie J. Are men at greater risk for Parkinson’s disease than women? J Neurol Neurosurg Psychiatry. 2004;75(4):637–639. doi:10.1136/jnnp.2003.020982
   PubMed Web of Science ®Google Scholar
• Peter I, Dubinsky M, Bressman S, et al. Anti-tumor necrosis factor therapy and incidence of Parkinson disease among patients with inflammatory bowel disease. JAMA Neurol. 2018;75(8):939–946. doi:10.1001/jamaneurol.2018.0605
   PubMed Web of Science ®Google Scholar
• Lin JC, Lin C-S, Hsu C-W, et al. Association between parkinson’s disease and inflammatory bowel disease: a Nationwide Taiwanese Retrospective Cohort Study. Inflamm Bowel Dis. 2016;22(5):1049–1055. doi:10.1097/MIB.0000000000000735
   PubMed Web of Science ®Google Scholar
• Weimers P, Halfvarson J, Sachs MC, et al. Inflammatory Bowel Disease and Parkinson’s Disease: a Nationwide Swedish Cohort Study. Inflamm Bowel Dis. 2019;25(1):111–123. doi:10.1093/ibd/izy190
   PubMed Web of Science ®Google Scholar
• Houser MC, Caudle WM, Chang J, et al. Experimental colitis promotes sustained, sex-dependent, T-cell-associated neuroinflammation and parkinsonian neuropathology. Acta Neuropathol Commun. 2021;9(1):139. doi:10.1186/s40478-021-01240-4
   PubMed Web of Science ®Google Scholar
• Lazaridis N, Germanidis G. Current insights into the innate immune system dysfunction in irritable bowel syndrome. Ann Gastroenterol. 2018;31(2):171–187. doi:10.20524/aog.2018.0229
   PubMed Web of Science ®Google Scholar
• Nagatsu T, Mogi M, Ichinose H, et al.Changes in cytokines and neurotrophins in Parkinson’s disease. J Neural Transm Suppl. 2000;(60):277–290. doi:10.1007/978-3-7091-6301-6_19
   PubMedGoogle Scholar
• Yang X, Qian Y, Xu S, et al. Longitudinal analysis of fecal microbiome and pathologic processes in a rotenone induced mice model of Parkinson’s disease. Front Aging Neurosci. 2017;9:441. doi:10.3389/fnagi.2017.00441
   PubMed Web of Science ®Google Scholar
• Morais LH, Hara DB, Bicca MA, et al. Early signs of colonic inflammation, intestinal dysfunction, and olfactory impairments in the rotenone-induced mouse model of Parkinson’s disease. Behav Pharmacol. 2018;29(2 and 3–Spec Issue):199–210. doi:10.1097/FBP.0000000000000389
   PubMed Web of Science ®Google Scholar
• Pan-Montojo F, Anichtchik O, Dening Y, et al. Progression of Parkinson’s disease pathology is reproduced by intragastric administration of rotenone in mice. PLoS One. 2010;5(1):e8762. doi:10.1371/journal.pone.0008762
   PubMed Web of Science ®Google Scholar
• Romano S, Savva GM, Bedarf JR, et al. Meta-analysis of the Parkinson’s disease gut microbiome suggests alterations linked to intestinal inflammation. NPJ Parkinsons Dis. 2021;7(1):27. doi:10.1038/s41531-021-00156-z
   PubMed Web of Science ®Google Scholar
• Keshavarzian A, Engen P, Bonvegna S, Cilia R. The gut microbiome in Parkinson’s disease: a culprit or a bystander? Prog Brain Res. 2020;252:357–450.
   PubMed Web of Science ®Google Scholar
• Buford TW. (Dis) Trust your gut: the gut microbiome in age-related inflammation, health, and disease. Microbiome. 2017;5(1):80. doi:10.1186/s40168-017-0296-0
   PubMed Web of Science ®Google Scholar
• Allen Reish HE, Standaert DG. Role of alpha-synuclein in inducing innate and adaptive immunity in Parkinson disease. J Parkinsons Dis. 2015;5(1):1–19. doi:10.3233/JPD-140491
   PubMedGoogle Scholar
• Croisier E, Moran LB, Dexter DT, et al. Microglial inflammation in the parkinsonian substantia nigra: relationship to alpha-synuclein deposition. J Neuroinflammation. 2005;2:14. doi:10.1186/1742-2094-2-14
   PubMed Web of Science ®Google Scholar
• Depboylu C, Schäfer MK-H, Arias-Carrión O, et al. Possible involvement of complement factor C1q in the clearance of extracellular neuromelanin from the substantia nigra in Parkinson disease. J Neuropathol Exp Neurol. 2011;70(2):125–132. doi:10.1097/NEN.0b013e31820805b9
   PubMed Web of Science ®Google Scholar
• Bortolussi R. Listeriosis: a primer. CMAJ. 2008;179(8):795–797. doi:10.1503/cmaj.081377
   PubMed Web of Science ®Google Scholar