Is Parkinson's disease a chronic low-grade inflammatory bowel disease?
Crohn’s disease
Enteric nervous system
Inflammatory bowel disease
LRRK2
Parkinson’s disease
Ulcerative colitis
Journal
Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161
Informations de publication
Date de publication:
Aug 2020
Aug 2020
Historique:
received:
31
03
2019
accepted:
10
04
2019
revised:
09
04
2019
pubmed:
17
4
2019
medline:
22
6
2021
entrez:
17
4
2019
Statut:
ppublish
Résumé
While the pathogenesis of Parkinson's disease is not fully understood, there is increasing evidence that inflammatory responses in the brain are implicated in both disease initiation and progression. The inflammatory process in Parkinson's disease is, however, not limited to the brain but also involves the gastrointestinal tract. High amounts of cytokines and inflammatory markers are found in the colon of Parkinson's disease patients and there is now strong epidemiological and genetical evidence linking Parkinson's disease to inflammatory bowel diseases. Recent findings obtained in both experimental inflammatory bowel diseases and Parkinson's disease further support a bidirectional link between gastrointestinal inflammation and brain neurodegeneration. Altogether, these observations suggest a role for gastrointestinal inflammation in the initiation and progression of Parkinson's disease.
Identifiants
pubmed: 30989372
doi: 10.1007/s00415-019-09321-0
pii: 10.1007/s00415-019-09321-0
doi:
Substances chimiques
Biomarkers
0
Cytokines
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2207-2213Références
Chapelet G, Leclair-Visonneau L, Clairembault T et al (2018) Can the gut be the missing piece in uncovering PD pathogenesis? Parkinsonism Relat Disord. https://doi.org/10.1016/j.parkreldis.2018.11.014
doi: 10.1016/j.parkreldis.2018.11.014
pubmed: 30448099
Edwards LL, Quigley EM, Pfeiffer RF (1992) Gastrointestinal dysfunction in Parkinson’s disease: frequency and pathophysiology. Neurology 42:726–732
doi: 10.1212/WNL.42.4.726
Beach TG, Adler CH, Sue LI et al (2010) Multi-organ distribution of phosphorylated alpha-synuclein histopathology in subjects with Lewy body disorders. Acta Neuropathol 119:689–702. https://doi.org/10.1007/s00401-010-0664-3
doi: 10.1007/s00401-010-0664-3
pubmed: 20306269
pmcid: 2866090
Gelpi E, Navarro-Otano J, Tolosa E et al (2014) Multiple organ involvement by alpha-synuclein pathology in Lewy body disorders. Mov Disord 29:1010–1018. https://doi.org/10.1002/mds.25776
doi: 10.1002/mds.25776
pubmed: 24395122
Wakabayashi K, Takahashi H, Takeda S et al (1988) Parkinson’s disease: the presence of Lewy bodies in Auerbach’s and Meissner’s plexuses. Acta Neuropathol 76:217–221
doi: 10.1007/BF00687767
Bialecka M, Kurzawski M, Klodowska-Duda G et al (2007) CARD15 variants in patients with sporadic Parkinson’s disease. Neurosci Res 57:473–476. https://doi.org/10.1016/j.neures.2006.11.012
doi: 10.1016/j.neures.2006.11.012
pubmed: 17174426
Maeda S, Hsu L-C, Liu H et al (2005) Nod2 mutation in Crohn’s disease potentiates NF-kappaB activity and IL-1beta processing. Science 307:734–738. https://doi.org/10.1126/science.1103685
doi: 10.1126/science.1103685
pubmed: 15692052
Umeno J, Asano K, Matsushita T et al (2011) Meta-analysis of published studies identified eight additional common susceptibility loci for Crohn’s disease and ulcerative colitis. Inflamm Bowel Dis 17:2407–2415. https://doi.org/10.1002/ibd.21651
doi: 10.1002/ibd.21651
pubmed: 21351207
Hui KY, Fernandez-Hernandez H, Hu J et al (2018) Functional variants in the LRRK2 gene confer shared effects on risk for Crohn’s disease and Parkinson’s disease. Sci Transl Med. https://doi.org/10.1126/scitranslmed.aai7795
doi: 10.1126/scitranslmed.aai7795
pubmed: 29321258
pmcid: 6028002
Bihari K, Lees AJ (1987) Cigarette smoking, Parkinson’s disease and ulcerative colitis. J Neurol Neurosurg Psychiatry 50:635
doi: 10.1136/jnnp.50.5.635
Fujioka S, Curry SE, Kennelly KD et al (2017) Occurrence of Crohn’s disease with Parkinson’s disease. Parkinsonism Relat Disord 37:116–117. https://doi.org/10.1016/j.parkreldis.2017.01.013
doi: 10.1016/j.parkreldis.2017.01.013
pubmed: 28215729
Lin J-C, Lin C-S, Hsu C-W et al (2016) Association between parkinson’s disease and inflammatory bowel disease: a Nationwide Taiwanese Retrospective Cohort Study. Inflamm Bowel Dis 22:1049–1055. https://doi.org/10.1097/MIB.0000000000000735
doi: 10.1097/MIB.0000000000000735
pubmed: 26919462
Peter I, Dubinsky M, Bressman S et al (2018) Anti-tumor necrosis factor therapy and incidence of parkinson disease among patients with inflammatory bowel disease. JAMA Neurol. https://doi.org/10.1001/jamaneurol.2018.0605
doi: 10.1001/jamaneurol.2018.0605
pubmed: 29710331
pmcid: 6142934
Villumsen M, Aznar S, Pakkenberg B et al (2018) Inflammatory bowel disease increases the risk of Parkinson’s disease: a Danish nationwide cohort study 1977–2014. Gut. https://doi.org/10.1136/gutjnl-2017-315666
doi: 10.1136/gutjnl-2017-315666
pubmed: 30158253
Weimers P, Halfvarson J, Sachs MC et al (2019) Inflammatory bowel disease and Parkinson’s disease: a Nationwide Swedish Cohort Study. Inflamm Bowel Dis 25:111–123. https://doi.org/10.1093/ibd/izy190
doi: 10.1093/ibd/izy190
pubmed: 29788069
Zhu F, Li C, Gong J et al (2019) The risk of Parkinson’s disease in inflammatory bowel disease: a systematic review and meta-analysis. Dig Liver Dis 51:38–42. https://doi.org/10.1016/j.dld.2018.09.017
doi: 10.1016/j.dld.2018.09.017
pubmed: 30309751
Marras C, Lang AE, Austin PC et al (2016) Appendectomy in mid and later life and risk of Parkinson’s disease: a population-based study. Mov Disord 31:1243–1247. https://doi.org/10.1002/mds.26670
doi: 10.1002/mds.26670
pubmed: 27241338
Mendes A, Gonçalves A, Vila-Chã N et al (2015) Appendectomy may delay Parkinson’s disease onset. Mov Disord 30:1404–1407. https://doi.org/10.1002/mds.26311
doi: 10.1002/mds.26311
pubmed: 26228745
Palacios N, Hughes KC, Cereda E et al (2018) Appendectomy and risk of Parkinson’s disease in two large prospective cohorts of men and women. Mov Disord 33:1492–1496. https://doi.org/10.1002/mds.109
doi: 10.1002/mds.109
pubmed: 30218460
pmcid: 6310901
Yilmaz R, Bayram E, Ulukan Ç et al (2017) Appendectomy history is not related to Parkinson’s disease. J Parkinsons Dis 7:347–352. https://doi.org/10.3233/JPD-171071
doi: 10.3233/JPD-171071
pubmed: 28387683
Svensson E, Horváth-Puhó E, Stokholm MG et al (2016) Appendectomy and risk of Parkinson’s disease: a nationwide cohort study with more than 10 years of follow-up. Mov Disord 31:1918–1922. https://doi.org/10.1002/mds.26761
doi: 10.1002/mds.26761
pubmed: 27621223
Killinger BA, Madaj Z, Sikora JW et al (2018) The vermiform appendix impacts the risk of developing Parkinson’s disease. Sci Transl Med. https://doi.org/10.1126/scitranslmed.aar5280
doi: 10.1126/scitranslmed.aar5280
pubmed: 30381408
pmcid: 6319259
Altschuler SM, Escardo J, Lynn RB, Miselis RR (1993) The central organization of the vagus nerve innervating the colon of the rat. Gastroenterology 104:502–509
doi: 10.1016/0016-5085(93)90419-D
Gray MT, Munoz DG, Gray DA et al (2014) Alpha-synuclein in the appendiceal mucosa of neurologically intact subjects. Mov Disord 29:991–998. https://doi.org/10.1002/mds.25779
doi: 10.1002/mds.25779
pubmed: 24352892
Russel MG, Dorant E, Brummer RJ et al (1997) Appendectomy and the risk of developing ulcerative colitis or Crohn’s disease: results of a large case-control study. South Limburg Inflammatory Bowel Disease Study Group. Gastroenterology 113:377–382
doi: 10.1053/gast.1997.v113.pm9247453
Devos D, Lebouvier T, Lardeux B et al (2013) Colonic inflammation in Parkinson’s disease. Neurobiol Dis 50:42–48. https://doi.org/10.1016/j.nbd.2012.09.007
doi: 10.1016/j.nbd.2012.09.007
pubmed: 23017648
Pochard C, Leclair-Visonneau L, Coron E et al (2018) Cyclooxygenase 2 is upregulated in the gastrointestinal tract in Parkinson’s disease. Mov Disord 33:493–494. https://doi.org/10.1002/mds.27237
doi: 10.1002/mds.27237
pubmed: 29150878
Perez-Pardo P, Dodiya HB, Engen PA et al (2018) Role of TLR4 in the gut-brain axis in Parkinson’s disease: a translational study from men to mice. Gut. https://doi.org/10.1136/gutjnl-2018-316844
doi: 10.1136/gutjnl-2018-316844
pubmed: 30554160
Eeckhaut V, Machiels K, Perrier C et al (2013) Butyricicoccus pullicaecorum in inflammatory bowel disease. Gut 62:1745–1752. https://doi.org/10.1136/gutjnl-2012-303611
doi: 10.1136/gutjnl-2012-303611
pubmed: 23263527
Houser MC, Chang J, Factor SA et al (2018) Stool immune profiles evince gastrointestinal inflammation in Parkinson’s disease. Mov Disord 33:793–804. https://doi.org/10.1002/mds.27326
doi: 10.1002/mds.27326
pubmed: 29572994
pmcid: 5992021
Schwiertz A, Spiegel J, Dillmann U et al (2018) Fecal markers of intestinal inflammation and intestinal permeability are elevated in Parkinson’s disease. Parkinsonism Relat Disord. https://doi.org/10.1016/j.parkreldis.2018.02.022
doi: 10.1016/j.parkreldis.2018.02.022
pubmed: 29454662
Eichele DD, Kharbanda KK (2017) Dextran sodium sulfate colitis murine model: an indispensable tool for advancing our understanding of inflammatory bowel diseases pathogenesis. World J Gastroenterol 23:6016–6029. https://doi.org/10.3748/wjg.v23.i33.6016
doi: 10.3748/wjg.v23.i33.6016
pubmed: 28970718
pmcid: 5597494
Villarán RF, Espinosa-Oliva AM, Sarmiento M et al (2010) Ulcerative colitis exacerbates lipopolysaccharide-induced damage to the nigral dopaminergic system: potential risk factor in Parkinson’s disease. J Neurochem 114:1687–1700. https://doi.org/10.1111/j.1471-4159.2010.06879.x
doi: 10.1111/j.1471-4159.2010.06879.x
pubmed: 20584104
Garrido-Gil P, Rodriguez-Perez AI, Dominguez-Meijide A et al (2018) Bidirectional neural interaction between central dopaminergic and gut lesions in Parkinson’s disease models. Mol Neurobiol. https://doi.org/10.1007/s12035-018-0937-8
doi: 10.1007/s12035-018-0937-8
pubmed: 29404956
Blandini F, Armentero M-T, Martignoni E (2008) The 6-hydroxydopamine model: news from the past. Parkinsonism Relat Disord 14(Suppl 2):S124–S129. https://doi.org/10.1016/j.parkreldis.2008.04.015
doi: 10.1016/j.parkreldis.2008.04.015
pubmed: 18595767
Pellegrini C, Fornai M, Colucci R et al (2016) Alteration of colonic excitatory tachykininergic motility and enteric inflammation following dopaminergic nigrostriatal neurodegeneration. J Neuroinflamm 13:146. https://doi.org/10.1186/s12974-016-0608-5
doi: 10.1186/s12974-016-0608-5
Zheng L-F, Wang Z-Y, Li X et al (2011) Reduced expression of choline acetyltransferase in vagal motoneurons and gastric motor dysfunction in a 6-OHDA rat model of Parkinson’s disease. Brain Res 1420:59–67. https://doi.org/10.1016/j.brainres.2011.09.006
doi: 10.1016/j.brainres.2011.09.006
pubmed: 21955729
Lema Tomé CM, Tyson T, Rey NL et al (2013) Inflammation and α-synuclein’s prion-like behavior in Parkinson’s disease—is there a link? Mol Neurobiol 47:561–574. https://doi.org/10.1007/s12035-012-8267-8
doi: 10.1007/s12035-012-8267-8
pubmed: 22544647
Houser MC, Tansey MG (2017) The gut-brain axis: is intestinal inflammation a silent driver of Parkinson’s disease pathogenesis? NPJ Parkinsons Dis 3:3. https://doi.org/10.1038/s41531-016-0002-0
doi: 10.1038/s41531-016-0002-0
pubmed: 28649603
pmcid: 5445611
Walter GC, Phillips RJ, Baronowsky EA, Powley TL (2009) Versatile, high-resolution anterograde labeling of vagal efferent projections with dextran amines. J Neurosci Methods 178:1–9. https://doi.org/10.1016/j.jneumeth.2008.11.003
doi: 10.1016/j.jneumeth.2008.11.003
pubmed: 19056424
Liu B, Fang F, Pedersen NL et al (2017) Vagotomy and Parkinson disease: a Swedish register-based matched-cohort study. Neurology 88:1996–2002. https://doi.org/10.1212/WNL.0000000000003961
doi: 10.1212/WNL.0000000000003961
pubmed: 28446653
pmcid: 5440238
Svensson E, Horváth-Puhó E, Thomsen RW et al (2015) Vagotomy and subsequent risk of Parkinson’s disease. Ann Neurol 78:522–529. https://doi.org/10.1002/ana.24448
doi: 10.1002/ana.24448
pubmed: 26031848
Prigent A, Lionnet A, Durieu E et al (2019) Enteric alpha-synuclein expression is increased in Crohn’s disease. Acta Neuropathol 137:359–361. https://doi.org/10.1007/s00401-018-1943-7
doi: 10.1007/s00401-018-1943-7
pubmed: 30506319
Prigent A, Gonzales J, Durand T et al (2018) Acute inflammation down-regulates alpha-synuclein expression in enteric neurons. J Neurochem. https://doi.org/10.1111/jnc.14656
doi: 10.1111/jnc.14656
Guan Q, Zhang J (2017) Recent advances: the imbalance of cytokines in the pathogenesis of inflammatory bowel disease. Mediat Inflamm 2017:4810258. https://doi.org/10.1155/2017/4810258
doi: 10.1155/2017/4810258
Fedorova TD, Seidelin LB, Knudsen K et al (2017) Decreased intestinal acetylcholinesterase in early Parkinson disease: an 11C-donepezil PET study. Neurology 88:775–781. https://doi.org/10.1212/WNL.0000000000003633
doi: 10.1212/WNL.0000000000003633
pubmed: 28100726
Greenland JC, Williams-Gray CH, Barker RA (2019) The clinical heterogeneity of Parkinson’s disease and its therapeutic implications. Eur J Neurosci 49:328–338. https://doi.org/10.1111/ejn.14094
doi: 10.1111/ejn.14094
pubmed: 30059179
Johnson ME, Stecher B, Labrie V et al (2019) Triggers, facilitators, and aggravators: redefining Parkinson’s disease pathogenesis. Trends Neurosci 42:4–13. https://doi.org/10.1016/j.tins.2018.09.007
doi: 10.1016/j.tins.2018.09.007
pubmed: 30342839
Zou W, Pu T, Feng W et al (2019) Blocking meningeal lymphatic drainage aggravates Parkinson’s disease-like pathology in mice overexpressing mutated α-synuclein. Transl Neurodegener 8:7. https://doi.org/10.1186/s40035-019-0147-y
doi: 10.1186/s40035-019-0147-y
pubmed: 30867902
pmcid: 6396507
Takagawa T, Kitani A, Fuss I et al (2018) An increase in LRRK2 suppresses autophagy and enhances Dectin-1-induced immunity in a mouse model of colitis. Sci Transl Med. https://doi.org/10.1126/scitranslmed.aan8162
doi: 10.1126/scitranslmed.aan8162
pubmed: 29875204
pmcid: 6636639