What a gastrointestinal biopsy can tell us about Parkinson's disease?

Neurogastroenterology and Motility

Volumn 28, Issue 7, 2016, Pages 966-974

  Corbille A G ^a,b,c   Clairembault, T ^a,b   Coron, E ^a,b,c   Leclair Visonneau, L ^a,b   Preterre, C ^a,c   Neunlist, M ^a,b,c   Derkinderen, P ^a,b,c  

^a INSERM   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c NANTES UNIVERSITY HOSPITAL   (France)

Author keywords

enteric glial cells; enteric nervous system; enteric neurons; gastrointestinal biopsy; Parkinson's disease

Indexed keywords

BIOLOGICAL MARKER; GREEN FLUORESCENT PROTEIN;

DIAGNOSTIC PROCEDURE; GASTROINTESTINAL BIOPSY; GENE OVEREXPRESSION; GLIA CELL; HUMAN; INTESTINE EPITHELIUM; INTESTINE EPITHELIUM CELL; LEWY BODY; MINIMALLY INVASIVE PROCEDURE; NEURITE; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; SUBMUCOUS PLEXUS; TIGHT JUNCTION;

EID: 84977103200     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/nmo.12797     Document Type: Review

References (75)

1. Qualman SJ, Haupt HM, Yang P, Hamilton SR. Esophageal Lewy bodies associated with ganglion cell loss in achalasia. Similarity to Parkinson's disease. Gastroenterology 1984; 87: 848–56.
2. Kupsky WJ, Grimes MM, Sweeting J, Bertsch R, Cote LJ. Parkinson's disease and megacolon: concentric hyaline inclusions (Lewy bodies) in enteric ganglion cells. Neurology 1987; 37: 1253–5.
3. Wakabayashi K, Takahashi H, Takeda S, Ohama E, Ikuta F. Parkinson's disease: the presence of Lewy bodies in Auerbach's and Meissner's plexuses. Acta Neuropathol 1988; 76: 217–21.
4. Edwards LL, Pfeiffer RF, Quigley EM, Hofman R, Balluff M. Gastrointestinal symptoms in Parkinson's disease. Mov Disord 1991; 6: 151–6.
5. Edwards L, Quigley EM, Hofman R, Pfeiffer RF. Gastrointestinal symptoms in Parkinson disease: 18-month follow-up study. Mov Disord 1993; 8: 83–6.
6. Beach TG, Adler CH, Sue LI, Vedders L, Lue L, White Iii CL, Akiyama H, Caviness JN et al. Multi-organ distribution of phosphorylated alpha-synuclein histopathology in subjects with Lewy body disorders. Acta Neuropathol 2009; 119: 689–702.
7. Schneider SA, Boettner M, Alexoudi A, Zorenkov D, Deuschl G, Wedel T. Can we use peripheral tissue biopsies to diagnose Parkinson's disease? A review of the literature. Eur J Neurol 2016; 23: 247–61.
8. Lebouvier T, Chaumette T, Damier P, Coron E, Touchefeu Y, Vrignaud S, Naveilhan P, Galmiche JP et al. Pathological lesions in colonic biopsies during Parkinson's disease. Gut 2008; 57: 1741–3.
9. Lebouvier T, Neunlist M, Bruley des Varannes S, Coron E, Drouard A, N'Guyen JM, Chaumette T, Tasselli M et al. Colonic biopsies to assess the neuropathology of Parkinson's disease and its relationship with symptoms. PLoS ONE 2010; 5: e12728.
10. Shannon KM, Keshavarzian A, Mutlu E, Dodiya HB, Daian D, Jaglin JA, Kordower JH. Alpha-synuclein in colonic submucosa in early untreated Parkinson's disease. Mov Disord 2012; 27: 709–15.
11. Sánchez-Ferro Á, Rábano A, Catalán MJ, Rodríguez-Valcárcel FC, Fernández Díez S, Herreros-Rodríguez J, García-Cobos E, Álvarez-Santullano MM et al. In vivo gastric detection of α-synuclein inclusions in Parkinson's disease. Mov Disord 2015; 30: 517–24.
12. Hilton D, Stephens M, Kirk L, Edwards P, Potter R, Zajicek J, Broughton E, Hagan H et al. Accumulation of α-synuclein in the bowel of patients in the pre-clinical phase of Parkinson's disease. Acta Neuropathol 2014; 127: 235–41.
13. Visanji NP, Marras C, Kern DS, Al Dakheel A, Gao A, Liu LW, Lang AE, Hazrati LN. Colonic mucosal a-synuclein lacks specificity as a biomarker for Parkinson disease. Neurology 2015; 84: 609–16.
14. Hanani M, Reichenbach A. Morphology of horseradish peroxidase (HRP)-injected glial cells in the myenteric plexus of the guinea-pig. Cell Tissue Res 1994; 278: 153–60.
15. Boesmans W, Lasrado R, Vanden Berghe P, Pachnis V. Heterogeneity and phenotypic plasticity of glial cells in the mammalian enteric nervous system. Glia 2015; 63: 229–41.
16. Messenger JP, Furness JB. Projections of chemically-specified neurons in the guinea-pig colon. Arch Histol Cytol 1990; 53: 467–95.
17. Neunlist M, Van Landeghem L, Mahé MM, Derkinderen P, des Varannes SB, Rolli-Derkinderen M. The digestive neuronal-glial-epithelial unit: a new actor in gut health and disease. Nat Rev Gastroenterol Hepatol 2013; 10: 90–100.
18. Lebouvier T, Coron E, Chaumette T, Paillusson S, Bruley des Varannes S, Neunlist M, Derkinderen P. Routine colonic biopsies as a new tool to study the enteric nervous system in living patients. Neurogastroenterol Motil 2010; 22: e11–4.
19. Devos D, Lebouvier T, Lardeux B, Biraud M, Rouaud T, Pouclet H, Coron E, Bruley des Varannes S et al. Colonic inflammation in Parkinson's disease. Neurobiol Dis 2013; 50: 42–8.
20. Clairembault T, Leclair-Visonneau L, Coron E, Bourreille A, Le Dily S, Vavasseur F, Heymann MF, Neunlist M et al. Structural alterations of the intestinal epithelial barrier in Parkinson's disease. Acta Neuropathol Commun 2015; 3: 12.
21. Clairembault T, Kamphuis W, Leclair-Visonneau L, Rolli-Derkinderen M, Coron E, Neunlist M, Hol EM, Derkinderen P. Enteric GFAP expression and phosphorylation in Parkinson's disease. J Neurochem 2014; 130: 805–15.
22. Corbillé A-G, Coron E, Neunlist M, Derkinderen P, Lebouvier T. Appraisal of the dopaminergic and noradrenergic innervation of the submucosal plexus in PD. J Parkinsons Dis 2014; 4: 571–6.
23. Pouclet H, Lebouvier T, Coron E, des Varannes SB, Neunlist M, Derkinderen P. A comparison between colonic submucosa and mucosa to detect Lewy pathology in Parkinson's disease. Neurogastroenterol Motil 2012; 24: e202–5.
24. Wallon C, Braaf Y, Wolving M, Olaison G, Söderholm JD. Endoscopic biopsies in Ussing chambers evaluated for studies of macromolecular permeability in the human colon. Scand J Gastroenterol 2005; 40: 586–95.
25. Dickson DW, Braak H, Duda JE, Duyckaerts C, Gasser T, Halliday GM, Hardy J, Leverenz JB et al. Neuropathological assessment of Parkinson's disease: refining the diagnostic criteria. Lancet Neurol 2009; 8: 1150–7.
26. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M. Alpha-synuclein in Lewy bodies. Nature 1997; 388: 839–40.
27. Beach TG, White CL, Hamilton RL, Duda JE, Iwatsubo T, Dickson DW, Leverenz JB, Roncaroli F et al. Evaluation of alpha-synuclein immunohistochemical methods used by invited experts. Acta Neuropathol 2008; 116: 277–88.
28. Gelpi E, Navarro-Otano J, Tolosa E, Gaig C, Compta Y, Rey MJ, Martí MJ, Hernández I et al. Multiple organ involvement by alpha-synuclein pathology in Lewy body disorders. Mov Disord 2014; 29: 1010–8.
29. Ito S, Takao M, Hatsuta H, Kanemaru K, Arai T, Saito Y, Fukayama M, Murayama S. Alpha-synuclein immunohistochemistry of gastrointestinal and biliary surgical specimens for diagnosis of Lewy body disease. Int J Clin Exp Pathol 2014; 7: 1714–23.
30. Pouclet H, Lebouvier T, Coron E, Rouaud T, Flamant M, Toulgoat F, Roy M, Vavasseur F et al. Analysis of colonic alpha-synuclein pathology in multiple system atrophy. Parkinsonism Relat Disord 2012; 18: 893–5.
31. Pouclet H, Lebouvier T, Coron E, des Varannes SB, Rouaud T, Roy M, Neunlist M, Derkinderen P. A comparison between rectal and colonic biopsies to detect Lewy pathology in Parkinson's disease. Neurobiol Dis 2012; 45: 305–9.
32. Levin TR, Conell C, Shapiro JA, Chazan SG, Nadel MR, Selby JV. Complications of screening flexible sigmoidoscopy. Gastroenterology 2002; 123: 1786–92.
33. Greffard S, Verny M, Bonnet AM, Beinis JY, Gallinari C, Meaume S, Piette F, Hauw JJ et al. Motor score of the Unified Parkinson Disease Rating Scale as a good predictor of Lewy body-associated neuronal loss in the substantia nigra. Arch Neurol 2006; 63: 584–8.
34. Annerino DM, Arshad S, Taylor GM, Adler CH, Beach TG, Greene JG. Parkinson's disease is not associated with gastrointestinal myenteric ganglion neuron loss. Acta Neuropathol 2012; 124: 665–80.
35. Greene JG. Causes and consequences of degeneration of the dorsal motor nucleus of the vagus nerve in Parkinson's disease. Antioxid Redox Signal 2014; 21: 649–67.
36. Cersosimo MG, Benarroch EE. Neural control of the gastrointestinal tract: implications for Parkinson disease. Mov Disord 2008; 23: 1065–75.
37. Sharkey KA. Emerging roles for enteric glia in gastrointestinal disorders. J Clin Invest 2015; 125: 918–25.
38. Hanani M. Neurons and glial cells of the enteric nervous system: studies in tissue culture. J Basic Clin Physiol Pharmacol 1993; 4: 157–79.
39. Hanani M, Francke M, Härtig W, Grosche J, Reichenbach A, Pannicke T. Patch-clamp study of neurons and glial cells in isolated myenteric ganglia. Am J Physiol Gastrointest Liver Physiol 2000; 278: G644–51.
40. Jessen KR, Mirsky R. Glial cells in the enteric nervous system contain glial fibrillary acidic protein. Nature 1980; 286: 736–7.
41. Jessen KR, Mirsky R. Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of enteric glia. J Neurosci 1983; 3: 2206–18.
42. Burda JE, Sofroniew MV. Reactive gliosis and the multicellular response to CNS damage and disease. Neuron 2014; 81: 229–48.
43. Middeldorp J, Hol EM. GFAP in health and disease. Prog Neurobiol 2011; 93: 421–43.
44. Tong J, Ang L-C, Williams B, Furukawa Y, Fitzmaurice P, Guttman M, Boileau I, Hornykiewicz O et al. Low levels of astroglial markers in Parkinson's disease: relationship to α-synuclein accumulation. Neurobiol Dis 2015; 82: 243–53.
45. Newcombe J, Woodroofe MN, Cuzner ML. Distribution of glial fibrillary acidic protein in gliosed human white matter. J Neurochem 1986; 47: 1713–9.
46. Ruhl A, Franzke S, Collins SM, Stremmel W. Interleukin-6 expression and regulation in rat enteric glial cells. Am J Physiol Gastrointest Liver Physiol 2001; 280: G1163–71.
47. Gerhard A, Pavese N, Hotton G, Turkheimer F, Es M, Hammers A, Eggert K, Oertel W et al. In vivo imaging of microglial activation with [11C](R)-PK11195 PET in idiopathic Parkinson's disease. Neurobiol Dis 2006; 21: 404–12.
48. Wakabayashi K, Mori F, Tanji K, Orimo S, Takahashi H. Involvement of the peripheral nervous system in synucleinopathies, tauopathies and other neurodegenerative proteinopathies of the brain. Acta Neuropathol 2010; 120: 1–12.
49. Paillusson S, Clairembault T, Biraud M, Neunlist M, Derkinderen P. Activity-dependent secretion of alpha-synuclein by enteric neurons. J Neurochem 2012; 125: 512–7.
50. Lee H-J, Suk J-E, Patrick C, Bae EJ, Cho JH, Rho S, Hwang D, Masliah E et al. Direct transfer of alpha-synuclein from neuron to astroglia causes inflammatory responses in synucleinopathies. J Biol Chem 2010; 285: 9262–72.
51. Neunlist M, Toumi F, Oreschkova T, Denis M, Leborgne J, Laboisse CL, Galmiche JP, Jarry A. Human ENS regulates the intestinal epithelial barrier permeability and a tight junction-associated protein ZO-1 via VIPergic pathways. Am J Physiol Gastrointest Liver Physiol 2003; 285: G1028–36.
52. Bush TG, Savidge TC, Freeman TC, Cox HJ, Campbell EA, Mucke L, Johnson MH, Sofroniew MV. Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 1998; 93: 189–201.
53. Aube AC, Cabarrocas J, Bauer J, Philippe D, Aubert P, Doulay F, Liblau R, Galmiche JP et al. Changes in enteric neurone phenotype and intestinal functions in a transgenic mouse model of enteric glia disruption. Gut 2006; 55: 630–7.
54. Braak H, de Vos RA, Bohl J, Del Tredici K. 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: 67–72.
55. Davies KN, King D, Billington D, Barrett JA. Intestinal permeability and orocaecal transit time in elderly patients with Parkinson's disease. Postgrad Med J 1996; 72: 164–7.
56. Salat-Foix D, Tran K, Ranawaya R, Meddings J, Suchowersky O. Increased intestinal permeability and Parkinson disease patients: chicken or egg? Can J Neurol Sci 2012; 39: 185–8.
57. Forsyth CB, Shannon KM, Kordower JH, Voigt RM, Shaikh M, Jaglin JA, Estes JD, Dodiya HB et al. Increased intestinal permeability correlates with sigmoid mucosa alpha-synuclein staining and endotoxin exposure markers in early Parkinson's disease. PLoS ONE 2011; 6: e28032.
58. Savica R, Rocca WA, Ahlskog JE. When does Parkinson disease start? Arch Neurol 2010; 67: 798–801.
59. Marek K, Jennings D, Tamagnan G, Seibyl J. Biomarkers for Parkinson's [corrected] disease: tools to assess Parkinson's disease onset and progression. Ann Neurol 2008; 64 (Suppl. 2): S111–21.
60. Parkinson Progression Marker Initiative. The Parkinson Progression Marker Initiative (PPMI). Prog Neurobiol 2011; 95: 629–35.
61. Eberling JL, Dave KD, Frasier MA. α-synuclein imaging: a critical need for Parkinson's disease research. J Parkinsons Dis 2013; 3: 565–7.
62. Kang J-H, Irwin DJ, Chen-Plotkin AS, Siderowf A, Caspell C, Coffey CS, Waligórska T, Taylor P et al. Association of cerebrospinal fluid β-amyloid 1-42, T-tau, P-tau181, and α-synuclein levels with clinical features of drug-naive patients with early Parkinson disease. JAMA Neurol 2013; 70: 1277–87.
63. Bloch A, Probst A, Bissig H, Adams H, Tolnay M. Alpha-synuclein pathology of the spinal and peripheral autonomic nervous system in neurologically unimpaired elderly subjects. Neuropathol Appl Neurobiol 2006; 32: 284–95.
64. Del Tredici K, Hawkes CH, Ghebremedhin E, Braak H. Lewy pathology in the submandibular gland of individuals with incidental Lewy body disease and sporadic Parkinson's disease. Acta Neuropathol 2009; 119: 703–13.
65. Beach TG, Adler CH, Dugger BN, Serrano G, Hidalgo J, Henry-Watson J, Shill HA, Sue LI et al. Submandibular gland biopsy for the diagnosis of Parkinson disease. J Neuropathol Exp Neurol 2013; 72: 130–6.
66. Adler CH, Dugger BN, Hinni ML, Lott DG, Driver-Dunckley E, Hidalgo J, Henry-Watson J, Serrano G et al. Submandibular gland needle biopsy for the diagnosis of Parkinson disease. Neurology 2014; 82: 858–64.
67. Zange L, Noack C, Hahn K, Stenzel W, Lipp A. Phosphorylated α-synuclein in skin nerve fibres differentiates Parkinson's disease from multiple system atrophy. Brain 2015; 138 (Pt 8): 2310–21.
68. Benarroch EE. Enteric nervous system: functional organization and neurologic implications. Neurology 2007; 69: 1953–7.
69. Buhner S, Li Q, Vignali S, Barbara G, De Giorgio R, Stanghellini V, Cremon C, Zeller F et al. Activation of human enteric neurons by supernatants of colonic biopsy specimens from patients with irritable bowel syndrome. Gastroenterology 2009; 137: 1425–34.
70. Camilleri M, Carlson P, Acosta A, Busciglio I, Nair AA, Gibbons SJ, Farrugia G, Klee EW. RNA sequencing shows transcriptomic changes in rectosigmoid mucosa in patients with irritable bowel syndrome-diarrhea: a pilot case-control study. Am J Physiol Gastrointest Liver Physiol 2014; 306: G1089–98.
71. Mogi M, Harada M, Kondo T, Riederer P, Inagaki H, Minami M, Nagatsu T. Interleukin-1 beta, interleukin-6, epidermal growth factor and transforming growth factor-alpha are elevated in the brain from parkinsonian patients. Neurosci Lett 1994; 180: 147–50.
72. Mogi M, Harada M, Riederer P, Narabayashi H, Fujita K, Nagatsu T. Tumor necrosis factor-alpha (TNF-alpha) increases both in the brain and in the cerebrospinal fluid from parkinsonian patients. Neurosci Lett 1994; 165: 208–10.
73. Gray MT, Woulfe JM. Striatal blood-brain barrier permeability in Parkinson's disease. J Cereb Blood Flow Metab 2015; 35: 747–50.
74. Gatto NM, Frucht H, Sundararajan V, Jacobson JS, Grann VR, Neugut AI. Risk of perforation after colonoscopy and sigmoidoscopy: a population-based study. J Natl Cancer Inst 2003; 95: 230–6.
75. Friedrich K, Scholl SG, Beck S, Gotthardt D, Stremmel W, Rex DK; bng-Study-Group, Sieg A. Respiratory complications in outpatient endoscopy with endoscopist-directed sedation. J Gastrointestin Liver Dis 2014; 23: 255–9.