Accumulation of α-synuclein in the bowel of patients in the pre-clinical phase of Parkinson's disease

Acta Neuropathologica

Volumn 127, Issue 2, 2014, Pages 235-241

  Hilton, David ^a   Stephens, Madeleine ^a   Kirk, Leanne ^a   Edwards, Philip ^a   Potter, Ross ^a   Zajicek, John ^b   Broughton, Ellie ^a   Hagan, Hannah ^a   Carroll, Camille ^b  

^a DERRIFORD HOSPITAL   (United Kingdom)

^b PLYMOUTH UNIVERSITY PENINSULA SCHOOLS OF MEDICINE AND DENTISTRY   (United Kingdom)

Author keywords

synuclein; Bowel; Parkinson's disease; Pre clinical

Indexed keywords

ALPHA SYNUCLEIN;

ADULT; AGED; ARTICLE; COLON BIOPSY; CONTROLLED STUDY; ESOPHAGUS; GALLBLADDER; GANGLION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTESTINE; LARGE INTESTINE; MAJOR CLINICAL STUDY; MIDDLE AGED; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SMALL INTESTINE; STOMACH; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ALPHA-SYNUCLEIN; ASYMPTOMATIC DISEASES; BIOLOGICAL MARKERS; BIOPSY; CASE-CONTROL STUDIES; HUMANS; INTESTINES; MIDDLE AGED; NERVE FIBERS; PARKINSON DISEASE; SENSITIVITY AND SPECIFICITY;

EID: 84896717250     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-013-1214-6     Document Type: Article

References (44)

1. Abbott RD, Petrovitch H, White LR et al (2001) Frequency of bowel movements and the future risk of Parkinson's disease. Neurology 57:456-462
2. Anderson G, Noorian AR, Taylor G et al (2007) Loss of enteric dopaminergic neurons and associated changes in colon motility in an MPTP mouse model of Parkinson's disease. Exp Neurol 207:4-12
3. Annerino DM, Arshad S, Taylor GM, Adler CH, Beach TG, Greene JG (2012) Parkinson's disease is not associated with gastrointestinal myenteric ganglion neuron loss. Acta Neuropathol 124:665-680
4. Beach TG, Adler CH, Dugger BN et al (2013) Submandibular gland biopsy for the diagnosis of Parkinson disease. J Neuropathol Exp Neurol 72:130-136
5. 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
6. Bloch A, Probst A, Bissig H, Adams H, Tolnay M (2006) Alpha-synuclein pathology of the spinal and peripheral autonomic nervous system in neurologically unimpaired elderly subjects. Neuropathol Appl Neurobiol 32:284-295
7. Böttner M, Zorenkov D, Hellwig I et al (2012) Expression pattern and localization of alpha-synuclein in the human enteric nervous system. Neurobiol Dis 48:474-480
8. Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 24:197-211
9. Cersosimo MG, Benarroch EE (2012) Autonomic involvement in Parkinson's disease: pathology, pathophysiology, clinical features and possible peripheral biomarkers. J Neurol Sci 313:57-63
10. Cersosimo MG, Benarroch EE (2012) Pathological correlates of gastrointestinal dysfunction in Parkinson's disease. Neurobiol Dis 46:559-564
11. Dorsey ER, Constantinescu R, Thompson JP et al (2007) Projected number of people with Parkinson disease in the most populous nations, 2005 through 2030. Neurology 68:384-386
12. Fumimura Y, Ikemura M, Saito Y et al (2007) Analysis of the adrenal gland is useful for evaluating pathology of the peripheral autonomic nervous system in lewy body disease. J Neuropathol Exp Neurol 66:354-362
13. George S, Rey NL, Reichenbach N, Steiner JA, Brundin P (2013) Alpha-synuclein: the long distance runner. Brain Pathol 23:350-357
14. Gold A, Turkalp ZT, Munoz DG (2013) Enteric alpha-synuclein expression is increased in Parkinson's disease but not Alzheimer's disease. Mov Disord 28:237-240
15. Greene JG, Noorian AR, Srinivasan S (2009) Delayed gastric emptying and enteric nervous system dysfunction in the rotenone model of Parkinson's disease. Exp Neurol 218:154-161
16. Hawkes CH, Del Tredici K, Braak H (2007) Parkinson's disease: a dual-hit hypothesis. Neuropathol Appl Neurobiol 33:599-614
17. Hawkes CH, Del Tredici K, Braak H (2009) Parkinson's disease: the dual hit theory revisited. Ann N Y Acad Sci 1170:615-622
18. Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181-184
19. Ikemura M, Saito Y, Sengoku R et al (2008) Lewy body pathology involves cutaneous nerves. J Neuropathol Exp Neurol 67:945-953
20. Jost WH (2010) Gastrointestinal dysfunction in Parkinson's disease. J Neurol Sci 289:69-73
21. Jost WH, Eckardt VF (2003) Constipation in idiopathic Parkinson's disease. Scand J Gastroenterol 38:681-686
22. Lebouvier T, Chaumette T, Damier P et al (2008) Pathological lesions in colonic biopsies during Parkinson's disease. Gut 57:1741-1743
23. Lebouvier T, Neunlist M, des Varannes Bruley S et al (2010) Colonic biopsies to assess the neuropathology of Parkinson's disease and its relationship with symptoms. PLoS One 5:e12728
24. Lees AJ, Hardy J, Revesz T (2009) Parkinson's disease. Lancet 373:2055-2066
25. Lim SY, Fox SH, Lang AE (2009) Overview of the extranigral aspects of Parkinson disease. Arch Neurol 66:167-172
26. MacKenzie JM, Dixon MF (1987) An immunohistochemical study of the enteric neural plexi in Hirschsprung's disease. Histopathology 11:1055-1066
27. Miki Y, Tomiyama M, Ueno T et al (2010) Clinical availability of skin biopsy in the diagnosis of Parkinson's disease. Neurosci Lett 469:357-359
28. Minguez-Castellanos A, Chamorro CE, Escamilla-Sevilla F et al (2007) Do alpha-synuclein aggregates in autonomic plexuses predate Lewy body disorders?: a cohort study. Neurology 68:2012-2018
29. Mu L, Sobotka S, Chen J et al (2013) Alpha-synuclein pathology and axonal degeneration of the peripheral motor nerves innervating pharyngeal muscles in Parkinson disease. J Neuropathol Exp Neurol 72:119-129
30. Mu L, Sobotka S, Chen J et al (2013) Parkinson disease affects peripheral sensory nerves in the pharynx. J Neuropathol Exp Neurol 72:614-623
31. Nussbaum RL, Ellis CE (2003) Alzheimer's disease and Parkinson's disease. N Engl J Med 348:1356-1364
32. Orimo S, Uchihara T, Nakamura A et al (2008) Axonal alpha-synuclein aggregates herald centripetal degeneration of cardiac sympathetic nerve in Parkinson's disease. Brain 131:642-650
33. Pan-Montojo F, Anichtchik O, Dening Y et al (2010) Progression of Parkinson's disease pathology is reproduced by intragastric administration of rotenone in mice. PLoS ONE 5:e8762
34. Pan-Montojo F, Schwarz M, Winkler C et al (2012) Environmental toxins trigger PD-like progression via increased alpha-synuclein release from enteric neurons in mice. Sci Rep 2:898
35. Pfeiffer RF (2003) Gastrointestinal dysfunction in Parkinson's disease. Lancet Neurol 2:107-116
36. Pouclet H, Lebouvier T, Coron E et al (2012) A comparison between rectal and colonic biopsies to detect Lewy pathology in Parkinson's disease. Neurobiol Dis 45:305-309
37. Shannon KM, Keshavarzian A, Dodiya HB, Jakate S, Kordower JH (2012) Is alpha-synuclein in the colon a biomarker for premotor Parkinson's disease? Evidence from 3 cases. Mov Disord 27:716-719
38. Shannon KM, Keshavarzian A, Mutlu E et al (2012) Alpha-synuclein in colonic submucosa in early untreated Parkinson's disease. Mov Disord 27:709-715
39. Singaram C, Ashraf W, Gaumnitz EA et al (1995) Dopaminergic defect of enteric nervous system in Parkinson's disease patients with chronic constipation. Lancet 346:861-864
40. Tasselli M, Chaumette T, Paillusson S et al (2013) Effects of oral administration of rotenone on gastrointestinal functions in mice. Neurogastroenterol Motil 25:e183-e193
41. Ueki A, Otsuka M (2004) Life style risks of Parkinson's disease: association between decreased water intake and constipation. J Neurol 251(Suppl 7):vII18-vII23
42. Verbaan D, Marinus J, Visser M, van Rooden SM, Stiggelbout AM, van Hilten JJ (2007) Patient-reported autonomic symptoms in Parkinson disease. Neurology 69:333-341
43. Wakabayashi K, Takahashi H, Takeda S, Ohama E, Ikuta F (1988) Parkinson's disease: the presence of Lewy bodies in Auerbach's and Meissner's plexuses. Acta Neuropathol 76:217-221
44. Witt M, Bormann K, Gudziol V et al (2009) Biopsies of olfactory epithelium in patients with Parkinson's disease. Mov Disord 24:906-914