Parkinson's disease is not associated with gastrointestinal myenteric ganglion neuron loss

Acta Neuropathologica

Volumn 124, Issue 5, 2012, Pages 665-680

  Annerino, Dana M ^a   Arshad, Shawn ^a   Taylor, Georgia M ^a   Adler, Charles H ^b   Beach, Thomas G ^c   Greene, James G ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MAYO CLINIC   (United States)

^c SUN HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

Acetylcholine; Catecholamine; Constipation; Enteric; Gastrointestinal; Gastroparesis; Lewy body; Nitric oxide; Synuclein; Vasoactive intestinal peptide

Indexed keywords

NITRIC OXIDE SYNTHASE; TYROSINE 3 MONOOXYGENASE; VASOACTIVE INTESTINAL POLYPEPTIDE;

AGED; ARTICLE; AUTOPSY; CELL DENSITY; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GASTROINTESTINAL MOTILITY DISORDER; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREACTIVITY; INTESTINE INNERVATION; LEWY BODY; MALE; MOTONEURON NUCLEUS; MYENTERIC PLEXUS; NERVE CELL LESION; NEUROPATHOLOGY; PARASYMPATHETIC INNERVATION; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; SYMPATHETIC INNERVATION; VAGUS NERVE;

AGED; AGED, 80 AND OVER; ALPHA-SYNUCLEIN; CATECHOLAMINES; CELL COUNT; ENTERIC NERVOUS SYSTEM; FEMALE; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; LEWY BODIES; MALE; MYENTERIC PLEXUS; NERVE TISSUE PROTEINS; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; PARKINSON DISEASE; TYROSINE 3-MONOOXYGENASE; VASOACTIVE INTESTINAL PEPTIDE;

EID: 84871028956     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-012-1040-2     Document Type: Article

References (58)

1. Abbott RD, Petrovitch H, White LR, Masaki KH, Tanner CM, Curb JD, Grandinetti A, Blanchette PL, Popper JS, Ross GW (2001) Frequency of bowel movements and the future risk of Parkinson's disease. Neurology 57(3):456-462
2. Anderson G, Noorian AR, Taylor G, Anitha M, Bernhard D, Srinivasan S, Greene JG (2007) Loss of enteric dopaminergic neurons and associated changes in colon motility in an MPTP mouse model of Parkinson's disease. Exp Neurol 207(1):4-12
3. Anlauf M, Schafer MK, Eiden L, Weihe E (2003) Chemical coding of the human gastrointestinal nervous system: cholinergic, VIPergic, and catecholaminergic phenotypes. J Comp Neurol 459(1):90-111
4. Ashraf W, Wszolek ZK, Pfeiffer RF, Normand M, Maurer K, Srb F, Edwards LL, Quigley EM (1995) Anorectal function in fluctuating (on-off) Parkinson's disease: evaluation by combined anorectal manometry and electromyography. Mov Disord 10(5):650-657
5. Aube AC, Cabarrocas J, Bauer J, Philippe D, Aubert P, Doulay F, Liblau R, Galmiche JP, Neunlist M (2006) Changes in enteric neurone phenotype and intestinal functions in a transgenic mouse model of enteric glia disruption. Gut 55(5):630-637. doi: 10.1136/gut.2005.067595
6. Beach TG, Adler CH, Sue LI, Vedders L, Lue L, White Iii CL, Akiyama H, Caviness JN, Shill HA, Sabbagh MN, Walker DG (2010) Multi-organ distribution of phosphorylated alpha-synuclein histopathology in subjects with Lewy body disorders. Acta Neuropathol 119(6):689-702
7. Beach TG, White CL, Hamilton RL, Duda JE, Iwatsubo T, Dickson DW, Leverenz JB, Roncaroli F, Buttini M, Hladik CL, Sue LI, Noorigian JV, Adler CH (2008) Evaluation of alphasynuclein immunohistochemical methods used by invited experts. Acta Neuropathol 116(3):277-288
8. Belai A, Burnstock G (1999) Distribution and colocalization of nitric oxide synthase and calretinin in myenteric neurons of developing, aging, and Crohn's disease human small intestine. Dig Dis Sci 44(8):1579-1587
9. Bernard CE, Gibbons SJ, Gomez-Pinilla PJ, Lurken MS, Schmalz PF, Roeder JL, Linden D, Cima RR, Dozois EJ, Larson DW, Camilleri M, Zinsmeister AR, Pozo MJ, Hicks GA, Farrugia G (2009) Effect of age on the enteric nervous system of the human colon. Neurogastroenterol Motil 21(7):746-e46
10. Bernardini N, Segnani C, Ippolito C, De Giorgio R, Colucci R, Faussone-Pellegrini MS, Chiarugi M, Campani D, Castagna M, Mattii L, Blandizzi C, Dolfi A (2012) Immunohistochemical analysis of myenteric ganglia and interstitial cells of Cajal in ulcerative colitis. J Cell Mol Med 16(2):318-327. doi:10.1111/j.1582-4934.2011.01298.x
11. Braak H, de Vos RA, Bohl J, Del Tredici K (2006) Gastric alphasynuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology. Neurosci Lett 396(1):67-72
12. Brehmer A, Schrodl F, Neuhuber W (2006) Morphology of VIP/ nNOS-immunoreactive myenteric neurons in the human gut. Histochem Cell Biol 125(5):557-565
13. Derkinderen P, Rouaud T, Lebouvier T, Bruley des Varannes S, Neunlist M, De Giorgio R (2011) Parkinson disease: the enteric nervous system spills its guts. Neurology 77(19):1761-1767. doi: 10.1212/WNL.0b013e318236ef60
14. Djaldetti R, Ziv I, Melamed E (1996) Impaired absorption of oral levodopa: a major cause for response fluctuations in Parkinson's disease. Isr J Med Sci 32(12):1224-1227
15. Edwards LL, Quigley EM, Pfeiffer RF (1992) Gastrointestinal dysfunction in Parkinson's disease: frequency and pathophysiology. Neurology 42(4):726-732
16. Ekblad E, Alm P, Sundler F (1994) Distribution, origin and projections of nitric oxide synthase-containing neurons in gut and pancreas. Neuroscience 63(1):233-248
17. Ekblad E, Mulder H, Uddman R, Sundler F (1994) NOS-containing neurons in the rat gut and coeliac ganglia. Neuropharmacology 33(11):1323-1331
18. Forsyth CB, Shannon KM, Kordower JH, Voigt RM, Shaikh M, Jaglin JA, Estes JD, Dodiya HB, Keshavarzian A (2011) Increased intestinal permeability correlates with sigmoid mucosa alpha-synuclein staining and endotoxin exposure markers in early Parkinson's disease. PLoS ONE 6(12):e28032. doi:10.1371/journal.pone.0028032
19. Furness JB (2006) The enteric nervous system. Blackwell, Malden
20. Ganns D, Schrodl F, Neuhuber W, Brehmer A (2006) Investigation of general and cytoskeletal markers to estimate numbers and proportions of neurons in the human intestine. Histol Histopathol 21(1):41-51
21. Goetze O, Nikodem AB, Wiezcorek J, Banasch M, Przuntek H, Mueller T, Schmidt WE, Woitalla D (2006) Predictors of gastric emptying in Parkinson's disease. Neurogastroenterol Motil 18(5):369-375
22. Goetze O, Wieczorek J, Mueller T, Przuntek H, Schmidt WE, Woitalla D (2005) Impaired gastric emptying of a solid test meal in patients with Parkinson's disease using 13C-sodium octanoate breath test. Neurosci Lett 375(3):170-173
23. 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(1):154-161
24. Hanani M, Fellig Y, Udassin R, Freund HR (2004) Age-related changes in the morphology of the myenteric plexus of the human colon. Auton Neurosci 113(1-2):71-78. doi:10.1016/j.autneu.2004.05.007
25. Hoff S, Zeller F, von Weyhern CW, Wegner M, Schemann M, Michel K, Ruhl A (2008) Quantitative assessment of glial cells in the human and guinea pig enteric nervous system with an anti- Sox8/9/10 antibody. J Comp Neurol 509(4):356-371
26. Ippolito C, Segnani C, De Giorgio R, Blandizzi C, Mattii L, Castagna M, Moscato S, Dolfi A, Bernardini N (2009) Quantitative evaluation of myenteric ganglion cells in normal human left colon: implications for histopathological analysis. Cell Tissue Res 336(2):191-201
27. Irwin DA (1931) The anatomy of Auerbach's plexus. Am J Anat 49:141-166
28. Johnson LR (2001) Gastrointestinal physiology. The Mosby Physiology Monograph Series, 6th edn. Mosby, Inc., St. Louis
29. Kupsky WJ, Grimes MM, Sweeting J, Bertsch R, Cote LJ (1987) Parkinson's disease and megacolon: concentric hyaline inclusions (Lewy bodies) in enteric ganglion cells. Neurology 37(7):1253-1255
30. Kurlan R, Rothfield KP, Woodward WR, Nutt JG, Miller C, Lichter D, Shoulson I (1988) Erratic gastric emptying of levodopa may cause "random" fluctuations of parkinsonian mobility. Neurology 38(3):419-421
31. Lebouvier T, Chaumette T, Damier P, Coron E, Touchefeu Y, Vrignaud S, Naveilhan P, Galmiche JP, Bruley des Varannes S, Derkinderen P, Neunlist M (2008) Pathological lesions in colonic biopsies during Parkinson's disease. Gut 57(12):1741-1743
32. Lebouvier T, Chaumette T, Paillusson S, Duyckaerts C, Bruley des Varannes S, Neunlist M, Derkinderen P (2009) The second brain and Parkinson's disease. Eur J Neurosci 30(5):735-741
33. Lebouvier T, Neunlist M, Bruley des Varannes S, Coron E, Drouard A, N'Guyen JM, Chaumette T, Tasselli M, Paillusson S, Flamand M, Galmiche JP, Damier P, Derkinderen P (2010) Colonic biopsies to assess the neuropathology of Parkinson's disease and its relationship with symptoms. PLoS ONE 5(9):e12728
34. Li ZS, Pham TD, Tamir H, Chen JJ, Gershon MD (2004) Enteric dopaminergic neurons: definition, developmental lineage, and effects of extrinsic denervation. J Neurosci 24(6):1330-1339
35. Murphy EM, Defontgalland D, Costa M, Brookes SJ, Wattchow DA (2007) Quantification of subclasses of human colonic myenteric neurons by immunoreactivity to Hu, choline acetyltransferase and nitric oxide synthase. Neurogastroenterol Motil 19(2):126-134
36. Neunlist M, Aubert P, Toquet C, Oreshkova T, Barouk J, Lehur PA, Schemann M, Galmiche JP (2003) Changes in chemical coding of myenteric neurones in ulcerative colitis. Gut 52(1):84-90
37. Neunlist M, Coquenlorge S, Aubert P, Duchalais-Dassonneville E, des Varannes SB, Meurette G, Coron E (2011) Colonic endoscopic full-thickness biopsies: from the neuropathological analysis of the myenteric plexus to the functional study of neuromuscular transmission. Gastrointest Endosc 73(5):1029-1034. doi:10.1016/j.gie.2011.01.041
38. Noorian AR, Taylor GM, Annerino DM, Greene JG (2011) Neurochemical phenotypes of myenteric neurons in the rhesus monkey. J Comp Neurol 519(17):3387-3401
39. Orimo S, Uchihara T, Nakamura A, Mori F, Kakita A, Wakabayashi K, Takahashi H (2008) Axonal alpha-synuclein aggregates herald centripetal degeneration of cardiac sympathetic nerve in Parkinson's disease. Brain 131(Pt 3):642-650
40. Pascale A, Gusev PA,Amadio M, Dottorini T, Govoni S, Alkon DL, Quattrone A (2004) Increase of the RNA-binding protein HuD and posttranscriptional up-regulation of the GAP-43 gene during spatial memory. Proc Nat Acad Sci USA 101(5):1217-1222
41. Pfeiffer RF (2003) Gastrointestinal dysfunction in Parkinson's disease. Lancet Neurol 2(2):107-116
42. Pfeiffer RF, Quigley EM (1999) Gastrointestinal motility problems in patients with Parkinson's disease: epidemiology, pathophysiology, and guidelines for management. CNS Drugs 11:435-448
43. Phillips RJ, Hargrave SL, Rhodes BS, Zopf DA, Powley TL (2004) Quantification of neurons in the myenteric plexus: an evaluation of putative pan-neuronal markers. J Neurosci Methods 133(1-2):99-107
44. Pimont S, Bruley Des Varannes S, Le Neel JC, Aubert P, Galmiche JP, Neunlist M (2003) Neurochemical coding of myenteric neurones in the human gastric fundus. Neurogastroenterol Motil 15(6):655-662
45. Porter AJ, Wattchow DA, Brookes SJ, Costa M (1997) The neurochemical coding and projections of circular muscle motor neurons in the human colon. Gastroenterology 113(6):1916-1923
46. Porter AJ, Wattchow DA, Brookes SJ, Costa M (2002) Cholinergic and nitrergic interneurones in the myenteric plexus of the human colon. Gut 51(1):70-75
47. Pouclet H, Lebouvier T, Coron E, Neunlist M, Derkinderen P (2012) Lewy pathology in gastric and duodenal biopsies in Parkinson's disease. Mov Disord 27(6):708. doi:10.1002/mds.24993
48. Qu ZD, Thacker M, Castelucci P, Bagyanszki M, Epstein ML, Furness JB (2008) Immunohistochemical analysis of neuron types in the mouse small intestine. Cell Tissue Res 334(2):147-161
49. Shannon KM, Keshavarzian A, Mutlu E, Dodiya HB, Daian D, Jaglin JA, Kordower JH (2012) Alpha-synuclein in colonic submucosa in early untreated Parkinson's disease. Mov Disord 27(6):709-715
50. Singaram C, Ashraf W, Gaumnitz EA, Torbey C, Sengupta A, Pfeiffer R, Quigley EM (1995) Dopaminergic defect of enteric nervous system in Parkinson's disease patients with chronic constipation. Lancet 346(8979):861-864
51. Ueki A, Otsuka M, Otsuka M (2004) Life style risks of Parkinson's disease: association between decreased water intake and constipation. J Neurol 251(Suppl 7):vII18-vII23
52. Wakabayashi K, Mori F, Tanji K, Orimo S, Takahashi H (2010) Involvement of the peripheral nervous system in synucleinopathies, tauopathies and other neurodegenerative proteinopathies of the brain. Acta Neuropathol 120(1):1-12
53. Wakabayashi K, Takahashi H, Ohama E, Ikuta F (1989) Tyrosine hydroxylase-immunoreactive intrinsic neurons in the Auerbach's and Meissner's plexuses of humans. Neurosci Lett 96(3):259-263
54. Wakabayashi K, Takahashi H, Ohama E, Ikuta F (1990) Parkinson's disease: an immunohistochemical study of Lewy body-containing neurons in the enteric nervous system. Acta Neuropathol 79:581-583
55. 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(3):217-221
56. Wakabayashi K, Takahashi H, Takeda S, Ohama E, Ikuta F (1989) Lewy bodies in the enteric nervous system in Parkinson's disease. Arch Histol Cytol 52(Suppl):191-194
57. Wedel T, Busing V, Heinrichs G, Nohroudi K, Bruch HP, Roblick UJ, Bottner M (2010) Diverticular disease is associated with an enteric neuropathy as revealed by morphometric analysis. Neurogastroenterol Motil 22(4):407-414 (e93-4). doi:10.1111/j.1365-2982.2009.01445.x
58. Wedel T, Roblick U, Gleiss J, Schiedeck T, Bruch HP, Kuhnel W, Krammer HJ (1999) Organization of the enteric nervous system in the human colon demonstrated by wholemount immunohistochemistry with special reference to the submucous plexus. Ann Anat 181(4):327-337