Intestinal dysmotility and enteric neurochemical changes in a Parkinson's disease rat model

Autonomic Neuroscience: Basic and Clinical

Volumn 169, Issue 2, 2012, Pages 77-86

  Colucci, Mario ^a   Cervio, Marila ^a   Faniglione, Marisa ^a   De Angelis, Stefano ^a   Pajoro, Massimo ^b   Levandis, Giovanna ^c   Tassorelli, Cristina ^a,c   Blandini, Fabio ^a,c   Feletti, Fausto ^a   De Giorgio, Roberto ^d   Dellabianca, Antonio ^a   Tonini, Stefano ^a   Tonini, Marcello ^a  

^a UNIVERSITY OF PAVIA   (Italy)

^b ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLA LOMBARDIA E DELL EMILIA ROMAGNA   (Italy)

^c C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

^d UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

D2 receptor; Enteric nervous system; Gut dysfunction; Neurochemical plasticity; Parkinson's disease

Indexed keywords

CHOLINE ACETYLTRANSFERASE; NEURONAL NITRIC OXIDE SYNTHASE; OXIDOPAMINE; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SUBPOPULATION; COLON; CONSTIPATION; CONTROLLED STUDY; DISEASE SEVERITY; DOPAMINERGIC NERVE CELL; ILEUM; INTESTINE MOTILITY; INTESTINE PRESSURE; MALE; MYENTERIC PLEXUS; NERVE CELL PLASTICITY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEREOTACTIC TREATMENT; TISSUE SECTION;

ANIMALS; CHOLINE O-ACETYLTRANSFERASE; COLON; DISEASE MODELS, ANIMAL; ENTERIC NERVOUS SYSTEM; GASTROINTESTINAL MOTILITY; ILEUM; INTESTINE, SMALL; MALE; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; PARKINSON DISEASE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84863860708     PISSN: 15660702     EISSN: 18727484     Source Type: Journal    
DOI: 10.1016/j.autneu.2012.04.005     Document Type: Article

References (62)

1. Abbott R.D., Petrovitch H., White L.R., Masaki K.H., Tanner C.M., Curb J.D., Grandinetti A., Blanchette P.L., Popper J.S., Ross G.W. Frequency of bowel movements and the future risk of Parkinson's disease. Neurology 2001, 57:456-462.
2. Anderson G., Noorian A.R., Taylor G., Anitha M., Bernhard D., Srinivasan S., Greene J.G. Loss of enteric dopaminergic neurons and associated changes in colon motility in an MPTP mouse model of Parkinson's disease. Exp. Neurol. 2007, 207:4-12.
3. Banach T., Urowski D., Gil K., Krygowska-Wajs A., Marszalek A., Thor P.J. Peripheral mechanisms of intestinal dysmotility in rats with salsolinol induced experimental Parkinson's disease. J. Physiol. Pharmacol. 2006, 57:291-300.
4. Belai A., Boulos P.B., Robson T., Burnstock G. Neurochemical coding in the small intestine of patients with Crohn's disease. Gut 1997, 40:767-774.
5. Benarroch E.E. Enteric nervous system: functional organization and neurologic implications. Neurology 2007, 69:1953-1957.
6. Benarroch E.E., Schmeichel A.M., Sandroni P., Low P.A., Parisi J.E. Involvement of vagal autonomic nuclei in multiple system atrophy and Lewy body disease. Neurology 2006, 66:378-383.
7. Berthoud H.R., Carlson N.R., Powley T.L. Topography of efferent vagal innervation of the rat gastrointestinal tract. Am. J. Physiol. 1991, 260:R200-R207.
8. Blandini F., Armentero M.T., Fancellu R., Blaugrund E., Nappi G. Neuroprotective effect of rasagiline in a rodent model of Parkinson's disease. Exp. Neurol. 2004, 187:455-459.
9. Blandini F., Balestra B., Levandis G., Cervio M., Greco R., Tassorelli C., Colucci M., Faniglione M., Bazzini E., Nappi G., Clavenzani P., Vigneri S., De Giorgio R., Tonini M. Functional and neurochemical changes of the gastrointestinal tract in a rodent model of Parkinson's disease. Neurosci. Lett. 2009, 467:203-207.
10. Braak H., Del Tredici K., Rüb U., de Vos R.A., Jansen Steur E.N., Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 2003, 24:197-211.
11. Braak H., Ghebremedhin E., Rüb U., Bratzke H., Del Tredici K. Stages in the development of Parkinson's disease-related pathology. Cell Tissue Res. 2004, 318:121-134.
12. Buchwalow I.B., Minin E.A., Samoilova V.E., Boecker W., Wellner M., Schmitz W., Neumann J., Punkt K. Compartmentalization of NO signaling cascade in skeletal muscles. Biochem. Biophys. Res. Commun. 2005, 330:615-621.
13. Caiazzo M., Dell'Anno M.T., Dvoretskova E., Lazarevic D., Taverna S., Leo D., Sotnikova T.D., Menegon A., Roncaglia P., Colciago G., Russo G., Carninci P., Pezzoli G., Gainetdinov R.R., Gustincich S., Dityatev A., Broccoli V. Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature 2011, 476:224-227.
14. Chaumette T., Lebouvier T., Aubert P., Lardeux B., Qin C., Li Q., Accary D., Bézard E., Bruley des Varannes S., P.Derkinderen, Neunlist M. Neurochemical plasticity in the enteric nervous system of a primate animal model of experimental Parkinsonism. Neurogastroenterol. Motil. 2009, 21:215-222.
15. de Vries P., Soret R., Suply E., Heloury Y., Neunlist M. Postnatal development of myenteric neurochemical phenotype and impact on neuromuscular transmission in the rat colon. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G539-G547.
16. Drolet R.E., Cannon J.R., Montero L., Greenamyre J.T. Chronic rotenone exposure reproduces Parkinson's disease gastrointestinal neuropathology. Neurobiol. Dis. 2009, 36:96-102.
17. Dunning C.J., Reyes J.F., Steiner J.A., Brundin P. Can Parkinson's disease pathology be propagated from one neuron to another? 2011, Prog, Neurobiol, (Electronic publication ahead of print).
18. Ekblad E., Bauer A.J. Role of vasoactive intestinal peptide and inflammatory mediators in enteric neuronal plasticity. Neurogastroenterol. Motil. 2004, 16:123-128.
19. Ekblad E., Mulder H., Sundler F. Vasoactive intestinal peptide expression in enteric neurons is upregulated by both colchicine and axotomy. Regul. Pept. 1996, 63:113-121.
20. Ekblad E., Sjuve R., Arner A., Sundler F. Enteric neuronal plasticity and a reduced number of interstitial cells of Cajal in hypertrophic rat ileum. Gut 1998, 42:836-844.
21. El-Salhy M., Danielsson A., Axelsson H., Qian B.F. Neuroendocrine peptide levels in the gastrointestinal tract of mice after unilateral cervical vagotomy. Regul. Pept. 2000, 88:15-20.
22. Gao X., Chen H., Schwarzschild M.A., Ascherio A. A prospective study of bowel movement frequency and risk of Parkinson's disease. Am. J. Epidemiol. 2011, 174:546-551.
23. Greene J.G., Noorian A.R., Srinivasan S. Delayed gastric emptying and enteric nervous system dysfunction in the rotenone model of Parkinson's disease. Exp. Neurol. 2009, 218:154-161.
24. Hopkins D.A., Bieger D., deVente J., Steinbusch W.M. Vagal efferent projections: viscerotopy, neurochemistry and effects of vagotomy. Prog. Brain Res. 1996, 107:79-96.
25. Hyatt-Sachs H., Schreiber R.C., Bennett T.A., Zigmond R.E. Phenotypic plasticity in adult sympathetic ganglia in vivo: effects of deafferentation and axotomy on the expression of vasoactive intestinal peptide. J. Neurosci. 1993, 13:1642-1653.
26. Jost W.H. Gastrointestinal dysfunction in Parkinson's Disease. J. Neurol. Sci. 2010, 289:69-73.
27. Kadowaki M., Wang X.O., Shimatani H., Yoneda S., Takaki M. 5-HT4 receptor enhances the propulsive power of the peristaltic reflex in the rat distal colon. Auton. Neurosci. 2002, 99:62-65.
28. Kalaitzakis M.E., Graeber M.B., Gentleman S.M., Pearce R.K. The dorsal motor nucleus of the vagus is not an obligatory trigger site of Parkinson's disease: a critical analysis of alpha-synuclein staging. Neuropathol. Appl. Neurobiol. 2008, 34:284-295.
29. Kasparek M.S., Fatima J., Iqbal C.W., Duenes J.A., Sarr M.G. Age-related changes in functional NANC innervation with VIP and substance P in the jejunum of Lewis rats. Auton. Neurosci. 2009, 151:127-134.
30. Lebouvier T., Chaumette T., Paillusson S., Duyckaerts C., Bruley des Varannes S., Neunlist M., Derkinderen P. The second brain and Parkinson's disease. Eur. J. Neurosci. 2009, 30:735-741.
31. Lebouvier T., Neunlist M., Bruley des Varannes S., Coron E., Drouard A., N'Guyen J.M., Chaumette T., Tasselli M., Paillusson S., Flamand M., Galmiche J.P., Damier P., Derkinderen P. Colonic biopsies to assess the neuropathology of Parkinson's disease and its relationship with symptoms. PLoS One 2010, 5:e12728.
32. Li Z.S., Pham T.D., Tamir H., Chen J.J., Gershon M.D. Enteric dopaminergic neurons: definition, developmental lineage, and effects of extrinsic denervation. J. Neurosci. 2004, 24:1330-1339.
33. Li Z.S., Schmauss C., Cuenca A., Ratcliffe E., Gershon M.D. Physiological modulation of intestinal motility by enteric dopaminergic neurons and the D2 receptor: analysis of dopamine receptor expression, location, development, and function in wild-type and knock-out mice. J. Neurosci. 2006, 26:2798-2807.
34. Li Z., Chalazonitis A., Huang Y.Y., Mann J.J., Margolis K.G., Yang Q.M., Kim D.O., Côté F., Mallet J., Gershon M.D. Essential roles of enteric neuronal serotonin in gastrointestinal motility and the development/survival of enteric dopaminergic neurons. J. Neurosci. 2011, 31:8998-9009.
35. Lin Z., Sandgren K., Ekblad E. Increased expression of vasoactive intestinal polypeptide in cultured myenteric neurons from adult rat small intestine. Auton. Neurosci. 2003, 107:9-19.
36. Luck M.S., Dahl J.L., Boyeson M.G., Bass P. Neuroplasticity in the smooth muscle of the myenterically and extrinsically denervated rat jejunum. Cell Tissue Res. 1993, 271:363-374.
37. Marruchella G., Ligios C., Albanese V., Cancedda M.G., Madau L., Lalatta-Costerbosa G., Mazzoni M., Clavenzani P., Chiocchetti R., Sarli G., De Grossi L., Agrimi U., Aguzzi A., Di Guardo G. Enteroglial and neuronal involvement without apparent neuron loss in ileal enteric nervous system plexuses from scrapie-affected sheep. J. Gen. Virol. 2007, 88:2899-2904.
38. McKinney M., Jacksonville M.C. Brain cholinergic vulnerability: relevance to behavior and disease. Biochem. Pharmacol. 2005, 70:1115-1124.
39. Nakamura K., Takahashi T., Taniuchi M., Hsu C.X., Owyang C. Nicotinic receptor mediates nitric oxide synthase expression in the rat gastric myenteric plexus. J. Clin. Invest. 1998, 101:1479-1489.
40. Nakao K., Takahashi T., Utsunomiya J., Owyang C. Extrinsic neural control of nitric oxide synthase expression in the myenteric plexus of rat jejunum. J. Physiol. 1998, 507:549-560.
41. Natale G., Kastsiushenka O., Fulceri F., Ruggieri S., Paparelli A., Fornai F. MPTP-induced parkinsonism extends to a subclass of TH-positive neurons in the gut. Brain Res. 2010, 1355:195-206.
42. Pan-Montojo F., Anichtchik O., Dening Y., Knels L., Pursche S., Jung R., Jackson S., Gille G., Spillantini M.G., Reichmann H., Funk R.H. Progression of Parkinson's disease pathology is reproduced by intragastric administration of rotenone in mice. PLoS One 2010, 5:e8762.
43. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press, San Diego, USA. forth edn.
44. Phillips R.J., Powley T.L. Innervation of the gastrointestinal tract: patterns of aging. Auton. Neurosci. 2007, 136:1-19.
45. Phillips R.J., Hargrave S.L., Rhodes B.S., Zopf D.A., Powley T.L. Quantification of neurons in the myenteric plexus: an evaluation of putative pan-neuronal markers. J. Neurosci. Methods 2004, 133:99-107.
46. Poewe W. Non-motor symptoms in Parkinson's disease. Eur. J. Neurol. 2008, 15(Suppl. 1):14-20.
47. Pouclet H., Lebouvier T., Coron E., Bruley des Varannes S., 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, 45:305-309.
48. Powley T.L. Vagal input to the enteric nervous system. Gut 2000, 47:iv30-iv32.
49. Sjölund K., Fasth S., Ekman R., Hultén L., Jiborn H., Nordgren S., Sundler F. Neuropeptides in idiopathic chronic constipation (slow transit constipation). Neurogastroenterol. Motil. 1997, 9:143-150.
50. Tian Y.M., Chen X., Luo D.Z., Zhang X.H., Xue H., Zheng L.F., Yang N., Wang X.M., Zhu J.X. Alteration of dopaminergic markers in gastrointestinal tract of different rodent models of Parkinson's disease. Neuroscience 2008, 153:634-644.
51. Tomé M., Moreira E., Pérez-Fígares J.M., Jiménez A.J. Presence of D1- and D2-like dopamine receptors in the rat, mouse and bovine multiciliated ependyma. J. Neural. Transm. 2007, 114:983-994.
52. Tonini M. Recent advances in the pharmacology of gastrointestinal prokinetics. Pharmacol. Res. 1996, 33:217-226.
53. Tonini M., Frigo G., Lecchini S., D'Angelo L., Crema A. Hyoscine-resistant peristalsis in guinea-pig ileum. Eur. J. Pharmacol. 1981, 71:375-381.
54. Tonini M., Spelta V., De Ponti F., De Giorgio R., D'Agostino G., Stanghellini V., Corinaldesi R., Sternini C., Crema F. Tachykinin-dependent and -independent components of peristalsis in the guinea pig isolated distal colon. Gastroenterology 2001, 120:938-945.
55. Tonini M., Vicini R., Cervio E., De Ponti F., De Giorgio R., Barbara G., Stanghellini V., Dellabianca A., Sternini C. 5-HT7 receptors modulate peristalsis and accommodation in the guinea pig ileum. Gastroenterology 2005, 129:1557-1566.
56. Van Nassauw L., Brouns I., Adriaensen D., Burnstock G., Timmermans J.P. Neurochemical identification of enteric neurons expressing P2X(3) receptors in the guinea-pig ileum. Histochem. Cell Biol. 2002, 118:193-203.
57. Walker J.K., Gainetdinov R.R., Mangel A.W., Caron M.G., Shetzline M.A. Mice lacking the dopamine transporter display altered regulation of distal colonic motility. Am. J. Physiol. Gastrointest. Liver Physiol. 2000, 279:G311-G318.
58. Wolters E.Ch. Non-motor extranigral signs and symptoms in Parkinson's disease. Parkinsonism Relat. Disord. 2009, 15(Suppl. 3):S6-S12.
59. Yoneda S., Kadowaki M., Kuramoto H., Fukui H., Takaki M. Enhanced colonic peristalsis by impairment of nitrergic enteric neurons in spontaneously diabetic rats. Auton. Neurosci. 2001, 92:65-71.
60. Zheng Z., Travagli R.A. Dopamine effects on identified rat vagal motoneurons. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 292:G1002-G1008.
61. Zheng L.F., Wang Z.Y., Li X.F., Song J., Hong F., Lian H., Wang Q., Feng X.Y., Tang Y.Y., Zhang Y., Zhu J.X. Reduced expression of choline acetyltransferase in vagal motoneurons and gastric motor dysfunction in a 6-OHDA rat model of Parkinson's disease. Brain Res. 2011, 1420:59-67.
62. Zhu H.C., Zhao J., Luo C.Y., Li Q.Q. Gastrointestinal dysfunction in a Parkinson's disease rat model and the changes of dopaminergic, nitric oxidergic, and cholinergic neurotransmitters in myenteric plexus. J. Mol. Neurosci. 2012, 47:15-25.