Autonomic dysfunction and plasticity in micturition reflexes in human α-synuclein mice

Developmental Neurobiology

Volumn 72, Issue 6, 2012, Pages 918-936

  Hamill, Robert W ^a   Tompkins, John D ^a   Girard, Beatrice M ^a   Kershen, Richard T ^a   Parsons, Rodney L ^a   Vizzard, Margaret A ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Conscious cystometry; Hyperreflexia; Intracellular recording; Neurochemistry; Quantitative PCR

Indexed keywords

ALPHA SYNUCLEIN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; MESSENGER RNA; NERVE GROWTH FACTOR; NEURONAL NITRIC OXIDE SYNTHASE; SUBSTANCE P; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTONOMIC DYSFUNCTION; BLADDER DYSFUNCTION; BLADDER FUNCTION; CELL INCLUSION; CONTROLLED STUDY; FEMALE; GANGLION; HISTOPATHOLOGY; INNERVATION; INTESTINE FUNCTION DISORDER; LEWY BODY; LOWER URINARY TRACT SYMPTOM; MALE; MICTURITION; MICTURITION REFLEX; MORBIDITY; MOTOR DYSFUNCTION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PARKINSON DISEASE; POSTGANGLIONIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; TRANSGENIC MOUSE;

ALPHA-SYNUCLEIN; ANIMALS; AUTONOMIC NERVOUS SYSTEM DISEASES; MICE; MICE, TRANSGENIC; NEURONS; REFLEX; URINARY BLADDER; URINATION;

EID: 84860913446     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20978     Document Type: Article

References (88)

1. Arms L, Vizzard MA. 2011. Neuropeptides in lower urinary tract function. Handb Exp Pharmacol 395-423.
2. Arms LA, Girard BM, Vizzard MA. 2010. Expression and function of CXCL12/CXCR4 in rat urinary bladder with cyclophosphamide-induced cystitis. Am J Physiol Renal Physiol 298: F589-600.
3. Birder LA, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanai AJ, Wang E, et al. 2002. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci 5: 856-860.
4. Bjorling DE, Jacobsen HE, Blum JR, Shih A, Beckman M, Wang ZY, Uehling DT. 2001. Intravesical Escherichia coli lipopolysaccharide stimulates an increase in bladder nerve growth factor. BJU Int 87: 697-702.
5. Braak H, Del Tredici K. 2008. Invited Article: Nervous system pathology in sporadic Parkinson disease. Neurology 70: 1916-1925.
6. Braak H, Ghebremedhin E, Rub U, Bratzke H, Del Tredici K. 2004. Stages in the development of Parkinson's disease-related pathology. Cell Tissue Res 318: 121-134.
7. Braak H, Rub U, Gai WP, Del Tredici K. 2003. Idiopathic Parkinson's disease: Possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J Neural Transm 110: 517-536.
8. Braas KM, May V, Zvara P, Nausch B, Kliment J, Dunleavy JD, Nelson MT, et al. 2006. Role for pituitary adenylate cyclase activating polypeptide in cystitis-induced plasticity of micturition reflexes. Am J Physiol Regul Integr Comp Physiol 290: R951-962.
9. Cheppudira BP, Girard BM, Malley SE, Schutz KC, May V, Vizzard MA. 2008. Upregulation of vascular endothelial growth factor isoform VEGF-164 and receptors (VEGFR-2, Npn-1, and Npn-2) in rats with cyclophosphamide-induced cystitis. Am J Physiol Renal Physiol 295: F826-836.
10. Clemow DB, Steers WD, McCarty R, Tuttle JB. 1998. Altered regulation of bladder nerve growth factor and neurally mediated hyperactive voiding. Am J Physiol Reg Integr Comp Physiol 44: R1279-1286.
11. Clemow DB, Steers WD, Tuttle JB. 2000. Stretch-activated signaling of nerve growth factor secretion in bladder and vascular smooth muscle cells from hypertensive and hyperactive rats. JCell Physiol 183: 289-300.
12. de Medinaceli L, Freed W, Wyatt R. 1982. An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Exp Neurol 77: 634-643.
13. Dmitrieva N, Shelton D, Rice ASC, McMahon SB. 1997. The role of nerve growth factor in a model of visceral inflammation. Neuroscience 78: 449-459.
14. Donovan MK, Winternitz SR, Wyss JM. 1983. An analysis of the sensory innervation of the urinary system of the rat. Brain Res Bull 11: 321-324.
15. Dorr W. 1992. Cystometry in mice-influence of bladder filling rate and circadian variations in bladder compliance. J Urol 148: 183-187.
16. Dunham N, Miya T. 1957. A note on a simple apparatus for detecting neurological deficit in rats and mice. J Am Pharmacol Assoc 46: 208-209.
17. Dupont MC, Spitsbergen JM, Kim KB, Tuttle JB, Steers WD. 2001. Histological and neurotrophic changes triggered by varying models of bladder inflammation. J Urol 166: 1111-1118.
18. Feng LR, Federoff HJ, Vicini S, Maguire-Zeiss KA. 2010. Alpha-synuclein mediates alterations in membrane conductance: A potential role for alpha-synuclein oligomers in cell vulnerability. Eur J Neurosci 32: 10-17.
19. Fowler CJ, Dalton C, Panicker JN. 2010. Review of neurologic diseases for the urologist. Urol Clin North Am 37: 517-526.
20. Galvin JE, Lee VM, Trojanowski JQ. 2001. Synucleinopathies: clinical and pathological implications. Arch Neurol 58: 186-190.
21. Garcia-Reitbock P, Anichtchik O, Bellucci A, Iovino M, Ballini C, Fineberg E, Ghetti B, etal. 2010. SNARE protein redistribution and synaptic failure in a transgenic mouse model of Parkinson's disease. Brain 133: 2032-2044.
22. Giasson BI, Duda JE, Quinn SM, Zhang B, Trojanowski JQ, Lee VM. 2002. Neuronal alpha-synucleinopathy with severe movement disorder in mice expressing A53T human alpha-synuclein. Neuron 34: 521-533.
23. Girard BM, May V, Bora SH, Fina F, Braas KM. 2002. Regulation of neurotrophic peptide expression in sympathetic neurons: Quantitative analysis using radioimmunoassay and real-time quantitative polymerase chain reaction. Regul Pept 109: 89-101.
24. Girard BM, Wolf-Johnston A, Braas KM, Birder LA, May V, Vizzard MA. 2008. PACAP-mediated ATP release from rat urothelium and regulation of PACAP/VIP and receptor mRNA in micturition pathways after cyclophosphamide (CYP)-induced cystitis. JMol Neurosci 36: 310-320.
25. Goldstein D, Sewell L, Sharabi Y. 2011. Autonomic dysfunction in PD: A window to early detection. J Neurol Sci 310: 118-122.
26. Guerios SD, Wang ZY, Boldon K, Bushman W, Bjorling DE. 2008. Blockade of NGF and trk receptors inhibits increased peripheral mechanical sensitivity accompanying cystitis in rats. Am J Physiol Regul Integr Comp Physiol 295: R111-122.
27. Hu VY, Zvara P, Dattilio A, Redman TL, Allen SJ, Dawbarn D, Stroemer RP, et al. 2005. Decrease in bladder overactivity with REN1820 in rats with cyclophosphamide induced cystitis. J Urol 173: 1016-1021.
28. Jaworski D, Soloway P, Caterina J, Falls W. 2006. Tissue inhibitor of metalloproteinase-2 (TIMP-2) deficient mice display motor deficits. J Neurobiol 66: 82-94.
29. Keast JR, Booth AM, de Groat WC. 1989. Distribution of neurons in the major pelvic ganglion of the rat which supply the bladder, colon or penis. Cell Tissue Res 256: 105-112.
30. Keast JR, de Groat WC. 1992. Segmental distribution and peptide content of primary afferent neurons innervating the urogenital organs and colon of male rats. JComp Neurol 319: 615-623.
31. Kim JC, Kim DB, Seo SI, Park YH, Hwang TK. 2004. Nerve growth factor and vanilloid receptor expression, and detrusor instability, after relieving bladder outlet obstruction in rats. BJU Int 94: 915-918.
32. Kim JC, Park EY, Hong SH, Seo SI, Park YH, Hwang TK. 2005. Changes of urinary nerve growth factor and prostaglandins in male patients with overactive bladder symptom. Int J Urol 12: 875-880.
33. Kim JC, Park EY, Seo SI, Park YH, Hwang TK. 2006. Nerve growth factor and prostaglandins in the urine of female patients with overactive bladder. J Urol 175: 1773-1776; discussion 1776.
34. Klinger MB, Girard B, Vizzard MA. 2008. p75(NTR) expression in rat urinary bladder sensory neurons and spinal cord with cyclophosphamide-induced cystitis. J Comp Neurol 507: 1379-1392.
35. Klinger MB, Vizzard MA. 2008. Role of p75NTR in female rat urinary bladder with cyclophosphamide-induced cystitis. Am J Physiol Renal Physiol 295: F1778-1789.
36. Kruger R, Kuhn W, Muller T, Woitalla D, Graeber M, Kosel S, Przuntek H, et al. 1998. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet 18: 106-108.
37. Kruger R, Muller T, Riess O. 2000. Involvement of alpha-synuclein in Parkinson's disease and other neurodegenerative disorders. J Neural Transm 107: 31-40.
38. Lamb K, Gebhart GF, Bielefeldt K. 2004. Increased nerve growth factor expression triggers bladder overactivity. J Pain 5: 150-156.
39. Larsen KE, Schmitz Y, Troyer MD, Mosharov E, Dietrich P, Quazi AZ, Savalle M, et al. 2006. Alpha-synuclein overexpression in PC12 and chromaffin cells impairs catecholamine release by interfering with a late step in exocytosis. J Neurosci 26: 11915-11922.
40. Lecci A, Giulani S, Santiciolo P, Maggi CA. 1994. Involvement of spinal tachykinin NK1 and NK2 receptors in detrusor hyperreflexia during chemical cystitis in anaesthetized rats. Eur J Pharmacol 259: 129-135.
41. Lewy F. 1913. Zur Pathologischen Anatomie der Paralysis Agitans. Deutsche Zeitschrift fur Nervenheilkunde 50: 50-55.
42. Lim Y, Kehm VM, Lee EB, Soper JH, Li C, Trojanowski JQ, Lee VM. 2011. {alpha}-Syn suppression reverses synaptic and memory defects in a mouse model of dementia with lewy bodies. J Neurosci 31: 10076-10087.
43. Liu HT, Chancellor MB, Kuo HC. 2008a. Urinary nerve growth factor level could be a biomarker in the differential diagnosis of mixed urinary incontinence in women. BJU Int 102: 1440-1444.
44. Liu HT, Chancellor MB, Kuo HC. 2008b. Urinary nerve growth factor levels are elevated in patients with detrusor overactivity and decreased in responders to detrusor botulinum toxin-A injection. Eur Urol 56: 700-706.
45. Liu HT, Kuo HC. 2007. Intravesical botulinum toxin A injections plus hydrodistension can reduce nerve growth factor production and control bladder pain in interstitial cystitis. Urology 70: 463-468.
46. Liu HT, Kuo HC. 2008a. Urinary nerve growth factor level could be a potential biomarker for diagnosis of overactive bladder. JUrol 179: 2270-2274.
47. Liu HT, Kuo HC. 2008b. Urinary nerve growth factor levels are increased in patients with bladder outlet obstruction with overactive bladder symptoms and reduced after successful medical treatment. Urology 72: 104-108.
48. Lowe EM, Anand P, Terenghi G, Williams-Chestnut RE, Sinicropi DV, Osborne JL. 1997. Increased nerve growth factor levels in the urinary bladder of women with idiopathic sensory urgency and interstitial cystitis. Br J Urol 79: 572-577.
49. Maggi CA, Santicioli P, Meli A. 1986. The nonstop transvesical cystometrogram in urethane-anesthetized rats: a simple procedure for quantitative studies on the various phases of urinary bladder voiding cycle. J Pharmacol Methods 15: 157-167.
50. Maskri L, Zhu X-R, Fritzen S, Kühn K, Ullmer C, Engels P, Andriske M, etal. 2004. Influence of different promoters on the expression pattern of mutated human α-synuclein in transgenic mice. Neurodegener Dis 1: 255-265.
51. Masliah E, Rockenstein E, Veinbergs I, Mallory M, Hashimoto M, Takeda A, Sagara Y, et al. 2000. Dopaminergic loss and inclusion body formation in alpha-synuclein mice: implications for neurodegenerative disorders. Science 287: 1265-1269.
52. May V, Vizzard MA. 2010. Bladder dysfunction and altered somatic sensitivity in PACAP-/- mice. J Urol 183: 772-779.
53. Minguez-Castellanos A, Chamorro CE, Escamilla-Sevilla F, Ortega-Moreno A, Rebollo AC, Gomez-Rio M, Concha A, et al. 2007. Do alpha-synuclein aggregates in autonomic plexuses predate Lewy body disorders? A cohort study. Neurology 68: 2012-2018.
54. Moore DJ, Dawson TM. 2008. Value of genetic models in understanding the cause and mechanisms of Parkinson's disease. Curr Neurol Neurosci Rep 8: 288-296.
55. Murray E, Malley SE, Qiao LY, Hu VY, Vizzard MA. 2004. Cyclophosphamide induced cystitis alters neurotrophin and receptor tyrosine kinase expression in pelvic ganglia and bladder. J Urol 172: 2434-2439.
56. Nadelhaft I, Vera PL. 1995. Central nervous system neurons infected by pseudorabies virus injected into the rat urinary bladder following unilateral transection of the pelvic nerve. J Comp Neurol 359: 443-456.
57. Nemani VM, Lu W, Berge V, Nakamura K, Onoa B, Lee MK, Chaudhry FA, et al. 2010. Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 65: 66-79.
58. Okragly AJ, Niles AL, Saban R, Schmidt D, Hoffman RL, Warner TF, Moon TD, et al. 1999. Elevated tryptase, nerve growth factor, neurotrophin-3 and glial cell line-derived neurotrophic factor levels in the urine of interstitial cystitis and bladder cancer patients. J Urol 161: 438-442.
59. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, et al. 1997. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276: 2045-2047.
60. Ragab MM, Mohammed ES. 2011. Idiopathic Parkinson's disease patients at the urologic clinic. Neurourol Urodyn 30: 1258-1261.
61. Richfield EK, Thiruchelvam MJ, Cory-Slechta DA, Wuertzer C, Gainetdinov RR, Caron MG, Di Monte DA, etal. 2002. Behavioral and neurochemical effects of wild-type and mutated human alpha-synuclein in transgenic mice. Exp Neurol 175: 35-48.
62. Schnegelsberg B, Sun TT, Cain G, Bhattacharya A, Nunn PA, Ford AP, Vizzard MA, et al. 2009. Overexpression of NGF in mouse urothelium leads to neuronal hyperinnervation, pelvic sensitivity and changes in urinary bladder function. Am J Physiol Regul Integr Comp Physiol 298: R534-547.
63. Scott DA, Tabarean I, Tang Y, Cartier A, Masliah E, Roy S. 2010. A pathologic cascade leading to synaptic dysfunction in alpha-synuclein-induced neurodegeneration. J Neurosci 30: 8083-8095.
64. Simuni T, Sethi K. 2008. Nonmotor manifestations of Parkinson's disease. Ann Neurol 64 Suppl 2: S65-80.
65. Spillantini MG, Goedert M. 2000. The alpha-synucleinopathies: Parkinson's disease, dementia with Lewy bodies, and multiple system atrophy. Ann N Y Acad Sci 920: 16-27.
66. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M. 1997. Alpha-synuclein in Lewy bodies. Nature 388: 839-840.
67. Steers WD, Kolbeck S, Creedon D, Tuttle JB. 1991. Nerve growth factor in the urinary bladder of the adult regulates neuronal form and function. J Clin Invest 88: 1709-1715.
68. Streng T, Hedlund P, Talo A, Andersson KE, Gillespie JI. 2006. Phasic non-micturition contractions in the bladder of the anaesthetized and awake rat. BJU Int 97: 1094-1101.
69. Studeny S, Cheppudira BP, Meyers S, Balestreire EM, Apodaca G, Birder LA, Braas KM, et al. 2008. Urinary bladder function and somatic sensitivity in vasoactive intestinal polypeptide (VIP)-/- mice. J Mol Neurosci 36: 175-187.
70. Tipre D, Goldstein D. 2005. Cardiac and extracardiac sympathetic denervation in Parkinson's disease with orthostatic hypotension and in pure autonomic failure. J Nucl Med 46: 1775-1781.
71. Tolosa E, Poewe W. 2009. Premotor Parkinson disease. Neurology 72: S1.
72. Tompkins JD, Girard BM, Vizzard MA, Parsons RL. 2010. VIP and PACAP effects on mouse major pelvic ganglia neurons. JMol Neurosci 42: 390-396.
73. Venda LL, Cragg SJ, Buchman VL, Wade-Martins R. 2010. alpha-Synuclein and dopamine at the crossroads of Parkinson's disease. Trends Neurosci 33: 559-568.
74. Vizzard MA. 1997. Increased expression of neuronal nitric oxide synthase in bladder afferent and spinal neurons following spinal cord injury. Dev Neurosci 19: 232-246.
75. Vizzard MA. 2000a. Alterations in spinal cord Fos protein expression induced by bladder stimulation following cystitis. Am J Physiol Regul Integr Comp Physiol 278: R1027-1039.
76. Vizzard MA. 2000b. Changes in urinary bladder neurotrophic factor mRNA and NGF protein following urinary bladder dysfunction. Exp Neurol 161: 273-284.
77. Vizzard MA. 2000c. Up-regulation of pituitary adenylate cyclase-activating polypeptide in urinary bladder pathways after chronic cystitis. J Comp Neurol 420: 335-348.
78. Vizzard MA. 2001. Alterations in neuropeptide expression in lumbosacral bladder pathways following chronic cystitis. J Chem Neuroanat 21: 125-138.
79. Vizzard MA, Boyle MM. 1999. Increased expression of growth-associated protein (GAP-43) in lower urinary tract pathways following cyclophosphamide (CYP)-induced cystitis. Brain Res 844: 174-187.
80. 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.
81. Yavich L, Tanila H, Vepsalainen S, Jakala P. 2004. Role of alpha-synuclein in presynaptic dopamine recruitment. J Neurosci 24: 11165-11170.
82. Yokoyama T, Kumon H, Nagai A. 2008. Correlation of urinary nerve growth factor level with pathogenesis of overactive bladder. Neurourol Urodyn 27: 417-420.
83. Yoshimura N, Bennett NE, Hayashi Y, Ogawa T, Nishizawa O, Chancellor MB, de Groat WC, et al. 2006. Bladder overactivity and hyperexcitability of bladder afferent neurons after intrathecal delivery of nerve growth factor in rats. J Neurosci 26: 10847-10855.
84. Yoshimura N, de Groat WC. 1999. Increased excitability of afferent neurons innervating rat urinary bladder after chronic bladder inflammation. J Neurosci 19: 4644-4653.
85. Zarranz JJ, Alegre J, Gomez-Esteban JC, Lezcano E, Ros R, Ampuero I, Vidal L, et al. 2004. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann Neurol 55: 164-173.
86. Zvara P, Folsom JB, Kliment JJr., Dattilio AL, Moravcikova A, Plante MK, Vizzard MA. 2004. Increased expression of neuronal nitric oxide synthase in bladder afferent cells in the lumbosacral dorsal root ganglia after chronic bladder outflow obstruction. Brain Res 1002: 35-42.
87. Zvara P, Vizzard MA. 2007. Exogenous overexpression of nerve growth factor in the urinary bladder produces bladder overactivity and altered micturition circuitry in the lumbosacral spinal cord. BMC Physiol 7: 9.
88. Zvarova K, Vizzard MA. 2006. Changes in galanin immunoreactivity in rat micturition reflex pathways after cyclophosphamide-induced cystitis. Cell Tissue Res 324: 213-224.