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Acta Neuropathologica

Erschienen in:

01.07.2010 | Review

Involvement of the peripheral nervous system in synucleinopathies, tauopathies and other neurodegenerative proteinopathies of the brain

verfasst von: Koichi Wakabayashi, Fumiaki Mori, Kunikazu Tanji, Satoshi Orimo, Hitoshi Takahashi

Erschienen in: Acta Neuropathologica | Ausgabe 1/2010

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Abstract

Involvement of the peripheral nervous system (PNS) is relatively common in some neurodegenerative proteinopathies of the brain and may be pathogenetically and diagnostically important. In Parkinson’s disease, neuronal α-synuclein aggregates are distributed throughout the nervous system, including the central nervous system (CNS), sympathetic ganglia, enteric nervous system, cardiac and pelvic plexuses, submandibular gland, adrenal medulla and skin. The pathological process may target the PNS and CNS at the same time. In multiple system atrophy, numerous glial cytoplasmic inclusions composed of filamentous α-synuclein are widely distributed in the CNS, while α-synuclein accumulation is minimal in the sympathetic ganglia and is restricted to neurons. Neurofibrillary tangles can occur in the sympathetic and spinal ganglia in tauopathy, although they appear to develop independently of cerebral Alzheimer’s disease pathology. In amyotrophic lateral sclerosis, neuronal loss with TDP-43-positive neuronal cytoplasmic inclusions in the spinal ganglia is more frequent than previously thought. Peripheral ganglia and visceral organs are also involved in polyglutamine diseases. Further elucidation and characterization of PNS lesions will have implications for intravital biopsy diagnosis in neurodegenerative proteinopathy, particularly in Parkinson’s disease.

Abbott RD, Ross GW, Petrovitch H et al (2007) Bowel movement frequency in late-life and incidental Lewy bodies. Mov Disord 22:1581–1586PubMed

Aguzzi A (2009) Cell biology: beyond the prion principle. Nature 459:924–925PubMed

Altschuler E (1996) Gastric Helicobacter pylori infection as a cause of idiopathic Parkinson disease and non-arteric anterior optic ischemic neuropathy. Med Hypotheses 47:413–414PubMed

Amino T, Orimo S, Itoh Y, Takahashi A, Uchihara T, Mizusawa H (2005) Profound cardiac sympathetic denervation occurs in Parkinson disease. Brain Pathol 15:29–34PubMed

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 207:4–12PubMed

Anlauf M, Schäfer MK, Eiden L, Weihe E (2003) Chemical coding of the human gastrointestinal nervous system: cholinergic, VIPergic, and catecholaminergic phenotypes. J Comp Neurol 459:90–111PubMed

Arai K, Kato N, Kawashima K, Hattori T (2000) Pure autonomic failure in association with human α-synucleinopathy. Neurosci Lett 296:171–173PubMed

Arai T, Hasegawa M, Akiyama H et al (2006) TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem Biophys Res Commun 351:602–611PubMed

Arima K, Uéda K, Sunohara N et al (1998) NACP/α-synuclein immunoreactivity in fibrillary components of neuronal and oligodendroglial cytoplasmic inclusions in the pontine nuclei in multiple system atrophy. Acta Neuropathol 96:439–444PubMed

10.

Arrasate M, Mitra S, Schweitzer ES, Segal MR, Finkbeiner S (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431:805–810PubMed

11.

Beach TG, Adler CH, Sue LI et al (2008) Reduced striatal tyrosine hydroxylase in incidental Lewy body disease. Acta Neuropathol 115:445–451PubMed

12.

Beach TG, Adler CH, Sue LI et al (2010) Multi-organ distribution of phosphorylated α-synuclein histopathology in subjects with Lewy body disorders. Acta Neuropathol 119:689–702PubMed

13.

Blackett H, Walker R, Wood B (2009) Urinary dysfunction in Parkinson’s disease: a review. Parkinsonism Relat Disord 15:81–87PubMed

14.

Bloch A, Probst A, Bissig H, Adams H, Tolnay M (2006) α-Synuclein pathology of the spinal and peripheral autonomic nervous system in neurologically unimpaired elderly subjects. Neuropathol Appl Neurobiol 32:284–295PubMed

15.

Bohl J, Ulbricht D, Steinmetz H (1997) Neurofibrillary tangles in peripheral autonomic ganglion cells. In: Iqbal K, Winblad B, Nishimura T, Takeda M, Wisniewski HM (eds) Alzheimer’s disease: biology. Diagnosis and therapeutics. Wiley, Chichester, pp 281–287

16.

Braak H, Alafuzoff I, Arzberger T et al (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112:389–404PubMed

17.

Braak H, Bohl JR, Müller CM et al (2006) The staging procedure for the inclusion body pathology associated with sporadic Parkinson’s disease reconsidered. Mov Disord 21:2042–2051PubMed

18.

Braak H, Braak E (1989) Cortical and subcortical argyrophilic grains characterize a disease associated with adult onset dementia. Neuropathol Appl Neurobiol 15:13–26PubMed

19.

Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82:239–259PubMed

20.

Braak H, de Vos RAI, Bohl J, Del Tredici K (2006) Gastric α-synuclein immunoreactive inclusions in Meissner’s and Auerbach’s plexuses in cases staged for Parkinson’s disease-related brain pathology. Neurosci Lett 396:67–72PubMed

21.

Braak H, Del Tredici K (2008) Nervous system pathology in sporadic Parkinson’s disease. Neurology 70:1916–1925PubMed

22.

Braak H, Del Tredici K, Rüb U et al (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211PubMed

23.

Braak H, Rüb 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 110:517–536PubMed

24.

Braak H, Sastre M, Bohl JR, de Vos RA, Del Tredici K (2007) Parkinson’s disease: lesions in dorsal horn layer I, involvement of parasympathetic and sympathetic pre- and postganglionic neurons. Acta Neuropathol 113:421–429PubMed

25.

Braak H, Sastre M, Del Tredici K (2007) Development of α-synuclein immunoreactive astrocytes in the forebrain parallels stages of intraneuronal pathology in sporadic Parkinson’s disease. Acta Neuropathol 114:231–241PubMed

26.

Brownell B, Oppenheimer DR, Hughes JT (1970) The central nervous system in motor neurone disease. J Neurol Neurosurg Psychiatry 33:338–357PubMed

27.

Cersosimo MG, Benarroch EE (2008) Neural control of the gastrointestinal tract: implications for Parkinson disease. Mov Disord 23:1065–1075PubMed

28.

Chaumette T, Lebouvier T, Aubert P et al (2009) Neurochemical plasticity in the enteric nervous system of a primate animal model of experimental Parkinsonism. Neurogastroenterol Motil 21:215–222PubMed

29.

Croisier E, Graeber MB (2006) Glial degeneration and reactive gliosis in alpha-synucleinopathies: the emerging concept of primary gliodegeneration. Acta Neuropathol 112:517–530PubMed

30.

Dabby R, Djaldetti R, Shahmurov M et al (2006) Skin biopsy for assessment of autonomic denervation in Parkinson’s disease. J Neural Transm 113:1169–1176PubMed

31.

Dabir DV, Robinson MB, Swanson E et al (2006) Impaired glutamate transport in a mouse model of tau pathology in astrocytes. J Neurosci 26:644–654PubMed

32.

Davidson Y, Kelley T, Mackenzie IR et al (2007) Ubiquitinated pathological lesions in frontotemporal lobar degeneration contain the TAR DNA-binding protein, TDP-43. Acta Neuropathol 113:521–533PubMed

33.

Del Tredici K, Hawkes CH, Ghebremedhin E, Braak H (2010) Lewy pathology in the submandibular gland of individuals with incidental Lewy body disease and sporadic Parkinson’s disease. Acta Neuropathol 119:703–707PubMed

34.

Del Tredici K, Rüb U, De Vos RA, Bohl JR, Braak H (2002) Where does parkinson disease pathology begin in the brain? J Neuropathol Exp Neurol 61:413–426PubMed

35.

DelleDonne A, Klos J, Fujishiro H et al (2008) Incidental Lewy body disease and preclinical Parkinson’s disease. Arch Neurol 65:1074–1080PubMed

36.

Den Hartog Jager WA (1970) Histochemistry of adrenal bodies in Parkinson’s disease. Arch Neurol 23:528–533

37.

Den Hartog Jager WA, Bethlem J (1960) The distribution of Lewy bodies in the central and autonomic nervous systems in idiopathic paralysis agitans. J Neurol Neurosurg Psychiatry 23:283–290

38.

Dickson DW, Bergeron C, Chin SS et al (2002) Office of rare diseases neuropathologic criteria for corticobasal degeneration. J Neuropathol Exp Neurol 61:935–946PubMed

39.

Dickson DW, Fujishiro H, DelleDonne A et al (2008) Evidence that incidental Lewy body disease is pre-symptomatic Parkinson’s disease. Acta Neuropathol 115:437–444PubMed

40.

Dickson DW, Fujishiro H, Orr C et al (2009) Neuropathology of non-motor features of Parkinson disease. Parkinsonism Relat Disord 15(Suppl 3):S1–S5PubMed

41.

Djaldetti R, Lev N, Melamed E (2009) Lesions outside the CNS in Parkinson’s disease. Mov Disord 24:793–800PubMed

42.

Dobbs RJ, Dobbs SM, Weller C et al (2008) Helicobacter hypothesis for idiopathic Parkinsonism: before and beyond. Helicobacter 13:309–322PubMed

43.

Engelender S (2008) Ubiquitination of α-synuclein and autophagy in Parkinson’s disease. Autophagy 4:372–374PubMed

44.

Ferrer I, Santpere G, van Leeuwen FW (2008) Argyrophilic grain disease. Brain 131:1416–1432PubMed

45.

Forno LS, Norville RL (1976) Ultrastructure of Lewy bodies in the stellate ganglion. Acta Neuropathol 34:183–197PubMed

46.

Foulds PG, Davidson Y, Mishra M et al (2009) Plasma phosphorylated-TDP-43 protein levels correlate with brain pathology in frontotemporal lobar degeneration. Acta Neuropathol 118:647–658PubMed

47.

Foulds P, McAuley E, Gibbons L et al (2008) TDP-43 protein in plasma may index TDP-43 brain pathology in Alzheimer’s disease and frontotemporal lobar degeneration. Acta Neuropathol 116:141–146PubMed

48.

Fujishiro H, Frigerio R, Burnett M et al (2008) Cardiac sympathetic denervation correlates with clinical and pathologic stages of Parkinson’s disease. Mov Disord 23:1085–1092PubMed

49.

Fujiwara H, Hasegawa M, Dohmae N et al (2002) α-Synuclein is phosphorylated in synucleinopathy lesions. Nature Cell Biol 4:160–164PubMed

50.

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 66:354–362PubMed

51.

Ghebremedhin E, Del Tredici K, Langston JW, Braak H (2009) Diminished tyrosine hydroxylase immunoreactivity in the cardiac conduction system and myocardium in Parkinson’s disease: an anatomical study. Acta Neuropathol 118:777–784PubMed

52.

Hague K, Lento P, Morgello S, Caro S, Kaufmann H (1997) The distribution of Lewy bodies in pure autonomic failure: autopsy findings and review of the literature. Acta Neuropathol 94:192–196PubMed

53.

Hasegawa M, Arai T, Nonaka T et al (2008) Phosphorylated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Ann Neurol 64:60–70PubMed

54.

Hattori M, Hashizume Y, Yoshida M et al (2003) Distribution of astrocytic plaques in the corticobasal degeneration brain and comparison with tuft-shaped astrocytes in the progressive supranuclear palsy brain. Acta Neuropathol 106:143–149PubMed

55.

Hawkes CH, Del Tredici K, Braak H (2007) Parkinson’s disease: a dual-hit hypothesis. Neuropathol Appl Neurobiol 33:599–614PubMed

56.

Hayashi Y, Kakita A, Yamada M et al (1998) Hereditary dentatorubral-pallidoluysian atrophy: detection of widespread ubiquitinated neuronal and glial intranuclear inclusions in the brain. Acta Neuropathol 96:547–552PubMed

57.

Herzog E (1928) Histopathologische Veränderungen im Sympathicus und ihre Bedeutung. Dtsch Z Nervenheilk 107:75–80

58.

Higuchi M, Zhang B, Forman MS et al (2005) Axonal degeneration induced by targeted expression of mutant human tau in oligodendrocytes of transgenic mice that model glial tauopathies. J Neurosci 25:9434–9443PubMed

59.

Horimoto Y, Matsumoto M, Akatsu H et al (2003) Autonomic dysfunctions in dementia with Lewy bodies. J Neurol 250:530–533PubMed

60.

Ikeda K, Haga C, Akiyama H et al (1992) Coexistence of paired helical filaments and glial filaments in astrocytic processes within ghost tangles. Neurosci Lett 148:126–128PubMed

61.

Ikemura M, Saito Y, Sengoku R et al (2008) Lewy body pathology involves cutaneous nerves. J Neuropathol Exp Neurol 67:945–953PubMed

62.

Iwanaga K, Wakabayashi K, Yoshimoto M et al (1999) Lewy body-type degeneration in cardiac plexus in Parkinson’s and incidental Lewy body diseases. Neurology 52:1269–1271PubMed

63.

Iwasaki Y, Yoshida M, Hashizume Y, Hattori M, Aiba I, Sobue G (2007) Widespread spinal cord involvement in progressive supranuclear palsy. Neuropathology 27:331–340PubMed

64.

Iwasaki Y, Yoshida M, Hattori M et al (2004) Distribution of tuft-shaped astrocytes in the cerebral cortex in progressive supranuclear palsy. Acta Neuropathol 108:399–405PubMed

65.

Iwasaki Y, Yoshida M, Hattori M, Hashizume Y, Sobue G (2005) Widespread spinal cord involvement in corticobasal degeneration. Acta Neuropathol 109:632–638PubMed

66.

Jackson M, Lennox G, Balsitis M, Lowe J (1995) Lewy body dysphagia. J Neurol Neurosurg Psychiatry 58:756–758PubMed

67.

Kanazawa M, Sanpei K, Toyoshima Y, Kawachi I, Honma Y, Takahashi H (2007) An autopsy case of dementia with Lewy bodies showing autonomic failure and dementia as the initial symptoms. Mov Disord 22:1212–1213PubMed

68.

Kanda T, Tsukagoshi H, Oda M, Miyamoto K, Tanabe H (1996) Changes of unmyelinated nerve fibers in sural nerve in amyotrophic lateral sclerosis, Parkinson’s disease and multiple system atrophy. Acta Neuropathol 91:145–154PubMed

69.

Kasai T, Tokuda T, Ishigami N et al (2009) Increased TDP-43 protein in cerebrospinal fluid of patients with amyotrophic lateral sclerosis. Acta Neuropathol 117:55–62PubMed

70.

Kato T, Hirano A, Weinberg MN, Jacobs AK (1986) Spinal cord lesions in progressive supranuclear palsy: some new observations. Acta Neuropathol 71:11–14PubMed

71.

Kaufmann H, Hague K, Perl D (2001) Accumulation of alpha-synuclein in autonomic nerves in pure autonomic failure. Neurology 56:980–981PubMed

72.

Kaufmann H, Nahm K, Purohit D, Wolfe D (2004) Autonomic failure as the initial presentation of Parkinson disease and dementia with Lewy bodies. Neurology 63:1093–1095PubMed

73.

Kawano H, Okada R, Yano K (2003) Histological study on the distribution of autonomic nerves in the human heart. Heart Vessels 18:32–39PubMed

74.

Kawasaki H, Murayama S, Tomonaga M, Izumiyama N, Shimada H (1987) Neurofibrillary tangles in human upper cervical ganglia: morphological study with immunohistochemistry and electron microscopy. Acta Neuropathol 75:156–159PubMed

75.

Kikuchi H, Doh-ura K, Kira J, Iwaki T (1999) Preferential neurodegeneration in the cervical spinal cord of progressive supranuclear palsy. Acta Neuropathol 97:577–584PubMed

76.

Klos KJ, Ahlskog JE, Josephs KA et al (2006) α-Synuclein pathology in the spinal cords of neurologically asymptomatic aged individuals. Neurology 66:1100–1102PubMed

77.

Komori T (1999) Tau-positive glial inclusions in progressive supranuclear palsy, corticobasal degeneration and Pick’s disease. Brain Pathol 9:663–679PubMed

78.

Konagaya M, Sakai M, Matsuoka Y, Konagaya Y, Hashizume Y (1999) Multiple system atrophy with remarkable frontal atrophy. Acta Neuropathol 97:423–428PubMed

79.

Kordower JH, Chu Y, Hauser RA, Freeman TB, Olanow CW (2008) Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson’s disease. Nat Med 14:504–506PubMed

80.

Kosaka K (1978) Lewy bodies in cerebral cortex. Report of three cases. Acta Neuropathol 42:127–134PubMed

81.

Kosaka K, Iseki E, Odawara T, Yamamoto T (1996) Cerebral type of Lewy body disease. Neuropathology 16:32–35

82.

Kovacs GG, Botond G, Budka H (2010) Protein coding of neurodegenerative dementias: the neuropathological basis of biomarker diagnostics. Acta Neuropathol 119:389–408PubMed

83.

Kövari E, Burkhardt K, Lobrinus JA, Bouras C (2007) Lewy body dysphagia. Acta Neuropathol 114:295–298PubMed

84.

Kuo YM, Li Z, Jiao Y, Gaborit N et al (2010) Extensive enteric nervous system abnormalities in mice transgenic for artificial chromosomes containing Parkinson disease-associated α-synuclein gene mutations precede central nervous system changes. Hum Mol Genet 19:1633–1650PubMed

85.

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 37:1253–1255PubMed

86.

Langston JW (2006) The Parkinson’s complex: Parkinsonism is just the tip of the iceberg. Ann Neurol 59:591–596PubMed

87.

Lebouvier T, Chaumette T, Damier P et al (2008) Pathological lesions in colonic biopsies during Parkinson’s disease. Gut 57:1741–1743PubMed

88.

Lerner A, Bagic A (2008) Olfactory pathogenesis of idiopathic Parkinson disease revisited. Mov Disord 23:1076–1084PubMed

89.

Li JY, Englund E, Holton JL et al (2008) Lewy bodies in grafted neurons in subjects with Parkinson’s disease suggest host-to-graft disease propagation. Nat Med 14:501–503PubMed

90.

Li M, Nakagomi Y, Kobayashi Y et al (1998) Nonneural nuclear inclusions of androgen receptor protein in spinal and bulbar muscular atrophy. Am J Pathol 153:695–701PubMed

91.

Lim SY, Fox SH, Lang AE (2009) Overview of the extranigral aspects of Parkinson disease. Arch Neurol 66:167–172PubMed

92.

Manome T, Kobayashi T, Oguchi K, Tsukagoshi H, Fujiwara M (1980) An autopsy case of amyotrophic lateral sclerosis with dysesthesia and superficial sensory disturbance. Clin Neurol (Tokyo) 20:225–232

93.

Matsumoto S, Hirano A, Goto S (1990) Spinal cord neurofibrillary tangles of Guamanian amyotrophic lateral sclerosis and parkinsonism-dementia complex: an immunohistochemical study. Neurology 40:975–979PubMed

94.

Meco G, Rubino A, Caravona N, Valente M (2008) Sexual dysfunction in Parkinson’s disease. Parkinsonism Relat Disord 14:451–456PubMed

95.

Miki Y, Mori F, Wakabayashi K, Kuroda N, Orimo S (2009) Incidental Lewy body disease restricted to the heart and stellate ganglia. Mov Disord 24:2299–2301PubMed

96.

Miki Y, Tomiyama M, Ueno T et al (2010) Clinical availability of skin biopsy in the diagnosis of Parkinson’s disease. Neurosci Lett 469:357–359PubMed

97.

Miller N, Noble E, Jones D, Burn D (2006) Hard to swallow: dysphagia in Parkinson’s disease. Age Ageing 35:614–618PubMed

98.

Minguez-Castellanos A, Chamorro CE, Escamilla-Sevilla F et al (2007) Do α-synuclein aggregates in autonomic plexuses predate Lewy body disorders? Neurology 68:2012–2018PubMed

99.

Miyamoto T, Miyamoto M, Inoue Y, Usui Y, Suzuki K, Hirata K (2006) Reduced cardiac ¹²³I-MIBG scintigraphy in idiopathic REM sleep behavior disorder. Neurology 67:2236–2238PubMed

100.

Mori F, Inenaga C, Yoshimoto M et al (2002) α-Synuclein immunoreactivity in normal and neoplastic Schwann cells. Acta Neuropathol 103:145–151PubMed

101.

Mori F, Nishie M, Kakita A, Yoshimoto M, Takahashi H, Wakabayashi K (2006) Relationship among α-synuclein accumulation, dopamine synthesis, and neurodegeneration in Parkinson disease substantia nigra. J Neuropathol Exp Neurol 65:808–815PubMed

102.

Mori F, Tanji K, Zhang H, Kakita A, Takahashi H, Wakabayashi K (2008) α-Synuclein pathology in the neostriatum in Parkinson’s disease. Acta Neuropathol 115:453–459PubMed

103.

Mori F, Tanji K, Zhang HX et al (2008) Maturation process of TDP-43-positive neuronal cytoplasmic inclusions in amyotrophic lateral sclerosis with and without dementia. Acta Neuropathol 116:193–203PubMed

104.

Nakano I, Iwatsubo T, Otsuka N et al (1992) Paired helical filaments in astrocytes: Electron microscopy and immunohistochemistry in a case of atypical Alzheimer’s disease. Acta Neuropathol 83:228–232PubMed

105.

Nakazato Y, Yamazaki H, Hirato J, Ishida Y, Yamaguchi H (1990) Oligodendroglial microtubular tangles in multiple system atrophy. J Neuropathol Exp Neurol 49:521–530PubMed

106.

Neumann M, Sampathu DM, Kwong LK et al (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314:130–133PubMed

107.

Nishie M, Mori F, Fujiwara H et al (2004) Accumulation of phosphorylated α-synuclein in the brain and peripheral ganglia of patients with multiple system atrophy. Acta Neuropathol 107:292–298PubMed

108.

Nishie M, Mori F, Yoshimoto M, Takahashi H, Wakabayashi K (2004) A quantitative investigation of neuronal cytoplasmic and intranuclear inclusions in the pontine and inferior olivary nuclei in multiple system atrophy. Neuropathol Appl Neurobiol 30:546–554PubMed

109.

Nishihira Y, Tan CF, Hoshi Y et al (2009) Sporadic amyotrophic lateral sclerosis of long duration is associated with relatively mild TDP-43 pathology. Acta Neuropathol 117:45–53PubMed

110.

Nishihira Y, Tan CF, Onodera O et al (2008) Sporadic amyotrophic lateral sclerosis: two pathological patterns shown by analysis of distribution of TDP-43-immunoreactive neuronal and glial cytoplasmic inclusions. Acta Neuropathol 116:169–182PubMed

111.

Nishihira Y, Tan CF, Toyoshima Y et al (2009) Sporadic amyotrophic lateral sclerosis: widespread multisystem degeneration with TDP-43 pathology in a patient after long-term survival on a respirator. Neuropathology 29:689–696PubMed

112.

Nishimura M, Namba Y, Ikeda K, Akiguchi I, Oda M (1993) Neurofibrillary tangles in the neurons of spinal dorsal root ganglia of patients with progressive supranuclear palsy. Acta Neuropathol 85:453–457PubMed

113.

Nolano M, Provitera V, Estraneo A et al (2008) Sensory deficit in Parkinson’s disease: evidence of a cutaneous denervation. Brain 131:1903–1911PubMed

114.

Ohama E, Ikuta F (1976) Parkinson’s disease. Distribution of Lewy bodies and monoamine neurons system. Acta Neuropathol 34:311–319PubMed

115.

Oinas M, Paetau A, Myllykangas L, Notkola IL, Kalimo H, Polvikoski T (2010) α-Synuclein pathology in the spinal cord autonomic nuclei associates with α-synuclein pathology in the brain: a population-based Vantaa 85+ study. Acta Neuropathol 119:715–722PubMed

116.

Olanow CW, Prusiner SB (2009) Is Parkinson’s disease a prion disorder? Proc Natl Acad Sci USA 106:12571–12572PubMed

117.

Orimo S, Amino T, Itoh Y et al (2005) Cardiac sympathetic denervation precedes neuronal loss in the sympathetic ganglia in Lewy body disease. Acta Neuropathol 109:583–588PubMed

118.

Orimo S, Amino T, Uchihara T et al (2007) Decreased cardiac uptake of MIBG is a potential biomarker for the presence of Lewy bodies. J Neurol 254(Suppl 4):21–28

119.

Orimo S, Amino T, Yokochi M et al (2005) Preserved cardiac sympathetic nerve accounts for normal cardiac uptake of MIBG in PARK2. Mov Disord 20:1350–1353PubMed

120.

Orimo S, Kanazawa T, Nakamura A et al (2007) Degeneration of cardiac sympathetic nerve can occur in multiple system atrophy. Acta Neuropathol 113:81–86PubMed

121.

Orimo S, Oka T, Miura H et al (2002) Sympathetic cardiac denervation in Parkinson’s disease and pure autonomic failure but not in multiple system atrophy. J Neurol Neurosurg Psychiatry 73:776–777PubMed

122.

Orimo S, Takahashi A, Uchihara T et al (2007) Degeneration of cardiac sympathetic nerve begins in the early disease process of Parkinson’s disease. Brain Pathol 17:24–30PubMed

123.

Orimo S, Uchihara T, Nakamura A et al (2008) Axonal α-synuclein aggregates herald centripetal degeneration of cardiac sympathetic nerve in Parkinson’s disease. Brain 131:642–650PubMed

124.

Orimo S, Uchihara T, Nakamura A et al (2008) Cardiac sympathetic denervation in Parkinson’s disease linked to SNCA duplication. Acta Neuropathol 116:575–577PubMed

125.

Oyanagi K, Wakabayashi K, Ohama E et al (1990) Lewy bodies in the lower sacral parasympathetic neurons of a patient with Parkinson’s disease. Acta Neuropathol 80:558–559PubMed

126.

Ozawa T, Paviour D, Quinn NP et al (2004) The spectrum of pathological involvement of the striatonigral and olivopontocerebellar systems in multiple system atrophy: clinicopathological correlations. Brain 127:2657–2671PubMed

127.

Papp MI, Kahn JE, Lantos PL (1989) Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J Neurol Sci 94:79–100PubMed

128.

Parent A (1996) Carpenter’s human neuroanatomy, 9th edn. Williams & Wilkins, Baltimore

129.

Pfeiffer RF (2003) Gastrointestinal dysfunction in Parkinson’s disease. Lancet Neurol 2:107–116PubMed

130.

Phillips RJ, Walter GC, Ringer BE, Higgs KM, Powley TL (2009) Alpha-synuclein immunopositive aggregates in the myenteric plexus of the aging Fischer 344 rat. Exp Neurol 220:109–119PubMed

131.

Piao YS, Hayashi S, Hasegawa M et al (2001) Co-localization of α-synuclein and phosphorylated tau in neuronal and glial cytoplasmic inclusions in a patient with multiple system atrophy of long duration. Acta Neuropathol 101:285–293PubMed

132.

Piao YS, Wakabayashi K, Kakita A et al (2003) Neuropathology with clinical correlations of sporadic amyotrophic lateral sclerosis: 102 autopsy cases examined between 1962 and 2000. Brain Pathol 13:10–22PubMed

133.

Qualman SJ, Haupt HM, Yang P, Hamilton SR (1984) Esophageal Lewy bodies associated with ganglion cell loss in achalasia Similarity to Parkinson’s disease. Gastroenterology 87:848–856PubMed

134.

Ross GW, Abbott RD, Petrovitch H et al (2006) Association of olfactory dysfunction with incidental Lewy bodies. Mov Disord 21:2062–2067PubMed

135.

Ross CA, Poirier MA (2004) Protein aggregation and neurodegenerative disease. Nat Med 10(Suppl):S10–S17PubMed

136.

Saito Y, Kawashima A, Ruberu NN et al (2003) Accumulation of phosphorylated α-synuclein in aging human brain. J Neuropathol Exp Neurol 62:644–654PubMed

137.

Saito Y, Murayama S (2000) Expression of tau immunoreactivity in the spinal motor neurons of Alzheimer’s disease. Neurology 55:1727–1729PubMed

138.

Saito Y, Rubbru NN, Sawabe M et al (2004) Staging of argyrophilic grains: an age-associated tauopathy. J Neuropathol Exp Neurol 63:911–918PubMed

139.

Sathasivam K, Hobbs C, Turmaine M et al (1999) Formation of polyglutamine inclusions in non-CNS tissue. Hum Mol Genet 8:813–822PubMed

140.

Schmidt RE, Beaudet LN, Plurad SB, Dorsey DA (1997) Axonal cytoskeletal pathology in aged and diabetic human sympathetic autonomic ganglia. Brain Res 769:375–383PubMed

141.

Sengoku R, Saito Y, Ikemura M et al (2008) Incidence and extent of Lewy body-related α-synucleinopathy in aging human olfactory bulb. J Neuropathol Exp Neurol 67:1072–1083PubMed

142.

Shankle WR, Landing BH, Ang SM, Chui H, Villarreal-Engelhardt G, Zarow C (1993) Studies of the enteric nervous system in Alzheimer disease and other dementias of the elderly: enteric neurons in Alzheimer disease. Modern Pathol 6:10–14

143.

Shibuya K, Nagatomo H, Iwabuchi K, Inoue M, Yagishita S, Itoh Y (2000) Asymmetrical temporal lobe atrophy with massive neuronal inclusions in multiple system atrophy. J Neurol Sci 179:50–58PubMed

144.

Shishido T, Ikemura M, Obi T et al (2010) α-Synuclein accumulation in skin nerve fibers revealed by skin biopsy in pure autonomic failure. Neurology 74:608–610PubMed

145.

Singaram C, Ashraf W, Gaumnitz EA et al (1995) Dopaminergic defect of enteric nervous system in Parkinson’s disease patients with chronic constipation. Lancet 346:861–864PubMed

146.

Sone M, Yoshida M, Hashizume Y, Hishikawa N, Sobue G (2005) α-Synuclein-immunoreactive structure formation is enhanced in sympathetic ganglia of patients with multiple system atrophy. Acta Neuropathol 110:19–26PubMed

147.

Steele JC, Richardson JC, Olszewski J (1964) Progressive supranuclear palsy. A heterogeneous degeneration involving the brain stem, basal ganglia and cerebellum with vertical gaze and pseudobulbar palsy, nuchal dystonia and dementia. Arch Neurol 10:333–359PubMed

148.

Su M, Yoshida Y, Hirata Y, Watahiki Y, Nagata K (2001) Primary involvement of the motor area in association with the nigrostriatal pathway in multiple system atrophy: neuropathological and morphometric evaluations. Acta Neuropathol 101:57–64PubMed

149.

Sugie M, Goto J, Kawamura M, Ota H (2005) Increased norepinephrine-associated adrenomedullary inclusions in Parkinson’s disease. Pathol Int 55:130–136PubMed

150.

Suzuki M, Mikami H, Watanabe T et al (2010) Increased expression of TDP-43 in the skin of amyotrophic lateral sclerosis. Acta Neurol Scand (epub ahead of print). doi:10.1111/j.1600-0404.2010.01321.x

151.

Takahashi H, Ohama E, Ikuta F (1991) Are Bunina bodies of endoplasmic reticulum origin? An ultrastructural study of subthalamic eosinophilic inclusions in a case of atypical motor neuron disease. Acta Pathol Jpn 41:889–894PubMed

152.

Takahashi H, Oyanagi K, Takeda S, Hinokuma K, Ikuta F (1989) Occurrence of 15-nm-wide straight tubules in neocortical neurons in progressive supranuclear palsy. Acta Neuropathol 79:233–239PubMed

153.

Takeda S, Yamazaki K, Miyakawa T, Arai H (1993) Parkinson’s disease with involvement of the parasympathetic ganglia. Acta Neuropathol 86:397–398PubMed

154.

Takeda S, Yamazaki K, Miyakawa T, Arai H (1994) Morphological investigations of the peripheral autonomic nervous system in Parkinson’s disease, progressive supranuclear palsy and senile dementia of Alzheimer type. Brain Pathol 4:531

155.

Taniwaki T, Minohara M, Hara H, Ohyagi Y, Yamada T, Kira J (2000) Striatonigral degeneration with motor neuron disease. J Neurol 247:395–396PubMed

156.

Tashiro K, Moriwaka F, Matsuura T, Matsumoto A, Hamada T (1988) Sensory findings in amyotrophic lateral sclerosis. In: Tsubaki T, Yase Y (eds) Amytrophic lateral sclerosis. Elsevier, Amsterdam, pp 183–188

157.

Tellez-Nagel I, Wisniewski HM (1973) Ultrastructure of neurofibrillary tangles in Steele-Richardson-Olszewski syndrome. Arch Neurol 29:324–327PubMed

158.

Terry RD (2000) Do neuronal inclusions kill the cell? J Neural Transm (Suppl) 59:91–93

159.

Tomonaga M, Saito M, Yoshimura M, Shimada H, Tohgi H (1978) Ultrastructure of the Bunina bodies in anterior horn cells of amyotrophic lateral sclerosis. Acta Neuropathol 42:81–86PubMed

160.

Tsika E, Moysidou M, Guo J et al (2010) Distinct region-specific α-synuclein oligomers in A53T transgenic mice: Implications for neurodegeneration. J Neurosci 30:3409–3418PubMed

161.

Tsuchiya K, Ozawa E, Haga C et al (2000) Constant involvement of the Betz cells and pyramidal tract in multiple system atrophy: a clinicopathological study of seven autopsy cases. Acta Neuropathol 99:628–636PubMed

162.

van Ingelghem E, van Zandijcke M, Lammens M (1994) Pure autonomic failure: a new case with clinical, biochemical, and necropsy data. J Neurol Neurosurg Psychiatry 57:745–747PubMed

163.

Wakabayashi K, Furuta A, Takahashi H, Ikuta F (1989) Occurrence of neurofibrillary tangles in the celiac ganglia. Acta Neuropathol 78:448PubMed

164.

Wakabayashi K, Hayashi S, Kakita A et al (1998) Accumulation of α-synuclein/NACP is a cytopathological feature common to Lewy body disease and multiple system atrophy. Acta Neuropathol 96:445–452PubMed

165.

Wakabayashi K, Hayashi S, Morita T, Shibasaki Y, Watanabe Y, Takahashi H (1999) Neurofibrillary tangles in the peripheral sympathetic ganglia of non-Alzheimer elderly individuals. Clin Neuropathol 18:171–175PubMed

166.

Wakabayashi K, Hayashi S, Yoshimoto M, Kudo H, Takahashi H (2000) NACP/α-synuclein-positive filamentous inclusions in astrocytes and oligodendrocytes of Parkinson’s disease brains. Acta Neuropathol 99:14–20PubMed

167.

Wakabayashi K, Horikawa Y, Oyake M, Suzuki S, Morita T, Takahashi H (1998) Sporadic motor neuron disease with severe sensory neuronopathy. Acta Neuropathol 95:426–430PubMed

168.

Wakabayashi K, Takahashi H (1997) The intermediolateral nucleus and Clarke’s column in Parkinson’s disease. Acta Neuropathol 94:287–289PubMed

169.

Wakabayashi K, Takahashi H (1997) Neuropathology of autonomic nervous system in Parkinson’s disease. Eur Neurol 38(Suppl 2):2–7PubMed

170.

Wakabayashi K, Takahashi H (2006) Cellular pathology in multiple system atrophy. Neuropathology 26:338–345PubMed

171.

Wakabayashi K, Takahashi H, Obata K, Ikuta F (1992) Immunocytochemical localization of synaptic vesicle-specific protein in Lewy body-containing neurons in Parkinson’s disease. Neurosci Lett 138:237–240PubMed

172.

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 96:259–263PubMed

173.

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 79:581–583PubMed

174.

Wakabayashi K, Takahashi H, Ohama E, Takeda S, Ikuta F (1993) Lewy bodies in the visceral autonomic nervous system in Parkinson’s disease. Adv Neurol 60:609–612PubMed

175.

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 76:217–221PubMed

176.

Wakabayashi K, Tanji K, Mori F, Takahashi H (2007) The Lewy body in Parkinson’s disease: molecules implicated in the formation and degradation of α-synuclein aggregates. Neuropathology 27:494–506PubMed

177.

Wenning GK, Stefanova N, Jellinger KA, Poewe W, Schlossmacher MG (2008) Multiple system atrophy: a primary oligodendrogliopathy. Ann Neurol 64:239–246PubMed

178.

Williams AJ, Paulson HL (2008) Polyglutamine neurodegeneration: protein misfolding revisited. Trends Neurosci 31:521–528PubMed

179.

Yamada M, Hayashi S, Tsuji S, Takahashi H (2001) Involvement of the cerebral cortex and autonomic ganglia in Machado-Joseph disease. Acta Neuropathol 101:140–144PubMed

180.

Yamada M, Sato T, Tsuji S, Takahashi H (2008) CAG repeat disorder models and human neuropathology: similarities and differences. Acta Neuropathol 115:71–86PubMed

181.

Yamada M, Wood JD, Shimohata T et al (2001) Widespread occurrence of intranuclear atrophin-1 accumulation in the central nervous system neurons of patients with dentatorubral-pallidoluysian atrophy. Ann Neurol 49:14–23PubMed

182.

Yamanaka Y, Asahina M, Hiraga A, Sakakibara R, Oka H, Hattori T (2007) Over 10 years of isolated autonomic failure preceding dementia and Parkinsonism in 2 patients with Lewy body disease. Mov Disord 22:595–597PubMed

Titel: Involvement of the peripheral nervous system in synucleinopathies, tauopathies and other neurodegenerative proteinopathies of the brain
verfasst von: Koichi Wakabayashi
Fumiaki Mori
Kunikazu Tanji
Satoshi Orimo
Hitoshi Takahashi
Publikationsdatum: 01.07.2010
Verlag: Springer-Verlag
Erschienen in: Acta Neuropathologica / Ausgabe 1/2010
Print ISSN: 0001-6322
Elektronische ISSN: 1432-0533
DOI: https://doi.org/10.1007/s00401-010-0706-x

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