Degeneration of the cerebellum in huntingtons disease (HD): Possible relevance for the clinical picture and potential gateway to pathological mechanisms of the disease process

Brain Pathology

Volumn 23, Issue 2, 2013, Pages 165-177

  Rüb, Udo ^a   Hoche, Franziska ^a   Brunt, Ewout R ^b   Heinsen, Helmut ^c   Seidel, Kay ^a   Del Turco, Domenico ^a   Paulson, Henry L ^d   Bohl, Jürgen ^e   Von Gall, Charlotte ^f   Vonsattel, Jean Paul ^g   Korf, Horst Werner ^a   Den Dunnen, Wilfred F ^b  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e JOHANNES GUTENBERG UNIVERSITY   (Germany)

^f HEINRICH HEINE UNIVERSITY   (Germany)

^g Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

cerebellum; Huntington's disease; neurodegeneration; pathoanatomy; polyglutamine diseases

Indexed keywords

ADULT; AGED; ARTICLE; CELL LOSS; CEREBELLUM ATROPHY; CEREBELLUM DEGENERATION; CLINICAL ARTICLE; CORPUS STRIATUM; DENTATE NUCLEUS; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE SEVERITY; FASTIGIAL NUCLEUS; FEMALE; HUMAN; HUNTINGTON CHOREA; INTERPOSITUS NUCLEUS; MALE; PURKINJE CELL; ATROPHY; CEREBELLUM; MIDDLE AGED; PATHOLOGY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ATROPHY; CEREBELLUM; CORPUS STRIATUM; DISEASE PROGRESSION; FEMALE; HUMANS; HUNTINGTON DISEASE; MALE; MIDDLE AGED; PURKINJE CELLS;

EID: 84874495861     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/j.1750-3639.2012.00629.x     Document Type: Article

References (70)

1. Bortz J, Lienert GA, Boehnke K, (1990) Verteilungsfreie Methoden in der Biostatistik. Springer: Berlin.
2. Braak E, Braak H, Mandelkow EM, (1994) A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol 87: 554-567.
3. Braak H, Braak E, (1992) The human entorhinal cortex: normal morphology and lamina-specific pathology in various diseases. Neurosci Res 15: 6-31.
4. Braak H, Rüb U, Del Tredici K, (2003) Involvement of precerebellar nuclei in multiple system atrophy. Neuropathol Appl Neurobiol 29: 60-76.
5. Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Del Tredici K, (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112: 389-404.
6. Bruyn GW, Bots GTAM, Dom R, (1979) Huntington's chorea: current neuropathological status. Adv Neurol 23: 83-93.
7. Davies JE, Sarkar S, Rubinsztein DC, (2007) The ubiquitin proteasome system in Huntington's disease and the spinocerebellar ataxias. BMC Biochem 8 (Suppl.): 1-8.
8. Deuschl G, Lücking CH, Schenck E, (1989) Hand muscle reflexes following electrical stimulation in choreatic movement disorders. J Neurol Neurosurg Psychiatry 52: 755-762.
9. De Vos KJ, Grierson AJ, Ackerley S, Miller CCJ, (2008) Role of axonal transport in neurodegenerative diseases. Annu Rev Neurosci 31: 1151-1173.
10. Dickson DW, (1999) Neuropathologic differentiation of progressive supranuclear palsy and corticobasal degeneration. J Neurol 246 (Suppl. 2): 6-15.
11. Fennema-Notestine C, Archibald SL, Jacobson MW, Corey-Bloom J, Paulsen JS, Peavy GM, et al (2004) In vivo evidence of cerebellar atrophy and cerebral white matter loss in Huntington disease. Neurology 63: 989-995.
12. Folstein SE, (1989) Huntington's Disease: A Disorder of Families. Johns Hopkins University: Baltimore.
13. Fujino Y, DeLucia MW, Davies P, Dickson DW, (2004) Ballooned neurons in the limbic lobe are associated with Alzheimer type pathology and lack diagnostic specificity. Neuropathol Appl Neurobiol 30: 676-682.
14. Ghez C, (1991) The cerebellum. In: Principles of Neural Science, 3rd edn., ER Kandel, JH Schwartz, TM Jessell, (eds), pp. 596-607. Elsevier: New York.
15. Gil JM, Rego AC, (2008) Mechanisms of neurodegeneration in Huntington's disease. Eur J Neurosci 27: 2803-2820.
16. Gilman S, (1992) Cerebellum and motor dysfunction. In: Diseases of the Nervous System: Clinical Neurobiology, 2nd edn., AK Asbury, GM McKhann, WI McDonald, (eds), pp. 368-389. Saunders: Philadelphia.
17. Graeber MB, Moran LB, (2002) Mechanisms of cell death in neurodegenerative diseases: fashion, fiction, and facts. Brain Pathol 12: 385-390.
18. Grinberg LT, Heinsen H, (2009) Argyrophilic grain disease. An update on a frequent cause of dementia. Dement Neuropsych 3: 2-7.
19. Gunawardena S, Goldstein LSB, (2005) Polyglutamine diseases and transport problems. Arch Neurol 62: 46-51.
20. Harper PS, (1992) The epidemiology of Huntington's disease. Hum Genet 89: 365-376.
21. Heinsen H, Rüb U, (1997) Quantitative investigations of neural circuits in Huntington's disease. J Neural Transm 104: 1139-1140.
22. Heinsen H, Strik M, Bauer M, Luther K, Ulmar G, Gangnus D, et al (1994) Cortical and striatal neurone number in Huntington's disease. Acta Neuropathol 88: 320-333.
23. Horn AK, Büttner U, Büttner-Ennever JA, (1999) Brainstem and cerebellar structures for eye movement generation. Adv Otorhinolaryngol 55: 1-25.
24. Hutchins B, Weber JT, (1983) A rapid myelin stain for frozen sections: modification of the Heidenhain procedure. J Neurosci Methods 7: 289-294.
25. Jeste DV, Barban L, Parisi J, (1984) Reduced Purkinje cell density in Huntington's disease. Exp Neurol 85: 78-86.
26. Kato S, Hirano A, Umahara T, Llena JF, Herz F, Ohama E, (1992) Ultrastructural and immunohistochemical studies on ballooned cortical neurons in Creutzfeldt-Jakob disease: expression of αB-crystallin, ubiquitin and stress-response protein 27. Acta Neuropathol 84: 443-448.
27. Koller WC, Trimble J, (1985) The gait abnormality of Huntington's disease. Neurology 35: 1450-1454.
28. Knikou M, (2008) The H-reflex as a probe: pathways and pitfalls. J Neurosci Methods 171: 1-12.
29. Kremer B, Weber B, Hayden MR, (1992) New insights into the clinical features, pathogenesis and molecular genetics of Huntington disease. Brain Pathol 2: 321-335.
30. Lange H, Thorner G, Hopf A, Schroder KF, (1976) Morphometric studies of the neuropathological changes in choreatic diseases. J Neurol Sci 28: 401-425.
31. Lange HW, (1981) Quantitative changes of telencephalon, diencephalon, and mesencephalon in Huntington's chorea, postencephalitic, and idiopathic Parkinsonism. Verh Anat Ges 73: 923-925.
32. Lasker AG, Zee DS, (1997) Ocular motor abnormalities in Huntington's disease. Vision Res 37: 3639-3645.
33. Lastres-Becker I, Rüb U, Auburger G, (2008) Spinocerebellar ataxia 2 (SCA2). Cerebellum 7: 115-124.
34. Margolis RL, Ross CA, (2003) Diagnosis of Huntington disease. Clin Chem 49: 1726-1732.
35. McLeod JG, (1969) H-reflex studies in patients with cerebellar disorders. J Neurol Neurosurg Psychiatry 32: 21-27.
36. Mink JW, (1996) The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50: 381-425.
37. Misiaszek JE, (2003) The H-reflex as a tool in neurophysiology: its limitations and uses in understanding nervous system function. Muscle Nerve 28: 144-160.
38. Myers RH, Vonsattel JP, Stevens TJ, Cupples LA, Richardson EP, Martin JB, Bird ED, (1988) Clinical and neuropathologic assessment of severity in Huntington's disease. Neurology 38: 341-347.
39. Oepen G, Hillesheimer W, (1981) Qualitative H-reflex testing in Huntington's disease. Arch Psychiatr Nervenkr 230: 221-226.
40. Oliveira JMA, (2010) Nature and cause of mitochondrial dysfunction in Huntington's disease: focusing on huntingtin and the striatum. J Neurochem 114: 1-12.
41. Pandey M, Mohanakumar KP, Usha R, (2010) Mitochondrial functional alterations in relation to pathophysiology of Huntington's disease. J Bioenerg Biomembr 42: 217-226.
42. Pattison LR, Kotter MR, Fraga D, Bonelli RM, (2006) Apoptotic cascades as possible targets for inhibiting cell death in Huntington's disease. J Neurol 253: 1137-1142.
43. Petersen A, Gil J, Maat-Schieman ML, Bjorkqvist M, Tanila H, Araujo IM, et al (2005) Orexin loss in Huntington's disease. Hum Mol Genet 14: 39-47.
44. Riess O, Rüb U, Pastore A, Bauer P, Schöls L, (2008) SCA3: neurological features, pathogenesis and animal models. Cerebellum 7: 125-137.
45. Robinson FR, Fuchs AF, (2001) The role of the cerebellum in voluntary eye movements. Annu Rev Neurosci 24: 981-1004.
46. Rodda RA, (1981) Cerebellar atrophy in Huntington's disease. J Neurol Sci 50: 147-157.
47. Roos RAC, (1986) Neuropathology of Huntington's chorea. In: Handbook of Clinical Neurology Vol. 5. Extrapyramidal Disorders, PJ Vinken, GW Bruyn, HL Klawans, (eds), pp. 315-325. Elsevier Science Publishers: Amsterdam.
48. Rosas HD, Koroshetz WJ, Chen YI, Skeuse C, Vangel M, Cudkowicz ME, Kaplan K, (2003) Evidence for more widespread cerebral pathology in early HD: an MRI-based morphometric analysis. Neurology 60: 1615-1620.
49. Ross CA, Tabrizi SJ, (2011) Huntington's disease: from molecular pathogenesis to clinical treatment. Lancet Neurol 10: 83-98.
50. Rüb U, Brunt ER, Gierga K, Seidel K, Schultz C, Schöls L, et al (2005) Spinocerebellar ataxia type 7 (SCA7): first report of a systematic neuropathological study of the brain of a patient with a very short expanded CAG-repeat. Brain Pathol 15: 287-295.
51. Rüb U, Brunt ER, Deller T, (2008) New insights into the pathoanatomy of spinocerebellar ataxia type 3 (Machado-Joseph disease). Curr Opin Neurol 21: 111-116.
52. Rüb U, Heinsen H, Brunt ER, Landwehrmeyer B, den, Dunnen WF, Gierga K, Deller T, (2009) The human premotor oculomotor brainstem system-can it help to understand oculomotor symptoms in Huntington's disease? Neuropathol Appl Neurobiol 35: 4-15.
53. Schmahmann JD, Doyon J, McDonald D, Holmes C, Lavoie K, Hurwitz AS, et al (1999) Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. Neuroimage 10: 233-260.
54. Smithson KG, MacVicar BA, Hatton GI, (1983) Polyethylene glycol embedding: a technique compatible with immunocytochemistry, enzyme histochemistry, histofluorescence and intracellular staining. J Neurosci Methods 7: 27-41.
55. Stover NP, Watts RL, (2001) Corticobasal degeneration. Semin Neurol 21: 49-58.
56. The Huntington's Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72: 971-983.
57. Thorner GW, Lange HW, Hopf A, (1977) Quantitative studies of human basal ganglia in extrapyramidal motor disorders. Verh Anat Ges 71: 99-101.
58. Trottier Y, Devys D, Imbert G, Saudou F, An I, Lutz Y, et al (1995) Cellular localization of the Huntington's disease protein and discrimination of the normal and mutated form. Nat Genet 10: 104-110.
59. Trottier Y, Lutz Y, Stevanin G, Imbert G, Devys D, Cancel G, et al (1995) Polyglutamine expansion as a pathological epitope in Huntington's disease and four dominant cerebellar ataxias. Nature 378: 403-406.
60. Vonsattel JP, (2008) Huntington disease models and human neuropathology: similarities and differences. Acta Neuropathol 115: 55-69.
61. Vonsattel JP, DiFiglia M, (1998) Huntington disease. J Neuropathol Exp Neurol 57: 369-384.
62. Vonsattel JP, Myers RH, Stevens TJ, Ferrante RJ, Bird ED, Richardson EP Jr, (1985) Neuropathological classification of Huntington's disease. J Neuropathol Exp Neurol 44: 559-577.
63. Voogd J, (2003) The human cerebellum. J Chem Neuroanat 26: 243-252.
64. Voogd J, Barmack NH, (2006) Oculomotor cerebellum. Prog Brain Res 151: 231-268.
65. Voogd J, Feirabend HKP, Schoen JHR, (1990) Cerebellum and precerebellar nuclei. In: The Human Central Nervous System, G Paxinos, (ed.), pp. 321-386. Academic Press: San Diego.
66. Voogd J, Schraa-Tam CKL, van der, Geest JN, De Zeeuw CI, (2012) Visuomotor cerebellum in human and nonhuman primates. Cerebellum 11: 392-410.
67. Walker FO, (2007) Huntington's disease. Lancet 369: 218-228.
68. Walker FO, (2007) Huntington's disease. Semin Neurol 27: 143-150.
69. Whitney ER, Kemper TL, Rosene DL, Bauman ML, Blatt GJ, (2008) Calbindin-D28k is a more reliable marker of human Purkinje cells than standard Nissl stains: a stereological experiment. J Neurosci Methods 168: 42-47.
70. Yanagisawa N, (1992) The spectrum of motor disorders in Huntington's disease. Clin Neurol Neurosurg 94 (Suppl.): 182-184.