Huntington's disease (HD): the neuropathology of a multisystem neurodegenerative disorder of the human brain

Brain Pathology

Volumn 26, Issue 6, 2016, Pages 726-740

  Rub U ^a   Seidel, K ^a   Heinsen, H ^b,c   Vonsattel, J P ^d   den Dunnen, W F ^e   Korf, H W ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF WÜRZBURG   (Germany)

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

^e UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

brainstem; cerebellum; cerebral cortex; pathoanatomy; polyglutamine diseases; thalamus

Indexed keywords

POLYGLUTAMINE; HTT PROTEIN, HUMAN; HUNTINGTIN; P62 PROTEIN, HUMAN; PEPTIDE; RNA BINDING PROTEIN;

ALLOCORTEX; ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; BRAIN ATROPHY; BRAIN STEM; CAG REPEAT; CAUDATE NUCLEUS; CEREBELLUM; CLINICAL FEATURE; CORPUS STRIATUM; DEGENERATIVE DISEASE; GLOBUS PALLIDUS; HUMAN; HUMAN TISSUE; HUNTINGTON CHOREA; NEOCORTEX; NERVE DEGENERATION; NEUROPATHOLOGY; PATHOLOGICAL ANATOMY; PATHOPHYSIOLOGY; PUTAMEN; SPINOCEREBELLAR DEGENERATION; SYSTEMIC DISEASE; THALAMUS NUCLEUS; BRAIN; COMPLICATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY;

BRAIN; GENE EXPRESSION REGULATION; HUMANS; HUNTINGTIN PROTEIN; HUNTINGTON DISEASE; NEURODEGENERATIVE DISEASES; PEPTIDES; RNA-BINDING PROTEINS;

EID: 84996969463     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/bpa.12426     Document Type: Article

References (82)

1. Alzheimer A (1911) Über die anatomische Grundlage der Huntington'schen Chorea und der choreatischen Bewegung überhaupt. Neurol Centralblatt 30:891–892.
2. Andrew SE, Goldberg YP, Kremer B, Telenius H, Theilmann J, Adam S et al (1993) The relationship between trinucleotide (CAG) repeat length and clinical features of Huntington's disease. Nat Genet 4:398–403.
3. Atkin G, Paulson H (2014) Ubiquitin pathways in neurodegenerative disease. Front Mol Neurosci 7:63.
4. Aziz NA, van der Marck MA, Pijl H, Olde Rikkert MG, Bloem BR, Roos RA (2008) Weight loss in neurodegenerative disorders. J Neurol 255:1872–1880.
5. Borrell-Pagès M, Zala D, Humbert S, Saudou F (2006) Huntington's disease: from huntingtin function and dysfunction to therapeutic strategies. Cell Mol Life Sci 63:2642–2660.
6. Braak H, Braak E (1992) The human entorhinal cortex: normal morphology and lamina-specific pathology in various diseases. Neurosci Res 15:6–31.
7. Braak H, Braak E (1992) Allocortical involvement in Huntington's disease. Neuropathol Appl Neurobiol 18:539–547.
8. Brodmann K (1909) Vergleichende Lokalisationslehre der Großhirnrinde. Johann Ambrosius Barth: Leipzig.
9. Brundin P, Melki R, Kopito R (2010) Prion-like transmission of protein aggregates in neurodegenerative diseases. Nat Rev Mol Cell Biol 11:301–307.
10. Bruyn GW, Bots GTAM, Dom R (1979) Huntington's chorea: current neuropathological status. Adv Neurol 23:83–93.
11. Costanzo M, Zurzolo C (2013) The cell biology of prion-like spread of protein aggregates: mechanisms and implication in neurodegeneration. Biochem J 452:1–17.
12. De la Monte SM, Vonsattel JP, Richardson EP Jr (1988) Morphometric demonstration of atrophic changes in the cerebral cortex, white matter, and neostriatum in Huntington's disease. J Neuropathol Exp Neurol 47:516–525.
13. De Vos KJ, Grierson AJ, Ackerley S, Miller CCJ (2008) Role of axonal transport in neurodegenerative diseases. Annu Rev Neurosci 31:1151–1173.
14. Dickson DW (1999) Neuropathologic differentiation of progressive supranuclear palsy and corticobasal degeneration. J Neurol 246:6–15.
15. Dom R, Malfroid M, Baro F (1976) Neuropathology of Huntington's chorea. Studies of the ventrobasal complex of the thalamus. Neurology 26:64–68.
16. Dunlap CB (1927) Pathologic changes in Huntington's chorea: with special reference to the corpus striatum. Arch Neurol Psychiatry 18:867–943.
17. Duyao M, Ambrose C, Myers R, Novelletto A, Persichetti F, Frontali M et al (1993) Trinucleotide repeat length instability and age of onset in Huntington's disease. Nat Genet 4:387–392.
18. Estrada-Sanchez AM, Rebec GV (2013) Role of cerebral cortex in the neuropathology of Huntington's disease. Front Neural Circuits 7:19.
19. Gabery S, Murphy K, Schultz K, Loy CT, McCusker E, Kirik D et al (2010) Changes in key hypothalamic neuropeptide populations in Huntington disease revealed by neuropathological analyses. Acta Neuropathol 120:777–788.
20. Gil JM, Rego AC (2008) Mechanisms of neurodegeneration in Huntington's disease. Eur J Neurosci 27:2803–2820.
21. Goedert M, Clavaguera F, Tolnay M (2010) The propagation of prion-like protein inclusions in neurodegenerative diseases. Trend Neurosci 33:317–325.
22. Graeber MB, Moran LB (2002) Mechanisms of cell death in neurodegenerative diseases: fashion, fiction, and facts. Brain Pathol 12:385–390.
23. Grimbergen YA, Knol MJ, Bloem BR, Kremer BP, Roos RA, Munneke M (2008) Falls and gait disturbances in Huntington's disease. Mov Disord 23:970–976.
24. Grinberg LT, Heinsen H (2009) Argyrophilic grain disease. An update on a frequent cause of dementia. Dement Neuropsych 3:2–7.
25. Harper PS (1992) The epidemiology of Huntington's disease. Hum Genet 89:365–376.
26. Heathfield KW (1973) Huntington's chorea: a centenary review. Postgrad Med J 49:32–45.
27. Hedreen JC, Peyser CE, Folstein SE, Ross CA (1991) Neuronal loss in layers V and VI of cerebral cortex in Huntington's disease. Neurosci Lett 133:257–261.
28. Heinsen H, Bauer M, Ulmar G, Gangnus D, Jungkunz G (1992) The entorhinal region in Huntington's disease: a cytoarchitectonic and quantitative investigation in five cases. Clin Neuropathol 11:226–226.
29. Heinsen H, Rüb U (1997) Quantitative investigations of neural circuits in Huntington's disease. J Neural Transm 104:1139–1140.
30. Heinsen H, Rüb U, Bauer M, Ulmar G, Bethke B, Schüler M et al (1999) Nerve cell loss in the thalamic mediodorsal nucleus in Huntington's disease. Acta Neuropathol 97:613–622.
31. Heinsen H, Rüb U, Gangnus D, Jungkunz G, Bauer M, Ulmar G et al (1996) Nerve cell loss in the thalamic centromedian-parafascicular complex in patients with Huntington's disease. Acta Neuropathol 91:161–168.
32. 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.
33. Hirai T, Jones EG (1989) A new parcellation of the human thalamus on the basis of histochemical staining. Brain Res Rev 14:1–34.
34. Hunt JR (1917) Progressive atrophy of the globus pallidus. Brain 40:58–148.
35. Huntington G (1872) On chorea. Med Surg Reporter 26:317–321.
36. Imarisio S, Carmichael J, Korolchuk V, Chen CW, Saiki S, Rose C et al (2008) Huntington's disease: from pathology and genetics to potential therapies. Biochem J 412:191–209.
37. Jelgersma G (1908) Über anatomische Befunde bei Paralyis agitans und bei chronischer Chorea. Neurol Centralblatt 27:995–996.
38. Jones EG (1985) The Thalamus. Plenum Press: New York, London.
39. Jucker M, Walker LC (2011) Pathogenic protein seeding in Alzheimer disease and other neurodegenerative disorders. Ann Neurol 70:532–540.
40. Lange H, Thorner G, Hopf A, Schröder KF (1976) Morphometric studies of the neuropathological changes in choreatic diseases. J Neurol Sci 28:401–425.
41. Lange HW (1981) Quantitative changes of telencephalon, diencephalon, and mesencephalon in Huntington's chorea, postencephalitic, and idiopathic Parkinsonism. Verh Anat Ges 73:923–925.
42. Lange HW, Aulich A (1986) Die Hirnatrophie bei der Huntingtonschen Krankheit. In: Die Huntingtonsche Krankheit. H Oepen (ed), pp. 25–41. Hippokrates: Stuttgart.
43. Lanska DJ (2000) George Huntington (1850-1916) and hereditary chorea. J Hist Neurosci 9:76–89.
44. Lanska DJ (2010) The history of movement disorders. In: Handbook of Clinical Neurology, Vol. 95. Finger S, Boller F, Tyler KL (eds), pp. 501–546. Elsevier: Amsterdam.
45. Lasker AG, Zee DS (1997) Ocular motor abnormalities in Huntington's disease. Vis Res 37:3639–3645.
46. Leigh RJ, Newman SA, Folstein SE, Lasker AG, Jensen BA (1983) Abnormal ocular motor control in Huntington's disease. Neurology 33:1268–1275.
47. Leigh RJ, Zee DS (2006) The Neurology of Eye Movements, 4th edn. Oxford University Press: Oxford.
48. Li JY, Conforti L (2013) Axonopathy in Huntington's disease. Exp Neurol 246:62–71.
49. Li XJ, Li S (2011) Proteasomal dysfunction in aging and Huntington disease. Neurobiol Dis 43:4–8.
50. Mann DM, Oliver R, Snowden JS (1993) The topographic distribution of brain atrophy in Huntington's disease and progressive supranuclear palsy. Acta Neuropathol 85:553–559.
51. Margolis RL, Ross CA (2003) Diagnosis of Huntington disease. Clin Chem 49:1726–1732.
52. McCaughey WTE (1961) The pathologic spectrum of Huntington's chorea. J Nerv Ment Dis 133:91–103.
53. Millecamps S, Julien JP (2013) Axonal transport deficits and neurodegenerative diseases. Nat Rev Neurosci 14:161–176.
54. Morel A, Magnin M, Jeanmonod D (1997) Multiarchitectonic and stereotactic atlas of the human thalamus. J Comp Neurol 387:588–630.
55. Myers RH (2004) Huntington's disease genetics. NeuroRx 1:255–262.
56. 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.
57. Norrby E (2011) Prions and protein-folding diseases. J Intern Med 270:1–14.
58. 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.
59. Rüb U, Hoche F, Brunt ER, Heinsen H, Seidel K, Del Turco D et al (2013) Degeneration of the cerebellum in Huntington's disease (HD): possible relevance for the clinical picture and potential gateway to pathological mechanisms of the disease process. Brain Pathol 23:165–177.
60. Rüb U, Hentschel M, Stratmann K, Brunt E, Heinsen H, Seidel K et al (2014) Huntington's disease (HD): degeneration of select nuclei, widespread occurrence of neuronal nuclear and axonal inclusions in the brainstem. Brain Pathol 24:247–260.
61. Rüb U, Jen JC, Braak H, Deller T (2008) Functional neuroanatomy of the human premotor oculomotor brainstem nuclei: insights from postmortem and advanced in vivo imaging studies. Exp Brain Res 187:167–180.
62. Rüb U, Schöls L, Paulson H, Auburger G, Kermer P, Jen JC et al (2013) Clinical features, neurogenetics and neuropathology of the polyglutamine spinocerebellar ataxias type 1, 2, 3, 6 and 7. Prog Neurobiol 104:38–66.
63. Rüb U, Seidel K, Vonsattel JP, Lange HW, Eisenmenger W, Götz M et al (2014) Huntington's disease (HD): neurodegeneration of Brodmann's primary visual area 17 (BA17). Brain Pathol 25:701–711.
64. Rüb U, Vonsattel JPG, Heinsen H, Korf HW (2015) The neuropathology of Huntington's disease: classical findings, recent developments and correlation to functional neuroanatomy. Adv Anat Embryol Cell Biol 217:1–146.
65. Seidel K, Siswanto S, Brunt ER, den Dunnen W, Korf HW, Rüb U (2012) Brain pathology of spinocerebellar ataxias. Acta Neuropathol 124:1–21.
66. Sheperd GM (2013) Corticostriatal connectivity and its role in disease. Nat Rev Neurosci 14:278–291.
67. Shoulson I, Young AB (2011) Milestones in Huntington disease. Mov Disord 26:1127–1133.
68. Sieradzan KA, Mann DM (2001) The selective vulnerability of nerve cells in Huntington's disease. Neuropathol Appl Neurobiol 27:1–21.
69. Sotrel A, Paskevich PA, Kiely DK, Bird ED, Williams RS, Myers RH (1991) Morphometric analysis of the prefrontal cortex in Huntington's disease. Neurology 41:1117–1121.
70. Stier E (1903) Zur pathologischen Anatomie der Huntingtonschen Chorea. Arch F Psychol 37:62–86.
71. Stone TT, Falstein EI (1938) Pathology of Huntington's chorea. J Nerv Ment Dis 88:602–628.
72. Tanner CM, Goldman SM (1994) Epidemiology of movement disorders. Curr Opin Neurol 7:340–345.
73. 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.
74. Thu DC, Oorschot DE, Tippett LJ, Nana AL, Hogg VM, Synek BJ, Luthi-Carter R, Waldvogel HJ, Faull RL (2010) Cell loss in the motor and cingulate cortex correlates with symptomatology in Huntington's disease. Brain 133:1094–1110
75. van Wamelen DJ, Aziz NA, Roos RA, Swaab DF (2014) Hypothalamic alterations in Huntington's disease patients: comparison with genetic rodent models. J Neuroendocrinol 26:761–775.
76. Vogt C, Vogt O (1920) Zur Lehre der Erkrankungen des striären Systems. J Psychol Neurol 25:631–846.
77. Vogt C, Vogt O (1942) Morphologische Gestaltungen unter normalen und pathogenen Bedingungen. Ein hirnanatomischer Beitrag zu ihrer Kenntnis. J Psychol Neurol 50:161–524.
78. Vonsattel JP (2008) Huntington disease models and human neuropathology: similarities and differences. Acta Neuropathol 115:55–69.
79. Vonsattel JP, DiFiglia M (1998) Huntington disease. J Neuropathol Exp Neurol 57:369–384.
80. 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.
81. Walker FO (2007) Huntington's disease. Semin Neurol 27:143–150.
82. Walker FO (2007) Huntington's disease. Lancet 369:218–228.