Pathoanatomy of cerebellar degeneration in spinocerebellar ataxia type 2 (SCA2) and type 3 (SCA3)

Cerebellum

Volumn 11, Issue 3, 2012, Pages 749-760

  Scherzed, W ^a   Brunt, E R ^b   Heinsen, H ^c   De Vos, R A ^d   Seidel, K ^a   Burk K ^e   Schols L ^e,f   Auburger, G ^a   Del Turco, D ^a   Deller, T ^a   Korf, H W ^a   Den Dunnen, W F ^b   Rub U ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d Laboratorium Pathologie Oost Nederland   (Netherlands)

^e UNIVERSITY OF TÜBINGEN   (Germany)

^f UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Cerebellum; Oculomotor system; Pathoanatomy; Polyglutamine diseases; Spinocerebellar ataxia

Indexed keywords

ADULT; AGED; ANTIBODY LABELING; ARTICLE; ASPIRATION PNEUMONIA; BRAIN ATROPHY; BRAIN TISSUE; CACHEXIA; CEREBELLUM CORTEX; CEREBELLUM DEGENERATION; CLINICAL ARTICLE; CLINICAL FEATURE; CONTROLLED STUDY; DEHYDRATION; DIAPHRAGM PARALYSIS; DYSARTHRIA; EUTHANASIA; EYE MOVEMENT DISORDER; FEMALE; GAZE; HEART ARREST; HUMAN; HUMAN TISSUE; MALE; NYSTAGMUS; PATHOGENESIS; PRIORITY JOURNAL; PURKINJE CELL; SPINOCEREBELLAR ATAXIA TYPE 2; SPINOCEREBELLAR ATAXIA TYPE 3; SPINOCEREBELLAR DEGENERATION; SUICIDE; TREMOR; URINARY TRACT INFECTION; WHITE MATTER;

ADULT; AGED; AGED, 80 AND OVER; ALLELES; ATROPHY; CEREBELLAR CORTEX; CEREBELLAR NUCLEI; CEREBELLUM; FEMALE; HUMANS; MALE; MIDDLE AGED; MYELIN SHEATH; NERVE DEGENERATION; PURKINJE CELLS; SPINOCEREBELLAR ATAXIAS; TOMOGRAPHY, X-RAY COMPUTED; YOUNG ADULT;

EID: 84864713198     PISSN: 14734222     EISSN: 14734230     Source Type: Journal    
DOI: 10.1007/s12311-011-0340-8     Document Type: Article

References (53)

1. Schöls L, Bauer P, Schmidt T, Schulte T, Riess O. Autosomal dominant cerebellar ataxias: clinical features, genetics, and pathogenesis. Lancet Neurol. 2004;3:291-304.
2. Soong BW, Paulson HL. Spinocerebellar ataxias: an update. Curr Opin Neurol. 2007;20:438-46.
3. Gilman S. The spinocerebellar ataxias. Clin Neuropharmacol. 2000;23:296-303.
4. Imbert G, Saudou F, Yvert G, Devys D, Trottier Y, Garnier JM, et al. Cloning of the gene for spinocerebellar ataxia 2 reveals a locus with high sensitivity to expanded CAG/glutamine repeats. Nat Genet. 1996;14:285-91.
5. Kawaguchi Y, Okamoto T, Taniwaki M, Aizawa M, Inoue M, Katayama S, et al. CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nat Genet. 1994;8:221-8.
6. Pulst SM, Nechiporuk A, Nechiporuk T, Gispert S, Chen XN, Lopes-Cendes I, et al. Moderate expansion of a normally biallelic trinucleotide repeat in spinocerebellar ataxia type 2. Nat Genet. 1996;14:269-76.
7. Riess O, Laccone FA, Gispert S, Schöls L, Zühlke C, Vieira- Saecker AM, et al. SCA2 trinucleotide expansion in German SCA patients. Neurogenetics. 1997;1:59-64.
8. Bürk K, Abele M, Fetter M, Dichgans J, Skalej M, Laccone F, et al. Autosomal dominant cerebellar ataxia type I-clinical features and MRI in families with SCA1, SCA2 and SCA3. Brain. 1996;119:1497-505.
9. Bürk K, Fetter M, Abele M, Laccone F, Brice A, Dichgans J, et al. Autosomal dominant cerebellar ataxia type I: oculomotor abnormalities in families with SCA1, SCA2 and SCA3. J Neurol. 1999;246:789-97.
10. Cancel G, Dürr A, Didierjean O, Imbert G, Bürk K, Lezin A, et al. Molecular and clinical correlations in spinocerebellar ataxia 2: a study of 32 families. Hum Mol Genet. 1997;6:709-15.
11. Dürr A, Smadja D, Cancel G, Lezin A, Stevanin G, Mikol J, et al. Autosomal dominant cerebellar ataxia type I in Martinique (French West Indies). Clinical and neuropathological analysis of 53 patients from three unrelated SCA2 families. Brain. 1995;118:1573-81.
12. Dürr A, Stevanin G, Cancel G, Duyckaerts C, Abbas N, Didierjean O, et al. Spinocerebellar ataxia 3 and Machado-Joseph disease: clinical, molecular, and neuropathological features. Ann Neurol. 1996;39:490-9.
13. Geschwind DH, Perlman S, Figueroa KP, Karrim J, Baloh RW, Pulst S.M. Spinocerebellar ataxia type 6. Frequency of the mutation and genotype-phenotype correlations. Neurology. 1997;49:1247-51.
14. Iwabuchi K, Tsuchiya K, Uchihara T, Yagishita S. Autosomal dominant spinocerebellar degenerations. Clinical, pathological, and genetic correlations. Rev Neurol. 1999;155:255-70.
15. Schöls L, Amoiridis G, Büttner T, Przuntek H, Epplen JT, Riess O. Autosomal dominant cerebellar ataxia: phenotypic differences in genetically defined subtypes? Ann Neurol. 1997;42:924-32.
16. Koeppen AH. The pathogenesis of spinocerebellar ataxia. Cerebellum. 2005;4:62-73.
17. Munoz E, Rey MJ, Mila M, Cardozo A, Ribalta T, Tolosa E, Ferrer I. Intranuclear inlcusions, neuronal loss and CAG mosaicism in two patients with Machado-Joseph disease. J Neurol Sci. 2002;200:19-25.
18. Rüb U, Del Turco D, Bürk K, Diaz GO, Auburger G, Mittelbronn M, et al. Extended pathoanatomical studies point to a consistent affection of the thalamus in spinocerebellar ataxia type 2. Neuropathol Appl Neurobiol. 2005;31:127-40.
19. Rüb U, Del Turco D, Del Tredici K, de Vos RA, Brunt ER, Reifenberger G, et al. Thalamic involvement in a spinocerebellar ataxia type 2 (SCA2) and a spinocerebellar ataxia type 3 (SCA3) patient, and its clinical relevance. Brain. 2003;126:2257-72.
20. Rüb U, de Vos RA, Brunt ER, Sebestény T, Schöls L, Auburger G, et al. Spinocerebellar ataxia type 3 (SCA3): thalamic neurodegeneration occurs independently from thalamic ataxin-3 immunopositive neuronal intranuclear inclusions. Brain Pathol. 2006;16:218-27.
21. Rüb U, Gierga K, Brunt ER, de Vos RA, Bauer M, Schöls L, et al. Spinocerebellar ataxias types 2 and 3: degeneration of the precerebellar nuclei isolates the three phylogenetically defined regions of the cerebellum. J Neural Transm. 2005;112:1523-45.
22. Rüb U, Seidel K, Özerden I, Gierga K, Brunt ER, Schöls L, et al. Consistent affection of the central somatosensory system in spinocerebellar ataxia type 2 and type 3 and its significance for clinical symptoms and rehabilitative therapy. Brain Res Rev. 2007;53:235-49.
23. Grinberg LT, Rüb U, Ferretti RE, Nitrini R, Farfel JM, Polichiso L, et al. The dorsal raphe nucleus shows phospho-tau neurofibrillary changes before the transentorhinal region in Alzheimer's disease. A precocious onset? Neuropathol Appl Neurobiol. 2009;35:406-15.
24. Braak H, Braak E. Demonstration of amyloid deposits and neurofibrillary changes in whole brain sections. Brain Pathol. 1991;1:213-6.
25. Smithson KG, MacVicar BA, Hatton GI. Polyethylene glycol embedding: a technique compatible with immunocytochemistry, enzyme histochemistry, histofluorescence and intracellular staining. J Neurosci Methods. 1983;7:27-41.
26. Braak H, Rüb U, Del Tredici. Involvement of precerebellar nuclei in multiple system atrophy. Neuropathol Appl Neurobiol. 2003;29:60-76.
27. Rüb U, Brunt ER, Del Turco D, de Vos RA, Gierga K, Paulson H, et al. Guidelines for the pathoanatomical examination of the lower brain stem in ingestive and swallowing disorders and its application to a dysphagic spinocerebellar ataxia type 3 patient. Neuropathol Appl Neurobiol. 2003;29:1-13.
28. Rüb U, Schultz C, Del Tredici K, Gierga K, Reifenberger G, de Vos RA, et al. Anatomically based guidelines for systematic investigation of the central somatosensory system and their application to a spinocerebellar ataxia type 2 (SCA2) patient. Neuropathol Appl Neurobiol. 2003;29:418-33.
29. Ghez C. The cerebellum. In: Kandel ER, Schwartz JH, Jessell TM, editors. Principles of neural science. 3dth ed. New York: Elsevier; 1992. p. 596-607.
30. Gilman S. Cerebellum and motor dysfunction. In: Asbury AK, McKhann GM, McDonald WI, editors. Diseases of the nervous system: clinical neurobiology. 2nd ed. Philadelphia: Saunders; 1992. p. 368-89.
31. Robertson LT, Dow R.S. Anatomy of the cerebellum. In: Schaltenbrand G,Walker AE, editors. Stereotaxy of the human brain. Stuttgart: Thieme; 1982. p. 60-70.
32. Schmahmann JD, Doyon J, McDonald D, Holmes C, Lavoie K, Hurwitz AS, et al. Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. NeuroImage. 1999;10:233-60.
33. Voogd J, Barmack NH. Oculomotor cerebellum. Prog Brain Res. 2006;151:231-68.
34. Voogd J, Feirabend HKP, Schoen J.H.R. Cerebellum and precerebellar nuclei. In: Paxinos G, editor. The human central nervous system. San Diego: Academic; 1990. p. 321-86.
35. Voogd J, Glickstein M. The anatomy of the cerebellum. Trends Neurosci. 1998;21:370-5.
36. Voogd J, Nieuwenhuys R, Van Dongen DAM, Ten Donkelhaar H.J. Mammals. In: Nieuwenhys R, Ten Donkelhaar HH, Nicholson C, editors. The central nervous system of vertebrates. Berlin: Springer; 1998. p. 1637-2097.
37. Hutchins B, Weber JT. A rapid myelin stain for frozen sections: modification of the Heidenhain procedure. J Neurosci Methods. 1983;7:289-94.
38. Riley HA. An atlas of the basal ganglia, brainstem and spinal cord. Baltimore: Williams & Wilkins; 1943.
39. Huynh D.P., Figueroa K, Hoang N, Pulst S.M. Nuclear localization or inclusion body formation of ataxin-2 are not necessary for SCA2 pathogenesis in mouse or human. Nat Genet. 2000;26:44-50.
40. Whitney ER, Kemper TL, Rosene DL, Bauman ML, Blatt G.J. Calbindin-D28k is a more reliable marker of human Purkinje cells than standard Nissl stains: a stereological experiment. J Neurosci Methods. 2008;168:42-7.
41. Bortz J, Lienert GA, Boehnke K. Verteilungsfreie methoden in der biostatistik. Berlin: Springer; 1990.
42. Rüb U, Brunt ER, de Vos RA, Del Turco D, Del Tredici K, Gierga K, et al. Degeneration of the central vestibular system in spinocerebellar ataxia type 3 (SCA3) patients and its possible clinical significance. Neuropathol Appl Neurobiol. 2004;30:402-14.
43. Rüb U, Brunt ER, Petrasch-Parwez E, Schöls L, Theegarten D, Auburger G, et al. Degeneration of ingestion-related brainstem nuclei in spinocerebellar ataxia type 2, 3, 6 and 7. Neuropathol Appl Neurobiol. 2006;32:635-49.
44. Gierga K, Schelhaas H, Brunt E, Seidel K, Scherzed W, Egensperger R, et al. Spinocerebellar ataxia type 6 (SCA6): neurodegeneration goes beyond the known brain predilection sites. Neuropathol Appl Neurobiol. 2009;35:515-27.
45. Gomez CM, Thompson RM, Gammack JT, Perlman SL, Dobyns WB, Truwit CL, et al. Spinocerebellar ataxia type 6: gaze-evoked and vertical nystagmus, Purkinje cell degeneration, and variable age of onset. Ann Neurol. 1997;42:933-50.
46. Rüb U, Brunt ER, Gierga K, Seidel K, Schultz C, Schöls L, et al. 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. 2005;15:287-95.
47. Rüb U, Brunt ER, Seidel K, Gierga K, Mooy CM, Kettner M, et al. Spinocerebellar ataxia type 7 (SCA7): widespread brain damage in an adult-onset patient with progressive visual impairments in comparison with an adult-onset patient without visual impairments. Neuropathol Appl Neurobiol. 2008;34:155-68.
48. Heinsen H, Heinsen Y.L. Serial thick, frozen, gallocyanin stained sections of human central nervous system. J Histotechnol. 1991;14:167-73.
49. Büttner U, Büttner-Ennever J.A. Present concepts of oculomotor organization. Prog Brain Res. 2006;151:1-42.
50. Horn AKE, Büttner U, Büttner-Ennever J.A. Brainstem and cerebellar structures for eye movement generation. In: Büttner U, editor. Vestibular dysfunction and its therapy. Basel: Karger; 1999. p. 1-25.
51. Leigh RJ, Zee D.S. The neurology of eye movements. 4th ed. Oxford: University Press; 2006.
52. Robinson FR, Fuchs A.F. The role of the cerebellum in voluntary eye movements. Annu Rev Neurosci. 2001;24:981-1004.
53. Streeter G. The development of the nervous system. In: Frenz K, Franklin PM, editors. Manual of human embryology. Philadelphia: Lippincott; 1912. p. 1-116.