Polyglutamine aggregation in Huntington's disease and spinocerebellar ataxia type 3: Similar mechanisms in aggregate formation

Neuropathology and Applied Neurobiology

Volumn 42, Issue 2, 2016, Pages 153-166

  Seidel, K ^a   Siswanto, S ^a   Fredrich, M ^a   Bouzrou, M ^a   Brunt, E R ^b   van Leeuwen, F W ^d   Kampinga, H H ^b   Korf, H W ^a   Rub U ^a   den Dunnen, W F A ^c  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Huntington's disease; Polyglutamine; Protein aggregation; Protein quality control; Spinocerebellar ataxia

Indexed keywords

POLYGLUTAMINE; PROTEIN AGGREGATE; PEPTIDE;

ADULT; AGED; ARTICLE; BRAIN REGION; CAG REPEAT; CAUDATE NUCLEUS; CELL NUCLEUS INCLUSION BODY; CELLULAR STRESS RESPONSE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOPLASM; DISEASE SEVERITY; FEMALE; FRONTAL CORTEX; HUMAN; HUMAN TISSUE; HUNTINGTON CHOREA; IMMUNOHISTOCHEMISTRY; MALE; MOLECULAR MECHANICS; NERVE CELL; NERVE DEGENERATION; NERVE FIBER; ONSET AGE; PERIKARYON; PONS; PONTINE NUCLEUS; PRIORITY JOURNAL; PROTEIN AGGREGATION; SPINOCEREBELLAR ATAXIA TYPE 3; SPINOCEREBELLAR DEGENERATION; UPREGULATION; BRAIN; MACHADO JOSEPH DISEASE; METABOLISM; MIDDLE AGED; PATHOLOGY; PROTEINOSIS; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; BRAIN; FEMALE; HUMANS; HUNTINGTON DISEASE; IMMUNOHISTOCHEMISTRY; INTRANUCLEAR INCLUSION BODIES; MACHADO-JOSEPH DISEASE; MALE; MIDDLE AGED; NERVE DEGENERATION; NEURONS; PEPTIDES; PROTEIN AGGREGATION, PATHOLOGICAL;

EID: 84959220863     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/nan.12253     Document Type: Article

References (54)

1. Paulson HL. Protein fate in neurodegenerative proteinopathies: polyglutamine diseases join the (mis)fold. Am J Hum Genet 1999; 2: 339-345
2. Williams AJ, Paulson HL. Polyglutamine neurodegeneration: protein misfolding revisited. Trends Neurosci 2008; 10: 521-528
3. Orr HT, Zoghbi HY. Trinucleotide repeat disorders. Annu Rev Neurosci 2007; 30: 575-621
4. Walker FO. Huntington's disease. Semin Neurol 2007; 2: 143-150
5. Rubinsztein DC, Barton DE, Davison BC, Ferguson-Smith MA. Analysis of the huntingtin gene reveals a trinucleotide-length polymorphism in the region of the gene that contains two CCG-rich stretches and a correlation between decreased age of onset of Huntington's disease and CAG repeat number. Hum Mol Genet 1993; 10: 1713-1715
6. Imarisio S, Carmichael J, Korolchuk V, Chen CW, Saiki S, Rose C, Krishna G, Davies JE, Ttofi E, Underwood BR, Rubinsztein DC. Huntington's disease: from pathology and genetics to potential therapies. Biochem J 2008; 2: 191-209
7. Myers RH. Huntington's disease genetics. NeuroRx 2004; 2: 255-262
8. Rub U, Hoche F, Brunt ER, Heinsen H, Seidel K, Del Turco D, Paulson HL, Bohl J, von Gall C, Vonsattel JP, Korf HW, den Dunnen WF. 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 2013; 2: 165-177
9. den Dunnen WF. Neuropathological diagnostic considerations in hyperkinetic movement disorders. Front Neurol 2013; 4: 7
10. Rub U, Heinsen H, Brunt ER, Landwehrmeyer B, den Dunnen WF, Gierga K, Deller T. The human premotor oculomotor brainstem system - can it help to understand oculomotor symptoms in Huntington's disease? Neuropathol Appl Neurobiol 2009; 1: 4-15
11. Vonsattel JP, Myers RH, Stevens TJ, Ferrante RJ, Bird ED, Richardson EP Jr. Neuropathological classification of Huntington's disease. J Neuropathol Exp Neurol 1985; 6: 559-577
12. Rub U, Hentschel M, Stratmann K, Brunt E, Heinsen H, Seidel K, Bouzrou M, Auburger G, Paulson H, Vonsattel JP, Lange H, Korf HW, den Dunnen W. Huntington's disease (HD): degeneration of select nuclei, widespread occurrence of neuronal nuclear and axonal inclusions in the brainstem. Brain Pathol 2014; 3: 247-260
13. Rub U, Seidel K, Vonsattel J, Lange H, Eisenmenger W, Gotz M, Del TD, Bouzrou M, Korf H, Heinsen H. Huntington's disease (HD): neurodegeneration of Brodmann's primary visual area 17 (BA17). Brain Pathol 2014.
14. Kawaguchi Y, Okamoto T, Taniwaki M, Aizawa M, Inoue M, Katayama S, Kawakami H, Nakamura S, Nishimura M, Akiguchi I. CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nat Genet 1994; 3: 221-228
15. Winborn BJ, Travis SM, Todi SV, Scaglione KM, Xu P, Williams AJ, Cohen RE, Peng J, Paulson HL. The deubiquitinating enzyme ataxin-3, a polyglutamine disease protein, edits Lys63 linkages in mixed linkage ubiquitin chains. J Biol Chem 2008; 39: 26436-26443
16. Durcan TM, Kontogiannea M, Thorarinsdottir T, Fallon L, Williams AJ, Djarmati A, Fantaneanu T, Paulson HL, Fon EA. The Machado-Joseph disease-associated mutant form of ataxin-3 regulates parkin ubiquitination and stability. Hum Mol Genet 2011; 1: 141-154
17. Schols L, Bauer P, Schmidt T, Schulte T, Riess O. Autosomal dominant cerebellar ataxias: clinical features, genetics, and pathogenesis. Lancet Neurol 2004; 5: 291-304
18. Seidel K, Siswanto S, Brunt ER, den Dunnen W, Korf HW, Rub U. Brain pathology of spinocerebellar ataxias. Acta Neuropathol 2012; 1: 1-21
19. Rub U, Schols L, Paulson H, Auburger G, Kermer P, Jen JC, Seidel K, Korf HW, Deller T. Clinical features, neurogenetics and neuropathology of the polyglutamine spinocerebellar ataxias type 1, 2, 3, 6 and 7. Prog Neurobiol 2013; 104: 38-66
20. Rub U, Brunt ER, Petrasch-Parwez E, Schols L, Theegarten D, Auburger G, Seidel K, Schultz C, Gierga K, Paulson H, van Broeckhoven C, Deller T, de Vos RA. Degeneration of ingestion-related brainstem nuclei in spinocerebellar ataxia type 2, 3, 6 and 7. Neuropathol Appl Neurobiol 2006; 6: 635-649
21. Scherzed W, Brunt ER, Heinsen H, de Vos RA, Seidel K, Burk K, Schols L, Auburger G, Del Turco D, Deller T, Korf HW, den Dunnen WF, Rub U. Pathoanatomy of cerebellar degeneration in spinocerebellar ataxia type 2 (SCA2) and type 3 (SCA3). Cerebellum 2012; 3: 749-760
22. Zijlstra MP, Rujano MA, Van Waarde MA, Vis E, Brunt ER, Kampinga HH. Levels of DNAJB family members (HSP40) correlate with disease onset in patients with spinocerebellar ataxia type 3. Eur J Neurosci 2010; 5: 760-770
23. Gunawardena S, Goldstein LS. Polyglutamine diseases and transport problems: deadly traffic jams on neuronal highways. Arch Neurol 2005; 1: 46-51
24. Seidel K, den Dunnen WF, Schultz C, Paulson H, Frank S, de Vos RA, Brunt ER, Deller T, Kampinga HH, Rub U. Axonal inclusions in spinocerebellar ataxia type 3. Acta Neuropathol 2010; 4: 449-460
25. Schmidt T, Lindenberg KS, Krebs A, Schols L, Laccone F, Herms J, Rechsteiner M, Riess O, Landwehrmeyer GB. Protein surveillance machinery in brains with spinocerebellar ataxia type 3: redistribution and differential recruitment of 26S proteasome subunits and chaperones to neuronal intranuclear inclusions. Ann Neurol 2002; 3: 302-310
26. McCampbell A, Taylor JP, Taye AA, Robitschek J, Li M, Walcott J, Merry D, Chai Y, Paulson H, Sobue G, Fischbeck KH. CREB-binding protein sequestration by expanded polyglutamine. Hum Mol Genet 2000; 14: 2197-2202
27. Paulson HL, Perez MK, Trottier Y, Trojanowski JQ, Subramony SH, Das SS, Vig P, Mandel JL, Fischbeck KH, Pittman RN. Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3. Neuron 1997; 2: 333-344
28. Arrasate M, Mitra S, Schweitzer ES, Segal MR, Finkbeiner S. Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 2004; 7010: 805-810
29. Arrasate M, Finkbeiner S. Protein aggregates in Huntington's disease. Exp Neurol 2012; 1: 1-11
30. Seidel K, Meister M, Dugbartey GJ, Zijlstra MP, Vinet J, Brunt ER, van Leeuwen FW, Rub U, Kampinga HH, den Dunnen WF. Cellular protein quality control and the evolution of aggregates in spinocerebellar ataxia type 3 (SCA3). Neuropathol Appl Neurobiol 2012; 6: 548-558
31. Hayashi M, Kobayashi K, Furuta H. Immunohistochemical study of neuronal intranuclear and cytoplasmic inclusions in Machado-Joseph disease. Psychiatry Clin Neurosci 2003; 2: 205-213
32. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, Vonsattel JP, Aronin N. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 1997; 5334: 1990-1993
33. Gutekunst CA, Li SH, Yi H, Mulroy JS, Kuemmerle S, Jones R, Rye D, Ferrante RJ, Hersch SM, Li XJ. Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J Neurosci 1999; 7: 2522-2534
34. Kampinga HH, Craig EA. The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 2010; 8: 579-592
35. Ciechanover A. The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J 1998; 24: 7151-7160
36. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 4: 463-477
37. Gamerdinger M, Hajieva P, Kaya AM, Wolfrum U, Hartl FU, Behl C. Protein quality control during aging involves recruitment of the macroautophagy pathway by BAG3. EMBO J 2009; 7: 889-901
38. Carrard G, Bulteau AL, Petropoulos I, Friguet B. Impairment of proteasome structure and function in aging. Int J Biochem Cell Biol 2002; 11: 1461-1474
39. Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005; 4: 603-614
40. Hageman J, Rujano MA, Van Waarde MA, Kakkar V, Dirks RP, Govorukhina N, Oosterveld-Hut HM, Lubsen NH, Kampinga HH. A DNAJB chaperone subfamily with HDAC-dependent activities suppresses toxic protein aggregation. Mol Cell 2010; 3: 355-369
41. Carra S, Sivilotti M, Chavez Zobel AT, Lambert H, Landry J. HspB8, a small heat shock protein mutated in human neuromuscular disorders, has in vivo chaperone activity in cultured cells. Hum Mol Genet 2005; 12: 1659-1669
42. Kakkar V, Prins LC, Kampinga HH. DNAJ proteins and protein aggregation diseases. Curr Top Med Chem 2012; 22: 2479-2490
43. Kakkar V, Meister-Broekema M, Minoia M, Carra S, Kampinga HH. Barcoding heat shock proteins to human diseases: looking beyond the heat shock response. Dis Model Mech 2014; 4: 421-434
44. Trottier Y, Lutz Y, Stevanin G, Imbert G, Devys D, Cancel G, Saudou F, Weber C, David G, Tora L. Polyglutamine expansion as a pathological epitope in Huntington's disease and four dominant cerebellar ataxias. Nature 1995; 6555: 403-406
45. Bjorkoy G, Lamark T, Johansen T. p62/SQSTM1: a missing link between protein aggregates and the autophagy machinery. Autophagy 2006; 2: 138-139
46. Wooten MW, Hu X, Babu JR, Seibenhener ML, Geetha T, Paine MG, Wooten MC. Signaling, polyubiquitination, trafficking, and inclusions: sequestosome 1/p62's role in neurodegenerative disease. J Biomed Biotechnol 2006; 3: 62079
47. Kuusisto E, Kauppinen T, Alafuzoff I. Use of p62/SQSTM1 antibodies for neuropathological diagnosis. Neuropathol Appl Neurobiol 2008; 2: 169-180
48. van Leeuwen FW, de Kleijn DP, van den Hurk HH, Neubauer A, Sonnemans MA, Sluijs JA, Koycu S, Ramdjielal RD, Salehi A, Martens GJ, Grosveld FG, Peter J, Burbach H, Hol EM. Frameshift mutants of beta amyloid precursor protein and ubiquitin-B in Alzheimer's and Down patients. Science 1998; 5348: 242-247
49. van Tijn P, Verhage MC, Hobo B, van Leeuwen FW, Fischer DF. Low levels of mutant ubiquitin are degraded by the proteasome in vivo. J Neurosci Res 2010; 11: 2325-2337
50. de Pril R, Fischer DF, Maat-Schieman ML, Hobo B, de Vos RA, Brunt ER, Hol EM, Roos RA, van Leeuwen FW. Accumulation of aberrant ubiquitin induces aggregate formation and cell death in polyglutamine diseases. Hum Mol Genet 2004; 16: 1803-1813
51. Braak H, Braak E. Allocortical involvement in Huntington's disease. Neuropathol Appl Neurobiol 1992; 6: 539-547
52. Schipper-Krom S, Juenemann K, Jansen AH, Wiemhoefer A, van den Nieuwendijk R, Smith DL, Hink MA, Bates GP, Overkleeft H, Ovaa H, Reits E. Dynamic recruitment of active proteasomes into polyglutamine initiated inclusion bodies. FEBS Lett 2014; 1: 151-159
53. Park SH, Kukushkin Y, Gupta R, Chen T, Konagai A, Hipp MS, Hayer-Hartl M, Hartl FU. PolyQ proteins interfere with nuclear degradation of cytosolic proteins by sequestering the Sis1p chaperone. Cell 2013; 1: 134-145
54. Trushina E, McMurray CT. Oxidative stress and mitochondrial dysfunction in neurodegenerative diseases. Neuroscience 2007; 4: 1233-1248