Cerebellar ataxia and functional genomics: Identifying the routes to cerebellar neurodegeneration

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 10, 2014, Pages 2030-2038

  Smeets, C J L M ^a   Verbeek, D S ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Cerebellar ataxia; Functional genomics; Genome wide expression profiling; Modifier gene; Neurodegeneration; Next generation sequencing

Indexed keywords

MICRORNA; TRANSCRIPTOME;

APOPTOSIS; CEREBELLAR ATAXIA; EPIGENETICS; EXOME; FUNCTIONAL GENOMICS; GENE EXPRESSION PROFILING; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; MODIFIER GENE; MUSCLE CONTRACTION; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEXT GENERATION SEQUENCING; NONHUMAN; PATHOGENESIS; PROTEIN FOLDING; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; SYNAPTIC TRANSMISSION; TRANSCRIPTION REGULATION;

EID: 84908318568     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.04.004     Document Type: Review

References (83)

1. Hersheson J., Haworth A., Houlden H. The inherited ataxias: genetic heterogeneity, mutation databases, and future directions in research and clinical diagnostics. Hum. Mutat. 2012, 33:1324-1332.
2. Sailer A., Houlden H. Recent advances in the genetics of cerebellar ataxias. Curr. Neurol. Neurosci. Rep. 2012, 12:227-236.
3. Anheim M., Tranchant C., Koenig M. The autosomal recessive cerebellar ataxias. N. Engl. J. Med. 2012, 366:636-646.
4. Klockgether T. Update on degenerative ataxias. Curr. Opin. Neurol. 2011, 24:339-345.
5. Durr A. Autosomal dominant cerebellar ataxias: polyglutamine expansions and beyond. Lancet Neurol. 2010, 9:885-894.
6. Verbeek D.S., Van de Warrenburg B.P.C. Genetics of the dominant ataxias. Semin. Neurol. 2011, 31:461-469.
7. Matilla-Dueñas A., Ashizawa T., Brice A., Magri S., McFarland K.N., Pandolfo M., et al. Consensus paper: pathological mechanisms underlying neurodegeneration in spinocerebellar ataxias. Cerebellum 2014, 13:269-302.
8. Wang J.L., Yang X., Xia K., Hu Z.M., Weng L., Jin X., et al. TGM6 identified as a novel causative gene of spinocerebellar ataxias using exome sequencing. Brain 2010, 133:3510-3518.
9. Duarri A., Jezierska J., Fokkens M., Meijer M., Schelhaas H.J., den Dunnen W.F.A., et al. Mutations in potassium channel kcnd3 cause spinocerebellar ataxia type 19. Ann. Neurol. 2012, 72:870-880.
10. Lee Y.-C., Durr A., Majczenko K., Huang Y.-H., Liu Y.-C., Lien C.-C., et al. Mutations in KCND3 cause spinocerebellar ataxia type 22. Ann. Neurol. 2012, 72:859-869.
11. Hekman K.E., Yu G.-Y., Brown C.D., Zhu H., Du X., Gervin K., et al. A conserved eEF2 coding variant in SCA26 leads to loss of translational fidelity and increased susceptibility to proteostatic insult. Hum. Mol. Genet. 2012, 21:5472-5483.
12. Doi H., Yoshida K., Yasuda T., Fukuda M., Fukuda Y., Morita H., et al. Exome sequencing reveals a homozygous SYT14 mutation in adult-onset, autosomal-recessive spinocerebellar ataxia with psychomotor retardation. Am. J. Hum. Genet. 2011, 89:320-327.
13. Bilguvar K., Tyagi N.K., Ozkara C., Tuysuz B., Bakircioglu M., Choi M., et al. Recessive loss of function of the neuronal ubiquitin hydrolase UCHL1 leads to early-onset progressive neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:3489-3494.
14. Hammer M.B., Eleuch-Fayache G., Schottlaender L.V., Nehdi H., Gibbs J.R., Arepalli S.K., et al. Mutations in GBA2 cause autosomal-recessive cerebellar ataxia with spasticity. Am. J. Hum. Genet. 2013, 92:245-251.
15. Zanni G., Calì T., Kalscheuer V.M., Ottolini D., Barresi S., Lebrun N., et al. Mutation of plasma membrane Ca2+ ATPase isoform 3 in a family with X-linked congenital cerebellar ataxia impairs Ca2+ homeostasis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:14514-14519.
16. Caramins M., Colebatch J.G., Bainbridge M.N., Scherer S.S., Abrams C.K., Hackett E.L., et al. Exome sequencing identification of a GJB1 missense mutation in a kindred with X-linked spinocerebellar ataxia (SCA-X1). Hum. Mol. Genet. 2013, 22(21):4329-4338.
17. Forman O.P., De Risio L., Stewart J., Mellersh C.S., Beltran E. Genome-wide mRNA sequencing of a single canine cerebellar cortical degeneration case leads to the identification of a disease associated SPTBN2 mutation. BMC Genet. 2012, 13:55.
18. Ikeda Y., Dick K.A., Weatherspoon M.R., Gincel D., Armbrust K.R., Dalton JC, et al. Spectrin mutations cause spinocerebellar ataxia type 5. Nat. Genet. 2006, 38:184-190.
19. Jia Y., Mu J.C., Ackerman S.L. Mutation of a U2 snRNA gene causes global disruption of alternative splicing and neurodegeneration. Cell 2012, 148:296-308.
20. Chang J.T., Nevins J.R. GATHER: a systems approach to interpreting genomic signatures. Bioinformatics 2006, 22:2926-2933.
21. Tsaur M.L., Chou C.C., Shih Y.H., Wang H.L. Cloning, expression and CNS distribution of Kv4.3, an A-type K+ channel alpha subunit. FEBS Lett. 1997, 400:215-220.
22. Jackson M., Song W., Liu M.Y., Jin L., Dykes-Hoberg M., Lin C.I., et al. Modulation of the neuronal glutamate transporter EAAT4 by two interacting proteins. Nature 2001, 410:89-93.
23. Haugen A.C., Di Prospero N.A., Parker J.S., Fannin R.D., Chou J., Meyer J.N., et al. Altered gene expression and DNA damage in peripheral blood cells from Friedreich's ataxia patients: cellular model of pathology. PLoS Genet. 2010, 6:e1000812.
24. Coppola G., Burnett R., Perlman S., Versano R., Gao F., Plasterer H., et al. A gene expression phenotype in lymphocytes from Friedreich ataxia patients. Ann. Neurol. 2011, 70:790-804.
25. Mancini C., Roncaglia P., Brussino A., Stevanin G., Lo Buono N., Krmac H., et al. Genome-wide expression profiling and functional characterization of SCA28 lymphoblastoid cell lines reveal impairment in cell growth and activation of apoptotic pathways. BMC Med. Genomics 2013, 6:22.
26. Ku S., Soragni E., Campau E., Thomas E.A., Altun G., Laurent L.C., et al. Friedreich's ataxia induced pluripotent stem cells model intergenerational GAA{dot operator}TTC triplet repeat instability. Cell Stem Cell 2010, 7:631-637.
27. Maltecca F., Magnoni R., Cerri F., Cox G.A., Quattrini A., Casari G. Haploinsufficiency of AFG3L2, the gene responsible for spinocerebellar ataxia type 28, causes mitochondria-mediated Purkinje cell dark degeneration. J. Neurosci. 2009, 29:9244-9254.
28. Serra H.G., Byam C.E., Lande J.D., Tousey S.K., Zoghbi H.Y., Orr H.T. Gene profiling links SCA1 pathophysiology to glutamate signaling in Purkinje cells of transgenic mice. Hum. Mol. Genet. 2004, 13:2535-2543.
29. Gatchel J.R., Watase K., Thaller C., Carson J.P., Jafar-Nejad P., Shaw C., et al. The insulin-like growth factor pathway is altered in spinocerebellar ataxia type 1 and type 7. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:1291-1296.
30. Damrath E., Heck M.V., Gispert S., Azizov M., Nowock J., Seifried C., et al. ATXN2-CAG42 sequesters PABPC1 into insolubility and induces FBXW8 in cerebellum of old ataxic knock-in mice. PLoS Genet. 2012, 8:e1002920.
31. Crespo-Barreto J., Fryer J.D., Shaw C.A., Orr H.T., Zoghbi H.Y. Partial loss of ataxin-1 function contributes to transcriptional dysregulation in spinocerebellar ataxia type 1 pathogenesis. PLoS Genet. 2010, 6:e1001021.
32. Chou A.-H.A., Yeh T.-H.T., Ouyang P.P., Chen Y.-L.Y., Chen S.-Y.S., Wang H.-L.H. Polyglutamine-expanded ataxin-3 causes cerebellar dysfunction of SCA3 transgenic mice by inducing transcriptional dysregulation. Neurobiol. Dis. 2008, 31:13-13.
33. Chou A.-H., Chen C.-Y., Chen S.-Y., Chen W.-J., Chen Y.-L., Weng Y.-S., et al. Polyglutamine-expanded ataxin-7 causes cerebellar dysfunction by inducing transcriptional dysregulation. Neurochem. Int. 2010, 56:329-339.
34. Yue Z., Horton A., Bravin M., DeJager P.L., Selimi F., Heintz N. A novel protein complex linking the delta 2 glutamate receptor and autophagy: implications for neurodegeneration in lurcher mice. Neuron 2002, 35:921-933.
35. Jen J.C., Wan J., Palos T.P., Howard B.D., Baloh R.W. Mutation in the glutamate transporter EAAT1 causes episodic ataxia, hemiplegia, and seizures. Neurology 2005, 65:529-534.
36. Goold R., Hubank M., Hunt A., Holton J., Menon R.P., Revesz T., et al. Down-regulation of the dopamine receptor D2 in mice lacking ataxin 1. Hum. Mol. Genet. 2007, 16:2122-2134.
37. Serra H.G.H., Duvick L.L., Zu T.T., Carlson K.K., Stevens S.S., Jorgensen N.N., et al. RORalpha-mediated Purkinje cell development determines disease severity in Adult SCA1 mice. Cell 2006, 127:697-708.
38. van de Leemput J., Chandran J., Knight M.A., Holtzclaw L.A., Scholz S., Cookson M.R., et al. Deletion at ITPR1 underlies ataxia in mice and spinocerebellar ataxia 15 in humans. PLoS Genet. 2007, 3:e108.
39. Guergueltcheva V., Azmanov D.N., Angelicheva D., Smith K.R., Chamova T., Florez L., et al. Autosomal-recessive congenital cerebellar ataxia is caused by mutations in metabotropic glutamate receptor 1. Am. J. Hum. Genet. 2012, 91:553-564.
40. Thangima Zannat M., Bhattacharjee R.B., Bag J. Depletion of cellular poly (A) binding protein prevents protein synthesis and leads to apoptosis in HeLa cells. Biochem. Biophys. Res. Commun. 2011, 408:375-381.
41. Kobayashi H., Abe K., Matsuura T., Ikeda Y., Hitomi T., Akechi Y., et al. Expansion of intronic GGCCTG hexanucleotide repeat in NOP56 causes SCA36, a type of spinocerebellar ataxia accompanied by motor neuron involvement. Am. J. Hum. Genet. 2011, 89:121-130.
42. Coppola G., Marmolino D., Lu D., Wang Q., Cnop M., Rai M., et al. Functional genomic analysis of frataxin deficiency reveals tissue-specific alterations and identifies the PPARgamma pathway as a therapeutic target in Friedreich's ataxia. Hum. Mol. Genet. 2009, 18:2452-2461.
43. Finck B.N., Kelly D.P. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 2006, 116:615-622.
44. Friedrich B., Euler P., Ziegler R., Kuhn A., Landwehrmeyer B.G., Luthi-Carter R., et al. Comparative analyses of Purkinje cell gene expression profiles reveal shared molecular abnormalities in models of different polyglutamine diseases. Brain Res. 2012, 1481:37-48.
45. Chen D.-H., Brkanac Z., Verlinde C.L.M.J., Tan X.-J., Bylenok L., Nochlin D., et al. Missense mutations in the regulatory domain of PKC gamma: a new mechanism for dominant nonepisodic cerebellar ataxia. Am. J. Hum. Genet. 2003, 72:839-849.
46. Miska E.A., Alvarez-Saavedra E., Townsend M., Yoshii A., Sestan N., Rakic P., et al. Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol. 2004, 5:R68.
47. Schratt G.M., Tuebing F., Nigh E.A., Kane C.G., Sabatini M.E., Kiebler M., et al. A brain-specific microRNA regulates dendritic spine development. Nature 2006, 439:283-289.
48. Schaefer A., O'Carroll D., Tan C.L., Hillman D., Sugimori M., Llinas R., et al. Cerebellar neurodegeneration in the absence of microRNAs. J. Exp. Med. 2007, 204:1553-1558.
49. Lee Y., Samaco R.C., Gatchel J.R., Thaller C., Orr H.T., Zoghbi H.Y. miR-19, miR-101 and miR-130 co-regulate ATXN1 levels to potentially modulate SCA1 pathogenesis. Nat. Neurosci. 2008, 11:1137-1139.
50. Persengiev S., Kondova I., Otting N., Koeppen A.H., Bontrop R.E. Genome-wide analysis of miRNA expression reveals a potential role for miR-144 in brain aging and spinocerebellar ataxia pathogenesis. Neurobiol. Aging 2011, 32:2316.e17-2316.e27.
51. Rodriguez-Lebron E., Liu G., Keiser M., Behlke M.A., Davidson B.L. Altered Purkinje cell miRNA expression and SCA1 pathogenesis. Neurobiol. Dis. 2013, 54:456-463.
52. Shi Y., Huang F., Tang B., Li J., Wang J., Shen L., et al. MicroRNA profiling in the serums of SCA3/MJD patients. Int. J. Neurosci. 2014, 124(2):97.
53. Shioya M., Obayashi S., Tabunoki H., Arima K., Saito Y., Ishida T., et al. Aberrant microRNA expression in the brains of neurodegenerative diseases: miR-29a decreased in Alzheimer disease brains targets neurone navigator 3. Neuropathol. Appl. Neurobiol. 2010, 36:320-330.
54. Gaughwin P.M., Ciesla M., Lahiri N., Tabrizi S.J., Brundin P., Björkqvist M. Hsa-miR-34b is a plasma-stable microRNA that is elevated in pre-manifest Huntington's disease. Hum. Mol. Genet. 2011, 20:2225-2237.
55. Mahishi L.H., Hart R.P., Lynch D.R., Ratan R.R. miR-886-3p levels are elevated in Friedreich ataxia. J. Neurosci. 2012, 32:9369-9373.
56. Egger G., Liang G., Aparicio A., Jones P.A. Epigenetics in human disease and prospects for epigenetic therapy. Nature 2004, 429:457-463.
57. Mastroeni D., Grover A., Delvaux E., Whiteside C., Coleman P.D., Rogers J. Epigenetic mechanisms in Alzheimer's disease. Neurobiol. Aging 2011, 32:1161-1180.
58. van Heesbeen H.J., Mesman S., Veenvliet J.V., Smidt M.P. Epigenetic mechanisms in the development and maintenance of dopaminergic neurons. Development 2013, 140:1159-1169.
59. Pedroso J.L., Povoas Barsottini O.G., Lin L., Melberg A., Oliveira A.S.B., Mignot E. A novel de novo Exon 21 DNMT1 mutation causes cerebellar ataxia, deafness, and narcolepsy in a Brazilian patient. Sleep 2013, 36:1257-1259.
60. Dion V., Wilson J.H. Instability and chromatin structure of expanded trinucleotide repeats. Trends Genet. 2009, 25:288-297.
61. Evans-Galea M.V., Carrodus N., Rowley S.M., Corben L.A., Tai G., Saffery R., et al. FXN methylation predicts expression and clinical outcome in Friedreich ataxia. Ann. Neurol. 2012, 71:487-497.
62. Valor L.M., Guiretti D., Lopez-Atalaya J.P., Barco A. Genomic landscape of transcriptional and epigenetic dysregulation in early onset polyglutamine disease. J. Neurosci. 2013, 33:10471-10482.
63. Fernandez-Funez P., Nino-Rosales M.L., de Gouyon B., She W.C., Luchak J.M., Martinez P., et al. Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 2000, 408:101-106.
64. Shieh S.-Y., Bonini N.M. Genes and pathways affected by CAG-repeat RNA-based toxicity in Drosophila. Hum. Mol. Genet. 2011, 20:4810-4821.
65. Lessing D., Bonini N.M. Polyglutamine genes interact to modulate the severity and progression of neurodegeneration in Drosophila. PLoS Biol. 2008, 6:e29.
66. Bilen J., Bonini N.M. Genome-wide screen for modifiers of ataxin-3 neurodegeneration in Drosophila. PLoS Genet. 2007, 3:1950-1964.
67. Latouche M., Lasbleiz C., Martin E., Monnier V., Debeir T., Mouatt-Prigent A., et al. A conditional pan-neuronal Drosophila model of spinocerebellar ataxia 7 with a reversible adult phenotype suitable for identifying modifier genes. J. Neurosci. 2007, 27:2483-2492.
68. Park J., Al-Ramahi I., Tan Q., Mollema N., Diaz-Garcia J.R., Gallego-Flores T., et al. RAS-MAPK-MSK1 pathway modulates ataxin 1 protein levels and toxicity in SCA1. Nature 2013, 498:325-331.
69. Ren J., Jegga A.G., Zhang M., Deng J., Liu J., Gordon C.B., et al. A Drosophila model of the neurodegenerative disease SCA17 reveals a role of RBP-J/Su(H) in modulating the pathological outcome. Hum. Mol. Genet. 2011, 20:3424-3436.
70. Koide R., Kobayashi S., Shimohata T., Ikeuchi T., Maruyama M., Saito M., et al. A neurological disease caused by an expanded CAG trinucleotide repeat in the TATA-binding protein gene: a new polyglutamine disease?. Hum. Mol. Genet. 1999, 8:2047-2053.
71. Emamian E.S.E., Kaytor M.D.M., Duvick L.A.L., Zu T.T., Tousey S.K.S., Zoghbi H.Y.H., et al. Serine 776 of Ataxin-1 is critical for polyglutamine-induced disease in SCA1 transgenic mice. Neuron 2003, 38(3):375-387.
72. Matilla-Dueñas A., Sánchez I., Corral-Juan M., Dávalos A., Alvarez R., Latorre P. Cellular and molecular pathways triggering neurodegeneration in the spinocerebellar ataxias. Cerebellum 2010, 9:148-166.
73. Rodriguez-Rodriguez P., Almeida A., Bolaños J.P. Brain energy metabolism in glutamate-receptor activation and excitotoxicity: role for APC/C-Cdh1 in the balance glycolysis/pentose phosphate pathway. Neurochem. Int. 2013, 62:750-756.
74. Corona J.C., Gimenez-Cassina A., Lim F., Díaz-Nido J. Hexokinase II gene transfer protects against neurodegeneration in the rotenone and MPTP mouse models of Parkinson's disease. J. Neurosci. Res. 2010, 88:1943-1950.
75. Maggio N., Blatt I., Vlachos A., Tanne D., Chapman J., Segal M. Treating seizures and epilepsy with anticoagulants?. Front. Cell. Neurosci. 2013, 7:19.
76. Pogačić Kramp V. List of drugs in development for neurodegenerative diseases: update October 2011. Neurodegener. Dis. 2012, 9:210-283.
77. Musumeci O., Naini A., Slonim A.E., Skavin N., Hadjigeorgiou G.L., Krawiecki N., et al. Familial cerebellar ataxia with muscle coenzyme Q10 deficiency. Neurology 2001, 56:849-855.
78. Vorgerd M., Schöls L., Hardt C., Ristow M., Epplen J.T., Zange J. Mitochondrial impairment of human muscle in Friedreich ataxia in vivo. Neuromuscul. Disord. 2000, 10:430-435.
79. Buchner D.A., Trudeau M., Meisler M.H. SCNM1, a putative RNA splicing factor that modifies disease severity in mice. Science 2003, 301:967-969.
80. Park S.-Y., Ludwig M.Z., Tamarina N.A., He B.Z., Carl S.H., Dickerson D.A., et al. Genetic complexity in a Drosophila model of diabetes-associated misfolded human proinsulin. Genetics 2014, 196:539-555.
81. Van de Warrenburg B.P.C., Hendriks H., Durr A., van Zuijlen M.C.A., Stevanin G., Camuzat A., et al. Age at onset variance analysis in spinocerebellar ataxias: a study in a Dutch-French cohort. Ann. Neurol. 2005, 57:505-512.
82. Chattopadhyay B., Ghosh S., Gangopadhyay P.K., Das S.K., Roy T., Sinha K.K., et al. Modulation of age at onset in Huntington's disease and spinocerebellar ataxia type 2 patients originated from eastern India. Neurosci. Lett. 2003, 345:93-96.
83. Pulst S.-M., Santos N., Wang D., Yang H., Huynh D., Velazquez L., et al. Spinocerebellar ataxia type 2: polyQ repeat variation in the CACNA1A calcium channel modifies age of onset. Brain 2005, 128:2297-2303.