Natural genetic variation determines susceptibility to aggregation or toxicity in a C. elegans model for polyglutamine disease

BMC Biology

Volumn 11, Issue , 2013, Pages

  Gidalevitz, Tali ^a,b   Wang, Ning ^a,c   Deravaj, Tanuja ^a   Alexander Floyd, Jasmine ^b   Morimoto, Richard I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b DREXEL UNIVERSITY   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Conformational disease; Genetic modifier; Natural variation; Polyglutamine; Protein aggregation

Indexed keywords

CAENORHABDITIS ELEGANS;

CAENORHABDITIS ELEGANS PROTEIN; PEPTIDE; POLYGLUTAMINE;

ALLELE; ANIMAL; ARTICLE; CAENORHABDITIS ELEGANS; DEGENERATIVE DISEASE; DISEASE MODEL; GENETIC VARIABILITY; GENETICS;

ALLELES; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DISEASE MODELS, ANIMAL; GENETIC VARIATION; NEURODEGENERATIVE DISEASES; PEPTIDES;

EID: 84884686553     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-11-100     Document Type: Article

References (81)

1. Kakizuka A. Protein precipitation: a common etiology in neurodegenerative disorders?. Trends Genet 1998, 14:396-402.
2. Chen S, Ferrone FA, Wetzel R. Huntington's disease age-of-onset linked to polyglutamine aggregation nucleation. Proc Natl Acad Sci USA 2002, 99:11884-11889.
3. Carrell RW, Lomas DA. Conformational disease. Lancet 1997, 350:134-138.
4. Bucciantini M, Giannoni E, Chiti F, Baroni F, Formigli L, Zurdo J, Taddei N, Ramponi G, Dobson CM, Stefani M. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 2002, 416:507-511.
5. Gidalevitz T, Ben-Zvi A, Ho KH, Brignull HR, Morimoto RI. Progressive disruption of cellular protein folding in models of polyglutamine diseases. Science 2006, 311:1471-1474.
6. Gidalevitz T, Krupinski T, Garcia S, Morimoto RI. Destabilizing protein polymorphisms in the genetic background direct phenotypic expression of mutant SOD1 toxicity. PLoS Genet 2009, 5:e1000399.
7. Hinault MP, Cuendet AF, Mattoo RU, Mensi M, Dietler G, Lashuel HA, Goloubinoff P. Stable alpha-synuclein oligomers strongly inhibit chaperone activity of the Hsp70 system by weak interactions with J-domain co-chaperones. J Biol Chem 2010, 285:38173-38182.
8. Olzscha H, Schermann SM, Woerner AC, Pinkert S, Hecht MH, Tartaglia GG, Vendruscolo M, Hayer-Hartl M, Hartl FU, Vabulas RM. Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 2011, 144:67-78.
9. Hipp MS, Patel CN, Bersuker K, Riley BE, Kaiser SE, Shaler TA, Brandeis M, Kopito RR. Indirect inhibition of 26S proteasome activity in a cellular model of Huntington's disease. J Cell Biol 2011, 196:573-587.
10. Chakrabarti O, Rane NS, Hegde RS. Cytosolic aggregates perturb the degradation of nontranslocated secretory and membrane proteins. Mol Biol Cell 2011, 22:1625-1637.
11. Eremenko E, Ben-Zvi A, Morozova-Roche LA, Raveh D. Aggregation of human S100A8 and S100A9 amyloidogenic proteins perturbs proteostasis in a yeast model. PLoS One 2012, 8:e58218.
12. Stine OC, Pleasant N, Franz ML, Abbott MH, Folstein SE, Ross CA. Correlation between the onset age of Huntington's disease and length of the trinucleotide repeat in IT-15. Hum Mol Genet 1993, 2:1547-1549.
13. Brinkman RR, Mezei MM, Theilmann J, Almqvist E, Hayden MR. The likelihood of being affected with Huntington disease by a particular age, for a specific CAG size. Am J Hum Genet 1997, 60:1202-1210.
14. Wexler NS, Lorimer J, Porter J, Gomez F, Moskowitz C, Shackell E, Marder K, Penchaszadeh G, Roberts SA, Gayan J, et al. Venezuelan kindreds reveal that genetic and environmental factors modulate Huntington's disease age of onset. Proc Natl Acad Sci USA 2004, 101:3498-3503.
15. Gusella JF, MacDonald ME. Huntington's disease: the case for genetic modifiers. Genome Med 2009, 1:80.
16. Lloret A, Dragileva E, Teed A, Espinola J, Fossale E, Gillis T, Lopez E, Myers RH, MacDonald ME, Wheeler VC. Genetic background modifies nuclear mutant huntingtin accumulation and HD CAG repeat instability in Huntington's disease knock-in mice. Hum Mol Genet 2006, 15:2015-2024.
17. Van Raamsdonk JM, Metzler M, Slow E, Pearson J, Schwab C, Carroll J, Graham RK, Leavitt BR, Hayden MR. Phenotypic abnormalities in the YAC128 mouse model of Huntington disease are penetrant on multiple genetic backgrounds and modulated by strain. Neurobiol Dis 2007, 26:189-200.
18. Tome S, Manley K, Simard JP, Clark GW, Slean MM, Swami M, Shelbourne PF, Tillier ER, Monckton DG, Messer A, et al. MSH3 polymorphisms and protein levels affect CAG repeat instability in Huntington's disease mice. PLoS Genet 2012, 9:e1003280.
19. Sanford LP, Kallapur S, Ormsby I, Doetschman T. Influence of genetic background on knockout mouse phenotypes. Methods Mol Biol 2001, 158:217-225.
20. Weatherall DJ. Phenotype-genotype relationships in monogenic disease: lessons from the thalassaemias. Nat Rev Genet 2001, 2:245-255.
21. Genin E, Feingold J, Clerget-Darpoux F. Identifying modifier genes of monogenic disease: strategies and difficulties. Hum Genet 2008, 124:357-368.
22. Doetschman T. Influence of genetic background on genetically engineered mouse phenotypes. Methods Mol Biol 2009, 530:423-433.
23. Hamilton BA, Yu BD. Modifier genes and the plasticity of genetic networks in mice. PLoS Genet 2012, 8:e1002644.
24. Kearney JA. Genetic modifiers of neurological disease. Curr Opin Genet Dev 2011, 21:349-353.
25. Morley JF, Brignull HR, Weyers JJ, Morimoto RI. The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc Natl Acad Sci USA 2002, 99:10417-10422.
26. Hsu AL, Murphy CT, Kenyon C. Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 2003, 300:1142-1145.
27. Muchowski PJ, Wacker JL. Modulation of neurodegeneration by molecular chaperones. Nat Rev Neurosci 2005, 6:11-22.
28. Bennett EJ, Shaler TA, Woodman B, Ryu KY, Zaitseva TS, Becker CH, Bates GP, Schulman H, Kopito RR. Global changes to the ubiquitin system in Huntington's disease. Nature 2007, 448:704-708.
29. Gidalevitz T, Prahlad V, Morimoto RI. The stress of protein misfolding: from single cells to multicellular organisms. Cold Spring Harb Perspect Biol 2011, 3:a009704.
30. Prahlad V, Morimoto RI. Neuronal circuitry regulates the response of Caenorhabditis elegans to misfolded proteins. Proc Natl Acad Sci USA 2011, 108:14204-14209.
31. Dipple KM, McCabe ER. Phenotypes of patients with "simple" Mendelian disorders are complex traits: thresholds, modifiers, and systems dynamics. Am J Hum Genet 2000, 66:1729-1735.
32. Hartman JL, Garvik B, Hartwell L. Principles for the buffering of genetic variation. Science 2001, 291:1001-1004.
33. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, et al. Finding the missing heritability of complex diseases. Nature 2009, 461:747-753.
34. Gibson G. Decanalization and the origin of complex disease. Nat Rev Genet 2009, 10:134-140.
35. Dickson SP, Wang K, Krantz I, Hakonarson H, Goldstein DB. Rare variants create synthetic genome-wide associations. PLoS Biol 2010, 8:e1000294.
36. Gibson G. Rare and common variants: twenty arguments. Nat Rev Genet 2012, 13:135-145.
37. Cruchaga C, Haller G, Chakraverty S, Mayo K, Vallania FL, Mitra RD, Faber K, Williamson J, Bird T, Diaz-Arrastia R, et al. Rare variants in APP, PSEN1 and PSEN2 increase risk for AD in late-onset Alzheimer's disease families. PLoS ONE 2012, 7:e31039.
38. Felix MA, Wagner A. Robustness and evolution: concepts, insights and challenges from a developmental model system. Heredity (Edinb) 2008, 100:132-140.
39. Jarosz DF, Taipale M, Lindquist S. Protein homeostasis and the phenotypic manifestation of genetic diversity: principles and mechanisms. Annu Rev Genet 2010, 44:189-216.
40. Queitsch C, Carlson KD, Girirajan S. Lessons from model organisms: phenotypic robustness and missing heritability in complex disease. PLoS Genet 2012, 8:e1003041.
41. Balch WE, Morimoto RI, Dillin A, Kelly JW. Adapting proteostasis for disease intervention. Science 2008, 319:916-919.
42. Powers ET, Morimoto RI, Dillin A, Kelly JW, Balch WE. Biological and chemical approaches to diseases of proteostasis deficiency. Annu Rev Biochem 2009, 78:959-991.
43. Gidalevitz T, Kikis EA, Morimoto RI. A cellular perspective on conformational disease: the role of genetic background and proteostasis networks. Curr Opin Struct Biol 2010, 20:23-32.
44. Rutherford SL, Lindquist S. Hsp90 as a capacitor for morphological evolution. Nature 1998, 396:336-342.
45. Queitsch C, Sangster TA, Lindquist S. Hsp90 as a capacitor of phenotypic variation. Nature 2002, 417:618-624.
46. Yeyati PL, Bancewicz RM, Maule J, van Heyningen V. Hsp90 selectively modulates phenotype in vertebrate development. PLoS Genet 2007, 3:e43.
47. Ben-Zvi A, Miller EA, Morimoto RI. Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc Natl Acad Sci USA 2009, 106:14914-14919.
48. Jarosz DF, Lindquist S. Hsp90 and environmental stress transform the adaptive value of natural genetic variation. Science 2010, 330:1820-1824.
49. Welte MA, Duncan I, Lindquist S. The basis for a heat-induced developmental defect: defining crucial lesions. Genes Dev 1995, 9:2240-2250.
50. Chow KL, Chan KW. Stress-induced phenocopy of C. elegans defines functional steps of sensory organ differentiation. Dev Growth Differ 1999, 41:629-637.
51. Walker DW, McColl G, Jenkins NL, Harris J, Lithgow GJ. Evolution of lifespan in C. elegans. Nature 2000, 405:296-297.
52. Jenkins NL, McColl G, Lithgow GJ. Fitness cost of extended lifespan in Caenorhabditis elegans. Proc Biol Sci 2004, 271:2523-2526.
53. Chen J, Senturk D, Wang JL, Muller HG, Carey JR, Caswell H, Caswell-Chen EP. A demographic analysis of the fitness cost of extended longevity in Caenorhabditis elegans. J Gerontol A Biol Sci Med Sci 2007, 62:126-135.
54. Krebs RA, Feder ME. Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 1997, 2:60-71.
55. Nollen EA, Morimoto RI. Chaperoning signaling pathways: molecular chaperones as stress-sensing 'heat shock' proteins. J Cell Sci 2002, 115:2809-2816.
56. Dai C, Whitesell L, Rogers AB, Lindquist S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 2007, 130:1005-1018.
57. Mendillo ML, Santagata S, Koeva M, Bell GW, Hu R, Tamimi RM, Fraenkel E, Ince TA, Whitesell L, Lindquist S. HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell 2012, 150:549-562.
58. Metzger S, Bauer P, Tomiuk J, Laccone F, Didonato S, Gellera C, Mariotti C, Lange HW, Weirich-Schwaiger H, Wenning GK, et al. Genetic analysis of candidate genes modifying the age-at-onset in Huntington's disease. Hum Genet 2006, 120:285-292.
59. Andresen JM, Gayan J, Cherny SS, Brocklebank D, Alkorta-Aranburu G, Addis EA, Cardon LR, Housman DE, Wexler NS. Replication of twelve association studies for Huntington's disease residual age of onset in large Venezuelan kindreds. J Med Genet 2007, 44:44-50.
60. Lee JM, Gillis T, Mysore JS, Ramos EM, Myers RH, Hayden MR, Morrison PJ, Nance M, Ross CA, Margolis RL, et al. Common SNP-based haplotype analysis of the 4p16.3 Huntington disease gene region. Am J Hum Genet 2012, 90:434-444.
61. Ayyadevara S, Ayyadevara R, Hou S, Thaden JJ, Shmookler Reis RJ. Genetic mapping of quantitative trait loci governing longevity of Caenorhabditis elegans in recombinant-inbred progeny of a Bergerac-BO x RC301 interstrain cross. Genetics 2001, 157:655-666.
62. Li Y, Alvarez OA, Gutteling EW, Tijsterman M, Fu J, Riksen JA, Hazendonk E, Prins P, Plasterk RH, Jansen RC, et al. Mapping determinants of gene expression plasticity by genetical genomics in C. elegans. PLoS Genet 2006, 2:e222.
63. Kammenga JE, Phillips PC, De Bono M, Doroszuk A. Beyond induced mutants: using worms to study natural variation in genetic pathways. Trends Genet 2008, 24:178-185.
64. Ehrenreich IM, Gerke JP, Kruglyak L. Genetic dissection of complex traits in yeast: insights from studies of gene expression and other phenotypes in the BYxRM cross. Cold Spring Harb Symp Quant Biol 2009, 74:145-153.
65. Stumpferl SW, Brand SE, Jiang JC, Korona B, Tiwari A, Dai J, Seo JG, Jazwinski SM. Natural genetic variation in yeast longevity. Genome Res 2012, 22:1963-1973.
66. Consortium CC. The genome architecture of the Collaborative Cross mouse genetic reference population. Genetics 2012, 190:389-401.
67. Nollen EA, Garcia SM, van Haaften G, Kim S, Chavez A, Morimoto RI, Plasterk RH. Genome-wide RNA interference screen identifies previously undescribed regulators of polyglutamine aggregation. Proc Natl Acad Sci USA 2004, 101:6403-6408.
68. Rockman MV, Kruglyak L. Recombinational landscape and population genomics of Caenorhabditis elegans. PLoS Genet 2009, 5:e1000419.
69. Herndon LA, Schmeissner PJ, Dudaronek JM, Brown PA, Listner KM, Sakano Y, Paupard MC, Hall DH, Driscoll M. Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 2002, 419:808-814.
70. Opal P, Zoghbi HY. The role of chaperones in polyglutamine disease. Trends Mol Med 2002, 8:232-236.
71. Calamini B, Silva MC, Madoux F, Hutt DM, Khanna S, Chalfant MA, Saldanha SA, Hodder P, Tait BD, Garza D, et al. Small-molecule proteostasis regulators for protein conformational diseases. Nat Chem Biol 2011, 8:185-196.
72. Alavez S, Lithgow GJ. Pharmacological maintenance of protein homeostasis could postpone age-related disease. Aging Cell 2012, 11:187-191.
73. Silva MC, Fox S, Beam M, Thakkar H, Amaral MD, Morimoto RI. A genetic screening strategy identifies novel regulators of the proteostasis network. PLoS Genet 2011, 7:e1002438.
74. Cohen E, Bieschke J, Perciavalle RM, Kelly JW, Dillin A. Opposing activities protect against age-onset proteotoxicity. Science 2006, 313:1604-1610.
75. Warrick JM, Chan HY, Gray-Board GL, Chai Y, Paulson HL, Bonini NM. Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat Genet 1999, 23:425-428.
76. Chan HY, Warrick JM, Gray-Board GL, Paulson HL, Bonini NM. Mechanisms of chaperone suppression of polyglutamine disease: selectivity, synergy and modulation of protein solubility in Drosophila. Hum Mol Genet 2000, 9:2811-2820.
77. Kover PX, Schaal BA. Genetic variation for disease resistance and tolerance among Arabidopsis thaliana accessions. Proc Natl Acad Sci USA 2002, 99:11270-11274.
78. Raberg L, Sim D, Read AF. Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 2007, 318:812-814.
79. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
80. Yang JS, Nam HJ, Seo M, Han SK, Choi Y, Nam HG, Lee SJ, Kim S. OASIS: online application for the survival analysis of lifespan assays performed in aging research. PLoS One 2011, 6:e23525.
81. OASIS. Online Application for Survival Analysis. http://sbi.postech.ac.kr/oasis.