A two-step path to inclusion formation of huntingtin peptides revealed by number and brightness analysis

Biophysical Journal

Volumn 98, Issue 12, 2010, Pages 3078-3085

  Ossato, Giulia ^a   Digman, Michelle A ^a,b   Aiken, Charity ^b   Lukacsovich, Tamas ^b   Marsh, J Lawrence ^b   Gratton, Enrico ^a,b  

^a University of California at Irvine   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77953567262     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.02.058     Document Type: Article

References (42)

1. Bates, G. 2003. Huntingtin aggregation and toxicity in Huntington's disease. Lancet. 361:1642-1644. (Pubitemid 36579005)
2. Marsh, J. L., H. Walker, ..., L. M. Thompson. 2000. Expanded polyglutamine peptides alone are intrinsically cytotoxic and cause neurodegeneration in Drosophila. Hum. Mol. Genet. 9:13-25.
3. Davies, S. W., M. Turmaine, ..., G. P. Bates. 1997. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell. 90:537-548.
4. DiFiglia, M., E. Sapp, ..., N. Aronin. 1997. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science. 277:1990-1993.
5. Ordway, J. M., S. Tallaksen-Greene, ..., P. J. Detloff. 1997. Ectopically expressed CAG repeats cause intranuclear inclusions and a progressive late onset neurological phenotype in the mouse. Cell. 91:753-763.
6. Yang, W., J. R. Dunlap, ..., R. Wetzel. 2002. Aggregated polyglutamine peptides delivered to nuclei are toxic to mammalian cells. Hum. Mol. Genet. 11:2905-2917.
7. Dobson, C. M. 2003. Protein folding and misfolding. Nature. 426: 884-890.
8. Jahn, T. R., M. J. Parker, ..., S. E. Radford. 2006. Amyloid formation under physiological conditions proceeds via a native-like folding intermediate. Nat. Struct. Mol. Biol. 13:195-201.
9. Wetzel, R. 2006. Kinetics and thermodynamics of amyloid fibril assembly. Acc. Chem. Res. 39:671-679.
10. Chen, S., F. A. Ferrone, and R. Wetzel. 2002. Huntington's disease age-of-onset linked to polyglutamine aggregation nucleation. Proc. Natl. Acad. Sci. USA. 99:11884-11889.
11. Muchowski, P. J. 2002. Protein misfolding, amyloid formation, and neurodegeneration: a critical role for molecular chaperones? Neuron. 35:9-12.
12. Kayed, R., E. Head, ..., C. G. Glabe. 2003. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science. 300:486-489.
13. Thakur, A. K., M. Jayaraman, ..., R. Wetzel. 2009. Polyglutamine disruption of the huntingtin exon 1 N terminus triggers a complex aggregation mechanism. Nat. Struct. Mol. Biol. 16:380-389.
14. Takahashi, Y., Y. Okamoto, ..., Y. Nagai. 2007. Detection of polyglutamine protein oligomers in cells by fluorescence correlation spectroscopy. J. Biol. Chem. 282:24039-24048.
15. Digman, M. A., R. Dalal, ..., E. Gratton. 2008. Mapping the number of molecules and brightness in the laser scanning microscope. Biophys. J. 94:2320-2332.
16. Dalal, R. B., M. A. Digman, ..., E. Gratton. 2008. Determination of particle number and brightness using a laser scanning confocal microscope operating in the analog mode. Microsc. Res. Tech. 71:69-81.
17. Cattaneo, E., and L. Conti. 1998. Generation and characterization of embryonic striatal conditionally immortalized ST14A cells. J. Neurosci. Res. 53:223-234.
18. Steffan, J. S., N. Agrawal, ..., J. L. Marsh. 2004. SUMO modification of Huntingtin and Huntington's disease pathology. Science. 304:100-104.
19. Arrasate, M., S. Mitra, ..., S. Finkbeiner. 2004. Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature. 431:805-810.
20. Gutekunst, C. A., S. H. Li, ..., X. J. Li. 1999. Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J. Neurosci. 19:2522-2534.
21. Kim, Y. J., Y. Yi, ..., M. DiFiglia. 2001. Caspase 3-cleaved N-terminal fragments of wild-type and mutant huntingtin are present in normal and Huntington's disease brains, associate with membranes, and undergo calpain-dependent proteolysis. Proc. Natl. Acad. Sci. USA. 98:12784-12789.
22. Bates, G. P., L. Mangiarini, ..., S. W. Davies. 1998. Polyglutamine expansion and Huntington's disease. Biochem. Soc. Trans. 26:471-475.
23. Parker, J. A., J. B. Connolly, ..., C. Neri. 2001. Expanded polyglutamines in Caenorhabditis elegans cause axonal abnormalities and severe dysfunction of PLM mechanosensory neurons without cell death. Proc. Natl. Acad. Sci. USA. 98:13318-13323.
24. Sokolov, S., A. Pozniakovsky, ..., F. Severin. 2006. Expression of an expanded polyglutamine domain in yeast causes death with apoptotic markers. Biochim. Biophys. Acta. 1757:660-666.
25. Steffan, J. S., L. Bodai, ..., L. M. Thompson. 2001. Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature. 413:739-743.
26. Tarlac, V., and E. Storey. 2003. Role of proteolysis in polyglutamine disorders. J. Neurosci. Res. 74:406-416.
27. Walker, F. O. 2007. Huntington's disease. Lancet. 369:218-228.
28. Padilla, S., N. Audugé, ..., M. Coppey-Moisan..., 2009. Quantitative comparison of different fluorescent protein couples for fast FRETFLIM acquisition. Biophys. J. 97:2368-2376.
29. Saudou, F., S. Finkbeiner, ..., M. E. Greenberg. 1998. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell. 95:55-66.
30. Cummings, C. J., E. Reinstein, ..., H. Y. Zoghbi. 1999. Mutation of the E6-AP ubiquitin ligase reduces nuclear inclusion frequency while accelerating polyglutamine-induced pathology in SCA1 mice. Neuron. 24:879-892.
31. Taylor, J. P., F. Tanaka, ..., K. H. Fischbeck. 2003. Aggresomes protect cells by enhancing the degradation of toxic polyglutamine-containing protein. Hum. Mol. Genet. 12:749-757.
32. Sánchez, I., C. Mahlke, and J. Yuan. 2003. Pivotal role of oligomerization in expanded polyglutamine neurodegenerative disorders. Nature. 421:373-379.
33. Nekooki-Machida, Y., M. Kurosawa, ..., M. Tanaka. 2009. Distinct conformations of in vitro and in vivo amyloids of huntingtin-exon1 show different cytotoxicity. Proc. Natl. Acad. Sci. USA. 106:9679-9684.
34. Conway, K. A., J. D. Harper, and P. T. Lansbury, Jr. 2000. Fibrils formed in vitro from alpha-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid. Biochemistry. 39:2552-2563.
35. Janson, J., R. H. Ashley, ..., P. C. Butler. 1999. The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediatesized toxic amyloid particles. Diabetes. 48:491-498.
36. Bucciantini, M., E. Giannoni, ..., M. Stefani. 2002. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature. 416:507-511.
37. Reference deleted in proof.
38. Fayazi, Z., S. Ghosh, ..., P. Kazemi-Esfarjani. 2006. A Drosophila ortholog of the human MRJ modulates polyglutamine toxicity and aggregation. Neurobiol. Dis. 24:226-244.
39. Gong, B., M. C. Lim, ..., A. J. Morton. 2008. Time-lapse analysis of aggregate formation in an inducible PC12 cell model of Huntington's disease reveals time-dependent aggregate formation that transiently delays cell death. Brain Res. Bull. 75:145-157.
40. Chen, Y., J. D. Müller, ..., E. Gratton. 1999. The photon counting histogram in fluorescence fluctuation spectroscopy. Biophys. J. 77:553-567.
41. Lee, C. C., R. H. Walters, and R. M. Murphy. 2007. Reconsidering the mechanism of polyglutamine peptide aggregation. Biochemistry. 46:12810-12820.
42. Kotliarova, S., N. R. Jana, ..., N. Nukina. 2005. Decreased expression of hypothalamic neuropeptides in Huntington disease transgenic mice with expanded polyglutamine-EGFP fluorescent aggregates. J. Neurochem. 93:641-653.