Super-resolution fluorescence of huntingtin reveals growth of globular species into short fibers and coexistence of distinct aggregates

ACS Chemical Biology

Volumn 9, Issue 12, 2014, Pages 2767-2778

  Duim, Whitney C ^a,b   Jiang, Yan ^a,c   Shen, Koning ^a   Frydman, Judith ^a   Moerner, W E ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUNTINGTIN; MONOMER; PROTEIN AGGREGATE; HTT PROTEIN, HUMAN; HYBRID PROTEIN; NERVE PROTEIN;

ADSORPTION; ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; EXON; FIBER; FLUORESCENCE IMAGING; IMAGE ANALYSIS; MORPHOLOGY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN AGGREGATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SURFACE PROPERTY; ULTRASOUND; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; MOLECULAR IMAGING; PROCEDURES; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SPECTROFLUOROMETRY; TIME FACTOR;

ESCHERICHIA COLI; EXONS; GENE EXPRESSION; HUMANS; MOLECULAR IMAGING; NERVE TISSUE PROTEINS; PROTEIN AGGREGATES; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RECOMBINANT FUSION PROTEINS; SONICATION; SPECTROMETRY, FLUORESCENCE; TIME FACTORS;

EID: 84919702871     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb500335w     Document Type: Article

References (61)

1. The Huntingtons Disease Collaborative Research Group. (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on huntington disease chromosomes Cell 72, 971-983
2. Imarisio, S., Carmichael, J., Korolchuk, V., Chen, C., Saiki, S., Rose, C., Krishna, G., Davies, J. E., Ttofi, E., Underwood, B. R., and Rubinsztein, D. C. (2008) Huntingtons disease: From pathology and genetics to potential therapies Biochem. J. 412, 191-209
3. DiFiglia, M., Sapp, E., Chase, K. O., Davies, S. W., Bates, G. P., Vonsattel, J. P., and Aronin, N. (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain Science 277, 1990-1993
4. Nagai, Y., Inui, T., Popiel, H. A., Fujikake, N., Hasegawa, K., Urade, Y., Goto, Y., Naiki, H., and Toda, T. (2007) A toxic monomeric conformer of the polyglutamine protein Nat. Struct. Mol. Biol. 14, 332-340
5. Miller, J., Arrasate, M., Brooks, E., Libeu, C. P., Legleiter, J., Hatters, D., Curtis, J., Cheung, K., Krishnan, P., Mitra, S., Widjaja, K., Shaby, B. A., Lotz, G. P., Newhouse, Y., Mitchell, E. J., Osmand, A., Gray, M., Thulasiramin, V., Saudou, F., Segal, M., Yang, X. W., Masliah, E., Thompson, L. M., Muchowski, P. J., Weisgraber, K. H., and Finkbeiner, S. (2011) Identifying polyglutamine protein species in situ that best predict neurodegeneration Nat. Chem. Biol. 7, 925-934
6. Schaffar, G., Breuer, P., Boteva, R., Behrends, C., Tzvetkov, N., Strippel, N., Sakahira, H., Siegers, K., Hayer-Hartl, M., and Hartl, F. U. (2004) Cellular toxicity of polyglutamine expansion proteins: Mechanism of transcription factor deactivation Mol. Cell 15, 95-105
7. Arrasate, M., Mitra, S., Schweitzer, E. S., Segal, M. R., and Finkbeiner, S. (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death Nature 431, 805-810
8. Pieri, L., Madiona, K., Bousset, L., and Melki, R. (2012) Fibrillar α-synuclein and huntingtin exon 1 assemblies are toxic to the cells Biophys. J. 102, 2894-2905
9. Poirier, M. A., Li, H., Macosko, J., Cai, S., Amzel, M., and Ross, C. A. (2002) Huntingtin spheroids and protofibrils as precursors in polyglutamine fibrilization J. Biol. Chem. 277, 41032-41037
10. Ross, C. A., Poirier, M. A., Wanker, E. E., and Amzel, M. (2003) Polyglutamine fibrillogenesis: The pathway unfolds Proc. Natl. Acad. Sci. U. S. A. 100, 1-3
11. Legleiter, J., Mitchell, E., Lotz, G. P., Sapp, E., Ng, C., DiFiglia, M., Thompson, L. M., and Muchowski, P. J. (2010) Mutant huntingtin fragments form oligomers in a polyglutamine length-dependent manner in vitro and in vivo J. Biol. Chem. 285, 14777-14790
12. Burke, K. A., Godbey, J., and Legleiter, J. (2011) Assessing mutant huntingtin fragment and polyglutamine aggregation by atomic force microscopy Methods 53, 275-284
13. Thakur, A. K., Jayaraman, M., Mishra, R., Thakur, M., Chellgren, V. M., Byeon, I.-J. L., Anjum, D. H., Kodali, R., Creamer, T. P., Conway, J. F., Gronenborn, A. M., and Wetzel, R. (2009) Polyglutamine disruption of the huntingtin exon 1 N terminus triggers a complex aggregation mechanism Nat. Struct. Mol. Biol. 16, 380-389
14. Tam, S., Spiess, C., Auyeung, W., Joachimiak, L., Chen, B., Poirier, M. A., and Frydman, J. (2009) The chaperonin TRiC blocks a huntingtin sequence element that promotes the conformational switch to aggregation Nat. Struct. Mol. Biol. 16, 1279-1285
15. Kim, M. W., Chelliah, Y., Kim, S. W., Otwinowski, Z., and Bezprozvanny, I. (2009) Secondary structure of huntingtin amino-terminal region Structure 17, 1205-1212
16. Sivanandam, V. N., Jayaraman, M., Hoop, C. L., Kodali, R., Wetzel, R., Van der Wel, and Patrick, C. A. (2011) The aggregation-enhancing huntingtin N-terminus is helical in amyloid fibrils J. Am. Chem. Soc. 133, 4558-4566
17. Kelley, N. W., Huang, X., Tam, S., Spiess, C., Frydman, J., and Pande, V. S. (2009) The predicted structure of the headpiece of the huntingtin protein and its implications on huntingtin aggregation J. Mol. Biol. 388, 919-927
18. Scherzinger, E., Sittler, A., Schweiger, K., Heiser, V., Lurz, R., Hasenbank, R., Bates, G. P., Lehrach, H., and Wanker, E. E. (1999) Self-assembly of polyglutamine-containing huntingtin fragments into amyloid-like fibrils: Implications for Huntingtons disease pathology Proc. Natl. Acad. Sci. U. S. A. 96, 4604-4609
19. Sathasivam, K., Lane, A., Legleiter, J., Warley, A., Woodman, B., Finkbeiner, S., Paganetti, P., Muchowski, P. J., Wilson, S., and Bates, G. P. (2010) Identical oligomeric and fibrillar structures captured from the brains of R6/2 and knock-in mouse models of huntingtons disease Hum. Mol. Genet. 19, 65-78
20. Suhr, S. T., Senut, M., Whitelegge, J. P., Faull, K. F., Cuizon, D. B., and Gage, F. H. (2001) Identities of sequestered proteins in aggregates from cells with induced polyglutamine expression J. Cell Biol. 153, 283-294
21. Muchowski, P. J. and Wacker, J. L. (2005) Modulation of neurodegeneration by molecular chaperones Nat. Rev. Neurosci. 6, 11-22
22. Tam, S., Geller, R., Spiess, C., and Frydman, J. (2006) The chaperonin TRiC controls polyglutamine aggregation and toxicity through subunit-specific interactions Nat. Cell Biol. 8, 1155-1162
23. Behrends, C., Langer, C. A., Boteva, R., Böttcher, U. M., Stemp, M. J., Schaffar, G., Rao, B. V., Giese, A., Kretzschmar, H., Siegers, K., and Hartl, F. U. (2006) Chaperonin TRiC promotes the assembly of polyQ expansion proteins into nontoxic oligomers Mol. Cell 23, 887-897
24. Kitamura, A., Kubota, H., Pack, C., Matsumoto, G., Hirayama, S., Takahashi, Y., Kimura, H., Kinjo, M., Morimoto, R. I., and Nagata, K. (2006) Cytosolic chaperonin prevents polyglutamine toxicity with altering the aggregation state Nat. Cell Biol. 8, 1163-1169
25. Inoue, Y., Kishimoto, A., Hirao, J., Yoshida, M., and Taguchi, H. (2001) Strong growth polarity of yeast prion fiber revealed by single fiber imaging J. Biol. Chem. 276, 35227-35230
26. Collins, S. R., Douglass, A., Vale, R. D., and Weissman, J. S. (2004) Mechanism of prion propagation: Amyloid growth occurs by monomer addition PLoS Biol. 2, e321
27. Ban, T., Hamada, D., Hasegawa, K., Naiki, H., and Goto, Y. (2003) Direct observation of amyloid fibril growth monitored by thioflavin T fluorescence J. Biol. Chem. 278, 16462-16465
28. Andersen, C. B., Yagi, H., Manno, M., Martorana, V., Ban, T., Christiansen, G., Otzen, D. E., Goto, Y., and Rischel, C. (2009) Branching in amyloid fibril growth Biophys. J. 96, 1529-1536
29. Ban, T., Hoshino, M., Takahashi, S., Hamada, D., Hasegawa, K., Naiki, H., and Goto, Y. (2004) Direct observation of Aβ amyloid fibril growth and inhibition J. Mol. Biol. 344, 757-767
30. Liang, Y., Lynn, D. G., and Berland, K. M. (2010) Direct observation of nucleation and growth in amyloid self-assembly J. Am. Chem. Soc. 132, 6306-6308
31. Huang, B., Babcock, H., and Zhuang, X. (2010) Breaking the diffraction barrier: Super-resolution imaging of cells Cell 143, 1047-1058
32. Thompson, M. A., Lew, M. D., and Moerner, W. E. (2012) Extending microscopic resolution with single-molecule imaging and active control Annu. Rev. Biophys. 41, 321-342
33. Duim, W. C., Chen, B., Frydman, J., and Moerner, W. E. (2011) Sub-diffraction imaging of huntingtin protein aggregates by fluorescence blink-microscopy and atomic force microscopy ChemPhysChem. 12, 2387-2390
34. Sahl, S. J., Weiss, L. E., Duim, W. C., Frydman, J., and Moerner, W. E. (2012) Cellular inclusion bodies of mutant huntingtin exon 1 obscure small fibrillar aggregate species Sci. Rep. 2, 1-7
35. Caron, N. S., Hung, C. L., Atwal, R. S., and Truant, R. (2014) Live cell imaging and biophotonic methods reveal two types of mutant huntingtin inclusions Hum. Mol. Genet. 23, 2324-2338
36. Kaminski Schierle, G. S., van de Linde, S., Erdelyi, M., Esbjorner, E. K., Klein, T., Rees, E., Bertoncini, C. W., Dobson, C. M., Sauer, M., and Kaminski, C. F. (2011) In situ measurements of the formation and morphology of intracellular beta-amyloid fibrils by super-resolution fluorescence imaging J. Am. Chem. Soc. 133, 12902-12905
37. Roberti, M. J., Folling, J., Celej, M. S., Bossi, M., Jovin, T. M., and Jares-Erijman, E. A. (2012) Imaging nanometer-sized α-synuclein aggregates by superresolution fluorescence localization microscopy Biophys. J. 102, 1598-1607
38. Ries, J., Udayar, V., Soragni, A., Hornemann, S., Nilsson, K. P., Riek, R., Hock, C., Ewers, H., Aguzzi, A. A., and Rajendran, L. (2013) Superresolution imaging of amyloid fibrils with binding-activated probes ACS Chem. Neurosci. 4, 1057-1061
39. Pinotsi, D., Buell, A. K., Galvagnion, C., Dobson, C. M., Kaminski Schierle, G. S., and Kaminski, C. F. (2014) Direct observation of heterogeneous amyloid fibril growth kinetics via two-color super-resolution microscopy Nano Lett. 14, 339-345
40. Dalal, V., Bhattacharya, M., Narang, D., Sharma, P. K., and Mukhopadhyay, S. (2012) Nanoscale fluorescence imaging of single amyloid fibrils J. Phys. Chem. Lett. 3, 1783-1787
41. Shahmoradian, S. H., Galaz-Montoya, J. G., Schmid, M. F., Cong, Y., Ma, B., Spiess, C., Frydman, J., Ludtke, S. J., and Chiu, W. (2013) TRiCs tricks inhibit huntingtin aggregation eLife 2, e00710
42. Heilemann, M., van de Linde, S., Schüttpelz, M., Kasper, R., Seefeldt, B., Mukherjee, A., Tinnefeld, P., and Sauer, M. (2008) Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes Angew. Chem., Int. Ed. 47, 6172-6176
43. Dempsey, G. T., Vaughan, J. C., Chen, K. H., Bates, M., and Zhuang, X. (2011) Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging Nat. Methods 8, 1027-1036
44. Mangiarini, L., Sathasivam, K., Seller, M., Cozens, B., Harper, A., Hetherington, C., Lawton, M., Trottier, Y., Lehrach, H., Davies, S. W., and Bates, G. P. (1996) Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice Cell 87, 493-506
45. Lee, S., Shin, J. Y., Lee, A., and Bustamante, C. (2012) Counting single photoactivatable fluorescent molecules by photoactivated localization microscopy (PALM) Proc. Natl. Acad. Sci. U. S. A. 109, 17436-17441
46. Annibale, P., Vanni, S., Scarselli, M., Rothlisberger, U., and Radenovic, A. (2011) Quantitative photo activated localization microscopy: Unraveling the effects of photoblinking PLoS One 6, e22678
47. Durisic, N., Laparra-Cuervo, L., Sandoval-Alvarez, A., Borbely, J. S., and Lakadamyali, M. (2014) Single-molecule evaluation of fluorescent protein photoactivation efficiency using an in vivo nanotemplate Nat. Methods 11, 156-162
48. Shroff, H., Galbraith, C. G., Galbraith, J. A., and Betzig, E. (2008) Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics Nat. Methods 5, 417-423
49. Jones, S. A., Shim, S., He, J., and Zhuang, X. (2011) Fast, three-dimensional super-resolution imaging of live cells Nat. Methods 8, 499-505
50. Lunkes, A. and Mandel, J. (1998) A cellular model that recapitulates major pathogenic steps of huntingtons disease Hum. Mol. Genet. 7, 1355-1361
51. Williams, T. L. and Serpell, L. C. (2011) Membrane and surface interactions of alzheimers abeta peptide-insights into the mechanism of cytotoxicity FEBS J. 278, 3905-3917
52. DiFiglia, M., Sapp, E., Chase, K., Schwarz, C., Meloni, A., Young, C., Martin, E., Vonsattel, J., Carraway, R., Reeves, S. A., Boyce, F. M., and Aronin, N. (1995) Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons Neuron 14, 1075-1081
53. Atwal, R. S., Xia, J., Pinchev, D., Taylor, J., Epand, R. M., and Truant, R. (2007) Huntingtin has a membrane association signal that can modulate huntingtin aggregation, nuclear entry and toxicity Hum. Mol. Genet. 16, 2600-2615
54. Kegel, K. B., Sapp, E., Alexander, J., Valencia, A., Reeves, P., Li, X., Masso, N., Sobin, L., Aronin, N., and DiFiglia, M. (2009) Polyglutamine expansion in huntingtin alters its interaction with phospholipids J. Neurochem. 110, 1585-1597
55. Chiti, F. and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75, 333-366
56. Eichner, T. and Radford, S. (2011) A diversity of assembly mechanisms of a generic amyloid fold Mol. Cell 43, 8-18
57. Fischer, H., Polikarpov, I., and Craievich, A. F. (2004) Average protein density is a molecular-weight-dependent function Protein Sci. 13, 2825-2828
58. Bolte, S. and Cordelieres, F. P. (2006) A guided tour into subcellular colocalization analysis in light microscopy J. Microsc. 224, 213-232
59. Dani, A., Huang, B., Bergan, J., Dulac, C., and Zhuang, X. (2010) Superresolution imaging of chemical synapses in the brain Neuron 68, 843-856
60. Biteen, J. S., Thompson, M. A., Tselentis, N. K., Bowman, G. R., Shapiro, L., and Moerner, W. E. (2008) Super-resolution imaging in live caulobacter crescentus cells using photoswitchable EYFP Nat. Methods 5, 947-949
61. Ptacin, J. L., Lee, S. F., Garner, E. C., Toro, E., Eckart, M., Comolli, L. R., Moerner, W. E., and Shapiro, L. (2010) A spindle-like apparatus guides bacterial chromosome segregation Nat. Cell Biol. 12, 791-798