The interaction of polyglutamine peptides with lipid membranes is regulated by flanking sequences associated with huntingtin

Journal of Biological Chemistry

Volumn 288, Issue 21, 2013, Pages 14993-15005

  Burke, Kathleen A ^a   Kauffman, Karlina J ^b   Umbaugh, C Samuel ^a   Frey, Shelli L ^b   Legleiter, Justin ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b GETTYSBURG COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRILLAR AGGREGATES; FLANKING SEQUENCE; HUNTINGTON DISEASE; INCLUSION BODIES; LANGMUIR TROUGH TECHNIQUE; LIPID MEMBRANES; MODEL MEMBRANES; SITU ATOMIC FORCE MICROSCOPY;

AMINO ACIDS; ATOMIC FORCE MICROSCOPY; LIPID BILAYERS; LIPIDS; MICA; PEPTIDES;

AGGREGATES;

GLUTAMINE; HUNTINGTIN; POLYGLUTAMINE; POLYPEPTIDE; POLYPROLINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA FLANKING REGION; EXON; LIPID BILAYER; LIPID MEMBRANE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION;

ATOMIC FORCE MICROSCOPY; HUNTINGTONS DISEASE; LIPIDS; POLYGLUTAMINE; POLYGLUTAMINE DISEASE; PROTEIN AGGREGATION;

ANIMALS; EXONS; LIPID BILAYERS; MICE; MICROSCOPY, ATOMIC FORCE; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84878217830     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.446237     Document Type: Article

References (57)

1. The Huntington Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72, 971-983
2. 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 (Pubitemid 27449140)
3. Ravina, B., Romer, M., Constantinescu, R., Biglan, K., Brocht, A., Kieburtz, K., Shoulson, I., and McDermott, M. P. (2008) The relationship between CAG repeat length and clinical progression in Huntington's disease. Movement Disord. 23, 1223-1227
4. Kim, Y. J., Yi, Y., Sapp, E., Wang, Y., Cuiffo, B., Kegel, K. B., Qin, Z. H., Aronin, N., and DiFiglia, M. (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. U.S.A. 98, 12784-12789 (Pubitemid 33020022)
5. Ratovitski, T., Gucek, M., Jiang, H., Chighladze, E., Waldron, E., D'Ambola, J., Hou, Z., Liang, Y., Poirier, M. A., Hirschhorn, R. R., Graham, R., Hayden, M. R., Cole, R. N., and Ross, C. A. (2009) Mutant Huntingtin N-terminal fragments of specific size mediate aggregation and toxicity in neuronal cells. J. Biol. Chem. 284, 10855-10867
6. Davies, S. W., Turmaine, M., Cozens, B. A., DiFiglia, M., Sharp, A. H., Ross, C. A., Scherzinger, E., Wanker, E. E., Mangiarini, L., and Bates, G. P. (1997) Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 90, 537-548 (Pubitemid 27347243)
7. Landles, C., Sathasivam, K., Weiss, A., Woodman, B., Moffitt, H., Finkbeiner, S., Sun, B., Gafni, J., Ellerby, L. M., Trottier, Y., Richards, W. G., Osmand, A., Paganetti, P., and Bates, G. P. (2010) Proteolysis of mutant Huntingtin produces an exon 1 fragment that accumulates as an aggregated protein in neuronal nuclei in Huntington disease. J. Biol. Chem. 285, 8808-8823
8. Bulone, D., Masino, L., Thomas, D. J., San Biagio, P. L., and Pastore, A. (2006) The interplay between polyQ and protein context delays aggregation by forming a reservoir of protofibrils. PLoS One 1, e111
9. Ignatova, Z., and Gierasch, L. M. (2006) Extended polyglutamine tracts cause aggregation and structural perturbation of an adjacent β barrel protein. J. Biol. Chem. 281, 12959-12967 (Pubitemid 43855389)
10. Jayaraman, M., Kodali, R., Sahoo, B., Thakur, A. K., Mayasundari, A., Mishra, R., Peterson, C. B., and Wetzel, R. (2012) Slow amyloid nucleation via α-helix-rich oligomeric intermediates in short polyglutamine-containing Huntingtin fragments. J. Mol. Biol. 415, 881-899
11. Thakur, A. K., Jayaraman, M., Mishra, R., Thakur, M., Chellgren, V. M., Byeon, I.-J., 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
12. Mishra, R., Jayaraman, M., Roland, B. P., Landrum, E., Fullam, T., Kodali, R., Thakur, A. K., Arduini, I., and Wetzel, R. (2012) Inhibiting the nucleation of amyloid structure in a Huntingtin fragment by targeting α-helixrich oligomeric intermediates. J. Mol. Biol. 415, 900-917
13. Bhattacharyya, A., Thakur, A. K., Chellgren, V. M., Thiagarajan, G., Williams, A. D., Chellgren, B. W., Creamer, T. P., and Wetzel, R. (2006) Oligoproline effects on polyglutamine conformation and aggregation. J. Mol. Biol. 355, 524-535 (Pubitemid 41785754)
14. Darnell, G., Orgel, J. P., Pahl, R., and Meredith, S. C. (2007) Flanking polyproline sequences inhibit β-sheet structure in polyglutamine segments by inducing PPII-like helix structure. J. Mol. Biol. 374, 688-704 (Pubitemid 350027728)
15. Kegel, K. B., Kim, M., Sapp, E., McIntyre, C., Castaño, J. G., Aronin, N., and DiFiglia, M. (2000) Huntingtin expression stimulates endosomal-lysosomal activity, endosome tubulation, and autophagy. J. Neurosci. 20, 7268-7278
16. Suopanki, J., Götz, C., Lutsch, G., Schiller, J., Harjes, P., Herrmann, A., and Wanker, E. E. (2006) Interaction of huntingtin fragments with brain membranes. Clues to early dysfunction in Huntington's disease. J. Neurochem. 96, 870-884
17. Valencia, A., Reeves, P. B., Sapp, E., Li, X., Alexander, J., Kegel, K. B., Chase, K., Aronin, N., and DiFiglia, M. (2010) Mutant Huntingtin and glycogen synthase kinase 3-β accumulate in neuronal lipid rafts of a presymptomatic knock-in mouse model of Huntington's disease. J. Neurosci. Res. 88, 179-190
18. Kegel, K. B., Sapp, E., Yoder, J., Cuiffo, B., Sobin, L., Kim, Y. J., Qin, Z. H., Hayden, M. R., Aronin, N., Scott, D. L., Isenberg, G., Goldmann, W. H., and DiFiglia, M. (2005) Huntingtin associates with acidic phospholipids at the plasma membrane. J. Biol. Chem. 280, 36464-36473 (Pubitemid 41633920)
19. Michalek, M., Salnikov, E. S., Werten, S., and Bechinger, B. (2013) Membrane interactions of the amphipathic amino terminus of Huntingtin. Biochemistry 52, 847-858
20. 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 (Pubitemid 47617727)
21. Trettel, F., Rigamonti, D., Hilditch-Maguire, P., Wheeler, V. C., Sharp, A. H., Persichetti, F., Cattaneo, E., and MacDonald, M. E. (2000) Dominant phenotypes produced by the HD mutation in STHdh(Q111) striatal cells. Hum. Mol. Genet. 9, 2799-2809
22. Rockabrand, E., Slepko, N., Pantalone, A., Nukala, V. N., Kazantsev, A., Marsh, J. L., Sullivan, P. G., Steffan, J. S., Sensi, S. L., and Thompson, L. M. (2007) The first 17 amino acids of Huntingtin modulate its subcellular localization, aggregation and effects on calcium homeostasis. Hum. Mol. Genet. 16, 61-77 (Pubitemid 46156597)
23. 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
24. Chen, S., and Wetzel, R. (2001) Solubilization and disaggregation of polyglutamine peptides. Protein Sci. 10, 887-891 (Pubitemid 32240515)
25. Muchowski, P. J., Schaffar, G., Sittler, A., Wanker, E. E., Hayer-Hartl, M. K., and Hartl, F. U. (2000) Hsp70 and Hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc. Natl. Acad. Sci. U.S.A. 97, 7841-7846 (Pubitemid 30460735)
26. Legleiter, J., Park, M., Cusick, B., and Kowalewski, T. (2006) Scanning probe acceleration microscopy (SPAM) in fluids. Mapping mechanical properties of surfaces at the nanoscale. Proc. Natl. Acad. Sci. U.S.A. 103, 4813-4818
27. Burke, K. A., Godbey, J., and Legleiter, J. (2011) Assessing mutant huntingtin fragment and polyglutamine aggregation by atomic force microscopy. Methods 53, 275-284
28. Legleiter, J., DeMattos, R. B., Holtzman, D. M., and Kowalewski, T. (2004) In situ AFM studies of astrocyte-secreted apolipoprotein E- and J-containing lipoproteins. J. Colloid. Interface Sci. 278, 96-106 (Pubitemid 39094480)
29. Gekko, K., and Noguchi, H. (1979) Compressibility of globular proteins in water at 25°C. J. Phys. Chem. 83, 2706-2714
30. Squire, P. G., and Himmel, M. E. (1979) Hydrodynamics and protein hydration. Arch. Biochem. Biophys. 196, 165-177
31. Seelig, A. (1987) Local anesthetics and pressure: a comparison of dibucaine binding to lipid monolayers and bilayers. Biochim. Biophys. Acta 899, 196-204
32. Anderson, R. L., and Davis, S. (1982) An organic phosphorus assay which avoids the use of hazardous perchloric acid. Clin. Chim. Acta 121, 111-116 (Pubitemid 12156751)
33. Rouser, G., Fkeischer, S., and Yamamoto, A. (1970) Two-dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids 5, 494-496
34. Chou, H. T., Wen, H. W., Kuo, T. Y., Lin, C. C., and Chen, W. J. (2010) Interaction of cationic antimicrobial peptides with phospholipid vesicles and their antibacterial activity. Peptides 31, 1811-1820
35. Lamazière, A., Burlina, F., Wolf, C., Chassaing, G., Trugnan, G., and Ayala-Sanmartin, J. (2007) Non-metabolic membrane tubulation and permeability induced by bioactive peptides. PLoS One 2, e201
36. 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
37. Groves, J. T., Ulman, N., and Boxer, S. G. (1997) Micropatterning fluid lipid bilayers on solid supports. Science 275, 651-653 (Pubitemid 27061329)
38. Seelig, A., Blatter, X. L., Frentzel, A., and Isenberg, G. (2000) Phospholipid binding of synthetic talin peptides provides evidence for an intrinsic membrane anchor of talin. J. Biol. Chem. 275, 17954-17961 (Pubitemid 30414739)
39. Shamitko-Klingensmith, N., Molchanoff, K. M., Burke, K. A., Magnone, G. J., and Legleiter, J. (2012) Mapping the mechanical properties of cholesterol-containing supported lipid bilayers with nanoscale spatial resolution. Langmuir 28, 13411-13422
40. Williamson, T. E., Vitalis, A., Crick, S. L., and Pappu, R. V. (2010) Modulation of polyglutamine conformations and dimer formation by the N-terminus of Huntingtin. J. Mol. Biol. 396, 1295-1309
41. 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
42. Clayton, D. F., and George, J. M. (1998) The synucleins. A family of proteins involved in synaptic function, plasticity, neurodegeneration and disease. Trends Neurosci. 21, 249-254 (Pubitemid 28239982)
43. Knight, J. D., and Miranker, A. D. (2004) Phospholipid catalysis of diabetic amyloid assembly. J. Mol. Biol. 341, 1175-1187 (Pubitemid 39099208)
44. Chen, S., Ferrone, F. A., and Wetzel, R. (2002) Huntington's disease age-of-onset linked to polyglutamine aggregation nucleation. Proc. Natl. Acad. Sci. U.S.A. 99, 11884-11889 (Pubitemid 34994493)
45. Burke, K. A., Yates, E. A., and Legleiter, J. (2013) Biophysical insights into how surfaces, including lipid membranes, modulate protein aggregation related to neurodegeneration. Front. Neurol. 4, 17
46. Hirakura, Y., Azimov, R., Azimova, R., and Kagan, B. L. (2000) Polyglutamine-induced ion channels. A possible mechanism for the neurotoxicity of Huntington and other CAG repeat diseases. J. Neurosci. Res. 60, 490-494 (Pubitemid 30252911)
47. Monoi, H., Futaki, S., Kugimiya, S., Minakata, H., and Yoshihara, K. (2000) Poly-L-glutamine forms cation channels. Relevance to the pathogenesis of the polyglutamine diseases. Biophys. J. 78, 2892-2899 (Pubitemid 30396922)
48. Darnell, G. D., Derryberry, J., Kurutz, J. W., and Meredith, S. C. (2009) Mechanism of cis-inhibition of polyQ fibrillation by polyP. PPII oligomers and the hydrophobic effect. Biophys. J. 97, 2295-2305
49. Atwal, R. S., Desmond, C. R., Caron, N., Maiuri, T., Xia, J., Sipione, S., and Truant, R. (2011) Kinase inhibitors modulate Huntingtin cell localization and toxicity. Nat. Chem. Biol. 7, 453-460
50. Gu, X., Greiner, E. R., Mishra, R., Kodali, R., Osmand, A., Finkbeiner, S., Steffan, J. S., Thompson, L. M., Wetzel, R., and Yang, X. W. (2009) Serines 13 and 16 are critical determinants of full-length human mutant Huntingtin induced disease pathogenesis in HD mice. Neuron 64, 828-840
51. Southwell, A. L., Ko, J., and Patterson, P. H. (2009) Intrabody gene therapy ameliorates motor, cognitive, and neuropathological symptoms in multiple mouse models of Huntington's disease. J. Neurosci. 29, 13589-13602
52. Colby, D. W., Garg, P., Holden, T., Chao, G., Webster, J. M., Messer, A., Ingram, V. M., and Wittrup, K. D. (2004) Development of a human light chain variable domain (V-L) intracellular antibody specific for the amino terminus of Huntingtin via yeast surface display. J. Mol. Biol. 342, 901-912 (Pubitemid 39165658)
53. Nekooki-Machida, Y., Kurosawa, M., Nukina, N., Ito, K., Oda, T., and Tanaka, M. (2009) Distinct conformations of in vitro and in vivo amyloids of huntingtin-exon1 show different cytotoxicity. Proc. Natl. Acad. Sci. U.S.A. 106, 9679-9684
54. Bugg, C. W., Isas, J. M., Fischer, T., Patterson, P. H., and Langen, R. (2012) Structural features and domain organization of huntingtin fibrils. J. Biol. Chem. 287, 31739-31746
55. Janmey, P. A., and Weitz, D. A. (2004) Dealing with mechanics. Mechanisms of force transduction in cells. Trends Biochem. Sci. 29, 364-370 (Pubitemid 38968753)
56. Vogel, V., and Sheetz, M. (2006) Local force and geometry sensing regulate cell functions. Nat. Rev. Mol. Cell Biol. 7, 265-275
57. Lloyd, K. G., and Davidson, L. (1979) H-3 GABA binding in brains from Huntington chorea patients, Altered regulation by phospholipids. Science 205, 1147-1149 (Pubitemid 9256373)