An intermediate structure in the thermal unfolding of the GTPase domain of human septin 4 (SEPT4/bradeion-β) forms amyloid-like filaments in vitro

Biochemistry

Volumn 46, Issue 39, 2007, Pages 11101-11109

  Garcia, Wanius ^a   De Araújo, Ana Paula Ulian ^a   Lara, Flávio ^b   Foguel, Debora ^b   Tanaka, Manami ^c   Tanaka, Tomoo ^d   Garratt, Richard Charles ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^d TOKAI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINESIS; EXOCYTOSIS; HETEROPOLYMERS; THERMAL UNFOLDING; VESICLE TRAFFICKING;

AGGLOMERATION; DISEASES; ELECTRON MICROSCOPY; KETONES; NUCLEOTIDES;

PROTEINS;

AMINO ACID; AMYLOID; CONGO RED; GUANOSINE TRIPHOSPHATASE; NUCLEOTIDE; SEPTIN; SEPTIN 4; TAU PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; CYTOKINESIS; ELECTRON MICROSCOPY; EXOCYTOSIS; HIGH TEMPERATURE; HUMAN; IMAGE ANALYSIS; MEASUREMENT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN UNFOLDING;

AMYLOID; CHROMATOGRAPHY, GEL; CIRCULAR DICHROISM; CONGO RED; CYTOSKELETAL PROTEINS; GTP PHOSPHOHYDROLASES; HEAT; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, BIOLOGICAL; MODELS, CHEMICAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; TRANSITION TEMPERATURE;

MAMMALIA;

EID: 34848893368     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700702w     Document Type: Article

References (40)

1. Frazier, J. A., Wong, M. L., Longtine, M. S., Pringle, J. R., Mann, M., Mitchison, T. J., and Field, C. (1998) Polymerization of purified yeast septins: Evidence that organized filament arrays may not be required for septin function, J. Cell Biol. 143, 737-749.
2. Field, C. M., al-Awar, O., Rosenblatt, J., Wong, M. L., Alberts, D., and Mitchison, T. J. (1996) A purified Drosophila septin complex forms filaments and exhibits GTPase activity, J. Cell Biol. 133, 605-616.
3. Hsu, S. C., Hazuka, C. D., Roth, R., Foletti, D. L., Heuser, J., and Scheller, R. H. (1998) Subunit composition, protein interactions, and structures of the mammalian brain sec6/8 complex and septin filaments, Neuron 20, 1111-1122.
4. Sheffield, P. J., Oliver, C. J., Kremer, B. E., Sheng, S., Shao, Z., and Macara, I. G. (2003) Borg/Septin interactions and the assembly of mammalian septin heterodimers, trimers, and filaments, J. Biol. Chem. 278, 3483-3488.
5. Kinoshita, M., Field, C. M., Coughlin, M. L., Straight, A. F., and Mitchison, T. J. (2002) Self- and actin-templated assembly of mammalian septins, Dev. Cell 3, 791-802.
6. Mendoza, M., Hyman, A. A., and Glotzer, M. (2002) GTP binding induces filament assembly of a recombinant septin, Curr. Biol. 12, 1858-1863.
7. Huang, Y., Surka, M. C., Reynaud, D., Pace-Asciak, C., and Trimble, W. S. (2006) GTP binding and hydrolysis of human septin2, FEBS J. 273, 3248-3260.
8. Macara, I. G., Baldarelli, R., Field, C. M., Glotzer, M., Hayashi, Y., Hsu, S. C., Kennedy, M. B., Kinoshita, M., Longtine, M., Low, C., Maltais, L. J., McKenzie, L., Mitchison, T. J., Nishikawa, T., Noda, M., Petty, E. M., Peifer, M., Pringle, J. R., Robinson, P. J., Roth, D., Russell, S. E., Stuhlmann, H., Tanaka, M., Tanaka, T., Trimble, W. S., Ware, J., Zeleznik-Le, N. J., and Zieger, B. (2002) Mammalian septins nomenclature, Mol. Biol. Cell 13, 4111-4113.
9. Kartmann, B., and Roth, D. (2001) Novel roles for mammalian septins: From vesicle trafficking to oncogenesis, J. Cell Sci. 114, 839-844.
10. Martinez, C., Sanjuan, M. A., Dent, J. A., Karlsson, L., and Ware, J. (2004) Human septin-septin interactions as a prerequisite for targeting septin complexes in the cytosol, Biochem. J. 382, 783-791.
11. Field, C. M., and Kellogg, D. (1999) Septins: Structural polymers or signaling GTPases, Trends Cell Biol. 9, 387-394.
12. Zhang, J., Kong, C., Xie, H., McPherson, P. S., Grinstein, S., and Trimble, W. S. (1999) Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP, Curr. Biol. 9, 1458-1467.
13. Hillebrand, S., Garcia, W., Cantu, M. D., Araújo, A. P. U., Tanaka, M., Tanaka, T., Garratt, R. C., and Carrilho, E. (2005) In vitro monitoring of GTPase activity and enzyme kinetics studies using capillary electrophoresis, Anal. Bioanal. Chem. 383, 92-97.
14. Tanaka, M., Tanaka, T., Kijima, H., Itoh, J., Matsuda, T., Hori, S., and Yamamoto, M. (2001) Characterization of tissue- and cell-type-specific expression of a novel human septin family gene, Bradeion, Biochem. Biophys. Res. Commun. 286, 547-553.
15. Xie, H., Surka, M., Howard, J., and Trimble, W. S. (1999) Characterization of the mammalian septin H5: Distinct patterns of cytoskeletal and membrane association from other septin proteins, Cell Motil. Cytoskeleton 43, 52-62.
16. Larisch, S., Youngsuk, Y., Lotan, R., Kerner, H., Eimerl, S., Parks, W. T., Gottfried, Y., Reffey, S. B., Caestecker, M. P., Danielpour, D., Book-Melamed, N., Timberg, R., Duckett, C. S., Lechleider, R. J., Steiler, H., Orly, J., Kim, S., and Roberts, A. B. (2000) A novel mitochondrial septin-like protein, ARTS, mediates apoptosis dependent on its P-loop motif, Nat. Cell Biol. 2, 915-921.
17. Tanaka, T., Kijima, H., Itoh, J., Matsuda, T., and Tanaka, T. (2002) Impaired expression of a human septin family gene Bradeion inhibits the growth and tumorigenesis of colorectal cancer in vitro and in vivo, Cancer Gene Ther. 9, 483-488.
18. Kinoshita, A., Kinoshita, M., Akiyama, H., Tomimoto, H., Akiguchi, I., Kumar, S., Noda, M., and Kimura, J. (1998) Identification of septins in neurofibrillary tangles in Alzheimer's disease, Am. J. Pathol. 153, 1551-1560.
19. Ihara, M., Tomimoto, H., Kitayama, H., Morioka, Y., Akigunchi, I., Shibasaki, H., Noda, M., and Kinoshita, M. (2003) Association of the cytoskeletal GTP-binding protein Sept4/H5 with cytoplasmatic inclusions found in Parkinson's disease and others synucleinopathies, J. Biol. Chem. 278, 24095-24012.
20. 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.
21. Selkoe, D. J. (2004) Cell biology of protein misfolding: The examples of Alzheimer's and Parkinson's diseases, Nat. Cell Biol. 6, 1054-1061.
22. Ross, C. A., and Poirier, M. A. (2004) Protein aggregation and neurodegenerative disease, Nat. Med. 10, S10-S17.
23. Dobson, C. M. (2003) Protein folding and misfolding, Nature 426, 884-890.
24. Ross, C. A., and Margolis, R. L. (2005) Neurogenetics: Insights into degenerative diseases and approaches to schizophrenia, Clin. Neurosci. Res. 5, 3-14.
25. Makin, O. S., and Serpell, L. C. (2005) Structures for amyloid fibrils, FEBS J. 272, 5950-5961.
26. Sunde, M., and Blake, C. F. (1998) From the globular to the fibrous state: Protein structure and structural conversion in amyloid formation, Q. Rev. Biophys. 31, 1-39.
27. Garcia, W., Araújo, A. P. U., Neto, M. O., Ballestero, M. R. M., Polikarpov, I., Tanaka, M., Tanaka, T., and Garratt, R. C. (2006) Dissection of a human Septin: Definition and characterization of distinct domains within human SEPT4, Biochemistry 45, 13918-13931.
28. Gill, S. C., and von Hippel, P. H. (1989) Calculation of proteins extinction coefficients from amino acid sequence data, Anal. Biochem. 182, 319-326.
29. Seckler, R., Wu, G. M., and Timasheff, S. N. (1990) Interactions of tubulin with guanylyl-(β-γ-methylene)diphosphate, J. Biol. Chem. 265, 7655-7661.
30. Edmonds, B. T., Bell, A., Wyckoff, J., Condeelis, J., and Leyh, T. S. (1998) The effect of F-actin on the binding and hydrolysis of guanine nucleotide by Dictyostelium elongation factor 1A, J. Biol. Chem. 273, 10288-10295.
31. Mitchison, T., and Field, C. M. (2002) Cytoskeleton: What does GTP do for dispatch septins? Curr. Biol. 12, R788-R790.
32. Semisotnov, G. V., Rodionova, A. N., Kutyshenko, V. P., Ebert, B., Blanck, J., and Ptitsyn, O. B. (1987) Sequential mechanism of refolding of carbonic anhydrase-b, FEBS Lett. 224, 9-13.
33. Srisailam, S., Wang, H. M., Kumar, T. K. S., Rajalingam, D., Sivaraja, V., Sheu, H. S., Chang, Y. C., and Yu, C. (2002) Amyloid-like fibril formation in an all β-barrel protein involves the formation of partially structured intermediate(s), J. Biol. Chem. 277, 19027-19036.
34. Fandrich, M., Forge, V., Buder, K., Kittler, M., Dobson, C. M., and Diekmann, S. (2003) Myoglobin forms amyloid fibrils by association of unfolded polypeptide segments, Proc. Natl. Acad. Sci. U.S.A. 100, 15463-15468.
35. Kang, F., Purich, D. L., and Southwick, F. S. (1999) Profilin promotes barbed-end actin filament assembly without lowering the critical concentration, J. Biol. Chem. 274, 36963-36972.
36. Romberg, L., Simon, M., and Erickson, H. P. (2001) Polymerization of FtsZ, a bacterial homolog of tubulin, is assembly cooperative, J. Biol. Chem. 276, 11743-11753.
37. Chiti, F., and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease, Annu. Rev. Biochem. 75, 333-366.
38. Hall, P., and Russell, S. (2004) The pathobiology of the septin gene family, J. Pathol. 204, 489-505.
39. Low, C., and Macara, I. G. (2006) Structural analysis of septin 2, 6 and 7 complexes, J. Biol. Chem. 281, 30697-30706.
40. Tanaka, M., Tanaka, T., Matsuzaki, S., Seto, Y., Matsuda, T., Komori, K., Itoh, J., Kijima, H., Tamai, K., Shibayama, M., Hashimoto, Y., Nakazawa, H., and Toma, H. (2003) Rapid and quantitative detection of human septin family Bradeion as a practical diagnostic method of colorectal and urologic cancers, Med. Sci. Monit. 9, CR2-CR9.