Benzalkonium chloride accelerates the formation of the amyloid fibrils of corneal dystrophy-associated peptides

Journal of Biological Chemistry

Volumn 288, Issue 35, 2013, Pages 25109-25118

  Kato, Yusuke ^a   Yagi, Hisashi ^a   Kaji, Yuichi ^b   Oshika, Tetsuro ^b   Goto, Yuji ^a  

^a OSAKA UNIVERSITY   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID FIBRIL; BENZALKONIUM CHLORIDE; EYE DROPS; POTENTIAL RISKS;

CHLORINE COMPOUNDS; DROPS; GLYCOPROTEINS; PEPTIDES; SODIUM DODECYL SULFATE;

CATIONIC SURFACTANTS;

AMYLOID; BENZALKONIUM CHLORIDE; DODECYL SULFATE SODIUM; KERATOEPITHELIN PEPTIDE; SYNTHETIC PEPTIDE; THIOFLAVINE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMYLOID FIBRILLATION; AMYLOIDOGENICITY; AMYLOIDOSIS; ARTICLE; BINDING AFFINITY; CHEMICAL STRUCTURE; CONCENTRATION (PARAMETERS); CORNEA DYSTROPHY; FLUORESCENCE ANALYSIS; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; RISK ASSESSMENT;

AMYLOID; CORNEA; FLUORESCENCE; MICROSCOPY; PATHOGENESIS; PEPTIDES; PROTEIN AGGREGATION;

AMYLOID; BENZALKONIUM COMPOUNDS; CORNEAL DISEASES; DETERGENTS; EXTRACELLULAR MATRIX PROTEINS; HUMANS; OPHTHALMIC SOLUTIONS; PEPTIDES; SODIUM DODECYL SULFATE; TRANSFORMING GROWTH FACTOR BETA;

EID: 84883311754     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.477695     Document Type: Article

References (44)

1. Munier, F. L., Korvatska, E., Djemaï, A., Le Paslier, D., Zografos, L., Pescia, G., and Schorderet, D. F. (1997) Kerato-epithelin mutations in four 5q31- linked corneal dystrophies. Nat. Genet. 15, 247-251
2. Dobson, C. M. (2003) Protein folding and misfolding. Nature 426, 884-890
3. Stoppini, M., Andreola, A., Foresti, G., and Bellotti, V. (2004) Neurodegenerative diseases caused by protein aggregation: a phenomenon at the borderline between molecular evolution and ageing. Pharmacol. Res. 50, 419-431
4. Kannabiran, C., and Klintworth, G. K. (2006) TGFBI gene mutations in corneal dystrophies. Hum. Mutat. 27, 615-625
5. Valleix, S., Gillmore, J. D., Bridoux, F., Mangione, P. P., Dogan, A., Nedelec, B., Boimard, M., Touchard, G., Goujon, J. M., Lacombe, C., Lozeron, P., Adams, D., Lacroix, C., Maisonobe, T., Planté-Bordeneuve, V., Vrana, J. A., Theis, J. D., Giorgetti, S., Porcari, R., Ricagno, S., Bolognesi, M., Stoppini, M., Delpech, M., Pepys, M. B., Hawkins, P. N., and Bellotti, V. (2012) Hereditary systemic amyloidosis due to Asp76Asn variant β2-microglobulin. N. Engl. J. Med. 366, 2276-2283
6. Schmitt-Bernard, C. F., Chavanieu, A., Derancourt, J., Arnaud, B., Demaille, J. G., Calas, B., and Argiles, A. (2000) In vitro creation of amyloid fibrils from native and Arg124Cys mutated βIGH3((110-131)) peptides, and its relevance for lattice corneal amyloid dystrophy type I. Biochem. Biophys. Res. Commun. 273, 649-653
7. Korvatska, E., Henry, H., Mashima, Y., Yamada, M., Bachmann, C., Munier, F. L., and Schorderet, D. F. (2000) Amyloid and non-amyloid forms of 5q31-linked corneal dystrophy resulting from kerato-epithelin mutations at Arg-124 are associated with abnormal turnover of the protein. J. Biol. Chem. 275, 11465-11469
8. Schmitt-Bernard, C. F., Chavanieu, A., Herrada, G., Subra, G., Arnaud, B., Demaille, J. G., Calas, B., and Argilés, A. (2002) BIGH3 (TGFBI) Arg124 mutations influence the amyloid conversion of related peptides in vitro. Eur. J. Biochem. 269, 5149-5156
9. Yuan, C., Berscheit, H. L., and Huang, A. J. (2007) Identification of an amyloidogenic region on keratoepithelin via synthetic peptides. FEBS Lett. 581, 241-247
10. Korvatska, E., Munier, F. L., Djemaï, A., Wang, M. X., Frueh, B., Chiou, A. G., Uffer, S., Ballestrazzi, E., Braunstein, R. E., Forster, R. K., Culbertson, W. W., Boman, H., Zografos, L., and Schorderet, D. F. (1998) Mutation hot spots in 5q31-linked corneal dystrophies. Am. J. Hum. Genet. 62, 320-324
11. El Kochairi, I., Letovanec, I., Uffer, S., Munier, F. L., Chaubert, P., and Schorderet, D. F. (2006) Systemic investigation of keratoepithelin deposits in TGFBI/BIGH3-related corneal dystrophy. Mol. Vis. 12, 461-466
12. Harrison, R. S., Sharpe, P. C., Singh, Y., and Fairlie, D. P. (2007) Amyloid peptides and proteins in review. Rev. Physiol. Biochem. Pharmacol. 159, 1-77
13. Abedini, A., and Raleigh, D. P. (2009) A critical assessment of the role of helical intermediates in amyloid formation by natively unfolded proteins and polypeptides. Protein Eng. Des. Sel. 22, 453-459
14. Lai, Z., Colón, W., and Kelly, J. W. (1996) The acid-mediated denaturation pathway of transthyretin yields a conformational intermediate that can self-assemble into amyloid. Biochemistry 35, 6470-6482
15. Khurana, R., Gillespie, J. R., Talapatra, A., Minert, L. J., Ionescu-Zanetti, C., Millett, I., and Fink, A. L. (2001) Partially folded intermediates as critical precursors of light chain amyloid fibrils and amorphous aggregates. Biochemistry 40, 3525-3535
16. Goldschmidt, L., Teng, P. K., Riek, R., and Eisenberg, D. (2010) Identifying the amylome, proteins capable of forming amyloid-like fibrils. Proc. Natl. Acad. Sci. U.S.A. 107, 3487-3492
17. Raimondi, S., Guglielmi, F., Giorgetti, S., Di Gaetano, S., Arciello, A., Monti, D. M., Relini, A., Nichino, D., Doglia, S. M., Natalello, A., Pucci, P., Mangione, P., Obici, L., Merlini, G., Stoppini, M., Robustelli, P., Tartaglia, G. G., Vendruscolo, M., Dobson, C. M., Piccoli, R., and Bellotti, V. (2011) Effects of the known pathogenic mutations on the aggregation pathway of the amyloidogenic peptide of apolipoprotein A-I. J. Mol. Biol. 407, 465-476
18. Yamamoto, S., Hasegawa, K., Yamaguchi, I., Tsutsumi, S., Kardos, J., Goto, Y., Gejyo, F., and Naiki, H. (2004) Low concentrations of sodium dodecyl sulfate induce the extension of β2-microglobulin-related amyloid fibrils at a neutral pH. Biochemistry 43, 11075-11082
19. Yamaguchi, K., Naiki, H., and Goto, Y. (2006) Mechanism by which the amyloid-like fibrils of a β2-microglobulin fragment are induced by fluorine- substituted alcohols. J. Mol. Biol. 363, 279-288
20. Sureshbabu, N., Kirubagaran, R., and Jayakumar, R. (2009) Surfactantinduced conformational transition of amyloid β-peptide. Eur. Biophys. J. 38, 355-367
21. Khan, J. M., Qadeer, A., Chaturvedi, S. K., Ahmad, E., Rehman, S. A., Gourinath, S., and Khan, R. H. (2012) SDS can be utilized as an amyloid inducer: a case study on diverse proteins. PLoS One 7, e29694
22. Otzen, D. E. (2010) Amyloid formation in surfactants and alcohols: membrane mimetics or structural switchers Curr. Protein Pept. Sci. 11, 355-371
23. Otzen, D. (2011) Protein-surfactant interactions: a tale of many states. Biochim. Biophys. Acta 1814, 562-591
24. Hoshino, M., Hagihara, Y., Hamada, D., Kataoka, M., and Goto, Y. (1997) Trifluoroethanol-induced conformational transition of hen egg-white lysozyme studied by small-angle X-ray scattering. FEBS Lett. 416, 72-76
25. Ozawa, D., Kaji, Y., Yagi, H., Sakurai, K., Kawakami, T., Naiki, H., and Goto, Y. (2011) Destruction of amyloid fibrils of keratoepithelin peptides by laser irradiation coupled with amyloid-specific thioflavin T. J. Biol. Chem. 286, 10856-10863
26. Mullen, W., Shepherd, W., and Labovitz, J. (1973) Ophthalmic preservatives and vehicles. Surv. Ophthalmol. 17, 469-483
27. Ohhashi, Y., Kihara, M., Naiki, H., and Goto, Y. (2005) Ultrasonicationinduced amyloid fibril formation of β2-microglobulin. J. Biol. Chem. 280, 32843-32848
28. So, M., Yagi, H., Sakurai, K., Ogi, H., Naiki, H., and Goto, Y. (2011) Ultrasonication- dependent acceleration of amyloid fibril formation. J. Mol. Biol. 412, 568-577
29. Yoshimura, Y., Lin, Y., Yagi, H., Lee, Y. H., Kitayama, H., Sakurai, K., So, M., Ogi, H., Naiki, H., and Goto, Y. (2012) Distinguishing crystal-like amyloid fibrils and glass-like amorphous aggregates from their kinetics of formation. Proc. Natl. Acad. Sci. U.S.A. 109, 14446-14451
30. Yoshimura, Y., So, M., Yagi, H., and Goto, Y. (2013) Ultrasonication: An Efficient Agitation for Accelerating the supersaturation-limited amyloid fibrillation of proteins. Jpn. J. Appl. Phys. 52, 07HA 01:01-08
31. Naiki, H., Higuchi, K., Hosokawa, M., and Takeda, T. (1989) Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin T1. Anal. Biochem. 177, 244-249
32. Biancalana, M., Makabe, K., Koide, A., and Koide, S. (2009) Molecular mechanism of thioflavin-T binding to the surface of β-rich peptide selfassemblies. J. Mol. Biol. 385, 1052-1063
33. Adriaens, E., Dierckens, K., Bauters, T. G., Nelis, H. J., van Goethem, F., Vanparys, P., and Remon, J. P. (2001) The mucosal toxicity of different benzalkonium chloride analogues evaluated with an alternative test using slugs. Pharm. Res. 18, 937-942
34. Bjellqvist, B., Hughes, G. J., Pasquali, C., Paquet, N., Ravier, F., Sanchez, J. C., Frutiger, S., and Hochstrasser, D. (1993) The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis 14, 1023-1031
35. Bjellqvist, B., Basse, B., Olsen, E., and Celis, J. E. (1994) Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions. Electrophoresis 15, 529-539
36. Ohhashi, Y., Hasegawa, K., Naiki, H., and Goto, Y. (2004) Optimum amyloid fibril formation of a peptide fragment suggests the amyloidogenic preference of β2-microglobulin under physiological conditions. J. Biol. Chem. 279, 10814-10821
37. Millucci, L., Paccagnini, E., Ghezzi, L., Bernardini, G., Braconi, D., Laschi, M., Consumi, M., Spreafico, A., Tanganelli, P., Lupetti, P., Magnani, A., and Santucci, A. (2011) Different factors affecting human ANP amyloid aggregation and their implications in congestive heart failure. PLoS One 6, e21870
38. Kaji, Y., Oshika, T., Takazawa, Y., Fukayama, M., and Fujii, N. (2012) Co-localisation of advanced glycation end products and D-β-aspartic acid- containing proteins in gelatinous drop-like corneal dystrophy. Br. J. Ophthalmol. 96, 1127-1131
39. Kaji, Y., Oshika, T., Takazawa, Y., Fukayama, M., and Fujii, N. (2010) Accumulation of D-β-aspartic acid-containing proteins in age-related ocular diseases. Chem. Biodivers. 7, 1364-1370
40. Fernandez-Escamilla, A. M., Rousseau, F., Schymkowitz, J., and Serrano, L. (2004) Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat. Biotechnol. 22, 1302-1306
41. Tartaglia, G. G., Pawar, A. P., Campioni, S., Dobson, C. M., Chiti, F., and Vendruscolo, M. (2008) Prediction of aggregation-prone regions in structured proteins. J. Mol. Biol. 380, 425-436
42. Conchillo-Solé, O., de Groot, N. S., Avilés, F. X., Vendrell, J., Daura, X., and Ventura, S. (2007) AGGRESCAN: a server for the prediction and evaluation of "hot spots" of aggregation in polypeptides. BMC Bioinformatics 8, 65
43. Trovato, A., Chiti, F., Maritan, A., and Seno, F. (2006) Insight into the structure of amyloid fibrils from the analysis of globular proteins. PLoS Comput. Biol. 2, e170
44. Thompson, M. J., Sievers, S. A., Karanicolas, J., Ivanova, M. I., Baker, D., and Eisenberg, D. (2006) The 3D profile method for identifying fibrilforming segments of proteins. Proc. Natl. Acad. Sci. U.S.A. 103, 4074-4078