Mishandling of the therapeutic peptide glucagon generates cytotoxic amyloidogenic fibrils

Pharmaceutical Research

Volumn 21, Issue 7, 2004, Pages 1274-1283

  Onoue, Satomi ^a   Ohshima, Keiichi ^b   Debari, Kazuhiro ^c   Koh, Keitatsu ^c   Shioda, Seiji ^c   Iwasa, Sumiko ^a   Kashimoto, Kazuhisa ^d   Yajima, Takehiko ^a  

^a TOHO UNIVERSITY   (Japan)

^b SHIZUOKA CANCER CENTER   (Japan)

^c SHOWA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d Itoham Foods Inc   (Japan)

Author keywords

aggregation; fibril toxicity; glucagon; salmon calcitonin

Indexed keywords

ACID; AMYLOID; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CALCITONIN; CASPASE 3; CASPASE INHIBITOR; DYE; GLUCAGON; MONOMER; PEPTIDE; SECRETIN;

ACIDITY; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL STRAIN; CELL STRAIN 3T3; CIRCULAR DICHROISM; CONCENTRATION (PARAMETERS); CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; ELECTRON MICROSCOPY; ENZYME ACTIVATION; FIBER; GEL PERMEATION CHROMATOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; RAT; SIGNAL TRANSDUCTION; STAINING; STRUCTURE ANALYSIS; TEMPERATURE; TIME;

AMYLOID; AMYLOIDOSIS; ANIMALS; CALCITONIN; CASPASE 3; CASPASES; CELL SURVIVAL; CHROMATOGRAPHY, GEL; CIRCULAR DICHROISM; GLUCAGON; HEATING; HUMANS; IMMUNE SERA; MICROSCOPY, ELECTRON; PROTEIN CONFORMATION; SECRETIN; TIME FACTORS; TUMOR CELLS, CULTURED;

EID: 3242735868     PISSN: 07248741     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:PHAM.0000033016.36825.2c     Document Type: Article

References (43)

1. M. Rodbell, L. Birnbaumer, S. L. Pohl, and F. Sundby. The reaction of glucagon with its receptor: evidence for discrete regions of activity and binding in the glucagon molecule. Proc. Natl. Acad. Sci. U.S.A. 68:909-913 (1971).
2. G. H. Beaven, W. B. Gratzer, and H. G. Davies. Formation and structure of gels and fibrils from glucagon. Eur. J. Biochem. 11: 37-42 (1969).
3. M. J. Burke and M. A. Rougvie. Cross-β protein structures. I. Insulin fibrils. Biochemistry 11:2435-2439 (1972).
4. D. K. Clodfelter, A. H. Pekar, D. M. Rebhun, K. A. Destrampe, H. A. Havel, S. R. Myers, and M. L. Brader. Effects of non-covalent self-association on the subcutaneous absorption of a therapeutic peptide. Pharm. Res. 15:254-262 (1998).
5. M. Cauchy, S. D'Aoust, B. Dawson, H. Rode, and M. Hefford. Thermal stability: a means to assure tertiary structure in therapeutic proteins. Biologicals 30:175-185 (2002).
6. R. J. Ellis and T. J. Pinheiro. Medicine: danger - misfolding proteins. Nature 416:483-484 (2002).
7. G. G. Glenner. Amyloid deposits and amyloidosis. The beta-fibrilloses (first of two parts). N. Engl. J. Med. 302:1283-1292 (1980).
8. G. G. Glenner. Amyloid deposits and amyloidosis: the beta-fibrilloses (second of two parts). N. Engl. J. Med. 302:1333-1343 (1980).
9. G. Vines. Alzheimer's disease - from cause to cure? Trends Biotechnol. 11:49-55 (1993).
10. G. J. Cooper, A. C. Willis, A. Clark, R. C. Turner, R. B. Sim, and K. B. Reid. Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients. Proc. Natl. Acad. Sci. U.S.A. 84:8628-8632 (1987).
11. S. B. Prusiner. Prions. Proc. Natl. Acad. Sci. U.S.A. 95:13363-13383 (1998).
12. E. Scherzinger, R. Lurz, M. Turmaine, L. Mangiarini, B. Hollenbach, R. Hasenbank, G. P. Bates, S. W. Davies, H. Lehrach, and E. E. Wanker. Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell 90:549-558 (1997).
13. J. D. Sipe. Amyloidosis. Annu. Rev. Biochem. 61:947-975 (1992).
14. W. G. Turnell and J. T. Finch. Binding of the dye congo red to the amyloid protein pig insulin reveals a novel homology amongst amyloid-forming peptide sequences. J. Mol. Biol. 227:1205-1223 (1992).
15. I. V. Kurochkin. Amyloidogenic determinant as a substrate recognition motif of insulin-degrading enzyme. FEBS Lett. 427:153-156 (1998).
16. Y. Liu and D. Schubert. Steroid hormones block amyloid fibril-induced 3-(4,5-dimethylthiazol-2- yl)-2,5-diphenyltetrazolium bromide (MTT) formazan exocytosis: relationship to neurotoxicity. J. Neurochem. 71:2322-2329 (1998).
17. V. Mutt, J. E. Jorpes, and S. Magnusson. Structure of porcine secretin. The amino acid sequence. Eur. J. Biochem. 15:513-519 (1970).
18. R. K. O'Dor, C. O. Parkes, and D. H. Copp. Amino acid composition of salmon calcitonin. Can. J. Biochem. 47:823-825 (1969).
19. R. B. Merrifield. Solid-phase peptide synthesis. Adv. Enzymol. Relat. Areas Mol. Biol. 32:221-296 (1969).
20. S. Onoue, K. Ohshima, K. Endo, T. Yajima, and K. Kashimoto. PACAP protects neuronal PC12 cells from the cytotoxicity of human prion protein fragment 106-126. FEBS Lett. 522:65-70 (2002).
21. S. Onoue, K. Endo, K. Ohshima, T. Yajima, and K. Kashimoto. The neuropeptide PACAP attenuates beta-amyloid (1-42)-induced toxicity in PC12 cells. Peptides 23:1471-1478 (2002).
22. W. E. Klunk, J. W. Pettegrew, and D. J. Abraham. Two simple methods for quantifying low-affinity dye-substrate binding. J. Histochem. Cytochem. 37:1293-1297 (1989).
23. H. LeVine iii. Thioflavine T interaction with synthetic Alzheimer's disease beta- amyloid peptides: detection of amyloid aggregation in solution. Protein Sci. 2:404-410 (1993).
24. S. Onoue, Y. Waki, Y. Nagano, S. Satoh, and K. Kashimoto. The neuromodulatory effects of VIP/PACAP on PC-12 cells are associated with their N-terminal structures. Peptides 22:867-872 (2001).
25. I. Isobe, M. Michikawa, and K. Yanagisawa. Enhancement of MTT, a tetrazolium salt, exocytosis by amyloid beta- protein and chloroquine in cultured rat astrocytes. Neurosci. Lett. 266:129-132 (1999).
26. N. Greenfield and G. D. Fasman. Computed circular dichroism spectra for the evaluation of protein conformation. Biochemistry 8:4108-4116 (1969).
27. J. Cort, Z. Liu, G. Lee, S. M. Harris, K. S. Prickett, L. S. Gaeta, and N. H. Andersen. Beta-structure in human amylin and two designer beta-peptides: CD and NMR spectroscopic comparisons suggest soluble beta-oligomers and the absence of significant populations of beta-strand dimers. Biochem. Biophys. Res. Commun. 204:1088-1095 (1994).
28. G. Forloni, N. Angeretti, R. Chiesa, E. Monzani, M. Salmona, O. Bugiani, and F. Tagliavini. Neurotoxicity of a prion protein fragment. Nature 362:543-546 (1993).
29. B. Solomon, R. Koppel, E. Hanan, and T. Katzav. Monoclonal antibodies inhibit in vitro fibrillar aggregation of the Alzheimer beta-amyloid peptide. Proc. Natl. Acad. Sci. U.S.A. 93:452-455 (1996).
30. W. E. Klunk, J. W. Pettegrew, and D. J. Abraham. Quantitative evaluation of congo red binding to amyloid-like proteins with a beta-pleated sheet conformation. J. Histochem. Cytochem. 37:1273-1281 (1989).
31. D. Frenkel, O. Katz, and B. Solomon. Immunization against Alzheimer's beta -amyloid plaques via EFRH phage administration. Proc. Natl. Acad. Sci. U.S.A. 97:11455-11459 (2000).
32. E. Hanan, O. Goren, M. Eshkenazy, and B. Solomon. Immunomodulation of the human prion peptide 106-126 aggregation. Biochem. Biophys. Res. Commun. 280:115-120 (2001).
33. K. Sasaki, S. Dockerill, D. A. Adamiak, I. J. Tickle, and T. Blundell. X-ray analysis of glucagon and its relationship to receptor binding. Nature 257:751-757 (1975).
34. J. Liu, M. Bhalgat, C. Zhang, Z. Diwu, B. Hoyland, and D. H. Klaubert. Fluorescent molecular probes V: a sensitive caspase-3 substrate for fluorometric assays. Bioorg. Med. Chem. Lett. 9: 3231-3236 (1999).
35. R. U. Janicke, M. L. Sprengart, M. R. Wati, and A. G. Porter. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J. Biol. Chem. 273:9357-9360 (1998).
36. D. W. Nicholson, A. Ambereen, N. A. Thornberry. J. P. Vaillancourt, C. K. Ding, M. Gallant, Y. Gareau, P. R. Griffin, M. Labelle, Y. A. Lazebnik, N. A. Munday, S. M. Raju, M. E. Smulson, T. T. Yamin, V. L. Yu, and D. K. Miller. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376:37-43 (1995).
37. E. A. Atkinson, M. Barry, A. J. Darmon, I. Shostak, P. C. Turner, R. W. Moyer, and R. C. Bleackley. Cytotoxic T lymphocyte-assisted suicide. Caspase 3 activation is primarily the result of the direct action of granzyme B. J. Biol. Chem. 273:21261-21266 (1998).
38. B. L. Chen, T. Arakawa, C. F. Morris, W. C. Kenney, C. M. Wells, and C. G. Pitt. Aggregation pathway of recombinant human keratinocyte growth factor and its stabilization. Pharm. Res. 11:1581-1587 (1994).
39. N. Demeester, C. Mertens, H. Caster, M. Goethals, J. Vandekerckhove, M. Rosseneu, and C. Labeur. Comparison of the aggregation properties, secondary structure and apoptotic effects of wild-type, Flemish and Dutch N-terminally truncated amyloid beta peptides. Eur. J. Neurosci. 13:2015-2024 (2001).
40. K. M. Pan, M. Baldwin, J. Kguyen, M. Gasset, A. Serban, D. Groth, I. Mehlhorn, Z. Huang, R. J. Fletterick, F. E. Cohen, and S. B. Prusiner. Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc. Natl. Acad. Sci. USA 90:10962-10966 (1993).
41. M. Kamihira, A. Naito, S. Tuzi, A. Y. Nosaka, and H. Saito. Conformational transitions and fibrillation mechanism of human calcitonin as studied by high-resolution solid-state 13C NMR. Protein Sci. 9:867-877 (2000).
42. H. J. Chae, S. W. Chae, N. H. An, J. H. Kim, C. W. Kim, S. K. Yoo, H. H. Kim, Z. H. Lee, and H. R. Kim. Cyclic-AMP inhibits nitric oxide-induced apoptosis in human osteoblast: the regulation of caspase-3, -6, -9 and the release of cytochrome c in nitric oxide-induced apoptosis by cAMP. Biol. Pharm. Bull. 24:453-460 (2001).
43. J. Li, S. Yang, and T. R. Billiar. Cyclic nucleotides suppress tumor necrosis factor alpha-mediated apoptosis by inhibiting caspase activation and cytochrome c release in primary hepatocytes via a mechanism independent of Akt activation. J. Biol. Chem. 275:13026-13034 (2000).