The influence of phospholipid membranes on bovine calcitonin secondary structure and amyloid formation

Protein Science

Volumn 14, Issue 6, 2005, Pages 1419-1428

  Wang, Steven S S ^a   Good, Theresa A ^b   Rymer, Dawn L ^c  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b University of Marylandw Baltimore County   (United States)

^c Texas AandM University   (United States)

Author keywords

Amyloid; Calcitonin; Phospholipid membranes; Secondary structure

Indexed keywords

AMYLOID; CALCITONIN; PHOSPHOLIPID;

AMYLOIDOSIS; ANALYTIC METHOD; AQUEOUS SOLUTION; ARTICLE; BETA SHEET; BINDING AFFINITY; CORRELATION ANALYSIS; ELECTRICITY; ENTHALPY; ENTROPY; INCUBATION TIME; IONIC STRENGTH; PHOSPHOLIPID MEMBRANE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; TEMPERATURE DEPENDENCE;

AMYLOID; ANIMALS; CALCITONIN; CATTLE; MEMBRANES, ARTIFICIAL; PHOSPHOLIPIDS; PROTEIN STRUCTURE, SECONDARY;

BOVINAE;

EID: 22444436329     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.041240105     Document Type: Article

References (74)

1. Arvinte, T. and Drake, A.F. 1993. Comparative study of human and salmon calcitonin secondary structure in solutions with low dielectric constants. J. Biol. Chem. 268: 6408-6414.
2. Arvinte, T., Cudd, A., and Drake, A.F. 1993. The structure and mechanism of formation of human calcitonin fibrils. J. Biol. Chem. 268: 6415-6422.
3. Atwood, C.S., Moir, R.D., Huang, X.D., Scarpa, R.C., Bacarra, N.M.E., Romano, D.M., Hartshorn, M.K., Tanzi, R.E., and Bush, A.I. 1998. Dramatic aggregation of Alzheimer A β by Cu(II) is induced by conditions representing physiological acidosis. J. Biol. Chem. 273: 12817-12826.
4. Avdulov, N.A., Chochina, S.V., Igbavboa, U., Warden, C.S., Vassiliev, A.V., and Wood, W.G. 1997. Lipid binding to amyloid β-peptide aggregates: Preferential binding of cholesterol as compared with phosphatidylcholine and fatty acids. J. Neurochem. 69: 1746-1752.
5. Bauer, H.H., Muller, M., Goette, J., Merkle, H.P., and Fringeli, U.P. 1994. Interfacial adsorption and aggregation associated changes in secondary structure of human calcitonin monitored by ATR-FTIR spectroscopy. Biochemistry 33: 12276-12282.
6. Berger, G., Berger, N., Guillaud, M.H., Trouillas, J., and Vauzelle, J.L. 1988. Calcitonin-like immunoreactivity of amyloid fibrils in medullary thyroid carcinomas. An immunoelectron microscope study. Virchows Arch. A Pathol. Anat. Histopathol. 412: 543-551.
7. Bodles, A.M., El-Agnaf, O.M., Greer, B., Guthrie, D.J., and Irvine, G.B. 2004. Inhibition of fibril formation and toxicity of a fragment of α-synuclein by an N-methylated peptide analogue. Neurosci. Lett. 359: 89-93.
8. Bradshaw, J.P. 1997. Phosphatydylglycerol promotes bilayer insertion of salmon calcitonin. Biophys. J. 72: 2180-2186.
9. Bretscher, M.S. 1973. Membrane structure: Some general principles. Science 181: 622-629.
10. Butler, M. and Khan, S. 1986. Immunoreactive calcitonin in amyloid fibrils of medullary carcinoma of the thyroid gland. An immunogold staining technique. Arch. Pathol. Lab. Med. 110: 647-649.
11. Byard, R.W., Thorner, P.S., Chan, H.S., Griffiths, A.M., and Cutz, E. 1990. Pathological features of multiple endocrine neoplasia type IIb in childhood. Pediatr. Pathol. 10: 581-592.
12. Chang, C.T., Wu, C.S., and Yang, J.T. 1978. Circular dichroic analysis of protein conformation: Inclusion of the β-turns. Anal. Biochem. 91: 13-31.
13. Chi, E.Y., Krishnan, S., Randolph, T.W., and Carpenter, J.F. 2003. Physical stability of proteins in aqueous solution: Mechanism and driving forces in nonnative protein aggregation. Pharm. Res. 20: 1325-1336.
14. Choo-Smith, L.P. and Surewicz, W.K. 1997. The interaction between Alzheimer amyloid β(1-40) peptide and ganglioside GM1-containing membranes. FEBS Lett. 402: 95-98.
15. Choo-Smith, L.P., Garzon-Rodriguez, W., Glabe, C.G., and Surewicz, W.K. 1997. Acceleration of amyloid fibril formation by specific binding of Aβ- (1-40) peptide to ganglioside-containing membrane vesicles. J. Biol. Chem. 272: 22987-22990.
16. Dammrich, J., Ormanns, W., and Schaffer, R. 1984. Electron microscopic demonstration of calcitonin in human medullary carcinoma of thyroid by the immuno gold staining method. Histochemistry 81: 369-372.
17. De Felice, F.G., Vieira, M.N., Saraiva, L.M., Figueroa-Villar, J.D., Garcia-Abreu, J., Liu, R., Chang, L., Klein, W.L., and Ferreira, S.T. 2004. Targeting the neurotoxic species in Alzheimer's disease: Inhibitors of Aβ oligomerization. FASEB J. 18: 1366-1372.
18. DeLellis, R.A., Nunnemacher, G., Bitman, W.R., Gagel, R.F., Tashjian Jr., A.H., Blount, M., andWolfe, H.J. 1979. C-cell hyperplasia and medullary thyroid carcinoma in the rat. An immunohistochemical and ultrastructural analysis. Lab. Invest. 40: 140-154.
19. Epand, R.M., Epand, R.F., Orlowski, R.C., Schlueter, R.J., Boni, L.T., and Hui, S.W. 1983. Amphipathic helix and its relationship to the interaction of calcitonin with phospholipids. Biochemistry 22: 5074-5084.
20. Epand, R.M., Epand, R.F., Orlowski, R.C., Seyler, J.K., and Colescott, R.L. 1986a. Conformational flexibility and biological activity of salmon calcitonin. Biochemistry 25: 1964-1968.
21. Epand, R.M., Seyler, J.K., and Orlowski, R.C. 1986b. The hydrophobic moment of the amphipathic helix of salmon calcitonin and biological potency. Eur. J. Biochem. 159: 125-127.
22. Fischer, J.A., Tobler, P.H.,Kaufmann, M., Born, W.,Henke,H., Cooper, P.E., Sagar, S.M., andMartin, J.B. 1981. Calcitonin: Regional distribution of the hormone and its binding sites in the human brain and pituitary. Proc. Natl. Acad. Sci. 78: 7801-7805.
23. Fletcher, J.R. 1970. Medullary (solid) carcinoma of the thyroid gland. A review of 249 cases. Arch. Surg. 100: 257-262.
24. Gilead, S. and Gazit, E. 2004. Inhibition of amyloid fibril formation by peptide analogues modified with α-aminoisobutyric acid. Angew Chem. Int. Ed. Engl. 43: 4041-4044.
25. Hazard, J.B. 1977. The C cells (parafollicular cells) of the thyroid gland and medullary thyroid carcinoma. A review. Am. J. Pathol. 88: 213-250.
26. Hill Jr., C.S., Ibanez, M.L., Samaan, N.A., Ahearn, M.J., and Clark, R.L. 1973. Medullary (solid) carcinoma of the thyroid gland: An analysis of the M.D. Anderson Hospital experience with patients with the tumor, its special features, and its histogenesis. Medicine (Baltimore) 52: 141-171.
27. Inzerillo, A.M., Zaidi, M., and Huang, C.L.H. 2004. Calcitonin: Physiological actions and clinical applications. J. Pediatr. Endocrinol. Metab. 17: 931-940.
28. Kakio, A., Nishimoto, S., Yanagisawa, K., Kozutsumi, Y., and Matsuzaki, K. 2002. Interactions of amyloid β-protein with various gangliosides in raft-like membranes: Importance of GM1 ganglioside-bound form as an endogenous seed for Alzheimer amyloid. Biochemistry 41: 7385-7390.
29. Kakio, A., Nishimoto, S., Kozutsumi, Y., and Matsuzaki, K. 2003. Formation of a membrane-active form of amyloid β-protein in raft-like model membranes. Biochem. Biophys. Res. Commun. 303: 514-518.
30. Kanaori, K. and Nosaka, A.Y. 1995. Study of human calcitonin fibrillation by proton nuclear magnetic resonance spectroscopy. Biochemistry 34: 12138-12143.
31. Kelly, J.W. 1996. Alternative conformations of amyloidogenic proteins govern their behavior. Curr. Opin. Struct. Biol. 6: 11-17.
32. Kirkitadze, M.D., Condron, M.M., and Teplow, D.B. 2001. Identification and characterization of key kinetic intermediates in amyloid β-protein fibrillogenesis. J. Mol. Biol. 312: 1103-1119.
33. Klunk, W.E., Pettegrew, J.W., and Abraham, D.J. 1989a. Quantitative evaluation of congo red binding to amyloid-like proteins with a β-pleated sheet conformation. J. Histochem. Cytochem. 37: 1273-1281.
34. Klunk, W.E., Pettegrew, J.W., and Abraham, D.J. 1989b. Two simple methods for quantifying low-affinity dye-substrate binding. J. Histochem. Cytochem. 37: 1293-1297.
35. Koppaka, V. and Axelsen, P.H. 2000. Accelerated accumulation of amyloid β proteins on oxidatively damaged lipid membranes. Biochemistry 39: 10011-10016.
36. Kurganov, B., Doh, M., and Arispe, N. 2004. Aggregation of liposomes induced by the toxic peptides Alzheimer's Aβs, human amylin and prion (106-126): Facilitation by membrane-bound GM1 ganglioside. Peptides 25: 217-232.
37. Lansbury Jr., P.T. 1999. Evolution of amyloid: What normal protein folding may tell us about fibrillogenesis and disease. Proc. Natl. Acad. Sci. 96: 3342-3344.
38. Liu, Y. and Schubert, D. 1997. Cytotoxic amyloid peptides inhibit cellular 3-(4, 5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction by enhancing MTT formazan exocytosis. J. Neurochem. 69: 2285-2293.
39. Ljungberg, O. 1966. Medullary carcinoma of the human thyroid gland. Autoradiographic localization of radioiodine. Acta Pathol. Microbiol. Scand. 68: 476-480.
40. Mandal, P.K. and Pettegrew, J.W. 2004. Alzheimer's disease: NMR studies of asialo (GM1) and trisialo (GT1b) ganglioside interactions with Aβ(1-40) peptide in a membrane mimic environment. Neurochem. Res. 29: 447-453.
41. Mason, R.P., Estermyer, J.D., Kelly, J.F., and Mason, P.E. 1996. Alzheimer's disease amyloid beta peptide 25-35 is localized in the membrane hydrocarbon core: X-ray diffraction analysis. Biochem. Biophys. Res. Commun. 222: 78-82.
42. Matsuzaki, K. and Horikiri, C. 1999. Interactions of amyloid β-peptide (1-40) with ganglioside-containing membranes. Biochemistry 38: 4137-4142.
43. McLaurin, J. and Chakrabartty, A. 1996.Membrane disruption by Alzheimer β-amyloid peptides mediated through specific binding to either phospholipids or gangliosides. Implications for neurotoxicity. J. Biol. Chem. 271: 26482-26489.
44. 1H NMR assignment and secondary structure determination of salmon calcitonin in solution. Biochemistry 28: 7996-8002.
45. Motta, A., Andreotti, G., Amodeo, P., Strazzullo, G., and Castiglione Morelli, M.A. 1998. Solution structure of human calcitonin in membrane-mimetic environment: The role of the amphipathic helix. Proteins 32: 314-323.
46. Murphy, R.M. 2002. Peptide aggregation in neurodegenerative disease. Annu. Rev. Biomed. Eng. 4: 155-174.
47. Nilsson, M.R. 2004. Techniques to study amyloid fibril formation in vitro. Methods 34: 151-160.
48. Ohnishi, S. and Takano, K. 2004. Amyloid fibrils from the viewpoint of protein folding. Cell. Mol. Life Sci. 61: 511-524.
49. Olofsson, A., Ostman, J., and Lundgren, E. 2002. Amyloid: Morphology and toxicity. Clin. Chem. Lab. Med. 40: 1266-1270.
50. Ono, K., Hasegawa, K., Yamada, M., and Naiki, H. 2002. Nicotine breaks down preformed Alzheimer's β-amyloid fibrils in vitro. Biol. Psychiatry 52: 880-886.
51. Perez, M., Sadqi, M., Munoz, V., and Avila, J. 2003. Inhibition by Aplidine of the aggregation of the prion peptide PrP 106-126 into β-sheet fibrils. Biochim. Biophys. Acta 1639: 133-139.
52. Ponder, B.A. 1984. Screening for familial medullary thyroid carcinoma: A review. J. R. Soc. Med. 77: 585-594.
53. Porat, Y., Mazor, Y., Efrat, S., and Gazit, E. 2004. Inhibition of islet amyloid polypeptide fibril formation: A potential role for heteroaromatic interactions. Biochemistry 43: 14454-14462.
54. Rijkers, D.T., Hoppener, J.W., Posthuma, G., Lips, C.J., and Liskamp, R.M. 2002. Inhibition of amyloid fibril formation of human amylin by N-alkylated amino acid and α-hydroxy acid residue containing peptides. Chemistry 8: 4285-4291.
55. Rizzo, A.J. and Goltzman, D. 1981. Calcitonin receptors in the central nervous system of the rat. Endocrinology 108: 1672-1677.
56. Rymer, D.L. and Good, T.A. 2001. The role of G protein activation in the toxicity of amyloidogenic Aβ-(1-40), Aβ-(25-35), and bovine calcitonin. J. Biol. Chem. 276: 2523-2530.
57. Schubert, D., Behl, C., Lesley, R., Brack, A., Dargusch, R., Sagara, Y., and Kimura, H. 1995. Amyloid peptides are toxic via a common oxidative mechanism. Proc. Natl. Acad. Sci. 92: 1989-1993.
58. Seilheimer, B., Bohrmann, B., Bondolfi, L., Muller, F., Stuber, D., and Dobeli, H. 1997. The toxicity of the Alzheimer's β-amyloid peptide correlates with a distinct fiber morphology. J. Struct. Biol. 119: 59-71.
59. Siligardi, G., Samori, B., Melandri, S., Visconti, M., and Drake, A.F. 1994. Correlations between biological activities and conformational properties for human, salmon, eel, porcine calcitonins and Elcatonin elucidated by CD spectroscopy. Eur. J. Biochem. 221: 1117-1125.
60. Silver, M.M., Hearn, S.A., Lines, L.D., and Troster, M. 1988. Calcitonin and chromogranin A localization in medullary carcinoma of the thyroid by immunoelectron microscopy. J. Histochem. Cytochem. 36: 1031-1036.
61. Sletten, K., Westermark, P., and Natvig, J.B. 1976. Characterization of amyloid fibril proteins from medullary carcinoma of the thyroid. J. Exp. Med. 143: 993-998.
62. Smith, P.K., Krohn, R.I., Hermanson, G.T., Mallia, A.K., Gartner, F.H., Provenzano, M.D., Fujimoto, E.K., Goeke, N.M., Olson, B.J., and Klenk, D.C. 1985. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150: 76-85.
63. Surewicz, W.K., Epand, R.M., Orlowski, R.C., and Mantsch, H.H. 1987. Structural properties of acidic phospholipids in complexes with calcitonin: A Fourier transform infrared spectroscopic investigation. Biochim. Biophys. Acta 899: 307-310.
64. Tashima, Y., Oe, R., Lee, S., Sugihara, G., Chambers, E.J., Takahashi, M., and Yamada, T. 2004. The effect of cholesterol and monosialoganglioside (GM1) on the release and aggregation of amyloid β-peptide from liposomes prepared from brain membrane-like lipids. J. Biol. Chem. 279: 17587-17595.
65. Terzi, E., Holzemann, G., and Seelig, J. 1997. Interaction of Alzheimer β-amyloid peptide(1-40) with lipid membranes. Biochemistry 36: 14845-14852.
66. Thompson, L.K. 2003. Unraveling the secrets of Alzheimer's β-amyloid fibrils. Proc. Natl. Acad. Sci. 100: 383-385.
67. Uyama, N., Geerts, A., and Reynaert, H. 2004. Neural connections between the hypothalamus and the liver. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A: 808-820.
68. Viani, P., Cervato, G., Gatti, P., and Cestaro, B. 1992. Calcitonin-induced changes in the organization of sulfatide-containing membranes. Biochim. Biophys. Acta 1106: 77-84.
69. Walsh, D.M., Lomakin, A., Benedek, G.B., Condron, M.M., and Teplow, D.B. 1997. Amyloid β-protein fibrillogenesis. Detection of a protofibrillar intermediate. J. Biol. Chem. 272: 22364-22372.
70. Wang, S.S., Rymer, D.L., and Good, T.A. 2001. Reduction in cholesterol and sialic acid content protects cells from the toxic effects of beta-amyloid peptides. J. Biol. Chem. 276: 42027-42034.
71. Ward, R.V., Jennings, K.H., Jepras, R., Neville, W., Owen, D.E., Hawkins, J., Christie, G., Davis, J.B., George, A., Karran, E.H., et al. 2000. Fractionation and characterization of oligomeric, protofibrillar and fibrillar forms of β-amyloid peptide. Biochem. J. 348 (Pt. 1): 137-144.
72. Wetzel, R. 1996. For protein misassembly, it's the "I" decade. Cell 86: 699-702.
73. Williams, E.D., Brown, C.L., and Doniach, I. 1966. Pathological and clinical findings in a series of 67 cases of medullary carcinoma of the thyroid. J. Clin. Pathol. 19: 103-113.
74. Yanagisawa, K. and Matsuzaki, K. 2002. Cholesterol-dependent aggregation of amyloid β-protein. Ann. N. Y. Acad. Sci. 977: 384-386.