Heterogeneous amyloid-formed ion channels as a common cytotoxic mechanism: Implications for therapeutic strategies against amyloidosis

Cell Biochemistry and Biophysics

Volumn 36, Issue 2-3, 2002, Pages 191-207

  Kourie, Joseph I ^a   Culverson, Amie L ^a   Farrelly, Peter V ^a   Henry, Christine L ^a   Laohachai, Karina N ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Amyloid; Amyloid protein; Cytotoxicity; Ion channel; Prion

Indexed keywords

ANIMALIA;

AMYLIN; AMYLOID; AMYLOID BETA PROTEIN; ATRIAL NATRIURETIC FACTOR; ION CHANNEL; NATRIURETIC PEPTIDE TYPE C;

AMYLOIDOSIS; ANIMAL; CHEMISTRY; DEGENERATIVE DISEASE; HUMAN; LIPID BILAYER; METABOLISM; PHYSIOLOGY; PRION; REVIEW; SIGNAL TRANSDUCTION;

AMYLOID; AMYLOID BETA-PROTEIN; AMYLOIDOSIS; ANIMALS; ATRIAL NATRIURETIC FACTOR; HUMANS; ION CHANNELS; LIPID BILAYERS; NATRIURETIC PEPTIDE, C-TYPE; NEURODEGENERATIVE DISEASES; PRIONS; SIGNAL TRANSDUCTION;

EID: 0036369164     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1385/CBB:36:2-3:191     Document Type: Review

References (73)

1. Kourie, J. I., Henry, C. L., and Farrelly, P. V. (2001) Diversity of amyloid β protein fragment [1-40]-formed channels. Cell. Mol. Neurobiol. 21, 255-284.
2. Arispe, N., Pollard, H. B., and Rojas, E. (1993) Giant multilevel cation channels formed by alzheimer disease amyloid β-protein. Proc. Natl. Acad. Sci. USA 90, 10,573-10,577.
3. Arispe, N., Rojas, E., and Pollard, H. B. (1993) Alzheimer disease amyloid β protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum. Proc. Natl. Acad. Sci. USA 90, 567-571.
4. 2+-channel hypothesis for neuronal death in Alzheimer disease. Mol. Cell. Biochem. 140, 119-125.
5. 2+ interaction with Alzheimer amyloid β protein calcium channels. Proc. Natl. Acad. Sci. USA 93, 1710-1715.
6. Durell, S. R., Guy, H. R., Arispe, N., Rojas, E., and Pollard, H. B. (1994) Theoretical models of the ion channel structure of amyloid beta-protein. Biophys. J. 67, 137-145.
7. Pollard, H. B., Arispe, N., and Rojas, E. (1995) Ion channel hypothesis for Alzheimer amyloid peptide neurotoxicity. Cell. Mol. Neurobiol. 15, 513-526.
8. 2+-sensitive, cation-selective channels across excised membrane patches from hypothalamic neurons. Biophys. J. 73, 67-75.
9. Kawahara, M., Kuroda, Y., Arispe, N., and Rojas, E. (2000) Alzheimer's disease β-amyloid, human islet amylin, and prion protein fragment evoke intracellular free calcium elevations by a common mechanism in hypothalamic GnRH neuronal cell line. J. Biol. Chem. 275, 14,077-14,063.
10. Mirzabekov, T. A., Lin, M. C., Yuan, W. L., Marshall, P. J., Carman, M., Tomaselli, K., et al. (1994) Channel formation in planar lipid bilayers by a neurotoxic fragment of the beta-amyloid peptide. Biochem. Biophys. Res. Commun. 202, 1142-1148.
11. Hirakura, Y., Lin, M. C., and Kagan, B. L. (1999) Alzheimer amyloid Aβ1-42 channels: effects of solvent, pH, and Congo Red. J. Neurosci. Res. 57, 458-466.
12. Hirakura, Y., Yiu, W. W., Yamamoto, A., and Kagan, B. L. (2000) Amyloid peptide channels: blockade by zinc and inhibition by congo red. Amyloid 7, 194-199.
13. Kourie, J. I. (2001). Mechanisms of amyloid-induced modification in the electrical properties of membranes. Cell. Mol. Neurobiol. 21, 173-213.
14. Catterall, W. (1992) Cellular and molecular biology of voltage-gated sodium channels. Physiol. Rev. 72, S15-S48.
15. Kourie, J. I. (2001) Mechanisms of prion-induced modification in membrane transport systems. Chem. Biol. Interact. 138, 1-26.
16. Bush, A. I., Pettingell, W. H., Jr, Paradis, M. D., and Tanzi, R. E. (1994). Modulation of A beta adhesiveness and secretase site cleavage by zinc. J. Biol. Chem. 269, 12,152-12,158.
17. Kourie, J. I., and Culverson, A. (2000) Prion peptide fragment PrP[106-126] forms distinct cation channel types. J. Neurosci. Res. 62, 120-133.
18. Lin, M-C., Mirzabekov, T., and Kagan, B. L. (1997) Channel formation by a neurotoxic prion protein fragment. J. Biol. Chem. 272, 44-47.
19. Manunta, M., Kunz, B., Sandmeier, E., Christen, P., and Schindler, H. (2000) Reported channel formation by prion protein fragment 106-126 in planar lipid bilayer cannot be reproduced. FEBS Lett. 474, 252-256.
20. Kourie, J. I. Farrelly, P. V., and Henry, C. L. (2001) Channel activity of deamidated isoforms of prion protein fragment 106-126 in planar lipid bilayers. J. Neurosci. Res. 66, 214-220.
21. Kunz, E., Sandmeier, E., and Christen, P. (1999) Neurotoxicity of prion peptide 106-126 not confirmed. FEBS Lett. 458, 65-68.
22. Chapron, Y., Peyrin, J-M., Crouzy, S., Jaegly, A., and Dormont, D. (2000) Theoretical analysis of the implication of PrP in neuronal death during transmissible subacute spongiform encephalopathies: hypothesis of a PrP oligomeric channel. J. Theor. Biol. 204, 103-111.
23. + channel. Am. J. Physiol. 277,C43-C50.
24. Jobling, M. F., Huang, X., Stewart, L. R., Barnham, K. J., Curtain, C., Volitakis, I., et al. (2001) Copper and zinc binding modulates the aggregation and neurotoxic properties of the prion peptide PrP106-126. Biochemistry 40, 8073-8084.
25. Sandmeier, E., Kunz, E., Hunziker, P., Sack, R., and Christen, P. (1999) Spontaneous deamidation and isomerization of Asn108 in prion peptide 106-126 and in full-length prion protein. Biochem. Biophys. Res. Commun. 261, 578-583.
26. Rauk, A., and Armstrong, D. A. (2000) Influence of β-sheet structure on the susceptibility of proteins to backbone oxidative damage: preference of αC-central radical formation at glycine residues of antiparallel β-sheets. J. Am. Chem. Soc. 122, 4185-4192.
27. Brown, D. R., Wong, B. S., Hafiz, F., Clive, C., Haswell, S. J., and Jones, I. M. (1999) Normal prion protein has an activity like that of superoxide dismutase. Biochem. J. 344, 1-5.
28. Brown, D. R., Clive, C., and Haswell, S. J. (2001) Antioxidant activity related to copper binding of native prion protein. J. Neurochem. 76, 69-76.
29. Florio, T., Grimaldi, M., Scorziello, A., Salmona, M., Bugiani, O., Tagliavini, F., et al. (1996) Intracellular calcium rise through L-type calcium channels, as molecular mechanism for prion protein fragment 106-126-induced astroglial proliferation. Biochem. Biophys. Res. Commun. 228, 397-405.
30. Barrow, P. A., Holmgren, C. D., Tapper, A. J., and Jefferys, J. G. (1999) Intrinsic physiological and morphological properties of principal cells of the hippocampus and neocortex in hamsters infected with scrapie. Neurobiol. Dis. 6, 406-423.
31. Kojima, M., Minamino, N., Kangawa, K., and Matsuo, H. (1990) Cloning and sequence analysis of a cDNA encoding precursor for rat C-type natriuretic peptide (CNP). FEBS Lett. 276, 209-213.
32. Sudoh, T., Minamino, N., Kenji, K., and Matsuo, H. (1990) C-Type natriuretic peptide (CNP): a new member of natriuretic peptide family identified in porcine brain. Biochem. Biophys. Res. Commun. 168, 863-870.
33. Komatsu, Y., Nakao, K., Suga, S., Ogawa, Y., Mukoyama, M., Arai, H., et al. (1991) C-Type natriuretic peptide (CNP) in rats and humans. Endocrinology 129, 1104-1106.
34. Mukoyama, M., Nakao, K., Hosoda, K., Suga, S., Saito, Y., Ogawa, Y., et al. (1991) Brain natriuretic peptide as a novel cardiac hormone in humans. Evidence for an exquisite dual natriuretic peptide system, atrial natriuretic peptide and brain natriuretic peptide. J. Clin. Invest. 87, 1402-1412.
35. Suga, S., Itoh, H., Komatsu, Y., Ogawa, Y., Hama, N., Yoshimasa, T., et al. (1993) Cytokine-induced C-type natriuretic peptide (CNP) secretion from vascular endothelial cells: evidence for CNP as a novel autocrine/paracrine regulator from endothelial cells. Endocrinology 133, 3038-3041.
36. Suga, S., Nakao, Hosoda, K., Mukoyama, M., Ogawa, Y. Shirakami, G., et al. (1992) Receptor selectivity of natriuretic peptide family, atrial natriuretic peptide, brain natriuretic peptide, and C-type natriuretic peptide. Endocrinology 130, 229-239.
37. de Plater, G. M., Martin, R. L., and Milburn, P. J. (1995) A pharmacological and biochemical investigation of the venom from the platypus (Ornithorhynchus anatinus). Toxicon 33, 157-169.
38. de Plater, G. M., Martin, R. L., and Milburn, P. J. (1998a) The natriuretic peptide (ovCNP) from platypus (Ornithorhynchus anatinus) venom relaxes the isolated rat uterus and promotes oedema and mast cell histamine release. Toxicon 36, 847-857.
39. Suga, S., Nakao, K., Itoh, H., Komatsu, Y., Ogawa, Y., Hama, N., et al. (1992) Endothelial production of C-type natriuretic peptide and its marked augmentation by transforming growth factor-beta. Possible existence of "vascular natriuretic peptide system." J. Clin. Invest. 90, 1145-1149.
40. Murayama, N., Hayashi, M., Ohi, H., Ferreira, L. A. F., Hermann, V., Saito, H., et al. (1997) Cloning and sequence analysis of a Bothrops jararaca cDNA encoding a precursor of seven bradykinin-potentiating peptides and a C-type natriuretic peptide. Proc. Nat. Acad. Sci. USA 94, 1189-1193.
41. Kourie, J. I. (1999) Synthetic mammalian C-type natriuretic peptide forms large cation channels. FEBS Lett. 445, 57-62.
42. Kourie, J. I. (1999) Characterisation of a C-type natriuretic peptide (CNP-39)-formed cation-selective channel from platypus (Ornithrhynchus anatinus) venom. J. Physiol. 518, 359-369.
43. Stingo, A. J., Clavell, A. L., Arthus, L., and Burnett, J. C., Jr. (1992) Cardiovascular and renal actions of C-type natriuretic peptide. Am. J. Physiol. 262, H308-H312.
44. Wei, C. M., Hu, S., Miller, V. M., and Burnett, J. C. J. (1994) Vascular actions of C-type natriuretic peptide in isolated porcine coronary arteries and coronary vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 205, 765-771.
45. White, R. E., Lee, A. B., Shcherbatko, A. D., Lincoln, T. M., Schonbrunn, A., and Armstrong, D. L. (1993) Potassium channel stimulation by natriuretic peptides through cGMP-dependent dephosphorylation. Nature 361, 263-266.
46. Kelley, T. J., Cotton, C. U., and Drumm, M. L. (1997) In vivo activation of CFTR-dependent chloride transport in murine airway epithelium by CNP. Am. J. Physiol. 273, L1065-L1072.
47. Kelley, T. J., Cotton, C. U., and Drumm, M. L. (1998) Regulation of amiloride-sensitive sodium absorption in murine airway epithelium by C-type natriuretic peptide. Am. J. Physiol. 273, L990-L996.
48. Solomon, R., Protter, A., McEnroe, G., Porter, J. G., and Silva, P. (1992) C-Type natriuretic peptides stimulate chloride secretion in the rectal gland of Squalus acanthias. Am. J. Physiol. 262, R707-R771.
49. Kurochkin, I. V. (1998) Amyloidogenic determinant as a substrate recognition motif of insulin-degrading enzyme. FEBS Lett. 427, 153-156.
50. Takemura, G., Takatsu, Y., Doyama, K., Itoh, H., Saito, Y., Koshiji, M., et al. (1998) Expression of atrial and brain natriuretic peptides and their genes in hearts of patients with cardiac amyloidosis. J. Am. Coll. Cardiol. 31, 754-765.
51. Takahashi, M., Hoshii, Y., Kawano, H., Gondo, T., Yokota, T., Okabyashi, H., et al. (1998) Ultrastructural evidence for the formation of amyloid fibrils within cardiomyocytes in isolated atrial amyloid. Amyloid 5, 35-42.
52. Barger, S. W. and Mattson, M. P. (1995) The secreted form of the Alzheimer's beta-amyloid precursor protein stimulates a membrane-associated guanylate cyclase. Biochem. J. 311, 45-47.
53. Jan, L. Y. and Jan, Y. H. (1997) Receptor-regulated ion channels. Curr. Opin. Cell Biol. 9, 155-160.
54. Hirakura, Y. and Kagan, B. L. (1999) Channel formation in the pathogenesis of Alzheimer's disease and other amyloidoses. Einstein Qu. J. Biol. Med. 16, 124-129.
55. Hama, N., Itoh, H., Shirakami, G., Suga, S., Komatsu, Y., Yoshimasa, T., et al. (1994) Detection of C-type natriuretic peptide in human circulation and marked increase of plasma CNP level in septic shock patients. Biochem. Biophys. Res. Comm. 198, 1177-1182.
56. de Plater, G. M., Martin, R. L., and Milburn, P. J. (1998) A C-Type natriuretic peptide from the venom of the platypus (Ornithorhynchus anatinus): structure and pharmacology. Comp. Biochem. Physiol. C 120, 99-110.
57. de Plater, G. M. (1998) Fractionation, primary structural characterisation and biological activities of polypeptides from the venom of the platypus (Ornithorhynchus anatinus). Ph.D. thesis, Australian National University. Canberra, Australia.
58. Kourie, J. I. and Rive, M. J. (1999) Role of natriuretic peptides in ion transport mechanisms. Med. Res. Rev. 19, 75-94.
59. Hille, B. (1992) Ionic Channels of Excitable Membranes (Hille, B., ed.), Sinaure Associates, Sunderland, MA.
60. Merrill, A. R., Steer, B. A., Prentice, G. A., Weller, M. J., and Szabo, A. G. (1997) Identification of a chameleon-like pH-sensitive segment within the colicin E1 channel domain that may serve as the pH-activated trigger for membrane bilayer association. Biochemistry 36, 6874-6884.
61. Minn, A. J., Velez, P., Schendel, S. L., Liang, H., Muchmore, S. W., Fesik, S. W., et al. (1997) Bcl-x(L) forms an ion channel in synthetic lipid membranes. Nature 385, 353-357.
62. Hinrichesn, R. D. (1993) Calcium-Dependent Potassium Channels R. G. Landes Company, Austin, TX.
63. Pallotta, B. (1985) N-Bromoacetamide removes a calcium-dependent component of channel opening from calcium-activated potassium channels in rat skeletal muscle. J. Gen. Physiol. 86, 601-611.
64. 2+ channels in hippocampal neurons. Science 395, 900-905.
65. 2+ concentration in smooth muscle as revealed by measurement on single cells. Proc. Natl. Acad. Sci. USA 85, 4109-4113.
66. Koller, K. J., Lowe, D. G., Bennett, G. L., Minamino, W., Kangawa, K., Matsuo, H., et al. (1991) Selective activation of the B natriuretic peptide receptor by C-type natriuretic peptide (CNP). Science 252, 120-123.
67. Morita, H., Hagike, M., Horiba, T., Miyake, K., Ohyama, H., Yamaouchi, H., et al. (1992) Effects of brain natriuretic peptide and C-type natriuretic peptide infusion on urine flow and jejunal absorption in anesthetized dogs. Jpn. J. Physiol. 42, 349-353.
68. Kourie, J. I., Hanna, E. A., and Henry, C. L. (2001). Properties of alpha human atrial natriuretic peptide (α-hANP)-formed ion channels. Can. J. Physiol. Pharmacol. 79, 654-664.
69. Mirzabekov, T. A., Lin, M. C., and Kagan, B. L. (1996) Pore formation by the cytotoxic islet amyloid peptide amylin. J. Biol. Chem. 271, 1988-1992.
70. McLean, L. R. and Balasubramaniam, A. (1992) Promotion of beta-structure by interaction of diabetes associated polypeptide (amylin) with phosphatidylcholine. Biochem. Biophys. Acta 1122, 317-320.
71. Charge, S. B., de Koning, E. J., and Clark, A. (1995) Effect of pH and insulin on fibrillogenesis of islet amyloid polypeptide in vitro. Biochemistry 34, 14,588-14,593.
72. Janson, J., Ashley, R. H., Harrison, D., McIntyre, S., and Butler, P. C. (1999) The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediate-sized toxic amyloid particles. Diabetes 48, 491-498.
73. Munoz, F. J. and Inestrosa, N. C. (1999). Neurotoxicity of acetylcholinesterase amyloid beta-peptide aggregates is dependent on the type of Abeta peptide and the AchE concentration present in the complexes. FEBS Lett. 450, 205-209.