THE ALZHEIMER'S PLAQUES, TANGLES AND MEMORY DEFICITS MAY HAVE A COMMON ORIGIN - PART IV: CAN CALPAIN ACT AS a-SECRETASE?

Ming Chen¹ and Hugo L. Fernandez²

^1,2 Neuroscience Research Laboratory, Medical Research Service (151), Bay Pines VA Medical Center, Bay Pines, Florida 33744, USA. ² Department of Pharmacology and Therapeutics; Department of Neurology and bDepartment of Physiology and Biophysics, University of South Florida College of Medicine, Tampa, Florida, 33612, USA

Received 11/25/98 Accepted 12/4/98

6. REFERENCES

1. Glenner, G. G. and Wong, C. W. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120, 885-890 (1984)

2. Kang, J. Lemaire, H. Unterbeck, A. Salbaum, J. M. Masters, C. L. Grzeschik, K. Multhaup, G. Beyreuther, K. and Muller-Hill, B. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 325, 733-736 (1987)

3. Selkoe, D. J. Alzheimer's disease: genotypes, phenotypes and treatments. Science 275, 630-631 (1997)

4. Buxbaum, J.D., Ruefli, A.A., Parker, C.A., Cypess, A.M. and Greengard, P. Calcium regulates processing of the Alzheimer amyloid protein precursor in a protein kinase C-indenpendent manner. Proc. Natl. Acad. Sci. USA. 91, 4489-4493 (1994)

5. Cordell, B. beta-Amyloid formation as a potential therapeutic target for Alzheimer's disease. Ann Rev Pharmacol Toxicol 34, 69-89 (1994)

6. Mattson, M. P. Cellular actions of ß-amyloid precursor protein and its solution and fibrillogenic derivatives. Physiol Rev 77, 1081-1132 (1997)

7. Chen, M. Alzheimer's a-secretase may be a calcium-dependent protease. FEBS Lett 417, 163-167 (1997)

8. Disterhoft, J. F. Gispen, W. E. Traber, J. and Khachaturian, Z. S. Eds: Calcium hypothesis of aging and dementia. Ann N Y Acad Sci vol.747, New York (1994)

9. Chen, M. Is Alzheimer's disease associated with a decreased intracellular level of calcium? Front Biosci 3, let1-2 (1998) (www.bioscience.org/v3/let/chen/list.htm)

10. Nixon, R. A. Calcium-activated neutral proteinases as regulators of cellular function. Implications for Alzheimer's disease pathogenesis. Ann N Y Acad Sci 568, 198-208 (1989)

11. Lynch, G. and Baudry, M. Brain spectrin, calpain and long-term changes in synaptic efficacy. Brain Res Bull 18, 809-815 (1987)

12. Slack, B. E. Breu, J. Muchnickl, L. and Wurtman, R. J. Rapid stimulation of amyloid precursor protein release by epidermal growth factor: role of protein kinase C. Biochem J 327, 245-249 (1997)

13. Mills, J. Laurent Charest, D. Lam, F. Beyreuther, K. Ida, N. Pelech, S. L. and Reiner, P. B. Regulation of amyloid precursor protein catabolism involves the mitogen-activated protein kinase signal transduction pathway. J Neurosci 17, 9415-9422 (1997)

14. Nishizuka, Y. Studies and perspectives of protein kinase C. Science 233, 305-312 (1986)

15. Zhang, W. Espinoza, D. Hines, V. Innis, M. Mehta, P. and Miller, D. L. Characterization of ß-amyloid peptide precursor processing by the yeast Yap3 and Mkc7 proteases. Biochim. Biophys. Acta 1359, 110-122 (1997)

15a. Komano, H. Seeger, M. Gandy, S. Wang, G. T. Krafft, G. A. and Fuller, R. S. Involvement of cell surface glycosyl-phosphatidylinositol-linked aspartyl proteases in alpha-secretase-type cleavage and ectodomain solubilization of human Alzheimer beta-amyloid precursor protein in yeast. J Biol Chem 273, 31648-31651 (1998)

16. Chen, M. The Alzheimer's plaques, tangles and memory deficits may have a common origin-Part I: A calcium deficit hypothesis. Front Biosci 3, a27-31 (1998)

17. Chen, M. The Alzheimer's plaques, tangles and memory deficits may have a common origin-Part II: Therapeutic rationale. Front Biosci 3, a32-37 (1998)

18. Chen, M. The Alzheimer's plaques, tangles and memory deficits may have a common origin-Part III: Animal model. Front Biosci 3, a47-51 (1998)

19. Craig, C.R. and Stitzel, R.E. Modern Pharmacology with Clinical Applications. 5th edn., Little, Brown & Co., Boston (1997)

20. Kim, S. H. Kim, Y. K. Jeong, S. J. Haass, C. Kim, Y. H. and Suh, Y. H. Enhanced release of secreted form of Alzheimer's amyloid precursor protein from PC12 cells by nicotine. Mol Pharmacol 52, 430-436 (1997)

21. Nitsch, R. M., Kim, C. and Growdon, J. H. Vasopressin and bradykinin regulate secretory processing of the amyloid protein precursor of Alzheimer's disease. Neurochem Res 23, 807-814 (1998).

22. Jolly-Tornetta, C. Gao, Z-Y. Lee, V. M.-Y. and Wolf, B. A. Regulation of amyloid precursor protein secretion by glutamate receptors in human Ntera 2 neurons (NT2N). J Biol Chem 273, 14015-14021 (1998)

23. Dickens, G. Lavarreda, M. Zheng, W. H. and Guroff, G. Involvement of protein kinase C in nerve growth factor- and K-252a-stimulated calcium uptake into PC12 cells. J Neurosci Res 47, 271-276 (1997)

24. Gray, R. Rajan, A. S. Radcliffe, K. A. Yakehiro, M. and Dani, J. A. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383, 713-716 (1996)

25. Zwick, E. Daub, H. Aoki, N. Yamaguchi-Aoki, Y. Tinhofer, I. Maly, K. and Ulrich, A. Critical role of calcium-dependent epidermal growth factor receptor transactivation in PC12 cell membrane depolarization and bradykinin signaling. J Biol Chem 272, 24767-24770 (1997)

26. DeLapp, N. Wu, S., Belagaje, R. Johnstone, E. Little, S. Shannon, H., Bymaster, F. et al. Effects of the M1 agonist xanomeline on processing of human ß-amyloid precursor protein (FAD, Swedish mutant) transfected into Chinese hamster overy-m1 cells. Biochem Biophys Res Commun 244, 156-160 (1998)

27. Pittel, Z. Heldman, E. Barg, J., Haring, R. and Fisher, A. Muscarinic control of amyloid precursor protein secretion in rat cerebral cortex and cerebellum. Brain Res 742, 299-304 (1996)

28. Farber, S. A., Nitsch, R. M. Schultz, J. G. and Wurtman, R. J. Regulated secretion of beta-amyloid precursor protein in rat brain. J Neurosci 15, 7442-7451 (1995)

28a. Greenfield, J. P. Gouras, G. K. and Xu, H. Cellular and molecular basis of ß-amyloid precursor protein metabolism. Front Biosci 3, d399-407 (1998)

29. Albert, B. Bray, D. Lewis, J. Raff, M. Roberts, K. and Watson, J. D. Molecular Biology of the Cell. 3rd edn., Garland, New York (1994)

30. Bond, J. S. and Butler, P. E. Intracellular proteases. Ann Rev Biochem 56, 333-364 (1987)

31. Lannfelt, L. Basun, H. Wahlund, L-O. Rowe, B. A. and Wagner, S. L. Decreased a-secretase-cleaved amyloid precursor protein as a diagnostic marker for Alzheimer's disease. Nature Med 1, 829-832 (1995)

32. Van Nostrand, W. E. Wagner, S. L. Shankle, W. R. Farrow, J. S. Dick, M. Rozemuller, J. M. Kuiper, M. A. Wolters, E.C. et al. Decreased levels of soluble amyloid-ß protein precursor in cerebrospinal fluid of live Alzheimer's disease patients. Proc Natl Acad Sci USA 89, 2551-2555 (1992)

33. Masters, C. L. Simms, G. Weinman, N. A. Multhaup, G. McDonald, B. L. and K. Beyreuther, K. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci USA 82, 4245-4249 (1985)

34. Haass, C. and Selkoe, D. J. Cellular processing of beta-amyloid precursor protein and the genesis of amyloid beta-peptide. Cell 75, 1039-1042 (1993)

35. Saido, T. C. Iwatsubo, T. Mann, D. M. Shimada, H. Ihara, Y. and Kawashima, S. Dominant and differential deposition of distinct ß-amyloid peptide species, Aß N3(pE), in senile plaques. Neuron 14, 457-466 (1995)

36.Ivy, G. O. Protease inhibition causes some manifestations of aging and Alzheimer's disease in rodent and primate brain. Ann N Y Acad Sci 674, 89-102 (1992)

37. Ladner, C. J. and Lee, J. M. Pharmacological drug treatment of Alzheimer disease: The cholinergic hypothesis revisited. J Neuropathol Exp Neurol 57, 719-731 (1998)

38. Iqbal, K. Alonso, A. D. C. Gong, C.-X. Khatoon, S. Pei, J.-J. Wang, J. Z. and Grundke-Iqbal, I. Mechanisms of neurofibrillary degeneration and the formation of neurofibrillary tangles. J Neuroal Transm (suppl) 53, 169-180 (1998)

39. Kurumatani, T. Fastbom, J. Bonkale, W. L. Bogdanovic, N. Winblad, B. Ohm, T. G. and Cowburn, R. F. Loss of inositol 1,4,5-trisphosphate receptors and decreased PKC levels correlate with staging of Alzheimer's disease neurofibrillary pathology. Brain Res 796, 209-211 (1998)

40. Sisodia, S. S. Beta-amyloid precursor protein cleavage by a membrane-bound protease. Proc Natl Acad Sci USA 89, 6075-6079 (1992)

41. Zhang, H. Komano, H. Fuller, R. S. Gandy, S. E. and Frail, D. E. Proteolytic processing and secretion of human beta-amyloid precursor protein in yeast. Evidence for a yeast secretase activity. J Biol Chem 269, 27799-27802 (1994)

42. McGowan, E. B. Yeo, K. T. and Detwiler, T. C. The action of calcium-dependent protease on platelet surface glycoproteins. Arch Biochem Biophys 227, 287-301 (1983)

43. Chen, M. Inestrosa, N. C. Ross, G. S. and Fernandez, H. L. Platelets are the primary source of amyloid beta-peptide in human blood. Biochem Biophys Res Commun 213, 96-103 (1995)

44. Van Nostrand, W. E. Schmaier, A. H. Farrow, J. S. and Cunningham, D. D. Protease nexin-II (amyloid beta-protein precursor): a platelet alpha-grandule protein. Science 248, 745-748 (1990)

45. Suzuki, K. Sorimachi, H. Yoshizawa, T. Kinbara, K. and Ishiura, S. Calpain: novel family members, activation, and physiologic function. Biol Chem Hoppe-Seyler 376, 523-529 (1995)

46. Ohno, S. Emori, Y. Imajoh, S. Kawasaki, H. Kisaragi, M. and Suzuki, K. Evolutionary origin of a calcium-dependent protease by fusion of genes for a thiol protease and a calcium-binding protein? Nature 312, 566-570 (1984)

47. Li, Q. X. Evin, G. Small, D. H. Multhaup, G. Beyreuther, K. and Masters, C. L. Proteolytic processing of Alzeimer's disease beta A4 amyloid precursor protein in human platelets. J Biol Chem 270, 14140-14147 (1995)

48. Hong, D. H. Huan, J. Ou, B. R. Yeh, J. Y. Saido, T. C. Cheeke, P. R. and Forsberg, N. E. Protein kinase C isoforms in muscle cells and their regulation by phorbol ester and calpain. Biochim Biophys Acta 1267, 45-54 (1995)

49. Chen, M. and Stracher, A. In site phosphorylation of platelet actin-binding protein by cAMP-dependent protein kinase stabilizes it against proteolysis by calpain. J Biol Chem 264, 14282-14289 (1989)

50. Salamino, F. De Tullio, R. Mengotti, P. Melloni, E. and Pontremoli, S. Differential regulation of mu- and m-calpain in rat hearts perfused with Ca2+ and cAMP. Biochem Biophys Res Commun 202, 1197-1203 (1994)

51. Kishimoto, A. Mikawa, K. Hashimoto, K. Yasuda, I. Tanaka, S. Tominaga, M. Kuroda, T. and Nishizuka, Y. Limited proteolysis of protein kinase C subspecies by calcium-dependent neutral protease (calpain). J Biol Chem 264, 4088-4092 (1989)

52. Siman, R. Card, J. P. and Davis, L. G. Proteolytic processing of beta-amyloid precursor by calpain. J Neurosci 10, 2400-2411 (1990)

53. Shimohama, S. Suenaga, T. Araki, W. Yamaoaka, Y. Shimizu, K. and Kimura, J. Presence of calpain II immunoreactivity in senile plaques in Alzheimer's disease. Brain Res 558, 105-108 (1991)

54. Perlmutter, L. S. Siman, R. Gall, C. Seubert, P. Baudry, M. and Lynch, G. The ultrastructural localization of calcium-activated protease "calpain" in rat brain. Synapse 2, 79-88 (1988)

55. Nixon, R. A. Saito, K. I. Grynspan, F. Griffin, W. R. Katayama, S. Honda, T. Mohan, P. S. Shea, T. B. and Beermann, M. Calcium-activated neutral proteinase (calpain) system in aging and Alzheimer's disease. Ann N Y Acad Sci 747, 77-91 (1994)

56. Saido, T. C. Yokota, M. Maruyama, K. Yamao-Harigaya, W. Tani, E. Ihara, Y. and Kawashima, S. Spatial resolution of the primary beta-amyloidogenic process induced in postischemic hippocampus. J Biol Chem 269, 15253-15257 (1994)

57. Klafki, H. Abramowski, D. Swoboda, R. Paganetti, P. A. and Staufenbiel, M. The carboxyl termini of beta-amyloid peptides 1-40 and 1-42 are generated by distinct gamma-secretase activities. J Biol Chem 271, 28655-28659 (1996)

58. Higaki, J. Quon, D. Zhong, Z.-Y. and Cordell, B. Inhibition of ß-amyloid formation indentifies proteolytic precursors and subcellular site of catabolism. Neuron 14, 651-659 (1995)

59. Querfurth, H. W. and Selkoe, D. J. Calcium ionophore increases amyloid ß peptide production by cultured cells. Biochemistry 33, 4450-4561 (1994)

60. Yamazaki, T. Haass, C. Saido, T. C. Omura, S. and Ihara, Y. Specific increase of amyloid beta-protein 42 secretion ratio by calpain inhibition. Biochemitry 36, 8377-8383 (1997)

61. Clemetson, K. J. Naim, H. Y. and Luscher, E. F. Relationship between glycocalicin and glycoprotein Ib of human platelets. Proc Natl Acad Sci USA 78, 2712-2716 (1981)

62. Kawasaki, H. and Kawashima, S. Regulation of the calpain-calpastatin system by membranes. Mol Membrane Biol 13, 217-224 (1996)

63. Croall, D. E. and DeMartino, G. N. Calcium-activated neutral protease (calpain) system: structure, function, and regulation. Physiol Rev 71, 813-847 (1991)

64. Takahashi, K. Calpain substrate specificity. In "Intracellular Calcium-dependent Proteolysis." Mellgren, R.L., and Muarchi, T., eds. pp55-74, CRC Press, Boca Raton (1990)

65. Massagué, J. and Pandiella, A. Membrane-anchored growth factors. Annu Rev Biochem 62, 515-541 (1993)

66. Arribas, J. and Massagué, J. Transforming growth factor-a and ß-amyloid precursor protein share a secretory mechanism. J Cell Biol 128, 433-441 (1995)

67. Saido, T. C. Sorimachi, H. and Suzuki, K. Calpain: new perspectives in molecualr diversity and physiological-pathological involvement. FASEB J 8, 814-822 (1994)

68. Buxbaum, J. D. Liu, K. N. Slack, J. L. Stocking, K. L. Peschon, J. J. Johnson, R. S. Castner, B. J. Cerretti, D. P. and Black, R. A. Evidence that tumor necrosis factor alpha converting enzyme is involved in regulated alpha-secretase cleavage of the Alzheimer amyloid protein precursor. J Biol Chem 273, 27765-27767 (1998)

69. Shinozaki, K. et al. The presenilin 2 loop domain interacts with the µ-calpain C-terminal region. Int J Mol Med 1, 797-799 (1998)

70. Zhang, W. Han, S. W. WcKeel, D. W. Goate, A. and Wu, J. Y. Interaction of presenilins with the filamin family of actin-binding proteins. J Neurosci 18, 914-922 (1998)

71. Takashima, A. Murayama, M. Murayama, O. Kohno, T. Honda, T. Yasutake, K. Nihonmatsu, N. Mercken, M. Yamaguchi, H. Sugihara, S. and Wolozin, B. Presenilin 1 associates with glycogen synthase-3beta and its substrate tau. Proc Natl Acad Sci USA 95, 9637-9641 (1998)

72. Buxbaum, J. D. Choi, E.-K. Luo, Y. Lillehook, C. Crowley, A. C. Merriam, D. E. and Wasco, W. Calsenilin: A calcium-binding protein that interacts with the presenilins and regulates the levels of a presenilin fragment. Nature Med 4, 1177-1181 (1998)

73. Zhou, J. Liyanage, U. Medina, Ho, C. Simmons, A. D. Lovett, M. and Kosik, K. S. Presenilin 1 interaction in the brain with a novel member of the Armadilo family. Neuroreport 8, 2085-2090 (1997)

74. Bullions, L. C. and Levine, A. J. The role of beta-catenin in cell adhesion, signal transduction, and cancer. Curr Opin Oncol 10, 81-87 (1998)

75. Furukawa, K. Guo, Q. Schellenberg, G. D. and Mattson, M. P. Presenilin-1 mutation alters NGF-induced neurite outgrowth, calcium homeostasis, and transcription factor (AP-1) activation in PC12 cells. J Neurosci Res 52, 618-624 (1998)

76. Palacino, J. J. Berechid, B. Alexander, P. Nye, J. and Wolozin, B. Presenilin 1 regulates stimulated cleavage of the amyloid precursor protein. Soc Neuroci Abstr Vol. 24, Part 1, p470 (1998)

77. Marambaud, P. Alves da Costa, C. Ancolio, K. and Checler, F. Alzheimer's disease-linked mutation of presenilin 2 (N141I-PS2) drastically lowers APP alpha-secretion: control by the proteasome. Biochem Biophys Res Commun 252, 134-138 (1998)

78. De Strooper, B. Saftig, P. Craessaerts, K. Vanderstichele, H. Guhde, G. Annaert, W. Von Figura, K. and Van Leuven, F. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391, 387-390 (1998)

79. Wong, P. C. Zheng, H. Chen, H. Becher, M. W., Sirinathsinghji, D. J. S. Trumbauer, M. E. Chen, H. Y. Price, D. L. Van der Ploeg, L. H. T. and Sisodia, S. S. Presenilin 1 is required for Notch1 and Dll1 expression in the paraxial mesoderm. Nature 387, 288-291 (1997)