Progress toward identification of protease activity involved in proteolysis of apolipoprotein E in human brain

Journal of Molecular Neuroscience

Volumn 24, Issue 1, 2004, Pages 73-80

  Marques, Marcos A ^a   Owens, Phillip A ^a   Crutcher, Keith A ^a,b  

^a ApoLogic Inc   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; apoE fragments; Protease inhibitor drug disease

Indexed keywords

AMYLOID; APOLIPOPROTEIN E; ASPARTIC PROTEINASE; PROTEINASE; ENZYME INHIBITOR; PEPTIDE FRAGMENT; PEPTIDE HYDROLASE;

ACIDITY; ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; BRAIN; BRAIN HOMOGENATE; CARBOXY TERMINAL SEQUENCE; CONFERENCE PAPER; DISEASE MARKER; DRUG EFFICACY; DRUG SCREENING; DRUG TARGETING; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HYPOTHESIS; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; MOLECULAR MECHANICS; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; RISK FACTOR; ANIMAL; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENETICS; METABOLISM; PATHOPHYSIOLOGY; REVIEW; SENILE PLAQUE;

MUS MUSCULUS;

ALZHEIMER DISEASE; ANIMALS; APOLIPOPROTEINS E; BRAIN; DRUG EVALUATION, PRECLINICAL; ENZYME INHIBITORS; HUMANS; NEUROFIBRILLARY TANGLES; PEPTIDE FRAGMENTS; PEPTIDE HYDROLASES; SENILE PLAQUES;

EID: 16544379360     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1385/jmn:24:1:073     Document Type: Conference Paper

References (77)

1. Aizawa Y., Fukatsu R., Takamaru Y., Tsuzuki K., Chiba H., et al. (1997) Amino-terminus truncated apolipoprotein E is the major species in amyloid deposits in Alzheimer's disease-affected brains: a possible role for apolipoprotein E in Alzheimer's disease. Brain Res. 768(1-2), 208-214.
2. Amaratunga A., Abraham C. R., Edwards R. B., Sandell J. H., Schreiber B. M., et al. (1996) Apolipoprotein E is synthesized in the retina by Muller glial cells, secreted into the vitreous, and rapidly transported into the optic nerve by retinal ganglion cells. J. Biol. Chem. 271(10), 5628-5632.
3. Bales K. R., Verina T.,Cummins D. J., Du Y., Dodel R. C., et al. (1999) Apolipoprotein E is essential for amyloid deposition in the APP(V717F) transgenic mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 96(26), 15233-15238.
4. Bellosta S., Nathan B. P., Orth M., Dong L. M., Mahley R. W., et al. (1995) Stable expression and secretion of apolipoproteins E3 and E4 in mouse neuroblastoma cells produces differential effects on neurite outgrowth. J. Biol. Chem. 270(45), 27063-27071.
5. Boyles J. K., Pitas R. E., Wilson E., Mahley R. W., and Taylor J. M. (1985) Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. J. Clin. Invest. 76(4), 1501-1513.
6. Bradley W. A., Gilliam E. B., Gotto A. M. J., and Gianturco S. H. (1982) Apolipoprotein E degradation in Human very low density lipoproteins by plasma protease(s): chemical and biological consequences. Biochem. Biophys. Res. Commun. 109, 1360-1367.
7. Browning P. J., Roberts D. D., Zabrenetzky V., Bryant J., Kaplan M., et al. (1994) Apolipoprotein E (ApoE), a novel heparin-binding protein inhibits the development of Kaposi's sarcoma-like lesions in BALB/cnu/nu mice. J. Exp. Med. 180(5), 1949-1954.
8. Buttini M., Akeefe H., Lin C., Mahley R. W., Pitas R. E., et al. (2000) Dominant negative effects of apolipoprotein E4 revealed in transgenic models of neurodegenerative disease. Neuroscience 97(2), 207-210.
9. Cambon K., Davies H. A., and Stewart M. G. (2000) Synaptic loss is accompanied by an increase in synaptic area in the dentate gyrus of aged human apolipoprotein E4 transgenic mice. Neuroscience 97(4), 685-692.
10. Cho H. S., Hyman B. T., Greenberg S. M., and Rebeck G. W. (2001) Quantification of apoE domains in Alzheimer disease brain suggests a role for apoE in Aβ aggregation. J. Neuropathol. Exp. Neurol. 60, 342-349.
11. Clay M. A., Anantharamaiah G. M., Mistry M. J., Balasubramaniam A., and Harmony J. A. (1995) Localization of a domain in apolipoprotein E with both cytostatic and cytotoxic activity. Biochemistry 34(35), 11142-11151.
12. Colton C. A., Brown C. M., Cook D., Needham L. K., Xu Q., et al. (2002). APOE and the regulation of microglial nitric oxide production: a link between genetic risk and oxidative stress. Neurobiol. Aging 23(5), 777-785.
13. Crutcher K. A., Clay M. A., Scott S. A., Tian X., Tolar M., et al. (1994) Neurite degeneration elicited by apolipoprotein E peptides. Exp. Neurol. 130(1), 120-126.
14. Crutcher K. A., Tolar M., Harmony J. A., and Marques M. A. (1997) A new hypothesis for the role of apolipoprotein E in Alzheimer's disease pathology, in Alzheimer's Disease: Biology, Diagnosis and Therapeutics, Iqbal, K., Winblad B., Nishimura T., Taketa M., and Wisniewski H. M., eds., John Wiley Chichester, U K, pp. 543-552.
15. Cummings M. H., Watts G. F., Umpleby A. M., Hennessy T. R., Kelly J. M., et al. (1995) Acute hyperinsulinemia decreases the hepatic secretion of very-low-density lipoprotein apolipoprotein B-100 in NIDDM. Diabetes 44(9), 1059-1065.
16. DeKroon R. M. and Armati P. J. (2001) The endosomal trafficking of apolipoprotein E3 and E4 in cultured human brain neurons and astrocytes. Neurobiol. Dis. 8(1), 78-89.
17. DeMattos R. B., Thorngate F. E. and Williams D. L. (1999). A test of the cytosolic apolipoprotein E hypothesis fails to detect the escape of apolipoprotein E from the endocytic pathway into the cytosol and shows that direct expression of apolipoprotein E in the cytosol is cytotoxic. J. Neurosci. 19(7), 2464-2473.
18. Dyer C. A. and Curtiss L. K. (1988) Apoprotein E-rich high density lipoproteins inhibit ovarian androgen synthesis. J. Biol. Chem. 263(22), 10965-10973.
19. Fillit H. (2002) Economics, pharmacoeconomics and drug discovery for dementias. Drug Discov. Today 7(15), 785-787.
20. Fillit H., Hill J. W., and Futterman R. (2002) Health care utilization and costs of Alzheimer's disease: the role of co-morbid conditions, disease stage, and pharmacotherapy. Fam. Med. 34(7), 528-535.
21. Han S. H., Einstein G., Weisgraber K. H., Strittmatter W. J., Saunders A. M., et al. (1994a) Apolipoprotein E is localized to the cytoplasm of human cortical neurons: a light and electron microscopic study. J. Neuropathol. Exp. Neurol. 53(5), 535-544.
22. Han S. H., Hulette C., Saunders A. M., Einstein G., Pericak-Vance M., et al. (1994b) Apolipoprotein E is present in hippocampal neurons without neurofibrillary tangles in Alzheimer's disease and in age-matched controls. Exp. Neurol. 128(1), 13-26.
23. Harris F. M., Brecht W. J., Xu Q., Tesseur I., Kekonius L., et al. (2003) Carboxyl-terminal-truncated apolipoprotein E4 causes Alzheimer's disease-like neurodegeneration and behavioral deficits in transgenic mice. Proc. Natl. Acad. Sci. USA 100, 10966-10971.
24. Hartman R. E., Wozniak D. F., Nardi A., Olney J. W., Sartorius L., et al. (2001) Behavioral phenotyping of GFAP-apoE3 and -apoE4 transgenic mice: apoE4 mice show profound working memory impairments in the absence of Alzheimer's-like neuropathology. Exp. Neurol. 170(2), 326-344.
25. Hashimoto Y., Jiang H., Niikura T., Ito Y., Hagiwara A., et al. (2000) Neuronal apoptosis by apolipoprotein E4 through low-density lipoprotein receptor-related protein and heterotrimeric GTPases. J. Neurosci. 20(22), 8401-8409.
26. Holtzman D. M., Bales K. R., Tenkova T., Fagan A. M., Parsadanian M., et al. (2000) Apolipoprotein E isoform-dependent amyloid deposition and neuritic degeneration in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 97(6), 2892-2897.
27. Holtzman D. M., Bales K. R., Wu S., Bhat P., Parsadanian M., et al. (1999) Expression of human apolipoprotein E reduces amyloid-beta deposition in a mouse model of Alzheimer's disease. J. Clin. Invest. 103(6), R15-R21.
28. Holtzman D. M., Pitas R. E., Kilbridge J., Nathan B., Mahley R. W., et al. (1995) Low density lipoprotein receptor-related protein mediates apolipoprotein E-dependent neurite outgrowth in a central nervous system-derived neuronal cell line. Proc. Natl. Acad. Sci. U. S. A. 92(21), 9480-9484.
29. Huang Y., Liu X. Q., Wyss-Coray T., Brecht W. J., Sanan D. A., et al. (2001) Apolipoprotein E fragments present in Alzheimer's disease brains induce neurofibrillary tangle-like intracellular inclusions in neurons. Proc. Natl. Acad. Sci. U. S. A. 98(15), 8838-8843.
30. Ignatius M. J., Gebicke-Harter P. J., Skene J. H., Schilling J. W., Weisgraber K. H., et al. (1986) Expression of apolipoprotein E during nerve degeneration and regeneration. Proc. Natl. Acad. Sci. U. S. A. 83(4), 1125-1129.
31. Innerarity T. L., Friedlander E. J., Rall S. C., Weisgraber K. H., and Mahley R. W. (1983) The receptor-binding domain of human apolipoprotein E. Binding of apolipoprotein E fragments. J. Biol. Chem. 258(20), 12341-12347.
32. Innerarity T. L., Weisgraber K. H., Rall S. C., and Mahley R. W. (1987) Functional domains of apolipoprotein E and apolipoprotein B. Acta Med. Scand. Suppl. 715(12), 51-59.
33. Kobayashi M., Ishiguro K., Katoh-Fukui Y., Yokoayama M., and Fujita S. C. (2003) Phosphorylation state of tau in the hippocampus of apolipoprotein E4 and E3 knockin mice. Neuroreport 14, 699-702.
34. Koppel R. (2002) Alzheimer's disease: the cost to U.S. businesses in 2002, June, Alzheimer's Association, Chicago, IL.
35. Lendon C. L., Ashall F., and Goate A. M. (1997) Exploring the etiology of Alzheimer disease using molecular genetics. JAMA 277(10), 825-831.
36. Lins L., Thomas-Soumarmon A., Pillot T., Vandekerchkhove J., Rosseneu M., et al. (1999) Molecular determinants of the interaction between the C-terminal domain of Alzheimer's beta-amyloid peptide and apolipoprotein E alpha-helices. J. Neurochem. 73(2), 758-769.
37. Mahley R. W. (1988) Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240(4852), 622-630.
38. Mahley R. W., Hui D. Y., Innerarity T. L., and Weisgraber K. H. (1981) Two independent lipoprotein receptors on hepatic membranes of dog, swine, and man. Apo-B,E and apo-E receptors. J. Clin. Invest. 68(5), 1197-1206.
39. Mahley R. W., Innerarity T. L., Rall S. C., and Weisgraber K. H. (1985) Lipoproteins of special significance in atherosclerosis. Insights provided by studies of type III hyperlipoproteinemia. Ann. N.Y. Acad. Sci. 454(8), 209-221.
40. Mahley R. W., Innerarity T. L., Weisgraber K. H., Rall S. C., Hui D. Y., et al. (1986) Cellular and molecular biology of lipoprotein metabolism: characterization of lipoprotein receptor-ligand interactions. Cold Spring Harb. Symp. Quant. Biol. 51(Pt. 2[1]), 821-828.
41. Mahley R. W. and Ji Z. S. (1999) Remnant lipoprotein metabolism: key pathways involving cell-surface heparan sulfate proteoglycans and apolipoprotein E. J. Lipid Res. 40(1), 1-16.
42. Majack R. A., Castle C. K., Goodman L. V., Weisgraber K. H., Mahley R. W., et al. (1988) Expression of apolipoprotein E by cultured vascular smooth muscle cells is controlled by growth state. J. Cell. Biol. 107(3), 1207-1213.
43. Marques M. A. and Crutcher K. A. (2003) Apolipoprotein E-related neurotoxicity as a therapeutic target for Alzheimer's disease. J. Mol. Neurosci. 20(3), 117-127.
44. Marques M. A., Tolar A., and Crutcher K. A. (1997) Apolipoprotein E exhibits isoform-specific neurotoxicity. Alzheimer's Res. 3, 1-6.
45. Marques M. A., Tolar M., Harmony J. A. and Crutcher K. A. (1996) A thrombin cleavage fragment of apolipoprotein E exhibits isoform-specific neurotoxicity. Neuroreport 7(15-17), 2529-2532.
46. Morrow J. A., Hatters D. M., Lu B., Hochtl P., Oberg K. A., et al. (2002) Apolipoprotein E4 forms a molten globule: A potential basis for Its association with disease. J. Biol. Chem. 277, 50380-50385.
47. Nakai M., Kawamata T., Taniguchi T., Maeda K., and Tanaka C. (1996) Expression of apolipoprotein E mRNA in rat microglia. Neurosci. Lett. 211(1), 41-44.
48. Namba Y., Tomonaga M., Kawasaki H., Otomo E., and Ikeda K. (1991) Apolipoprotein E immunoreactivity in cerebral amyloid deposits and neurofibrillary tangles in Alzheimer's disease and kuru plaque amyloid in Creutzfeldt-Jakob disease. Brain Res. 541(1), 163-166.
49. Naslund J., Thyberg J., Tjernberg L. O., Wernstedt C., Karlstrom A. R., et al. (1995) Characterization of stable complexes involving apolipoprotein E and the amyloid beta peptide in Alzheimer's disease brain. Neuron 15(1), 219-228.
50. Nathan B. P., Bellosta S., Sanan D. A., Weisgraber K. H., Mahley R. W., et al. (1994) Differential effects of apolipoproteins E3 and E4 on neuronal growth in vitro. Science 264(5160), 850-852.
51. Nathan B. P., Chang K. C., Bellosta S., Brisch E., Ge N., et al. (1995) The inhibitory effect of apolipoprotein E4 on neurite outgrowth is associated with microtubule depolymerization. J. Biol. Chem. 270(34), 19791-19799.
52. Paka L., Goldberg I. J., Obunike J. C., Choi S. Y., Saxena U., et al. (1999) Perlecan mediates the antiproliferative effect of apolipoprotein E on smooth muscle cells. An underlying mechanism for the modulation of smooth muscle cell growth? J. Biol. Chem. 274(51), 36403-36408.
53. Pillot T., Goethals M., Najib J., Labeur C., Lins L., et al. (1999) Beta-amyloid peptide interacts specifically with the carboxy-terminal domain of human apolipoprotein E: relevance to Alzheimer's disease. J. Neurochem. 72(1), 230-237.
54. Poirier J. (1994) Apolipoprotein E in animal models of CNS injury and in Alzheimer's disease. Trends Neurosci. 17(12), 525-530.
55. Price D. L. and Sisodia S. S. (1994) Cellular and molecular biology of Alzheimer's disease and animal models. Annu. Rev. Med. 45(1), 435-446.
56. Qiu Z., Crutcher K. A., Hyman B. T., and Rebeck G. W. (2003) ApoE isoforms affect neuronal NMDA calcium responses and toxicity via receptor-mediated processes. Neuroscience 122, 291-303.
57. Saunders A. M., Schmader K., Breitner J. C., Benson M. D., Brown W. T., et al. (1993) Apolipoprotein E epsilon 4 allele distributions in late-onset Alzheimer's disease and in other amyloid-forming diseases. Lancet 342(8873), 710,711.
58. Stannard A. K., Riddell D. R., Sacre S. M., Tagalakis A. D., Langer C., et al. (2001) Cell-derived apolipoprotein E (ApoE) particles inhibit vascular cell adhesion molecule-1 (VCAM-1) expression in human endothelial cells. J. Biol. Chem. 276(49), 46011-46016.
59. Strittmatter W. J., Saunders A. M., Schmechel D., Pericak V. M., Enghild J., et al. (1993) Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 90(5), 1977-1981.
60. Terry R. D. (1994). Neuropathological changes in Alzheimer disease. Prog. Brain Res. 101(2), 383-390.
61. Terry R. D. and Katzman R. (1983). Senile dementia of the Alzheimer type. Ann. Neurol. 14(5), 497-506.
62. Tesseur I., Van Dorpe J., Spittaels K., Van den Haute C., Moechars D., et al. (2000) Expression of human apolipoprotein E4 in neurons causes hyperphosphorylation of protein tau in the brains of transgenic mice. Am. J. Pathol. 156(3), 951-964.
63. Tolar M., Keller J. N., Chan S., Mattson M. P., Marques M. A., et al. (1999) Truncated apolipoprotein E (ApoE) causes increased intracellular calcium and may mediate ApoE neurotoxicity. J. Neurosci. 19(16), 7100-7110.
64. Tolar M., Marques M. A., Harmony J. A., and Crutcher K. A. (1997) Neurotoxicity of the 22 kDa thrombin-cleavage fragment of apolipoprotein E and related synthetic peptides is receptor-mediated. J. Neurosci. 17(15), 5678-5686.
65. Vogel T., Guo N. H., Guy R., Drezlich N., Krutzsch H. C., et al. (1994). Apolipoprotein E: a potent inhibitor of endothelial and tumor cell proliferation. J. Cell. Biochem. 54(3), 299-308.
66. Weisgraber K. H. (1994) Apolipoprotein E: structure-function relationships. Adv. Protein Chem. 45, 249-302.
67. Weisgraber K. H., Innerarity T. L., Rall S. C., and Mahley R. W. (1985a) Apolipoprotein E: receptor binding properties. Adv. Exp. Med. Biol. 183(8), 159-171.
68. Weisgraber K. H., Innerarity T. L., Rall S. C., and Mahley R. W. (1985b) Receptor interactions controlling lipoprotein metabolism. Can. J. Biochem. Cell. Biol. 63(8), 898-905.
69. Weisgraber K. H., Rall S. C., Mahley R. W., Milne R. W., Marcel Y. L., et al. (1986) Human apolipoprotein E. Determination of the heparin binding sites of apolipoprotein E3. J. Biol. Chem. 261(5), 2068-2076.
70. Wetterau J. R., Aggerbeck L. P., Rall S. C., and Weisgraber K. H. (1988) Human apolipoprotein E3 in aqueous solution. I. Evidence for two structural domains. J. Biol. Chem. 263(13), 6240-6248.
71. Whitehouse P. J., Landreth G., and Younkin S. (1993) Molecular biology of Alzheimer's disease. Mol. Genet. Med. 3, 95-137.
72. Wisniewski T., Golabek A., Matsubara E., Ghiso J., and Frangione B. (1993) Apolipoprotein E: binding to soluble Alzheimer's beta-amyloid. Biochem. Biophys. Res. Commun. 192(2), 359-365.
73. Wisniewski T., Lalowski M., Golabek A., Vogel T., and Frangione B. (1995) Is Alzheimer's disease an apolipoprotein E amyloidosis? Lancet 345(8955), 956-958.
74. Xu Q., Li Y., Cyras C., Sanan D. A., and Cordell B. (2000) Isolation and characterization of apolipoproteins from murine microglia. Identification of a low density lipoprotein-like apolipoprotein j-rich but e-poor spherical particle. J. Biol. Chem. 275(41), 31770-31777.
75. Zeleny M., Swertfeger D. K., Weisgraber K. H., and Hui D. Y. (2002) Distinct apolipoprotein E isoform preference for inhibition of smooth muscle cell migration and proliferation. Biochemistry 41(39), 11820-11823.
76. Zhang D., McQuade J.-A., Shockley K. P., Marques M. A., and Crutcher K. A. (2001) Proteolysis of apolipoprotein E and Alzheimer's disease pathology. Alzheimers Rep. 4, 67-79.
77. Zhu B., Kuhel D. G., Witte D. P., and Hui D. Y. (2000) Apolipoprotein E inhibits neointimal hyperplasia after arterial injury in mice. Am. J. Pathol. 157(6), 1839-1848.