Apolipoprotein E uptake and low-density lipoprotein receptor-related protein expression by the NTera2/D1 cell line: A cell culture model of relevance for late-onset Alzheimer's disease

Neurobiology of Disease

Volumn 4, Issue 1, 1997, Pages 58-67

  Williams, Kieran R ^a   Pye, Victoria ^a   Saunders, Ann M ^b   Roses, Allen D ^b   Armati, Patricia J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; LIPOPROTEIN RECEPTOR; RETINOIC ACID;

ALLELISM; ALZHEIMER DISEASE; ARTICLE; CELL DIFFERENTIATION; HUMAN; HUMAN CELL; LIPOPROTEIN METABOLISM; NEUROFIBRILLARY TANGLE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN SYNTHESIS; RISK FACTOR;

EID: 0030716322     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1006/nbdi.1997.0131     Document Type: Article

References (58)

1. Anwar, N., Lovestone, S., Cheetham, M. E., Levy, R., & Powell, J. F. (1993) Apolipoprotein E-epsilon 4 allele and Alzheimer's disease. Lancet 342, 1308-1309. [Letter]
2. Bellosta, S., Nathan, B. P., Orth, M., Dong, L.-M., Mahley, R. W., & Pitas, R. E. (1995) Stable expression and secretion of apolipoproteins E3 and E4 in mouse neuroblastoma cells produces differential effects on neurite outgrowth. J. Biol. Chem. 270, 27063-27071.
3. Boyles, J. K., Pitas, R. E., Wilson, E., Mahley, R. W., & 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, 1501-1513.
4. Boyles, J. K., Notterpek, L. M., & Anderson, L. J. (1990) Accumulation of apolipoproteins in the regenerating and remyelinating mammalian peripheral nerve. Identification of apolipoprotein D, apolipoprotein A-IV, apolipoprotein E, and apolipoprotein A-I. J. Biol. Chem. 265, 17805-17815.
5. Braak, H., & Braak, E. (1991) Neuropathological staging of Alzheimer-related changes. Acta Neuropathol. 82, 239-259. [Review]
6. Breslow, J. L. (1985) Human apolipoprotein molecular biology and genetic variation. Annu. Rev. Biochem. 54, 699-727. [Review]
7. Carlsson, J., Armstrong, V. W., Reiber, H., Felgenhauer, K., & Seidel, D. (1991) Clinical relevance of the quantification of apolipoprotein E in cerebrospinal fluid. Clin. Chim. Acta 196, 167-176.
8. Chen, W. J., Goldstein, J. L., & Brown, M. S. (1990) NPXY, a sequence often found in cytoplasmic tails is required for coated pitmediated internalization of the LDL receptor. J. Biol. Chem. 265, 3116-3123.
9. Corder, E. H., Saunders, A. M., Strittmatter, W. J., Schmechel, D. E., Gaskell, P. C., Small, G. W., Roses, A. D., Haines, J. L., & Pericak-Vance, M. A. (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261, 921-923.
10. Corder, E. H., Saunders, A. M., Risch, N. J., Strittmatter, W. J., Schmechel, D. E., Gaskell, P. C., Rimmler, J. B., Locke, P. A., Conneally, P. M., Schmader, K. E., Small, G. W., Roses, A. D., Haines, J. L., & Pericak-Vance, M. A. (1994) Protective effect of apolipoprotein E type 2 allele for late-onset Alzheimer's disease. Nature Genet. 7, 180-184.
11. Draper, R. K., & Simon, M. I. (1980) The entry of diphtheria toxin into mammalian cell cytoplasm: Evidence for lysosomal involvement. J. Cell Biol. 87, 849-854.
12. Falnes, P. O., & Olsnes, S. (1995) Cell-mediated reduction and incomplete membrane translocation of diphtheria toxin mutants with internal disulfides in the A fragment. J. Cell Biol. 270, 20787-20793.
13. Han, S-H., Einstein, G., Weisgraber, K. H., Strittmatter, W. J., Saunders, A. M., Pericak-Vance, M. A., Roses, A. D., & Schmechel, D. E. (1994a) Apolipoprotein E is localised to the cytoplasm of human cortical neurons: A light and electron microscopic study. J. Neuropathol. Exp. Neurol. 53, 535-544.
14. Han, S-H., Hulette, C., Saunders, A. M., Einstein, G., Pericak-Vance, M., Strittmatter, W. J., Roses, A. D., & Schmechel, D. E. (1994b) Apolipoprotein E is present in hippocampal neurons without neurofibrillary tangles in Alzheimer's disease and in age-matched controls. Exp. Neurol. 128, 13-26.
15. Handelmann, G. E., Boyles, J. K., Weisgraber, K. H., Mahley, R. W, & Pitas, R. E. (1992) Effects of apolipoprotein E, beta-very low density lipoproteins, and cholesterol on the extension of neurites by rabbit dorsal root ganglia in vitro. J. Lipid Res. 33, 1677-1688.
16. Hirokawa, N. (1994) Microtubule organisation and dynamics dependent on microtubule-associated proteins. Curr. Opin. Cell Biol. 6, 74-81. [Review]
17. Holtzman, D. M., Pitas, R. E., Kilbridge, J., Nathan, B., Mahley, R. W., Bu, G., & Schwartz, A. L. (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. USA 92, 9480-9484.
18. Houlden, H., Crook, R., Hardy, J., Roques, P., Collinge, J., & Rossor, M. (1994) Confirmation that familial clustering and age of onset in late onset Alzheimer's disease are determined at the apolipoprotein E locus. Neurosci. Lett. 174, 222-224.
19. Ignatius, M. J., Gebicke-Harter, P. J., Skene, J. H., Schilling, J. W., Weisgraber, K. H., Mahley, R. W., & Shooter, E. M. (1986) Expression of apolipoprotein E during nerve degeneration and regeneration. Proc. Natl. Acad. Sci. USA 83, 1125-1129.
20. Ignatius, M. J., Shooter, E. M., Pitas, R. E., & Mahley, R. W. (1987) Lipoprotein uptake by neuronal growth cones in vitro. Science 236, 959-962.
21. Jensen, T. G., Roses, A. D., & Jorgensen, A. L. (1994) Apolipoprotein E uptake and degradation via chloroquine-sensitive pathway in cultivated monkey cells overexpressing low density lipoprotein receptor. Neurosci. Lett. 180, 193-196.
22. Lee, V. M., & Andrews, P. W. (1986) Differentiation of NTERA-2 clonal human embryonal carcinoma cells into neurons involves the induction of all three neurofilament proteins. J. Neurosci. 6, 514-521.
23. Lestavel, S., & Fruchart, J. C. (1994) Lipoprotein receptors. Cell. Mol. Biol. 40, 461-481.
24. Mahley, R. W. (1988) Apolipoprotein E: Cholesterol transport protein with expanding role in cell biology. Science 240, 622-630.
25. Mahley, R. W., & Innerarity, T. L. (1983) Lipoprotein receptors and cholesterol homeostasis. Biochim. Biophys. Acta 737, 197-222.
26. Muller, H. W., Gebicke-Herter, P. J., Hangen, D. H., & Shooter, E. M. (1985) A specific 37,000-dalton protein that accumulates in regenerating but not in nonregenerating mammalian nerves. Science 228, 499-501.
27. Namba, Y., Tomonaga, M., Kawasaki, H., Otomo, E., & 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, 163-166.
28. Nathan, B. P., Bellosta, S., Sanan, D. A., Weisgraber, K. H., Mahley, R. W., & Pitas, R. E. (1994) Differential effects of apolipoproteins E3 and E4 on neuronal growth in vitro. Science 264, 850-852.
29. Penfold, M., Armati, P J., & Cunningham, A. L. (1994) Axonal transport of herpes simplex virions to epidermal cells. Evidence for a specialised mode of virus transport and assembly. Proc. Natl. Acad. Sci. USA 91, 6529-6533.
30. Pitas, R. E., Boyles, J. K., Lee, S. H., Hui, D., & Weisgraber, K. H. (1987a). Lipoproteins and their receptors in the central nervous system. Characterisation of the lipoproteins in cerebrospinal fluid and identification of apolipoprotein B,E(LDL) receptors in the brain. J. Biol. Chem. 262, 14352-14360.
31. Pitas, R. E., Boyles, J. K., Lee, S. H., Foss, D., & Mahley, R. W. (1987b) Astrocytes synthesize apolipoprotein E and metabolize apolipoprotein E-containing lipoproteins. Biochim. Biophys. Acta 917, 148-161.
32. Pleasure, S. J., Page, C., & Lee, V. M. (1992) Pure, postmitotic, polarised human neurons derived from NTera 2 cells provide a system for expressing exogenous proteins in terminally differentiated neurons. J. Neurol. Sci. 12, 1802-1815.
33. Pleasure, S. J., & Lee, V. M. (1993) NTera 2 cells: A human cell line which displays characteristics expected of a human committed neuronal progenitor cell. J. Neurosci. Res. 35, 585-602.
34. Poirier, J., Hess, M., May, P. C., & Finch, C. E. (1991) Astrocytic apolipoprotein E mRNA and GFAP mRNA in hippocampus after entorhinal cortex lesioning. Brain Res. Mol. Brain Res. 11, 97-106.
35. Poirier, J., Davignon, J., Bouthillier, D., Kogan, S., Bertrand, P., & Gauthier, S. (1993) Apolipoprotein E polymorphism and Alzheimer's disease. Lancet 342, 697-699.
36. Rebeck, G. W., Reiter, J. S., Strickland, D. K., & Hyman, B. T. (1993) Apolipoprotein E in sporadic Alzheimer's disease: Allelic variation and receptor interactions. Neuron 11, 575-580.
37. Rebeck, G. W., Harr, S. D., Strickland, D. K., & Hyman, B. T. (1995) Multiple, diverse senile plaque-associated proteins are ligands of an apolipoprotein E receptor, the alpha 2-macroglobulin receptor/ low-density-lipoprotein receptor-related protein. Ann. Neurol. 37, 211-217.
38. Roheim, P. S., Carey, M., Forte, T., & Vega, G. L. (1979) Apolipoproteins in human cerebrospinal fluid. Proc. Natl. Acad. Sci. USA 76, 4646-4649.
39. Roses, A. D., Einstein, G., Gilbert, J., Goedert, M., Han, S-H., Huang, D., Hulette, C., Masliah, E., Pericak-Vance, M. A., Sanders, A. M., Schmechel, D. E., Strittmatter, W. J., Weisgraber, K. H., & Xi, P-T. (1996) Morphological, biochemical and genetic support for an apolipoprotein E effect of microtubular metabolism. Ann. N.Y. Acad. Sci. 777, 146-157.
40. Sandvig, K., & Olsnes, S. (1980) Diphtheria toxin entry into cells is facilitated by low pH. J. Cell Biol. 87, 828-832.
41. Saunders, A. M., Strittmatter, W. J., Schmechel, D. E., St. George-Hyslop, P. H., Pericak-Vance, M. A., Joo, S. H., Rose, B. L., Gusella, J. F., Crapper-MacLachlan, D. R., & Alberts, M. J. (1993) Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer's disease. Neurology 43, 1467-1472.
42. Schmechel, D. E., Saunders, A. M., Strittmatter, W. J., Grain, B. J., Hulette, C. M., Joo, S. H., Pericak-Vance, M. A., Goldgaber, D., & Roses, A. D. (1993) Increased amyloid beta-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset Alzheimer's disease. Proc. Natl. Acad. Sci. USA 90, 9649-9653.
43. Snipes, G. J., McGuire, C. B., Norden, J. J., & Freeman, J. A. (1986) Nerve injury stimulates the secretion of apolipoprotein E by nonneuronal cells. Proc. Natl. Acad. Sci. USA 83, 1130-1134.
44. Strittmatter, W. J., Saunders, A. M., Schmechel, D., Pericak-Vance, M., Enghild, J., Salvesen, G. S., & Roses, A. D. (1993a) 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. USA 90, 1977-1981.
45. Strittmatter, W. J., Weisgraber, K. H., Huang, D. Y., Dong, L. M., Salvesen, G. S., Pericak-Vance, M., Schmechel, D., Saunders, A. M., Goldgaber, D., & Roses, A. D. (1993b) Binding of human apolipoprotein to synthetic amyloid beta peptide: Isoform-specific effects and implications for late onset Alzheimer's disease. Proc. Natl. Acad. Sci. USA 90, 8098-8102.
46. Strittmatter, W. J., Saunders, A. M., Goedert, M., Weisgraber, K. H., Dong, L. M., Jakes, R., Huang, D. Y., Pericak-Vance, M., Schmechel, D. E., & Roses, A. D. (1994a) Isoform-specific interactions of apolipoprotein E with microtubule-associated protein tau: Implications for Alzheimer's disease. Proc. Natl. Acad. Sci. USA 91, 11183-11186.
47. Strittmatter, W. J., Weisgraber, K. H., Goedert, M., Saunders, A. M., Huang, D., Corder, E. H., Dong, L., Jakes, R., Alberts, M. J., Gilbert, J. R., Han, S. H., Hulette, C., Einstein, G., Schmechel, D. E., Pericak-Vance, M. A., & Roses, A. D. (1994b). Hypothesis: Microtubule instability and paired helical filament formation in the Alzheimer's disease brain are related to apolipoprotein E genotype. Exp. Neurol. 125, 163-171.
48. Tsai, M. S., Tangalos, E. G., Petersen, R. C., Smith, G. E., Schaid, D. J., Kokmen, E., Ivnik, R. J., & Thibodeau, S. N. (1994) Apolipoprotein E: Risk factor for Alzheimer disease. Am. J. Hum. Genet. 54, 643-649.
49. Utermann, G., Langenbeck, U., Beisiegel, U., & Weber, W. (1980). Genetics of the apolipoprotein E system in man. Am. J. Hum. Genet. 32, 339-347.
50. Vogel, T., Weisgraber, K. H., Zeevi, M. I., Ben-Artzi, H., Levanon, A. Z., Rall, S. C., Innerarity, T. L., Hui, D. Y., Taylor, J. M., Kanner, D., Yavin, Z., Amit, B., Aviv, H., Gorecki, M., & Mahley, R. W. (1985) Human apolipoprotein E expression in Escherichia coli: Structural and functional identity of the bacterially produced protein with plasma apolipoprotein E. Proc. Natl. Acad. Sci. USA 82, 8696-8700.
51. Weisgraber, K. H., Roses, A. D., & Strittmatter, W. J. (1994) The role of apolipoprotein E in the nervous system. Curr. Opin. Lipids 5, 110-115.
52. Wertkin, A. M., Turner, R. S., Pleasure, S. J., Golde, T. E., Younkin, S. G., Trojanowski, J. Q., & Lee, V. M. (1993) Human neurons derived from a teratocarcinoma cell line express solely the 696-amino acid amyloid precursor protein and produce intracellular β-amyloid or A4 peptides. Proc. Natl. Acad. Sci. USA 90, 9513-9517.
53. Wischik, C. M. (1991) Molecular neuropathology of Alzheimer's disease. In Carers, Professionals and Alzheimer's Disease (O'Neill, D. Ed), pp. 239-251. Libbey, London.
54. Wolf, B. A., Wertkin, A. M., Jolly, Y. C., Yasuda, R. P., Wolfe, B. B., Konrad, R. J., Manning, D., Ravi, S., Williamson, J. R., & Lee, V. M. (1995) Muscarinic regulation of Alzheimer's disease amyloid precursor protein secretion and amyloid beta-protein production in human neuronal NT2N cells. J. Biol. Chem. 270, 4916-4922.
55. Wolf, B. B., Lopes, M. B., VandenBerg, S. R., & Gonias, S. L. (1992) Characterization and immunohistochemical localization of alpha 2-macroglobulin receptor (low-density lipoprotein receptor-related protein) in human brain. Am. J. Pathol. 141, 37-42.
56. Xu, P.-T., Schmechel, D., Rothrock-Christian, T., Burkhart, D. S., Qiu, H.-L., Popko, B., Sullivan, P., Maeda, N., Saunders, A. M., Roses, A. D., & Gilbert, J. R. (1996) Human apolipoprotein E2, E3, and E4 isoform-specific transgenic mice: Human-like pattern of glial and neuronal immunoreactivity in central nervous system not observed in wild-type mice. Neurobiol. Dis. 3, 229-245.
57. Younkin, D. P., Tang, C. M., Hardy, M., Reddy, U. R., Shi, Q. Y., Pleasure, S. J., Lee, V. M., & Pleasure, D. (1993) Inducible expression of neuronal glutamate receptor channels in the NT2 human cell line. Proc. Natl. Acad. Sci. USA 90, 2174-2178.
58. Zeller, M., & Strauss, W. L. (1995) Retinoic acid induces cholinergic differentiation of NTera 2 human embryonal carcinoma cells. Int. J. Dev. Neurosci. 13, 437-445.