Sialic acid moiety of apolipoprotein E3 at Thr194 affects its interaction with β-amyloid1-42 peptides

Clinica Chimica Acta

Volumn 388, Issue 1-2, 2008, Pages 123-129

  Sugano, Mitsutoshi ^a   Yamauchi, Kazuyoshi ^a   Kawasaki, Kenji ^a   Tozuka, Minoru ^b   Fujita, Kiyotaka ^c   Okumura, Nobuo ^c   Ota, Hiroyoshi ^c  

^a SHINSHU UNIVERSITY HOSPITAL   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c SHINSHU UNIVERSITY   (Japan)

Author keywords

Alzheimer's disease; Apolipoprotein E; Cerebrospinal fluid; Senile plaque; Sialic acid; Surface plasmon resonance assay

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; APOLIPOPROTEIN E3; LIPOSOME; SIALIC ACID; THREONINE;

ALZHEIMER DISEASE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN PROCESSING; SURFACE PLASMON RESONANCE;

AMYLOID BETA-PROTEIN; APOLIPOPROTEIN E3; CELL LINE; HUMANS; KINETICS; LIPOSOMES; MUTATION; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; PEPTIDE FRAGMENTS; PROTEIN BINDING; SURFACE PLASMON RESONANCE; THREONINE;

EID: 37249063936     PISSN: 00098981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cca.2007.10.024     Document Type: Article

References (48)

1. Mahley R.W. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240 (1988) 622-630
2. Beisiegel U., Weber W., Ihrke G., Herz J., and Stanley K.K. The LDL-receptor-related protein, LRP, is an apolipoprotein E-binding protein. Nature 341 (1989) 162-164
3. Elshourbagy N.A., Liao W.S., Mahley R.W., and Taylor J.M. Apolipoprotein E mRNA is abundant in the brain and adrenals, as well as in the liver, and is present in other peripheral tissues of rats and marmosets. Proc Natl Acad Sci U S A 82 (1985) 203-207
4. Boyles J.K., Pitas R.E., Wilson E., Mahley R.W., and Taylor J.M. Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. J Clin Invest 76 (1985) 1501-1513
5. Pitas R.E., Boyles J.K., Lee S.H., Hui D., and Weisgraber K.H. Lipoproteins and their receptors in the central nervous system. Characterization of the lipoproteins in cerebrospinal fluid and identification of apolipoprotein B, E(LDL) receptors in the brain. J Biol Chem 262 (1987) 14352-14360
6. Pitas R.E., Boyles J.K., Lee S.H., Foss D., and Mahley R.W. Astrocytes synthesize apolipoprotein E and metabolize apolipoprotein E-containing lipoproteins. Biochim Biophys Acta 917 (1987) 148-161
7. Roheim P.S., Carey M., Forte T., and Vega G.L. Apolipoproteins in human cerebrospinal fluid. Proc Natl Acad Sci U S A 76 (1979) 4646-4649
8. Miida T., Yamazaki F., Sakurai M., et al. The apolipoprotein E content of HDL in cerebrospinal fluid is higher in children than in adults. Clin Chem 45 (1999) 1294-1296
9. Yamauchi K., Tozuka M., Hidaka H., Hidaka E., Kondo Y., and Katsuyama T. Characterization of apolipoprotein E-containing lipoproteins in cerebrospinal fluid: effect of phenotype on the distribution of apolipoprotein E. Clin Chem 45 (1999) 1431-1438
10. Namba Y., Tomonaga M., Kawasaki H., Otomo E., and Ikeda K. 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 (1991) 163-166
11. Wisniewski T., and Frangione B. Apolipoprotein E: a pathological chaperone protein in patients with cerebral and systemic amyloid. Neurosci Lett 135 (1992) 235-238
12. MacRaild C.A., Stewart C.R., Mok Y.F., et al. Non-fibrillar components of amyloid deposits mediate the self-association and tangling of amyloid fibrils. J Biol Chem 279 (2004) 21038-21045
13. Gunzburg MJ, Perugini MA, Howlett GJ. Structural basis for the recognition and cross-linking of amyloid fibrils by human apolipoprotein E. J Biol Chem 2007 in press.
14. Saunders A.M., Strittmatter W.J., Schmechel D., et al. Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer's disease. Neurology 43 (1993) 1467-1472
15. Strittmatter W.J., Saunders A.M., Schmechel D., et al. Apolipoprotein E: high-avidity binding to β-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc Natl Acad Sci U S A 90 (1993) 1977-1981
16. Corder E.H., Saunders A.M., Strittmatter W.J., et al. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261 (1993) 921-923
17. Wang B., Jin F., Yang Z., et al. The insertion polymorphism in angiotensin-converting enzyme gene associated with the APOE epsilon 4 allele increases the risk of late-onset Alzheimer disease. J Mol Neurosci 30 (2006) 267-271
18. Levi O., and Michaelson D.M. Environmental enrichment stimulates neurogenesis in apolipoprotein E3 and neuronal apoptosis in apolipoprotein E4 transgenic mice. J Neurochem 100 (2007) 202-210
19. LaDu M.J., Falduto M.T., Manelli A.M., Reardon C.A., Getz G.S., and Frail D.E. Isoform-specific binding of apolipoprotein E to β-amyloid. J Biol Chem 269 (1994) 23403-23406
20. LaDu M.J., Pederson T.M., Frail D.E., Reardon C.A., Getz G.S., and Falduto M.T. Purification of apolipoprotein E attenuates isoform-specific binding to β-amyloid. J Biol Chem 270 (1995) 9039-9042
21. Tokuda T., Calero M., Matsubara E., et al. Lipidation of apolipoprotein E influences its isoform-specific interaction with Alzheimer's amyloid β peptides. Biochem J 348 (2000) 359-365
22. Munson G.W., Roher A.E., Kuo Y.M., et al. SDS-stable complex formation between native apolipoprotein E3 and β-amyloid peptides. Biochemistry 39 (2000) 16119-16124
23. Bentley N.M., Ladu M.J., Rajan C., Getz G.S., and Reardon C.A. Apolipoprotein E structural requirements for the formation of SDS-stable complexes with β-amyloid-(1-40): the role of salt bridges. Biochem J 366 (2002) 273-279
24. Morikawa M., Fryer J.D., Sullivan P.M., et al. Production and characterization of astrocyte-derived human apolipoprotein E isoforms from immortalized astrocytes and their interactions with amyloid-β. Neurobiol Dis 19 (2005) 66-76
25. Malek G., Johnson L.V., Mace B.E., et al. Apolipoprotein E allele-dependent pathogenesis: a model for age-related retinal degeneration. Proc Natl Acad Sci U S A 102 (2005) 11900-11905
26. Manelli A.M., Bulfinch L.C., Sullivan P.M., and LaDu M.J. Aβ42 neurotoxicity in primary co-cultures: effect of apoE isoform and Aβ conformation. Neurobiol Aging 28 (2007) 1139-1147
27. Zannis V.I., Kurnit D.M., and Breslow J.L. Hepatic apo-A-I and apo-E and intestinal apo-A-I are synthesized in precursor isoprotein forms by organ cultures of human fetal tissues. J Biol Chem 257 (1982) 536-544
28. Zannis V.I., Breslow J.L., SanGiacomo T.R., Aden D.P., and Knowles B.B. Characterization of the major apolipoproteins secreted by two human hepatoma cell lines. Biochemistry 20 (1981) 7089-7096
29. Zannis V.I., McPherson J., Goldberger G., Karathanasis S.K., and Breslow J.L. Synthesis, intracellular processing, and signal peptide of human apolipoprotein E. J Biol Chem 259 (1984) 5495-5499
30. Zanni E.E., Kouvatsi A., Hadzopoulou-Cladaras M., Krieger M., and Zannis V.I. Expression of ApoE gene in Chinese hamster cells with a reversible defect in O-glycosylation. Glycosylation is not required for apoE secretion. J Biol Chem 264 (1989) 9137-9140
31. Wernette-Hammond M.E., Lauer S.J., Corsini A., Walker D., Taylor J.M., and Rall Jr. S.C. Glycosylation of human apolipoprotein E. The carbohydrate attachment site is threonine 194. J Biol Chem 264 (1989) 9094-9101
32. Schauer R. Sialic acids as antigenic determinants of complex carbohydrates. Adv Exp Med Biol 228 (1988) 47-72
33. Varki A. Sialic acids as ligands in recognition phenomena. FASEB J 11 (1997) 248-255
34. Munday J., Floyd H., and Crocker P.R. Sialic acid binding receptors (siglecs) expressed by macrophages. J Leukoc Biol 66 (1999) 705-711
35. Keppler O.T., Horstkorte R., Pawlita M., Schmidt C., and Reutter W. Biochemical engineering of the N-acyl side chain of sialic acid: biological implications. Glycobiology 11 (2001) 11R-18R
36. Kannagi R. Regulatory roles of carbohydrate ligands for selectins in the homing of lymphocytes. Curr Opin Struct Biol 12 (2002) 599-608
37. Crocker P.R. Siglecs: sialic-acid-binding immunoglobulin-like lectins in cell-cell interactions and signalling. Curr Opin Struct Biol 12 (2002) 609-615
38. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
39. Yamauchi K., Tozuka M., Nakabayashi T., et al. Higher avidity binding of apolipoprotein (E-AII) complex than of apolipoprotein E monomer to β-amyloid. J Neurosci Res 58 (1999) 301-307
40. Yamauchi K., Tozuka M., Nakabayashi T., et al. Apolipoprotein E in cerebrospinal fluid: relation to phenotype and plasma apolipoprotein E concentrations. Clin Chem 45 (1999) 497-504
41. Siest G., and Shuvaev V.V. Interaction between human amphipathic apolipoproteins and amyloid β-peptide: surface plasmon resonance studies. FEBS Lett 383 (1996) 9-12
42. LaDu M.J., Stine Jr. W.B., Narita M., Getz G.S., Reardon C.A., and Bu G. Self-assembly of HEK cell-secreted ApoE particles resembles ApoE enrichment of lipoproteins as a ligand for the LDL receptor-related protein. Biochemistry 45 (2006) 381-390
43. Shuvaev V.V., and Siest G. Heparin specifically inhibits binding of apolipoprotein E to amyloid β-peptide. Neurosci Lett 280 (2000) 131-134
44. Baumann M.H., Kallijärvi J., Lankinen H., Soto C., and Haltia M. Apolipoprotein E includes a binding site which is recognized by several amyloidogenic polypeptides. Biochem J 349 (2000) 77-84
45. Ladu M.J., Reardon C., Van Eldik L., et al. Lipoproteins in the central nervous system. Ann N Y Acad Sci 903 (2000) 167-175
46. Hiesberger T., Trommsdorff M., Howell B.W., et al. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24 (1999) 481-489
47. Cooper J.A., and Howell B.W. Lipoprotein receptors: signaling functions in the brain?. Cell 97 (1999) 671-674
48. Michikawa M. Cholesterol paradox: is high total or low HDL cholesterol level a risk for Alzheimer's disease?. J Neurosci Res 72 (2003) 141-146