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Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Research Article

Amyloid β Binds to Albumin-Associated Lrp-Like Plasma O-Glycoproteins: Albumin Prevents Inhibition of Binding by LDL

Author(s): Sreedevi Karthi, K. C. Sumitha, Mandagini Geetha and Padinjaradath S. Appukuttan*

Volume 26, Issue 11, 2019

Page: [869 - 878] Pages: 10

DOI: 10.2174/0929866526666190722151027

Price: $65

Abstract

Background: Albumin was reported to engage nearly 95% of plasma Amyloid β (Aβ) and to reverse Aβ fibril formation in brain.

Objective: Since O-glycosylated LRP family of receptors capture Aβ in brain we compared Aβ binding to electrophoretically purified albumin and to O-glycoproteins AOP1 and AOP2 that adhere noncovalently to plasma albumin.

Methods: Strength of Aβ-protein interaction was measured as fluorescence increase in Fluorescentlabeled Aβ (F-Aβ) resulting from conformational changes. Alternatively, differential segregation of free and protein-bound Aβ in Density Gradient Ultracentrifugation (DGUC) was also examined.

Results: Fluorescence enhancement in F-Aβ was significantly greater by AOP1 and AOP2 than by known Aβ reactants α -synuclein and β -cyclodextrin, but nil by albumin. In DGUC Aβ migrated with the O-glycoproteins but not with albumin. Free O-glycoproteins unlike their albumin-bound forms were blocked by LDL from capturing F-Aβ. Associated albumin did not affect Aβ binding of O-glycoproteins. De-O-glycosylation of AOP1/AOP2 enhanced their Aβ binding showing that peptide sequences at O-glycosylated regions were recognized by Aβ. Unlike albumin, AOP1 and AOP2 were immunologically cross-reactive with LRP. Albumin sample used earlier to report albumin-Aβ interaction contained two O-glycoproteins cross-reactive with human LRP and equal in size to human AOP1 or AOP2.

Conclusion: Unlike albumin, albumin-bound O-glycoproteins, immunologically cross-reactive with LRP, bind plasma Aβ. These O-glycoproteins are potential anti-amyloidogenic therapeutics if they inhibit Aβ aggregation as other Aβ reactants do. Circulating immune complexes of albuminbound O-glycoproteins with O-glycoprotein-specific natural antibodies can bind further to LRP-like membrane proteins and are possible O-glycoprotein transporters to tissues.

Keywords: Anti-α-galactoside antibody, anti-β-glucoside antibody, albumin-associated-O-glycosylated protein, amyloid β, serine- and threonine-rich peptide sequence, LRP.

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[1]
Biere, A.L.; Ostaszewski, B.; Stimson, E.R.; Hyman, B.T.; Maggio, J.E.; Selkoe, D.J. Amyloid β-peptide is transported on lipoproteins and albumin in human plasma. J. Biol. Chem., 1996, 271(51), 32916-32922.
[http://dx.doi.org/10.1074/jbc.271.51.32916] [PMID: 8955133]
[2]
Karthi, S.; Sabarinath, P.S.; Geetha, M.; Appukuttan, P.S. Anti-α-galactoside and anti-β-glucoside antibodies are partially occupied by either of two albumin-bound O-glycoproteins and circulate as ligand-binding triplets. Immunol. Invest., 2019, 48(3), 222-241.
[http://dx.doi.org/10.1080/08820139.2018.1502299] [PMID: 30081721]
[3]
Geetha, M.; Kalaivani, V.; Sabarinath, P.S.; Appukuttan, P.S. Plasma anti-α-galactoside antibody binds to serine- and threonine-rich peptide sequence of apo(a) subunit in Lp(a). Glycoconj. J., 2014, 31(4), 289-298.
[http://dx.doi.org/10.1007/s10719-014-9521-2] [PMID: 24723206]
[4]
Sandrin, M.S.; Vaughan, H.A.; Xing, P.X.; McKenzie, I.F. Natural human anti-Gal alpha(1,3)Gal antibodies react with human mucin peptides. Glycoconj. J., 1997, 14(1), 97-105.
[http://dx.doi.org/10.1023/A:1018521217276] [PMID: 9076519]
[5]
Kanekiyo, T.; Bu, G. The low-density lipoprotein receptor-related protein 1 and amyloid-β clearance in Alzheimer’s disease. Front. Aging Neurosci., 2014, 6, 93.
[http://dx.doi.org/10.3389/fnagi.2014.00093] [PMID: 24904407]
[6]
Geetha, M.; Annamma, K.I.; Mathai, J.; Appukuttan, P.S. Normal human plasma anti-β-glucoside antibody has markedly elevated IgA content and binds fungal and yeast polysaccharides. Immunol. Invest., 2007, 36(1), 73-83.
[http://dx.doi.org/10.1080/08820130600745737] [PMID: 17190651]
[7]
Jaison, P.L.; Appukuttan, P.S. Rapid isolation of human plasma anti-alpha-galactoside antibody using sugar-specific binding to guar galactomannan or agarose. Indian J. Biochem. Biophys., 1992, 29(3), 266-270.
[PMID: 1512012]
[8]
Heyderman, E.; Strudly, K.; Richardson, T.C. Immunohisto-chemistry in Pathology. In: Handbook. Of Experimental Immunology; Weir, D.M.; Herzenberg, L.A., Eds.; Blackwell Scientific Publications, Ltd: Hoboken, New Jersey, 1986, pp. 12910-12927.
[9]
Towbin, H.; Staehelin, T.; Gordon, J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA, 1979, 76(9), 4350-4354.
[http://dx.doi.org/10.1073/pnas.76.9.4350] [PMID: 388439]
[10]
Camilleri, P.; Haskins, N.J.; Howlett, D.R. beta-Cyclodextrin interacts with the Alzheimer amyloid beta-A4 peptide. FEBS Lett., 1994, 341(2-3), 256-258.
[http://dx.doi.org/10.1016/0014-5793(94)80467-2] [PMID: 7907994]
[11]
Jensen, P.H.; Hojrup, P.; Hager, H.; Nielsen, M.S.; Jacobsen, L.; Olesen, O.F.; Gliemann, J.; Jakes, R. Binding of Abeta to α- and β-synucleins: identification of segments in α-synuclein/NAC precursor that bind Abeta and NAC. Biochem. J., 1997, 323(Pt 2), 539-546.
[http://dx.doi.org/10.1042/bj3230539] [PMID: 9163350]
[12]
Becker, L.; Cook, P.M.; Wright, T.G.; Koschinsky, M.L. Quantitative evaluation of the contribution of weak lysine-binding sites present within apolipoprotein(a) kringle IV types 6-8 to lipoprotein(a) assembly. J. Biol. Chem., 2004, 279(4), 2679-2688.
[http://dx.doi.org/10.1074/jbc.M309414200] [PMID: 14581473]
[13]
Sureshkumar, G.; Appukuttan, P.S.; Basu, D. α-Galactose-specific lectin from jack fruit seeds (Artocarpus integrifolia). J. Biosci., 1982, 4, 257-261.
[http://dx.doi.org/10.1007/BF02702736]
[14]
Bachhuber, T.; Katzmarski, N.; McCarter, J.F.; Loreth, D.; Tahirovic, S.; Kamp, F.; Abou-Ajram, C.; Nuscher, B.; Serrano-Pozo, A.; Müller, A.; Prinz, M.; Steiner, H.; Hyman, B.T.; Haass, C.; Meyer-Luehmann, M. Inhibition of amyloid-β plaque formation by α-synuclein. Nat. Med., 2015, 21(7), 802-807.
[http://dx.doi.org/10.1038/nm.3885] [PMID: 26099047]
[15]
Pedersen, N.B.; Wang, S.; Narimatsu, Y.; Yang, Z.; Halim, A.; Schjoldager, K.T-B.G.; Madsen, T.D.; Seidah, N.G.; Bennett, E.P.; Levery, S.B.; Clausen, H. Low density lipoprotein receptor class A repeats are O-glycosylated in linker regions. J. Biol. Chem., 2014, 289(25), 17312-17324.
[http://dx.doi.org/10.1074/jbc.M113.545053] [PMID: 24798328]
[16]
Yamamoto, K.; Shimada, H.; Koh, H.; Ataka, S.; Miki, T. Serum levels of albumin-amyloid beta complexes are decreased in Alzheimer’s disease. Geriatr. Gerontol. Int., 2014, 14(3), 716-723.
[http://dx.doi.org/10.1111/ggi.12147] [PMID: 24020590]
[17]
Andrianantoandro, E. Inducing conformational change in the ligand. Sci. Signal., 2012, 5(236)ec207
[http://dx.doi.org/10.1126/Sciesignal.2003473]
[18]
Lee, Y.C. Fluorescence spectrometry in studies of carbohydrate-protein interactions. J. Biochem., 1997, 121(5), 818-825.
[http://dx.doi.org/10.1093/oxfordjournals.jbchem.a021658] [PMID: 9192718]
[19]
Sridharan, R.; Zuber, J.; Connelly, S.M.; Mathew, E.; Dumont, M.E. Fluorescent approaches for understanding interactions of ligands with G protein coupled receptors. Biochim. Biophys. Acta, 2014, 1838(1 Pt A), 15-33.
[http://dx.doi.org/10.1016/j.bbamem.2013.09.005] [PMID: 24055822]
[20]
George, G.; Chellappan, S.K.; Geetha, M.; Appukuttan, P.S. Possible molecular basis for macromolecular antigen attachment to host cells: their immune complex with plasma antibodies have unoccupied binding sites enabling binding to smaller ligands. AIMS Mol. Sci., 2017, 4, 91-102.
[http://dx.doi.org/10.3934/molsci.2017.1.91]
[21]
Zhang, X.; Tian, Y.; Zhang, C.; Tian, X.; Ross, A.W.; Moir, R.D.; Sun, H.; Tanzi, R.E.; Moore, A.; Ran, C. Near-infrared fluorescence molecular imaging of amyloid β species and monitoring therapy in animal models of Alzheimer’s disease. Proc. Natl. Acad. Sci. USA, 2015, 112(31), 9734-9739.
[http://dx.doi.org/10.1073/pnas.1505420112] [PMID: 26199414]
[22]
Ryan, T.M.; Caine, J.; Mertens, H.D.T.; Kirby, N.; Nigro, J.; Breheney, K.; Waddington, L.J.; Streltsov, V.A.; Curtain, C.; Masters, C.L.; Roberts, B.R. Ammonium hydroxide treatment of Aβ produces an aggregate free solution suitable for biophysical and cell culture characterization. Peer J., 2013, 1e73
[http://dx.doi.org/10.7717/peerj.73] [PMID: 23678397]
[23]
Stanyon, H.F.; Viles, J.H. Human serum albumin can regulate amyloid-β peptide fiber growth in the brain interstitium: implications for Alzheimer disease. J. Biol. Chem., 2012, 287(33), 28163-28168.
[http://dx.doi.org/10.1074/jbc.C112.360800] [PMID: 22718756]
[24]
Herzog, B.H.; Fu, J.; Xia, L. Mucin-type O-glycosylation is critical for vascular integrity. Glycobiology, 2014, 24(12), 1237-1241.
[http://dx.doi.org/10.1093/glycob/cwu058] [PMID: 24946788]
[25]
Johanson, C.; Flaherty, S.; Messier, A.; Duncan, J.; Silverberg, G. Expression of the beta-amyloid transporter, LRP-1, in aging choroid plexus: implications for the CSF-brain system in NPH and Alzheimer’s disease. Cerebrospinal Fluid Res., 2006, 3, S29.
[http://dx.doi.org/10.1186/1743-8454-3-S1-S29]
[26]
Bitel, C.L.; Kasinathan, C.; Kaswala, R.H.; Klein, W.L.; Frederikse, P.H. Amyloid-β and tau pathology of Alzheimer’s disease induced by diabetes in a rabbit animal model. J. Alzheimers Dis., 2012, 32(2), 291-305.
[http://dx.doi.org/10.3233/JAD-2012-120571] [PMID: 22785400]
[27]
Yaffe, K.; Blackwell, T.; Kanaya, A.M.; Davidowitz, N.; Barrett-Connor, E.; Krueger, K. Diabetes, impaired fasting glucose, and development of cognitive impairment in older women. Neurology, 2004, 63(4), 658-663.
[http://dx.doi.org/10.1212/01.WNL.0000134666.64593.BA] [PMID: 15326238]
[28]
Nilsson, A.; Radeborg, K.; Björck, I. Effects on cognitive performance of modulating the postprandial blood glucose profile at breakfast. Eur. J. Clin. Nutr., 2012, 66(9), 1039-1043.
[http://dx.doi.org/10.1038/ejcn.2012.80] [PMID: 22781020]
[29]
Cutler, R.G.; Kelly, J.; Storie, K.; Pedersen, W.A.; Tammara, A.; Hatanpaa, K.; Troncoso, J.C.; Mattson, M.P. Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer’s disease. Proc. Natl. Acad. Sci. USA, 2004, 101(7), 2070-2075.
[http://dx.doi.org/10.1073/pnas.0305799101] [PMID: 14970312]
[30]
Llewellyn, D.J.; Langa, K.M.; Friedland, R.P.; Lang, I.A. Serum albumin concentration and cognitive impairment. Curr. Alzheimer Res., 2010, 7(1), 91-96.
[http://dx.doi.org/10.2174/156720510790274392] [PMID: 20205675]
[31]
Reed, B.; Villeneuve, S.; Mack, W.; DeCarli, C.; Chui, H.C.; Jagust, W. Associations between serum cholesterol levels and cerebral amyloidosis. JAMA Neurol., 2014, 71(2), 195-200.
[http://dx.doi.org/10.1001/jamaneurol.2013.5390] [PMID: 24378418]

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