Non-toxic amyloid beta formed in the presence of glypican-1 or its deaminatively generated heparan sulfate degradation products

Glycobiology

Volumn 23, Issue 12, 2013, Pages 1510-1519

  Cheng, Fang ^a   Ruscher, Karsten ^b   Fransson, Lars Åke ^a   Mani, Katrin ^a  

^a LUND UNIVERSITY   (Sweden)

^b Laboratory for Experimental Brain Research   (Sweden)

Author keywords

Amyloid beta; Glypican 1; Heparan sulfate; Oligomerization; Toxicity

Indexed keywords

A11 ANTIBODY; AMYLOID BETA PROTEIN ANTIBODY; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; GLYPICAN 1; HEPARAN SULFATE; OLIGOMER; OLIGOSACCHARIDE; PROTEOGLYCAN; UNCLASSIFIED DRUG; AMYLOID BETA PROTEIN; GLYPICAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG DEGRADATION; IMMUNOREACTIVITY; MOUSE; NEUROBLASTOMA CELL; NEUROTOXICITY; NONHUMAN; OLIGOMERIZATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN MULTIMERIZATION; RAT; TUMOR GROWTH; ANIMAL; BIOSYNTHESIS; BRAIN CORTEX; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DEAMINATION; DRUG EFFECTS; HUMAN; METABOLISM; NERVE CELL; NEUROBLASTOMA; PATHOLOGY; TOXICITY; WISTAR RAT;

AMYLOID BETA-PEPTIDES; ANIMALS; CELL SURVIVAL; CEREBRAL CORTEX; DEAMINATION; GLYPICANS; HEPARITIN SULFATE; HUMANS; MICE; NEUROBLASTOMA; NEURONS; RATS; RATS, WISTAR;

EID: 84887975783     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwt079     Document Type: Article

References (53)

1. Abramov E, Dolev I, Fogel H., Ciccotosto GD, Ruff E, Slutsky I. 2009. Amyloid-β as a positive endogenous regulator of release probability at hippo-campal synapses. Nat Neurosci. 12:1567-1576.
2. Benilova I, Karran E, De Strooper B. 2012. The toxic Aβ oligomer and Alzheimer's disease: An emperor in need of clothes. Nat Neurosci. 15:1-9.
3. Cappai R, Cheng F, Ciccotosto G.D., Needham BE, Masters CL, Multhaup G, Fransson L-Å, Mani K. 2005. The amyloid precursor protein (APP) of Alzheimer disease and its paralog, APLP2, modulate the Cu/Zn-nitric oxide-catalyzed degradation of glypican-1 heparan sulfate in vivo. J Biol Chem. 280:13913-13920.
4. Cheng F, Cappai R, Ciccotosto G.D., Svensson G., Multhaup G, Fransson L-Å, Mani K. 2011. Suppression of amyloid β A11 antibody immunoreactivity by vitamin C. Possible role of heparan sulfate oligosaccharides derived from glypican-1 by ascorbate-induced, nitric oxide (NO)-catalyzed degradation. J Biol Chem. 286:27559-27572.
5. Cheng F, Johnsson R, Nilsson J., Fransson L-Å, Ellervik U, Mani K. 2009. Potentiation of naphthoxyloside cytotoxicity on human tumor cells by difluoro-methylornithine and spermine-NONOate. Cancer Lett. 273:148-154.
6. Cheng F, Mani K, van den Born J, Ding K, Belting M, Fransson L-Å. 2002. Nitric oxide-dependent processing of heparan sulfate in recycling S-nitrosylated glypican-1 takes place in caveolin-1 containing endosomes. J Biol Chem. 277:44431-44439.
7. Cheng F, Petersson P, Arroyo-Yanguas Y, Westergren-Thorsson G. 2001. Differences in uptake and nuclear localization of anti-proliferative heparan sulfate between human lung fibroblasts and human lung carcinoma cells. J Cell Biochem. 83:597-606.
8. Cheng F, Svensson G, Fransson L-Å, Mani K. 2012. Non-conserved, S-nitrosylated cysteines in glypican-1 react with N-unsubstituted glucosa-mines in heparan sulfate and catalyze deaminative cleavage. Glycobiology. 22:1480-1486.
9. Ding K, Mani K, Cheng F., Belting M, Fransson L-Å. 2002. Copper-dependent autocleavage of glypican-1 heparan sulfate by nitric oxide derived from intrinsic nitrosothiols. J Biol Chem. 277:33353-33360.
10. Ding K, Sandgren S, Mani K., Belting M, Fransson L-Å. 2001. Modulations of glypican-1 heparan sulfate by inhibition of endogenous polyamine synthesis. Mapping of spermine-binding sites and heparanase, heparin lyase and nitric oxide/nitrite cleavage sites. J Biol Chem. 276:46779-46791.
11. Fedarko NS, Conrad HE 1986. A unique heparan sulfate in the nuclei of hepatocytes: Structural changes with the growth state of the cells. J Cell Biol. 102:587-599.
12. Fransson L-Å, Belting M, Cheng F, Jönsson M, Mani K, Sandgren S. 2004. Novel aspects of glypican glycobiology. Cell Mol Life Sci. 61:1016-1024.
13. Fransson L-Å, Sjöberg I, Havsmark B. 1980. Structural studies on heparan sulfates. Characterization of oligosaccharides obtained by periodate oxidation and alkaline elimination. Eur J Biochem. 106:59-69.
14. Giulian D, Haverkamp LJ, Yu J, Karshin W., Tom D, Kazanskaia A, Kirkpatrick J., Roher AE 1998. The HHQK domain of beta-amyloid provides a structural basis for the immunopathology of Alzheimer's disease. J Biol Chem. 273:29719-29726.
15. Glabe CG. 2008. Structural classification of toxic amyloid aggregates. J Biol Chem. 283:29639-29643.
16. Gouras GK, Willén K, Tampellini D. 2012. Critical role of intraneuronal Aβ in Alzheimer's disease: Technical challenges in studying intracellular Aβ. Life Sci. 91:1153-1158.
17. Hu X, Crick SL, Bu G, Frieden C., Pappu RH, Lee J-M. 2009. Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-beta peptide. Proc Natl Acad Sci USA. 106:20324-20329.
18. Ishihara M, Fedarko NS, Conrad HE 1986. Transport of heparan sulfate into the nuclei of hepatocytes. J Biol Chem. 261:13575-13580.
19. Jin L-W, Maezawa I., Vincent I, Bird T. 2004. Intracellular accumulation of amyloidogenic fragments of amyloid-β precursor protein in neurons with Niemann-Pick type C defects is associated with endosomal abnormalities. Amer J Pathol. 164:975-985.
20. Kagan BL. 2012. Membrane pores in the pathogenesis of neurodegenerative disease. Proc Mol Biol Transl Sci. 107:295-325.
21. Kanekiyo T, Bu G. 2009. Receptor-associated protein interacts with amyloid-β peptide and promotes its cellular uptake. J Biol Chem. 284:33352-33359.
22. 40 ratio. EMBO J. 29:3408-3420.
23. Ladiwala ARA, Lin JC, Bale S.S., Marcelino-Cruz AM, Bhattacharaya M, Dordick J.S., Tessier PM 2010. Resveratrol selectively remodels soluble oligomers and fibrils of amyloid Aβ into off-pathway conformers. J Biol Chem. 285:24228-24237.
24. Larson ME, Lesné SE. 2012. Soluble Aβ oligomer production and toxicity. J Neurochem. 120(Suppl. 1):125-139.
25. Mani K, Belting M, Ellervik U., Falk N, Svensson G, Sandgren S., Cheng F, Fransson L-Å. 2004. Tumor attenuation by 2(6-hydroxynaphthyl)-β-D- xylopyranoside requires priming of heparan sulfate and nuclear targeting of the product. Glycobiology. 14:387-397.
26. Mani K, Cheng F, Fransson L-Å. 2006a. Defective NO-dependent, deaminative cleavage of glypican-1 heparan sulfate in Niemann-Pick C1 fibroblasts. Glycobiology. 16:711-718.
27. Mani K, Cheng F, Fransson L-Å. 2006b. Constitutive and vitamin C-induced, NO-catalyzed release of heparan sulfate from recycling glypican-1 in late endosomes. Glycobiology. 16:1251-1261.
28. Mani K, Cheng F, Fransson L-Å. 2007. Heparan sulfate degradation products can associate with oxidized proteins and proteasomes. J Biol Chem. 282:21934-21944.
29. Mani K, Cheng F, Havsmark B., Jönsson M, Belting M., Fransson L-Å. 2003. Prion, amyloid-β-derived Cu(II) ions or free Zn(II) ions support S-nitroso-dependent autocleavage of glypican-1 heparan sulfate. J Biol Chem. 278:38956-38965.
30. Mani K, Cheng F, Sandgren S., van den Born J, Havsmark B, Ding K, Fransson L-Å. 2004. The heparan sulfate-specific epitope 10E4 is NO-sensitive and partly inaccessible in glypican-1. Glycobiology. 14:599-607.
31. McLaurin J, Franklin T, Zhang X., Deng J, Fraser PE 1999. Interactions of amyloid-beta peptides with glycosaminoglycans: Effects on fibril nucleation and growth. Eur J Biochem. 266:1101-1110.
32. Nilsson U, Johnsson R, Fransson L-Å, Ellervik U, Mani K. 2010. Attenuation of tumor growth by formation of antiproliferative glycosaminoglycans correlates with low acetylation of histone H3. Cancer Res. 70:3771-3779.
33. O'Brien R.J., Wong PC 2011. Amyloid precursor protein and Alzheimer's disease. Annu Rev Neurosci. 34:185-204.
34. Ohmi K, Zhao HZ, Neufeld EF 2011. Defects in the medial entorhinal cortex and dentate gyrus in the mouse model of Sanfilippo syndrome type B. PLoS One. 6:e27461.
35. 40 ratios in Alzheimers disease. J Biol Chem. 287:5650-5660.
36. Puzzo D, Privitera L, Fá M, Staniszewska A, Hashimoto G, Aziz F, Sakurai M, Ribe EM, Troy CM, Mercken M, et al. 2011. Endogenous amyloid-β is necessary for hippocampal synaptic plasticity and memory. Ann Neurol. 69:819-830.
37. Querfurth HW, LaFerla FM 2010. Alzheimer's disease. N Engl J Med. 362:329-344.
38. Regberg J, Eriksson JN, Langel U. 2013. Cell-penetrating peptides: From cell cultures to in vivo applications. Front Biosci. 5:509-516.
39. Reinhard C, Hébert S, De Strooper B. 2005. The amyloid-β precursor protein: Integrating structure with biological function. EMBO J. 24:3996-4006.
40. Ruscher K, Fernandes E, Capela J.P., Bastos ML, Wieloch T, Dirnagl U, Meisel A., Carvalho F. 2011. Effect of 3,4-methylenedioxyamphetamine on dendritic spine dynamics in rat neocortical neurons-involvement of heat shock protein 27. Brain Res. 1370:43-52.
41. Sandgren S, Wittrup A, Cheng F., Jönsson M, Eklund E., Busch S, Belting M. 2004. The human antimicrobial peptide LL-37 transfers extracellular DNA plasmids to the nuclear compartment of mammalian cells via lipid rafts and proteoglycan-dependent endocytosis. J Biol Chem. 279:17951-17956.
42. Sandwall E, O'Callaghan P, Zhang X, Lindahl U., Lannfelt L, Li J-P. 2010. Heparan sulfate mediates amyloid-beta internalization and cytotoxicity. Glycobiology. 20:533-541.
43. Senechal Y, Kelly PH, Cryan J.F., Natt F., Dev KK 2007. Amyloid precursor protein knockdown by siRNA impairs spontaneous alternation in adult mice. J Neurochem. 102:1928-1940.
44. Svensson G, Awad W, Håkansson M, Mani K., Logan DT 2012. Crystal structure of N-glycosylated human glypican-1 core protein: Structure of two loops evolutionally conserved in vertebrate glypican-1. J Biol Chem. 287:14040-14051.
45. Svensson G, Linse S, Mani K. 2009. Chemical and thermal unfolding of glypican-1: Effect of heparan sulfate against heat-induced irreversible aggregation. Biochemistry. 48:9994-10004.
46. Svensson G, Mani K. 2009. S-nitrosylation of secreted recombinant human glypican-1. Glycoconj J. 26:1247-1257.
47. Takahashi RH, Almeida CG, Kearney P.F., Yu F., Lin MT, Milner TA, Gouras GK 2004. Oligomerization of Alzheimer's beta-amyloid within processes and synapses of cultured neurons and brain. J Neurosci. 24: 3592-3599.
48. Teich AF, Arancio O. 2012. Is the amyloid hypothesis of Alzheimer's disease therapeutically relevant? Biochem J. 446:165-177.
49. Thinakaran G, Koo EH 2008. APP Trafficking, processing and function. J Biol Chem. 283:29615-29619.
50. Umeda T, Tomiyama T, Sakama N., Tanaka S, Lambert MP, Klein W.L., Mori H. 2011. Intraneuronal amyloid oligomers cause cell death via endoplasmic reticulum stress, endosomal/lysosomal leakage, and mitochondrial dysfunction in vivo. J Neurosci Res. 89:1031-1042.
51. Walsh DM, Minogue AM, Sala Frigerio C, Fadeeva JV, Wasco W, Selkoe DJ 2007. The APP family of proteins: Similarities and differences. Biochem Soc Trans. 35:416-420.
52. Watanabe N, Araki W, Chui D.H., Makifuchi T., Ihara Y, Tabira T. 2004. Glypican-1 as an Abeta binding HSPG in the human brain: Its localization in DIG domains and possible roles in the pathogenesis of Alzheimer's disease. FASEB J. 18:1013-1015.
53. Williamson TG, Mok SS, Henry A, Cappai R., Lander AD, Nurcombe V, Beyreuther K, Masters C.L., Small DH 1996. Secreted glypican binds to the amyloid precursor protein of Alzheimer's disease (APP) and inhibits APP-induced neurite outgrowth. J Biol Chem. 271:31215-31221.