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Glycosaminoglycans in Neurodegenerative Diseases

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The Role of Glycosylation in Health and Disease

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1325))

Abstract

Glycosaminoglycans (GAGs) are linear polysaccharides that consist of alternating disaccharides sequences of uronic acids and/or galactose hexamino sugars most of which are sulfated. GAGs are ubiquitously expressed on the cell surface, in the intracellular milieu and in the extracellular matrix of all animal cells. Thus, GAGs exhibit many essential roles in a variety of physiological and pathological processes. The targets of GAGs are GAG-binding proteins and related proteins that are of significant interest to both the academic community and in the pharmaceutical industry. In this review, the structures of GAGs, their binding proteins, and analogs are presented that further the development of GAGs and their analogs for the treatment of neurodegenerative diseases agents.

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References

  • Alavi Naini SM, Soussi-Yanicostas N (2018) Heparan sulfate as a therapeutic target in Tauopathies: insights from Zebrafish. Front Cell Dev Biol 6:163

    Article  PubMed  PubMed Central  Google Scholar 

  • Alberts B, Johnson A, Lewis J, Morgan D, Raff M, Roberts K et al (2015) Cell junctions and the extracellular matrix. In: Molecular biology of the cell. Garland Science, New York

    Google Scholar 

  • Alzheimer’s Association (2020) Alzheimer’s disease facts and figures (2020). Alzheimers Dement

    Google Scholar 

  • Ancsin JB (2003) Amyloidogenesis: historical and modern observations point to heparan sulfate proteoglycans as a major culprit. Amyloid 10(2):67–79

    Article  CAS  PubMed  Google Scholar 

  • Appel SH, Smith RG, Le WD (1996) Immune-mediated cell death in neurodegenerative disease. Adv Neurol 69:153–159

    CAS  PubMed  Google Scholar 

  • Arai H, Kashiwagi S, Nagasaka Y, Uchida K, Hoshii Y, Nakamura K (1999) Oxidative modification of apolipoprotein E in human very-low-density lipoprotein and its inhibition by glycosaminoglycans. Arch Biochem Biophys 367(1):1–8

    Article  CAS  PubMed  Google Scholar 

  • Ariga T, Miyatake T, Yu RK (2010) Role of proteoglycans and glycosaminoglycans in the pathogenesis of Alzheimer’s disease and related disorders: amyloidogenesis and therapeutic strategies – a review. J Neurosci Res 88(11):2303–2315

    Google Scholar 

  • Arlov O, Skjak-Braek G (2017) Sulfated alginates as heparin analogues: a review of chemical and functional properties. Molecules 22(5):778

    Article  PubMed Central  CAS  Google Scholar 

  • Avram S, Shaposhnikov S, Buiu C, Mernea M (2014) Chondroitin sulfate proteoglycans: structure-function relationship with implication in neural development and brain disorders. Biomed Res Int 2014:642798

    Article  PubMed  PubMed Central  Google Scholar 

  • Bame KJ, Danda J, Hassall A, Tumova S (1997) Abeta(1-40) prevents heparanase-catalyzed degradation of heparan sulfate glycosaminoglycans and proteoglycans in vitro. A role for heparan sulfate proteoglycan turnover in Alzheimer’s disease. J Biol Chem 272(27):17005–17011

    Article  CAS  PubMed  Google Scholar 

  • Barros CS, Franco SJ, Muller U (2011) Extracellular matrix: functions in the nervous system. Cold Spring Harb Perspect Biol 3(1):a005108

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bejoy J, Song L, Wang Z, Sang QX, Zhou Y, Li Y (2018) Neuroprotective activities of heparin, Heparinase III, and hyaluronic acid on the Abeta42-treated forebrain spheroids derived from human stem cells. ACS Biomater Sci Eng 4(8):2922–2933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bellucci C, Lilli C, Baroni T, Parnetti L, Sorbi S, Emiliani C et al (2007) Differences in extracellular matrix production and basic fibroblast growth factor response in skin fibroblasts from sporadic and familial Alzheimer’s disease. Mol Med 13(9–10):542–550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ben-Zaken O, Tzaban S, Tal Y, Horonchik L, Esko JD, Vlodavsky I et al (2003) Cellular heparan sulfate participates in the metabolism of prions. J Biol Chem 278(41):40041–40049

    Article  CAS  PubMed  Google Scholar 

  • Bergamaschini L, Rossi E, Vergani C, De Simoni MG (2009) Alzheimer’s disease: another target for heparin therapy. ScientificWorldJournal 9:891–908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernstein HG, Stricker R, Dobrowolny H, Steiner J, Bogerts B, Trubner K et al (2013) Nardilysin in human brain diseases: both friend and foe. Amino Acids 45(2):269–278

    Article  CAS  PubMed  Google Scholar 

  • Bullock SL, Fletcher JM, Beddington RS, Wilson VA (1998) Renal agenesis in mice homozygous for a gene trap mutation in the gene encoding heparan sulfate 2-sulfotransferase. Genes Dev 12(12):1894–1906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Capila I, Linhardt RJ (2002) Heparin-protein interactions. Angew Chem Int Ed Engl 41(3):391–412

    Article  PubMed  Google Scholar 

  • Carmen L, Maria V, Morales-Medina JC, Vallelunga A, Palmieri B, Iannitti T (2019) Role of proteoglycans and glycosaminoglycans in Duchenne muscular dystrophy. Glycobiology 29(2):110–123

    Article  CAS  PubMed  Google Scholar 

  • Carulli D, Laabs T, Geller HM, Fawcett JW (2005) Chondroitin sulfate proteoglycans in neural development and regeneration. Curr Opin Neurobiol 15(1):116–120

    Article  PubMed  CAS  Google Scholar 

  • Castillo GM, Ngo C, Cummings J, Wight TN, Snow AD (1997) Perlecan binds to the beta-amyloid proteins (A beta) of Alzheimer’s disease, accelerates A beta fibril formation, and maintains A beta fibril stability. J Neurochem 69(6):2452–2465

    Article  CAS  PubMed  Google Scholar 

  • Castillo GM, Cummings JA, Yang W, Judge ME, Sheardown MJ, Rimvall K et al (1998) Sulfate content and specific glycosaminoglycan backbone of perlecan are critical for perlecan’s enhancement of islet amyloid polypeptide (amylin) fibril formation. Diabetes 47(4):612–620

    Article  CAS  PubMed  Google Scholar 

  • Castillo GM, Lukito W, Wight TN, Snow AD (1999) The sulfate moieties of glycosaminoglycans are critical for the enhancement of beta-amyloid protein fibril formation. J Neurochem 72(4):1681–1687

    Article  CAS  PubMed  Google Scholar 

  • Celesia GG (1991) Alzheimer’s disease: the proteoglycans hypothesis. Semin Thromb Hemost 17(Suppl 2):158–160

    PubMed  Google Scholar 

  • Cescon M, Chen P, Castagnaro S, Gregorio I, Bonaldo P (2016) Lack of collagen VI promotes neurodegeneration by impairing autophagy and inducing apoptosis during aging. Aging (Albany NY) 8(5):1083–1101

    Article  CAS  Google Scholar 

  • Cheng F, Cappai R, Lidfeldt J, Belting M, Fransson LA, Mani K (2014) Amyloid precursor protein (APP)/APP-like protein 2 (APLP2) expression is required to initiate endosome-nucleus-autophagosome trafficking of glypican-1-derived heparan sulfate. J Biol Chem 289(30):20871–20878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christner JE, Distler JJ, Jourdian GW (1979) Biosynthesis of keratan sulfate: purification and properties of a galactosyltransferase from bovine cornea. Arch Biochem Biophys 192(2):548–558

    Article  CAS  PubMed  Google Scholar 

  • Cohlberg JA, Li J, Uversky VN, Fink AL (2002) Heparin and other glycosaminoglycans stimulate the formation of amyloid fibrils from alpha-synuclein in vitro. Biochemistry 41(5):1502–1511

    Article  CAS  PubMed  Google Scholar 

  • Collinge J (2016) Mammalian prions and their wider relevance in neurodegenerative diseases. Nature 539(7628):217–226

    Article  PubMed  Google Scholar 

  • Constantopoulos G, Dekaban AS (1975) Chemical definition of the mucopolysaccharidoses. Clin Chim Acta 59(3):321–336

    Article  CAS  PubMed  Google Scholar 

  • Coombe DR, Kett WC (2012) Heparin mimetics. Handb Exp Pharmacol 207:361–383

    Article  CAS  Google Scholar 

  • Corder EH, Saunders AM, Risch NJ, Strittmatter WJ, Schmechel DE, Gaskell PC Jr et al (1994) Protective effect of apolipoprotein E type 2 allele for late onset Alzheimer disease. Nat Genet 7(2):180–184

    Article  CAS  PubMed  Google Scholar 

  • Coria F, Castano E, Prelli F, Larrondo-Lillo M, van Duinen S, Shelanski ML et al (1988) Isolation and characterization of amyloid P component from Alzheimer’s disease and other types of cerebral amyloidosis. Lab Investig 58(4):454–458

    CAS  PubMed  Google Scholar 

  • Cotman SL, Halfter W, Cole GJ (2000) Agrin binds to beta-amyloid (Abeta), accelerates abeta fibril formation, and is localized to Abeta deposits in Alzheimer’s disease brain. Mol Cell Neurosci 15(2):183–198

    Article  CAS  PubMed  Google Scholar 

  • Cui H, Freeman C, Jacobson GA, Small DH (2013) Proteoglycans in the central nervous system: role in development, neural repair, and Alzheimer’s disease. IUBMB Life 65(2):108–120

    Article  CAS  PubMed  Google Scholar 

  • Danielsen B, Sorensen IJ, Nybo M, Nielsen EH, Kaplan B, Svehag SE (1997) Calcium-dependent and -independent binding of the pentraxin serum amyloid P component to glycosaminoglycans and amyloid proteins: enhanced binding at slightly acid pH. Biochim Biophys Acta 1339(1):73–78

    Article  CAS  PubMed  Google Scholar 

  • Dawkins E, Small DH (2014) Insights into the physiological function of the beta-amyloid precursor protein: beyond Alzheimer’s disease. J Neurochem 129(5):756–769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deepa SS, Umehara Y, Higashiyama S, Itoh N, Sugahara K (2002) Specific molecular interactions of oversulfated chondroitin sulfate E with various heparin-binding growth factors. Implications as a physiological binding partner in the brain and other tissues. J Biol Chem 277(46):43707–43716

    Article  CAS  PubMed  Google Scholar 

  • Djerbal L, Lortat-Jacob H, Kwok J (2017) Chondroitin sulfates and their binding molecules in the central nervous system. Glycoconj J 34(3):363–376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong J, Peters-Libeu CA, Weisgraber KH, Segelke BW, Rupp B, Capila I et al (2001) Interaction of the N-terminal domain of apolipoprotein E4 with heparin. Biochemistry 40(9):2826–2834

    Article  CAS  PubMed  Google Scholar 

  • Dudas B, Semeniken K (2012) Glycosaminoglycans and neuroprotection. Handb Exp Pharmacol 207:325–343

    Article  CAS  Google Scholar 

  • Dudas B, Rose M, Cornelli U, Pavlovich A, Hanin I (2008) Neuroprotective properties of glycosaminoglycans: potential treatment for neurodegenerative disorders. Neurodegener Dis 5(3–4):200–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Egea J, Garcia AG, Verges J, Montell E, Lopez MG (2010) Antioxidant, antiinflammatory and neuroprotective actions of chondroitin sulfate and proteoglycans. Osteoarthr Cartil 18(Suppl 1):S24–S27

    Article  Google Scholar 

  • Eisenberg S, Sehayek E, Olivecrona T, Vlodavsky I (1992) Lipoprotein lipase enhances binding of lipoproteins to heparan sulfate on cell surfaces and extracellular matrix. J Clin Invest 90(5):2013–2021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farrugia BL, Whitelock JM, O’Grady R, Caterson B, Lord MS (2016) Mast cells produce a unique chondroitin sulfate epitope. J Histochem Cytochem 64(2):85–98

    Article  CAS  PubMed  Google Scholar 

  • Fawcett JW, Oohashi T, Pizzorusso T (2019) The roles of perineuronal nets and the perinodal extracellular matrix in neuronal function. Nat Rev Neurosci 20(8):451–465

    Article  CAS  PubMed  Google Scholar 

  • Foyez T, Takeda-Uchimura Y, Ishigaki S, Narentuya, Zhang Z, Sobue G et al (2015) Microglial keratan sulfate epitope elicits in central nervous tissues of transgenic model mice and patients with amyotrophic lateral sclerosis. Am J Pathol 185(11):3053–3065

    Article  CAS  PubMed  Google Scholar 

  • Fraser PE, Darabie AA, McLaurin JA (2001) Amyloid-beta interactions with chondroitin sulfate-derived monosaccharides and disaccharides. Implications for drug development. J Biol Chem 276(9):6412–6419

    Article  CAS  PubMed  Google Scholar 

  • Fu Y, Zhao J, Atagi Y, Nielsen HM, Liu CC, Zheng H et al (2016) Apolipoprotein E lipoprotein particles inhibit amyloid-beta uptake through cell surface heparan sulphate proteoglycan. Mol Neurodegener 11(1):37

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fukuchi K, Hart M, Li L (1998) Alzheimer’s disease and heparan sulfate proteoglycan. Front Biosci 3:d327–d337

    Article  CAS  PubMed  Google Scholar 

  • Funderburgh JL (2000) Keratan sulfate: structure, biosynthesis, and function. Glycobiology 10(10):951–958

    Article  CAS  PubMed  Google Scholar 

  • Gallagher J (2015) Fell-Muir lecture: Heparan sulphate and the art of cell regulation: a polymer chain conducts the protein orchestra. Int J Exp Pathol 96(4):203–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia B, Martin C, Garcia-Suarez O, Muniz-Alonso B, Ordiales H, Fernandez-Menendez S et al (2017) Upregulated expression of Heparanase and Heparanase 2 in the brains of Alzheimer’s disease. J Alzheimers Dis 58(1):185–192

    Article  CAS  PubMed  Google Scholar 

  • Genedani S, Agnati LF, Leo G, Buzzega D, Maccari F, Carone C et al (2010) Beta-amyloid fibrillation and/or hyperhomocysteinemia modify striatal patterns of hyaluronic acid and dermatan sulfate: possible role in the pathogenesis of Alzheimer’s disease. Curr Alzheimer Res 7(2):150–157

    Article  CAS  PubMed  Google Scholar 

  • Geneste A, Guillaume YC, Magy-Bertrand N, Lethier L, Gharbi T, Andre C (2014) The protease activity of transthyretin reverses the effect of pH on the amyloid-beta protein/heparan sulfate proteoglycan interaction: a biochromatographic study. J Pharm Biomed Anal 97:88–96

    Article  CAS  PubMed  Google Scholar 

  • Goedert M, Spillantini MG (2017) Propagation of Tau aggregates. Mol Brain 10(1):18

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Goedert M, Jakes R, Spillantini MG, Hasegawa M, Smith MJ, Crowther RA (1996) Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans. Nature 383(6600):550–553

    Article  CAS  PubMed  Google Scholar 

  • Gonzales JC, Gordts PL, Foley EM, Esko JD (2013) Apolipoproteins E and AV mediate lipoprotein clearance by hepatic proteoglycans. J Clin Invest 123(6):2742–2751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordts P, Foley EM, Lawrence R, Sinha R, Lameda-Diaz C, Deng L et al (2014) Reducing macrophage proteoglycan sulfation increases atherosclerosis and obesity through enhanced type I interferon signaling. Cell Metab 20(5):813–826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grondin R, Littrell OM, Zhang Z, Ai Y, Huettl P, Pomerleau F et al (2019) GDNF revisited: a novel mammalian cell-derived variant form of GDNF increases dopamine turnover and improves brain biodistribution. Neuropharmacology 147:28–36

    Article  CAS  PubMed  Google Scholar 

  • Gundersen RW (1987) Response of sensory neurites and growth cones to patterned substrata of laminin and fibronectin in vitro. Dev Biol 121(2):423–431

    Article  CAS  PubMed  Google Scholar 

  • Guyton AC, Hall JE (2006) Textbook of medical physiology. Elsevier Saunders, Philadelphia

    Google Scholar 

  • Hamazaki H (1987) Ca2+-mediated association of human serum amyloid P component with heparan sulfate and dermatan sulfate. J Biol Chem 262(4):1456–1460

    Article  CAS  PubMed  Google Scholar 

  • Hardy J (2000) Pathways to primary neurodegenerative disease. Ann N Y Acad Sci 924:29–34

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa M, Crowther RA, Jakes R, Goedert M (1997) Alzheimer-like changes in microtubule-associated protein Tau induced by sulfated glycosaminoglycans. Inhibition of microtubule binding, stimulation of phosphorylation, and filament assembly depend on the degree of sulfation. J Biol Chem 272(52):33118–33124

    Article  CAS  PubMed  Google Scholar 

  • Hashimura K, Sudhir K, Nigro J, Ling S, Williams MR, Komesaroff PA et al (2005) Androgens stimulate human vascular smooth muscle cell proteoglycan biosynthesis and increase lipoprotein binding. Endocrinology 146(4):2085–2090

    Article  CAS  PubMed  Google Scholar 

  • Hayes AJ, Melrose J (2018) Glycans and glycosaminoglycans in neurobiology: key regulators of neuronal cell function and fate. Biochem J 475(15):2511–2545

    Article  CAS  PubMed  Google Scholar 

  • Heegaard NH (1998) A heparin-binding peptide from human serum amyloid P component characterized by affinity capillary electrophoresis. Electrophoresis 19(3):442–447

    Article  CAS  PubMed  Google Scholar 

  • Hillen AEJ, Burbach JPH, Hol EM (2018) Cell adhesion and matricellular support by astrocytes of the tripartite synapse. Prog Neurobiol 165–167:66–86

    Article  PubMed  CAS  Google Scholar 

  • Hirano K, Ohgomori T, Kobayashi K, Tanaka F, Matsumoto T, Natori T et al (2013) Ablation of keratan sulfate accelerates early phase pathogenesis of ALS. PLoS One 8(6):e66969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holmes BB, DeVos SL, Kfoury N, Li M, Jacks R, Yanamandra K et al (2013) Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds. Proc Natl Acad Sci U S A 110(33):E3138–E3147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horonchik L, Tzaban S, Ben-Zaken O, Yedidia Y, Rouvinski A, Papy-Garcia D et al (2005) Heparan sulfate is a cellular receptor for purified infectious prions. J Biol Chem 280(17):17062–17067

    Article  CAS  PubMed  Google Scholar 

  • Hubert T, Grimal S, Carroll P, Fichard-Carroll A (2009) Collagens in the developing and diseased nervous system. Cell Mol Life Sci 66(7):1223–1238

    Article  CAS  PubMed  Google Scholar 

  • Huynh MB, Villares J, Diaz JE, Christiaans S, Carpentier G, Ouidja MO et al (2012) Glycosaminoglycans from aged human hippocampus have altered capacities to regulate trophic factors activities but not Abeta42 peptide toxicity. Neurobiol Aging 33(5):1005.e11–1005.e22

    Article  CAS  Google Scholar 

  • Huynh MB, Ouidja MO, Chantepie S, Carpentier G, Maiza A, Zhang G et al (2019) Glycosaminoglycans from Alzheimer’s disease hippocampus have altered capacities to bind and regulate growth factors activities and to bind tau. PLoS One 14(1):e0209573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iqbal K, Wang X, Blanchard J, Liu F, Gong CX, Grundke-Iqbal I (2010) Alzheimer’s disease neurofibrillary degeneration: pivotal and multifactorial. Biochem Soc Trans 38(4):962–966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jendresen CB, Cui H, Zhang X, Vlodavsky I, Nilsson LN, Li JP (2015) Overexpression of heparanase lowers the amyloid burden in amyloid-beta precursor protein transgenic mice. J Biol Chem 290(8):5053–5064

    Article  CAS  PubMed  Google Scholar 

  • Kadomatsu K (2005) The midkine family in cancer, inflammation and neural development. Nagoya J Med Sci 67(3–4):71–82

    CAS  PubMed  Google Scholar 

  • Kadomatsu K, Muramatsu T (2004) Midkine and pleiotrophin in neural development and cancer. Cancer Lett 204(2):127–143

    Article  CAS  PubMed  Google Scholar 

  • Kaksonen M, Pavlov I, Voikar V, Lauri SE, Hienola A, Riekki R et al (2002) Syndecan-3-deficient mice exhibit enhanced LTP and impaired hippocampus-dependent memory. Mol Cell Neurosci 21(1):158–172

    Article  CAS  PubMed  Google Scholar 

  • Kalaria RN, Galloway PG, Perry G (1991) Widespread serum amyloid P immunoreactivity in cortical amyloid deposits and the neurofibrillary pathology of Alzheimer’s disease and other degenerative disorders. Neuropathol Appl Neurobiol 17(3):189–201

    Article  CAS  PubMed  Google Scholar 

  • Kastana P, Choleva E, Poimenidi E, Karamanos N, Sugahara K, Papadimitriou E (2019) Insight into the role of chondroitin sulfate E in angiogenesis. FEBS J 286(15):2921–2936

    Article  CAS  PubMed  Google Scholar 

  • Kero D, Bilandzija TS, Arapovic LL, Vukojevic K, Saraga-Babic M (2018) Syndecans and enzymes involved in Heparan sulfate biosynthesis and degradation are differentially expressed during human Odontogenesis. Front Physiol 9:732

    Article  PubMed  PubMed Central  Google Scholar 

  • Khan AR, Yang X, Du X, Yang H, Liu Y, Khan AQ et al (2020) Chondroitin sulfate derived theranostic and therapeutic nanocarriers for tumor-targeted drug delivery. Carbohydr Polym 233:115837

    Article  CAS  PubMed  Google Scholar 

  • Kisilevsky R, Ancsin JB, Szarek WA, Petanceska S (2007) Heparan sulfate as a therapeutic target in amyloidogenesis: prospects and possible complications. Amyloid 14(1):21–32

    Article  CAS  PubMed  Google Scholar 

  • Kleene R, Schachner M (2004) Glycans and neural cell interactions. Nat Rev Neurosci 5(3):195–208

    Article  CAS  PubMed  Google Scholar 

  • Konno T, Oiki S, Hasegawa K, Naiki H (2004) Anionic contribution for fibrous maturation of protofibrillar assemblies of the human tau repeat domain in a fluoroalcohol solution. Biochemistry 43(42):13613–136120

    Article  CAS  PubMed  Google Scholar 

  • Koyuncu S, Fatima A, Gutierrez-Garcia R, Vilchez D (2017) Proteostasis of huntingtin in health and disease. Int J Mol Sci 18(7):1568

    Article  CAS  PubMed Central  Google Scholar 

  • Kwok JC, Afshari F, Garcia-Alias G, Fawcett JW (2008) Proteoglycans in the central nervous system: plasticity, regeneration and their stimulation with chondroitinase ABC. Restor Neurol Neurosci 26(2–3):131–145

    PubMed  Google Scholar 

  • Lam V, Takechi R, Pallebage-Gamarallage MM, Galloway S, Mamo JC (2011) Colocalisation of plasma derived apo B lipoproteins with cerebral proteoglycans in a transgenic-amyloid model of Alzheimer’s disease. Neurosci Lett 492(3):160–164

    Article  CAS  PubMed  Google Scholar 

  • Lau LW, Cua R, Keough MB, Haylock-Jacobs S, Yong VW (2013) Pathophysiology of the brain extracellular matrix: a new target for remyelination. Nat Rev Neurosci 14(10):722–729

    Article  CAS  PubMed  Google Scholar 

  • Lauri SE, Kaukinen S, Kinnunen T, Ylinen A, Imai S, Kaila K et al (1999) Regulatory role and molecular interactions of a cell-surface heparan sulfate proteoglycan (N-syndecan) in hippocampal long-term potentiation. J Neurosci 19(4):1226–1235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lazarov O, Demars M (2012) All in the family: how the APPs regulate neurogenesis (review). Front Neurosci 6:81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehri-Boufala S, Ouidja MO, Barbier-Chassefiere V, Henault E, Raisman-Vozari R, Garrigue-Antar L et al (2015) New roles of glycosaminoglycans in alpha-synuclein aggregation in a cellular model of Parkinson disease. PLoS One 10(1):e0116641

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leonova EI, Galzitskaia OV (2015) Role of syndecan-2 in amyloid plaque formation. Mol Biol (Mosk) 49(1):89–98

    Article  CAS  Google Scholar 

  • Leveugle B, Ding W, Durkin JT, Mistretta S, Eisle J, Matic M et al (1997) Heparin promotes beta-secretase cleavage of the Alzheimer’s amyloid precursor protein. Neurochem Int 30(6):543–548

    Article  CAS  PubMed  Google Scholar 

  • Li JP, Kusche-Gullberg M (2016) Heparan sulfate: biosynthesis, structure, and function. Int Rev Cell Mol Biol 325:215–273

    Article  CAS  PubMed  Google Scholar 

  • Li JP, Gong F, Hagner-McWhirter A, Forsberg E, Abrink M, Kisilevsky R et al (2003) Targeted disruption of a murine glucuronyl C5-epimerase gene results in heparan sulfate lacking L-iduronic acid and in neonatal lethality. J Biol Chem 278(31):28363–28366

    Article  CAS  PubMed  Google Scholar 

  • Li JP, Galvis ML, Gong F, Zhang X, Zcharia E, Metzger S et al (2005) In vivo fragmentation of heparan sulfate by heparanase overexpression renders mice resistant to amyloid protein A amyloidosis. Proc Natl Acad Sci U S A 102(18):6473–6477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Li ZX, Jin T, Wang ZY, Zhao P (2017) Tau pathology promotes the reorganization of the extracellular matrix and inhibits the formation of Perineuronal nets by regulating the expression and the distribution of hyaluronic acid synthases. J Alzheimers Dis 57(2):395–409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lima M, Rudd T, Yates E (2017) New applications of heparin and other glycosaminoglycans. Molecules 22(5):749

    Article  PubMed Central  CAS  Google Scholar 

  • Lindahl B, Eriksson L, Spillmann D, Caterson B, Lindahl U (1996) Selective loss of cerebral keratan sulfate in Alzheimer’s disease. J Biol Chem 271(29):16991–16994

    Article  CAS  PubMed  Google Scholar 

  • Lindahl B, Westling C, Gimenez-Gallego G, Lindahl U, Salmivirta M (1999) Common binding sites for beta-amyloid fibrils and fibroblast growth factor-2 in heparan sulfate from human cerebral cortex. J Biol Chem 274(43):30631–30635

    Article  CAS  PubMed  Google Scholar 

  • Liu CC, Zhao N, Yamaguchi Y, Cirrito JR, Kanekiyo T, Holtzman DM et al (2016) Neuronal heparan sulfates promote amyloid pathology by modulating brain amyloid-beta clearance and aggregation in Alzheimer’s disease. Sci Transl Med 8(332):332ra44

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ma Q, Schultz C, Neville B, Jeske W, Hoppensteadt D, Cornelli U et al (2003) Pharmacodynamics and pharmacokinetics of C3, a heparin-derived oligosaccharide mixture, in non-human primates. Thromb Res 112(4):249–255

    Article  CAS  PubMed  Google Scholar 

  • Ma Q, Cornelli U, Hanin I, Jeske WP, Linhardt RJ, Walenga JM et al (2007) Heparin oligosaccharides as potential therapeutic agents in senile dementia. Curr Pharm Des 13(15):1607–1616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma J, Ma C, Li J, Sun Y, Ye F, Liu K et al (2020) Extracellular matrix proteins involved in Alzheimer’s disease. Chemistry 26(53):12101–12110

    Article  CAS  PubMed  Google Scholar 

  • Madine J, Clayton JC, Yates EA, Middleton DA (2009) Exploiting a (13)C-labelled heparin analogue for in situ solid-state NMR investigations of peptide-glycan interactions within amyloid fibrils. Org Biomol Chem 7(11):2414–2420

    Article  CAS  PubMed  Google Scholar 

  • Maeda N (2010) Structural variation of chondroitin sulfate and its roles in the central nervous system. Cent Nerv Syst Agents Med Chem 10(1):22–31

    Article  CAS  PubMed  Google Scholar 

  • Maeda N, Fukazawa N, Ishii M (2010) Chondroitin sulfate proteoglycans in neural development and plasticity. Front Biosci (Landmark Ed) 15:626–644

    Article  Google Scholar 

  • Mahley RW (1996) Heparan sulfate proteoglycan/low density lipoprotein receptor-related protein pathway involved in type III hyperlipoproteinemia and Alzheimer’s disease. Isr J Med Sci 32(6):414–429

    CAS  PubMed  Google Scholar 

  • Mahley RW, Ji ZS (1999) Remnant lipoprotein metabolism: key pathways involving cell-surface heparan sulfate proteoglycans and apolipoprotein E. J Lipid Res 40(1):1–16

    Article  CAS  PubMed  Google Scholar 

  • Maiza A, Chantepie S, Vera C, Fifre A, Huynh MB, Stettler O et al (2018) The role of heparan sulfates in protein aggregation and their potential impact on neurodegeneration. FEBS Lett 592(23):3806–3818

    Article  CAS  PubMed  Google Scholar 

  • Malavaki C, Mizumoto S, Karamanos N, Sugahara K (2008) Recent advances in the structural study of functional chondroitin sulfate and dermatan sulfate in health and disease. Connect Tissue Res 49(3):133–139

    Article  CAS  PubMed  Google Scholar 

  • Malmstrom A, Bartolini B, Thelin MA, Pacheco B, Maccarana M (2012) Iduronic acid in chondroitin/dermatan sulfate: biosynthesis and biological function. J Histochem Cytochem 60(12):916–925

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marras C, Beck JC, Bower JH, Roberts E, Ritz B, Ross GW et al (2018) Prevalence of Parkinson’s disease across North America. NPJ Parkinsons Dis 4:21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumoto K, Wanaka A, Takatsuji K, Muramatsu H, Muramatsu T, Tohyama M (1994) A novel family of heparin-binding growth factors, pleiotrophin and midkine, is expressed in the developing rat cerebral cortex. Brain Res Dev Brain Res 79(2):229–241

    Article  CAS  PubMed  Google Scholar 

  • Mehra S, Ghosh D, Kumar R, Mondal M, Gadhe LG, Das S et al (2018) Glycosaminoglycans have variable effects on alpha-synuclein aggregation and differentially affect the activities of the resulting amyloid fibrils. J Biol Chem 293(34):12975–12991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mende M, Bednarek C, Wawryszyn M, Sauter P, Biskup MB, Schepers U et al (2016) Chemical synthesis of glycosaminoglycans. Chem Rev 116(14):8193–8255

    Article  CAS  PubMed  Google Scholar 

  • Meyer K, Linker A, Davidson EA, Weissmann B (1953) The mucopolysaccharides of bovine cornea. J Biol Chem 205(2):611–616

    Article  CAS  PubMed  Google Scholar 

  • Mikami T, Kitagawa H (2013) Biosynthesis and function of chondroitin sulfate. Biochim Biophys Acta 1830(10):4719–4733

    Article  CAS  PubMed  Google Scholar 

  • Miyata S, Kitagawa H (2015) Mechanisms for modulation of neural plasticity and axon regeneration by chondroitin sulphate. J Biochem 157(1):13–22

    Article  CAS  PubMed  Google Scholar 

  • Mizuguchi S, Capretta A, Suehiro S, Nishiyama N, Luke P, Potter RF et al (2010) Carbon monoxide-releasing molecule CORM-3 suppresses vascular endothelial cell SOD-1/SOD-2 activity while up-regulating the cell surface levels of SOD-3 in a heparin-dependent manner. Free Radic Biol Med 49(10):1534–1541

    Article  CAS  PubMed  Google Scholar 

  • Mizumoto S, Fongmoon D, Sugahara K (2013) Interaction of chondroitin sulfate and dermatan sulfate from various biological sources with heparin-binding growth factors and cytokines. Glycoconj J 30(6):619–632

    Article  CAS  PubMed  Google Scholar 

  • Morla S (2019) Glycosaminoglycans and glycosaminoglycan Mimetics in cancer and inflammation. Int J Mol Sci 20(8):1963

    Article  CAS  PubMed Central  Google Scholar 

  • Mouw JK, Ou G, Weaver VM (2014) Extracellular matrix assembly: a multiscale deconstruction. Nat Rev Mol Cell Biol 15(12):771–785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muramatsu T (1993) Midkine (MK): a retinoic acid-responsive, heparin-binding growth factor in relationship with differentiation, development, cancer and neural function. Seikagaku 65(12):1494–1504

    CAS  PubMed  Google Scholar 

  • Naba A, Clauser KR, Hoersch S, Liu H, Carr SA, Hynes RO (2012) The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices. Mol Cell Proteomics 11(4):M111.014647

    Article  PubMed  CAS  Google Scholar 

  • Nagai N, Habuchi H, Kitazume S, Toyoda H, Hashimoto Y, Kimata K (2007) Regulation of heparan sulfate 6-O-sulfation by beta-secretase activity. J Biol Chem 282(20):14942–149451

    Article  CAS  PubMed  Google Scholar 

  • Nalivaeva NN, Turner AJ (2013) The amyloid precursor protein: a biochemical enigma in brain development, function and disease. FEBS Lett 587(13):2046–2054

    Article  CAS  PubMed  Google Scholar 

  • Nandini CD, Mikami T, Ohta M, Itoh N, Akiyama-Nambu F, Sugahara K (2004) Structural and functional characterization of oversulfated chondroitin sulfate/dermatan sulfate hybrid chains from the notochord of hagfish. Neuritogenic and binding activities for growth factors and neurotrophic factors. J Biol Chem 279(49):50799–50809

    Article  CAS  PubMed  Google Scholar 

  • Nature Springer (2020a) https://www.nature.com/subjects/neurodegenerative-diseases. Accessed 8 Apr 2020

  • Nature Springer (2020b) https://www.niehs.nih.gov/research/supported/health/neurodegenerative/index.cfm. Accessed 8 Apr 2020

  • Nguyen K, Rabenstein DL (2016) Interaction of the heparin-binding consensus sequence of beta-amyloid peptides with heparin and heparin-derived oligosaccharides. J Phys Chem B 120(9):2187–2197

    Article  CAS  PubMed  Google Scholar 

  • Nita M, Strzalka-Mrozik B, Grzybowski A, Mazurek U, Romaniuk W (2014) Age-related macular degeneration and changes in the extracellular matrix. Med Sci Monit 20:1003–1016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Callaghan P, Sandwall E, Li JP, Yu H, Ravid R, Guan ZZ et al (2008) Heparan sulfate accumulation with Abeta deposits in Alzheimer’s disease and Tg2576 mice is contributed by glial cells. Brain Pathol 18(4):548–561

    PubMed  PubMed Central  Google Scholar 

  • O’Callaghan P, Zhang X, Li JP (2018) Heparan sulfate proteoglycans as relays of Neuroinflammation. J Histochem Cytochem 66(4):305–319

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oohira A, Ida M, Matsui F (2004) Development and regeneration of the central nervous system and neural chondroitin sulfate proteoglycans. Tanpakushitsu Kakusan Koso 49(15 Suppl):2342–2347

    CAS  PubMed  Google Scholar 

  • Ori A, Wilkinson MC, Fernig DG (2011) A systems biology approach for the investigation of the heparin/heparan sulfate interactome. J Biol Chem 286(22):19892–19904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patey SJ (2006) The role of heparan sulfate in the generation of Abeta. Drug News Perspect 19(7):411–416

    Article  CAS  PubMed  Google Scholar 

  • Patey SJ, Edwards EA, Yates EA, Turnbull JE (2006) Heparin derivatives as inhibitors of BACE-1, the Alzheimer’s beta-secretase, with reduced activity against factor Xa and other proteases. J Med Chem 49(20):6129–6132

    Article  CAS  PubMed  Google Scholar 

  • Patey SJ, Edwards EA, Yates EA, Turnbull JE (2008) Engineered heparins: novel beta-secretase inhibitors as potential Alzheimer’s disease therapeutics. Neurodegener Dis 5(3–4):197–199

    Article  CAS  PubMed  Google Scholar 

  • Peng C, Trojanowski JQ, Lee VM (2020) Protein transmission in neurodegenerative disease. Nat Rev Neurol 16(4):199–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peterson S, Frick A, Liu J (2009) Design of biologically active heparan sulfate and heparin using an enzyme-based approach. Nat Prod Rep 26(5):610–627

    Article  CAS  PubMed  Google Scholar 

  • Presto J, Thuveson M, Carlsson P, Busse M, Wilen M, Eriksson I et al (2008) Heparan sulfate biosynthesis enzymes EXT1 and EXT2 affect NDST1 expression and heparan sulfate sulfation. Proc Natl Acad Sci USA 105(12):4751–4756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purushothaman A, Sugahara K, Faissner A (2012) Chondroitin sulfate “wobble motifs” modulate maintenance and differentiation of neural stem cells and their progeny. J Biol Chem 287(5):2935–2942

    Article  CAS  PubMed  Google Scholar 

  • Rani A, Patel S, Goyal A (2018) Chondroitin sulfate (CS) Lyases: structure, function and application in therapeutics. Curr Protein Pept Sci 19(1):22–33

    CAS  PubMed  Google Scholar 

  • Rauch JN, Chen JJ, Sorum AW, Miller GM, Sharf T, See SK et al (2018) Tau internalization is regulated by 6-O Sulfation on Heparan Sulfate Proteoglycans (HSPGs). Sci Rep 8(1):6382

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rauvala H, Paveliev M, Kuja-Panula J, Kulesskaya N (2017) Inhibition and enhancement of neural regeneration by chondroitin sulfate proteoglycans. Neural Regen Res 12(5):687–691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reed RK, Lilja K, Laurent TC (1988) Hyaluronan in the rat with special reference to the skin. Acta Physiol Scand 134(3):405–411

    Article  CAS  PubMed  Google Scholar 

  • Reed MJ, Damodarasamy M, Pathan JL, Chan CK, Spiekerman C, Wight TN et al (2019) Increased hyaluronan and TSG-6 in association with neuropathologic changes of Alzheimer’s disease. J Alzheimers Dis 67(1):91–102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivas RJ, Burmeister DW, Goldberg DJ (1992) Rapid effects of laminin on the growth cone. Neuron 8(1):107–115

    Article  CAS  PubMed  Google Scholar 

  • Rolls A, Avidan H, Cahalon L, Schori H, Bakalash S, Litvak V et al (2004) A disaccharide derived from chondroitin sulphate proteoglycan promotes central nervous system repair in rats and mice. Eur J Neurosci 20(8):1973–1983

    Article  PubMed  Google Scholar 

  • Ross CA, Poirier MA (2004) Protein aggregation and neurodegenerative disease. Nat Med 10(Suppl):S10–S17

    Article  PubMed  CAS  Google Scholar 

  • Rusmini P, Crippa V, Cristofani R, Rinaldi C, Cicardi ME, Galbiati M et al (2016) The role of the protein quality control system in SBMA. J Mol Neurosci 58(3):348–364

    Article  CAS  PubMed  Google Scholar 

  • Sangwan S, Eisenberg DS (2016) Perspective on SOD1 mediated toxicity in amyotrophic lateral sclerosis. Postepy Biochem 62(3):362–369

    Article  CAS  PubMed  Google Scholar 

  • Scheltens P, Blennow K, Breteler MM, de Strooper B, Frisoni GB, Salloway S et al (2016) Alzheimer’s disease. Lancet 388(10043):505–517

    Article  CAS  PubMed  Google Scholar 

  • Schworer R, Zubkova OV, Turnbull JE, Tyler PC (2013) Synthesis of a targeted library of heparan sulfate hexa- to dodecasaccharides as inhibitors of beta-secretase: potential therapeutics for Alzheimer’s disease. Chemistry 19(21):6817–6823

    Article  PubMed  CAS  Google Scholar 

  • Sepulveda-Diaz JE, Alavi Naini SM, Huynh MB, Ouidja MO, Yanicostas C, Chantepie S et al (2015) HS3ST2 expression is critical for the abnormal phosphorylation of tau in Alzheimer’s disease-related tau pathology. Brain 138(Pt 5):1339–1354

    Article  PubMed  PubMed Central  Google Scholar 

  • Shuvaev VV, Siest G (2000) Heparin specifically inhibits binding of apolipoprotein E to amyloid beta-peptide. Neurosci Lett 280(2):131–134

    Article  CAS  PubMed  Google Scholar 

  • Small DH, Nurcombe V, Reed G, Clarris H, Moir R, Beyreuther K et al (1994) A heparin-binding domain in the amyloid protein precursor of Alzheimer’s disease is involved in the regulation of neurite outgrowth. J Neurosci 14(4):2117–2127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith PD, Coulson-Thomas VJ, Foscarin S, Kwok JC, Fawcett JW (2015) “GAG-ing with the neuron”: the role of glycosaminoglycan patterning in the central nervous system. Exp Neurol 274(Pt B):100–114

    Article  CAS  PubMed  Google Scholar 

  • Snow AD, Mar H, Nochlin D, Sekiguchi RT, Kimata K, Koike Y et al (1990) Early accumulation of heparan sulfate in neurons and in the beta-amyloid protein-containing lesions of Alzheimer’s disease and Down’s syndrome. Am J Pathol 137(5):1253–1270

    CAS  PubMed  PubMed Central  Google Scholar 

  • Snow AD, Sekiguchi R, Nochlin D, Fraser P, Kimata K, Mizutani A et al (1994) An important role of heparan sulfate proteoglycan (Perlecan) in a model system for the deposition and persistence of fibrillar A beta-amyloid in rat brain. Neuron 12(1):219–234

    Article  CAS  PubMed  Google Scholar 

  • Snow AD, Kinsella MG, Parks E, Sekiguchi RT, Miller JD, Kimata K et al (1995) Differential binding of vascular cell-derived proteoglycans (perlecan, biglycan, decorin, and versican) to the beta-amyloid protein of Alzheimer’s disease. Arch Biochem Biophys 320(1):84–95

    Article  CAS  PubMed  Google Scholar 

  • Snow DM, Brown EM, Letourneau PC (1996) Growth cone behavior in the presence of soluble chondroitin sulfate proteoglycan (CSPG), compared to behavior on CSPG bound to laminin or fibronectin. Int J Dev Neurosci 14(3):331–349

    Article  CAS  PubMed  Google Scholar 

  • Solera C, Macchione G, Maza S, Kayser MM, Corzana F, de Paz JL et al (2016) Chondroitin sulfate Tetrasaccharides: synthesis, three-dimensional structure and interaction with Midkine. Chemistry 22(7):2356–2369

    Article  CAS  PubMed  Google Scholar 

  • Solovyev N, Drobyshev E, Bjorklund G, Dubrovskii Y, Lysiuk R, Rayman MP (2018) Selenium, selenoprotein P, and Alzheimer’s disease: is there a link? Free Radic Biol Med 127:124–133

    Article  CAS  PubMed  Google Scholar 

  • Som Chaudhury S, Das Mukhopadhyay C (2018) Functional amyloids: interrelationship with other amyloids and therapeutic assessment to treat neurodegenerative diseases. Int J Neurosci 128(5):449–463

    Article  CAS  PubMed  Google Scholar 

  • Song I, Dityatev A (2018) Crosstalk between glia, extracellular matrix and neurons. Brain Res Bull 136:101–108

    Article  CAS  PubMed  Google Scholar 

  • Stanford KI, Bishop JR, Foley EM, Gonzales JC, Niesman IR, Witztum JL et al (2009) Syndecan-1 is the primary heparan sulfate proteoglycan mediating hepatic clearance of triglyceride-rich lipoproteins in mice. J Clin Invest 119(11):3236–3245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stanford KI, Wang L, Castagnola J, Song D, Bishop JR, Brown JR et al (2010) Heparan sulfate 2-O-sulfotransferase is required for triglyceride-rich lipoprotein clearance. J Biol Chem 285(1):286–294

    Article  CAS  PubMed  Google Scholar 

  • Stevens RL, Fox CC, Lichtenstein LM, Austen KF (1988) Identification of chondroitin sulfate E proteoglycans and heparin proteoglycans in the secretory granules of human lung mast cells. Proc Natl Acad Sci U S A 85(7):2284–2287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stewart KL, Hughes E, Yates EA, Akien GR, Huang TY, Lima MA et al (2016) Atomic details of the interactions of Glycosaminoglycans with amyloid-beta fibrils. J Am Chem Soc 138(27):8328–8331

    Article  CAS  PubMed  Google Scholar 

  • Stewart KL, Hughes E, Yates EA, Middleton DA, Radford SE (2017) Molecular origins of the compatibility between Glycosaminoglycans and Abeta40 amyloid fibrils. J Mol Biol 429(16):2449–2462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stopschinski BE, Holmes BB, Miller GM, Manon VA, Vaquer-Alicea J, Prueitt WL et al (2018) Specific glycosaminoglycan chain length and sulfation patterns are required for cell uptake of tau versus alpha-synuclein and beta-amyloid aggregates. J Biol Chem 293(27):10826–10840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Streit A, Nolte C, Rasony T, Schachner M (1993) Interaction of astrochondrin with extracellular matrix components and its involvement in astrocyte process formation and cerebellar granule cell migration. J Cell Biol 120(3):799–814

    Article  CAS  PubMed  Google Scholar 

  • Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stutzmann JM, Mary V, Wahl F, Grosjean-Piot O, Uzan A, Pratt J (2002) Neuroprotective profile of enoxaparin, a low molecular weight heparin, in in vivo models of cerebral ischemia or traumatic brain injury in rats: a review. CNS Drug Rev 8(1):1–30

    Article  PubMed  PubMed Central  Google Scholar 

  • Sugahara K, Kitagawa H (2000) Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans. Curr Opin Struct Biol 10(5):518–527

    Article  CAS  PubMed  Google Scholar 

  • Sugahara K, Mikami T (2007) Chondroitin/dermatan sulfate in the central nervous system. Curr Opin Struct Biol 17(5):536–545

    Article  CAS  PubMed  Google Scholar 

  • Sullivan R, Yau WY, O’Connor E, Houlden H (2019) Spinocerebellar ataxia: an update. J Neurol 266(2):533–544

    Article  PubMed  Google Scholar 

  • Sun L, Zhou R, Yang G, Shi Y (2017) Analysis of 138 pathogenic mutations in presenilin-1 on the in vitro production of Abeta42 and Abeta40 peptides by gamma-secretase. Proc Natl Acad Sci USA 114(4):E476–E485

    Article  CAS  PubMed  Google Scholar 

  • Szczubialka K, Kaminski K, Zasada K, Karewicz A, Nowakowska M (2012) Heparin – a key drug in the treatment of the circulatory degenerative diseases: controlling its action with polymers. Curr Pharm Des 18(18):2591–2606

    Google Scholar 

  • Takase H, Tanaka M, Yamamoto A, Watanabe S, Takahashi S, Nadanaka S et al (2016) Structural requirements of glycosaminoglycans for facilitating amyloid fibril formation of human serum amyloid A. Amyloid 23(2):67–75

    Article  CAS  PubMed  Google Scholar 

  • Thacker BE, Xu D, Lawrence R, Esko JD (2014) Heparan sulfate 3-O-sulfation: a rare modification in search of a function. Matrix Biol 35:60–72

    Article  CAS  PubMed  Google Scholar 

  • Thompson HL, Schulman ES, Metcalfe DD (1988) Identification of chondroitin sulfate E in human lung mast cells. J Immunol 140(8):2708–2713

    Article  CAS  PubMed  Google Scholar 

  • Timmer NM, Schirris TJ, Bruinsma IB, Otte-Holler I, van Kuppevelt TH, de Waal RM et al (2010) Aggregation and cytotoxic properties towards cultured cerebrovascular cells of Dutch-mutated Abeta40 (DAbeta(1-40)) are modulated by sulfate moieties of heparin. Neurosci Res 66(4):380–389

    Article  CAS  PubMed  Google Scholar 

  • Timpl R (1989) Structure and biological activity of basement membrane proteins. Eur J Biochem 180(3):487–502

    Article  CAS  PubMed  Google Scholar 

  • Toole BP (2004) Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer 4(7):528–539

    Article  CAS  PubMed  Google Scholar 

  • Trott A, Houenou LJ (2012) Mini-review: spinocerebellar ataxias: an update of SCA genes. Recent Pat DNA Gene Seq 6(2):115–121

    Article  CAS  PubMed  Google Scholar 

  • Uchimura K, Rosen SD (2006) Sulfated L-selectin ligands as a therapeutic target in chronic inflammation. Trends Immunol 27(12):559–565

    Article  CAS  PubMed  Google Scholar 

  • Ueoka C, Kaneda N, Okazaki I, Nadanaka S, Muramatsu T, Sugahara K (2000) Neuronal cell adhesion, mediated by the heparin-binding neuroregulatory factor midkine, is specifically inhibited by chondroitin sulfate E. Structural ans functional implications of the over-sulfated chondroitin sulfate. J Biol Chem 275(48):37407–37413

    Article  CAS  PubMed  Google Scholar 

  • van Horssen J, Wesseling P, van den Heuvel LP, de Waal RM, Verbeek MM (2003) Heparan sulphate proteoglycans in Alzheimer’s disease and amyloid-related disorders. Lancet Neurol 2(8):482–492

    Article  PubMed  Google Scholar 

  • van Horssen J, de Vos RA, Steur EN, David G, Wesseling P, de Waal RM et al (2004) Absence of heparan sulfate proteoglycans in Lewy bodies and Lewy neurites in Parkinson’s disease brains. J Alzheimers Dis 6(5):469–474

    Article  PubMed  Google Scholar 

  • Vera C, Alvarez-Orozco JA, Maiza A, Chantepie S, Chehin RN, Ouidja MO et al (2017) Heparan sulphates, amyloidosis and neurodegeneration. Rev Neurol 65(10):457–468

    CAS  PubMed  Google Scholar 

  • Vieira MS, Santos AK, Vasconcellos R, Goulart VAM, Parreira RC, Kihara AH et al (2018) Neural stem cell differentiation into mature neurons: mechanisms of regulation and biotechnological applications. Biotechnol Adv 36(7):1946–1970

    Article  CAS  PubMed  Google Scholar 

  • Volpi N (2006) Therapeutic applications of glycosaminoglycans. Curr Med Chem 13(15):1799–1810

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Ding K (2014) Proteoglycans and glycosaminoglycans in misfolded proteins formation in Alzheimer’s disease. Protein Pept Lett 21(10):1048–1056

    Article  PubMed  CAS  Google Scholar 

  • Warner RG, Hundt C, Weiss S, Turnbull JE (2002) Identification of the heparan sulfate binding sites in the cellular prion protein. J Biol Chem 277(21):18421–18430

    Article  CAS  PubMed  Google Scholar 

  • Weiss RJ, Esko JD, Tor Y (2017) Targeting heparin and heparan sulfate protein interactions. Org Biomol Chem 15(27):5656–5668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wesen E, Gallud A, Paul A, Lindberg DJ, Malmberg P, Esbjorner EK (2018) Cell surface proteoglycan-mediated uptake and accumulation of the Alzheimer’s disease peptide Abeta(1-42). Biochim Biophys Acta Biomembr 1860(11):2204–2214

    Article  CAS  PubMed  Google Scholar 

  • Woodbury ME, Ikezu T (2014) Fibroblast growth factor-2 signaling in neurogenesis and neurodegeneration. J Neuroimmune Pharmacol 9(2):92–101

    Article  PubMed  Google Scholar 

  • Xu D, Esko JD (2014) Demystifying heparan sulfate-protein interactions. Annu Rev Biochem 83:129–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Masuko S, Takieddin M, Xu H, Liu R, Jing J et al (2011) Chemoenzymatic synthesis of homogeneous ultralow molecular weight heparins. Science 334(6055):498–501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada S, Sugahara K, Ozbek S (2011) Evolution of glycosaminoglycans: comparative biochemical study. Commun Integr Biol 4(2):150–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang G, Zhou R, Zhou Q, Guo X, Yan C, Ke M et al (2019) Structural basis of Notch recognition by human gamma-secretase. Nature 565(7738):192–197

    Article  CAS  PubMed  Google Scholar 

  • Yasuhara O, Muramatsu H, Kim SU, Muramatsu T, Maruta H, McGeer PL (1993) Midkine, a novel neurotrophic factor, is present in senile plaques of Alzheimer disease. Biochem Biophys Res Commun 192(1):246–251

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Li JP (2010) Heparan sulfate proteoglycans in amyloidosis. Prog Mol Biol Transl Sci 93:309–334

    Article  CAS  PubMed  Google Scholar 

  • Zhang GL, Zhang X, Wang XM, Li JP (2014) Towards understanding the roles of heparan sulfate proteoglycans in Alzheimer’s disease. Biomed Res Int 2014:516028

    PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Takeda-Uchimura Y, Foyez T, Ohtake-Niimi S, Narentuya, Akatsu H et al (2017) Deficiency of a sulfotransferase for sialic acid-modified glycans mitigates Alzheimer’s pathology. Proc Natl Acad Sci U S A 114(14):E2947–E2954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Zheng L, Cheng S, Peng Y, Fu L, Zhang X et al (2019) Comparison of the interactions of different growth factors and Glycosaminoglycans. Molecules 24(18):3360

    Article  CAS  PubMed Central  Google Scholar 

  • Zhang X, Lin L, Huang H, Linhardt RJ (2020) Chemoenzymatic synthesis of Glycosaminoglycans. Acc Chem Res 53(2):335–346

    Article  CAS  PubMed  Google Scholar 

  • Zhao D, Zhang S, Meng Y, Xiongwei D, Zhang D, Liang Y et al (2014) Polyanion binding accelerates the formation of stable and low-toxic aggregates of ALS-linked SOD1 mutant A4V. Proteins 82(12):3356–3372

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Huvent I, Lippens G, Eliezer D, Zhang A, Li Q et al (2017) Glycan determinants of heparin-tau interaction. Biophys J 112(5):921–932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Zhu Y, Song X, Xiao Y, Su G, Liu X et al (2019) Rare 3-O-sulfation of Heparan sulfate enhances tau interaction and cellular uptake. Angew Chem Int Ed Engl 58:2–11

    CAS  Google Scholar 

  • Zhou R, Yang G, Guo X, Zhou Q, Lei J, Shi Y (2019) Recognition of the amyloid precursor protein by human gamma-secretase. Science 363(6428):eaaw0930

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. College of Biotechnology and Bioengineering, Zhejiang University of Technology, Hangzhou, China

    Weihua Jin

  2. Department of Chemical and Biological Engineering, Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, NY, USA

    Weihua Jin, Fuming Zhang & Robert J. Linhardt

  3. Department of Biological Science, Departments of Chemistry and Chemical Biology and Biomedical Engineering, Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, NY, USA

    Robert J. Linhardt

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  1. Weihua Jin
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Correspondence to Fuming Zhang or Robert J. Linhardt .

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  1. Faculty of Pharmacy and Biochemistry, University of Zagreb, Zagreb, Croatia

    Gordan Lauc

  2. Genos Glycoscience Research Laboratory, Zagreb, Croatia

    Irena Trbojević-Akmačić

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Funding: This research was funded through grants from the NIH (DK111958, CA231074, AG062344 and AG069039 to RL).

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Ethical approval: This article does not contain any studies with animals performed by any of the authors.

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Jin, W., Zhang, F., Linhardt, R.J. (2021). Glycosaminoglycans in Neurodegenerative Diseases. In: Lauc, G., Trbojević-Akmačić, I. (eds) The Role of Glycosylation in Health and Disease. Advances in Experimental Medicine and Biology, vol 1325. Springer, Cham. https://doi.org/10.1007/978-3-030-70115-4_9

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