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Neuroprotective activities of natural products from marine macroalgae during 1999–2015

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Abstract

This review focuses on macroalgae-derived compounds with neuroprotective activity that may provide lead compounds for the prevention and treatment of neurodegenerative diseases such as Alzheimer’s, Parkinson’s, and Huntington’s disease. Coverage is provided from 1999 to 2015. A total of 99 pure compounds have been reported. The main in vitro bioactivities of these compounds include inhibition of beta amyloid protein (Aβ), inhibition of acetylcholinesterase (AChE) and butyrylcholinesterase (BuChE), reduction in oxidative stress, anti-inflammatory activity, inhibition of kinases, enhancement of neurite outgrowth and the reduction in dopaminergic neurotoxicity. The majority of these bioactive compounds are derived from Phaeophyceae (57.6 %), followed by Rhodophyta (28.3 %) and Chlorophyta (14.1 %). This review presents valuable knowledge on macroalgae-derived compounds and their known pathways of neuroprotection to further explore the potential of these compounds in preventing and treating neurodegenerative diseases.

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References

  • Ahn BR, Moon HE, Kim HR, Jung HA, Choi JS (2012) Neuroprotective effect of edible brown alga Eisenia bicyclis on amyloid beta peptide-induced toxicity in PC12 cells. Arch Pharm Res 35:1989–1998

    Article  CAS  PubMed  Google Scholar 

  • Alghazwi M, Kan Y, Zhang W, Gai W, Yan X (2016) Neuroprotective activities of marine natural products from marine sponges. Curr Med Chem 23:360–382

    Article  CAS  PubMed  Google Scholar 

  • Avila J, Santa-Maria I, Perez M, Hernandez F, Moreno F (2006) Tau phosphorylation, aggregation, and cell toxicity. BioMed Res Int 2006:1–5

    Google Scholar 

  • Banati RB, Gehrmann J, Schubert P, Kreutzberg GW (1993) Cytotoxicity of microglia. Glia 7:111–118

    Article  CAS  PubMed  Google Scholar 

  • Barbosa M, Valentão P, Andrade PB (2014) Bioactive compounds from macroalgae in the new millennium: implications for neurodegenerative diseases. Mar Drugs 12:4934–4972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bartus RT, Dean RL, Beer B, Lippa AS (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408–414

    Article  CAS  PubMed  Google Scholar 

  • Bezprozvanny I (2009) Calcium signaling and neurodegenerative diseases. Trends Mol Med 15:89–100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blennow K, de Leon MJ, Zetterberg H (2006) Alzheimer’s disease. Lancet 368:387–403

    Article  CAS  PubMed  Google Scholar 

  • Bolognesi ML, Cavalli A, Melchiorre C (2009) Memoquin: a multi-target-directed ligand as an innovative therapeutic opportunity for Alzheimer’s disease. Neurotherapeutics 6:152–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonda DJ, Wang X, Perry G, Nunomura A, Tabaton M, Zhu X, Smith MA (2010) Oxidative stress in Alzheimer disease: a possibility for prevention. Neuropharmacology 59:290–294

    Article  CAS  PubMed  Google Scholar 

  • Cai Z-Y, Yan Y (2007) Pathway and mechanism of oxidative stress in Alzheimer’s disease. J Medical Colleges PLA 22:320–325

    Article  CAS  Google Scholar 

  • Castro LSEPW, Pinheiro TS, Castro AJG, Dore CMPG, da Silva NB, Faustino Alves MGC, Santos MSN, Leite EL (2014) Fucose-containing sulfated polysaccharides from brown macroalgae Lobophora variegata with antioxidant, anti-inflammatory, and antitumoral effects. J Appl Phycol 26:1783–1790

    Article  CAS  Google Scholar 

  • Cavalli A, Bolognesi ML, Minarini A, Rosini M, Tumiatti V, Recanatini M, Melchiorre C (2008) Multi-target-directed ligands to combat neurodegenerative diseases. J Med Chem 51:347–372

    Article  CAS  PubMed  Google Scholar 

  • Cho M, Lee H-S, Kang I-J, Won M-H, You S (2011) Antioxidant properties of extract and fractions from Enteromorpha prolifera, a type of green seaweed. Food Chem 127:999–1006

    Article  CAS  PubMed  Google Scholar 

  • Choi D-Y, Choi H (2015) Natural products from marine organisms with neuroprotective activity in the experimental models of Alzheimer’s disease, Parkinson’s disease and ischemic brain stroke: their molecular targets and action mechanisms. Arch Pharm Res 38:139–170

    Article  CAS  PubMed  Google Scholar 

  • Choi BW, Lee HS, Shin HC, Lee BH (2015a) Multifunctional activity of polyphenolic compounds associated with a potential for Alzheimer’s disease therapy from Ecklonia cava. Phytother Res 29:549–553

    Article  CAS  PubMed  Google Scholar 

  • Choi JS, Haulader S, Karki S, Jung HJ, Kim HR, Jung HA (2015b) Acetyl-and butyryl-cholinesterase inhibitory activities of the edible brown alga Eisenia bicyclis. Arch Pharm Res 38:1477–1487

    Article  CAS  PubMed  Google Scholar 

  • Cui Y-Q, Zhang L-J, Zhang T, Luo D-Z, Jia Y-J, Guo Z-X, Zhang Q-B, Wang X, Wang X-M (2010) Inhibitory effect of fucoidan on nitric oxide production in lipopolysaccharide-activated primary microglia. Clin Exp Pharmacol Physiol 37:422–428

    Article  CAS  PubMed  Google Scholar 

  • Cui YQ, Jia YJ, Zhang T, Zhang QB, Wang XM (2012) Fucoidan protects against lipopolysaccharide-induced rat neuronal damage and inhibits the production of proinflammatory mediators in primary microglia. CNS Neurosci Ther 18:827–833

    Article  CAS  PubMed  Google Scholar 

  • Darvesh S, Hopkins DA (2003) Differential distribution of butyrylcholinesterase and acetylcholinesterase in the human thalamus. J Comp Neurol 463:25–43

    Article  CAS  PubMed  Google Scholar 

  • de Souza MCR, Marques CT, Dore CMG, da Silva FRF, Rocha HAO, Leite EL (2007) Antioxidant activities of sulfated polysaccharides from brown and red seaweeds. J Appl Phycol 19:153–160

    Article  CAS  Google Scholar 

  • de Souza ÉT, Pereira de Lira D, Cavalcanti de Queiroz A, Costa da Silva DJ, Bezerra de Aquino A, Campessato Mella EA, Prates Lorenzo V, De Miranda GEC, De Araújo-Júnior JX, de Oliveira Chaves MC (2009) The antinociceptive and anti-inflammatory activities of caulerpin, a bisindole alkaloid isolated from seaweeds of the genus Caulerpa. Mar Drugs 7:689–704

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • de Souza BC, Cirne-Santos CC, Garrido V, Barcelos I, Stephens PRS, Giongo V, Teixeira VL, de Palmer Paixão ICN (2016) Anti-HIV-1 activity of compounds derived from marine alga Canistrocarpus cervicornis. J Appl Phycol 28:2523–2527

  • Dolan PJ, Johnson GV (2010) The role of tau kinases in Alzheimer’s disease. Curr Opin Drug Discov Devel 13:595–603

    CAS  PubMed  PubMed Central  Google Scholar 

  • Drechsel DN, Hyman A, Cobb MH, Kirschner M (1992) Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell 3:1141–1154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fang Z, Jeong SY, Jung HA, Choi JS, Min BS, Woo MH (2010) Anticholinesterase and antioxidant constituents from Gloiopeltis furcata. Chem Pharm Bull (Tokyo) 58:1236–1239

    Article  CAS  Google Scholar 

  • Fang J, Li Y, Liu R, Pang X, Li C, Yang R, He Y, Lian W, A-l L, G-h D (2015) Discovery of multitarget-directed ligands against Alzheimer’s disease through systematic prediction of chemical-protein interactions. J Chem Inf Model 55:149–164

    Article  CAS  PubMed  Google Scholar 

  • Fukuyama R, Wadhwani KC, Galdzicki Z, Rapoport SI, Ehrenstein G (1994) β-Amyloid polypeptide increases calcium-uptake in PC12 cells: a possible mechanism for its cellular toxicity in Alzheimer’s disease. Brain Res 667:269–272

    Article  CAS  PubMed  Google Scholar 

  • Gao Y, Dong C, Yin J, Shen J, Tian J, Li C (2012a) Neuroprotective effect of fucoidan on H2O2-induced apoptosis in PC12 cells via activation of PI3K/Akt pathway. Cell Mol Neurobiol 32:523–529

    Article  CAS  PubMed  Google Scholar 

  • Gao Y, Li C, Yin J, Shen J, Wang H, Wu Y, Jin H (2012b) Fucoidan, a sulfated polysaccharide from brown algae, improves cognitive impairment induced by infusion of Aβ peptide in rats. Environ Toxicol Pharmacol 33:304–311

    Article  CAS  PubMed  Google Scholar 

  • Gerlach M, Riederer P, Przuntek H, Youdim MB (1991) MPTP mechanisms of neurotoxicity and their implications for Parkinson’s disease. Eur J Pharm-Molec Ph 208:273–286

    Article  CAS  Google Scholar 

  • Goedert M, Wischik C, Crowther R, Walker J, Klug A (1988) Cloning and sequencing of the cDNA encoding a core protein of the paired helical filament of Alzheimer disease: identification as the microtubule-associated protein tau. Proc Nat Acad Sci 85:4051–4055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Götz J, Ittner A, Ittner LM (2012) Tau‐targeted treatment strategies in Alzheimer’s disease. Br J Pharmacol 165:1246–1259

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Greig NH, Lahiri DK, Sambamurti K (2002) Butyrylcholinesterase: an important new target in Alzheimer’s disease therapy. Int Psychogeriatr 14:77–91

    Article  PubMed  Google Scholar 

  • Greig NH, Utsuki T, Ingram DK, Wang Y, Pepeu G, Scali C, Yu Q-S, Mamczarz J, Holloway HW, Giordano T, Chen D, Furukawa K, Sambamurti K, Brossi A, Lahiri DK (2005) Selective butyrylcholinesterase inhibition elevates brain acetylcholine, augments learning and lowers Alzheimer β amyloid peptide in rodent. Proc Nat Acad Sci 102:17213–17218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grutzendler J, Morris JC (2001) Cholinesterase inhibitors for Alzheimer’s disease. Drugs 61:41–52

    Article  CAS  PubMed  Google Scholar 

  • Guiry MD (2012) How many species of algae are there? J Phycol 48:1057–1063

    Article  PubMed  Google Scholar 

  • Hanger DP, Seereeram A, Noble W (2009) Mediators of tau phosphorylation in the pathogenesis of Alzheimer’s disease. Expert Rev Neurother 9:1647–1666

    Article  CAS  PubMed  Google Scholar 

  • Hefti F (1997) Pharmacology of neurotrophic factors. Annu Rev Pharmacol Toxicol 37:239–267

    Article  CAS  PubMed  Google Scholar 

  • Heo S-J, Ko S-C, Kang S-M, Kang H-S, Kim J-P, Kim S-H, Lee K-W, Cho M-G, Jeon Y-J (2008) Cytoprotective effect of fucoxanthin isolated from brown algae Sargassum siliquastrum against H2O2-induced cell damage. Eur Food Res Technol 228:145–151

    Article  CAS  Google Scholar 

  • Heo S-J, Cha S-H, Kim K-N, Lee S-H, Ahn G, Kang D-H, Oh C, Choi Y-U, Affan A, Kim D, Jeon Y-J (2012) Neuroprotective effect of phlorotannin isolated from Ishige okamurae against H2O2-induced oxidative stress in murine hippocampal neuronal cells, HT22. Appl Biochem Biotechnol 166:1520–1532

    Article  CAS  PubMed  Google Scholar 

  • Hirokawa N, Funakoshi T, Sato-Harada R, Kanai Y (1996) Selective stabilization of tau in axons and microtubule-associated protein 2C in cell bodies and dendrites contributes to polarized localization of cytoskeletal proteins in mature neurons. J Cell Biol 132:667–679

    Article  CAS  PubMed  Google Scholar 

  • Hoover BR, Reed MN, Su J, Penrod RD, Kotilinek LA, Grant MK, Pitstick R, Carlson GA, Lanier LM, Yuan L-L (2010) Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration. Neuron 68:1067–1081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274:99–102

    Article  CAS  PubMed  Google Scholar 

  • Hu J, Geng M, Li J, Xin X, Wang J, Tang M, Zhang J, Zhang X, Ding J (2004) Acidic oligosaccharide sugar chain, a marine-derived acidic oligosaccharide, inhibits the cytotoxicity and aggregation of amyloid beta protein. J Pharmacol Sci 95:248–255

    Article  CAS  PubMed  Google Scholar 

  • Hussain I, Powell D, Howlett DR, Tew DG, Meek TD, Chapman C, Gloger IS, Murphy KE, Southan CD, Ryan DM, Smith TS, Simmons DL, Walsh FS, Dingwall C, Christie G (1999) Identification of a novel aspartic protease (Asp 2) as β-secretase. Mol Cell Neurosci 14:419–427

    Article  CAS  PubMed  Google Scholar 

  • Ina A, Hayashi K-I, Nozaki H, Kamei Y (2007) Pheophytin a, a low molecular weight compound found in the marine brown alga Sargassum fulvellum, promotes the differentiation of PC12 cells. Int J Dev Neurosci 25:63–68

    Article  CAS  PubMed  Google Scholar 

  • Inestrosa NC, Alvarez A, Pérez CA, Moreno RD, Vicente M, Linker C, Casanueva OI, Soto C, Garrido J (1996) Acetylcholinesterase accelerates assembly of amyloid-beta-peptides into Alzheimer’s fibrils: possible role of the peripheral site of the enzyme. Neuron 16:889–891

    Article  Google Scholar 

  • Jhamandas JH, Wie MB, Harris K, MacTavish D, Kar S (2005) Fucoidan inhibits cellular and neurotoxic effects of beta-amyloid (A beta) in rat cholinergic basal forebrain neurons. Eur J Neurosci 21:2649–2659

    Article  PubMed  Google Scholar 

  • John V (2006) Human β-secretase (BACE) and BACE inhibitors: progress report. Curr Top Med Chem 6:569–578

    Article  CAS  PubMed  Google Scholar 

  • Jung M, Jang KH, Kim B, Lee BH, Choi BW, Oh K-B, Shin J (2008) Meroditerpenoids from the brown alga Sargassum siliquastrum. J Nat Prod 71:1714–1719

    Article  CAS  PubMed  Google Scholar 

  • Jung HA, Oh SH, Choi JS (2010) Molecular docking studies of phlorotannins from Eisenia bicyclis with BACE1 inhibitory activity. Bioorg Med Chem Lett 20:3211–3215

    Article  CAS  PubMed  Google Scholar 

  • Kamei Y, Tsang CK (2003) Sargaquinoic acid promotes neurite outgrowth via protein kinase A and MAP kinases-mediated signaling pathways in PC12D cells. Int J Dev Neurosci 21:255–262

    Article  CAS  PubMed  Google Scholar 

  • Kang HS, Chung HY, Kim JY, Son BW, Jung HA, Choi JS (2004) Inhibitory phlorotannins from the edible brown alga Ecklonia stolonifera on total reactive oxygen species (ROS) generation. Arch Pharm Res 27:194–198

    Article  CAS  PubMed  Google Scholar 

  • Kang KA, Lee KH, Chae S, Koh YS, Yoo BS, Kim JH, Ham YM, Baik JS, Lee NH, Hyun JW (2005) Triphlorethol-A from Ecklonia cava protects V79-4 lung fibroblast against hydrogen peroxide induced cell damage. Free Radic Res 39:883–892

    Article  CAS  PubMed  Google Scholar 

  • Kang S-M, Cha S-H, Ko J-Y, Kang M-C, Kim D, Heo S-J, Kim J-S, Heu MS, Kim Y-T, Jung W-K, Jeon Y-J (2012) Neuroprotective effects of phlorotannins isolated from a brown alga, Ecklonia cava, against H2O2-induced oxidative stress in murine hippocampal HT22 cells. Environ Toxicol Pharmacol 34:96–105

    Article  CAS  PubMed  Google Scholar 

  • Kannan RR, Aderogba MA, Ndhlala AR, Stirk WA, Van Staden J (2013) Acetylcholinesterase inhibitory activity of phlorotannins isolated from the brown alga, Ecklonia maxima (Osbeck) Papenfuss. Food Res Int 54:1250–1254

    Article  CAS  Google Scholar 

  • Kim HS, Lee K, Kang KA, Lee NH, Hyun JW, Kim H-S (2012) Phloroglucinol exerts protective effects against oxidative stress-induced cell damage in SH-SY5Y cells. J Pharmacol Sci 119:186–192

    Article  CAS  PubMed  Google Scholar 

  • Kim M, Li Y-X, Dewapriya P, Ryu B, Kim S-K (2013) Floridoside suppresses pro-inflammatory responses by blocking MAPK signaling in activated microglia. BMB Rep 46:398–403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312–318

    Article  CAS  PubMed  Google Scholar 

  • Kromer LF (1986) Nerve growth factor treatment after brain injury prevents neuronal death. Science 235:214–216

    Article  Google Scholar 

  • LaFerla FM, Green KN, Oddo S (2007) Intracellular amyloid-β in Alzheimer’s disease. Nat Rev Neurosci 8:499–509

    Article  CAS  PubMed  Google Scholar 

  • Langston J, Forno L, Tetrud J, Reeves A, Kaplan J, Karluk D (1999) Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure. Ann Neurol 46:598–605

    Article  CAS  PubMed  Google Scholar 

  • Lee B, Sur B, Park J, Shin H, Kwon S, Yeom M, Kim SJ, Kim K, Shim I, Yin CS (2012) Fucoidan ameliorates scopolamine-induced neuronal impairment and memory dysfunction in rats via activation of cholinergic system and regulation of cAMP-response element-binding protein and brain-derived neurotrophic factor expressions. J Kor Soc Appl Biol 55:711–720

    Article  CAS  Google Scholar 

  • Lee C, Park GH, Ahn EM, Kim B, Park C-I, Jang J-H (2013) Protective effect of Codium fragile against UVB-induced pro-inflammatory and oxidative damages in HaCaT cells and BALB/c mice. Fitoterapia 86:54–63

    Article  CAS  PubMed  Google Scholar 

  • Leon R, Garcia AG, Marco‐Contelles J (2013) Recent advances in the multitarget‐directed ligands approach for the treatment of Alzheimer’s disease. Med Res Rev 33:139–189

  • Li B, Lu F, Wei X, Zhao R (2008) Fucoidan: structure and bioactivity. Molecules 13:1671–1695

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Qian Z-J, Ryu B, Lee S-H, Kim M-M, Kim S-K (2009) Chemical components and its antioxidant properties in vitro: an edible marine brown alga, Ecklonia cava. Bioorg Med Chem 17:1963–1973

    Article  CAS  PubMed  Google Scholar 

  • Li K, Li X-M, Gloer JB, Wang B-G (2012) New nitrogen-containing bromophenols from the marine red alga Rhodomela confervoides and their radical scavenging activity. Food Chem 135:868–872

    Article  CAS  PubMed  Google Scholar 

  • Lima-Filho JVM, Carvalho AFFU, Freitas SM, Melo VMM (2002) Antibacterial activity of extracts of six macroalgae from the Northeastern Brazilian coast. Braz J Microbiol 33:311–313

    Article  Google Scholar 

  • Liu H, Gu L (2012) Phlorotannins from brown algae (Fucus vesiculosus) inhibited the formation of advanced glycation endproducts by scavenging reactive carbonyls. J Agric Food Chem 60:1326–1334

    Article  CAS  PubMed  Google Scholar 

  • Liu M, Nie Q, Xin X, Geng M (2008) Identification of AOSC-binding proteins in neurons. Chin J Oceanol Limn 26:394–399

    Article  CAS  Google Scholar 

  • Liu D-Q, Mao S-C, Zhang H-Y, Yu X-Q, Feng M-T, Wang B, Feng L-H, Guo Y-W (2013) Racemosins A and B, two novel bisindole alkaloids from the green alga Caulerpa racemosa. Fitoterapia 91:15–20

    Article  CAS  PubMed  Google Scholar 

  • Lobban CS, Harrison PJ (1994) Morphology, life histories, and morphogenesis. In: Lobban CS, Harrison PJ (eds) Seaweed ecology and physiology. Cambridge University Press, New York, pp 1–68

    Chapter  Google Scholar 

  • Lowenthal RM, Fitton JH (2015) Are seaweed-derived fucoidans possible future anti-cancer agents? J Appl Phycol 27:2075–2077

    Article  CAS  Google Scholar 

  • Lull ME, Block ML (2010) Microglial activation and chronic neurodegeneration. Neurotherapeutics 7:354–365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo D, Zhang Q, Wang H, Cui Y, Sun Z, Yang J, Zheng Y, Jia J, Yu F, Wang X (2009) Fucoidan protects against dopaminergic neuron death in vivo and in vitro. Eur J Pharmacol 617:33–40

    Article  CAS  PubMed  Google Scholar 

  • McGeer P, Itagaki S, Boyes B, McGeer E (1988) Reactive microglia are positive for HLA‐DR in the substantia nigra of Parkinson’s and Alzheimer’s disease brains. Neurology 38:1285–1285

    Article  CAS  PubMed  Google Scholar 

  • Meraz-Ríos MA, Toral-Rios D, Franco-Bocanegra D, Villeda-Hernández J, Campos-Peña V (2013) Inflammatory process in Alzheimer’s disease. Front Integr Neurosci. doi:10.3389/fnint.2013.00059

    PubMed  PubMed Central  Google Scholar 

  • Mori J, Iwashima M, Wakasugi H, Saito H, Matsunaga T, Ogasawara M, Takahashi S, Suzuki H, Hayashi T (2005) New plastoquinones isolated from the brown alga, Sargassum micracanthum. Chem Pharm Bull (Tokyo) 53:1159–1163

    Article  CAS  Google Scholar 

  • Murakami N, Nakajima T, Kobayashi M (2001) Total synthesis of lembehyne A, a neuritogenic spongean polyacetylene. Tet Lett 42:1941–1943

    Article  CAS  Google Scholar 

  • Murphy C, Hotchkiss S, Worthington J, McKeown SR (2014) The potential of seaweed as a source of drugs for use in cancer chemotherapy. J Appl Phycol 26:2211–2264

    Article  CAS  Google Scholar 

  • Noble W, Pooler AM, Hanger DP (2011) Advances in tau-based drug discovery. Expert Opin Drug Dis 6:797–810

    Article  CAS  Google Scholar 

  • Pangestuti R, Kim S-K (2011a) Biological activities and health benefit effects of natural pigments derived from marine algae. J Funct Foods 3:255–266

    Article  CAS  Google Scholar 

  • Pangestuti R, Kim S-K (2011b) Neuroprotective effects of marine algae. Mar Drugs 9:803–818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pascale A, Etcheberrigaray R (1999) Calcium alterations in Alzheimer’s disease: pathophysiology, models and therapeutic opportunities. Pharmacol Res 39:81–88

    Article  CAS  PubMed  Google Scholar 

  • Pinho BR, Ferreres F, Valentão P, Andrade PB (2013) Nature as a source of metabolites with cholinesterase‐inhibitory activity: an approach to Alzheimer’s disease treatment. J Pharm Pharmacol 65:1681–1700

    Article  CAS  PubMed  Google Scholar 

  • Qi H, Zhang Q, Zhao T, Chen R, Zhang H, Niu X, Li Z (2005) Antioxidant activity of different sulfate content derivatives of polysaccharide extracted from Ulva pertusa (Chlorophyta) in vitro. Int J Biol Macromol 37:195–199

    Article  CAS  PubMed  Google Scholar 

  • Rees TM, Brimijoin S (2003) The role of acetylcholinesterase in the pathogenesis of Alzheimer’s disease. Drugs Today (Barc) 39:75–83

    Article  CAS  Google Scholar 

  • Reichelt JL, Borowitzka MA (1984) Antibiotics from algae: results of a large scale screening programme. Hydrobiologia 116/117:158–168

    Article  Google Scholar 

  • Rengasamy KRR, Amoo SO, Aremu AO, Stirk WA, Gruz J, Šubrtová M, Doležal K, Van Staden J (2015) Phenolic profiles, antioxidant capacity, and acetylcholinesterase inhibitory activity of eight South African seaweeds. J Appl Phycol 27:1599–1605

    Article  CAS  Google Scholar 

  • Roberds SL, Anderson J, Basi G, Bienkowski MJ, Branstetter DG, Chen KS, Freedman S, Frigon NL, Games D, Hu K (2001) BACE knockout mice are healthy despite lacking the primary β-secretase activity in brain: implications for Alzheimer’s disease therapeutics. Hum Mol Genet 10:1317–1324

    Article  CAS  PubMed  Google Scholar 

  • Ryu G, Park SH, Kim ES, Choi BW, Ryu SY, Lee BH (2003) Cholinesterase inhibitory activity of two farnesylacetone derivatives from the brown alga Sargassum sagamianum. Arch Pharm Res 26:796–799

    Article  CAS  PubMed  Google Scholar 

  • Sangeetha RK, Bhaskar N, Baskaran V (2009) Comparative effects of beta-carotene and fucoxanthin on retinol deficiency induced oxidative stress in rats. Mol Cell Biochem 331:59–67

    Article  CAS  PubMed  Google Scholar 

  • Sarithakumari C, Kurup GM (2013) Alginic acid isolated from Sargassum wightii exhibits anti-inflammatory potential on type II collagen induced arthritis in experimental animals. Int Immunopharmacol 17:1108–1115

    Article  CAS  PubMed  Google Scholar 

  • Selkoe DJ (1997) Alzheimer’s disease: genotypes, phenotypes, and treatments. Science 275:630–631

    Article  CAS  PubMed  Google Scholar 

  • Soreq H, Seidman S (2001) Acetylcholinesterase—new roles for an old actor. Nat Rev Neurosci 2:294–302

    Article  CAS  PubMed  Google Scholar 

  • Sperling RA, Jack CR, Aisen PS (2011) Testing the right target and right drug at the right stage. Sci Transl Med 3:111cm133

    Article  Google Scholar 

  • Tang K, Hynan LS, Baskin F, Rosenberg RN (2006) Platelet amyloid precursor protein processing: a bio-marker for Alzheimer’s disease. J Neurol Sci 240:53–58

    Article  CAS  PubMed  Google Scholar 

  • Thorsett ED, Latimer LH (2000) Therapeutic approaches to Alzheimer’s disease. Curr Opin Chem Biol 4:377–382

    Article  CAS  PubMed  Google Scholar 

  • Tohgi H, Abe T, Hashiguchi K, Saheki M, Takahashi S (1994) Remarkable reduction in acetylcholine concentration in the cerebrospinal fluid from patients with Alzheimer type dementia. Neurosci Lett 177:139–142

    Article  CAS  PubMed  Google Scholar 

  • Tsang CK, Sagara A, Kamei Y (2001) Structure-activity relationship of a neurite outgrowth-promoting substance purified from the brown alga, Sargassum macrocarpum, and its analogues on PC12D cells. J Appl Phycol 13:349–357

    Article  CAS  Google Scholar 

  • Tsang CK, Ina A, Goto T, Kamei Y (2005) Sargachromenol, a novel nerve growth factor-potentiating substance isolated from Sargassum macrocarpum, promotes neurite outgrowth and survival via distinct signaling pathways in PC12D cells. Neuroscience 132:633–643

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Ooi EV, Ang PO Jr (2008) Antiviral activities of extracts from Hong Kong seaweeds. J Zhejiang Univ-Sc B 9:969–976

    Article  CAS  Google Scholar 

  • Wijesekara I, Yoon NY, Kim SK (2010) Phlorotannins from Ecklonia cava (Phaeophyceae): Biological activities and potential health benefits. Biofactors 36:408–414

    Article  CAS  PubMed  Google Scholar 

  • Yabuta Y, Fujimura H, Kwak CS, Enomoto T, Watanabe F (2010) Antioxidant activity of the phycoerythrobilin compound formed from a dried Korean purple laver (Porphyra sp.) during in vitro digestion. Food Sci Technol Res 16:347–352

    Article  CAS  Google Scholar 

  • Yan X, Chuda Y, Suzuki M, Nagata T (1999) Fucoxanthin as the major antioxidant in Hijikia fusiformis, a common edible seaweed. Biosci Biotechnol Biochem 63:605–607

  • Yang Y-I, Jung S-H, Lee K-T, Choi J-H (2014) 8, 8ʹ-Bieckol, isolated from edible brown algae, exerts its anti-inflammatory effects through inhibition of NF-kB signaling and ROS production in LPS-stimulated macrophages. Int Immunopharmacol 23:460–468

    Article  CAS  PubMed  Google Scholar 

  • Yang P, Liu D-Q, Liang T-J, Li J, Zhang H-Y, Liu A-H, Guo Y-W, Mao S-C (2015) Bioactive constituents from the green alga Caulerpa racemosa. Bioorg Med Chem 23:38–45

    Article  PubMed  CAS  Google Scholar 

  • Yoon NY, Chung HY, Kim HR, Choi JE (2008) Acetyl- and butyrylcholinesterase inhibitory activities of sterols and phlorotannins from Ecklonia stolonifera. Fisheries Sci 74:200–207

    Article  CAS  Google Scholar 

  • Yoon NY, Lee S-H, Kim S-K (2009) Phlorotannins from Ishige okamurae and their acetyl-and butyrylcholinesterase inhibitory effects. J Funct Foods 1:331–335

    Article  CAS  Google Scholar 

  • Yuen EC, Howe CL, Li Y, Holtzman DM, Mobley WC (1996) Nerve growth factor and the neurotrophic factor hypothesis. Brain Dev 18:362–368

    Article  CAS  PubMed  Google Scholar 

  • Zarros A (2009) In which cases is neuroprotection useful. Adv Alternat Thinking Neurosci 1:3–5

    Google Scholar 

  • Zhang H, Xiao X, Conte MM, Khalil Z, Capon RJ (2012) Spiralisones A–D: acylphloroglucinol hemiketals from an Australian marine brown alga, Zonaria spiralis. Org Biomol Chem 10:9671–9676

    Article  CAS  PubMed  Google Scholar 

  • Zhang FL, He Y, Zheng Y, Zhang WJ, Wang Q, Jia YJ, Song HL, An HT, Zhang HB, Qian YJ (2014) Therapeutic effects of fucoidan in 6-hydroxydopamine-lesioned rat model of Parkinson’s disease: role of NADPH oxidase-1. CNS Neurosci Ther 20:1036–1044

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Mousa Alghazwi is supported by a scholarship from The Ministry of Higher Education in Saudi Arabia. The research project is supported by Flinders Centre for Marine Bioproducts Development, Flinders University. WPG is supported by NHMRC Fellowship (535014) and Flinders Fellowship and the Flinders-CSU seeding grant.

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Alghazwi, M., Kan, Y.Q., Zhang, W. et al. Neuroprotective activities of natural products from marine macroalgae during 1999–2015. J Appl Phycol 28, 3599–3616 (2016). https://doi.org/10.1007/s10811-016-0908-2

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  • DOI: https://doi.org/10.1007/s10811-016-0908-2

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