Generic placeholder image

Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Review Article

Applications of Algal Polysaccharides and Derivatives in Therapeutic and Agricultural Fields

Author(s): Soukaina Bouissil, Guillaume Pierre, Zainab El Alaoui-Talibi, Philippe Michaud, C. El Modafar and Cedric Delattre*

Volume 25, Issue 11, 2019

Page: [1187 - 1199] Pages: 13

DOI: 10.2174/1381612825666190425162729

Price: $65

Abstract

Background: Recently, researchers have given more and more consideration to natural polysaccharides thanks to their huge properties such as stability, biodegradability and biocompatibility for food and therapeutics applications.

Methods: a number of enzymatic and chemical processes were performed to generate bioactive molecules, such as low molecular weight fractions and oligosaccharides derivatives from algal polysaccharides.

Results: These considerable characteristics allow algal polysaccharides and their derivatives such as low molecular weight polymers and oligosaccharides structures to have great potential to be used in lots of domains, such as pharmaceutics and agriculture etc.

Conclusion: The present review describes the mains polysaccharides structures from Algae and focuses on the currents agricultural (fertilizer, bio-elicitor, stimulators, signaling molecules and activators) and pharmaceutical (wound dressing, tissues engineering and drugs delivery) applications by using polysaccharides and/or their oligosaccharides derivatives obtained by chemical, physical and enzymatic processes.

Keywords: Agriculture, algae, biological applications, elicitation, oligosaccharides, pharmaceutics, polysaccharides.

[1]
Dumitriu S. Structural diversity and functional versatility New York: Marcel Dekker 2005; Xviii.
[2]
Rinaudo M. Seaweed polysaccharides. In: Kamerling JP (ed) Comprehensive glycoscience from chemistry to systems biology. 2007; vol 2: 691-735 [http://dx.doi.org/10.1016/B978-044451967-2/00140-9]
[3]
Mohnen D. Pectin structure and biosynthesis. Curr Opin Plant Biol 2008; 11(3): 266-77.
[http://dx.doi.org/10.1016/j.pbi.2008.03.006] [PMID: 18486536]
[4]
Badel S, Laroche C, Gardarin C, Bernardi T, Michaud P. New method showing the influence of matrix components in Leuconostoc mesenteroides biofilm formation. Appl Biochem Biotechnol 2008; 151(2-3): 364-70.
[http://dx.doi.org/10.1007/s12010-008-8199-y] [PMID: 18401560]
[5]
Delattre C, Pierre G, Laroche C, Michaud P. Production, extraction and characterization of microalgal and cyanobacterial exopolysaccharides. Biotechnol Adv 2016; 34(7): 1159-79.
[http://dx.doi.org/10.1016/j.biotechadv.2016.08.001] [PMID: 27530696]
[6]
Saeidy S, Nasirpour A, Djelveh G, et al. Rheological and functional properties of asafoetida gum Int J Biol Macromol 2018; 118(Pt A): 1168-73.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.06.177] [PMID: 30001603]
[7]
Cosenza VA, Navarro DA, Ponce NMA, Stortz CA. Seaweed polysaccharides: Structure and applications. Industrial Applications of Renewable Biomass Products 2017.
[http://dx.doi.org/10.1007/978-3-319-61288-1_3]
[8]
Kraan S. Algal Polysaccharides, Novel Applications and Outlook. Carbohydrates 2012.
[9]
Berteau O, Mulloy B. Sulfated fucans, fresh perspectives: structures, functions, and biological properties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide. Glycobiology 2003; 13(6): 29R-40R.
[http://dx.doi.org/10.1093/glycob/cwg058] [PMID: 12626402]
[10]
Bruce AS. Chemistry of β -glucans, in Chemistry, Biochemistry, and Biology of 1-3 Beta Glucans and Related Polysaccharides 2009.
[11]
Jiao G, Yu G, Zhang J, Ewart HS. Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Mar Drugs 2011; 9(2): 196-223.
[http://dx.doi.org/10.3390/md9020196] [PMID: 21566795]
[12]
Lahaye M, Robic A. Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 2007; 8(6): 1765-74.
[http://dx.doi.org/10.1021/bm061185q] [PMID: 17458931]
[13]
Barreteau H, Delattre C, Michaud P. Production of oligosaccharides as promising new food additive generation. Food Technol Biotechnol 2006; 44: 323-33.
[14]
Xu SY, Huang X, Cheong KL. Recent advances in marine algae polysaccharides: isolation, structure and activities. Mar Drugs 2017; 15(12): 388.
[http://dx.doi.org/10.3390/md15120388] [PMID: 29236064]
[15]
Delattre C, Fenoradosoa TA, Michaud P. Galactans: An overview of their most important sourcing and applications as natural polysaccharides. Braz Arch Biol Technol 2011; 54: 1075-92.
[http://dx.doi.org/10.1590/S1516-89132011000600002]
[16]
Pierre G, Delattre C, Laroche C, et al. Galactans and its applications. Polysaccharides 2014; 1: 1-37.
[17]
Kloareg B, Quatrano RS. Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr Mar Biol Annu Rev 1988; 26: 259-315.
[18]
Laurienzo P. Marine polysaccharides in pharmaceutical applications: An overview. Mar Drugs 2010; 8(9): 2435-65.
[http://dx.doi.org/10.3390/md8092435] [PMID: 20948899]
[19]
Schaeffer DJ, Krylov VS. Anti-HIV activity of extracts and compounds from algae and cyanobacteria. Ecotoxicol Environ Saf 2000; 45(3): 208-27.
[http://dx.doi.org/10.1006/eesa.1999.1862] [PMID: 10702339]
[20]
Güven KC, Özsoy Y, Ulutin ON. Anticoagulant, fibrinolytic and antiaggregant activity of carrageenans and alginic acid. Bot Mar 1991; 34: 429-32.
[http://dx.doi.org/10.1515/botm.1991.34.5.429]
[21]
Parish C. Pharmacological properties of a marine natural product. Biophys Acta 1987; 936: 55-9.
[22]
Nagaoka M, Shibata H, Kimura-Takagi I, et al. Anti-ulcer effects and biological activities of polysaccharides from marine algae. Biofactors 2000; 12(1-4): 267-74.
[http://dx.doi.org/10.1002/biof.5520120140] [PMID: 11216495]
[23]
Patier P, Yvin JC, Kloareg B, et al. Seaweed liquid fertilizer from Ascophyllum nodosum contains elicitors of plant D-glycanases. J Appl Phycol 1993; 5: 343-9.
[http://dx.doi.org/10.1007/BF02186237]
[24]
Bodin-Dubigeon C, Lahaye M, Barry JL. Human colonic bacterial degradability of dietary fibres from sea-lettuce (Ulva sp.). J Sci Food Agric 1997; 73: 149-59.
[http://dx.doi.org/10.1002/(SICI)1097-0010(199702)73:2<149:AID-JSFA685>3.0.CO;2-L]
[25]
Lahaye M. Marine algae as sources of fibres: determination of soluble and insoluble DF contents in some sea vegetables. J Sci Food Agric 1991; 54: 587-94.
[http://dx.doi.org/10.1002/jsfa.2740540410]
[26]
Ray B, Lahaye M. Cell-wall polysaccharides from the marine green alga Ulva rigida (Ulvales, Chlorophyta). Extraction and chemical composition. Carbohydr Res 1995; 274: 251-61.
[http://dx.doi.org/10.1016/0008-6215(95)00138-J]
[27]
Lahaye M, Jegou D, Buleon A. Chemical characteristics of insoluble glucans from the cell wall of the marine green alga Ulva lactuca (L.) Thuret. Carbohydr Res 1994; 262: 115-25.
[http://dx.doi.org/10.1016/0008-6215(94)84008-3]
[28]
Hentati F, Delattre C, Ursu AV, et al. Structural characterization and antioxidant activity of water-soluble polysaccharides from the Tunisian brown seaweed Cystoseira compressa. Carbohydr Polym 2018; 198: 589-600.
[http://dx.doi.org/10.1016/j.carbpol.2018.06.098] [PMID: 30093038]
[29]
Alginates GP. Carbohydr Polym 1988; 8: 161-82.
[http://dx.doi.org/10.1016/0144-8617(88)90001-X]
[30]
Draget KI, Smidsrød O, Skjak-Braek G. Alginates from Algae. In Biopolymers: Polysaccharides from eukaryotes. De Baets S., Vandamme E.J., Steinbüchel A. eds., Wileg-VCH, Germany, 2002; 215-244
[31]
Ertesvåg H, Valla S. Biosynthesis and applications of alginates. Polym Degrad Stabil 1998; 59: 85-91.
[http://dx.doi.org/10.1016/S0141-3910(97)00179-1]
[32]
Lim SJ, Aida WMW. Oligosaccharides engineering from plants and algae - Applications in Biotechnology and therapeutic. Minerva Biotecnol 2005; 17: 107-17.
[33]
Delattre C, Michaud P, Courtois B, et al. Oligosaccharides engineering from plants and algae - Applications in Biotechnology and therapeutic. Minerva Biotecnol 2005; 17: 107-17.
[34]
Hjerde T, Kristiansen TS, Stokke BT, et al. Conformation-dependent depolymerization kinetics of polysaccharides studied by viscosity measurements. Carbohydr Polym 1994; 24: 265-75.
[http://dx.doi.org/10.1016/0144-8617(94)90070-1]
[35]
Hu X, Jiang X, Aubree E, et al. Preparation and in vivo antitumor activity of kappa-carrageenan oligosaccharides. Pharm Biol 2006; 44: 646-50.
[http://dx.doi.org/10.1080/13880200601006848]
[36]
Yuan H, Song J, Li X, Li N, Dai J. Immunomodulation and antitumor activity of kappa-carrageenan oligosaccharides. Cancer Lett 2006; 243(2): 228-34.
[http://dx.doi.org/10.1016/j.canlet.2005.11.032] [PMID: 16410037]
[37]
Nardella A, Chaubet F, Boisson-Vidal C, Blondin C, Durand P, Jozefonvicz J. Anticoagulant low molecular weight fucans produced by radical process and ion exchange chromatography of high molecular weight fucans extracted from the brown seaweed Ascophyllum nodosum. Carbohydr Res 1996; 289: 201-8.
[http://dx.doi.org/10.1016/0008-6215(96)00110-3] [PMID: 8805780]
[38]
El Modafar C, Elgadda M, El Boutachfaiti R, et al. Induction of natural defense accompanied by salicylic acid-dependant systemic acquired resistance in tomato seedlings in response to bioelicitors isolated from green algae. Sci Hortic (Amsterdam) 2012; 138: 55-63.
[http://dx.doi.org/10.1016/j.scienta.2012.02.011]
[39]
Knutsen SH, Sletmoen M, Kristensen T, Barbeyron T, Kloareg B, Potin P. A rapid method for the separation and analysis of carrageenan oligosaccharides released by iota- and kappa -carrageenase. Carbohydr Res 2001; 331(1): 101-6.
[http://dx.doi.org/10.1016/S0008-6215(00)00324-4] [PMID: 11284500]
[40]
De Borba Gurpilhares D, Moreira TR, Da Luz Bueno J, et al. Algae’s sulfated polysaccharides modifications: Potential use of microbial enzymes. Process Biochem 2016; 51: 989-98.
[http://dx.doi.org/10.1016/j.procbio.2016.04.020]
[41]
Ustyuzhanina NE, Bilan MI, Ushakova NA, Usov AI, Kiselevskiy MV, Nifantiev NE. Fucoidans: pro- or antiangiogenic agents? Glycobiology 2014; 24(12): 1265-74.
[http://dx.doi.org/10.1093/glycob/cwu063] [PMID: 24973252]
[42]
Zaporozhets T, Besednova N. Prospects for the therapeutic application of sulfated polysaccharides of brown algae in diseases of the cardiovascular system review. Pharm Biol 2016; 54(12): 3126-35.
[http://dx.doi.org/10.1080/13880209.2016.1185444] [PMID: 27252012]
[43]
Takahashi H, Kawaguchi M, Kitamura K, et al. An exploratory study on the anti-inflammatory effects of fucoidan in relation to quality of life in advanced cancer patients. Integr Cancer Ther 2018; 17(2): 282-91.
[http://dx.doi.org/10.1177/1534735417692097] [PMID: 28627320]
[44]
Wang W, Wu J, Zhang X, et al. Inhibition of influenza a virus infection by fucoidan targeting viral neuraminidase and cellular EGFR pathway. Sci Rep 2017; 7: 40760.
[http://dx.doi.org/10.1038/srep40760] [PMID: 28094330]
[45]
Ushakova NA, Morozevich GE, Ustyuzhanina NE, et al. Anticoagulant activity of fucoidans from brown algae. Biochem (Moscow). Supp Series B: Biomed Chem 2009; 3: 77-83.
[46]
Rui X, Pan HF, Shao SL, Xu XM. Anti-tumor and anti-angiogenic effects of Fucoidan on prostate cancer: possible JAK-STAT3 pathway. BMC Complement Altern Med 2017; 17(1): 378.
[http://dx.doi.org/10.1186/s12906-017-1885-y] [PMID: 28764703]
[47]
Cumashi A, Ushakova NA, Preobrazhenskaya ME, et al. A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology 2007; 17(5): 541-52.
[http://dx.doi.org/10.1093/glycob/cwm014] [PMID: 17296677]
[48]
Croci DO, Cumashi A, Ushakova NA, et al. Fucans, but not fucomannoglucuronans, determine the biological activities of sulfated polysaccharides from Laminaria saccharina brown seaweed. PLoS One 2011; 6(2)e17283
[http://dx.doi.org/10.1371/journal.pone.0017283] [PMID: 21387013]
[49]
Ustyuzhanina NE, Ushakova NA, Zyuzina KA, et al. Influence of fucoidans on hemostatic system. Mar Drugs 2013; 11(7): 2444-58.
[http://dx.doi.org/10.3390/md11072444] [PMID: 23857111]
[50]
Li B, Lu F, Wei X, Zhao R. Fucoidan: structure and bioactivity. Molecules 2008; 13(8): 1671-95.
[http://dx.doi.org/10.3390/molecules13081671] [PMID: 18794778]
[51]
Zhao X, Xue CH, Li BF. Study of antioxidant activities of sulfated polysaccharides from Laminaria japonica. J Appl Phycol 2008; 20: 431-6.
[http://dx.doi.org/10.1007/s10811-007-9282-4]
[52]
Turnbull J, Powell A, Guimond S. Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell Biol 2001; 11(2): 75-82.
[http://dx.doi.org/10.1016/S0962-8924(00)01897-3] [PMID: 11166215]
[53]
Wang J, Liu L, Zhang Q, et al. Synthesized oversulphated, acetylated and benzoylated derivatives of fucoidan extracted from Laminaria japonica and their potential antioxidant activity in vitro. Food Chem 2009; 114: 1285-90.
[http://dx.doi.org/10.1016/j.foodchem.2008.10.082]
[54]
Nishino T, Nagumo T. Anticoagulant and antithrombin activities of oversulfated fucans. Carbohydr Res 1992; 229(2): 355-62.
[http://dx.doi.org/10.1016/S0008-6215(00)90581-0] [PMID: 1394292]
[55]
Qiu X, Amarasekara A, Doctor V. Effect of oversulfation on the chemical and biological properties of fucoidan. Carbohydr Polym 2006; 63: 224-8.
[http://dx.doi.org/10.1016/j.carbpol.2005.08.064]
[56]
Koyanagi S, Tanigawa N, Nakagawa H, Soeda S, Shimeno H. Oversulfation of fucoidan enhances its anti-angiogenic and antitumor activities. Biochem Pharmacol 2003; 65(2): 173-9.
[http://dx.doi.org/10.1016/S0006-2952(02)01478-8] [PMID: 12504793]
[57]
Kwak JY. Fucoidan as a marine anticancer agent in preclinical development. Mar Drugs 2014; 12(2): 851-70.
[http://dx.doi.org/10.3390/md12020851] [PMID: 24477286]
[58]
Chollet L, Saboural P, Chauvierre C, Villemin JN, Letourneur D, Chaubet F. Fucoidans in Nanomedicine. Mar Drugs 2016; 14(8): 145.
[http://dx.doi.org/10.3390/md14080145] [PMID: 27483292]
[59]
Mathew L, Burney M, Gaikwad A, et al. Preclinical evaluation of safety of fucoidan extracts from Undaria pinnatifida and Fucus vesiculosus for use in cancer treatment. Integr Cancer Ther 2017; 16(4): 572-84.
[http://dx.doi.org/10.1177/1534735416680744] [PMID: 29096568]
[60]
Venkatesan J, Bhatnagar I, Kim SK. Chitosan-alginate biocomposite containing fucoidan for bone tissue engineering. Mar Drugs 2014; 12(1): 300-16.
[http://dx.doi.org/10.3390/md12010300] [PMID: 24441614]
[61]
Puvaneswary S, Talebian S, Raghavendran HB, et al. Fabrication and in vitro biological activity of βTCP-Chitosan-Fucoidan composite for bone tissue engineering. Carbohydr Polym 2015; 134: 799-807.
[http://dx.doi.org/10.1016/j.carbpol.2015.07.098] [PMID: 26428187]
[62]
Lee JB, Hayashi K, Hashimoto M, Nakano T, Hayashi T. Novel antiviral fucoidan from sporophyll of Undaria pinnatifida (Mekabu). Chem Pharm Bull (Tokyo) 2004; 52(9): 1091-4.
[http://dx.doi.org/10.1248/cpb.52.1091] [PMID: 15340195]
[63]
Ahmadi A, Moghadamtousi SZ, Abubakar S, et al. Antiviral potential of algae polysaccharides isolated from marine sources: A review. BioMed Res Int 2015; 2015: 1-10.
[http://dx.doi.org/10.1155/2015/825203]
[64]
Mandal P, Mateu CG, Chattopadhyay K, Pujol CA, Damonte EB, Ray B. Structural features and antiviral activity of sulphated fucans from the brown seaweed Cystoseira indica. Antivir Chem Chemother 2007; 18(3): 153-62.
[http://dx.doi.org/10.1177/095632020701800305] [PMID: 17626599]
[65]
Raghavendran HRB, Srinivasan P, Rekha S. Immunomodulatory activity of fucoidan against aspirin-induced gastric mucosal damage in rats. Int Immunopharmacol 2011; 11(2): 157-63.
[http://dx.doi.org/10.1016/j.intimp.2010.11.002] [PMID: 21084063]
[66]
Teng H, Yang Y, Wei H, et al. Fucoidan suppresses hypoxia-induced lymphangiogenesis and lymphatic metastasis in mouse hepatocarcinoma. Mar Drugs 2015; 13(6): 3514-30.
[http://dx.doi.org/10.3390/md13063514] [PMID: 26047481]
[67]
Yang Y, Gao Z, Ma Y, et al. Fucoidan inhibits lymphangiogenesis by downregulating the expression of VEGFR3 and PROX1 in human lymphatic endothelial cells. Oncotarget 2016; 7(25): 38025-35.
[http://dx.doi.org/10.18632/oncotarget.9443] [PMID: 27203545]
[68]
Cong Q, Chen H, Liao W, et al. Structural characterization and effect on anti-angiogenic activity of a fucoidan from Sargassum fusiforme. Carbohydr Polym 2016; 136: 899-907.
[http://dx.doi.org/10.1016/j.carbpol.2015.09.087] [PMID: 26572427]
[69]
Usoltseva RV, Anastyuk SD, Ishina IA, et al. Structural characteristics and anticancer activity in vitro of fucoidan from brown alga Padina boryana. Carbohydr Polym 2018; 184: 260-8.
[http://dx.doi.org/10.1016/j.carbpol.2017.12.071] [PMID: 29352918]
[70]
Faggio C, Morabito M, Minicante SA, et al. Potential use of polysaccharides from the brown alga Undaria pinnatifida as anticoagulants. Braz Arch Biol Technol 2015; 58: 798-804.
[http://dx.doi.org/10.1590/S1516-8913201500400]
[71]
Camara RBG, Costa LS, Fidelis GP, et al. Heterofucans from the brown seaweed Canistrocarpus cervicornis with anticoagulant and antioxidant activities. Mar Drugs 2011; 9(1): 124-38.
[http://dx.doi.org/10.3390/md9010124] [PMID: 21339951]
[72]
Leal D, Mansilla A, Matsuhiro B, et al. Chemical structure and biological properties of sulfated fucan from the sequential extraction of subAntarctic Lessonia sp (Phaeophyceae). Carbohydr Polym 2018; 199: 304-13.
[http://dx.doi.org/10.1016/j.carbpol.2018.07.012] [PMID: 30143133]
[73]
de Sousa Pinheiro T, Nascimento Santos MS, Will Castro LSEP, et al. A fucan of a brown seaweed and its antitumoral property on HT-29 and immunomodulatory activity in murine RAW 264.7 macrophage cell line. J Appl Phycol 2017; 29: 2061-75.
[http://dx.doi.org/10.1007/s10811-017-1075-9]
[74]
Dinesh S, Menon T, Hanna LE, Suresh V, Sathuvan M, Manikannan M. In vitro anti-HIV-1 activity of fucoidan from Sargassum swartzii. Int J Biol Macromol 2016; 82: 83-8.
[http://dx.doi.org/10.1016/j.ijbiomac.2015.09.078] [PMID: 26472515]
[75]
Menezes MM, Nobre LTDB, Rossi GR, et al. A low-molecular-weight galactofucan from the seaweed, Spatoglossum schröederi, binds fibronectin and inhibits capillary-like tube formation in vitro. Int J Biol Macromol 2018; 111: 1067-75.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.01.119] [PMID: 29366897]
[76]
Li X, Li X, Zhang Q, Zhao T. Low molecular weight fucoidan and its fractions inhibit renal epithelial mesenchymal transition induced by TGF-β1 or FGF-2. Int J Biol Macromol 2017; 105(Pt 2): 1482-90.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.06.058] [PMID: 28627391]
[77]
Tabriz AG, Hermida MA, Leslie NR, Shu W. Three-dimensional bioprinting of complex cell laden alginate hydrogel structures. Biofabrication 2015; 7(4)045012
[http://dx.doi.org/10.1088/1758-5090/7/4/045012] [PMID: 26689257]
[78]
Gepp MM, Fischer B, Schulz A, et al. Bioactive surfaces from seaweed-derived alginates for the cultivation of human stem cells. J Appl Phycol 2017; 29: 2451-61.
[http://dx.doi.org/10.1007/s10811-017-1130-6]
[79]
Fatoni A, Dwiasi DW, Hermawan D. Alginate cryogel based glucose biosensor. IOP Cong Ser: Mater Sci Eng. 2016; 107: 012010.
[80]
Ng WY, Migotto A, Ferreira TS, Lopes LB. Monoolein-alginate beads as a platform to promote adenosine cutaneous localization and wound healing. Int J Biol Macromol 2017; 102: 1104-11.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.04.094] [PMID: 28456646]
[81]
Devillard R, Rémy M, Kalisky J, et al. In vitro assessment of a collagen/alginate composite scaffold for regenerative endodontics. Int Endod J 2017; 50(1): 48-57.
[http://dx.doi.org/10.1111/iej.12591] [PMID: 26650723]
[82]
Rahim SA, Carter PA, Elkordy AA. Design and evaluation of effervescent floating tablets based on hydroxyethyl cellulose and sodium alginate using pentoxifylline as a model drug. Drug Des Devel Ther 2015; 9: 1843-57.
[PMID: 25848220]
[83]
Espona-Noguera A, Ciriza J, Cañibano-Hernández A, et al. Tunable injectable alginate-based hydrogel for cell therapy in Type 1 Diabetes Mellitus. Int J Biol Macromol 2018; 107(Pt A): 1261-9.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.09.103] [PMID: 28962846]
[84]
Thu QTM, Luong DV, Nu NT, et al. Effect of sulfation on the structure and anticoagulant activity of ulvan extracted from green seaweed Ulva reticulata. J Sci Technol 2016; 54: 373-9.
[85]
Adrien A, Dufour D, Baudouin S, Maugard T, Bridiau N. Evaluation of the anticoagulant potential of polysaccharide-rich fractions extracted from macroalgae. Nat Prod Res 2017; 31(18): 2126-36.
[http://dx.doi.org/10.1080/14786419.2017.1278595] [PMID: 28147712]
[86]
Rahimi F, Tabarsa M, Rezaei M. Ulvan from green algae Ulva intestinalis: optimization of ultrasound-assisted extraction and antioxidant activity. J Appl Phycol 2016; 28: 1-12.
[http://dx.doi.org/10.1007/s10811-016-0824-5]
[87]
Thanh TT, Quach TMT, Nguyen TN, Vu Luong D, Bui ML, Tran TT. Structure and cytotoxic activity of ulvan extracted from green seaweed Ulva lactuca. Int J Biol Macromol 2016; 93(Pt A): 695- 702.
[http://dx.doi.org/10.1016/j.ijbiomac.2016.09.040] [PMID: 27637450]
[88]
Qi H, Sun Y. Antioxidant activity of high sulfate content derivative of ulvan in hyperlipidemic rats. Int J Biol Macromol 2015; 76: 326-9.
[http://dx.doi.org/10.1016/j.ijbiomac.2015.03.006] [PMID: 25773592]
[89]
Tran TTV, Truong HB, Tran NHV, et al. Structure, conformation in aqueous solution and antimicrobial activity of ulvan extracted from green seaweed Ulva reticulata. Nat Prod Res 2017; 4: 1-6.
[http://dx.doi.org/10.1080/14786419.2017.1408095] [PMID: 29199449]
[90]
Dash M, Samal SK, Bartoli C, et al. Biofunctionalization of ulvan scaffolds for bone tissue engineering. ACS Appl Mater Interfaces 2014; 6(5): 3211-8.
[http://dx.doi.org/10.1021/am404912c] [PMID: 24494863]
[91]
Kim HJ, Kim WJ, Koo BW, et al. Anticancer activity of sulfated polysaccharides isolated from the antarctic red seaweed Iridaea cordata. Ocean Polar Res 2016; 38: 129-37.
[http://dx.doi.org/10.4217/OPR.2016.38.2.129]
[92]
Sudharsan S, Giji S, Seedevi P, Vairamani S, Shanmugam A. Isolation, characterization and bioactive potential of sulfated galactans from Spyridia hypnoides (Bory) Papenfuss. Int J Biol Macromol 2018; 109: 589-97.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.12.097] [PMID: 29273523]
[93]
Mendes GS, Duarte MER, Colodi FG, et al. Structure and anti-metapneumovirus activity of sulfated galactans from the red seaweed Cryptonemia seminervis. Carbohydr Polym 2014; 101: 313-23.
[http://dx.doi.org/10.1016/j.carbpol.2013.09.026] [PMID: 24299779]
[94]
Extraction process optimization of sulfated galactan-rich fractions from Hypnea musciformis in order to obtain antioxidant, anticoagulant, or immunomodulatory polysaccharides. J Appl Phycol 2016; 28: 1931-42.
[http://dx.doi.org/10.1007/s10811-015-0705-3]
[95]
Flórez N, Gonzalez-Munoz MJ, Ribeiro D, Fernandes E, Dominguez H, Freitas M. Algae polysaccharides’ chemical characterization and their role in the inflammatory process. Curr Med Chem 2017; 24(2): 149-75.
[http://dx.doi.org/10.2174/0929867323666161028160416] [PMID: 27804878]
[96]
Pereira RF, Bártolo PJ. Traditional Therapies for Skin Wound Healing. Adv Wound Care (New Rochelle) 2016; 5(5): 208-29.
[http://dx.doi.org/10.1089/wound.2013.0506] [PMID: 27134765]
[97]
Yegappan R, Selvaprithiviraj V, Amirthalingam S, Jayakumar R. Carrageenan based hydrogels for drug delivery, tissue engineering and wound healing. Carbohydr Polym 2018; 198: 385-400.
[http://dx.doi.org/10.1016/j.carbpol.2018.06.086] [PMID: 30093014]
[98]
Markeb AA, El-Maali NA, Sayed DM, et al. Synthesis, structural characterization, and preclinical efficacy of a novel paclitaxel-loaded alginate nanoparticle for breast cancer treatment. Int J Breast Cancer 2016; 20167549372
[http://dx.doi.org/10.1155/2016/7549372] [PMID: 27660726]
[99]
Bouhlal R, Haslin C, Chermann JC, et al. Antiviral activities of sulfated polysaccharides isolated from Sphaerococcus coronopifolius (Rhodophytha, Gigartinales) and Boergeseniella thuyoides (Rhodophyta, Ceramiales). Mar Drugs 2011; 9(7): 1187-209.
[http://dx.doi.org/10.3390/md9071187] [PMID: 21822410]
[100]
Guan J, Li L, Mao S. Applications of carrageenan in advanced drug delivery.Seaweed polysaccharides Isolation, biological and biomedical applications 2017; 283-304.
[http://dx.doi.org/10.1016/B978-0-12-809816-5.00015-3]
[101]
Heil M, Bostock RM. Induced systemic resistance (ISR) against pathogens in the context of induced plant defences. Ann Bot 2002; 89(5): 503-12.
[http://dx.doi.org/10.1093/aob/mcf076] [PMID: 12099523]
[102]
Walters D, Walsh D, Newton A, Lyon G. Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathology 2005; 95(12): 1368-73.
[http://dx.doi.org/10.1094/PHYTO-95-1368] [PMID: 18943546]
[103]
Anderson AJ, Blee KA, Yang KY. Commercialization of plant systemic defence activation: theory, problems and successes. Multigenic and Induced Systemic Resistance in Plants 2006; pp. 386-414.
[http://dx.doi.org/10.1007/0-387-23266-4_17]
[104]
Walters DR, Fountaine JM. Practical application of induced resistance to plant diseases: An appraisal of effectiveness under field conditions. J Agric Sci 2009; 147: 523-35.
[http://dx.doi.org/10.1017/S0021859609008806]
[105]
Vallad GE, Goodman RM. Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci 2004; 44: 1920-34.
[http://dx.doi.org/10.2135/cropsci2004.1920]
[106]
Nürnberger T, Scheel D. Signal transmission in the plant immune response. Trends Plant Sci 2001; 6(8): 372-9.
[http://dx.doi.org/10.1016/S1360-1385(01)02019-2] [PMID: 11495791]
[107]
Ebel J, Mithöfer A. Early events in the elicitation of plant defense. Planta 1998; 206: 335-48.
[http://dx.doi.org/10.1007/s004250050409]
[108]
Bari R, Jones JD. Role of plant hormones in plant defence responses. Plant Mol Biol 2009; 69(4): 473-88.
[http://dx.doi.org/10.1007/s11103-008-9435-0] [PMID: 19083153]
[109]
Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC. Networking by small-molecule hormones in plant immunity. Nat Chem Biol 2009; 5(5): 308-16.
[http://dx.doi.org/10.1038/nchembio.164] [PMID: 19377457]
[110]
Bart RS, Chern M, Vega-Sánchez ME, Canlas P, Ronald PC. Rice Snl6, a cinnamoyl-CoA reductase-like gene family member, is required for NH1-mediated immunity to Xanthomonas oryzae pv. oryzae. PLoS Genet 2010; 6(9)e1001123
[http://dx.doi.org/10.1371/journal.pgen.1001123] [PMID: 20862311]
[111]
Gallego-Giraldo L, Jikumaru Y, Kamiya Y, Tang Y, Dixon RA. Selective lignin downregulation leads to constitutive defense response expression in alfalfa (Medicago sativa L.). New Phytol 2011; 190(3): 627-39.
[http://dx.doi.org/10.1111/j.1469-8137.2010.03621.x] [PMID: 21251001]
[112]
Klarzynski O, Fritig B. Stimulation des défenses naturelles des plantes C R Acad Sci Paris, Sciences de la vie 2001; 324: 953-63.
[113]
Elboutachfaiti R, Delattre C, Michaud P, Courtois B, Courtois J. Oligogalacturonans production by free radical depolymerization of polygalacturonan. Int J Biol Macromol 2008; 43(3): 257-61.
[http://dx.doi.org/10.1016/j.ijbiomac.2008.06.003] [PMID: 18601947]
[114]
Cluzet S, Torregrosa C, Jacquet C, et al. Gene expression profiling and protection of Medicago truncatula against a fungal infection in response to an elicitor from green algae Ulva spp. Plant Cell Environ 2004; 27: 917-28.
[http://dx.doi.org/10.1111/j.1365-3040.2004.01197.x]
[115]
Jaulneau V, Lafitte C, Jacquet C, et al. Ulvan, a sulfated polysaccharide from green algae, activates plant immunity through the jasmonic acid signaling pathway. J Biomed Biotechnol 2010; 2010525291
[http://dx.doi.org/10.1155/2010/525291] [PMID: 20445752]
[116]
De Freitas MB, Stadnik MJ. Ulvan-Induced Resistance in Arabidopsis Thaliana against Alternaria Brassicicola Requires Reactive Oxygen Species Derived from NADPH Oxidase. Physiol Mol Plant Pathol 2015; 90: 49-56.
[http://dx.doi.org/10.1016/j.pmpp.2015.03.002]
[117]
Paulert R, Ebbinghaus D, Urlass C, et al. Priming of the oxidative burst in rice and wheat cell cultures by ulvan, a polysaccharide from green macroalgae, and enhanced resistance against powdery mildew in wheat and barley plants. Plant Pathol 2010; 59: 634-42.
[http://dx.doi.org/10.1111/j.1365-3059.2010.02300.x]
[118]
Jaulneau V, Lafitte C, Corio-Costet MF, et al. An Ulva armoricana extract protects plants against three powdery mildew pathogens. Eur J Plant Pathol 2011; 131: 393.
[http://dx.doi.org/10.1007/s10658-011-9816-0]
[119]
El Boutachfaiti R, Delattre C, Petit E, et al. Improved isolation of glucuronan from algae and the production of glucuronic acid oligosaccharides using a glucuronan lyase. Carbohydr Res 2009; 344: 1670-5.
[http://dx.doi.org/10.1016/j.carres.2009.05.031]
[120]
de Freitas MB, Stadnik MJ. Race-specific and ulvan-induced defense responses in bean (Phaseolus vulgaris) against Colletotrichum lindemuthianum. Physiol Mol Plant Pathol 2012; 78: 8-13.
[http://dx.doi.org/10.1016/j.pmpp.2011.12.004]
[121]
Abouraïcha E, El Alaoui-Talibi Z, El Boutachfaiti R, et al. Induction of natural defense and protection against Penicillium expansum and Botrytis cinerea in apple fruit in response to bioelicitors isolated from green algae. Sci Hortic (Amsterdam) 2015; 181: 121-8.
[http://dx.doi.org/10.1016/j.scienta.2014.11.002]
[122]
Ben Salah I, Aghrouss S, Douira A, et al. Seaweed polysaccharides as bio-elicitors of natural defenses in olive trees against verticillium wilt of olive. J Plant Interact 2018; 13: 248-55.
[http://dx.doi.org/10.1080/17429145.2018.1471528]
[123]
Klarzynski O, Descamps V, Plesse B, Yvin JC, Kloareg B, Fritig B. Sulfated fucan oligosaccharides elicit defense responses in tobacco and local and systemic resistance against tobacco mosaic virus. Mol Plant Microbe Interact 2003; 16(2): 115-22.
[http://dx.doi.org/10.1094/MPMI.2003.16.2.115] [PMID: 12575745]
[124]
Chandía NP, Matsuhiro B. Characterization of a fucoidan from Lessonia vadosa (Phaeophyta) and its anticoagulant and elicitor properties. Int J Biol Macromol 2008; 42(3): 235-40.
[http://dx.doi.org/10.1016/j.ijbiomac.2007.10.023] [PMID: 18054382]
[125]
Mercier L, Lafitte C, Borderies G, et al. The algal polysaccharide carrageenans can act as an elicitor of plant defence. New Phytol 2001; 149: 43-51.
[http://dx.doi.org/10.1046/j.1469-8137.2001.00011.x]
[126]
Jayaraj J, Wan A, Rahman M, et al. Seaweed extract reduces foliar fungal diseases on carrot. Crop Prot 2008; 27: 1360-6.
[http://dx.doi.org/10.1016/j.cropro.2008.05.005]
[127]
Schons RF, de Freitas MB, Stadnik MJ. Persistence of ulvan induced resistance and effect of inoculums concentration in the control of bean anthracnose. Biosci J 2011; 27: 544-51.
[128]
Araujo L, Stadnik MJ. Cultivar-specific and ulvan-induced resistance of apple plants to Glomerella leaf spot are associated with enhanced activity of peroxidases. Acta Sci Agron 2013; 35: 287-93.
[http://dx.doi.org/10.4025/actasciagron.v35i3.16174]
[129]
Briand X, Cluzet S, Dumas B, et al. Use of ulvans as elicitors of mechanisms for nitrogen absorption and protein synthesis WO2005094581A1 2005.
[130]
Chandía NP, Matsuhiro B, Mejías E, et al. Alginic acids in Lessonia vadosa: partial hydrolysis and elicitor properties of the polymannuronic acid fraction. J Appl Phycol 2004; 16: 127-33.
[http://dx.doi.org/10.1023/B:JAPH.0000044778.44193.a8]
[131]
Laporte D, Vera J, Chandía NP, et al. Structurally unrelated algal oligosaccharides differentially stimulate growth and defense against tobacco mosaic virus in tobacco plants. J Appl Phycol 2007; 19: 79-88.
[http://dx.doi.org/10.1007/s10811-006-9114-y]
[132]
Akimoto C, Aoyagi H, Dicosmo F, Tanaka H. Synergistic effect of active oxygen species and alginate on chitinase production by Wasabia japonica cells and its application. J Biosci Bioeng 2000; 89(2): 131-7.
[http://dx.doi.org/10.1016/S1389-1723(00)88726-5] [PMID: 16232715]
[133]
Hu J, Shi B, Ojokoh ES, et al. Effects of alginate oligosaccharides on the accumulation of glyceollins in soybean. Sc Agr Sininica 2012; 45: 1576-86.
[134]
Zhang S, Tang W, Jiang L, et al. Elicitor activity of algino-oligosaccharide and its potential application in protection of rice plant (Oryza saliva L.) against Magnaporthe grisea. Biotechnol Biotechnol Equip 2015; 29: 646-52.
[http://dx.doi.org/10.1080/13102818.2015.1039943]
[135]
Steimetz E, Trouvelot S, Gindro K, et al. Influence of leaf age on induced resistance in grapevine against Plasmopara viticola. Physiol Mol Plant Pathol 2012; 79: 89-96.
[http://dx.doi.org/10.1016/j.pmpp.2012.05.004]
[136]
Bi F, Iqbal S, Arman M, et al. Carrageenan as an elicitor of induced secondary metabolites and its effects on various growth characters of chickpea and maize plants. J Saudi Chem Soc 2011; 15: 269-73.
[http://dx.doi.org/10.1016/j.jscs.2010.10.003]
[137]
Zhao J, Zhu WH, Hu Q, et al. Improvement of indole alkaloid production in Catharanthus roseus cell cultures by osmotic shock. Biotechnol Lett 2000; 22: 1227-31.
[http://dx.doi.org/10.1023/A:1005653113794]
[138]
Xu A, Zhan JC, Huang WD. Oligochitosan and sodium alginate enhance stilbene production and induce defense responses in Vitis vinifera cell suspension cultures. Acta Physiol Plant 2015; 37: 144.
[http://dx.doi.org/10.1007/s11738-015-1900-1]
[139]
An QD, Zhang GL, Wu HT, et al. Alginate-deriving oligosaccharide production by alginase from newly isolated Flavobacterium sp. LXA and its potential application in protection against pathogens. J Appl Microbiol 2009; 106(1): 161-70.
[http://dx.doi.org/10.1111/j.1365-2672.2008.03988.x] [PMID: 19054241]
[140]
Patier P, Potin P, Rochas C, et al. Free or silica-bound oligokappa-carrageenans elicit laminarinase activity in Rubus cells and protoplasts. Plant Sci 1995; 110: 27-35.
[http://dx.doi.org/10.1016/0168-9452(95)04182-T]
[141]
Vera J, Castro J, Contreras RA, et al. Oligo-carrageenans induce a long-term and broad-range protection against pathogens in tobacco plants (var. Xanthi). Physiol Mol Plant Pathol 2012; 79: 31-9.
[http://dx.doi.org/10.1016/j.pmpp.2012.03.005]
[142]
Sangha JS, Ravichandran S, Prithiviraj K, et al. Sulfated macroalgal polysaccharides λ-carrageenan and ι-carrageenan differentially alter Arabidopsis thaliana resistance to Sclerotinia sclerotiorum. Physiol Mol Plant Pathol 2010; 75: 38-45.
[http://dx.doi.org/10.1016/j.pmpp.2010.08.003]
[143]
Kobayashi A, Tai A, Kanzaki H, et al. Elicitor-active oligosaccharides from algal laminaran stimulate the production of antifungal compounds in alfalfa. Z Naturforsch C Bio Sci 1993; 48: 575-9.
[http://dx.doi.org/10.1515/znc-1993-7-808]
[144]
Keen NT, Yoshikawa M. β-1, 3-Endoglucanase from soybean releases elicitor-active carbohydrates from fungus cell walls. Plant Physiol 1983; 71(3): 460-5.
[http://dx.doi.org/10.1104/pp.71.3.460] [PMID: 16662849]
[145]
Inui H, Yamaguchi Y, Hirano S. Elicitor actions of N-acetylchitooligosaccharides and laminarioligosaccharides for chitinase and L-phenylalanine ammonia-lyase induction in rice suspension culture. Biosci Biotechnol Biochem 1997; 61(6): 975-8.
[http://dx.doi.org/10.1271/bbb.61.975] [PMID: 9214757]
[146]
Cardinale F, Jonak C, Ligterink W, Niehaus K, Boller T, Hirt H. Differential activation of four specific MAPK pathways by distinct elicitors. J Biol Chem 2000; 275(47): 36734-40.
[http://dx.doi.org/10.1074/jbc.M007418200] [PMID: 10973984]
[147]
Aziz A, Poinssot B, Daire X, et al. Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Mol Plant Microbe Interact 2003; 16(12): 1118-28.
[http://dx.doi.org/10.1094/MPMI.2003.16.12.1118] [PMID: 14651345]
[148]
Klarzynski O, Plesse B, Joubert JM, et al. Linear β-1,3 glucans are elicitors of defense responses in tobacco. Plant Physiol 2000; 124(3): 1027-38.
[http://dx.doi.org/10.1104/pp.124.3.1027] [PMID: 11080280]
[149]
Ménard R, de Ruffray P, Fritig B, Yvin JC, Kauffmann S. Defense and resistance-inducing activities in tobacco of the sulfated β-1,3 glucan PS3 and its synergistic activities with the unsulfated molecule. Plant Cell Physiol 2005; 46(12): 1964-72.
[http://dx.doi.org/10.1093/pcp/pci212] [PMID: 16215271]
[150]
van Aubel G, Cambier P, Dieu M, Van Cutsem P. Plant immunity induced by COS-OGA elicitor is a cumulative process that involves salicylic acid. Plant Sci 2016; 247: 60-70.
[http://dx.doi.org/10.1016/j.plantsci.2016.03.005] [PMID: 27095400]
[151]
Conclusion on pesticide peer review regarding the risk assessment of the active substance heptamaloxyloglucan. EFSA Scientific Report 2009; 334: 1-52.
[152]
Sobhy IS, Erb M, Lou Y, Turlings TCJ. The prospect of applying chemical elicitors and plant strengtheners to enhance the biological control of crop pests. Philos Trans R Soc Lond B Biol Sci 2014; 369(1639)20120283
[http://dx.doi.org/10.1098/rstb.2012.0283] [PMID: 24535390]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy