Antiviral Effects and Mechanisms of Action of Water Extracts and Polysaccharides of Microalgae and Cyanobacteria
PDF

Keywords

Microalgae (MA)
cyanobacteria (CB)
polysaccharides (PS)
exopolysaccharides (EPS)
antiviral, anti-inflammatory
antioxidant and immunomodulatory activities

How to Cite

Besednova, N. N. ., Andryukov, B. G. ., Kuznetsova, T. A. ., Zaporozhets, T. S. ., Kryzhanovsky, S. P. ., Ermakova, S. P. ., & Shchelkanov, M. Y. . (2022). Antiviral Effects and Mechanisms of Action of Water Extracts and Polysaccharides of Microalgae and Cyanobacteria. Journal of Pharmacy and Nutrition Sciences, 12, 54–73. https://doi.org/10.29169/1927-5951.2022.12.05

Abstract

Microalgae (MA) and cyanobacteria (CB) are currently attracting much attention from scientists due to the high biological activity of many secondary metabolites of these aquatic organisms. This review presents up-to-date modern data on the prospects for using polysaccharides (PS) of these marine aquatic organisms as effective and practically safe antiviral agents. These natural biopolymers are polyvalent compounds, which allows them to bind to several complementary biological target receptors. Particular emphasis is placed on the exopolysaccharides (EPS) Spirulina sp. (Arthrospira sp.), Porphyridium sp., Chlorella sp., and Euglena sp., whose antiviral activity makes them promising for the creation of drugs, biologically active food supplements, and products for functional nutrition. The mechanisms of the biological action of PS and the targets of these compounds are presented with a brief description of PS's anti-inflammatory, immunomodulatory and antioxidant actions, which make the most significant contribution to the antiviral effects. The authors hope to draw the attention of researchers to the use of water extracts and polysaccharides of microalgae and cyanobacteria as potential broad-spectrum antiviral agents that can become the basis for new antivirus strategies.

https://doi.org/10.29169/1927-5951.2022.12.05
PDF

References

Lvov DK, Shchelkanov MYu, Alkhovsky SV, et al. Zoonotic viruses of Northern Eurasia. Taxonomy and Ecology. Academic Press, 2015; p. 452.

Pagarete A, Ramos AS, Puntervoll P, et al. Antiviral potential of algal metabolites – a comprehensive review. Mar Drugs 2021; 19(2): 94. https://doi.org/10.3390/md19020094

Yan X, Xu X, Wang M, et al. Climate warming and cyanobacteria blooms: looks at their relationships from a new perspective. Water Research 2017; 125(15): 449-457. https://doi.org/10.1016/j.watres.2017.09.008

Ferrazzano GF, Papa C, Pollio A, et al. Cyanobacteria and microalgae as sources of functional foods to improve human general and oral health. Molecules 2020; 25(21): 5164. https://doi.org/10.3390/molecules25215164

Priyadarshani I, Rath B: Bioactive compounds from microalgae and cyanobacteria: utility and applications. Int J Pharm Sci Res 2012; 3(11): 4123-4130.

Bremer S. Microalgae as a source for antibiotic discovery; The Pharmaceutical Journal 2015; https://doi.org/10.1211/PJ.2015.20068909

Barzkar N, Jahromi ST, Poorsaheli HB, Vianello F. Metabolites from marine microorganisms, micro, and macroalgae: immense scope for pharmacology. Mar. Drugs 2019; 17(8): 464. https://doi.org/10.3390/md17080464

Ahmadi, A.; Zorofchian Moghadamtousi, S.; Abubakar, S.; Zandi, K. Antiviral potential of algae polysaccharides isolated from marine sources: A review. BioMed Res Int 2015; 30: 1967-1976. https://doi.org/10.1155/2015/825203

Iha RK, Zi-rong X. Biomedical compounds from marine organisms. Marine Drugs 2004; 2(3): 123-146.

Carbone DA, Pellone P, Lubritto C, Ciniglia C. Evaluation of microalgae antiviral activity and their bioactive compounds. Antibiotics 2021; 10: 746. https://doi.org/10.3390/antibiotics10060746

Ahirwar A, Kesharwani K, Deka R, et al. Microalgae drugs: a promising therapeutic reserve for the future. J Biotechnology 2022; 349: 32-46. https://doi.org/10.1016/j.jbiotec.2022.03.012

Wu J, Gu X, Yang D, et al. Bioactive substances and potentiality of marine microalgae. Food Sci Nutr 2021; 9(9): 5279-5292. https://doi.org/10.1002/fsn3.2471

Raposo MF, de Morais RMSC, de Morais AMMB. Bioactivity and application of sulfated polysaccharides from marine microalgae. Mar Drugs 2013; 11: 233-252; https://doi.org/10.3390/md1010233

Gargouch N, Elleuch F, Karkouch I, et al. Potential of exopolysaccharide from Porphyridium marinum to contend with bacterial proliferation, biofilm formation and brest cancer. Mar Drugs 2021; 19(2): 66. https://doi.org/10.3390/md19020066

Delattre C, Pierre G, Laroche C, Michaud P. Production, extraction and characterization of microalgal and cyanobacterial exopolysaccharides. Biotechnol Adv 2016; 34(7): 1159-1179. https://doi.org/10.1016/j.biotechadv.2016.08.001

Gaignard C, Laroche C, Pierre G, et al. Screening of marine microalgae: investigation of new exopolysaccharide producers. Algal Research 2019; 44: 101711. https://doi.org/10.1016/j.algal.2019

Casas-Arrojo V, Decara J, Arrojo-Agudo MA, et al. Immunomodulatory, antioxidant activity and cytotoxic effect of sulfated polysaccharides from Porphyridium cruentum (S.F. Gray) Nageli. Biomolecules 2021; 24. https://doi.org/10.3390/biom11040488

Costa JAV, Lucas BF, Alvarenga AGP, et al. Microalgae polysaccharides: an overview of production, characterization and potential applications. Polysaccharides 2021; 2: 759-772. https://doi.org/10.3390/polysaccharides.2040046

Patel AK, Singhania RR, Awasth MK, et al. Emerging prospects of macro- and microalgae as prebiotic. Microb Cell Fact 2021; 20: 112. https://doi.org/10.1186/s12934-021-01601-7

Khaligh SF, Asoodeh A. Recent advances in the bio-application of microalgae-derived biochemical metabolites and development trends of photobioreactor-based culture systems. 3.Biotech 2022; 12: 260. https://doi.org/10.1007/s13205-022-03327-8

Krylova NN, Kravchenko AO, Iunikhina OB, et al. Influenze of the structural features of carrageenans from red algae of the Fahr Eastern Seas on their antiviral properties. Mar Drugs 2022; 20(1): 60. https://doi.org/10.3390/md20010060

Besednova NN, Zvyagintseva TN, Andriukov BG, et al. Seaweed-derived sulfated polysaccharides as potential agents for prevention and treatment of influenza and COVID-19. Antibiotiki I Khimioter = Antibiotics and Chemotherapy 2021; 66: 7-8: 50-66. https://doi.org/10.24411/0235-2990-2021-66-7-8-50-66

Álvarez-Viñas M, Souto S, Flórez-Fernández N, et al. Antiviral activity of carrageenans and processing implications. Mar Drugs 2021; 19: 437. https://doi.org/10.3390/md19080437

Singh S, Dwivedi V, Sanyal D, Dasgupta S. Therapeutic and nutritional of Spirulina in combating COVID-19 infection. AIJR Preprints. Section: coronavirus. Article Id: 49. Version: 1 2020; https://preprints.aijr.org/index.php/

Hachicha R, Elleuch F, Hlima HB, et al. Biomolecules from microalgae and cyanobacteria: applications and market survey. Appl Sci 2022; 12: 1924. https://doi.org/10.3390/app120412041924

Levasseur W, Perré P, Pozzobon V. A review of high value-added molecules production by microalgae in light of the classification. Biotechnol Adv 2020; 41: 107545. https://doi.org/10.1016/j.biotechadv.2020.107545

Laroche C. Exopolysaccharides from microalgae and cyanobacteria: diversity of strains, production strategies, and application. Mar Drugs 2022; 20(5): 336. https://doi.org/10.3390/md20050336

Li S, Ji L, Shi Q, et al. Advances in the production of bioactive substances from marine unicellular microalgae Porphyridium sp. Bioresour Technol 2019; 292: 122048. https://doi.org/10.1016/j.biortech.2019.122048

Babich O, Sukhikh S, Larina V, et al. Algae: study of edible and biologically active fractions, their properties and applications. Plants 2022; 11(16): 780. https://doi.org/10.3390/plants11060780

Panggabean JA, Adiguna S, Rahmawati SI, et al. Antiviral activities of algal-based sulfated polysaccharides. Molecules 2022; 27: 1178. https://doi.org/10.3390/molecules27041178

Varner CT, Rosen T, Martin JT, Kane RS. Recent advances in engineering polyvalent biological interactions. Biomacromolecules 2015; 16(1): 43-55. https://doi.org/10.1021/bm5014469

Ghosh SA, Dubinsky Z, Verdelho V. Unconventional high-value products from microalgae: a review. Bioresource Technology 2021; 329: 124895. https://doi.org/10.1016/biortech.2021.124895

Moreira JB, Vaz BS, Cardias BB, et al. Microalgae polysaccharides: an alternative source for food production and sustainable agriculture. Polysaccharides 2022; 3: 441-457. https://doi.org/10.3390/polysaccharides3020027

Mazur-Marzec H, Ceglowska M, Konkel R, Pyrc K. Antiviral cyanometabolites. Biomolecules 2021; 11: 474. https://doi.org/10.3390/biom11030474

Kiran BR, Mohan SV. Microalgal cell-biofactory-therapeutic, nutraceutical and functional food applications. Plants (Basel) 2021; 10(5): 836. https://doi.org/10.3390/plants10050836

Umezawa I, Komiyama K. Acidic polysaccharide CH-1 isolated from Chlorella pyrenoidosa and the use thereof. U.S. Patent 4533548A, 7 August 1985.

Hayashi K, Hayashi T, Kojima I. A natural sulfated polysaccharide, calcium spirulan, isolated from Spirulina platensis: in vitro and ex vivo evaluation of anti-herpes simplex virus and anti-human immunodeficiency virus activities. AIDS Res Hum Retroviruses 1996; 12(15): 1463-71. https://doi.org/10.1089/aid.1996.12.1463

Hayashi T, Hayashi K, Maeda M, Kojima I. Calcium spirulan, an inhibitor of enveloped virus replication, from a blue-green alga Spirulina platensis. J Nat Prod 1996a; 59: 83-87. https://doi.org/10.1021/np960017o

Ayehunie S, Belay A, Baba, TW, Ruprecht RM. Inhibition of HIV-1 replication by an aqueous extract of Spirulina platensis (Arthrospira platensis). J Acquir Immune Defic Syndr Hum Retrovirol 1998; 18: 7-12. https://doi.org/10.1097/00042560-199805010-00002

Worraprat C, Yuthana P, Thanongsak C, et al. The antiviral activity of bacterial, fungal and algal polysaccharides as bioactive enhancing immune systems and preventing viruses. Front Nutr 2021; 8: 772033. https://doi.org/10.3389/fnut.2021.772033

Raposo MFJ, Morais AMMB, Morais RMSC. Influence of sulphate on the composition and antibacterial and antiviral properties of the exopolysaccharide from Porphyridium cruentum. Life 2014; 101(1-2): 56-63. https://doi.org/10.1016/j.lfs.2014.02.013

Li S, Xiong Q, Lai X, et al. Molecular modification of polysaccharides and resulting bioactivities. Compr Rev Food Sci Food Saf 2016; 15: 237-250; https://doi.org/10.1111/1541-4337.12161

Musale AS, Kumar GRK, Sapre A, Dasgupta S. Marine algae as a natural source for antiviral compounds. AIJR Preprints. Series: coronavirus. Article Id: 38, version: 1, 2020. https://preprints.aijr.оrg/index.php/ap/preprint/view/38.

Prabhu S, Vijayakumar S, Praseeta P. Cyanobacterial metabolites as novel drug candidates in corona viral therapies: a review. Cronic Dis and Translational Medicine 2022; 1-12. https://doi.org/10.1002/cdt3.11

Abdo SM, Hetta MH, El-Senousy WM, et al. Antiviral activity of freshwater algae. J Applied Pharmaceutical Science 2012; o2(02): 21-25.

Sayda MA, Mona HH, Waleed M, et al. Antiviral activity of fresh water algae. J Appl Pharmaceutical Sci 2012; 2(2): 21-25.

Hernandez-Corona Neves I, Meckes M, et al. Antiviral activity of Spirulina maxima against herpes simplex virus type 2. Antiviral Res 2002; 56(3): 279-285; https://doi.org/10.1016/s0166-3542(02)00132-8

Lee YK. Microalgal mass culture systems and methods: their limitation and potential. J Appl Phycol 2001; 13: 307-315. https://doi.org/10.1023/A:1017560006941

Mader J, Gailo A, Schommartz T, et al. Calcium spirulan derived from Spirulina platensis inhibits herpes simplex virus 1 attachment to human keratinocytes and protects against herpes labialis. Immune Deficiencies, Infection and Systemic Immune Disorders 2016; 137(1): 197-203. https://doi.org/10.1016/j.jaci.2015.07.027

Ogura F, Hayashi K, Lee J-B, et al. Evaluation of an edible blue-green alga Aphanothece sacrum, for its inhibitory effect on replication of herpes simplex virus type 2 and influenza virus type A. Bioscience, Biotechnology and Biochemistry 2010; 74(8): 1687-1690. https://doi.org/10.1271/bbb.100336

Chen YH, Chang GK, Kuo SM, et al. Well tolerated Spirulina extract inhibits influenza virus replication and reduces virus-induced mortality. Sci Rep 2016; 6: 24253. https://doi.org/10.1038/srep2453

Lee J-B, Hayashi K, Hirata M, et al. Antiviral sulfated polysaccharide from Navicula directa a diatom collected from deep-sea water in Toyama bay. Biol Pharm 2006; 29(10): 2135-2139. https://doi.org/10.1248/bpb.29.2135

Kanekiyo K, Lee J-B, Hayashi K, et al. Isolation of an antiviral polysaccharide, nostoflan, from a terrestrial, Nostoc flagelliforme. J Nat Prod 2005; 68(7): 1037-1041. https://doi.org/10.1021/np050056c

Hasui M, Matsuda M, Okutani K, Shigeta S. In vitro antiviral activities of sulfated polysaccharides from a marine microalga Cochlodinium polykrikoides against human immunodeficiency virus and other enveloped viruses. Int J Biological Macromolecules 1995; 17(5): 293-297. https://doi.org/10.1016/0141-8130(95)98157-T

Kim M, Yim JH, Kim S-Y, et al. In vitro inhibition of influenza A virus infection by marine microalga-derived sulfated polysaccharide p-KG03. Antiviral Res 2012; 93(2): 253-259 https://doi.org/10.1016/j.antiviral.2011.12.006

Yim JH, Kim SJ, Ahn SH, et al. Antiviral effects of sulfated exopolysaccharide from the marine microalga Gyrodinium impudicum. Marine Biotechnol 2004; 6(1): 17-25. https://doi.org/10.1007/s10126-003-0002-z

Huleihel M, Ishanu V, Tal J, Arad SM. Activity of Porphyridium sp. polysaccharide against herpes simplex viruses in vitro and in vivo. J Biochemical and Biophysical Methods 2002; 50(2-3): 189-200. https://doi.org/10.1016/s0165-022x(01)00186-5

Santoyo S, Plaza M, Jaime L, et al. Pressurized liquid extraction as an alternative process to obtain antiviral agents from the edible microalga Chlorella vulgaris. J Agric Food Chem 2010; 58(15): 8522-8527.

Pyne SK, Bhattacharjee P, Srivastav PP. Microalgae (Spirulina platensis) and its bioactive molecules: review. Indian J Nutrition 2017; 4(2): ISSN: 2395-2326.

Mathew F, Saral AM. Pharmaceutical and commercial importance of marine organisms – a review. J Farm and Tech 2017; 10(2): 4429-4438. https://doi.org/10.5958/0974

Karkos PD, Leong SC, Karkos CD. et al. Spirulina in Clinical Practice: Evidence-Based Human Applications. Evid Based Complement Alternat Med 2008. https://doi.org/10.1093/ecam/nen058

Joseph J, Karthika T, Ajyay A, et al. Green tea and Spirulina extracts inhibit SARS, MERS and SARS-2 spike pseudotyped virus entry in vitro. Current Pharmaceutical Biotechnology. https://doi.org/10.2174/1389201022666210810111716

Shchelkanov MYu, Kolobukhina LV, Lvov DK. Influenza: history, clinics, pathogenesis. The Practitioner 2011; 10: 33-38. [in Russian] URL: https://www.lvrach.ru/2011/10/ 15435275/

Breslav NV, Shevchenko ES, Abramov DD, et al. Efficacy of anti-neuraminidase drugs application during and after influenza pandemic. Voprosy Virusologii 2013; 58(1): 28-32. [in Russian].

Kolobukhina LV, Merkulova LN, Burtseva EI, et al. Efficacy of ozeltamivir (Tamiflu) in adult influenza on the epidemic rise of morbidity in Russia in the 2006-2007 season. VoprosyVirusologii 2008; 53(4): 23-26. [in Russian]

Shchelkanov MYu, Shibnev VA, Finogenova MP, et al. The antiviral activity of adamantane derivatives against the influenza A (H1N1) pdm2009 model in vivo. Voprosy Virusologii 2014; 59(2): 37-40. [in Russian].

Chen Y-H, Liao YC, Huang J-Y, et al. Hot water extract of Arthrospira maxima (AHWE) has broad-spectrum antiviral activity against RNA virus including coronavirus SARS-CoV-2 and the antivirus spray application 2021. bioRxiv preprint. https://doi.org/https://doi.org/10.1101/2021.06.06.446935

Hirahashi T, Matsumoto M, Hazeki K, et al. Activation of the human innate immune system by spirulina: augmentation of interferon production and NK cytotoxicity by oral administration of hot water extract of Spirulina platensis. Int Immunopharmacol 2002; 2: 423-434.

Jingi J, Conk-Dalay S, Cakli, Bal C. The effect of Spirulina on allergic rhinitis. Eur Arch Otorhinolaringol 2008; 265(10): 1219-1223. https://doi.org/10.1007/s00405-008-0642-8

Raj TK, Ranjithkumar R, Gopenath TS. C-Phycocyanin of Spirulina platensis inhibits NSP12 required for replication of SARS-CoV-2: a novel finding in silico. Int J Pharm Sci and Res 2020; 11(9): 4271-4278. https://doi.org/10.13040/IJPRS.0975-8232

Pendyala B, Patras A. In silico screening of food bioactive compounds to predict potential inhibitors of COVID-19 main protease (Mpro) and RNA-dependent RNA polymerase (RdRp). ChemRxiv[Preprints] 2020; 1-11. https://doi.org/10.26434/chemrxiv.12051927.v2

Pradhan B, Nayak R, Patra S, et al. Cyanobacteria and algae-derived bioactive metabolites as antiviral agents: evidence, mode of action, and scope for further expansion; a comprehensive review in light of the SARS-CoV-2-outbreack. Antioxidants (Basel) 2022; 11(2): 354. https://doi.org/10.3390/antiox11020354

Shchelkanov MYu, Popova AYu, Dedkov VG, et al. History of investigation and current classification of coronaviruses (Nidovirales: Coronaviridae). Russian Journal of Infection and Immunity 2020; 10(2): 221-246. [in Russian] https://doi.org/10.15789/2220-7619-hoi-1412

Terasawa M, Hayashi K, Lee J, et al. Anti-influenza A virus activity of rhamnan sulfate from green algae Monostroma nitidum in mice with normal and compromised immunity. Mar Drugs 2020; 18(5): 254. https://doi.org/10.3390/md18050254

Tokita Y, Nakajima K, Mochida H, et al. Development of a fucoidan-specific antibody and measurement of fucoidan in serum and urine by sandvich ELISA//Biosci. Biotechnol Biochem 2010; 74: 350-357. https://doi.org/10.1271/bbb.90705

Tokita Y, Hirayama M, Nakajima K, et al. Detection of fucoidan in urine after oral intake of traditional Japanese seaweed Okinava mozuku (Cladosiphon ocamuranus Tokida). J Nutr Sci Vitaminol 2017; 63: 419-421. https://doi.org/10.3177/jnsv63.419

Yakoot M, Salem A. Spirulina platensis versus silymarin in the treatment of chronic hepatitis C virus infection. A pilot randomized, comparative clinical trial. BMC Gastroenterology 2012; 12: 32. http://www.biomedcentral.com/1471-230x/12/32

Rechter S, Konig T, Auerochs S, et al. Antiviral activity of Arthrospira derived spirulan-like substances. Antiviral Res 2006; 72(3): 197-206. https://doi.org/10.1016/j.antiviral.2006.06.004

Lee J-B, Hayashi T, Hayashi K, Sankawa U. Structural analysis of calcium spirulan (Ca-Sp)-derived oligosaccharides using electrospray ionization mass spectrometry. J Nat Prod 2000; 63(1): 136-138. https://doi.org/10.1021/np990348b

Hayashi K, Hayashi T, Morita M. An extract from Spirulina platensis is a selective inhibitor of herpes simplex virus type 1 penetration into HeLa cells. Phytother Res 1993; 7: 76-80. https://doi.org/10.1002/ptr.2650070118

Deng Y-Q, Dai J-X, Ji G-H, Jiang T, Wang H-J, et al. A broadly Flavivirus cross-neutralizing monoclonal antibody that recognizes a novel Epitope within the fusion loop of E protein. PLoS ONE 2011; 6(1): e16059. https://doi.org/10.1371/journal.pone.0016059

Lee J-B, Hou X, Hayashi T. Effect of partial desulfation and oversulfation of sodium spirulan on the potency of anti-herpetic activities. Carbohydr Polym 2007; 69: 651-658. https://doi.org/10.1016/j.carbpol.2007.01.024

Ray B, Ali I, Jana S, et al. Antiviral strategies using natural source-derived sulfated polysaccharides in the COVID-19-pandemic and major human pathogenic viruses. Viruses 2022; 14: 35. https://doi.org/10.3390/v14010035

Matufi F, Maghsudi H, Choopani A. Spirulina and its role in immune system: a review. J Immunol Res Ther 2020; 5(1): 204-2011.

Luescher MM. Algae, a possible source for new drugs in the treatment of HIV and other viral diseases. Curr Med Chem Anti-Infect Agents 2003; 2: 219-225. https://doi.org/10.2174/1568012033483051

Simpore J, Zongo F, Kabore F, et al. Nutrition rehabilitation of HIV-infected and HIV-negative undernourished children utilizing Spirulina. Ann Nutr Metab 2005; 49: 373-380. https://doi.org/10.1159/000088889

Furmaniaks MA, Misztak AE, Franczuk MD, et al. Edible cyanobacterial genus Arthrospira: actual state of the art in cultivation methods, genetics, and application in medicine. Front Microbiol 2017. https://doi.org/10.3389/fmicb.2017.02541

El-Sheekh M, Abomohra AE. The therapeutic potential of Spirulina to combat COVID-19 infection. J Botany 2020; 60(3): 605-609. https://doi.org/10.21608/ejbo.2020.49345.1581

Reichert M, Bergmann S, Lindenberger C, et al. Antiviral activity of exopolysaccharides from Arthrospira platensis against koi herpesvirus. J Fish Disease 2017; 40(10): 1441-1450. https://doi.org/10.1111/jfd.12618

Galkwad M, Pawar Y, Nagle V, Dasgupta S. Marine red alga Porphyridium sp. as a source of sulfated polysaccharides for combating against COVID-19. Preprints (www.preprints.0rg)2020.Posted: 10 April 2020.

Rodas-Zuluaga LI, Castillo-Zacarias C, Nunez-Goitia et al. Implementation of kLa-based strategy for scaling up Porphyridium purpureum (red marine microalga) to produce high-value phycoerythrin, fatti acids and proteins. Mar Drugs 2021; 19(6): 290. https://doi.org/10.1039/md19060290

Esqueda B, Gardarin C, Laroche C. Exploringthe diversity of red microalgae for exopolysaccharide production. Mar Drugs 2022; 20: 246. https://doi.org/10.3390/md20040246

Soanen N, Da Silva E, Gardarin C. Improvement of exopolysaccharide production by Porphyridium marinum. Bioresour Technol 2016; 213: 231-238. https://doi.org/10.1016/j.biortech.2016.02.075

Simon B, Geresh S, Arad S. Degradation cell-wall polysaccharide of Porphyridium sp. (Rhodophyta) by means of enzymatic activity of its predator, Gymnodinium sp. (Pyrrophyta). J Phycology 1992; 28(4): 460-465. https://doi.org/10.1111/j.0022-3646.1992.00460.x

Nunez-Montero K, Guerrero-Barrantes M, Gomez Espinoza O. Microalgae-based approaches to overcome the effects of the COVID-19 pandemic technologiaenMarcha-Mayo 2022; 35: especial COVID-19. https://doi.org/10.18845/tm.v35i5.6190

Ziadi M, Bouzaiene T, M’Hir S. Evaluation of the Efficiency of Ethanol Precipitation and Ultrafiltration on the Purification and Characteristics of Exopolysaccharides Produced by Three Lactic Acid Bacteria. BioMed Research International Volume 2018; Article ID 1896240. https://doi.org/10.1155/2018/1896240

Baltic R, Le Bach, Brodu N, et al. Concentration and purification of Porphyridium cruentum exopolysaccharides by membrane filtration at various cross-flow velocities. Process Biochemistry 2018; 74: 175-184. https://doi.org/10.1016/j.procbio.2018.06.021

Abu-Galiyun E, Huleihel M, Levy-Ontman M. Antiviral bioactivity of renewable polysaccharides against Varicella Zoster. Cell Cycle 2019; 18(240): 3540-3549. https://doi.org/10.1080/15384101.2019.1691363

Yakovlev A.B. Shingles and chickenpox. Effective Pharmacotherapie 2021; 17(1): 22-30 https://doi.org/10.33978/2307-3586-2021-17-1-22-30

Encarnacao T, Pais AACC, Campos MG, Burrows HD. Cyanobacteria and microalgae: a renevable source of bioactive compounds and other chemicals. Science Progress 2015; 98(2): 145-168. https://doi.org/10.31847003685015×14298590596266

Jin Z, Du X, Xu Y, et al. Structure of M from SARS-COV-2 and discovery of its inhibitors. Nature 2020; 582(7811): 289-293. https://doi.org/10.1038/s41586-020-2223-y

Farhat A, Hlima HB, Khemakhem B, et al. Apigenin analogues as SARS-COV-2 main protease inhibitors: in silico screening approach. Bioegineered 2022; 13(2): 3350-3361. https://doi.org/10.1080/216655979.2022.2027181

Hlima HB, Farhat A, Akermi S, et al. In silico evidence of antiviral activity against SARS-COV-2 main protease of oligosaccharides from Porphyridium sp. Sci Total Approx 2022; 836: 155580. https://doi.org/10.1016/j.scitotenv.2022.155580

Gissibl A, Sun A, Care A, et al. Bioproducts from Euglena gracilis: synthesis and applications. Front Bioeng Biotechnol 2019; 7: 108. https://doi.org/10.3389/fbioe.2019.00108

Guo Q, Bi D, Wu M, et al. Immune activation of murine RAW264.7 macrophages by sonicated and alkalized paramylon from Euglena gracilis. BMC Microbiol 2020; 20: 171. https://doi.org/10.1186/s12866-020-01782-y

Barsanti L, Gualtieri P. Paramylon, a potent immunomodulatory from WZSL mutant of Euglena gracilis. Molecules 2019; 24(17): 3114. https://doi.org/10.3390/molecules24173114

Koizumi N, Sakagami H, Utsumi A, et al. Anti HIV (human immunodeficience virus) activity of sulfated paramylon. Antiviral Res 1993; 21(1): 1-14. https://doi.org/10.1016/0166-3542(93)90063-o

Nakashima A, Suzuki K, Asayama, Y, et al. Oral administration of Euglena gracilis Z and its carbohydrate storage substance provides survival protection against influenza virus infection in mice. Biochem Biophys Res Commun 2017; 494: 379-383.

Yasuda K, Nakashima A, Murata I, et al. Euglena gracilis and β-glucan paramylon induce Ca2+ signaling in intestinal tract epithelial, immune, and neutral cells. Nutrients 2020; 12(8): 2293. https://doi.org/10.3390/nu12082293

Nakashima A, Horio Y, Susuki K, Isegawa Y. Antiviral activity and underlying action mechanism of Euglena extract against influenza virus. Nutrients 2021; 13: 3911. https://doi.org/10.3390/nu13113911

Herrlinger K, Lasrado J, Wonderling L, Zhu Y. Compositions containing Euglena gracilis for viral protection and related methods. Patent WO 2019/108319 A1 от 6.06.2019.

Russo R, Barsanti L, Evangelista V, et al. Euglena gracilis paramylon activates lymphocytes by upregulating pro-inflammatory factors. Food Sci Nutr 2017; 5(2): 205214. https://doi.org/10.1002/fsn3.383

Widyaningrum D, Prianto AD. Chlorella as a source of functional food ingredients: short review. 4th International Conference on Eco Engineering Development 2020. IOP Conf. Series: Earth and Environmental Science 2021; 794: 012148. https://doi.org/10.1088/1755-1315/794/1/012148

Sui Z, Gizaw Y, Miller JN. Extraction of polysaccharides from a species of Chlorella. Carbohydr Polym 2012; 90: 1-7. https://doi.org/10.1016/j.carbpol.2012.03.062

El-Naggar NE, Hussein MH, Shaaban-Dessuuki SA. Production, extraction and characterization of Chlorella vulgaris soluble polysaccharides and their applications in AgNPs biosynthesis and biostimulation of plant growth. Sci Rep 2020; 10: 3011. https://doi.org/10.1038/s41598-020-59945-w

Azocar J, Diaz A. Efficacy and safety of Chlorella supplementation in adults with chronic hepatitis C virus infection. World J Gastroenterol 2013; 21: 1085-1090. https://doi.org/10.3748/wjg.v19.17.1085

Kim DH, Kim JH, Kim DH, et al. Functional foods with antiviral activity. Food Sci Biotechnol 2022; 31: 527-538. https://doi.org/10.1007/s10068-022-01073-4

Ruiz DG, Willalobos-Sanchez E, Alam-Escamilla D, Elizondo-Quiroga D. In vitro inhibition of SARS-COV-2 infection by dry algae powders. Research Article 2022. https://doi.org/10.21203/rs.3.rs-1416575/v1

Cantu-Bernal S, Dominguez-Gamez, Medina-Peraza I, et al. Bifidobacterium longum and Lactobacillus plantarum in combination with Chlorella sorokiniana in a dairy product. Frontiers in Microbiology 2020; 11: article number 875. https://doi.org/10.3389/fmicb.2020.00875

Halperin SA, Smith B, Nolan C, et al. Safety and immunoenhancing effect of a Chlorella-derived dietary supplement in healthy adults undergoing influenza vaccination: randomized, double-blind, placebo-controlled trial. CMAJ 2003; 169: 111-117.

Negishi H, Mills G, Mori H, Yamori Y. Supplementation of elderly Japanese men and women with fucoidan from seaweed increases immune responses to seasonal influenza vaccination. J Nutr 2013; 143(11): 1794-1798. https://doi.org/10.3945/jn.113.179036

Zaporozhets TS, Kryzhanovsky SP, Persianova EV, et al. The corrective effect of fucoidan, a sulfated polysaccharide extracted from brown algae Fucus evanescens, in the formation of a specific immune response against seasonal influenza viruses in the elderly (In Russia). Antibiotics and Chemotherapy 2020; 65(3-4): 23-28. https://doi.org/10.37489/0235-2990-2020-65-3-4-23-28

Maginnis MS. Virus–Receptor Interactions: The key to cellular invasion. J Mol Biol 2018; 430: 2590-2611. https://doi.org/10.1016/j.jmb.2018.06.024

Kim SY, Jin W, Sood A, et al. Characterization of heparin and severe acute respiratory syndrome-related coronavirus 2 (SARS-CoV-2) spike glycoprotein binding interactions. Antivir Res 2020; 181: 104873. https://doi.org/10.1016/j.antiviral.2020.104873

Reinolds D, Huesemann M. Viral inhibitors derived from macroalgae, microalgae, and cyanobacteria: a review of antiviral potential throughout pathogenesis. Algal Research 2021; 57: 102331. https://doi.org/10.1016/j.algal.2021.102331

Ahmad SAA, Palanisamy UD, Tejo BA, et al. Geraniin extracted from the rind of Nephelium lappaceum binds to dengue virus type-2 envelope protein and inhibits early stage of virus replication. Virology Journal 2017; 14: 229. https://doi.org/10.1186/s12985-017-0895-1

Koerdt A, Jachlewski S, Ghosh A, et al. Complementation of Sulfolobussol fataricus PBL2025 with an alpha-mannosidase: Effects on surface attachment and biofilm formation. Extrem Life UnderExtrem Cond 2012; 16: 115-125. https://doi.org/10.1007/s00792-011-0411-2

Bello-Morales R, Andreu S, Ruiz-Carpio V, et al. Extracellular polymeric substances: still promising antivirals. Viruses 2022; 14; 1337. https://doi.org/10.3390/v14061337

Wang W, Wang S.X, Guan H.S. The antiviral activities and mechanisms of marine polysaccharides: an overview. Mar Drugs 2012; 10: 2795-2816. https://doi.org/10.3390/md10122795

Carlucci MJ, Scolaro LA, Damonte EB. Herpes simplex virus type 1 variants arising after selection with an antiviral carrageenan: lack of correlation between drug susceptibility and syn phenotype. J Med Virol 2002; 68: 92-98. https://doi.org/10.1002/jmv.10174

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: 1-14. https://doi.org/10.1038/srep40760

Hans N, Malik A, Naik S. Antiviral activity of sulfated polysaccharides from marine algae and its application in combating COVID-19: mini review. Bioresour Technol Rep 2021; 13: 100623. https://doi.org/10.1016/j.biteb.2020.100623

Claus-Desbonnet H, Nikly E, Nalbantova V, et al. Polysaccharides and their derivatives as potential antiviral molecules. Viruses 2022; 14: 426. https://doi.org/10.3390/v14020426

Pirrone V, Wigdahl B, Krebs F.C. The rise and fall of polyanionic inhibitors of the human immunodeficiency virus type 1. Antivir Res 2011; 90: 168-182. https://doi.org/10.1016/j.antiviral.2011.03.176

Chen X, Song L, Wang H, et al. Partial characterization, the immunomodulation and anticancer activities of sulfated polysaccharides from filamentous microalgae Tribonema sp. Molecules 2019; 24(2): 322. https://doi.org/10.3390/molecules24020322

Hayashi K, Lee J.B, Nakano T, Hayashi T. Anti-influenza A virus characteristics of a fucoidan from sporophyll of Undaria pinnatifida in mice with normal and compromised immunity. Microbes Infect 2013; 15: 302-309. https://doi.org/10.1016/j.micinf.2012.12.004

Chen X, Han W, Wang G, Zhao X. Application prospect of polysaccharides in the development of anti-novel coronavirus drugs and vaccines. Int J Biol Macromol 2020; 164: 331-343. https://doi.org/10.1016/j.ijbiomac.2020.07.106

Talukdar J, Dasgupta S, Nagle V, Bhadra B. COVID-19: potential of microalgae derived natural astaxanthin as adjunctive supplement in alleviating cytokine storm. (April 18, 2020). Available at SSRN: https://ssrn.com/abstract=3579738

Choo W-T, Choo M-L, Teoh S-M, et al. Microalgae as potential anti-inflammatory natural product against human inflammatory skin diseases. Front. Pharmacol 2020; 11: 1086-1097.

Arulselvan P, Fard M.T, Tan W.S, et al. Role of antioxidants and natural products in inflammation. Oxid. With cell longev 2016; 2016: 5276130.

Lauritano JH, Andersen JH, Hansen E, et al. Bioactivity screening of microalgae for antioxidant, anti-inflammatory, anticancer, anti-diabetes, and antibacterial activities. Front Mar Sci 2016; 3: 1-12.

Fereira AO, Polonini HC, Dijkers EC. Postulated adjuvant therapies for COVID-19. J Personalized Medicine 2020; 10(3): 1-33. https://doi.org/10.3390/jpm10030080

Keys S, Oh HJ, Song JH, et al. Spirulina maxima extract prevents activation of the NLRP3 inflammasome by inhibiting. Sci Rep 2020; 10: 2075. https://doi.org/10.1038/s41598-020-58896-6

Riccio G, Lauritano C. Microalgae with immunomodulatory activities. Mar Drugs 2020; 18(1): 2 https://doi.org/10.3390/md18010002

Nigam S, Singh R, Bhardwaj SK, et al. Perspective on the therapeutic applications of algal polysaccharides. J Polym Environ 2022; 30: 785-809. https://doi.org/10.1007/s10924-021-02231-1

Anwar AA, Nowruzi B. Bioactive peptides of Spirulina: a review. Microbial Bioactives 2021; 4(1): 134-142. https://doi.org/10.25163/microbbioacts.412117BO719110521

Parages ML. Rico RM, Abdala-Diaz RT, et al. Acid polysaccharides of Arthrospira platensis (Spirulina) induce the synthesis of TNFα in RAW macrophages. J Appl Phycol 2012; 24: 1537-1546.

Bahramzadeh S, Tabarsa M, You S.G, et al. Purification, structural analysis and mechanism of murine macrophage cell activation by sulfated polysaccharides from Cystoseira indica. Carbohydrate Polymers 2019; 205(1): 261-270.

Li J, Zhang Y, Yang S, et al. Isolation, purification, characterization, and immunomodulatory activity analysis of α-glucans from Spirulina platensis. ACS Omega 2021; 6: 21384-21394.

Tzachor A, Rozen O, Khatib S, et al. Phothosinthetically controlled Spirulina, but not solar Spirulina, inhibits TNFα secretion: potential implications for COVID-19-related cytokine storm therapy. Mar Biotechnol (NY) 2021; 23(1): 149-155.

Seyidoglu N, Galip N, Bud S, Uzabaci D. The effects of Spirulina platensis (Arthrospira platensis) and Saccharomyces cerevisiae on the distribution and cytokine production of CD4+ and CD8+ T-lymphocytes in rabbits. Austral J Veterinare Sciences 2017; 49(3). https://doi.org/10.4067/S0719-81322017000300185

Appel K, Munoz E, Navarrete C, et al. Immunomodulatory and inhibitory effect of Immulina, and immunloges in the IgE mediated activation of RBL-2H3 cells A new role in allergic inflammatory responses. Plants (Basel) 2018; 7(1): 13. https://doi.org/10.3390/plants7010013

Moor VA, Pieme AC, Nkeck JR, Biapa PC, et al. Spirulina platensis enhances immune status, inflammatory and oxidative markers of HIV patients on antiretroviral therapy in Cameroon 2020; preprint. https://doi.org/10.21203/rs.2.22360/v1

Mirzaie S, Tabarsa M, Safavi M. Effects of extracted polysaccharides from a Chlorella vulgaris biomass on expression of interferon-γ and interleukin-2 in chicken peripheral blood mononuclear cells. J Appl Phycol 2021; 33: 409-418. https://doi.org/10.1007/s10811-020-02301-2

Kwak JH, Baek SH, Woo Y, et al. Beneficial immunostimulatory effect of short-term Chlorella supplementation: enhancement of natural killer cell activity and early inflammatory response (randomized, double-blinded, placebo-controlled trial). Nutr J 2012; 11: 53. https://doi.org/10.1186/1475-2891-11-53

Levy-Ontman O, Huleihel M, Hamias R, et al. An anti-inflammatory effect of red microalga polysaccharides in coronary artery endothelial cells. Atherosclerosis 2017; 264: 11-18. https://doi.org/10.1016/j.atherosclerosis.2017.07.017

Barborikova J, Sutovska M, Kazimierova I, Joskova M, et al. Extracellular polysaccharide produced by Chlorella vulgaris – chemical characterization and anti-asthmatic profile. Int J Biol Macromol 2019; 135: 1-11. https://doi.org/10.1016/j.ijbiomac 2019.05.104

Andrade A, Hort MA, Schmith LE, et al. Antinoceptive and anti-inflammatory effects of cellular and extracellular extracts from microalga Chlamidomonas pumilioniformis on mice. Acta Scientiarum Biological Sciences 2021; 43: e52889. https://doi.org/10.4025/actascibiolsci.v43i1.52889

Liu J, Obaidi, Nagar S, et al. The antiviral potential of algal-derived macromolecules. Current Research in Biotechnology 2021; 3: 120-134. https://doi.org/10.1016/j.crbiot.2021.04.003

Darenskaya M, Kolesnikova L, Kolesnikov S. The association of respiratory viruses with oxidative stress and antioxidants. Implications for anti-COVID-19 pandemic. Curr Pharm Des 2021; 27(13): 1618-1627. https://doi.org/10.2174/1381612827666210222113351

Naeini F, Zrezadeh M, Mohiti S, et al. Spirulina supplementation as an adjuvant therapy in enhancement of antioxidant capacity: a systematic review and meta-analysis of controlled clinical trials. Clinical Practice 2021; 75(10): e14618.

Rajasekar P, Palanisamy S, Anjali M, et al. Isolation and structural characterization of sulfated polysaccharide from Spirulina platensis and its bioactive potential: in vitro antioxidant, antibacterial activity and zebrafish growth and reproductive performance. Int J Biological Macromolecules 2019; 141: 809-821. https://doi.org/10.1016//j.ijbiomac.2019.09.024

Singab ANB, Ibrahim NA, El-Khair A, et al. Antiviral, cytotoxic, antioxidant and anticholinesterase activities of polysaccharides isolated from microalgae Spirulina platensis, Scenedesmus obliquus and Dunaliella salina. Archives of Pharmaceutical Sciences Ain Shams University 2018; 2(2): 121-137.

https://doi.org10.21608/aps2018.18740

Jonsson M, Allagholi L, Sardari RRR, et al. Extraction and modification of macroalgal polysaccharides for current and next-generation applications. Molecules 2020; 25(4): 930. https://doi.org/10.3390/molecules25040930

Sun H, Gao L, Xue C, Mao X. Marine-polysaccharide degrading enzymes: status and prospects. Comprehensive Reviews in Food Science and Food Safety 2020; 19(6): 2767-2796.

Specht E.A, Mayfield S.P. Algae based oral recombinant vaccines. Front. Microbiol 2014; 17: 60. https://doi.org/10.3389/fmicb.2014.00060

Nunez-Montero K, Guerrero-Barrantes M, Gomez-Espinoza O. Microalgae-based approaches to overcome the effects of the COVID-19 pandemic. Technologia en Marcha. Mayo 2022; 35: 84-93. https://doi.org/10.18845/tm.v35i5.61-90

Rosales-Mendoza I. García-Silva O. González-Ortega et al. The Potential of Algal Biotechnology to Produce Antiviral Compounds and Biopharmaceuticals. Mol 2020; 25: 4049. https://doi.org/10.3390/MOLECULES25184049

Ratha SK, Renuka N, Rawat M, et al. Prospective options of algae derived nutraceuticals as supplements to combat COVID-19 and human coronavirus diseases. Nutrition 2021; 83: 111089. https://doi.org/10.1016/j.nut2020.111089

Khavari F, Saidijam M, Taheri M, Nouri F. Microalgae: therapeutic potentials and applications. Mol Biol Rep 2021; 48(5): 4757-4765. https://doi.org/10.1007/s11033-021-06422-w

Hempel F, Maurer M, Brockmann B, et al. From hibridomas to a robust microalgal-based production platform: molecular design of a diatom secreting monoclonal antibodies directed against the Marburg virus nucleoprotein. Microb Cell Fact 2017; 16: 131. https://doi.org/10.1186/s12934-017-0745-2

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.