Sulfated polysaccharide-rich extract from <i>Navicula incerta</i>: physicochemical characteristics, antioxidant activity, and anti-hemolytic property

Ricardo I. González-Vega; Carmen L. Del-Toro-Sánchez; Ramón A. Moreno-Corral; José A. López-Elías; Aline Reyes-Díaz; Norma García-Lagunas; Elizabeth Carvajal-Millán; Diana Fimbres-Olivarría; Ricardo I. González-Vega; Carmen L. Del-Toro-Sánchez; Ramón A. Moreno-Corral; José A. López-Elías; Aline Reyes-Díaz; Norma García-Lagunas; Elizabeth Carvajal-Millán; Diana Fimbres-Olivarría

doi:10.3934/bioeng.2022027

AIMS Bioengineering

2022, Volume 9, Issue 4: 364-382. doi: 10.3934/bioeng.2022027

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Sulfated polysaccharide-rich extract from Navicula incerta: physicochemical characteristics, antioxidant activity, and anti-hemolytic property

1.
University of Guadalajara (UDG), Cienega University Center, Universidad Ave. 1115, Lindavista, 47820, Ocotlán, Jalisco, México
2.
University of Sonora (UNISON), Rosales y Niños Héroes S/N, 83000, Hermosillo, Sonora, México
3.
State University of Sonora (UES), Navojoa Academic Unit, Manlio Fabio Beltrones Blvd. 810, 85875, Navojoa, Sonora, México
4.
Research Center for Food and Development (CIAD, A.C.), Carretera Gustavo Enrique Astiazarán Rosas, 46, 83304, Hermosillo, Sonora, México

Received: 09 October 2022 Revised: 23 November 2022 Accepted: 06 December 2022 Published: 23 December 2022

A sulfated polysaccharide from Navicula incerta (SPNi) was extracted, and its physicochemical characteristics, antioxidant activity, and anti-hemolytic property were investigated. The polysaccharide yield was 4.8% (SPNi weight/biomass dry weight). Glucose, galactose, mannose, and xylose were the primary sugars. The sulfate content and Mw values were 0.46% and 45 kDa, respectively. The FT-IR spectrum showed characteristic bands at 3276,1079,1255, and 820 cm⁻¹, related to -OH, C-O-C, S=O, and C-O-S stretching vibration. The ¹H-NMR analysis revealed signals of anomeric protons, indicating the presence of CH₂-O and CH-O groups. SPNi registered ferric-reducing antioxidant power (up to 1.47 µmol TE/g) and 54% anti-radical activity on ABTS⁺. This polysaccharide registered 90% hemolysis inhibition achieving integrity of the erythrocyte membrane. The results indicate that SPNi could be a candidate for biotechnology applications where antioxidant activity and hemolysis inhibition are required.
- Navicula incerta,
- benthic diatoms,
- sulfated polysaccharide,
- antioxidant activity,
- anti-hemolytic property,
- bioactivity
Citation: Ricardo I. González-Vega, Carmen L. Del-Toro-Sánchez, Ramón A. Moreno-Corral, José A. López-Elías, Aline Reyes-Díaz, Norma García-Lagunas, Elizabeth Carvajal-Millán, Diana Fimbres-Olivarría. Sulfated polysaccharide-rich extract from Navicula incerta: physicochemical characteristics, antioxidant activity, and anti-hemolytic property[J]. AIMS Bioengineering, 2022, 9(4): 364-382. doi: 10.3934/bioeng.2022027

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Abstract

A sulfated polysaccharide from Navicula incerta (SPNi) was extracted, and its physicochemical characteristics, antioxidant activity, and anti-hemolytic property were investigated. The polysaccharide yield was 4.8% (SPNi weight/biomass dry weight). Glucose, galactose, mannose, and xylose were the primary sugars. The sulfate content and Mw values were 0.46% and 45 kDa, respectively. The FT-IR spectrum showed characteristic bands at 3276,1079,1255, and 820 cm⁻¹, related to -OH, C-O-C, S=O, and C-O-S stretching vibration. The ¹H-NMR analysis revealed signals of anomeric protons, indicating the presence of CH₂-O and CH-O groups. SPNi registered ferric-reducing antioxidant power (up to 1.47 µmol TE/g) and 54% anti-radical activity on ABTS⁺. This polysaccharide registered 90% hemolysis inhibition achieving integrity of the erythrocyte membrane. The results indicate that SPNi could be a candidate for biotechnology applications where antioxidant activity and hemolysis inhibition are required.

Acknowledgments

This research received funding from CONACYT, grant number 319684. The authors are pleased to acknowledge the DICTUS, CIAD, DIPA, and DIPM spectroscopy laboratory of Universidad de Sonora for use of the facilities to characterize the material.

Conflict of interest

All authors declare no conflicts of interest in this paper.

Author contributions

Ricardo I. González-Vega: Conceptualization, methodology, formal analysis, investigation, writing—review and editing, visualization, supervision. Carmen L. Del-Toro-Sánchez: resources, writing—review and editing. Ramón A. Moreno-Corral: methodology, writing—review and editing. José A. López-Elías: resources, writing—review and editing. Aline Reyes-Díaz: methodology, writing—review and editing. Norma García-Lagunas: formal analysis, writing—review and editing. Elizabeth Carvajal-Millán: Supervision, Project administration, Funding acquisition, Conceptualization, Writing- Reviewing and Editing, Validation. Diana Fimbres-Olivarría: Conceptualization, methodology, investigation, writing—original draft preparation, writing—review and editing, visualization, supervision.

References

[1]	Raposo MF de J, de Morais RMSC, de Morais AMM (2013) Bioactivity and applications of sulphated polysaccharides from marine microalgae. Mar Drugs 11: 233-252. https://doi.org/10.3390/md11010233
[2]	Staats N, De Winder B, Stal LJ, et al. (1999) Isolation and characterization of extracellular polysaccharides from the epipelic diatoms Cylindrotheca closterium and Navicula salinarum. Eur J Phycol 34: 161-169. https://doi.org/10.1080/09670269910001736212
[3]	Yim JH, Kim SJ, Ahn SH, et al. (2007) Characterization of a novel bioflocculant, p-KG03, from a marine dinoflagellate, Gyrodinium impudicum KG03. Bioresour Technol 98: 361-367. https://doi.org/10.1016/j.biortech.2005.12.021
[4]	Nomoto K, Yokokura T, Satoh HMM (1983) Antitumor activity of chlorella extract, PCM-4, by oral administration. Cancer Chemother 10: 781-785.
[5]	Yim JH, Kim SJ, Ahn SH, et al. (2004) Antiviral effects of sulfated exopolysaccharide from the marine microalga Gyrodinium impudicum strain KG03. Mar Biotechnol 6: 17-25. https://doi.org/10.1007/s10126-003-0002-z
[6]	Yu Y, Zhu S, Hou Y, et al. (2020) Sulfur contents in sulfonated hyaluronic acid direct the cardiovascular cells fate. ACS Appl Mater Interfaces 12: 46827-46836. https://doi.org/10.1021/acsami.0c15729
[7]	Feriani A, Tir M, Hamed M, et al. (2020) Multidirectional insights on polysaccharides from Schinus terebinthifolius and Schinus molle fruits: Physicochemical and functional profiles, in vitro antioxidant, anti-genotoxicity, antidiabetic, and antihemolytic capacities, and in vivo anti-inflammatory and anti-nociceptive properties. Int J Biol Macromol 165: 2576-2587. https://doi.org/10.1016/j.ijbiomac.2020.10.123
[8]	Meng Q, Chen F, Xiao T, et al. (2019) Inhibitory effects of polysaccharide from Diaphragma juglandis fructus on α-amylase and α-D-glucosidase activity, streptozotocin-induced hyperglycemia model, advanced glycation end-products formation, and H2O2-induced oxidative damage. Int J Biol Macromol 124: 1080-1089. https://doi.org/10.1016/j.ijbiomac.2018.12.011
[9]	Duan S, Zhao M, Wu B, et al. (2020) Preparation, characteristics, and antioxidant activities of carboxymethylated polysaccharides from blackcurrant fruits. Int J Biol Macromol 155: 1114-1122. https://doi.org/10.1016/j.ijbiomac.2019.11.078
[10]	Yu Y, Zhu SJ, Dong HT, et al. A novel MgF2/PDA/S-HA coating on the bio-degradable ZE21B alloy for better multi-functions on cardiovascular application (2021). https://doi.org/10.1016/j.jma.2021.06.015
[11]	Wijesinghe WAJP, Jeon YJ (2012) Biological activities and potential industrial applications of fucose rich sulfated polysaccharides and fucoidans isolated from brown seaweeds: A review. Carbohydr Polym 88: 13-20. https://doi.org/10.1016/j.carbpol.2011.12.029
[12]	Lo TCT, Chang CA, Chiu KH, et al. (2011) Correlation evaluation of antioxidant properties on the monosaccharide components and glycosyl linkages of polysaccharide with different measuring methods. Carbohydr Polym 86: 320-327. https://doi.org/10.1016/j.carbpol.2011.04.056
[13]	Guerra-Dore CMP, Faustino Alves MG, Pofírio Will LSE, et al. (2013) A sulfated polysaccharide, fucans, isolated from brown algae Sargassum vulgare with anticoagulant, antithrombotic, antioxidant and anti-inflammatory effects. Carbohydr Polym 91: 467-475. https://doi.org/10.1016/j.carbpol.2012.07.075
[14]	Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms: I. Cyclotella Nana Hustedt, and Detonula Confervacea (CLEVE) Gran. Can J Microbiol 8: 229-239. https://doi.org/10.1139/m62-029
[15]	Fimbres-Olivarria D, Lopez-Elias JA, Carvajal-Millan E, et al. (2016) Navicula sp. Sulfated polysaccharide gels induced by Fe(III): Rheology and microstructure. Int J Mol Sci 17: 1238. https://doi.org/10.3390/ijms17081238
[16]	Terho TT, Hartiala K (1971) Method for determination of the sulfate content of glycosaminoglycans. Anal Biochem 41: 471-476. https://doi.org/10.1016/0003-2697(71)90167-9
[17]	AOACOfficial Methods of Analysis of AOAC International, Washington DC, USA, Arlington, VA (1995). Available from: http://lib3.dss.go.th/fulltext/scan_ebook/aoac_1995_v78_n3.pdf.
[18]	Rouau X, Surget A (1994) A rapid semi-automated method for the determination of total and water-extractable pentosans in wheat flours. Carbohydr Polym 24: 123-132. https://doi.org/10.1016/0144-8617(94)90022-1
[19]	Fimbres-Olivarria D, Carvajal-Millan E, Lopez-Elias JA, et al. (2018) Chemical characterization and antioxidant activity of sulfated polysaccharides from Navicula sp. Food Hydrocoll 75: 229-236. https://doi.org/10.1016/j.foodhyd.2017.08.002
[20]	Lee SY, Mediani A, Maulidiani M, et al. (2018) Comparison of partial least squares and random forests for evaluating relationship between phenolics and bioactivities of Neptunia oleracea. J Sci Food Agric 98: 240-252. https://doi.org/10.1002/jsfa.8462
[21]	Re R, Pellegrini N, Proteggenete A, et al. (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26: 1231-1237. https://doi.org/10.1016/S0891-5849(98)00315-3
[22]	Benzie I, Strain J (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Anal Biochem 239: 70-76. https://doi.org/10.1006/abio.1996.0292
[23]	López-Mata MA, Ruiz-Cruz S, Silva-Beltrán NP, et al. (2013) Physicochemical, antimicrobial and antioxidant properties of chitosan films incorporated with carvacrol. Molecules 18: 13735-13753. https://doi.org/10.3390/molecules181113735
[24]	Lynch EC (1990) Peripheral blood smear. Clinical Methods: The History, Physical, and Laboratory Examinations. Boston: Butterworth 732-734.
[25]	D'Archivio AA, Maggi MA, Ruggieri F (2018) Extraction of curcuminoids by using ethyl lactate and its optimisation by response surface methodology. J Pharm Biomed Anal 149: 89-95. https://doi.org/10.1016/j.jpba.2017.10.042
[26]	Wiercigroch E, Szafraniec E, Czamara K, et al. (2017) Raman and infrared spectroscopy of carbohydrates: A review. Spectrochim Acta - Part A Mol Biomol Spectrosc 185: 317-335. https://doi.org/10.1016/j.saa.2017.05.045
[27]	Wang L, Wang X, Wu H, et al. (2014) Overview on biological activities and molecular characteristics of sulfated polysaccharides from marine green algae in recent years. Mar Drugs 12: 4984-5020. https://doi.org/10.3390/md12094984
[28]	Matsuhiro B (1996) Vibrational spectroscopy of seaweed galactans. Hydrobiologia 326: 481-489. https://doi.org/10.1007/BF00047849
[29]	Barboríková J, Šutovská M, Kazimierová I, et al. (2019) Extracellular polysaccharide produced by Chlorella vulgaris – Chemical characterization and anti-asthmatic profile. Int J Biol Macromol 135: 1-11. https://doi.org/10.1016/j.ijbiomac.2019.05.104
[30]	Goo BG, Baek G, Jin Choi D, et al. (2013) Characterization of a renewable extracellular polysaccharide from defatted microalgae Dunaliella tertiolecta. Bioresour Technol 129: 343-350. https://doi.org/10.1016/j.biortech.2012.11.077
[31]	Huang SQ, Li JW, Li YQ, et al. (2011) Purification and structural characterization of a new water-soluble neutral polysaccharide GLP-F1-1 from Ganoderma lucidum. Int J Biol Macromol 48: 165-169. https://doi.org/10.1016/j.ijbiomac.2010.10.015
[32]	Rani RP, Anandharaj M, Ravindran A (2018) Characterization of a novel exopolysaccharide produced by Lactobacillus gasseri FR4 and demonstration of its in vitro biological properties. Int J Biol Macromol 109: 772-783. https://doi.org/10.1016/j.ijbiomac.2017.11.062
[33]	Rajasekar P, Palanisamy S, Anjali R, et al. (2019) 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 Biol Macromol 141: 809-821. https://doi.org/10.1016/j.ijbiomac.2019.09.024
[34]	Yuan F, Gao Z, Liu W, et al. (2019) Characterization, antioxidant, anti-aging and organ protective effects of sulfated polysaccharides from flammulina velutipes. Molecules 24: 3517. https://doi.org/10.3390/molecules24193517
[35]	Trabelsi I, Ben Slima S, Ktari N, et al. (2021) Structure analysis and antioxidant activity of a novel polysaccharide from katan seeds. Biomed Res Int 2021: 6349019. https://doi.org/10.1155/2021/6349019
[36]	Gurgel Rodrigues JA, Neto ÉM, dos Santos GRC, et al. (2014) Structural analysis of a sulfated polysaccharidic fraction obtained from the coenocytic green seaweed Caulerpa cupressoides var. lycopodium. Acta Sci Technol 36: 203-210. https://doi.org/10.4025/actascitechnol.v36i2.17866
[37]	Alencar POC, Lima GC, Barros FCN, et al. (2019) A novel antioxidant sulfated polysaccharide from the algae Gracilaria caudata: In vitro and in vivo activities. Food Hydrocoll 90: 28-34. https://doi.org/10.1016/j.foodhyd.2018.12.007
[38]	Wijesekara I, Pangestuti R, Kim SK (2011) Biological activities and potential health benefits of sulfated polysaccharides derived from marine algae. Carbohydr Polym 84: 14-21. https://doi.org/10.1016/j.carbpol.2010.10.062
[39]	Moore BG, Tischer RG (1964) Extracellular polysaccharides of algae: effects on life-support systems. Science 145: 586-587. https://doi.org/10.1126/science.145.3632.586
[40]	Raveendran S, Yoshida Y, Maekawa T, et al. (2013) Pharmaceutically versatile sulfated polysaccharide based bionano platforms. Nanomed Nanotechnol Biol Med 9: 605-626. https://doi.org/10.1016/j.nano.2012.12.006
[41]	Markou G, Nerantzis E (2013) Microalgae for high-value compounds and biofuels production: A review with focus on cultivation under stress conditions. Biotechnol Adv 31: 1532-1542. https://doi.org/10.1016/j.biotechadv.2013.07.011
[42]	Han PP, Sun Y, Jia SR, et al. (2014) Effects of light wavelengths on extracellular and capsular polysaccharide production by Nostoc flagelliforme. Carbohydr Polym 105: 145-151. https://doi.org/10.1016/j.carbpol.2014.01.061
[43]	Borowitzka MA, Beardall J, Raven JA The physiology of microalgae (2016). https://doi.org/10.1007/978-3-319-24945-2
[44]	Lee JB, Hayashi K, Hirata M, et al. (2006) Antiviral sulfated polysaccharide from Navicula directa, a diatom collected from deep-sea water in toyama bay. Biol Pharm Bull 29: 2135-2139. https://doi.org/10.1248/bpb.29.2135
[45]	Khandeparker RD, Bhosle NB (2001) Extracellular polymeric substances of the marine fouling diatom amphora rostrata Wm.Sm. Biofouling 17: 117-127. https://doi.org/10.1080/08927010109378471
[46]	Sudharsan S, Subhapradha N, Seedevi P, et al. (2015) Antioxidant and anticoagulant activity of sulfated polysaccharide from Gracilaria debilis (Forsskal). Int J Biol Macromol 81: 1031-1038. https://doi.org/10.1016/j.ijbiomac.2015.09.046
[47]	Seedevi P, Moovendhan M, Viramani S, et al. (2017) Bioactive potential and structural chracterization of sulfated polysaccharide from seaweed (Gracilaria corticata). Carbohydr Polym 155: 516-524. https://doi.org/10.1016/j.carbpol.2016.09.011
[48]	Leandro SM, Gil MC, Delgadillo I (2003) Partial characterisation of exopolysaccharides exudated by planktonic diatoms maintained in batch cultures. Acta Oecologica 24: 49-55. https://doi.org/10.1016/S1146-609X(03)00004-3
[49]	López-Mata MA, Ruiz-Cruz S, Silva-Beltrán NP, et al. (2015) Physicochemical and antioxidant properties of chitosan films incorporated with cinnamon Oil. Int J Polym Sci 2015: 974506. https://doi.org/10.1155/2015/974506
[50]	Majdoub H, Mansour M Ben, Chaubet F, et al. (2009) Anticoagulant activity of a sulfated polysaccharide from the green alga Arthrospira platensis. Biochim Biophys Acta Gen Subj 1790: 1377-1381. https://doi.org/10.1016/j.bbagen.2009.07.013
[51]	Zhang Z, Wang F, Wang X, et al. (2010) Extraction of the polysaccharides from five algae and their potential antioxidant activity in vitro. Carbohydr Polym 82: 118-121. https://doi.org/10.1016/j.carbpol.2010.04.031
[52]	Fedorov SN, Ermakova SP, Zvyagintseva TN, et al. (2013) Anticancer and cancer preventive properties of marine polysaccharides: Some results and prospects. Mar Drugs 11: 4876-4901. https://doi.org/10.3390/md11124876
[53]	Ale MT, Mikkelsen JD, Meyer AS (2011) Important determinants for fucoidan bioactivity: A critical review of structure-function relations and extraction methods for fucose-containing sulfated polysaccharides from brown seaweeds. Mar Drugs 9: 2106-2130. https://doi.org/10.3390/md9102106
[54]	Usov AI (2011) Chapter 4 - Polysaccharides of the red algae. Advances in Carbohydrate Chemistry and Biochemistry. UK: Academic Press 115-217. https://doi.org/10.1016/B978-0-12-385520-6.00004-2
[55]	Guo JH, Skinner GW, Harcum WW, et al. (1998) Pharmaceutical applications of naturally occurring water-soluble polymers. Pharm Sci Technol Today 1: 254-261. https://doi.org/10.1016/S1461-5347(98)00072-8
[56]	Melo MRS, Feitosa JPA, Freitas ALP, et al. (2002) Isolation and characterization of soluble sulfated polysaccharide from the red seaweed Gracilaria cornea. Carbohydr Polym 49: 491-498. https://doi.org/10.1016/S0144-8617(02)00006-1
[57]	Rengasamy KR, Mahomoodally MF, Aumeeruddy MZ, et al. (2020) Bioactive compounds in seaweeds: An overview of their biological properties and safety. Food Chem Toxicol 135: 111013. https://doi.org/10.1016/j.fct.2019.111013
[58]	Barros FCN, Da Silva DC, Sombra VG, et al. (2013) Structural characterization of polysaccharide obtained from red seaweed Gracilaria caudata (J Agardh). Carbohydr Polym 92: 598-603. https://doi.org/10.1016/j.carbpol.2012.09.009
[59]	Ale MT, Maruyama H, Tamauchi H, et al. (2011) Fucose-containing sulfated polysaccharides from brown seaweeds inhibit proliferation of melanoma cells and induce apoptosis by activation of caspase-3 in vitro. Mar Drugs 9: 2605-2621. https://doi.org/10.3390/md9122605
[60]	Patel S (2012) Therapeutic importance of sulfated polysaccharides from seaweeds: updating the recent findings. 3 Biotech 2: 171-185. https://doi.org/10.1007/s13205-012-0061-9
[61]	Chen C, Zhao Z, Ma S, et al. (2019) Optimization of ultrasonic-assisted extraction, refinement and characterization of water-soluble polysaccharide from Dictyosphaerium sp. and evaluation of antioxidant activity in vitro. J Food Meas Charact 14: 963-977. https://doi.org/10.1007/s11694-019-00346-7
[62]	Kan Y, Chen T, Wu Y, et al. (2015) Antioxidant activity of polysaccharide extracted from Ganoderma lucidum using response surface methodology. Int J Biol Macromol 72: 151-157. https://doi.org/10.1016/j.ijbiomac.2014.07.056
[63]	Gómez-Ordóñez E, Jiménez-Escrig A, Rupérez P (2014) Bioactivity of sulfated polysaccharides from the edible red seaweed Mastocarpus stellatus. Bioact Carbohydrates Diet Fibre 3: 29-40. https://doi.org/10.1016/j.bcdf.2014.01.002
[64]	Yarnpakdee S, Benjakul S, Senphan T (2019) Antioxidant activity of the extracts from freshwater macroalgae (Cladophora glomerata) grown in Northern Thailand and its preventive effect against lipid oxidation of refrigerated eastern little tuna slice. Turkish J Fish Aquat Sci 19: 209-219. https://doi.org/10.4194/1303-2712-v19_03_04
[65]	Wang J, Hu S, Nie S, et al. (2016) Reviews on mechanisms of in vitro antioxidant activity of polysaccharides. Oxid Med Cell Longev 2016: 5692852. https://doi.org/10.1155/2016/5692852
[66]	de Oliveira FC, Coimbra JS dos R, de Oliveira EB, et al. (2016) Food Protein-polysaccharide Conjugates Obtained via the Maillard Reaction: A Review. Crit Rev Food Sci Nutr 56: 1108-1125. https://doi.org/10.1080/10408398.2012.755669
[67]	Alisi IO, Uzairu A, Abechi SE (2020) Free radical scavenging mechanism of 1,3,4-oxadiazole derivatives: thermodynamics of O–H and N–H bond cleavage. Heliyon 6: e03683. https://doi.org/10.1016/j.heliyon.2020.e03683
[68]	El Kady EM (2019) New Trends of the Polysaccharides as a Drug. World J Agric Soil Sci 3: 1-22. https://doi.org/10.33552/wjass.2019.03.000572
[69]	Li H, Mao W, Zhang X, et al. (2011) Structural characterization of an anticoagulant-active sulfated polysaccharide isolated from green alga Monostroma latissimum. Carbohydr Polym 85: 394-400. https://doi.org/10.1016/j.carbpol.2011.02.042
[70]	Guru SMM, Vasanthi M, Achary A (2015) Antioxidant and free radical scavenging potential of crude sulphated polysaccharides from Turbinaria ornata. Biologia (Bratisl) 70: 27-33. https://doi.org/10.1515/biolog-2015-0004
[71]	Shao P, Chen X, Sun P (2014) Chemical characterization, antioxidant and antitumor activity of sulfated polysaccharide from Sargassum horneri. Carbohydr Polym 105: 260-269. https://doi.org/10.1016/j.carbpol.2014.01.073
[72]	Cao M, Wang S, Gao Y, et al. (2020) Study on physicochemical properties and antioxidant activity of polysaccharides from Desmodesmus armatus. J Food Biochem 44: 1-13. https://doi.org/10.1111/jfbc.13243
[73]	Díaz-Gutierrez D, Méndez Ortega W, de Oliveira e Silva AM, et al. (2015) Comparation of antioxidants properties and polyphenols content of aqueous extract from seaweeds Bryothamnion triquetrum and Halimeda opuntia. Ars Pharm 56: 89-99. https://doi.org/10.4321/S2340-98942015000200003
[74]	Khalili M, Ebrahimzadeh MA, Safdari Y (2014) Antihaemolytic activity of thirty herbal extracts in mouse red blood cells. Arch Ind Hyg Toxicol 65: 399-406. https://doi.org/10.2478/10004-1254-65-2014-2513
[75]	Hernández-Ruiz KL, Ruiz-Cruz S, Cira-Chávez LA, et al. (2018) Evaluation of antioxidant capacity, protective effect on human erythrocytes and phenolic compound identification in two varieties of plum fruit (Spondias spp.) by UPLC-MS. Molecules 23: 3200. https://doi.org/10.3390/molecules23123200
[76]	García-Romo JS, Noguera-Artiaga L, Gálvez-Iriqui AC, et al. (2020) Antioxidant, antihemolysis, and retinoprotective potentials of bioactive lipidic compounds from wild shrimp (Litopenaeus stylirostris) muscle. CYTA-J Food 18: 153-163. https://doi.org/10.1080/19476337.2020.1719210
[77]	Liu RH, Finley J (2005) Potential cell culture models for antioxidant research. J Agric Food Chem 53: 4311-4314. https://doi.org/10.1021/jf058070i
[78]	Babu BH, Shylesh BS, Padikkala J (2001) Antioxidant and hepatoprotective effect of Acanthus ilicifolius. Fitoterapia 72: 272-277. https://doi.org/10.1016/S0367-326X(00)00300-2
[79]	Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408: 239-247. https://doi.org/10.1038/35041687
[80]	Ingrosso D, D'Angelo S, di Carlo E, et al. (2000) Increased methyl esterification of altered aspartyl residues erythrocyte membrane proteins in response to oxidative stress. Eur J Biochem 267: 4397-4405. https://doi.org/10.1046/j.1432-1327.2000.01485.x
[81]	Prior RL, Wu X, Schaich K (2005) Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem 53: 4290-4302. https://doi.org/10.1021/jf0502698

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