Abstract
Sulfated polysaccharides were isolated from two Tunisian fish skins grey triggerfish (Balistes capriscus) (GTSP) and smooth hound (Mustelus mustelus) (SHSP). Their chemical and physical characteristics were investigated. The Analysis of surface morphology by scanning electron microscopy of both sulfated polysaccharides displayed the same shape with netted structure. The antioxidant activities of GTSP and SHSP were evaluated using various in vitro antioxidant assays: 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical-scavenging activity, reducing power, β-carotene bleaching inhibition assay (IC50 GTSP = 0.5 mg mL−1 and IC50 SHSP = 0.6 mg mL−1) and DNA nicking assay. Both sulfated polysaccharides exhibited good antioxidant activities. The sulfated polysaccharides showed strong angiotensin I-converting enzyme inhibitory activities (IC50 GTSP = 0.16 mg mL−1 and IC50 SHSP = 0.18 mg mL−1). These results revealed that GTSP and SHSP exhibited significant antihypertensive activities. Overall, the results indicated that grey triggerfish and smooth hound skins can be used to generate high value-added products, thus offering a valuable source of bioactive sulfated polysaccharides for application in wide range of biotechnological applications.
Similar content being viewed by others
References
Sila A, Haddar A, Martinez-Alvarez O, Bougatef A (2013) Angiotensin-I-converting enzyme inhibitory and antioxidant activities of protein hydrolysate from muscle of barbel (Barbus callensis). J Chem (Article ID 545303)
Shahidi F, Xiao-Qing H, Synowiecki J (1995) Production and characteristics of protein hydrolysates from capelin (Mallotus villosus). Food Chem 53:285
Johnston-Banks FA (1990) Gelatine. In: Harris P (ed) Food gels. Elsevier Science, Essex, pp 233–289
Chakraborty K, Paulraj R (2010) Sesquiterpenoids with free-radical-scavengingproperties from marine macroalga Ulva fasciata Delile. Food Chem 122:31
Ye H, Wang KQ, Zhou CH, Liu J, Zeng XX (2008) Purification, antitumorand antioxidant activities in vitro of polysaccharides from the brown seaweed Sargassum pallidum. Food Chem 111:428
Wang ZH, Wu BJ, Zhang XH, Xu M, Chang HM, Lu XY, Ren X (2012) Purification of a polysaccharide from Boschniakia rossica and its synergistic antitumoreffect combined with 5-Fluorouracil. Carbohydr Polym 89:31
Becker CF, Guimarães JA, Mourão PAS, Verli H (2007) Conformationof sulfated galactan and sulfated fucan in aqueous solutions: implications totheir anticoagulant activities. J Mol Graph Model 26:391
Melo MRS, Feitosa JPA, Freitas ALP, De Paula RCM (2002) Isolation and characterization of soluble sulfated polysaccharide from the red seaweed Gracilaria cornea. Carbohydr Polym 49:491
Kil HY, Seong ES, Ghimire BK, Chung IM, Kwon SS, Goh EJ, Heo K, Kim MJ, Lim JD, Lee D, Yu CY (2009) Antioxidant and antimicrobial activities of crude sorghum extract. Food Chem 115:1234
Nikolić M, Glamočlija J, Ferreira ICFR, Calhelha RC, Fernandes A, Marković T, Giweli A, Soković M (2014) Chemical composition, antimicrobial, antioxidant and antitumor activity of Thymus serpyllum L., Thymus algeriensis Boiss. and Reut and Thymus vulgaris L. essential oils. Ind Crops Prod 52:183
Li HB, Wong CC, Cheng KW, Chen F (2008) Antioxidant properties in vitro and total phenolic contents in methanol extracts from medicinal plants. LWT Food Sci Technol 41:385
Wu M, Wu Y, Qu M, Li W, Yan X (2013) Evaluation of antioxidant activities of water-soluble polysaccharides from brown alga Hizikia fusiformis. Int J Biol Macromol 56:28
Abdelmalek BE, Sila A, Krichen F, Karoud W, Martinez-Alvarez O, Ellouz-Chaabouni S, Ayadi MA, Bougatef A (2015) Sulfated polysaccharides from Loligo vulgaris skin: potential biological activities and partial purification. Int J Biol Macromol 72:1143
Chen Y, Zhang H, Wang Y, Nie S, Li C, Xie M (2014) Acetylation and carboxymethylation of the polysaccharide from Ganoderma atrum and their antioxidant and immunomodulating activities. Food Chem 156:279
Shao P, Chen X, Sun P (2013) In vitro antioxidant and antitumor activities of different sulfated polysaccharides isolated from three algae. Int J Biol Macromol 62:155
Wang J, Zhang Q, Zhang Z, Zhang J, Li P (2009) Synthesized phosphorylated and aminated derivatives of fucoidan and their potential antioxidant activity in vitro. Int J Biol Macromol 44:170
Erdös EG (1975) Angiotensin I-converting enzyme. Circ Res 36:247
Balti R, Nedjar-Arroume N, Bougatef A, Guillochon D, Nasri M (2010) Three novel angiotensin I-converting enzyme (ACE) inhibitory peptides from cuttlefish (Sepia officinalis) using digestive proteases. Food Res Int 43:11361
Bougatef A, Nedjar-Arroume N, Ravallec-Plé R, Leroy Y, Guillochon D, Barkia A, Nasri M (2008) Angiotensin I-converting enzyme (ACE) inhibitory activities of sardinelle (Sardinella aurita) by-products protein hydrolysates obtained by treatment with microbial and visceral fish serine proteases. Food Chem 111:350
Acharya KR, Sturrock ED, Riordan JF, Ehlers MRW (2003) ACE revisited: a new target for structure-based drug design. Nat Rev Drug Discov 2:891
Ben Mansour M, Majdoub H, Bataille I, Roudesli MS, Hassine M, Ajzenberg N, Chaubet F, Maaroufi RM (2009) Polysaccharides from the skin of the ray Raja radula. Partial characterization and anticoagulant activity. Thromb Res 123:671
AOAC (2000) Official methods of analysis, 17th edn. Association of Official Analytical, Washington
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350
Bitter T, Muir HM (1962) A modified uronic acid carbazole reaction. Anal Biochem 4:330
López-Franco YL, Cervantes-Montaño CI, Martínez-Robinson KG, Lizardi-Mendoza J, Robles-Ozuna LE (2013) Physicochemical characterization and functional properties of galactomannans from mesquite seeds (Prosopis spp.). Food Hydrocoll 30:656
Bersuder P, Hole M, Smith G (1998) Antioxidants from a heated histidine–glucose model system. I. Investigation of the antioxidant role of histidine and isolation of antioxidants by high performance liquid chromatography. J Am Oil Chem Soc 75:181
Zhao GR, Xiang ZJ, Ye TX, Yuan YJ, Guo ZX (2006) Antioxidant activities of Salvia miltiorrhiza and Panax notoginseng. Food Chem 99:676
Koleva II, van Beek TA, Linssen JPH, de Groot A, Evstatieva LN (2002) Screening of plant extracts for antioxidant activity: a comparative study on three testing methods. Phytochem Anal 13:817
Lee J, Kim H, Kim J, Jang Y (2002) Antioxidant property of an ethanol extract of the stem of Opuntia ficus-indica var. Saboten. J Agric Food Chem 50:6490
Nakamura Y, Yamamoto N, Sakai K, Okubo A, Yamazaki S, Takano T (1995) Purification and characterization of angiotensin I-converting-enzyme inhibitors from Sour milk. J Dairy Sci 78:777
Krichen F, Karoud W, Sila A, Abdelmalek BE, Ghorbel R, Ellouz-Chaabouni S, Bougatef A (2015) Extraction, characterization and antimicrobial activity of sulfated polysaccharides from fish skins. Int J Biol Macromol 75:283
Cardozo FTGS, Camelini CM, Cordeiro MNS, Mascarello A, Malagoli BG, Iv Larsen, Rossi MJ, Nunes RJ, Braga FC, Brandt CR, Simões CMO (2013) Characterization and cytotoxic activity of sulfated derivatives of polysaccharides from Agaricus brasiliensis. Int J Biol Macromol 57:265
Hong JH, Choi YH (2006) Physico-chemical properties of protein-bound polysaccharide from Agaricus blazei Murill prepared by ultrafiltration and spray drying process. Int J Food Sci Technol 42:18
Nep EI, Conway BR (2009) Physicochemical characterization of grewia polysaccharide gum: effect of drying method. J Pharm Pharmacol 61:A47
Yang Y, Liu D, Wu J, Chen Y, Wang S (2011) In vitro antioxidant activities of sulfated polysaccharide fractions extracted from Corallina officinalis. Int J Biol Macromol 49:1031
Dakia P, Blecker C, Robert C, Wathelet B, Paquot M (2008) Composition and physicochemical properties of locust bean gum extracted from whole seeds by acid or water dehulling pre-treatment. Food Hydrocoll 22:807
Zhao X, Li B, Xue C, Sun L (2012) Effect of molecular weight on the antioxidant property of low molecular weight alginate from Laminaria japonica. J App Phycol 24:295
Barahona T, Chandıa NP, Encinas MV, Matsuhiro B, Zuniga EA (2011) Antioxidant capacity of sulfated polysaccharides from seaweeds. A kinetic approach. Food Hydrocoll 25:529
Chen SK, Tsai ML, Huang JR, Chen RH (2009) In vitro antioxidant activities of low-molecular-weight polysaccharides with various functional groups. J Agric Food Chem 57:2699
Wang H, Gao XD, Zhou GC, Cai L, Yao WB (2008) In vitro and in vivo antioxidant activity of aqueous extract from Choerospondias axillaris fruit. Food Chem 106:888
Souza BWS, Cerqueira MA, Bourbon AI, Pinheiro AC, Martins JT, Teixeira JA, Coimbra MA, Vicente AA (2012) Chemical characterization and antioxidant activity of sulfated polysaccharide from the red seaweed Gracilaria birdiae. Food Hydrocol 27:287
Vijayabaskar P, Vaseela N (2012) In vitro antioxidant properties of sulfated polysaccharide from brown marine algae Sargassum tenerrimum. Asian Pac J Trop Disease 2:S890
Abu R, Jiang Z, Ueno M, Okimura T, Yamaguchi K, Oda T (2013) In vitro antioxidant activities of sulfated polysaccharide ascophyllan isolated from Ascophyllum nodosum Int. J Biol Macromol 59:305
Jayaprakasha GK, Singh RP, Sakariah KK (2001) Antioxidant activity of grape seed (Vitis vinifera) extracts on peroxidation models in vitro. Food Chem 73:285
Chandrasekara A, Shahidi F (2011) Bioactivities and antiradical properties of millet grains and hulls. J Agric Food Chem 59:9563
Kittiphattanabawon P, Benjakul S, Visessanguan W, Shahidi F (2013) Inhibition of angiotensin converting enzyme, human LDL cholesterol and DNA oxidation by hydrolysates from blacktip shark gelatin. LWT Food Sci Technol 51:177
Davies KJA (1995) Oxidative stress: the paradox of aerobic life. In: Rice-Evans C, Halliwell B, Lunt GG (eds) Free radical and oxidative stress: environments, drugs and food additives. Portland Press Ltd., London, p 16
Zhong Y, Shahidi F (2012) Lipophilised epigallocatechin gallate (EGCG) derivatives and their antioxidant potential in food and biological systems. Food Chem 131:22
Agostoni A, Cicardi M (2001) Drug-induced angioedema without urticaria incidence, prevention and management. Drug Saf 24:599
Nakamura H (1987) Effects of antihypertensive drugs on plasma lipids. Am J Cardiol 60:24E
Sesoko S, Kaneko Y (1985) Cough associated with the use of captopril. Arch Intern Med 145:1524
Acknowledgments
This work was funded by Ministry of Higher Education and Scientific Research, Tunisia.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Krichen, F., Karaoud, W., Sayari, N. et al. Sulfated Polysaccharides from Tunisian Fish Skins: Antioxidant, DNA Damage Protective Effect and Antihypertensive Activities. J Polym Environ 24, 166–175 (2016). https://doi.org/10.1007/s10924-016-0759-6
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10924-016-0759-6