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Sulfated Polysaccharides from Tunisian Fish Skins: Antioxidant, DNA Damage Protective Effect and Antihypertensive Activities

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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.

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References

  1. 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)

  2. Shahidi F, Xiao-Qing H, Synowiecki J (1995) Production and characteristics of protein hydrolysates from capelin (Mallotus villosus). Food Chem 53:285

    Article  CAS  Google Scholar 

  3. Johnston-Banks FA (1990) Gelatine. In: Harris P (ed) Food gels. Elsevier Science, Essex, pp 233–289

    Chapter  Google Scholar 

  4. Chakraborty K, Paulraj R (2010) Sesquiterpenoids with free-radical-scavengingproperties from marine macroalga Ulva fasciata Delile. Food Chem 122:31

    Article  CAS  Google Scholar 

  5. 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

    Article  CAS  Google Scholar 

  6. 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

    Article  Google Scholar 

  7. 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

    Article  CAS  Google Scholar 

  8. 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

    Article  CAS  Google Scholar 

  9. 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

    Article  CAS  Google Scholar 

  10. 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

    Article  Google Scholar 

  11. 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

    Article  CAS  Google Scholar 

  12. 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

    Article  CAS  Google Scholar 

  13. 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

    Article  CAS  Google Scholar 

  14. 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

    Article  CAS  Google Scholar 

  15. 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

    Article  CAS  Google Scholar 

  16. 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

    Article  Google Scholar 

  17. Erdös EG (1975) Angiotensin I-converting enzyme. Circ Res 36:247

    Article  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. 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

    Article  CAS  Google Scholar 

  20. 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

    Article  CAS  Google Scholar 

  21. 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

    Article  CAS  Google Scholar 

  22. AOAC (2000) Official methods of analysis, 17th edn. Association of Official Analytical, Washington

    Google Scholar 

  23. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350

    Article  CAS  Google Scholar 

  24. Bitter T, Muir HM (1962) A modified uronic acid carbazole reaction. Anal Biochem 4:330

    Article  CAS  Google Scholar 

  25. 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

    Article  Google Scholar 

  26. 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

    Article  CAS  Google Scholar 

  27. Zhao GR, Xiang ZJ, Ye TX, Yuan YJ, Guo ZX (2006) Antioxidant activities of Salvia miltiorrhiza and Panax notoginseng. Food Chem 99:676

    Article  Google Scholar 

  28. 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

    Article  Google Scholar 

  29. 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

    Article  CAS  Google Scholar 

  30. 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

    Article  CAS  Google Scholar 

  31. 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

    Article  CAS  Google Scholar 

  32. 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

    Article  CAS  Google Scholar 

  33. 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

    Google Scholar 

  34. Nep EI, Conway BR (2009) Physicochemical characterization of grewia polysaccharide gum: effect of drying method. J Pharm Pharmacol 61:A47

    Article  Google Scholar 

  35. 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

    Article  CAS  Google Scholar 

  36. 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

    Article  CAS  Google Scholar 

  37. 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

    Article  CAS  Google Scholar 

  38. 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

    Article  CAS  Google Scholar 

  39. 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

    Article  CAS  Google Scholar 

  40. 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

    Article  CAS  Google Scholar 

  41. 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

    Article  CAS  Google Scholar 

  42. 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

    Article  CAS  Google Scholar 

  43. 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

    Article  CAS  Google Scholar 

  44. Jayaprakasha GK, Singh RP, Sakariah KK (2001) Antioxidant activity of grape seed (Vitis vinifera) extracts on peroxidation models in vitro. Food Chem 73:285

    Article  CAS  Google Scholar 

  45. Chandrasekara A, Shahidi F (2011) Bioactivities and antiradical properties of millet grains and hulls. J Agric Food Chem 59:9563

    Article  CAS  Google Scholar 

  46. 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

    Article  CAS  Google Scholar 

  47. 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

    Google Scholar 

  48. Zhong Y, Shahidi F (2012) Lipophilised epigallocatechin gallate (EGCG) derivatives and their antioxidant potential in food and biological systems. Food Chem 131:22

    Article  CAS  Google Scholar 

  49. Agostoni A, Cicardi M (2001) Drug-induced angioedema without urticaria incidence, prevention and management. Drug Saf 24:599

    Article  CAS  Google Scholar 

  50. Nakamura H (1987) Effects of antihypertensive drugs on plasma lipids. Am J Cardiol 60:24E

    Article  CAS  Google Scholar 

  51. Sesoko S, Kaneko Y (1985) Cough associated with the use of captopril. Arch Intern Med 145:1524

    Article  CAS  Google Scholar 

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Acknowledgments

This work was funded by Ministry of Higher Education and Scientific Research, Tunisia.

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Correspondence to Ali Bougatef.

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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

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  • DOI: https://doi.org/10.1007/s10924-016-0759-6

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