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Effect of Desulfation of Polysaccharides from Sea Urchin Eggs Paracentrotus Lividus on Antiproliferative Activity

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Abstract

This study aims to study the impact of reducing the sulfate content and molecular weight of polysaccharides extracted from sea urchin eggs (Paracentrotus lividus) on antiproliferative activity against Caco-2 and B16 cell lines. Sulfated polysaccharides were initially extracted from sea urchin eggs, followed by a desulfation process. The characterization involved various techniques: Fourier-transform infrared spectroscopy for demonstrating desulfation, Gas Chromatography/Mass Spectrometry for determining monosaccharide composition, Size Exclusion Chromatography for confirming molecular weight reduction, and centesimal analysis for quantifying sulfate content. The initial molecular weight was 24,000 kg/mol decreased to 960 kg/mol, and sulfate content reduced from 9.41 to 1.31% after 4 h of desulfation. The investigation reveals that a decrease in sulfate content corresponded to a reduction in molecular weight, leading to an increase in antiproliferative activity. At a concentration of 400 µg/mL, inhibition percentages against Caco-2 cells increased from 43.14% for native sulfated polysaccharide to 79.68% after 4 h of desulfation. Similarly, for antiproliferative activity against B16 cells, native polysaccharide exhibited 60.71% inhibition, whereas desulfated polysaccharide after 4 h showed an increased inhibition percentage of 82.23%. This investigation demonstrates the specific contributions of these two factors to the observed antiproliferative effects. While sulfate content plays a role in antiproliferative activity, molecular weight emerged as the most crucial factor for enhancing this effect. These findings contribute valuable insights into the optimization of sea urchin eggs-derived polysaccharides for potential anticancer treatment, highlighting the importance of balancing sulfate content and molecular weight for therapeutic efficacy.

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References

  1. Hossain A, Dave D, Shahidi F (2023) Sulfated polysaccharides in sea cucumbers and their biological properties: a review. Int J Biol Macromol 253:127329. https://doi.org/10.1016/j.ijbiomac.2023.127329

    Article  CAS  PubMed  Google Scholar 

  2. Sibiya A, Jeyavani J, Sivakamavalli J, Ravi C, Divya M, Vaseeharan B (2021) Bioactive compounds from various types of sea urchin and their therapeutic effects — a review Reg. Stud Mar Sci 44:101760. https://doi.org/10.1016/j.rsma.2021.101760

    Article  Google Scholar 

  3. He Y, Xu M, Lu S, Zou W, Wang Y, Kulyar MFA, Iqbal M, Li K (2023) Seaweed polysaccharides treatment alleviates injury of inflammatory responses and gut barrier in LPS-induced mice. Microb Pathog 180:106159. https://doi.org/10.1016/j.micpath.2023.106159

    Article  CAS  PubMed  Google Scholar 

  4. Ju J, Yang J, Zhang WC, Wei Y, Yuan H, Tan Y (2023) Seaweed polysaccharide fibers: solution properties, processing and applications. J Mater Sci Technol 140:1–18. https://doi.org/10.1016/j.jmst.2022.07.053

    Article  CAS  Google Scholar 

  5. Hu Y, Zhang Y, Xu J, Zi Y, Peng J, Zheng Y, Wang X, Zhong J (2022) Fish gelatin-polysaccharide Maillard products for fish oil-loaded emulsion stabilization: effects of polysaccharide type, reaction time, and reaction pH. LWT 172:114220. https://doi.org/10.1016/j.lwt.2022.114220

    Article  CAS  Google Scholar 

  6. Rifna EJ, Rajauria G, Dwivedi M, Tiwari BK (2024) Circular economy approaches for the production of high-value polysaccharides from microalgal biomass grown on industrial fish processing wastewater: a review. Int J Biol Macromol 254:126887. https://doi.org/10.1016/j.ijbiomac.2023.126887

    Article  CAS  PubMed  Google Scholar 

  7. Yosri N, Khalifa AMS, Guo Z, Xu B, Zou X, El-Seedi RH (2021) Marine organisms: Pioneer natural sources of polysaccharides/proteins for green synthesis of nanoparticles and their potential applications. Int J Biol Macromol 193:1767–1798. https://doi.org/10.1016/j.ijbiomac.2021.10.229

    Article  CAS  PubMed  Google Scholar 

  8. Cui R, Zhu F (2021) Ultrasound modified polysaccharides: a review of structure, physicochemical properties, biological activities and food applications. Trends Food Sci Technol 107:491–508. https://doi.org/10.1016/j.tifs.2020.11.018

    Article  CAS  Google Scholar 

  9. Robbins NJ, McKeever TJ (1990) Developing a Newfoundland sea urchin fishery, Trinity-Placentia Development Association. Canada/ Newfoundland Inshore Fisheries Development

  10. Barrier C, Ternengo S, El Idrissi O, Piacentini L, Barrier N, Lett C, Pasqualini V, Durieux EDH (2024) Edible Sea urchin (Paracentrotus lividus) larval dispersal and connectivity modelling in the northwestern Mediterranean Sea. J Sea Res 197:102464. https://doi.org/10.1016/j.seares.2023.102464

    Article  Google Scholar 

  11. Elmasry E, Abdelrazek FA, El-Sayed AFM (2023) Growth pattern and population status of the sea urchin Paracentrotus lividus (Lamarck, 1816) on the Mediterranean coast of Egypt Egypt. J Aquat Res 49:409–416. https://doi.org/10.1016/j.ejar.2023.07.001

    Article  Google Scholar 

  12. Camacho C, Correia T, Teixeira B, Mendes R, Valente LMP, Pessoa MF, Nunes ML, Gonçalves A (2023) Nucleotides and free amino acids in sea urchin Paracentrotus lividus gonads: contributions for freshness and overall taste. Food Chem 404:134505. https://doi.org/10.1016/j.foodchem.2022.134505

    Article  CAS  PubMed  Google Scholar 

  13. Zarrouk A, Salem YB, Hafsa J, Sghaier R, Charfeddine B, Limem K, Hammami M, Majdoub H (2018) 7β-hydroxycholesterol-induced cell death, oxidative stress, and fatty acid metabolism dysfunctions attenuated with sea urchin egg oil. Biochimie 153:210–219. https://doi.org/10.1016/j.biochi.2018.06.027

    Article  CAS  PubMed  Google Scholar 

  14. Arafa S, Chouaibi M, Sadok S, ElAbed A (2012) The influence of season on the gonad index and biochemical composition of the sea urchin Paracentrotus lividus from the Golf of Tunis. Sci World J 815935. https://doi.org/10.1100/2012/815935

  15. Riediger ND, Othman RA, Suh M, Moghadasian MH (2009) A systemic review of the roles of n-3 fatty acids in health and disease. J Am Diet Assoc 109:668–679. https://doi.org/10.1016/j.jada.2008.12.022

    Article  CAS  PubMed  Google Scholar 

  16. Salem YB, Amri S, Hammi KM, Abdelhamid A, LeCerf D, Bouraoui A, Majdoub H (2017) Physico-chemical characterization and pharmacological activities of Sulfated Polysaccharide from Sea Urchin, Paracentrotus lividus. Int J Biol Macromol 97:8–15. https://doi.org/10.1016/j.ijbiomac.2017.01.007

    Article  CAS  PubMed  Google Scholar 

  17. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597. https://doi.org/10.1007/s10811-010-9632-5

    Article  CAS  Google Scholar 

  18. Li B, Lu F, Wei X, Zhao R (2008) Fucoidan: structure and Bioactivity. Molecules 13:1671–1695. https://doi.org/10.3390/molecules13081671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Fernandes PAR, Coimbra MA (2023) The antioxidant activity of polysaccharides: a structure-function relationship overview. Carbohydr Polym 314:120965. https://doi.org/10.1016/j.carbpol.2023.120965

    Article  CAS  PubMed  Google Scholar 

  20. Necas J, Bartosikova L (2013) Carrageenan: a review. J Vet Med 58:187–205

    CAS  Google Scholar 

  21. Gao N, Chen R, Mou R, Xiang J, Zhou K, Li Z, Zhao J (2020) Purification, structural characterization and anticoagulant activities of four sulfated polysaccharides from sea cucumber Holothuria fuscopunctata. Int J Biol Macromol 164:3421–3428. https://doi.org/10.1016/j.ijbiomac.2020.08.150

    Article  CAS  PubMed  Google Scholar 

  22. Zhu Q, Lin L, Zhao M (2020) Sulfated fucan/fucosylated chondroitin sulfate-dominated polysaccharide fraction from low-edible-value sea cucumber ameliorates type 2 diabetes in rats: New prospects for sea cucumber polysaccharide based-hypoglycemic functional food. Int J Biol Macromol 159:34–45. https://doi.org/10.1016/j.ijbiomac.2020.05.043

    Article  CAS  PubMed  Google Scholar 

  23. Mansour MB, Majdoub M, Bataille I, AJzenberg N, Chaubet F, Maaroufi RM (2009) Polysaccharides from the skin of the ray Raja radula. Partial characterization and anticoagulant activity. Thromb Res 123:671–678. https://doi.org/10.1016/j.thromres.2008.05.018

    Article  CAS  PubMed  Google Scholar 

  24. Bougatef H, Ghlissi Z, Kallel R, Amour IB, Boudawara T, Gargouri J, Sahnoun Z, Volpi N, Sila A, Bougatef A (2020) Chondroitin/dermatan sulfate purified from corb (Sciaena umbra) skin and bone: in vivo assessment of anticoagulant activity. Int J Biol Macromol 164:131–139. https://doi.org/10.1016/j.ijbiomac.2020.07.096

    Article  CAS  PubMed  Google Scholar 

  25. Mansour MB, Balti R, Ollivier V, Jannet HB, Chaubet F, Maaroufi RM (2017) Characterization and anticoagulant activity of a fucosylated chondroitin sulfate with unusually procoagulant effect from sea cucumber. Carbohydr Polym 174:760–771. https://doi.org/10.1016/j.carbpol.2017.06.128

    Article  CAS  PubMed  Google Scholar 

  26. Shao P, Pei Y, Fang Z, Sun P (2014) Effects of partial desulfation on antioxidant and inhibition of DLD cancer cell of Ulva fasciata polysaccharide. Int J Biol Macromol 65:307–313. https://doi.org/10.1016/j.ijbiomac.2014.01.043

    Article  CAS  PubMed  Google Scholar 

  27. Karmakar P, Pujol CA, Damonte EB, Ghosh T, Ray B (2010) Polysaccharides from Padina Tetrastromatica: structural features, chemical modification and antiviral activity. Carbohydr Polym 80:513–520. https://doi.org/10.1016/j.carbpol.2009.12.014

    Article  CAS  Google Scholar 

  28. Li X, Li S, Liu J, Lin L, Sun H, Yang W, Cai Y, Gao N, Zhou L, Qin H, Yin R, Zhao JH (2021) A regular fucan sulfate from Stichopus herrmanni and its peroxide depolymerization: structure and anticoagulant activity. Carbohydr Polym 256:117513. https://doi.org/10.1016/j.carbpol.2020.117513

    Article  CAS  PubMed  Google Scholar 

  29. Miller IJ, Blunt JW (1998) Desulfation of algal galactans. Carbohydr Res 309:39–43. https://doi.org/10.1016/S0008-6215(98)00104-9

    Article  CAS  Google Scholar 

  30. Kolender AA, Matulewicz MC (2004) Desulfation of sulfated galactans with chlorotrimethylsilane. Characterization of β-carrageenan by 1 H NMR spectroscopy. Carbohydr Res 339:1619–1629. https://doi.org/10.1016/j.carres.2004.03.029

    Article  CAS  PubMed  Google Scholar 

  31. Mansour MB, Balti R, Yacoubi L, Olivier V, Chaubet F, Maaroufi RM (2019) Primary structure and anticoagulant activity of fucoidan from the sea cucumber Holothuria Polii. Int J Biol Macromol 121:1145–1153. https://doi.org/10.1016/j.ijbiomac.2018.10.129

    Article  CAS  PubMed  Google Scholar 

  32. Han W, Li Q, Lv Y, Wang QC, Zhao X (2018) Preparation and structural characterization of regioselective 4-O/6-O-desulfated chondroitin sulfate. Carbohydr Res 460:8–13. https://doi.org/10.1016/j.carres.2018.01.010

    Article  CAS  PubMed  Google Scholar 

  33. Navarro DA, Flores ML, Stortz CA (2007) Microwave-assisted desulfation of sulfated polysaccharides. Carbohydr Polym 69:742–747. https://doi.org/10.1016/j.carbpol.2007.02.009

    Article  CAS  Google Scholar 

  34. Usov A, Miroshnikova L, Kochetkov N (1972) Polysaccharides of algae IX. Solvolytic removal of sulfate groups from polysaccharides obtained from the red alga Laingia Pacifica. Zhurnal Obshcheii Khimii 42:945–949

    CAS  Google Scholar 

  35. Sakly N, Marzouk W, Ben Ouada H, Majdoub H (2017) Enhancing performances of colorimetric response of carboxymethylcellulose-stabilized silver nanoparticles: a fully eco-friendly assay for Hg2+ detection. Sens Actuators B Chem 253:918–927. https://doi.org/10.1016/j.snb.2017.07.035

    Article  CAS  Google Scholar 

  36. Zimm BH (1948) Apparatus and methods for measurement and interpretation of the angular variation of light scattering; preliminary results on polystyrene solutions. J Chem Phys 16:1099–1116. https://doi.org/10.1063/1.1746740

    Article  CAS  Google Scholar 

  37. Majdoub H, Roudesli S, Picton L, LeCerf D, Muller G, Grisel M (2001) Prickly pear nopals pectin from Opuntia ficus-indica physico-chemical study in dilute and semi- dilute solutions. Carbohydr Polym 46:69–79. https://doi.org/10.1016/S0144-8617(00)00284-8

    Article  CAS  Google Scholar 

  38. Sfar M, Souid G, Mzoughi Z, Le Cerf D, Majdoub H (2023) Hepatoprotective Effect against Cadmium-Induced Liver toxicity in rats of Foeniculum vulgare seed polysaccharides. Chem Afr 6:1–13. https://doi.org/10.1007/s42250-023-00621-7

    Article  CAS  Google Scholar 

  39. Ali G, Rihouey C, Larreta-Garde V, LeCerf D, Picton L (2013) Molecular size characterization and kinetics studies on hydrolysis of pullulan by pullulanase in an entangled alginate medium. Biomacromolecules 14:2234–2241. https://doi.org/10.1021/bm400371

    Article  CAS  PubMed  Google Scholar 

  40. Hammi KM, Hammami M, Rihouey C, LeCerf D, Ksouri R, Majdoub H (2016) Optimization extraction of polysaccharide from Tunisian Zizyphus lotus fruit by response surface methodology: composition and antioxidant activity. Food Chem 212:476–484. https://doi.org/10.1016/j.foodchem.2016.06.004

    Article  CAS  Google Scholar 

  41. Teka N, Lazreg H, Horchani M, Rihouey C, Le Cerf D, Ben Jannet H, Majdoub H (2022) Characterization, α-amylase inhibition and in silico docking study of polysaccharides extracted from rosy garlic (Allium Roseum) bulbs. Chem Afr 5:1997–2009. https://doi.org/10.1007/s42250-022-00497-z

    Article  CAS  Google Scholar 

  42. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63. https://doi.org/10.1016/0022-1759(83)90303-4

    Article  CAS  PubMed  Google Scholar 

  43. Yang J, Yi M, Pan J, Zhao J, Sun L, Lin X, Cao Y, Huang L, Zhu B, Yu C (2015) Sea urchin (Strongylocentrotus Intermedius) polysaccharide enhanced BMP-2 induced osteogenic differentiation and its structural analysis. J Funct Foods 14:519–528. https://doi.org/10.1016/j.jff.2015.02.025

    Article  CAS  Google Scholar 

  44. Dammak MI, Majdoub H (2023) A review of the characterization and Biological Properties of Polysaccharides from Food Waste. Chem Afr 1–15

  45. Kawashima T, Murakami K, Nishimura I, Nakano T, Obata A (2012) A sulfated polysaccharide, fucoidan, enhances the immunomodulatory effects of lactic acid bacteria. Int J Mol Med 29:447–453. https://doi.org/10.3892/ijmm.2011.854

    Article  CAS  PubMed  Google Scholar 

  46. Mazepa E, Noseda MD, Ferreira LG, DeCarvalho MM, Gonçalves AG, Ducatti DRB, Bellan DL, Gomes RP, Trindade ES, Franco CRC, Pellizziari FM, Winnischafer SMB, Duarte MER (2021) Chemical structure of native and modified sulfated heterorhamnans from the green seaweed Gayralia brasiliensis and their cytotoxic effect on U87MG human glioma cells. Int J Biol Macromol 187:710–721. https://doi.org/10.1016/j.ijbiomac.2021.07.145

    Article  CAS  PubMed  Google Scholar 

  47. Castro MO, Pomin VH, Santos LL, Vilela-Silva AC, Hirohashi N, Pol-Fachin L, Verli H, Mourão PAS (2009) A unique 2-Sulfated β-Galactan from the egg jelly of the sea urchin glyptocidaris crenularis: conformation flexibility versus induction of the sperm acrosome reaction. J Biol Chem 284:18790–18800. https://doi.org/10.1074/jbc.M109.005702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Vilela-Silva AC, Castro MO, Valente AP, Biermann CH, Mourão PAS (2002) Sulfated fucans from the egg jellies of the closely related sea urchins Strongylocentrotus droebachiensis and Strongylocentrotus pallidus ensure species-specific fertilization. J Biol Chem 277:379–387. https://doi.org/10.1074/jbc.M108496200

    Article  CAS  PubMed  Google Scholar 

  49. Maurya AK, Sharma P, Samanta P, Shami AA, Misra SK, Zhang F, Thara R, Kumar D, Shi D, Linhardt RJ, Sharp JS, Doerksen RJ, Tandon R, Pomin VH (2023) Structure, Anti-SARS-CoV-2, and Anticoagulant effects of two Sulfated Galactans from the Red Alga Botryocladia occidentalis. Int J Biol Macromol 238:124168. https://doi.org/10.1016/j.ijbiomac.2023.124168

    Article  CAS  PubMed  Google Scholar 

  50. Alves AP, Mulloy B, Diniz JA, Moura PA (1997) Sulfated Polysaccharides from the Egg Jelly Layer are species-specific inducers of Acrosomal Reaction in Sperms of Sea urchins. Am J Biochem Mol Biol 272:6965–6971. https://doi.org/10.1074/jbc.272.11.6965

    Article  CAS  Google Scholar 

  51. Qi J, Kim SM (2018) Effects of the molecular weight and protein and sulfate content of Chlorella ellipsoidea polysaccharides on their immunomodulatory activity. Int J Biol Macromol 107:70–77. https://doi.org/10.1016/j.ijbiomac.2017.08.144

    Article  CAS  PubMed  Google Scholar 

  52. Chen J, Zhou S, Wang Z, Liu S, Li R, Jia X, Chen J, Liu X, Song B, Zhong S (2022) Anticoagulant and anti-inflammatory effects of a degraded sulfate glycosaminoglycan from swimming bladder. Food Res Int 157:111444. https://doi.org/10.1016/j.foodres.2022.111444

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Laboratoire des Interfaces et des Matériaux Avancés (LIMA), Faculté des Science de Monastir, Université de Monastir, 5000, Monastir, Tunisie

    Asma Msehli, Yosra Ben Salem, Mariem Itaimi Dammak & Hatem Majdoub

  2. Unité de Recherche Analyses et Procédés Appliqués à l’Environnement UR17ES32-Institut Supérieur des Sciences Appliquées et de Technologie de Mahdia, Université de Monastir, 5111, Monastir, Mahdia, Tunisia

    Hedi Ben Mansour

  3. Laboratoire Polymères Biopolymères Surfaces (PBS), UMR 6270 & FR3038CNRS, Université de Rouen, 76821, Mon Saint Aignan, France

    Christophe Rihouey & Didier Le Cerf

  4. Laboratoire de Développement Chimique, Galénique et Pharmacologique des Médicaments, Faculté de Pharmacie de Monastir, Université de Monastir, 5000, Monastir, Tunisia

    Abderrahman Bouraoui

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  1. Asma Msehli
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Msehli, A., Salem, Y.B., Dammak, M.I. et al. Effect of Desulfation of Polysaccharides from Sea Urchin Eggs Paracentrotus Lividus on Antiproliferative Activity. Chemistry Africa (2024). https://doi.org/10.1007/s42250-024-00968-5

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