Skip to main content
SpringerLink
Log in

Marine-sulfated polysaccharides extract of Ulva armoricana green algae exhibits an antimicrobial activity and stimulates cytokine expression by intestinal epithelial cells

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

An aqueous marine-sulfated polysaccharide (MSP) extract, prepared from the green macroalga Ulva armoricana, was tested as an antibacterial compound against 42 bacterial strains and isolates found in livestock animals. Both Gram-positive and Gram-negative bacteria growths were affected. The most susceptible pathogens were Pasteurella multocida, Mannheimia haemolytica, Erysipelothrix rhusiopathiae, Staphylococcus aureus, and Streptococcus suis, with a minimum inhibitory concentration (MIC) ranging from 0.16 to 6.25 mg mL−1. Enterococcus cecorum, Streptococcus dysgalactiae, Corynebacterium, Trueperella pyogenes, and Bordetella bronchiseptica strains were also susceptive to MSP with a complete inhibition recorded at MIC values of 25 and 50 mg mL−1. The stimulation of the immune response mediators of the host’s gut with the extract was evaluated using an in vitro system of differentiated porcine intestinal epithelial cells (IPEC-1). RT-qPCR analysis showed a significant increase of mRNA expression of cytokines such as IL1α, IL1β, L6, IL8, TNFα, and TGFβ as well as the chemokine CCL20. The extract also significantly induced the expression of PPARγ, a ligand-activated transcription factor, and TLR2 receptor.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abd El-Baky HH, Hussein MM, El-Baroty GS (2008) Algal extracts improve antioxidant defense abilities and salt tolerance of wheat plant irrigated with sea water. Afr J Biochem Res 2:151–164

    Google Scholar 

  • Aguilar-Briseño JA, Cruz-Suarez LE, Sassi J-F, Ricque-Marie D, Zapata-Benavides P, Mendoza-Gamboa E, Rodríguez-Padilla C, Trejo-Avila LM (2015) Sulphated polysaccharides from Ulva clathrata and Cladosiphon okamuranus seaweeds both inhibit viral attachment/entry and cell-cell fusion, in NDV Infection. Mar Drugs 13:697–712

    Article  PubMed  PubMed Central  Google Scholar 

  • Artis D, Grencis RK (2008) The intestinal epithelium: sensors to effectors in nematode infection. Mucosal Immunol 1:252–64

    Article  CAS  PubMed  Google Scholar 

  • Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489

    Article  CAS  PubMed  Google Scholar 

  • Bruel T, Guibon R, Melo S, Guillen N, Salmon H, Girard-Misguich F, Meurens F (2010) Epithelial induction of porcine suppressor of cytokine signaling 2 (SOCS2) gene expression in response to Entamoeba histolytica. Dev Com Immunol 34:562–571

    Article  CAS  Google Scholar 

  • Chen D, Wu XZ, Wen ZY (2008) Sulphated polysaccharides and immune response: promotor or inhibitor? Panminerva Med 50:177–183

    CAS  PubMed  Google Scholar 

  • Chojnacka K, Saeid A, Witkowska Z, Tuhy L (2012) Biologically active compounds in seaweed extracts—the prospects for the application. Open Conf Proceed J 3(1-M4):20–28

    Article  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Economou V, Gousia P (2015) Agriculture and food animals as a source of antimicrobial-resistant bacteria. Infect Drug Resist 8:49–61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faulkner DJ (2002) Marine natural products. Nat Prod Rep 19:1–48

    CAS  PubMed  Google Scholar 

  • Fedorov SN, Ermakova SP, Zvyagintseva TN, Stonik VA (2013) Anticancer and cancer preventive properties of marine polysaccharides: some results and prospects. Mar Drugs 11:4876–4901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferreira LG, Noseda MD, Goncalves AG, Ducatti DRB, Fujii MT, Duarte MER (2012) Chemical structure of the complex pyruvylated and sulfated agaran from the red seaweed Palisada flagellifera (Ceramiales, Rhodophyta). Carbohydr Res 347:83–94

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Vallina R, Wang H, Zhan R, Berschneider HM, Lee RM, Davidson NO, Black DD (1996) Lipoprotein and apolipoprotein secretion by a newborn piglet intestinal cell line (IPEC-1). Am J Physiol 271:249–259

    Google Scholar 

  • Hellio C, Bremer G, Pons AM, Le Gal Y, Bourgougnon N (2000) Inhibition of the development of microorganisms (bacteria and fungi) by extracts of marine algae from Brittany (France). Appl Microb Biotechnol 54:543–549

    Article  CAS  Google Scholar 

  • Hellio C, De La Broise D, Dufosse L, Le Gal Y, Bourgougnon N (2001) Inhibition of marine bacteria by extracts of macroalgae: potential use for environmentally friendly antifouling paints. Mar Environ Res 52:231–247

    Article  CAS  PubMed  Google Scholar 

  • Hellio C, Marechal JP, Veron B, Bremer G, Clare AS, Yves Le Gal Y (2004) Seasonal variation of antifouling activities of marine algae from the Brittany Coast (France). Mar Biotechnol 6:67–82

    Article  CAS  PubMed  Google Scholar 

  • Holdt S, Kraan S (2011) Bioactive compounds in seaweed; functional food applications and legislation. Rev Artic J Appl Phycol 23:543–597

    Article  CAS  Google Scholar 

  • Ito T, Carson WF, Cavassani KA, Connett JM, Kunkel SL (2011) CCR6 as a mediator of immunity in the lung and gut. Exp Cell Res 317:613–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaques LB, Ballieux RE, Dietrich CP, Kavanagh LW (1968) A microelectrophoresis method for heparin. Can J Physiol Pharmacol 46:351–360

    Article  CAS  PubMed  Google Scholar 

  • Jaswir I, Monsur HA (2011) Anti-inflammatory compounds of macro algae origin: a review. J Med Plants Res 5:7146–7154

    CAS  Google Scholar 

  • Jiménez-Escrig A, Gómez-Ordóñez E, Rupérez P (2011) Seaweed as a source of novel nutraceuticals: sulfated polysaccharides and peptides. Adv Food Nutr Res 64:325–37

    Article  PubMed  Google Scholar 

  • Karnjanapratum S, Tabarsa M, MyoungLae C, You S (2012) Characterization and immunomodulatory activities of sulfated polysaccharides from Capsosiphon fulvescens. Int J Biol Macromol 51:720–729

    Article  CAS  PubMed  Google Scholar 

  • Kim JK, Cho ML, Karnjanapratum S, Shin IS, You SG (2011) In vitro and in vivo immunomodulatory activity of sulfated polysaccharides from Enteromorpha prolifera. Int J Biol Macromol 49:1051–1058

    Article  CAS  PubMed  Google Scholar 

  • Lahaye M, Robic A (2007) Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8:1765–1774

    Article  CAS  PubMed  Google Scholar 

  • Laurienzo P (2010) Marine polysaccharides in pharmaceutical applications: an overview. Mar Drugs 8:2435–2465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JC, Hou MF, Huang HW, Chang FR, Yeh CC, Tang JY, Chang HW (2013) Marine algal natural products with anti-oxidative, anti-inflammatory, and anti-cancer properties. Cancer Cell Int 13:55. doi:10.1186/1475-2867-13-55

    Article  PubMed  PubMed Central  Google Scholar 

  • Leiro JM, Castro R, Arranz JA, Lamas J (2007) Immunomodulating activities of acidic sulphated polysaccharides obtained from the seaweed Ulva rigida C. Agardh. Int Immunopharmacol 7:879–888

    Article  CAS  PubMed  Google Scholar 

  • Leppkes M, Roulis M, Neurath MF, Kollias G, Becker C (2014) Pleiotropic functions of TNF-α in the regulation of the intestinal epithelial response to inflammation. Int Immunol 26:509–15

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2-∆∆Ct method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Meurens F, Berri M, Siggers RH, Willing BP, Salmon H, Van Kessel AG, Gerdts V (2007) Commensal bacteria and expression of two major intestinal chemokines, TECK/CCL25 and MEC/CCL28, and their receptors. PLoS ONE 2:e677

    Article  PubMed  PubMed Central  Google Scholar 

  • Miron N, Cristea V (2012) Enterocytes: active cells in tolerance to food and microbial antigens in the gut. Clin Exp Immunol 167:405–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montreuil, J., Bouquelet, S., Debray, H., Fournet, B., Spik, G. and Strecker, G. (1986) Glycoproteins. In carbohydrate analysis: a practical approach. Chaplin MF and Kennedy JF (eds). New York Oxford University Press, pp143–204

  • Na WJ, Kim SM, Kim JW, Park SM, Lee SO, Kim SS, Synytsya A, Park Y (2010) Purification, characterization and immunostimulating activity of water-soluble polysaccharide isolated from Capsosiphon fulvescens. Int Immunopharmacol 10:364–370

    Article  CAS  PubMed  Google Scholar 

  • Ngoa DH, Wijesekara I, Voa TS, Ta QV, Kim SK (2011) Marine food-derived functional ingredients as potential antioxidants in the food industry: an overview. Food Res Int 44:523–529

    Article  Google Scholar 

  • Orhan I, Sener B, Brun R, Perozzo R, Tasdemir D (2006) Turkish freshwater and marine macrophyte extracts show in vitro antiprotozoal activity and inhibit FabI, a key enzyme of Plasmodium falciparum fatty acid biosynthesis. Phytomedicine 13:388–393

    Article  CAS  PubMed  Google Scholar 

  • O’Sullivan L, Murphy B, McLoughlin P, Duggan P, Lawlor PG, Hughes H, Gardiner GE (2010) Prebiotics from marine macroalgae for human and animal health applications. Mar Drugs 8:2038–2064

    Article  PubMed  PubMed Central  Google Scholar 

  • Oswald IP (2006) Role of intestinal epithelial cells in the innate immune defense of the pig intestine. Vet Res 37:359–68

    Article  CAS  PubMed  Google Scholar 

  • Peterson LW, Artis D (2014) Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 14:141–153

    Article  CAS  PubMed  Google Scholar 

  • Qi H, Huang L, Liu X, Liu D, Zhang Q, Liu S (2011) Antihyperlipidemic activity of high sulfate content derivative of polysaccharide extracted from Ulva pertusa (Chlorophyta). Carbohydr Polym 87:1637–1640

    Article  Google Scholar 

  • Raposo MFJ, Morais RMSC, Morais AMMB (2013) Health applications of bioactive compounds from marine microalgae. Life Sci 93:479–486

    Article  CAS  Google Scholar 

  • Rioux LE, Turgeon SL, Beaulieu M (2007) Characterization of polysaccharides extracted from brown seaweeds. Carbohydr Polym 69:530–537

    Article  CAS  Google Scholar 

  • Silva TH, Alves A, Pop EG, Reys LL, Gomes ME, Sousa RA, Silva SS, Mano JF, Reis RL (2012) Marine algae sulfated polysaccharides for tissue engineering and drug delivery approaches. Biomatter 2:278–289

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Article  CAS  PubMed  Google Scholar 

  • Spavieri J, Kaiser M, Casey R, Hingley-Wilson S, Lalvani A, Blunden G, Tasdemir D (2010) Antiprotozoal, antimycobacterial and cytotoxic potential of some British green algae. Phytother Res 24:1095–1098

    Article  PubMed  Google Scholar 

  • Stadnyk AW (2002) Intestinal epithelial cells as a source of inflammatory cytokines and chemokines. Can J Gastroenterol 16:241–246

    Article  PubMed  Google Scholar 

  • Stavnezer J, Kang J (2009) The surprising discovery that TGF specifically induces the IgA class switch. J Immunol 182:5–7

    Article  CAS  PubMed  Google Scholar 

  • Tabarsa M, Rezaei M, Ramezanpour Z, Waaland JR (2012) Chemical compositions of the marine algae Gracilaria salicornia (Rhodophyta) and Ulva lactuca (Chlorophyta) as a potential food source. J Sci Food Agric 92:2500–2506

    Article  CAS  PubMed  Google Scholar 

  • Takenoshita S, Fukushima T, Kumamoto K, Iwadate M (2002) The role of TGF-β in digestive organ disease. J Gastroenterol 37:991–999

    Article  CAS  PubMed  Google Scholar 

  • Tyagi S, Gupta P, Saini AS, Kaushal C, Sharma S (2011) The peroxisome proliferator-activated receptor: a family of nuclear receptors role in various diseases. J Adv Pharm Technol Res 2:236–40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vo TS, Ngo D, Kim SK (2012) Potential targets for anti inflammatory and anti-allergic activities of marine algae: an overview inflammation and allergy. Drug Targets 11:90–101

    CAS  PubMed  Google Scholar 

  • Walia B, Wang L, Merlin D, Sitaraman SV (2003) TGF-β down-regulates IL-6 signaling in intestinal epithelial cells: critical role of SMAD-2. FASEB 17:2130–2132

    CAS  Google Scholar 

  • Wijesekara I, Pangestuti R, Kima SK (2011) Biological activities and potential health benefits of sulfated polysaccharides derived from marine algae. Carbohydr Polym 84:14–21

    Article  CAS  Google Scholar 

  • Wijesinghe WAJP, Jeon YJ (2011) Biological activities and potential cosmeceutical applications of bioactive components from brown seaweeds: a review. Phytochem Rev 10:431–443

    Article  CAS  Google Scholar 

  • Williams IR (2006) CCR6 and CCL20: partners in intestinal immunity and lymphorganogenesis. Ann N Y Acad Sci 1072:52–61

    Article  CAS  PubMed  Google Scholar 

  • Zanello G, Berri M, Dupont J, Sizaret PY, D'Inca R, Salmon H, Meurens F (2011) Saccharomyces cerevisiae modulates immune gene expressions and inhibits ETEC-mediated ERK1/2 and p38 signaling pathways in intestinal epithelial cells. PLoS One 6(4), e18573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zubia M, Fabre MS, Kerjean V, Deslandes E (2009) Antioxidant and cytotoxic activities of some red algae (Rhodophyta) from Brittany coasts (France). Bot Mar 52:268–277

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Dr. Nathalie Guriec, CHU de Brest, for her constructive comments on the article. We also thank Claire Boisset (chromatography platform, CERMAV, Grenoble, France) and Marie-Francoise Bricot (Service de Microanalyse, Institut de Chimie des Substances Naturelles, CNRS UPR2301, Gif-sur-Yvette cedex France) for elementary analyses. This work was made possible by the support granted by Banque Publique d’Investissement (BPI, France) to the company Amadeite, Bréhan (France), via the ISI ULVANS project.

Author information

Authors and Affiliations

  1. INRA, UMR 1282 Infectiologie et Santé Publique, 37380, Nouzilly, France

    Mustapha Berri, Cindy Slugocki, Michel Olivier, Emmanuelle Helloin, Isabelle Jacques & Henri Salmon

  2. UMR 1282 Infectiologie et Santé Publique, Université de Tours, 37000, Tours, France

    Mustapha Berri, Cindy Slugocki, Michel Olivier, Emmanuelle Helloin, Isabelle Jacques & Henri Salmon

  3. Biovet Conseil, 1 Route du Linès, 56700, Merlevenez, France

    Hervé Demais

  4. Amadéite SAS “Pôle biotechnologique” du Haut du Bois, 56580, Bréhan, France

    Matthieu Le Goff & Pi Nyvall Collen

Authors
  1. Mustapha Berri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cindy Slugocki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michel Olivier
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Emmanuelle Helloin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Isabelle Jacques
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Henri Salmon
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hervé Demais
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Matthieu Le Goff
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Pi Nyvall Collen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mustapha Berri.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Berri, M., Slugocki, C., Olivier, M. et al. Marine-sulfated polysaccharides extract of Ulva armoricana green algae exhibits an antimicrobial activity and stimulates cytokine expression by intestinal epithelial cells. J Appl Phycol 28, 2999–3008 (2016). https://doi.org/10.1007/s10811-016-0822-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-016-0822-7

Keywords

Search

Navigation