Abstract
Endotoxemia is mainly caused by translocation of bacterial lipopolysaccharides (LPS) into the bloodstream. This in turn enhances systemic inflammation and inappropriate production of reactive oxygen species, leading to oxidative injury of vital internal organs and other dangerous effects that can be life-threatening. Here, we evaluated/compared the modulatory effects of consuming two different doses (2% and 4% of the diet) of brown seaweeds (Sargassum latifolium) for 40 consecutive days on thermo-respiratory response, inflammation, and oxidative stress in Barki male sheep (Ovis aries) challenged twice with bacterial LPS (1.25 μg/kg body weight, injected intravenously on days 28 and 35 of the experimental period). The results showed that the diet containing Sargassum latifolium (especially at 4%) modulated significantly (P < 0.05–0.001) the increase in the thermo-respiratory response (skin and rectal temperatures, and respiration rate) and the obtained systemic inflammation (blood leukocytosis, the elevation in the erythrocyte sedimentation rate, and the increase in serum proinflammatory cytokines and heat shock protein-70 concentrations) in the LPS-challenged sheep. In addition, it improved significantly (P < 0.001, especially at 4%) the total antioxidant capacity of the blood of LPS-challenged sheep by increasing the catalase and superoxide dismutase activities. Moreover, it decreased the blood markers of tissue damage (malondialdehyde concentration and the activities of alanine aminotransferase and lactate dehydrogenase) in the LPS-challenged sheep. In conclusion, the diet containing 4% Sargassum latifolium may have potential impact in protecting the ruminant livestock from the serious effects of endotoxemia through improving the animals’ antioxidant defense system and regulating their inflammatory and thermo-respiratory responses.
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Abbreviations
- ALAT:
-
Alanine aminotransferase
- CAT:
-
Catalase
- CD14:
-
Cluster of differentiation number 14
- COX-2:
-
Cyclooxygenase-2
- ESR:
-
Erythrocyte sedimentation rate
- HSP:
-
Heat shock protein
- Ig:
-
Immunoglobulin
- IκB:
-
Nuclear factor of kappa light polypeptide gene enhancer in B-cells inhibitor
- IL:
-
Interleukin
- LDH:
-
Lactate dehydrogenase
- LPO:
-
Lipid peroxidation
- LPS:
-
Lipopolysaccharides
- MDA:
-
Malondialdehyde;
- NADPH:
-
The reduced form of nicotinamide adenine dinucleotide phosphate
- NF-κB:
-
Nuclear factor kappa-light-chain-enhancer of activated B-cells
- PG:
-
Prostaglandin
- ROS:
-
Reactive oxygen species
- RR:
-
Respiration rate
- RT:
-
Rectal temperature
- SOD:
-
Superoxide dismutase
- ST:
-
Skin temperature
- TAC:
-
Total antioxidant capacity
- TLR:
-
Toll-like receptor
- TNF:
-
Tumor necrosis factor
References
Ayala A, Munoz MF, Arguelles S (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Med Cell Longev 2014:360438–360431. https://doi.org/10.1155/2014/360438
Blatteis CM, Li S, Li Z, Feleder C, Perlik V (2005) Cytokines, PGE2 and endotoxic fever: a re-assessment. Prostaglandins Other Lipid Mediat 76:1–18. https://doi.org/10.1016/j.prostaglandins.2005.01.001
Calderwood SK, Gong J, Murshid A (2016) Extracellular HSPs: the complicated roles of extracellular HSPs in immunity. Front Immunol 7:159. https://doi.org/10.3389/fimmu.2016.00159
Dore CM, das Faustino Alves MGC, Will LS, Costa TG, Sabry DA, de Souza Rego LA, Accardo CM, Rocha HA, Filgueira LG, Leite EL (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
El Shora HM, Abou El Wafa GS, Abu Eftouh NM (2018) Fucoidan and fucoidanase from brown seaweeds and applications. Int J Curr Microbiol App Sci 7:3707–3715. https://doi.org/10.20546/ijcmas.2018.702.440
Evans SS, Repasky EA, Fisher DT (2015) Fever and the thermal regulation of immunity: the immune system feels the heat. Nat Rev Immunol 15:335–349. https://doi.org/10.1038/nri3843
Fawzy MA, Gomaa M, Hifney AF, Abdel-Gawad KM (2017) Optimization of alginate alkaline extraction technology from Sargassum latifolium and its potential antioxidant and emulsifying properties. Carbohydr Polym 157:1903–1912. https://doi.org/10.1016/j.carbpol.2016.11.077
Fouda WA, Ibrahim WM, Ellamie AM, Ramadan G (2019) Biochemical and mineral compositions of six brown seaweeds collected from Red Sea at Hurghada Coast. Indian J Geo Marine Sci 48:484–491
Guo S, Al-Sadi R, Said HM, Ma TY (2013) Lipopolysaccharide causes an increase in intestinal tight junction permeability in vitro and in vivo by inducing enterocyte membrane expression and localization of TLR-4 and CD14. Am J Pathol 182:375–387. https://doi.org/10.1016/j.ajpath.2012.10.014
Han RM, Zhang JP, Skibsted LH (2012) Reaction dynamics of flavonoids and carotenoids as antioxidants. Molecules 17:2140–2160. https://doi.org/10.3390/molecules17022140
Hasegawa S, Ichiyama T, Sonaka I, Ohsaki A, Okada S, Wakiguchi H, Kudo K, Kittaka S, Hara M, Furukawa S (2012) Cysteine, histidine and glycine exhibit anti-inflammatory effects in human coronary arterial endothelial cells. Clin Exp Immunol 167:269–274. https://doi.org/10.1111/j.1365-2249.2011.04519.x
Hira K, Sultana V, Khatoon N, Ara J, Ehteshamul-Haque S (2019) Protective effect of crude sulphated polysaccharides from Sargassum Swartzii (Turn.) C.Ag. against acetaminophen induced liver toxicity in rats. Clin Phytosci 5:14. https://doi.org/10.1186/s40816-019-0108-0
Hwang PA, Chien SY, Chan YL, Lu MK, Wu CH, Kong ZL, Wu CJ (2011) Inhibition of lipopolysaccharide (LPS)-induced inflammatory responses by Sargassum hemiphyllum sulfated polysaccharide extract in RAW 264.7 macrophage cells. J Agric Food Chem 59:2062–2068. https://doi.org/10.1021/jf1043647
Jaffer U, Wade RG, Gourlay T (2010) Cytokines in the systemic inflammatory response syndrome: a review. HSR Proc Intensive Care Cardiovasc Anesth 2:161–175
Jiang F, Zhang Y, Dusting GJ (2011) NADPH oxidase-mediated redox signaling: roles in cellular stress response, stress tolerance, and tissue repair. Pharmacol Rev 63:218–242. https://doi.org/10.1124/pr.110.002980
Jiao G, Yu G, Zhang J, Ewart HS (2011) Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Mar Drugs 9:196–223. https://doi.org/10.3390/md9020196
Kadam SU, O’Donnell CP, Rai DK, Hossain MB, Burgess CM, Walsh D, Tiwari BK (2015) Laminarin from Irish brown seaweeds Ascophyllum nodosum and Laminaria hyperborea: ultrasound assisted extraction, characterization and bioactivity. Mar Drugs 13:4270–4280. https://doi.org/10.3390/md13074270
Kang JY, Khan MN, Park NH, Cho JY, Lee MC, Fujii H, Hong YK (2008) Antipyretic, analgesic, and anti-inflammatory activities of the seaweed Sargassum fulvellum and Sargassum thunbergii in mice. J Ethnopharmacol 116:187–190. https://doi.org/10.1016/j.jep.2007.10.032
Kell DB, Pretorius E (2015) On the translocation of bacteria and their lipopolysaccharides between blood and peripheral locations in chronic, inflammatory diseases: the central roles of LPS and LPS-induced cell death. Integr Biol (Camb) 7:1339–1377. https://doi.org/10.1039/c5ib00158g
Khan HA, Alhomida AS, Sobki SH, Habib SS, Al Aseri Z, Khan AA, Al Moghairi A (2013) Serum markers of tissue damage and oxidative stress in patients with acute myocardial infarction. Biomed Res 24:15–20
Kim JA, Kong CS, Kim SK (2010) Effect of Sargassum thunbergii on ROS mediated oxidative damage and identification of polyunsaturated fatty acid components. Food Chem Toxicol 48:1243–1249. https://doi.org/10.1016/j.fct.2010.02.017
Kurutas EB (2016) The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: current state. Nutr J 15:71. https://doi.org/10.1186/s12937-016-0186-5
Lee CT, Repasky EA (2012) Opposing roles for heat and heat shock proteins in macrophage functions during inflammation: a function of cell activation state? Front Immunol 3:140. https://doi.org/10.3389/fimmu.2012.00140
Li Y, Fu X, Duan D, Liu X, Xu J, Gao X (2017) Extraction and identification of phlorotannins from the brown alga, Sargassum fusiforme (Harvey) Setchell. Mar Drugs 15. https://doi.org/10.3390/md15020049
Lopez-Posadas R, Ballester I, Mascaraque C, Suarez MD, Zarzuelo A, Martinez-Augustin O, Sanchez de Medina F (2010) Flavonoids exert distinct modulatory actions on cyclooxygenase 2 and NF-kappaB in an intestinal epithelial cell line (IEC18). Br J Pharmacol 160:1714–1726. https://doi.org/10.1111/j.1476-5381.2010.00827.x
Mahat MY, Kulkarni NM, Vishwakarma SL, Khan FR, Thippeswamy BS, Hebballi V, Adhyapak AA, Benade VS, Ashfaque SM, Tubachi S, Patil BM (2010) Modulation of the cyclooxygenase pathway via inhibition of nitric oxide production contributes to the anti-inflammatory activity of kaempferol. Eur J Pharmacol 642:169–176. https://doi.org/10.1016/j.ejphar.2010.05.062
Makkar HPS, Tran G, Heuzé V, Giger-Reverdin S, Lessiree M, Lebas F, Ankers P (2016) Seaweeds for livestock diets: a review. Anim Feed Sci Technol 212:1–17. https://doi.org/10.1016/j.anifeedsci.2015.09.018
Meena B, Anbin Ezhilan R, Rajesh R, Sheik Hussain A, Ganesan B, Anandan R (2008) Antihepatotoxic potential of Sargassum polycystum (Phaeophyceae) on antioxidant defense status in D-galactosamine-induced hepatitis in rats. Afr J Biochem Res 2:051–055
Park HS, Jung HY, Park EY, Kim J, Lee WJ, Bae YS (2004) Cutting edge: direct interaction of TLR4 with NAD(P)H oxidase 4 isozyme is essential for lipopolysaccharide-induced production of reactive oxygen species and activation of NF-kappa B. J Immunol 173:3589–3593. https://doi.org/10.4049/jimmunol.173.6.3589
Quintal-Novelo C, Rangel-Mendez J, Ortiz-Tello A, Graniel-Sabido M, Perez-Cabeza de Vaca R, Moo-Puc R (2018) A Sargassum fluitans Borgesen ethanol extract exhibits a hepatoprotective effect in vivo in acute and chronic liver damage models. Biomed Res Int 2018:6921845–6921849. https://doi.org/10.1155/2018/6921845
Raghavendran HR, Sathivel A, Devaki T (2005) Protective effect of Sargassum polycystum (brown alga) against acetaminophen-induced lipid peroxidation in rats. Phytother Res 19:113–115. https://doi.org/10.1002/ptr.1552
Ricciotti E, FitzGerald GA (2011) Prostaglandins and inflammation. Arterioscler Thromb Vasc Biol 31:986–1000. https://doi.org/10.1161/ATVBAHA.110.207449
Rodrigues E, Mariutti LR, Chiste RC, Mercadante AZ (2012) Development of a novel micro-assay for evaluation of peroxyl radical scavenger capacity: application to carotenoids and structure-activity relationship. Food Chem 135:2103–2111. https://doi.org/10.1016/j.foodchem.2012.06.074
Salvesen O, Reiten MR, Heegaard PM, Tranulis MA, Espenes A, Skovgaard K, Ersdal C (2016) Activation of innate immune genes in caprine blood leukocytes after systemic endotoxin challenge. BMC Vet Res 12:241. https://doi.org/10.1186/s12917-016-0870-x
Sanjeewa KKA, Fernando IPS, Kim SY, Kim HS, Ahn G, Jee Y, Jeon YJ (2018) In vitro and in vivo anti-inflammatory activities of high molecular weight sulfated polysaccharide; containing fucose separated from Sargassum horneri: short communication. Int J Biol Macromol 107:803–807. https://doi.org/10.1016/j.ijbiomac.2017.09.050
Sujatha M, Suganya P, Pradeepa V (2017) Antioxidant and anticancerous activities of fucoxanthin isolated from brown seaweed Sargassum wightii against HepG2 cell lines. IJIRSET 6:16734–16742
Turner JR, Thayer J (2001) Introduction to analysis of variance: design, analysis & interpretation. SAGE, Thousand Oaks
van Lier D, Geven C, Leijte GP, Pickkers P (2019) Experimental human endotoxemia as a model of systemic inflammation. Biochimie 159:99–106. https://doi.org/10.1016/j.biochi.2018.06.014
Wang C-H, Chou P-C, Chung F-T, Lin H-C, Huang K-H, Kuo H-P (2017) Heat shock protein70 is implicated in modulating NF-κB activation in alveolar macrophages of patients with active pulmonary tuberculosis. Sci Rep 7. https://doi.org/10.1038/s41598-017-01405-z
Wang L, Hou Y, Yi D, Li Y, Ding B, Zhu H, Liu J, Xiao H, Wu G (2015) Dietary supplementation with glutamate precursor alpha-ketoglutarate attenuates lipopolysaccharide-induced liver injury in young pigs. Amino Acids 47:1309–1318. https://doi.org/10.1007/s00726-015-1966-5
Wen ZS, Liu LJ, OuYang XK, Qu YL, Chen Y, Ding GF (2014) Protective effect of polysaccharides from Sargassum horneri against oxidative stress in RAW264.7 cells. Int J Biol Macromol 68:98–106. https://doi.org/10.1016/j.ijbiomac.2014.04.037
Wen ZS, Xiang XW, Jin HX, Guo XY, Liu LJ, Huang YN, OuYang XK, Qu YL (2016) Composition and anti-inflammatory effect of polysaccharides from Sargassum horneri in RAW264.7 macrophages. Int J Biol Macromol 88:403–413. https://doi.org/10.1016/j.ijbiomac.2016.02.025
Yang EJ, Ham YM, Lee WJ, Lee NH, Hyun CG (2013) Anti-inflammatory effects of apo-9′-fucoxanthinone from the brown alga, Sargassum muticum. Daru 21:62. https://doi.org/10.1186/2008-2231-21-62
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G. R. and A. M. E. planned the study, designed all experiments, and summarized, discussed, and interpreted the results. W. A. F. and W. M. I. collected, identified, and characterized the brown seaweeds. W. A. F. carried out the experiments, performed the statistical analysis, and drafted the manuscript with assistance from G. R and A. M. E.
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The animals were housed in suitable yards under veterinary care according to the program of the Ministry of Agriculture; and the study design was carried out in accordance with the EC Directive 86/609/EEC guidelines for the animal experiments and approved by the Research Ethics Committee at Faculty of Science, Ain Shams University (6/2014), prior to the commencement of the study.
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Patent registration number: 1716/2019 (Patent Office, Academy of Scientific Research and Technology, Ministry of Scientific Research, Cairo, Egypt); inventors (authors): Wafaa A. Fouda, Gamal Ramadan, Ashgan M. Ellamie and Wael M. Ibrahim. The authors have no other potential financial conflict of interest
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Ramadan, G., Fouda, W.A., Ellamie, A.M. et al. Dietary supplementation of Sargassum latifolium modulates thermo-respiratory response, inflammation, and oxidative stress in bacterial endotoxin-challenged male Barki sheep. Environ Sci Pollut Res 27, 33863–33871 (2020). https://doi.org/10.1007/s11356-020-09568-5
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DOI: https://doi.org/10.1007/s11356-020-09568-5