Top

Published in:

01-08-2020 | Original Article

Marine sponges Sarcotragus foetidus, Xestospongia carbonaria and Spongia obscura constituents ameliorate IL-1 β and IL-6 in lipopolysaccharide-induced RAW 264.7 macrophages and carrageenan-induced oedema in rats

Authors: Sayli Chaudhari, Maushmi S. Kumar

Published in: Inflammopharmacology | Issue 4/2020

Abstract

Marine sponges are prolific producers of an array of diverse chemical structures containing compounds with multiple biological activities. In this study, whole methanol extracts and fractionated compounds from three marine sponges namely Xestospongia carbonaria, Sarcotragus foetidus and Spongia obscura were thoroughly investigated for their antibacterial, antifungal, antioxidant and anti-inflammatory activities. Methanol extracts and fractionated compounds were characterised using high performance liquid chromatography–mass spectrometry and gas chromatography–mass spectrometry. Extracts were checked for cytotoxicity in RAW macrophages by MTT assay, before using them for the treatment study. Enzyme linked immunosorbent assay kits were used to check the effects on inflammatory mediator’s levels (PGE₂, COX-2, IL-6, IL-1β, TNF-α) in vitro. The results demonstrated good anti-inflammatory activity of all the three marine sponges; X. carbonaria, S. foetidus and S. obscura suppressed the levels of anti-inflammatory cytokines in vitro. Reverse transcriptase-polymerase chain reaction confirmed the inhibition of IL-1β and IL-6 genes expression by the isolates of X. carbonaria and S. foetidus, while reducing cytokine levels in lipopolysaccharide-induced inflammation in vitro as well as in carrageenan-induced inflammation in rats. Two semi pure compounds isolated from X. carbonaria and S. foetidus also confirmed suppression of IL-1β and IL-6 genes expression in RAW macrophages.

Graphic abstract

Ali K, Iqbal M, Yuliana ND, Lee Y-J, Park S, Han S, Lee J-W, Lee H-S, Verpoorte R, Choi YH (2013) Identification of bioactive metabolites against adenosine A1 receptor using NMR-based metabolomics. Metabolomics 9:778–785

Alvi KA, Rodriguez J, Diaz MC, Moretti R, Wilhelm RS, Lee RH, Slate DL, Crews P (1993) Protein tyrosine kinase inhibitory properties of planar polycyclics obtained from the marine sponge Xestospongiacf. carbonaria and from total synthesis. J Org Chem 58(18):4871–4880

Andriani Y, Marlina L, Mahamad H, Amir H, Radzi SAM, Saidin J (2017) Anti-inflammatory activity of Bacteria associated with marine sponges (Haliclona amboinensis) via reducing NO production and inhibiting cyclooxygenase-1, cyclooxygenase-2, and secretory Phospholipase A2 activities. Asian J Pharm Clin Res 10(11):95–100

Ankisetty S, Gochfeld DJ, Díaz MC, Khan SI, Slattery M (2010) Chemical constituents of the deep reef Caribbean sponges Plakortis angulospiculatus and Plakortis halichondrioides and their anti-inflammatory activities. J Nat Prod 73(9):1494–1498. https://doi.org/10.1021/np100233d CrossRefPubMed

Ankisetty S, Slattery M (2012) Antibacterial secondary metabolites from the Cave sponge Xestospongia sp. Mar Drugs 10(5):1037–1043PubMedPubMedCentral

Aspirin (2019) Aspirin Side Effects Centre, Rx List. https://www.rxlist.com/aspirin-side-effects-drug-center.htm

Athira Krishnan KA, Keerthi TF (2016) Analyses of methanol extracts of two marine sponges, Spongia officinalis var. ceylonensis and Sigmadocia carnosa from Southwest coast of India for their bioactivities. Int J Curr Microbio App Sci 5(2):722–734

Azevedo LG, Persia GG, Lerner C, Soares A, Murcia N, Muccillo-Baisch AL (2008) Investigation of the anti-inflammatory and analgesic effects from an extract of Aplysina caissara, a marine sponge. Fund Clin Pharmacol 22(5):549–556. https://doi.org/10.1111/j.1472-8206.2008.00624.x CrossRef

Barthel D, Gutt J, Tendal OS (1991) New information on the biology of Antarctic deep-water sponges derived from underwater photography. Mar Ecol Prog Ser 69:303–307

Basic Principles of RT-qPCR (2019) ThermoFischer Scientific. https://www.thermofisher.com/in/en/home/brands/thermo-scientific/molecular-biology/molecular-biology-learning-center/molecular-biology-resource-library/spotlight-articles/basic-principles-rt-qpcr.html

Bauvais C, Bonneau N, Blond A, Pérez T, Bourguet-Kondracki ML, Zirah S (2017) Furanoterpene diversity and variability in the metal polluted sponge Spongia officinalis, from untargeted LC-MS/MS metabolic profiling to furano lactam derivatives. Metabolites 7(2):27PubMedCentral

Bell JJ (2007) Contrasting patterns of species and functional composition for coral reef sponge assemblages. Mar Ecol Prog Ser 339:73–81

Cheenpracha S, Park EJ, Rostama B, Pezzuto JM, Chang LC (2010) Inhibition of nitric oxide (NO) production in lipopolysaccharide (LPS)-activated murine macrophage RAW 264.7 cells by the norsesterterpene peroxide Epimuqubilin A. Mar Drugs 8(3):429–437. https://doi.org/10.3390/md8030429 CrossRefPubMedPubMedCentral

Costantino V, Fattorusso E, Mangoni A, Perinu C, Cirino G, de Gruttola L, Roviezzo F (2009) Tedanol: a potent anti-inflammatory ent-pimarane diterpene from the Caribbean Sponge Tedania ignis. Bioorg Med Chem 17(21):7542–7547. https://doi.org/10.1016/j.bmc.2009.09.010 CrossRefPubMed

Dayton PK, Robilliard GA, Paine RT, Dayton LB (1974) Biological accommodation in the benthic community at McMurdo sound, Antarctica. Ecol Monogr 44:105–128

De Almeida LP, Carroll AR, Towerzet L, King G et al (2018) Exiguaquinol: a novel pentacyclic hydroquinone from Neopetrosia exigua that exhibits Helicobacter pyroli. Murl Org Lett 10(12):2585–2588

Dellai A, Deghrigue M, Laroche-Clary A, Masour HB, Chouchane N, Robert J et al (2012) Evaluation of antiproliferative and anti-inflammatory activities of methanol extract and its fractions from the Mediterranean sponge. Cancer Cell Int 12:18PubMedPubMedCentral

Dellai A, Laroche-Clary A, Mhadhebi L, Robert J, Bouraoui A (2010) Anti-inflammatory and antiproliferative activities of crude extract and its fractions of the defensive secretion from the Mediterranean sponge Spongia officianlis. Drug Develop Res 71(7):412–418

Diaz MC, Alvarez B, Laughlin RA (1990) The sponge fauna on a fringing coral reef in Venezuela, II: community structure. In: Rutzler K (ed) New perspectives in sponge biology. Smithsonian Institute Press, London, pp 367–375

Ebada SS, Edrada RA, Lin W, Proksch P (2008) Methods for isolation, purification and structural elucidation of bioactive secondary metabolites from marine invertebrates. Nat Protoc 3(12):1820–1831PubMed

El-Shitany NA, Shaala LA, Abbas AT, Abdel-Dayem UA, Azhar EI, Ali SS et al (2015) Evaluation of the anti-inflammatory, antioxidant and immunomodulatory effect of the organic extract of the red sea marine sponge Xestospongia testudinaria against carrageenan induced rat paw inflammation. PLoS ONE 10(9):e0138917PubMedPubMedCentral

Elsayed Y, Refaat J, Abdelmohsen UR, Othman EM, Stopper H, Fouad MA (2018) Metabolomic profiling and biological investigation of the marine sponge-derived bacterium Rhodococcus sp. UA13. Phytochem Anal 29(6):543–548PubMed

Enticknap JJ, Kelly M, Peraud O, Hill RT (2006) Characterization of a culturable alphaproteobacterial symbiont common to many marine sponges and evidence for vertical transmission via sponge larvae. Appl Environ Microbiol 72:3724–3732PubMedPubMedCentral

George SC, Lisk M, Eadington P (2004) Fluid inclusion evidence for an early, marine-sourced oil charge prior to gas-condensate migration, Bayu-1, Timor Sea Australia. Mar Petrol Geol 21(9):1107–1128

Goulitquer S, Potin P, Tonon T (2012) Mass spectrometry-based Metabolomics to elucidate functions in the marine organisms and ecosystems. Mar Drugs 10:849–880PubMedPubMedCentral

Hardoim CCP, Costa R (2014) Microbial communities and bioactive compounds in marine sponges of the Family Irciniidae—a review. Mar Drugs 12(10):5089–5122. https://doi.org/10.3390/md12105089 CrossRefPubMedPubMedCentral

Huang M, Lu JJ, Huang MQ, Bao JL, Chen XP, Wang YT (2012) Terpenoids: natural products for cancer therapy. Expert Opin Investig Drugs 21(12):1801–1818. https://doi.org/10.1517/13543784.2012.727395 CrossRefPubMed

Koehn FE, Carter GT (2005) The evolving role of natural products in drug discovery. Nat Rev Drug Discov 4(3):206–220PubMed

Kosmides AK, Kamisoglu K, Calvano SE, Corbett SA, Androulakis IP (2013) Metabolomic fingerprinting: challenges and opportunities. Crit Rev Biomed Eng 41:205–221PubMedPubMedCentral

Kumar MS, Pal AK (2012) Investigation of bioactivity of extracts of Marine Sponge, Spongosorites halichondrioides (Dendy, 1905) from western coastal areas of India. Asian Pac J Trop Biomed 2(3):S1784–S1789

Kumar MS, Pandita NS, Pal AK (2012) LC-MS/MS as a tool for identification of bioactive compounds in Marine sponge Spongosorites halichondriodes (Dendy 1905). Toxicon 60:1135–1147PubMed

Kumar MS, Vijaylaxmi KK, Pal AK (2014) Anti-inflammatory and antioxidant properties of Spongosorites halichondriodes, a marine sponge. Turk J Pharm Sci 11(3):285–294

Kumar S, Mohite SA, Mohite AS, Salvi PV (2018) Diversity of sponges (Porifera) in coastal waters of South-West coast of Maharashtra, India. Indian Res J Genet Biotech 10(3):363–374

Laport MS, Santos OS, Muricy G (2009) Marine sponges: potential sources of new antimicrobial drugs. Curr Pharm Biotechnol 10:86–105PubMed

Laskin DL, Laskin JD (2001) Role of macrophages and inflammatory mediators in chemically induced toxicity. Toxicology 160(1–3):111–118PubMed

Lee OO, Chui PY, Wong YH, Pawlik JR, Qian PY (2009) Evidence for vertical transmission of bacterial symbionts from adult to embryo in the Caribbean sponge Svenzea zeai. Appl Environ Microbiol 75:6147–6156PubMedPubMedCentral

Liu T, Li J, Liu Y et al (2012) Short-chain fatty acids suppress lipopolysaccharide-induced production of nitric oxide and proinflammatory cytokines through inhibition of NF-kB pathway in RAW 264.7 cells. Inflammation 35(5):1676–1684PubMed

Liu Y, Jung JH, Ji H, Zhang S (2006) Glycerolipids from a Sarcotragus species sponge. Molecules 11(9):714–719PubMedPubMedCentral

Mabhiza D, Chitermerere T, Mukanganyama S (2016) Antibacterial properties of alkaloid extracts from Calkistemon citrinus and Vermont’s adoensis against Staphylococcus aureus and Pseudomonas aeruginosa. Int J Med Chem. https://doi.org/10.1155/2016/6304163 CrossRefPubMedPubMedCentral

Mahajna S, Azab M, Zaid H, Farich BA, Battah FA, Mashner S et al (2015) In vitro evaluations of cytotoxicity and anti-inflammatory effects of Peganum harmala seed extracts inTHP-1 derived macrophages. Eur J Med Plant 5(2):165–175

Mahdi-Pour B, Jothy SL, Latha LY, Chen Y, Sasidharan S (2012) Antioxidant activity of methanol extracts of different parts of Lantana camara. Asian Pac J Trop Biomed 2(12):960–965. https://doi.org/10.1016/S2221-1691(13)60007-6 CrossRefPubMedPubMedCentral

McInnes I, Schett G (2007) Cytokines in the pathogenesis of rheumatoid arthritis. Nat Rev Immunol 7:29–442. https://doi.org/10.1038/nri2094 CrossRef

Mensor LL, Menezes FS, Leitao GG, Reis AS, Dos Santos TC, Coube CS et al (2001) Screening of Brazilian plant extracts for antioxidant activity by the use of DPPH free radical. Phytother Res 15(2):127–130PubMed

Mizushima Y, Kobayashi M (1968) Interaction of anti-inflammatory drugs with serum proteins, especially with some biologically active proteins. J Pharma Pharmacol 20:169–173

Moles J, Torrent A, Jose Alcaraz M, Ruhi R, Avila C (2014) Anti-inflammatory activity in the selected Antarctic benthic organisms. Front Mar Sci 1:24. https://doi.org/10.3389/fmars.2014.00024 CrossRef

Morris CJ (2003) Carrageenan-induced paw edema in the rat and mouse. Methods Mol Biol Inflam Protocols. https://doi.org/10.1385/1-59259-374-7:115 CrossRef

Morris SA (1986) Novel Secondary Metabolites Isolated from Selected Marine Invertebrates. University of British Columbia.

Nagalla S, Bray PF (2019) Drug-Induced platelet dysfunction. Hematology. Cancer Therapy Advisor. https://www.cancertherapyadvisor.com/home/decision-support-in-medicine/hematology/drug-induced-platelet-dysfunction/

Northcote PT (1989) Novel terpenoids metabolites from the marine sponge Xestospongia vanillia. University of British Columbia

Odebiyi A, Sofowora AE (1990) Phytochemical screening of Nigerian medicinal plants Part III. Lloydia 41(3):234–246

Pacienza N, Lee RH, Bae EH, Kim DK, Lou Q, Prockop DJ et al (2018) In vitro macrophages assay predicts the in vivo anti-inflammatory potential of exosomes from human mesenchymal stromal cells. Mol Ther Methods Clin Dev 13:67–76PubMedPubMedCentral

Pallela R, Ramjee K, Srikanth K, Gunda V, Gopal V et al (2011) Comparative morphometry, biochemical and elemental composition of three marine sponges (Petrosiidae) from Gulf of Mannar, India. Chem Spec Bioavail 23(1):16–23

Park EJ, Cheenpracha S, Chang LC, Pezzuto JM (2011) Suppression of cyclooxygenase-2 and inducible nitric oxide synthase expression by epimuqubilin A via IKK/IκB/NF-κB pathways in lipopolysaccharide-stimulated RAW 264.7 cells. Phytochem Lett 4(4):426–431. https://doi.org/10.1016/j.phytol.2011.07.009 CrossRefPubMedPubMedCentral

Posadas I, de Rosa S, Carmen Terencio M, Payá M, Alcaraz MJ (2003) Cacospongionolide B suppresses the expression of inflammatory enzymes and tumour necrosis factor-α by inhibiting nuclear factor-κB activation. Br J Pharmacol 138(8):1571–1579. https://doi.org/10.1038/sj.bjp.0705189 CrossRefPubMedPubMedCentral

Putra MY, Hadi TA, Murniqsih T (2016) In vitro antibacterial and antifungal activities of twelve sponges collected from the Anambas Islands, Indonesia. Asian Pac J Trop Dis 6(9):732–735

Qaralleh H, Idid SO, Idid SZ, Saad S, Darnis DS, Taher BM et al (2010) Antifungal and antibacterial activities of four Malaysian sponge species (Petrosiidae). J Med Mycol 20(4):315–320

Quintana J, Brango-Vanegas J, Costa GM, Castellanos L, Arévalo C, Duque C (2015) Marine organisms as source of exacts to disrupt bacterial communication: bioguided isolation and identification of quorum sensing inhibitors from Ircinia felix. Rev Bras Farmacogn 25(3):199–207

Radzi SAM, Andriani Y, Mohamad H, Mohamad TST, Saidin J (2015) In-vitro anti-inflammatory activities of extracts from bacteria associated with marine sponges Theonella sp. J Teknol 77(25):165–169. https://doi.org/10.1016/j.bjp.2015.03.013 CrossRef

Rutzler K (1975) The role of burrowing sponges in bioerosion. Oecologia 19:203–219PubMed

Sathe BS, Jagtap VA, Deshmukh SD, Jain BV (2011) Screening of in vitro anti-inflammatory activity of some newly synthesized fluorinated benzothiazolo imidazole compounds. Int J Pharm Pharm Sci 3(3):220–222

Schoggins JW, Randall G (2013) Lipids in innate antiviral defense. Cell Host Microbe 14(4):379–385. https://doi.org/10.1016/j.chom.2013.09.010 CrossRefPubMedPubMedCentral

Seo YJ, Lee KT, Rho JR, Choi JH (2015) Phobaketal A, isolated from the marine sponge Phorbas sp., exerts its anti-inflammatory effects via NF-кB inhibition and heme oxygenase-1 activation in lipopolysaccharide-stimulated macrophages. Mar Drugs 13(11):7005–7019PubMedPubMedCentral

Shady NH, El-Hossary EM, Fouad MA, Gulder TAM, Kamel MS, Abdelmohsen UR (2017) Bioactive natural products of marine sponges from the genus Hyrtios. Molecules 22(5):7981. https://doi.org/10.3390/molecules22050781 CrossRef

Sharma JN, Al-Omran A, Parvathy SS (2007) Role of nitric oxide in inflammatory diseases. Inflammopharmacol 15(6):252–259

Steger D, Ettinger-Epstein P, Whalan S, Hentschel U, de Nys R, Wagner M et al (2008) Diversity and mode of transmission of ammonia-oxidizing archaea in marine sponges. Environ Microbiol 10:1087–1094PubMed

Terracciano S, Aquino M, Rodriquez M, Chiara Monti M, Casapullo A, Riccio R et al (2006) Chemistry and biology of anti-inflammatory marine natural products: molecules interfering with cyclooxygenase, NF-kB and other unidentified targets. Curr Med Chem 13(16):1947–1969. https://doi.org/10.2174/092986706777585095 CrossRefPubMed

Tommonaro G, Iodice C, Abd El-Hady FK, Guerriero G, Pejin B (2015) The Mediterranean Sponge dysidea avara as a 40 year inspiration of marine natural product chemists. J Biodivers Endanger Specs S 1:001. https://doi.org/10.4172/2332-2543.S1-001 CrossRef

Vogel AI (1974) Practical Organic Chemistry including qualitative organic analysis, 3rd edn, Longmans, Green and Co., New York, pp 1214

Wulff JL (2006) Ecological interactions of marine sponges. Can J Zoo 84:46–166

Title: Marine sponges Sarcotragus foetidus, Xestospongia carbonaria and Spongia obscura constituents ameliorate IL-1 β and IL-6 in lipopolysaccharide-induced RAW 264.7 macrophages and carrageenan-induced oedema in rats
Authors: Sayli Chaudhari
Maushmi S. Kumar
Publication date: 01-08-2020
Publisher: Springer International Publishing
Published in: Inflammopharmacology / Issue 4/2020
Print ISSN: 0925-4692
Electronic ISSN: 1568-5608
DOI: https://doi.org/10.1007/s10787-020-00699-2

At a glance: The STEP trials

Springer Medicine

Marine sponges Sarcotragus foetidus, Xestospongia carbonaria and Spongia obscura constituents ameliorate IL-1 β and IL-6 in lipopolysaccharide-induced RAW 264.7 macrophages and carrageenan-induced oedema in rats

Abstract

Graphic abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Graphic abstract

Please log in to get access to this content

Other articles of this Issue 4/2020

An ethyl-acetate fraction of Holothuria scabra modulates inflammation in vitro through inhibiting the production of nitric oxide and pro-inflammatory cytokines via NF-κB and JNK pathways

Low-dose curcumin reduced TNBS-associated mucin depleted foci in mice by scavenging superoxide anion and lipid peroxides, rebalancing matrix NO synthase and aconitase activities, and recoupling mitochondria

Retraction Note: Selected TLR7/8 agonist and type I interferon (IFN‑α) cooperatively redefine the microglia transcriptome

Hesperidin methyl chalcone interacts with NFκB Ser276 and inhibits zymosan-induced joint pain and inflammation, and RAW 264.7 macrophage activation

Preoperative meloxicam versus postoperative meloxicam for pain control, patients’ satisfaction and function recovery in hip osteoarthritis patients who receive total hip arthroplasty: a randomized, controlled study

Significant action of Tridax procumbens L. leaf extract on reducing the TNF-α and COX-2 gene expressions in induced inflammation site in Swiss albino mice