Abstract
Fractionated compounds and methanol extract of the sponge Haliclona cratera (Schmidt, 1862) were investigated for their antioxidant and anti-inflammatory activities. The extract was also analyzed for its cytotoxicity in RAW macrophages by MTT assay. Enzyme-linked immunosorbent assay was performed to check the inflammatory mediators’ levels (TNF-α, COX-2, IL-1β, PGE2, IL-6). High-performance liquid chromatography–mass spectrometry was used for characterization of fractionated compounds. The extracts showed good bovine serum albumin denaturation inhibition and poor antioxidant activity. It was also observed that the sponge extract did not show good cell viability which indicated its cytotoxic nature. Hc_EA_2, Hc_CHCl3_7, Hc_EA_5, and Hc_CHCl3_6 showed best IL-1β and IL-6 inhibition in the range of 14.10–61.91%. Hc_EA_2, Hc_EA_5, Hc_CHCl3_7 and Hc_CHCl3_6 inhibited TNF-α levels at 74.78, 80.45, 74.16 and 81.29%, respectively. Fractionated compounds reduced the levels of IL-1β, IL-6, PGE2, TNF-α and NO considerably in rats subjected to carrageenan-induced inflammation. Three compounds were characterized as per MS data, namely Sphingosine with isopropyl terminus, 24-methyl-5~-cholesta-7,9(11),24(28) ~-trien-38-o1 and 24-vinyl-cholest-9-ene-3β, 24-diol.
Similar content being viewed by others
REFERENCES
Al-Massarani, S.M., El-Gamal, A.A., Al-Said, M.S., et al., Studies on the Red Sea sponge Haliclona sp. for its chemical and cytotoxic properties, Pharmacogn. Mag., 2016, vol. 12, no. 46, pp. 114–119.
Aneiros, A. and Garateix, A., Bioactive peptides from marine sources: pharmacological properties and isolation procedures, J. Chromatogr. B: Anal. Technol. Biomed. Life Sci., 2004, vol. 803, no. 1, pp. 41–53.
Anjum, K., Abbas, S.Q., Shah, S.A.A. et al., Marine sponges as a drug treasure, Biomol. Ther., 2016, vol. 24, no. 4, pp. 347–362.
Asagabaldan, M.A., Ayuningrum, D., Kristiana, R. et al., Identification and antibacterial activity of bacteria isolated from marine sponge Haliclona (Reniera) sp. against multidrug resistant human pathogen, IOP Conf. Ser.: Earth Environ. Sci., 2017, vol. 55, art. ID 012019.
Athira Krishnan, K.A., and Keerthi, T.F., 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. Microbiol. Appl. Sci., 2016, vol. 5, no. 2, pp. 722–734.
Baker, B.J., Scheuer, P.J., and Shoolery, J.N., Papuamine, an antifungal pentacyclic alkaloid from a marine sponge, Haliclona sp., J. Am. Chem. Soc., 1988, vol. 110, no. 3, pp. 965–966.
Cimino, G., Mattia, C.A., Mazzarella, L. et al., Unprecedented alkaloid skeleton from the Mediterranean sponge Reniera sarai: X-ray structure of an acetate derivative of sarain-a, Tetrahedron, 1989, vol. 45, no. 12, pp. 3863–3872.
Clark, R.J., Garson, M.J., and Hooper, J.N.A., Antifungal alkyl amino alcohols from the tropical marine sponge Haliclona n. sp, J. Nat. Prod., 2001, vol. 64, no. 12, pp. 1568–1571.
De Bary, A., Die Erscheinung der Symbiose, Strassburg: Verlag von Karl J. Trübner, 1879.
Ebada, S.S., Edrada, R.A., Lin, W. et al., Methods for isolation, purification and structural elucidation of bioactive secondary metabolites from marine invertebrates, Nat. Protoc., 2008, vol. 3, pp. 1820–31.
Erickson, K.L., Beutler, J.A., Cardellina, J.H., and Boyd, M.R., Salicylihalamides A and B, novel cytotoxic macrolides from the marine sponge, J. Org. Chem., 1997, vol. 62, no. 23, pp. 8188–8192.
Fahy, E., Molinski, T.F., Harper, M.K. et al., Haliclonadiamine, an antimicrobial alkaloid from the sponge Haliclona sp., Tetrahedron Lett., 1988, vol. 29, no. 28, pp. 3427–3428.
Gözcelioğlu, B. and Konuklugil, B., Qualitative detection of some secondary metabolites from three Turkish marine sponges, FABAD J. Pharm. Sci., 2012, vol. 37, pp. 73–78.
Gunathilake, V., Bertolino, M., Bavestrello, G., et al., Immunomodulatory activity of the marine sponge, Haliclona (Soestella) sp. (Haplosclerida: Chalinidae), from Sri Lanka in Wistar albino rats: Immunosuppression and Th1-skewed cytokine response, J. Immunol. Res., 2020, vol. 2020, art. ID 7281295.
Hara, S., Makino, K., and Hamada, Y., Total synthesis of halipeptin A, a potent anti-inflammatory cyclodepsipeptide from a marine sponge, Tetrahedron Lett., 2006, vol. 47, no. 7, pp. 1081–1085.
Hort, M.A., Da Silva Júnior, F., Garcia, E.M., et al., Antinociceptive and anti-inflammatory activities of marine sponges Aplysina caissara, Haliclona sp. and Dragmacidon reticulatum, Braz. Arch. Biol. Technol., 2018, vol. 61, art. ID e18180104.
Keyzers, R.A., and Davies-Coleman, M.T., Anti-inflammatory metabolites from marine sponges, Chem. Soc. Rev., 2005, vol. 34, no. 4, pp. 355–365.
Kim, S.K., and Dewapriya, P., Bioactive compounds from marine sponges and their symbiotic microbes: a potential source of nutraceuticals, Adv. Food Nutr. Res., 2012, vol. 65, pp. 137–151.
Koh, S-I., and Shin, H-S., The Anti-rotaviral and anti-inflammatory effects of Hyrtios and Haliclona species, J. Microbiol. Biotechnol., 2016, vol. 26, no. 11, pp. 2006–2011.
Kumar, M.S., Pandita, N.S., and Pal, A.K., LC-MS/MS as a tool for identification of bioactive compounds in the marine sponge Spongosorites halichondriodes (Dendy 1905), Toxicon, 2012, vol. 60, no. 6, pp. 1135–1147.
Liu, T., Li, J., Liu, Y., et al., Short-chain fatty acids suppress lipopolysaccharide-induced production of nitric oxide and proinflammatory cytokines through inhibition of NF-kB pathway in RAW264.7 Cells, Inflammation, 2012, vol. 35, pp. 1676–1684.
Luter, H.M., Widder, S., Botté, E.S. et al., Biogeographic variation in the microbiome of the ecologically important sponge, Carteriospongia foliascens, PeerJ, 2015, vol. 3, art. ID e1435.
Mahajna, S., Azab, M., Zaid, H. et al., In vitro evaluations of cytotoxicity and anti-inflammatory effects of Peganum harmala seed extracts in THP-1 derived macrophages, Eur. J. Med. Plants, 2015, vol. 5, pp. 165–175.
Mahdian, D., Iranshahy, M., Shakeri, A., et al., Cytotoxicity evaluation of extracts and fractions of five marine sponges from the Persian Gulf and HPLC fingerprint analysis of cytotoxic extracts, Asian Pac. J. Trop. Biomed., 2015, vol. 5, no. 11, pp. 896–901.
Mayer, A.M.S., Hall, M.L., Lynch, S.M. et al., Differential modulation of microglia superoxide anion and thromboxane B2 generation by the marine manzamines, BMC Pharmacol., 2005, vol. 5, art. ID 6.
Mensor, L.L., Menezes, F.S., Leitão, G.G. et al., Screening of Brazilian plant extracts for antioxidant activity by the use of DPPH free radical method, Phytother. Res., 2001, vol. 15, no. 2, pp. 127–130.
Mizushima, Y., and Kobayashi, M., Interaction of anti-inflammatory drugs with serum proteins, especially with some biologically active proteins, J. Pharm. Pharmacol., 1968, vol. 20, no. 3, pp. 169–173.
Mohamed, N.M., Colman, A.S., Tal, Y., et al., Diversity and expression of nitrogen fixation genes in bacterial symbionts of marine sponges, Environ. Microbiol., 2008, vol. 10, no. 11, pp. 2910–2921.
Moles, J., Torrent, A., José Alcaraz, M., et al., Anti-inflammatory activity in the selected Antarctic benthic organisms, Front. Mar. Sci., 2014, vol. 1, art. ID 24.
Nakagawa, M., Endo, M., Tanaka, N., et al., Structures of xestospongin A, B, C and D, novel vasodilative compounds from marine sponge, Xestospongia exigua, Tetrahedron Lett., 1984, vol. 25, no. 30, pp. 3227–3230.
Odebiyi, A., and Sofowora, A.E., Phytochemical screening of Nigerian medicinal plants. Part III, Lloydia, 1990, vol. 41, no. 3, pp. 234–246.
Olson, J.B., and McCarthy, P.J., Associated bacterial communities of two deep-water sponges, Aquat. Microb. Ecol., 2005, vol. 39, pp. 47–55.
Pacienza, N., Lee, R.H., Bae, E.H., et al., In vitro macrophages assay predicts the in vivo anti-inflammatory potential of exosomes from human mesenchymal stromal cells, Mol. Ther.–Methods Clin. Dev., 2018, vol. 13, pp. 67–76.
Pajic, I., Kljajic, Z., Dogovic, N., et al., A novel lectin from the sponge Haliclona cratera: isolation, characterization and biological activity, Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol., 2002, vol. 132, no. 2, pp. 213–221.
Pallela, R., Koigoora, S., Gunda, V.G., et al., Comparative morphometry, biochemical and elemental composition of three marine sponges (Petrosiidae) from Gulf of Mannar, India, Chem. Speciation Bioavailability, 2011, vol. 23, no. 1, pp. 16–23.
Park, E.J., Cheenpracha, S., Chang, L.C., et al., Suppression of cyclooxygenase-2 and inducible nitric oxide synthase expression by epimuqubilin A via IKK/IκB/NF-κB pathways in lipopolysaccharide-stimulated RAW264.7 cells, Phytochem. Lett., 2011, vol. 4, no. 4, pp. 426– 431.
Posadas, I., Terencio, M.C., Giannini, C. et al., Dysidotronic acid, a new sesquiterpenoid, inhibits cytokine production and the expression of nitric oxide synthase, Eur. J. Pharmacol., 2001, vol. 415, nos. 2–3, pp. 285–292.
Randazzo, A., Bifulco, G., Giannini, C., et al., Halipeptins A and B: Two novel potent anti-inflammatory cyclic depsipeptides from the Vanuatu marine sponge Haliclona species, J. Am. Chem. Soc., 2001, vol. 123, no. 44, pp. 10870–10876.
Rashid, M.A., Gustafson, K.R., Boswell, J.L., et al., Haligramides A and B, two new cytotoxic hexapeptides from the marine sponge Haliclona nigra, J. Nat. Prod., 2000, vol. 63, no. 7, pp. 956–959.
Sakai, R., Kohmoto, S., Higa, T. et al., Two novel alkaloids from the sponge Haliclona sp., Tetrahadron Lett., 1987, vol. 28, pp. 5493–5496.
Sathe, B.S., Jagtap, V.A., Deshmukh, S.D., et al., Screening of in vitro anti-inflammatory activity of some newly synthesized fluorinated benzothiazolo imidazole compounds, Int. J. Pharm. Pharm. Sci., 2011, vol. 3, pp. 220–222.
Schmitz, J., Hollenbeak, K.H., and Campbell, D.C., Marine natural products: halitoxin, toxic complex of several marine sponges of the genus Haliclona, J. Org. Chem., 1978, vol. 43, no. 20, pp. 3916–3922.
Sipkema, D., Holmes, B., Nichols, S.A., and Blanch, H.W., Biological characterisation of Haliclona (? gellius) sp.: sponge and associated microorganisms, Microb. Ecol., 2009, vol. 58, no. 4, pp. 903–920.
Vogel, A.I., A Textbook of Practical Organic Chemistry including Quantitative Organic Analysis, London: Longman Group, 1958.
Webster, N.S., Negri, A.P., Munro, M.M.H.G., et al., Diverse microbial communities inhabit Antarctic sponges, Environ. Microbiol., 2004, vol. 6, no. 3, pp. 288–300.
Yu, S., Deng, Z., Proksch, P., et al., Oculatol, oculatolide, and A-nor sterols from the sponge Haliclona oculata, J. Nat. Prod., 2006, vol. 69, no. 9, pp. 1330–1334.
ACKNOWLEDGMENTS
I express my gratitude to Mr. Shailendra Rane, Dr. Swapnaja Mohite, and Ms. Sayli Chaudhary for helping with analysis and sponge identification and to SVKM’s NMIMS for all the support.
Funding
This work was financially supported by the Department of Biotechnology, Government of India (Project no. BT/PR12182/AAQ/3/696/2014).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests. The authors declare that they have no conflict of interest.
Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Rights and permissions
About this article
Cite this article
Kumar, M.S. Chemical Constituents and Anti-inflammatory Properties of the Marine Sponge Haliclona cratera from Konkan, India. Russ J Mar Biol 48, 285–296 (2022). https://doi.org/10.1134/S106307402204006X
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S106307402204006X