Biological activity, chemical profiling and molecular docking of tissue extracts of the sea snail Trochus erithreus

Khaled M. Zayed; Mosad A. Ghareeb; Mohamed R. Habib; Hanaa M. Abu El-Einin; Rasha E.M. Ali; Rasha M. Gad El-Karim; Rehab Sabour; Ahmed A. Hamed

doi:10.7324/JAPS.2023.119765

Abstract

The biodiversity of marine mollusks, along with their worldwide availability and ease of harvesting, makes them an enticing subject for scientific research. Mollusks are frequently the target of pharmaceutical scientists who are searching for novel compounds to benefit the population. This study targets the investigation of the antioxidant, antibiofilm, antimicrobial, and cytotoxic activities of different solvent extracts of marine mollusk Trochus erithreus. The chemical constituents of the most promising extract and molecular docking analyses are also investigated. Results showed that ethyl alcohol extract had the highest phenolic content (213.90 ± 4.88 mg GAE/ g extract), total antioxidant activity (545.33 ± 4.02 mg AAE/ g extract), and antibacterial activity against Staphylococcus aureus (31.32 ± 1.49), while the acetone extract had the highest scavenging effect against 2,2-diphenyl-1-picryl-hydrazyl radical (IC50: 53.59 ± 1.71 μg/ml). The acetone extract also displayed pronounced antibacterial activity against Proteus vulgaris with an inhibition ratio of up to 67.93% and it had potent cytotoxic effects against both prostate (IC50: 1.666 ± 0.07 μg/ml) and human lung carcinoma cell lines (IC50: 12.04 ± 0.55 μg/ml). Gas chromatography-mass spectrometry investigation of the acetone extract resulted in the recognition of 45 compounds. Bisabolol oxide A (24.63%), (E)-α-farnesene (7.89%), and tricyclo[8.2.0.0(2,5)] dodeca-3,6,8,11-tetraene (5.41%) were detected as major components. The molecular docking study demonstrated strong binding scores and modes of interactions of several major compounds, inside the active binding sites of bacterial enzymes, thymidylate kinase, DNA gyrase B, and DNA topoisomerase IV/subunit Bs.

Keyword: Marine mollusca chemical constituents molecular docking bioactivities antimicrobial antibiofilm

Citation:

Zayed KM, Ghareeb MA, Habib MR, El-Einin HMA, Ali REM, El-Karim RMG, Sabour R, Hamed AA. Biological activity, chemical profiling and molecular docking of tissue extracts of the sea snail Trochus erithreus. J Appl Pharm Sci, 2023. https://doi.org/10.7324/JAPS.2023.119765

Copyright: © The Author(s). This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Reference

Abdel-Wareth MTA, Ghareeb AM, Abdel-Aziz SM, El-Hagrassi MA. Snailicidal, antimicrobial, antioxidant and anticancer activities of Beauveria bassiana, Metarhizium anisopliae and Paecilomyces lilacinus fungal extracts. Egypt J Aquat Biol Fish, 2019; 23:195-212. https://doi.org/10.21608/ejabf.2019.30550

Abu El-Einin AA, Gad El-Karim RM, Habib MR, Zayed KM, Ali REM. Identification of the gastropod snails and shells collected from Ain El- Sokhna region, Red Sea, Egypt. Egypt J Aquat Biol Fisher, 2021; 25:101-17. https://doi.org/10.21608/ejabf.2021.172857

Agour MA, Hamed AA, Ghareeb MA, Abdel-Hamid EAA, Ibrahim MK. Bioactive secondary metabolites from marine Actinomyces sp. AW6 with an evaluation of ADME related physicochemical properties. Arch Microbiol, 2022; 204:537; doi:10.1007/s00203-022-03092-5 https://doi.org/10.1007/s00203-022-03092-5

Ameri A, Shushizadeh MR, Bagher Nabavi SM, Espere F, Zarei Ahmady A. Antibacterial evaluation and biochemical characterization of Thais savignyi gastropod extracts from the Persian Gulf. Jundishapur J Nat Pharm Prod, 2017; 12:e13942. https://doi.org/10.5812/jjnpp.13942

Andrade MA, Azevedo CDS, Motta FN, Santos ML, dos Silva CL, Santana JM, de Bastos IMD. Essential oils: in vitro activity against Leishmania amazonensis, cytotoxicity and chemical composition. BMC Complement Altern Med, 2016; 16:444; doi:10.1186/s12906-016-1401-9 https://doi.org/10.1186/s12906-016-1401-9

Anitha C, Rose SMB Antimicrobial activity of the hemolymph and whole body extract of a fresh water clam, Villorita cyprinoides (Gray, 1825). Int J Zool Appl Biosci, 2018; 3:151-6.

Bae H, Jayaprakasha GK, Crosby K, Jifon JL, Patil BS. Influence of extraction solvents on antioxidant activity and the content of bioactive compounds in non-pungent peppers. Plant Foods Hum Nutr, 2012; 67:120-8. https://doi.org/10.1007/s11130-012-0290-4

Bazes A, Silkina A, Douzenel P, Faÿ F, Kervarec N, Morin D, Berge JP, Bourgougnon N. Investigation of the antifouling constituents from the brown alga Sargassum muticum (Yendo) Fensholt. J Appl Phycol, 2009; 21:395-403. https://doi.org/10.1007/s10811-008-9382-9

Bhatnagar I, Kim SK. Immense essence of excellence: marine microbial bioactive compounds. Mar. Drugs, 2010; 8:2673-701. https://doi.org/10.3390/md8102673

Boman HG. Peptide antibiotics and their role in innate immunity. Annu Rev Immunol, 1995;13:61-92. https://doi.org/10.1146/annurev.iy.13.040195.000425

Cavalieri E, Bergamini C, Mariotto S, Leoni S, Perbellini L, Darra E, Suzuki H, Fato R, Lenaz G. Involvement of mitochondrial permeability transition pore opening in α-bisabolol induced apoptosis. FEBS J, 2009; 276:3990-4000. https://doi.org/10.1111/j.1742-4658.2009.07108.x

Elkhouly HI, Hamed AA, El Hosainy AM, Ghareeb MA, Sidkey NM. Bioactive secondary metabolite from endophytic Aspergillus Tubenginses ASH4 isolated from Hyoscyamus muticus: antimicrobial, antibiofilm, antioxidant and anticancer activity. Pharmacogn J, 2021a; 13(2):434-42; doi:10.5530/pj.2021.13.55 https://doi.org/10.5530/pj.2021.13.55

Elkhouly HI, Sidkey NM, Ghareeb MA, El Hosainy AM, Hamed AA. Bioactive secondary metabolites from endophytic Aspergillus terreus AH1 isolated from Ipomoea carnea growing in Egypt. Egypt J Chem, 2021b; 64(12):7511-20; doi:10.21608/EJCHEM.2021.85908.4161 https://doi.org/10.21608/ejchem.2021.85908.4161

Estari M, Satyanarayana J, Kumar BS, Bikshapati T, Reddy AS, Venkanna L. In vitro study of antimicrobial activity in freshwater mussel (Lamellidens marginalis) extracts. Biol Med, 2011; 3:191-5.

Faulkner DJ. Chemical defenses of marine molluscs. In: Ecological roles of marine natural products. Cornell University Press, Ithaca, NY, pp 119-63, 2019. https://doi.org/10.7591/9781501737435-008

Gad El-Karim RM, Habib MR, Ghareeb MA, Ali REM. Assessment of the antioxidant capacity of Lanistes carinatus tissue extract and its immune-boosting influence on Biomphalaria alexandrina against infection with Schistosoma mansoni. Egypt J Aquat Biol Fish, 2022; 26(4):361-76; doi:10.21608/EJABF.2022.249977 https://doi.org/10.21608/ejabf.2022.249977

Gerwick WH. Drugs from the sea: the search continues. J Pharm Technol, 1987; 3:136-41. https://doi.org/10.1177/875512258700300407

Ghareeb MA, Hussein AH, Hassan MFM, Laila AR, Mona AM, Amal MS. Antioxidant and cytotoxic activities of Tectona grandis linn leaves. Int J Phytopharm, 2014; 5:143-57.

Ghareeb MA, Saad AM, Abdou AM, Refahy LAG, Ahmed WS. A new kaempferol glycoside with antioxidant activity from Chenopodium ambrosioides growing in Egypt. Orient J Chem, 2016; 32:3054-61. https://doi.org/10.13005/ojc/320626

Ghareeb MA, Tammam MA, El-Demerdash A, Atanasov AG. Insights about clinically approved and preclinically investigated marine natural products. Curr Res Biotechnol, 2020; 2:88-102; doi:10.1016/j. crbiot.2020.09.001 https://doi.org/10.1016/j.crbiot.2020.09.001

Gueguen Y, Herpin A, Aumelas A, Garnier J, Fievet J, Escoubas JM, Bulet P, Gonzalez M, Lelong C, Favrel P. Characterization of a defensin from the oyster Crassostrea gigas: recombinant production, folding, solution structure, antimicrobial activities, and gene expression. J Biol Chem, 2006; 281:313-23. https://doi.org/10.1074/jbc.M510850200

Habib MR, Hamed AA, Ali REM, Zayed KM, Gad El-Karim RM, Sabour R, Abu El-Einin HM, Ghareeb MA. Thais savignyi tissue extract: bioactivity, chemical composition, and molecular docking. Pharm Biol, 2022; 60(1):1899-914; doi:10.1080/13880209.2022.2123940 https://doi.org/10.1080/13880209.2022.2123940

Hamed AA, Soldatou S, Qader MM, Arjunan S, Miranda KJ, Casolari F, Pavesi C, Diyaolu OA, Thissera B, Eshelli M, Belbahri L, Luptakova L, Ibrahim NA, Abdel-Aziz MS, Eid BM, Ghareeb MA, Rateb ME, Ebel R. Screening fungal endophytes derived from under-explored Egyptian marine habitats for antimicrobial and antioxidant properties in factionalised textiles. Microorganisms, 2020; 8:1617; doi:10.3390/microorganisms8101617 https://doi.org/10.3390/microorganisms8101617

Hinzmann M, Bessa LJ, Teixeira A, Da Costa PM, Machado J. Antimicrobial and antibiofilm activity of unionid mussels from the north of Portugal. J Shellfish Res, 2018; 37:121-9. https://doi.org/10.2983/035.037.0110

Ibrahim AM, Hamed AA, Ghareeb MA. Marine, freshwater, and terrestrial snails as models in the biomedical applications. Egypt J Aquat Biol Fish, 2021; 25(3):23-38; doi:10.21608/EJABF.2021.172142 https://doi.org/10.21608/ejabf.2021.172142

Jamal M, Ahmad W, Andleeb S, Jalil F, Imran M, Nawaz MA, Hussain T, Ali M, Rafiq M, Kamil MA. Bacterial biofilm and associated infections. J Chin Med Assoc, 2018; 81:7-11; doi:10.1016/j.jcma.2017.07.012 https://doi.org/10.1016/j.jcma.2017.07.012

Kaczor AA, Polski A, Sobótka-Polska K, Pachuta-Stec A, Makarska-Bialokoz M, Pitucha M. Novel antibacterial compounds and their drug targets-successes and challenges. Curr Med Chem, 2017; 24; doi:10.21 74/0929867323666161213102127 https://doi.org/10.2174/0929867323666161213102127

Kawatkar SP, Keating TA, Olivier NB, Breen JN, Green OM, Guler SY, Hentemann MF, Loch JT, McKenzie AR, Newman JV, Otterson LG, Martínez-Botella G. Antibacterial inhibitors of gram-positive Thymidylate Kinase: structure-activity relationships and chiral preference of a new hydrophobic binding region. J Med Chem, 2014; 57:4584-97; doi:10.1021/jm500463c https://doi.org/10.1021/jm500463c

Kumar KS, Ganesan K, Rao PS. Antioxidant potential of solvent extracts of Kappaphycus alvarezii (Doty) Doty-An edible seaweed. Food Chem, 2008; 107:289-95. https://doi.org/10.1016/j.foodchem.2007.08.016

Kuppusamy A, Ulagesan S. Antimicrobial activity of protein hydrolysate from marine molluscs Babylonia spirata (Linnaeus, 1758). J Appl Pharm Sci, 2016; 6:073-7. https://doi.org/10.7324/JAPS.2016.60711

Khalaf MO, Abdel-Aziz MS, El-Hagrassi AM, Osman AF, Ghareeb MA. Biochemical aspect, antimicrobial and antioxidant activities of Melaleuca and Syzygium species (Myrtaceae) grown in Egypt. J Phys Conf Ser, 2021; 1879:022-62; doi:10.1088/1742- 6596/1879/2/022062 https://doi.org/10.1088/1742-6596/1879/2/022062

Madkour HM, Ghareeb MA, Abdel-Aziz MS, Khalaf OM, Saad AM, El-Ziaty AK, Abdel-Mogib M. Gas chromatography-mass spectrometry analysis, antimicrobial, anticancer and antioxidant activities of n-hexane and methylene chloride extracts of Senna italica. J Appl Pharm Sci, 2017; 7:23-32.

Mayers DL, Sobel JD, Ouellette M, Kaye KS, Marchaim D. Antimicrobial drug resistance: clinical and epidemiological aspects, Springer International Publishing AG, Cham, Switzerland, 2, 2017. https://doi.org/10.1007/978-3-319-47266-9

Mitta G, Hubert F, Noël T, Roch P. Myticin, a novel cysteine-rich antimicrobial peptide isolated from haemocytes and plasma of the mussel Mytilus galloprovincialis. Eur J Biochem, 1999; 265:71-8. https://doi.org/10.1046/j.1432-1327.1999.00654.x

Moure A, Cruz JM, Franco D, Dom??nguez JM, Sineiro J, Dom??nguez H, Núñez MJ, Parajó JC. Natural antioxidants from residual sources. Food Chem, 2001; 72:145-71. https://doi.org/10.1016/S0308-8146(00)00223-5

Murata Y, Kokuryo T, Yokoyama Y, Yamaguchi J, Miwa T, Shibuya M, Yamamoto Y, Nagino M. The anticancer effects of novel α-bisabolol derivatives against pancreatic cancer. Anticancer Res, 2017; 37:589-98; doi:10.21873/anticanres.11352 https://doi.org/10.21873/anticanres.11352

Nazeer RA, Naqash SY. In vitro antioxidant activity of two molluscs, Loligo duvauceli Orbigny and Donax cuneatus Linnaeus, by solvent extraction methods. Mediterr J Nutr Metab, 2013; 6:17-21. https://doi.org/10.1007/s12349-011-0088-1

Olicard C, Renault T, Torhy C, Benmansour A, Bourgougnon N. Putative antiviral activity in hemolymph from adult Pacific oysters, Crassostrea gigas. Antiviral Res, 2005; 66:147-52. https://doi.org/10.1016/j.antiviral.2005.03.003

Prieto P, Pineda M, Aguilar M. Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem, 1999; 269:337-41. https://doi.org/10.1006/abio.1999.4019

Roch P, Yang Y, Toubiana M, Aumelas A. NMR structure of mussel mytilin, and antiviral-antibacterial activities of derived synthetic peptides. Dev Comp Immunol, 2008; 32:227-38. https://doi.org/10.1016/j.dci.2007.05.006

Santhiya N, Sanjeevi SB. Antibacterial activity of freshwater mussel Parreysia corrugata (Muller 1774) from lower Anaicut Reservoir India. Int J Pharm Life Sci, 2014; 5:3899-02.

Seki T, Kokuryo T, Yokoyama Y, Suzuki H, Itatsu K, Nakagawa A, Mizutani T, Miyake T, Uno M, Yamauchi K. Antitumor effects of α-bisabolol against pancreatic cancer. Cancer Sci, 2011; 102:2199-205. https://doi.org/10.1111/j.1349-7006.2011.02082.x

Sharifi-Rad M, Nazaruk J, Polito L, Morais-Braga MFB, Rocha JE, Coutinho HDM, Salehi B, Tabanelli G, Montanari C, del Mar Contreras M, Yousaf Z, Setzer WN, Verma DR, Martorell M, Sureda A, Sharifi-Rad J. Matricaria genus as a source of antimicrobial agents: From farm to pharmacy and food applications. Microbiol Res, 2018; 215:76-88 doi:10.1016/j.micres.2018.06.010 https://doi.org/10.1016/j.micres.2018.06.010

Shawky TB, Nagah M, Ghareeb AM, El-Sherbiny MG, Moghannem AM, Abdel-Aziz M. Evaluation of antioxidants, total phenolics and antimicrobial activities of ethyl acetate extracts from fungi grown on rice straw. J Renew Mater, 2019; 7:667-82; doi:10.32604/jrm.2019.04524 https://doi.org/10.32604/jrm.2019.04524

Shirwaikar A, Prabhu KS, Samraj PI. In vitro antioxidant studies of Sphaeranthus indicus (Linn). Indian J Exp Biol, 2006; 44(12):993-6.

Shoeb HA, Madkour HM, Refahy LA, Mohamed MA, Saad AM, Ghareeb MA. Antioxidant and cytotoxic activities of Gmelina arborea ROXB. leaves. J Pharm Res Int, 2014; 4:125-44. https://doi.org/10.9734/BJPR/2014/6018

Silver LL. Multi-targeting by monotherapeutic antibacterials. Nat Rev Drug Discov, 2007; 6:41-55; doi:10.1038/nrd2202 https://doi.org/10.1038/nrd2202

Simões NG, Bettencourt AF, Monge N, Ribeiro IAC. Novel antibacterial agents: an emergent need to win the battle against infections. Mini-Rev Med Chem, 2017; 17; doi:10.2174/1389557516666160907151454 https://doi.org/10.2174/1389557516666160907151454

Tari LW, Trzoss M, Bensen DC, Li X, Chen Z, Lam T, Zhang J, Creighton CJ, Cunningham ML, Kwan B, Stidham M, Shaw KJ, Lightstone FC, Wong SE, Nguyen TB, Nix J, Finn J. Pyrrolopyrimidine inhibitors of DNA gyrase B (GyrB) and topoisomerase IV (ParE). Part I: Structure guided discovery and optimization of dual targeting agents with potent, broad-spectrum enzymatic activity. Bioorg Med Chem Lett, 2013; 23:1529-36; doi:10.1016/j.bmcl.2012.11.032 https://doi.org/10.1016/j.bmcl.2012.11.032

Uno M, Kokuryo T, Yokoyama Y, Senga T, Nagino M. α-Bisabolol inhibits invasiveness and motility in pancreatic cancer through KISS1R activation. Anticancer Res, 2016; 36:583-9.

Williams C. The nabobs of Berkshire. Goosecroft Publications, UK, 2010.

Zasloff M. Antimicrobial peptides of multicellular organisms. Nature, 2002; 415:389-95. https://doi.org/10.1038/415389a

Ziebuhr W, Hennig S, Eckart M, Kränzler H, Batzilla C, Kozitskaya S. Nosocomial infections by Staphylococcus epidermidis: how a commensal bacterium turns into a pathogen. Int J Antimicrob Agents, 2006; 28:14-20. https://doi.org/10.1016/j.ijantimicag.2006.05.012

Abstract

HTML Full Text

Reference

Article Metrics

Related Search

Citiaion Alert By Google Scholar

Similar Articles