Radical-Scavenging and Anti-inflammatory Activities of Fermented Eucheuma cottonii from Lombok

Authors

  • Agustina L. N. Aminin Department of Chemistry, Diponegoro University, Semarang 50275, Indonesia https://orcid.org/0000-0003-3422-0872
  • Ella Anggraeni Department of Chemistry, Diponegoro University, Semarang 50275, Indonesia
  • Safira A. Ramoza Department of Chemistry, Diponegoro University, Semarang 50275, Indonesia
  • Meiny Suzery Department of Chemistry, Diponegoro University, Semarang 50275, Indonesia https://orcid.org/0000-0002-1163-4186
  • Bambang Cahyono Department of Chemistry, Diponegoro University, Semarang 50275, Indonesia https://orcid.org/0000-0002-9800-6683
  • Anoosh Eghdami Department of Biology, Islamic Azad University, Saveh Branch, Saveh, Iran

DOI:

https://doi.org/10.70099/BJ/2024.01.03.18

Keywords:

Eucheuma cottonii, fermentation, Lactobacillus plantarum, antioxidant, anti-inflammation

Abstract

Eucheuma cottonii, a widely cultivated seaweed from the Island of Lombok, Indonesia, contains various bioactive compounds. Its utilization, however, is mainly limited based on its high carbohydrate content. Nevertheless, plant fermentation using lactic acid bacteria is renowned for increasing bioactive compounds and enhancing bioactivities. This study unveiled the potential of Lactobacillus plantarum-fermented E. cottonii as a functional food. E. cottonii was fermented using L. plantarum for 24 h. The folin-Ciocalteau method was used to determine the total phenolic content. The antioxidant capacity was measured using 2,2'-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) assay. Anti-inflammatory activity was carried out using cyclooxygenase (COX) inhibition assay against cervical cancer (HeLa) and colon cancer (WiDr) cells. Overall, fermentation successfully enhanced the bioactivities of E. cottonii. Fermented products exhibited higher antioxidant capacity than unfermented ones. Interestingly, the bioactivities only showed a moderate correlation with total phenolic content. Regarding anti-inflammatory activity, fermented extracts exhibited higher cyclooxygenase inhibition against HeLa cells, whereas no significant differences were observed between the fermented and unfermented products in WiDr cells. These findings indicate that L. plantarum-fermented E. cottonii holds promise to be a profitable functional food and has the potential to be utilised as an additional food therapy for cancer treatment.

References

1. Pizzino G, Irrera N, Cucinotta M, Pallio G, Mannino F, Arcoraci V, et al. Oxidative stress: harms and benefits for human health. Oxidative medicine and cellular longevity. 2017, 2017, 1-13. https://doi.org/10.1155/2017/8416763

2. Lee H-H, Lin C-T, Yang L-L. Neuroprotection and free radical scavenging effects of Osmanthus fragrans. Journal of Biomedical Science. 2007, 14, 819-827. https://doi.org/10.1007/s11373-007-9179-x

3. Duan X-J, Zhang W-W, Li X-M, Wang B-G. Evaluation of antioxidant property of extract and fractions obtained from a red alga, Polysiphonia urceolata. Food chemistry. 2006, 95, 37-43. https://doi.org/10.1016/j.foodchem.2004.12.015

4. Kulisic T, Radonic A, Katalinic V, Milos M. Use of different methods for testing antioxidative activity of oregano essential oil. Food chemistry. 2004, 85, 633-640. https://doi.org/10.1016/j.foodchem.2003.07.024

5. Moure A, Cruz JM, Franco D, Domı́nguez JM, Sineiro J, Domı́nguez H, et al. Natural antioxidants from residual sources. Food chemistry. 2001, 72, 145-171. https://doi.org/10.1016/s0308-8146(00)00223-5

6. Wu S-C, Wang F-J, Pan C-L. The comparison of antioxidative properties of seaweed oligosaccharides fermented by two lactic acid bacteria. Journal of Marine Science and Technology. 2010, 18, 1-11. https://doi.org/10.51400/2709-6998.1908

7. Gupta S, Abu-Ghannam N, Scannell AG. Growth and kinetics of Lactobacillus plantarum in the fermentation of edible Irish brown seaweeds. Food and Bioproducts Processing. 2011, 89, 346-355. https://doi.org/10.1016/j.fbp.2010.10.001

8. Ratanaburee A, Kantachote D, Charernjiratrakul W, Penjamras P, Chaiyasut C. Enhancement of γ-aminobutyric acid in a fermented red seaweed beverage by starter culture Lactobacillus plantarum DW12. Electronic Journal of Biotechnology. 2011, 14, 1-14. https://doi.org/10.2225/vol14-issue3-fulltext-2

9. Shobharani P, Halami P, Sachindra N. Potential of marine lactic acid bacteria to ferment Sargassum sp. for enhanced anticoagulant and antioxidant properties. Journal of Applied Microbiology. 2013, 114, 96-107. https://doi.org/10.1111/jam.12023

10. Teo BSX, Gan RY, Abdul Aziz S, Sirirak T, Mohd Asmani MF, Yusuf E. In vitro evaluation of antioxidant and antibacterial activities of Eucheuma cottonii extract and its in vivo evaluation of the wound‐healing activity in mice. Journal of cosmetic dermatology. 2021, 20, 993-1001. https://doi.org/10.1111/jocd.13624

11. Arsianti A, Aziza YAN, Kurniasari KD, Mandasari BKD, Masita R, Zulfa FR, et al. Phytochemical test and cytotoxic activity of macroalgae Eucheuma cottonii against cervical HeLa cells. Pharmacognosy Journal. 2018, 10, 1012-1017. https://doi.org/10.5530/pj.2018.5.172

12. Sumardianto R, PH A, AD R, Rianingsih L. Phenol content and antioxidant activity in seawed fermented with lactic acid bacteria. Food Res. 2021, 5, 7-13. https://doi.org/10.26656/fr.2017.5(s3).006

13. Dey TB, Kuhad RC. Enhanced production and extraction of phenolic compounds from wheat by solid-state fermentation with Rhizopus oryzae RCK2012. Biotechnology Reports. 2014, 4, 120-127. https://doi.org/10.1016/j.btre.2014.09.006

14. Xiao Y, Xing G, Rui X, Li W, Chen X, Jiang M, et al. Enhancement of the antioxidant capacity of chickpeas by solid state fermentation with Cordyceps militaris SN-18. Journal of functional foods. 2014, 10, 210-222. https://doi.org/10.1016/j.jff.2014.06.008

15. Purbosari N, Warsiki E, Syamsu K, Santoso J. The potential of Eucheuma cottonii extract as a candidate for fish anesthetic agent. Aquaculture and Fisheries. 2022, 7, 427-432. https://doi.org/10.1016/j.aaf.2021.06.003

16. Purbosari N, Warsiki E, Syamsu K, Santoso J. Effect of Harvest Age and Solvents on the Phenolic Content of Eucheuma cot-tonii Extract. Makara Journal of Science. 2020, 24, 141-147. https://doi.org/10.7454/mss.v24i3.1177

17. Zhang S, Hu X, Ma J, Ma Z, Liu X, Cui L. Study on feed fermented from seaweed waste. African Journal of Microbiology Research. 2012, 6, 7610-7615. https://doi.org/10.5897/ajmr12.2439

18. Wang Y, Wu J, Lv M, Shao Z, Hungwe M, Wang J, et al. Metabolism characteristics of lactic acid bacteria and the expanding applications in food industry. Frontiers in bioengineering and biotechnology. 2021, 1-19. https://doi.org/10.3389/fbioe.2021.612285

19. Naczk M, Shahidi F. Extraction and analysis of phenolics in food. Journal of chromatography A. 2004, 1054, 95-111. https://doi.org/10.1016/s0021-9673(04)01409-8

20. Rodríguez H, Curiel JA, Landete JM, de las Rivas B, de Felipe FL, Gómez-Cordovés C, et al. Food phenolics and lactic acid bacteria. International journal of food microbiology. 2009, 132, 79-90. https://doi.org/10.1016/j.ijfoodmicro.2009.03.025

21. Shahidi F, Yeo J. Insoluble-bound phenolics in food. Molecules. 2016, 21, 1-22. https://doi.org/10.3390/molecules21091216

22. Kaprasob R, Kerdchoechuen O, Laohakunjit N, Sarkar D, Shetty K. Fermentation-based biotransformation of bioactive phenolics and volatile compounds from cashew apple juice by select lactic acid bacteria. Process Biochemistry. 2017, 59, 141-149. https://doi.org/10.1016/j.procbio.2017.05.019

23. Saputri RK, Setiawan B, Nugrahenny D, Kania N, Wahyuni ES, Widodo MA. The effects of Eucheuma cottonii on alveolar macrophages and malondialdehyde levels in bronchoalveolar lavage fluid in chronically particulate matter 10 coal dust-exposed rats. Iranian Journal of Basic Medical Sciences. 2014, 17, 541-545.

24. Kim D-O, Lee KW, Lee HJ, Lee CY. Vitamin C equivalent antioxidant capacity (VCEAC) of phenolic phytochemicals. Journal of Agricultural and food chemistry. 2002, 50, 3713-3717. https://doi.org/10.1021/jf020071c

25. Wang Z, Zhao C, Guo Z, Li S, Zhu Z, Grimi N, et al. Fermentation of Betaphycus gelatinum Using Lactobacillus brevis: Growth of Probiotics, Total Polyphenol Content, Polyphenol Profile, and Antioxidant Capacity. Foods. 2023, 12, 1-16. https://doi.org/10.3390/foods12183334

26. Matanjun P, Mohamed S, Mustapha NM, Muhammad K. Nutrient content of tropical edible seaweeds, Eucheuma cottonii, Caulerpa lentillifera and Sargassum polycystum. Journal of Applied Phycology. 2009, 21, 75-80. https://doi.org/10.1007/s10811-008-9326-4

27. Turgeon SL, Gauthier SF, Paquin P. Interfacial and emulsifying properties of whey peptide fractions obtained with a two-step ultrafiltration process. Journal of Agricultural and Food chemistry. 1991, 39, 673-676. https://doi.org/10.1021/jf00004a009

28. Elias RJ, Kellerby SS, Decker EA. Antioxidant activity of proteins and peptides. Critical reviews in food science and nutrition. 2008, 48, 430-441. https://doi.org/10.1080/10408390701425615

29. Muhialdin BJ, Rani NFA, Hussin ASM. Identification of antioxidant and antibacterial activities for the bioactive peptides generated from bitter beans (Parkia speciosa) via boiling and fermentation processes. Lwt. 2020, 131, 1-7. https://doi.org/10.1016/j.lwt.2020.109776

30. Makkar HP, Siddhuraju P, Becker K. Plant secondary metabolites. Springer, 2007; pp. 1-122.https://doi.org/10.1007/978-1-59745-425-4

31. Rocha de Souza MC, Marques CT, Guerra Dore CM, Ferreira da Silva FR, Oliveira Rocha HA, Leite EL. Antioxidant activities of sulfated polysaccharides from brown and red seaweeds. Journal of applied phycology. 2007, 19, 153-160. https://doi.org/10.1007/s10811-006-9121-z

32. Zhao Y, Li Q, Wang M, Wang Y, Piao C, Yu H, et al. Structural characterization of polysaccharides after fermentation from Ganoderma lucidum and its antioxidant activity in HepG2 cells induced by H2O2. Food Chemistry: X. 2023, 18, 1-13. https://doi.org/10.1016/j.fochx.2023.100682

33. Rizwan S, ReddySekhar P, MalikAsrar B. Reactive oxygen species in inflammation and tissue injury. Antioxidants & redox signaling. 2014, 1126-1167. https://doi.org/10.1089/ars.2012.5149

34. Hu Y-P, Peng Y-B, Zhang Y-F, Wang Y, Yu W-R, Yao M, et al. Reactive oxygen species mediated prostaglandin E2 contributes to acute response of epithelial injury. Oxidative medicine and cellular longevity. 2017, 2017, 1-8. https://doi.org/10.1155/2017/4123854

35. Smith WL, DeWitt DL, Garavito RM. Cyclooxygenases: structural, cellular, and molecular biology. Annual review of biochemistry. 2000, 69, 145-182. https://doi.org/10.1146/annurev.biochem.69.1.145

36. Li Y, Pu D, Li Y. The expression of cyclooxygenase-2 in cervical cancers and Hela cells was regulated by estrogen/progestogen. Journal of Huazhong University of Science and Technology. 2007, 27, 457-460. https://doi.org/10.1007/s11596-007-0428-z

37. Ahmad N, Mukhtar H. Antioxidants meet molecular targets for cancer prevention and therapeutics. Antioxid Redox Signal. 2013, 19, 85-88. https://doi.org/10.1089/ars.2013.5299

38. Prasasty VD, Haryani B, Hutagalung RA, Mulyono N, Yazid F, Rosmalena R, et al. Evaluation of antioxidant and antidiabetic activities from red seaweed (Eucheuma cottonii). Systematic Reviews in Pharmacy. 2019, 10, 276-288.

39. Zhang Y, Luo L, Han C, Lv H, Chen D, Shen G, et al. Design, synthesis, and biological activity of tetrahydrobenzo [4, 5] thieno [2, 3-d] pyrimidine derivatives as anti-inflammatory agents. Molecules. 2017, 22, 1-21. https://doi.org/10.3390/molecules22111960

40. Kryshchyshyn A, Roman O, Lozynskyi A, Lesyk R. Thiopyrano [2, 3-d] thiazoles as new efficient scaffolds in medicinal chemistry. Scientia Pharmaceutica. 2018, 86, 1-24. https://doi.org/10.3390/scipharm86020026

41. Muthulakshmi A, Mohan V. GC-MS analysis of bioactive components of Feronia elephantum Correa (Rutaceae). Journal of Applied Pharmaceutical Science. 2012, 69-74.

42. Johnson TO, Odoh KD, Nwonuma CO, Akinsanmi AO, Adegboyega AE. Biochemical evaluation and molecular docking assessment of the anti-inflammatory potential of Phyllanthus nivosus leaf against ulcerative colitis. Heliyon. 2020, 6, 1-10. https://doi.org/10.1016/j.heliyon.2020.e03893

43. Mun OJ, Kwon MS, Karadeniz F, Kim M, Lee SH, Kim YY, et al. Fermentation of Sargassum thunbergii by Kimchi‐Derived Lactobacillus sp. SH‐1 Attenuates LPS‐Stimulated Inflammatory Response Via Downregulation of JNK. Journal of Food Biochemistry. 2017, 41, 1-9. https://doi.org/10.1111/jfbc.12306

44. Di Domenico F, Foppoli C, Coccia R, Perluigi M. Antioxidants in cervical cancer: chemopreventive and chemotherapeutic effects of polyphenols. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease. 2012, 1822, 737-747. https://doi.org/10.1016/j.bbadis.2011.10.005

45. Chen L, Deng H, Cui H, Fang J, Zuo Z, Deng J, et al. Inflammatory responses and inflammation-associated diseases in organs. Oncotarget. 2018, 9, 7204-7218. https://doi.org/10.18632/oncotarget.23208

46. Satomi Y, Nishino H. Implication of mitogen-activated protein kinase in the induction of G1 cell cycle arrest and gadd45 expression by the carotenoid fucoxanthin in human cancer cells. Biochimica et Biophysica Acta (BBA)-General Subjects. 2009, 1790, 260-266. https://doi.org/10.1016/j.bbagen.2009.01.003

47. Lee J, Wang J, Ng K, Tan C, Rabina P, Teo S. In-vitro anticancer activity of Eucheuma cottonii extracts against HeLa cell line, humn lung carcinoma cell line (SK-LU-1), human colon carcinoma cell line (HCT-116), and fibroblast. IJCMS. 2015, 1, 69-73.

48. Arsianti A, Fadilah F, Fatmawaty Y, Wibisono L, Kusmardi S, Azizah N, et al. Phytochemical composition and anticancer activity of seaweeds Ulva lactuca and Eucheuma cottonii against breast MCF-7 and colon HCT-116 cells. Asian J Pharm Clin Res. 2016, 9, 115-119. https://doi.org/10.22159/ajpcr.2016.v9i6.13798

49. Singh N, Ranjana R, Kumari M, Kumar B. A review on biological activities of hydrazone derivatives. Int J Pharm Clin Res. 2016, 8, 162-166.

50. Karrouchi K, Radi S, Ramli Y, Taoufik J, Mabkhot YN, Al-Aizari FA, et al. Synthesis and pharmacological activities of pyrazole derivatives: A review. Molecules. 2018, 23, 1-86. https://doi.org/10.3390/molecules23010134

Downloads

Published

2024-09-15

How to Cite

Aminin, A. L. N., Anggraeni, E., Ramoza, S. A., Suzery, M., Cahyono, B., & Eghdami, A. (2024). Radical-Scavenging and Anti-inflammatory Activities of Fermented Eucheuma cottonii from Lombok. BioNatura Journal: Ibero-American Journal of Biotechnology and Life Sciences, 1(3), 12. https://doi.org/10.70099/BJ/2024.01.03.18

Issue

Section

Research Articles

Categories