Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter January 29, 2020

Immune stimulatory and anti-HIV-1 potential of extracts derived from marine brown algae Padina tetrastromatica

  • Dinesh Subramaniam EMAIL logo , Luke Elizabeth Hanna EMAIL logo , Kuppusamy Maheshkumar , Karuppiah Ponmurugan , Naif Abdullah Al-Dhabi and P. Murugan

Abstract

Background

Marine brown algae are biologically diverse and their medicinal value has been explored limited. We assessed whether Padina tetrastromatica Hauck will possess the immune stimulatory and human immunodeficiency virus (HIV-1) inhibitory activity.

Materials and Methods

Aqueous and methanolic extracts were tested for the Th1/Th2 cytokines using PBMC. Subsequently, leukotriene B4 (LTB4), nitric oxide (NO) and anti-oxidant effect were analyzed using RAW264.7 cells. In addition, Padina extracts were tested for the HIV-1 clade C & A by measuring the levels of viral p24 antigen in infected peripheral blood mononuclear cells (PBMCs) and against reverse transcriptase (RT).

Results

At 100 μg/mL, aqueous and methanolic extracts produced a significant amount of IL-10 and IFN-γ at 24 h and 72 h post-stimulation by PBMCs. It also produced a significant amount of LTB4, NO and had an antioxidant effect on RAW264.7 cell, suggesting the immune stimulating potential of P. tetrastromatica. Upon infection of PBMCs with 100 TCID50, aqueous and methanolic extracts of P. tetrastromatica inhibited HIV-1 C (>90%) and HIV-1 A (>50%) showed a significant reduction in HIV-1 p24 levels and HIV-1 RT inhibition (>50%). GC-MS study revealed a relative abundance of tetradecanoic and oleic acid in the methanolic extract of P. tetrastromatica, which might be responsible for immune stimulation and anti-HIV-1 activity.

Conclusion

At lower concentrations (100 mg/mL), the aqueous and methanolic extracts of P. tetrastromatica showed the strong immune stimulation and greatest anti-HIV-1 potential in vitro. This study demonstrates the therapeutic potential of these brown algae P. tetrastromatica for the benefit of mankind.

Acknowledgments

The authors would like to acknowledge Dr Soumya Swaminathan, Scientist G, Former Director, Clinical Research (HIV & TB), National Institute for Research in Tuberculosis (NIRT), Chetpet, Chennai, TN, India to utilize the laboratory facilities.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: None declared.

  3. Employment or leadership: None declared.

  4. Honorarium: None declared.

  5. Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.

Abbreviations

PBS, Phosphate buffer saline; FBS, fetal bovine serum; RPMI, Rosewell park memorial institute; DMEM, Dulbecco’s Modified Eagle’s Medium, ELISA, Enzyme linked immunosorbent assay; LTB4, Leukotriene B4; NO, nitric oxide; DPPH, 2,2-Diphenyl-1-picryl-hydrazyl; TCID50, Tissue culture infectious dose 50; HIV/AIDS, Human Immunodeficiency virus/acquired immunodeficiency syndrome; AZT, azidothymidine.

References

[1] Sanjeewa KK, Kang N, Ahn G, Jee Y, Kim Y-T, Jeon Y-J. Bioactive potentials of sulfated polysaccharides isolated from brown seaweed Sargassum spp in related to human health applications: a review. Food Hydrocoll 2018;81:200–8.10.1016/j.foodhyd.2018.02.040Search in Google Scholar

[2] Sanjeewa KA, Lee JS, Kim W-S, Jeon Y-J. The potential of brown-algae polysaccharides for the development of anticancer agents: an update on anticancer effects reported for fucoidan and laminaran. Carbohydr Polym 2017;177:451–9.10.1016/j.carbpol.2017.09.005Search in Google Scholar

[3] Wang C-Y, Wu T-C, Hsieh S-L, Tsai Y-H, Yeh C-W, Huang C-Y. Antioxidant activity and growth inhibition of human colon cancer cells by crude and purified fucoidan preparations extracted from Sargassum cristaefolium. J Food Drug Anal 2015;23:766–77.10.1016/j.jfda.2015.07.002Search in Google Scholar

[4] Wu L, Sun J, Su X, Yu Q, Yu Q, Zhang P. A review about the development of fucoidan in antitumor activity: progress and challenges. Carbohydr Polym 2016;154:96–111.10.1016/j.carbpol.2016.08.005Search in Google Scholar

[5] Gutiérrez-Rodríguez AG, Juárez-Portilla C, Olivares-Bañuelos T, Zepeda RC. Anticancer activity of seaweeds. Drug Discov Today 2017;23:434–47.10.1016/j.drudis.2017.10.019Search in Google Scholar

[6] Patel S. Seaweed-derived sulfated polysaccharides: scopes and challenges in implication in health care. Bioact Seaweeds Food Appl 2018;1:71–93.10.1016/B978-0-12-813312-5.00004-2Search in Google Scholar

[7] Plantier JC, Leoz M, Dickerson JE, De Oliveira F, Cordonnier F, Lemée V, et al. A new human immunodeficiency virus derived from gorillas. Nat Med 2009;15:871.10.1038/nm.2016Search in Google Scholar

[8] Hemelaar J, Gouws E, Ghys PD, Osmanov S. Global and regional distribution of HIV-1 genetic subtypes and recombinants in 2004. Aids 2006;20:13–23.10.1097/01.aids.0000247564.73009.bcSearch in Google Scholar

[9] Senevirathne M, Kim SH, Siriwardhana N, Ha JH, Lee KW, Jeon YJ. Antioxidant potential of ecklonia cavaon reactive oxygen species scavenging, metal chelating, reducing power and lipid peroxidation inhibition. Food Sci Technol Int 2006;12:27–38. 10.1177/1082013206062422Search in Google Scholar

[10] Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl 1968;97:77–89.Search in Google Scholar

[11] Chi YS, Lim H, Park H, Kim HP. Effects of wogonin, a plant flavone from Scutellaria radix, on skin inflammation: in vivo regulation of inflammation-associated gene expression. Biochem Pharmacol 2003;66:1271–8.10.1016/S0006-2952(03)00463-5Search in Google Scholar

[12] Leiro JM, Castro R, Arranz JA, Lamas J. Immunomodulating activities of acidic sulphated polysaccharides obtained from the seaweed Ulva rigida C. Agardh Int Immunopharmacol 2007;7:879–88.10.1016/j.intimp.2007.02.007Search in Google Scholar

[13] Lee S-A, Hong S-K, Suh C-I, Oh M-H, Park J-H, Choi B-W, et al. Anti-HIV-1 efficacy of extracts from medicinal plants. J Microbiol 2010;48:249–52.10.1007/s12275-009-0176-9Search in Google Scholar

[14] Suresh V, Senthilkumar N, Thangam R, Rajkumar M, Anbazhagan C, Rengasamy R, et al. Separation, purification and preliminary characterization of sulfated polysaccharides from Sargassum plagiophyllum and its in vitro anticancer and antioxidant activity. Process Biochem 2013;48:364–73.10.1016/j.procbio.2012.12.014Search in Google Scholar

[15] Mosmann TR, Sad S. The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today 1996;17:138–46.10.1016/0167-5699(96)80606-2Search in Google Scholar

[16] Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F. Colorimetric method for determination of sugars and related substances. Anal Chemistry 1956;28:350–6.10.1021/ac60111a017Search in Google Scholar

[17] Dodgson K, Price R. A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochem J 1962;84:106.10.1042/bj0840106Search in Google Scholar

[18] Filisetti-Cozzi TM, Carpita NC. Measurement of uronic acids without interference from neutral sugars. Anal Biochem 1991;197:157–62.10.1016/0003-2697(91)90372-ZSearch in Google Scholar

[19] Jin B, Sun T, Yu X-H, Yang Y-X, Yeo AE. The effects of TLR activation on T-cell development and differentiation. Clin Dev Immunol 2012:1–32.10.1155/2012/836485Search in Google Scholar PubMed PubMed Central

[20] Schepetkin IA, Kouakou K, Yapi A, Kirpotina LN, Jutila MA, Quinn MT. Immunomodulatory and hemagglutinating activities of acidic polysaccharides isolated from Combretum racemosum. Int Immunopharmacol 2013;15:628–37.10.1016/j.intimp.2013.01.015Search in Google Scholar PubMed PubMed Central

[21] Ashalatha K, Venkateswarlu Y, Priya AM, Lalitha P, Krishnaveni M, Jayachandran S. Anti inflammatory potential of Decalepis hamiltonii (Wight and Arn) as evidenced by down regulation of pro inflammatory cytokines—TNF-α and IL-2. J Ethnopharmacol 2010;130:167–70.10.1016/j.jep.2010.04.022Search in Google Scholar PubMed

[22] Yeap SK, Alitheen NB, Ho WY, Omar AR, Ali AM, Beh BK, et al. Immunomodulatory role of Rhaphidophora korthalsii methanol extract on human peripheral blood mononuclear cell proliferation, cytokine secretion and cytolytic activity. J Med Plants Res 2011;5:958–65.Search in Google Scholar

[23] Chevrier MR, Ryan AE, Lee DY, Zhongze M, Wu-Yan Z, Via CS. Boswellia carterii extract inhibits TH1 cytokines and promotes TH2 cytokines in vitro. Clin Diag Lab Immunol 2005;12:575–80.10.1128/CDLI.12.5.575-580.2005Search in Google Scholar PubMed PubMed Central

[24] Huang R, Lee H-T. Immunological properties of the marine brown alga endarachne binghamiae (Phaeophyceae). Int J Appl Sci Eng 2005;3:167–73.Search in Google Scholar

[25] Lawrence T, Willoughby DA, Gilroy DW. Anti-inflammatory lipid mediators and insights into the resolution of inflammation. Nat Rev Immunol 2002;2:787.10.1038/nri915Search in Google Scholar PubMed

[26] Bertin J, Barat C, Bélanger D, Tremblay MJ. Leukotrienes inhibit early stages of HIV-1 infection in monocyte-derived microglia-like cells. J Neuroinflamm 2012;9:55.10.1186/1742-2094-9-55Search in Google Scholar PubMed PubMed Central

[27] Okamoto F, Saeki K, Sumimoto H, Yamasaki S, Yokomizo T. Leukotriene B4 augments and restores FcγRs-dependent phagocytosis in macrophages. J Biol Chem 2010;285:41113–21.10.1074/jbc.M110.175497Search in Google Scholar PubMed PubMed Central

[28] Jiang Z, Okimura T, Yamaguchi K, Oda T. The potent activity of sulfated polysaccharide, ascophyllan, isolated from Ascophyllum nodosum to induce nitric oxide and cytokine production from mouse macrophage RAW264. 7 cells: comparison between ascophyllan and fucoidan. Nitric Oxide 2011;25:407–15.10.1016/j.niox.2011.10.001Search in Google Scholar PubMed

[29] Xia L, Liu X, Guo H, Zhang H, Zhu J, Ren F. Partial characterization and immunomodulatory activity of polysaccharides from the stem of Dendrobium officinale (Tiepishihu) in vitro. J Funct Foods 2012;4:294–301.10.1016/j.jff.2011.12.006Search in Google Scholar

[30] Vinayak RC, Sabu A, Chatterji A. Bio-prospecting of a few brown seaweeds for their cytotoxic and antioxidant activities. Evid Based Complement Alternat Med 2011;2011:1–9.10.1093/ecam/neq024Search in Google Scholar PubMed PubMed Central

[31] Leteane MM, Ngwenya BN, Muzila M, Namushe A, Mwinga J, Musonda R, et al. Old plants newly discovered: Cassia sieberiana dc and Cassia abbreviata Oliv. Oliv. root extracts inhibit in vitro HIV-1c replication in peripheral blood mononuclear cells (PBMCs) by different modes of action. J Ethnopharmacol 2012;141:48–56.10.1016/j.jep.2012.01.044Search in Google Scholar PubMed

[32] Klos M, Van de Venter M, Milne P, Traore H, Meyer D, Oosthuizen V. In vitro anti-HIV activity of five selected South African medicinal plant extracts. J Ethnopharmacol 2009;124:182–8.10.1016/j.jep.2009.04.043Search in Google Scholar PubMed

[33] Artan M, Li Y, Karadeniz F, Lee SH, Kim MM, Kim SK. Anti-HIV-1 activity of phloroglucinol derivative, 6, 6’-bieckol, from Ecklonia cava. Bioorg Med Chem 2008;16:7921–6.10.1016/j.bmc.2008.07.078Search in Google Scholar PubMed

[34] Artan M, Karadeniz F, Karagozlu MZ, Kim M-M, Kim S-K. Anti-HIV-1 activity of low molecular weight sulfated chitooligosaccharides. Carbohydr Res 2010;345:656–62.10.1016/j.carres.2009.12.017Search in Google Scholar PubMed

[35] Forthal DN, Phan TB, Slepenkin AV, Landucci G, Chu H, Elofsson M, et al. In vitro anti-HIV-1 activity of salicylidene acylhydrazide compounds. Int J Antimicrob Agents 2012;40:354–60.10.1016/j.ijantimicag.2012.05.023Search in Google Scholar PubMed PubMed Central

[36] Ahn MJ, Yoon KD, Kim CY, Kim JH, Shin CG, Kim J. Inhibitory activity on HIV-1 reverse transcriptase and integrase of a carmalol derivative from a brown Alga, Ishige okamurae. Phytotherapy Res: Int J Devoted Pharmacol Toxicol Eval Nat Prod Derivatives 2006;20:711–3.10.1002/ptr.1939Search in Google Scholar PubMed

[37] Ahn G, Hwang I, Park E, Kim J, Jeon Y-J, Lee J, et al. Immunomodulatory effects of an enzymatic extract from Ecklonia cava on murine splenocytes. Marine Biotechnol 2008;10:278–89.10.1007/s10126-007-9062-9Search in Google Scholar PubMed

[38] Karmakar P, Pujol CA, Damonte EB, Ghosh T, Ray B. Polysaccharides from Padina tetrastromatica: Structural features, chemical modification and antiviral activity. Carbohydr Polym 2010;80:513–20.10.1016/j.carbpol.2009.12.014Search in Google Scholar

Received: 2019-03-12
Accepted: 2019-07-28
Published Online: 2020-01-29

© 2020 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 22.3.2023 from https://www.degruyter.com/document/doi/10.1515/jcim-2019-0071/html
Scroll Up Arrow