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Journal of Applied Phycology

, Volume 31, Issue 2, pp 1333–1341 | Cite as

Seasonal effects on antioxidant and anti-HIV activities of Brazilian seaweeds

  • Janaína Pires SantosEmail author
  • Priscila Bezerra Torres
  • Déborah Y. A. C. dos Santos
  • Lucimar B. Motta
  • Fungyi Chow
Article

Abstract

In recent years phytotherapy has been encouraged by Brazilian government agencies and has gained more and more credibility as a way of alternative therapy to complement allopathy. Although little explored in Brazil, seaweeds are promising marine bioresources as herbal medicine. In this context, the aim of the present study was to evaluate the antioxidant activities and reverse transcriptase inhibition (RT-HIV) of crude extracts (methanolic, aqueous, and hot aqueous) from three abundant species in Brazilian rocky shores, Sargassum vulgare (Ochrophyta), Palisada flagellifera (Rhodophyta), and Ulva fasciata (Chlorophyta), under two seasons (dry and rainy). Methanolic extracts from S. vulgare (EC50 = 18.22 ± 2.91 μg mg−1, dry), P. flagellifera (EC50 = 24.85 ± 3.13 μg mg−1, rainy), and U. fasciata (EC50 = 33.41 ± 1.53 μg mg−1, dry) showed the highest β-carotene bleaching activities, while hot aqueous extracts from S. vulgare showed the highest RT-HIV inhibition and antioxidant activities in ABTS, FRAP, and Folin-Ciocalteu assays. In general, the three macroalgae showed considerable antioxidant effects; however, only S. vulgare showed an anti-HIV potential (IC50 10.15 ± 1.77 mg mL−1 for the dry season and IC50 = 22.41 ± 5.74 μg mL−1 for rainy season). Regarding both extract yields and bioactivities, S. vulgare in the rainy season was the most promising alga. In conclusion, the studied seaweeds may be an effective alternative for Brazilian herbal medicine; additionally, seasonal studies are essential, since there were significant differences mainly for extract yields.

Keywords

Anti-HIV Antioxidants Biotechnology Seasonality Seaweeds 

Notes

Acknowledgements

The authors thank Dr. Beatriz Torrano da Silva, Marizete Pereira dos Santos, and CEPLAC (Comissão Executiva de Planejamento da Lavoura Cacaueira) for research cooperation.

Funding information

The authors would like to thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) and FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo (Biota/Fapesp 2013/50731-1) for financial support. FC thanks CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for the productivity fellowship (Proc. 303937/2015-7).

References

  1. Almeida CL, Falcão HS, Lima GR, Montenegro CA, Lira NS, de Athayde-Filho PF, Rodrigues LC, De Souza MFV, Barbosa-Filho JM, Batista LM (2011) Bioactivities from marine algae of the genus Gracilaria. Int J Mol Sci 12:4550–4573CrossRefGoogle Scholar
  2. Anwar H, Hussain G, Mustafa I (2018) Antioxidants from natural sources. In: Shalaby E, Azzam GM (eds) Antioxidants in foods and its applications. IntechOpen. https://www.intechopen.com/books/antioxidants-in-foods-and-itsapplications/antioxidants-from-natural-sources. Accessed 2 Sept 2018
  3. Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76CrossRefGoogle Scholar
  4. Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT - Food Sci Technol 28:25–30CrossRefGoogle Scholar
  5. Brown EM, Allsopp PJ, Magee PJ, Gill CIR, Nitecki S, Strain CR, McSorley EM (2014) Seaweed and human health. Nutr Rev 72:205–216CrossRefGoogle Scholar
  6. Cerri GG (2016) The challenges of health care in Brazil. Rev Med 95(60):60Google Scholar
  7. Chew YL, Lim YY, Omar M, Khoo KS (2008) Antioxidant activity of three edible seaweeds from two areas in South East Asia. LWT - Food Sci Technol 41:1067–1072CrossRefGoogle Scholar
  8. Cornish ML, Garbary DJ (2010) Antioxidants from macroalgae: potential applications in human health and nutrition. Algae 25:155–171CrossRefGoogle Scholar
  9. Craigie JS, MacKinnon SL, Walter JA (2008) Liquid seaweed extracts identified using 1H NMR profiles. J Appl Phycol 20:665–671CrossRefGoogle Scholar
  10. Cutler B, Justman J (2008) Vaginal microbicides and the prevention of HIV transmission. Lancet Infect Dis 8:685–697CrossRefGoogle Scholar
  11. Devasagayam TPA, Tilak JC, Boloor KK, Sane KS, Ghaskadbi SS, Lele RD (2004) Free radicals and antioxidants in human health: current status and future prospects. J Assoc Physicians India 52:794–804Google Scholar
  12. Dinesh S, Menon T, Hanna LE, Suresh V, Sathuvan M, Manikannan M (2016) In vitro anti-HIV-1 activity of fucoidan from Sargassum swartzii. Int J Biol Macromol 82:83–88CrossRefGoogle Scholar
  13. Fleurence J, Levine I (eds) (2016) Seaweed in health and disease prevention. Elsevier, Amsterdam, p 476Google Scholar
  14. Guiry MD, Blunden G (1991) Seaweed resources in Europe: uses and potential. Wiley, ChichesterGoogle Scholar
  15. Gülçin I (2012) Antioxidant activity of food constituents: an overview. Arch Toxicol 86:345–391CrossRefGoogle Scholar
  16. Gupta S, Abu-Ghannam N (2011) Recent developments in the application of seaweeds or seaweed extracts as a means for enhancing the safety and quality attributes of foods. Innov Food Sci Emerg Technol 12:600–609CrossRefGoogle Scholar
  17. Hamed I, Özogul F, Özogul Y, Regenstein JM (2015) Marine bioactive compounds and their health benefits: a review. Compr Rev Food Sci Food Saf 14:446–465CrossRefGoogle Scholar
  18. Harb TB, Torres PB, Pires JP, Santos DYAC, Chow F (2016) Ensaio em microplaca do potencial antioxidante através do sistema quelante de metais para extratos de algas. Instituto de Biociências, Universidade de São Paulo, São Paulo. Retrieved from http://www2.ib.usp.br/index.php?option=com_docman&task=doc_view&gid=67&tmpl=component&format=raw&Itemid=98 on 06 May 2018
  19. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597CrossRefGoogle Scholar
  20. Holec AD, Mandal S, Prathipati PK, Destache CJ (2018) Nucleotide reverse transcriptase inhibitors: a thorough review, present status and future perspective as HIV therapeutics. Curr HIV Res 15:411–421CrossRefGoogle Scholar
  21. Huynh QN, Nguyen HD (1998) The seaweed resources of Vietnam. In: Critchley AT, Ohno M (eds) Seaweed resources of the world. JICA:62–69Google Scholar
  22. Jeong JH, Jung H, Lee SR, Lee HJ, Hwang KT, Kim TY (2010) Anti-oxidant, anti-proliferative and anti-inflammatory activities of the extracts from black raspberry fruits and wine. Food Chem 123:338–344CrossRefGoogle Scholar
  23. Jeong SC, Jeong YT, Lee SM, Kim JH (2015) Immune-modulating activities of polysaccharides extracted from brown algae Hizikia fusiforme. Biosci Biotechnol Biochem 79:1362–1365CrossRefGoogle Scholar
  24. Kasrati A, Jamali CA, Abbad A (2017) Antioxidant properties of various extracts from selected wild Moroccan aromatic and medicinal species. Trends Phytochem Res 1:175–182Google Scholar
  25. Kohen R, Nyska A (2002) Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol 30:620–650CrossRefGoogle Scholar
  26. Lage MÁP, García MAM, Álvarez JAV, Anders Y, Curran TP (2013) A new microplate procedure for simultaneous assessment of lipophilic and hydrophilic antioxidants and pro-oxidants, using crocin and β-carotene bleaching methods in a single combined assay: tea extracts as a case study. Food Res Int 53:836–846CrossRefGoogle Scholar
  27. Lordan S, Ross RP, Stanton C (2011) Marine bioactives as functional food ingredients: potential to reduce the incidence of chronic diseases. Mar Drugs 9:1056–1100CrossRefGoogle Scholar
  28. Loutfy MR, Wu W, Letchumanan M, Bondy L, Antoniou T, Margolese S, Zhang Y, Rueda S, McGee F, Peck R, Binder L, Allard P, Rourke SB, Ronchon PA (2013) Systematic review of HIV transmission between heterosexual serodiscordant couples where the HIV-positive partner is fully suppressed on antiretroviral therapy. PLoS One 8:e55747CrossRefGoogle Scholar
  29. Mahapatra A, Tshikalange TE, Meyer JJM, Lall N (2012) Synthesis and HIV-1 reverse transcriptase inhibition activity of 1,4-naphoquinone derivatives. Chem Nat Compd 47:776–779CrossRefGoogle Scholar
  30. Marco G (1968) A rapid method for evaluation of antioxidants. J Am Oil Chem Soc 45:594–598CrossRefGoogle Scholar
  31. Matanjun P, Mohamed S, Mustapha NM, Muhammad K, Ming CH (2008) Antioxidant activities and phenolics content of eight species of seaweeds from north Borneo. J Appl Phycol 20:367–373CrossRefGoogle Scholar
  32. Miliauskas G, Venskutonis PR, Van Beek TA (2004) Screening of radical scavenging activity of some medicinal and aromatic plant extracts. Food Chem 85:231–237CrossRefGoogle Scholar
  33. Miller HE (1971) A simplified method for the evaluation of antioxidants. J Am Oil Chem Soc 48:91–91CrossRefGoogle Scholar
  34. Min B, McClung AM, Chen MH (2011) Phytochemicals and antioxidant capacities in rice brans of different color. J Food Sci 76:C117–C126CrossRefGoogle Scholar
  35. Mols-Mortensen A, Ortind EG, Jacobsen C, Holdt SL (2017) Variation in growth, yield and protein concentration in Saccharina latissima (Laminariales, Phaeophyceae) cultivated with different wave and current exposures in the Faroe Islands. J Appl Phycol 29:2277–2286CrossRefGoogle Scholar
  36. Myers SP, O’Connor J, Fitton JH, Brooks L, Rolfe M, Connellan P, Wohlmuth H, Cheras P, Morris C (2010) A combined phase I and II open label study on the effects of a seaweed extract nutrient complex on osteoarthritis. Biol Targets Ther 4:33–44CrossRefGoogle Scholar
  37. Nwobike JC (2006) Pharmaceutical corporations and access to drugs in developing countries: the way forward. Int J Hum Rights 4:126–143Google Scholar
  38. Orisatoki RO, Oguntibeju OO (2010) The role of herbal medicine use in HIV/AIDS treatment. Arch Clin Microbiol 1(3)Google Scholar
  39. Pires JS, Torres PB, Santos DYAC, Chow F (2017a) Ensaio em microplaca de substâncias redutoras pelo método do Folin-Ciocalteu para extratos de algas. Instituto de Biociências, Universidade de São Paulo, São Paulo. Retrieved from http://www2.ib.usp.br/index.php?option=com_docman&task=doc_view&gid=73&tmpl=component&format=raw&Itemid=98 on 06 May 2018
  40. Pires J, Torres PB, Santos DYAC dos Chow F (2017b) Ensaio em microplaca do potencial antioxidante através do método de sequestro do radical livre DPPH para extratos de algas. Instituto de Biociências, Universidade de São Paulo, São Paulo. Retrieved from http://www2.ib.usp.br/index.php?option=com_docman&task=doc_view&gid=72&tmpl=component&format=raw&Itemid=98 on 06 May 2018
  41. Pirian K, Moein S, Sohrabipour J, Rabiei R, Blomster J (2017) Antidiabetic and antioxidant activities of brown and red macroalgae from the Persian Gulf. J Appl Phycol 29:3151–3159CrossRefGoogle Scholar
  42. Rajan S, Mahalakshmi S, Deepa VM, Sathya K, Shajitha S, Thirunalasundari T (2011) Antioxidant potentials of Punica granatum fruit rind extracts. Int J Pharm Pharm Sci 3:82–88Google Scholar
  43. Rosa C, Câmara SG, Béria JU (2011) Representações e intenção de uso da fitoterapia na atenção básica à saúde. Cien Saude Colet 16:311–318CrossRefGoogle Scholar
  44. Rufino MSM, Alves RE, Brito ES, Morais SM, Sampaio CG, Pérez-Jimenez J, Saura-Calixto FD (2007) Metodologia científica: determinação da atividade antioxidante total em frutas pela captura do radical livre ABTS•+ Embrapa, FortalezaGoogle Scholar
  45. Ruzagira E, Wandiembe S, Abaasa A, Bwanika AN, Bahemuka U, Amornkul P, Price MA, Grosskurth H, Kamali A (2011) HIV incidence and risk factors for acquisition in HIV discordant couples in Masaka, Uganda: an HIV vaccine preparedness study. PLoS One 6(8):e0024037CrossRefGoogle Scholar
  46. Saunders GW (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Phil Trans Roy Soc B 360:1879–1888CrossRefGoogle Scholar
  47. Sekmokienė D, Liutkevičius A, Malakauskas M (2007) Functional food and its ingredients. Vet Zoot 37:72–78Google Scholar
  48. Stengel DB, Connan S, Popper ZA (2011) Algal chemodiversity and bioactivity: sources of natural variability and implications for commercial application. Biotechnol Adv 29:483–501CrossRefGoogle Scholar
  49. Suresh Kumar K, Ganesan K, Subba Rao PV (2015) Seasonal variation in nutritional composition of Kappaphycus alvarezii (Doty) Doty—an edible seaweed. J Food Sci Technol 52:2751–2760CrossRefGoogle Scholar
  50. Teas J, Irhimeh MR (2012) Dietary algae and HIV/AIDS: proof of concept clinical data. J Appl Phycol 24:575–582CrossRefGoogle Scholar
  51. Teas J, Hebert JR, Fitton JH, Zimba PV (2004) Algae—a poor man’s HAART? Med Hypotheses 62:507–510CrossRefGoogle Scholar
  52. Torres PB, Pires JS, Santos DYAC, Chow F (2017) Ensaio do potencial antioxidante de extratos de algas através do sequestro do ABTS•+ em microplaca. Instituto de Biociências, Universidade de São Paulo, São Paulo. Retrieved from http://www2.ib.usp.br/index.php?option=com_docman&task=doc_view&gid=74&tmpl=component&format=raw&Itemid=98 on 06 May 2018
  53. Unaids (2013) Global report: UNAIDS report on the global AIDS epidemic 2013. Retrieved from http://www.unaids.org/sites/default/files/media_asset/UNAIDS_Global_Report_2013_en_1.pdf on 08 May 2018
  54. Urrea-Victoria V, Pires J, Torres PB, Santos DYAC, Chow F (2016) Ensaio antioxidante em microplaca do poder de redução do ferro (FRAP) para extratos de algas. Instituto de Biociências, Universidade de São Paulo, São Paulo. Retrieved from http://www2.ib.usp.br/index.php?option=com_docman&task=doc_view&gid=66&tmpl=component&format=raw&Itemid=98 on 06 May 2018
  55. Verkleij FN (1992) Seaweed extracts in agriculture and horticulture: a review. Biol Agric Hortic 8:309–324CrossRefGoogle Scholar
  56. Vieira C, Gaubert J, De Clerck O, Payri C, Culioli G, Thomas OP (2017) Biological activities associated to the chemodiversity of the brown algae belonging to genus Lobophora (Dictyotales, Phaeophyceae). Phytochem Rev 16:1–17CrossRefGoogle Scholar
  57. Wang B, Huang H, Xiong HP, Xie EY, Li ZM (2010) Analysis on nutrition constituents of Sargassum naozhouense sp.nov Food Res Dev 31:195–197Google Scholar
  58. Waterman PG, Mole S (1994) Extraction and chemical quantification. In: Analysis of phenolic plant metabolites. Wiley Blackwell, pp 333–360Google Scholar
  59. Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH (2017) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29:949–982CrossRefGoogle Scholar
  60. Woradulayapinij W, Soonthornchareonnon N, Wiwat C (2005) In vitro HIV type 1 reverse transcriptase inhibitory activities of Thai medicinal plants and Canna indica L. rhizomes. J Ethnopharmacol 101:84–89CrossRefGoogle Scholar
  61. World Health Organization (2005) WHO Traditional Medicine Strategy 2002–2005. World Health Organization, Geneva. Retrieved from http://www.wpro.who.int/health_technology/book_who_traditional_medicine_strategy_2002_2005.pdf on 06 May 2018
  62. World Health Organization (2007) Countries at the core. WHO Medicines Strategy 2004–2007 1–12. World Health Organization, Geneva. Retrieved from http://www.who.int/management/background_4a.pdf on 07 August 2018
  63. Yermak IM, Sokolova EV, Davydova VN, Solov’eva TF, Aminin DL, Reunov AV, Lapshina LA (2016) Influence of red algal polysaccharides on biological activities and supramolecular structure of bacterial lipopolysaccharide. J Appl Phycol 28:619–627CrossRefGoogle Scholar
  64. Zubia M, Robledo D, Freile-Pelegrin Y (2007) Antioxidant activities in tropical marine macroalgae from the Yucatan Peninsula, Mexico. J Appl Phycol 19:449–458CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.University of São PauloInstitute of BiosciencesSão PauloBrazil

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