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Bioactive compounds against neglected diseases isolated from macroalgae: a review

  • VI REDEALGAS WORKSHOP (RIO DE JANEIRO, BRAZIL)
  • Published:
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Abstract

To survive in a very competitive environment, marine macroalgae had to evolve defense strategies, resulting in an enormous diversity of compounds from different metabolic pathways. These secondary metabolites have been explored by the pharmaceutical industries in order to generate new drugs to treat several diseases. Recent publications in drug research from natural sources have indicated algae as an interesting choice to provide novel drugs to fulfill this gap. This review highlights algal metabolites that showed bioactivities suggesting their potential against neglected diseases. Drug discovery for neglected diseases has been overlooked by the Big Pharmas, mainly because they affect poor people, most of them living in developing countries. Moreover, this review shows the commercial application of the most explored chemicals from algae such as terpenes, phenols, quinones, macrolides, alkaloids, lipids, chromones, and other related metabolites and an overview regarding the status of green extraction technologies for seaweeds and their concepts.

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References

  • Abdulla MH, Ruelas DS, Wolff B, Snedecor J, Lim KC, Xu F, Renslo AR, Williams J, McKerrow JH, Caffrey CR (2009) Drug discovery for schistosomiasis: hit and lead compounds identified in a library of known drugs by medium-throughput phenotypic screening. PLoS Negl Trop Dis 3:e478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Afolayan AF, Bolton JJ, Lategan CA, Smith PJ, Beukes DR (2008) Fucoxanthin, tetraprenylated toluquinone and toluhydroquinone metabolites from Sargassum heterophyllum inhibit the in vitro growth of the malaria parasite Plasmodium falciparum. Z Naturforsch C 63:848–852

    Article  CAS  PubMed  Google Scholar 

  • Albarelli JQ, Santos DT, Cocero MJ, Meireles MAA (2016) Economic analysis of an integrated annatto seeds-sugarcane biorefinery using supercritical CO2 extraction as a first step. Materials 9:494

    Article  PubMed Central  Google Scholar 

  • Anaelle T, Leon ES, Laurent V, Elena I, Mendiola JA, Stephane C, Nelly K, Stephane LB, Luc M, Valerie SP (2013) Green improved processes to extract bioactive phenolic compounds from brown macroalgae using Sargassum muticum as model. Talanta 104:44–52

    Article  CAS  PubMed  Google Scholar 

  • Awad NE (2004) Bioactive brominated diterpenes from the marine red alga Jania rubens (L.) Lamx. Phytother Res 18:275–279

    Article  CAS  PubMed  Google Scholar 

  • Baker JT (1984) Seaweeds in pharmaceutical studies and applications. Hydrobiologia 116/117:29–40

    Article  Google Scholar 

  • Barbosa JP, Pereira RC, Abrantes JL, dos Santos CCC, Rebello MA, Frugulhetti I, Teixeira VL (2004) In vitro antiviral diterpenes from the Brazilian brown alga Dictyota pfaffii. Planta Med 70:856–860

    Article  CAS  PubMed  Google Scholar 

  • Barone A, Chi DC, Theoret MR, Chen H, He K, Kufrin D, Helms WS, Subramaniam S, Zhao H, Patel A, Goldberg KB, Keegan P, Pazdur R (2017) FDA approval summary: trabectedin for unresectable or metastatic liposarcoma or leiomyosarcoma following an anthracycline-containing regimen. Clin Cancer Res 23:7448–7453

    Article  CAS  PubMed  Google Scholar 

  • Barros-Alvarez X, Gualdron-Lopez M, Acosta H, Caceres AJ, Graminha MAS, Michels PAM, Concepcion JL, Quinones W (2014) Glycosomal targets for anti-trypanosomatid drug discovery. Curr Med Chem 21:1679–1706

    Article  CAS  PubMed  Google Scholar 

  • Bawakid NO, Alarif WM, Alorfi HS, Al-Footy KO, Alburae NA, Ghandourah MA, Al-Lihaibi SS, Abdul-Hameed ZH (2017) Antimicrobial sesquiterpenoids from Laurencia obtusa Lamouroux. Open Chem 15:219–224

    Article  CAS  Google Scholar 

  • Becerra M, Boutefnouchet S, Cordoba O, Vitorino GP, Brehu L, Lamour I, Laimay F, Efstathiou A, Smirlis D, Michel S, Kritsanida M, Flores ML, Grougnet R (2015) Antileishmanial activity of fucosterol recovered from Lessonia vadosa Searles (Lessoniaceae) by SFE, PSE and CPC. Phytochem Lett 11:418–423

    Article  CAS  Google Scholar 

  • Bikker P, van Krimpen MM, van Wikselaar P, Houweling-Tan B, Scaccia N, van Hal JW, Huijgen WJJ, Cone JW, López-Contreras AM (2016) Biorefinery of the green seaweed Ulva lactuca to produce animal feed, chemicals and biofuels. J Appl Phycol 28:3511–3525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bin L, Pengpeng H, Yuyang P, Tiantian L, Weiling G, Ruibo J, Lina Z, Zhenjin C, Xiaoqin J, Zirui H (2017) Preparation method of seaweed whole active substances. Chinese Patent 106942739

  • Boisvert C, Beaulieu L, Bonnet C, Pelletier E (2015) Assessment of the antioxidant and antibacterial activities of three species of edible seaweeds. J Food Biochem 39:377–387

    Article  CAS  Google Scholar 

  • Boulho R, Marty C, Freile-Pelegrin Y, Robledo D, Bourgougnon N, Bedoux G (2017) Antiherpetic (HSV-1) activity of carrageenans from the red seaweed Solieria chordalis (Rhodophyta, Gigartinales) extracted by microwave-assisted extraction (MAE). J Appl Phycol 29(5):2219–2228

    Article  CAS  Google Scholar 

  • Campos A, Souza CB, Lhullier C, Falkenberg M, Schenkel EP, Ribeiro-do-Valle RM, Siqueira JM (2012) Anti-tumour effects of elatol, a marine derivative compound obtained from red algae Laurencia microcladia. J Pharm Pharmacol 64:1146–1154

    Article  CAS  PubMed  Google Scholar 

  • Cantillo-Ciau Z, Moo-Puc R, Quijano L, Freile-Pelegrin Y (2010) The tropical brown alga Lobophora variegata: a source of antiprotozoal compounds. Mar Drugs 8:1292–1304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardozo KHM, Guaratini T, Barros MP, Falcao VR, Tonon AP, Lopes NP, Campos S, Torres MA, Souza AO, Colepicolo P, Pinto E (2007) Metabolites from algae with economical impact. Comp Biochem Physiol C 146:60–78

    Article  CAS  Google Scholar 

  • Chakraborty A (2016) Understanding the biology of the Plasmodium falciparum apicoplast; an excellent target for antimalarial drug development. Life Sci 158:104–110

    Article  CAS  PubMed  Google Scholar 

  • Charoensiddhi S, Franco C, Su P, Zhang W (2015) Improved antioxidant activities of brown seaweed Ecklonia radiata extracts prepared by microwave-assisted enzymatic extraction. J Appl Phycol 27:2049–2058

    Article  CAS  Google Scholar 

  • Chemat F, Rombaut N, Meullemiestre A, Turk M, Perino S, Fabiano-Tixier AS, Abert-Vian M (2017) Review of green food processing techniques. Preservation, transformation, and extraction. Innov Food Sci Emerg Technol 41:357–377

    Article  CAS  Google Scholar 

  • Chen J-H, Lim J-D, Sohn E-H, Choi Y-S, Han E-T (2009) Growth-inhibitory effect of a fucoidan from brown seaweed Undaria pinnatifida on Plasmodium parasites. Parasitol Res 104:245–250

    Article  PubMed  Google Scholar 

  • Chen J-Y, Huang C-Y, Lin Y-S, Hwang T-L, Wang W-L, Chiou S-F, Sheu J-H (2016) Halogenated sesquiterpenoids from the red alga Laurencia tristicha collected in Taiwan. J Nat Prod 79:2315–2323

    Article  CAS  PubMed  Google Scholar 

  • Chun BS, Hong SG (2002) Method for extracting chlorophyll and carotenoid pigments from seaweeds, crustacea and echinodermata using supercritical and subcritical carbon dioxides with entrainer. Korean Patent 1020020000660

  • Crowther GJ, Booker ML, He M, Li T, Raverdy S, Novelli JF, He P, Dale NR, Fife AM, Barker RH Jr, Kramer ML, Van Voorhis WC, Carlow CK, Wang MW (2014) Cofactor-independent phosphoglycerate mutase from nematodes has limited druggability, as revealed by two high-throughput screens. PLoS Negl Trop Dis 8:e2628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cuevas C, Francesch A (2009) Development of Yondelis (trabectedin, ET-743). A semisynthetic process solves the supply problem. Nat Prod Rep 26:332–337

    Article  CAS  Google Scholar 

  • Dalzell JJ, Warnock ND, McVeigh P, Marks NJ, Mousley A, Atkinson L, Maule AG (2012) Considering RNAi experimental design in parasitic helminths. Parasitol 139:589–604

    Article  CAS  Google Scholar 

  • Dang TT, Vuong QV, Schreider MJ (2017) Optimisation of ultrasound-assisted extraction conditions for phenolic content and antioxidant activities of the alga Hormosira banksii using response surface methodology. J Appl Phycol 29:3161–3173

    Article  CAS  Google Scholar 

  • Davyt D, Fernandez R, Suescun L, Mombru AW, Saldana J, Dominguez L, Coll J, Fujii MT, Manta E (2001) New sesquiterpene derivatives from the red alga Laurencia scoparia. Isolation, structure determination, and anthelmintic activity. J Nat Prod 64:1552–1555

    Article  CAS  PubMed  Google Scholar 

  • Davyt D, Fernandez R, Suescun L, Mombru AW, Saldana J, Dominguez L, Fujii MT, Manta E (2006) Bisabolanes from the red alga Laurencia scoparia. J Nat Prod 69:1113–1116

    Article  CAS  PubMed  Google Scholar 

  • De Corato U, Salimbeni R, De Pretis A, Avella N, Patruno G (2017) Antifungal activity of crude extracts from brown and red seaweeds by a supercritical carbon dioxide technique against fruit postharvest fungal diseases. Postharvest Biol Tec 131:16–30

    Article  CAS  Google Scholar 

  • Dekun Y, Xuehui S (2017) Method for preparing fucoxanthin from kelp seaweeds. Chinese Patent 106518814

  • Desoti VC, Lazarin-Bidoia D, Sudatti DB, Pereira RC, Alonso A, Ueda-Nakamura T, Dias Filho BP, Nakamura CV, Silva SO (2012) Trypanocidal action of (-)-elatol involves an oxidative stress triggered by mitochondria dysfunction. Mar Drugs 10:1631–1646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Docampo R, Huang G (2015) Calcium signaling in trypanosomatid parasites. Cell Calcium 57:194–202

    Article  CAS  PubMed  Google Scholar 

  • Domínguez L, Saldaña J, Chernin J (2000) Use of L4 larvae of Nippostrongylus brasiliensis for the in vivo screening of anthelmintic drugs. Can J Vet Res 64:160–163

    PubMed  PubMed Central  Google Scholar 

  • dos Santos AO, Veiga-Santos P, Ueda-Nakamura T, Dias Filho BP, Sudatti DB, Bianco EM, Pereira RC, Nakamura CV (2010) Effect of Elatol, isolated from red seaweed Laurencia dendroidea, on Leishmania amazonensis. Mar Drugs 8:2733–2743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • dos Santos AO, Britta EA, Bianco EM, Ueda-Nakamura T, Dias Filho BP, Pereira RC, Nakamura CV (2011) 4-Acetoxydolastane diterpene from the Brazilian brown alga Canistrocarpus cervicornis as antileishmanial agent. Mar Drugs 9:2369–2383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fagang H, Xiaoli N (2012) Vitiligo covering composition and preparation method thereof. Chinese Patent 102793640

  • Feng M-T, Yu X-Q, Yang P, Yang H, Lin K, Mao S-C (2015) Two new antifungal polyunsaturated fatty acid ethyl esters from the red alga Laurencia okamurai. Chem Nat Compd 51:418–422

    Article  CAS  Google Scholar 

  • Ferreira AF, Ribeiro LA, Batista AP, Marques PA, Nobre BP, Palavra AM, da Silva PP, Gouveia L, Silva C (2013) A biorefinery from Nannochloropsis sp microalga—energy and CO2 emission and economic analyses. Bioresour Technol 138:235–244

    Article  CAS  PubMed  Google Scholar 

  • Flórez-Fernández N, López-García M, González-Muñoz MJ, Vilariño JML, Domínguez H (2017) Ultrasound-assisted extraction of fucoidan from Sargassum muticum. J Appl Phycol 29:1553–1561

    Article  CAS  Google Scholar 

  • Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Prentice IC, Ramankutty N, Snyder PK (2005) Global consequences of land use. Science 309:570–574

    Article  CAS  PubMed  Google Scholar 

  • Freemantle M (2004) Scaled-up synthesis of discodermolide. Chem Eng News 82:33–35

    Article  Google Scholar 

  • Galle J-B, Attioua B, Kaiser M, Rusig A-M, Lobstein A, Vonthron-Senecheau C (2013) Eleganolone, a diterpene from the French marine alga Bifurcaria bifurcata inhibits growth of the human pathogens Trypanosoma brucei and Plasmodium falciparum. Mar Drugs 11:599–610

    Article  PubMed  PubMed Central  Google Scholar 

  • Geldhof P, Visser A, Clark D, Saunders G, Britton C, Gilleard J, Berriman M, Knox D (2007) RNA interference in parasitic helminths: current situation, potential pitfalls and future prospects. Parasitology 134:609–619

    Article  CAS  PubMed  Google Scholar 

  • Gilbert-López B, Mendiola JA, van den Broekb LAM, Tan BH, Sijtsma L, Cifuentes A, Herrero M, Ibáñez E (2017) Green compressed fluid technologies for downstream processing of Scenedesmus obliquus in a biorefinery approach. Algal Res 24:111–121

    Article  Google Scholar 

  • Golberg A (2017) Method and device for non-thermal extraction of phytochemicals from macroalgae. WO Patent Application 2017/081677

  • Gorka B, Wieczorek PP (2017) Simultaneous determination of nine phytohormones in seaweed and algae extracts by HPLC-PDA. J Chromatogr B 1057:32–39

    Article  CAS  Google Scholar 

  • Gosbert GN, YOU H, Mcmanus DP (2014) Gaining biological perspectives from schistosome genomes. Mol Biochem Parasitol 196:21–28

    Article  CAS  Google Scholar 

  • Grant WN, Behm CA (2007) Target identification and validation for anthelmintic discovery. Expert Opin Drug Discov 2:S91–S98

    Article  CAS  PubMed  Google Scholar 

  • Gressler V, Fujii MT, Martins AP, Colepicolo P, Mancini-Filho J, Pinto E (2011a) Biochemical composition of two red seaweed species grown on the Brazilian coast. J Sci Food Agric 91:1687–1692

    Article  CAS  PubMed  Google Scholar 

  • Gressler V, Stein EM, Dörr F, Fujii MT, Colepicolo P, Pinto E (2011b) Sesquiterpenes from the essential oil of Laurencia dendroidea (Ceramiales, Rhodophyta): isolation, biological activities and distribution among seaweeds. Rev Bras Farmacogn-Braz J Pharmacog 21:248–254

    Article  CAS  Google Scholar 

  • Guiry MD, Guiry GM (2018) AlgaeBase. World-wide electronic publication, National University of Ireland. http://www.algaebase.org. Accessed 20 February 2018

  • He S, Zhu L, Liu F, Liu Q, Shao Y, Hua M, Ding H, Shao W, Du Y, Hou X, Ren C, Liu M, Shen J (2018) Functions of the Vasa gene in Schistosoma japonicum as assessed by RNA interference. Gene 638:13–19

    Article  CAS  PubMed  Google Scholar 

  • Heffernan N, Smyth TJ, Fitzgerald RJ, Soler-Vila A, Brunton N (2014) Antioxidant activity and phenolic content of pressurised liquid and solid-liquid extracts from four Irish origin macroalgae. Int J Food Sci Tech 49:1765–1772

    Article  CAS  Google Scholar 

  • Horie S, Tsutsumi S, Takada Y, Kimura J (2008) Antibacterial quinone metabolites from the brown alga, Sargassum sagamianum. Bull Chem Soc Jpn 81:1125–1130

    Article  CAS  Google Scholar 

  • Huang Y, Rorrer GL (2002) Optimal temperature and photoperiod for the cultivation of Agardhiella subulata microplantlets in a bubble-column photobioreactor. Biotechnol Bioeng 79:135–144

    Article  CAS  PubMed  Google Scholar 

  • Hudson A, Nwaka S (2007) The concept paper on the helminth drug initiative. Onchocerciasis/lymphatic filariasis and schistosomiasis: opportunities and challenges for the discovery of new drugs/diagnostics. Expert Opin Drug Disc 2:S3–S7

    Article  CAS  Google Scholar 

  • Inoki S, Nakanishi K, Nakabayashi T (1958) Study of Leishmania donovani with special reference to the kinetoplast, mitochondria, and golgi zone by electron microscope employing thin section technique. Biken J 1:194–197

    Google Scholar 

  • Ioannou E, Quesada A, Rahman MM, Gibbons S, Vagias C, Roussis V (2011) Dolabellanes with antibacterial activity from the brown alga Dilophus spiralis. J Nat Prod 74:213–222

    Article  CAS  PubMed  Google Scholar 

  • Ioannou E, Quesada A, Rahman MM, Gibbons S, Vagias C, Roussis V (2012) Structures and antibacterial activities of minor dolabellanes from the brown alga Dilophus spiralis. Eur J Org Chem:5177–5186

  • Jorge ST, Marivel SG, José NGM (2014) Antioxidant extract from brown macroalgae and method for obtaining same. WO Patent application 2014/167162

  • Jorge ST, Marivel SG, José NGM (2016a) Antioxidant extract from brown macroalgae and method for obtaining same. US Patent 2016/0074317

  • Jorge ST, Marivel SG, José NGM (2016b) Antioxidant extract from brown macroalgae and method for obtaining same. European Patent 2997963

  • Kadam SU, O'Donnell CP, Rai DK, Hossain MB, Burgess CM, Walsh D, Tiwari BK (2015) Laminarin from Irish brown seaweeds Ascophyllum nodosum and Laminaria hyperborea: ultrasound assisted extraction, characterization and bioactivity. Mar Drugs 13:4270–4280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamei Y, Sueyoshi M, Hayashi K-i, Terada R, Nozaki H (2009) The novel anti-Propionibacterium acnes compound, Sargafuran, found in the marine brown alga Sargassum macrocarpum. J Antibiot 62:259–263

    Article  CAS  PubMed  Google Scholar 

  • Kang JY, Chun B-S, Lee M-C, Choi J-S, Choi I-S, Hong Y-K (2016) Anti-inflammatory activity and chemical composition of essential oil extracted with supercritical CO2 from the brown seaweed Undaria pinnatifida. J Essent Oil Bear Pl 19:46–51

    Article  CAS  Google Scholar 

  • Konig GM, Wright AD, Franzblau SG (2000) Assessment of antimycobacterial activity of a series of mainly marine derived natural products. Planta Med 66:337–342

    Article  CAS  PubMed  Google Scholar 

  • Lang KL, Silva IT, Zimmermann LA, Lhullier C, Mañalich Arana MV, Palermo JA, Falkenberg M, Simões CM, Schenkel EP, Durán FJ (2012) Cytotoxic activity of semi-synthetic derivatives of elatol and isoobtusol. Mar Drugs 10:2254–2264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laurens LML, Chen-Glasser M, McMillan JD (2017) A perspective on renewable bioenergy from photosynthetic algae as feedstock for biofuels and bioproducts. Algal Res 24:261–264

    Article  Google Scholar 

  • Li JWH, Vederas JC (2009) Drug discovery and natural products: end of an era or an endless frontier? Science 325:161–165

    Article  CAS  PubMed  Google Scholar 

  • Li XC, Jacob MR, Ding YQ, Agarwal AK, Smillie TJ, Khan SI, Nagle DG, Ferreira D, Clark AM (2006) Capisterones A and B, which enhance fluconazole activity in Saccharomyces cerevisiae, from the marine green alga Penicillus capitatus. J Nat Prod 69:542–546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li M-C, Sun W-S, Cheng W, Liu D, Liang H, Zhang Q-Y, Lin W-H (2016) Four new minor brominated indole related alkaloids with antibacterial activities from Laurencia similis. Bioorg Med Chem Lett 26:3590–3593

    Article  CAS  PubMed  Google Scholar 

  • Liu A-H, Liu D-Q, Liang T-J, Yu X-Q, Feng M-T, Yao L-G, Fang Y, Wang B, Feng L-H, Zhang M-X, Mao S-C (2013) Caulerprenylols A and B, two rare antifungal prenylated para-xylenes from the green alga Caulerpa racemosa. Bioorg Med Chem Lett 23:2491–2494

    Article  CAS  PubMed  Google Scholar 

  • Liu M, Liu Y, Cao M-J, Liu G-M, Chen Q, Sun L, Chen H (2017) Antibacterial activity and mechanisms of depolymerized fucoidans isolated from Laminaria japonica. Carbohydr Polym 172:294–305

    Article  CAS  PubMed  Google Scholar 

  • Macintyre F, Adoke Y, Tiono AB et al (2017) A randomised, double-blind clinical phase II trial of the efficacy, safety, tolerability and pharmacokinetics of a single dose combination treatment with artefenomel and piperaquine in adults and children with uncomplicated Plasmodium falciparum malaria. BMC Med 15:181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maradhupandi T, Kumar TTA (2013) Antibacterial effect from fucoidan from Sargassum wightii against the chosen human bacterial pathogens. Interna Curr Pharmaceut J 2(10):156–158

    Article  Google Scholar 

  • Marcellino C, Gut J, Lim KC, Singh R, McKerrow J, Sakanari J (2012) WormAssay: a novel computer application for whole-plate motion-based screening of macroscopic parasites. PLoS Negl Trop Dis 6:e1494

    Article  PubMed  PubMed Central  Google Scholar 

  • Martins AP, Yokoya NS, Colepicolo P (2016) Biochemical modulation by carbon and nitrogen addition in cultures of Dictyota menstrualis (Dictyotales, Phaeophyceae) to generate oil-based bioproducts. Mar Biotechnol 18:314–326

    Article  CAS  PubMed  Google Scholar 

  • Maule AG, McVeigh P, Dalzell JJ, Atkinson L, Mousley A, Marks NJ (2011) An eye on RNAi in nematode parasites. Trends Parasitol 27:505–513

    Article  CAS  PubMed  Google Scholar 

  • McCarthy JS, Baker M, O'Rourke P, Marquart L, Griffin P, van Huijsduijnen RH, Mohrle JJ (2016) Efficacy of OZ439 (artefenomel) against early Plasmodium falciparum blood-stage malaria infection in healthy volunteers. J Antimicrob Chemother 71:2620–2627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mickel SJ, Niederer D, Daeffler R, Osmani A, Kuesters E, Schmid E, Schaer K, Gamboni R, Chen WC, Loeser E, Kinder FR Jr, Konigsberger K, Prasad K, Ramsey TM, Repic O, Wang RM, Florence G, Lyothier I, Paterson I (2004) Large-scale synthesis of the anti-cancer marine natural product (+)-discodermolide. Part 5: linkage of fragments c1–6 and c7–24 and finale. Org Process Res Dev 8:122–130

    Article  CAS  Google Scholar 

  • Mittal R, Tavanandi HA, Mantri VA, Raghavarao KSMS (2017) Ultrasound assisted methods for enhanced extraction of phycobiliproteins from marine macro-algae, Gelidium pusillum (Rhodophyta). Ultrason Sonochem 38:92–103

    Article  CAS  PubMed  Google Scholar 

  • Mobegi FM, Zomer A, de Jonge MI, van Hijum SAFT (2017) Advances and perspectives in computational prediction of microbial gene essentiality. Brief Funct Genomics 16:70–79

    Article  CAS  PubMed  Google Scholar 

  • Molyneux DH (2016) The London declaration on neglected tropical diseases: 5 years on. Trans Roy Soc Trop Med Hyg 110:623–625

    Google Scholar 

  • Moon WK, Moon JN, Kim JY, Ahn DH (2015) Cosmetic composition containing seaweed extract. WO Patent Application 2015/099280

  • Moreira R, Sineiro J, Chenlo F, Arufe S, Díaz-Varela D (2017) Aqueous extracts of Ascophyllum nodosum obtained by ultrasound-assisted extraction: effects of drying temperature of seaweed on the properties of extracts. J Appl Phycol 29:3191–3200

    Article  CAS  Google Scholar 

  • Newman DJ, Cragg GM (2016) Natural products as sources of new drugs from 1981 to 2014. J Nat Prod 79:629–661

    Article  CAS  PubMed  Google Scholar 

  • Ogungbe IV, Setzer WN (2016) The potential of secondary metabolites from plants as drugs or leads against protozoan neglected diseases—part III: in-silico molecular docking investigations. Molecules 21:E1389

    Article  CAS  PubMed  Google Scholar 

  • de Oliveira Fernandes F, de Oliveira SR, Klein V, do Amaral Carneiro MA, Colepicolo P, Marinho-Soriano E (2017) Effect of fertilization pulses on the production of Gracilaria birdiae seedlings under laboratory and field conditions. J Appl Phycol 29:695–705

    Article  CAS  Google Scholar 

  • Oryan A, Akbari M (2016) Worldwide risk factors in leishmaniasis. Asian Pac J Trop Med 9:901–909

    Article  Google Scholar 

  • Ospina M, Castro-Vargas HI, Parada-Alfonso F (2017) Antioxidant capacity of Colombian seaweeds: 1. Extracts obtained from Gracilaria mammillaris by means of supercritical fluid extraction. J Supercrit Fluids 128:314–322

    Article  CAS  Google Scholar 

  • Passalacqua TG, Torres FA, Nogueira CT, de Almeida L, Del Cistia ML, dos Santos MB, Dutra LA, Bolzani VS, Regasini LO, Graminha MA, Marchetto R, Zottis A (2015) The 2′,4′-dihydroxychalcone could be explored to develop new inhibitors against the glycerol-3-phosphate dehydrogenase from Leishmania species. Bioorg Med Chem Lett 25:3564–3568

  • Paveley RA, Mansour NR, Hallyburton I, Bleicher LS, Benn AE, Mikic I, Guidi A, Gilbert IH, Hopkins AL, Bickle QD (2012) Whole organism high-content screening by label-free, image-based bayesian classification for parasitic diseases. PLoS Negl Trop Dis 6:e1762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira CG, Meireles MAA (2010) Supercritical fluid extraction of bioactive compounds: fundamentals, applications and economic perspectives. Food Bioprocess Technol 3:340–372

    Article  CAS  Google Scholar 

  • Pinto MC, da Rosa JA, Fernandes ZMT, Graminha MAS, Mine JC, Allegretti SM, Delort S, Riedel C, Paes EL, Cupolillo E (2005) Isolation and isoenzyme characterization of Leishmania (Viannia) braziliensis from a case of human cutaneous leishmaniasis in northeast centre of the state of Sao Paulo. Mem Inst Oswaldo Cruz 100:733–734

    Article  CAS  PubMed  Google Scholar 

  • Pinto MC, Barbieri K, Silva MC, Graminha MA, Casanova C, Andrade AJ, Eiras AE (2011) Octenol as attractant to Nyssomyia neivai (Diptera: Psychodidae: Phlebotominae) in the field. J Med Entomol 48:39–44

    Article  CAS  PubMed  Google Scholar 

  • Postma PR, Cerezo-Chinarro O, Akkerman RJ, Olivieri G, Wijffels RH, Brandenburg WA, Eppink MHM (2018) Biorefinery of the macroalgae Ulva lactuca: extraction of proteins and carbohydrates by mild disintegration. J Appl Phycol 30:1281–1293

    Article  CAS  PubMed  Google Scholar 

  • Prieto-Sandoval V, Jaca C, Ormazabal M (2018) Towards a consensus on the circular economy. J Clean Prod 179:605–615

    Article  Google Scholar 

  • Puglisi MP, Tan LT, Jensen PR, Fenical W (2004) Capisterones A and B from the tropical green alga Penicillus capitatus: unexpected anti-fungal defenses targeting the marine pathogen Lindra thallasiae. Tetrahedron 60:7035–7039

    Article  CAS  Google Scholar 

  • Quitain A, Hiroshi T, Kazuhiro O, Yoshiro N (2010) Method and apparatus for extracting fucoxanthin from seaweed. Japan patent 2010/006783

  • Reichelt JL, Borowitzka MA (1984) Antimicrobial activity from marine algae: results of a large-scale screening programme. Hydrobiologia 116/117:158–168

    Article  Google Scholar 

  • Rodrigues D, Alves C, Horta A, Pinteus S, Silva J, Culioli G, Thomas OP, Pedrosa R (2015) Antitumor and antimicrobial potential of bromoditerpenes isolated from the red alga, Sphaerococcus coronopifolius. Mar Drugs 13:713–726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Jasso RM, Mussatto SI, Pastrana L, Aguilar CN, Teixeira JA (2011) Microwave-assisted extraction of sulfated polysaccharides (fucoidan) from brown seaweed. Carbohydr Polym 86:1137–1144

    Article  CAS  Google Scholar 

  • Rorrer GL, Modrell J, Zhi C, Yoo HD, Nagle DN, Gerwick WH (1995) Bioreactor seaweed cell culture for production of bioactive oxylipins. J Appl Phycol 7:187–198

    Article  CAS  Google Scholar 

  • Santoyo S, Plaza M, Jaime L, Ibañez E, Reglero G, Señorans J (2011) Pressurized liquids as an alternative green process to extract antiviral agents from the edible seaweed Himanthalia elongata. J Appl Phycol 23:909–917

    Article  CAS  Google Scholar 

  • Saravana PS, Cho YJ, Park YB, Woo HC, Chun BS (2016) Structural, antioxidant, and emulsifying activities of fucoidan from Saccharina japonica using pressurized liquid extraction. Carbohydr Polym 153:518–525

    Article  CAS  PubMed  Google Scholar 

  • Saravana PS, Getachew AT, JinCho Y, Choi JH, Park YB, Woo HC, Chun BS (2017) Influence of co-solvents on fucoxanthin and phlorotannin recovery from brown seaweed using supercritical CO2. J Supercrit Fluids 120:295–303

    Article  CAS  Google Scholar 

  • Shin H (2004) Method for producing D-cysteinolic acid extract. Japan Patent 2004/143112

  • da Silva Machado FL, Pacienza-Lima W, Rossi-Bergmann B, de Souza Gestinari LM, Fujii MT, de Paula JC, Costa SS, Lopes NP, Kaiser CR, Soares AR (2011) Antileishmanial sesquiterpenes from the Brazilian red alga Laurencia dendroidea. Plant Med 77:733–735

    Article  CAS  Google Scholar 

  • Simeonov A, Jadhav A, Sayed AA, Wang Y, Nelson ME, Thomas CJ, Inglese J, Williams DL, Austin CP (2008) Quantitative high-throughput screen identifies inhibitors of the Schistosoma mansoni redox cascade. PLoS Negl Trop Dis 2:e127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sivagnanam SP, Yin S, Choi JH, Park YB, Woo HC, Chun BS (2015) Biological properties of fucoxanthin in oil recovered from two brown seaweeds using supercritical CO2 extraction. Mar Drugs 13:3422–3442

    Article  CAS  PubMed  Google Scholar 

  • Smyrniotopoulos V, Vagias C, Rahman MM, Gibbons S, Roussis V (2008) Brominated diterpenes with antibacterial activity from the red alga Sphaerococcus coronopifolius. J Nat Prod 71:1386–1392

    Article  CAS  PubMed  Google Scholar 

  • Smyrniotopoulos V, Vagias C, Rahman MM, Gibbons S, Roussis V (2010) Structure and antibacterial activity of brominated diterpenes from the red alga Sphaerococcus coronopifolius. Chem Biodivers 7:186–195

    Article  CAS  PubMed  Google Scholar 

  • Smyrniotopoulos V, Merten C, Kaiser M, Tasdemir D (2017) Bifurcatriol, a new antiprotozoal acyclic diterpene from the brown alga Bifurcaria bifurcata. Mar Drugs 15:245

    Article  CAS  PubMed Central  Google Scholar 

  • Soares DC, Calegari-Silva TC, Lopes UG, Teixeira VL, de Palmer Paixao ICN, Cirne-Santos C, Bou-Habib DC, Saraiva EM (2012) Dolabelladienetriol, a compound from Dictyota pfaffii algae, inhibits the infection by Leishmania amazonensis. PLoS Negl Trop Dis 6:e1787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soares DC, Szlachta MM, Teixeira VL, Soares AR, Saraiva EM (2016) The brown alga Stypopodium zonale (Dictyotaceae): a potential source of anti-Leishmania drugs. Mar Drugs 14:163

    Article  PubMed Central  Google Scholar 

  • de Sousa CB, Gangadhar KN, Morais TR, Conserva GAA, Vizetto-Duarte C, Pereira H, Laurenti MD, Campino L, Levy D, Uemi M, Barreira L, Custodio L, Passero LFD, Lago JHG, Varela J (2017) Antileishmanial activity of meroditerpenoids from the macroalgae Cystoseira baccata. Exp Parasitol 174:1–9

    Article  CAS  Google Scholar 

  • Sterner M, Edlund U (2016) Multicomponent fractionation of Saccharina latissima brown algae using chelating salt solutions. J Appl Phycol 28:2561–2574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stoppani AOM, Docampo R, Deboiso JF, Frasch ACC (1980) Effect of inhibitors of electron-transport and oxidative-phosphorylation on Trypanosoma cruzi respiration and growth. Mol Biochem Parasitol 2:3–21

    Article  CAS  PubMed  Google Scholar 

  • Stout EP, Cervantes S, Prudhomme J, France S, La Clair JJ, Le Roch K, Kubanek J (2011) Bromophycolide A targets heme crystallization in the human malaria parasite Plasmodium falciparum. ChemMedChem 6:1572–1577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka Y, Okuda M, Sonoda M (1975) Effect of Chlorella on levels of cholesterol and triglyceride in liver and serum. Artery 1:339–339

    Google Scholar 

  • Tierney M, Smiyth TJ, Hayes M, Soler-Vila A, Croft AK, Brunton N (2013) Influence of pressurised liquid extraction and solid–liquid extraction methods on the phenolic content and antioxidant activities of Irish macroalgae. Int J Food Sci Technol 48:860–869

    Article  CAS  Google Scholar 

  • Tomazela DM, Pupo MT, Passador EAP, da Silva M, Vieira PC, Fernandes JB, Fo ER, Oliva G, Pirani JR (2000) Pyrano chalcones and a flavone from Neoraputia magnifica and their Trypanosoma cruzi glycosomal glyceraldehyde-3-phosphate dehydrogenase-inhibitory activities. Phytochemistry 55:643–651

    Article  CAS  PubMed  Google Scholar 

  • Tong L, Zhang Y, Liu A-H, Yao L-G, Guo Y-W, Mao S-C, Wang B (2017) Two pairs of rare naturally occurring 4-hydroxy-4-methyl-2,5-heptanedione derivatives from the red alga Chondria crassicaulis. J Asian Nat Prod Res 19:572–580

    Article  CAS  PubMed  Google Scholar 

  • Topuz OK, Gokoglu N, Yerlikaya P, Ucak I, Gumus B (2016) Optimization of antioxidant activity and phenolic compound extraction conditions from red seaweed (Laurencia obtusa). J Aquat Food Prod Technol 25:414–422

    Article  CAS  Google Scholar 

  • Torres FAE, Passalacqua TG, Velasquez AMA, de Souza RA, Colepicolo P, Graminha MAS (2014) New drugs with antiprotozoal activity from marine algae: a review. Rev Bras Farmacog-Braz J Pharmacog 24:265–276

    Article  CAS  Google Scholar 

  • United Nations, Department of Economic and Social Affairs, Population Division (2017). World population prospects: the 2017 revision, key findings and advance tables. Working Paper No. ESA/P/WP/248

  • Vairappan CS (2003) Potent antibacterial activity of halogenated metabolites from Malaysian red algae, Laurencia majuscula (Rhodomelaceae, Ceramiales). Biomol Eng 20:255–259

    Article  CAS  PubMed  Google Scholar 

  • Vairappan CS, Kawamoto T, Miwa H, Suzuki M (2004) Potent antibacterial activity of halogenated compounds against antibiotic-resistant bacteria. Planta Med 70:1087–1090

    Article  CAS  PubMed  Google Scholar 

  • Veiga-Santos P, Pelizzaro-Rocha KJ, Santos AO, Ueda-Nakamura T, Dias Filho BP, Silva SO, Sudatti DB, Bianco EM, Pereira RC, Nakamura CV (2010) In vitro anti-trypanosomal activity of elatol isolated from red seaweed Laurencia dendroidea. Parasitol 137:1661–1670

    Article  CAS  Google Scholar 

  • Ventura BTL, da Silva Machado FL, de Araujo MH, de Souza Gestinari LM, Kaiser CR, Esteves FdA, Lasunskaia EB, Soares AR, Muzitano MF (2015) Nitric oxide production inhibition and anti-mycobacterial activity of extracts and halogenated sesquiterpenes from the Brazilian red alga Laurencia dendroidea J. Agardh. Pharmacogn Mag 11: S611-S618

  • WHO (2014) Proportion of population living in urban area. http://gamapserver.who.int/gho/interactive_charts/urban_health/population/atlas.html?indicator=i1&date=2010; Searched on 4 June 2018

  • WHO (2018) Neglected tropical diseases. http://www.who.int/neglected_diseases/about/en/; Searched on 4 June 2018

  • Xu X, Yin L, Gao J, Gao L, Song F (2014) Antifungal bromophenols from marine red alga Symphyocladia latiuscula. Chem Biodivers 11:807–811

    Article  CAS  PubMed  Google Scholar 

  • Yaming F, Yeyan Z, Guijuan X, Yongheng C (2010) Seaweed flavor powder. China Patent 101919541

  • Yongmei L, Chen W, Jing C, Yongzhi G, Xiumei Z (2015) Method for extracting and purifying fucoxanthin. China Patent 104327017

  • Yoshino TP, Dinguirard N, Mourao MD (2010) In vitro manipulation of gene expression in larval Schistosoma: a model for postgenomic approaches in Trematoda. Parasitol 137:463–483

    Article  CAS  Google Scholar 

  • Yuan Y, Macquarrie D (2015) Microwave-assisted extraction of sulfated polysaccharides (fucoidan) from brown seaweed. Carbohyd Polym 86:1137–1144

    Google Scholar 

  • Yuan Y, Xu X, Jing C, Zou P, Zhang C, Li Y (2018) Microwave assisted hydrothermal extraction of polysaccharides from Ulva prolifera: functional properties and bioactivities. Carbohyd Polym 181:902–910

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Postgraduate Program in Pharmacy, Health Sciences Center, Federal University of Santa Catarina (UFSC), Florianópolis, Brazil

    Miriam Falkenberg, Gabriele A. Zatelli & Ana Claudia Philippus

  2. Parasitology Laboratory, Butantan Institute (IB), São Paulo, SP, Brazil

    Eliana Nakano, Rafaela Paula Freitas & Lenita de Freitas Tallarico

  3. University of São Paulo (USP), Institute of Chemistry (USP), São Paulo, SP, Brazil

    Leonardo Zambotti-Villela & Pio Colepicolo

  4. School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, Brazil

    Kely Braga Imamura, Angela Maria Arenas Velasquez & Marcia A. S. Graminha

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  1. Miriam Falkenberg
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  2. Eliana Nakano
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  3. Leonardo Zambotti-Villela
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  4. Gabriele A. Zatelli
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  11. Marcia A. S. Graminha
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Correspondence to Marcia A. S. Graminha.

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Falkenberg, M., Nakano, E., Zambotti-Villela, L. et al. Bioactive compounds against neglected diseases isolated from macroalgae: a review. J Appl Phycol 31, 797–823 (2019). https://doi.org/10.1007/s10811-018-1572-5

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