Chemical and biological aspects of octocorals from the Brazilian coast

Almeida, Maria Tereza R.; Moritz, Maria Izabel G.; Capel, Katia C.C.; Pérez, Carlos D.; Schenkel, Eloir P.

doi:10.1016/j.bjp.2014.05.002

Maria Tereza R. Almeida ^**Corresponding author. E-mail: tereza.rojo@posgrad.ufsc.br (M.T.R. Almeida).

Departamento de Ciências Farmacêuticas, Universidade Federal de Santa Catarina, Florianópolis, SC, Brazil

Maria Izabel G. Moritz

Departamento de Ciências Farmacêuticas, Universidade Federal de Santa Catarina, Florianópolis, SC, Brazil

Katia C.C. Capel

Centro de Biologia Marinha, Universidade de São Paulo, São Sebastião, SP, Brazil

Carlos D. Pérez

Grupo de Pesquisa em Antozoários, Universidade Federal de Pernambuco, Centro Acadêmico de Vitória, Vitória de Santo Antão, PE, Brazil

Eloir P. Schenkel

Departamento de Ciências Farmacêuticas, Universidade Federal de Santa Catarina, Florianópolis, SC, Brazil

*Corresponding author. E-mail: tereza.rojo@posgrad.ufsc.br (M.T.R. Almeida).

Conflicts of interest

The authors declare no conflicts of interest.

Authors' contributions

MTRA (Postdoctoral student) contributed with the concept, design, and arrangement of the present review article, including data collection, selection of papers and writing of the sections related to natural products. MIGM (PhD student) contributed with data collection, writing of the sections related to natural products and formatting of the manuscript. KCCC (PhD student) contributed with data collection, selection of papers and thesis and writing of the sections related to taxonomical aspects. CDP contributed with expertise related to taxonomic aspects and critical reading of the draft manuscript. EPS supervised the process of drafting and contributed in finalizing the article through critical reading of the draft manuscript. All the authors have read the final manuscript and approved submission. MTRA, MIGM and KCCC contributed equally to this work.

Species	Extracts/Compounds	Biological activities	References
Carijoa riisei^a a Reef species.	polyoxygenated steroids, sterol glycosides	cytotoxicity	Maia et al., 2000Maia, L.F., Epifanio, R.A., Fenical, W., 2000. New cytotoxic sterol glycosides from the octocoral Carijoa (Telesto) riisei. J. Nat. Prod. 63,1427-1430.
	punaglandins	antiproliferative	Baker and Scheuer, 1994Baker, B.J., Scheuer, P.J., 1994. The punaglandins: 10-chloroprostanoids from the octocorals Telesto riisei. J. Nat. Prod. 57,1346-1353.; Baker et al., 1994Baker, B.J., Scheuer, P.J., 1994. The punaglandins: 10-chloroprostanoids from the octocorals Telesto riisei. J. Nat. Prod. 57,1346-1353.; Verbitski et al., 2004Verbitski, S.M., Mullally, J.E., Fitzpatrick, F.A., Ireland, C.M., 2004. Punaglandins, chlorinated prostaglandins, function as potent Michael receptors to inhibit ubiquitin isopeptidase activity. J. Med. Chem. 47,2062-2070.
	pregnanes	antileishmanial	Maia et al., 1998Maia, L.F., Epifanio, R.A., Pinto, A.C., 1998. Steroid composition in Carijoa riisei (Telestacea). Bol. Soc. Chil. Quim. 43,39-45.; Almeida et al., 2012Almeida, M.T.R., Tonini, M.L., Guimarães, T.R., Bianco, E.M., Moritz, M.I.G., Oliveira, S.Q., Cabrera, G.M., Palermo, J.A., Reginatto, F.H., Steindel, M., Schenkel, E.P., 2012. Antiinfective pregnane steroid from the octocoral Carijoa riisei collected in South Brazil. Lat. Am. J. Pharm. 31,1489-1495.
	amides, polyoxygenated steroids	cytotoxicity	Liyanage and Schmitz, 1996Liyanage, G.K., Schmitz, F.J., 1996. Cytotoxic amides from the octocorals Telesto riisei. J. Nat. Prod. 59,148-151.
	18-acetoxypregna-1,4,20-trien-3-one	cytotoxicity, antileishmanial	Seleghim et al., 2007Seleghim, M.H.R., Lira, S.P., Kossuga, M.H., Batista, T., Berlinck, R.G.S., Hajdu, E., Muricy, G., Rocha, R.M., Nascimento, G.G.F., Silva, M., Pimenta, E.F., Thiemann, O., Olivo, G., Cavalcanti, B.C., Pessoa, C., de Moraes, M.O., Galetti, F.C.S., Silva, C.L., de Souza, A.O., Peixinho, S., 2007. Antibiotic, cytotoxic and enzyme inhibitory activity of crude extracts from Brazilian marine invertebrates. Rev. Bras. Farmacogn. 17,287-318.; Kossuga et al., 2007Kossuga, M.H., de Lira, S.P., Nascimento, A.M., Gambardella, M.T.P., Berlinck, R.G.S., Torres, Y.R., Nascimento, G.G.F., Pimenta, E.F., Silva, M., Thiemann, O.H., Oliva, G., Tempone, A.G., Melhem, M.S.C., de Souza, A.O., Galetti, F.C.S., Silva, C.L., Cavalcanti, B., Pessoa, C.O., Moraes, M.O., Hadju, E., Peixinho, S. Rocha, R.M., 2007. Isolamento e atividades Biológicas de produtos naturais das esponjas Monanchora arbuscula, Aplysina sp., Petromica ciocalyptoides e Topsentia ophiraphidites, da ascídia Didemnum ligulum e do octocoral Carijoa riisei. Quim. Nova 30,1194-1202.; Ross and Scheuer, 1979Ross, R.A., Scheuer, P.J., 1979. 18-Acetoxy- and 18-hydroxypregna-1,4,20-trien-3-one from telestacean octocoral Telesto riisei (Duchassaing & Michelotti). Tetrahedron Lett. 69,4701-4704.; Reimão et al., 2008Reimão, J.Q., Migotto, A.E., Kossuga, M.H., Berlinck, R.G.S., Tempone, A.G., 2008. Antiprotozoan activity of Brazilian marine cnidarian extracts and of a modified steroid from the octocoral Carijoa riisei. Parasitol. Res. 103,1445-1450.
	carotenoids	-	Maia et al., 2013Maia, L.F., De Oliveira, V.E., Oliveira, M.E.R., Reis, F.D., Fleury, B.G., Edwards, H.G.M., De Oliveira, L.F.C., 2013. Colour diversification in octocorals based on conjugated polyenes: A Raman spectroscopic view. J. Raman Spectrosc. 44,560-566.
Chromonephthea brazíliensis	23-ketocladiellin-A	feeding deterrent	Fleury et al., 2008Fleury, B.G., Lages, B.G., Barbosa, J.P., Kaiser, C.R., Pinto, A.C., 2008. New hemiketal steroid from the introduced soft coral Chromonephthea braziliensis is a chemical defense against predatory fishes. J. Chem. Ecol. 34,987-993.
	polyenes	-	Maia et al., 2011bMaia, L.F., Fleury, B.G., Lages, B.G., Barbosa, J.P., Pinto, A. C., Castro, H.V., 2011b. Oliveira, V.E., Edwards, H.G.M., Oliveira, L.F.C. Identification of reddish pigments in octocorals by Raman Spectroscopy. J. Raman Spectrosc. 42,653-658.
	extract	feeding deterrent	Lages et al., 2006Lages, B.G., Fleury, B.G., Ferreira, C.E.L., Pereira, R.C., 2006. Chemical defense of an exotic coral as invasion strategy. J. Exp. Mar. Biol. Ecol. 328,127-135.
	extracts	genotoxicity	Carpes et al., 2013Carpes, R.M., Fleury, B.G., Lages, B.G., Pinto, A.C., Aiub, C.A.F., Felzenszwalb, I., 2013. Mutagenicity, genotoxicity, and scavenging activities of extracts from the soft coral Chromonephthea braziliensis: a possibility of new bioactive compounds. Genet. Mol. Res. 12,3575-3587.
Convexella magelhaenica	dolabellane diterpenoids	cytotoxicity	Almeida et al., 2010Almeida, M.T.R., Siless, G.E., Perez, C.D., Veloso, M.J., Schejter, L., Puricelli, L., Palermo, J.A., 2010. Dolabellane Diterpenoids from the South Atlantic gorgonian Convexella magelhaenica. J. Nat. Prod. 73,1714-1717.
Dasystenella acanthina	sesquiterpenoids, polyoxygenated steroids	-	Mellado et al., 2004Mellado, G.G., Zubıa, E., Ortega, M.J., Lopez, G.P.J., 2004. New polyoxygenated steroids from the Antarctic octocorals Dasystenella acanthine. Steroids 69,291-299.; Gavagnin et al., 2003Gavagnin, M., Mollo, E., Castelluccio, F., Crispino, A., Cimino, G., 2003. Sesquiterpene metabolites of the antarctic gorgonian Dasystenella acanthine. J. Nat. Prod. 66,1517-1519.
Heterogorgia uatumani^a a Reef species.	eunicellane diterpenoid, sesquiterpene lactone, heterogorgiolide	feeding inhibition	Maia et al., 1999Maia, L.F., Epifanio, R.A., Eve, T., Fenical, W., 1999. New fish feeding deterrents, including a novel sesquiterpenoid heterogorgiolide, from the Brazilian gorgonian Heterogorgia uatumani (Octocorallia, Gorgonacea). J. Nat. Prod. 62,1322-1324.
Leptogorgia punicea^a a Reef species.	hidroquinone, steroids, punicin		Epifanio et al., 1998Epifanio, R.A., Maia, L.F., Pinto, A.C., Hardt, I., Fenical, W., 1998. Natural products from gorgonian Lophogorgia punicea: isolation and structure elucidation of an unusual 17-hydroxy sterol. J. Braz. Chem. Soc. 9,187-192.
	carotenoids	-	Maia et al., 2013Maia, L.F., De Oliveira, V.E., Oliveira, M.E.R., Reis, F.D., Fleury, B.G., Edwards, H.G.M., De Oliveira, L.F.C., 2013. Colour diversification in octocorals based on conjugated polyenes: A Raman spectroscopic view. J. Raman Spectrosc. 44,560-566.
Leptogorgia setacea	pukalide 11β,12β-epoxypukalide	antifouling, feeding deterrent	Ksebati et al., 1984Ksebati, M.B., Ciereszko, L.S., Schmitz, F.J., 1984. 11β,12β-Epoxypukalide, a furanocembranolide from the gorgonian Leptogorgia setacea. J. Nat. Prod. 47,1009-1012.; Gerhart et al., 1988Gerhart, D.J., Rittschof, D., Mayo, S.W., 1988. Chemical ecology and the search for marine antifoulants. Studies of a predatorprey symbiosis. J. Chem. Ecol. 14,1905-1917.; Gerhart et al., 1993Gerhart, D.J., Coll, J.C., 1993. Pukalide, a widely distributed octocoral diterpenoid, induces vomiting in fish. J. Chem. Ecol. 19,2697-2704.
	homarine	antifouling, antimicrobial	Targett et al., 1983Targett, N.M., Bishop, S.S., McConnell, O.J., Yoder, J. A., 1983. Antifouling agents against the benthic marine diatom, Navicula salinicola: homarine from the gorgonians Leptogorgia virgulata and L. setacea and analogs. J. Chem. Ecol. 9,817-829.; Shapo et al., 2007Shapo, J.L., Moeller, P.D., Galloway, S.B., 2007. Antimicrobial activity in the common seawhip Leptogorgia virgulata (Cnidaria: Gorgonaceae). Comp. Biochem. Phys. B 148B,65-73.
	polyenals	-	Maia et al., 2013Maia, L.F., De Oliveira, V.E., Oliveira, M.E.R., Reis, F.D., Fleury, B.G., Edwards, H.G.M., De Oliveira, L.F.C., 2013. Colour diversification in octocorals based on conjugated polyenes: A Raman spectroscopic view. J. Raman Spectrosc. 44,560-566.
Leptogorgia violacea (E)^a a Reef species.	lophotoxin, deoxylophotoxin, 13-acetoxy-11β,12β-epoxypukalide, furanocembranolides	feeding deterrent	Epifanio et al., 2000Epifanio, R.A., Maia, L.F., Fenical, W., 2000. Chemical defenses of the endemic Brazilian gorgonian Lophogorgia violacea Pallas (Octocorallia, Gorgonacea). J. Braz. Chem. Soc. 11,584-591.
	polyenals	-	Maia et al., 2011bMaia, L.F., Fleury, B.G., Lages, B.G., Barbosa, J.P., Pinto, A. C., Castro, H.V., 2011b. Oliveira, V.E., Edwards, H.G.M., Oliveira, L.F.C. Identification of reddish pigments in octocorals by Raman Spectroscopy. J. Raman Spectrosc. 42,653-658.
Muricea atlântica	carotenoids	-	Maia et al., 2013Maia, L.F., De Oliveira, V.E., Oliveira, M.E.R., Reis, F.D., Fleury, B.G., Edwards, H.G.M., De Oliveira, L.F.C., 2013. Colour diversification in octocorals based on conjugated polyenes: A Raman spectroscopic view. J. Raman Spectrosc. 44,560-566.
Muricea flamma	polyenals	-	Maia et al., 2013Maia, L.F., De Oliveira, V.E., Oliveira, M.E.R., Reis, F.D., Fleury, B.G., Edwards, H.G.M., De Oliveira, L.F.C., 2013. Colour diversification in octocorals based on conjugated polyenes: A Raman spectroscopic view. J. Raman Spectrosc. 44,560-566.
Muriceopsis flavida	steroids, sesquiterpenes	antimicrobial	Kokke et al., 1982Kokke, W.C.M.C., Bohlin, L., Fenical, W., Djerassi, C., 1982. Novel dinoflagellate 4α-methylated sterols from four Caribbean gorgonians. Phytochemistry 21,881-887.; Liu et al., 2012Liu, T., Tang, H., Gong, W., Sun, P., Liu, B., Li, L., Zhang, W., 2012. Sesquiterpenes from the South China Sea gorgonian Muriceopsis flavida. Yaoxue Shijian Zazhi 30,100-102.; 2011Maia, L.F., Fleury, B.G., Lages, B.G., Barbosa, J.P., Pinto, A. C., Castro, H.V., 2011b. Oliveira, V.E., Edwards, H.G.M., Oliveira, L.F.C. Identification of reddish pigments in octocorals by Raman Spectroscopy. J. Raman Spectrosc. 42,653-658.
	steroids	antiproliferative	Liu et al., 2013Liu, T.F., Lu, X., Tang, H., Zhang, M.M., Wang, P., Sun, P., Liu, Z.Y., Wang, Z.L., Li, L., Rui, Y.C., Li, T.J., Zhang, W., 2013. 3β, 5α, 6β-Oxygenated sterols from the South China Sea gorgonian Muriceopsis flavida and their tumor cell growth inhibitory activity and apoptosis-inducing function. Steroids 78,108-114.
Neospongodes atlantica (E)^a a Reef species.	crude extract	feeding stimulation	Epifanio et al., 1999Epifanio, R.A., Martins, D.L., Villaca, R., Gabriel, R., 1999. Chemical defenses against fish predation in three Brazilian octocorals: 11β,12β-epoxypukalide as a feeding deterrent in Phyllogorgia dilatata. J. Chem. Ecol. 25,2255-2265.
Nicela goreauii	crude extract	feeding deterrent	O'Neal and Pawlik, 2002O'Neal, W., Pawlik, J.R., 2002. A reappraisal of the chemical and physical defenses of Caribbean gorgonian corals against predatory fishes. Mar. Ecol. Prog. Ser. 240,117-126.
Phyllogorgia dilatata (E)^a a Reef species.	steroids	-	Kelecom et al., 1980Kelecom, A., Sole-Cava, A.M., Kannengiesser, G.J., 1980. Occurrence of 23,24ε-dimethylcholesta-5,22-dien-3β-ol in the Brazilian gorgonian Phyllogorgia dilatata (Octocorallia, Gorgonacea) and in its associated zooxanthella. B. Soc. Chim. Belg. 89,1013-1014.
	diterpene epoxypukalide,
	germacrane sesquiterpene	antipredatory, antifouling	Epifanio et al, 1999Epifanio, R.A., Martins, D.L., Villaca, R., Gabriel, R., 1999. Chemical defenses against fish predation in three Brazilian octocorals: 11β,12β-epoxypukalide as a feeding deterrent in Phyllogorgia dilatata. J. Chem. Ecol. 25,2255-2265.; 2006Epifanio, R.A., da Gama, B.A.P., Pereira, R.C., 2006. 11β,12βepoxypukalide as the antifouling agent from the Brazilian endemic sea fan Phyllogorgia dilatata Esper. Biochem. Syst. Ecol. 34,446-448.; Martins and Epifanio, 1998Martins, D.L., Epifanio, R.A., 1998. A new germacrane sesquiterpene from the Brazilian endemic gorgonian Phyllogorgia dilatata Esper. J. Braz. Chem. Soc. 9,586-590.
	nardosinane sesquiterpene	-	Kelecom et al., 1980Kelecom, A., Sole-Cava, A.M., Kannengiesser, G.J., 1980. Occurrence of 23,24ε-dimethylcholesta-5,22-dien-3β-ol in the Brazilian gorgonian Phyllogorgia dilatata (Octocorallia, Gorgonacea) and in its associated zooxanthella. B. Soc. Chim. Belg. 89,1013-1014.; Fernandes and Kelecom, 1995Fernandes, L., Kelecom, A., 1995. A further nardosinane sesquiterpene from the gorgonian Phyllogorgia dilatata (Octocorallia, Gorgonacea). An. Acad. Bras. Cienc. 67,171-173.
	crude extract	antifouling	Pereira et al., 2002Pereira, R.C., Carvalho, A.G.V., Gama, B.A.P., Coutinho, R., 2002. Field experimental evaluation of secondary metabolites from marine invertebrates as antifoulants. Braz. J. Biol. 62,311-320.
	polyenals, carotenoids	-	Maia et al., 2011aMaia, L.F., Oliveira, V.E., Oliveira, M.E.R., Fleury, B. G., Oliveira, L.F.C., 2011a. Polyenic pigments from the Brazilian octocoral Phyllogorgia dilatata Esper, 1806 characterized by Raman spectroscopy. J. Raman Spectrosc. 43,161-164.; 2013Maia, L.F., De Oliveira, V.E., Oliveira, M.E.R., Reis, F.D., Fleury, B.G., Edwards, H.G.M., De Oliveira, L.F.C., 2013. Colour diversification in octocorals based on conjugated polyenes: A Raman spectroscopic view. J. Raman Spectrosc. 44,560-566.
	peptide	antimicrobial	De Lima et al., 2013De Lima, L.A., Migliolo L., Barreiro e Castro, C., Pires, D. O., Lopez-Abarrategui, C., Goncalves, E.F., Vasconcelos, I.M., Oliveira, J.T.A. Otero-Gonzalez, A.J., Franco, O.L. Dias, S.C. 2013. Identification of a novel antimicrobial peptide from Brazilian coast coral Phyllogorgia dilatata. Protein. Pept. Lett. 20,1153-1158.
Plexaurella dichotoma^a a Reef species.	cetylpalmitate	-	Rodríguez et al., 1983Rodríguez, A., Benito-Pruna, L., Huneck, S., Henriques, R.D., 1983. Chemical studies of Cuban gorgonians. Part II: Chimyl and batyl dipalmitate from Plexaurella dichotoma. Pharmazie 38,267-269.
	eicosatetraenoic acid	-	Di Marzo et al., 1996Di Marzo, V., Ventriglia, M., Mollo, E., Mosca, M., Cimino, G., 1996. Occurrence and biosynthesis of 11(R)-hydroxyeicosatetraenoic acid (11-R-HETE) in the Caribbean soft coral Plexaurella dichotoma. Experientia 52,834-838.
	muurolene sesquiterpene, bisbolene	-	Weinheimer et al., 1967Weinheimer, A.J., Schmitz, F.J., Ciereszko, L.S., 1967. Chemistry of coelenterates. VII. The occurrence of terpenoid compounds in gorgonians. In Drugs Sea, Trans. Drugs Sea Symp. Whashington, USA. p. 135-140.
Plexaurella regia (E)^a a Reef species.	crude extract	feeding stimulation	Epifanio et al., 1999Epifanio, R.A., Martins, D.L., Villaca, R., Gabriel, R., 1999. Chemical defenses against fish predation in three Brazilian octocorals: 11β,12β-epoxypukalide as a feeding deterrent in Phyllogorgia dilatata. J. Chem. Ecol. 25,2255-2265.
Renilla reniformis	briarane-type diterpenes	antifouling, feeding deterrent	Rueda et al., 2001Rueda, A., Zubia, E., Ortega, M.J., Salva, J., 2001a. New acyclic sesquiterpenes and norsesquiterpenes from the Caribbean gorgonian Plexaurella grisea. J. Nat. Prod. 64,401-405.; Barsby and Kubanek, 2005Barsby, T., Kubanek, J., 2005. Isolation and structure elucidation of feeding deterrent diterpenoids from the Sea Pansy Renilla reniformis. J. Nat. Prod. 68,511-516.
	extracts	feeding deterrent	Clavico et al., 2013Clavico E.E.G., Gama, B.A.P., Soares, A.R., Cassiano, R.C., 2013. Interaction of chemical and structural components providing defences to sea pansies Renilla reniformis and Renilla muelleri. Mar. Biol. Res. 9,285-292.
Renilla muelleri	polyenals	-	Maia et al., 2013Maia, L.F., De Oliveira, V.E., Oliveira, M.E.R., Reis, F.D., Fleury, B.G., Edwards, H.G.M., De Oliveira, L.F.C., 2013. Colour diversification in octocorals based on conjugated polyenes: A Raman spectroscopic view. J. Raman Spectrosc. 44,560-566.
	extracts	feeding deterrent	Clavico et al., 2013Clavico E.E.G., Gama, B.A.P., Soares, A.R., Cassiano, R.C., 2013. Interaction of chemical and structural components providing defences to sea pansies Renilla reniformis and Renilla muelleri. Mar. Biol. Res. 9,285-292.
Swiftia exerta	glycosylated pregnene	-	Wright et al., 2004Wright, A.E., Reed, J.K., Longley, R.E., 2004. Biologically active pregnene compounds,US patent US6784160B120040831.
Tripalea clavaria	secosteroids	antimicrobial	Rodríguez Brasco et al., 2007Rodríguez Brasco, M.F., Genzano, G.N., Palermo, J.A., 2007. New C-secosteroids from the gorgonian Tripalea clavaria. Steroids 72,908-913.

[1] *Corresponding author. E-mail: tereza.rojo@posgrad.ufsc.br (M.T.R. Almeida).

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Chemical and biological aspects of octocorals from the Brazilian coast