Evaluation of acetylcholinesterase inhibitory activity of Brazilian red macroalgae organic extracts

Machado, Levi P.; Carvalho, Luciana R.; Young, Maria Cláudia M.; Cardoso-Lopes, Elaine M.; Centeno, Danilo C.; Zambotti-Villela, Leonardo; Colepicolo, Pio; Yokoya, Nair S.

doi:10.1016/j.bjp.2015.09.003

Levi P. Machado

Núcleo de Pesquisa em Ficologia, Instituto de Botânica, São Paulo, SP, Brazil

Luciana R. Carvalho

Núcleo de Pesquisa em Ficologia, Instituto de Botânica, São Paulo, SP, Brazil

Maria Cláudia M. Young

Núcleo de Pesquisa em Fisiologia e Bioquímica, Instituto de Botânica, São Paulo, SP, Brazil

Elaine M. Cardoso-Lopes

Departamento de Farmácia, Universidade Nove de Julho, São Paulo, SP, Brazil

Danilo C. Centeno

Centro de Ciências Naturais e Humanas, Universidade Federal do ABC, São Paul, SP, Brazil

Leonardo Zambotti-Villela

Instituto de Química, Universidade de São Paulo, São Paulo, SP, Brazil

Pio Colepicolo

Instituto de Química, Universidade de São Paulo, São Paulo, SP, Brazil

Nair S. Yokoya ^** Corresponding author. E-mail:nyokoya@pq.cnpq.br (N.S. Yokoya).

Núcleo de Pesquisa em Ficologia, Instituto de Botânica, São Paulo, SP, Brazil

* Corresponding author. E-mail:nyokoya@pq.cnpq.br (N.S. Yokoya).

Authors’ contributions

LPM collected and identified seaweed samples, as well as carried out lab experiments, analyzed the data, and wrote the manuscript. LRC performed chemical and chromatographic analyses and provided critical reading of the manuscript. MCMY and EMCL performed laboratory experiments involving biological studies. DCC and LZV carried out chemical studies. PC and NSY designed the study, supervised the laboratory work and contributed to critical reading of the manuscript. All authors have read the final manuscript and approved the submission.

Conflicts of interest

Authors have no conflicts of interest to declare.

Seaweed	Fresh weight (g)	Dried extracts (g)	Yield (%)	R_f of AChEI compounds	Intensity of AChEI activity
Hypnea musciformis	200	1.82	0.91	0.01	Low
Pterocladiella capillacea	200	0.4	0.2	0.65	Low
Ochtodes secundiramea	200	2.82	1.41	0.62–0.71	Strong

Peak	Retention time (min)	(%) Area	Molecular mass m / z	M⁺−halogen	Main mass fragments (intensity of signal)	Molecular formula	Reference
1	18.036	5.23	136	–	41(50) 69(100) 78, 81(20) 93(90) 107(25) 119(50) 135(80) 136 (trace)	C₁₀H₁₆	Polzin and Rorrer (2003)Polzin, J.P., Rorrer, G.L., 2003. Halogenated monoterpene production by microplantlets of the marine red alga Ochtodes secundiramea within an airlift photobioreactor under nutrient medium perfusion. Biotechnol. Bioeng. 82, 415-428.
2	30.913	11.41	229; 230	149 (M⁺−Br)	41(40) 53(40) 79(70) 91(100) 105 (95) 122(85) 133(55) 149(80) 185(30) 229, 230(70)	C₁₀H₁₅OBr	Paul et al. (1980)Paul, V.J., McConnell, O.J., Fenical, W., 1980. Cyclic monoterpenoid feeding deterrents from the red marine alga Ochtodes crockeri. J. Org. Chem. 45, 3401-3407.
3	31.636	2.82	292; 294; 296	213(M⁺−Br) 133(M⁺ -Br₂)	41(15) 65(15) 77(20) 93(50) 105(40) 118(50) 133(100)	C₁₀H₁₄Br₂	Barahona and Rorrer (2003)Barahona, L.F., Rorrer, G.L., 2003. Isolation of halogenated monoterpenes from bioreactor-cultured microplantlets of the macrophytic red algae Ochtodes secundiramea and Portieria hornemannii. J. Nat. Prod. 66, 743-751.
4	36.215	3.09	248; 249; 251	214(M⁺−Cl) 167(M⁺−Br) 133 (M⁺−BrCl)	44(60) 51(10) 65(20) 77(30) 93(100) 105(40) 117(60) 133(60)167 169(20) 212 213(5)	C₁₀H₁₄BrCl	Burreson et al. (1975)Burreson, B.J., Woolard, F.X., Moore, R.M., 1975. Evidence for the biogenesis of halogenated myrcenes from the red alga Chondrococcus hornemanii. Chem. Lett. 4, 1111-1114.
5	39.856	13.82	311	229(M⁺−Br) 149 (M⁺−Br₂)	41(50) 55 (50) 65(40) 79(80) 91(100) 105(40) 118(60) 133(95) 149(25) 229(20)	C₁₀H₁₂OBr₂	Paul et al. (1980)Paul, V.J., McConnell, O.J., Fenical, W., 1980. Cyclic monoterpenoid feeding deterrents from the red marine alga Ochtodes crockeri. J. Org. Chem. 45, 3401-3407.
6	40.682	5.81	323;325	217 (M⁺−BrCl) 167 (M⁺−Br₂) 133(M⁺−Br₂Cl)	41(40) 65(30) 77(50) 93(95) 105(50) 117(60) 133(100) 167(40) 217(40)	C₁₀H₁₃Br₂Cl	Polzin et al. (2003)Polzin, J.J., Rorrer, G.L., Cheney, D.P., 2003. Metabolic flux analysis of halogenated monoterpene biosynthesis in microplantlets of the macrophytic red alga Ochtodes secundiramea. Biomol. Eng. 20, 205-215.
7	43.298	13.81	408; 410	375 (M⁺−Cl) 329 (M⁺−Br) 249 (M⁺−Br₂) 167(M⁺−Br3) 133 (M⁺−Br₃Cl)	41(10) 77(40) 91(50) 105(30) 117(50) 133(100) 167 197 213 249 294 329 375 (5)	C₁₀H₁₄Br₃Cl	Gerwick, 1984Gerwick, W.H., 1984. 2-Chloro-1,6 (S*),8-tribromo-3-(8) (Z)-ochtodene: a metabolite of the tropical red seaweed Ochtodes secundiramea. Phytochemistry 23, 1323-1324.
8	45.273	30.13	328; 330; 332	294 (M⁺−BrCl) 249 (M⁺−Br) 213 (M⁺−BrCl) 167 (M⁺−Br₂) 133 (M⁺−Br₂Cl)	69(15) 77(40) 93(50) 105(40) 133(100) 167(50) 213(5) 249(5) 294(3)	C₁₀H₁₅Br₂Cl	Coll and Wright (1987)Coll, J.C., Wright, A.D., 1987. Tropical marine algae. I. New halogenated monoterpenes from Chondrococcus hornemannii (Rhodophyta, Gigartinales, Rhizophyllidaceae). Aust. J. Chem. 40, 1893-1900.
9	46.900	2.52	344; 346; 348	310 (M⁺−Cl) 267 (M⁺−Br) 229 (M⁺−BrCl) 185(M⁺−Br₂) 147 (M⁺−Br₂Cl)	65(20) 77(30) 91(100) 105(40) 117(60) 133(60); 147(15) 185, 187 (20) 197, 199(5) 212, 213(5) 229(10); 267 269(5) 285 287 (5); 310 311(5)	C₁₀H₁₅Br₂C_lO	Naylor et al. (1983)Naylor, S., Hanke, F.J., Manes, L.V., Crews, P., 1983. Chemical and biological aspects of marine monoterpenes. Fortschritte der Chemie Organischer Naturstoffe/Prog. Chem. Org. Nat. Prod. 44, 189-241.
10	47.972	18.36	360; 362; 364	329 (M⁺−Cl) 294(M⁺−Cl₂) 284 (M⁺−Br₂) 247 (M⁺−BrCl) 213 (M⁺−BrCl₂) 167 (M⁺−Br₂Cl) 133 (M⁺−Br₂Cl₂)	77(40) 91(50) 105 (30) 117(50) 133(100) 167(80) 213(40) 247(15) 284(20) 294(15) 329 (5)	C₁₀H₁₄Br₂C_l2	Coll et al. (1988)Coll, J.C., Skelton, B.W., White, A.H., Wright, A.D., 1988. Tropical marine algae. II. The structure determination of new halogenated monoterpenes from Plocamium hamatum (Rhodophyta, Gigartinales, Plocamiaceae). Aust. J. Chem. 41, 1743-1753.

[1] * Corresponding author. E-mail:nyokoya@pq.cnpq.br (N.S. Yokoya).

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Evaluation of acetylcholinesterase inhibitory activity of Brazilian red macroalgae organic extracts

Abstract