Methanol extracts from Cystoseira tamariscifolia and Cystoseira nodicaulis are able to inhibit cholinesterases and protect a human dopaminergic cell line from hydrogen peroxide-induced cytotoxicity

Figures & data

Table 1. Radical scavenging activity (RSA) on DPPH radicals of methanol extracts of different species of macroalgae.

	Concentration
Phylum/species	1 mg/mL	5 mg/mL	10 mg/mL
Ochrophyta
Cystoseira tamarascifolia	92.0 ± 0.7^a	nt	nt
C. usneoides	37.1 ± 0.5^d	102.1 ± 1.0^a	109.0 ± 1.1^a
C. nodicaulis	39.6 ± 2.4^d	75.7 ± 0.7^b	95.1 ± 1.6^a
C. baccata	21.6 ± 1.9^f	65.4 ± 1.7^c	90.4 ± 0.9^a
C. humilis	8.8 ± 2.5^i	24.9 ± 2.8^e	41.1 ± 1.8^c
Dictyota dichotoma	8.2 ± 0.5^i	19.4 ± 1.2^f	44.4 ± 1.0^c
D. spiralis	2.20 ± 0.5^l	32.9 ± 0.7^d	64.9 ± 0.9^b
Sargassum vulgare	30.6 ± 0.9^e	80.3 ± 0.6^b	98.2 ± 0.4^a
S. muticum	13.7 ± 0.4^g	38.3 ± 1.4^d	58.2 ± 0.7^b
Taonia atomaria	18.7 ± 0.4^f	17.9 ± 0.6^f	25.9 ± 0.9^e
Rhodophyta
Asparagopsis armata	8.6 ± 0.5^i	13.3 ± 0.2^g	23.9 ± 0.3^e
Peyssonnelia sp.	8.0 ± 0.5^i	23.2 ± 0.9^e	40.5 ± 1.0^c
P. squamaria	2.9 ± 0.6^l	3.6 ± 0.7^h	4.7 ± 0.7^g
Pterocladiella capillacea	5.2 ± 0.7^k	10.2 ± 0.6^g	12.9 ± 0.6^f
Jania sp.	6.9 ± 0.7^j	18.1 ± 0.7^f	31.1 ± 0.9^d
Chlorophyta
Chaetomorpha sp.	9.4 ± 0.4^h	17.2 ± 1.0^f	34.9 ± 1.8^d
Codium fragile	−6.7 ± 0.7^m	9.0 ± 0.6^g	10.8 ± 0.6^f
Codium sp	4.6 ± 0.6^k	10.5 ± 0.6^g	15.8 ± 0.5^f
Enteromorpha sp.	12.0 ± 0.5^g	12.9 ± 0.5^g	25.1 ± 0.5^e
Ulva sp.	10.3 ± 0.6^g	5.5 ± 0.8^h	16.0 ± 0.8^f
Cladophora albida	9.8 ± 0.6^h	23.2 ± 0.8^e	41.2 ± 1.4^c
BHT*	95.1 ± 2.2^a	nt	nt

Values represent average ± standard error (n = 9); nt, not tested;

* positive control. For the same column, different letters are significantly different (Duncan’s new multiple range test, p < 0.05).

Table 2. Metal chelating activity on iron and copper of methanol extracts of different species of macroalgae.

	Metal chelating activity on iron			Metal chelating activity on copper
Phylum/species	1 mg/mL	5 mg/mL	10 mg/mL	1 mg/mL	5 mg/mL	10 mg/mL
Ochrophyta
Cystoseira tamarascifolia	7.1 ± 0.3^d	8.8 ± 0.4^de	12.0 ± 0.6^f	11.2 ± 1.7^d	21.5 ± 0.9^bc	33.2 ± 0.8^c
C. usneoides	7.2 ± 1.0^d	13.2 ± 1.2^cd	12.4 ± 1.2^f	21.0 ± 1.4^cd	33.0 ± 1.0^b	44.3 ± 0.5^b
C. nodicaulis	19.0 ± 1.2^b	48.0 ± 2.5^a	75.0 ± 1.6^a	40.0 ± 1.8^b	42.3 ± 4.1^ab	54.0 ± 6.1^ab
C. baccata	16.2 ± 0.5^b	36.1 ± 1.7^ab	57.2 ± 1.0^bc	28.3 ± 7.5^c	48.7 ± 1.3^a	66.3 ± 0.8^a
C. humilis	16.0 ± 2.0^b	43.0 ± 4.2^a	70.4 ± 2.8^a	31.1 ± 4.8^c	42.3 ± 5.7^ab	47.2 ± 7.1^b
Dictyota dichotoma	25.3 ± 1.4^b	42.3 ± 1.0^a	52.3 ± 1.3^bc	19.0 ± 1.0^cd	26.0 ± 2.4^bc	46.4 ± 0.4^b
D. spiralis	20.0 ± 1.5^b	39.0 ± 3.2^ab	48.1 ± 2.0^c	18.9 ± 0.6^cd	38.2 ± 0.9^b	56.0 ± 0.7^ab
Sargassum vulgare	12.1 ± 1.1^c	28.3 ± 2.7^b	28.3 ± 3.5^de	18.2 ± 1.1^cd	43.2 ± 1.0^ab	55.0 ± 1.0^ab
S. muticum	9.7 ± 0.8^c	23.2 ± 2.1^bc	45.0 ± 1.4^c	28.3 ± 3.1^c	28.5 ± 3.0^bc	54.8 ± 1.7^ab
Taonia atomaria	12.4 ± 1.5^c	15.4 ± 1.7^c	17.2 ± 1.7^ef	19.0 ± 0.8	35.2 ± 1.0^b	55.1 ± 1.0^ab
Rhodophyta
Asparagopsis armata	11.0 ± 1.4^c	31.0 ± 3.6^b	34.0 ± 1.8^d	17.4 ± 1.1^cd	24.0 ± 0.9^bc	17.3 ± 0.5
Peyssonnelia sp.	6.9 ± 0.6^d	13.1 ± 1.0^cd	24.6 ± 2.1^e	18.2 ± 1.6^cd	43.3 ± 0.8^ab	59.2 ± 0.8^ab
P. squamaria	13.2 ± 1.2^c	15.6 ± 0.6^cd	23.2 ± 0.9^e	27.0 ± 4.5^c	24.0 ± 4.4^bc	18.4 ± 4.1^d
Pterocladiella capillacea	8.1 ± 0.7^d	23.3 ± 2.5^bc	32.1 ± 1.2^d	19.3 ± 1.6^cd	47.4 ± 0.5^a	62.0 ± 0.4^a
Jania sp.	5.3 ± 1.2^d	25.0 ± 2.1^bc	60.8 ± 2.6^b	na	10.1 ± 2.2^c	28.1 ± 0.8
Chlorophyta
Chaetomorpha sp.	5.9 ± 0.8^d	6.2 ± 1.0^e	9.4 ± 1.0^f	10.2 ± 1.0^d	22.9 ± 0.9^bc	38.3 ± 0.7^bc
Codium fragile	11.0 ± 2.2^c	14.1 ± 3.3^c	22.0 ± 2.2^e	11.4 ± 1.2^d	20.0 ± 1.0^bc	26.0 ± 0.8^c
Codium sp	5.5 ± 1.1^d	17.3 ± 2.6^c	22.3 ± 3.3^e	10.8 ± 1.2^d	23.2 ± 0.8^bc	33.7 ± 1.2^c
Enteromorpha sp.	7.0 ± 1.3^d	15.0 ± 1.7^c	30.2 ± 1.9^d	16.0 ± 2.0^d	37.1 ± 1.4^b	56.1 ± 1.1^ab
Ulva sp.	8.0 ± 1.7^d	12.2 ± 1.2^d	20.4 ± 1.4^e	17.2 ± 0.7^cd	35.3 ± 0.9^b	53.3 ± 0.6^ab
Cladophora albida	12.3 ± 4.3^c	11.0 ± 1.1^d	19.7 ± 0.7^e	12.0 ± 1.4^d	38.0 ± 0.9^b	62.0 ± 1.5^a
EDTA*	97.1 ± 1.3^a	nt	nt	86.3 ± 6.0^a	nt	nt

Values represent average ± standard error (n = 9); na, no activity; nt, not tested;

* positive control. For the same column, different letters are significantly different (Duncan’s new multiple range test, p < 0.05).

Table 3. Acetylcholinesterase (AChE) inhibitory activity of methanol extracts of different species of macroalgae.

	Concentration
Phylum/species	1 mg/mL	5 mg/mL	10 mg/mL
Ochrophyta
Cystoseira tamarascifolia	70.1 ± 2.5^b	80.6 ± 2.9^a	85.3 ± 2.5^a
C. usneoides	20.2 ± 1.4^d	40.2 ± 2.0^c	47.1 ± 1.8^d
C. nodicaulis	46.2 ± 5.9^c	61.0 ± 3.5^b	64.4 ± 1.9^b
C. baccata	na	na	34.7 ± 4.7^e
C. humilis	24.6 ± 2.7^d	39.2 ± 1.7^c	50.1 ± 2.4^cd
Dictyota dichotoma	na	8.1 ± 1.6^ef	2.7 ± 0.5^g
D. spiralis	na	na	na
Sargassum vulgare	29.3 ± 1.2^d	32.0 ± 2.7^cd	45.2 ± 1.7^d
S. muticum	6.1 ± 0.6^f	31.4 ± 4.0^cd	39.3 ± 1.9^e
Taonia atomaria	12.0 ± 2.5^e	28.3 ± 3.3^d	40.5 ± 3.5^de
Rhodophyta
Asparagopsis armata	13.2 ± 2.2^e	26.0 ± 2.4^d	58.4 ± 1.0^c
Peyssonnelia sp.	na	5.1 ± 0.7^f	13.0 ± 2.6^f
P. squamaria	11.5 ± 1.4^e	22.2 ± 3.9^d	na
Pterocladiella capillacea	9.3 ± 1.3^ef	11.0 ± 1.5^e	10.1 ± 0.9^f
Jania sp.	na	na	na
Cladophora albida	na	na	12.3 ± 6.5^f
Chlorophyta
Chaetomorpha sp.	8.7 ± 0.4^f	6.7 ± 1.1^ef	6.9 ± 1.0^g
Codium fragile	na	12.0 ± 1.6^e	11.9 ± 2.8^f
Codium sp	na	na	na
Enteromorpha sp.	3.0 ± 0.8^g	6.7 ± 0.9^ef	8.2 ± 1.7^fg
Ulva sp.	na	12.4 ± 1.6^e	19.7 ± 2.5^f
Galanthamine*	90.3 ± 0.6^a	nt	nt

Values represent average ± standard error (n = 9); na: no activity; nt: not tested;

* positive control. For the same column, different letters are significantly different (Duncan’s new multiple range test, p < 0.05).

Table 4. Butyrylcholinesterase (BuChE) and tyrosinase (TYRO) inhibitory activity of methanol extracts of selected species of macroalgae.

	BuChE			TYRO
Species/compound	1 mg/mL	5 mg/mL	10 mg/mL	1 mg/mL	5 mg/mL	10 mg/mL
Cystoseira. tamarascifolia	83.2 ± 0.6^a	97.3 ± 0.9^a	100.0 ± 1.5^a	45.3 ± 3.8^c	56.0 ± 5.1^b	86.3 ± 8.7^a
C. nodicaulis	84.5 ± 0.7^a	91.2 ± 0.6^a	92.7 ± 0.7^b	85.6 ± 2.1^a	90.1 ± 4.8^a	110.1 ± 8.4^a
Asparagopsis armata	33.4 ± 4.1^b	55.0 ± 3.1^b	66.8 ± 1.3^c	36.3 ± 3.5^c	54.0 ± 8.6^b	81.4 ± 5.2^a
Galanthamine*	80.3 ± 0.1^a	nt	nt	-	-	-
Arbutin*	-	-	-	78.0 ± 0.1^b	nt	nt

Values represent average ± standard error (n = 9); nt, not tested;

* positive control. For the same column, different letters are significantly different (Duncan’s new multiple range test, p < 0.05).

Figure 1. Protective effect of methanol extracts of C. tamariscifolia and C. nodicaulis in SH-SY5Y cells. Cells were pre-treated with different concentrations of the extracts for 24 h, and exposed to 3.12 μM of H₂O₂. Each value represents the mean ± SEM of three replicates. Significantly different than that of the H₂O₂-treated group: *p < 0.05; **p < 0.01.

Table 5. Bioactive constituents (mg/g, dry weight) of methanol extracts of C. tamariscifolia and C. nodicaulis.

Class of compound	C. tamariscifolia	C. nodicaulis
Total phenols (F–C)^1	105.0 ± 6.9^a	59.9 ± 3.7^b
Hydroxycinnamic acids^2	106 ± 2.0^a	9.79 ± 0.5^b
Flavone and flavonols^3	25.1 ± 0.6^a	4.15 ± 0.29^b
Total condensed tannins^4	64.2 ± 1.0^a	4.23 ± 0.78^b

Values are mean ± SD (n = 6).

¹mg GAE/g DW;

²mg CAE/g DW;

³mg QE/g DW;

⁴mg CE/g DW. For the same row, different letters are significantly different (Duncan’s new multiple range test, p < 0.05).