Polyacanthoside A, a new oleanane-type triterpenoid saponin with cytotoxic effects from the leaves of Acacia polyacantha (Fabaceae)

Article abstract of DOI:10.1080/14786419.2018.1486312

The chemical investigation of the leaves and stem bark of Acacia polyacantha (Fabaceae) led to the isolation of a new oleanane-type triterpenoid saponin named polyacanthoside A 1 together with fifteen known compounds. Their structures were established from spectral, mainly HRESIMS, 1D NMR and 2D NMR and by comparison with literature data. The cytotoxicity of compound 1 and the analogues 8 as well as doxorubicin was determined in a panel of 9 cancer cell lines including sensitive and drug resistant phenotypes. Unlike the analogue 8, compound 1 as well as doxorubicin displayed cytotoxic effects in all the 9 tested cancer cell lines with IC₅₀ values ranged from 8.90 μM (towards CCRF-CEM leukemia cells) to 35.21 μM (towards HepG2 hepatocarcinoma cells) for compound 1 and from 0.02 μM (towards CCRF-CEM leukemia cells) to 66.83 μM (against CEM/ADR5000 leukemia cells) for doxorubicin.

Full text of DOI:10.1080/14786419.2018.1486312

Natural Product Research
Formerly Natural Product Letters
ISSN: 1478-6419 (Print) 1478-6427 (Online) Journal homepage: http://www.tandfonline.com/loi/gnpl20
Polyacanthoside A, a new oleanane-type
triterpenoid saponin with cytotoxic effects from
the leaves of Acacia polyacantha (Fabaceae)
Ghislain Fotso W., Jean Na-Iya, Armelle Mbaveng T., Patrick Ango Yves,
Ibrahim Demirtas, Victor Kuete, Yeboah Samuel, Bathelemy Ngameni,
Thomas Efferth & Bonaventure Ngadjui T.
To cite this article: Ghislain Fotso W., Jean Na-Iya, Armelle Mbaveng T., Patrick Ango Yves,
Ibrahim Demirtas, Victor Kuete, Yeboah Samuel, Bathelemy Ngameni, Thomas Efferth &
Bonaventure Ngadjui T. (2018): Polyacanthoside A, a new oleanane-type triterpenoid saponin with
cytotoxic effects from the leaves of Acacia polyacantha (Fabaceae), Natural Product Research,
DOI: 10.1080/14786419.2018.1486312
To link to this article: https://doi.org/10.1080/14786419.2018.1486312
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Natural Product research, 2018
https://doi.org/10.1080/14786419.2018.1486312
Polyacanthoside A, a new oleanane-type triterpenoid saponin
with cytotoxic effects from the leaves of Acacia polyacantha
(Fabaceae)
Ghislain Fotso W.a, Jean Na-Iyaa, Armelle Mbaveng T.b,c, Patrick Ango Yvesa,
Ibrahim Demirtasd , Victor Kuetec, Yeboah Samuele, Bathelemy Ngamenif,
Thomas Efferthb and Bonaventure Ngadjui T.a,f
adepartment of organic chemistry, Faculty of science, university of Yaoundé I, Yaoundé, cameroon;
bdepartment of Pharmaceutical Biology, Institute of Pharmacy and Biochemistry, university of Mainz, Mainz,
Germany; cdepartment of Biochemistry, Faculty of science, university of dschang, dschang, cameroon;
e
ddepartment of chemistry, cankiri Karatekin university, Istanbul, turkey; department of chemistry, Faculty
of science, university of Botswana, Gaborone, Botswana; fdepartment of Pharmacognosy and Pharmaceutical
chemistry, Faculty of Medicine and Biomedical science, university of Yaoundé I, Yaoundé, cameroon
ABSTRACT
ARTICLE HISTORY
received 6 april 2018
accepted 31 May 2018
The chemical investigation of the leaves and stem bark of Acacia
polyacantha (Fabaceae) led to the isolation of a new oleanane-
type triterpenoid saponin named polyacanthoside A 1 together
with fifteen known compounds. Their structures were established
from spectral data, mainly HRESIMS, 1D NMR and 2D NMR and by
comparison with literature data. The cytotoxicity of compound 1 and
the analogues 8 as well as doxorubicin was determined in a panel of
9 cancer cell lines including sensitive and drug resistant phenotypes.
Unlike the analogue 8, compound 1 as well as doxorubicin displayed
cytotoxic effects in all the 9 tested cancer cell lines with IC50 values
ranged from 8.90 μM (towards CCRF-CEM leukemia cells) to 35.21 μM
(towards HepG2 hepatocarcinoma cells) for compound 1 and from
0.02 μM (towards CCRF-CEM leukemia cells) to 66.83 μM (against CEM/
ADR5000 leukemia cells) for doxorubicin.
KEYWORDS
Acacia polyacantha;
Fabaceae; polyacanthoside a;
3-O-methyl-d-chiro-inositol;
drug resistant phenotypes;
cytotoxicity; leukemia cells
CONTACT Ghislain Fotso W.
ghis152001@yahoo.fr; Bathelemy Ngameni
bath_ngameni@yahoo.fr
the supplemental data for this article can be accessed at https://doi.org/10.1080/14786419.2018.1486312.
© 2018 Informa uK limited, trading as taylor & Francis Group

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G. FOTSO W. ET AL.
1. Introduction
Acacia species are used in folk medicine by rural population as a remedy for tuberculosis,
leprosy, small pox, dysentery, cough, ophthalmic, toothache, skin ulcers, cancer, as astrin-
gents, antispasmodics, and aphrodisiac (Khidir 2009). Acacia polyacantha is one of the plants
used by farmers to treat livestock diseases, such as Salmonellosis and gastrointestinal dis-
eases in general (Koudoro et al. 2015). The genus Acacia is known to be a rich source of tri-
terpenoidal saponins (Youngwan et al. 2002; Jayatilake et al. 2003; Tchoukoua et al. 2017,
2018). Plants of this genus displayed a wide range of biological activities such as antibacterial,
cytototoxic or enzyme inhibitory effects (Jæger et al. 2018). As part of our search of anti-can-
cer secondary metabolites from the Fabaceae family (Fotso et al. 2017) we have carried out
the chemical investigation of the leaves and stem bark of Acacia polyacantha. The present
work describes the isolation of a new oleane-type triterpenoid saponin from leaves of that
plant together with the evaluation of the cytotoxicity of the new compound in a panel of 9
cancer cell lines including sensitive and drug resistant phenotypes.
2. Results and discussion
The intensive purification of the leaves extract of A. polyacantha resulted on the isolation of
eight compounds among which a new oleanane-type triterpenoid saponin, named polya-
canthoside A or 3-O-[β-D-xylopyranosyl-(1→4)-β-D-galactopyranosyl]-oleanolic acid (1) and
seven known compounds including: oleanolic acid (2) (Kuete et al. 2007), stigmasterol (3)
(Chaturvedula and Prakash 2012), stigmasterol-3-O-β-glucopyranosyl (4) (Freire et al. 2005),
epicatechin (5) (Adnyana et al. 2000), quercetin-3-O-glucoside (6) (Xu et al. 2012), 3-O-methyl-
D-Chiro-inositol (7) (Sharma et al. 2016) and 3-O-[β-D- galactopyranosyl-(1→4)-β-D-ga-
lactopyranosyl]-oleanolic acid (8) (Chaturvedula et al. 2003). The same protocol on the stem
bark of A. polyacantha afforded nine compounds identified as epicatechin (5) (Adnyana
et al. 2000), lupeol (9) (Fotso et al. 2014), β-sitosterol (10) (Chaturvedula and Prakash 2012),
betulin (11) (Fotso et al. 2014), betulinic acid (12) (Kuete et al. 2007), apigenin (13) (Fajriah
and Megawati 2016), methylgallate (14) (Choi et al. 2009), 2,3-dihydroxypropyltetracosa-
noate (15) (Lee et al. 2000) and 2,3-dihydroxypropyl-24- hydroxytetracosanoate (16) (Lee
et al. 2000). (Figure S1, Supplementary data).
Compound 1 was obtained as a beige crystal, mp: 216–217 °C, soluble in methanol. It
showed positive Molish and Liebermann–Burchard reactions demonstrating its saponin
nature (Zheng et al. 2010). Its molecular formula C41H66O12 was deduced from its HRESIMS
in positive-ion mode which exhibited a pseudo-molecular ion peak [M + Na]+ at m/z
773.4395 (calcd 773,4452 for C41H66O12Na+) (Figure S1, Supplementary data). Its IR spectrum
(Figure S2, Supplementary data) displayed characteristic bands of bands for hydroxyl, car-
boxylic acid and alkene respectively at 3358, 1688 and 1637 cm−1 respectively. Based on
the reported method (Tchoukoua et al. 2017) compound 1 was hydrolyzed to give an
oleanolic acid identified by co-TLC with an authentic sample and the monosaccharides
(D-galactose and D-xylose. This was in accordance with the molecular formula of 1, C41H66O12
corresponding to a triterpene (C-30) linked to a hexose (C-6) and a pentose (C-5). The 1H
and 13C NMR data of 1 (Table S1, Supplementary data) coupled with its HSQC and DEPT
spectra (Figures S2−S6, Supplementary data) displayed characteristic signals for oleanane
triterpenoid (Krief et al. 2005) with seven angular methyl groups as singlets at δH/δC 0.81/16.3,

NATURAL PRODUCT RESEARCH
3
0.84/15.6, 0.90/32.2, 0.93/22.6, 0.94/14.5, 1.05/27.1 and 1.15/25.0; a double bond between
C-12 and C-13 in the aglycone at δc 122.2 and 143.8 respectively; The HSQC spectrum of 1
also displayed the signals of two anomeric protons at δ 4.83 (d, J = 7.8 Hz, 2H) correlating
with the anomeric carbon signals at δ 104.0 and 105.1. Based on the high coupling constants
of the anomeric protons and the chemical shifts of the anomeric carbons, the anomeric
configurations of the sugar moieties were determined as β for the two sugars. The high
chemical shift of C-28 (δc 180.5) also indicated that 1 is a monodesmodic type triterpenoidal
saponin with the two sugars units linked at C-3 (Debella et al. 2000). At this point, the struc-
ture of 1 was closely similar to the one of Polyfoliolide A or 3-O-β-D-galactopyranosyl-(1→4)-
β-D-xylopyranosyloleanolic acid isolated from the infrutescences of Polyscias amplifolia
(Chaturvedula et al. 2003). However, the HMBC spectrum of 1 (Figures S7c and S7d,
Supplementary data) showed correlations between H-1′ of Gal (δH 4.34) and C-3 of the
aglcone (δc 89.5) and between H-3 of the aglycone (δH 3.16) and C-1′ of Gal (δc 105.1). In
addition, the two diastereotopic protons of the D-xylose at δH 3.26 and 3.90 were shown to
correlate with the second anomeric carbon at δc 104.0 and C-4″ of Xyl at δc 69.5. This allowed
us to suggest that 1 has a terminal β-xylopyranosyl and a 4-substituted β- galactopyranoxyl
unit linked to the aglycone at C-3. This was in accordance with the high chemical shift of
C-4 of Gal (δc 79.5) due to the effect of the O-glycosylation. The connectivity of the two
sugar units was confirmed by the HMBC spectrum of 1 (Figures S7c, Supplementary data)
in which a correlation was observed between H-4′ of Gal (δH 3.50) and C-1″ of Xyl (δc 104.0).
This was also confirmed by the HRESIMS spectra of 1 (Figures S1, Supplementary data) in
positive mode in which the ion fragment [M− CO2− xylose + 2H]++ resulting from the lost
of the terminal xylose was observed at m/z 575. The ion fragment [M − CO2− xylose−
galactose + H ]+ at m/z 409 coming from the lost of the second sugar unit was also observed.
To further confirm the terminal xylopyranosyl group, the partial hydrolysis of 1with oxalic
acid was performed and afforded the known 3-O-β-D-galactopyranosyloleanolic acid
(Elujoba et al. 1990) (Figures S8–9, Supplementary data). Compound 1 was then univocally
characterized as 3-O-[β-D-xylopyranosyl-(1→4)-β-D-galactopyranosyl]-oleanolic acid. To the
best of our knowledge 1 is a new triterpenoid saponin to which the trival name polyacan-
thoside A was given.
Compound 1 as well as doxorubicin displayed cytotoxic effects in all the nine tested
cancer cell lines (Table S2, Supplementary data). The recorded IC50 values ranged from
8.90 0.58 μM (towards CCRF-CEM leukemia cells) to 35.21 1.51 μM (towards HepG2 hepa-
tocarcinoma cells) for compound 1 and from 0.02 0.00 μM (towards CCRF-CEM leukemia
cells) to 66.83 2.20 μM (against CEM/ADR5000 leukemia cells) for doxorubicin. Significant
cytotoxic activity with IC50 values 10 μM (Kuete and Efferth 2015) was obtained with com-
pound 1 towards CCRF-CEM cells. Hypersensitivity (degree of resistance or D.R. below 0.90)
(Mbaveng et al. 2017) of MDA-MB231/BCRP breast adenocarcinoma cells compared to it
sensitive parental cell line MDA-MB231 cells was noted with compounds 1 (Table S2,
Supplementary data); Besides, the D.R. of this compound towards the resistant cells
HCT116(p53-/-) cells, U87MG.ΔEGFR cells was also below 1. In addition, the D.R. of compound
1 in all tested resistant cancer cell lines was lower than that of doxorubicin. This is an indi-
cation that this compound could be helpful in the fight against multi-drug resistant (MDR)
cancer cells. Though the selectivity index of this compound was below 1, it was still better
than that of the reference drug, doxorubicin. The overall data highlight the possibility of
using compound 1 to fight drug sensitive and resistant cancers. For a comparative study of

4
G. FOTSO W. ET AL.
1 with compound 8, a preliminary study was performed in the sensitive CCRF-CEM leukemia
cells; however this compound rather showed low cytotoxic effects with a recorded IC50 values
35.16 μM; Consequently it was no further tested in other cancer cell lines; This clearly indi-
cates that the presence of galactopyranosyl sugar unit (Compound 8) instead of xylopyra-
nosyl (Compound 1) significantly reduce the cytotoxicity towards CCRF-CEM cells (Table S2,
Supplementary data).
3. Experimental (Supplementary data)
3.1. 3-O-[β-D-xylopyranosyl-(1→4)-β-D-galactopyranosyl]-oleanolic acid
Beige crystals; mp: 216–217 °C;[ꢀ]2D5: +23.2° (c 1.25, MeOH); IR (KBr, ν, cm−1): 3358, 2940, 1688,
1637, 1512, 1461, 1160, 1024; 1H NMR (MeOD, 600 MHz): aglycone: 3.16 (1H, dd; 11.9, 3.8, H-3),
5.23 (1H, brs, H-12), 1.05 (3H, s, H-23), 0.84 (3H, s, H-24), 0.94 (3H, s, H-25), 0.81 (3H, s, H-26),
1.15 (3H, s, H-27), 0.90 (3H, s, H-29), 0.93 (3H, s, H-30), sugar moiety: 4.34 (1H, d, 7.7, H-1′), 3.23
(d, 4.7, H-2′), 3.45 (1H, d, 8.9, H-3′), 3.50 (1H, d, 8.9, H-4′), 3.38 (1H, d, 9.2, H-5′), 3.84 (2H, brs,
H-6′), 4.34 (1H, d, 7.7, H-1″), 3.20 (1H, d, 8.5, H-2″), 3.32 (1H, d, 9.2, H-3″), 3.48 (1H, m, H-4″), 3.90
(1H, dd; 11.3, 5.2, H-5″eq), 3.26 (1, d, 10.4, H-5″ax); 13C NMR (MeOD, 150 MHz): aglycone: 38.4
(C-1), 25.6 (C-2), 89.5 (C-3), 38.7 (C-4), 55.6 (C-5), 17.9 (C-6), 32.6 (C-7), 41.3 (C-8), 47.6 (C-9), 36.5
(C-10), 23.1 (C-11), 122.2 (C-12), 143.8 (C-13), 41.5 (C-14), 27.4 (C-15), 22.7 (C-16), 46.2 (C-17),
39.2 (C-18), 45.8 (C-19), 30.2 (C-20), 33.5 (C-21), 32.4 (C-22), 27.1 (C-23), 15.6 (C-24), 14.5 (C-25),
16.3 (C-26), 25.0 (C-27), 180.5 (C-28), 32.2(C-29), 22.6 (C-30), sugar moiety: 105.1 (C-1′), 74.0
(C-2′), 74.9 (C-3′), 79.5 (C-4′), 74.6 (C-5′), 60.6 (C-6′), 104.0 (C-1″), 73.5 (C-2″), 76.4 (C-3″), 69.5
(C-4″), 65.7 (C-5″); HRESIMS m/z: 773.4395 [M + Na]+ (calcd 773,4452 for C41H66O12Na+), m/z
575 [M− CO2− xylose + 2H]++, m/z 409 [M − CO2− xylose− galactose + H ]+.
4. Conclusion
This work reports the chemical investigation of the leaves and stem bark of Acacia polya-
cantha from which a new oleanane-type triterpenoid saponin named polyacanthoside A
was isolated. The cytotoxicity of polyacanthoside A was evaluated in a panel of 9 cancer cell
lines including sensitive and drug resistant phenotypes. This compound showed significant
cytotoxic activity especially on leukemia cells with a hypersensitivity on some resistant cancer
cell lines demonstrating the interesting anticancer potential.
Supplementary material
Experimental section, NMR, MS and cytotoxicity data of compound 1 and all the isolated compounds
are available alongside Figures S1–S10, Table S1-S2.
Acknowledgements
G.W.F is grateful to the Network of Analytical and Bioassay Services in Africa (NABSA) for two months
financial support (Travel grant and maintenance allowance) at the University of Botswana. ATM is
thankful to Alexander von Humboldt Foundation for an 18 months fellowship in Prof. Dr. Thomas
Efferth’s laboratory in Mainz, Germany through the‘‘Georg Foster Research Fellowship for Experienced
Researcher program. VK is very grateful to the Alexander von Humboldt Foundation for the funding
through the Linkage program (2015–2018).

NATURAL PRODUCT RESEARCH
5
Disclosure statement
No potential conflict of interest was reported by the authors.
ORCID
Ibrahim Demirtas
http://orcid.org/0000-0001-8946-647X
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