Tumor-suppressing effect of bartogenic acid in ovarian (SKOV-3) xenograft mouse model.
Animals
Antineoplastic Agents, Phytogenic
/ administration & dosage
Antineoplastic Combined Chemotherapy Protocols
/ administration & dosage
Cell Line, Tumor
Female
Humans
Inhibitory Concentration 50
Mice
Mice, SCID
NF-kappa B
/ metabolism
Ovarian Neoplasms
/ drug therapy
Paclitaxel
/ administration & dosage
Triterpenes
/ administration & dosage
Xenograft Model Antitumor Assays
Barringtonia racemosa
Bartogenic acid
NF-κB
Ovarian tumor
SKOV-3
Journal
Naunyn-Schmiedeberg's archives of pharmacology
ISSN: 1432-1912
Titre abrégé: Naunyn Schmiedebergs Arch Pharmacol
Pays: Germany
ID NLM: 0326264
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
received:
19
10
2020
accepted:
07
04
2021
pubmed:
14
7
2021
medline:
11
1
2022
entrez:
13
7
2021
Statut:
ppublish
Résumé
Bartogenic acid (BA), a natural pentacyclic triterpenoid, proved to have chemomodulatory, anticancer, antidiabetic, anti-arthritic, and anti-inflammatory activity. Based on structure-activity relationship (SAR) approaches, BA has close structural resemblance to oleanolic acid and ursolic acid. These two pentacyclic triterpenoids are well accepted with respect to their therapeutic value in various ailments including anti-cancer activity. The aim of this study is to evaluate the efficacy of BA as a possible antitumor agent, along with its safety in SKOV-3 ovarian cancer. In vitro cytotoxicity of BA and paclitaxel on human ovarian cancer cells (SKOV-3) was assessed using MTT assay. Antitumor potential of BA alone, standard anticancer drug (paclitaxel) alone, and BA in combination with paclitaxel were evaluated in SKOV-3 xenografted SCID mice. Immunohistochemical analysis of NF-κB was performed and analyzed in SKOV-3 tumors. BA alone and BA in combination with paclitaxel significantly inhibited the tumor growth. IC
Identifiants
pubmed: 34255109
doi: 10.1007/s00210-021-02088-0
pii: 10.1007/s00210-021-02088-0
doi:
Substances chimiques
Antineoplastic Agents, Phytogenic
0
NF-kappa B
0
Triterpenes
0
bartogenic acid
0
Paclitaxel
P88XT4IS4D
Types de publication
Comparative Study
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1815-1826Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Akhtar MF, Saleem A, Rasul A, Faran Ashraf Baig MM, Bin-Jumah M, Abdel Daim MM (2020) Anticancer natural medicines: an overview of cell signaling and other targets of anticancer phytochemicals. Eur J Pharmacol. https://doi.org/10.1016/j.ejphar.2020.173488
doi: 10.1016/j.ejphar.2020.173488
pubmed: 33271153
An JH, Kim GJ, Jo HJ, Lee KJ, Choi JW (2018) Oleanolic acid induces p53-dependent apoptosis via the ERK/JNK/AKT pathway in cancer cell lines in prostatic cancer xenografts in mice. Oncotarget 9(41):26370–26386
doi: 10.18632/oncotarget.25316
Belotti D, Paganoni P, Manenti L, Garofalo A, Marchini S, Taraboletti G, Giavazzi R (2003) Matrix metalloproteinases (MMP9 and MMP2) induce the release of vascular endothelial growth factor (VEGF) by ovarian carcinoma cells: implications for ascites formation. Cancer Res 63(17):5224–5229
pubmed: 14500349
Bishayee A, Ahmed S, Brankov N, Perloff M (2011) Triterpenoids as potential agents for the chemoprevention and therapy of breast cancer. Front Biosci 16:980–996
doi: 10.2741/3730
Chiang YC, Chen CA, Chiang CJ, Hsu TH, Lin MC, You SL, Lai M, Cheng WF, Lai MS (2013) Trends in incidence and survival outcome of epithelial ovarian cancer: 30-year national population-based registry in Taiwan. J Gynecol Oncol 4:342–351. https://doi.org/10.3802/jgo.2013.24.4.342
doi: 10.3802/jgo.2013.24.4.342
Feng XM, Su XL (2019) Anticancer effect of ursolic acid via mitochondria-dependent pathways (Review). Oncol Lett 17:4761–4767. https://doi.org/10.3892/ol.2019.10171
doi: 10.3892/ol.2019.10171
pubmed: 31186681
pmcid: 6507317
Ge GB, Zou LW, Dou TY, Wang P, Lei W, Weng ZM, Hou J, Wang DD, Fan YM, Zhang WD, Yang L (2017) Structure activity relationship of pentacyclic triterpenoids as potent and selective inhibitors against human carboxylesterase 1. Front Pharmacol 8:435. https://doi.org/10.3389/fphar.2017.00435
doi: 10.3389/fphar.2017.00435
pubmed: 28713276
pmcid: 5491650
Gowri PM, Tiwari AK, Ali AZ, Rao JM (2007) Inhibition of α-glucosidase and amylase by bartogenic acid isolated from Barringtonia racemosa Roxb. Seeds. Phytother Res 21:796–799. https://doi.org/10.1002/ptr.2176
doi: 10.1002/ptr.2176
pubmed: 17533638
Gowri PM, Radhakrishnan SV, Basha SJ, Sarma AV, Rao JM (2009) Oleanane-type isomeric triterpenoids from Barringtonia racemosa. J Nat Prod 72(4):791–795. https://doi.org/10.1021/np8007396
doi: 10.1021/np8007396
pubmed: 19388709
Guglielmo GMD, Soares IN, Viana R, Trelford CB, Chan E, Thai B, Cino EA (2020) The synthetic oleanane triterpenoid CDDO-Me binds and inhibits pyruvate kinase M2. Pharmacol Rep 72:631–640. https://doi.org/10.1007/s43440-019-00045-6
doi: 10.1007/s43440-019-00045-6
pubmed: 32040844
Guo W, Xu B, Wang X, Zheng B, Du J, Liu S (2020) The analysis of the anti-tumor mechanism of ursolic acid using connectively map approach in breast cancer cells line MCF-7. Cancer Manag Res 12:3469–3476. https://doi.org/10.2147/CMAR.S241957
doi: 10.2147/CMAR.S241957
pubmed: 32523377
pmcid: 7237111
Harrington BS, Annunziata CM (2019) NF-κB signaling in ovarian cancer. Cancers 11:1182. https://doi.org/10.3390/cancers11081182
doi: 10.3390/cancers11081182
pmcid: 6721592
Huang L, Li J, Ye H, Li C, Wang H, Liu B, Zhang Y (2012) Molecular characterization of the pentacyclic triterpenoid biosynthetic pathway in Catharanthus roseus. Planta 236:1571–1581. https://doi.org/10.1007/s00425-012-1712-0
doi: 10.1007/s00425-012-1712-0
pubmed: 22837051
Jäger S, Trojan H, Kopp T, Laszczyk MN, Scheffler A (2009) Pentacyclic triterpene distribution in various plants–rich sources for a new group of multi-potent plant extracts. Molecules 14:2016–2031. https://doi.org/10.3390/molecules14062016
doi: 10.3390/molecules14062016
pubmed: 19513002
pmcid: 6254168
Jo H, Oh JH, Park DW, Lee C, Min CK (2018) Oleanolic acid 3-acetate, a minor element of ginsenosides, induces apoptotic cell death in ovarian carcinoma and endometrial carcinoma cells via the involvement of a reactive oxygen specieseindependent mitochondrial pathway. J Ginseng Res 44:96–104. https://doi.org/10.1016/j.jgr.2018.09.003
doi: 10.1016/j.jgr.2018.09.003
pubmed: 32095097
pmcid: 7033343
Kriplani D, Patel MM (2013) Immunohistochemistry: a diagnostic aid in differentiating primary epithelial ovarian tumors and tumors metastatic to the ovary. South Asian J Cancer 2(4):254–258. https://doi.org/10.4103/2278-330X.119888
doi: 10.4103/2278-330X.119888
pubmed: 24455652
pmcid: 3889055
Kundu CN, Patil KR, Mohapatra P, Patel HM, Goyal SN, Ojha S, Patil CR (2015) Pentacyclic triterpenoids inhibit IKKβ mediated activation of NF-κB pathway: in silico and in vitro evidences. Plos One 10(5):e0125709. https://doi.org/10.1371/journal.pone.0125709
doi: 10.1371/journal.pone.0125709
pubmed: 25938234
pmcid: 4418667
Leng S, Hao Y, Du D, Xie S, Hong L, Gu H, Zhu X, Zhang J, Fan D, Kung HF (2013) Ursolic acid promotes cancer cell death by inducing Atg5-dependent autophagy. Int J Cancer 133:2781–2790. https://doi.org/10.1002/ijc.28301
doi: 10.1002/ijc.28301
pubmed: 23737395
Li G, Wang J, Jin M, Jin C, Ye C, Zhou Y, Wang R, Cui H, Zhou W (2020) A new pentacyclic triterpenoid from the leaves of Rhododendron dauricum L. with inhibition of NO production in LPS-induced RAW 264.7 cells. Nat Prod Res 34(23):3313–3319. https://doi.org/10.1080/14786419.2019.1566822
doi: 10.1080/14786419.2019.1566822
pubmed: 30810367
Litaudon M, Jolly C, Callonec CL, Cuong DD, Retailleau P, Nosjean O, Nguyen VH, Pfeiffer B, Boutin JA, Guéritte F (2009) Cytotoxic pentacyclic triterpenoids from Combretum sundaicum and Lantana camara as inhibitors of Bcl-xL/BakBH3 domain peptide interaction. J Nat Prod 72:1314–1320. https://doi.org/10.1021/np900192r
doi: 10.1021/np900192r
pubmed: 19572612
Morsy RA, Khater D, Kasem RF (2017) Immunohistochemical analysis of Nf-κB expression and its relation to apoptosis and proliferation in different odontogenic tumors. Int J Cancer res 13(2):76–83. https://doi.org/10.3923/ijcr.2017.76.83
doi: 10.3923/ijcr.2017.76.83
Meyerholz DK, Gibson-Corley KN, Olivier AK (2013) Principles for valid histopathologic scoring in research. Vet Pathol 50(6):1007–1015. https://doi.org/10.1177/0300985813485099
doi: 10.1177/0300985813485099
pubmed: 23558974
Ojha S, Patil CR, Sonara BM, Mahajan UB, Patil KR, Patil DD, Jadhav RB, Goyal SN (2016) Chemomodulatory potential of bartogenic acid against DMBA/croton oil induced two-step skin carcinogenesis in mice. J Cancer 7(14):2139–2147. https://doi.org/10.7150/jca.16446
doi: 10.7150/jca.16446
pubmed: 27877231
pmcid: 5118679
Patil KR, Patil CR (2017) Anti-inflammatory activity of bartogenic acid containing fraction of fruits of Barringtonia racemosa Roxb. in acute and chronic animal models of inflammation. J Tradit Complement Med 7:86–93. https://doi.org/10.1016/j.jtcme.2016.02.001
doi: 10.1016/j.jtcme.2016.02.001
pubmed: 28053892
Patil KR, Patil CR, Jadhav RB, Mahajan VK, Patil PR, Gaikwad PS (2011) Anti-arthritic activity of bartogenic acid isolated from fruits of Barringtonia racemosa Roxb. (Lecythidaceae). Evid Based Complement Alternat Med. https://doi.org/10.1093/ecam/nep148
doi: 10.1093/ecam/nep148
pubmed: 21785651
pmcid: 3140190
Patil CR, Kamble SM, Goyal SN (2014) Multifunctional pentacyclic triterpenoids as adjuvants in cancer chemotherapy: a review. RSC Adv 4:33370. https://doi.org/10.1039/C4RA02784A
doi: 10.1039/C4RA02784A
Paduch R, Kandefer-Szerszeń M (2014) Antitumor and antiviral activity of pentacyclic triterpenes. Mini-Rev Org Chem 11:262–268. https://doi.org/10.2174/1570193X1103140915105240
doi: 10.2174/1570193X1103140915105240
Rajkumar T, Natarajan A, Ramachandran B, Gopisetty G, Jayavelu S, Sundersingh S (2020) Pioglitazone modulates doxorubicin resistance in a in vivo model of drug resistant osteosarcoma xenograft. Naunyn-Schmiedeberg’s Arch Pharmacol. https://doi.org/10.1007/s00210-020-01982-3
doi: 10.1007/s00210-020-01982-3
Reid BM, Permuth JB, Sellers TA (2017) Epidemiology of ovarian cancer: a review. Cancer Biol Med 14(1):9–32. https://doi.org/10.20892/j.issn.2095-3941.2016.0084
doi: 10.20892/j.issn.2095-3941.2016.0084
pubmed: 28443200
pmcid: 5365187
Patlolla JMR, Rao CV (2012) Triterpenoids for cancer prevention and treatment: current status and future prospects. Curr Pharm Biotechnol 13:147–155. https://doi.org/10.2174/138920112798868719
doi: 10.2174/138920112798868719
pubmed: 21466427
Shanmugam MK, Nguyen AH, Kumar AP, Tan BKH, Sethi G (2012) Targeted Inhibition of tumor proliferation, survival, and metastasis by pentacyclic triterpenoids: potential role in prevention and therapy of cancer. Cancer Lett 320(2):158–170. https://doi.org/10.1016/j.canlet.2012.02.037
doi: 10.1016/j.canlet.2012.02.037
pubmed: 22406826
Shi Z, Chen ZS, Yan XJ, Gong LH, Zheng FY, Cheng KJ (2014) Triterpenoids as reversal agents for anticancer drug resistance treatment. Drug Discovery Today 19(4):482–488. https://doi.org/10.1016/j.drudis.2013.07.018
doi: 10.1016/j.drudis.2013.07.018
pubmed: 23954181
Shishodia S, Majumdar S, Banerjee S, Aggarwal BB (2003) Ursolic acid inhibits nuclear factor-kappaB activation induced by carcinogenic agents through suppression of IkappaBalpha kinase and p65 phosphorylation: correlation with down-regulation of cyclooxygenase 2, matrix metalloproteinase 9, and cyclin D1. Cancer Res 63(15):4375–4383
pubmed: 12907607
Shukla S, Shankar E, Fu P, MacLennan GT, Gupta S (2015) Suppression of NF-κB and NF-κB-regulated gene expression by apigenin through IκBα and IKK pathway in TRAMP mice. Plos One 10(9):e0138710. https://doi.org/10.1371/journal.pone.0138710
doi: 10.1371/journal.pone.0138710
pubmed: 26379052
pmcid: 4574560
Thomas TJ, Panikkar B, Subramoniam A, Nair MK, Panikkar KR (2002) Antitumour property and toxicity of Barringtonia racemosa Roxb seed extract in mice. J Ethnopharmacol 82(2–3):223–227. https://doi.org/10.1016/S0378-8741(02)00074-0
doi: 10.1016/S0378-8741(02)00074-0
pubmed: 12241999
Wang Y, Xiang J, Wang J, Ji Y (2018) Downregulation of TGF-β1 suppressed proliferation and increased chemosensitivity of ovarian cancer cells by promoting BRCA1/Smad3 signaling. Biol Res 51:58. https://doi.org/10.1186/s40659-018-0205-4
doi: 10.1186/s40659-018-0205-4
pubmed: 30594239
pmcid: 6310971
Wu YJ, Muldoon LL, Dickey DT, Lewin SJ, Varallyay CG, Neuwelt EA (2009) Cyclophosphamide enhances human tumor growth in nude rat xenografted tumor models. Neoplasia 11(2):187–195. https://doi.org/10.1593/neo.81352
doi: 10.1593/neo.81352
pubmed: 19177203
pmcid: 2631143
Xia Y, Verma IM, Shen S (2014) NF-kB, an active player in human cancers. Cancer Immunol Res 2(9):823–830. https://doi.org/10.1158/2326-6066.CIR-14-0112
doi: 10.1158/2326-6066.CIR-14-0112
pubmed: 25187272
pmcid: 4155602
Yadav VR, Aggarwal BB, Prasad S, Sung B, Kannappan R (2010) Targeting inflammatory pathways by triterpenoids for prevention and treatment of cancer. Toxins 2:2428–2466. https://doi.org/10.3390/toxins2102428
doi: 10.3390/toxins2102428
pubmed: 22069560
pmcid: 3153165
Yilmaz E, Gul M, Melekoglu R, Koleli I (2018) Immunhistochemical analysis of nuclear factor kappa beta expression in etiopathogenesis of ovarian tumors. Acta Cir Bras 33(7):641–650. https://doi.org/10.1590/s0102-865020180070000009
doi: 10.1590/s0102-865020180070000009
pubmed: 30110065
Yu M, Si L, Wang Y, Wu Y, Yu F, Jiao P, Shi Y, Wang H, Xiao S, Fu G, Tian K, Wang YT, Guo Z, Ye XS, Zhang LH, Zhou D (2014) Discovery of pentacyclic triterpenoids as potential entry inhibitors of influenza viruses. J Med Chem. https://doi.org/10.1021/jm5014067
doi: 10.1021/jm5014067
pubmed: 25469863
pmcid: 4266342
Zhang Y, Luo G, Li M, Guo P, Xiao Y, Ji H, Hao Y (2019) Global patterns and trends in ovarian cancer incidence: age, period and birth cohort analysis. BMC Cancer 19:984–998. https://doi.org/10.1186/s12885-019-6139-6
doi: 10.1186/s12885-019-6139-6
pubmed: 31640608
pmcid: 6806513
Zhao YC, Zhang L, Feng SS, Hong L, Zheng HL, Chen LL, Zheng XL, Ye YQ, Zhao MD, Wang WX, Zheng CH (2016) Efficient delivery of Notch1 siRNA to SKOV3 cells by cationic cholesterol derivative-based liposome. Int J Nanomedicine 20(11):5485–5496. https://doi.org/10.2147/IJN.S115367
doi: 10.2147/IJN.S115367
Zheng J (1998) Immunohistochemistry and immunocytochemistry. Methods Mol Biol 105:307–314. https://doi.org/10.1385/0-89603-491-7:307
doi: 10.1385/0-89603-491-7:307
pubmed: 10427573
Zheng L, Liu J, Zhong J, Wu N, Liu G, Lin X (2014) Oleanolic acid induces protective autophagy in cancer cells through the JNK and mTOR pathways. Oncol Rep 32(2):567–572. https://doi.org/10.3892/or.2014.3239
doi: 10.3892/or.2014.3239
pubmed: 24912497