Rice Science ›› 2021, Vol. 28 ›› Issue (1): 13-30.DOI: 10.1016/j.rsci.2020.11.004
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Ramakrishna Wusirika1(
), Kumari Anuradha1, Rahman Nafeesa2, Mandave Pallavi3
Received:2020-03-14
Accepted:2020-05-09
Online:2021-01-28
Published:2021-01-28
About author:#These authors contributed equally to this work
Ramakrishna Wusirika, Kumari Anuradha, Rahman Nafeesa, Mandave Pallavi. Anticancer Activities of Plant Secondary Metabolites: Rice Callus Suspension Culture as a New Paradigm[J]. Rice Science, 2021, 28(1): 13-30.
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| Phytochemical (Source) (Dose) | Cancer type | Mode of action and its target | Reference |
|---|---|---|---|
| Apigenin (sorghum) and quercetin (cowpea) (0.1 µmol/L) | Caco-2 cell model and non-cancer CCD-18Co cell line | Activity of efflux transporters in Caco-2 modified by inhibiting expression of ABC transporters, BCRP, MRP2, MRP3 and MDR1 | |
| Altholactone (Goniothalamus sp.) (10, 20 and 40 µmol/L) | LNCaP, PC-3 and DU-145 prostate cancer cells | Inhibited STAT3 and NF-κB transcription | |
| Curcumin (Curcuma longa) (20 µmol/L) | Colorectal cancer cell lines | Suppressed the Sp-1 activation and its downstream genes, ADEM10, calmodulin, EPHB2, HDAC4 and SEPP1 | |
| Fisetin (Fragaria ananassa) (1-10 µmol/L) | Hepatic, colorectal and pancreatic cancer cell lines | Modulated CDK5, glucocorticoid signaling and ERK/ MAPK signaling, mediated by the activation of CDKN1A, SEMA3E, GADD45α and GADD45β and down-regulation of TOP2α, CCNB, KIF20A and CCNB1 genes | |
| Goniothalamin (Goniothalamus sp.) (300 µmol/L) | HeLa cervical cancer, MCF-7 breast cancer and HT-29 colon cancer cells | Induced oxidative stress in cancer cells leading to apoptosis. Up-regulation of p53 stabilized by NQO1 leading to caspase-2-dependent mitochondrial-mediated apoptosis | |
| Ursolic acid (Oldenlandia diffusa) (25 µmol/L) | Lung cancer | Inhibited the activity of a mitotic kinase, vaccinia-related kinase 1 | |
| Ethanolic extract with Avicennones D and E (Avicennia marina) (200 mg/kg) | MB-231 cell induced tumor in nude mice | Avicennones D and E containing ethanolic extract treatment decreased MMP2, MMP9, cyclin B, vimentin, PARP, caspase 8 and snail protein expression and increased caspase 3 expression | |
| Curcumin (Curcuma longa) (45 mg/kg) | NSCLC (A549) subcutaneous xenograft tumor model | Inhibited in vivo tumor growth, adiponectin and MMPs expression | |
| Genistein (Glycine max) (500 mg/kg) | A431 and Colo205 xenografts (mouse) | Upregulated GLUT3 and downregulated ERα | |
| Resveratrol (Vitis vinifera) (100-1000 mg) | Clinical trials for colorectal and prostate cancers | Regulated nuclear factor κB (NF-κB) signaling pathway and p53, inhibited IGF-1R/Akt/Wnt and PI3K/Akt/mTOR pathways | |
| Usnic and salazinic acids (Flavocetraria cucullata extract) (10 µmol/L usnic acid; 5 µg/mL extract) | A549 cell induced lung cancer in Balb/c nude mouse | Activated apoptotic signaling pathway in vitro and reduced levels of phosphor-Akt | |
| Ursolic acid (Punica granatum) (266 mg/kg) | Postmenopausal breast cancer model | Anti-tumor effect through Akt/mTOR signaling | |
| Withaferin A (Withania somnifera) (2 mg/kg) | HCT116 colon cancer cells injected into BALB/c nude mouse | Anticancer effect mediated by the inhibition of STAT3 signaling pathway |
Table 1 In vitro examples of plant bioactive compounds and their molecular targets.
| Phytochemical (Source) (Dose) | Cancer type | Mode of action and its target | Reference |
|---|---|---|---|
| Apigenin (sorghum) and quercetin (cowpea) (0.1 µmol/L) | Caco-2 cell model and non-cancer CCD-18Co cell line | Activity of efflux transporters in Caco-2 modified by inhibiting expression of ABC transporters, BCRP, MRP2, MRP3 and MDR1 | |
| Altholactone (Goniothalamus sp.) (10, 20 and 40 µmol/L) | LNCaP, PC-3 and DU-145 prostate cancer cells | Inhibited STAT3 and NF-κB transcription | |
| Curcumin (Curcuma longa) (20 µmol/L) | Colorectal cancer cell lines | Suppressed the Sp-1 activation and its downstream genes, ADEM10, calmodulin, EPHB2, HDAC4 and SEPP1 | |
| Fisetin (Fragaria ananassa) (1-10 µmol/L) | Hepatic, colorectal and pancreatic cancer cell lines | Modulated CDK5, glucocorticoid signaling and ERK/ MAPK signaling, mediated by the activation of CDKN1A, SEMA3E, GADD45α and GADD45β and down-regulation of TOP2α, CCNB, KIF20A and CCNB1 genes | |
| Goniothalamin (Goniothalamus sp.) (300 µmol/L) | HeLa cervical cancer, MCF-7 breast cancer and HT-29 colon cancer cells | Induced oxidative stress in cancer cells leading to apoptosis. Up-regulation of p53 stabilized by NQO1 leading to caspase-2-dependent mitochondrial-mediated apoptosis | |
| Ursolic acid (Oldenlandia diffusa) (25 µmol/L) | Lung cancer | Inhibited the activity of a mitotic kinase, vaccinia-related kinase 1 | |
| Ethanolic extract with Avicennones D and E (Avicennia marina) (200 mg/kg) | MB-231 cell induced tumor in nude mice | Avicennones D and E containing ethanolic extract treatment decreased MMP2, MMP9, cyclin B, vimentin, PARP, caspase 8 and snail protein expression and increased caspase 3 expression | |
| Curcumin (Curcuma longa) (45 mg/kg) | NSCLC (A549) subcutaneous xenograft tumor model | Inhibited in vivo tumor growth, adiponectin and MMPs expression | |
| Genistein (Glycine max) (500 mg/kg) | A431 and Colo205 xenografts (mouse) | Upregulated GLUT3 and downregulated ERα | |
| Resveratrol (Vitis vinifera) (100-1000 mg) | Clinical trials for colorectal and prostate cancers | Regulated nuclear factor κB (NF-κB) signaling pathway and p53, inhibited IGF-1R/Akt/Wnt and PI3K/Akt/mTOR pathways | |
| Usnic and salazinic acids (Flavocetraria cucullata extract) (10 µmol/L usnic acid; 5 µg/mL extract) | A549 cell induced lung cancer in Balb/c nude mouse | Activated apoptotic signaling pathway in vitro and reduced levels of phosphor-Akt | |
| Ursolic acid (Punica granatum) (266 mg/kg) | Postmenopausal breast cancer model | Anti-tumor effect through Akt/mTOR signaling | |
| Withaferin A (Withania somnifera) (2 mg/kg) | HCT116 colon cancer cells injected into BALB/c nude mouse | Anticancer effect mediated by the inhibition of STAT3 signaling pathway |
Fig. 1. Major players and pathways involved in cancer metabolism and their regulation by plant metabolites.Curcumin and other plant natural compounds regulating PI3K/Akt/mTOR pathway are shown. Adapted from Porta et al (2014), Eales et al (2016), and Kastenhuber and Lowe (2017).Akt, Protein kinase B; C-Myc, Cellular myelocytomatosis; 4E-BP1, Eukaryotic initiation factor 4E binding protein 1; FKBP-12, Drug FK506 binding protein-12; GLUT, Glucose transporter; HIF-1α, Hypoxia-inducible factor-1 alpha; mTOR, Mammalian or mechanistic target of rapamycin; OCT1, Octamer binding transcription factor-1; PDH, Pyruvate dehydrogenase; PDK, Pyruvate dehydrogenase kinase; PKM2, Pyruvate kinase M2; PTEN, Phosphatase and tensin homolog; PI3K, Phosphatidylinositol-3-kinase; SCO2, Synthesis of cytochrome C oxidase 2; TCA cycle, Tricarboxylic acid cycle; TIGAR, Tumor protein 53 inducible glycolysis and apoptosis regulator.
Fig. 2. Initiation phase of apoptosis and their regulation by plant metabolites.Both pathways (extrinsic and intrinsic) result in the formation of an apoptotic body, which is a diagnostic biomarker of apoptosis. Curcumin, delphinidin and malvidin regulate both intrinsic and extrinsic pathways. Adapted from Kuppusamy et al (2013).APAF-1, Apoptotic protease activating factor-1; Cyt C, Cytochrome C; FADD, FAS-associated death domain; FASL, Fas ligand; FLIP, FADD-like Interleukin-1beta-converting enzyme inhibitory protein; TNF, Tumor necrosis factor; TRAIL, TNF-related apoptosis inducing ligand; XIAP, X-linked inhibitor of apoptosis.
Fig. 3. Effects of rice callus suspension culture (RCSC) and Taxol® on normal and cancer cells.RCSC reduces the viability of cancer cells with minimal or no effect on the normal cells compared to Taxol® based on Deshpande et al (2012) and Rahman et al (2016).
Fig. 4. Molecular mechanisms regulating cytotoxic activity of rice callus suspension culture (RCSC). RCSC upregulates the transcription factor, NF-κB, which induces the production of the tumor necrosis factor, FASLG, leading to apoptosis via extrinsic pathway. Up-regulation of c-Jun leads to downregulation of cyclins and cyclin-dependent kinases, resulting in apoptosis via intrinsic pathway. c-Jun has also been shown to upregulate NF-κB. RCSC increases ROS levels in cancer cells, leading to DNA damage and loss of membrane integrity. CCND3, Cyclin D3; CDK, Cyclin-dependent kinase; c-Jun, Cellular protooncogene; FASLG, Tumor necrosis factor ligand superfamily member 6; NF-κB, Nuclear factor kappa light chain enhancer of activated B cells; LDH, Lactate dehydrogenase; ROS, Reactive oxygen species.
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