Phytochemicals for the Prevention and Treatment of Gastric Cancer: Effects and Mechanisms
Abstract
:1. Introduction
2. Epidemiological Studies
3. Experimental Studies
3.1. Inhibition of Cell Proliferation
3.2. Induction of Apoptosis
3.3. Autophagy
3.4. Inhibition of Tumor Angiogenesis
3.5. Suppression of Cell Metastasis
3.6. Inhibition of Helicobacter Pylori
3.7. Modulation of Gut Microbiota
3.8. Adjuvant Therapy
4. Clinical Trials
5. Bioavailability
6. Safety
7. Conclusions
Author Contributions
Funding
Conflicts of Interest
Abbreviations
AMPK | AMP-activated protein kinase |
ATF4 | activating transcription factor 4 |
ATG5 | autophagy related 5; ABCG2 |
ABCG2 | ATP binding cassette subfamily G member 2 |
Bad | Bcl-2 associated agonist of cell death |
Bax | Bcl-2-associated X protein |
Bcl-2 | B-cell lymphoma 2 |
Bcl-xL | B-cell lymphoma-extralarge |
Bid | BH3 interacting domain death agonist |
Bik | Bcl-2 interacting killer |
Cdc42 | cell division cycle 42 |
CDC25C | cell division cycle 25C |
CDK4 | cyclin dependent kinase 4 |
CHOP | -CCAAT-enhancer-binding protein homologous protein |
EMT | epithelial-mesenchymal transition |
ERK1/2 | extracellular signal-regulated kinase |
FasL | Fas Ligand |
GRP78 | glucose regulated protein 78 |
GSH | glutathione |
Hes-1 | hes family bHLH transcription factor 1 |
Hey-1 | hes related family bHLH transcription factor with YRPW motif 1 |
IκB-α | inhibitor of NF-κB |
ITGβ6 | integrin subunit beta 6 |
Jagged1/2 | 2 serrate-like ligands |
JNK | c-Jun N-terminal kinase |
ki-67 | a cell proliferation marker |
LC3B | microtubule associated protein 1 light chain 3 beta |
Mad1 | Mitotic arrest-deficient 1 |
MAPK | mitogen-activating protein kinase |
Mcl-1 | apoptosis regulator blongs to Bcl-2 family member |
miR-410 | a tumor-suppressive microRNA |
MMP-2 | matrix metallopeptidase 2 |
MT2A | metallothionein 2A |
MTUS2 | microtubule-associated tumor suppressor candidate 2 |
NF-κB | nuclear factor kappa light chain-enhancer of activated B cells |
Notch1 | notch receptor 1 |
PARP | poly (ADP-ribose) polymerase |
p-ERK1/2 | phosphorylation of extracellular signal-regulated kinase |
p-Chkl | phosphorylation of checkpoint kinase-1 |
p-IRE1 | phosphorylates inositol-requiring-1 |
p-JNK | phosphorylates c-Jun N-terminal protein kinase |
p-4EBP1 | phosphorylated 4E binding protein 1 |
p-p70S6K | phosphorylated ribosomal protein S6 kinase |
p-eIF4E | phosphorylated eukaryotic translation initiation factor 4E |
PI3K | phoshatidylinositol-3-kinase |
p-IκB-α | phosphorylation of p-IκB-α |
Rac1 | Rac family small GTPase 1 |
RhoA | ras homolog family member A |
RhoB | ras homolog family member B |
ROS | reactive oxygen species |
STAT3 | signal transducer and activator of transcription 3 |
TIMP | tissue inhibitor of metalloproteinase |
TrxR1 | thioredoxin reductase 1 |
TRAIL | tumour necrosis factor (TNF)-related apoptosis-inducing ligand |
Twist1 | twist family bHLH transcription factor 1 |
VEGF | vascular endothelial growth factor |
VEGF-R2 | vascular endothelial growth factor receptor 2 |
XIAP | X-linked inhibitor of apoptosis protein |
References
- Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2018, 68, 394–424. [Google Scholar] [CrossRef] [Green Version]
- Bertuccio, P.; Alicandro, G.; Rota, M.; Pelucchi, C.; Bonzi, R.; Galeone, C.; Bravi, F.; Johnson, K.C.; Hu, J.; Palli, D.; et al. Citrus fruit intake and gastric cancer: The stomach cancer pooling (StoP) project consortium. Int. J. Cancer 2019, 144, 2936–2944. [Google Scholar] [CrossRef]
- Yan, S.; Li, B.; Bai, Z.Z.; Wu, J.Q.; Xie, D.W.; Ma, Y.C.; Ma, X.X.; Zhao, J.H.; Guo, X.J. Clinical epidemiology of gastric cancer in Hehuang valley of China: A 10-year epidemiological study of gastric cancer. World J. Gastroenterol. 2014, 20, 10486–10494. [Google Scholar] [CrossRef]
- Wang, G.S.; Hu, N.; Yang, H.H.; Wang, L.M.; Su, H.; Wang, C.Y.; Clifford, R.; Dawsey, E.M.; Li, J.M.; Ding, T.; et al. Comparison of global gene expression of gastric cardia and noncardia cancers from a high-risk population in China. PLoS ONE 2013, 8, e63826. [Google Scholar] [CrossRef]
- Donida, B.M.; Tomasello, G.; Ghidini, M.; Buffoli, F.; Grassi, M.; Liguigli, W.; Maglietta, G.; Pergola, L.; Ratti, M.; Sabadini, G.; et al. Epidemiological, clinical and pathological characteristics of gastric neoplasms in the province of Cremona: The experience of the first population-based specialized gastric cancer registry in Italy. BMC Cancer 2019, 19, 212. [Google Scholar] [CrossRef] [Green Version]
- Goh, K.L.; Cheah, P.L.; Noorfaridah, M.; Quek, K.F.; Parasakthi, N. Ethnicity and H. pylori as risk factors for gastric cancer in Malaysia: A prospective case control study. Am. J. Gastroenterol. 2007, 102, 40–45. [Google Scholar] [CrossRef]
- Izuishi, K.; Mori, H. Recent strategies for treating stage IV gastric cancer: Roles of palliative gastrectomy, chemotherapy, and radiotherapy. J. Gastrointest. Liver 2016, 25, 87–94. [Google Scholar]
- Ren, F.; Li, S.D.; Zhang, Y.; Zhao, Z.F.; Wang, H.M.; Cui, Y.X.; Wang, M.Y. Efficacy and safety of intensity-modulated radiation therapy versus three-dimensional conformal radiation treatment for patients with gastric cancer: A systematic review and meta-analysis. Radiat. Oncol. 2019, 14, 84. [Google Scholar] [CrossRef]
- Macdonald, J.S.; Smalley, S.R.; Benedetti, J.; Hundahl, S.A.; Estes, N.C.; Stemmermann, G.N.; Haller, D.G.; Ajani, J.A.; Gunderson, L.L.; Jessup, J.M.; et al. Chemoradiotherapy after surgery compared with surgery alone for adenocarcinoma of the stomach or gastroesophageal junction. N. Engl. J. Med. 2001, 345, 725–730. [Google Scholar] [CrossRef]
- Yu, L.L.; Wu, J.G.; Dai, N.; Yu, H.G.; Si, J.M. Curcumin reverses chemoresistance of human gastric cancer cells by downregulating the NF-κB transcription factor. Oncol. Rep. 2011, 26, 1197–1203. [Google Scholar] [CrossRef] [Green Version]
- Bertuccio, P.; Rosato, V.; Andreano, A.; Ferraroni, M.; Decarli, A.; Edefonti, V.; La Vecchia, C. Dietary patterns and gastric cancer risk: A systematic review and meta-analysis. Ann. Oncol. 2013, 24, 1450–1458. [Google Scholar] [CrossRef]
- Li, Y.; Li, S.; Meng, X.; Gan, R.Y.; Zhang, J.J.; Li, H.B. Dietary natural products for prevention and treatment of breast cancer. Nutrients 2017, 9, 728. [Google Scholar] [CrossRef] [Green Version]
- Nouraie, M.; Pietinen, P.; Kamangar, F.; Dawsey, S.M.; Abnet, C.C.; Albanes, D.; Virtamo, J.; Taylor, P.R. Fruits, vegetables, and antioxidants and risk of gastric cancer among male smokers. Cancer Epidemiol. Biomark. 2005, 14, 2087–2092. [Google Scholar] [CrossRef] [Green Version]
- Zhou, Y.; Li, Y.; Zhou, T.; Zheng, J.; Li, S.; Li, H.B. Dietary natural products for prevention and treatment of liver cancer. Nutrients 2016, 8, 156. [Google Scholar] [CrossRef] [Green Version]
- Zheng, J.; Zhou, Y.; Li, Y.; Xu, D.P.; Li, S.; Li, H.B. Spices for prevention and treatment of cancers. Nutrients 2016, 8, 495. [Google Scholar] [CrossRef]
- Fang, X.X.; Wei, J.Y.; He, X.Y.; An, P.; Wang, H.; Jiang, L.; Shao, D.D.; Liang, H.; Li, Y.; Wang, F.D.; et al. Landscape of dietary factors associated with risk of gastric cancer: A systematic review and dose-response meta-analysis of prospective cohort studies. Eur. J. Cancer 2015, 51, 2820–2832. [Google Scholar] [CrossRef]
- Palli, D.; Russo, A.; Saieva, C.; Salvini, S.; Amorosi, A.; Decarli, A. Dietary and familial determinants of 10-year survival among patients with gastric carcinoma. Cancer Am. Cancer Soc. 2000, 89, 1205–1213. [Google Scholar] [CrossRef]
- Wada, K.; Tsuji, M.; Tamura, T.; Konishi, K.; Kawachi, T.; Hori, A.; Tanabashi, S.; Matsushita, S.; Tokimitsu, N.; Nagata, C. Soy isoflavone intake and stomach cancer risk in Japan: From the Takayama study. Int. J. Cancer 2015, 137, 885–892. [Google Scholar] [CrossRef]
- Ekstrom, A.M.; Serafini, M.; Nyren, O.; Wolk, A.; Bosetti, C.; Bellocco, R. Dietary quercetin intake and risk of gastric cancer: Results from a population-based study in Sweden. Ann. Oncol. 2011, 22, 438–443. [Google Scholar] [CrossRef]
- Chen, W.; Zhao, Z.; Li, Y.Q. Simultaneous increase of mycelial biomass and intracellular polysaccharide from Fomes fomentarius and its biological function of gastric cancer intervention. Carbohyd. Polym. 2011, 85, 369–375. [Google Scholar] [CrossRef]
- Zou, P.; Xia, Y.Q.; Ji, J.S.; Chen, W.Q.; Zhang, J.S.; Chen, X.; Rajamanickam, V.; Chen, G.Z.; Wang, Z.; Chen, L.F.; et al. Piperlongumine as a direct TrxR1 inhibitor with suppressive activity against gastric cancer. Cancer Lett. 2016, 375, 114–126. [Google Scholar] [CrossRef] [PubMed]
- Kim, T.W.; Lee, S.Y.; Kim, M.; Cheon, C.; Ko, S.G. Kaempferol induces autophagic cell death via IRE1-JNK-CHOP pathway and inhibition of G9a in gastric cancer cells. Cell Death Dis. 2018, 9, 875. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Wang, J.Q.; Lin, L.; He, L.J.; Wu, Y.Y.; Zhang, L.; Yi, Z.F.; Chen, Y.H.; Pang, X.F.; Liu, M.Y. Inhibition of STAT3 signaling pathway by nitidine chloride suppressed the angiogenesis and growth of human gastric cancer. Mol. Cancer Ther. 2012, 11, 277–287. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lei, C.S.; Hou, Y.C.; Pai, M.H.; Lin, M.T.; Yeh, S.L. Effects of quercetin combined with anticancer drugs on metastasis-associated factors of gastric cancer cells: In vitro and in vivo studies. J. Nutr. Biochem. 2018, 51, 105–113. [Google Scholar] [CrossRef] [PubMed]
- Nowak, R.; Nowacka-Jechalke, N.; Juda, M.; Malm, A. The preliminary study of prebiotic potential of Polish wild mushroom polysaccharides: The stimulation effect on Lactobacillus strains growth. Eur. J. Nutr. 2018, 57, 1511–1521. [Google Scholar] [CrossRef] [Green Version]
- Mahady, G.B.; Pendland, S.L.; Yun, G.; Lu, Z. Turmeric (Curcuma longa) and curcumin inhibit the growth of Helicobacter pylori, a group 1 carcinogen. Anticancer Res. 2002, 22, 4179–4181. [Google Scholar]
- Bastos, J.; Lunet, N.; Peleteiro, B.; Lopes, C.; Barros, H. Dietary patterns and gastric cancer in a Portuguese urban population. Int. J. Cancer 2010, 127, 433–441. [Google Scholar] [CrossRef]
- Nagata, C.; Takatsuka, N.; Kawakami, N.; Shimizu, H. A prospective cohort study of soy product intake and stomach cancer death. Br. J. Cancer 2002, 87, 31–36. [Google Scholar] [CrossRef] [Green Version]
- Palli, D.; Russo, A.; Ottini, L.; Masala, G.; Saieva, C.; Amorosi, A.; Cama, A.; D’Amico, C.; Falchetti, M.; Palmirotta, R.; et al. Red meat, family history, and increased risk of gastric cancer with microsatellite instability. Cancer Res. 2001, 61, 5415–5419. [Google Scholar]
- Pourfarzi, F.; Whelan, A.; Kaldor, J.; Malekzadeh, R. The role of diet and other environmental factors in the causation of gastric cancer in Iran-A population-based study. Int. J. Cancer 2009, 125, 1953–1960. [Google Scholar] [CrossRef] [Green Version]
- Bae, J.M.; Lee, E.J.; Guyatt, G. Citrus fruit intake and stomach cancer risk: A quantitative systematic review. Gastric Cancer 2008, 11, 23–32. [Google Scholar] [CrossRef] [PubMed]
- Kim, H.J.; Chang, W.K.; Kim, M.K.; Lee, S.S.; Choi, B.Y. Dietary factors and gastric cancer in Korea: A case-control study. Int. J. Cancer 2002, 97, 531–535. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kobayashi, M.; Tsubono, Y.; Sasazuki, S.; Sasaki, S.; Tsugane, S.; GRP, J.S. Vegetables, fruit and risk of gastric cancer in japan: A 10-year follow-up of the JPHC Study Cohort I. Int. J. Cancer 2002, 102, 39–44. [Google Scholar] [CrossRef]
- Steevens, J.; Schouten, L.J.; Goldbohm, R.A.; van den Brandt, P.A. Vegetables and fruits consumption and risk of esophageal and gastric cancer subtypes in the Netherlands cohort study. Int. J. Cancer 2011, 129, 2681–2693. [Google Scholar] [CrossRef]
- McCullough, M.L.; Robertson, A.S.; Jacobs, E.J.; Chao, A.; Calle, E.E.; Thun, M.J. A prospective study of diet and stomach cancer mortality in United States men and women. Cancer Epidemiol. Biomark. 2001, 10, 1201–1205. [Google Scholar]
- Zhou, Y.; Zhuang, W.; Hu, W.; Liu, G.J.; Wu, T.X.; Wu, X.T. Consumption of large amounts of allium vegetables reduces risk for gastric cancer in a meta-analysis. Gastroenterology 2011, 141, 80–89. [Google Scholar] [CrossRef]
- Ko, K.P.; Park, S.K.; Park, B.; Yang, J.J.; Cho, L.Y.; Kang, C.; Kim, C.S.; Gwack, J.; Shin, A.; Kim, Y.; et al. Isoflavones from Phytoestrogens and gastric cancer risk: A nested case-control study within the Korean multicenter cancer cohort. Cancer Epidemiol. Biomark. 2010, 19, 1292–1300. [Google Scholar] [CrossRef] [Green Version]
- Kweon, S.S.; Shu, X.O.; Xiang, Y.B.; Cai, H.; Yang, G.; Ji, B.T.; Li, H.L.; Gao, Y.T.; Zheng, W.; Epplein, M. Intake of specific nonfermented soy foods may be inversely associated with risk of distal gastric cancer in a Chinese population. J. Nutr. 2013, 143, 1736–1742. [Google Scholar] [CrossRef] [Green Version]
- Persson, C.; Sasazuki, S.; Inoue, M.; Kurahashi, N.; Iwasaki, M.; Miura, T.; Ye, W.; Tsugane, S.; Grp, J.S. Plasma levels of carotenoids, retinol and tocopherol and the risk of gastric cancer in Japan: A nested case-control study. Carcinogenesis 2008, 29, 1042–1048. [Google Scholar] [CrossRef] [Green Version]
- Woo, H.D.; Lee, J.; Choi, I.J.; Kim, C.G.; Lee, J.Y.; Kwon, O.; Kim, J. Dietary Flavonoids and gastric cancer risk in a Korean population. Nutrients 2014, 6, 4961–4973. [Google Scholar] [CrossRef] [Green Version]
- Kim, J.H.; Lee, J.; Choi, I.J.; Kim, Y.I.; Kwon, O.; Kim, H.; Kim, J. Dietary carotenoids intake and the risk of gastric cancer: A case control study in Korea. Nutrients 2018, 10, 1031. [Google Scholar] [CrossRef] [Green Version]
- Petrick, J.L.; Steck, S.E.; Bradshaw, P.T.; Trivers, K.F.; Abrahamson, P.E.; Engel, L.S.; He, K.; Chow, W.H.; Mayne, S.T.; Risch, H.A.; et al. Dietary intake of flavonoids and oesophageal and gastric cancer: Incidence and survival in the United States of America (USA). Br. J. Cancer 2015, 112, 1291–1300. [Google Scholar] [CrossRef] [PubMed]
- Moy, K.A.; Yuan, J.M.; Chung, F.L.; Wang, X.L.; Van Den Berg, D.; Wang, R.W.; Gao, Y.T.; Yu, M.C. Isothiocyanates, glutathione S-transferase M1 and T1 polymorphisms and gastric cancer risk: A prospective study of men in Shanghai, China. Int. J. Cancer 2009, 125, 2652–2659. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shimazu, T.; Wakai, K.; Tamakoshi, A.; Tsuji, I.; Tanaka, K.; Matsuo, K.; Nagata, C.; Mizoue, T.; Inoue, M.; Tsugane, S.; et al. Association of vegetable and fruit intake with gastric cancer risk among Japanese: A pooled analysis of four cohort studies. Ann. Oncol. 2014, 25, 1228–1233. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez, C.A.; Lujan-Barroso, L.; Bueno-de-Mesquita, H.B.; Jenab, M.; Duell, E.J.; Agudo, A.; Tjonneland, A.; Boutron-Ruault, M.C.; Clavel-Chapelon, F.; Touillaud, M.; et al. Fruit and vegetable intake and the risk of gastric adenocarcinoma: A reanalysis of the European prospective investigation into cancer and nutrition (EPIC-EURGAST) study after a longer follow-up. Int. J. Cancer 2012, 131, 2910–2919. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Larsson, S.C.; Bergkvist, L.; Wolk, A. Fruit and vegetable consumption and incidence of gastric cancer: A prospective study. Cancer Epidemiol. Biomark. 2006, 15, 1998–2001. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Epplein, M.; Shu, X.O.; Xiang, Y.B.; Chow, W.H.; Yang, G.; Li, H.L.; Ji, B.T.; Cai, H.; Gao, Y.T.; Zheng, W. Fruit and vegetable consumption and risk of distal gastric cancer in the Shanghai women’s and men’s health studies. Am. J. Epidemiol. 2010, 172, 397–406. [Google Scholar] [CrossRef]
- Kim, H.; Keum, N.; Giovannucci, E.L.; Fuchs, C.S.; Bao, Y. Garlic intake and gastric cancer risk: Results from two large prospective US cohort studies. Int. J. Cancer 2018, 143, 1047–1053. [Google Scholar] [CrossRef] [Green Version]
- Hara, A.; Sasazuki, S.; Inoue, M.; Iwasaki, M.; Shimazu, T.; Sawada, N.; Yamaji, T.; Tsugane, S.; Ctr-Based, J.P.H. Isoflavone intake and risk of gastric cancer: A population-based prospective cohort study in Japan. Am. J. Clin. Nutr. 2012, 95, 147–154. [Google Scholar] [CrossRef] [Green Version]
- Sun, L.; Subar, A.F.; Bosire, C.; Dawsey, S.M.; Kahle, L.L.; Zimmerman, T.P.; Abnet, C.C.; Heller, R.; Graubard, B.I.; Cook, M.B.; et al. Dietary flavonoid intake reduces the risk of head and neck but not esophageal or gastric cancer in US men and women. J. Nutr. 2017, 147, 1729–1738. [Google Scholar]
- Botterweck, A.A.M.; van den Brandt, P.A.; Goldbohm, R.A. Vitamins, carotenoids, dietary fiber, and the risk of gastric carcinoma—Results from a prospective study after 6.3 years of follow-up. Cancer Am. Cancer Soc. 2000, 88, 737–748. [Google Scholar]
- Lan, H.; Lu, Y.Y. Allitridi induces apoptosis by affecting Bcl-2 expression and caspase-3 activity in human gastric cancer cells. Acta Pharmacol. Sin. 2004, 25, 219–225. [Google Scholar] [PubMed]
- Liu, Y.B.; Nair, M.G. Labdane diterpenes in Curcuma mangga rhizomes inhibit lipid peroxidation, cyclooxygenase enzymes and human tumour cell proliferation. Food Chem. 2011, 124, 527–532. [Google Scholar] [CrossRef]
- Zhu, X.Y.; Luo, F.L.; Zheng, Y.X.; Zhang, J.K.; Huang, J.Z.; Sun, C.D.; Li, X.; Chen, K.S. Characterization, purification of poncirin from edible Citrus Ougan (Citrus reticulate cv. Suavissima) and its growth inhibitory effect on human gastric cancer cells SGC-7901. Int. J. Mol. Sci. 2013, 14, 8684–8697. [Google Scholar] [CrossRef] [Green Version]
- Wu, K.; Yuan, L.H.; Xia, W. Inhibitory effects of apigenin on the growth of gastric carcinoma SGC-7901 cells. World J. Gastroenterol. 2005, 11, 4461–4464. [Google Scholar] [CrossRef]
- Xu, X.Y.; Song, G.Q.; Yu, Y.Q.; Ma, H.Y.; Ma, L.; Jin, Y.N. Apoptosis and G2/M arrest induced by Allium ursinum (ramson) watery extract in an AGS gastric cancer cell line. OncoTargets Ther. 2013, 6, 779–783. [Google Scholar] [CrossRef] [Green Version]
- Ling, H.; Lu, L.F.; He, J.; Xiao, G.H.; Jiang, H.; Su, Q. Diallyl disulfide selectively causes checkpoint kinase-1 mediated G2/M arrest in human MGC803 gastric cancer cell line. Oncol. Rep. 2014, 32, 2274–2282. [Google Scholar] [CrossRef] [Green Version]
- Yuan, J.P.; Wang, G.H.; Ling, H.; Su, Q.; Yang, Y.H.; Song, Y.; Tang, R.J.; Liu, Y.; Huang, C. Diallyl disulfide-induced G2/M arrest of human gastric cancer MGC803 cells involves activation of p38 MAP kinase pathways. World J. Gastroenterol. 2004, 10, 2731–2734. [Google Scholar] [CrossRef]
- Ling, H.; Zhang, L.Y.; Su, Q.; Song, Y.; Luo, Z.Y.; Zhou, X.T.; Zeng, X.; He, J.; Tan, H.; Yuan, J.P. ERK is involved in the differentiation induced by diallyl disulfide in the human gastric cancer cell line MGC803. Cell. Mol. Biol. Lett. 2006, 11, 408–423. [Google Scholar] [CrossRef]
- Choi, Y.H. Diallyl trisulfide induces apoptosis and mitotic arrest in AGS human gastric carcinoma cells through reactive oxygen species-mediated activation of AMP-activated protein kinase. Biomed. Pharmacother. 2017, 94, 63–71. [Google Scholar] [CrossRef]
- Batool, S.; Joseph, T.P.; Hussain, M.; Vuai, M.S.; Khinsar, K.H.; Din, S.R.U.; Padhiar, A.A.; Zhong, M.; Ning, A.H.; Zhang, W.; et al. LP1 from Lentinula edodes C91-3 induces autophagy, apoptosis and reduces metastasis in human gastric cancer cell line SGC-7901. Int. J. Mol. Sci. 2018, 19, 2986. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Feng, J.F.; Chen, X.N.; Wang, Y.Y.; Du, Y.W.; Sun, Q.Q.; Zang, W.Q.; Zhao, G.Q. Myricetin inhibits proliferation and induces apoptosis and cell cycle arrest in gastric cancer cells. Mol. Cell. Biochem. 2015, 408, 163–170. [Google Scholar] [CrossRef] [PubMed]
- Zhu, X.S.; Jiang, X.Y.; Li, A.; Sun, Y.Y.; Liu, Y.; Sun, X.; Feng, X.L.; Li, S.Y.; Zhao, Z.X. S-allylmercaptocysteine suppresses the growth of human gastric cancer xenografts through induction of apoptosis and regulation of MAPK and PI3K/Akt signaling pathways. Biochem. Biophys. Res. Commun. 2017, 491, 821–826. [Google Scholar] [CrossRef] [PubMed]
- Ishiguro, K.; Ando, T.; Maeda, O.; Ohmiya, N.; Niwa, Y.; Kadomatsu, K.; Goto, H. Ginger ingredients reduce viability of gastric cancer cells via distinct mechanisms. Biochem. Biophys. Res. Commun. 2007, 362, 218–223. [Google Scholar] [CrossRef]
- Yang, C.G.; Du, W.F.; Yang, D.G. Inhibition of green tea polyphenol EGCG((-)-epigallocatechin-3-gallate) on the proliferation of gastric cancer cells by suppressing canonical wnt/β-catenin signalling pathway. Int. J. Food Sci. Nutr. 2016, 67, 818–827. [Google Scholar] [CrossRef]
- Xu, X.Y.; Zhao, C.N.; Cao, S.Y.; Tang, G.Y.; Gan, R.Y.; Li, H.B. Effects and mechanisms of tea for the prevention and management of cancers: An updated review. Crit. Rev. Food Sci. Nutr. 2019, 1–13. [Google Scholar] [CrossRef]
- Shang, A.; Cao, S.Y.; Xu, X.Y.; Gan, R.Y.; Tang, G.Y.; Corke, H.; Mavumengwana, V.; Li, H.B. Bioactive compounds and biological functions of garlic (Allium sativum L.). Foods 2019, 8, 246. [Google Scholar] [CrossRef] [Green Version]
- Fesik, S.W. Promoting apoptosis as a strategy for cancer drug discovery. Nat. Rev. Cancer 2005, 5, 876–885. [Google Scholar] [CrossRef]
- Lin, H.H.; Chen, J.H.; Huang, C.C.; Wang, C.J. Apoptotic effect of 3,4-dihydroxybenzoic acid on human gastric carcinoma cells involving JNK/p38 MAPK signaling activation. Int. J. Cancer 2007, 120, 2306–2316. [Google Scholar] [CrossRef]
- Saralamma, V.V.G.; Nagappan, A.; Hong, G.E.; Lee, H.J.; Yumnam, S.; Raha, S.; Heo, J.D.; Lee, S.J.; Lee, W.S.; Kim, E.H.; et al. Poncirin induces apoptosis in AGS human gastric cancer cells through extrinsic apoptotic pathway by up-regulation of Fas Ligand. Int. J. Mol. Sci. 2015, 16, 22676–22691. [Google Scholar] [CrossRef] [Green Version]
- Kim, M.J.; Park, H.J.; Hong, M.S.; Park, H.J.; Kim, M.S.; Leem, K.H.; Kim, J.B.; Kim, Y.J.; Kim, H.K. Citrus reticulata Blanco induces apoptosis in human gastric cancer cells SNU-668. Nutr. Cancer 2005, 51, 78–82. [Google Scholar] [CrossRef] [PubMed]
- Shan, T.; Cui, X.J.; Li, W.; Lin, W.R.; Lu, H.W.; Li, Y.M.; Chen, X.; Wu, T. α-Mangostin suppresses human gastric adenocarcinoma cells In Vitro via blockade of STAT3 signaling pathway. Acta Pharmacol. Sin. 2014, 35, 1065–1073. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ohyama, K.; Akaike, T.; Imai, M.; Toyoda, H.; Hirobe, C.; Bessho, T. Human gastric signet ring carcinoma (KATO-III) cell apoptosis induced by Vitex agnus-castus fruit extract through intracellular oxidative stress. Int. J. Biochem. Cell Biol. 2005, 37, 1496–1510. [Google Scholar] [CrossRef] [PubMed]
- Chen, W.; Zhao, Z.; Li, L.; Wu, B.; Chen, S.F.; Zhou, H.; Wang, Y.; Li, Y.Q. Hispolon induces apoptosis in human gastric cancer cells through a ROS-mediated mitochondrial pathway. Free Radic. Biol. Med. 2008, 45, 60–72. [Google Scholar] [CrossRef]
- Zou, Y.P.; Chang, S.K.C. Effect of black soybean extract on the suppression of the proliferation of human ags gastric cancer cells via the induction of apoptosis. J. Agric. Food Chem. 2011, 59, 4597–4605. [Google Scholar] [CrossRef]
- Hibasami, H.; Komiya, T.; Achiwa, Y.; Ohnishi, K.; Kojima, T.; Nakanishi, K.; Akashi, K.; Hara, Y. Induction of apoptosis in human stomach cancer cells by green tea catechins. Oncol. Rep. 1998, 5, 527–529. [Google Scholar] [CrossRef]
- Hibasami, H.; Komiya, T.; Achiwa, Y.; Ohnishi, K.; Kojima, T.; Nakanishi, K.; Sugimoto, Y.; Hasegawa, M.; Akatsuka, R.; Hara, Y. Black tea theaflavins induce programmed cell death in cultured human stomach cancer cells. Int. J. Mol. Med. 1998, 1, 725–727. [Google Scholar] [CrossRef]
- Hibasami, H.; Jin, Z.X.; Hasegawa, M.; Urakawa, K.; Nakagawa, M.; Ishii, Y.; Yoshioka, K. Oolong tea polyphenol extract induces apoptosis in human stomach cancer cells. Anticancer Res. 2000, 20, 4403–4406. [Google Scholar]
- Li, G.Y.; Zhang, Y.R.; Xie, E.J.; Yang, X.; Wang, H.; Wang, X.J.; Li, W.W.; Song, Z.J.; Mu, Q.D.; Zhan, W.H.; et al. Functional characterization of a potent anti-tumor polysaccharide in a mouse model of gastric cancer. Life Sci. 2019, 219, 11–19. [Google Scholar] [CrossRef]
- Song, X.; Zhang, X.; Wang, X.; Zhu, F.; Guo, C.; Wang, Q.; Shi, Y.; Wang, J.; Chen, Y.; Zhang, L. Tumor suppressor gene PDCD4 negatively regulates autophagy by inhibiting the expression of autophagy-related gene ATG5. Autophagy 2013, 9, 743–755. [Google Scholar] [CrossRef] [Green Version]
- Gump, J.M.; Thorburn, A. Autophagy and apoptosis: What is the connection? Trends Cell Biol. 2011, 21, 387–392. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, H.J.; Saralamma, V.V.G.; Kim, S.M.; Ha, S.E.; Raha, S.; Lee, W.S.; Kim, E.H.; Lee, S.J.; Heo, J.D.; Kim, G.S. Pectolinarigenin induced cell cycle arrest, autophagy, and apoptosis in gastric cancer cell via PI3K/AKT/mTOR signaling pathway. Nutrients 2018, 10, 1043. [Google Scholar] [CrossRef] [Green Version]
- Ye, Y.; Fang, Y.F.; Xu, W.X.; Wang, Q.; Zhou, J.W.; Lu, R.Z. 3,3‘-Diindolylmethane induces anti-human gastric cancer cells by the miR-30e-ATG5 modulating autophagy. Biochem. Pharmacol. 2016, 115, 77–84. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Liu, S.S.; Feng, Q.; Huang, X.Y.; Wang, X.Y.; Peng, Y.; Zhao, Z.H.; Liu, Z. Perilaldehyde activates AMP-activated protein kinase to suppress the growth of gastric cancer via induction of autophagy. J. Cell. Biochem. 2019, 120, 1716–1725. [Google Scholar] [CrossRef] [PubMed]
- Wang, K.; Liu, R.; Li, J.Y.; Mao, J.L.; Lei, Y.L.; Wu, J.H.; Zeng, J.; Zhang, T.; Wu, H.; Chen, L.J.; et al. Quercetin induces protective autophagy in gastric cancer cells Involvement of Akt-mTOR- and hypoxia-induced factor 1 α-mediated signaling. Autophagy 2011, 7, 966–978. [Google Scholar] [CrossRef] [Green Version]
- Gao, J.H.; Wang, C.H.; Tong, H.; Wen, S.L.; Huang, Z.Y.; Tang, C.W. Targeting inhibition of extracellular signal-regulated kinase pathway with AZD6244 (ARRY-142886) suppresses growth and angiogenesis of gastric cancer. Sci. Rep. 2015, 5, 16382. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.; Han, J.; Yang, X.; Shao, C.; Xu, Z.; Cheng, R.; Cai, W.; Ma, J.; Yang, Z.; Gao, G. Pigment epithelium-derived factor inhibits angiogenesis and growth of gastric carcinoma by down-regulation of VEGF. Oncol. Rep. 2011, 26, 681–686. [Google Scholar]
- Zang, M.D.; Hu, L.; Zhang, B.G.; Zhu, Z.L.; Li, J.F.; Zhu, Z.G.; Yan, M.; Liu, B.Y. Luteolin suppresses angiogenesis and vasculogenic mimicry formation through inhibiting Notchl-VEGF signaling in gastric cancer. Biochem. Biophys. Res. Commun. 2017, 490, 913–919. [Google Scholar] [CrossRef]
- Tsuboi, K.; Matsuo, Y.; Shamoto, T.; Shibata, T.; Koide, S.; Morimoto, M.; Guha, S.; Sung, B.; Aggarwal, B.B.; Takahashi, H.; et al. Zerumbone inhibits tumor angiogenesis via NF-κB in gastric cancer. Oncol. Rep. 2014, 31, 57–64. [Google Scholar] [CrossRef] [Green Version]
- Ho, H.H.; Chang, C.S.; Ho, W.C.; Liao, S.Y.; Wu, C.H.; Wang, C.J. Anti-metastasis effects of gallic acid on gastric cancer cells involves inhibition of NF-κB activity and downregulation of PI3K/AKT/small GTPase signals. Food Chem. Toxicol. 2010, 48, 2508–2516. [Google Scholar] [CrossRef]
- Kuo, H.C.; Kuo, Y.R.; Lee, K.F.; Hsieh, M.C.; Huang, C.Y.; Hsieh, Y.Y.; Lee, K.C.; Kuo, H.L.; Lee, L.Y.; Chen, W.P.; et al. A comparative proteomic analysis of erinacine A’s inhibition of gastric cancer cell viability and invasiveness. Cell. Physiol. Biochem. 2017, 43, 195–208. [Google Scholar] [CrossRef] [PubMed]
- Zang, M.D.; Hu, L.; Fan, Z.Y.; Wang, H.X.; Zhu, Z.L.; Cao, S.; Wu, X.Y.; Li, J.F.; Su, L.P.; Li, C.; et al. Luteolin suppresses gastric cancer progression by reversing epithelial-mesenchymal transition via suppression of the Notch signaling pathway. J. Transl. Med. 2017, 15, 52. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, X.K.; Zheng, L.M.; Sun, Y.G.; Wang, T.X.; Wang, B.C. Tangeretin enhances radiosensitivity and inhibits the radiation-induced epithelial-mesenchymal transition of gastric cancer cells. Oncol. Rep. 2015, 34, 302–310. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Park, H.S.; Kim, G.Y.; Choi, I.W.; Kim, N.D.; Hwang, H.J.; Choi, Y.W.; Choi, Y.H. Inhibition of matrix metalloproteinase activities and tightening of tight junctions by diallyl disulfide in AGS human gastric carcinoma cells. J. Food Sci. 2011, 76, T105–T111. [Google Scholar] [CrossRef]
- Liu, Q.; Meng, X.; Li, Y.; Zhao, C.N.; Tang, G.Y.; Li, S.; Gan, R.Y.; Li, H.B. Natural products for the prevention and management of Helicobacter pylori infection. Compr. Rev. Food Sci. Food 2018, 17, 937–952. [Google Scholar] [CrossRef] [Green Version]
- Covacci, A.; Telford, J.L.; Del Giudice, G.; Parsonnet, J.; Rappuoli, R. Helicobacter pylori virulence and genetic geography. Science 1999, 284, 1328–1333. [Google Scholar] [CrossRef] [Green Version]
- Overby, A.; Zhao, C.M.; Chen, D. Plant phytochemicals: Potential anticancer agents against gastric cancer. Curr. Opin. Pharmacol. 2014, 19, 6–10. [Google Scholar] [CrossRef]
- Wang, Y.C. Medicinal plant activity on Helicobacter pylori related diseases. World J. Gastroenterol. 2014, 20, 10368–10382. [Google Scholar] [CrossRef]
- Vale, F.F.; Oleastro, M. Overview of the phytomedicine approaches against Helicobacter pylori. World J. Gastroenterol. 2014, 20, 5594–5609. [Google Scholar] [CrossRef] [Green Version]
- Mahady, G.B.; Pendland, S.L.; Yun, G.S.; Lu, Z.Z.; Stoia, A. Ginger (Zingiber officinale Roscoe) and the gingerols inhibit the growth of Cag A+ strains of Helicobacter pylori. Anticancer Res. 2003, 23, 3699–3702. [Google Scholar]
- Sekiguchi, H.; Washida, K.; Murakami, A. Suppressive effects of selected food phytochemicals on CD74 expression in NCI-N87 gastric carcinoma cells. J. Clin. Biochem. Nutr. 2008, 43, 109–117. [Google Scholar] [CrossRef] [Green Version]
- Kuo, C.H.; Weng, B.C.; Wu, C.C.; Yang, S.F.; Wu, D.C.; Wang, Y.C. Apigenin has anti-atrophic gastritis and anti-gastric cancer progression effects in Helicobacter pylon-infected Mongolian gerbils. J. Ethnopharmacol. 2014, 151, 1031–1039. [Google Scholar] [CrossRef] [PubMed]
- De, R.; Kundu, P.; Swarnakar, S.; Ramamurthy, T.; Chowdhury, A.; Nair, G.B.; Mukhopadhyay, A.K. Antimicrobial activity of curcumin against Helicobacter pylori isolates from india and during infections in mice. Antimicrob. Agents Chemother. 2009, 53, 1592–1597. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Qi, Y.F.; Sun, J.N.; Ren, L.F.; Cao, X.L.; Dong, J.H.; Tao, K.; Guan, X.M.; Cui, Y.N.; Su, W. Intestinal microbiota is altered in patients with gastric cancer from Shanxi province, China. Digest. Dis. Sci. 2019, 64, 1193–1203. [Google Scholar] [CrossRef] [PubMed]
- Nagano, T.; Otoshi, T.; Hazama, D.; Kiriu, T.; Umezawa, K.; Katsurada, N.; Nishimura, Y. Novel cancer therapy targeting microbiome. OncoTargets Ther. 2019, 12, 3619–3624. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lofgren, J.L.; Whary, M.T.; Ge, Z.M.; Muthupalani, S.; Taylor, N.S.; Mobley, M.; Potter, A.; Varro, A.; Eibach, D.; Suerbaum, S.; et al. Lack of commensal flora in Helicobacter pylori-infected INS-GAS mice reduces gastritis and delays intraepithelial neoplasia. Gastroenterology 2011, 140, 210–220. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kikuchi, H.; Ohtsuki, T.; Koyano, T.; Kowithayakorn, T.; Sakai, T.; Ishibashi, M. Activity of mangosteen xanthones and teleocidin A-2 in death receptor expression enhancement and tumor necrosis factor related apoptosis-inducing ligand assays. J. Nat. Prod. 2010, 73, 452–455. [Google Scholar] [CrossRef]
- Huang, W.F.; Wan, C.P.; Luo, Q.C.; Huang, Z.J.; Luo, Q. Genistein-Inhibited cancer stem cell-like properties and reduced chemoresistance of gastric cancer. Int. J. Mol. Sci. 2014, 15, 3432–3443. [Google Scholar] [CrossRef] [Green Version]
- Jin, H.; Park, M.H.; Kim, S.M. 3,3‘-Diindolylmethane potentiates paclitaxel-induced antitumor effects on gastric cancer cells through the Akt/FOXM1 signaling cascade. Oncol. Rep. 2015, 33, 2031–2036. [Google Scholar] [CrossRef] [Green Version]
- Pan, Y.M.; Lin, S.Y.; Xing, R.; Zhu, M.; Lin, B.N.; Cui, J.T.; Li, W.M.; Gao, J.; Shen, L.; Zhao, Y.Y.; et al. Epigenetic upregulation of metallothionein 2a by diallyl trisulfide enhances chemosensitivity of human gastric cancer cells to docetaxel through attenuating NF-κB activation. Antioxid. Redox Sign. 2016, 24, 839–854. [Google Scholar] [CrossRef] [Green Version]
- Jiang, X.Y.; Zhu, X.S.; Xu, H.Y.; Zhao, Z.X.; Li, S.Y.; Li, S.Z.; Cai, J.H.; Cao, J.M. Diallyl trisulfide suppresses tumor growth through the attenuation of Nrf2/Akt and activation of p38/JNK and potentiates cisplatin efficacy in gastric cancer treatment. Acta Pharmacol. Sin. 2017, 38, 1048–1058. [Google Scholar] [CrossRef] [PubMed]
- Luo, Y.J.; Zha, L.; Luo, L.M.; Chen, X.; Zhang, Q.; Gao, C.X.; Zhuang, X.B.; Yuan, S.J.; Qiao, T.K. [6]-Gingerol enhances the cisplatin sensitivity of gastric cancer cells through inhibition of proliferation and invasion via PI3K/Akt signaling pathway. Phytother. Res. 2019, 33, 1353–1362. [Google Scholar] [CrossRef] [PubMed]
- Jia, N.; Xiong, Y.L.L.; Kong, B.H.; Liu, Q.; Xia, X.F. Radical scavenging activity of black currant (Ribes nigrum L.) extract and its inhibitory effect on gastric cancer cell proliferation via induction of apoptosis. J. Funct. Foods 2012, 4, 382–390. [Google Scholar] [CrossRef]
- Pan, M.H.; Chang, Y.H.; Badmaev, V.; Nagabhushanam, K.; Ho, C.T. Pterostilbene induces apoptosis and cell cycle arrest in human gastric carcinoma cells. J. Agric. Food Chem. 2007, 55, 7777–7785. [Google Scholar] [CrossRef] [PubMed]
- Hong, J.Y.; Song, S.H.; Park, H.J.; Cho, Y.J.; Pyee, J.H.; Lee, S.K. Antioxidant, antiinflamatory, and antiproliferative activities of strawberry extracts. Biomol. Ther. 2008, 16, 286–292. [Google Scholar] [CrossRef] [Green Version]
- Jung, E.B.; Trinh, T.A.; Lee, T.K.; Yamabe, N.; Kang, K.S.; Song, J.H.; Choi, S.; Lee, S.; Jang, T.S.; Kim, K.H.; et al. Curcuzedoalide contributes to the cytotoxicity of Curcuma zedoaria rhizomes against human gastric cancer AGS cells through induction of apoptosis. J. Ethnopharmacol. 2018, 213, 48–55. [Google Scholar] [CrossRef]
- Olivas-Aguirre, F.J.; Rodrigo-Garcia, J.; Martinez-Ruiz, N.D.; Cardenas-Robles, A.I.; Mendoza-Diaz, S.O.; Alvarez-Parrilla, E.; Gonzalez-Aguilar, G.A.; de la Rosa, L.A.; Ramos-Jimenez, A.; Wall-Medrano, A. Cyanidin-3-O-glucoside: Physical-chemistry, foodomics and health effects. Molecules 2016, 21, 1264. [Google Scholar] [CrossRef] [Green Version]
- Itoh, H.; Ito, H.; Hibasami, H. Blazein of a new steroid isolated from Agaricus blazei Murrill (himematsutake) induces cell death and morphological change indicative of apoptotic chromatin condensation in human lung cancer LU99 and stomach cancer KATO III cells. Oncol. Rep. 2008, 20, 1359–1361. [Google Scholar]
- Oliveira, M.; Reis, F.S.; Sousa, D.; Tavares, C.; Lima, R.T.; Ferreira, I.C.F.R.; dos Santos, T.; Vasconcelos, M.H. A methanolic extract of Ganoderma lucidum fruiting body inhibits the growth of a gastric cancer cell line and affects cellular autophagy and cell cycle. Food Funct. 2014, 5, 1389–1394. [Google Scholar] [CrossRef]
- Liang, C.Y.; Li, H.R.; Zhou, H.; Zhang, S.Q.; Liu, Z.Y.; Zhou, Q.L.; Sun, F. Recombinant Lz-8 from Ganoderma lucidum induces endoplasmic reticulum stress-mediated autophagic cell death in SGC-7901 human gastric cancer cells. Oncol. Rep. 2012, 27, 1079–1089. [Google Scholar] [CrossRef] [Green Version]
- Shomori, K.; Yamamoto, M.; Arifuku, I.; Teramachi, K.; Ito, H. Antitumor effects of a water-soluble extract from Maitake (Grifola frondosa) on human gastric cancer cell lines. Oncol. Rep. 2009, 22, 615–620. [Google Scholar] [CrossRef] [Green Version]
- Oliveira, H.; Cai, X.S.; Zhang, Q.; de Freitas, V.; Mateus, N.; He, J.R.; Fernandes, I. Gastrointestinal absorption, antiproliferative and anti-inflammatory effect of the major carotenoids of Gardenia jasminoides Ellis on cancer cells. Food Funct. 2017, 8, 1672–1679. [Google Scholar] [CrossRef]
- Lee, S.H.; Choi, W.C.; Kim, K.S.; Park, J.W.; Lee, S.H.; Yoon, S.W. Shrinkage of gastric cancer in an elderly patient who received Rhus verniciflua stokes extract. J. Altern. Complem. Med. 2010, 16, 497–500. [Google Scholar] [CrossRef] [PubMed]
- Li, W.Q.; Zhang, J.Y.; Ma, J.L.; Li, Z.X.; Zhang, L.; Zhang, Y.; Guo, Y.; Zhou, T.; Li, J.Y.; Shen, L.; et al. Effects of Helicobacter pylori treatment and vitamin and garlic supplementation on gastric cancer incidence and mortality: Follow-up of a randomized intervention trial. BMJ Br. Med. J. 2019, 366, 15016. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ina, K.; Kataoka, T.; Ando, T. The use of lentinan for treating gastric cancer. Anti-Cancer Agents Med. Chem. 2013, 13, 681–688. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ito, G.; Tanaka, H.; Ohira, M.; Yoshii, M.; Muguruma, K.; Kubo, N.; Yashiro, M.; Yamada, N.; Maeda, K.; Sawada, T.; et al. Correlation between efficacy of PSK postoperative adjuvant immunochemotherapy for gastric cancer and expression of MHC class I. Exp. Ther. Med. 2012, 3, 925–930. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Banerjee, S.; Kong, D.J.; Wang, Z.W.; Bao, B.; Hillman, G.G.; Sarkar, F.H. Attenuation of multi-targeted proliferation-linked signaling by 3,3‘-diindolylmethane (DIM): From bench to clinic. Mutat. Res. Rev. Mutat. 2011, 728, 47–66. [Google Scholar] [CrossRef] [Green Version]
- Mannava, M.K.C.; Suresh, K.; Bommaka, M.K.; Konga, D.B.; Nangia, A. Curcumin-artemisinin coamorphous solid: Xenograft model preclinical study. Pharmaceutics 2018, 10, 7. [Google Scholar] [CrossRef] [Green Version]
- Correa-Betanzo, J.; Allen-Vercoe, E.; McDonald, J.; Schroeter, K.; Corredig, M.; Paliyath, G. Stability and biological activity of wild blueberry (Vaccinium angustifolium) polyphenols during simulated in vitro gastrointestinal digestion. Food Chem. 2014, 165, 522–531. [Google Scholar] [CrossRef] [PubMed]
- Fang, J. Bioavailability of anthocyanins. Drug Metab. Rev. 2014, 46, 508–520. [Google Scholar] [CrossRef]
- Aditya, N.P.; Shim, M.; Lee, I.; Lee, Y.; Im, M.H.; Ko, S. Curcumin and genistein coloaded nanostructured lipid carriers: In vitro digestion and antiprostate cancer activity. J. Agric. Food Chem. 2013, 61, 1878–1883. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.; Xia, Z.Y.; Zheng, J.K.; Qiu, P.J.; Zhang, L.J.; McClements, D.J.; Xiao, H. Nanoemulsion-based delivery systems for nutraceuticals: Influence of carrier oil type on bioavailability of pterostilbene. J. Funct. Foods 2015, 13, 61–70. [Google Scholar] [CrossRef]
- Daware, M.B.; Mujumdar, A.M.; Ghaskadbi, S. Reproductive toxicity of piperine in Swiss albino mice. Planta Med. 2000, 66, 231–236. [Google Scholar] [CrossRef] [PubMed]
- Walsh, K.R.; Zhang, Y.C.; Vodovotz, Y.; Schwartz, S.J.; Failla, M.L. Stability and bioaccessibility of isoflavones from soy bread during in vitro digestion. J. Agric. Food Chem. 2003, 51, 4603–4609. [Google Scholar] [CrossRef] [PubMed]
- Reis, F.S.; Martins, A.; Vasconcelos, M.H.; Morales, P.; Ferreira, I.C.F.R. Functional foods based on extracts or compounds derived from mushrooms. Trends Food Sci. Technol. 2017, 66, 48–62. [Google Scholar] [CrossRef]
- Leibelt, D.A.; Hedstrom, O.R.; Fischer, K.A.; Pereira, C.B.; Williams, D.E. Evaluation of chronic dietary exposure to indole-3-carbinol and absorption-enhanced 3,3‘-diindolylmethane in Sprague-Dawley rats. Toxicol. Sci. 2003, 74, 10–21. [Google Scholar] [CrossRef] [Green Version]
- Li, G.; Yu, K.; Li, F.S.; Xu, K.P.; Li, J.; He, S.J.; Cao, S.S.; Tan, G.S. Anticancer potential of Hericium erinaceus extracts against human gastrointestinal cancers. J. Ethnopharmacol. 2014, 153, 521–530. [Google Scholar] [CrossRef]
- Balaji, S.; Chempakam, B. Pharmacokinetics prediction and drugability assessment of diphenylheptanoids from turmeric (Curcuma longa L). Med. Chem. 2009, 5, 130–138. [Google Scholar] [CrossRef]
Natural Products | Phytochemicals | Subjects | Study Type | Consumed Levels | Effects | Ref. |
---|---|---|---|---|---|---|
Fruits | ||||||
Citrus fruits | NA | 217 Gastric cancer cases (mean age: 65.4; 151 men) and controls (mean age: 64.3; 265 men) in Iran | Case-control | ≥3 times/week vs. never or infrequently intake of citrus fruits | Reducing gastric cancer risk (OR, 0.31; 95% CI, 0.17–0.59) | [30] |
Citrus fruits | NA | 120,852 Subjects in Netherlands (58,279 men and 62,573 women), 156 gastric cardia adenocarcinoma cases and 460 gastric noncardia adenocarcinoma cases; aged 55–69 years | Cohort study | The highest (median = 156 g/d) vs. the lowest quintile (median = 0 g/d) of citrus fruits | Reducing the risk of gastric noncardia cancer (RR, 0.38; 95% CI, 0.21–0.69) | [34] |
Total fruits (except watermelon) | NA | 559,247 Chinese men in the cohort and 132 distal gastric cancer cases; aged 40–74 years | Cohort study | >104.2 vs. ≤20.1 g/d all fruits (except watermelon) | Reducing distal gastric cancer risk (HR, 0.50; 95% CI, 0.29–0.84) | [47] |
Total fruits (except watermelon) | NA | 73,064 Chinese women in the cohort and 206 distal gastric cancer cases; aged 40–70 years | Cohort study | >208.0 vs. ≤61.5 g/d all fruits (except watermelon) | No association (HR, 1.02; 95% CI, 0.68–1.54) | |
Total fruit | NA | 191,232 Japanese subjects, (87,771 men and 103,461 women) and 2995 gastric cancer cases (2104 men and 891 women) | Pooled analysis | The highest quintile vs. the lowest quintile of total fruit | No association (HR, 0.9; 95% CI, 0.67–1.22) | [44] |
Vegetables | ||||||
Brassica vegetables | NA | 120,852 Subjects in Netherlands (58,279 men and 62,573 women), 156 gastric cardia adenocarcinoma cases and 460 gastric noncardia adenocarcinoma cases; aged 55–69 years | Cohort study | The highest (median = 59 g/d) vs. the lowest quintile (median = 11 g/d) of Brassica vegetables | Reducing the risk of gastric noncardia cancer (RR, 0.51; 95% CI, 0.28–0.92) | [34] |
Total vegetables | NA | 559,247 Chinese men in the cohort and 132 distal gastric cancer; aged 40–74 years | Cohort study | >429.3 vs. ≤212.9 g/d total vegetables | No association (HR, 1.00; 95% CI, 0.59–1.68) | [47] |
Total vegetables | NA | 73,064 Chinese women in the cohort and 206 distal gastric cancer cases; aged 40–70 years | Cohort study | >373.7 vs. ≤179.5 g/d total vegetables | No association (HR, 0.89; 95% CI, 0.60–1.31) | |
Total vegetables | NA | 191,232 Japanese subjects, (87,771 men and 103,461 women) and 2995 gastric cancer cases (2104 men and 891 women) | Pooled analysis | The highest quintile vs. the lowest quintile of total vegetable | Reducing distal gastric cancer risk in men (multivariate HR, 0.78; 95% CI, 0.63–0.97) | [44] |
Fruits and vegetables | ||||||
Fruits and vegetables | β-carotene | 511 Japanese gastric cancer cases (342 men) and 511 controls (342 men); aged 40–69 years | Nested case-control | ≥27.0 vs. ≤8.0 ug/dL β-carotene | Reducing gastric cancer risk (OR, 0.46; 95% CI, 0.28–0.75) | [39] |
Vegetables, citrus fruits, and whole grains | NA | 970,045 American subjects (533,391 women and 436,654 men) and 439 women and 910 men died from gastric cancer | Cohort study | The highest vs. the lowest tertile of plant foods | Reducing gastric cancer risk in men (RR, 0.79; 95% CI, 0.67–0.93) | [35] |
Fruits, vegetables and beverages | Quercetin | 505 Swedish gastric cancer cases (336 men) and 1116 controls (746 men); aged 40–79 years | Case-control | ≥11.9 vs. <4 mg /day quercetin | Reducing noncardia gastric adenocarcinoma risk (OR, 0.57; 95% CI, 0.40–0.83) | [19] |
Spices | ||||||
Allium vegetables | NA | 543,220 Total subjects | Meta-analysis | The highest vs. the lowest consumption category of allium vegetables | Reducing gastric cancer risk (OR, 0.54; 95% CI, 0.43–0.65) | [36] |
Garlic | NA | 217 Gastric cancer cases (mean age: 65.4; 151 men) and controls (mean age: 64.3; 265 men) in Iran | Case-control | ≥3 times/week vs. never or infrequently intake of garlic | Reducing gastric cancer risk (OR, 0.35; 95% CI, 0.13–0.95) | [30] |
Onion | NA | ≥ once per day vs. ≤2 times/week onion | Reducing gastric cancer risk (OR, 0.34; 95% CI, 0.19–0.62) | |||
Soy and soy products | ||||||
Soy | Isoflavone | 84,881 Japanese subjects (39,569 men and 45,312 women), 1249 gastric cancer cases; aged 45–74 years | Cohort study | The highest vs. the lowest quartile of isoflavone | No association (HR, 1.00; 95% CI, 0.81-1.24 for men and HR, 1.07; 0.77–1.50 for women) | [49] |
Soy | Isoflavone | 30,792 Japanese subjects (14,219 men and 16,573 women), 678 gastric cancer cases (441 men and 237 women); aged ≥ 35 years | Cohort study | >53 vs. ≤28 mg/d isoflavone | Reducing gastric cancer risk in women (HR, 0.60; 95% CI, 0.37–0.98) | [18] |
>122 vs. ≤62 g/d soy food | Reducing gastric cancer risk in men(HR, 0.71; 95% CI, 0.53–0.96) and women (HR, 0.58; 95% CI, 0.36–0.94) | |||||
Tofu | NA | 128,687 Chinese subjects (70,446 women and 58,241 men), 493 distal gastric cancer cases; aged 40–74 years | Cohort study | >8.4 vs. <3.1 g/d tofu | Reducing distal gastric cancer risk in men (HR, 0.64; 95% CI, 0.42–0.99) | [38] |
Dry bean | NA | >0.9 vs. 0.0 g/d dry bean | Reducing gastric cancer risk in postmenopausal women (HR, 0.63; 95% CI, 0.43–0.91) | |||
Total soy product | NA | 30,304 Japanese subjects (13,880 men and 16,424 women) and 121 gastric cancer deaths; aged ≥ 35 years | Cohort study | The highest (median = 49.7 g/d) vs. the lowest tertile (median = 140 g/d) of total soy product | Reducing the risk of gastric cancer death (HR, 0.5; 95% CI, 0.26–0.93) | [28] |
Cereals | ||||||
Other | ||||||
Flavonoids | 469,008 American subjects (275,982 men and 193,026 women), 1297 gastric cancer cases; aged 50–71 years | Cohort study | 438.0–4211.2 vs. 0–84.1 mg/d total flavonoids | No association (HR, 1.02; 95% CI, 0.78–1.34) for gastric cardia cancer; (HR, 1.11; 95% CI, 0.86–1.44) for gastric noncardia cancer | [50] | |
Flavonoids | 334 Korean gastric cancer cases (208 men) and 334 controls (208 men); aged 35–75 years | Case-control study | The highest tertile (median = 152.3 mg/d) vs. the lowest tertile (median = 52.5 mg/d) of flavonoids | Reducing gastric cancer risk (OR, 0.49; 95% CI, 0.31–0.76) | [40] | |
Anthocyanidins | 248 American gastric cardia cancer cases and 662 controls; aged 30–79 years | Case-control study | ≥18.48 vs. ≤7.21 mg/d anthocyanidins | Reducing the risk of mortality for gastric cardia cancer (HR, 0.63; 95% CI, 0.42–0.95) | [42] |
Natural Products | Phytochemicals | Study Type | Models | Mechanisms | Molecular Targets | Ref. |
---|---|---|---|---|---|---|
Fruits | ||||||
Citrus reticulata Blanco extract | NA | In vitro | SNU-668 cells | Induced apoptosis | ↓ Bcl-2 ↑ Bax and caspase-3 | [71] |
Cirsium chanroenicum | Pectolinarigenin | In vitro | AGS and MKN-28 cells | Induced autophagy and apoptosis Inhibited cell growth and proliferation | ↓ p-4EBP1, p-p70S6K, and p-eIF4E, ↑ LC3-II conversion | [82] |
Citrus fruits | Poncirin | In vitro | AGS cells | Induced apoptosis Inhibited cell proliferation | ↑ FasL, caspase-8, caspase-3 and PARP cleavage | [70] |
Black currant | Phenolic compounds | In vitro | SGC-7901 cells | NA | [113] | |
Blueberries | Pterostilbene | In vitro | AGS cells | ↓ p-Rb, cyclin A, cyclin E, Cdk2, Cdk4, and Cdk6, ↑ caspase-2, -3, -8, and -9, PARP cleavage, p53, p2l, p27, and p16 proteins | [114] | |
Citrus fruits | Tangeretin | In vitro | SGC7901 cells | Inhibited radiation-mediated EMT, migration and invasion | ↓ Notch-1, Jagged1/2, Hey-1 and Hes-1, ↑ miR-410 | [93] |
Mangosteen | α-Mangostin | In vitro | BGC-823 and SGC-7901 cells | Induced apoptosis Inhibited the cell viability | ↓ STAT3, Bcl-xL and Mcl-1, ↑ cytochrome c | [72] |
Mangosteen | Gartanin and TRAIL | In vitro | AGS cells | Enhanced the sensitization of AGS cells to TRAIL | ↑ death receptor 5 | [107] |
Strawberry | NA | In vitro | SNU-638 cells | Inhibited cell growth | NA | [115] |
Citrus reticulate cv. Suavissima | Poncirin | In vitro | SGC-7901 cells | [54] | ||
Vegetables | ||||||
Cruciferous vegetables | 3,3’-Diindolylmethane | In vitro | BGC-823 and SGC-7901 cells | Inhibited cell proliferation Induced autophagy | ↓ MicroRNA-30e, ↑ ATG5 and LC3 | [83] |
In vivo | Female nude mice | Inhibited the growth of gastric tumor | ↑ LC3 | |||
Cruciferous vegetables | Paclitaxel and 3,3’-diindolylmethane | In vitro | SNU638 cell | Induced apoptosis Inhibited proliferation | ↑ PARP, caspase-9, ↓ CDK4, p53, cyclin D1 and p-Akt | [109] |
Spices | ||||||
Fruit of long pepper | Piperlongumine | In vitro | SGC-7901, BGC-823 and KATO III cells | Induced apoptosis | ↓ TrxR1, ↑ ROS | [21] |
In vivo | Female BALB/cA athymic mice | Reduced tumor cell burden | ↓ TrxR1 | |||
Allitridi | NA | In vitro | BGC823 cells | Induced apoptosis Inhibited cell proliferation | ↓ Bcl-2, ↑ caspase-3 | [52] |
Allium ursinum L | NA | In vitro | AGS cells | ↓ cyclin B | [56] | |
Garlic | Diallyl trisulfide | In vitro | AGS cells | ↑ ROS, phosphorylation of AMPK and histone H3 | [60] | |
Ginger | 6-Shogaol | In vitro | HGC, AGS and KATO III cells | Inhibited cell viability Induced mitotic arrest Damaged microtubules | NA | [64] |
In vivo | Athymic nude mice | Suppressed tumor growth | NA | |||
Ginger | Zerumbone | In vitro | AGS cells | Anti-angiogenesis | ↓ VEGF and NF-κB | [89] |
Ginger | 6-Gingerol and cisplatin | In vitro | HGC-27 cells | Inhibited cell proliferation, migration and invasion | ↑ P21 and P27, ↓ cyclin D1, cyclin A2, MMP-9, p-PI3K, Akt, and p-Akt | [112] |
Curcuma zedoaria rhizomes | Curcuzedoalide | In vitro | AGS cells | Induced apoptosis Inhibited cell viability | ↑ cleavage of caspase-8, caspase-9, caspase-3 and PARP | [116] |
Curcuma mangga rhizomes | Labdane diterpenes | In vitro | AGS cells | Inhibited cell proliferation | NA | [53] |
Turmeric | Curcumin, etoposide and doxorubicin | In vitro | SGC-7901 cells | Enhanced the anticancer efficacy of etoposide and doxorubicin | ↓ NF-κB, Bcl-2 and Bcl-xL | [10] |
Garlic | Diallyl trisulfide and docetaxel | In vitro | BGC823 cells | Induced apoptosis Induced G2/M cell cycle arrest | ↑ MT2A, IκB-α, cyclin B1, activated caspase-3, and Bax, ↓ p-IκB-α, p-P65, cyclin D1, and XIAP | [110] |
In vivo | Female BALB/c athymic mice | Inhibited tumor growth | ↑ MT2A, IjB-a, CCNB1, and a-CASP3, ↓ CCND1 | |||
Garlic | Diallyl disulfide | In vitro | MGC803 cells | Inhibited cell growth Induced cell differentiation | ↓ CDC25C, cyclin B1, p-ERK1/2, ↑ p-Chkl | [57,59] |
Garlic | Diallyl disulfide | In vitro | AGS cells | Inhibited tumor cell motility and invasion | ↓ MMP-2, MMP-9, claudin proteins (claudin-2, -3, and -4), ↑ TIMP-1, TIMP-2 | [94] |
Garlic derivatives | S-allylmercaptocysteine | In vivo | Female BALB/c nude mice | Inhibited the growth of gastric tumor | NA | [63] |
Zanthoxylum nitidum (Roxb) DC | Nitidine chloride | In vitro | SGC-7901 and AGS cells | Induced apoptosis Inhibited cell viability and angiogenesis | ↓ p-STAT3, cyclin D1, Bcl-2, Bcl-xL, and VEGF | [23] |
In vivo | Male BALB/cA nude mice | Reduced the volume of tumors | ↓ STAT3 and VEGF | |||
Mushroom | ||||||
Liang Jin mushroom | 3’-azido-3’-deoxythymidine (AZT) and RNA-protein complex (FA-2-b-β) | In vitro | MKN-45 cells | Induced apoptosis Inhibited cell proliferation | ↓ tumor cell telomerase and Bcl-2, ↑caspase-3 | [117] |
Agaricus blazei Murrill | Blazein | In vitro | KATO III cells | Induced apoptosis Suppressed cell growth | NA | [118] |
Phellinus linteus | Polyphenol compound hispolon | In vitro | SGC-7901, MGC-803, and MKN-45 cells | Induced apoptosis | ↓ Bcl-2, ↑ ROS, cytochrome c, caspase-3 and caspase-9 | [74] |
Hericium erinaceus mycelium | Erinacine A | In vitro | TSGH9201 and MKN-28 human gastric cancer cells | Induced apoptosis Inhibited the viability and invasiveness | ↓ Bcl-2 and Bcl-XL, ↑ ROS, MTUS2, TRAIL, caspase 8, caspase 9, caspase 3, cytochrome c and phosphorylation of FAK/Akt/p70S6K and PAK1 | [91] |
Lentinula edodes C91-3 | Latcripin 1 protein | In vitro | SGC-7901 and BGC-823 cells | Induced autophagy and apoptosis Inhibit cell growth and proliferation | ↓ Bcl-2, MMP-2 and MMP-9, ↑ Bax, caspase-3, ATG7, ATG5, ATG12, ATG14 and Beclin1 | [61] |
Ganoderma lucidum | NA | In vitro | AGS cells | ↑ LC3-II | [119] | |
Recombinant Lz-8 protein | In vitro | SGC-7901 cells | Induced autophagic cell death Inhibited cell growth | ↑ CHOP, ATF4 and GRP78 | [120] | |
Fomes Fomentarius | Polysaccharide | In vitro | SGC-7901 and MKN-45 cells | Inhibited cell proliferation | NA | [20] |
Maitake (Grifola frondosa) | NA | In vitro | TMK-1, MKN-28, MKN-45 and MKN-74 cells | NA | [121] | |
Soy | ||||||
Black soybean | NA | In vitro | AGS cells | Induced apoptosis Inhibited cell proliferation | ↓ Bcl-2, ↑ Bax, caspase-3, PARP cleavage | [75] |
Soy products | Genistein, fluorouracil and ciplatin | In vitro | MGC-803 cells | Decreased chemoresistance | ↓ ABCG2, ERK1/2 | [108] |
Traditional medicine | ||||||
Gardenia jasminoides Ellis | Carotenoids | In vitro | MKN-28 cells | Inhibited cell proliferation | NA | [122] |
Perilla frutescens | Perillaldehyde | In vitro | MFCs and GC9811-P cells | Induced autophagy | ↑ p-AMPK | [84] |
In vivo | Female BAL B/c nude mice | Inhibited the growth of gastric tumor Induced autophagy | ↑ beclin-1, LC3-II, cathepsin, caspase-3 and p53 | |||
Vitex agnus-castus fruit | NA | In vitro | KATO-III Cells | Induced apoptosis | ↓ Bcl-2, Bcl-XL, Bid, Mn-superoxide dismutase and catalase, GSH, ↑ Bad, cytochrome c, caspase-3 caspases-8, caspases-9, hemeoxygenase-1 and thioredoxin reductase | [73] |
Bamboo shavings | Polysaccharides | In vivo | Syngeneic murine gastric cancer model | Inhibited tumor growth Prolonged the survival | ↑ cleaved caspase 3, Bax and Bik | [79] |
Other | ||||||
Protocatechuic acid | In vitro | AGS cells | Induced apoptosis Inhibited cell proliferation | ↓ cyclin B, ↑ JNK and p38 MAPK | [69] | |
Kaempferol | In vitro | AGS, NCI-N87, SNU-638 and MKN-74 cells | Induced autophagic cell death Decreased cell viability | ↓ p62, ↑ LC3B, Beclin-1, ATG5, p-IRE1 and p-JNK | [22] | |
Myricetin | In vitro | HGC-27 and SGC7901 cells | Inhibited cell proliferation | ↑ Mad1 | [62] | |
Apigenin | In vitro | SGC-7901 cells | Inhibited cell growth | NA | [55] | |
Luteolin | In vitro | Hs-746T and MKN-28 cells | Induced cell apoptosis Inhibited cell proliferation, invasion, and migration | ↓ Notch1 | [92] | |
In vivo | Male BALB/c nude mice | Reduced gastric tumor volume and tumor weight | ↓ β-catenin, Notch1 and Ki-67 | |||
Gallic acid | In vitro | AGS cells | Inhibited cell metastasis | ↓ MMP-2, MMP-9, NF-κB, Ras, Cdc42, Rac1, RhoA, RhoB and PI3K | [90] | |
Luteolin | In vitro | MGC-803 and Hs-746T cells | Anti-angiogenesis Inhibited the formation of vasculogenic mimicry tube | ↓ VEGF and Notch1 | [88] | |
Quercetin and SN-38 (a metabolite of irinotecan) | In vivo | Female BALB/c nude mice | Reduced the volume of tumors Anti-angiogenesis and anti-metastasis | ↓ cyclooxygenase-2, Twist1, ITGβ6, VEGF-R2 and VEGF-A | [24] | |
In vitro | AGS cells | Induced apoptosis | ↓ β-catenin |
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Mao, Q.-Q.; Xu, X.-Y.; Shang, A.; Gan, R.-Y.; Wu, D.-T.; Atanasov, A.G.; Li, H.-B. Phytochemicals for the Prevention and Treatment of Gastric Cancer: Effects and Mechanisms. Int. J. Mol. Sci. 2020, 21, 570. https://doi.org/10.3390/ijms21020570
Mao Q-Q, Xu X-Y, Shang A, Gan R-Y, Wu D-T, Atanasov AG, Li H-B. Phytochemicals for the Prevention and Treatment of Gastric Cancer: Effects and Mechanisms. International Journal of Molecular Sciences. 2020; 21(2):570. https://doi.org/10.3390/ijms21020570
Chicago/Turabian StyleMao, Qian-Qian, Xiao-Yu Xu, Ao Shang, Ren-You Gan, Ding-Tao Wu, Atanas G. Atanasov, and Hua-Bin Li. 2020. "Phytochemicals for the Prevention and Treatment of Gastric Cancer: Effects and Mechanisms" International Journal of Molecular Sciences 21, no. 2: 570. https://doi.org/10.3390/ijms21020570