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 |
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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
APA StyleMao, Q. -Q., Xu, X. -Y., Shang, A., Gan, R. -Y., Wu, D. -T., Atanasov, A. G., & Li, H. -B. (2020). Phytochemicals for the Prevention and Treatment of Gastric Cancer: Effects and Mechanisms. International Journal of Molecular Sciences, 21(2), 570. https://doi.org/10.3390/ijms21020570