Chemopreventive Effects of Strawberry and Black Raspberry on Colorectal Cancer in Inflammatory Bowel Disease
Abstract
:1. Introduction
2. Animal Models of Inflammatory Bowel Disease and IBD-Related Colorectal Cancer
3. Molecular Mechanisms Associated with Chronic Inflammation and Colorectal Cancer
3.1. Inflammation-Dependent Oxidative Stress
3.2. Genomic Instability
3.3. Cytokines
3.4. NFκB
3.5. Microbiome
4. Chemoprevention of Colorectal Cancer in Inflammatory Bowel Disease with Anti-Inflammation Pharmaceuticals
5. Chemoprevention of Colorectal Cancer in Inflammatory Bowel Disease with Berries
5.1. Efficiency of Strawberry and Black Raspberry in Cell Lines and Animal Models
5.2. Efficiency of Black Raspberry in Clinical Studies
5.3. Major Bioactive Components in Berries
5.4. Mechanisms Associated with Preventative Effects of Berries on Colon Cancer
6. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Systems | Major Findings | Ref. |
---|---|---|
Black Raspberry | ||
1. CRC Cell Lines | ||
HT-29 /HT-116 cell lines | Regulating cell cycle and apoptosis | [56,57] |
2. Animal Models of IBD | ||
DSS treated mouse | Colonic epithelium acute injury↓, ulceration↓, TNF-α and IL-1β↓, COX2 and NFκB↓ | [58] |
DSS treated mouse | Ulceration↓, macrophages and neutrophils infiltrated the colon tissue↓, NFκB↓, Dkk3↑, β-Catenin nuclear localization↓,c-Myc, DNMT3B, HDAC1, HDAC2, MBD2↓ | [59] |
IL-10 knockout mice | Ulceration↓, Wnt pathway↓, wif1, sox17, and qki↑,dnmt3b, hdac1, hdac2, and mbd2↓ | [60] |
3. Animal Models of IBD-Related CRC | ||
Mouse epidermal JB6Cl41 cells | AP-1, NFκB, and COX-2↓ | [61,62] |
AOM induced rat model | ACF multiplicity↓, total tumor multiplicity↓, urinary 8-OHdG↓ | [63] |
Muc2−/− mice | COX-2, TNF-α, IL-1, IL-6, and IL-10 ↓ | [64] |
4.Clinical Studies of CRC | ||
CRC patients | GM-CSF and IL-8↓, Ki-67↓, apoptosis↓ | [65] |
CRC patients | Wnt pathway↓ (SFRP2, WIF1, β-catenin, E-cadherin), DNMT1↓ | [66] |
Strawberry | ||
1. CRC Cell Lines | ||
HT-29 cell lines | Proliferation↓, cell apoptosis and p21WAF1↑ | [57,67] |
CaCo-2 | Proliferation↓ | [68] |
HCT-116 | Proliferation↓ | [69] |
2. Animal Models of IBD | ||
Gum acacia induced IBD rats | Disease activity index↓, lesion scores↓, antioxidant enzymes myeloperoxidase↑, tissue catalase↑, superoxide dismutase↑ | [70] |
3. Animal Models of IBD-Related CRC | ||
AOM/DSS mouse | Tumor incidence↓, nitrosative stress↓, TNF-α, IL-1β, IL-6, COX-2 and iNOS ↓, PI3K, Akt, ERK and NFκB↓ | [18] |
Strawberry | Black Raspberry | ||||
---|---|---|---|---|---|
mg/ 100 mg | % by mg | mg/ 100 mg | % by mg | ||
Anthocyanins | Anthocyanins | ||||
pelargonidin glucoside | 367.7 | 41.1 | cyanidin rutinoside | 2924.7 | 58.2 |
pelargonidin malonyl glucoside | 83.9 | 9.4 | cyanidin xylorutinoside | 916.3 | 18.2 |
pelargonidin rutinoside | 55.3 | 6.2 | cyanidin glucoside | 245.1 | 4.9 |
cyanidin glucoside | 14.9 | 1.7 | cyanidin sambubioside | 103.5 | 2.1 |
pelargonidin rutinoside | 38.3 | 0.8 | |||
130.4 | 58.4% | 4227.9 | 84.2% | ||
Ellagitannins | Ellagitannins | ||||
ellagitannin | 64.1 | 7.2 | sanguiin H6 | 173.2 | 3.4 |
ellagitannin | 11.4 | 1.3 | ellagitannin 783-1 | 101.1 | 2.0 |
ellagitannin | 23.1 | 2.6 | ellagitannin 933-2 | 75.8 | 1.5 |
Lambertianin | 20.3 | 2.3 | elagitannin 783-2 | 75.8 | 1.5 |
ellagitannin 935-1 | 62.8 | 1.3 | |||
ellagitannin 933-1 | 50.5 | 1.0 | |||
Lambertiannin | 31.3 | 0.6 | |||
ellagitannin 935-2 | 7.9 | 0.2 | |||
118.9 | 13.3% | 578.5 | 11.5% | ||
Ellagic acid and derivatives | Ellagic acid and derivatives | ||||
Agrimoniin | 144.5 | 16.2 | methyl ellagic acid pentoside | 16.0 | 0.3 |
ellagic acid rhamnoside | 23.1 | 2.6 | ellagic acid | 9.3 | 0.2 |
ellagic acid | 7.3 | 0.8 | ellagic acid rhamnoside | 5.8 | 0.1 |
myricetin hexoside, EA derivative (coelution) | 3.8 | 0.1 | |||
174.9 | 19.5% | 34.8 | 0.7% | ||
Flavonols | Flavonols | ||||
quercetin hexuronide | 58.8 | 6.6 | quercetin hexuronide | 82.2 | 1.6 |
kaempferol glucoside/hexuronide | 14.5 | 1.6 | rutin (quercetin rutinoside) | 75.4 | 1.5 |
kaempferol malonyl hexoside | 5.1 | 0.6 | quercetin xylorutinoside | 24.2 | 0.5 |
78.4 | 8.8% | 181.8 | 3.6% |
Original Sources | Models | Major Findings | Anthocyanin Profiles | Ref. |
---|---|---|---|---|
Cell Lines | ||||
1. Black Raspberry | ||||
Black raspberry extract | Cell line HT-29 HCT-116 | Inhibited cell growth HT-29 IC50 = 89.11, HCT-116, IC50 = 89.00 | cyanidin-3-sophoroside rhamnoside, cyanidin-3-sambubioside rhamnoside, cyanidin-3-rutinoside | [57] |
Black raspberry anthocyanin-enriched extract | Cell line HCT116 | Decreased DNMT activity; decreased methylation of CDKN2A, SFRP5, SFRP2 and WIF1; suppressed cell proliferation; induced apoptosis | cyanidin-3-O-glucoside, cyanidin- 3-O-rutinoside, cyanidin-3-O-xylosylrutinoside, cyanidin-3-O-sambubioside | [58] |
2. Strawberry | ||||
Strawberry extract | Cell line HT-29 HCT-116 | Inhibited cell growth HT-29 IC50 = 114.30, HCT-116, IC50 = 62.00 | cyanidin-3-glucoside, pelargonidin-3-glucoside, pelargonidin-3-rutinoside | [57] |
Strawberry extract | Cell line HT29 HCT-116 | Antioxidative effects. | cyanidin-3-glucoside, pelargonidin, cyanidin-3-glucoside, pelargonidin, pelargonidin-3-rutinoside | [66] |
Strawberry extract | Cell line HT29 | Inhibited proliferation; reduced expression of p21WAF1 | cyanidin derivative; pelargonidin derivative | [67] |
3. Anthocyanins | ||||
cyanidin-3-glycoside | Cell line HCEC | Decreased DNA strand breakage | cyanidin-3-glycoside | [72] |
Cyanidin-3-glycoside | Cell line Caoco-2 | Reduced cytotoxicity induced by AAPH; suppressed apoptosis; decreased sub-G1 phase cell population | cyanidin-3-glycoside | [73] |
Cyanidin-3-O-beta glucopyranoside, cyanidin chloride | Cell line Caoco-2 | Inhibited cell growth and proliferation; decreased reactive oxygen species (ROS) level | cyanidin-3-O-beta glucopyranoside, cyanidin chloride | [74] |
4. Protocatechuic Acid (PCA) | ||||
Brown rice extracted PCA | Cell line SW480 | Inhibited cell growth and colony formation | PCA | [75] |
5. Other Fruit and Vegetables | ||||
Blueberry | Cell line Caoco-2 | IC50 0.53 ± 0.04 | delphinidin 3-galactoside, delphinidin 3-glucoside, cyanidin 3-galactoside, delphinidin 3-arabinoside, cyanidin 3-glucoside, petunidin 3-galactoside, cyanidin 3-arabinoside, petunidin 3-glucoside, peonidin 3-galactoside, petunidin 3-arabinoside, peonidin 3-glucoside, malvidin 3-galactoside, peonidin 3-arabinoside, malvidin 3-glucoside, malvidin 3-arabinoside | [76] |
Blueberry extract | Cell lines HT-29 | Inhibited cell growth; induced apoptosis | delphinidin 3-O-β-glucopyranoside; cyanidin 3-O-β-galactopyranoside; cyanidin 3-O-β-glucopyranoside; petunidin 3-O-β-glucopyranoside; peonidin 3-O-β-galactopyranoside; peonidin 3-O-β-glucopyranoside; malvidin 3-O-β-glucopyranoside. | [77] |
Bilberry purified anthocyanins | Cell line HCT-116 | Decreased cell viability | pelargonidin, cyanidin, peonidin, delphinidin, and malvidin | [78] |
Cocoplum anthocyanins exert | Cell line HT-29 | Cell proliferation was suppressed; increased intracellular ROS production; increased intracellular ROS production | delphinidin-3-glucoside, cyanidin 3-glucoside, petunidin 3-glucoside, delphinidin 3-(6-acetoyl) galactoside, delphinidin 3-(6-oxaloyl) arabinoside, peonidin 3-glucoside, petunidin 3-(6-acetoyl) galactoside, petunidin 3-(6-oxaloyl) arabinoside, peonidin 3-(6-acetoyl) glucoside, peonidin 3-(6-oxaloyl) arabinoside | [79] |
Eugenia jambolana (Java Plum) fruit extract | Cell lines HCT-116 colon cancer stem cells | Inhibited proliferation; induced apoptosis | delphinidin-3,5-diglucoside, cyanidin-3,5-diglucoside, ptunidin-3,5-diglucosid, dtunidin-3,5-diglucosid, peonidin-3,5-diglucoside, monidin-3,5-diglucosid, cyanidin-3-glucoside, petunidin-3-glucoside, etunidin-3-glucosi | [80] |
Anthocyanin-containing baked purple-fleshed potato extract | Colon cancer stem cells | Suppressed proliferation; elevated apoptosis; decreased β-catenin, c-Myc and Cyclin D1 | pet-3-rut-5-glc, mal-3-rut-5-glc, cya-3-O(6-O-malonyl- β-d-glc), peo-3-(p-coum)-isophoro-5-glc, peo-3-rut-5-glc, pet-3-(p-coum)-rut-5-glc, peo-3-caffeyl-rut-5-glc, pel-3-(p-coum)-rut-5-glc, pel-3-(4-ferul-rut)-5-glc, peo-3-(p-coum)-rut-5-glc, mal-3-(p-coum)-rut-5-glc | [81] |
Blue maize extract | Cell line Caco2 and HT29 | Suppressed proliferation | cyanidin 3-glucoside, cyanidin 3-glucoside, cyanidin malonyl-glucoside, cyanidin succinyl-glucoside, pelargonidin 3-glucoside, pelargonidin malonyl-glucoside | [82] |
Eggplant extract | Cell lines HT-29 | Decreased DNA damage | delphinidin-3-rhamnosyl-glucoside-5-glucoside, delphinidin-3-rutinoside-5-glucoside | [83] |
anthocyanin-enriched purple-fleshed sweet potato | Cell line SW480 | Decreased cell number, G1 phase arrest | peonidin-3-glucoside | [84] |
Vitis coignetiae Pullia extract | Inhibited cell invasion; suppressed MMP-2, MMP-9, NFkB | delphinidin-3,5-diglucoside, cyanidin-3,5-diglucoside, petunidin-3,5-diglucoside, delphinidin-3-glucoside, malvdin-3,5-diglucoside, peonidin-3,5-diglucoside, cyanidin-3-glucoside, petunidin-3-glucoside, peonidin-3-glucoside, malvidin-3-glucoside | [85] | |
Blackberry extract | Cell lines HT-29 | Inhibited cell growth; inhibited IL-12 release | cyanidin-3-glucoside, cyanidin-3-arabinoside, delphinidin-3-xyloside, cyanidin-3-xyloside, cyanidin-3-malonylglucoside, cyanidin-3-dioxalylglucoside | [86] |
Tart cherry anthocyanin | Cell line HT 29, HCT16 | Inhibited cell growth | 3-cyanidin 2″-O-β-d-glucopyranosyl-6″-O-α-l-rhamnopyransyl-β-d-glucopyranoside | [87] |
Animal Models | ||||
1. PCA | ||||
PCA | AOM-treated rat | Decreased the number of aberrant crypt foci, ornithine decarboxylase activity and AgNOR | PCA | [88,89] |
PCA | DSS-treated rat | Prevented diarrhea and bleeding; decreased pro-inflammatory cytokines; nitric oxide concentration, oxidative damage, and expression of COX-2 and iNOS | PCA | [90] |
2. Other fruit and vegetables | ||||
Anthocyanin-rich extracts from bilberry, chokeberry, and grape | AOM-treated rat | Reduced total ACF and the number of large ACF Suppressed cell proliferation reduces COX-2 | [91] | |
Anthocyanin derived from purple sweet potato color in their basal diet | AOM/DSS rats | Decreased MDF, colon weight, low-grade dysplasia and total histopathology changes; decreased the expression of β-catenin, Ki67and Cyclin D1 | [92] | |
anthocyanin-enriched purple-fleshed sweet potato | Animal AOM mice | Suppressed formation of aberrant crypt foci; decreased PCNA; increased caspase-3 | peonidin-3-glucoside | [84] |
Tart cherry anthocyanin | ApcMin mice | Decreased the number and volume of adenomas | 3-cyanidin 6″-O-α-l-rhamnopyranosyl-β-d-glucopyranoside | [87] |
Tomato | DSS mice | Increased bacterial Parabacteroides and Lactobacilli | [93] |
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Chen, T.; Shi, N.; Afzali, A. Chemopreventive Effects of Strawberry and Black Raspberry on Colorectal Cancer in Inflammatory Bowel Disease. Nutrients 2019, 11, 1261. https://doi.org/10.3390/nu11061261
Chen T, Shi N, Afzali A. Chemopreventive Effects of Strawberry and Black Raspberry on Colorectal Cancer in Inflammatory Bowel Disease. Nutrients. 2019; 11(6):1261. https://doi.org/10.3390/nu11061261
Chicago/Turabian StyleChen, Tong, Ni Shi, and Anita Afzali. 2019. "Chemopreventive Effects of Strawberry and Black Raspberry on Colorectal Cancer in Inflammatory Bowel Disease" Nutrients 11, no. 6: 1261. https://doi.org/10.3390/nu11061261