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Research Article

Dietary Tomato Powder Inhibits High-Fat Diet–Promoted Hepatocellular Carcinoma with Alteration of Gut Microbiota in Mice Lacking Carotenoid Cleavage Enzymes

Hui Xia, Chun Liu, Cheng-Chung Li, Maobin Fu, Shingo Takahashi, Kang-Quan Hu, Koichi Aizawa, Suganuma Hiroyuki, Guojun Wu, Liping Zhao and Xiang-Dong Wang
Hui Xia
1Nutrition and Cancer Biology Laboratory, Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University, Boston, Massachusetts.
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Chun Liu
1Nutrition and Cancer Biology Laboratory, Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University, Boston, Massachusetts.
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Cheng-Chung Li
1Nutrition and Cancer Biology Laboratory, Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University, Boston, Massachusetts.
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Maobin Fu
2Nature and Wellness Research Department, Research and Development Division, Kagome Co., Ltd., Tochigi, Japan.
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Shingo Takahashi
2Nature and Wellness Research Department, Research and Development Division, Kagome Co., Ltd., Tochigi, Japan.
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Kang-Quan Hu
1Nutrition and Cancer Biology Laboratory, Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University, Boston, Massachusetts.
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Koichi Aizawa
1Nutrition and Cancer Biology Laboratory, Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University, Boston, Massachusetts.
2Nature and Wellness Research Department, Research and Development Division, Kagome Co., Ltd., Tochigi, Japan.
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Suganuma Hiroyuki
2Nature and Wellness Research Department, Research and Development Division, Kagome Co., Ltd., Tochigi, Japan.
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  • ORCID record for Suganuma Hiroyuki
Guojun Wu
3Department of Biochemistry and Microbiology, School of Environmental and Biological Sciences, Rutgers University, New Brunswick, New Jersey.
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Liping Zhao
3Department of Biochemistry and Microbiology, School of Environmental and Biological Sciences, Rutgers University, New Brunswick, New Jersey.
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Xiang-Dong Wang
1Nutrition and Cancer Biology Laboratory, Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University, Boston, Massachusetts.
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  • For correspondence: xiang-dong.wang@tufts.edu
DOI: 10.1158/1940-6207.CAPR-18-0188 Published December 2018
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    Figure 1.

    Liver tumor quantification and histopathologic examination of liver tumor in BCO1−/−BCO2−/− double KO mice fed with DEN+HFD or DEN+HFD+TP. A, The total liver organ was exhibited between DEN+HFD and DEN+HFD+TP groups. B and C, The histopathologic images of livers with H&E staining under 100x and 400x magnification of microscope, respectively.

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    Figure 2.

    Effects of TP feeding on hepatic mRNA and protein expression of SIRT1, SIRT1 activity, NAMPT, and hepatic mRNA expression of circadian clock–related genes in DEN+HFD-fed BCO1−/−BCO2−/− double KO mice. Beta-actin was used as control unless specified otherwise. Graphical representation of fold change in (A) SIRT1 protein, (B) Ac-FOXO1 protein, (C) Sirt1 mRNA, (D) NAMPT protein, (E) NAMPT mRNA, and (F) Clock, Cry2, Per2, Wee1 mRNAs. Values are expressed as mean ± SEM. Differences between groups were analyzed by the Student t test. *Significantly different from the DEN+HFD, P < 0.05. Clock, circadian locomotor output cycles kaput; Cry2, cryptochrome-2; Per2, period 2.

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    Figure 3.

    Effects of TP feeding on steatosis severity and hepatic mRNA and protein expression of AMPK and its downstream gene mRNA expression in DEN+HFD-fed BCO1−/−BCO2−/− double KO mice. The histopathology images of (A) hepatic steatosis and (B) hepatic steatosis score are presented. Graphical representation of fold change in (C) P-AMPK protein and (D) PGC-1, PPARα, CPT1, ACOX1, CD36, and DGAT1 genes. Values are expressed as mean ± SEM. Differences between groups were analyzed by Student t test. *Significantly different from the DEN+HFD, P < 0.05. PPARα, peroxisome proliferator-activated receptor α.

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    Figure 4.

    Effects of TP feeding on inflammation foci and hepatic mRNA and protein expression of Ac-NF-κB and its downstream genes in DEN+HFD-fed BCO1−/−BCO2−/− double KO mice. A, The histopathologic images of inflammation foci between DEN+HFD and DEN+HFD+TP groups. B, The difference in inflammation foci numbers between DEN+HFD and DEN+HFD+TP groups. Graphical representation of fold change in (C) Ac-NF-κB protein and (D) MCP1, iNOS, TNFα, IL1β, IL6, and IL12 α genes. Values are expressed as mean ± SEM. Differences between groups were analyzed by Student t test. *Significantly different from the DEN+HFD, P < 0.05.

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    Figure 5.

    Effects of TP feeding on microbiota richness and distribution at phylum, genus, and species levels in DEN+HFD-fed BCO1−/−BCO2−/− double KO mice. A, Observed OTUs, Chao1, and ACE, representing community richness. B, Shannon index, representing community evenness. C, Relative abundance of gram-positive bacteria or gram-negative bacteria. D, Relative abundance of major bacteria at phylum level. E and F, Relative abundance of major bacteria at genus, species levels. *Significantly different from the DEN+HFD, P < 0.05.

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    Figure 6.

    Effects of TP feeding on Mucispirillum and Clostridium abundance in DEN+HFD-fed BCO1−/−BCO2−/− double KO mice. A, Deferribacteres abundance at phylum level between DEN+HFD and DEN+HFD+TP groups. B and C, Relative abundance of genus Mucispirillum and species Mucispirillum schaedleri as part of phylum Deferribacteres. D, Relative abundance of Clostridium at genus level. E, and F, Relative abundance of Clostridium sp.ID4 and Clostridium sp.Clone.9 at species level. *Significantly different from the DEN+HFD, P < 0.05.

Tables

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  • Table 1.

    Body weight, liver weight, visceral fat weight, hepatic lycopene concentration, and tumor outcomes

    DEN+HFDDEN+HFD+TP
    Number of micen = 8n = 9
    Final body weight, g55.6 ± 4.148.9 ± 4.2
    Liver weight, g2.6 ± 0.32.3 ± 0.4
    Visceral fat weight, g2.3 ± 0.22.2 ± 0.2
    Hepatic lycopene (nmol/g liver)ND5.0 ± 0.7
    Liver tumor incidence, %10033.3a
    Multiplicity, #9.8 ± 1.81.7 ± 0.8a
    Volume, mm31007.5 ± 449.625.4 ± 20.6a
    • NOTE: Student t test was used to examine the difference between DEN+HFD and DEN+HFD+TP.

    • Abbreviation: ND, not detected.

    • ↵aP < 0.05 for comparison between DEN+HFD and DEN+HFD+TP.

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Cancer Prevention Research: 11 (12)
December 2018
Volume 11, Issue 12
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Dietary Tomato Powder Inhibits High-Fat Diet–Promoted Hepatocellular Carcinoma with Alteration of Gut Microbiota in Mice Lacking Carotenoid Cleavage Enzymes
Hui Xia, Chun Liu, Cheng-Chung Li, Maobin Fu, Shingo Takahashi, Kang-Quan Hu, Koichi Aizawa, Suganuma Hiroyuki, Guojun Wu, Liping Zhao and Xiang-Dong Wang
Cancer Prev Res December 1 2018 (11) (12) 797-810; DOI: 10.1158/1940-6207.CAPR-18-0188

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Dietary Tomato Powder Inhibits High-Fat Diet–Promoted Hepatocellular Carcinoma with Alteration of Gut Microbiota in Mice Lacking Carotenoid Cleavage Enzymes
Hui Xia, Chun Liu, Cheng-Chung Li, Maobin Fu, Shingo Takahashi, Kang-Quan Hu, Koichi Aizawa, Suganuma Hiroyuki, Guojun Wu, Liping Zhao and Xiang-Dong Wang
Cancer Prev Res December 1 2018 (11) (12) 797-810; DOI: 10.1158/1940-6207.CAPR-18-0188
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