6-shogaol, an active constituent of dietary ginger, Impairs cancer development and lung metastasis by inhibiting the secretion of CC-chemokine ligand 2 (CCL2) in tumor-associated dendritic cells

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 6, 2015, Pages 1730-1738

  Hsu, Ya Ling ^a   Hung, Jen Yu ^b,c   Tsai, Ying Ming ^a,c   Tsai, Eing Mei ^a   Huang, Ming Shyan ^b,c   Hou, Ming Feng ^a   Kuo, Po Lin ^a,d,e  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^e NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

Author keywords

6 shogaol; breast cancer; CCL2; lung cancer; metastasis

Indexed keywords

BIOLOGICAL ORGANS; CELLS; CYTOLOGY; LIGANDS; PATHOLOGY; STEM CELLS; TUMORS;

6-SHOGAOL; BREAST CANCER; CCL2; LUNG CANCER; METASTASIS;

DISEASES;

MUS; ZINGIBER OFFICINALE;

ANTINEOPLASTIC AGENT; CATECHOL DERIVATIVE; MONOCYTE CHEMOTACTIC PROTEIN 1; SHOGAOL;

ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST TUMOR; CELL MOTION; CHEMISTRY; DENDRITIC CELL; DIET; DRUG EFFECTS; DRUG SCREENING; FEMALE; GINGER; HUMAN; IMMUNOTHERAPY; LUNG TUMOR; MALE; MOUSE; NEOPLASM METASTASIS; PATHOLOGY; SECONDARY; SECRETION (PROCESS); TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; ANTICARCINOGENIC AGENTS; BREAST NEOPLASMS; CATECHOLS; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINE CCL2; DENDRITIC CELLS; DIET; FEMALE; GINGER; HUMANS; IMMUNOTHERAPY; LUNG NEOPLASMS; MALE; MICE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84923233589     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf504934m     Document Type: Article

References (35)

1. Swann, J. B.; Smyth, M. J. Immune surveillance of tumors J. Clin. Invest. 2007, 117, 1137-1146
2. Pinzon-Charry, A.; Maxwell, T.; López, J. A. Dendritic cell dysfunction in cancer: a mechanism for immunosuppression Immunol. Cell Biol. 2005, 83, 451-461
3. Pyfferoen, L.; Mestdagh, P.; Vergote, K.; De Cabooter, N.; Vandesompele, J.; Lambrecht, B. N.; Vermaelen, K. Y. Lung tumours reprogram pulmonary dendritic cell immunogenicity at the microRNA level Int. J. Cancer 2014, 10.1002/ijc.28945
4. Obermajer, N.; Muthuswamy, R.; Lesnock, J.; Edwards, R. P.; Kalinski, P. Positive feedback between PGE2 and COX2 redirects the differentiation of human dendritic cells toward stable myeloid-derived suppressor cells Blood 2011, 118, 5498-5505
5. Zhou, Z.; Li, W.; Song, Y.; Wang, L.; Zhang, K.; Yang, J.; Zhang, W.; Su, H.; Zhang, Y. Growth differentiation factor-15 suppresses maturation and function of dendritic cells and inhibits tumor-specific immune response PLoS One 2013, 8 e78618
6. Kuo, P. L.; Huang, M. S.; Hung, J. Y.; Chou, S. H.; Chiang, S. Y.; Huang, Y. F.; Yang, C. J.; Tsai, M. J.; Chang, W. A.; Hsu, Y. L. Synergistic effect of lung tumor-associated dendritic cell-derived HB-EGF and CXCL5 on cancer progression Int. J. Cancer 2014, 135, 96-108
7. Kuo, C. H.; Chen, K. F.; Chou, S. H.; Huang, Y. F.; Wu, C. Y.; Cheng, D. E.; Chen, Y. W.; Yang, C. J.; Hung, J. Y.; Huang, M. S. Lung tumor-associated dendritic cell-derived resistin promoted cancer progression by increasing Wolf-Hirschhorn syndrome candidate 1/Twist pathway Carcinogenesis 2013, 34, 2600-2609
8. Hansen, M. T.; Forst, B.; Cremers, N.; Quagliata, L.; Ambartsumian, N.; Grum-Schwensen, B.; Klingelhöfer, J.; Abdul-Al, A.; Herrmann, P.; Osterland, M.; Stein, U.; Nielsen, G. H.; Scherer, P. E.; Lukanidin, E.; Sleeman, J. P.; Grigorian, M. A link between inflammation and metastasis: serum amyloid A1 and A3 induce metastasis, and are targets of metastasis-inducing S100A4 Oncogene 2014, 10.1038/onc.2013.568
9. Slattery, M. L.; John, E. M.; Torres-Mejia, G.; Lundgreen, A.; Herrick, J. S.; Baumgartner, K. B.; Hines, L. M.; Stern, M. C.; Wolff, R. K. Genetic variation in genes involved in hormones,inflammation and energetic factors and breast cancer risk in an admixed population Carcinogenesis 2012, 33, 1512-1521
10. Kurihara, T.; Bravo, R. Cloning and functional expression of mCCR2, a murine receptor for the C-C chemokines JE and FIC J. Biol. Chem. 1996, 271, 11603-11607
11. Chen, K.; Liu, M.; Liu, Y.; Wang, C.; Yoshimura, T.; Gong, W.; Le, Y.; Tessarollo, L.; Wang, J. M. Signal relay by CC chemokine receptor 2 (CCR2) and formylpeptide receptor 2 (Fpr2) in the recruitment of monocyte-derived dendritic cells in allergic airway inflammation J. Biol. Chem. 2013, 288, 16262-16273
12. Ueno, T.; Toi, M.; Saji, H.; Muta, M.; Bando, H.; Kuroi, K.; Koike, M.; Inadera, H.; Matsushima, K. Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer Clin. Cancer Res. 2000, 6, 3282-3289
13. Rahuman, A. A.; Gopalakrishnan, G.; Venkatesan, P.; Geetha, K.; Bagavan, A. Mosquito larvicidal activity of isolated compounds from the rhizome of Zingiber officinale Phytother. Res. 2008, 22, 1035-1039
14. Weng, C. J.; Chou, C. P.; Ho, C. T.; Yen, G. C. Molecular mechanism inhibiting human hepatocarcinoma cell invasion by 6-shogaol and 6-gingerol Mol. Nutr. Food Res. 2012, 56, 1304-1314
15. Weng, C. J.; Wu, C. F.; Huang, H. W.; Ho, C. T.; Yen, G. C. Anti-invasion effects of 6-shogaol and 6-gingerol, two active components in ginger, on human hepatocarcinoma cells Mol. Nutr. Food Res. 2010, 54, 1618-1627
16. Shieh, P. C.; Chen, Y. O.; Kuo, D. H.; Chen, F. A.; Tsai, M. L.; Chang, I. S.; Wu, H.; Sang, S.; Ho, C. T.; Pan, M. H. Induction of apoptosis by [8]-shogaol via reactive oxygen species generation, glutathione depletion, and caspase activation in human leukemia cells J. Agric. Food Chem. 2010, 58, 3847-3854
17. Sang, S.; Hong, J.; Wu, H.; Liu, J.; Yang, C. S.; Pan, M. H.; Badmaev, V.; Ho, C. T. Increased growth inhibitory effects on human cancer cells and anti-inflammatory potency of shogaols from Zingiber officinale relative to gingerols J. Agric. Food Chem. 2009, 57, 10645-10650
18. Pan, M. H.; Hsieh, M. C.; Hsu, P. C.; Ho, S. Y.; Lai, C. S.; Wu, H.; Sang, S.; Ho, C. T. 6-Shogaol suppressed lipopolysaccharide-induced up-expression of iNOS and COX-2 in murine macrophages Mol. Nutr. Food Res. 2008, 52, 1467-1477
19. Pan, M. H.; Hsieh, M. C.; Kuo, J. M.; Lai, C. S.; Wu, H.; Sang, S.; Ho, C. T. 6-Shogaol induces apoptosis in human colorectal carcinoma cells via ROS production, caspase activation, and GADD 153 expression Mol. Nutr. Food Res. 2008, 52, 527-537
20. Tsuyada, A.; Chow, A.; Wu, J.; Somlo, G.; Chu, P.; Loera, S.; Luu, T.; Li, A. X.; Wu, X.; Ye, W.; Chen, S.; Zhou, W.; Yu, Y.; Wang, Y. Z.; Ren, X.; Li, H.; Scherle, P.; Kuroki, Y.; Wang, S. E. CCL2 mediates cross-talk between cancer cells and stromal fibroblasts that regulates breast cancer stem cells Cancer Res. 2012, 72, 2768-2779
21. Xiang, T.; Long, H.; He, L.; Han, X.; Lin, K.; Liang, Z.; Zhuo, W.; Xie, R.; Zhu, B. Interleukin-17 produced by tumor microenvironment promotes self-renewal of CD133(+) cancer stem-like cells in ovarian cancer Oncogene 2013, 10.1038/onc.2013.537
22. Louie, E.; Chen, X. F.; Coomes, A.; Ji, K.; Tsirka, S.; Chen, E. I. Neurotrophin-3 modulates breast cancer cells and the microenvironment to promote the growth of breast cancer brain metastasis Oncogene 2013, 32, 4064-4077
23. Watkins, S. K.; Zhu, Z.; Riboldi, E.; Shafer-Weaver, K. A.; Stagliano, K. E.; Sklavos, M. M.; Ambs, S.; Yagita, H.; Hurwitz, A. A. FOXO3 programs tumor-associated DCs to become tolerogenic in human and murine prostate cancer J. Clin. Invest. 2011, 121, 1361-1372
24. Gottfried, E.; Kunz-Schughart, L. A.; Ebner, S.; Mueller-Klieser, W.; Hoves, S.; Andreesen, R.; Mackensen, A.; Kreutz, M. Tumor-derived lactic acid modulates dendritic cell activation and antigen expression Blood 2006, 107, 2013-2021
25. Wu, J.; Liu, X.; Wang, Y. Predictive value of preoperative serum CCL2, CCL18, and VEGF for the patients with gastric cancer BMC Clin. Pathol. 2013, 13, 15
26. Steiner, J. L.; Murphy, E. A. Importance of chemokine (CC-motif) ligand 2 in breast cancer Int. J. Biol. Markers 2012, 27, e179-e185
27. Zhang, X. W.; Qin, X.; Qin, C. Y.; Yin, Y. L.; Chen, Y.; Zhu, H. L. Expression of monocyte chemoattractant protein-1 and CC chemokine receptor 2 in non-small cell lung cancer and its significance Cancer Immunol. Immunother. 2013, 62, 563-570
28. Li, X.; Xu, Q.; Wu, Y.; Li, J.; Tang, D.; Han, L.; Fan, Q. A CCL2/ROS autoregulation loop is critical for cancer-associated fibroblasts-enhanced tumor growth of oral squamous cell carcinoma Carcinogenesis 2014, 35, 1362-1370
29. Lin, T. H.; Liu, H. H.; Tsai, T. H.; Chen, C. C.; Hsieh, T. F.; Lee, S. S.; Lee, Y. J.; Chen, W. C.; Tang, C. H. CCL2 increases αvβ3 integrin expression and subsequently promotes prostate cancer migration Biochim. Biophys. Acta 2013, 1830, 4917-4927
30. Arendt, L. M.; McCready, J.; Keller, P. J.; Baker, D. D.; Naber, S. P.; Seewaldt, V.; Kuperwasser, C. Obesity promotes breast cancer by CCL2-mediated macrophage recruitment and angiogenesis Cancer Res. 2013, 73, 6080-6093
31. van Deventer, H. W.; Palmieri, D. A.; Wu, Q. P.; McCook, E. C.; Serody, J. S. Circulating fibrocytes prepare the lung for cancer metastasis by recruiting Ly-6C+ monocytes via CCL2 J. Immunol. 2013, 190, 4861-4867
32. Kudo-Saito, C.; Shirako, H.; Ohike, M.; Tsukamoto, N.; Kawakami, Y. CCL2 is critical for immunosuppression to promote cancer metastasis Clin. Exp. Metastasis 2013, 30, 393-405
33. Fukuda, A.; Wang, S. C.; Morris, J. P., 4th; Folias, A. E.; Liou, A.; Kim, G. E.; Akira, S.; Boucher, K. M.; Firpo, M. A.; Mulvihill, S. J.; Hebrok, M. Stat3 and MMP7 contribute to pancreatic ductal adenocarcinoma initiation and progression Cancer Cell 2011, 19, 441-455
34. Vasquez-Dunddel, D.; Pan, F.; Zeng, Q.; Gorbounov, M.; Albesiano, E.; Fu, J.; Blosser, R. L.; Tam, A. J.; Bruno, T.; Zhang, H.; Pardoll, D.; Kim, Y. STAT3 regulates arginase-I inmyeloid-derived suppressor cells from cancer patients J. Clin. Invest. 2013, 123, 1580-1589
35. Sanseverino, I.; Purificato, C.; Varano, B.; Conti, L.; Gessani, S.; Gauzzi, M. C. STAT3-silenced human dendritic cells have an enhanced ability to prime IFNγ production by both αβ and γδ T lymphocytes Immunobiology 2014, 219, 503-511