The role of cancer stem cells in the anti-carcinogenicity of curcumin

Molecular Nutrition and Food Research

Volumn 57, Issue 9, 2013, Pages 1630-1637

  Norris, Leonie ^a   Karmokar, Ankur ^a   Howells, Lynne ^a   Steward, William P ^a   Gescher, Andreas ^a   Brown, Karen ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Cancer chemoprevention; Cancer stem cell; Carcinogenesis; Curcumin; Dietary agent

Indexed keywords

ANTINEOPLASTIC AGENT; CURCUMIN; INTERLEUKIN 8; NOTCH RECEPTOR; SONIC HEDGEHOG PROTEIN; STAT PROTEIN; WNT PROTEIN;

ANIMAL; CANCER CHEMOPREVENTION; CANCER STEM CELL; CARCINOGENESIS; DIETARY AGENT; DISEASE MODEL; DRUG EFFECT; GENETICS; HUMAN; METABOLISM; REVIEW; SIGNAL TRANSDUCTION;

CANCER CHEMOPREVENTION; CANCER STEM CELL; CARCINOGENESIS; CURCUMIN; DIETARY AGENT;

ANIMALS; ANTICARCINOGENIC AGENTS; CURCUMIN; DISEASE MODELS, ANIMAL; HEDGEHOG PROTEINS; HUMANS; INTERLEUKIN-8; NEOPLASTIC STEM CELLS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS; WNT PROTEINS;

EID: 84883318030     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201300120     Document Type: Review

References (62)

1. Bruce, W. R., Van Der Gaag, H., A quantitative assay for the number of murine lymphoma cells capable of proliferation in vivo. Nature 1963, 199, 79-80.
2. Kleinsmith, L. J., Pierce, G. B., Jr., Multipotentiality of single embryonal carcinoma cells. Cancer Res. 1964, 24, 1544-1551.
3. Makino, S., Further evidence favoring the concept of the stem cell in ascites tumors of rats. Ann. N. Y. Acad. Sci. 1956, 63, 818-830.
4. Park, C. H., Bergsagel, D. E., McCulloch, E. A., Mouse myeloma tumor stem cells: a primary cell culture assay. J. Natl. Cancer Inst. 1971, 46, 411-422.
5. Tan, B. T., Park, C. Y., Ailles, L. E., Weissman, I. L., The cancer stem cell hypothesis: a work in progress. Lab. Invest.:J. Tech. Methods Pathol. 2006, 86, 1203-1207.
6. Polyak, K., Hahn, W. C., Roots and stems: stem cells in cancer. Nature Med. 2006, 12, 296-300.
7. Passegue, E., Jamieson, C. H., Ailles, L. E., Weissman, I. L., Normal and leukemic hematopoiesis: are leukemias a stem cell disorder or a reacquisition of stem cell characteristics? Proc. Natl. Acad. Sci. U. S. A. 2003, 100(Suppl 1), 11842-11849.
8. Irving, G. R., Howells, L. M., Sale, S., Kralj-Hans, I. et al., Prolonged biologically active colonic tissue levels of curcumin achieved after oral administration: a clinical pilot study including assessment of patient acceptability. Cancer Prev. Res. 2012, 6, 119-128.
9. Reya, T., Morrison, S. J., Clarke, M. F., Weissman, I. L., Stem cells, cancer, and cancer stem cells. Nature 2001, 414, 105-111.
10. Zhao, C., Blum, J., Chen, A., Kwon, H. Y. et al., Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell 2007, 12, 528-541.
11. Korkaya, H., Paulson, A., Charafe-Jauffret, E., Ginestier, C. et al., Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling. PLoS Biol. 2009, 7, e1000121.
12. Jaiswal, A. S., Marlow, B. P., Gupta, N., Narayan, S., Beta-catenin-mediated transactivation and cell-cell adhesion pathways are important in curcumin (diferuylmethane)-induced growth arrest and apoptosis in colon cancer cells. Oncogene 2002, 21, 8414-8427.
13. Ryu, M. J., Cho, M., Song, J. Y., Yun, Y. S. et al., Natural derivatives of curcumin attenuate the Wnt/beta-catenin pathway through down-regulation of the transcriptional coactivator p300. Biochem. Biophys. Res. Commun. 2008, 377, 1304-1308.
14. Hidalgo, M., Maitra, A., The hedgehog pathway and pancreatic cancer. New Engl. J. Med. 2009, 361, 2094-2096.
15. Takezaki, T., Hide, T., Takanaga, H., Nakamura, H. et al., Essential role of the Hedgehog signaling pathway in human glioma-initiating cells. Cancer Sci. 2011, 102, 1306-1312.
16. Zhao, C., Chen, A., Jamieson, C. H., Fereshteh, M. et al., Hedgehog signalling is essential for maintenance of cancer stem cells in myeloid leukaemia. Nature 2009, 458, 776-779.
17. Li, C., Heidt, D. G., Dalerba, P., Burant, C. F. et al., Identification of pancreatic cancer stem cells. Cancer Res. 2007, 67, 1030-1037.
18. Pasca di Magliano, M., Hebrok, M., Hedgehog signalling in cancer formation and maintenance. Nature Rev. Cancer 2003, 3, 903-911.
19. Slusarz, A., Shenouda, N. S., Sakla, M. S., Drenkhahn, S. K. et al., Common botanical compounds inhibit the hedgehog signaling pathway in prostate cancer. Cancer Res. 2010, 70, 3382-3390.
20. Lim, K. J., Bisht, S., Bar, E. E., Maitra, A. et al., A polymeric nanoparticle formulation of curcumin inhibits growth, clonogenicity and stem-like fraction in malignant brain tumors. Cancer Biol. Ther. 2011, 11, 464-473.
21. Bisht, S., Mizuma, M., Feldmann, G., Ottenhof, N. A. et al., Systemic administration of polymeric nanoparticle-encapsulated curcumin (NanoCurc) blocks tumor growth and metastases in preclinical models of pancreatic cancer. Mol. Cancer Therapeut. 2010, 9, 2255-2264.
22. Wang, Z., Li, Y., Banerjee, S., Sarkar, F. H., Emerging role of Notch in stem cells and cancer. Cancer Lett. 2009, 279, 8-12.
23. Dontu, G., Jackson, K. W., McNicholas, E., Kawamura, M. J. et al., Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res. 2004, 6, R605-R615.
24. Subramaniam, D., Ponnurangam, S., Ramamoorthy, P., Standing, D. et al., Curcumin induces cell death in esophageal cancer cells through modulating Notch signaling. PloS One 2012, 7, e30590.
25. Wang, Z., Zhang, Y., Banerjee, S., Li, Y. et al., Notch-1 down-regulation by curcumin is associated with the inhibition of cell growth and the induction of apoptosis in pancreatic cancer cells. Cancer 2006, 106, 2503-2513.
26. Calo, V., Migliavacca, M., Bazan, V., Macaluso, M. et al., STAT proteins: from normal control of cellular events to tumorigenesis. J. Cell. Physiol. 2003, 197, 157-168.
27. Frank, D. A., STAT3 as a central mediator of neoplastic cellular transformation. Cancer Lett. 2007, 251, 199-210.
28. Germain, D., Frank, D. A., Targeting the cytoplasmic and nuclear functions of signal transducers and activators of transcription 3 for cancer therapy. Clin. Cancer Res. 2007, 13, 5665-5669.
29. Turkson, J., Jove, R., STAT proteins: novel molecular targets for cancer drug discovery. Oncogene 2000, 19, 6613-6626.
30. Lin, L., Fuchs, J., Li, C., Olson, V. et al., STAT3 signaling pathway is necessary for cell survival and tumorsphere forming capacity in ALDH(+)/CD133(+) stem cell-like human colon cancer cells. Biochem. Biophys. Res. Commun. 2011, 416, 246-251.
31. Shishodia, S., Chaturvedi, M. M., Aggarwal, B. B., Role of curcumin in cancer therapy. Curr. Probl. Cancer 2007, 31, 243-305.
32. Corvinus, F. M., Orth, C., Moriggl, R., Tsareva, S. A. et al., Persistent STAT3 activation in colon cancer is associated with enhanced cell proliferation and tumor growth. Neoplasia 2005, 7, 545-555.
33. Marotta, L. L., Almendro, V., Marusyk, A., Shipitsin, M. et al., The JAK2/STAT3 signaling pathway is required for growth of CD44(+)CD24(-) stem cell-like breast cancer cells in human tumors. J. Clin. Invest. 2011, 121, 2723-2735.
34. Bharti, A. C., Donato, N., Aggarwal, B. B., Curcumin (diferuloylmethane) inhibits constitutive and IL-6-inducible STAT3 phosphorylation in human multiple myeloma cells. J. Immunol. 2003, 171, 3863-3871.
35. Chen, W. H., Chen, Y., Cui, G. H., Gu, J. X. et al., Effect of curcumin on STAT5 signaling pathway in primary CML cells. Zhongguo Shi Yan Xue Ye Xue Za Zhi 2004, 12, 572-576.
36. Chen, W. H., Chen, Y., Gu, J. X., He, J., Effect of curcumin on STAT5 signaling molecule in K562 cells. Zhonghua Xue Ye Xue Za Zhi 2004, 25, 151-153.
37. Lin, L., Liu, Y., Li, H., Li, P. K. et al., Targeting colon cancer stem cells using a new curcumin analogue, GO-Y030. Br. J. Cancer 2011, 105, 212-220.
38. Hidaka, H., Ishiko, T., Furuhashi, T., Kamohara, H. et al., Curcumin inhibits interleukin 8 production and enhances interleukin 8 receptor expression on the cell surface: impact on human pancreatic carcinoma cell growth by autocrine regulation. Cancer 2002, 95, 1206-1214.
39. Belperio, J. A., Keane, M. P., Arenberg, D. A., Addison, C. L. et al., CXC chemokines in angiogenesis. J. Leukoc. Biol. 2000, 68, 1-8.
40. Singh, J. K., Farnie, G., Bundred, N. J., Simoes, B. M. et al., Targeting CXCR1/2 significantly reduces breast cancer stem cell activity and increases the efficacy of inhibiting HER2 via HER2-dependent and -independent mechanisms. Clin. Cancer Res. 2012, 19, 643-656.
41. Ginestier, C., Liu, S., Diebel, M. E., Korkaya, H. et al., CXCR1 blockade selectively targets human breast cancer stem cells in vitro and in xenografts. J. Clin. Invest. 2010, 120, 485-497.
42. Kakarala, M., Brenner, D. E., Korkaya, H., Cheng, C. et al., Targeting breast stem cells with the cancer preventive compounds curcumin and piperine. Breast Cancer Res. Treat. 2010, 122, 777-785.
43. Nautiyal, J., Kanwar, S. S., Yu, Y., Majumdar, A. P., Combination of dasatinib and curcumin eliminates chemo-resistant colon cancer cells. J. Mol. Signal. 2011, 6, 7.
44. Yu, Y., Kanwar, S. S., Patel, B. B., Nautiyal, J. et al., Elimination of colon cancer stem-like cells by the combination of curcumin and FOLFOX. Translat. Oncol. 2009, 2, 321-328.
45. Fong, D., Yeh, A., Naftalovich, R., Choi, T. H., Chan, M. M., Curcumin inhibits the side population (SP) phenotype of the rat C6 glioma cell line: towards targeting of cancer stem cells with phytochemicals. Cancer Lett. 2010, 293, 65-72.
46. Pastrana, E., Silva-Vargas, V., Doetsch, F., Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell 2011, 8, 486-498.
47. Klonisch, T., Wiechec, E., Hombach-Klonisch, S., Ande, S. R. et al., Cancer stem cell markers in common cancers: therapeutic implications. Trends Mol. Med. 2008, 14, 450-460.
48. Li, L., Ahmed, B., Mehta, K., Kurzrock, R., Liposomal curcumin with and without oxaliplatin: effects on cell growth, apoptosis, and angiogenesis in colorectal cancer. Mol. Cancer Therapeut. 2007, 6, 1276-1282.
49. Howells, L. M., Mitra, A., Manson, M. M., Comparison of oxaliplatin- and curcumin-mediated antiproliferative effects in colorectal cell lines. Int. J. Cancer (Journal international du cancer) 2007, 121, 175-183.
50. Howells, L. M., Sale, S., Sriramareddy, S. N., Irving, G. R. et al., Curcumin ameliorates oxaliplatin-induced chemoresistance in HCT116 colorectal cancer cells in vitro and in vivo. Int. J. Cancer 2011, 129, 476-486.
51. Harbottle, A., Daly, A. K., Atherton, K., Campbell, F. C., Role of glutathione S-transferase P1, P-glycoprotein and multidrug resistance-associated protein 1 in acquired doxorubicin resistance. Int. J. Cancer (Journal international du cancer) 2001, 92, 777-783.
52. Patel, B. B., Sengupta, R., Qazi, S., Vachhani, H. et al., Curcumin enhances the effects of 5-fluorouracil and oxaliplatin in mediating growth inhibition of colon cancer cells by modulating EGFR and IGF-1R. Int. J. Cancer (Journal international du cancer) 2008, 122, 267-273.
53. Dean, M., Fojo, T., Bates, S., Tumour stem cells and drug resistance. Nature Rev. Cancer 2005, 5, 275-284.
54. Patel, B. B., Gupta, D., Elliott, A. A., Sengupta, V. et al., Curcumin targets FOLFOX-surviving colon cancer cells via inhibition of EGFRs and IGF-1R. Anticancer Res. 2010, 30, 319-325.
55. Cheng, A. L., Hsu, C. H., Lin, J. K., Hsu, M. M. et al., Phase I clinical trial of curcumin, a chemopreventive agent, in patients with high-risk or pre-malignant lesions. Anticancer Res. 2001, 21, 2895-2900.
56. Irving, G. R., Howells, L. M., Sale, S., Kralj-Hans, I. et al., Prolonged biologically active colonic tissue levels of curcumin achieved after oral administration: a clinical pilot study including assessment of patient acceptability. Cancer Prev. Res. 2013, 6, 119-128.
57. Ireson, C., Orr, S., Jones, D. J., Verschoyle, R. et al., Characterization of metabolites of the chemopreventive agent curcumin in human and rat hepatocytes and in the rat in vivo, and evaluation of their ability to inhibit phorbol ester-induced prostaglandin E2 production. Cancer Res. 2001, 61, 1058-1064.
58. Anand, P., Thomas, S. G., Kunnumakkara, A. B., Sundaram, C. et al., Biological activities of curcumin and its analogues (Congeners) made by man and Mother Nature. Biochemical Pharmacol. 2008, 76, 1590-1611.
59. Almanaa, T. N., Geusz, M. E., Jamasbi, R. J., Effects of curcumin on stem-like cells in human esophageal squamous carcinoma cell lines. BMC Complement. Alternat. Med. 2012, 12, 195-209.
60. Brabletz, T., Jung, A., Spaderna, S., Hlubek, F., Kirchner, T., Opinion: migrating cancer stem cells-an integrated concept of malignant tumour progression. Nature Rev. Cancer 2005, 5, 744-749.
61. Barker, N., van Es, J. H., Kuipers, J., Kujala, P. et al., Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449, 1003-1007.
62. Barker, N., Ridgway, R. A., van Es, J. H., van de Wetering, M. et al., Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009, 457, 608-611.