Curcumin: A promising agent targeting cancer stem cells

Anti-Cancer Agents in Medicinal Chemistry

Volumn 14, Issue 6, 2014, Pages 787-792

  Zang, Shufei ^a,b   Liu, Tao ^c   Shi, Junping ^b   Qiao, Liang ^d  

^a ZHEJIANG CHINESE MEDICAL UNIVERSITY   (China)

^b HANGZHOU FIRST PEOPLE'S HOSPITAL   (China)

^c LANZHOU UNIVERSITY   (China)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Cancer stem cells; Combination; Curcumin; microRNA; Therapy

Indexed keywords

ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; BETA CATENIN; BRCA1 PROTEIN; BRCA2 PROTEIN; CHOLESTERY HYALURONIC ACID CURCUMIN; CURCUMIN; CYCLOOXYGENASE 2; DASATINIB; DEMETHOXYCURCUMIN; DIDEMETHOXYCURCUMIN; DIFLUORINATED CURCUMIN; EPIDERMAL GROWTH FACTOR RECEPTOR; FLUOROURACIL; HERMES ANTIGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA 145; MICRORNA 21; MYC PROTEIN; OXALIPLATIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3, 4, 5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN BAX; PROTEIN BCL XL; PROTEIN KINASE B; SOMATOMEDIN C; STAT3 PROTEIN; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; UNINDEXED DRUG; WNT PROTEIN; ANTINEOPLASTIC AGENT;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BRAIN CANCER; BREAST CANCER; CANCER STEM CELL; CHEMICAL MODIFICATION; CHEMICAL STRUCTURE; COLORECTAL CANCER; DRUG EFFICACY; ESOPHAGUS CANCER; GENE MUTATION; GLIOMA CELL; HEAD AND NECK CANCER; HUMAN; LUNG CANCER; NEOPLASM; NONHUMAN; PANCREAS CANCER; PHARMACOLOGICAL PARAMETERS; PHASE 1 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; REVIEW; TARGET CELL; ANIMAL; CHEMISTRY; CURCUMA; DRUG EFFECTS; ISOLATION AND PURIFICATION; NEOPLASMS; PATHOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CURCUMA; CURCUMIN; HUMANS; MOLECULAR STRUCTURE; NEOPLASMS; NEOPLASTIC STEM CELLS;

EID: 84904117834     PISSN: 18715206     EISSN: 18755992     Source Type: Journal    
DOI: 10.2174/1871520614666140521114735     Document Type: Review

References (74)

1. Frank, N.Y.; Schatton, T.; Frank, M.H. The therapeutic promise of the cancer stem cell concept. J. Clin. Invest., 2010, 120, 41-50.
2. Gupta, P.B.; Chaffer, C.L.; Weinberg, R.A. Cancer stem cells: Mirage or reality? Nat. Med., 2009, 15, 1010-1012.
3. Jones, R.J.; Matsui, W.H.; Smith, B.D. Cancer stem cells: Are we missing the target? J. Natl. Cancer. Inst., 2004, 96, 583-585.
4. Ginestier, C.; Hur, M.H.; Charafe-Jauffret, E.; Monville, F.; Dutcher, J.; Brown, M.; Jacquemier, J.; Viens, P.; Kleer, C.G.; Liu, S.; Schott, A.; Hayes, D.; Birnbaum, D.; Wicha, M.S.; Dontu, G. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell. Stem. Cell., 2007, 1, 555-567.
5. Yang, Z.F.; Ho, D.W.; Ng, M.N.; Lau, C.K.; Yu, W.C.; Ngai, P.; Chu, P.W.; Lam C.T.; Poon, R.T.; Fan, S.T. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell, 2008, 13, 153-166.
6. O'Brien, C.A.; Pollett, A.; Gallinger, S.; Dick, J.E. A human colon cancer cell capable of initiating tumour growth in immune deficient mice. Nature, 2007, 445, 106-110.
7. Ricci-Vitiani, L.; Lombardi, D.G.; Pilozzi, E.; Biffoni, M.; Todaro, M.; Peschle, C.; De Maria, R. Identification and expansion of human colon-cancer-initiating cells. Nature, 2007, 445, 111-115.
8. Singh, S.K.; Clarke, I.D.; Terasaki, M.; Bonn, V.E.; Hawkins, C.; Squire, J.; Dirks, P.B. Identification of a cancer stem cell in human brain tumors. Cancer. Res., 2003, 63, 5821-5828.
9. Prince, M.E.; Sivanandan, R.; Kaczorowski, A.; Wolf, G.T.; Kaplan, M.J.; Dalerba, P.; Weissman, I.L.; Clarke, M.F.; Ailles, L.E. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc. Natl. Acad. Sci. USA, 2007, 104, 973-978.
10. Li, C.; Heidt, D.G.; Dalerba, P.; Burant, C.F.; Zhang, L.; Adsay, V.; Wicha, M.; Clarke, M.F.; Simeone, D.M. Identification of pancreatic cancer stem cells. Cancer Res., 2007, 67, 1030-1037.
11. Yamazaki, J.; Mizukami, T.; Takizawa, K.; Kuramitsu, M.; Momose, H.; Masumi, A.; Ami, Y.; Hasegawa, H.; Hall, W.W.; Tsujimoto, H.; Hamaguchi, I.; Yamaguchi, K. Identification of cancer stem cells in a Tax-transgenic (Tax-Tg) mouse model of adult T-cell leukemia/lymphoma. Blood, 2009, 114, 2709-2720.
12. Fong, M.Y.; Kakar, S.S. The role of cancer stem cells and the side population in epithelial ovarian cancer. Histol. Histopathol., 2010, 25, 113-120.
13. Sachlos, E.; Risueño, R.M.; Laronde, S.; Shapovalova, Z.; Lee, J.H.; Russell, J.; Malig, M.; McNicol, J.D.; Fiebig-Comyn, A.; Graham, M.; Levadoux-Martin, M.; Lee, J.B.; Giacomelli, A.O.; Hassell, J.A.; Fischer-Russell, D.; Trus, M.R.; Foley, R.; Leber, B.; Xenocostas, A.; Brown, E.D.; Collins, T.J.; Bhatia, M. Identification of drugs including a dopamine receptor antagonist that selectively target cancer stem cells. Cell, 2012, 149, 1284-1297.
14. Vermeulen, L.; Sousae Melo, F.; Richel, D.J.; Medema, J.P. The developing cancer stem-cell model: Clinical challenges and opportunities. Lancet Oncol., 2012, 13, 83-89.
15. Aggarwal, B.B.; Sundaram, C.; Malani, N.; Ichikawa, H. Curcumin: The Indian solid gold. Adv. Exp. Med. Biol., 2007, 595, 1-75.
16. Shao, Z.M.; Shen, Z.Z.; Liu, C.H.; Sartippour, M.R.; Go, V.L.; Heber, D.; Nguyen, M. Curcumin exerts multiple suppressive effects on human breast carcinoma cells. Int. J. Cancer., 2002, 98, 234-240.
17. Li, Y.; Wicha, M.S.; Schwartz, S.J.; Sun, D. Implications of cancer stem cell theory for cancer chemoprevention by natural dietary compounds. J. Nutr. Biochem., 2011, 22, 799-806.
18. Rao, E.V.; Sudheer, P. Revisiting curcumin chemistry part I: A new strategy for the synthesis of curcuminoids. Indian. J. Pharm. Sci., 2011, 73, 262-270.
19. Shishodia, S. Molecular mechanisms of curcumin action: Gene expression. Biofactors, 2013, 39, 37-55.
20. Shehzad, A.; Lee, Y.S. Molecular mechanisms of curcumin action: Signal transduction. Biofactors, 2013, 39, 27-36.
21. Jemal, A.; Bray, F.; Cen-ter, M.M.; Ferlay, J.; Ward, E.; Forman, D. Global cancer statistics. CA. Cancer J. Clin., 2011, 61, 69-90.
22. Neugut, A.I.; Lautenbach, E.; Abi-Rached, B.; Forde, K.A. Incidence of adenomas after curative resection for colorectal cancer. Am. J. Gastroenterol., 1996, 91, 2096-2098.
23. Jordan, C.T.; Guzman, M.L.; Noble, M. Cancer stem cells. N. Engl. J. Med., 2006, 355, 1253-1261.
24. Yu, Y.; Kanwar, S.S.; Patel, B.B.; Nautiyal, J.; Sarkar, F.H.; Majumdar, A.P. Elimination of colon cancer stem-like cells by the combination of curcumin and FOLFOX. Transl. Oncol., 2009, 2, 321-328.
25. 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, 20, 6-7.
26. Chen, J. Prevention of obesity-associated colon cancer by (-)- epigallocatechin-3 gallate and curcumin. Transl. Gastrointest. Cancer., 2012, 1, 243-249.
27. Patel, B.B.; Gupta, D.; Elliott, A.A.; Sengupta, V.; Yu, Y.; Majumdar A.P. Curcumin targets FOLFOX-surviving colon cancer cells via inhibition of EGFRs and IGF-1R. Anticancer. Res., 2010, 30, 319-325.
28. Anand, P.; Kunnumakkara, A.B.; Newman, R.A.; Aggarwal, B.B. Bioavailability of curcumin: Problems and promises. Mol. Pharm., 2007, 4, 807-818.
29. Padhye, S.; Yang, H.; Jamadar, A.; Cui, Q.C.; Chavan, D.; Dominiak K.; McKinney, J.; Banerjee, S.; Dou, Q.P.; Sarkar, F.H. New difluoro Knoevenagel condensates of curcumin, their Schiff bases and copper complexes as proteasome inhibitors and apoptosis inducers in cancer cells. Pharm. Res., 2009, 26, 1874-1880.
30. Kanwar, S.S.; Yu, Y.; Nautiyal, J.; Patel, B.B.; Padhye, S.; Sarkar, F.H.; Majumdar, A.P. Difluorinated-curcumin (CDF): A novel curcumin analog is a potent inhibitor of colon cancer stem-like cells. Pharm. Res., 2011, 28, 827-838.
31. Chen, J.; Huang, X.F.; Qiao, L.; Katsifis, A. Insulin caused drug resistance to oxaliplatin in colon cancer cell line HT29. J. Gastrointest. Oncol., 2011, 2, 27-33.
32. Wang, Z.H.; Gao, Q.Y.; Fang, J.Y. Loss of PTEN expression as a predictor of resistance to anti-EGFR monoclonal therapy in metastatic colorectal cancer: Evidence from retrospective studies. Cancer Chemother. Pharmacol., 2012, 69, 1647-1655.
33. Chen, J. Multiple signal pathways in obesity-associated cancer. Obes. Rev., 2011, 12, 1063-1070.
34. Roy, S.; Yu, Y.; Padhye, S.B.; Sarkar, F.H.; Majumdar, A.P. Difluorinated-curcumin (cdf) restores PTEN expression in colon cancer cells by down-regulating miR-21. PLoS One, 2013, 24, 8, e68543.
35. Lin, L.; Liu, Y.; Li, H.; Li, P.K.; Fuchs, J.; Shibata, H.; Iwabuchi, Y.; Lin, J. Targeting colon cancer stem cells using a new curcumin analogue, GO-Y030. Br. J. Cancer, 2011, 105, 212-220.
36. Lin, L.; Fuchs, J.; Li, C.; Olson, V.; Bekaii-Saab, T.; Lin, J. STAT3 signaling pathway is necessary for cell survival and tumorsphere forming capacity in ALDH1+/CD133+ stem cell-like human colon cancer cells. Biochem.Biophys. Res. Commun., 2011, 416, 246-251.
37. Wang, K.; Zhang, T.; Liu, L.; Wang, X.; Wu, P.; Chen, Z.; Ni, C.; Zhang, J.; Hu, F.; Huang, J. Novel micelle formulation of curcumin for enhancing antitumor activity and inhibiting colorectal cancer stem cells. Int. J. Nanomedicine., 2012, 7, 4487-4497.
38. Hezel, A.F.; Kimmelman, A.C.; Stanger, B.Z.; Bardeesy, N.; Depinho, R.A. Genetics and biology of pancreatic ductal adenocarcinoma. Genes. Dev., 2006, 20, 1218-1249.
39. Li, D.; Xie, K.; Wolff, R.; Abbruzzese, J.L. Pancreatic cancer. Lancet, 2004, 363, 1049-1057.
40. Gaviraghi, M.; Tunici, P.; Valensin, S.; Rossi, M.; Giordano, C.; Magnoni, L.; Dandrea, M.; Montagna, L.; Ritelli, R.; Scarpa, A.; Bakker, A. Pancreatic cancer spheres are more than just aggregates of stem marker-positive cells. Biosci. Rep., 2011, 31, 45-55.
41. Ischenko, I.; Seeliger, H.; Kleespies, A.; Angele, M.K.; Eichhorn, M.E.; Jauch, K.W.; Bruns, C.J. Pancreatic cancer stem cells: New understanding of tumorigenesis, clinical implications. Langenbecks. Arch. Surg., 2010, 395, 1-10.
42. Wang, Z.; Li, Y.; Ahmad, A.; Azmi, A.S.; Kong, D.; Banerjee, S.; Sarkar, F.H. Targeting miRNAs involved in cancer stem cell and EMT regulation: An emerging concept in overcoming drug resistance. Drug Resist. Updat., 2010, 13, 109-118.
43. Yu, Y.; Kanwar, S.S.; Patel, B.B.; Oh, P.S.; Nautiyal, J.; Sarkar, F.H.; Majumdar, A.P. MicroRNA-21 induces stemness by down regulating transforming growth factor beta receptor2 (TGFβR2) in colon cancer cells. Carcinogenesis, 2012, 3, 68-76.
44. Bao, B.; Ali, S.; Kong, D.; Sarkar, S.H.; Wang, Z.; Banerjee, S.; Aboukameel, A.; Padhye, S.; Philip, P.A.; Sarkar, F.H. Anti-tumor activity of a novel compound-CDF is mediated by regulating miR- 21, miR-200, and PTEN in pancreatic cancer. PLoS One, 2011, 6, e17850.
45. Bao, B.; Azmi, AS.; Ali, S.; Ahmad, A.; Li, Y.; Banerjee, S.; Kong, D.; Sarkar, F.H. The biological kinship of hypoxia with CSC and EMT and their relationship with deregulated expression of miRNAs and tumor aggressiveness. Biochim. Biophys. Acta., 2012, 1826, 272-296.
46. Bao, B.; Ali, S.; Ahmad, A.; Azmi, AS.; Li, Y.; Banerjee, S.; Kong, D.; Sethi, S.; Aboukameel, A.; Padhye, S.B.; Sarkar, F.H. Hypoxia-induced aggressiveness of pancreatic cancer cells is due to increased expression of VEGF, IL-6 and miR-21, which can be attenuated by CDF treatment. PLoS One., 2012, 7, e50165.
47. Mani, S.A.; Guo, W.; Liao, M.J.; Eaton, E.N.; Ayyanan, A.; Zhou, A.Y.; Brooks, M.; Reinhard, F.; Zhang, C.C.; Shipitsin, M.; Campbell, L.L.; Polyak, K.; Brisken, C.; Yang, J.; Weinberg, R.A. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell, 2008, 133, 704-715.
48. Soubani, O.; Ali, A.S.; Logna, F.; Ali, S.; Philip, P.A.; Sarkar, F.H. Re-expression of miR-200 by novel approaches regulates the expression of PTEN and MT1-MMP in pancreatic cancer. Carcinogenesis, 2012, 33, 1563-1571.
49. Bao, B.; Ali, S.; Banerjee, S.; Wang, Z.; Logna, F.; Azmi, A.S.; Kong, D.; Ahmad, A.; Li, Y.; Padhye, S.; Sarkar, F.H. Curcumin analogue CDF inhibits pancreatic tumor growth by switching on suppressor microRNAs and attenuating EZH2 expression. Cancer Res., 2012, 72, 335-345.
50. Sun, M.; Estrov, Z.; Ji, Y.; Coombes, K.R.; Harris, D.H.; Kurzrock, R. Curcumin (diferuloylmethane) alters the expression profiles of microRNAs in human pancreatic cancer cells. Mol. Cancer. Ther., 2008, 7, 464-473.
51. Ali, S.; Ahmad, A.; Aboukameel, A.; Bao, B.; Padhye, S.; Philip, P.A.; Sarkar, F.H. Increased RasGTPase activity is regulated by miRNAs that can be attenuated by CDF treatment in pancreatic cancer cells. Cancer Lett., 2012, 319, 173-181.
52. Louis, D.N.; Ohgaki, H.; Wiestler, O.D.; Cavenee, W.K.; Burger, P.C.; Jouvet, A.; Scheithauer, B.W.; Kleihues, P. The 2007 WHO classification of tumours of the central nervous system. Acta. Neuropathol., 2007, 114, 97-109.
53. Zhou, B.B.; Zhang, H.; Damelin, M.; Geles, K.G.; Grindley, J.C.; Dirks, P.B. Tumour-initiating cells: Challenges and opportunities for anticancer drug discovery. Nat. Rev. Drug. Discov., 2009, 8, 806-823.
54. Das, S.; Srikanth, M.; Kessler, J.A. Cancer stem cells and glioma. Nat. Clin. Pract. Neurol., 2008, 4, 427-435.
55. 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.
56. Feng, X.; Zhou, Q.; Liu, C.; Tao, M.L. Drug screening study using gliomastem-like cells. Mol. Med. Rep., 2012, 6, 1117-1120.
57. Hossain, M.; Banik, N.L.; Ray, S.K. Synergistic anti-cancer mechanisms of curcumin and paclitaxel for growth inhibition of human brain tumor stem cells and LN18 and U138MG cells. Neurochem. Int., 2012, 61, 1102-1113.
58. Lim, K.J.; Bisht S.; Bar, E.E.; Maitra, A.; Eberhart, C.G. A polymeric nanoparticle formulation of curcumin inhibits growth, clonogenicity and stem-like fraction in malignant brain tumors. Cancer. Biol. Ther., 2011, 11, 464-473.
59. Zhuang, W.; Long, L.; Zheng, B.; Ji, W.; Yang, N.; Zhang, Q.; Liang, Z. Curcumin promotes differentiation of glioma-initiating cells by inducing autophagy. Cancer Sci., 2012, 103, 684-690.
60. Zhuang, W.; Li, B.; Long, L.; Chen, L.; Huang, Q.; Liang, Z. Induction of autophagy promotes differentiation of gliomainitiating cells and their radio sensitivity. Int. J. Cancer, 2011, 129, 2720-2731.
61. Aoki, H.; Takada, Y.; Kondo, S.; Sawaya, R.; Aggarwal, B.B.; Kondo, Y. Evidence that curcumin suppresses the growth of malignant gliomas in vitro and in vivo through induction of autophagy: Role of Akt and extracellular signal-regulated kinase signaling pathways. Mol.Pharmacol., 2007, 72, 29-39.
62. Easton, D.F. How many more breast cancer predisposition genes are there? Breast Cancer Res., 1999, 1, 14-17.
63. Pal, T.; Permuth-Wey, J.; Betts, J.A.; Krischer, J.P.; Fiorica, J.; Arango, H.; LaPolla, J.; Hoffman, M.; Martino, M.A.; Wakeley, K.; Wilbanks, G.; Nicosia, S.; Cantor, A.; Sutphen, R. BRCA1 and BRCA2 mutations account for a large proportion of ovarian carcinoma cases. Cancer, 2005, 104, 2807-2816.
64. Chen, S.; Parmigiani, G. Meta-analysis of BRCA1 and BRCA2 penetrance. J. Clin. Oncol., 2007, 25, 1329-1333.
65. Ginestier, C.; Hur, M.H.; Charafe-Jauffret, E.; Monville, F.; Dutcher, J.; Brown, M.; Jacquemier, J.; Viens, P.; Kleer, C.G.; Liu, S.; Schott, A.; Hayes, D.; Birnbaum, D.; Wicha, M.S.; Dontu, G. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell, 2007, 1, 555-567.
66. Kakarala, M.; Brenner, D.E.; Korkaya, H.; Cheng, C.; Tazi, K.; Ginestier, C.; Liu, S.; Dontu, G.; Wicha, M.S. Targeting breast stem cells with the cancer preventive compounds curcumin and piperine. Breast Cancer Res. Treat., 2010, 122, 777-785.
67. Wei, X.; Senanayake, T.H.; Warren, G.; Vinogradov, S.V. Hyaluronic acid-based nanogel-drug conjugates with enhanced anticancer activity designed for the targeting of CD44-positive and drug-resistant tumors. Bioconjug. Chem., 2013, 24, 658-668.
68. 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. Altern. Med., 2012, 12,195.
69. Almanaa, T.N.; Geusz, M.E.; Jamasbi, R.J. A new method for identifying stem-like cells in esophageal cancer cell lines. J. Cancer, 2013, 4, 536-548.
70. Yan, D.; Geusz, M.E.; Jamasbi, R.J. Properties of lewis lung carcinoma cells surviving curcumin toxicity. J. Cancer, 2012, 3, 32-41.
71. Yu, C.C.; Tsai, L.L.; Wang, M.L.; Yu, C.H.; Lo, W.L.; Chang, Y.C.; Chiou, G.Y.; Chou, M.Y.; Chiou, S.H. MiR145 targets the SOX9/ADAM17axis to inhibit tumor-initiating cells and IL-6- mediated paracrine effects in head and neck cancer. Cancer Res., 2013, 73, 3425-3240.
72. Cheng, A.L.; Hsu, C.H.; Lin, J.K.; Hsu, M.M.; Ho, Y.F.; Shen, T.S.; Ko, J.Y.; Lin, J.T.; Lin, B.R.; Ming-Shiang, W.; Yu, H.S.; Jee, S.H.; Chen, G.S.; Chen, T.M.; Chen, C.A.; Lai, M.K.; Pu, Y.S.; Pan, M.H.; Wang, Y.J.; Tsai, C.C.; Hsieh, C.Y. Phase I clinical trial of curcumin, a chemopreventive agent, in patients with high-risk or pre-malignant lesions. Anticancer. Res., 2001, 21, 2895-2900.
73. Epelbaum, R.; Schaffer, M.; Vizel, B.; Badmaev, V.; Bar-Sela, G. Curcumin and gemcitabine in patients with advanced pancreatic cancer. Nutr. Cancer, 2010, 62, 1137-1141.
74. Cao, J.; Jia, L.; Zhou, H.M.; Liu, Y.; Zhong, L.F. Mitochondrial and nuclear DNA damage induced by curcumin in human hepatoma G2 cells. Toxicol. Sci., 2006, 91, 476-83.