Curcumin improves the efficacy of cisplatin by targeting cancer stem-like cells through p21 and cyclin D1-mediated tumour cell inhibition in non-small cell lung cancer cell lines

Oncology Reports

Volumn 35, Issue 1, 2016, Pages 13-25

  Baharuddin, Puteri ^a   Satar, Nazilah ^b   Fakiruddin, Kamal Shaik ^a   Zakaria, Norashikin ^b   Lim, Moon Nian ^a   Yusoff, Narazah Mohd ^b   Zakaria, Zubaidah ^a   Yahaya, Badrul Hisham ^b  

^a INSTITUTE FOR MEDICAL RESEARCH   (Malaysia)

^b ADVANCED MEDICAL AND DENTAL INSTITUTE   (Malaysia)

Author keywords

Cancer stem like cells; Cisplatin; Curcumin; Non small cell lung cancer

Indexed keywords

ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE 9; CISPLATIN; CURCUMIN; CYCLIN D1; EPITHELIAL CELL ADHESION MOLECULE; MESSENGER RNA; PROTEIN P21; ANTINEOPLASTIC AGENT; CCND1 PROTEIN, HUMAN; CDKN1A PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 1A;

A549 CELL LINE; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER STEM CELL; CELL CYCLE ARREST; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; DRUG EXPOSURE; DRUG POTENTIATION; DRUG SENSITIVITY; DRUG TARGETING; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION REGULATION; GROWTH INHIBITION; H2170 CELL LINE; HUMAN; HUMAN CELL; IC50; LUNG CANCER CELL LINE; METASTASIS INHIBITION; MIGRATION INHIBITION; NON SMALL CELL LUNG CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; CELL CYCLE; CELL MOTION; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECTS; GENETICS; LUNG TUMOR; METABOLISM; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CARCINOMA, NON-SMALL-CELL LUNG; CELL CYCLE; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; CISPLATIN; CURCUMIN; CYCLIN D1; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DRUG SYNERGISM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; NEOPLASTIC STEM CELLS; SIGNAL TRANSDUCTION;

EID: 84954062937     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2015.4371     Document Type: Article

References (71)

1. Siegel R, Naishadham D and Jemal A: Cancer statistics, 2012. CA Cancer J Clin 62: 10-29, 2012.
2. Jemal A, Bray F, Center MM, Ferlay J, Ward E and Forman D: Global cancer statistics. CA Cancer J Clin 61: 69-90, 2011.
3. Hanahan D and Weinberg RA: The hallmarks of cancer. Cell 100: 57-70, 2000.
4. Mountain CF, Lukeman JM, Hammar SP, Chamberlain DW, Coulson WF, Page DL, Victor TA and Weiland LH: Lung cancer classification: The relationship of disease extent and cell type to survival in a clinical trials population. J Surg Oncol 35: 147-156, 1987.
5. Curtis SJ, Sinkevicius KW, Li D, Lau AN, Roach RR, Zamponi R, Woolfenden AE, Kirsch DG, Wong K-K and Kim CF: Primary tumor genotype is an important determinant in identification of lung cancer propagating cells. Cell Stem Cell 7: 127-133, 2010.
6. Tan BT, Park CY, Ailles LE and Weissman IL: The cancer stem cell hypothesis: A work in progress. Lab Invest 86: 1203-1207, 2006.
7. Gil J, Stembalska A, Pesz KA and Sasiadek MM: Cancer stem cells: The theory and perspectives in cancer therapy. J Appl Genet 49: 193-199, 2008.
8. Li L and Neaves WB: Normal stem cells and cancer stem cells: The niche matters. Cancer Res 66: 4553-4557, 2006.
9. Mukherjee S, Kong J and Brat DJ: Cancer stem cell division: When the rules of asymmetry are broken. Stem Cells Dev 24: 405-416, 2015.
10. Chen S and Huang EH: The colon cancer stem cell microenvironment holds keys to future cancer therapy. J Gastrointest Surg 18: 1040-1048, 2014.
11. O'Flaherty JD, Barr M, Fennell D, Richard D, Reynolds J, O'Leary J and O'Byrne K: The cancer stem-cell hypothesis: Its emerging role in lung cancer biology and its relevance for future therapy. J Thorac Oncol 7: 1880-1890, 2012.
12. Hong IS, Lee HY and Nam JS: Cancer stem cells: The 'Achilles heel' of chemo-resistant tumors. Recent Patents Anticancer Drug Discov 10: 2-22, 2015.
13. Orian-Rousseau V and Ponta H: Perspectives of CD44 targeting therapies. Arch Toxicol 89: 3-14, 2015.
14. Ma J, Fang B, Zeng F, Pang H, Zhang J, Shi Y, Wu X, Cheng L, Ma C, Xia J, et al: Curcumin inhibits cell growth and invasion through up-regulation of miR-7 in pancreatic cancer cells. Toxicol Lett 231: 82-91, 2014.
15. Mukherjee S, Mazumdar M, Chakraborty S, Manna A, Saha S, Khan P, Bhattacharjee P, Guha D, Adhikary A, Mukhjerjee S, et al: Curcumin inhibits breast cancer stem cell migration by amplifying the E-cadherin/β-catenin negative feedback loop. Stem Cell Res Ther 5: 116, 2014.
16. Sarkar R, Mukherjee A, Mukherjee S, Biswas R, Biswas J and Roy M: Curcumin augments the efficacy of antitumor drugs used in leukemia by modulation of heat shock proteins via HDAC6. Environ Pathol Toxicol Oncol 33: 247-263, 2014.
17. Xiao C, Wang L, Zhu L, Zhang C and Zhou J: Curcumin inhibits oral squamous cell carcinoma SCC-9 cells proliferation by regulating miR-9 expression. Biochem Biophys Res Commun 454: 576-580, 2014.
18. Ye M, Zhang J, Zhang J, Miao Q, Yao L and Zhang J: Curcumin promotes apoptosis by activating the p53-miR-192-5p/215-XIAP pathway in non-small cell lung cancer. Cancer Lett 357: 196-205, 2015.
19. Anand P, Sundaram C, Jhurani S, Kunnumakkara AB and Aggarwal BB: Curcumin and cancer: An 'old-age' disease with an 'age-old' solution. Cancer Lett 267: 133-164, 2008.
20. Andjelkovic T, Pesic M, Bankovic J, Tanic N, Markovic ID and Ruzdijic S: Synergistic effects of the purine analog sulfinosine and curcumin on the multidrug resistant human non-small cell lung carcinoma cell line (NCI-H460/R). Cancer Biol Ther 7: 1024-1032, 2008.
21. Ebert B, Seidel A and Lampen A: Phytochemicals induce breast cancer resistance protein in Caco-2 cells and enhance the transport of benzo(a)pyrene-3-sulfate. Toxicol Sci 96: 227-236, 2007.
22. Hou X-L, Takahashi K, Tanaka K, Tougou K, Qiu F, Komatsu K, Takahashi K and Azuma J: Curcuma drugs and curcumin regulate the expression and function of P-gp in Caco-2 cells in completely opposite ways. Int J Pharm 358: 224-229, 2008.
23. Chanvorachote P, Pongrakhananon V, Wannachaiyasit S, Luanpitpong S, Rojanasakul Y and Nimmannit U: Curcumin sensitizes lung cancer cells to cisplatin-induced apoptosis through superoxide anion-mediated Bcl-2 degradation. Cancer Invest 27: 624-635, 2009.
24. Li S, Liu Z, Zhu F, Fan X, Wu X, Zhao H and Jiang L: Curcumin lowers erlotinib resistance in non-small cell lung carcinoma cells with mutated EGF receptor. Oncol Res 21: 137-144, 2013.
25. Chan MM, Fong D, Soprano KJ, Holmes WF and Heverling H: Inhibition of growth and sensitization to cisplatin-mediated killing of ovarian cancer cells by polyphenolic chemopreventive agents. J Cell Physiol 194: 63-70, 2003.
26. Chan MM, Soprano KJ, Weinstein K and Fong D: Epigallo catechin-3-gallate delivers hydrogen peroxide to induce death of ovarian cancer cells and enhances their cisplatin susceptibility. J Cell Physiol 207: 389-396, 2006.
27. Duarte VM, Han E, Veena MS, Salvado A, Suh JD, Liang LJ, Faull KF, Srivatsan ES and Wang MB: Curcumin enhances the effect of cisplatin in suppression of head and neck squamous cell carcinoma via inhibition of IKKβ protein of the NFκB pathway. Mol Cancer Ther 9: 2665-2675, 2010.
28. Notarbartolo M, Poma P, Perri D, Dusonchet L, Cervello M and D'Alessandro N: Antitumor effects of curcumin, alone or in combination with cisplatin or doxorubicin, on human hepatic cancer cells. Analysis of their possible relationship to changes in NF-κB activation levels and in IAP gene expression. Cancer Lett 224: 53-65, 2005.
29. Aggarwal BB, Shishodia S, Takada Y, Banerjee S, Newman RA, Bueso-Ramos CE, Price JE: Curcumin suppresses the paclitaxel-induced nuclear factor-kappaB pathway in breast cancer cells and inhibits lung metastasis of human breast cancer in nude mice. Clin Cancer Res 11: 7490-7498, 2005.
30. Cheng AL, Hsu CH, Lin JK, Hsu MM, Ho YF, Shen TS, Ko JY, Lin JT, Lin BR, Ming-Shiang W, et al: Phase I clinical trial of curcumin, a chemopreventive agent, in patients with high-risk or pre-malignant lesions. Anticancer Res 21: 2895-2900, 2001.
31. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, et al: ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555-567, 2007.
32. Kakarala M, Brenner DE, Korkaya H, Cheng C, Tazi K, Ginestier C, Liu S, Dontu G and Wicha MS: Targeting breast stem cells with the cancer preventive compounds curcumin and piperine. Breast Cancer Res Treat 122: 777-785, 2010.
33. Fong D, Yeh A, Naftalovich R, Choi TH and Chan MM: Curcumin inhibits the side population (SP) phenotype of the rat C6 glioma cell line: Towards targeting of cancer stem cells with phytochemicals. Cancer Lett 293: 65-72, 2010.
34. Zhuang W, Long L, Zheng B, Ji W, Yang N, Zhang Q and Liang Z: Curcumin promotes differentiation of glioma-initiating cells by inducing autophagy Cancer Sci 103: 684-690, 2012.
35. Pellacani D, Oldridge EE, Collins AT and Maitland NJ: Prominin-1 (CD133) expression in the prostate and prostate cancer: A marker for quiescent stem cells. Adv Exp Med Biol 777: 167-184, 2013.
36. Reyes EE, Kunovac SK, Duggan R, Kregel S and Vander Griend DJ: Growth kinetics of CD133-positive prostate cancer cells. Prostate 73: 724-733, 2013.
37. Vander Griend DJ, Karthaus WL, Dalrymple S, Meeker A, DeMarzo AM and Isaacs JT: The role of CD133 in normal human prostate stem cells and malignant cancer-initiating cells. Cancer Res 68: 9703-9711, 2008.
38. Bi CL, Fang JS, Chen FH, Wang YJ and Wu J: Chemoresistance of CD133(+) tumor stem cells from human brain glioma. Zhong Nan Da Xue Xue Bao Yi Xue Ban 32: 568-573, 2007 (In Chinese).
39. Choi SA, Wang KC, Phi JH, Lee JY, Park CK, Park SH and Kim SK: A distinct subpopulation within CD133 positive brain tumor cells shares characteristics with endothelial progenitor cells. Cancer Lett 324: 221-230, 2012.
40. Li MC, Deng YW, Wu J, Chen FH, Liu JF and Fang JS: Isolation and characterization of brain tumor stem cells in human medulloblastoma. Ai Zheng 25: 241-246, 2006 (In Chinese).
41. Singh S and Dirks PB: Brain tumor stem cells: Identification and concepts. Neurosurg Clin N Am 18: 31-38, 2007
42. Kozovska Z, Gabrisova V and Kucerova L: Colon cancer: Cancer stem cells markers, drug resistance and treatment. Biomed Pharmacother 68: 911-916, 2014
43. Mərgaritescu C, Pirici D, Cherciu I, Bərbəlan A, Cârtânə T and Səftoiu A: CD133/CD166/Ki-67 triple immunofluorescence assessment for putative cancer stem cells in colon carcinoma. J Gastrointestin Liver Dis 23: 161-170, 2014
44. Vincent Z, Urakami K, Maruyama K, Yamaguchi K and Kusuhara M: CD133-positive cancer stem cells from Colo205 human colon adenocarcinoma cell line show resistance to chemotherapy and display a specific metabolomic profile. Genes Cancer 5: 250-260, 2014
45. Cogliati B, Aloia TP, Bosch RV, Alves VA, Hernandez-Blazquez FJ and Dagli ML: Identification of hepatic stem/progenitor cells in canine hepatocellular and cholangiocellular carcinoma. Vet Comp Oncol 8: 112-121, 2010.
46. Tomuleasa C, Soritau O, Rus-Ciuca D, Pop T, Todea D, Mosteanu O, Pintea B, Foris V, Susman S, Kacsó G, et al: Isolation and characterization of hepatic cancer cells with stem-like properties from hepatocellular carcinoma. J Gastrointestin Liver Dis 19: 61-67, 2010.
47. Yang XR, Xu Y, Yu B, Zhou J, Qiu SJ, Shi GM, Zhang BH, Wu WZ, Shi YH, Wu B, et al: High expression levels of putative hepatic stem/progenitor cell biomarkers related to tumour angiogenesis and poor prognosis of hepatocellular carcinoma. Gut 59: 953-962, 2010.
48. + hepatic cancer stem cells, blocking their contributions to hepatocellular carcinoma. Cancer Res 72: 4276-4285, 2012.
49. + cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci USA 106: 16281-16286, 2009
50. Salnikov AV, Gladkich J, Moldenhauer G, Volm M, Mattern J and Herr I: CD133 is indicative for a resistance phenotype but does not represent a prognostic marker for survival of non-small cell lung cancer patients. Int J Cancer 126: 950-958, 2010.
51. Sullivan JP, Spinola M, Dodge M, Raso MG, Behrens C, Gao B, Schuster K, Shao C, Larsen JE, Sullivan LA, et al: Aldehyde dehydrogenase activity selects for lung adenocarcinoma stem cells dependent on notch signaling. Cancer Res 70: 9937-9948, 2010.
52. Woo T, Okudela K, Mitsui H, Yazawa T, Ogawa N, Tajiri M, Yamamoto T, Rino Y, Kitamura H and Masuda M: Prognostic value of CD133 expression in stage I lung adenocarcinomas. Int J Clin Exp Pathol 4: 32-42, 2010.
53. Sterlacci W, Savic S, Fiegl M, Obermann E and Tzankov A: Putative stem cell markers in non-small-cell lung cancer: A clinicopathologic characterization. J Thorac Oncol 9: 41-49, 2014.
54. Zhang WC, Shyh-Chang N, Yang H, Rai A, Umashankar S, Ma S, Soh BS, Sun LL, Tai BC, Nga ME, et al: Glycine decarboxylase activity drives non-small cell lung cancer tumor-initiating cells and tumorigenesis. Cell 148: 259-272, 2012.
55. Zakaria N, Yusoff NM, Zakaria Z, Lim MN, Baharuddin PJN, Fakiruddin KS and Yahaya B: Human non-small cell lung cancer expresses putative cancer stem cell markers and exhibits the transcriptomic profile of multipotent cells. BMC Cancer 15: 84, 2015.
56. Chen K, Huang YH and Chen JL: Understanding and targeting cancer stem cells: Therapeutic implications and challenges. Acta Pharmacol Sin 34: 732-740, 2013.
57. Xu X-M, Zhang Y, Qu D, Liu H-B, Gu X, Jiao G-Y and Zhao L: Combined anticancer activity of osthole and cisplatin in NCI-H460 lung cancer cells in vitro. Exp Ther Med 5: 707-710, 2013.
58. Douillard J-Y, Eckardt J and Scagliotti GV: Challenging the platinum combinations in the chemotherapy of NSCLC. Lung Cancer 38 (Suppl 4): 21-28, 2002.
59. Stewart DJ: Mechanisms of resistance to cisplatin and carboplatin. Crit Rev Oncol Hematol 63: 12-31, 2007.
60. Burnett J, Newman B and Sun D: Targeting cancer stem cells with natural products. Curr Drug Targets 13: 1054-1064, 2012.
61. Mondal S, Bandyopadhyay S, Ghosh MK, Mukhopadhyay S, Roy S and Mandal C: Natural products: Promising resources for cancer drug discovery. Anticancer Agents Med Chem 12: 49-75, 2012.
62. Ye MX, Zhao YL, Li Y, Miao Q, Li ZK, Ren XL, Song LQ, Yin H and Zhang J: Curcumin reverses cis-platin resistance and promotes human lung adenocarcinoma A549/DDP cell apoptosis through HIF-1alpha and caspase-3 mechanisms. Phytomedicine 19: 779-787, 2012.
63. Zhou B-BS, Zhang H, Damelin M, Geles KG, Grindley JC and Dirks PB: Tumour-initiating cells: Challenges and opportunities for anticancer drug discovery. Nat Rev Drug Discov 8: 806-823, 2009.
64. Buhrmann C, Kraehe P, Lueders C, Shayan P, Goel A and Shakibaei M: Curcumin suppresses crosstalk between colon cancer stem cells and stromal fibroblasts in the tumor microenvironment: Potential role of EMT. PLoS One 9: e107514, 2014.
65. Charpentier MS, Whipple RA, Vitolo MI, Boggs AE, Slovic J, Thompson KN, Bhandary L and Martin SS: Curcumin targets breast cancer stem-like cells with microtentacles that persist in mammospheres and promote reattachment. Cancer Res 74: 1250-1260, 2014.
66. Wang X, Zhu Y, Ma Y, Wang J, Zhang F, Xia Q and Fu D: The role of cancer stem cells in cancer metastasis: New perspective and progress. Cancer Epidemiol 37: 60-63, 2013.
67. Fazilaty H, Gardaneh M, Bahrami T, Salmaninejad A and Behnam B: Crosstalk between breast cancer stem cells and meta-static niche: Emerging molecular metastasis pathway? Tumour Biol 34: 2019-2030, 2013.
68. Croker AK, Goodale D, Chu J, Postenka C, Hedley BD, Hess DA and Allan AL: High aldehyde dehydrogenase and expression of cancer stem cell markers selects for breast cancer cells with enhanced malignant and metastatic ability. J Cell Mol Med 13: 2236-2252, 2009.
69. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ and Heeschen C: Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1: 313-323, 2007.
70. Srivastava RK, Chen Q, Siddiqui I, Sarva K and Shankar S: Linkage of curcumin-induced cell cycle arrest and apoptosis by cyclin-dependent kinase inhibitor p21(/WAF1/CIP1). Cell Cycle 6: 2953-2961, 2007.
71. Zhang H, Yu T, Wen L, Wang H, Fei D and Jin C: Curcumin enhances the effectiveness of cisplatin by suppressing CD133(+) cancer stem cells in laryngeal carcinoma treatment. Exp Ther Med 6: 1317-1321, 2013.