Curcumin induces proapoptotic effects against human melanoma cells and modulates the cellular response to immunotherapeutic cytokines

Molecular Cancer Therapeutics

Volumn 8, Issue 9, 2009, Pages 2726-2735

  Bill, Matthew A ^a   Bakan, Courtney ^a   Benson Jr , Don M ^a   Fuchs, James ^a   Young, Gregory ^b   Lesinski, Gregory B ^a,c  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c Division of Hematology and Oncology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CURCUMIN; GAMMA INTERFERON; GRANZYME B; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL 2; RECOMBINANT GAMMA INTERFERON; RECOMBINANT INTERLEUKIN 2; STAT1 PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN;

APOPTOSIS; ARTICLE; CANCER CELL DESTRUCTION; CANCER IMMUNOTHERAPY; CELLULAR IMMUNITY; COCULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DNA FLANKING REGION; DRUG ANTAGONISM; ENZYME SYNTHESIS; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOMODULATION; MELANOMA CELL; NATURAL KILLER CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TARGET CELL; TRANSCRIPTION REGULATION;

APOPTOSIS; BLOTTING, WESTERN; CURCUMIN; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; IMMUNOTHERAPY; INTERFERONS; KILLER CELLS, NATURAL; MELANOMA; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR; TUMOR CELLS, CULTURED;

EID: 70349479218     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-09-0377     Document Type: Article

References (70)

1. Goel A, Kunnumakkara AB, Aggarwal BB. Curcumin as "curecumin": from kitchen to clinic. Biochem Pharmacol 2008;75:787-809.
2. Duvoix A, Blasius R, Delhalle S, et al. Chemopreventive and therapeutic effects of curcumin. Cancer Lett 2005;223:181-190
3. Shishodia S, Chaturvedi MM, Aggarwal BB. Role of curcumin in cancer therapy. Curr Probl Cancer 2007;31:243-305.
4. Cheng AL, Hsu CH, Lin JK, 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
5. Shoba G, Joy D, Joseph T, Majeed M, Rajendran R, Srinivas PS. Influence of piperine on the pharmacokinetics of curcumin in animals and human volunteers. Planta Med 1998;64:353-356 (Pubitemid 28234275)
6. Holder GM, Plummer JL, Ryan AJ. The metabolism and excretion of curcumin (1,7-bis-(4-hydroxy-3-methoxyphenyl)-1,6-heptadiene-3, 5-dione) in the rat. Xenobiotica 1978;8:761-768
7. Aggarwal BB, Shishodia S, Takada Y, et al. Curcumin suppresses the paclitaxel-induced nuclear factor-κB pathway in breast cancer cells and inhibits lung metastasis of human breast cancer in nude mice. Clin Cancer Res 2005;11:7490-7498 (Pubitemid 41507710)
8. Bachmeier B, Nerlich AG, Iancu CM, et al. The chemopreventive polyphenol Curcumin prevents hematogenous breast cancer metastases in immunodeficient mice. Cell Physiol Biochem 2007;19:137-152 (Pubitemid 46270897)
9. Busquets S, Carbo N, Almendro V, Quiles MT, Lopez-Soriano FJ, Argiles JM. Curcumin, a natural product present in turmeric, decreases tumor growth but does not behave as an anticachectic compound in a rat model. Cancer Lett 2001;167:33-38 (Pubitemid 32373266)
10. Li L, Braiteh FS, Kurzrock R. Liposome-encapsulated curcumin: in vitro and in vivo effects on proliferation, apoptosis, signaling, and angiogenesis. Cancer 2005;104:1322-1331 (Pubitemid 41282806)
11. LoTempio MM, Veena MS, Steele HL, et al. Curcumin suppresses growth of head and neck squamous cell carcinoma. Clin Cancer Res 2005;11:6994-7002. (Pubitemid 41428759)
12. Menon LG, Kuttan R, Kuttan G. Inhibition of lung metastasis in mice induced by B16F10 melanoma cells by polyphenolic compounds. Cancer Lett 1995;95:221-225
13. Odot J, Albert P, Carlier A, Tarpin M, Devy J, Madoulet C. In vitro and in vivo anti-tumoral effect of curcumin against melanoma cells. Int J Cancer 2004;111:381-387
14. Yoysungnoen P, Wirachwong P, Bhattarakosol P, Niimi H, Patumraj S. Effects of curcumin on tumor angiogenesis and biomarkers, COX-2 and VEGF, in hepatocellular carcinoma cell-implanted nude mice. Clin Hemorheol Microcirc 2006;34:109-115 (Pubitemid 43351018)
15. Ascierto PA, Kirkwood JM. Adjuvant therapy of melanoma with interferon: lessons of the past decade. J Transl Med 2008;6:62.
16. Wheatley K, Ives N, Eggermont A, Suciu S. Interferon-α as adjuvant therapy formelanoma: an individual patient data meta-analysis of randomised trials. Proc Am Soc Clin Oncol 2007;478S, (abstr 8526).
17. Agarwala S. Improving survival in patients with high-risk and metastatic melanoma: immunotherapy leads the way. Am J Clin Dermatol 2003;4:333-346 (Pubitemid 36560719)
18. Yang JC, Sherry RM, Steinberg SM, et al. Randomized study of highdose and low-dose interleukin-2 in patients with metastatic renal cancer. J Clin Oncol 2003;21:3127-3132
19. Malek TR. The biology of interleukin-2. Annu Rev Immunol 2008;26:453-479
20. Moschos SJ, Edington HD, Land SR, et al. Neoadjuvant treatment of regional stage IIIB melanoma with high-dose interferon alfa-2b induces objective tumor regression in association with modulation of tumor infiltrating host cellular immune responses. J Clin Oncol 2006;24:3164-3171
21. Waithman J, Gebhardt T, Davey GM, Heath WR, Carbone FR. Cutting edge: enhanced IL-2 signaling can convert self-specific T cell response from tolerance to autoimmunity. J Immunol 2008;180:5789-5793
22. Huang S, Bucana CD, Van Arsdall M, Fidler IJ. Stat1 negatively regulates angiogenesis, tumorigenicity and metastasis of tumor cells. Oncogene 2002;21:2504-2512 (Pubitemid 34438103)
23. Lesinski GB, Trefry J, Brasdovich M, et al. Melanoma cells exhibit variable signal transducer and activator of transcription 1 phosphorylation and a reduced response to IFN-α compared with immune effector cells. Clin Cancer Res 2007;13:5010-5019 (Pubitemid 47502065)
24. Levy DE, Gilliland DG. Divergent roles of STAT1 and STAT5 in malignancy as revealed by gene disruptions in mice. Oncogene 2000;19:2505-2510
25. Pansky A, Hildebrand P, Fasler-Kan E, et al. Defective Jak-STAT signal transduction pathway in melanoma cells resistant to growth inhibition by interferon-α. Int J Cancer 2000;85:720-725 (Pubitemid 30080488)
26. Thyrell L, Erickson S, Zhivotovsky B, et al. Mechanisms of interferon-α induced apoptosis in malignant cells. Oncogene 2002;21:1251-1262 (Pubitemid 34185242)
27. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 2002;3:991-998 (Pubitemid 35363648)
28. Dunn GP, Bruce AT, Sheehan KC, et al. A critical function for type I interferons in cancer immunoediting. Nat Immunol 2005;6:722-729 (Pubitemid 41716746)
29. Dunn GP, Koebel CM, Schreiber RD. Interferons, immunity and cancer immunoediting. Nat Rev Immunol 2006;6:836-848
30. Baker PE, Gillis S, Smith KA. Monoclonal cytolytic T-cell lines. J Exp Med 1979;149:273-278
31. Grimm EA, Mazumder A, Zhang HZ, Rosenberg SA. Lymphokine-activated killer cell phenomenon. Lysis of natural killer-resistant fresh solid tumor cells by interleukin 2-activated autologous human peripheral blood lymphocytes. J Exp Med 1982;155:1823-1841 (Pubitemid 12074218)
32. Lotze MT, Grimm EA, Mazumder A, Strausser JL, Rosenberg SA. Lysis of fresh and cultured autologous tumor by human lymphocytes cultured in T-cell growth factor. Cancer Res 1981;41:4420-4425 (Pubitemid 12201351)
33. Satyamoorthy K, DeJesus E, Linnenbach AJ, et al. Melanoma cell lines from different stages of progression and their biological and molecular analyses. Melanoma Res 1997;7 Suppl 2:S35-42. (Pubitemid 27501624)
34. Parihar R, Dierksheide J, Hu Y, Carson WE. IL-12 enhances the natural killer cell cytokine response to Ab-coated tumor cells. J Clin Invest 2002;110:983-992
35. Venkateswarlu S, Ramachandra MS, Subbaraju GV. Synthesis and biological evaluation of polyhydroxycurcuminoids. Bioorg Med Chem 2005;13:6374-6380
36. Park BS, Kim JG, Kim MR, et al. Curcuma longa L. constituents inhibit sortase A and Staphylococcus aureus cell adhesion to fibronectin. J Agric Food Chem 2005;53:9005-9009
37. Lesinski GB, Raig T, Guenterberg K, et al. IFN-α and bortezomib overcome Bcl-2 and Mcl-1 overexpression in melanoma cells by stimulating the extrinsic pathway of apopotsis. Cancer Res 2008;68:8351-8360
38. Lesinski GB, Kondadasula SV, Crespin T, et al. Multiparametric flow cytometric analysis of inter-patient variation in STAT1 phosphorylation following interferon α immunotherapy. J Natl Cancer Inst 2004;96:1331-1342 (Pubitemid 39264122)
39. Varker KA, Kondadasula SV, Go MR, et al. Multiparametric flow cytometric analysis of signal transducer and activator of transcription 5 phosphorylation in immune cell subsets in vitro and following interleukin-2 immunotherapy. Clin Cancer Res 2006;12:5850-5858
40. Parihar R, Nadella P, Lewis A, et al. A phase I study of interleukin 12 with trastuzumab in patients with human epidermal growth factor receptor-2-overexpressing malignancies: analysis of sustained interferon γ production in a subset of patients. Clin Cancer Res 2004;10:5027-5037 (Pubitemid 39099777)
41. Shafer-Weaver KA, Sayers T, Kuhns DB, et al. Evaluating the cytotoxicity of innate immune effector cells using the GrB ELISPOT assay. J Transl Med 2004;2:31. (Pubitemid 40617859)
42. Kamat AM, Sethi G, Aggarwal BB. Curcumin potentiates the apoptotic effects of chemotherapeutic agents and cytokines through downregulation of nuclear factor-κB and nuclear factor-κB-regulated gene products in IFN-α-sensitive and IFN-α-resistant human bladder cancer cells. Mol Cancer Ther 2007;6:1022-1030 (Pubitemid 46554572)
43. Kunnumakkara AB, Diagaradjane P, Guha S, et al. Curcumin sensitizes human colorectal cancer xenografts in nude mice to γ-radiation by targeting nuclear factor-κB-regulated gene products. Clin Cancer Res 2008;14:2128-2136 (Pubitemid 351551125)
44. Kaplan DH, Shankaran V, Dighe AS, et al. Demonstration of an interferon γ-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci U S A 1998;95:7556-7561 (Pubitemid 28293291)
45. Yu H, Jove R. The STATs of cancer-new molecular targets come of age. Nat Rev Cancer 2004;4:97-105. (Pubitemid 38198738)
46. Ramsauer K, Sadzak I, Porras A, et al. p38 MAPK enhances STAT1-dependent transcription independently of Ser-727 phosphorylation. Proc Natl Acad Sci U S A 2002;99:12859-12864
47. Malek TR, Yu A, Zhu L, Matsutani T, Adeegbe D, Bayer AL. IL-2 family of cytokines in T regulatory cell development and homeostasis. J Clin Immunol 2008;28:635-639
48. Whitney AR, Diehn M, Popper SJ, et al. Individuality and variation in gene expression patterns in human blood. Proc Natl Acad Sci U S A 2003;100:1896-1901 (Pubitemid 36254545)
49. Becknell B, Caligiuri MA. Natural killer cells in innate immunity and cancer. J Immunother 2008;31:685-692
50. Milacic V, Banerjee S, Landis-Piwowar KR, Sarkar FH, Majumdar AP, Dou QP. Curcumin inhibits the proteasome activity in human colon cancer cells in vitro and in vivo. Cancer Res 2008;68:7283-7292
51. Bhattacharyya S, Mandal D, Saha B, Sen GS, Das T, Sa G. Curcumin prevents tumor-induced T cell apoptosis through Stat-5a-mediated Bcl-2 induction. J Biol Chem 2007;282:15954-15964 (Pubitemid 47100378)
52. Jagetia GC, Aggarwal BB. "Spicing up" of the immune system by curcumin. J Clin Immunol 2007;27:19-35.
53. Jeong YI, Kim SW, Jung ID, et al. Curcumin suppresses the induction of indoleamine 2,3-dioxygenase by blocking the Janus-activated kinaseprotein kinase Cdelta-STAT1 signaling pathway in interferon-γ-stimulated murine dendritic cells. J Biol Chem 2009;284:3700-3708
54. Bakhshi J, Weinstein L, Poksay KS, Nishinaga B, Bresdesen DE, Rao RV. Coupling endoplasmic reticulum stress to the cell death program in mouse melanoma cells: effect of curcumin. Apoptosis 2008;13:904-914
55. Bush JA, Cheung KJ, Jr., Li G. Curcumin induces apoptosis in human melanoma cells through a Fas receptor/caspase-8 pathway independent of p53. Exp Cell Res 2001;271:305-314 (Pubitemid 33141212)
56. Siwak DR, Shishodia S, Aggarwal BB, Kurzrock R. Curcumin-induced antiproliferative and proapoptotic effects in melanoma cells are associated with suppression of IκB kinase and nuclear factor κB activity and are independent of the B-Raf/mitogen-activated/extracellular signal-regulated protein kinase pathway and the Akt pathway. Cancer 2005;104:879-890 (Pubitemid 41113691)
57. Zheng M, Ekmekcioglu S, Walch ET, Tang CH, Grimm EA. Inhibition of nuclear factor-κB and nitric oxide by curcumin inducesG2/M cell cycle arrest and apoptosis in human melanoma cells. Melanoma Res 2004;14:165-171 (Pubitemid 38879577)
58. Bharti AC, Donato N, Aggarwal BB. Curcumin (diferuloylmethane) inhibits constitutive and IL-6-inducible STAT3 phosphorylation in human multiple myeloma cells. J Immunol 2003;171:3863-3871 (Pubitemid 37254592)
59. Blasius R, Reuter S, Henry E, Dicato M, Diederich M. Curcumin regulates signal transducer and activator of transcription (STAT) expression in K562 cells. Biochem Pharmacol 2006;72:1547-1554 (Pubitemid 44666746)
60. Kim HY, Park EJ, Joe EH, Jou I. Curcumin suppresses Janus kinase-STAT inflammatory signaling through activation of Src homology 2 domain-containing tyrosine phosphatase 2 in brainmicroglia. J Immunol 2003;171:6072-6079 (Pubitemid 37467228)
61. Lesinski GB, Anghelina M, Zimmerer J, et al. The anti-tumor effects of interferon-α are abrogated in a STAT1-deficient mouse. J Clin Invest 2003;112:170-180 (Pubitemid 38056353)
62. Behbod F, Nagy ZS, Stepkowski SM, et al. Specific inhibition of Stat5a/b promotes apoptosis of IL-2-responsive primary and tumor-derived lymphoid cells. J Immunol 2003;171:3919-3927 (Pubitemid 37238663)
63. Fung MM, Rohwer F, McGuire KL. IL-2 activation of a PI3K-dependent STAT3 serine phosphorylation pathway in primary human T cells. Cell Signal 2003;15:625-636 (Pubitemid 36385168)
64. Yu TK, Caudell EG, Smid C, Grimm EA. IL-2 activation of NK cells: involvement of MKK1/2/ERK but not p38 kinase pathway. J Immunol 2000;164:6244-6251 (Pubitemid 30408804)
65. Imada K, Bloom ET, Nakajima H, et al. Stat5b is essential for natural killer cell-mediated proliferation and cytolytic activity. J Exp Med 1998;188:2067-2074 (Pubitemid 28562523)
66. Moriggl R, Sexl V, Piekorz R, Topham D, Ihle JN. Stat5 activation is uniquely associated with cytokine signaling in peripheral T cells. Immunity 1999;11:225-230 (Pubitemid 29428815)
67. Moriggl R, TophamDJ, Teglund S, et al. Stat5 is required for IL-2-induced cell cycle progression of peripheral T cells. Immunity 1999;10:249-259 (Pubitemid 29115630)
68. Kurien BT, Singh A, Matsumoto H, Scofield RH. Improving the solubility and pharmacological efficacy of curcumin by heat treatment. Assay Drug Dev Technol 2007;5:567-576 (Pubitemid 47548073)
69. Gogas H, Ioannovich J, Dafni U, et al. Prognostic significance of autoimmunity during treatment of melanoma with interferon. N Engl J Med 2006;354:709-718 (Pubitemid 43247141)
70. Golden EB, Lam PY, Kardosh A, et al. Green tea polyphenols block the anticancer effects of bortezomib and other boronic acid-based proteasome inhibitors. Blood 2009.