Curcumin in chemoprevention of breast cancer
Katarzyna Terlikowska 1 , Anna Witkowska 1 , Sławomir Terlikowski 2Abstract
Breast cancer is the most common malignant cancer among women, both in Poland and worldwide. Due to the constantly increasing number of breast cancer cases, it is vital to develop effective activities in primary and secondary prevention. One of the promising methods of best value, connecting both types of cancer prevention, appears to be chemoprevention. Chemoprevention uses natural or synthetic compounds to inhibit, delay or reverse the process of carcinogenesis. Among ingredients of natural origin, great attention is paid to curcumin – a broad-spectrum anti-cancer polyphenol derivative, extracted from the rhizome of Curcuma longa L. Curcumin has a number of chemopreventive properties such as anti-inflammatory activity, induction of apoptosis, inhibition of angiogenesis as well as tumor metastasis. Numerous in vitro and in vivo studies have demonstrated the mentioned anti-cancer effect in the epithelial breast cell line MCF-10A and in the epithelial breast cell lines MCF-7, BT-474, SK-BR-3-hr and MDA-MB-231. The main problem associated with the use of curcumin as a chemopreventive agent in humans is its low absorption from the gastrointestinal tract, poor solubility in body fluids and low bioavailability. Current studies are underway to increase the bioavailability and effectiveness of curcumin in vivo. Good results in the prevention and the treatment of breast cancer could be ensured by curcumin nanoparticles coated with albumin, known as nanocurcumin. The studies using nanocurcumin, however, are still in the preclinical stage, which is why there is a need to conduct extensive long-term randomized clinical trials to determine its effectiveness.
References
- 1. Aggarwal B.B., Shishodia S., Takada Y., Banerjee S., Newman R.A.,Bueso-Ramos C.E., Price J.E.: Curcumin suppresses the paclitaxel-inducednuclear factor-κB pathway in breast cancer cells and inhibitslung metastasis of human breast cancer in nude mice. Clin. CancerRes., 2005; 20: 7490-7498
Google Scholar - 2. Aggarwal B.B., Sundaram C., Malani N., Ichikawa H.: Curcumin.The Indian solid gold. Adv. Exp. Med. Biol., 2007; 595: 1-75
Google Scholar - 3. Anand P., Kunnumakkara A.B., Newman R.A., Aggarwal B.B.: Bioavailabilityof curcumin: problems and promises. Mol. Pharm., 2007;4: 807-818
Google Scholar - 4. Arpino G., Bardou V.J., Clark G.M., Elledge R.M.: Infiltrating lobularcarcinoma of the breast: tumor characteristics and clinical outcome.Breast Cancer Res., 2004; 6: R149-R156
Google Scholar - 5. Basnet P., Skalko-Basnet N.: Curcumin: an anti-inflammatorymolecule from a curry spice on the path to cancer treatment. Molecules,2011; 16: 4567-4598
Google Scholar - 6. Bayet-Robert M., Kwiatkowski F., Leheurteur M., Gachon F., PlanchatE., Abrial C., Mouret-Reynier M.A., Durando X., Barthomeuf C.,Chollet P.: Phase I dose escalation trial of docetaxel plus curcuminin patients with advanced and metastatic breast cancer. Cancer Biol.Therapy, 2010; 9: 8-14
Google Scholar - 7. Bennett A.: The production of prostanoids in human cancers,and their implications for tumor progression. Prog. Lipid Res., 1986;25: 539-542
Google Scholar - 8. Biswas T.K., Mukherjee B.: Plant medicines of Indian origin for woundhealing activity: a review. Int. J. Low. Extrem. Wounds, 2003; 2: 25-39
Google Scholar - 9. Boland G.P., Butt I.S., Prasad R., Knox W.F., Bundred N.J.: COX-2expression is associated with an aggressive phenotype in ductalcarcinoma in situ. Br. J. Cancer, 2004; 90: 423-429
Google Scholar - 10. Burgos-Morón E., Calderon-Montano J.M., Salvador J., RoblesA., Lopez-Lazaro M.: The dark side of curcumin. Int. J. Cancer, 2010;126: 1771-1775
Google Scholar - 11. Carroll C.E., Benakanakere I., Besch-Williford C., Ellersieck M.R.,Hyder S.M.: Curcumin delays development of medroxyprogesteroneacetate-accelerated 7,12-dimethylbenz[a]anthracene-induced mammarytumors. Menopause, 2010; 17: 178-184
Google Scholar - 12. Carroll C.E., Ellersieck M.R., Hyder S.M.: Curcumin inhibits MPAinducedsecretion of VEGF from T47-D human breast cancer cells.Menopause, 2008; 15: 570-574
Google Scholar - 13. Chaudhri K.R.: Turmeric, haldi or haridra, in eye diseases. Antiseptic,1950; 47: 67
Google Scholar - 14. Chen Y.R., Tan T.H.: Inhibition of the c-Jun N-terminal kinase(JNK) signaling pathway by curcumin. Oncogene, 1998; 17: 173-178
Google Scholar - 15. 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., ChenT.M., Chen C.A. i wsp.: Phase I clinical trial of curcumin, a chemopreventiveagent, in patients with high-risk or pre-malignant lesions.Anticancer Res., 2001; 21: 2895-2900
Google Scholar - 16. Chlebowski R.T., Kuller L.H., Prentice R.L., Stefanick M.L., MansonJ.E., Gass M., Aragaki A.K., Ockene J.K., Lane D.S., Sarto G.E., RajkovicA., Schenken R., Hendrix S.L., Ravdin P.M., Rohan T.E. i wsp.:Breast cancer after use of estrogen plus progestin in postmenopausalwomen. N. Engl. J. Med., 2009; 360: 573-587
Google Scholar - 17. Choudhuri T., Pal S., Das T., Sa G.: Curcumin selectively inducesapoptosis in deregulated cyclin D1-expressed cells at G2 phase of cellcycle in a p53-dependent manner. J. Biol. Chem., 2005; 280: 20059-20068
Google Scholar - 18. Dal Masol L., Zucchetto A., Talamini R., Serraino D., Stocco C.F.,Vercelli M., Falcini F., Franceschi S.: Effect of obesity and other lifestylefactors on mortality in women with breast cancer. Int. J. Cancer,2008; 123: 2188-2194
Google Scholar - 19. Dhandapani K.M., Mahesh V.B., Brann D.W.: Curcumin suppressesgrowth and chemoresistance of human glioblastoma cells via AP-1and NFκB transcription factors. J. Neurochem., 2007; 102: 522-538
Google Scholar - 20. Didkowska J., Wojciechowska U., Zatoński W.: Nowotwory zło-śliwe w Polsce w 2009 roku. Centrum Onkologii Instytut im. M.Skłodowskiej-Curie, Warszawa 2011
Google Scholar - 21. Djonov V., Cresto N., Aebersold D.M., Burri P.H., Altermatt H.J.,Hristic M., Berclaz G., Ziemiecki A., Andres A.C.: Tumor cell specificexpression of MMP-2 correlates with tumor vascularisation in breastcancer. Int. J. Oncol., 2002; 21: 25-30
Google Scholar - 22. Duvoix A., Blasius R., Delhalle S., Schnekenburger M., Morceau F.,Henry E., Dicato M., Diederich M.: Chemopreventive and therapeuticeffects of curcumin. Cancer Lett., 2005; 223: 181-190
Google Scholar - 23. Egeblad M., Werb Z.: New functions for the matrix metalloproteinasesin cancer progression. Nat. Rev. Cancer., 2002; 2: 161-174
Google Scholar - 24. Esatbeyoglu T., Huebbe P., Ernst I.M., Chin D., Wagner A.E., RimbachG.: Curcumin-from molecule to biological function. Angew.Chem. Int. Ed. Engl., 2012; 51: 5308-5332
Google Scholar - 25. Ferlay J., Shin H.R., Bray F., Forman D., Mathers C., Parkin D.M.:Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008.Int. J. Cancer, 2010; 127: 2893-2917
Google Scholar - 26. Fogg V.C., Lanning N.J., MacKeigan J.P.: Mitochondria in cancer:at the crossroads of life and death. Chin. J. Cancer, 2011; 30: 526-539
Google Scholar - 27. Gasparini G., Toi M., Gion M., Verderio P., Dittadi R., HanataniM., Matsubara I., Vinante O., Bonoldi E., Boracchi P., Gatti C., SuzukiH., Tominaga T.: Prognostic significance of vascular endothelialgrowth factor protein in node-negative breast carcinoma. J. Natl.Cancer Inst., 1997; 89: 139-147
Google Scholar - 28. Gasparini G., Toi M., Miceli R., Vermeulen P.B., Dittadi R., BiganzoliE., Morabito A., Fanelli M., Gatti C., Suzuki H., Tominaga T.,Dirix L.Y., Gion M.: Clinical relevance of vascular endothelial growthfactor and thymidine phosphorylase in patients with node-positivebreast cancer treated with either adjuvant chemotherapy or hormonetherapy. Cancer J. Sci. Am., 1999; 5: 101-111
Google Scholar - 29. Gupta S.G., Sung B., Kim J.H., Prasad S., Li S., Aggarwal B.B.: Multitargettingby tumeric, the golden spiece: from kitchen to clinic.Mol. Food Res., 2013; 57: 1510-1528
Google Scholar - 30. Harris S.L., Levine A.J.: The p53 pathway: positive and negativefeedback loops. Oncogene, 2005; 24: 2899-2908
Google Scholar - 31. Hassan Z.K., Daghestani M.H.: Curcumin effect on MMPs andTIMPs genes in a breast cancer cell line. Asian Pac. J. Cancer Prev.,2012; 13: 3259-3264
Google Scholar - 32. Hayden M.S., Ghosh S.: Shared principles in NF-κB signaling.Cell, 2008; 132: 344-362
Google Scholar - 33. Jacobson M.D.: Reactive oxygen species and programmed celldeath. Trends Biochem. Sci., 1996; 21: 83-86
Google Scholar - 34. Jithan A., Madhavi K., Madhavi M., Prabhakar K.: Preparationand characterization of albumin nanoparticles encapsulating curcuminintended for the treatment of breast cancer. Int. J. Pharm.Investig., 2011; 1: 119-125
Google Scholar - 35. John A., Tuszynski G.: The role of matrix metalloproteinasesin tumor angiogenesis and tumor metastasis. Pathol. Oncol. Res.,2001; 7: 14-23
Google Scholar - 36. Kamat A.M., Sethi G., Aggarwal B.B.: Curcumin potentiatesthe apoptotic effects of chemotherapeutic agents and cytokinesthrough down-regulation of nuclear factor-κB and nuclearfactor-κB-regulated gene products in IFN-α-sensitive and IFN-α-resistant human bladder cancer cells. Mol. Cancer Ther., 2007;6: 1022-1030
Google Scholar - 37. Kang J., Chen J., Shi Y., Jia J., Zhang Y.: Curcumin-induced histonehypoacetylation: the role of reactive oxygen species. Biochem.Pharmacol., 2005; 69: 1205-1213
Google Scholar - 38. Kieran M.W., Kalluri R., Cho Y.J.: The VEGF pathway in cancerand disease: responses, resistance, and the path forward. Cold SpringHarb. Perspect. Med., 2012; 2: a006593
Google Scholar - 39. Kohrmann A., Kammerer U., Kapp M., Dietl J., Anacker J.: Expressionof matrix metalloproteinases (MMPs) in primary human breastcancer and breast cancer cell lines: New findings and review of theliterature. BMC Cancer, 2009; 9: 188
Google Scholar - 40. Kopczyńska E., Makarewicz R., Tyrakowski T.: Rola angiopoetyn 1 i 2 w regulacji angiogenezy nowotworowej. Współcz. Onkol.,2007; 11: 350-354
Google Scholar - 41. Lai H.W., Chien S.Y., Kuo S.J., Tseng L.M., Lin H.Y., Chi C.W., ChenD.R.: The potential utility of curcumin in the treatment of HER-2-overexpressed breast cancer: an in vitro and in vivo comparisonstudy with herceptin. Evid. Based Complement. Alternat. Med.,2012; 2012: 486568
Google Scholar - 42. Lao C.D., Ruffin M.T., Normolle D., Heath D.D., Murray S.I., BaileyJ.M., Boggs M.E., Crowell J., Rock C.L., Brenner D.E.: Dose escalationof a curcuminoid formulation. BMC Complement. Altern.Med., 2006; 6: 10-14
Google Scholar - 43. Lee J., Im Y.H., Jung H.H., Kim J.H., Park J.O., Kim K., Kim W.S.,Ahn J.S., Jung C.W., Park Y.S., Kang W.K., Park K.: Curcumin inhibitsinterferon-α induced NF-κB and COX-2 in human A549 non-smallcell lung cancer cells. Biochem. Biophys. Res. Commun., 2005; 334:313-318
Google Scholar - 44. Lee K.H., Kim B.S., Keum K.S., You H.H., Kim Y.H., Chang B.S, RaJ.Y., Moon H.D., Seo B.R., Choi N.Y., You Y.O.: Essential oil of Curcumalonga inhibits Streptococcus mutans biofilm formation. J. Food Sci.,2011; 76: H226-H230
Google Scholar - 45. Lee K.W., Kim J.H., Lee H.J., Surh Y.J.: Curcumin inhibits phorbolester-induced up-regulation of cyclooxygenase-2 and matrix metalloproteinase-9by blocking ERK1/2 phosphorylation and NF-κBtranscriptional activity in MCF10A human breast epithelial cells.Antioxid. Redox Signal., 2005; 7: 1612-1620
Google Scholar - 46. Leppa S., Saarto T., Vehmanen L., Blomqvist C., Elomaa I.: A highserum matrix metalloproteinase-2 level is associated with an adverseprognosis in node-positive breast carcinoma. Clin. CancerRes., 2004; 10: 1057-1063
Google Scholar - 47. Leppert D., Lindberg R.L., Kappos L., Leib S.L.: Matrix metalloproteinases:multifunctional effectors of inflammation in multiplesclerosis and bacterial meningitis. Brain Res. Rev., 2001; 36: 249-257
Google Scholar - 48. Liotta L.A., Stetler-Stevenson W.G.: Tumor invasion and metastasis:an imbalance of of positive and negative regulation. CancerRes., 1991; 51: 5054s-5059s
Google Scholar - 49. Liu M., Sakamaki T., Casimiro M.C., Willmarth N.E., Quong A.A.,Ju X., Ojeifo J., Jiao X. Yeow W.S., Katiyar S., Shirley L.A., Joyce D.,Lisanti M.P., Albanese C., Pestell R.G.: The canonical NF-κB pathwaygoverns mammary tumorigenesis in transgenic mice and tumorstem cell expansion. Cancer Res., 2010; 70: 10464-10473
Google Scholar - 50. Liu X.H., Rose D.P.: Differential expression and regulation of cyclooxygenase-1and -2 in the human breast cancer cell lines. CancerRes., 1996; 56: 5125-5127
Google Scholar - 51. Luo J.L., Hideaki K., Karin M.: IKK/NF-κB signaling: balancinglife and death – a new approach to cancer therapy. J. Clin. Invest.,2005; 115: 2625-2632
Google Scholar - 52. Mahoney M.C., Bevers T., Linos E., Willett C.W.: Opportunitiesand strategies for breast cancer prevention through risk reduction.CA Cancer J. Clin., 2008; 58: 347-371
Google Scholar - 53. Mazhar D., Ang R., Waxman J.: COX inhibitors and breast cancer.Br. J. Cancer, 2006; 94: 346-350
Google Scholar - 54. Miłobędzka J., Kostanecki S., Lampe V.: Zur kenntnis des curcumins.Ber. Dtsch. Chem. Ges., 1910; 43: 2163-2170
Google Scholar - 55. Mulik R.S., Mönkkönen J., Juvonen R.O., Mahadik K.R., ParadkarA.R.: Transferrin mediated solid lipid nanoprticles containing curcumin:enhanced in vitro anticancer activity by induction of apoptosis.Int. J. Pharm., 2010; 398: 190-203
Google Scholar - 56. Nagase H.: Activation mechanisms of matrix metalloproteinases.Biol. Chem., 1997; 378: 151-160
Google Scholar - 57. Nagase H., Woessner J.F.Jr.: Matrix metalloproteinases. J. Biol.Chem., 1999; 274: 21491-21494
Google Scholar - 58. Niederau C., Gopfert E.: The effect of cheliodonium-and turmericroot extract on upper abdominal pain due to functional disorders ofthe biliary system. Results from a placebo-controlled double-blindstudy. Med. Klin., 1999; 94: 425-430
Google Scholar - 59. Ramachandran C., Rodrigues S., Ramachandran R., Raveendran NairP.K., Fonesca H., Khatib Z., Escalone E., Melnick S.J.: Expression profilesof apoptotic genes induces by curcumin in human breast cancer andmammary epithelial cell lines. Anticancer Res., 2005; 25: 3293-3302
Google Scholar - 60. Ramachandran C., You W.: Differential sensitivity of humanmammary epithelial and breast carcinoma cell lines to curcumin.Breast Cancer Res. Treat., 1999; 54: 269-278
Google Scholar - 61. Ristimaki A., Sivula J., Lundin J., Ristimaki A., Sivula A., LundinJ., Lundin M., Salminen T., Haglund C., Joensuu H., Isola J.: Prognosticsignificance of elevated cyclooxygenase-2 expression in breastcancer. Cancer Res., 2002; 62: 632-635
Google Scholar - 62. Rossouw J.E., Anderson G.L., Prentice R.L., LaCroix A.Z., KooperbergC., Stefanick M.L., Jackson R.D., Beresford S.A., Howard B.V., Johnson K.C.,Kotchen J.M., Ockene J.: Risks and benefits of estrogen plus progestin inhealthy postmenopausal women: principal results from the Women’sHealth Initiative randomized controlled trial. JAMA, 2002; 288: 321-333
Google Scholar - 63. Sa G., Das T.: Anti cancer effects of curcumin: cycle of life anddeath. Cell Div., 2008; 3: 14
Google Scholar - 64. Schindler R., Mentlein R.: Flavonoids and vitamin E reduce therelease of the angiogenic peptide vascular endothelial growth factorfrom human tumor cells. J. Nutr., 2006; 136: 1477-1482
Google Scholar - 65. Scientific opinion on the re-evaluation of curcumin (E 100) asa food additive. EFSA Journal, 2010; 8: 167
Google Scholar - 66. Screy M.P., Patel K.V.: Prostaglandin E2 production and metabolismin human breast cancer cells and breast fibroblasts. Regulationby inflammatory mediators. Br. J. Cancer, 1995; 72: 1412-1419
Google Scholar - 67. Shao Z.M., Shen Z.Z., Liu C.H., Sartippour M.R., Liang Go V., HerbertD., Nguyen M.: Curcumin exerts multiple suppressive effectson human breast carcinoma cells. Int. J. Cancer, 2002; 98: 234-240
Google Scholar - 68. Sheen-Chen S.M., Chen H.S., Eng H.L., Sheen C.C., Chen W.J.:Serum levels of matrix metalloproteinase 2 in patients with breastcancer. Cancer Lett., 2001; 173: 79-82
Google Scholar - 69. Shehzad A., Wahid F., Lee Y.S.: Curcumin in cancer chemoprevention:molecular targets, pharmacokinetics, bioavailability, andclinical trials. Arch. Pharm., 2010; 343: 489-499
Google Scholar - 70. Shishodia S., Potdar P., Gairola G.C., Aggarwal B.B.: Curcumin(diferuloylmethane) down-regulates cigarette smoke-induced NF-κBactivation through inhibition of IκBα kinase in human lung epithelialcells: correlation with suppression of COX-2, MMP-9 and cyclinD1. Carcinogenesis, 2003; 24: 1269-1279
Google Scholar - 71. Shostak K., Chariot A.: NF-κB, stem cells and breast cancer: thelinks get stronger. Breast Cancer Res., 2011; 13: 214
Google Scholar - 72. Sidhu G.S., Mani H., Gaddipati JP., Singh A. K., Seth P., BanaudhaK.K., Patnaik G.K., Srimal R.C., Maheshwari R.K.: Curcumin enhanceswound healing in streptozotocin induced diabetic rats and geneticallydiabetic mice. Wound Repair Regen., 1999; 7: 362-374
Google Scholar - 73. Śliwowska I., Kopczyński Z.: Metaloproteinazy macierzy zewną-trzkomórkowej – charakterystyka biochemiczna i kliniczna wartośćoznaczania u chorych na raka piersi. Współcz. Onkol., 2005; 9: 327-335
Google Scholar - 74. Somasundaram S., Edumnd N.A., Moore D.T., Small G.W., Shi Y.Y.,Orlowski R.Z.: Dietary curcumin inhibits chemotherapy-induced apoptosisin model of human breast cancer. Cancer Res., 2002; 62: 3868-3875
Google Scholar - 75. Surh Y.J., Chun K.S., Cha H.H., Han S.S., Keum Y.S., Park K.K.,Lee S.S.: Molecular mechanisms underlying chemopreventive activitiesof anti-inflammatory phytochemicals: down-regulation ofCOX-2 and iNOS through suppression of NF-κB activation. Mutat.Res., 2001; 480-481: 243-268
Google Scholar - 76. Syng-ai C., Kumari A.L., Khar A.: Effect of curcumin on normaland tumor cells: role of glutatione and bcl-2. Mol. Cancer Ther.,2004; 3: 1101-1108
Google Scholar - 77. Szczepański M.A., Grzanka A.: Chemoprewencyjne i przeciwnowotworowewłaściwości kurkuminy. Nowotwory. J. Oncol., 2009;59: 377-384
Google Scholar - 78. Talvensaari-Mattila A., Turpeenniemi-Hujanen T.: Preoperativeserum MMP-9 immunoreactive protein is a prognostic indicatorfor relapse-free survival in breast carcinoma. Cancer Lett.,2005; 217: 237-242
Google Scholar - 79. Wang X.: The expanding role of mitochondria in apoptosis.Genes. Dev., 2001; 15: 2922-2933
Google Scholar - 80. Wang Y.J., Pan M.H., Cheng A.L., Lin L.I., Ho Y.S., Hsieh C.Y.,Lin J.K.: Stability of curcumin in buffer solutions and characterizationof its degradation products. J. Pharm. Biomed. Anal., 1997; 15:1867-1876
Google Scholar - 81. Wojciechowska U., Didkowska J., Zatoński W.: Nowotwory zło-śliwe w Polsce w 2006 roku. Centrum Onkologii Instytut im. M.Skłodowskiej-Curie, Warszawa 2008
Google Scholar - 82. Yong V.W., Power C., Forsyth P., Edwards D.R.: Metalloproteinasesin biology and pathology of the nervous system. Nat. Rev. Neurosci.,2001; 2: 502-511
Google Scholar - 83. Yoshiji H., Gomez D., Shibuya U., Thorgeirsson U.P.: Expression ofvascular endothelial growth factor, its receptor, and other angiogenicfactors in human breast cancer. Cancer Res., 1996; 56: 2013-2016
Google Scholar - 84. Zografos G.C., Panou M., Panou N.: Common risk factors of breastand ovarian cancer: recent view. Int. J. Gynecol. Cancer, 2004; 14:721-740
Google Scholar