Suppression of inflammatory cascade is implicated in methyl amooranin-mediated inhibition of experimental mammary carcinogenesis

Molecular Carcinogenesis

Volumn 53, Issue 12, 2014, Pages 999-1010

  Mandal, Animesh ^a   Bhatia, Deepak ^a   Bishayee, Anupam ^b  

^a NORTHEAST OHIO MEDICAL UNIVERSITY   (United States)

^b American University of Health Sciences   (United States)

Author keywords

Breast tumor; COX 2; DMBA; HSP90; Inflammation; NF B; Oleanane triterpenoid

Indexed keywords

ANTINEOPLASTIC AGENT; CYCLOOXYGENASE 2; DIMETHYLBENZ[A]ANTHRACENE; HEAT SHOCK PROTEIN 90; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; METHYL AMOORANIN; TRITERPENOID; UNCLASSIFIED DRUG; ANTIINFLAMMATORY AGENT; I KAPPA B; METHYL 25-HYDROXY-3-OXOOLEAN-12-EN-28-OATE; NF-KAPPAB INHIBITOR ALPHA; OLEANOLIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BREAST CARCINOGENESIS; CANCER INHIBITION; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG SYNTHESIS; FEMALE; IMMUNOHISTOCHEMISTRY; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; BREAST NEOPLASMS; CARCINOGENESIS; CELL PROLIFERATION; CHEMOPROPHYLAXIS; DRUG EFFECTS; INFLAMMATION; MAMMARY NEOPLASMS, EXPERIMENTAL; METABOLISM; PROCEDURES; SPRAGUE DAWLEY RAT;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTICARCINOGENIC AGENTS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CARCINOGENESIS; CELL PROLIFERATION; CHEMOPREVENTION; CYCLOOXYGENASE 2; DOWN-REGULATION; FEMALE; HSP90 HEAT-SHOCK PROTEINS; I-KAPPA B PROTEINS; INFLAMMATION; MAMMARY NEOPLASMS, EXPERIMENTAL; NF-KAPPA B; OLEANOLIC ACID; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84911450432     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.22067     Document Type: Article

References (94)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61:69-90.
2. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013; 63:11-33.
3. Sagiv SK, Gaudet MM, Eng SM, et al. Polycyclic aromatic hydrocarbon-DNA adducts and survival among women with breast cancer. Environ Res 2009; 109:287-291.
4. Crujeiras AB, Díaz-Lagares A, Carreira MC, Amil M, Casanueva FF. Oxidative stress associated to dysfunctional adipose tissue: A potential link between obesity, type 2 diabetes mellitus and breast cancer. Free Radic Res 2013; 47:243-256.
5. Pierobon M, Frankenfeld CL. Obesity as a risk factor for triple-negative breast cancers: A systematic review and meta-analysis. Breast Cancer Res Treat 2013; 137:307-314.
6. Jia Y. Lu Y, Wu K, et al. Does night work increase the risk of breast cancer? A systematic review and meta-analysis of epidemiological studies. Cancer Epidemiol 2013; 37:196-206.
7. Jordan VC. Chemoprevention of breast cancer with selective oestrogen-receptor modulators. Nat Rev Cancer 2007; 7:46-53.
8. Castrellon AB, Glück S. Chemoprevention of breast cancer. Expert Rev Anticancer Ther 2008; 8:443-452.
9. Cazzaniga M, Bonanni B. Breast cancer chemoprevention: Old and new approaches. J Biomed Biotechnol 2012; 2012:985620.
10. Bozovic-Spasojevic I, Azambuja E, McCaskill-Stevens W, Dinh P, Cardoso F. Chemoprevention for breast cancer. Cancer Treat Rev 2012; 38:329-339.
11. Cuzick J, DeCensi A, Arun B, et al. Preventive therapy for breast cancer: A consensus statement. Lancet Oncol 2011; 12:496-503.
12. Geldenhuys WJ, Bishayee A, Darvesh AS, Carroll RT. Natural products of dietary origin as lead compounds in virtual screening and drug design. Curr Pharm Biotechnol 2012; 13:117-124.
13. Cragg GM, Newman DJ. Natural products: A continuing source of novel drug leads. Biochim Biophys Acta 2013; 1830:3670-3695.
14. Adams LS, Chen S. Phytochemicals for breast cancer prevention by targeting aromatase. Front Biosci 2009; 14:3846-3863.
15. Sinha D, Biswas J, Sung B, Aggarwal BB, Bishayee A. Chemopreventive and chemotherapeutic potential of curcumin in breast cancer. Curr Drug Targets 2012; 13:1799-1819.
16. Reuben SC, Gopalan A, Petit DM, Bishayee A. Modulation of angiogenesis by dietary phytoconstituents in the prevention and intervention of breast cancer. Mol Nutr Food Res 2012; 56:14-29.
17. Vadodkar AS, Suman S, Lakshmanaswamy R, Damodaran C. Chemoprevention of breast cancer by dietary compounds. Anticancer Agents Med Chem 2012; 12:1185-1202.
18. Biersack B, Schobert R. Indole compounds against breast cancer: Recent developments. Curr Drug Targets 2012; 13:1705-1719.
19. Aiyer HS, Warri AM, Woode DR, Hilakivi-Clarke L, Clarke R. Influence of berry polyphenols on receptor Signaling and cell-death pathways: Implications for breast cancer prevention. J Agric Food Chem 2012; in press, PMID: 22300613.
20. You L, An R, Liang K, Wang X. Anti-breast cancer agents from Chinese herbal medicines. Mini Rev Med Chem 2013; 13:101-105.
21. Kado K, Forsyth A, Patel PR, Schwartz JA. Dietary supplements and natural products in breast cancer trials. Front Biosci 2012; 4:546-567.
22. Connolly JD, Hill RA. Triterpenoids. Nat Prod Rep 2010; 27:79-132.
23. Liby KT, Yore MM, Sporn MB. Triterpenoids and rexinoids as multifunctional agents for the prevention and treatment of cancer. Nat Rev Cancer 2007; 7:357-369.
24. Petronelli A, Pannitteri G, Testa U. Triterpenoids as new promising anticancer drugs. Anticancer Drugs 2009; 20:880-892.
25. Yadav VR, Prasad S, Sung B, Kannappan R, Aggarwal BB. Targeting inflammatory pathways by triterpenoids for prevention and treatment of cancer. Toxins 2010; 2:2428-2466.
26. Bishayee A, Ahmed S, Brankov N, Perloff M. Triterpenoids as potential agents for the chemoprevention and therapy of breast cancer. Front Biosci 2011; 16:980-996.
27. Liu J. Oleanolic acid and ursolic acid: Research perspectives. J Ethnopharmacol 2005; 100:92-94.
28. Sultana N, Ata A. Oleanolic acid and related derivatives as medicinally important compounds. J Enzyme Inhib Med Chem 2008; 23:739-756.
29. Ovesná Z, Vachálková A, Horváthová K, Tóthová D. Pentacyclic triterpenoic acids: New chemoprotective compounds. Neoplasma 2004; 51:327-333.
30. Laszczyk MN. Pentacyclic triterpenes of the lupane, oleanane and ursane group as tools in cancer therapy. Planta Med 2009; 75:1549-1560.
31. Shanmugam MK, Nguyen AH, Kumar AP, Tan BK, Sethi G. Targeted inhibition of tumor proliferation, survival, and metastasis by pentacyclic triterpenoids: Potential role in prevention and therapy of cancer. Cancer Lett 2012; 320:158-170.
32. Sporn MB, Liby KT, Yore MM, Fu L, Lopchuk JM, Gribble GW. New synthetic triterpenoids: Potent agents for prevention and treatment of tissue injury caused by inflammatory and oxidative stress. J Nat Prod 2011; 74:537-545.
33. Liby KT, Sporn MB. Synthetic oleanane triterpenoids: Multifunctional drugs with a broad range of applications for prevention and treatment of chronic disease. Pharmacol Rev 2012; 64:972-1003.
34. Rabi T. Antitumor activity of amooranin from Amoora rohituka stem bark. Curr Sci 1996; 70:80-81.
35. Rabi T, Karunagaram D, Nair MK, Bhattathiri VN. Cytotoxic activity of amooranin and its derivatives. Phytother Res 2002; 16:S84-S86.
36. Rabi T, Ramachandran C, Fonseca HB, et al. Novel drug amooranin induces apoptosis through caspase activity in human breast carcinoma cell lines. Breast Cancer Res Treat 2003; 80:321-330.
37. Rabi T, Wang L, Banerjee S. Novel triterpenoid 25-hydroxy-3-oxoolean-12-en-28-oic acid induces growth arrest and apoptosis in breast cancer cells. Breast Cancer Res Treat 2007; 101:27-36.
38. Ramachandran C, Rabi T, Fonseca HB, Melnick SJ, Escalon EA. Novel plant triterpenoid drug amooranin overcomes multidrug resistance in human leukemia and colon carcinoma cell lines. Int J Cancer 2003; 105:784-789.
39. Ramachandran C, Nair PK, Alamo A, Cochrane CB, Escalon E, Melnick SJ. Anticancer effects of amooranin in human colon carcinoma cell line in vitro and in nude mice xenografts. Int J Cancer 2006; 119:2443-2454.
40. Rabi T, Banerjee S. Novel synthetic triterpenoid methyl 25-hydroxy-3-oxoolean-12-en-28-oate induces apoptosis through JNK and p38 MAPK pathways in human breast adenocarcinoma MCF-7 cells. Mol Carcinog 2008; 47:415-423.
41. Rabi T, Banerjee S. Novel semisynthetic triterpenoid AMR-Me inhibits telomerase activity in human leukemic CEM cells and exhibits in vivo antitumor activity against Dalton's lymphoma ascites tumor. Cancer Lett 2009; 278:156-163.
42. Rabi T, Huwiler A, Zangemeister-Wittke U. AMR-Me inhibits PI3K/Akt signaling in hormone-dependent MCF-7 breast cancer cells and inactivates NF-κB in hormone-independent MDA-MB-231 cells. Mol Carcinog 2013; in press, PMID: 23475563.
43. Bishayee A, Mandal A, Thoppil RJ, Darvesh AS, Bhatia D. Chemopreventive effect of a novel oleanane triterpenoid in a chemically induced rodent model of breast cancer. Int J Cancer 2013; 133:1054-1064.
44. Costa I, Solanas M, Escrich E. Histopathological characterization of mammary neoplastic lesions induced with 7, 12-dimethylbenz(a)anthracene in the rat: A comparative analysis with human breast tumors. Arch Pathol Lab Med 2002; 126:915-927.
45. Witty JP, Cempka T, Coffe RJ, Jr Matrisian LM. Decreases tumor formation in 7, 12-dimethylbenz(a)anthracene-treated stromelysin-1 transgenic mice is associated with alterations in mammary epithelial cells apoptosis. Cancer Res 1995; 55:1401-1406.
46. Macciò A, Madeddu C. Obesity, inflammation, and postmenopausal breast cancer: Therapeutic implications. ScientificWorldJournal 2011; 11:2020-2036.
47. Shostak K, Chariot A. NF-κB, stem cells and breast cancer: The links get stronger. Breast Cancer Res 2011; 13:214.
48. Baumgarten SC, Frasor J, Minireview: Inflammation: An instigator of more aggressive estrogen receptor (ER) positive breast cancers. Mol Endocrinol 2012; 26:360-371.
49. Bishayee A, Thoppil RJ, Mandal A, et al. Black currant phytoconstituents exert chemoprevention of diethylnitrosamine-initiated hepatocarcinogenesis by suppression of the inflammatory response. Mol Carcinog 2013; 52:304-317.
50. Rozen S. Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, editors. Bioinformatics methods and protocols: Methods in molecular biology. Totowa, NJ: Humana Press; 2000. pp. 365-386.
51. Pick E, Kluger Y, Giltnane JM, et al. High HSP90 expression is associated with decreased survival in breast cancer. Cancer Res 2007; 67:2932-2937.
52. Cheng Q, Chang JT, Geradts J, et al., Amplification and high-level expression of heat shock protein 90 marks aggressive phenotypes of human epidermal growth factor receptor 2 negative breast cancer. Breast Cancer Res 2012; 14:R62.
53. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008; 454:436-444.
54. Chaturvedi MM, Sung B, Yadav VR, Kannappan R, Aggarwal BB. NF-κB addiction and its role in cancer: 'One size does not fit all'. Oncogene 2011; 30:1615-1630.
55. Kim YS, Young MR, Bobe G, Colburn NH, Milner JA. Bioactive food components, inflammatory targets, and cancer prevention. Cancer Prev Res 2009; 2:200-208.
56. Gupta SC, Kim JH, Prasad S, Aggarwal BB. Regulation of survival, proliferation, invasion, angiogenesis, and metastasis of tumor cells through modulation of inflammatory pathways by nutraceuticals. Cancer Metastasis Rev 2010; 29:405-434.
57. Aravindaram K, Yang NS. Anti-inflammatory plant natural products for cancer therapy. Planta Med 2010; 76:1103-1117.
58. Singh-Ranger G, Salhab M, Mokbel K. The role of cyclooxygenase-2 in breast cancer: Review. Breast Cancer Res Treat 2008; 109:189-198.
59. Howe LR. Inflammation and breast cancer. Cyclooxygenase/prostaglandin signaling and breast cancer. Breast Cancer Res 2007; 9:210.
60. Harris RE. Cyclooxygenase-2 (cox-2) blockade in the chemoprevention of cancers of the colon, breast, prostate, and lung. Inflammopharmacology 2009; 17:55-567.
61. Zhao Y, Agarwal VR, Mendelson CR, Simpson ER. Estrogen biosynthesis proximal to a breast tumor is stimulated by PGE2 via cyclic AMP, leading to activation of promoter II of the CYP19 (aromatase) gene. Endocrinology 1996; 137:5739-5742.
62. Glover JA, Hughes CM, Cantwell MM, Murray LJ. A systematic review to establish the frequency of cyclooxygenase-2 expression in normal breast epithelium, ductal carcinoma in situ, microinvasive carcinoma of the breast and invasive breast cancer. Br J Cancer 2011; 105:13-17.
63. Takkouche B, Regueira-Méndez C, Etminan M. Breast cancer and use of nonsteroidal anti-inflammatory drugs: A meta-analysis. J Natl Cancer Inst 2008; 100:1439-1447.
64. Suzui N, Sugie S, Rahman KM, et al. Inhibitory effects of diallyl disulfide or aspirin on 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine-induced mammary carcinogenesis in rats. Jpn J Cancer Res 1997; 88:705-711.
65. Nakatsugi S, Ohta T, Kawamori T, et al. Chemoprevention by nimesulide, a selective cyclooxygenase-2 inhibitor, of 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine (PhIP)-induced mammary gland carcinogenesis in rats. Jpn J Cancer Res 2000; 91:886-892.
66. Harris RE, Alshafie GA, Abou-Issa H, Seibert K. Chemoprevention of breast cancer in rats by celecoxib, a cyclooxygenase 2 inhibitor. Cancer Res 2000; 60:2101-2103.
67. Kubatka P, Ahlers I, Ahlersová E, et al. Chemoprevention of mammary carcinogenesis in female rats by rofecoxib. Cancer Lett 2003; 202:131-136.
68. Shou M, Korzekwa KR, Krausz KW, et al. Specificity of cDNA-expressed human and rodent cytochrome P450s in the oxidative metabolism of the potent carcinogen 7, 12-dimethylbenz[a]anthracene. Mol Carcinog 1996; 17:241-249.
69. Garcia Rodriguez LA, Cea-Soriano L, Tacconelli S, Patrignani P. Coxibs: Pharmacology, toxicity and efficacy in cancer clinical trials. Recent Results Cancer Res 2013; 191:67-93.
70. Roubille C, Martel-Pelletier J, Davy JM, Haraoui B, Pelletier JP. Cardiovascular adverse effects of anti-inflammatory drugs. Antiinflamm Antiallergy Agents Med Chem 2013; 12:55-67.
71. Kampinga HH, Hageman J, Vos MJ, et al. Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 2009; 14:105-111.
72. Calderwood SK, Gong J. Molecular chaperons in mammary cancer growth and breast tumor therapy. J Cell Biochem 2012; 113:1096-1103.
73. Shimp SK 3rd, Parson CD, Regna NL, et al. HSP90 inhibition by 17-DMAG reduces inflammation in J774 macrophages through suppression of Akt and nuclear factor-κB pathways. Inflamm Res 2012; 61:521-533.
74. Tamura Y, Torigoe T, Kutomi G, Hirata K, Sato N. New paradigm for intrinsic function of heat shock proteins as endogenous ligands in inflammation and innate immunity. Curr Mol Med 2012; 12:1198-1206.
75. Kumar P, Kolls JK. Act1-hsp90 heats up TH17 inflammation. Nat Immunol 2013; 14:16-17.
76. Ciocca DR, Calderwood SK. Heat shock proteins in cancer: Diagnostic prognostic, predictive, and treatment implications. Cell Stress Chaperon 2005; 10:86-103.
77. Calderwood SK. Heat shock proteins in breast cancer progression-A suitable case for treatment? Int J Hyperthermia 2010; 26:681-685.
78. Ciocca DR, Arrigo AP, Calderwood SK. Heat shock proteins and heat shock factor 1 in carcinogenesis and tumor development: An update. Arch Toxicol 2013; 87:19-48.
79. Trepel J, Mollapour M, Giaccone G, Neckers L. Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer 2010; 10:537-549.
80. Sankhala KK, Mita MM, Mita AC, Takimoto CH. Heat shock proteins: A potential anticancer target. Curr Drug Targets 2011; 12:2001-2008.
81. Barrott JJ, Haystead TA, Hsp90, an unlikely ally in the war on cancer. FEBS J 2013; 280:1381-1396.
82. Park K, Choi K, Kim H, et al. Isoflavone-deprived soy peptide suppresses mammary tumorigenesis by inducing apoptosis. Exp Mol Med 2009; 41:371-381.
83. Ono N, Yamazaki T, Nakanishi Y, et al. Preclinical antitumor activity of the novel heat shock protein 90 inhibitor CH5164840 against human epidermal growth factor receptor 2 (HER2)-overexpressing cancers. Cancer Sci 2012; 103:342-349.
84. Ghosh S, Karin M. Missing pieces in the NF-κB puzzle. Cell 2002; 109:S81-S96.
85. Zubair A, Frieri M. Role of nuclear factor-κB in breast and colorectal cancer. Curr Allergy Asthma Rep 2013; 13:44-49.
86. Sovak MA, Bellas RE, Kim DW, et al. Aberrant nuclear factor-kappaB/Rel expression and the pathogenesis of breast cancer. J Clin Invest 1997; 100:2952-2960.
87. Huber MA, Azoitei N, Baumann B, et al. NF-kappaB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression. Clin Invest 2004; 114:569-581.
88. Cogswell PC, Guttridge DC, Funkhouser WK. Baldwin AS Jr. Selective activation of NF-kappa B subunits in human breast cancer: Potential roles for NF-kappa B2/p52 and for Bcl-3. Oncogene 2000; 19:1123-1131.
89. Jana D, Das S, Sarkar DK, Mandal S, Maji A, Mukhopadhyay M. Role of nuclear factor-κB in female breast cancer: A study in Indian patients. Asian Pac J Cancer Prev 2012; 13:5511-5515.
90. Sethi G, Sung B, Aggarwal BB. Nuclear factor-kappaB activation: From bench to bedside. Exp Biol Med 2008; 233:21-31.
91. Ralhan R, Pandey MK, Aggarwal BB. Nuclear factor-kappaB links carcinogenic and chemopreventive agents. Front Biosci 2009; 1:45-60.
92. Kim DW, Sovak MA, Zanieski G, et al. Activation of NF-kappaB/Rel occurs early during neoplastic transformation of mammary cells. Carcinogenesis 2000; 21:871-879.
93. Broemer M, Krappmann D, Scheidereit C. Requirement of Hsp90 activity for IkappaB kinase (IKK) biosynthesis and for constitutive and inducible IKK and NF-kappaB activation. Oncogene 2004; 23:5378-5386.
94. Salminen A, Paimela T, Suuronen T, Kaarniranta K. Innate immunity meets with cellular stress at the IKK complex: Regulation of the IKK complex by HSP70 and HSP90. Immunol Lett 2008; 117:9-15.