Characterization of synergistic anti-cancer effects of docosahexaenoic acid and curcumin on DMBA-induced mammary tumorigenesis in mice

BMC Cancer

Volumn 13, Issue , 2013, Pages

  Siddiqui, Rafat A ^a,b,c   Harvey, Kevin A ^a,b   Walker, Candace ^a,b   Altenburg, Jeffrey ^a,b   Xu, Zhidong ^a,b   Terry, Colin ^b   Camarillo, Ignacio ^d   Jones Hall, Yava ^e   Mariash, Cary ^b,c  

^a INDIANA UNIVERSITY HEALTH   (United States)

^b METHODIST RESEARCH INSTITUTE   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d PURDUE UNIVERSITY   (United States)

^e PURDUE UNIVERSITY   (United States)

Author keywords

Breast cancer; Cancer cell differentiation; In vivo studies; Maspin; Survivin; Tumor growth; Tumor incidence

Indexed keywords

CURCUMIN; DOCOSAHEXAENOIC ACID; MASPIN; SURVIVIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER GROWTH; CANCER PREVENTION; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; FEMALE; GENE EXPRESSION; IMMUNOHISTOLOGY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; WESTERN BLOTTING;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CLUSTER ANALYSIS; CURCUMIN; DIET; DOCOSAHEXAENOIC ACIDS; DRUG SYNERGISM; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; INHIBITOR OF APOPTOSIS PROTEINS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; RECEPTOR, ERBB-2; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; SERPINS; TUMOR BURDEN; TUMOR MICROENVIRONMENT;

EID: 84883696280     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-13-418     Document Type: Article

References (89)

1. Saw CL, Huang Y, Kong AN. Synergistic anti-inflammatory effects of low doses of curcumin in combination with polyunsaturated fatty acids: docosahexaenoic acid or eicosapentaenoic acid. Biochem Pharmacol 2010, 79:421-430. 10.1016/j.bcp.2009.08.030, 19744468.
2. Swamy MV, Citineni B, Patlolla JM, Mohammed A, Zhang Y, Rao CV. Prevention and treatment of pancreatic cancer by curcumin in combination with omega-3 fatty acids. Nutr Cancer 2008, 60(Suppl 1):81-89.
3. Cheah YH, Nordin FJ, Sarip R, Tee TT, Azimahtol HL, Sirat HM, Rashid BA, Abdullah NR, Ismail Z. Combined xanthorrhizol-curcumin exhibits synergistic growth inhibitory activity via apoptosis induction in human breast cancer cells MDA-MB-231. Cancer Cell Int 2009, 9:1. 10.1186/1475-2867-9-1, 2630298, 19118501.
4. Berg JP, Glattre E, Haldorsen T, Hostmark AT, Bay IG, Johansen AF, Jellum E. Longchain serum fatty acids and risk of thyroid cancer: a population-based case-control study in Norway. Cancer Causes Control 1994, 5:433-439. 10.1007/BF01694757, 7999965.
5. Schloss I, Kidd MS, Tichelaar HY, Young GO, O'Keefe SJ. Dietary factors associated with a low risk of colon cancer in coloured west coast fishermen. S Afr Med J 1997, 87:152-158.
6. Kaizer L, Boyd NF, Kriukov V, Tritchler D. Fish consumption and breast cancer risk: an ecological study. Nutr Cancer 1989, 12:61-68. 10.1080/01635588909514002, 2710648.
7. Vogel VG, McPherson RS. Dietary epidemiology of colon cancer. Hematol Oncol Clin North Am 1989, 3:35-63.
8. Connolly JM, Gilhooly EM, Rose DP. Effects of reduced dietary linoleic acid intake, alone or combined with an algal source of docosahexaenoic acid, on MDA-MB-231 breast cancer cell growth and apoptosis in nude mice. Nutr Cancer 1999, 35:44-49. 10.1207/S1532791444-49, 10624705.
9. Rose DP, Connolly JM, Coleman M. Effect of omega-3 fatty acids on the progression of metastases after the surgical excision of human breast cancer cell solid tumors growing in nude mice. Clin Cancer Res 1996, 2:1751-1756.
10. Rose DP, Connolly JM. Antiangiogenicity of docosahexaenoic acid and its role in the suppression of breast cancer cell growth in nude mice. Int J Oncol 1999, 15:1011-1015.
11. Ghumare SS, Cunningham JE. Breast cancer trends in Indian residents and emigrants portend an emerging epidemic for India. Asian Pac J Cancer Prev 2007, 8:507-512.
12. Choudhuri T, Pal S, Das T, Sa G. Curcumin selectively induces apoptosis in deregulated cyclin D1-expressed cells at G2 phase of cell cycle in a p53-dependent manner. J Biol Chem 2005, 280:20059-20068. 10.1074/jbc.M410670200, 15738001.
13. Perkins S, Verschoyle RD, Hill K, Parveen I, Threadgill MD, Sharma RA, Williams ML, Steward WP, Gescher AJ. Chemopreventive efficacy and pharmacokinetics of curcumin in the min/+ mouse, a model of familial adenomatous polyposis. Cancer Epidemiol Biomarkers Prev 2002, 11:535-540.
14. Chen A, Xu J, Johnson AC. Curcumin inhibits human colon cancer cell growth by suppressing gene expression of epidermal growth factor receptor through reducing the activity of the transcription factor Egr-1. Oncogene 2006, 25:278-287.
15. Huang MT, Lou YR, Ma W, Newmark HL, Reuhl KR, Conney AH. Inhibitory effects of dietary curcumin on forestomach, duodenal, and colon carcinogenesis in mice. Cancer Res 1994, 54:5841-5847.
16. Singh SV, Hu X, Srivastava SK, Singh M, Xia H, Orchard JL, Zaren HA. Mechanism of inhibition of benzo[a]pyrene-induced forestomach cancer in mice by dietary curcumin. Carcinogenesis 1998, 19:1357-1360. 10.1093/carcin/19.8.1357, 9744529.
17. Dorai T, Dutcher JP, Dempster DW, Wiernik PH. Therapeutic potential of curcumin in prostate cancer-V: Interference with the osteomimetic properties of hormone refractory C4-2B prostate cancer cells. Prostate 2004, 60:1-17. 10.1002/pros.10359, 15129424.
18. Cui X, Schiff R, Arpino G, Osborne CK, Lee AV. Biology of progesterone receptor loss in breast cancer and its implications for endocrine therapy. J Clin Oncol 2005, 23:7721-7735. 10.1200/JCO.2005.09.004, 16234531.
19. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 2001, 98:10869-10874. 10.1073/pnas.191367098, 58566, 11553815.
20. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, et al. Molecular portraits of human breast tumours. Nature 2000, 406:747-752. 10.1038/35021093, 10963602.
21. Prat A, Perou CM. Deconstructing the molecular portraits of breast cancer. Mol Oncol 2011, 5:5-23. 10.1016/j.molonc.2010.11.003, 21147047.
22. Prat A, Ellis MJ, Perou CM. Practical implications of gene-expression-based assays for breast oncologists. Nat Rev Clin Oncol 2011, 9:48-57. 10.1038/nrclinonc.2011.178, 3703639, 22143140.
23. Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, Davies S, Fauron C, He X, Hu Z, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 2009, 27:1160-1167. 10.1200/JCO.2008.18.1370, 2667820, 19204204.
24. Pusztai L, Mazouni C, Anderson K, Wu Y, Symmans WF. Molecular classification of breast cancer: limitations and potential. Oncologist 2006, 11:868-877. 10.1634/theoncologist.11-8-868, 16951390.
25. Cardiff RD, Anver MR, Gusterson BA, Hennighausen L, Jensen RA, Merino MJ, Rehm S, Russo J, Tavassoli FA, Wakefield LM, et al. The mammary pathology of genetically engineered mice: the consensus report and recommendations from the Annapolis meeting. Oncogene 2000, 19:968-988. 10.1038/sj.onc.1203277, 10713680.
26. Weigelt B, Baehner FL, Reis-Filho JS. The contribution of gene expression profiling to breast cancer classification, prognostication and prediction: a retrospective of the last decade. J Pathol 2010, 220:263-280.
27. Heppner GH, Wolman SR. MCF-10AT: a model for human breast cancer development. Breast J 1999, 5:122-129. 10.1046/j.1524-4741.1999.00136.x, 11348271.
28. Shekhar PV, Chen ML, Werdell J, Heppner GH, Miller FR, Christman JK. Transcriptional activation of functional endogenous estrogen receptor gene expression in MCF10AT cells: a model for early breast cancer. Int J Oncol 1998, 13:907-915.
29. Subik K, Lee JF, Baxter L, Strzepek T, Costello D, Crowley P, Xing L, Hung MC, Bonfiglio T, Hicks DG, Tang P. The expression patterns of ER, PR, HER2, CK5/6, EGFR, Ki-67 and AR by immunohistochemical analysis in breast cancer cell lines. Breast Cancer (Auckl) 2010, 4:35-41.
30. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, Clark L, Bayani N, Coppe J-P, Tong F, et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes.[see comment]. Cancer Cell 2006, 10:515-527. 10.1016/j.ccr.2006.10.008, 2730521, 17157791.
31. Tallarida RJ, Stone DJ, Raffa RB. Efficient designs for studying synergistic drug combinations. Life Sci 1997, 61:417-425.
32. Altenburg JD, Bieberich AA, Terry C, Harvey KA, Vanhorn JF, Xu Z, Jo Davisson V, Siddiqui RA. A synergistic antiproliferation effect of curcumin and docosahexaenoic acid in SK-BR-3 breast cancer cells: unique signaling not explained by the effects of either compound alone. BMC Cancer 2011, 11:149. 10.1186/1471-2407-11-149, 3111403, 21510869.
33. Yager JD. Endogenous estrogens as carcinogens through metabolic activation. J Natl Cancer Inst Monogr 2000, 27:67-73.
34. Bendsen NT, Stender S, Szecsi PB, Pedersen SB, Basu S, Hellgren LI, Newman JW, Larsen TM, Haugaard SB, Astrup A. Effect of industrially produced trans fat on markers of systemic inflammation: evidence from a randomized trial in women. J Lipid Res 2011, 52:1821-1828. 10.1194/jlr.M014738, 3173005, 21795740.
35. Mense SM, Chhabra J, Bhat HK. Preferential induction of cytochrome P450 1A1 over cytochrome P450 1B1 in human breast epithelial cells following exposure to quercetin. J Steroid Biochem Mol Biol 2008, 110:157-162. 10.1016/j.jsbmb.2008.03.029, 2533731, 18456490.
36. Potter GA, Patterson LH, Wanogho E, Perry PJ, Butler PC, Ijaz T, Ruparelia KC, Lamb JH, Farmer PB, Stanley LA, Burke MD. The cancer preventative agent resveratrol is converted to the anticancer agent piceatannol by the cytochrome P450 enzyme CYP1B1. Br J Cancer 2002, 86:774-778. 10.1038/sj.bjc.6600197, 2375304, 11875742.
37. Androutsopoulos VP, Ruparelia K, Arroo RR, Tsatsakis AM, Spandidos DA. CYP1-mediated antiproliferative activity of dietary flavonoids in MDA-MB-468 breast cancer cells. Toxicol 2009, 264:162-170.
38. Androutsopoulos VP, Mahale S, Arroo RR, Potter G. Anticancer effects of the flavonoid diosmetin on cell cycle progression and proliferation of MDA-MB 468 breast cancer cells due to CYP1 activation. Oncol Rep 2009, 21:1525-1528.
39. Jernstrom H, Henningson M, Johansson U, Olsson H. Coffee intake and CYP1A2*1F genotype predict breast volume in young women: implications for breast cancer. Br J Cancer 2008, 99:1534-1538. 10.1038/sj.bjc.6604687, 2579678, 18813311.
40. Khalkhali-Ellis Z, Christian AL, Kirschmann DA, Edwards EM, Rezaie-Thompson M, Vasef MA, Gruman LM, Seftor RE, Norwood LE, Hendrix MJ. Regulating the tumor suppressor gene maspin in breast cancer cells: a potential mechanism for the anticancer properties of tamoxifen. Clin Cancer Res 2004, 10:449-454. 10.1158/1078-0432.CCR-1002-03, 14760064.
41. Fukuda S, Pelus LM. Survivin, a cancer target with an emerging role in normal adult tissues. Mol Cancer Ther 2006, 5:1087-1098. 10.1158/1535-7163.MCT-05-0375, 16731740.
42. Medina D, Lane HW, Shepherd F. Effect of dietary selenium levels on 7,12-dimethylbenzanthracene-induced mouse mammary tumorigenesis. Carcinogenesis 1983, 4:1159-1163. 10.1093/carcin/4.9.1159, 6411377.
43. Lane HW, Butel JS, Howard C, Shepherd F, Halligan R, Medina D. The role of high levels of dietary fat in 7,12-dimethylbenzanthracene-induced mouse mammary tumorigenesis: lack of an effect on lipid peroxidation. Carcinogenesis 1985, 6:403-407. 10.1093/carcin/6.3.403, 3919956.
44. Plante I, Stewart MK, Laird DW. Evaluation of mammary gland development and function in mouse models. J Vis Exp 2011, 53:e2828.
45. Dunn TB. The Pathophysiology of Cancer 1959, New York: Hoeber-Harper, 2.
46. Creighton CJ. The molecular profile of luminal B breast cancer. Biologics 2012, 6:289-297. 3430090, 22956860.
47. Hoadley KA, Weigman VJ, Fan C, Sawyer LR, He X, Troester MA, Sartor CI, Rieger-House T, Bernard PS, Carey LA, Perou CM. EGFR associated expression profiles vary with breast tumor subtype. BMC Genomics 2007, 8:258. 10.1186/1471-2164-8-258, 2014778, 17663798.
48. Cragg GM, Newman DJ, Snader KM. Natural products in drug discovery and development. J Nat Prod 1997, 60:52-60. 10.1021/np9604893, 9014353.
49. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126(4):663-676. 10.1016/j.cell.2006.07.024, 16904174.
50. Fischer SM, Conti CJ, Locniskar M, Belury MA, Maldve RE, Lee ML, Leyton J, Slaga TJ, Bechtel DH. The effect of dietary fat on the rapid development of mammary tumors induced by 7,12-dimethylbenz(a)anthracene in SENCAR mice. Cancer Res 1992, 52:662-666.
51. Wurz GT, Read KC, Marchisano-Karpman C, Gregg JP, Beckett LA, Yu Q, Degregorio MW. Ospemifene inhibits the growth of dimethylbenzanthracene-induced mammary tumors in Sencar mice. J Steroid Biochem Mol Biol 2005, 97:230-240. 10.1016/j.jsbmb.2005.06.027, 16153821.
52. Wang Y, Huang S, Sah VP, Ross J, Brown JH, Han J, Chien KR. Cardiac muscle cell hypertrophy and apoptosis induced by distinct members of the p38 mitogen-activated protein kinase family. J Biol Chem 1998, 273:2161-2168. 10.1074/jbc.273.4.2161, 9442057.
53. Herschkowitz JI, Simin K, Weigman VJ, Mikaelian I, Usary J, Hu Z, Rasmussen KE, Jones LP, Assefnia S, Chandrasekharan S, et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol 2007, 8:R76. 10.1186/gb-2007-8-5-r76, 1929138, 17493263.
54. McCord A, Burnett AK, Wolf CR, Morrison V, Craft JA. Role of specific cytochrome P-450 isoenzymes in the regio-selective metabolism of 7,12-dimethylbenz[a]anthracene in microsomes from rats treated with phenobarbital or Sudan III. Carcinogenesis 1988, 9:1485-1491. 10.1093/carcin/9.8.1485, 3135957.
55. Mukhopadhyay A, Basu N, Ghatak N, Gujral PK. Anti-inflammatory and irritant activities of curcumin analogues in rats. Agents Actions 1982, 12:508-515. 10.1007/BF01965935, 7180736.
56. Schlezinger JJ, Liu D, Farago M, Seldin DC, Belguise K, Sonenshein GE, Sherr DH. A role for the aryl hydrocarbon receptor in mammary gland tumorigenesis. Biol Chem 2006, 387:1175-1187.
57. Nishiumi S, Yoshida K, Ashida H. Curcumin suppresses the transformation of an aryl hydrocarbon receptor through its phosphorylation. Arch Biochem Biophys 2007, 466:267-273. 10.1016/j.abb.2007.08.007, 17880909.
58. Owens DW, Lane EB. The quest for the function of simple epithelial keratins. Bioessays 2003, 25:748-758. 10.1002/bies.10316, 12879445.
59. Becker M, Nitsche A, Neumann C, Aumann J, Junghahn I, Fichtner I. Sensitive PCR method for the detection and real-time quantification of human cells in xenotransplantation systems. Br J Cancer 2002, 87:1328-1335. 10.1038/sj.bjc.6600573, 2408903, 12439725.
60. Schaller G, Fuchs I, Pritze W, Ebert A, Herbst H, Pantel K, Weitzel H, Lengyel E. Elevated keratin 18 protein expression indicates a favorable prognosis in patients with breast cancer. Clin Cancer Res 1996, 2:1879-1885.
61. Thompson EW, Paik S, Brunner N, Sommers CL, Zugmaier G, Clarke R, Shima TB, Torri J, Donahue S, Lippman ME, et al. Association of increased basement membrane invasiveness with absence of estrogen receptor and expression of vimentin in human breast cancer cell lines. J Cell Physiol 1992, 150:534-544. 10.1002/jcp.1041500314, 1537883.
62. Sommers CL, Byers SW, Thompson EW, Torri JA, Gelmann EP. Differentiation state and invasiveness of human breast cancer cell lines. Breast Cancer Res Treat 1994, 31:325-335. 10.1007/BF00666165, 7881109.
63. Sommers CL, Heckford SE, Skerker JM, Worland P, Torri JA, Thompson EW, Byers SW, Gelmann EP. Loss of epithelial markers and acquisition of vimentin expression in adriamycin- and vinblastine-resistant human breast cancer cell lines. Cancer Res 1992, 52:5190-5197.
64. Buhler H, Schaller G. Transfection of keratin 18 gene in human breast cancer cells causes induction of adhesion proteins and dramatic regression of malignancy in vitro and in vivo. Mol Cancer Res 2005, 3:365-371. 10.1158/1541-7786.MCR-04-0117, 16046547.
65. Bayliss J, Hilger A, Vishnu P, Diehl K, El-Ashry D. Reversal of the estrogen receptor negative phenotype in breast cancer and restoration of antiestrogen response. Clin Cancer Res 2007, 13:7029-7036. 10.1158/1078-0432.CCR-07-0587, 18056179.
66. Hojo T, Akiyama Y, Nagasaki K, Maruyama K, Kikuchi K, Ikeda T, Kitajima M, Yamaguchi K. Association of maspin expression with the malignancy grade and tumor vascularization in breast cancer tissues. Cancer Lett 2001, 17(1):103-110.
67. Maass N, Hojo T, Rosel F, Ikeda T, Jonat W, Nagasaki K. Down regulation of the tumor suppressor gene maspin in breast carcinoma is associated with a higher risk of distant metastasis. Clin Biochem 2001, 34:303-307. 10.1016/S0009-9120(01)00220-X, 11440731.
68. Prasad CP, Rath G, Mathur S, Bhatnagar D, Ralhan R. Expression analysis of maspin in invasive ductal carcinoma of breast and modulation of its expression by curcumin in breast cancer cell lines. Chem Biol Interact 2010, 183:455-461. 10.1016/j.cbi.2009.11.019, 19944674.
69. Zhang S, Cao HJ, Davis FB, Tang HY, Davis PJ, Lin HY. Oestrogen inhibits resveratrol-induced post-translational modification of p53 and apoptosis in breast cancer cells. Br J Cancer 2004, 91:178-185. 10.1038/sj.bjc.6601902, 2364738, 15188005.
70. Ju H, Venema VJ, Liang H, Harris MB, Zou R, Venema RC. Bradykinin activates the Janus-activated kinase/signal transducers and activators of transcription (JAK/STAT) pathway in vascular endothelial cells: localization of JAK/STAT signalling proteins in plasmalemmal caveolae. Biochem J 2000, 351:257-264. 10.1042/0264-6021:3510257, 1221357, 10998369.
71. Zhang W, Zhang M. Tissue microarray analysis of maspin expression and its reverse correlation with mutant p53 in various tumors. Int J Oncol 2002, 20:1145-1150.
72. Oshiro MM, Watts GS, Wozniak RJ, Junk DJ, Munoz-Rodriguez JL, Domann FE, Futscher BW. Mutant p53 and aberrant cytosine methylation cooperate to silence gene expression. Oncogene 2003, 22:3624-3634. 10.1038/sj.onc.1206545, 12789271.
73. Latha K, Zhang W, Cella N, Shi HY, Zhang M. Maspin mediates increased tumor cell apoptosis upon induction of the mitochondrial permeability transition. Mol Cell Biol 2005, 25:1737-1748. 10.1128/MCB.25.5.1737-1748.2005, 549349, 15713631.
74. Bailey CM, Hendrix MJ. IRF6 in development and disease: a mediator of quiescence and differentiation. Cell Cycle 2008, 7:1925-1930. 10.4161/cc.7.13.6221, 2581479, 18604160.
75. Bailey CM, Abbott DE, Margaryan NV, Khalkhali-Ellis Z, Hendrix MJ. Interferon regulatory factor 6 promotes cell cycle arrest and is regulated by the proteasome in a cell cycle-dependent manner. Mol Cell Biol 2008, 28:2235-2243. 10.1128/MCB.01866-07, 2268429, 18212048.
76. Burgermeister E, Tencer L, Liscovitch M. Peroxisome proliferator-activated receptor-gamma upregulates caveolin-1 and caveolin-2 expression in human carcinoma cells. Oncogene 2003, 22:3888-3900. 10.1038/sj.onc.1206625, 12813462.
77. Song Z, Yao X, Wu M. Direct interaction between survivin and Smac/DIABLO is essential for the anti-apoptotic activity of survivin during taxol-induced apoptosis. J Biol Chem 2003, 278:23130-23140. 10.1074/jbc.M300957200, 12660240.
78. Suzuki A, Ito T, Kawano H, Hayashida M, Hayasaki Y, Tsutomi Y, Akahane K, Nakano T, Miura M, Shiraki K. Survivin initiates procaspase 3/p21 complex formation as a result of interaction with Cdk4 to resist Fas-mediated cell death. Oncogene 2000, 19:1346-1353. 10.1038/sj.onc.1203429, 10713676.
79. Suzuki A, Shiraki K. Tumor cell "dead or alive": caspase and survivin regulate cell death, cell cycle and cell survival. Histol Histopathol 2001, 16:583-593.
80. Fukuda S, Pelus LM. Survivin, a cancer target with an emerging role in normal adult tissues. Mol Cancer Ther 2006, 5:1087-1098. 10.1158/1535-7163.MCT-05-0375, 16731740.
81. Kennedy SM, O'Driscoll L, Purcell R, Fitz-Simons N, McDermott EW, Hill AD, O'Higgins NJ, Parkinson M, Linehan R, Clynes M. Prognostic importance of survivin in breast cancer. Br J Cancer 2003, 88:1077-1083. 10.1038/sj.bjc.6600776, 2376388, 12671708.
82. Zhao L, Moos MPW, Grabner R, Pedrono F, Fan J, Kaiser B, John N, Schmidt S, Spanbroek R, Lotzer K, et al. The 5-lipoxygenase pathway promotes pathogenesis of hyperlipidemia-dependent aortic aneurysm.[see comment]. Nat Med 2004, 10:966-973. 10.1038/nm1099, 15322539.
83. Doolittle H, Moore A, Talbot D. Survivin-directed anticancer therapies - a review of preclinical data and early-phase clinical trials. Eur Oncol 2010, 6:10-14.
84. Tracey L, Perez-Rosado A, Artiga MJ, Camacho F, Rodriquez A, Martinez N, Ruiz-Ballesteros E, Mollejo M, Martinez B, Cuadros M, et al. Expression of the NF-kappaB targets BCL2 and BIRC5/Survivin characterizes small B-cell and aggressive B-cell lymphomas, respectively. J Pathol 2005, 206(2):123-134. 10.1002/path.1768, 15880597.
85. Hoffman WH, Biade S, Zilfou JT, Chen J, Murphy M. Transcriptional repression of the anti-apoptotic survivin gene by wild type p53. J Biol Chem 2002, 277:3247-3257. 10.1074/jbc.M106643200, 11714700.
86. Verhagen AM, Kratina TK, Hawkins CJ, Silke J, Ekert PG, Vaux DL. Identification of mammalian mitochondrial proteins that interact with IAPs via N-terminal IAP binding motifs. Cell Death Differ 2007, 14:348-357. 10.1038/sj.cdd.4402001, 16794601.
87. Elrod HA, Sun SY. PPARgamma and Apoptosis in Cancer. PPAR Res 2008, 2008:704165. 2442903, 18615184.
88. Lu M, Kwan T, Yu C, Chen F, Freedman B, Schafer JM, Lee EJ, Jameson JL, Jordan VC, Cryns VL. Peroxisome proliferator-activated receptor gamma agonists promote TRAIL-induced apoptosis by reducing survivin levels via cyclin D3 repression and cell cycle arrest. J Biol Chem 2005, 280:6742-6751. 10.1074/jbc.M411519200, 15569667.
89. Connolly JM, Liu XH, Rose DP. Dietary linoleic acid-stimulated human breast cancer cell growth and metastasis in nude mice and their suppression by indomethacin, a cyclooxygenase inhibitor. Nutr Cancer 1996, 25:231-240. 10.1080/01635589609514447, 8771566.