A TDO2-AhR signaling axis facilitates anoikis resistance and metastasis in triple-negative breast cancer

Cancer Research

Volumn 75, Issue 21, 2015, Pages 4651-4664

  D'Amato, Nicholas C ^a   Rogers, Thomas J ^a   Gordon, Michael A ^a   Greene, Lisa I ^a   Cochrane, Dawn R ^a   Spoelstra, Nicole S ^a   Nemkov, Travis G ^b   D'alessandro, Angelo ^b   Hansen, Kirk C ^b   Richer, Jennifer K ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; KYNURENINE; TRYPTOPHAN; TRYPTOPHAN 2,3 DIOXYGENASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SMALL INTERFERING RNA;

AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOIKIS; ARTICLE; BREAST CANCER CELL LINE; CELL ANCHORAGE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; IN VIVO STUDY; METASTASIS; MOUSE; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST CANCER; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL MOTION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; RNA INTERFERENCE; SCID MOUSE; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; ANOIKIS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KYNURENINE; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NF-KAPPA B; RECEPTORS, ARYL HYDROCARBON; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST NEOPLASMS; TRYPTOPHAN OXYGENASE;

EID: 84946554555     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-2011     Document Type: Article

References (47)

1. Fidler IJ. Critical factors in the biology of human cancer metastasis: Twenty-eighth G.H.A. Clowes memorial award lecture. Cancer Res 1990;50:6130-8.
2. Liedtke C, Mazouni C, Hess KR, Andre F, Tordai A, Mejia JA, et al. Response to neoadjuvant therapy and long-term survival in patients with triplenegative breast cancer. J Clin Oncol 2008;26:1275-81.
3. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 2007;13:4429-34.
4. Lin NU, Vanderplas A, Hughes ME, Theriault RL, Edge SB, Wong YN, et al. Clinicopathologic features, patterns of recurrence, and survival among women with triple-negative breast cancer in the National Comprehensive Cancer Network. Cancer 2012;118:5463-72.
5. Kassam F, Enright K, Dent R, Dranitsaris G, Myers J, Flynn C, et al. Survival outcomes for patients with metastatic triple-negative breast cancer: implications for clinical practice and trial design. Clin Breast Cancer 2009;9: 29-33.
6. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science 2011;331:1559-64.
7. Frisch SM, Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 1994;124:619-26.
8. Simpson CD, Anyiwe K, Schimmer AD. Anoikis resistance and tumor metastasis. Cancer Lett 2008;272:177-85.
9. Paoli P, Giannoni E, Chiarugi P. Anoikis molecular pathways and its role in cancer progression. Biochim Biophys Acta 2013;1833:3481-98.
10. Kamarajugadda S, Stemboroski L, Cai Q, Simpson NE, Nayak S, Tan M, et al. Glucose oxidation modulates anoikis and tumor metastasis. Mol Cell Biol 2012;32:1893-907.
11. Schafer ZT, Grassian AR, Song L, Jiang Z, Gerhart-Hines Z, Irie HY, et al. Antioxidant and oncogene rescue of metabolic defects caused by loss of matrix attachment. Nature 2009;461:109-13.
12. Opitz CA, Litzenburger UM, Sahm F, Ott M, Tritschler I, Trump S, et al. An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor. Nature 2011;478:197-203.
13. Rose DP. Tryptophan metabolism in carcinoma of the breast. Lancet 1967;1:239-41.
14. Poulter JM, Dickerson JW, White WF. Tryptophan metabolism in patients with breast cancer. Acta vitaminologica et enzymologica 1985;7:93-7.
15. Peters JC. Tryptophan nutrition and metabolism: An overview. Adv Exp Med Biol 1991;294:345-58.
16. Stone TW, Darlington LG. Endogenous kynurenines as targets for drug discovery and development. Nat Rev Drug Discov 2002;1:609-20.
17. Salter M, Pogson CI. The role of tryptophan 2, 3-dioxygenase in the hormonal control of tryptophan metabolism in isolated rat liver cells. Effects of glucocorticoids and experimental diabetes. Biochem J 1985; 229:499-504.
18. Ball HJ, Sanchez-Perez A, Weiser S, Austin CJ, Astelbauer F, Miu J, et al. Characterization of an indoleamine 2, 3-dioxygenase-like protein found in humans and mice. Gene 2007;396:203-13.
19. Metz R, Duhadaway JB, Kamasani U, Laury-Kleintop L, Muller AJ, Prendergast GC. Novel tryptophan catabolic enzyme IDO2 is the preferred biochemical target of the antitumor indoleamine 2, 3-dioxygenase inhibitory compound D-1-methyl-tryptophan. Cancer Res 2007;67:7082-7.
20. Platten M, Wick W, Van den Eynde BJ. Tryptophan catabolism in cancer: beyond IDO and tryptophan depletion. Cancer Res 2012;72:5435-40.
21. Lob S, Konigsrainer A, Rammensee HG, Opelz G, Terness P. Inhibitors of indoleamine-2, 3-dioxygenase for cancer therapy: can we see the wood for the trees? Nat Rev Cancer 2009;9:445-52.
22. Poland A, Knutson JC. 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin and related halogenated aromatic hydrocarbons: examination of the mechanism of toxicity. Annu Rev Pharmacol Toxicol 1982;22:517-54.
23. Burbach KM, Poland A, Bradfield CA. Cloning of the Ah-receptor cDNA reveals a distinctive ligand-activated transcription factor. Proc Natl Acad Sci U S A 1992;89:8185-9.
24. Gonzalez FJ, Fernandez-Salguero P, Ward JM. The role of the aryl hydrocarbon receptor in animal development, physiological homeostasis and toxicity of TCDD. J Toxicol Sci 1996;21:273-7.
25. Lew BJ, Collins LL, O'Reilly MA, Lawrence BP. Activation of the aryl hydrocarbon receptor during different critical windows in pregnancy alters mammary epithelial cell proliferation and differentiation. Toxicol Sci 2009;111:151-62.
26. Hushka LJ, Williams JS, Greenlee WF. Characterization of 2, 3, 7, 8-tetrachlorodibenzofuran- dependent suppression and AH receptor pathway gene expression in the developing mouse mammary gland. Toxicol Appl Pharmacol 1998;152:200-10.
27. Brooks J, Eltom SE. Malignant transformation of mammary epithelial cells by ectopic overexpression of the aryl hydrocarbon receptor. Curr Cancer Drug Targets 2011;11:654-69.
28. Goode G, Pratap S, Eltom SE. Depletion of the aryl hydrocarbon receptor in MDA-MB-231 human breast cancer cells altered the expression of genes in key regulatory pathways of cancer. PLoS One 2014;9:e100103.
29. Sadek CM, Allen-Hoffmann BL. Suspension-mediated induction of Hepa 1c1c7 Cyp1a-1 expression is dependent on the Ah receptor signal transduction pathway. J Biol Chem 1994;269:31505-9.
30. Howe EN, Cochrane DR, Richer JK. Targets of miR-200c mediate suppression of cell motility and anoikis resistance. Breast Cancer Res 2011;13: R45-R45.
31. Howe EN, Cochrane DR, Cittelly DM, Richer JK. miR-200c targets a NF-kB up-regulated TrkB/NTF3 autocrine signaling loop to enhance anoikis sensitivity in triple negative breast cancer. PloS One 2012;7:e49987.
32. Richter CA, Tillitt DE, Hannink M. Regulation of subcellular localization of the aryl hydrocarbon receptor (AhR). Arch Biochem Biophys 2001;389: 207-17.
33. Mezrich JD, Fechner JH, Zhang X, Johnson BP, Burlingham WJ, Bradfield CA. An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells. J Immunol 2010;185:3190-8.
34. Di Natale BC, Murray IA, Schroeder JC, Flaveny CA, Lahoti TS, Laurenzana EM, et al. Kynurenic acid is a potent endogenous aryl hydrocarbon receptor ligand that synergistically induces interleukin-6 in the presence of inflammatory signaling. Toxicol Sci 2010;115:89-97.
35. Denison MS, Nagy SR. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu Rev Pharmacol Toxicol 2003;43:309-34.
36. Hsu S, Kim M, Hernandez L, Grajales V, Noonan A, Anver M, et al. IKKepsilon coordinates invasion and metastasis of ovarian cancer. Cancer Res 2012;72:5494-504.
37. Curtis C, Shah SP, Chin SF, TurashviliG, Rueda OM, Dunning MJ, et al. The genomic and transcriptomic architecture of 2, 000 breast tumours reveals novel subgroups. Nature 2012;486:346-52.
38. Pilotte L, Larrieu P, Stroobant V, Colau D, Dolusic E, Frederick R, et al. Reversal of tumoral immune resistance by inhibition of tryptophan 2, 3- dioxygenase. Proc Natl Acad Sci U S A 2012;109:2497-502.
39. Muller AJ, DuHadaway JB, Donover PS, Sutanto-Ward E, Prendergast GC. Inhibition of indoleamine 2, 3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy.Nat Med 2005;11:312-9.
40. Suzuki S, Tone S, Takikawa O, Kubo T, Kohno I, Minatogawa Y. Expression of indoleamine 2, 3-dioxygenase and tryptophan 2, 3-dioxygenase in early concepti. Biochem J 2001;355:425-9.
41. Furuya M, Horiguchi J, Nakajima H, Kanai Y, Oyama T. Correlation of Ltype amino acid transporter 1 and CD98 expression with triple negative breast cancer prognosis. Cancer Sci 2012;103:382-9.
42. Tang X, Lin CC, Spasojevic I, Iversen ES, Chi JT, Marks JR. A joint analysis of metabolomics and genetics of breast cancer. Breast Cancer Res 2014; 16:415.
43. Davidson B, Abeler VM, Forsund M, Holth A, Yang Y, Kobayashi Y, et al. Gene expression signatures of primary and metastatic uterine leiomyosarcoma. Hum Pathol 2014;45:691-700.
44. Bos PD, Zhang XH, Nadal C, Shu W, Gomis RR, Nguyen DX, et al. Genes that mediate breast cancer metastasis to the brain. Nature 2009;459: 1005-9.
45. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, et al. Genes that mediate breast cancer metastasis to lung. Nature 2005;436:518-24.
46. Tran C, Richmond O, Aaron L, Powell JB. Inhibition of constitutive aryl hydrocarbon receptor (AhR) signaling attenuates androgen independent signaling and growth in (C4-2) prostate cancer cells. Biochem Pharmacol 2013;85:753-62.
47. Saito R, Miki Y, Hata S, Takagi K, Iida S, Oba Y, et al. Aryl hydrocarbon receptor in breast cancer-a newly defined prognostic marker. Horm Cancer 2014;5:11-21.