Transcription factor ATF3 links host adaptive response to breast cancer metastasis

Journal of Clinical Investigation

Volumn 123, Issue 7, 2013, Pages 2893-2906

  Wolford, Chris C ^a   McConoughey, Stephen J ^a   Jalgaonkar, Swati P ^a   Leon, Marino ^a   Merchant, Anand S ^a,b   Dominick, Johnna L ^a   Yin, Xin ^a   Chang, Yiseok ^a   Zmuda, Erik J ^a   O'Toole, Sandra A ^c   Millar, Ewan K A ^c   Roller, Stephanie L ^a   Shapiro, Charles L ^a,b   Ostrowski, Michael C ^a,b   Sutherland, Robert L ^c   Hai, Tsonwin ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BREAST CANCER; CONTROLLED STUDY; DISEASE COURSE; EPITHELIUM CELL; FEMALE; HOST CELL; HOST RESISTANCE; IMMUNOHISTOCHEMISTRY; MACROPHAGE; METASTASIS; MONONUCLEAR CELL; NONHUMAN; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STROMA;

ACTIVATING TRANSCRIPTION FACTOR 3; ADAPTIVE IMMUNITY; ANIMALS; BREAST NEOPLASMS; CELL MOVEMENT; COCULTURE TECHNIQUES; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; MACROPHAGES; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIVARIATE ANALYSIS; NEOPLASM TRANSPLANTATION; NEOPLASTIC CELLS, CIRCULATING; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, MESSENGER; TISSUE ARRAY ANALYSIS; TRANSCRIPTOME; TUMOR BURDEN; TUMOR CELLS, CULTURED;

EID: 84879631330     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI64410     Document Type: Article

References (56)

1. Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell. 2012;21(3):309-322.
2. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer. 2009;9(4):239-252.
3. Bissell MJ, Radisky D. Putting tumours in context. Nat Rev Cancer. 2001;1(1):46-54. (Pubitemid 33741880)
4. Cichon MA, Degnim AC, Visscher DW, Radisky DC. Microenvironmental influences that drive progression from benign breast disease to invasive breast cancer. J Mammary Gland Biol Neoplasia. 2010; 15(4):389-397.
5. Psaila B, Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer. 2009;9(4):285-293.
6. DeNardo DG, Johansson M, Coussens LM. Immune cells as mediators of solid tumor metastasis. Cancer Metastasis Rev. 2008;27(1):11-18.
7. Direkze NC, Alison MR. Bone marrow and tumour stroma: an intimate relationship. Hematol Oncol. 2006;24(4):189-195. (Pubitemid 46032892)
8. Johansson M, Denardo DG, Coussens LM. Polarized immune responses differentially regulate cancer development. Immunol Rev. 2008;222:145-154. (Pubitemid 351430362)
9. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer. 2006;6(1):24-37. (Pubitemid 43053650)
10. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140(6):883-899.
11. Mantovani A, Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol. 2010;22(2):231-237.
12. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell. 2010;141(1):39-51.
13. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 2002; 23(11):549-555. (Pubitemid 35223554)
14. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 2010;141(1):52-67.
15. Chen BPC, Liang G, Whelan J, Hai T. ATF3 and ATF3DeltaZip: Transcriptional repression versus activation by alternatively spliced isoforms. J Biol Chem. 1994;269(22):15819-15826.
16. Hai T, Hartman MG. The molecular biology and nomenclature of the ATF/CREB family of transcription factors: ATF proteins and homeostasis. Gene. 2001;273(1):1-11.
17. Thompson MR, Xu D, Williams BR. ATF3 transcription factor and its emerging roles in immunity and cancer. J Mol Med. 2009;87(11):1053-1060.
18. Hai T, Wolfgang CD, Marsee DK, Allen AE, Sivaprasad U. ATF3 and stress responses. Gene Expr. 1999;7(4-6):321-335. (Pubitemid 29372076)
19. Hai T, Wolford CC, Chang YS. ATF3, a hub of the cellular adaptive-response network, in the pathogenesis of diseases: Is modulation of inflammation a unifying component? Gene Expr. 2010;15(1):1-11.
20. Hai T. The ATF transcription factors in cellular adaptive responses. In: Ma J, ed. Gene Expression And Regulation. Beijing, China and New York, USA: Higher Education Press and Springer; 2006:322-333.
21. Yin X, DeWille J, Hai T. A potential dichotomous role of ATF3, an adaptive-response gene, in cancer development. Oncogene. 2008;27(15):2118-2127. (Pubitemid 351483383)
22. Yin X, Wolford CC, McConoughey SJ, Ramsey SA, Aderem A, Hai T. ATF3, an adaptive-response gene, enhances TGFbeta signaling and cancer initiating cell features in breast cancer cells. J Cell Sci. 2010;123(pt 20):3558-3565.
23. Wang A, et al. The transcription factor ATF3 acts as an oncogene in mouse mammary tumorigenesis. BMC Cancer. 2008;8:268.
24. Mantovani A, Schioppa T, Porta C, Allavena P, Sica A. Role of tumor-associated macrophages in tumor progression and invasion. Cancer Metastasis Rev. 2006;25(3):315-322. (Pubitemid 44922352)
25. Condeelis J, Pollard JW. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell. 2006;124(2):263-266. (Pubitemid 43121975)
26. Ruffell B, Au A, Rugo HS, Esserman LJ, Hwang ES, Coussens LM. Leukocyte composition of human breast cancer. Proc Natl Acad Sci U S A. 2012; 109(8):2796-2801.
27. Hartman MG, et al. Role for activating transcription factor 3 in stress-induced beta-cell apoptosis. Mol Cell Biol. 2004;24(13):5721-5732. (Pubitemid 38787958)
28. Davie SA, et al. Effects of FVB/NJ and C57BL/6J strain backgrounds on mammary tumor phenotype in inducible nitric oxide synthase deficient mice. Transgenic Res. 2007;16(2):193-201. (Pubitemid 46440615)
29. Borowsky AD, et al. Syngeneic mouse mammary carcinoma cell lines: two closely related cell lines with divergent metastatic behavior. Clin Exp Metastasis. 2005;22(1):47-59. (Pubitemid 41185861)
30. Pei XF, et al. Explant-cell culture of primary mammary tumors from MMTV-c-Myc transgenic mice. In Vitro Cell Dev Biol Anim. 2004;40(1-2):14-21. (Pubitemid 38756888)
31. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. Conditional gene targeting in macrophages and granulocytes using LysM-cre mice. Transgenic Res. 1999;8(4):265-277. (Pubitemid 29523965)
32. Lucas T, Abraham D, Aharinejad S. Modulation of tumor associated macrophages in solid tumors. Front Biosci. 2008;13:5580-5588.
33. Siveen KS, Kuttan G. Role of macrophages in tumour progression. Immunol Lett. 2009;123(2):97-102.
34. Debnath J, Muthuswamy SK, Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods. 2003;30(3):256-268. (Pubitemid 36677560)
35. DeNardo DG, et al. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell. 2009;16(2):91-102.
36. O'Brien LE, Zegers MM, Mostov KE. Opinion: Building epithelial architecture: insights from three-dimensional culture models. Nat Rev Mol Cell Biol. 2002;3(7):531-537. (Pubitemid 34733434)
37. Finak G, et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat Med. 2008; 14(5):518-527. (Pubitemid 351655218)
38. Gilchrist M, et al. Systems biology approaches identify ATF3 as a negative regulator of Toll-like receptor 4. Nature. 2006;441(7090):173-178.
39. Hoetzenecker W, et al. ROS-induced ATF3 causes susceptibility to secondary infections during sepsis- associated immunosuppression. Nat Med. 2012; 18(1):128-134.
40. Whitmore MM, Iparraguirre A, Kubelka L, Weninger W, Hai T, Williams BR. Negative regulation of TLRsignaling pathways by activating transcription factor- 3. J Immunol. 2007;179(6):3622-3630.
41. Khuu CH, Barrozo RM, Hai T, Weinstein SL. Activating transcription factor 3 (ATF3) represses the expression of CCL4 in murine macrophages. Mol Immunol. 2007;44(7):1598-1605.
42. Calle EE, Kaaks R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer. 2004;4(8):579-591. (Pubitemid 39025053)
43. Chida Y, Hamer M, Wardle J, Steptoe A. Do stressrelated psychosocial factors contribute to cancer incidence and survival? Nat Clin Pract Oncol. 2008; 5(8):466-475.
44. Pandey V, Vijayakumar MV, Ajay AK, Malvi P, Bhat MK. Diet-induced obesity increases melanoma progression: involvement of Cav-1 and FASN. Int J Cancer. 2012;130(3):497-508.
45. Novosyadlyy R, et al. Insulin-mediated acceleration of breast cancer development and progression in a nonobese model of type 2 diabetes. Cancer Res. 2010; 70(2):741-751.
46. Sloan EK, et al. The sympathetic nervous system induces a metastatic switch in primary breast cancer. Cancer Res. 2010;70(18):7042-7052.
47. Zabuawala T, et al. An Ets2-driven transcriptional program in tumor-associated macrophages promotes tumor metastasis. Cancer Res. 2010; 70(4):1323-1333.
48. Stockmann C, et al. Deletion of vascular endothelial growth factor in myeloid cells accelerates tumorigenesis. Nature. 2008;456(7223):814-818.
49. Qian BZ, et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 2011;475(7355):222-225.
50. Doedens AL, et al. Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res. 2010;70(19):7465-7475.
51. Sharda DR, et al. Regulation of macrophage arginase expression and tumor growth by the Ron receptor tyrosine kinase. J Immunol. 2011;187(5):2181-2192.
52. Kaplan RN, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 2005;438(7069):820-827. (Pubitemid 41753060)
53. Ma C, Wang XF. In vitro assays for the extracellular matrix protein-regulated extravasation process. CSH Protoc. 2008;2008:pdb.prot5034.
54. Sorlie T, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A. 2001; 98(19):10869-10874.
55. van 't Veer LJ, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature. 2002; 415(6871):530-536.
56. Minn AJ, et al. Genes that mediate breast cancer metastasis to lung. Nature. 2005;436(7050):518-524. (Pubitemid 41112921)