Interferon-induced transmembrane protein 1 (IFITM1) overexpression enhances the aggressive phenotype of SUM149 inflammatory breast cancer cells in a signal transducer and activator of transcription 2 (STAT2)-dependent manner

Breast Cancer Research

Volumn 18, Issue 1, 2016, Pages

  Ogony, Joshua ^a   Choi, Hye Joung ^a   Lui, Asona ^a   Cristofanilli, Massimo ^b   Lewis Wambi, Joan ^a  

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

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

BRG1; IFITM1; Inflammatory breast cancer; Interferon stimulated genes; JAK STAT signaling

Indexed keywords

ALPHA INTERFERON; INTERFERON INDUCED TRANSMEMBRANE PROTEIN 1; MEMBRANE PROTEIN; MESSENGER RNA; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; STAT1 PROTEIN; STAT2 PROTEIN; UNCLASSIFIED DRUG; DIFFERENTIATION ANTIGEN; LEU-13 ANTIGEN; STAT2 PROTEIN, HUMAN;

ARTICLE; BREAST CANCER CELL LINE; BRG1 GENE; CELL CYCLE; CELL INVASION; CELL MIGRATION; CELLULAR DISTRIBUTION; COLONY FORMATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IFITM1 GENE; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE MICROSCOPY; INFLAMMATORY BREAST CANCER; MDA IBC 3 CELL LINE; PHENOTYPE; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; SUM149 CELL LINE; WESTERN BLOTTING; BIOSYNTHESIS; CELL MOTION; FEMALE; GENE EXPRESSION REGULATION; GENETICS; PATHOLOGY; TRANSCRIPTION INITIATION; TRIPLE NEGATIVE BREAST CANCER; TUMOR CELL LINE; TUMOR INVASION;

ANTIGENS, DIFFERENTIATION; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INFLAMMATORY BREAST NEOPLASMS; NEOPLASM INVASIVENESS; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT2 TRANSCRIPTION FACTOR; TRANSCRIPTIONAL ACTIVATION; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84958529629     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-016-0683-7     Document Type: Article

References (60)

1. Fouad TM, Kogawa T, Liu DD, Shen Y, Masuda H, El-Zein R, et al. Overall survival differences between patients with inflammatory and noninflammatory breast cancer presenting with distant metastasis at diagnosis. Breast Cancer Res Treat. 2015;152(2):407-16.
2. Robertson FM, Bondy M, Yang W, Yamauchi H, Wiggins S, Kamrudin S, et al. Inflammatory breast cancer: the disease, the biology, the treatment. CA Cancer J Clin. 2010;60(6):351-75.
3. Bertucci F, Ueno NT, Finetti P, Vermeulen P, Lucci A, Robertson FM, et al. Gene expression profiles of inflammatory breast cancer: correlation with response to neoadjuvant chemotherapy and metastasis-free survival. Ann Oncol. 2014;25(2):358-65.
4. Woodward WA, Krishnamurthy S, Yamauchi H, El-Zein R, Ogura D, Kitadai E, et al. Genomic and expression analysis of microdissected inflammatory breast cancer. Breast Cancer Res Treat. 2013;138(3):761-72.
5. Cristofanilli M, Valero V, Buzdar AU, Kau SW, Broglio KR, Gonzalez-Angulo AM, et al. Inflammatory breast cancer (IBC) and patterns of recurrence: understanding the biology of a unique disease. Cancer. 2007;110(7):1436-44.
6. Silvera D, Arju R, Darvishian F, Levine PH, Zolfaghari L, Goldberg J, et al. Essential role for eIF4GI overexpression in the pathogenesis of inflammatory breast cancer. Nat Cell Biol. 2009;11(7):903-8.
7. Bertucci F, Finetti P, Vermeulen P, Van Dam P, Dirix L, Birnbaum D, et al. Genomic profiling of inflammatory breast cancer: a review. Breast. 2014;23(5):538-45.
8. Sarasin-Filipowicz M, Wang X, Yan M, Duong FH, Poli V, Hilton DJ, et al. Alpha interferon induces long-lasting refractoriness of JAK-STAT signaling in the mouse liver through induction of USP18/UBP43. Mol Cell Biol. 2009;29(17):4841-51.
9. Ivashkiv LB, Donlin LT. Regulation of type I interferon responses. Nat Rev Immunol. 2014;14(1):36-49.
10. Critchley-Thorne RJ, Simons DL, Yan N, Miyahira AK, Dirbas FM, Johnson DL, et al. Impaired interferon signaling is a common immune defect in human cancer. Proc Natl Acad Sci U S A. 2009;106(22):9010-5.
11. Khodarev NN, Roizman B, Weichselbaum RR. Molecular pathways: interferon/Stat1 pathway: role in the tumor resistance to genotoxic stress and aggressive growth. Clin Cancer Res. 2012;18(11):3015-21.
12. Lee HJ, Zhuang G, Cao Y, Du P, Kim HJ, Settleman J. Drug resistance via feedback activation of Stat3 in oncogene-addicted cancer cells. Cancer Cell. 2014;26(2):207-21.
13. Calo V, Migliavacca M, Bazan V, Macaluso M, Buscemi M, Gebbia N, et al. STAT proteins: from normal control of cellular events to tumorigenesis. J Cell Physiol. 2003;197(2):157-68.
14. Lee J, Goh SH, Song N, Hwang JA, Nam S, Choi IJ, et al. Overexpression of IFITM1 has clinicopathologic effects on gastric cancer and is regulated by an epigenetic mechanism. Am J Pathol. 2012;181(1):43-52.
15. He JD, Luo HL, Li J, Feng WT, Chen LB. Influences of the interferon induced transmembrane protein 1 on the proliferation, invasion, and metastasis of the colorectal cancer SW480 cell lines. Chin Med J (Engl). 2012;125(3):517-22.
16. Yang G, Xu Y, Chen X, Hu G. IFITM1 plays an essential role in the antiproliferative action of interferon-γ. Oncogene. 2007;26(4):594-603.
17. Johnson MC, Sangrador-Vegas A, Smith TJ, Cairns MT. Cloning and characterization of two genes encoding rainbow trout homologues of the IFITM protein family. Vet Immunol Immunopathol. 2006;110(3-4):357-62.
18. Hatano H, Kudo Y, Ogawa I, Tsunematsu T, Kikuchi A, Abiko Y, et al. IFN-induced transmembrane protein 1 promotes invasion at early stage of head and neck cancer progression. Clin Cancer Res. 2008;14(19):6097-105.
19. Yu F, Ng SS, Chow BK, Sze J, Lu G, Poon WS, et al. Knockdown of interferon-induced transmembrane protein 1 (IFITM1) inhibits proliferation, migration, and invasion of glioma cells. J Neurooncol. 2011;103(2):187-95.
20. Pan Z, Chen S, Pan X, Wang Z, Han H, Zheng W, et al. Differential gene expression identified in Uigur women cervical squamous cell carcinoma by suppression subtractive hybridization. Neoplasma. 2010;57(2):123-8.
21. Gomes AQ, Correia DV, Grosso AR, Lança T, Ferreira C, Lacerda JF, et al. Identification of a panel of ten cell surface protein antigens associated with immunotargeting of leukemias and lymphomas by peripheral blood γδ T cells. Haematologica. 2010;95(8):1397-404.
22. Debeb BG, Cohen EN, Boley K, Freiter EM, Li L, Robertson FM, et al. Pre-clinical studies of Notch signaling inhibitor RO4929097 in inflammatory breast cancer cells. Breast Cancer Res Treat. 2012;134(2):495-510.
23. Johnatty SE, Beesley J, Chen X, Macgregor S, Duffy DL, Spurdle AB, et al. Evaluation of candidate stromal epithelial cross-talk genes identifies association between risk of serous ovarian cancer and TERT, a cancer susceptibility "hot-spot". PLoS Genet. 2010;6(7):e1001016.
24. Luszczek W, Cheriyath V, Mekhail TM, Borden EC. Combinations of DNA methyltransferase and histone deacetylase inhibitors induce DNA damage in small cell lung cancer cells: correlation of resistance with IFN-stimulated gene expression. Mol Cancer Ther. 2010;9(8):2309-21.
25. Gongora C, Candeil L, Vezzio N, Copois V, Denis V, Breil C, et al. Altered expression of cell proliferation-related and interferon-stimulated genes in colon cancer cells resistant to SN38. Cancer Biol Ther. 2008;7(6):822-32.
26. Choi HJ, Lui A, Ogony J, Jan R, Sims PJ, Lewis-Wambi J. Targeting interferon response genes sensitizes aromatase inhibitor resistant breast cancer cells to estrogen-induced cell death. Breast Cancer Res. 2015;17:6.
27. Van Laere S, Van der Auwera I, Van den Eynden G, Van Hummelen P, van Dam P, Van Marck E, et al. Distinct molecular phenotype of inflammatory breast cancer compared to non-inflammatory breast cancer using Affymetrix-based genome-wide gene-expression analysis. Br J Cancer. 2007;97(8):1165-74.
28. Li J, Gonzalez-Angulo AM, Allen PK, Yu TK, Woodward WA, Ueno NT, et al. Triple-negative subtype predicts poor overall survival and high locoregional relapse in inflammatory breast cancer. Oncologist. 2011;16(12):1675-83.
29. Cabioglu N, Gong Y, Islam R, Broglio KR, Sneige N, Sahin A, et al. Expression of growth factor and chemokine receptors: new insights in the biology of inflammatory breast cancer. Ann Oncol. 2007;18(6):1021-9.
30. Masuda H, Zhang D, Bartholomeusz C, Doihara H, Hortobagyi GN, Ueno NT. Role of epidermal growth factor receptor in breast cancer. Breast Cancer Res Treat. 2012;136(2):331-45.
31. Yamauchi H, Cristofanilli M, Nakamura S, Hortobagyi GN, Ueno NT. Molecular targets for treatment of inflammatory breast cancer. Nat Rev Clin Oncol. 2009;6(7):387-94.
32. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity. 2004;21(2):137-48.
33. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science (New York, NY). 2011;331(6024):1565-70.
34. Ferrantini M, Capone I, Marincola FM, Parmiani G, Belardelli F. International meeting "Immunotherapy of Cancer: Challenges and Needs". Cancer Immunol Immunother. 2007;56(4):581-5.
35. Moschos S, Kirkwood JM. Present role and future potential of type I interferons in adjuvant therapy of high-risk operable melanoma. Cytokine Growth Factor Rev. 2007;18(5-6):451-8.
36. Buess M, Nuyten DS, Hastie T, Nielsen T, Pesich R, Brown PO. Characterization of heterotypic interaction effects in vitro to deconvolute global gene expression profiles in cancer. Genome Biol. 2007;8(9):R191.
37. Cheon H, Borden EC, Stark GR. Interferons and their stimulated genes in the tumor microenvironment. Semin Oncol. 2014;41(2):156-73.
38. Khodarev NN, Roach P, Pitroda SP, Golden DW, Bhayani M, Shao MY, et al. STAT1 pathway mediates amplification of metastatic potential and resistance to therapy. PLoS One. 2009;4(6):e5821.
39. Kleer CG, Zhang Y, Pan Q, Gallagher G, Wu M, Wu ZF, et al. WISP3 and RhoC guanosine triphosphatase cooperate in the development of inflammatory breast cancer. Breast Cancer Res. 2004;6(1):R110-5.
40. van Golen KL, Bao L, DiVito MM, Wu Z, Prendergast GC, Merajver SD. Reversion of RhoC GTPase-induced inflammatory breast cancer phenotype by treatment with a farnesyl transferase inhibitor. Mol Cancer Ther. 2002;1(8):575-83.
41. van Golen KL, Wu ZF, Qiao XT, Bao L, Merajver SD. RhoC GTPase overexpression modulates induction of angiogenic factors in breast cells. Neoplasia (New York, NY). 2000;2(5):418-25.
42. Arpaia E, Blaser H, Quintela-Fandino M, Duncan G, Leong HS, Ablack A, et al. The interaction between caveolin-1 and Rho-GTPases promotes metastasis by controlling the expression of alpha5-integrin and the activation of Src. Ras and Erk Oncogene. 2012;31(7):884-96.
43. Yu F, Xie D, Ng SS, Lum CT, Cai MY, Cheung WK, et al. IFITM1 promotes the metastasis of human colorectal cancer via CAV-1. Cancer Lett. 2015;368(1):135-43.
44. Fuertes MB, Woo SR, Burnett B, Fu YX, Gajewski TF. Type I interferon response and innate immune sensing of cancer. Trends Immunol. 2013;34(2):67-73.
45. Gajewski TF, Schreiber H, Fu YX. Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol. 2013;14(10):1014-22.
46. Yang X, Zhang X, Fu ML, Weichselbaum RR, Gajewski TF, Guo Y, et al. Targeting the tumor microenvironment with interferon-beta bridges innate and adaptive immune responses. Cancer Cell. 2014;25(1):37-48.
47. Perou CM, Jeffrey SS, van de Rijn M, Rees CA, Eisen MB, Ross DT, et al. Distinctive gene expression patterns in human mammary epithelial cells and breast cancers. Proc Natl Acad Sci U S A. 1999;96(16):9212-7.
48. Suomela S, Cao L, Bowcock A, Saarialho-Kere U. Interferon alpha-inducible protein 27 (IFI27) is upregulated in psoriatic skin and certain epithelial cancers. J Invest Dermatol. 2004;122(3):717-21.
49. Cai D, Cao J, Li Z, Zheng X, Yao Y, Li W, et al. Up-regulation of bone marrow stromal protein 2 (BST2) in breast cancer with bone metastasis. BMC Cancer. 2009;9:102.
50. Ning S, Pagano JS, Barber GN. IRF7: activation, regulation, modification and function. Genes Immun. 2011;12(6):399-414.
51. Blaszczyk K, Olejnik A, Nowicka H, Ozgyin L, Chen YL, Chmielewski S, et al. STAT2/IRF9 directs a prolonged ISGF3-like transcriptional response and antiviral activity in the absence of STAT1. Biochem J. 2015;466(3):511-24.
52. Brierley MM, Marchington KL, Jurisica I, Fish EN. Identification of GAS-dependent interferon-sensitive target genes whose transcription is STAT2-dependent but ISGF3-independent. FEBS J. 2006;273(7):1569-81.
53. Steen HC, Gamero AM. STAT2 phosphorylation and signaling. JAKSTAT. 2013;2(4):e25790.
54. Perry ST, Buck MD, Lada SM, Schindler C, Shresta S. STAT2 mediates innate immunity to Dengue virus in the absence of STAT1 via the type I interferon receptor. PLoS Pathog. 2011;7(2):e1001297.
55. Brierley MM, Fish EN. Functional relevance of the conserved DNA-binding domain of STAT2. J Biol Chem. 2005;280(13):13029-36.
56. Huang M, Qian F, Hu Y, Ang C, Li Z, Wen Z. Chromatin-remodelling factor BRG1 selectively activates a subset of interferon-alpha-inducible genes. Nat Cell Biol. 2002;4(10):774-81.
57. Cui K, Tailor P, Liu H, Chen X, Ozato K, Zhao K. The chromatin-remodeling BAF complex mediates cellular antiviral activities by promoter priming. Mol Cell Biol. 2004;24(10):4476-86.
58. Yan Z, Cui K, Murray DM, Ling C, Xue Y, Gerstein A, et al. PBAF chromatin-remodeling complex requires a novel specificity subunit, BAF200, to regulate expression of selective interferon-responsive genes. Genes Dev. 2005;19(14):1662-7.
59. Ni Z, Karaskov E, Yu T, Callaghan SM, Der S, Park DS, et al. Apical role for BRG1 in cytokine-induced promoter assembly. Proc Natl Acad Sci U S A. 2005;102(41):14611-6.
60. Liu H, Kang H, Liu R, Chen X, Zhao K. Maximal induction of a subset of interferon target genes requires the chromatin-remodeling activity of the BAF complex. Mol Cell Biol. 2002;22(18):6471-9.