G1P3, an interferon- and estrogen-induced survival protein contributes to hyperplasia, tamoxifen resistance and poor outcomes in breast cancer

Oncogene

Volumn 31, Issue 17, 2012, Pages 2222-2236

  Cheriyath, V ^a,c   Kuhns, M A ^a   Jacobs, B S ^a   Evangelista, P ^a   Elson, P ^b   Downs Kelly, E ^b   Tubbs, R ^b   Borden, E C ^a  

^a TAUSSIG CANCER INSTITUTE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c TEXAS A AND M UNIVERSITY COMMERCE   (United States)

Author keywords

apoptosis; breast cancer; G1P3; hyperplasia; interferon stimulated genes; tamoxifen resistance

Indexed keywords

BIM PROTEIN; ESTROGEN; ESTROGEN RECEPTOR; INTERFERON; PROTEIN; PROTEIN BCL 2; PROTEIN G1P3; TAMOXIFEN; UNCLASSIFIED DRUG;

ACINAR CELL; ANOIKIS; APOPTOSIS; ARTICLE; BIOASSAY; BREAST; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CANCER PATIENT; CANCER RESISTANCE; CANCER STAGING; CANCER SURVIVAL; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; DRUG RESISTANCE; EX VIVO STUDY; HUMAN; HUMAN CELL; HYPERPLASIA; INTRADUCTAL CARCINOMA; MITOCHONDRIAL MEMBRANE POTENTIAL; MORPHOGENESIS; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECURRENCE FREE SURVIVAL; SIGNAL TRANSDUCTION; UPREGULATION;

ANTINEOPLASTIC AGENTS, HORMONAL; APOPTOSIS REGULATORY PROTEINS; BREAST NEOPLASMS; CELL LINE, TUMOR; DISEASE-FREE SURVIVAL; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; HYPERPLASIA; MEMBRANE PROTEINS; MITOCHONDRIAL PROTEINS; NEOPLASMS, HORMONE-DEPENDENT; PROGNOSIS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, ESTROGEN; TAMOXIFEN; UP-REGULATION;

EID: 84860270474     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.393     Document Type: Article

References (63)

1. Anderson LR, Sutherland RL, Butt AJ. (2010). BAG-1 overexpression attenuates luminal apoptosis in MCF-10A mammary epithelial cells through enhanced RAF-1 activation. Oncogene 29: 527-538.
2. Bae SI, Cheriyath V, Jacobs BS, Reu FJ, Borden EC. (2008). Reversal of methylation silencing of Apo2L/TRAIL receptor 1 (DR4) expression overcomes resistance of SK-MEL-3 and SK-MEL-28 melanoma cells to interferons (IFNs) or Apo2L/TRAIL. Oncogene 27: 490-498.
3. Bani MR, Nicoletti MI, Alkharouf NW, Ghilardi C, Petersen D, Erba E. et al. (2004). Gene expression correlating with response to paclitaxel in ovarian carcinoma xenografts. Mol Cancer Ther 3: 111-121.
4. Bektas N, Noetzel E, Veeck J, Press MF, Kristiansen G, Naami A. et al. (2008). The ubiquitin-like molecule interferon-stimulated gene 15 (ISG15) is a potential prognostic marker in human breast cancer. Breast Cancer Res 10: R58.
5. Bharadwaj S, Thanawala R, Bon G, Falcioni R, Prasad GL. (2005). Resensitization of breast cancer cells to anoikis by tropomyosin-1: role of Rho kinase-dependent cytoskeleton and adhesion. Oncogene 24: 8291-8303.
6. Borden EC, Sen GC, Uze G, Silverman RH, Ransohoff RM, Foster GR. et al. (2007). Interferons at age 50: past, current and future impact on biomedicine. Nat Rev Drug Discov 6: 975-990.
7. Braig M, Schmitt CA. (2006). Oncogene-induced senescence: putting the brakes on tumor development. Cancer Res 66: 2881-2884.
8. Callagy GM, Webber MJ, Pharoah PD, Caldas C. (2008). Metaanalysis confirms BCL2 is an independent prognostic marker in breast cancer. BMC Cancer 8: 153.
9. Calogero RA, Cordero F, Forni G, Cavallo F. (2007). Inflammation and breast cancer. Inflammatory component of mammary carcinogenesis in ErbB2 transgenic mice. Breast Cancer Res 9: 211.
10. Chen DT, Nasir A, Culhane A, Venkataramu C, Fulp W, Rubio R. et al. (2010). Proliferative genes dominate malignancy-risk gene ignature in histologically-normal breast tissue. Breast Cancer Res Treat 119: 335-346.
11. Cheng AS, Culhane AC, Chan MW, Venkataramu CR, Ehrich M, Nasir A. et al. (2008). Epithelial progeny of estrogen-exposed breast progenitor cells display a cancer-like methylome. Cancer Res 68: 1786-1796.
12. Cheriyath V, Glaser KB, Waring JF, Baz R, Hussein MA, Borden EC. (2007). G1P3, an IFN-induced survival factor, antagonizes TRAIL-induced apoptosis in human myeloma cells. J Clin Invest 117: 3107-3117.
13. Cheriyath V, Leaman DW, Borden E. (2010). Emerging roles of FAM14 family members (G1P3/ISG(6-16) and ISG12) in innate immunity and cancer. J Interferon Cytokine Res 31: 173-181.
14. Cheriyath V, Leaman DW, Borden EC. (2011). Emerging roles of FAM14 family members (G1P3/ISG 6-16 and ISG12/IFI27) in innate immunity and cancer. J Interferon Cytokine Res 31: 173-181.
15. Chin K, DeVries S, Fridlyand J, Spellman PT, Roydasgupta R, Kuo WL. et al. (2006). Genomic and transcriptional aberrations linked to breast cancer pathophysiologies. Cancer Cell 10: 529-541.
16. Chin SF, Teschendorff AE, Marioni JC, Wang Y, Barbosa-Morais NL, Thorne NP. et al. (2007). High-resolution aCGH and expression profiling identifies a novel genomic subtype of ER negative breast cancer. Genome Biol 8: R215.
17. Dawson SJ, Makretsov N, Blows FM, Driver KE, Provenzano E, Le Quesne J. et al. (2010). BCL2 in breast cancer: a favourable prognostic marker across molecular subtypes and independent of adjuvant therapy received. Br J Cancer 103: 668-675.
18. Debnath J, Mills KR, Collins NL, Reginato MJ, Muthuswamy SK, Brugge JS. (2002). The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 111: 29-40.
19. Debnath J, Muthuswamy SK, Brugge JS. (2003). Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in threedimensional basement membrane cultures. Methods 30: 256-268.
20. DeNardo DG, Coussens LM. (2007). Inflammation and breast cancer. Balancing immune response: crosstalk between adaptive and innate immune cells during breast cancer progression. Breast Cancer Res 9: 212.
21. DeNardo DG, Johansson M, Coussens LM. (2008). Immune cells as mediators of solid tumor metastasis. Cancer Metast Rev 27: 11-18.
22. Desmedt C, Piette F, Loi S, Wang Y, Lallemand F, Haibe-Kains B. et al. (2007). Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin Cancer Res 13: 3207-3214.
23. de Visser KE, Eichten A, Coussens LM. (2006). Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 6: 24-37.
24. Dunn GP, Koebel CM, Schreiber RD. (2006). Interferons, immunity and cancer immunoediting. Nat Rev Immunol 6: 836-848.
25. Einav U, Tabach Y, Getz G, Yitzhaky A, Ozbek U, Amariglio N. et al. (2005). Gene expression analysis reveals a strong signature of an interferon-induced pathway in childhood lymphoblastic leukemia as well as in breast and ovarian cancer. Oncogene 24: 6367-6375.
26. Eroles P, Bosch A, Bermejo B, Lluch A. (2010). Mechanisms of resistance to hormonal treatment in breast cancer. Clin Transl Oncol 12: 246-252.
27. Franken NA, Rodermond HM, Stap J, Haveman J, van Bree C. (2006). Clonogenic assay of cells in vitro. Nat Protoc 1: 2315-2319.
28. Friedman RL, Manly SP, McMahon M, Kerr IM, Stark GR. (1984). Transcriptional and posttranscriptional regulation of interferoninduced gene expression in human cells. Cell 38: 745-755.
29. Gimenez-Bonafe P, Tortosa A, Perez-Tomas R. (2009). Overcoming drug resistance by enhancing apoptosis of tumor cells. Curr Cancer Drug Targets 9: 320-340.
30. Haqq C, Nosrati M, Sudilovsky D, Crothers J, Khodabakhsh D, Pulliam BL. et al. (2005). The gene expression signatures of melanoma progression. Proc Natl Acad Sci USA 102: 6092-6097.
31. Hebner C, Weaver VM, Debnath J. (2008). Modeling morphogenesis and oncogenesis in three-dimensional breast epithelial cultures. Annu Rev Pathol 3: 313-339.
32. Idziorek T, Estaquier J, De Bels F, Ameisen JC. (1995). YOPRO-1 permits cytofluorometric analysis of programmed cell death (apoptosis) without interfering with cell viability. J Immunol Methods 185: 249-258.
33. Jordan VC, O'Malley BW. (2007). Selective estrogen-receptor modulators and antihormonal resistance in breast cancer. J Clin Oncol 25: 5815-5824.
34. Luszcek R, Cheriyath V, Mekhail T, Borden E. (2010). Combinations of DNA methyltransferase and histone deacetylase inhibitors induce DNA damage in small cell lung cancer cells: correlation of resistance to interferon stimulated gene expression. Mol Cancer Therap 9: 2309-2321.
35. Ma XJ, Hilsenbeck SG, Wang W, Ding L, Sgroi DC, Bender RA. et al. (2006). The HOXB13:IL17BR expression index is a prognostic factor in early-stage breast cancer. J Clin Oncol 24: 4611-4619.
36. Mailleux AA, Overholtzer M, Brugge JS. (2008a). Lumen formation during mammary epithelial morphogenesis: insights from in vitro and in vivo models. Cell Cycle 7: 57-62.
37. Mailleux AA, Overholtzer M, Brugge JS. (2008b). Entosis, a cell death process related to cell cannibalism between tumor cells. Med Sci (Paris) 24: 246-248.
38. Mailleux AA, Overholtzer M, Schmelzle T, Bouillet P, Strasser A, Brugge JS. (2007a). BIM regulates apoptosis during mammary ductal morphogenesis, and its absence reveals alternative cell death mechanisms. Dev Cell 12: 221-234.
39. Mailleux AA, Overholtzer M, Schmelzle T, Bouillet P, Strasser A, Brugge JS. (2007b). BIM regulates apoptosis during mammary ductal morphogenesis, and its absence reveals alternative cell death mechanisms. Dev Cell 12: 221-234.
40. Mantovani A, Allavena P, Sica A, Balkwill F. (2008). Cancer-related inflammation. Nature 454: 436-444.
41. Miller TW, Hennessy BT, Gonzalez-Angulo AM, Fox EM, Mills GB, Chen H. et al. (2010). Hyperactivation of phosphatidylinositol-3 kinase promotes escape from hormone dependence in estrogen receptor-positive human breast cancer. J Clin Invest 120: 2406-2413.
42. Muthuswamy SK, Li D, Lelievre S, Bissell MJ, Brugge JS. (2001). ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat Cell Biol 3: 785-792.
43. Nelson CM, Bissell MJ. (2005). Modeling dynamic reciprocity: engineering three-dimensional culture models of breast architecture, function, and neoplastic transformation. Semin Cancer Biol 15: 342-352.
44. Nuovo GJ, Elton TS, Nana-Sinkam P, Volinia S, Croce CM, Schmittgen TD. (2009). A methodology for the combined in situ analyses of the precursor and mature forms of microRNAs and correlation with their putative targets. Nat Protoc 4: 107-115.
45. Parker N, Porter AC. (2004). Identification of a novel gene family that includes the interferon-inducible human genes 6-16 and ISG12. BMC Genomics 5: 8.
46. Puisieux A, Valsesia-Wittmann S, Ansieau S. (2006). A twist for urvival and cancer progression. Br J Cancer 94: 13-17.
47. Radisky ES, Radisky DC. (2007). Stromal induction of breast cancer:inflammation and invasion. Rev Endocr Metab Disord 8: 279-287.
48. Rasmussen UB, Wolf C, Mattei MG, Chenard MP, Bellocq JP,Chambon P. et al. (1993). Identification of a new interferon-alphainducible gene (p27) on human chromosome 14q32 and its expression in breast carcinoma. Cancer Res 53: 4096-4101.
49. Reginato MJ, Mills KR, Paulus JK, Lynch DK, Sgroi DC, Debnath J. et al. (2003). Integrins and EGFR coordinately regulate the pro-apoptotic protein Bim to prevent anoikis. Nat Cell Biol 5:733-740.
50. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA. et al. (2006). TM4 microarray software suite. Methods Enzymol 411: 134-193.
51. Segara D, Biankin AV, Kench JG, Langusch CC, Dawson AC,Skalicky DA. et al. (2005). Expression of HOXB2, a retinoic acid signaling target in pancreatic cancer and pancreatic intraepithelial neoplasia. Clin Cancer Res 11: 3587-3596.
52. Sorbello V, Fuso L, Sfiligoi C, Scafoglio C, Ponzone R, Biglia N et al.(2003). Quantitative real-time RT-PCR analysis of eight novel estrogen-regulated genes in breast cancer. Int J Biol Markers 18:123-129.
53. Sotiriou C, Wirapati P, Loi S, Harris A, Fox S, Smeds J. et al. (2006 Gene expression profiling in breast cancer: understanding the molecular basis of histologic grade to improve prognosis. J Natl Cancer Inst 98: 262-272.
54. Swan EA, Jasser SA, Holsinger FC, Doan D, Bucana C, Myers J.N. (2003). Acquisition of anoikis resistance is a critical step in the progression of oral tongue cancer. Oral Oncol 39: 648-655.
55. Tahara Jr E, Tahara H, Kanno M, Naka K, Takeda Y, Matsuzaki T. et al. (2005). G1P3, an interferon inducible gene 6-16, is expressed in gastric cancers and inhibits mitochondrial-mediated apoptosis in gastric cancer cell line TMK-1 cell. Cancer ImmunolImmunother 54:729-740.
56. Thomadaki H, Scorilas A. (2008). Molecular profile of the BCL2 family of the apoptosis related genes in breast cancer cells after treatment with cytotoxic/cytostatic drugs. Connect Tissue Res 49: 261-264.
57. Thomadaki H, Talieri M, Scorilas A. (2007). Prognostic value of the apoptosis related genes BCL2 and BCL2L12 in breast cancer.Cancer Lett 247: 48-55.
58. Tsai MH, Cook JA, Chandramouli GV, DeGraff W, Yan H, Zhao S. et al. (2007). Gene expression profiling of breast, prostate, and glioma cells following single versus fractionated doses of radiation. Cancer Res 67: 3845-3852.
59. Weichselbaum RR, Ishwaran H, Yoon T, Nuyten DS, Baker SW, Khodarev N. et al. (2008). An interferon-related gene signature for DNA damage resistance is a predictive marker for chemotherapy and radiation for breast cancer. Proc Natl Acad Sci USA 105: 18490-18495.
60. Weigelt B, Bissell MJ. (2008). Unraveling the microenvironmental influences on the normal mammary gland and breast cancer. Semin Cancer Biol 18: 311-321.
61. Wurmbach E, Chen YB, Khitrov G, Zhang W, Roayaie S, SchwartzM. et al. (2007). Genome-wide molecular profiles of HCV-induced dysplasia and hepatocellular carcinoma. Hepatology 45: 938-947.
62. Ye H, Yu T, Temam S, Ziober BL, Wang J, Schwartz JL. et al. (2008).Transcriptomic dissection of tongue squamous cell carcinoma.BMC Genomics 9: 69.
63. Zhang HP, Singer B. (1999). Recursive Partitioning in the Health Sciences. Springer: New York.