Hypoxia modulates A431 cellular pathways association to tumor radioresistance and enhanced migration revealed by comprehensive proteomic and functional studies

Molecular and Cellular Proteomics

Volumn 12, Issue 2, 2013, Pages 485-498

  Ren, Yan ^a   Hao, Piliang ^a   Dutta, Bamaprasad ^a   Cheow, Esther Sok Hwee ^a   Sim, Kae Hwan ^a   Gan, Chee Sian ^b   Lim, Sai Kiang ^c   Sze, Siu Kwan ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b AGILENT TECHNOLOGIES   (Singapore)

^c INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CITRATE SYNTHASE; DEOXYGLUCOSE; FIBRONECTIN; FUMARATE HYDRATASE; GLUCOSE 6 PHOSPHATE ISOMERASE; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 3; GLYCOPROTEIN; GLYCOSYLTRANSFERASE; HEXOKINASE; INTEGRIN; LACTATE DEHYDROGENASE; MALATE DEHYDROGENASE; OXOGLUTARATE DEHYDROGENASE; PROTEIN; PYRUVATE DEHYDROGENASE; STAT1 PROTEIN;

ARTICLE; CELL ADHESION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; GLUCOSE METABOLISM; GLYCOLYSIS; HYPOXIA; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; METASTASIS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEOMICS; RADIOSENSITIVITY; REOXYGENATION; UPREGULATION; WESTERN BLOTTING;

ANTIGENS, NUCLEAR; CELL ADHESION; CELL HYPOXIA; CELL LINE, TUMOR; CELL MOVEMENT; DNA END-JOINING REPAIR; DNA-BINDING PROTEINS; GAMMA RAYS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTEGRINS; NEOPLASMS; OXIDATIVE STRESS; PROTEIN MULTIMERIZATION; PROTEIN SYNTHESIS INHIBITORS; PROTEOMICS; RADIATION TOLERANCE; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR;

EID: 84874102235     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.018325     Document Type: Article

References (91)

1. Brown, J. M., and Giaccia, A. J. (1998) The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res. 58, 1408-1416
2. Harris, A. L. (2002) Hypoxia-a key regulatory factor in tumour growth. Nat. Rev. Cancer 2, 38-47
3. Park, J. E., Tan, H. S., Datta, A., Lai, R. C., Zhang, H., Meng, W., Lim, S. K., and Sze, S. K. (2010) Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes. Mol. Cell. Proteomics 9, 1085-1099
4. Wilson, W. R., and Hay, M. P. (2011) Targeting hypoxia in cancer therapy. Nat. Rev. Cancer 11, 393-410
5. Gray, L. H., Conger, A. D., Ebert, M., Hornsey, S., and Scott, O. C. (1953) The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy. Br. J. Radiol. 26, 638-648
6. Moulder, J. E., and Rockwell, S. (1987) Tumor hypoxia: its impact on cancer therapy. Cancer Metastasis Rev. 5, 313-341
7. Le Q. T., Giaccia A. J., and Brown J. M. (2005) Squamous Cell Head and Neck Cancer: The role of tumor hypoxia in head and neck cancer radiotherapy, pp. 145-163, Cleveland Clinic Foundation
8. Liu, J., Zhang, J., Wang, X., Li, Y., Chen, Y., Li, K., Zhang, J., Yao, L., and Guo, G. (2010) HIF-1 and NDRG2 contribute to hypoxia-induced radioresistance of cervical cancer Hela cells. Exp. Cell Res. 316, 1985-1993
9. Moeller, B. J., and Dewhirst, M. W. (2006) HIF-1 and tumour radiosensitiv- ity. Br. J. Cancer 95, 1-5
10. Markowska, J., Grabowski, J. P., Tomaszewska, K., Kojs, Z., Pudelek, J., Skrzypczak, M., Sobotkowski, J., Emerich, J., Olejek, A., and Filas, V. (2007) Significance of hypoxia in uterine cervical cancer. Multicentre study. Eur. J. Gynaecol. Oncol. 28, 386-388
11. Dellas, K., Bache, M., Pigorsch, S. U., Taubert, H., Kappler, M., Holzapfel, D., Zorn, E., Holzhausen, H. J., and Haensgen, G. (2008) Prognostic impact of HIF-1alpha expression in patients with definitive radiotherapy for cervical cancer. Strahlenther Onkol.184, 169-174
12. Tribius, S., Pidel, A., and Casper, D. (2001) ATM protein expression corre- lates with radioresistance in primary glioblastoma cells in culture. Int. J. Radiat. Oncol. Biol. Phys. 50, 511-523
13. Munshi, A., Kurland, J. F., Nishikawa, T., Tanaka, T., Hobbs, M. L., Tucker, S. L., Ismail, S., Stevens, C., and Meyn, R. E. (2005) Histone deacetylase inhibitors radiosensitize human melanoma cells by suppressing DNA repair activity. Clin. Cancer Res. 11, 4912-4922
14. Meng, A. X., Jalali, F., Cuddihy, A., Chan, N., Bindra, R. S., Glazer, P. M., and Bristow, R. G. (2005) Hypoxia down-regulates DNA double strand break repair gene expression in prostate cancer cells. Radiother. Oncol. 76, 168-176
15. Bindra, R. S., Schaffer, P. J., Meng, A., Woo, J., Maseide, K., Roth, M. E., Lizardi, P., Hedley, D. W., Bristow, R. G., and Glazer, P. M. (2004) Down-regulation of Rad51 and decreased homologous recombination in hypoxic cancer cells. Mol. Cell. Biol. 24, 8504-8518
16. Bindra, R. S., Schaffer, P. J., Meng, A., Woo, J., Maseide, K., Roth, M. E., Lizardi, P., Hedley, D. W., Bristow, R. G., and Glazer, P. M. (2005) Alterations in DNA repair gene expression under hypoxia: elucidating the mechanisms of hypoxia-induced genetic instability. Ann. N.Y. Acad. Sci. 1059, 184-195
17. Bindra, R. S., Gibson, S. L., Meng, A., Westermark, U., Jasin, M., Pierce, A. J., Bristow, R. G., Classon, M. K., and Glazer, P. M. (2005) Hypoxiainduced down-regulation of BRCA1 expression by E2Fs. Cancer Res. 65, 11597-11604
18. Graeber, T. G., Osmanian, C., Jacks, T., Housman, D. E., Koch, C. J., Lowe, S. W., and Giaccia, A. J. (1996) Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379, 88-91
19. Young, S. D., Marshall, R. S., and Hill, R. P. (1988) Hypoxia induces DNA overreplication and enhances metastatic potential of murine tumor cells. Proc. Natl. Acad. Sci. U.S.A. 85, 9533-9537
20. Brizel, D. M., Scully, S. P., Harrelson, J. M., Layfield, L. J., Bean, J. M., Prosnitz, L. R., and Dewhirst, M. W. (1996) Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma. Cancer Res. 56, 941-943
21. Cairns, R. A., and Hill, R. P. (2004) Acute hypoxia enhances spontaneous lymph node metastasis in an orthotopic murine model of human cervical carcinoma. Cancer Res. 64, 2054-2061
22. Fyles, A., Milosevic, M., Hedley, D., Pintilie, M., Levin, W., Manchul, L., and Hill, R. P. (2002) Tumor hypoxia has independent predictor impact only in patients with node-negative cervix cancer. J. Clin. Oncol. 20, 680-687
23. Liotta, L. A., Kleinerman, J., Catanzaro, P., and Rynbrandt, D. (1977) Degradation of basement membrane by murine tumor cells. J. Natl. Cancer Inst. 58, 1427-1431
24. Montagner, M., Enzo, E., Forcato, M., Zanconato, F., Parenti, A., Rampazzo, E., Basso, G., Leo, G., Rosato, A., Bicciato, S., Cordenonsi, M., and Piccolo, S. (2012) SHARP1 suppresses breast cancer metastasis by promoting degradation of hypoxia-inducible factors. Nature 487, 380-384
25. Sahai, E. (2007) Illuminating the metastatic process. Nat. Rev. Cancer 7, 737-749
26. Horwitz, A. R., and Parsons, J. T. (1999) Cell migration-movin' on. Science 286, 1102-1103
27. Yoon, S. O., Park, S. J., Yun, C. H., and Chung, A. S. (2003) Roles of matrix metalloproteinases in tumor metastasis and angiogenesis. J. Biochem. Mol. Biol. 36, 128-137
28. Liao, S. H., Zhao, X. Y., Han, Y. H., Zhang, J., Wang, L. S., Xia, L., Zhao, K. W., Zheng, Y., Guo, M., and Chen, G. Q. (2009) Proteomics-based identification of two novel direct targets of hypoxia-inducible factor-1 and their potential roles in migration/invasion of cancer cells. Proteomics 9, 3901-3912
29. Arimoto-Ishida, E., Sakata, M., Sawada, K., Nakayama, M., Nishimoto, F., Mabuchi, S., Takeda, T., Yamamoto, T., Isobe, A., Okamoto, Y., Lengyel, E., Suehara, N., Morishige, K., and Kimura, T. (2009) Up-regulation of alpha5-integrin by E-cadherin loss in hypoxia and its key role in the migration of extravillous trophoblast cells during early implantation. Endocrinology 150, 4306-4315
30. Kim, S. H., Xia, D., Kim, S. W., Holla, V., Menter, D. G., and Dubois, R. N. (2010) Human enhancer of filamentation 1 Is a mediator of hypoxiainducible factor-1alpha-mediated migration in colorectal carcinoma cells. Cancer Res. 70, 4054-4063
31. Kuonen, F., Secondini, C., and Ruegg, C. (2012) Molecular Pathways: Emerging pathways mediating growth, invasion and metastasis of tumors progressing in an irradiated microenvironment. Clin. Cancer Res.
32. Stockwin, L. H., Blonder, J., Bumke, M. A., Lucas, D. A., Chan, K. C., Conrads, T. P., Issaq, H. J., Veenstra, T. D., Newton, D. L., and Rybak, S. M. (2006) Proteomic analysis of plasma membrane from hypoxiaadapted malignant melanoma. J. Proteome Res. 5, 2996-3007
33. Sørensen, B. S., Horsman, M. R., Vorum, H., Honoré, B., Overgaard, J., and Alsner, J. (2009) Proteins upregulated by mild and severe hypoxia in squamous cell carcinomas in vitro identified by proteomics. Radiother. Oncol. 92, 443-449
34. Vorum, H., østergaard, M., Hensechke, P., Enghild, J. J., Riazati, M., and Rice, G. E. (2004) Proteomic analysis of hyperoxia-induced responses in the human choriocarcinoma cell line JEG-3. Proteomics 4, 861-867
35. Kumar, G. K., and Klein, J. B. (2004) Analysis of expression and posttrans- lational modification of proteins during hypoxia. J. Appl. Physiol. 96, 1178-1186; discussion 1170-1172
36. Dettmer, K., Nürnberger, N., Kaspar, H., Gruber, M. A., Almstetter, M. F., and Oefner, P. J. (2011) Metabolite extraction from adherently growing mammalian cells for metabolomics studies: optimization of harvesting and extraction protocols. Anal. Bioanal. Chem. 399, 1127-1139
37. Finley, L. W., Carracedo, A., Lee, J., Souza, A., Egia, A., Zhang, J., Teruya-Feldstein, J., Moreira, P. I., Cardoso, S. M., Clish, C. B., Pandolfi, P. P., and Haigis, M. C. (2011) SIRT3 opposes reprogramming of cancer cell metabolism through HIF1alpha destabilization. Cancer Cell 19, 416-428
38. Lara, P. C., Lloret, M., Clavo, B., Apolinario, R. M., Bordon, E., Rey, A., Falcon, O., Alonso, A. R., and Belka, C. (2008) Hypoxia downregulates Ku70/80 expression in cervical carcinoma tumors. Radiother. Oncol. 89, 222-226
39. Chen, D. J., and Nirodi, C. S. (2007) The epidermal growth factor receptor: a role in repair of radiation-induced DNA damage. Clin. Cancer Res. 13, 6555-6560
40. Ting, N. S., Chan, D. W., Lintott, L. G., Allalunis-Turner, J., and Lees-Miller, S. P. (1999) Protein-DNA complexes containing DNA-dependent protein kinase in crude extracts from human and rodent cells. Radiat. Res. 151, 414-422
41. Lou, Z., Chen, B. P., Asaithamby, A., Minter-Dykhouse, K., Chen, D. J., and Chen, J. (2004) MDC1 regulates DNA-PK autophosphorylation in response to DNA damage. J. Biol. Chem. 279, 46359-46362
42. Salton, M., Lerenthal, Y., Wang, S. Y., Chen, D. J., and Shiloh, Y. (2010) Involvement of Matrin 3 and SFPQ/NONO in the DNA damage response. Cell Cycle 9, 1568-1576
43. Kumari, A., Mazina, O. M., Shinde, U., Mazin, A. V., and Lu, H. (2009) A role for SSRP1 in recombination-mediated DNA damage response. J. Cell. Biochem. 108, 508-518
44. Li, Y., Bolderson, E., Kumar, R., Muniandy, P. A., Xue, Y., Richard, D. J., Seidman, M., Pandita, T. K., Khanna, K. K., and Wang, W. (2009) HSSB1 and hSSB2 form similar multiprotein complexes that participate in DNA damage response. J. Biol. Chem. 284, 23525-23531
45. Clements, P. M., Breslin, C., Deeks, E. D., Byrd, P. J., Ju, L., Bieganowski, P., Brenner, C., Moreira, M. C., Taylor, A. M., and Caldecott, K. W. (2004) The ataxia-oculomotor apraxia 1 gene product has a role distinct from ATM and interacts with the DNA strand break repair proteins XRCC1 and XRCC4. DNA Repair 3, 1493-1502
46. Mahajan, K. N., and Mitchell, B. S. (2003) Role of human Pso4 in mamma- lian DNA repair and association with terminal deoxynucleotidyl transferase. Proc. Natl. Acad. Sci. U.S.A. 100, 10746-10751
47. Boros, L. G., Lee, W. N., and Go, V. L. (2002) A metabolic hypothesis of cell growth and death in pancreatic cancer. Pancreas 24, 26-33
48. Chen, C., Pore, N., Behrooz, A., Ismail-Beigi, F., and Maity, A. (2001) Regulation of glut1 mRNA by hypoxia-inducible factor-1. Interaction between H-ras and hypoxia. J. Biol. Chem. 276, 9519-9525
49. Mikuriya, K., Kuramitsu, Y., Ryozawa, S., Fujimoto, M., Mori, S., Oka, M., Hamano, K., Okita, K., Sakaida, I., and Nakamura, K. (2007) Expression of glycolytic enzymes is increased in pancreatic cancerous tissues as evidenced by proteomic profiling by two-dimensional electrophoresis and liquid chromatography-mass spectrometry/mass spectrometry. Int. J. Oncol. 30, 849-855
50. Cai, Z., Zhao, J. S., Li, J. J., Peng, D. N., Wang, X. Y., Chen, T. L., Qiu, Y. P., Chen, P. P., Li, W. J., Xu, L. Y., Li, E. M., Tam, J. P., Qi, R. Z., Jia, W., and Xie, D. (2010) A combined proteomics and metabolomics profiling of gastric cardia cancer reveals characteristic dysregulations in glucose metabolism. Mol. Cell. Proteomics 9, 2617-2628
51. Izumi, H., Takahashi, M., Uramoto, H., Nakayama, Y., Oyama, T., Wang, K. Y., Sasaguri, Y., Nishizawa, S., and Kohno, K. (2011) Monocarboxylate transporters 1 and 4 are involved in the invasion activity of human lung cancer cells. Cancer Sci. 102, 1007-1013
52. Fan, J., Zhou, J. Q., Yu, G. R., and Lu, D. D. (2010) Glucose transporter protein 1-targeted RNA interference inhibits growth and invasion of the osteosarcoma cell line MG63 in vitro. Cancer Biother. Radiopharm. 25, 521-527
53. Maschek, G., Savaraj, N., Priebe, W., Braunschweiger, P., Hamilton, K., Tidmarsh, G. F., De Young, L. R., and Lampidis, T. J. (2004) 2-deoxyD-glucose increases the efficacy of adriamycin and paclitaxel in human osteosarcoma and non-small cell lung cancers in vivo. Cancer Res. 64, 31-34
54. Zhong, D., Xiong, L., Liu, T., Liu, X., Liu, X., Chen, J., Sun, S. Y., Khuri, F. R., Zong, Y., Zhou, Q., and Zhou, W. (2009) The glycolytic inhibitor 2-deoxyglucose activates multiple prosurvival pathways through IGF1R. J. Biol. Chem. 284, 23225-23233
55. Gilcrease, M. Z., Truong, L., and Brown, R. W. (1996) Correlation of very late activation integrin and CD44 expression with extrarenal invasion and metastasis of renal cell carcinomas. Hum. Pathol. 27, 1355-1360
56. Hynes, R. O. (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687
57. Chammas, R., and Brentani, R. (1991) Integrins and metastases: an over- view. Tumour Biol. 12, 309-320
58. Janik, M. E., Lityńska, A., and Vereecken, P. (2010) Cell migration-the role of integrin glycosylation. Biochim. Biophys. Acta 1800, 545-555
59. Leitinger, B., and Hohenester, E. (2007) Mammalian collagen receptors. Matrix Biol. 26, 146-155
60. Ryu, M. H., Park, H. M., Chung, J., Lee, C. H., and Park, H. R. (2010) Hypoxia-inducible factor-1alpha mediates oral squamous cell carcinoma invasion via upregulation of alpha5 integrin and fibronectin. Biochem. Biophys. Res. Commun. 393, 11-15
61. Hogg, N., and Landis, R. C. (1993) Adhesion molecules in cell interactions. Curr. Opin. Immunol. 5, 383-390
62. Fitsialos, G., Bourget, I., Augier, S., Ginouvès, A., Rezzonico, R., Odorisio, T., Cianfarani, F., Virolle, T., Pouyssé gur, J., Meneguzzi, G., Berra, E., Ponzio, G., and Busca, R. (2008) HIF1 transcription factor regulates laminin-332 expression and keratinocyte migration. J. Cell Sci. 121, 2992-3001
63. Kajimoto, T., and Node, M. (2009) Inhibitors against glycosidases as med- icines. Curr. Top. Med. Chem. 9, 13-33
64. Elbein, A. D. (1991) Glycosidase inhibitors: inhibitors of N-linked oligosac- charide processing. FASEB J 5, 3055-3063
65. Kornfeld, R., and Kornfeld, S. (1985) Assembly of asparagine-linked oligo- saccharides. Annu. Rev. Biochem. 54, 631-664
66. Zhao, Y., Liu, W., Zhou, Y., Zhang, X., and Murphy, P. V. (2010) N-(8-(3- ethynylphenoxy)octyl-1-deoxynojirimycin suppresses growth and migration of human lung cancer cells. Bioorg. Med. Chem. Lett. 20, 7540-7543
67. Shuai, K., Schindler, C, Prezioso, V. R., and Darnell, J. E., Jr. (1992) Activation of transcription by IFN-gamma: tyrosine phosphorylation of a 91-kD DNA binding protein. Science 258, 1808-1812
68. Schindler, C, Levy, D. E., and Decker, T. (2007) JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 282, 20059-20063
69. Khodarev, N. N., Roach, P., Pitroda, S. P., Golden, D. W., Bhayani, M., Shao, M. Y., Darga, T. E., Beveridge, M. G., Sood, R. F., Sutton, H. G., Beckett, M. A., Mauceri, H. J., Posner, M. C, and Weichselbaum, R. R. (2009) STAT1 pathway mediates amplification of metastatic potential and resistance to therapy. PLoS One 4, e5821
70. Wen, Z., Zhong, Z., and Darnell, J. E., Jr. (1995) Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82, 241-250
71. Decker, T., and Kovarik, P. (2000) Serine phosphorylation of STATs. On- cogene 19, 2628-2637
72. Ouchi, T., Lee, S. W., Ouchi, M., Aaronson, S. A., and Horvath, C. M. (2000) Collaboration of signal transducer and activator of transcription 1 (STAT1) and BRCA1 in differential regulation of IFN-gamma target genes. Proc. Natl. Acad. Sci. U.S.A. 97, 5208-5213
73. Zhang, J. J., Zhao, Y., Chait, B. T., Lathem, W. W., Ritzi, M., Knippers, R., and Darnell, J. E., Jr. (1998) Ser727-dependent recruitment of MCM5 by STAT1 αlpha in IFN-gamma-induced transcriptional activation. EMBO J. 17, 6963-6971
74. Pine, R. (1997) Convergence of TNFalpha and IFNgamma signalling path- ways through synergistic induction of IRF-1/ISGF-2 is mediated by a composite GAS/kappaB promoter element. Nucleic Acids Res. 25, 4346-4354
75. Mamane, Y., Heylbroeck, C, Genin, P., Algarte, M., Servant, M. J., LePage, C, DeLuca, C, Kwon, H., Lin, R., and Hiscott, J. (1999) Interferon regulatory factors: the next generation. Gene 237, 1-14
76. Liu, B., Liao, J., Rao, X., Kushner, S. A., Chung, C. D., Chang, D. D., and Shuai, K. (1998) Inhibition of Stat1-mediated gene activation by PIAS1. Proc. Natl. Acad. Sci. U.S.A. 95, 10626-10631
77. Lee, M. Y., Joung, Y. H., Lim, E. J., Park, J. H., Ye, S. K., Park, T., Zhang, Z., Park, D. K., Lee, K. J., and Yang, Y. M. (2006) Phosphorylation and activation of STAT proteins by hypoxia in breast cancer cells. Breast 15, 187-195
78. Terui, K., Haga, S., Enosawa, S., Ohnuma, N., and Ozaki, M. (2004) Hypoxia/re-oxygenation-induced, redox-dependent activation of STAT1 (signal transducer and activator of transcription 1) confers resistance to apoptotic cell death via hsp70 induction. Biochem. J. 380, 203-209
79. Stephanou, A., Brar, B. K., Scarabelli, T. M., Jonassen, A. K., Yellon, D. M., Marber, M. S., Knight, R. A., and Latchman, D. S. (2000) Ischemiainduced STAT-1 expression and activation play a critical role in cardiomyocyte apoptosis. J. Biol. Chem. 275, 10002-10008
80. Stephanou, A. (2002) Activated STAT-1 pathway in the myocardium as a novel therapeutic target in ischaemia/reperfusion injury. Eur. Cytokine Netw. 13, 401-403
81. Ivanov, S. V., Salnikow, K., Ivanova, A. V., Bai, L., and Lerman, M. I. (2007) Hypoxic repression of STAT1 and its downstream genes by a pVHL/ HIF-1 target DEC1/STRA13. Oncogene 26, 802-812
82. Chin, Y. E., Kitagawa, M., Su, W. C, You, Z. H., Iwamoto, Y., and Fu, X. Y. (1996) Cell growth arrest and induction of cyclin-dependent kinase inhibitor p21 WAF1/CIP1 mediated by STAT1. Science 272, 719-722
83. Chin, Y. E., Kitagawa, M., Kuida, K., Flavell, R. A., and Fu, X. Y. (1997) Activation of the STAT signaling pathway can cause expression of caspase 1 and apoptosis. Mol. Cell. Biol. 17, 5328-5337
84. Bromberg, J. F., Fan, Z., Brown, C, Mendelsohn, J., and Darnell, J. E., Jr. (1998) Epidermal growth factor-induced growth inhibition requires Stat1 activation. Cell Growth Differ. 9, 505-512
85. Taniguchi, T. (1997) Transcription factors IRF-1 and IRF-2: linking the immune responses and tumor suppression. J. Cell. Physiol. 173, 128-130
86. Lee, K. Y., Anderson, E., Madani, K., and Rosen, G. D. (1999) Loss of STAT1 expression confers resistance to IFN-gamma-induced apoptosis in ME180 cells. FEBS Lett. 459, 323-326
87. Hiroi, M., Mori, K., Sakaeda, Y., Shimada, J., and Ohmori, Y. (2009) STAT1 represses hypoxia-inducible factor-1-mediated transcription. Biochem. Biophys. Res. Commun. 387, 806-810
88. Huang, S., Bucana, C. D., Van Arsdall, M., and Fidler, I. J. (2002) Stat1 negatively regulates angiogenesis, tumorigenicity and metastasis of tumor cells. Oncogene 21, 2504-2512
89. Hu, Y., Hu, X., Boumsell, L., and Ivashkiv, L. B. (2008) IFN-gamma and STAT1 arrest monocyte migration and modulate RAC/CDC42 pathways. J. Immunol. 180, 8057-8065
90. Dutreix, M., Cosset, J. M., and Sun, J. S. (2010) Molecular therapy in support to radiotherapy. Mutat. Res. 704, 182-189
91. Kim, Y. J., and Varki, A. (1997) Perspectives on the significance of altered glycosylation of glycoproteins in cancer. Glycoconj. J. 14, 569-576