The NF-κB p65 and p50 homodimer cooperate with IRF8 to activate iNOS transcription

BMC Cancer

Volumn 15, Issue 1, 2015, Pages

  Simon, Priscilla S ^a,b   Sharman, Sarah K ^a   Lu, Chunwan ^a,b   Yang, Dafeng ^a,b   Paschall, Amy V ^a,b   Tulachan, Sidhartha S ^a   Liu, Kebin ^a,b  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Colon cancer; IFN ; INOS; IRF8; NF B; PSTAT1

Indexed keywords

CHROMATIN DNA; DNA; GAMMA INTERFERON; HOMODIMER; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; STAT1 PROTEIN; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; INTERFERON REGULATORY FACTOR; NOS2 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; COLON; COLON CARCINOMA; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; NOS2 GENE; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TUMOR MICROENVIRONMENT; UPREGULATION; ANIMAL; COLON TUMOR; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; COLON; COLONIC NEOPLASMS; HUMANS; INTERFERON REGULATORY FACTORS; INTERFERON-GAMMA; MICE; MYELOID CELLS; NF-KAPPA B P50 SUBUNIT; NITRIC OXIDE SYNTHASE TYPE II; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTOR RELA; TUMOR MICROENVIRONMENT;

EID: 84945124329     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/s12885-015-1808-6     Document Type: Article

References (63)

1. Mishra BB, Rathinam VA, Martens GW, Martinot AJ, Kornfeld H, Fitzgerald KA, et al. Nitric oxide controls the immunopathology of tuberculosis by inhibiting NLRP3 inflammasome-dependent processing of IL-1beta. Nat Immunol. 2013;14:52-60.
2. Nascimento FR, Gomes EA, Russo M, Lepique AP. Interferon regulatory factor (IRF)-1 is a master regulator of the cross talk between macrophages and L929 fibrosarcoma cells for nitric oxide dependent tumoricidal activity. PLoS One. 2015;10:e0117782.
3. Crowell JA, Steele VE, Sigman CC, Fay JR. Is inducible nitric oxide synthase a target for chemoprevention? Mol Cancer Ther. 2003;2:815-23.
4. Fukumura D, Kashiwagi S, Jain RK. The role of nitric oxide in tumour progression. Nat Rev Cancer. 2006;6:521-34.
5. Kotamraju S, Williams CL, Kalyanaraman B. Statin-induced breast cancer cell death: role of inducible nitric oxide and arginase-dependent pathways. Cancer Res. 2007;67:7386-94.
6. Cook T, Wang Z, Alber S, Liu K, Watkins SC, Vodovotz Y, et al. Nitric oxide and ionizing radiation synergistically promote apoptosis and growth inhibition of cancer by activating p53. Cancer Res. 2004;64:8015-21.
7. Ramasamy K, Dwyer-Nield LD, Serkova NJ, Hasebroock KM, Tyagi A, Raina K, et al. Silibinin prevents lung tumorigenesis in wild-type but not in iNOS-/- mice: potential of real-time micro-CT in lung cancer chemoprevention studies. Clin Cancer Res. 2011;17:753-61.
8. Coursey TG, Chen PW, Niederkorn JY. Abrogating TNF-alpha expression prevents bystander destruction of normal tissues during iNOS-mediated elimination of intraocular tumors. Cancer Res. 2011;71:2445-54.
9. Mehibel M, Singh S, Chinje EC, Cowen RL, Stratford IJ. Effects of cytokine-induced macrophages on the response of tumor cells to banoxantrone (AQ4N). Mol Cancer Ther. 2009;8:1261-9.
10. Liu Q, Chan ST, Mahendran R. Nitric oxide induces cyclooxygenase expression and inhibits cell growth in colon cancer cell lines. Carcinogenesis. 2003;24:637-42.
11. Moochhala S, Chhatwal VJ, Chan ST, Ngoi SS, Chia YW, Rauff A. Nitric oxide synthase activity and expression in human colorectal cancer. Carcinogenesis. 1996;17:1171-4.
12. Hao XP, Pretlow TG, Rao JS, Pretlow TP. Inducible nitric oxide synthase (iNOS) is expressed similarly in multiple aberrant crypt foci and colorectal tumors from the same patients. Cancer Res. 2001;61:419-22.
13. Scott DJ, Hull MA, Cartwright EJ, Lam WK, Tisbury A, Poulsom R, et al. Lack of inducible nitric oxide synthase promotes intestinal tumorigenesis in the Apc(Min/+) mouse. Gastroenterology. 2001;121:889-99.
14. Hussain SP, Trivers GE, Hofseth LJ, He P, Shaikh I, Mechanic LE, et al. Nitric oxide, a mediator of inflammation, suppresses tumorigenesis. Cancer Res. 2004;64:6849-53.
15. De Boo S, Kopecka J, Brusa D, Gazzano E, Matera L, Ghigo D, et al. iNOS activity is necessary for the cytotoxic and immunogenic effects of doxorubicin in human colon cancer cells. Mol Cancer. 2009;8:108.
16. Cianchi F, Cortesini C, Fantappie O, Messerini L, Schiavone N, Vannacci A, et al. Inducible nitric oxide synthase expression in human colorectal cancer: correlation with tumor angiogenesis. Am J Pathol. 2003;162:793-801.
17. Gochman E, Mahajna J, Shenzer P, Dahan A, Blatt A, Elyakim R, et al. The expression of iNOS and nitrotyrosine in colitis and colon cancer in humans. Acta Histochem. 2012;114:827-35.
18. Erdman SE, Rao VP, Poutahidis T, Rogers AB, Taylor CL, Jackson EA, et al. Nitric oxide and TNF-alpha trigger colonic inflammation and carcinogenesis in Helicobacter hepaticus-infected, Rag2-deficient mice. Proc Natl Acad Sci U S A. 2009;106:1027-32.
19. Sikora AG, Gelbard A, Davies MA, Sano D, Ekmekcioglu S, Kwon J, et al. Targeted inhibition of inducible nitric oxide synthase inhibits growth of human melanoma in vivo and synergizes with chemotherapy. Clin Cancer Res. 2010;16:1834-44.
20. Engels K, Knauer SK, Loibl S, Fetz V, Harter P, Schweitzer A, et al. NO signaling confers cytoprotectivity through the survivin network in ovarian carcinomas. Cancer Res. 2008;68:5159-66.
21. Cianchi F, Cortesini C, Fantappie O, Messerini L, Sardi I, Lasagna N, et al. Cyclooxygenase-2 activation mediates the proangiogenic effect of nitric oxide in colorectal cancer. Clin Cancer Res. 2004;10:2694-704.
22. Ahn B, Ohshima H. Suppression of intestinal polyposis in Apc(Min/+) mice by inhibiting nitric oxide production. Cancer Res. 2001;61:8357-60.
23. Nam KT, Oh SY, Ahn B, Kim YB, Jang DD, Yang KH, et al. Decreased Helicobacter pylori associated gastric carcinogenesis in mice lacking inducible nitric oxide synthase. Gut. 2004;53:1250-5.
24. Lopez-Rivera E, Jayaraman P, Parikh F, Davies MA, Ekmekcioglu S, Izadmehr S, et al. Inducible nitric oxide synthase drives mTOR pathway activation and proliferation of human melanoma by reversible nitrosylation of TSC2. Cancer Res. 2014;74:1067-78.
25. Cheng H, Wang L, Mollica M, Re AT, Wu S, Zuo L. Nitric oxide in cancer metastasis. Cancer Lett. 2014;353:1-7.
26. Hanada T, Kobayashi T, Chinen T, Saeki K, Takaki H, Koga K, et al. IFNgamma-dependent, spontaneous development of colorectal carcinomas in SOCS1-deficient mice. J Exp Med. 2006;203:1391-7.
27. Ausiliatrice Puglisi M, Cenciarelli C, Tesori V, Cappellari M, Martini M, Di Francesco AM, et al. High nitric oxide production, secondary to inducible-nitric oxide synthase expression, is essential for regulation of the tumour-initiating properties of colon cancer stem cells. J Pathol. 2015.
28. Granados-Principal S, Liu Y, Guevara ML, Blanco E, Choi DS, Qian W, et al. Inhibition of iNOS as a novel effective targeted therapy against triple-negative breast cancer. Breast Cancer Res. 2015;17:25.
29. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol. 2012;12:253-68.
30. Mundy-Bosse BL, Lesinski GB, Jaime-Ramirez AC, Benninger K, Khan M, Kuppusamy P, et al. Myeloid-derived suppressor cell inhibition of the IFN response in tumor-bearing mice. Cancer Res. 2011;71:5101-10.
31. Ito H, Ando T, Ogiso H, Arioka Y, Seishima M. Inhibition of induced nitric oxide synthase enhances the anti-tumor effects on cancer immunotherapy using TLR7 agonist in mice. Cancer Immunol Immunother. 2015;64:429-36.
32. Dufait I, Schwarze JK, Liechtenstein T, Leonard W, Jiang H, Escors D, et al. Ex vivo generation of myeloid-derived suppressor cells that model the tumor immunosuppressive environment in colorectal cancer. Oncotarget. 2015.
33. Lu G, Zhang R, Geng S, Peng L, Jayaraman P, Chen C, et al. Myeloid cell-derived inducible nitric oxide synthase suppresses M1 macrophage polarization. Nat Commun. 2015;6:6676.
34. Jayaraman P, Alfarano MG, Svider PF, Parikh F, Lu G, Kidwai S, et al. iNOS expression in CD4+ T cells limits Treg induction by repressing TGFbeta1: combined iNOS inhibition and Treg depletion unmask endogenous antitumor immunity. Clin Cancer Res. 2014;20:6439-51.
35. Hatano E, Bennett BL, Manning AM, Qian T, Lemasters JJ, Brenner DA. NF-kappaB stimulates inducible nitric oxide synthase to protect mouse hepatocytes from TNF-alpha- and Fas-mediated apoptosis. Gastroenterology. 2001;120:1251-62.
36. Thurston RD, Larmonier CB, Majewski PM, Ramalingam R, Midura-Kiela M, Laubitz D, et al. Tumor necrosis factor and interferon-gamma down-regulate Klotho in mice with colitis. Gastroenterology. 2010;138:1384-94. 1394 e1381-1382.
37. Davis RL, Sanchez AC, Lindley DJ, Williams SC, Syapin PJ. Effects of mechanistically distinct NF-kB inhibitors on glial inducible nitric-oxide synthase expression. Nitric Oxide. 2005;12:200-9.
38. Chen F, Castranova V. Nuclear factor-kappaB, an unappreciated tumor suppressor. Cancer Res. 2007;67:11093-8.
39. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, Egan LJ, et al. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell. 2004;118:285-96.
40. Liu F, Bardhan K, Yang D, Thangaraju M, Ganapathy V, Waller JL, et al. NF-kappaB Directly Regulates Fas Transcription to Modulate Fas-mediated Apoptosis and Tumor Suppression. J Biol Chem. 2012;287:25530-40.
41. Chien Y, Scuoppo C, Wang X, Fang X, Balgley B, Bolden JE, et al. Control of the senescence-associated secretory phenotype by NF-{kappa}B promotes senescence and enhances chemosensitivity. Genes Dev. 2011;25:2125-36.
42. Jennewein C, Karl S, Baumann B, Micheau O, Debatin KM, Fulda S. Identification of a novel pro-apoptotic role of NF-kappaB in the regulation of TRAIL- and CD95-mediated apoptosis of glioblastoma cells. Oncogene. 2012;31:1468-74.
43. Karl S, Pritschow Y, Volcic M, Hacker S, Baumann B, Wiesmuller L, et al. Identification of a novel pro-apopotic function of NF-kappaB in the DNA damage response. J Cell Mol Med. 2009;13:4239-56.
44. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P, et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell. 2007;131:669-81.
45. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, et al. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature. 2001;410:1107-11.
46. Tamura T, Thotakura P, Tanaka TS, Ko MS, Ozato K. Identification of target genes and a unique cis element regulated by IRF-8 in developing macrophages. Blood. 2005;106:1938-47.
47. Yang J, Hu X, Zimmerman M, Torres CM, Yang D, Smith SB, et al. Cutting edge: IRF8 regulates Bax transcription in vivo in primary myeloid cells. J Immunol. 2011;187:4426-30.
48. Zimmerman M, Yang D, Hu X, Liu F, Singh N, Browning D, et al. IFN-γ Upregulates Survivin and Ifi202 Expression to Induce Survival and Proliferation of Tumor-Specific T Cells. PLoS One. 2010;5:e14076.
49. Zimmerman MA, Rahman NT, Yang D, Lahat G, Lazar AJ, Pollock RE, et al. Unphosphorylated STAT1 promotes sarcoma development through repressing expression of Fas and bad and conferring apoptotic resistance. Cancer Res. 2012;72:4724-32.
50. Zimmerman MA, Singh N, Martin PM, Thangaraju M, Ganapathy V, Waller JL, et al. Butyrate suppresses colonic inflammation through HDAC1-dependent Fas upregulation and Fas-mediated apoptosis of T cells. Am J Physiol Gastrointest Liver Physiol. 2012;302:G1405-15.
51. Hu X, Yang D, Zimmerman M, Liu F, Yang J, Kannan S, et al. IRF8 regulates acid ceramidase expression to mediate apoptosis and suppresses myelogeneous leukemia. Cancer Res. 2011;71:2882-91.
52. Bardhan K, Paschall AV, Yang D, Chen MR, Simon PS, Bhutia YD, et al. IFNgamma induces DNA methylation-silenced GPR109A expression via pSTAT1/p300 and H3K18 acetylation in colon cancer. Cancer Immunol Res. 2015;3:795-805.
53. Schmidt N, Pautz A, Art J, Rauschkolb P, Jung M, Erkel G, et al. Transcriptional and post-transcriptional regulation of iNOS expression in human chondrocytes. Biochem Pharmacol. 2010;79:722-32.
54. Altamirano F, Lopez JR, Henriquez C, Molinski T, Allen PD, Jaimovich E. Increased resting intracellular calcium modulates NF-kappaB-dependent inducible nitric-oxide synthase gene expression in dystrophic mdx skeletal myotubes. J Biol Chem. 2012;287:20876-87.
55. Li K, Yao J, Shi L, Sawada N, Chi Y, Yan Q, et al. Reciprocal regulation between proinflammatory cytokine-induced inducible NO synthase (iNOS) and connexin43 in bladder smooth muscle cells. J Biol Chem. 2011;286:41552-62.
56. Stempelj M, Kedinger M, Augenlicht L, Klampfer L. Essential role of the JAK/STAT1 signaling pathway in the expression of inducible nitric-oxide synthase in intestinal epithelial cells and its regulation by butyrate. J Biol Chem. 2007;282:9797-804.
57. Xiong H, Zhu C, Li H, Chen F, Mayer L, Ozato K, et al. Complex formation of the interferon (IFN) consensus sequence-binding protein with IRF-1 is essential for murine macrophage IFN-gamma-induced iNOS gene expression. J Biol Chem. 2003;278:2271-7.
58. Paschall AV, Zhang R, Qi CF, Bardhan K, Peng L, Lu G, et al. IFN Regulatory Factor 8 Represses GM-CSF Expression in T Cells To Affect Myeloid Cell Lineage Differentiation. J Immunol. 2015;194:2369-79.
59. Kanno Y, Levi BZ, Tamura T, Ozato K. Immune cell-specific amplification of interferon signaling by the IRF-4/8-PU.1 complex. J Interferon Cytokine Res. 2005;25:770-9.
60. McAdam E, Haboubi HN, Forrester G, Eltahir Z, Spencer-Harty S, Davies C, et al. Inducible nitric oxide synthase (iNOS) and nitric oxide (NO) are important mediators of reflux-induced cell signalling in esophageal cells. Carcinogenesis. 2012;33:2035-43.
61. Mizel SB, Honko AN, Moors MA, Smith PS, West AP. Induction of macrophage nitric oxide production by Gram-negative flagellin involves signaling via heteromeric Toll-like receptor 5/Toll-like receptor 4 complexes. J Immunol. 2003;170:6217-23.
62. Gao J, Morrison DC, Parmely TJ, Russell SW, Murphy WJ. An interferon-gamma-activated site (GAS) is necessary for full expression of the mouse iNOS gene in response to interferon-gamma and lipopolysaccharide. J Biol Chem. 1997;272:1226-30.
63. Ganster RW, Taylor BS, Shao L, Geller DA. Complex regulation of human inducible nitric oxide synthase gene transcription by Stat 1 and NF-kappa B. Proc Natl Acad Sci U S A. 2001;98:8638-43.