NF-κB: linking inflammation and immunity to cancer development and progression (original) (raw)
Balkwill, F. & Mantovani, A. Inflammation and cancer: back to Virchow? Lancet357, 539–545 (2001). ArticleCASPubMed Google Scholar
Kuper, H., Adami, H. O. & Trichopoulos, D. Infections as a major preventable cause of human cancer. J. Intern. Med.248, 171–183 (2000). ArticleCASPubMed Google Scholar
Roder, D. M. The epidemiology of gastric cancer. Gastric Cancer5 (Suppl. 1), 5–11 (2002). ArticlePubMed Google Scholar
Warzocha, K. et al. Genetic polymorphisms in the tumor necrosis factor locus influence non-Hodgkin's lymphoma outcome. Blood91, 3574–3581 (1998). CASPubMed Google Scholar
El-Omar, E. M. et al. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature404, 398–402 (2000). ArticleCASPubMed Google Scholar
Sun, J. et al. Sequence variants in Toll-like receptor gene cluster (TLR6_–_TLR1_–_TLR10) and prostate cancer risk. J. Natl Cancer Inst.97, 525–532 (2005). ArticleCASPubMed Google Scholar
Bharti, A. C. & Aggarwal, B. B. Chemopreventive agents induce suppression of nuclear factor-κB leading to chemosensitization. Ann. NY Acad. Sci.973, 392–395 (2002). ArticleCASPubMed Google Scholar
Wang, W. H. et al. Non-steroidal anti-inflammatory drug use and the risk of gastric cancer: a systematic review and meta-analysis. J. Natl Cancer Inst.95, 1784–1791 (2003). ArticleCASPubMed Google Scholar
Garber, K. Aspirin for cancer chemoprevention: still a headache? J. Natl Cancer Inst.96, 252–253 (2004). ArticlePubMed Google Scholar
Ness, R. B. & Cottreau, C. Possible role of ovarian epithelial inflammation in ovarian cancer. J. Natl Cancer Inst.91, 1459–1467 (1999). ArticleCASPubMed Google Scholar
Chang, E. T. et al. Aspirin and the risk of Hodgkin's lymphoma in a population-based case–control study. J. Natl Cancer Inst.96, 305–315 (2004). ArticleCASPubMed Google Scholar
Cerhan, J. R. et al. Association of aspirin and other non-steroidal anti-inflammatory drug use with incidence of non-Hodgkin lymphoma. Int. J. Cancer106, 784–788 (2003). ArticleCASPubMed Google Scholar
Schernhammer, E. S. et al. A prospective study of aspirin use and the risk of pancreatic cancer in women. J. Natl Cancer Inst.96, 22–28 (2004). ArticleCASPubMed Google Scholar
Burnet, F. M. The concept of immunological surveillance. Prog. Exp. Tumor Res.13, 1–17 (1970). ArticleCASPubMed Google Scholar
Dunn, G. P., Old, L. J. & Schreiber, R. D. The immunobiology of cancer immunosurveillance and immunoediting. Immunity21, 137–148 (2004). ArticleCASPubMed Google Scholar
Pardoll, D. Does the immune system see tumours as foreign or self? Annu. Rev. Immunol.21, 807–839 (2003). References 16 and 17 are excellent reviews of the theory of immunoediting. ArticleCASPubMed Google Scholar
Philip, M., Rowley, D. A. & Schreiber, H. Inflammation as a tumor promoter in cancer induction. Semin. Cancer Biol.14, 433–439 (2004). ArticleCASPubMed Google Scholar
Luo, J. L., Maeda, S., Hsu, L. C., Yagita, H. & Karin, M. Inhibition of NF-κB in cancer cells converts inflammation-induced tumor growth mediated by TNFα to TRAIL-mediated tumor regression. Cancer Cell6, 297–305 (2004). ArticleCASPubMed Google Scholar
Chisari, F. V. Hepatitis B virus transgenic mice: insights into the virus and the disease. Hepatology22, 1316–1325 (1995). CASPubMed Google Scholar
de Visser, K. E., Korets, L. V. & Coussens, L. M. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell7, 411–423 (2005). ArticleCASPubMed Google Scholar
Karin, M., Cao, Y., Greten, F. R. & Li, Z. W. NF-κB in cancer: from innocent bystander to major culprit. Nature Rev. Cancer2, 301–310 (2002). ArticleCAS Google Scholar
Greten, F. R. et al. IKKβ links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell118, 285–296 (2004). ArticleCASPubMed Google Scholar
Pikarsky, E. et al. NF-κB functions as a tumour promoter in inflammation-associated cancer. Nature431, 461–466 (2004). References 23 and 24 were the first to describe IKK-β-dependent NF-κB activation as the molecular link between inflammation and cancer. ArticleCASPubMed Google Scholar
Bonizzi, G. & Karin, M. The two NF-κB activation pathways and their role in innate and adaptive immunity. Trends Immunol.25, 280–288 (2004). ArticleCASPubMed Google Scholar
Lawrence, T., Bebien, M., Liu, G. Y., Nizet, V. & Karin, M. IKKα limits macrophage NF-κB activation and contributes to the resolution of inflammation. Nature434, 1138–1143 (2005). ArticleCASPubMed Google Scholar
Maeda, S., Kamata, H., Luo, J. L., Leffert, H. & Karin, M. IKKβ couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell121, 977–990 (2005). This paper describes the role of IKK-β-dependent NF-κB activation in chemically induced HCC, and it was the first to show that compensatory proliferation that depends on production of pro-inflammatory cytokines is important in carcinogenesis. ArticleCASPubMed Google Scholar
Mauad, T. H. et al. Mice with homozygous disruption of the mdr2 P-glycoprotein gene. A novel animal model for studies of nonsuppurative inflammatory cholangitis and hepatocarcinogenesis. Am. J. Pathol.145, 1237–1245 (1994). CASPubMedPubMed Central Google Scholar
Becker, C. et al. TGF-β suppresses tumor progression in colon cancer by inhibition of IL-6 _trans_-signaling. Immunity21, 491–501 (2004). This paper describes the importance of T-cell-mediated, IL-6 signalling in the development of CAC. ArticleCASPubMed Google Scholar
Li, Z.-W. et al. The IKKβ subunit of IκB kinase (IKK) is essential for NF-κB activation and prevention of apoptosis. J. Exp. Med.189, 1839–1845 (1999). ArticleCASPubMedPubMed Central Google Scholar
Kamata, H. et al. Reactive oxygen species promote TNFα-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell120, 649–661 (2005). ArticleCASPubMed Google Scholar
Vakkila, J. & Lotze, M. T. Inflammation and necrosis promote tumour growth. Nature Rev. Immunol.4, 641–648 (2004). ArticleCAS Google Scholar
Zeh, H. J. & Lotze, M. T. Addicted to death: invasive cancer and the immune response to unscheduled cell death. J. Immunother.28, 1–9 (2005). ArticlePubMed Google Scholar
Conejo-Garcia, J. R. et al. Tumor-infiltrating dendritic cell precursors recruited by a β-defensin contribute to vasculogenesis under the influence of Vegf-A. Nature Med.10, 950–958 (2004). ArticleCASPubMed Google Scholar
Moore, R. J. et al. Mice deficient in tumor necrosis factor-α are resistant to skin carcinogenesis. Nature Med.5, 828–831 (1999). ArticleCASPubMed Google Scholar
Arnott, C. H. et al. Expression of both TNF-α receptor subtypes is essential for optimal skin tumour development. Oncogene23, 1902–1910 (2004). ArticleCASPubMed Google Scholar
Szabowski, A. et al. c-Jun and JunB antagonistically control cytokine-regulated mesenchymal–epidermal interaction in skin. Cell103, 745–755 (2000). ArticleCASPubMed Google Scholar
Arnott, C. H. et al. Tumour necrosis factor-α mediates tumour promotion via a PKC α- and AP-1-dependent pathway. Oncogene21, 4728–4738 (2002). ArticleCASPubMed Google Scholar
van Hogerlinden, M., Rozell, B. L., Ahrlund-Richter, L. & Toftgard, R. Squamous cell carcinomas and increased apoptosis in skin with inhibited Rel/nuclear factor-κB signaling. Cancer Res.59, 3299–3303 (1999). CASPubMed Google Scholar
van Hogerlinden, M., Auer, G. & Toftgard, R. Inhibition of Rel/nuclear factor-κB signaling in skin results in defective DNA damage-induced cell cycle arrest and Ha-ras- and p53-independent tumor development. Oncogene21, 4969–4977 (2002). ArticleCASPubMed Google Scholar
Seitz, C. S., Lin, Q., Deng, H. & Khavari, P. A. Alterations in NF-κB function in transgenic epithelial tissue demonstrate a growth inhibitory role for NF-κB. Proc. Natl Acad. Sci. USA95, 2307–2312 (1998). ArticleCASPubMedPubMed Central Google Scholar
Dajee, M. et al. NF-κB blockade and oncogenic Ras trigger invasive human epidermal neoplasia. Nature421, 639–643 (2003). ArticleCASPubMed Google Scholar
Lind, M. H. et al. Tumor necrosis factor receptor 1-mediated signaling is required for skin cancer development induced by NF-κB inhibition. Proc. Natl Acad. Sci. USA101, 4972–4977 (2004). ArticleCASPubMedPubMed Central Google Scholar
Zhang, J. Y., Green, C. L., Tao, S. & Khavari, P. A. NF-κB RelA opposes epidermal proliferation driven by TNFR1 and JNK. Genes Dev.18, 17–22 (2004). References 46 and 47 describe TNF as a tumour promoter and show that the balance between JNK and NF-κB activation is essential for the development of skin cancer. ArticleCASPubMedPubMed Central Google Scholar
Korner, H. et al. Tumor necrosis factor sustains the generalized lymphoproliferative disorder (gld) phenotype. J. Exp. Med.191, 89–96 (2000). ArticleCASPubMedPubMed Central Google Scholar
Balkwill, F. Tumor necrosis factor or tumor promoting factor? Cytokine Growth Factor Rev.13, 135–141 (2002). ArticleCASPubMed Google Scholar
Galban, S. et al. von Hippel–Lindau protein-mediated repression of tumor necrosis factor α translation revealed through use of cDNA arrays. Mol. Cell. Biol.23, 2316–2328 (2003). ArticleCASPubMedPubMed Central Google Scholar
Nauts, H. C., Fowler, G. A. & Bogatko, F. H. A review of the influence of bacterial infection and of bacterial products (Coley's toxins) on malignant tumors in man; a critical analysis of 30 inoperable cases treated by Coley's mixed toxins, in which diagnosis was confirmed by microscopic examination selected for special study. Acta Med. Scand. Suppl.144, 1–103 (1953). Google Scholar
Duncan, L. M., Richards, L. A. & Mihm, M. C. Jr. Increased mast cell density in invasive melanoma. J. Cutan. Pathol.25, 11–15 (1998). ArticleCASPubMed Google Scholar
Pollard, J. W. Tumour-educated macrophages promote tumour progression and metastasis. Nature Rev. Cancer4, 71–78 (2004). ArticleCAS Google Scholar
Menetrier-Caux, C. et al. Inhibition of the differentiation of dendritic cells from CD34+ progenitors by tumor cells: role of interleukin-6 and macrophage colony-stimulating factor. Blood92, 4778–4791 (1998). CASPubMed Google Scholar
Curiel, T. J. et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nature Med.10, 942–949 (2004). ArticleCASPubMed Google Scholar
Iellem, A. et al. Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4+CD25+ regulatory T cells. J. Exp. Med.194, 847–853 (2001). ArticleCASPubMedPubMed Central Google Scholar
Erdman, S. E. et al. CD4+CD25+ regulatory lymphocytes induce regression of intestinal tumors in ApcMin/+ mice. Cancer Res.65, 3998–4004 (2005). ArticleCASPubMed Google Scholar
Balkwill, F., Charles, K. A. & Mantovani, A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell7, 211–217 (2005). ArticleCASPubMed Google Scholar
Fadok, V. A., Bratton, D. L., Guthrie, L. & Henson, P. M. Differential effects of apoptotic versus lysed cells on macrophage production of cytokines: role of proteases. J. Immunol.166, 6847–6854 (2001). ArticleCASPubMed Google Scholar
Engle, S. J. et al. Transforming growth factor β1 suppresses nonmetastatic colon cancer at an early stage of tumorigenesis. Cancer Res.59, 3379–3386 (1999). CASPubMed Google Scholar
Berg, D. J. et al. Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4+ TH1-like responses. J. Clin. Invest.98, 1010–1020 (1996). ArticleCASPubMedPubMed Central Google Scholar
Goodman, J. E., Hofseth, L. J., Hussain, S. P. & Harris, C. C. Nitric oxide and p53 in cancer-prone chronic inflammation and oxyradical overload disease. Environ. Mol. Mutagen.44, 3–9 (2004). ArticleCASPubMed Google Scholar
Bando, H. & Toi, M. Tumor angiogenesis, macrophages, and cytokines. Adv. Exp. Med. Biol.476, 267–284 (2000). ArticleCASPubMed Google Scholar
Leek, R. D. et al. Macrophage infiltration is associated with VEGF and EGFR expression in breast cancer. J. Pathol.190, 430–436 (2000). ArticleCASPubMed Google Scholar
Barleon, B. et al. Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood87, 3336–3343 (1996). CASPubMed Google Scholar
Sparmann, A. & Bar-Sagi, D. Ras-induced interleukin-8 expression plays a critical role in tumor growth and angiogenesis. Cancer Cell6, 447–458 (2004). ArticleCASPubMed Google Scholar
Jung, Y. J., Isaacs, J. S., Lee, S., Trepel, J. & Neckers, L. IL-1β-mediated up-regulation of HIF-1α via an NF-κB/COX-2 pathway identifies HIF-1 as a critical link between inflammation and oncogenesis. FASEB J.17, 2115–2117 (2003). ArticleCASPubMed Google Scholar
Weinreich, D. M. et al. Effect of interleukin 1 receptor antagonist gene transduction on human melanoma xenografts in nude mice. Cancer Res.63, 5957–5961 (2003). CASPubMed Google Scholar
Melcher, A. et al. Tumor immunogenicity is determined by the mechanism of cell death via induction of heat shock protein expression. Nature Med.4, 581–587 (1998). ArticleCASPubMed Google Scholar
Houghton, J. et al. Gastric cancer originating from bone marrow-derived cells. Science306, 1568–1571 (2004). This paper describes how bone-marrow-derived cells can differentiate into epithelial cancer cells, and it provides the first molecular evidence of a role for inflammation in tumour initiation. ArticleCASPubMed Google Scholar
Keates, S., Hitti, Y. S., Upton, M. & Kelly, C. P. Helicobacter pylori infection activates NF-κB in gastric epithelial cells. Gastroenterology113, 1099–1109 (1997). ArticleCASPubMed Google Scholar
Barnes, P. J. & Karin, M. NF-κB — a pivotal transcription factor in chronic inflammatory diseases. N. Engl. J. Med.336, 1066–1071 (1997). ArticleCASPubMed Google Scholar
Radisky, D. C. et al. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature436, 123–127 (2005). This paper provides a molecular mechanism by which protease-induced epithelial–mesenchymal transition can stimulate ROS production and thereby increase genomic instability. ArticleCASPubMedPubMed Central Google Scholar
Shankaran, V. et al. IFNγ and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature410, 1107–1111 (2001). ArticleCASPubMed Google Scholar
Girardi, M. et al. Regulation of cutaneous malignancy by γδ T cells. Science294, 605–609 (2001). ArticleCASPubMed Google Scholar
Girardi, M. et al. The distinct contributions of murine T cell receptor (TCR)γδ+ and TCRαβ+ T cells to different stages of chemically induced skin cancer. J. Exp. Med.198, 747–755 (2003). ArticleCASPubMedPubMed Central Google Scholar
Street, S. E., Cretney, E. & Smyth, M. J. Perforin and interferon-γ activities independently control tumor initiation, growth, and metastasis. Blood97, 192–197 (2001). ArticleCASPubMed Google Scholar
Kaplan, D. H. et al. Demonstration of an interferon γ-dependent tumor surveillance system in immunocompetent mice. Proc. Natl Acad. Sci. USA95, 7556–7561 (1998). CASPubMedPubMed Central Google Scholar
Interferon α versus chemotherapy for chronic myeloid leukemia: a metaanalysis of seven randomized trials: Chronic Myeloid Leukemia Trialists' Collaborative Group. J. Natl Cancer Inst.89, 1616–1620 (1997).
Schmidt, M. et al. Lack of interferon consensus sequence binding protein (ICSBP) transcripts in human myeloid leukemias. Blood91, 22–29 (1998). CASPubMed Google Scholar
Takaoka, A. et al. Integration of interferon-α/β signalling to p53 responses in tumour suppression and antiviral defence. Nature424, 516–523 (2003). This paper shows that type I IFNs can sensitize cells to p53-mediated apoptosis, implying that type II IFNs might not be the only IFNs involved in tumour development. ArticleCASPubMed Google Scholar
Smyth, M. J. et al. Nature's TRAIL — on a path to cancer immunotherapy. Immunity18, 1–6 (2003). ArticleCASPubMed Google Scholar
Dranoff, G. Cytokines in cancer pathogenesis and cancer therapy. Nature Rev. Cancer4, 11–22 (2004). ArticleCAS Google Scholar
Koehne, C. H. & Dubois, R. N. COX-2 inhibition and colorectal cancer. Semin. Oncol.31, 12–21 (2004). ArticleCASPubMed Google Scholar
Steinbach, G. et al. The effect of celecoxib, a cyclooxygenase-2 inhibitor, in familial adenomatous polyposis. N. Engl. J. Med.342, 1946–1952 (2000). ArticleCASPubMed Google Scholar
Solomon, S. D. et al. Cardiovascular risk associated with celecoxib in a clinical trial for colorectal adenoma prevention. N. Engl. J. Med.352, 1071–1080 (2005). ArticleCASPubMed Google Scholar
Bresalier, R. S. et al. Cardiovascular events associated with rofecoxib in a colorectal adenoma chemoprevention trial. N. Engl. J. Med.352, 1092–1102 (2005). ArticleCASPubMed Google Scholar
Karin, M., Yamamoto, Y. & Wang, Q. M. The IKK NF-κB system: a treasure trove for drug development. Nature Rev. Drug Discov.3, 17–26 (2004). ArticleCAS Google Scholar
Li, Q. & Verma, I. M. NF-κB regulation in the immune system. Nature Rev. Immunol.2, 725–734 (2002). ArticleCAS Google Scholar