HIF-1α restricts NF-κB-dependent gene expression to control innate immunity signals

DMM Disease Models and Mechanisms

Volumn 8, Issue 2, 2015, Pages 169-181

  Bandarra, Daniel ^a   Biddlestone, John ^a   Mudie, Sharon ^a   Müller, H Arno J ^a   Rocha, Sonia ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Drosophila; HIF 1; Hypoxia; IKK; Inflammation; Nf b

Indexed keywords

CYCLIN DEPENDENT KINASE 6; HYPOXIA INDUCIBLE FACTOR 1ALPHA; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHOTRANSFERASE; PROTEIN TAK; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; MAP KINASE KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; SIMA PROTEIN, DROSOPHILA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE REPRESSION; HYPOXIA; IMMUNE RESPONSE; INFLAMMATION; INNATE IMMUNITY; MAMMAL CELL; MORTALITY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANGIOGENESIS; ANIMAL; CELL LINE; ESCHERICHIA COLI INFECTION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HUMAN; IMMUNOLOGY; MAMMAL; METABOLISM; MICROBIOLOGY; PATHOLOGY; SURVIVAL ANALYSIS;

DROSOPHILA MELANOGASTER; MAMMALIA;

ANIMALS; CELL LINE; CYCLIN-DEPENDENT KINASE 6; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ESCHERICHIA COLI INFECTIONS; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; I-KAPPA B KINASE; IMMUNITY, INNATE; MAMMALS; MAP KINASE KINASE KINASES; NEOVASCULARIZATION, PHYSIOLOGIC; NF-KAPPA B; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS;

EID: 84922485491     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.017285     Document Type: Article

References (74)

1. Adli, M. and Baldwin, A. S. (2006). IKK-i/IKKepsilon controls constitutive, cancer cell-associated NF-kappaB activity via regulation of Ser-536 p65/RelA phosphorylation. J. Biol. Chem. 281, 26976-26984.
2. Albrecht, S. C., Barata, A. G., Grosshans, J., Teleman, A. A. and Dick, T. P. (2011). In vivo mapping of hydrogen peroxide and oxidized glutathione reveals chemical and regional specificity of redox homeostasis. Cell Metab. 14, 819-829.
3. Arquier, N., Vigne, P., Duplan, E., Hsu, T., Therond, P. P., Frelin, C. and D'Angelo, G. (2006). Analysis of the hypoxia-sensing pathway in Drosophila melanogaster. Biochem. J. 393, 471-480.
4. Ashall, L., Horton, C. A., Nelson, D. E., Paszek, P., Harper, C. V., Sillitoe, K., Ryan, S., Spiller, D. G., Unitt, J. F., Broomhead, D. S. et al. (2009). Pulsatile stimulation determines timing and specificity of NF-kappaB-dependent transcription. Science 324, 242-246.
5. Bandarra, D., Biddlestone, J., Mudie, S., Muller, H. A. and Rocha, S. (2014). Hypoxia activates IKK-NF-κB and the immune response in Drosophila melanogaster. Biosci. Rep. 34, e00127.
6. Benassi, V., Coustau, C. and Carton, Y. (2000). Insect immunity: a genetic factor (hrtp) is essential for antibacterial peptide expression in Drosophila after infection by parasitoid wasps. Arch. Insect Biochem. Physiol. 43, 64-71.
7. Bikker, F. J., Kaman-van Zanten, W. E., de Vries-van de Ruit, A. M., Voskamp-Visser, I., van Hooft, P. A., Mars-Groenendijk, R. H., de Visser, P. C. and Noort, D. (2006). Evaluation of the antibacterial spectrum of drosocin analogues. Chem. Biol. Drug Des. 68, 148-153.
8. Bonello, S., Zöhringer, C., BelAiba, R. S., Djordjevic, T., Hess, J., Michiels, C., Kietzmann, T. and Görlach, A. (2007). Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site. Arterioscler. Thromb. Vasc. Biol. 27, 755-761.
9. Buss, H., Dörrie, A., Schmitz, M. L., Hoffmann, E., Resch, K. and Kracht, M. (2004). Constitutive and interleukin-1-inducible phosphorylation of p65 NF-kappaB at serine 536 is mediated by multiple protein kinases including IkappaB kinase (IKK)-alpha, IKKbeta, IKKepsilon, TRAF family member-associated (TANK)-binding kinase 1 (TBK1), and an unknown kinase and couples p65 to TATA-binding protein-associated factor II31-mediated interleukin-8 transcription. J. Biol. Chem. 279, 55633-55643.
10. Buss, H., Handschick, K., Jurrmann, N., Pekkonen, P., Beuerlein, K., Müller, H., Wait, R., Saklatvala, J., Ojala, P. M., Schmitz, M. L. et al. (2012). Cyclin-dependent kinase 6 phosphorylates NF-κB P65 at serine 536 and contributes to the regulation of inflammatory gene expression. PLoS ONE 7, e51847.
11. Campbell, K. J., Witty, J. M., Rocha, S. and Perkins, N. D. (2006). Cisplatin mimics ARF tumor suppressor regulation of RelA (p65) nuclear factor-kappaB transactivation. Cancer Res. 66, 929-935.
12. Catrina, S. B., Okamoto, K., Pereira, T., Brismar, K. and Poellinger, L. (2004). Hyperglycemia regulates hypoxia-inducible factor-1alpha protein stability and function. Diabetes 53, 3226-3232.
13. Centanin, L., Ratcliffe, P. J. and Wappner, P. (2005). Reversion of lethality and growth defects in Fatiga oxygen-sensor mutant flies by loss of hypoxia-inducible factor-alpha/Sima. EMBO Rep. 6, 1070-1075.
14. Chan, D. A., Kawahara, T. L., Sutphin, P. D., Chang, H. Y., Chi, J. T. and Giaccia, A. J. (2009). Tumor vasculature is regulated by PHD2-mediated angiogenesis and bone marrow-derived cell recruitment. Cancer Cell 15, 527-538.
15. Chandel, N. S. (2010). Mitochondrial regulation of oxygen sensing. Adv. Exp. Med. Biol. 661, 339-354.
16. Chen, L. F., Williams, S. A., Mu, Y., Nakano, H., Duerr, J. M., Buckbinder, L. and Greene, W. C. (2005). NF-kappaB RelA phosphorylation regulates RelA acetylation. Mol. Cell. Biol. 25, 7966-7975.
17. Cudic, M., Bulet, P., Hoffmann, R., Craik, D. J. and Otvos, L., Jr. (1999). Chemical synthesis, antibacterial activity and conformation of diptericin, an 82-mer peptide originally isolated from insects. Eur. J. Biochem. 266, 549-558.
18. Culver, C., Sundqvist, A., Mudie, S., Melvin, A., Xirodimas, D. and Rocha, S. (2010). Mechanism of hypoxia-induced NF-kappaB. Mol. Cell. Biol. 30, 4901-4921.
19. Culver, C., Melvin, A., Mudie, S. and Rocha, S. (2011). HIF-1α depletion results in SP1-mediated cell cycle disruption and alters the cellular response to chemotherapeutic drugs. Cell Cycle 10, 1249-1260.
20. Dehne, N. and Brüne, B. (2014). Sensors, transmitters, and targets in mitochondrial oxygen shortage-a hypoxia-inducible factor relay story. Antioxid. Redox Signal. 20, 339-352.
21. Feinman, R., Deitch, E. A., Watkins, A. C., Abungu, B., Colorado, I., Kannan, K. B., Sheth, S. U., Caputo, F. J., Lu, Q., Ramanathan, M. et al. (2010). HIF-1 mediates pathogenic inflammatory responses to intestinal ischemia-reperfusion injury. Am. J. Physiol. 299, G833-G843.
22. Fujisaka, S., Usui, I., Ikutani, M., Aminuddin, A., Takikawa, A., Tsuneyama, K., Mahmood, A., Goda, N., Nagai, Y., Takatsu, K. et al. (2013). Adipose tissue hypoxia induces inflammatory M1 polarity of macrophages in an HIF-1α-dependent and HIF-1α-independent manner in obese mice. Diabetologia 56, 1403-1412.
23. Gale, D. P. and Maxwell, P. H. (2010). The role of HIF in immunity. Int. J. Biochem. Cell Biol. 42, 486-494.
24. Gloire, G., Legrand-Poels, S. and Piette, J. (2006). NF-kappaB activation by reactive oxygen species: fifteen years later. Biochem. Pharmacol. 72, 1493-1505.
25. Goldszmid, R. S. and Trinchieri, G. (2012). The price of immunity. Nat. Immunol. 13, 932-938.
26. Görlach, A. and Bonello, S. (2008). The cross-talk between NF-kappaB and HIF-1: further evidence for a significant liaison. Biochem. J. 412, e17-e19.
27. Handschick, K., Beuerlein, K., Jurida, L., Bartkuhn, M., Müller, H., Soelch, J., Weber, A., Dittrich-Breiholz, O., Schneider, H., Scharfe, M. et al. (2014). Cyclindependent kinase 6 is a chromatin-bound cofactor for NF-κB-dependent gene expression. Mol. Cell 53, 193-208.
28. Hayden, M. S. and Ghosh, S. (2008). Shared principles in NF-kappaB signaling. Cell 132, 344-362.
29. Hayden, M. S., West, A. P. and Ghosh, S. (2006). NF-kappaB and the immune response. Oncogene 25, 6758-6780.
30. Hetru, C. and Hoffmann, J. A. (2009). NF-kappaB in the immune response of Drosophila. Cold Spring Harb. Perspect. Biol. 1, a000232.
31. Horak, P., Crawford, A. R., Vadysirisack, D. D., Nash, Z. M., DeYoung, M. P., Sgroi, D. and Ellisen, L. W. (2010). Negative feedback control of HIF-1 through REDD1-regulated ROS suppresses tumorigenesis. Proc. Natl. Acad. Sci. USA 107, 4675-4680.
32. Ichim, T. E., Minev, B., Braciak, T., Luna, B., Hunninghake, R., Mikirova, N. A., Jackson, J. A., Gonzalez, M. J., Miranda-Massari, J. R., Alexandrescu, D. T. et al. (2011). Intravenous ascorbic acid to prevent and treat cancer-associated sepsis? J. Transl. Med. 9, 25.
33. Kaelin, W. G. (2005). Proline hydroxylation and gene expression. Annu. Rev. Biochem. 74, 115-128.
34. Karin, M., Yamamoto, Y. and Wang, Q. M. (2004). The IKK NF-kappa B system: a treasure trove for drug development. Nat. Rev. Drug Discov. 3, 17-26.
35. Kenneth, N. S. and Rocha, S. (2008). Regulation of gene expression by hypoxia. Biochem. J. 414, 19-29.
36. Kenneth, N. S., Mudie, S., van Uden, P. and Rocha, S. (2009). SWI/SNF regulates the cellular response to hypoxia. J. Biol. Chem. 284, 4123-4131.
37. Kenneth, N. S., Mudie, S. and Rocha, S. (2010). IKK and NF-kappaB-mediated regulation of Claspin impacts on ATR checkpoint function. EMBO J. 29, 2966-2978.
38. Kenneth, N. S., Mudie, S., Naron, S. and Rocha, S. (2013). TfR1 interacts with the IKK complex and is involved in IKK-NF-κB signalling. Biochem. J. 449, 275-284.
39. Kim, J. W., Tchernyshyov, I., Semenza, G. L. and Dang, C. V. (2006). HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 3, 177-185.
40. Kleino, A. and Silverman, N. (2014). The Drosophila IMD pathway in the activation of the humoral immune response. Dev. Comp. Immunol. 42, 25-35.
41. Kojima, H., Gu, H., Nomura, S., Caldwell, C. C., Kobata, T., Carmeliet, P., Semenza, G. L. and Sitkovsky, M. V. (2002). Abnormal B lymphocyte development and autoimmunity in hypoxia-inducible factor 1alpha -deficient chimeric mice. Proc. Natl. Acad. Sci. USA 99, 2170-2174.
42. Kounatidis, I. and Ligoxygakis, P. (2012). Drosophila as a model system to unravel the layers of innate immunity to infection. Open Biol. 2, 120075.
43. Lu, Y., Wu, L. P. and Anderson, K. V. (2001). The antibacterial arm of the drosophila innate immune response requires an IkappaB kinase. Genes Dev. 15, 104-110.
44. Mahlen, S. D. (2011). Serratia infections: from military experiments to current practice. Clin. Microbiol. Rev. 24, 755-791.
45. Maxwell, P. J., Gallagher, R., Seaton, A., Wilson, C., Scullin, P., Pettigrew, J., Stratford, I. J., Williams, K. J., Johnston, P. G. and Waugh, D. J. (2007). HIF-1 and NF-kappaB-mediated upregulation of CXCR1 and CXCR2 expression promotes cell survival in hypoxic prostate cancer cells. Oncogene 26, 7333-7345.
46. Maynard, M. A., Qi, H., Chung, J., Lee, E. H., Kondo, Y., Hara, S., Conaway, R. C., Conaway, J. W. and Ohh, M. (2003). Multiple splice variants of the human HIF-3 alpha locus are targets of the von Hippel-Lindau E3 ubiquitin ligase complex. J. Biol. Chem. 278, 11032-11040.
47. Moniz, S., Biddlestone, J. and Rocha, S. (2014). Grow(2): The HIF system, energy homeostasis and the cell cycle. Histol. Histopathol. 29, 589-600.
48. Perkins, N. D. (2006). Post-translational modifications regulating the activity and function of the nuclear factor kappa B pathway. Oncogene 25, 6717-6730.
49. Perkins, N. D. (2012). The diverse and complex roles of NF-κB subunits in cancer. Nat. Rev. Cancer 12, 121-132.
50. Perkins, N. D. and Gilmore, T. D. (2006). Good cop, bad cop: the different faces of NF-kappaB. Cell Death Differ. 13, 759-772.
51. Perkins, N. D., Felzien, L. K., Betts, J. C., Leung, K., Beach, D. H. and Nabel, G. J. (1997). Regulation of NF-kappaB by cyclin-dependent kinases associated with the p300 coactivator. Science 275, 523-527.
52. Poole, J. C., Thain, A., Perkins, N. D. and Roninson, I. B. (2004). Induction of transcription by p21Waf1/Cip1/Sdi1: role of NFkappaB and effect of non-steroidal anti-inflammatory drugs. Cell Cycle 3, 929-938.
53. Renner, F. and Schmitz, M. L. (2009). Autoregulatory feedback loops terminating the NF-kappaB response. Trends Biochem. Sci. 34, 128-135.
54. Rius, J., Guma, M., Schachtrup, C., Akassoglou, K., Zinkernagel, A. S., Nizet, V., Johnson, R. S., Haddad, G. G. and Karin, M. (2008). NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature 453, 807-811.
55. Rocha, S. (2007). Gene regulation under low oxygen: holding your breath for transcription. Trends Biochem. Sci. 32, 389-397.
56. Schmitz, M. L., Bacher, S. and Kracht, M. (2001). I kappa B-independent control of NF-kappa B activity by modulatory phosphorylations. Trends Biochem. Sci. 26, 186-190.
57. Schofield, C. J. and Ratcliffe, P. J. (2004). Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5, 343-354.
58. Scholz, C. C. and Taylor, C. T. (2013). Targeting the HIF pathway in inflammation and immunity. Curr. Opin. Pharmacol. 13, 646-653.
59. Semenza, G. L. (2011). Oxygen sensing, homeostasis, and disease. N. Engl. J. Med. 365, 537-547.
60. Semenza, G. L. and Wang, G. L. (1992). A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol. Cell. Biol. 12, 5447-5454.
61. Shoshani, T., Faerman, A., Mett, I., Zelin, E., Tenne, T., Gorodin, S., Moshel, Y., Elbaz, S., Budanov, A., Chajut, A. et al. (2002). Identification of a novel hypoxia-inducible factor 1-responsive gene, RTP801, involved in apoptosis. Mol. Cell. Biol. 22, 2283-2293.
62. Sung, M. H., Li, N., Lao, Q., Gottschalk, R. A., Hager, G. L. and Fraser, I. D. (2014). Switching of the relative dominance between feedback mechanisms in lipopolysaccharide-induced NF-κB signaling. Sci. Signal. 7, ra6.
63. Tanji, T., Hu, X., Weber, A. N. and Ip, Y. T. (2007). Toll and IMD pathways synergistically activate an innate immune response in Drosophila melanogaster. Mol. Cell. Biol. 27, 4578-4588.
64. Taylor, P. C. and Sivakumar, B. (2005). Hypoxia and angiogenesis in rheumatoid arthritis. Curr. Opin. Rheumatol. 17, 293-298.
65. Terry, A. J. and Chaplain, M. A. (2011). Spatio-temporal modelling of the NF-κB intracellular signalling pathway: the roles of diffusion, active transport, and cell geometry. J. Theor. Biol. 290, 7-26.
66. Tsichritzis, T., Gaentzsch, P. C., Kosmidis, S., Brown, A. E., Skoulakis, E. M., Ligoxygakis, P. and Mosialos, G. (2007). A Drosophila ortholog of the human cylindromatosis tumor suppressor gene regulates triglyceride content and antibacterial defense. Development 134, 2605-2614.
67. van Uden, P., Kenneth, N. S. and Rocha, S. (2008). Regulation of hypoxia-inducible factor-1alpha by NF-kappaB. Biochem. J. 412, 477-484.
68. van Uden, P., Kenneth, N. S., Webster, R., Müller, H. A., Mudie, S. and Rocha, S. (2011). Evolutionary conserved regulation of HIF-1β by NF-κB. PLoS Genet. 7, e1001285.
69. Walmsley, S. R., Print, C., Farahi, N., Peyssonnaux, C., Johnson, R. S., Cramer, T., Sobolewski, A., Condliffe, A. M., Cowburn, A. S., Johnson, N. et al. (2005). Hypoxia-induced neutrophil survival is mediated by HIF-1alpha-dependent NF-kappaB activity. J. Exp. Med. 201, 105-115.
70. Wang, G. L. and Semenza, G. L. (1995). Purification and characterization of hypoxia-inducible factor 1. J. Biol. Chem. 270, 1230-1237.
71. Waugh, D. J. and Wilson, C. (2008). The interleukin-8 pathway in cancer. Clin. Cancer Res. 14, 6735-6741.
72. Wuerzberger-Davis, S. M. and Miyamoto, S. (2010). TAK-ling IKK activation: "Ub" the judge. Sci. Signal. 3, pe3.
73. Yamada, K., Ono, M., Perkins, N. D., Rocha, S. and Lamond, A. I. (2013). Identification and functional characterization of FMN2, a regulator of the cyclin-dependent kinase inhibitor p21. Mol. Cell 49, 922-933.
74. Yoon, M. K., Mitrea, D. M., Ou, L. and Kriwacki, R. W. (2012). Cell cycle regulation by the intrinsically disordered proteins p21 and p27. Biochem. Soc. Trans. 40, 981-988.