BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Distinct Differences between TNF Receptor 1- and TNF Receptor 2- mediated Activation of NFκB

  • Thommesen, Liv (Norwegian University of Science and Technology, Department of Cancer Research and Molecular Medicine) ;
  • Laegreid, Astrid (Norwegian University of Science and Technology, Department of Cancer Research and Molecular Medicine)
  • Published : 2005.05.31
Download PDF
⟨ Previous Next ⟩

Abstract

Tumor necrosis factor (TNF) signaling is mediated via two distinct receptors, TNFR2 and TNFR1, which shows partially overlapping signaling mechanisms and biological roles. In the present study, TNFR2 and TNFR1 signal transduction mechanisms involved in activation of $NF{\kappa}B$ and CMV promoter-enhancer were compared with respect to their susceptibility towards inhibitors of intracellular signaling. For this, we used SW480 cells, where we have shown that TNF-signaling can occur independently through each of the two receptors. The TNFR1 response was inhibited by D609, bromophenacyl bromide (BPB), nordihydroguararetic acid (NDGA), and by sodium salicylate, while TNFR2-mediated activation of $NF{\kappa}B$ and CMV promoter-enhancer was resistant to these compounds. The signaling mechanisms known to be affected by these inhibitors include phospholipases as well as redox- and pH-sensitive intracellular components. Our results imply that TNFR2 signaling involved in $NF{\kappa}B$ activation proceeds independently of these inhibitor-sensitive signaling components, indicating distinct signaling pathways not shared with TNFR1.

Keywords

References

  1. Abe, Y., Gatanaga, M., Osuka, Y., Kimura, S., Burger, R., Granger, G. and Gatanaga, T. (1993) Role of 55- and 75-kDa tumor necrosis factor membrane receptors in the regulation of intercellular adhesion molecules-1 expression by HL-60 human promyelocytic leukemia cells in vitro. J. Immunol. 150, 5070- 5079
  2. Anthonsen, M. W., Solhaug, A. and Johansen, B. (2001) Functional coupling between secretory and cytosolic phospholipase A2 modulates tumor necrosis factor-alpha- and interleukin-1betainduced NF-kappa B activation. J. Biol. Chem. 276, 30527- 30536 https://doi.org/10.1074/jbc.M008481200
  3. Baeuerle, P. A. and Henkel, T. (1994) Function and activation of NF-kappa B in the immune system. Annu. Rev. Immunol. 12, 141-179 https://doi.org/10.1146/annurev.iy.12.040194.001041
  4. Baxter, G. T., Kuo, R. C., Jupp, O. J., Vandenabeele, P. and MacEwan, D. J. (1999) Tumor necrosis factor-alpha mediates both apoptotic cell death and cell proliferation in a human hematopoietic cell line dependent on mitotic activity and receptor subtype expression. J. Biol. Chem. 274, 9539-9547 https://doi.org/10.1074/jbc.274.14.9539
  5. Beg, A. A., Finco, T. S., Nantermet, P. V. and Baldwin, A. S. Jr (1993) Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of I kappa B alpha: a mechanism for NF-kappa B activation. Mol. Cell. Biol. 13, 3301-3310
  6. Beutler, B. and van Huffel, C. (1994) Unraveling function in the TNF ligand and receptor families. Science 264, 667-668 https://doi.org/10.1126/science.8171316
  7. Brockhaus, M., Schoenfeld, H. J., Schlaeger, E. J., Hunziker, W., Lesslauer, W. and Loetscher, H. (1990) Identification of two types of tumor necrosis factor receptors on human cell lines by monoclonal antibodies. Proc. Natl. Acad. Sci. 87, 3127-3131 https://doi.org/10.1073/pnas.87.8.3127
  8. Declercq, W., Denecker, G., Fiers, W. and Vandenabeele, P. (1998) Cooperation of both TNF receptors in inducing apoptosis: involvement of the TNF receptor-associated factor binding domain of the TNF receptor 75. J. Immunol. 161, 390-399
  9. Folgueira, L., McElhinny, J. A., Bren, G. D., MacMorran, W. S., Diaz-Meco, M. T., Moscat, J. and Paya, C. V. (1996) Protein kinase C-zeta mediates NF-kappa B activation in human immunodeficiency virus-infected monocytes. J. Virol. 70, 223- 231
  10. Fontaine, V., Mohand-Said, S., Hanoteau, N., Fuchs, C., Pfizenmaier, K. and Eisel, U. (2002) Neurodegenerative and neuroprotective effects of tumor Necrosis factor (TNF) in retinal ischemia: opposite roles of TNF receptor 1 and TNF receptor 2. J. Neurosci. 22, 216
  11. Galloway, C. J., Madanat, M. S., Sarr, T., Espevik, T., Dumas, M. L., Mitra, G. and Ranges, G. E. (1992) Anti-tumor necrosis factor receptor and tumor necrosis factor agonist activity by an anti-idiotypic antibody. Eur. J. Immunol. 22, 3045-3048 https://doi.org/10.1002/eji.1830221143
  12. Grell, M., Becke, F. M., Wajant, H., Mannel, D. N. and Scheurich, P. (1998) TNF receptor type 2 mediates thymocyte proliferation independently of TNF receptor type 1. Eur. J. Immunol. 28, 257-263 https://doi.org/10.1002/(SICI)1521-4141(199801)28:01<257::AID-IMMU257>3.0.CO;2-G
  13. Grell, M., Zimmermann, G., Gottfried, E., Chen, C. M., Grunwald, U., Huang, D. C., Wu Lee, Y. H., Durkop, H., Engelmann, H., Scheurich, P., Wajant, H. and Strasser, A. (1999) Induction of cell death by tumour necrosis factor (TNF) receptor 2, CD40 and CD30: a role for TNF-R1 activation by endogenous membrane-anchored TNF. EMBO J. 18, 3034-3043 https://doi.org/10.1093/emboj/18.11.3034
  14. Heller, R. A., Song, K., Fan, N. and Chang, D. J. (1992) The p70 tumor necrosis factor receptor mediates cytotoxicity. Cell. 70, 47-56 https://doi.org/10.1016/0092-8674(92)90532-H
  15. Holtmann, M. H., Schuchmann, M., Zeller, G., Galle, P. R. and Neurath, M. F. (2002) The emerging distinct role of TNFreceptor 2 (p80) signaling in chronic inflammatory disorders. Arch. Immunol. Ther. Exp. 50, 279-288
  16. Hsu, H., Huang, J., Shu, H. B., Baichwal, V. and Goeddel, D. V. (1996) TNF-dependent recruitment of the protein kinase RIP to the TNF receptor-1 signaling complex. Immunity, 4, 387-396 https://doi.org/10.1016/S1074-7613(00)80252-6
  17. Hsu, H., Xiong, J. and Goeddel, D. V. (1995) The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 81, 495-504 https://doi.org/10.1016/0092-8674(95)90070-5
  18. Jiang, G., Dallas-Yang, Q., Liu, F., Moller, D. E. and Zhang, B. B. (2003) Salicylic acid reverses phorbol 12-myristate-13-acetate (PMA)- and tumor necrosis factor alpha (TNFalpha)-induced insulin receptor substrate 1 (IRS1) serine 307 phosphorylation and insulin resistance in human embryonic kidney 293 (HEK293) cells. J. Biol. Chem. 278, 180-186 https://doi.org/10.1074/jbc.M205565200
  19. Karin, M. and Ben-Neriah, Y. (2000) Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu. Rev. Immunol. 18, 621-663 https://doi.org/10.1146/annurev.immunol.18.1.621
  20. Kopp, E. and Ghosh, S. (1994) Inhibition of NF-kappa B by sodium salicylate and aspirin. Science 265, 956-959 https://doi.org/10.1126/science.8052854
  21. Laegreid, A., Medvedev, A., Nonstad, U., Bombara, M. P., Ranges, G., Sundan, A. and Espevik, T. (1994) Tumor necrosis factor receptor p75 mediates cell-specific activation of nuclear factor kappa B and induction of human cytomegalovirus enhancer. J. Biol. Chem. 269, 7785-7791
  22. Laegreid, A., Thommesen, L., Jahr, T. G., Sundan, A. and Espevik, T. (1995) Tumor necrosis factor induces lipopolysaccharide tolerance in a human adenocarcinoma cell line mainly through the TNF p55 receptor. J. Biol. Chem. 270, 25418-25425 https://doi.org/10.1074/jbc.270.43.25418
  23. Liu, Z. G., Hsu, H., Goeddel, D. V. and Karin, M. (1996) Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell. 87, 565-576 https://doi.org/10.1016/S0092-8674(00)81375-6
  24. Lozano, J., Berra, E., Municio, M. M., Diaz-Meco, M. T., Dominguez, I., Sanz, L. and Moscat, J. (1994) Protein kinase C zeta isoform is critical for kappa B-dependent promoter activation by sphingomyelinase. J. Biol. Chem. 269, 19200- 19202
  25. MacEwan, D. J. (2002) TNF receptor subtype signalling: differences and cellular consequences. Cell. Signal. 14, 477- 492 https://doi.org/10.1016/S0898-6568(01)00262-5
  26. Marshall, L. A., Bauer, J., Sung, M. L. and Chang, J. Y. (1991) Evaluation of antirheumatic drugs for their effect in vitro on purified human synovial fluid phospholipase A2. J. Rheumatol. 18, 59-65
  27. Martin, T. W., Wysolmerski, R. B. and Lagunoff, D. (1987) Phosphatidylcholine metabolism in endothelial cells: evidence for phospholipase A and a novel $Ca^{2+}$-independent phospholipase C. Biochim. Biophys. Acta. 917, 296-307 https://doi.org/10.1016/0005-2760(87)90134-2
  28. McFarlane, S. M., Pashmi, G., Connell, M. C., Littlejohn, A. F., Tucker, S. J., Vandenabeele, P. and MacEwan, D. J. (2002) Differential activation of nuclear factor-kappaB by tumour necrosis factor receptor subtypes. TNFR1 predominates whereas TNFR2 activates transcription poorly. FEBS Lett. 515, 119-126 https://doi.org/10.1016/S0014-5793(02)02450-X
  29. Medvedev, A. E., Espevik, T., Ranges, G. and Sundan, A. (1996) Distinct roles of the two tumor necrosis factor (TNF) receptors in modulating TNF and lymphotoxin alpha effects. J. Biol. Chem. 271, 9778-9784 https://doi.org/10.1074/jbc.271.16.9778
  30. Medvedev, A. E., Laegreid, A., Sundan, A. and Espevik, T. (1996b) A non-competitive P55 TNF receptor antibody enhances the specific activity of lymphotoxin-alpha. Scand. J. Immunol. 43, 439-448 https://doi.org/10.1046/j.1365-3083.1996.d01-58.x
  31. Medvedev, A. E., Sundan, A. and Espevik, T. (1994) Involvement of the tumor necrosis factor receptor p75 in mediating cytotoxicity and gene regulating activities. Eur. J. Immunol. 24, 2842-2849 https://doi.org/10.1002/eji.1830241139
  32. Miyazawa, K., Iimori, Y., Makino, M., Mikami, T. and Miyasaka, K. (1985) Effects of some non-steroidal anti-inflammatory drugs and other agents on cyclooxygenase and lipoxygenase activities in some enzyme preparations. J. Pharmacol. 38, 199- 205
  33. Montag, A. G., Oka, T., Baek, K. H., Choi, C. S., Jay, G. and Agarwal, K. (1993) Tumors in hepatobiliary tract and pancreatic islet tissues of transgenic mice harboring gastrin simian virus 40 large tumor antigen fusion gene. Proc. Natl. Acad. Sci. USA 90, 6696-6700
  34. Mukhopadhyay, A., Suttles, J., Stout, R. D. and Aggarwal, B. B. (2001) Genetic deletion of the tumor necrosis factor receptor p60 or p80 abrogates ligand-mediated activation of nuclear factor-kappa B and of mitogen-activated protein kinases in macrophages. J. Biol. Chem. 276, 31906-31912 https://doi.org/10.1074/jbc.M105252200
  35. Muller-Decker, K. (1989) Interruption of TPA-induced signals by an antiviral and antitumoral xanthate compound: inhibition of a phospholipase C-type reaction. Biochem. Biophys. Res. Commun. 162, 198-205 https://doi.org/10.1016/0006-291X(89)91981-5
  36. Niki, E. (1987) Antioxidants in relation to lipid peroxidation. Chem. Phys. Lipids, 44, 227-253 https://doi.org/10.1016/0009-3084(87)90052-1
  37. Old, L. J. (1988) Tumor necrosis factor. Sci. Am. 258, 59-60 https://doi.org/10.1038/scientificamerican0588-59
  38. Palombella, V. J., Rando, O. J., Goldberg, A. L. and Maniatis, T. (1994) The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell. 78, 773-785 https://doi.org/10.1016/S0092-8674(94)90482-0
  39. Pan, S., An, P., Zhang, R., He, X., Yin, G. and Min, W. (2002) Etk/Bmx as a tumor necrosis factor receptor type 2-specific kinase: role in endothelial cell migration and angiogenesis. Mol. Cell. Biol. 22, 7512-7523 https://doi.org/10.1128/MCB.22.21.7512-7523.2002
  40. Pierce, J. W., Read, M. A., Ding, H., Luscinskas, F. W. and Collins, T. (1996) Salicylates inhibit I kappa B-alpha phosphorylation, endothelial-leukocyte adhesion molecule expression, and neutrophil transmigration. J. Immunol. 156, 3961-3969
  41. Rothe, M., Pan, M. G., Henzel, W. J., Ayres, T. M. and Goeddel, D. V. (1995a) The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins. Cell. 83, 1243-1252 https://doi.org/10.1016/0092-8674(95)90149-3
  42. Rothe, M., Sarma, V., Dixit, V. M. and Goeddel, D. V. (1995b) TRAF2-mediated activation of NF-kappa B by TNF receptor 2 and CD40. Science 269, 1424-1427 https://doi.org/10.1126/science.7544915
  43. Rothe, M., Wong, S. C., Henzel, W. J. and Goeddel, D. V. (1994) A novel family of putative signal transducers associated with the cytoplasmic domain of the 75 kDa tumor necrosis factor receptor. Cell. 78, 681-692 https://doi.org/10.1016/0092-8674(94)90532-0
  44. Sagone, A. L. Jr and Husney, R. M. (1987) Oxidation of salicylates by stimulated granulocytes: evidence that these drugs act as free radical scavengers in biological systems. J. Immunol. 138, 2177-2183
  45. Schulze-Osthoff, K., Beyaert, R., Vandevoorde, V., Haegeman, G. and Fiers, W. (1993) Depletion of the mitochondrial electron transport abrogates the cytotoxic and gene-inductive effects of TNF. EMBO J. 12, 3095-3104
  46. Schutze, S., Potthoff, K., Machleidt, T., Berkovic, D., Wiegmann, K. and Kronke, M. (1992) TNF activates NF-kappa B by phosphatidylcholine-specific phospholipase C-induced 'acidic' sphingomyelin breakdown. Cell. 71, 765-776 https://doi.org/10.1016/0092-8674(92)90553-O
  47. Schwenger, P., Alpert, D., Skolnik, E. Y. and Vilcek, J. (1998) Activation of p38 mitogen-activated protein kinase by sodium salicylate leads to inhibition of tumor necrosis factor-induced IkappaB alpha phosphorylation and degradation. Mol. Cell. Biol. 18, 78-84
  48. Shalaby, M. R., Sundan, A., Loetscher, H., Brockhaus, M., Lesslauer, W. and Espevik, T. (1990) Binding and regulation of cellular functions by monoclonal antibodies against human tumor necrosis factor receptors. J. Exp. Med. 172, 1517-1520 https://doi.org/10.1084/jem.172.5.1517
  49. Smith, C. A., Farrah, T. and Goodwin, R. G. (1994) The TNF receptor superfamily of cellular and viral proteins: activation, costimulation, and death. Cell. 76, 959-962 https://doi.org/10.1016/0092-8674(94)90372-7
  50. Stanger, B. Z., Leder, P., Lee, T. H., Kim, E. and Seed, B. (1995) RIP: a novel protein containing a death domain that interacts with Fas/APO-1 (CD95) in yeast and causes cell death. Cell. 81, 513-523 https://doi.org/10.1016/0092-8674(95)90072-1
  51. Suzuki, Y. J., Forman, H. J. and Sevanian, A. (1997) Oxidants as stimulators of signal transduction. Free Radic. Biol. Med. 22, 269-285 https://doi.org/10.1016/S0891-5849(96)00275-4
  52. Tartaglia, L. A., Weber, R. F., Figari, I. S., Reynolds, C., Palladino, M. A. Jr and Goeddel, D. V. (1991) The two different receptors for tumor necrosis factor mediate distinct cellular responses. Proc. Natl. Acad. Sci. USA 88, 9292-9296 https://doi.org/10.1073/pnas.88.20.9292
  53. Thommesen, L., Sjursen, W., Gasvik, K., Hanssen, W., Brekke, O. L., Skattebol, L., Holmeide, A. K., Espevik, T., Johansen, B. and Laegreid, A. (1998) Selective inhibitors of cytosolic or secretory phospholipase A2 block TNF-induced activation of transcription factor nuclear factor-kappa B and expression of ICAM-1. J. Immunol. 161, 3421-3430
  54. Updyke, T. V. and Nicolson, G. L. (1984) Immunoaffinity isolation of membrane antigens with biotinylated monoclonal antibodies and immobilized streptavidin matrices. J. Immunol. Methods 73, 83-95 https://doi.org/10.1016/0022-1759(84)90034-6
  55. van Puijenbroek, A. A., Wissink, S., van der Saag, P. T. and Peppelenbosch, M. P. (1999) Phospholipase A2 inhibitors and leukotriene synthesis inhibitors block TNF-induced NF-kappaB activation. Cytokine 11, 104-110 https://doi.org/10.1006/cyto.1998.0404
  56. Vane, J. R. and Botting, R. M. (1995) New insights into the mode of action of anti-inflammatory drugs. Inflamm. Res. 44, 1-10 https://doi.org/10.1007/BF01630479
  57. Wiegmann, K., Schutze, S., Machleidt, T., Witte, D. and Kronke, M. (1994) Functional dichotomy of neutral and acidic sphingomyelinases in tumor necrosis factor signaling. Cell. 78, 1005-1015 https://doi.org/10.1016/0092-8674(94)90275-5
  58. Yang, Z., Costanzo, M., Golde, D. W. and Kolesnick, R. N. (1993) Tumor necrosis factor activation of the sphingomyelin pathway signals nuclear factor kappa B translocation in intact HL-60 cells. J. Biol. Chem. 268, 20520-20523

Cited by

  1. Differential regulation of TNF receptor 1 and receptor 2 in adiponectin expression following myocardial ischemia vol.168, pp.3, 2013, https://doi.org/10.1016/j.ijcard.2013.01.222
  2. Differential pro-inflammatory responses of TNF-α receptors (TNFR1 and TNFR2) on LOX-1 signalling vol.42, pp.6, 2015, https://doi.org/10.1007/s11033-014-3841-y
  3. Microglia in cerebral ischemia: molecular actions and interactionsThis paper is one of a selection of papers published in this Special Issue, entitled Young Investigator's Forum. vol.84, pp.1, 2006, https://doi.org/10.1139/Y05-143
  4. Genetic deletion of TNFRII gene enhances the Alzheimer-like pathology in an APP transgenic mouse model via reduction of phosphorylated I B  vol.23, pp.18, 2014, https://doi.org/10.1093/hmg/ddu206
  5. Serum-soluble tumor necrosis factor receptor 2 (sTNF-R2) level determines clinical outcome in patients with aggressive non-Hodgkin's lymphoma vol.77, pp.3, 2006, https://doi.org/10.1111/j.1600-0609.2006.00702.x
  6. Chlorpyrifos and Cypermethrin Induce Apoptosis in Human Neuroblastoma Cell Line SH-SY5Y vol.116, pp.2, 2015, https://doi.org/10.1111/bcpt.12285
  7. Molecular and functional interactions between tumor necrosis factor-alpha receptors and the glutamatergic system in the mouse hippocampus: Implications for seizure susceptibility vol.161, pp.1, 2009, https://doi.org/10.1016/j.neuroscience.2009.03.005
  8. Immunoregulatory role of TNFα in inflammatory kidney diseases vol.76, pp.3, 2009, https://doi.org/10.1038/ki.2009.142
  9. Liver innate immune cells and insulin resistance: the multiple facets of Kupffer cells vol.280, pp.2, 2016, https://doi.org/10.1111/joim.12483
  10. Tumor necrosis factor receptor cross-talk vol.278, pp.6, 2011, https://doi.org/10.1111/j.1742-4658.2011.08017.x
  11. TNF-alpha-induced apoptosis is prevented by erythropoietin treatment on SH-SY5Y cells vol.315, pp.3, 2009, https://doi.org/10.1016/j.yexcr.2008.11.005
  12. Enhanced Apoptosis of Monocytes from Complication-Free Juvenile-Onset Diabetes Mellitus Type 1 May Be Ameliorated by TNF-αInhibitors vol.2014, 2014, https://doi.org/10.1155/2014/946209
  13. Immune-Neuroendocrine Integration at the Adrenal Gland: Cytokine Control of the Adrenomedullary Transcriptome vol.48, pp.2, 2012, https://doi.org/10.1007/s12031-012-9745-1
  14. The ErbB4 Growth Factor Receptor Is Required for Colon Epithelial Cell Survival in the Presence of TNF vol.136, pp.1, 2009, https://doi.org/10.1053/j.gastro.2008.09.023
  15. Tumour necrosis factor (TNF)-mediated NF-κB activation facilitates cellular invasion of non-professional phagocytic epithelial cell lines by Trypanosoma cruzi vol.13, pp.10, 2011, https://doi.org/10.1111/j.1462-5822.2011.01636.x