Orphan nuclear receptor Nur77 is involved in caspase-independent macrophage cell death

Journal of Experimental Medicine

Volumn 197, Issue 11, 2003, Pages 1441-1452

  Kim, Sung Ouk ^a   Ono, Koh ^a   Tobias, Peter S ^a   Han, Jiahuai ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

AICD; LPS; MEF2; zVAD

Indexed keywords

BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE; CASPASE INHIBITOR; CELL NUCLEUS RECEPTOR; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; MYOCYTE SPECIFIC ENHANCER BINDING FACTOR 2 TRANSCRIPTION FACTOR; NUCLEAR RECEPTOR NUR77; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ETS; TRANSCRIPTION FACTOR NAP; TRANSCRIPTION FACTOR RCE; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CONTROLLED STUDY; FEMALE; KNOCKOUT MOUSE; MACROPHAGE; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SEPSIS; SIGNAL TRANSDUCTION;

AMINO ACID CHLOROMETHYL KETONES; AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BASE SEQUENCE; CASPASES; CYSTEINE PROTEINASE INHIBITORS; DNA-BINDING PROTEINS; FEMALE; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; MYOGENIC REGULATORY FACTORS; PROMOTER REGIONS (GENETICS); RECEPTORS, CELL SURFACE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, STEROID; SEPSIS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS; TRANSCRIPTION FACTORS;

EID: 0037944263     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20021842     Document Type: Article

References (55)

1. Rathmell, J.C., and C.B. Thompson. 1999. The central effectors of cell death in the immune system. Annu. Rev. Immunol. 17:781-828.
2. Conroy, L.A., and D.R. Alexander. 1996. The role of intracellular signalling pathways regulating thymocyte and leukemic T cell apoptosis. Leukemia. 10:1422-1435.
3. Winoto, A. 1997. Genes involved in T-cell receptor-mediated apoptosis of thymocytes and T-cell hybridomas. Semin. Immunol. 9:51-58.
4. Donjerkovic, D., and D.W. Scott. 2000. Activation-induced cell death in B lymphocytes. Cell Res. 10:179-192.
5. Munn, D.H., A.C. Beall, D. Song, R.W. Wrenn, and D.C. Throckmorton. 1995. Activation-induced apoptosis in human macrophages: developmental regulation of a novel cell death pathway by macrophage colony-stimulating factor and interferon-γ. J. Exp. Med. 181:127-136.
6. Baumann, S., A. Krueger, S. Kirchhoff, and P.H. Krammer. 2002. Regulation of T cell apoptosis during the immune response. Curr. Mol. Med. 2:257-272.
7. Kroesen, B.J., B. Pettus, C. Luberto, M. Busman, H. Sietsma, L. de Leij, and Y.A. Hannun. 2001. Induction of apoptosis through B-cell receptor cross-linking occurs via de novo generated C16-ceramide and involves mitochondria. J. Biol. Chem. 276:13606-13614.
8. van Rooijen, N., and A. Sanders. 1997. Elimination, blocking, and activation of macrophages: three of a kind? J. Leukoc. Biol. 62:702-709.
9. Gotoh, T., and M. Mori. 1999. Arginase II downregulates nitric oxide (NO) production and prevents NO-mediated apoptosis in murine macrophage-derived RAW 264.7 cells. J. Cell Biol. 144:427-434.
10. Brune, B., C. Gotz, U.K. Messmer, K. Sandau, M.R. Hirvonen, and E.G. Lapetina. 1997. Superoxide formation and macrophage resistance to nitric oxide-mediated apoptosis. J. Biol. Chem. 272:7253-7258.
11. Adler, B., H. Adler, T.W. Jungi, and E. Peterhans. 1995. Interferon-alpha primes macrophages for lipopolysaccharide-induced apoptosis. Biochem. Biophys. Res. Commun. 215:921-927.
12. Adams, D.O., and T.A. Hamilton. 1984. The cell biology of macrophage activation. Annu. Rev. Immunol. 2:283-318.
13. Ricevuti, G. 1997. Host tissue damage by phagocytes. Ann. NY Acad. Sci. 832:426-448.
14. Sullivan, G.W., I.J. Sarembock, and J. Linden. 2000. The role of inflammation in vascular diseases. J. Leukoc. Biol. 67:591-602.
15. Kim, S.O., K. Ono, and J. Han. 2001. Apoptosis by pan-caspase inhibitors in lipopolysaccharide-activated macrophages. Am. J. Physiol. Lung Cell. Mol. Physiol. 281:L1095-L1105.
16. Xaus, J., M. Cardo, A.F. Valledor, C. Soler, J. Lloberas, and A. Celada. 1999. Interferon gamma induces the expression of p21waf-1 and arrests macrophage cell cycle, preventing induction of apoptosis. Immunity. 11:103-113.
17. Talanian, R.V., K.D. Brady, and V.L. Cryns. 2000. Caspases as targets for anti-inflammatory and anti-apoptotic drug discovery. J. Med. Chem. 43:3351-3371.
18. Hotchkiss, R.S., K.C. Chang, P.E. Swanson, K.W. Tinsley, J.J. Hui, P. Klender, S. Xanthoudakis, S. Roy, C. Black, E. Grimm, et al. 2000. Caspase inhibitors improve survival in sepsis: a critical role of the lymphocyte. Nat. Immunol. 1:496-501.
19. Rabinovich, G.A. 2000. Apoptosis as a target for gene therapy in rheumatoid arthritis. Mem. Inst. Oswaldo Cruz. 95 (Suppl.):225-233.
20. Bouchon, A., P.H. Krammer, and H. Walczak. 2000. Critical role for mitochondria in B cell receptor-mediated apoptosis. Eur. J. Immunol. 30:69-77.
21. Kawahara, A., Y. Ohsawa, H. Matsumura, Y. Uchiyama, and S. Nagata. 1998. Caspase-independent cell killing by Fas-associated protein with death domain. J. Cell Biol. 143:1353-1360.
22. Mateo, V., L. Lagneaux, D. Bron, G. Biron, M. Armant, G. Delespesse, and M. Sarfati. 1999. CD47 ligation induces caspase-independent cell death in chronic lymphocytic leukemia. Nat. Med. 5:1277-1284.
23. Drenou, B., V. Blancheteau, D.H. Burgess, R. Fauchet, D.J. Charron, and N.A. Mooney. 1999. A caspase-independent pathway of MHC class II antigen-mediated apoptosis of human B lymphocytes. J. Immunol. 163:4115-4124.
24. Holler, N., R. Zaru, O. Micheau, M. Thome, A. Attinger, S. Valitutti, J.L. Bodmer, P. Schneider, B. Seed, and J. Tschopp. 2000. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 1:489-495.
25. Du, C., M. Fang, Y. Li, L. Li, and X. Wang. 2000. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell. 102:33-42.
26. Hunot, S., and R.A. Flavell. 2001. Apoptosis. Death of a monopoly? Science. 292:865-866.
27. Woronicz, J.D., B. Calnan, V. Ngo, and A. Winoto. 1994. Requirement for the orphan steroid receptor Nur77 in apoptosis of T-cell hybridomas. Nature. 367:277-281.
28. Liu, Z.G., S.W. Smith, K.A. McLaughlin, L.M. Schwartz, and B.A. Osborne. 1994. Apoptotic signals delivered through the T-cell receptor of a T-cell hybrid require the immediate-early gene nur77. Nature. 367:281-284.
29. Winoto, A. 1994. Molecular characterization of the Nur77 orphan steroid receptor in apoptosis. Int. Arch. Allergy Immunol. 105:344-346.
30. Kuang, A.A., D. Cado, and A. Winoto. 1999. Nur77 transcription activity correlates with its apoptotic function in vivo. Eur. J. Immunol. 29:3722-3728.
31. Li, H., S.K. Kolluri, J. Gu, M.I. Dawson, X. Cao, P.D. Hobbs, B. Lin, G. Chen, J. Lu, F. Lin, Z. Xie, J.A. Fontana, J.C. Reed, and X. Zhang. 2000. Cytochrome c release and apoptosis induced by mitochondrial targeting of nuclear orphan receptor TR3. Science. 289:1159-1164.
32. Baker, C.C., I.H. Chaudry, H.O. Gaines, and A.E. Baue. 1983. Evaluation of factors affecting mortality rate after sepsis in a murine cecal ligation and puncture model. Surgery. 94:331-335.
33. Border, J.R. 1988. Hypothesis: sepsis, multiple systems organ failure, and the macrophage. Arch. Surg. 123:285-286.
34. Mathison, J.C., E. Wolfson, and R.J. Ulevitch. 1988. Participation of tumor necrosis in the mediation of gram-negative bacterial lipopolysaccharide-induced injury in rabbits. J. Clin. Invest. 81:1925-1937.
35. Kravchenko, V.V., Z. Pan, J. Han, J.M. Herbert, R.J. Ulevitch, and R.D. Ye. 1995. Platelet-activating factor induces NF-kappa B activation through a GX protein-coupled pathway. J. Biol. Chem. 270:14928-14934.
36. Lee, S.L., R.L. Wesselschmidt, G.P. Linette, O. Kanagawa, J.H. Russell, and J. Milbrandt. 1995. Unimpaired thymic and peripheral T cell death in mice lacking the nuclear receptor NGFI-B (Nur77). Science. 269:532-535.
37. Cheng, L.E., F.K. Chan, D. Cado, and A. Winoto. 1997. Functional redundancy of the Nur77 and Nor-1 orphan steroid receptors in T-cell apoptosis. EMBO J. 16:1865-1875.
38. Winoto, A., and D.R. Littman. 2002. Nuclear hormone receptors in T lymphocytes. Cell. 109(Suppl.):S57-S66.
39. Okamoto, S., Z. Li, C. Ju, M.N. Scholzke, E. Mathews, J. Cui, G.S. Salvesen, E. Bossy-Wetzel, and S.A. Lipton. 1999. Dominant-interfering forms of MEF2 generated by caspase cleavage contribute to NMDA-induced neuronal apoptosis. Proc. Natl. Acad. Sci. USA. 99:3974-3979.
40. Li, M., D.A. Linseman, M.P. Allen, M.K. Meintzer, X. Wang, T. Laessig, M.E. Wierman, and K.A. Heidenreich. 2001. Myocyte enhancer factor 2A and 2D undergo phosphorylation and caspase-mediated degradation during apoptosis of rat cerebellar granule neurons. J. Neurosci. 21:6544-6552.
41. Youn, H.D., L. Sun, R. Prywes, and J.O. Liu. 1999. Apoptosis of T cells mediated by Ca2+-induced release of the transcription factor MEF2. Science. 286:790-793.
42. Youn, H.D., and J.O. Liu. 2000. Cabin1 represses MEF2-dependent Nur77 expression and T cell apoptosis by controlling association of histone deacetylases and acetylases with MEF2. Immunity. 13:85-94.
43. Chen, X., V. Zachar, C. Chang, P. Ebbesen, and X. Liu. 1998. Differential expression of Nur77 family members in human T-lymphotropic virus type 1-infected cells: transactivation of the TR3/nur77 gene by Tax protein. J. Virol. 72:6902-6906.
44. Liu, X., X. Chen, V. Zachar, C. Chang, and P. Ebbesen. 1999. Transcriptional activation of human TR3/nur77 gene expression by human T-lymphotropic virus type I Tax protein through two AP-1-like elements. J. Gen. Virol. 80:3073-3081.
45. Schwandner, R., R. Dziarski, H. Wesche, M. Rothe, and C.J. Kirschning. 1999. Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by toll-like receptor 2. J. Biol. Chem. 274:17406-17409.
46. Zhu, W., J.S. Downey, J. Gu, F. di Padova, H. Gram, and J. Han. 2000. Regulation of TNF Expression by multiple mitogen-activated protein kinase pathways. J. Immunol. 164:6349-6358.
47. Sanghera, J.S., S.L. Weinstein, M. Aluwalia, J. Girn, and S.L. Pelech. 1996. Activation of multiple proline-directed kinases by bacterial lipopolysaccharide in murine macrophages. J. Immunol. 156:4457-4465.
48. Bidere, N., and A. Senik. 2001. Caspase-independent apoptotic pathways in T lymphocytes: a minireview. Apoptosis. 6:371-375.
49. Hara, H., A. Takeda, M. Takeuchi, A.C. Wakeham, A. Itie, M. Sasaki, T.W. Mak, A. Yoshimura, K. Nomoto, and H. Yoshida. 2002. The apoptotic protease-activating factor 1-mediated pathway of apoptosis is dispensable for negative selection of thymocytes. J. Immunol. 168:2288-2295.
50. Masuyama, N., K. Oishi, Y. Mori, T. Ueno, Y. Takahama, and Y. Gotoh. 2001. Akt inhibits the orphan nuclear receptor Nur77 and T-cell apoptosis. J. Biol. Chem. 276:32799-32805.
51. Salh, B., R. Wagey, A. Marotta, J.S. Tao, and S. Pelech. 1998. Activation of phosphatidylinositol 3-kinase, protein kinase B, and p70 S6 kinases in lipopolysaccharide-stimulated Raw 264.7 cells: differential effects of rapamycin, Ly294002, and wortmannin on nitric oxide production. J. Immunol. 161:6947-6954.
52. Slagsvold, H.H., A.C. Ostvold, A.B. Fallgren, and R.E. Paulsen. 2002. Nuclear receptor and apoptosis initiator NGFI-B is a substrate for kinase ERK2. Biochem. Biophys. Res. Commun. 291:1146-1150.
53. Tebo, J.M., W. Chaoqun, Y. Ohmori, and T.A. Hamilton. 1994. Murine inhibitory protein-kappa B alpha negatively regulates kappa B-dependent transcription in lipopolysaccharide-stimulated RAW 264.7 macrophages. J. Immunol. 153:4713-4720.
54. Chakravortty, D., Y. Kato, T. Sugiyama, N. Koide, M.M. Mu, T. Yoshida, and T. Yokochi. 2001. Inhibition of caspase 3 abrogates lipopolysaccharide-induced nitric oxide production by preventing activation of NF-kappaB and c-Jun NH2-terminal kinase/stress-activated protein kinase in RAW 264.7 murine macrophage cells. Infect. Immun. 69:1315-1321.
55. Castillo, S.O., Q. Xiao, M.S. Lyu, C.A. Kozak, and V.M. Nikodem. 1997. Organization, sequence, chromosomal localization, and promoter identification of the mouse orphan nuclear receptor Nurr1 gene. Genomics. 41:250-257.