C/EBPβ phosphorylation rescues macrophage dysfunction and apoptosis induced by anthrax lethal toxin

American Journal of Physiology - Cell Physiology

Volumn 293, Issue 6, 2007, Pages

  Buck, Martina ^a   Chojkier, Mario ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Macrophages; Mitogen associated protein kinase; Ribosomal S6 kinase 2

Indexed keywords

ANTHRAX TOXIN; CCAAT ENHANCER BINDING PROTEIN; S6 KINASE; BACTERIAL ANTIGEN; BACTERIAL TOXIN; CCAAT ENHANCER BINDING PROTEIN BETA; MITOGEN ACTIVATED PROTEIN KINASE KINASE; RIBOSOMAL PROTEIN S6 KINASE, 90KDA, POLYPEPTIDE 3; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ANIMAL; DRUG EFFECT; GENETICS; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

BACILLUS ANTHRACIS; MUS; MUS MUSCULUS;

ANIMALS; ANTIGENS, BACTERIAL; APOPTOSIS; BACTERIAL TOXINS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PHAGOCYTOSIS; PHOSPHORYLATION; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA;

EID: 37149024557     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00141.2007     Document Type: Article

References (52)

1. Agrawal A, Lingappa J, Leppla SH, Agrawal S, Jabbar A, Quinn C, Pulendran B. Impairment of dendritic cells and adaptive immunity by anthrax lethal toxin. Nature 424: 329-334, 2003.
2. Akira S, Isshiki H, Sugita T, Tanabe O, Kinoshita S, Nishio Y, Nakajima T, Hirano T, Kishimoto T. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J 9: 1897-1906, 1990.
3. An MR, Hsieh CC, Reisner PD, Rabek JP, Scott SG, Kuninger DT, Papaconstantinou J. Evidence for posttranscriptional regulation of C/EBPα and C/EBPβ isoform expression during the lipopolysaccharide- mediated acute-phase response. Mol Cell Biol 16: 2295-2306, 1996.
4. Ashkenazi A, Dixit V. Death receptors: signaling and modulation. Science 281: 1305-1308, 1998.
5. Bardwell A, Abdollahi M, Bardwell L. Anthrax lethal factor-cleavage products of MAPK (mitogen-activated protein kinase) kinases exhibit reduced binding to their cognate MAPKs. Biochem J 378: 569-577, 2004.
6. Bhatt R, Ferrell J. The protein kinase p90 Rsk as an essential mediator of cytostatic factor activity. Science 286: 1362-1365, 1999.
7. Bonni A, Brunet A, West A, Datta S, Takasu M, Greenberg M. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286: 1358-1362, 1999.
8. Buck M, Chojkier M. C/EBPβ assocoiates with caspase 8 complex proteins and modulates apoptosis in hepatic stellate cells. J Clin Gastroenterol. In press.
9. Buck M, Poli V, Hunter T, Chojkier M. C/EBPβ phosphorylation by RSK creates a functional XEXD caspase inhibitory box critical for cell survival. Mol Cell 8: 807-816, 2001.
10. Buck M, Poli V, van der Geer P, Chojkier M, Hunter T. Phosphorylation of rat serine 105 or mouse threonine 217 in C/EBPβ is required for hepatocyte proliferation induced by TGFα. Mol Cell 4: 1087-1092, 1999.
11. Chakravarti D, LaMorte VJ, Nelson MC, Nakajima T, Schulman IG, Juguilon H, Montminy M, Evans RM. Role of CBP/P300 in nuclear receptor signalling. Nature 383: 99-103, 1996.
12. Chaudry GJ, Moayeri M, Liu S, Leppla SH. Quickening the pace of anthrax research: three advances point towards possible therapies. Trends Microbiol 10: 58-62, 2002.
13. Chopra AP, Boone S, Liang X, Duesbery NS. Anthrax lethal factor proteolysis and inactivation of MAPK kinase. J Biol Chem 278: 9402-9406, 2003.
14. Cui X, Li Y, Haley M, Moayeri M, Fitz Y, Leppla SH, Eichaker PD. Sublethal doses of Bacillus anthracis lethal toxin inhibit inflammation with lipopolysaccharide and Escherichia coli challenge but have opposite effects on survival. J Infect Dis 193: 829-840, 2007.
15. Duesbery NS, Webb CP, Leppla SH, Gordon VM, Klimpel KR, Copeland TD, Ahn NG, Oskarsson MK, Fukasawa K, Paull KD, Vande Woude GF. Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280: 734-737, 1998.
16. Friedlander AM. Macrophages are sensitive to anthrax lethal toxin through an acid-dependent process. J Biol Chem 261: 7123-7126, 1986.
17. Grinberg JM, Abramova FA, Yampolskaya OV, Walker DH, Smith JH. Quantitative pathology of inhalational anthrax I: quantitative microscopic findings. Mod Pathol 14: 482-495, 2002.
18. Rsk. Science 286: 1365-1367, 1999.
19. Guidi-Rontani C. The alveolar macrophage: the Trojan horse of Bacillus anthracis. Trends Microbiol 10: 405-409, 2002.
20. Hsu LC, Park JM, Zhang K, Luo JL, Maeda S, Kaufman RJ, Eckmann L, Guiney DG, Karin M. The protein kinase PKR is required for macrophage apoptosis after activation of Toll-like receptor 4. Nature 428: 341-345, 2004.
21. Huang RP. Detection of multiple proteins in an antibody-based protein microarray system. J Immunol Methods 255: 1-13, 2001.
22. Johnson GL, Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298: 1911-1934, 2002.
23. Kamei Y, Xu L, Heinzel T, Torchia J, Kurokawa R, Gloss B, Lin SC, Heyman RA, Rose DW, Glass CK, Rosenfeld MG. A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors. Cell 85: 403-414, 1996.
24. Knapp S, Matt U, Leitinger N, van der Poll T. Oxidized phospholipids inhibit phagocytosis and impair outcome in gram-negative sepsis in vivo. J Immunol 178: 993-1001, 2007.
25. Kowenz-Leutz E, Twamley G, Ansieau S, Leutz A. Novel mechanism of C/EBP beta (NF-M) transcriptional control: activation through derepression. Genes Dev 8: 2781-2791, 1994.
26. Lang R, Rutschman RL, Greaves DR, Murray PJ. Autocrine deactivation of macrophages in transgenic mice constitutively overexpressing il-10 under control of the human CD68 promoter. J Immunol 168: 3402-3411, 2002.
27. Menard C, Hein P, Paquin A, Savelson A, Yang XM, Lederfein D, Barnabe-Heider F, Mir AA, Sterneck E, Peterson AC, Johnson PF, Vinson C, Miller F. An essential role for a MEK-C/EBP pathway during growth factor-regulated cortical neurogenesis. Neuron 36: 597-610, 2002.
28. Moayeri M, Haines D, Young HA, Leppla SH. Bacillus anthracis lethal toxin induces TNF-α-independent hypoxia-mediated toxicity in mice. J Clin Invest 112: 670-682, 2003.
29. Mourez M, Lacy DB, Cunningham K, Legmann R, Sellman BR, Mogridge J, Collier RJ. 2001: a year of major advances in anthrax toxin research. Trends Microbiol 10: 287-293, 2002.
30. Muehlbauer SM, Evering TH, Bonuccelli G, Squires RC, Ashton AW, Porcelli SA, Lisanti MP, Brojatsch J. Anthrax lethal toxin kills macrophages in a strain-specific manner by apoptosis or caspase-1-mediated necrosis. Cell Cycle 6: 758-766, 2007.
31. Nakagawa R, Naka T, Tsutsui H, Fujimoto M, Kimura A, Abe T, Seki E, Sato S, Takeuchi O, Takeda K, Akira S, Yamanishi K, Kawase I, Nakanishi K, Kishimoto T. SOCS-1 participates in negative regulation of LPS responses. Immunity 17: 677-687, 2002.
32. Natsuka S, Akira S, Nishio Y, Hashimoto S, Sugita T, Isshiki H, Kishimoto T. Macrophage differentiation-specific expression of NF-IL6, a transcription factor for interleukin-6. Blood 79: 460-466, 1992.
33. Ness SA, Kowenz-Leutz E, Casini T, Graf T, Leutz A. Myb and NF-M: combinatorial activators of myeloid genes in heterologous cell types. Genes Dev 7: 749-759, 1993.
34. Panchal RG, Ruthel G, Brittingham KC, Lane D, Kenny TA, Gussio R, Lazo JS, Bavari S. Chemical genetic screening identifies critical pathways in anthrax lethal toxin-induced pathogenesis. Chem Biol 14: 245-255, 2007.
35. Park JM, Greten FR, Li ZW, Karin M. Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition. Science 297: 2048-2051, 2002.
36. Popov SG, Villasmil R, Bernardi J, Grene E, Cardwell J, Wu A, Alibek D, Bailey C, Alibek K. Lethal toxin of Bacillus anthracis causes apoptosis of macrophages. Biochem Biophys Res Commun 293: 349-355, 2002.
37. Ranjan P, Boss J. C/EBPβ regulates TNF induced MnSOD expression and protection against apoptosis. Apoptosis 11: 1837-1849, 2006.
38. Ribot WJ, Panchal RG, Brittingham KC, Ruthel G, Kenny TA, Lane D, Curry B, Hoover TA, Friedlander AM, Bavari S. Anthrax lethal toxin impairs innate immune functions of alveolar macrophages and facilitates Bacillus anthracis survival. Infect Immun 74: 5029-5034, 2006.
39. Rudel T, Bokoch G. Membrane and morphological changes in apoptotic cells regulated by caspase-mediated activation of PAK2. Science 276: 1571-1574, 1997.
40. Sasmono RT, Oceandy D, Pollard JW, Tong W, Pavli P, Wainwright BJ, Ostrowski MC, Himes SR, Hume DA. A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse. Blood 101: 1155-1163, 2003.
41. Sassone-Corsi P, Mizzen C, Cheung P, Crosio C, Monaco L, Jacquot S, Hanauer A, Allis C. Requirement of Rsk-2 for epidermal growth factor-activated phosphorylation of histone H3. Science 285: 886-891, 1999.
42. Screpanti I, Romani L, Musiani P, Modesti A, Fattori E, Lazzaro D, Sellitto C, Scarpa S, Bellavia D, Lattanzio G, Bistoni F, Frati L, Cortese R, Gulino A, Ciliberto G, Constantini F, Poli V. Lymphoproliferative disorder and imbalanced T-helper response in C/EBPβ-deficient mice. EMBO J 14: 1932-1941, 1995.
43. Stennicke HR, Salvesen GS. Caspase assays. Methods Enzymol 322: 91-100, 2000.
44. Tanaka T, Akira S, Yoshida K, Umemoto M, Yoneda Y, Shirafuji N, Fujiwara H, Suematsu S, Yoshida N, Kishimoto T. Targeted disruption of the NF-IL6 gene discloses its essential role in bacteria killing and tumor cytotoxicity by macrophages. Cell 80: 353-361, 1995.
45. Thornberry N, Lazebnik Y. Caspases: enemies within. Science 281: 1312-1316, 1998.
46. Vitale G, Bernardi L, Napolitani G, Mock M, Montecucco C. Susceptibility of mitogen-activated protein kinase family members to proteolysis by anthrax lethal factor. Biochem J 352: 739-745, 2000.
47. Vitale G, Pellizzari R, Recchi C, Napolitani G, Mock M, Montecucco C. Anthrax lethal factor cleaves the n-terminus of MAPKKs and induces tyrosine/threonine phosphorylation of MAPKs in cultured macrophages. Biochem Biophys Res Commun 248: 706-711, 1998.
48. Watts C. The bell tolls for phagosome maturation. Science 304: 976-977, 2004.
49. Whitmarsh A, Davis R. A central control for cell growth. Nature 403: 255-256, 2000.
50. Yoon K, Zhu S, Ewing SJ, Smart RC. Decreased survival of C//EBPβ-deficient keratinocytes is due to aberrant regulation of p53 levels and function. Oncogene 26: 360-367, 2006.
51. Yu T, Robotham JL, Yoon Y. Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc Natl Acad Sci USA 103: 2653-2658, 2006.
52. Zhou HR, Islam Z, Pestka JJ. Induction of competing apoptotic and survival signaling pathways in the macrophage by the ribotoxic trichothecene deoxynivalenol. Toxicol Sci 87: 113-122, 2005.