Bacillus anthracis Lethal Toxin Represses MMTV Promoter Activity through Transcription Factors

Journal of Molecular Biology

Volumn 389, Issue 3, 2009, Pages 595-605

  Kang, Zhigang ^a   Webster Marketon, Jeanette I ^b   Johnson, Antoinette ^a   Sternberg, Esther M ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

anthrax lethal toxin (LeTx); MMTV promoter; overexpression; repression; transcription factors

Indexed keywords

ANTHRAX LETHAL TOXIN; BACTERIAL TOXIN; BETA ACTIN; HEPATOCYTE NUCLEAR FACTOR 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; OCTAMER TRANSCRIPTION FACTOR 1; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN C FOS; PROTEIN C JUN; PROTEINASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACILLUS ANTHRACIS; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE REPRESSION; LETHAL GENE; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN INDUCTION;

BACILLUS ANTHRACIS; MOUSE MAMMARY TUMOR VIRUS;

EID: 65849488847     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.04.030     Document Type: Article

References (84)

1. Bhatnagar R., and Batra S. Anthrax toxin. Crit. Rev. Microbiol. 27 (2001) 167-200
2. Collier R.J., and Young J.A. Anthrax toxin. Annu. Rev. Cell Dev. Biol. 19 (2003) 45-70
3. Leppla S.H. Anthrax toxin. In: Aktories K., and Just I. (Eds). Bacterial Protein Toxins (2000), Springer, Berlin, Germany 445-472
4. Young J.A., and Collier R.J. Anthrax toxin: receptor binding, internalization, pore formation, and translocation. Annu. Rev. Biochem. 76 (2007) 243-265
5. Mock M., and Fouet A. Anthrax. Annu. Rev. Microbiol. 55 (2001) 647-671
6. Mourez M., Lacy D.B., Cunningham K., Legmann R., Sellman B.R., Mogridge J., and Collier R.J. 2001: a year of major advances in anthrax toxin research. Trends Microbiol. 10 (2002) 287-293
7. Duesbery N.S., Webb C.P., Leppla S.H., Gordon V.M., Klimpel K.R., Copeland T.D., et al. Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280 (1998) 734-737
8. Klimpel K.R., Arora N., and Leppla S.H. Anthrax toxin lethal factor contains a zinc metalloprotease consensus sequence which is required for lethal toxin activity. Mol. Microbiol. 13 (1994) 1093-1100
9. Pellizzari R., Guidi-Rontani C., Vitale G., Mock M., and Montecucco C. Anthrax lethal factor cleaves MKK3 in macrophages and inhibits the LPS/IFNγ-induced release of NO and TNFα. FEBS Lett. 462 (1999) 199-204
10. Pellizzari R., Guidi-Rontani C., Vitale G., Mock M., and Montecucco C. Lethal factor of Bacillus anthracis cleaves the N-terminus of MAPKKs: analysis of the intracellular consequences in macrophages. Int. J. Med. Microbiol. 290 (2000) 421-427
11. Vitale G., Bernardi L., Napolitani G., Mock M., and Montecucco C. Susceptibility of mitogen-activated protein kinase kinase family members to proteolysis by anthrax lethal factor. Biochem. J. 352 Pt. 3 (2000) 739-745
12. Welkos S.L., Keener T.J., and Gibbs P.H. Differences in susceptibility of inbred mice to Bacillus anthracis. Infect. Immun. 51 (1986) 795-800
13. Comer J.E., Galindo C.L., Chopra A.K., and Peterson J.W. GeneChip analyses of global transcriptional responses of murine macrophages to the lethal toxin of Bacillus anthracis. Infect. Immun. 73 (2005) 1879-1885
14. Sapra R., Gaucher S.P., Lachmann J.S., Buffleben G.M., Chirica G.S., Comer J.E., et al. Proteomic analyses of murine macrophages treated with Bacillus anthracis lethal toxin. Microb. Pathog. 41 (2006) 157-167
15. Moayeri M., and Leppla S.H. The roles of anthrax toxin in pathogenesis. Curr. Opin. Microbiol. 7 (2004) 19-24
16. Webster J.I., and Sternberg E.M. Anthrax lethal toxin represses glucocorticoid receptor (GR) transactivation by inhibiting GR-DNA binding in vivo. Mol. Cell. Endocrinol. 241 (2005) 21-31
17. Webster J.I., Tonelli L.H., Moayeri M., Simons Jr. S.S., Leppla S.H., and Sternberg E.M. Anthrax lethal factor represses glucocorticoid and progesterone receptor activity. Proc. Natl Acad. Sci. USA 100 (2003) 5706-5711
18. Edwards C.K.I., Yunger L.M., Lorence R.M., Dantzer R., and Kelley K.W. The pituitary gland is required for protection against lethal effects of Salmonella typhimurium. Proc. Natl Acad. Sci. USA 88 (1991) 2274-2277
19. Gomez S.A., Fernandez G.C., Vanzulli S., Dran G., Rubel C., Berki T., et al. Endogenous glucocorticoids attenuate Shiga toxin-2-induced toxicity in a mouse model of haemolytic uraemic syndrome. Clin. Exp. Immunol. 131 (2003) 217-224
20. MacPhee I.A., Antoni F.A., and Mason D.W. Spontaneous recovery of rats from experimental allergic encephalomyelitis is dependent on regulation of the immune system by endogenous adrenal corticosteroids. J. Exp. Med. 169 (1989) 431-445
21. Moayeri M., Webster J.I., Wiggins J.F., Leppla S.H., and Sternberg E.M. Endocrine perturbation increases susceptibility of mice to anthrax lethal toxin. Infect. Immun. 73 (2005) 4238-4244
22. Ruzek M.C., Pearce B.D., Miller A.H., and Biron C.A. Endogenous glucocorticoids protect against cytokine-mediated lethality during viral infection. J. Immunol. 162 (1999) 3527-3533
23. Sternberg E.M., Hill J.M., Chrousos G.P., Kamilaris T., Listwak S.J., Gold P.W., and Wilder R.L. Inflammatory mediator-induced hypothalamic-pituitary-adrenal axis activation is defective in streptococcal cell wall arthritis-susceptible Lewis rats. Proc. Natl Acad. Sci. USA 86 (1989) 2374-2378
24. Webster J.I., and Sternberg E.M. Role of the hypothalamic-pituitary-adrenal axis, glucocorticoids and glucocorticoid receptors in toxic sequelae of exposure to bacterial and viral products. J. Endocrinol. 181 (2004) 207-221
25. Zuckerman S.H., and Qureshi N. In vivo inhibition of lipopolysaccharide-induced lethality and tumor necrosis factor synthesis by Rhodobacter sphaeroides diphosphoryl lipid A is dependent on corticosterone induction. Infect. Immun. 60 (1992) 2581-2587
26. Kinyamu H.K., and Archer T.K. Modifying chromatin to permit steroid hormone receptor-dependent transcription. Biochim. Biophys. Acta 1677 (2004) 30-45
27. McKenna N.J., Lanz R.B., and O'Malley B.W. Nuclear receptor coregulators: cellular and molecular biology. Endocr. Rev. 20 (1999) 321-344
28. Metivier R., Penot G., Hubner M.R., Reid G., Brand H., Kos M., and Gannon F. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115 (2003) 751-763
29. Geisse S., Scheidereit C., Westphal H.M., Hynes N.E., Groner B., and Beato M. Glucocorticoid receptors recognize DNA sequences in and around murine mammary tumour virus DNA. EMBO J. 1 (1982) 1613-1619
30. Lefebvre P., Berard D.S., Cordingley M.G., and Hager G.L. Two regions of the mouse mammary tumor virus long terminal repeat regulate the activity of its promoter in mammary cell lines. Mol. Cell. Biol. 11 (1991) 2529-2537
31. Pierce J., Fee B.E., Toohey M.G., and Peterson D.O. A mouse mammary tumor virus promoter element near the transcription initiation site. J. Virol. 67 (1993) 415-424
32. Archer T.K., Lefebvre P., Wolford R.G., and Hager G.L. Transcription factor loading on the MMTV promoter: a bimodal mechanism for promoter activation. Science 255 (1992) 1573-1576
33. Bresnick E.H., John S., Berard D.S., LeFebvre P., and Hager G.L. Glucocorticoid receptor-dependent disruption of a specific nucleosome on the mouse mammary tumor virus promoter is prevented by sodium butyrate. Proc. Natl Acad. Sci. USA 87 (1990) 3977-3981
34. Holmqvist P.H., Belikov S., Zaret K.S., and Wrange O. FoxA1 binding to the MMTV LTR modulates chromatin structure and transcription. Exp. Cell Res. 304 (2005) 593-603
35. Beato M. Transcriptional control by nuclear receptors. FASEB J. 5 (1991) 2044-2051
36. Truss M., Bartsch J., Mows C., Chavez S., and Beato M. Chromatin structure of the MMTV promoter and its changes during hormonal induction. Cell. Mol. Neurobiol. 16 (1996) 85-101
37. Herrlich P. Cross-talk between glucocorticoid receptor and AP-1. Oncogene 20 (2001) 2465-2475
38. Belikov S., Astrand C., Holmqvist P.H., and Wrange O. Chromatin-mediated restriction of nuclear factor 1/CTF binding in a repressed and hormone-activated promoter in vivo. Mol. Cell. Biol. 24 (2004) 3036-3047
39. Kim J., Choi M.K., Koo B.S., and Yoon M.Y. Development of high-throughput assay of lethal factor using native substrate. Anal. Biochem. 341 (2005) 33-39
40. Peinado J.R., Kacprzak M.M., Leppla S.H., and Lindberg I. Cross-inhibition between furin and lethal factor inhibitors. Biochem. Biophys. Res. Commun. 321 (2004) 601-605
41. Turk B.E., Wong T.Y., Schwarzenbacher R., Jarrell E.T., Leppla S.H., Collier R.J., et al. The structural basis for substrate and inhibitor selectivity of the anthrax lethal factor. Nat. Struct. Mol. Biol. 11 (2004) 60-66
42. Kobiler D., Gozes Y., Rosenberg H., Marcus D., Reuveny S., and Altboum Z. Efficiency of protection of guinea pigs against infection with Bacillus anthracis spores by passive immunization. Infect. Immun. 70 (2002) 544-560
43. Staats H.F., Alam S.M., Scearce R.M., Kirwan S.M., Zhang J.X., Gwinn W.M., and Haynes B.F. In vitro and in vivo characterization of anthrax anti-protective antigen and anti-lethal factor monoclonal antibodies after passive transfer in a mouse lethal toxin challenge model to define correlates of immunity. Infect. Immun. 75 (2007) 5443-5452
44. Turnbull P.C., Broster M.G., Carman J.A., Manchee R.J., and Melling J. Development of antibodies to protective antigen and lethal factor components of anthrax toxin in humans and guinea pigs and their relevance to protective immunity. Infect. Immun. 52 (1986) 356-363
45. Funder J.W. Mineralocorticoids, glucocorticoids, receptors and response elements. Science 259 (1993) 1132-1133
46. Hsu T.C., Melchiorre Jr. L.P., Maksymowych A.B., Kmiec E., and Litwack G. Assembly of glucocorticoid receptor and c-JUN homodimer on the promoter of mouse mammary tumor virus-long terminal repeat is influenced by order of addition. Biochem. Biophys. Res. Commun. 197 (1993) 1260-1266
47. Siddique H.R., and Sarkar N.H. The interaction of a c-Jun/Fos related protein factor with the U3 sequences of the mouse mammary tumor virus LTR. Biochem. Biophys. Res. Commun. 172 (1990) 348-356
48. Sugiyama T., Scott D.K., Wang J.C., and Granner D.K. Structural requirements of the glucocorticoid and retinoic acid response units in the phosphoenolpyruvate carboxykinase gene promoter. Mol. Endocrinol. 12 (1998) 1487-1498
49. Espinas M.L., Roux J., Pictet R., and Grange T. Glucocorticoids and protein kinase A coordinately modulate transcription factor recruitment at a glucocorticoid-responsive unit. Mol. Cell. Biol. 15 (1995) 5346-5354
50. Stafford J.M., Wilkinson J.C., Beechem J.M., and Granner D.K. Accessory factors facilitate the binding of glucocorticoid receptor to the phosphoenolpyruvate carboxykinase gene promoter. J. Biol. Chem. 276 (2001) 39885-39891
51. Wang J.C., Stromstedt P.E., O'Brien R.M., and Granner D.K. Hepatic nuclear factor 3 is an accessory factor required for the stimulation of phosphoenolpyruvate carboxykinase gene transcription by glucocorticoids. Mol. Endocrinol. 10 (1996) 794-800
52. Wang J.C., Stromstedt P.E., Sugiyama T., and Granner D.K. The phosphoenolpyruvate carboxykinase gene glucocorticoid response unit: identification of the functional domains of accessory factors HNF3 beta (hepatic nuclear factor-3 beta) and HNF4 and the necessity of proper alignment of their cognate binding sites. Mol. Endocrinol. 13 (1999) 604-618
53. Belikov S., Holmqvist P.H., Astrand C., and Wrange O. Nuclear factor 1 and octamer transcription factor 1 binding preset the chromatin structure of the mouse mammary tumor virus promoter for hormone induction. J. Biol. Chem. 279 (2004) 49857-49867
54. Bruggemeier U., Kalff M., Franke S., Scheidereit C., and Beato M. Ubiquitous transcription factor OTF-1 mediates induction of the MMTV promoter through synergistic interaction with hormone receptors. Cell 64 (1991) 565-572
55. Prefontaine G.G., Lemieux M.E., Giffin W., Schild-Poulter C., Pope L., LaCasse E., et al. Recruitment of octamer transcription factors to DNA by glucocorticoid receptor. Mol. Cell. Biol. 18 (1998) 3416-3430
56. Toohey M.G., Lee J.W., Huang M., and Peterson D.O. Functional elements of the steroid hormone-responsive promoter of mouse mammary tumor virus. J. Virol. 64 (1990) 4477-4488
57. Maroder M., Farina A.R., Vacca A., Felli M.P., Meco D., Screpanti I., et al. Cell-specific bifunctional role of Jun oncogene family members on glucocorticoid receptor-dependent transcription. Mol. Endocrinol. 7 (1993) 570-584
58. Cho H.J., Kang J.H., Kwak J.Y., Lee T.S., Lee I.S., Park N.G., et al. Ascofuranone suppresses PMA-mediated matrix metalloproteinase-9 gene activation through the Ras/Raf/MEK/ERK- and AP1-dependent mechanisms. Carcinogenesis 28 (2007) 1104-1110
59. Lamph W.W., Wamsley P., Sassone-Corsi P., and Verma I.M. Induction of proto-oncogene JUN/AP-1 by serum and TPA. Nature 334 (1988) 629-631
60. Bromberg-White J.L., and Duesbery N.S. Biological and biochemical characterization of anthrax lethal factor, a proteolytic inhibitor of MEK signaling pathways. Methods Enzymol. 438 (2008) 355-365
61. Chopra A.P., Boone S.A., Liang X., and Duesbery N.S. Anthrax lethal factor proteolysis and inactivation of MAPK kinase. J. Biol. Chem. 278 (2003) 9402-9406
62. Vitale G., Pellizzari R., Recchi C., Napolitani G., Mock M., and Montecucco C. Anthrax lethal factor cleaves the N-terminus of MAPKKs and induces tyrosine/threonine phosphorylation of MAPKS in cultured macrophages. J. Appl. Microbiol. 87 (1999) 288
63. Barson H.V., Mollenkopf H., Kaufmann S.H., and Rijpkema S. Anthrax lethal toxin suppresses chemokine production in human neutrophil NB-4 cells. Biochem. Biophys. Res. Commun. 374 (2008) 288-293
64. Warfel J.M., and D'Agnillo F. Anthrax lethal toxin enhances TNF-induced endothelial VCAM-1 expression via an IFN regulatory factor-1-dependent mechanism. J. Immunol. 180 (2008) 7516-7524
65. Batty S., Chow E.M., Kassam A., Der S.D., and Mogridge J. Inhibition of mitogen-activated protein kinase signalling by Bacillus anthracis lethal toxin causes destabilization of interleukin-8 mRNA. Cell. Microbiol. 8 (2006) 130-138
66. Khan M.A., Bouzari S., Ma C., Rosenberger C.M., Bergstrom K.S., Gibson D.L., et al. Flagellin-dependent and -independent inflammatory responses following infection by enteropathogenic Escherichia coli and Citrobacter rodentium. Infect. Immun. 76 (2008) 1410-1422
67. Simantov R. Neurotransporters: regulation, involvement in neurotoxicity, and the usefulness of antisense nucleic acids. Biochem. Pharmacol. 50 (1995) 435-442
68. Yang H.S., Jansen A.P., Nair R., Shibahara K., Verma A.K., Cmarik J.L., and Colburn N.H. A novel transformation suppressor, Pdcd4, inhibits AP-1 transactivation but not NF-kappaB or ODC transactivation. Oncogene 20 (2001) 669-676
69. Yokoo T., and Kitamura M. Antioxidant PDTC induces stromelysin expression in mesangial cells via a tyrosine kinase-AP-1 pathway. Am. J. Physiol. 270 (1996) F806-F811
70. Nomura S., and Takano-Yamamoto T. Molecular events caused by mechanical stress in bone. Matrix Biol. 19 (2000) 91-96
71. Reme C.E., Grimm C., Hafezi F., Iseli H.P., and Wenzel A. Why study rod cell death in retinal degenerations and how?. Doc. Ophthalmol. 106 (2003) 25-29
72. Sevilla L., Zaldumbide A., Pognonec P., and Boulukos K.E. Transcriptional regulation of the bcl-x gene encoding the anti-apoptotic Bcl-xL protein by Ets, Rel/NFkappaB, STAT and AP1 transcription factor families. Histol. Histopathol. 16 (2001) 595-601
73. Gruart-Gouilleux V., Engels P., and Sullivan M. Characterization of the human interleukin-5 gene promoter: involvement of octamer binding sites in the gene promoter activity. Eur. J. Immunol. 25 (1995) 1431-1435
74. La Bella F., and Heintz N. Histone gene transcription factor binding in extracts of normal human cells. Mol. Cell. Biol. 11 (1991) 5825-5831
75. Matthias P. Lymphoid-specific transcription mediated by the conserved octamer site: who is doing what?. Semin. Immunol. 10 (1998) 155-163
76. Murphy S., Yoon J.B., Gerster T., and Roeder R.G. Oct-1 and Oct-2 potentiate functional interactions of a transcription factor with the proximal sequence element of small nuclear RNA genes. Mol. Cell. Biol. 12 (1992) 3247-3261
77. Kaestner K.H. The hepatocyte nuclear factor 3 (HNF3 or FOXA) family in metabolism. Trends Endocrinol. Metab. 11 (2000) 281-285
78. Zaret K. Developmental competence of the gut endoderm: genetic potentiation by GATA and HNF3/fork head proteins. Dev. Biol. 209 (1999) 1-10
79. Kaestner K.H., Katz J., Liu Y., Drucker D.J., and Schutz G. Inactivation of the winged helix transcription factor HNF3alpha affects glucose homeostasis and islet glucagon gene expression in vivo. Genes Dev. 13 (1999) 495-504
80. Karin M., Liu Z., and Zandi E. AP-1 function and regulation. Curr. Opin. Cell Biol. 9 (1997) 240-246
81. Johnson R.S., Spiegelman B.M., and Papaioannou V. Pleiotropic effects of a null mutation in the c-fos proto-oncogene. Cell 71 (1992) 577-586
82. Kubovcakova L., Kvetnansky R., and Krizanova O. Use of knock-out mice in studies of stress reactions. Cesk. Fysiol. 52 (2003) 118-128
83. Boyce B.F., Hughes D.E., Wright K.R., Xing L., and Dai A. Recent advances in bone biology provide insight into the pathogenesis of bone diseases. Lab. Invest. 79 (1999) 83-94
84. Wagner E.F. Functions of AP1 (Fos/Jun) in bone development. Ann. Rheum. Dis. 61 Suppl. 2 (2002) ii40-ii42