Anthrax SET protein: A potential virulence determinant that epigenetically represses Nf-κB activation in infected macrophages

Journal of Biological Chemistry

Volumn 288, Issue 32, 2013, Pages 23458-23472

  Mujtaba, Shiraz ^a   Winer, Benjamin Y ^b   Jaganathan, Anbalagan ^a   Patel, Jigneshkumar ^a   Sgobba, Miriam ^c   Schuch, Raymond ^b   Gupta, Yogesh K ^a   Haider, Shozeb ^c   Wang, Rong ^a   Fischetti, Vincent A ^b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRACIS; HUMAN PATHOGENS; PROTEIN FUNCTIONS;

BACTERIA;

PROTEINS;

BACTERIAL PROTEIN; HISTONE H1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SET PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACILLUS ANTHRACIS; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL VIRULENCE; CELL NUCLEUS; CONTROLLED STUDY; EMBRYO; EPIGENETICS; GENE EXPRESSION; GENE SILENCING; HISTONE METHYLATION; HUMAN; HUMAN CELL; MACROPHAGE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHYLOGENY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; REGULATORY MECHANISM; SET GENE; STRAIN DIFFERENCE; WILD TYPE;

B. ANTHRACIS; EPIGENETICS; GENE REGULATION; HISTONE METHYLATION; HOST-PATHOGEN INTERACTIONS; MICROBIAL PATHOGENESIS; NF-ΚB; SEPTATION;

ANIMALS; ANTHRAX; BACILLUS ANTHRACIS; BACTERIAL PROTEINS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, BACTERIAL; HELA CELLS; HUMANS; MACROPHAGES; MICE; NF-KAPPA B; PROTEIN METHYLTRANSFERASES; TRANSCRIPTION, GENETIC; VIRULENCE FACTORS;

EID: 84881449055     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.467696     Document Type: Article

References (59)

1. Finlay, B. B., and McFadden, G. (2006) Anti-immunology. Evasion of the host immune system by bacterial and viral pathogens. Cell 124, 767-782
2. Sweet, C. R., Conlon, J., Golenbock, D. T., Goguen, J., and Silverman, N. (2007) YopJ targets TRAF proteins to inhibit TLR-mediated NF-κB, MAPK, and IRF3 signal transduction. Cell Microbiol. 9, 2700-2715
3. Zhou, H., Monack, D. M., Kayagaki, N., Wertz, I., Yin, J., Wolf, B., and Dixit, V. M. (2005) Yersinia virulence factor YopJ acts as a deubiquitinase to inhibit NF-κB activation. J. Exp. Med. 202, 1327-1332
4. Mukherjee, S., Keitany, G., Li, Y., Wang, Y., Ball, H. L., Goldsmith, E. J., and Orth, K. (2006) Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312, 1211-1214
5. Paquette, N., Conlon, J., Sweet, C., Rus, F., Wilson, L., Pereira, A., Rosadini, C. V., Goutagny, N., Weber, A. N., Lane, W. S., Shaffer, S. A., Maniatis, S., Fitzgerald, K. A., Stuart, L., and Silverman, N. (2012) Serine/threonine acetylation of TGF-activated kinase (TAK1) by Yersinia pestis YopJ inhibits innate immune signaling. Proc. Natl. Acad. Sci. U.S.A. 109, 12710-12715
6. Meinzer, U., Barreau, F., Esmiol-Welterlin, S., Jung, C., Villard, C., Léger, T., Ben-Mkaddem, S., Berrebi, D., Dussaillant, M., Alnabhani, Z., Roy, M., Bonacorsi, S., Wolf-Watz, H., Perroy, J., Ollendorff, V., and Hugot, J. P. (2012) Yersinia pseudotuberculosis effector YopJ subverts the Nod2/ RICK/TAK1 pathway and activates caspase-1 to induce intestinal barrier dysfunction. Cell Host Microbe. 11, 337-351
7. Kim, D. W., Lenzen, G., Page, A. L., Legrain, P., Sansonetti, P. J., and Parsot, C. (2005) The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc. Natl. Acad. Sci. U.S.A. 102, 14046-14051
8. Arbibe, L., Kim, D. W., Batsche, E., Pedron, T., Mateescu, B., Muchardt, C., Parsot, C., and Sansonetti, P. J. (2007) An injected bacterial effector targets chromatin access for transcription factor NF-κB to alter transcription of host genes involved in immune responses. Nat. Immunol. 8, 47-56
9. Mujtaba, S., and Zhou, M. M. (2011) Anti-viral opportunities during transcriptional activation of latent HIV in the host chromatin. Methods 53, 97-101
10. Mujtaba, S., He, Y., Zeng, L., Farooq, A., Carlson, J. E., Ott, M., Verdin, E., and Zhou, M. M. (2002) Structural basis of lysine-acetylated HIV-1 Tat recognition by PCAF bromodomain. Mol. Cell 9, 575-586
11. Qadri, I., Conaway, J. W., Conaway, R. C., Schaack, J., and Siddiqui, A. (1996) Hepatitis B virus transactivator protein, HBx, associates with the components of TFIIH and stimulates the DNA helicase activity of TFIIH. Proc. Natl. Acad. Sci. U.S.A. 93, 10578-10583
12. Ezzell, J. W., and Welkos, S. L. (1999) The capsule of Bacillus anthracis, A review. J. Appl. Microbiol. 87, 250
13. Turnbull, P. C. (2002) Introduction. Anthrax history, disease, and ecology. Curr. Top Microbiol. Immunol. 271, 1-19
14. Koehler, T. M. (2009) Bacillus anthracis physiology and genetics. Mol. Aspects Med. 30, 386-396
15. Barua, S., McKevitt, M., DeGiusti, K., Hamm, E. E., Larabee, J., Shakir, S., Bryant, K., Koehler, T. M., Blanke, S. R., Dyer, D., Gillaspy, A., and Ballard, J. D. (2009) The mechanism of Bacillus anthracis intracellular germination requires multiple and highly diverse genetic loci. Infect. Immun. 77, 23-31
16. Vitale, G., Bernardi, L., Napolitani, G., Mock, M., and Montecucco, C. (2000) Susceptibility of mitogen-activated protein kinase kinase family members to proteolysis by anthrax lethal factor. Biochem. J. 352, 739-745
17. Firoved, A. M., Miller, G. F., Moayeri, M., Kakkar, R., Shen, Y., Wiggins, J. F., McNally, E. M., Tang, W. J., and Leppla, S. H. (2005) Bacillus anthracis edema toxin causes extensive tissue lesions and rapid lethality in mice. Am. J. Pathol. 167, 1309-1320
18. Leppla, S. H. (1982) Anthrax toxin edema factor. A bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc. Natl. Acad. Sci. U.S.A. 79, 3162-3166
19. Duesbery, N. S., Webb, C. P., Leppla, S. H., Gordon, V. M., Klimpel, K. R., Copeland, T. D., Ahn, N. G., Oskarsson, M. K., Fukasawa, K., Paull, K. D., and Vande Woude, G. F. (1998) Proteolytic inactivation of MAP kinase kinase by anthrax lethal factor. Science 280, 734-737
20. Vitale, G., Pellizzari, R., Recchi, C., Napolitani, G., Mock, M., and Montecucco, C. (1998) Anthrax lethal factor cleaves theNterminus of MAPKKs and induces tyrosine/threonine phosphorylation of MAPKs in cultured macrophages. Biochem. Biophys. Res. Commun. 248, 706-711
21. McGillivray, S. M., Ebrahimi, C. M., Fisher, N., Sabet, M., Zhang, D. X., Chen, Y., Haste, N. M., Aroian, R. V., Gallo, R. L., Guiney, D. G., Friedlander, A. M., Koehler, T. M., and Nizet, V. (2009) ClpX contributes to innate defense peptide resistance and virulence phenotypes of Bacillus anthracis. J. Innate Immun. 1, 494-506
22. Tournier, J. N., Ulrich, R. G., Quesnel-Hellmann, A., Mohamadzadeh, M., and Stiles, B. G. (2009) Anthrax, toxins and vaccines. a 125-year journey targeting Bacillus anthracis. Expert Rev. Anti. Infect. Ther. 7, 219-236
23. Zhang, Y., and Reinberg, D. (2001) Transcription regulation by histone methylation. Interplay between different covalent modifications of the core histone tails. Genes Dev. 15, 2343-2360
24. Martin, C., and Zhang, Y. (2005) The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell Biol. 6, 838-849
25. Kouzarides, T. (2002) Histone methylation in transcriptional control. Curr. Opin. Genet. Dev. 12, 198-209
26. Noma, K., Allis, C. D., and Grewal, S. I. (2001) Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 293, 1150-1155
27. Huang, J., and Berger, S. L. (2008) The emerging field of dynamic lysine methylation of non-histone proteins. Curr. Opin. Genet. Dev. 18, 152-158
28. Lachner, M., O'Sullivan, R. J., and Jenuwein, T. (2003) An epigenetic road map for histone lysine methylation. J. Cell Sci. 116, 2117-2124
29. Aravind, L., and Iyer, L. M. (2003) Provenance of SET-domain histone methyltransferases through duplication of a simple structural unit. Cell Cycle 2, 369-376
30. Alvarez-Venegas, R., Sadder, M., Tikhonov, A., and Avramova, Z. (2007) Origin of the bacterial SET domain genes. Vertical or horizontal? Mol. Biol. Evol. 24, 482-497
31. Bannister, A. J., Schneider, R., and Kouzarides, T. (2002) Histone methylation. Dynamic or static? Cell 109, 801-806
32. Sims, R. J., 3rd, Nishioka, K., and Reinberg, D. (2003) Histone lysine methylation. A signature for chromatin function. Trends Genet. 19, 629-639
33. Altschul, S. F., Madden, T. L., SchAffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST. A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402
34. Di Tommaso, P., Moretti, S., Xenarios, I., Orobitg, M., Montanyola, A., Chang, J. M., Taly, J. F., and Notredame, C. (2011) T-Coffee. A web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res. 39, W13-W17
35. Notredame, C., Higgins, D. G., and Heringa, J. (2000) T-Coffee. A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217
36. Sali, A., and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815
37. Southall, S. M., Wong, P. S., Odho, Z., Roe, S. M., and Wilson, J. R. (2009) Structural basis for the requirement of additional factors for MLL1 SET domain activity and recognition of epigenetic marks. Mol. Cell 33, 181-191
38. Couture, J. F., Hauk, G., Thompson, M. J., Blackburn, G. M., and Trievel, R. C. (2006) Catalytic roles for carbon-oxygen hydrogen bonding in SET domain lysine methyltransferases. J. Biol. Chem. 281, 19280-19287
39. Mujtaba, S., Manzur, K. L., Gurnon, J. R., Kang, M., Van Etten, J. L., and Zhou, M. M. (2008) Epigenetic transcriptional repression of cellular genes by a viral SET protein. Nat. Cell Biol. 10, 1114-1122
40. Borah, J. C., Mujtaba, S., Karakikes, I., Zeng, L., Muller, M., Patel, J., Moshkina, N., Morohashi, K., Zhang, W., Gerona-Navarro, G., Hajjar, R. J., and Zhou, M. M. (2011) A small molecule binding to the coactivator CREBbinding protein blocks apoptosis in cardiomyocytes. Chem. Biol. 18, 531-541
41. Mujtaba, S., He, Y., Zeng, L., Yan, S., Plotnikova, O., Sachchidanand, Sanchez, R., Zeleznik-Le, N. J., Ronai, Z., and Zhou, M. M. (2004) Structural mechanism of the bromodomain of the coactivator CBP in p53 transcriptional activation. Mol. Cell 13, 251-263
42. Dixon, T. C., Fadl, A. A., Koehler, T. M., Swanson, J. A., and Hanna, P. C. (2000) Early Bacillus anthracis-macrophage interactions. Intracellular survival survival and escape. Cell Microbiol. 2, 453-463
43. Gut, I. M., Tamilselvam, B., Prouty, A. M., Stojkovic, B., Czeschin, S., van der Donk, W. A., and Blanke, S. R. (2011) Bacillus anthracis spore interactions with mammalian cells. Relationship between germination state and the outcome of in vitro. BMC Microbiol. 11, 46
44. Fazzini, M. M., Schuch, R., and Fischetti, V. A. (2010) A novel spore protein, ExsM, regulates formation of the exosporium in Bacillus cereus and Bacillus anthracis and affects spore size and shape. J. Bacteriol. 192, 4012-4021
45. Schuch, R., and Fischetti, V. A. (2009) The secret life of the anthrax agent Bacillus anthracis. Bacteriophage-mediated ecological adaptations. PLoS ONE 4, e6532
46. Dodatko, T., Akoachere, M., Muehlbauer, S. M., Helfrich, F., Howerton, A., Ross, C., Wysocki, V., Brojatsch, J., and Abel-Santos, E. (2009) Bacillus cereus spores release alanine that synergizes with inosine to promote germination. PLoS ONE 4, e6398
47. Giebel, J. D., Carr, K. A., Anderson, E. C., and Hanna, P. C. (2009) The germination-specific lytic enzymes SleB, CwlJ1, and CwlJ2 each contribute to Bacillus anthracis spore germination and virulence. J. Bacteriol. 191, 5569-5576
48. Schuch, R., Nelson, D., and Fischetti, V. A. (2002) A bacteriolytic agent that detects and kills Bacillus anthracis. Nature 418, 884-889
49. Goodman, R. H., and Smolik, S. (2000) CBP/p300 in cell growth, transformation, and development. Genes Dev. 14, 1553-1577
50. Giles, R. H., Peters, D. J., and Breuning, M. H. (1998) Conjunction dysfunction. CBP/p300 in human disease. Trends Genet. 14, 178-183
51. Imhof, A., Yang, X. J., Ogryzko, V. V., Nakatani, Y., Wolffe, A. P., and Ge, H. (1997) Acetylation of general transcription factors by histone acetyltransferases. Curr. Biol. 7, 689-692
52. Pellizzari, R., Guidi-Rontani, C., Vitale, G., Mock, M., and Montecucco, C. (2000) Lethal factor of Bacillus anthracis cleaves the N terminus of MAPKKs. Analysis of the intracellular consequences in macrophages. Int. J. Med. Microbiol. 290, 421-427
53. Kirby, J. E. (2004) Anthrax lethal toxin induces human endothelial cell apoptosis. Infect. Immun. 72, 430-439
54. Mogridge, J. (2004) Anthrax and bioterrorism. Are we prepared? Lancet 364, 393-395
55. Wang, S., Arends, S. J., Weiss, D. S., and Newman, E. B. (2005)Adeficiency in S-adenosylmethionine synthetase interrupts assembly of the septal ring in Escherichia coli K-12. Mol. Microbiol. 58, 791-799
56. Ling, B. M., Gopinadhan, S., Kok, W. K., Shankar, S. R., Gopal, P., Bharathy, N., Wang, Y., and Taneja, R. (2012) G9a mediates Sharp-1-dependent inhibition of skeletal muscle differentiation. Mol. Biol. Cell 23, 4778-4785
57. Ling, B. M., Bharathy, N., Chung, T. K., Kok, W. K., Li, S., Tan, Y. H., Rao, V. K., Gopinadhan, S., Sartorelli, V., Walsh, M. J., and Taneja, R. (2012) Lysine methyltransferase G9a methylates the transcription factor MyoD and regulates skeletal muscle differentiation. Proc. Natl. Acad. Sci. U.S.A. 109, 841-846
58. Kuzmichev, A., Jenuwein, T., Tempst, P., and Reinberg, D. (2004) Different EZH2-containing complexes target methylation of histone H1 or nucleosomal histone H3. Mol. Cell 14, 183-193
59. Weiss, T., Hergeth, S., Zeissler, U., Izzo, A., Tropberger, P., Zee, B. M., Dundr, M., Garcia, B. A., Daujat, S., and Schneider, R. (2010) Histone H1 variant-specific lysine methylation by G9a/KMT1C and Glp1/KMT1D. Epigenetics Chromatin 3, 7