A small molecule deubiquitinase inhibitor increases localization of inducible nitric oxide synthase to the macrophage phagosome and enhances bacterial killing

Infection and Immunity

Volumn 79, Issue 12, 2011, Pages 4850-4857

  Burkholder, Kristin M ^a   Perry, Jeffrey W ^a   Wobus, Christiane E ^a   Donato, Nicholas J ^a   Showalter, Hollis D ^b   Kapuria, Vaibhav ^c   O'Riordan, Mary X D ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DEUBIQUITINASE INHIBITOR WP1130; ENZYME INHIBITOR; INDUCIBLE NITRIC OXIDE SYNTHASE; LISTERIOLYSIN O; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; DEGRASYN; NITRILE; PROTEINASE; PROTEINASE INHIBITOR; PYRIDINE DERIVATIVE;

ANIMAL CELL; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL INFECTION; BACTERICIDAL ACTIVITY; BONE MARROW; CELL VIABILITY; CONTROLLED STUDY; INNATE IMMUNITY; LISTERIA MONOCYTOGENES; MACROPHAGE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; ANIMAL; CELL LINE; DRUG EFFECT; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN TRANSPORT;

ANIMALS; CELL LINE; ENDOPEPTIDASES; ESCHERICHIA COLI; LISTERIA MONOCYTOGENES; MACROPHAGES; MICE; NITRIC OXIDE SYNTHASE TYPE II; NITRILES; PHAGOSOMES; PROTEASE INHIBITORS; PROTEIN TRANSPORT; PYRIDINES; UBIQUITIN;

EID: 84855756293     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05456-11     Document Type: Article

References (38)

1. Alonso, S., K. Pethe, D. G. Russell, and G. E. Purdy. 2007. Lysosomal killing of Mycobacterium mediated by ubiquitin-derived peptides is enhanced by autophagy. Proc. Natl. Acad. Sci. U. S. A. 104:6031-6036.
2. Badwey, J. A., and M. L. Karnovsky. 1980. Active oxygen species and the functions of phagocytic leukocytes. Annu. Rev. Biochem. 49:695-726.
3. Chen, Z. J. 2005. Ubiquitin signalling in the NF-kappaB pathway. Nat. Cell Biol. 7:758-765.
4. Cohen, P., and M. Tcherpakov. 2010. Will the ubiquitin system furnish as many drug targets as protein kinases? Cell 143:686-693.
5. Collins, C. A., et al. 2009. Atg5-independent sequestration of ubiquitinated mycobacteria. PLoS Pathog. 5:e1000430.
6. Davis, A. S., et al. 2007. Mechanism of inducible nitric oxide synthase exclusion from mycobacterial phagosomes. PLoS Pathog. 3:e186.
7. Evans, P. C. 2005. Regulation of pro-inflammatory signalling networks by ubiquitin: identification of novel targets for anti-inflammatory drugs. Expert Rev. Mol. Med. 7:1-19.
8. Finley, D. 2009. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78:477-513.
9. Flannagan, R. S., G. Cosio, and S. Grinstein. 2009. Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat. Rev. Microbiol. 7:355-366.
10. Freitag, N. E., G. C. Port, and M. D. Miner. 2009. Listeria monocytogenes- from saprophyte to intracellular pathogen. Nat. Rev. Microbiol. 7:623-628.
11. Glomski, I. J., A. L. Decatur, and D. A. Portnoy. 2003. Listeria monocytogenes mutants that fail to compartmentalize listerolysin O activity are cytotoxic, avirulent, and unable to evade host extracellular defenses. Infect. Immun. 71:6754-6765.
12. Glynne, P. A., K. E. Darling, J. Picot, and T. J. Evans. 2002. Epithelial inducible nitric-oxide synthase is an apical EBP50-binding protein that directs vectorial nitric oxide output. J. Biol. Chem. 277:33132-33138.
13. Hamill, P., K. Brown, H. Jenssen, and R. E. Hancock. 2008. Novel antiinfectives: is host defence the answer? Curr. Opin. Biotechnol. 19:628-636.
14. Hicke, L., and R. Dunn. 2003. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19:141-172.
15. Hoyer-Hansen, M., et al. 2007. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol. Cell 25:193-205.
16. Johnston, R. B., Jr., C. A. Godzik, and Z. A. Cohn. 1978. Increased superoxide anion production by immunologically activated and chemically elicited macrophages. J. Exp. Med. 148:115-127.
17. Jones, S., and D. A. Portnoy. 1994. Characterization of Listeria monocytogenes pathogenesis in a strain expressing perfringolysin O in place of listeriolysin O. Infect. Immun. 62:5608-5613.
18. Kapuria, V., et al. 2010. Deubiquitinase inhibition by small-molecule WP1130 triggers aggresome formation and tumor cell apoptosis. Cancer Res. 70:9265-9276.
19. Katz, E. J., M. Isasa, and B. Crosas. 2010. A new map to understand deubiquitination. Biochem. Soc. Trans. 38:21-28.
20. Ke, P. Y., and S. S. Chen. 2011. Activation of the unfolded protein response and autophagy after hepatitis C virus infection suppresses innate antiviral immunity in vitro. J. Clin. Invest. 121:37-56.
21. Kirkin, V., D. G. McEwan, I. Novak, and I. Dikic. 2009. A role for ubiquitin in selective autophagy. Mol. Cell 34:259-269.
22. Kolodziejski, P. J., A. Musial, J. S. Koo, and N. T. Eissa. 2002. Ubiquitination of inducible nitric oxide synthase is required for its degradation. Proc. Natl. Acad. Sci. U. S. A. 99:12315-12320.
23. Mazumdar, T., et al. 2010. Regulation of NF-kappaB activity and inducible nitric oxide synthase by regulatory particle non-ATPase subunit 13 (Rpn13). Proc. Natl. Acad. Sci. U. S. A. 107:13854-13859.
24. Miller, B. H., et al. 2004. Mycobacteria inhibit nitric oxide synthase recruitment to phagosomes during macrophage infection. Infect. Immun. 72:2872-2878.
25. Mullally, J. E., and F. A. Fitzpatrick. 2002. Pharmacophore model for novel inhibitors of ubiquitin isopeptidases that induce p53-independent cell death. Mol. Pharmacol. 62:351-358.
26. Nagai, A., et al. 2009. USP14 inhibits ER-associated degradation via interaction with IRE1alpha. Biochem. Biophys. Res. Commun. 379:995-1000.
27. Nathan, C. F., and J. B. Hibbs, Jr. 1991. Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol. 3:65-70.
28. Perrin, A. J., X. Jiang, C. L. Birmingham, N. S. So, and J. H. Brumell. 2004. Recognition of bacteria in the cytosol of mammalian cells by the ubiquitin system. Curr. Biol. 14:806-811.
29. Pham, L. V., et al. 2010. Degrasyn potentiates the antitumor effects of bortezomib in mantle cell lymphoma cells in vitro and in vivo: therapeutic implications. Mol. Cancer Ther. 9:2026-2036.
30. Portnoy, D. A., and S. Jones. 1994. The cell biology of Listeria monocytogenes infection (escape from a vacuole). Ann. N. Y. Acad. Sci. 730:15-25.
31. Radtke, A. L., et al. 2011. Listeria monocytogenes exploits cystic fibrosis transmembrane conductance regulator (CFTR) to escape the phagosome. Proc. Natl. Acad. Sci. U. S. A. 108:1633-1638.
32. Randow, F., and P. J. Lehner. 2009. Viral avoidance and exploitation of the ubiquitin system. Nat. Cell Biol. 11:527-534.
33. Ratia, K., et al. 2008. A noncovalent class of papain-like protease/deubiquitinase inhibitors blocks SARS virus replication. Proc. Natl. Acad. Sci. U. S. A. 105:16119-16124.
34. Schmidt, H. H., T. D. Warner, M. Nakane, U. Forstermann, and F. Murad. 1992. Regulation and subcellular location of nitrogen oxide synthases in RAW264.7 macrophages. Mol. Pharmacol. 41:615-624.
35. Schuerch, D. W., E. M. Wilson-Kubalek, and R. K. Tweten. 2005. Molecular basis of listeriolysin O pH dependence. Proc. Natl. Acad. Sci. U. S. A. 102:12537-12542.
36. Tilney, L. G., and D. A. Portnoy. 1989. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109:1597-1608.
37. Vodovotz, Y., D. Russell, Q. W. Xie, C. Bogdan, and C. Nathan. 1995. Vesicle membrane association of nitric oxide synthase in primary mouse macrophages. J. Immunol. 154:2914-2925.
38. Widjaja, I., et al. 2010. Inhibition of the ubiquitin-proteasome system affects influenza A virus infection at a postfusion step. J. Virol. 84:9625-9631.