Bordetella pertussis adenylate cyclase toxin blocks induction of bactericidal nitric oxide in macrophages through cAMP-dependent activation of the SHP-1 phosphatase

Journal of Immunology

Volumn 194, Issue 10, 2015, Pages 4901-4913

  Cerny, Ondrej ^a   Kamanova, Jana ^a,b   Masin, Jiri ^a   Bibova, Ilona ^a   Skopova, Karolina ^a   Sebo, Peter ^a  

^a INSTITUTE OF MATHEMATICS   (Czech Republic)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE TOXIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PROTEIN TYROSINE PHOSPHATASE SHP 1; PROTEIN TYROSINE PHOSPHATASE SHP 2; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR AP 1; PTPN6 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; BORDETELLA PERTUSSIS; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; IMMUNE EVASION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; BORDETELLOSIS; C57BL MOUSE; CELL LINE; ENZYME ACTIVATION; ENZYMOLOGY; HUMAN; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ADENYLATE CYCLASE TOXIN; ANIMALS; BORDETELLA INFECTIONS; BORDETELLA PERTUSSIS; CELL LINE; CYCLIC AMP; ENZYME ACTIVATION; HUMANS; MACROPHAGES; MICE; MICE, INBRED C57BL; NITRIC OXIDE; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84929103798     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402941     Document Type: Article

References (70)

1. Glaser, P., A. Danchin, D. Ladant, O. Barzu, and A. Ullmann. 1988. Bordetella pertussis adenylate cyclase: the gene and the protein. Tokai J. Exp. Clin. Med. 13 (Suppl): 239-252.
2. Goodwin, M. S., and A. A. Weiss. 1990. Adenylate cyclase toxin is critical for colonization and pertussis toxin is critical for lethal infection by Bordetella pertussis in infant mice. Infect. Immun. 58: 3445-3447.
3. Khelef, N., H. Sakamoto, and N. Guiso. 1992. Both adenylate cyclase and hemolytic activities are required by Bordetella pertussis to initiate infection. Microb. Pathog. 12: 227-235.
4. Vojtova, J., J. Kamanova, and P. Sebo. 2006. Bordetella adenylate cyclase toxin: a swift saboteur of host defense. Curr. Opin. Microbiol. 9: 69-75.
5. Weiss, A. A., E. L. Hewlett, G. A. Myers, and S. Falkow. 1984. Pertussis toxin and extracytoplasmic adenylate cyclase as virulence factors of Bordetella pertussis. J. Infect. Dis. 150: 219-222.
6. Wolff, J., G. H. Cook, A. R. Goldhammer, and S. A. Berkowitz. 1980. Calmodulin activates prokaryotic adenylate cyclase. Proc. Natl. Acad. Sci. USA 77: 3841-3844.
7. Guermonprez, P., N. Khelef, E. Blouin, P. Rieu, P. Ricciardi-Castagnoli, N. Guiso, D. Ladant, and C. Leclerc. 2001. The adenylate cyclase toxin of Bordetella pertussis binds to target cells via the alpha(M)beta(2) integrin (CD11b/CD18). J. Exp. Med. 193: 1035-1044.
8. Confer, D. L., and J. W. Eaton. 1982. Phagocyte impotence caused by an invasive bacterial adenylate cyclase. Science 217: 948-950.
9. Eby, J. C., M. C. Gray, and E. L. Hewlett. 2014. Cyclic AMP-mediated suppression of neutrophil extracellular trap formation and apoptosis by the Bordetella pertussis adenylate cyclase toxin. Infect. Immun. 82: 5256-5269.
10. Pearson, R. D., P. Symes, M. Conboy, A. A. Weiss, and E. L. Hewlett. 1987. Inhibition of monocyte oxidative responses by Bordetella pertussis adenylate cyclase toxin. J. Immunol. 139: 2749-2754.
11. Kamanova, J., O. Kofronova, J. Masin, H. Genth, J. Vojtova, I. Linhartova, O. Benada, I. Just, and P. Sebo. 2008. Adenylate cyclase toxin subverts phagocyte function by RhoA inhibition and unproductive ruffling. J. Immunol. 181: 5587-5597.
12. Weingart, C. L., and A. A. Weiss. 2000. Bordetella pertussis virulence factors affect phagocytosis by human neutrophils. Infect. Immun. 68: 1735-1739.
13. Adkins, I., J. Kamanova, A. Kocourkova, M. Svedova, J. Tomala, H. Janova, J. Masin, B. Chladkova, L. Bumba, M. Kovar, et al. 2014. Bordetella adenylate cyclase toxin differentially modulates toll-like receptor-stimulated activation, migration and T cell stimulatory capacity of dendritic cells. PLoS ONE 9: e104064.
14. Friedman, R. L., K. Nordensson, L. Wilson, E. T. Akporiaye, and D. E. Yocum. 1992. Uptake and intracellular survival of Bordetella pertussis in human macrophages. Infect. Immun. 60: 4578-4585.
15. Lamberti, Y. A., J. A. Hayes, M. L. Perez Vidakovics, E. T. Harvill, and M. E. Rodriguez. 2010. Intracellular trafficking of Bordetella pertussis in human macrophages. Infect. Immun. 78: 907-913.
16. Mühl, H., M. Bachmann, and J. Pfeilschifter. 2011. Inducible NO synthase and antibacterial host defence in times of Th17/Th22/T22 immunity. Cell. Microbiol. 13: 340-348.
17. Canthaboo, C., D. Xing, X. Q. Wei, and M. J. Corbel. 2002. Investigation of role of nitric oxide in protection from Bordetella pertussis respiratory challenge. Infect. Immun. 70: 679-684.
18. MacMicking, J., Q. W. Xie, and C. Nathan. 1997. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15: 323-350.
19. Bian, K., F. Ghassemi, A. Sotolongo, A. Siu, L. Shauger, A. Kots, and F. Murad. 2012. NOS-2 signaling and cancer therapy. IUBMB Life 64: 676-683.
20. Bonaparte, K. L., C. A. Hudson, C. Wu, and P. T. Massa. 2006. Inverse regulation of inducible nitric oxide synthase (iNOS) and arginase I by the protein tyrosine phosphatase SHP-1 in CNS glia. Glia 53: 827-835.
21. Pautz, A., J. Art, S. Hahn, S. Nowag, C. Voss, and H. Kleinert. 2010. Regulation of the expression of inducible nitric oxide synthase. Nitric Oxide 23: 75-93.
22. Forget, G., D. J. Gregory, L. A. Whitcombe, and M. Olivier. 2006. Role of host protein tyrosine phosphatase SHP-1 in Leishmania donovani-induced inhibition of nitric oxide production. Infect. Immun. 74: 6272-6279.
23. Massa, P. T., and C. Wu. 1996. The role of protein tyrosine phosphatase SHP-1 in the regulation of IFN-gamma signaling in neural cells. J. Immunol. 157: 5139-5144.
24. Osickova, A., J. Masin, C. Fayolle, J. Krusek, M. Basler, E. Pospisilova, C. Leclerc, R. Osicka, and P. Sebo. 2010. Adenylate cyclase toxin translocates across target cell membrane without forming a pore. Mol. Microbiol. 75: 1550-1562.
25. Buasri, W., A. Impoolsup, C. Boonchird, A. Luengchaichawange, P. Prompiboon, J. Petre, and W. Panbangred. 2012. Construction of Bordetella pertussis strains with enhanced production of genetically-inactivated Pertussis Toxin and Pertactin by unmarked allelic exchange. BMC Microbiol. 12: 61.
26. Weber, C., C. Boursaux-Eude, G. Coralie, V. Caro, and N. Guiso. 2001. Polymorphism of Bordetella pertussis isolates circulating for the last 10 years in France, where a single effective whole-cell vaccine has been used for more than 30 years. J. Clin. Microbiol. 39: 4396-4403.
27. Weischenfeldt, J., and B. Porse. 2008. Bone marrow-derived macrophages (BMM): isolation and applications. CSH Protoc. 2008:pdb.prot5080.
28. Anderson, K. E., K. B. Boyle, K. Davidson, T. A. Chessa, S. Kulkarni, G. E. Jarvis, A. Sindrilaru, K. Scharffetter-Kochanek, O. Rausch, L. R. Stephens, and P. T. Hawkins. 2008. CD18-dependent activation of the neutrophil NADPH oxidase during phagocytosis of Escherichia coli or Staphylococcus aureus is regulated by class III but not class I or II PI3Ks. Blood 112: 5202-5211.
29. Marletta, M. A., P. S. Yoon, R. Iyengar, C. D. Leaf, and J. S. Wishnok. 1988. Macrophage oxidation of L-arginine to nitrite and nitrate: nitric oxide is an intermediate. Biochemistry 27: 8706-8711.
30. Cortese-Krott, M. M., A. Rodriguez-Mateos, G. G. Kuhnle, G. Brown, M. Feelisch, and M. Kelm. 2012. A multilevel analytical approach for detection and visualization of intracellular NO production and nitrosation events using diaminofluoresceins. Free Radic. Biol. Med. 53: 2146-2158.
31. Corraliza, I. M., M. L. Campo, G. Soler, and M. Modolell. 1994. Determination of arginase activity in macrophages: a micromethod. J. Immunol. Methods 174: 231-235.
32. Kubista, M., J. M. Andrade, M. Bengtsson, A. Forootan, J. Jonák, K. Lind, R. Sindelka, R. Sjöback, B. Sjögreen, L. Strömbom, et al. 2006. The real-time polymerase chain reaction. Mol. Aspects Med. 27: 95-125.
33. Stainer, D. W., and M. J. Scholte. 1970. A simple chemically defined medium for the production of phase I Bordetella pertussis. J. Gen. Microbiol. 63: 211-220.
34. Noda, T., and F. Amano. 1997. Differences in nitric oxide synthase activity in a macrophage-like cell line, RAW264.7 cells, treated with lipopolysaccharide (LPS) in the presence or absence of interferon-gamma (IFN-gamma): possible heterogeneity of iNOS activity. J. Biochem. 121: 38-46.
35. Dyet, K., and J. Moir. 2006. Effect of combined oxidative and nitrosative stress on Neisseria meningitidis. Biochem. Soc. Trans. 34: 197-199.
36. Potter, A. J., S. P. Kidd, J. L. Edwards, M. L. Falsetta, M. A. Apicella, M. P. Jennings, and A. G. McEwan. 2009. Thioredoxin reductase is essential for protection of Neisseria gonorrhoeae against killing by nitric oxide and for bacterial growth during interaction with cervical epithelial cells. J. Infect. Dis. 199: 227-235.
37. Mandell, G. L., and E. W. Hook. 1969. Leukocyte bactericidal activity in chronic granulomatous disease: correlation of bacterial hydrogen peroxide production and susceptibility to intracellular killing. J. Bacteriol. 100: 531-532.
38. Eby, J. C., M. C. Gray, J. M. Warfel, C. D. Paddock, T. F. Jones, S. R. Day, J. Bowden, M. D. Poulter, G. M. Donato, T. J. Merkel, and E. L. Hewlett. 2013. Quantification of the adenylate cyclase toxin of Bordetella pertussis in vitro and during respiratory infection. Infect. Immun. 81: 1390-1398.
39. Katada, T., and M. Ui. 1982. Direct modification of the membrane adenylate cyclase system by islet-activating protein due to ADP-ribosylation of a membrane protein. Proc. Natl. Acad. Sci. USA 79: 3129-3133.
40. Bokoch, G. M., T. Katada, J. K. Northup, E. L. Hewlett, and A. G. Gilman. 1983. Identification of the predominant substrate for ADP-ribosylation by islet activating protein. J. Biol. Chem. 258: 2072-2075.
41. Cheung, G. Y., P. Dickinson, G. Sing, M. Craigon, P. Ghazal, R. Parton, and J. G. Coote. 2008. Transcriptional responses of murine macrophages to the adenylate cyclase toxin of Bordetella pertussis. Microb. Pathog. 44: 61-70.
42. Perkins, D. J., M. C. Gray, E. L. Hewlett, and S. N. Vogel. 2007. Bordetella pertussis adenylate cyclase toxin (ACT) induces cyclooxygenase-2 (COX-2) in murine macrophages and is facilitated by ACT interaction with CD11b/CD18 (Mac-1). Mol. Microbiol. 66: 1003-1015.
43. Kadl, A., A. K. Meher, P. R. Sharma, M. Y. Lee, A. C. Doran, S. R. Johnstone, M. R. Elliott, F. Gruber, J. Han, W. Chen, et al. 2010. Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2. Circ. Res. 107: 737-746.
44. Peters-Golden, M. 2009. Putting on the brakes: cyclic AMP as a multipronged controller of macrophage function. Sci. Signal. 2: pe37.
45. Bain, J., L. Plater, M. Elliott, N. Shpiro, C. J. Hastie, H. McLauchlan, I. Klevernic, J. S. Arthur, D. R. Alessi, and P. Cohen. 2007. The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408: 297-315.
46. Blanchette, J., I. Abu-Dayyeh, K. Hassani, L. Whitcombe, and M. Olivier. 2009. Regulation of macrophage nitric oxide production by the protein tyrosine phosphatase Src homology 2 domain phosphotyrosine phosphatase 1 (SHP-1). Immunology 127: 123-133.
47. Kant, A. M., P. De, X. Peng, T. Yi, D. J. Rawlings, J. S. Kim, and D. L. Durden. 2002. SHP-1 regulates Fcgamma receptor-mediated phagocytosis and the activation of RAC. Blood 100: 1852-1859.
48. Lee, S. M., E. J. Kim, K. Suk, and W. H. Lee. 2011. Synthetic peptides containing ITIM-like sequences of IREM-1 inhibit BAFF-mediated regulation of interleukin-8 expression and phagocytosis through SHP-1 and/or PI3K. Immunology 134: 224-233.
49. Koide, M., Y. Kawahara, I. Nakayama, T. Tsuda, and M. Yokoyama. 1993. Cyclic AMP-elevating agents induce an inducible type of nitric oxide synthase in cultured vascular smooth muscle cells. Synergism with the induction elicited by inflammatory cytokines. J. Biol. Chem. 268: 24959-24966.
50. Messmer, U. K., and B. Brüne. 1994. Modulation of inducible nitric oxide synthase in RINm5F cells. Cell. Signal. 6: 17-24.
51. Pang, L., and J. R. Hoult. 1997. Repression of inducible nitric oxide synthase and cyclooxygenase-2 by prostaglandin E2 and other cyclic AMP stimulants in J774 macrophages. Biochem. Pharmacol. 53: 493-500.
52. Chang, S. Y., D. B. Kim, G. R. Ryu, S. H. Ko, I. K. Jeong, Y. B. Ahn, Y. H. Jo, and M. J. Kim. 2013. Exendin-4 inhibits iNOS expression at the protein level in LPS-stimulated Raw264.7 macrophage by the activation of cAMP/PKA pathway. J. Cell. Biochem. 114: 844-853.
53. Koide, N., T. Sugiyama, I. Mori, M. M. Mu, T. Yoshida, and T. Yokochi. 2003. C2-ceramide inhibits LPS-induced nitric oxide production in RAW 264.7 macrophage cells through down-regulating the activation of Akt. J. Endotoxin Res. 9: 85-90.
54. Kuo, P. C., R. A. Schroeder, and S. T. Bartlett. 1997. Endotoxin-mediated synthesis of nitric oxide is dependent on Gq protein signal transduction. Surgery 122: 394-402; discussion 402-393.
55. Bumba, L., J. Masin, R. Fiser, and P. Sebo. 2010. Bordetella adenylate cyclase toxin mobilizes its beta2 integrin receptor into lipid rafts to accomplish translocation across target cell membrane in two steps. PLoS Pathog. 6: e1000901.
56. Gordon, V. M., S. H. Leppla, and E. L. Hewlett. 1988. Inhibitors of receptormediated endocytosis block the entry of Bacillus anthracis adenylate cyclase toxin but not that of Bordetella pertussis adenylate cyclase toxin. Infect. Immun. 56: 1066-1069.
57. Gordon, V. M., W. W. Young, Jr., S. M. Lechler, M. C. Gray, S. H. Leppla, and E. L. Hewlett. 1989. Adenylate cyclase toxins from Bacillus anthracis and Bordetella pertussis. Different processes for interaction with and entry into target cells. J. Biol. Chem. 264: 14792-14796.
58. Rogel, A., and E. Hanski. 1992. Distinct steps in the penetration of adenylate cyclase toxin of Bordetella pertussis into sheep erythrocytes. Translocation of the toxin across the membrane. J. Biol. Chem. 267: 22599-22605.
59. Sebo, P., R. Osicka, and J. Masin. 2014. Adenylate cyclase toxin-hemolysin relevance for pertussis vaccines. Expert Rev. Vaccines 13: 1215-1227.
60. Fang, F. C., and A. Vazquez-Torres. 2002. Nitric oxide production by human macrophages: there's NO doubt about it. Am. J. Physiol. Lung Cell. Mol. Physiol. 282: L941-L943.
61. Tsukamoto, K., K. Hazeki, M. Hoshi, K. Nigorikawa, N. Inoue, T. Sasaki, and O. Hazeki. 2008. Critical roles of the p110 beta subtype of phosphoinositide 3-kinase in lipopolysaccharide-induced Akt activation and negative regulation of nitrite production in RAW 264.7 cells. J. Immunol. 180: 2054-2061.
62. Qi, X. F., D. H. Kim, Y. S. Yoon, J. H. Li, S. B. Song, D. Jin, X. Z. Huang, Y. C. Teng, and K. J. Lee. 2009. The adenylyl cyclase-cAMP system suppresses TARC/CCL17 and MDC/CCL22 production through p38 MAPK and NFkappaB in HaCaT keratinocytes. Mol. Immunol. 46: 1925-1934.
63. Hickey, F. B., C. F. Brereton, and K. H. Mills. 2008. Adenylate cycalse toxin of Bordetella pertussis inhibits TLR-induced IRF-1 and IRF-8 activation and IL-12 production and enhances IL-10 through MAPK activation in dendritic cells. J. Leukoc. Biol. 84: 234-243.
64. la Sala, A., J. He, L. Laricchia-Robbio, S. Gorini, A. Iwasaki, M. Braun, G. S. Yap, A. Sher, K. Ozato, and B. Kelsall. 2009. Cholera toxin inhibits IL-12 production and CD8alpha+ dendritic cell differentiation by cAMP-mediated inhibition of IRF8 function. J. Exp. Med. 206: 1227-1235.
65. Delgado, M., and D. Ganea. 2000. Inhibition of IFN-gamma-induced janus kinase-1-STAT1 activation in macrophages by vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. J. Immunol. 165: 3051-3057.
66. Tai, Z., Y. Lin, Y. He, J. Huang, J. Guo, L. Yang, G. Zhang, and F. Wang. 2014. Luteolin sensitizes the antiproliferative effect of interferon α/γ by activation of Janus kinase/signal transducer and activator of transcription pathway signaling through protein kinase A-mediated inhibition of protein tyrosine phosphatase SHP-2 in cancer cells. Cell. Signal. 26: 619-628.
67. Pellegrino, M. J., and P. J. Stork. 2006. Sustained activation of extracellular signal-regulated kinase by nerve growth factor regulates c-fos protein stabilization and transactivation in PC12 cells. J. Neurochem. 99: 1480-1493.
68. Nandan, D., R. Lo, and N. E. Reiner. 1999. Activation of phosphotyrosine phosphatase activity attenuates mitogen-activated protein kinase signaling and inhibits c-FOS and nitric oxide synthase expression in macrophages infected with Leishmania donovani. Infect. Immun. 67: 4055-4063.
69. Gomez, M. A., I. Contreras, M. Hallé, M. L. Tremblay, R. W. McMaster, and M. Olivier. 2009. Leishmania GP63 alters host signaling through cleavage-activated protein tyrosine phosphatases. Sci. Signal. 2: ra58.
70. Hardin, A. O., E. A. Meals, T. Yi, K. M. Knapp, and B. K. English. 2006. SHP-1 inhibits LPS-mediated TNF and iNOS production in murine macrophages. Biochem. Biophys. Res. Commun. 342: 547-555.