Distinct spatiotemporal distribution of bacterial toxin-produced cellular camp differentially inhibits opsonophagocytic signaling

Hasan, Shakir; Rahman, W. U.; Sebo, P.; Osicka, R.

doi:10.3390/toxins11060362

Article (Scientific journals)

Distinct spatiotemporal distribution of bacterial toxin-produced cellular camp differentially inhibits opsonophagocytic signaling

Hasan, Shakir; Rahman, W. U.; Sebo, P. et al.

2019 • In Toxins, 11 (6)

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/248022

DOI
10.3390/toxins11060362

PubMed
31226835

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Hasan et al. 2019 ET and CyaA.pdf

Publisher postprint (3.07 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Adenylate cyclase toxin; Edema toxin; Opsonophagocytosis; Phagocytes; Pyk2; Signaling pathway; Syk; Vav; Vav protein; Bacillus anthracis; Bordetella pertussis; Review

Abstract :

[en] Myeloid phagocytes have evolved to rapidly recognize invading pathogens and clear them through opsonophagocytic killing. The adenylate cyclase toxin (CyaA) of Bordetella pertussis and the edema toxin (ET) of Bacillus anthracis are both calmodulin-activated toxins with adenylyl cyclase activity that invade host cells and massively increase the cellular concentrations of a key second messenger molecule, 3′,5′-cyclic adenosine monophosphate (cAMP). However, the two toxins differ in the kinetics and mode of cell entry and generate different cAMP concentration gradients within the cell. While CyaA rapidly penetrates cells directly across their plasma membrane, the cellular entry of ET depends on receptor-mediated endocytosis and translocation of the enzymatic subunit across the endosomal membrane. We show that CyaA-generated membrane-proximal cAMP gradient strongly inhibits the activation and phosphorylation of Syk, Vav, and Pyk2, thus inhibiting opsonophagocytosis. By contrast, at similar overall cellular cAMP levels, the ET-generated perinuclear cAMP gradient poorly inhibits the activation and phosphorylation of these signaling proteins. Hence, differences in spatiotemporal distribution of cAMP produced by the two adenylyl cyclase toxins differentially affect the opsonophagocytic signaling in myeloid phagocytes. © 2019 by the authors. Licensee MDPI, Basel, Switzerland.

Disciplines :

Microbiology

Author, co-author :

Hasan, Shakir ; Université de Liège - ULiège > I3-Immunophysiology

Rahman, W. U.; Institute of Microbiology of the CAS, v. v. i., Videnska 1083Prague 142 20, Czech Republic

Sebo, P.; Institute of Microbiology of the CAS, v. v. i., Videnska 1083Prague 142 20, Czech Republic

Osicka, R.; Institute of Microbiology of the CAS, v. v. i., Videnska 1083Prague 142 20, Czech Republic

Language :

English

Title :

Distinct spatiotemporal distribution of bacterial toxin-produced cellular camp differentially inhibits opsonophagocytic signaling

Publication date :

2019

Journal title :

Toxins

eISSN :

2072-6651

Publisher :

MDPI AG

Volume :

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 05 June 2020

Statistics

Number of views

30 (1 by ULiège)

Number of downloads

33 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Rosales, C.; Uribe-Querol, E. Phagocytosis: A Fundamental Process in Immunity. Biomed. Res. Int. 2017, 2017, 9042851.
Gordon, S. Phagocytosis: An Immunobiologic Process. Immunity 2016, 44, 463–475.
Allen, L.A.; Aderem, A. Molecular definition of distinct cytoskeletal structures involved in complement- and Fc receptor-mediated phagocytosis in macrophages. J. Exp. Med. 1996, 184, 627–637.
Caron, E.; Hall, A. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 1998, 282, 1717–1721.
Kaplan, G. Differences in the mode of phagocytosis with Fc and C3 receptors in macrophages. Scand. J. Immunol. 1977, 6, 797–807.
Schafer, G.; Jacobs, M.; Wilkinson, R.J.; Brown, G.D. Non-opsonic recognition of Mycobacterium tuberculosis by phagocytes. J. Innate Immun. 2009, 1, 231–243.
Ofek, I.; Goldhar, J.; Keisari, Y.; Sharon, N. Nonopsonic phagocytosis of microorganisms. Ann. Rev. Microbiol. 1995, 49, 239–276.
Shi, Y.; Tohyama, Y.; Kadono, T.; He, J.; Miah, S.M.; Hazama, R.; Tanaka, C.; Tohyama, K.; Yamamura, H. Protein-tyrosine kinase Syk is required for pathogen engulfment in complement-mediated phagocytosis. Blood 2006, 107, 4554–4562.
Crowley, M.T.; Costello, P.S.; Fitzer-Attas, C.J.; Turner, M.; Meng, F.; Lowell, C.; Tybulewicz, V.L.; DeFranco, A.L. A critical role for Syk in signal transduction and phagocytosis mediated by Fcgamma receptors on macrophages. J. Exp. Med. 1997, 186, 1027–1039.
Paone, C.; Rodrigues, N.; Ittner, E.; Santos, C.; Buntru, A.; Hauck, C.R. The Tyrosine Kinase Pyk2 Contributes to Complement-Mediated Phagocytosis in Murine Macrophages. J. Innate Immun. 2016, 8, 437–451.
Kedzierska, K.; Vardaxis, N.J.; Jaworowski, A.; Crowe, S.M. FcgammaR-mediated phagocytosis by human macrophages involves Hck, Syk, and Pyk2 and is augmented by GM-CSF. J. Leukoc. Biol. 2001, 70, 322–328.
Gakidis, M.A.; Cullere, X.; Olson, T.; Wilsbacher, J.L.; Zhang, B.; Moores, S.L.; Ley, K.; Swat, W.; Mayadas, T.; Brugge, J.S. Vav GEFs are required for beta2 integrin-dependent functions of neutrophils. J. Cell Biol. 2004, 166, 273–282.
Patel, J.C.; Hall, A.; Caron, E. Vav regulates activation of Rac but not Cdc42 during FcgammaR-mediated phagocytosis. Mol. Biol. Cell 2002, 13, 1215–1226.
Hall, A.B.; Gakidis, M.A.; Glogauer, M.; Wilsbacher, J.L.; Gao, S.; Swat, W.; Brugge, J.S. Requirements for Vav guanine nucleotide exchange factors and Rho GTPases in FcgammaR- and complement-mediated phagocytosis. Immunity 2006, 24, 305–316.
Leppla, S.H. Anthrax toxin edema factor: A bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc. Natl. Acad. Sci. USA 1982, 79, 3162–3166.
Confer, D.L.; Eaton, J.W. Phagocyte impotence caused by an invasive bacterial adenylate cyclase. Science 1982, 217, 948–950.
Ahuja, N.; Kumar, P.; Bhatnagar, R. The adenylate cyclase toxins. Crit. Rev. Microbiol. 2004, 30, 187–196.
Hewlett, E.; Wolff, J. Soluble adenylate cyclase from the culture medium of Bordetella pertussis: Purification and characterization. J. Bacteriol. 1976, 127, 890–898.
Aronoff, D.M.; Canetti, C.; Serezani, C.H.; Luo, M.; Peters-Golden, M. Cutting edge: Macrophage inhibition by cyclic AMP (cAMP): Differential roles of protein kinase A and exchange protein directly activated by cAMP-1. J. Immunol. 2005, 174, 595–599.
Yeager, L.A.; Chopra, A.K.; Peterson, J.W. Bacillus anthracis edema toxin suppresses human macrophage phagocytosis and cytoskeletal remodeling via the protein kinase A and exchange protein activated by cyclic AMP pathways. Infect. Immun. 2009, 77, 2530–2543.
Liu, S.; Miller-Randolph, S.; Crown, D.; Moayeri, M.; Sastalla, I.; Okugawa, S.; Leppla, S.H. Anthrax toxin targeting of myeloid cells through the CMG2 receptor is essential for establishment of Bacillus anthracis infections in mice. Cell Host Microbe 2010, 8, 455–462.
O’Brien, J.; Friedlander, A.; Dreier, T.; Ezzell, J.; Leppla, S. Effects of anthrax toxin components on human neutrophils. Infect. Immun. 1985, 47, 306–310.
Tournier, J.N.; Quesnel-Hellmann, A.; Mathieu, J.; Montecucco, C.; Tang, W.J.; Mock, M.; Vidal, D.R.; Goossens, P.L. Anthrax edema toxin cooperates with lethal toxin to impair cytokine secretion during infection of dendritic cells. J. Immunol. 2005, 174, 4934–4941.
Boyd, A.P.; Ross, P.J.; Conroy, H.; Mahon, N.; Lavelle, E.C.; Mills, K.H. Bordetella pertussis adenylate cyclase toxin modulates innate and adaptive immune responses: Distinct roles for acylation and enzymatic activity in immunomodulation and cell death. J. Immunol. 2005, 175, 730–738.
Sassone-Corsi, P. The cyclic AMP pathway. Cold Spring Harb. Perspect. Biol. 2012, 4.
Masin, J.; Osicka, R.; Bumba, L.; Sebo, P. Bordetella adenylate cyclase toxin: A unique combination of a pore-forming moiety with a cell-invading adenylate cyclase enzyme. Pathog. Dis. 2015, 73, ftv075.
Bumba, L.; Masin, J.; Fiser, R.; Sebo, P. Bordetella adenylate cyclase toxin mobilizes its beta2 integrin receptor into lipid rafts to accomplish translocation across target cell membrane in two steps. PLoS Pathog. 2010, 6, e1000901.
Rogel, A.; Hanski, E. 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. 1992, 267, 22599–22605.
Novak, J.; Cerny, O.; Osickova, A.; Linhartova, I.; Masin, J.; Bumba, L.; Sebo, P.; Osicka, R. Structure-Function Relationships Underlying the Capacity of Bordetella Adenylate Cyclase Toxin to Disarm Host Phagocytes. Toxins (Basel) 2017, 9, 300.
Fiser, R.; Masin, J.; Bumba, L.; Pospisilova, E.; Fayolle, C.; Basler, M.; Sadilkova, L.; Adkins, I.; Kamanova, J.; Cerny, J. et al. Calcium influx rescues adenylate cyclase-hemolysin from rapid cell membrane removal and enables phagocyte permeabilization by toxin pores. PLoS Pathog. 2012, 8, e1002580.
Friebe, S.; van der Goot, F.G.; Burgi, J. The Ins and Outs of Anthrax Toxin. Toxins (Basel) 2016, 8, 69.
Abrami, L.; Liu, S.; Cosson, P.; Leppla, S.H.; van der Goot, F.G. Anthrax toxin triggers endocytosis of its receptor via a lipid raft-mediated clathrin-dependent process. J. Cell Biol. 2003, 160, 321–328.
Dal Molin, F.; Tonello, F.; Ladant, D.; Zornetta, I.; Zamparo, I.; Di Benedetto, G.; Zaccolo, M.; Montecucco, C. Cell entry and cAMP imaging of anthrax edema toxin. EMBO J. 2006, 25, 5405–5413.
Cerny, O.; Kamanova, J.; Masin, J.; Bibova, I.; Skopova, K.; Sebo, P. Bordetella pertussis Adenylate Cyclase Toxin Blocks Induction of Bactericidal Nitric Oxide in Macrophages through cAMP-Dependent Activation of the SHP-1 Phosphatase. J. Immunol. 2015, 194, 4901–4913.
Kamanova, J.; Kofronova, O.; Masin, J.; Genth, H.; Vojtova, J.; Linhartova, I.; Benada, O.; Just, I.; Sebo, P. Adenylate cyclase toxin subverts phagocyte function by RhoA inhibition and unproductive ruffling. J. Immunol. 2008, 181, 5587–5597.
Osicka, R.; Osickova, A.; Hasan, S.; Bumba, L.; Cerny, J.; Sebo, P. Bordetella adenylate cyclase toxin is a unique ligand of the integrin complement receptor 3. Elife 2015, 4, e10766.
Deshpande, A.; Hammon, R.J.; Sanders, C.K.; Graves, S.W. Quantitative analysis of the effect of cell type and cellular differentiation on protective antigen binding to human target cells. FEBS Lett. 2006, 580, 4172–4175.
Fujikura, D.; Toyomane, K.; Kamiya, K.; Mutoh, M.; Mifune, E.; Ohnuma, M.; Higashi, H. ANTXR-1 and 2 independent modulation of a cytotoxicity mediated by anthrax toxin in human cells. J. Vet. Med. Sci. 2016, 78, 1311–1317.
Puhar, A.; Dal Molin, F.; Horvath, S.; Ladant, D.; Montecucco, C. Anthrax edema toxin modulates PKA-and CREB-dependent signaling in two phases. PLoS ONE 2008, 3, e3564.
Raymond, B.; Leduc, D.; Ravaux, L.; Le Goffic, R.; Candela, T.; Raymondjean, M.; Goossens, P.L.; Touqui, L. Edema toxin impairs anthracidal phospholipase A2 expression by alveolar macrophages. PLoS Pathog. 2007, 3, e187.
Trinidad, A.G.; de la Puerta, M.L.; Fernandez, N.; Bayon, Y.; Crespo, M.S.; Alonso, A. Coupling of C3bi to IgG inhibits the tyrosine phosphorylation signaling cascade downstream Syk and reduces cytokine induction in monocytes. J. Leukoc. Biol. 2006, 79, 1073–1082.
Chung, I.C.; OuYang, C.N.; Yuan, S.N.; Li, H.P.; Chen, J.T.; Shieh, H.R.; Chen, Y.J.; Ojcius, D.M.; Chu, C.L.; Yu, J.S. et al. Pyk2 activates the NLRP3 inflammasome by directly phosphorylating ASC and contributes to inflammasome-dependent peritonitis. Sci. Rep. 2016, 6, 36214.
Yan, S.R.; Novak, M.J. Beta2 integrin-dependent phosphorylation of protein-tyrosine kinase Pyk2 stimulated by tumor necrosis factor alpha and fMLP in human neutrophils adherent to fibrinogen. FEBS Lett. 1999, 451, 33–38.
Deckert, M.; Tartare-Deckert, S.; Couture, C.; Mustelin, T.; Altman, A. Functional and physical interactions of Syk family kinases with the Vav proto-oncogene product. Immunity 1996, 5, 591–604.
Shen, Y.; Zhukovskaya, N.L.; Zimmer, M.I.; Soelaiman, S.; Bergson, P.; Wang, C.R.; Gibbs, C.S.; Tang, W.J. Selective inhibition of anthrax edema factor by adefovir, a drug for chronic hepatitis B virus infection. Proc. Natl. Acad. Sci. USA 2004, 101, 3242–3247.
Kalamidas, S.A.; Kuehnel, M.P.; Peyron, P.; Rybin, V.; Rauch, S.; Kotoulas, O.B.; Houslay, M.; Hemmings, B.A.; Gutierrez, M.G.; Anes, E. et al. cAMP synthesis and degradation by phagosomes regulate actin assembly and fusion events: Consequences for mycobacteria. J. Cell Sci. 2006, 119, 3686–3694.
Pryzwansky, K.B.; Kidao, S.; Merricks, E.P. Compartmentalization of PDE-4 and cAMP-dependent protein kinase in neutrophils and macrophages during phagocytosis. Cell Biochem. Biophys. 1998, 28, 251–275.
Pryzwansky, K.B.; Steiner, A.L.; Spitznagel, J.K.; Kapoor, C.L. Compartmentalization of cyclic AMP during phagocytosis by human neutrophilic granulocytes. Science 1981, 211, 407–410.
Aronoff, D.M.; Canetti, C.; Peters-Golden, M. Prostaglandin E2 inhibits alveolar macrophage phagocytosis through an E-prostanoid 2 receptor-mediated increase in intracellular cyclic AMP. J. Immunol. 2004, 173, 559–565.
Arumugham, V.B.; Ulivieri, C.; Onnis, A.; Finetti, F.; Tonello, F.; Ladant, D.; Baldari, C.T. Compartmentalized Cyclic AMP Production by the Bordetella pertussis and Bacillus anthracis Adenylate Cyclase Toxins Differentially Affects the Immune Synapse in T Lymphocytes. Front. Immunol. 2018, 9, 919.
Zaccolo, M.; Di Benedetto, G.; Lissandron, V.; Mancuso, L.; Terrin, A.; Zamparo, I. Restricted diffusion of a freely diffusible second messenger: Mechanisms underlying compartmentalized cAMP signalling. Biochem. Soc. Trans. 2006, 34, 495–497.
Davare, M.A.; Avdonin, V.; Hall, D.D.; Peden, E.M.; Burette, A.; Weinberg, R.J.; Horne, M.C.; Hoshi, T.; Hell, J.W. A beta2 adrenergic receptor signaling complex assembled with the Ca2+ channel Cav1.2. Science 2001, 293, 98–101.
Cerny, O.; Anderson, K.E.; Stephens, L.R.; Hawkins, P.T.; Sebo, P. cAMP Signaling of Adenylate Cyclase Toxin Blocks the Oxidative Burst of Neutrophils through Epac-Mediated Inhibition of Phospholipase C Activity. J. Immunol. 2017, 198, 1285–1296.
Lomas, O.; Zaccolo, M. Phosphodiesterases maintain signaling fidelity via compartmentalization of cyclic nucleotides. Physiology (Bethesda) 2014, 29, 141–149.
Di Benedetto, G.; Zoccarato, A.; Lissandron, V.; Terrin, A.; Li, X.; Houslay, M.D.; Baillie, G.S.; Zaccolo, M. Protein kinase A type I and type II define distinct intracellular signaling compartments. Circ. Res. 2008, 103, 836–844.
Brock, T.G.; Serezani, C.H.; Carstens, J.K.; Peters-Golden, M.; Aronoff, D.M. Effects of prostaglandin E2 on the subcellular localization of Epac-1 and Rap1 proteins during Fcgamma-receptor-mediated phagocytosis in alveolar macrophages. Exp. Cell Res. 2008, 314, 255–263.
Baillie, G.S.; Scott, J.D.; Houslay, M.D. Compartmentalisation of phosphodiesterases and protein kinase A: Opposites attract. FEBS Lett. 2005, 579, 3264–3270.
Klezovich-Benard, M.; Corre, J.P.; Jusforgues-Saklani, H.; Fiole, D.; Burjek, N.; Tournier, J.N.; Goossens, P.L. Mechanisms of NK cell-macrophage Bacillus anthracis crosstalk: A balance between stimulation by spores and differential disruption by toxins. PLoS Pathog. 2012, 8, e1002481.
Le Cabec, V.; Carreno, S.; Moisand, A.; Bordier, C.; Maridonneau-Parini, I. Complement receptor 3 (CD11b/CD18) mediates type I and type II phagocytosis during nonopsonic and opsonic phagocytosis, respectively. J. Immunol. 2002, 169, 2003–2009.
Osicka, R.; Osickova, A.; Basar, T.; Guermonprez, P.; Rojas, M.; Leclerc, C.; Sebo, P. Delivery of CD8(+) T-cell epitopes into major histocompatibility complex class I antigen presentation pathway by Bordetella pertussis adenylate cyclase: Delineation of cell invasive structures and permissive insertion sites. Infect. Immun. 2000, 68, 247–256.
Karimova, G.; Pidoux, J.; Ullmann, A.; Ladant, D. A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Nat. Acad. Sci. USA 1998, 95, 5752–5756.
Santos, J.L.; Montes, M.J.; Gutierrez, F.; Ruiz, C. Evaluation of phagocytic capacity with a modified flow cytometry technique. Immunol. Lett. 1995, 45, 1–4.