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http://dx.doi.org/10.4014/jmb.1612.12043

The Poly-γ-ᴅ-Glutamic Acid Capsule of Bacillus licheniformis, a Surrogate of Bacillus anthracis Capsule Induces Interferon-Gamma Production in NK Cells through Interactions with Macrophages  

Lee, Hae-Ri (Division of High-Risk Pathogen Research, Center for Infectious Diseases, Korea National Institute of Health)
Jeon, Jun Ho (Division of High-Risk Pathogen Research, Center for Infectious Diseases, Korea National Institute of Health)
Rhie, Gi-Eun (Division of High-Risk Pathogen Research, Center for Infectious Diseases, Korea National Institute of Health)
Publication Information
Journal of Microbiology and Biotechnology / v.27, no.5, 2017 , pp. 1032-1037 More about this Journal
Abstract
The poly-${\gamma}$-$\small{D}$-glutamic acid (PGA) capsule, a major virulence factor of Bacillus anthracis, provides protection of the bacterium from phagocytosis and allows its unimpeded growth in the host. We investigated crosstalk between murine natural killer (NK) cells and macrophages stimulated with the PGA capsule of Bacillus licheniformis, a surrogate of the B. anthracis capsule. PGA induced interferon-gamma production from NK cells cultured with macrophages. This effect was dependent on macrophage-derived IL-12 and cell-cell contact interaction with macrophages through NK cell receptor NKG2D and its ligand RAE-1. The results showed that PGA could enhance NK cell activation by inducing IL-12 production in macrophages and a contact-dependent crosstalk with macrophages.
Keywords
Bacillus anthracis; poly-${\gamma}$-$\small{D}$-glutamic acid; interferon gamma; NK cells; macrophages;
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1 Coggeshall KM, Lupu F, Ballard J, Metcalf JP, James JA, Farris D, et al. 2013. The sepsis model: an emerging hypothesis for the lethality of inhalation anthrax. J. Cell. Mol. Med. 17: 914-920.   DOI
2 Adib-Conquy M, Cavaillon JM. 2007. Stress molecules in sepsis and systemic inflammatory response syndrome. FEBS Lett. 581: 3723-3733.   DOI
3 Gold JA, Hoshino Y, Jones MB, Hoshino S, Nolan A, Weiden MD. 2007. Exogenous interferon-${\alpha}$ and interferon-${\gamma}$ increase lethality of murine inhalational anthrax. PLoS One 8: e736.
4 Newman KC, Riley EM. 2007. Whatever turns you on: accessory-cell-dependent activation of NK cells by pathogens. Nat. Rev. Immunol. 7: 279-291.   DOI
5 Schoenborn JR, Wilson CB. 2007. Regulation of interferongamma during innate and adaptive immune responses. Adv. Immunol. 96: 41-101.
6 Roberts LM, Davies JS, Sempowski GD, Frelinger JA. 2014. IFN-gamma, but not IL-17A, is required for survival during secondary pulmonary Francisella tularensis Live Vaccine Stain infection. Vaccine 32: 3595-3603.   DOI
7 Walberg K, Baron S, Poast J, Schwartz B, Izotova L, Pestka S, et al. 2008. Interferon protects mice against inhalation anthrax. J. Interferon Cytokine Res. 28: 597-601.   DOI
8 Gold JA, Hoshino Y, Hoshino S, Jones MB, Nolan A, Weiden MD. 2004. Exogenous gamma and alpha/beta interferon rescues human macrophages from cell death induced by Bacillusanthracis. Infect. Immun. 72: 1291-1297.   DOI
9 Gonzales CM, Williams CB, Calderon VE, Huante MB, Moen S T, P opov V L, et al. 2012. Antibacterial role for natural killer cells in host defense to Bacillus anthracis. Infect. Immun. 80: 234-242.   DOI
10 Klezovich-Benard M, Corre JP, Jusforgues-Saklani H, Fiole D, Burjek N, Tournier JN, et al. 2012. Mechanisms of NK cellmacrophage Bacillus anthracis crosstalk: a balance between stimulation by spores and differential disruption by toxins. PLoS Pathog. 8: e1002481.   DOI
11 Lee HR, Jeon JH, Park OK, Chun JH, Park J, Rhie GE. 2015. The poly-gamma-d-glutamicacid capsule surrogate of the Bacillus anthracis capsule induces nitric oxide production via the platelet activating factor receptor signaling pathway. Mol. Immunol. 68: 244-252.   DOI
12 Siren J, Sareneva T, Pirhonen J, Strengell M, Veckman V, Julkunen I, et al. 2004. Cytokine and contact-dependent activation of natural killer cells by influenza A or Sendai virus-infected macrophages. J. Gen. Virol. 85: 2357-2364.   DOI
13 Makino S, Watarai M, Cheun HI, Shirahata T, Uchida I. 2002. Effect of the lower molecular capsule released from the cell surface of Bacillus anthracis on the pathogenesis of anthrax. 186: 227-233   DOI
14 Birrer GA, Cromwick AM, Gross RA. 1994. Gammapoly( glutamic acid) formation by Bacillus licheniformis 9945a: physiological and biological studies. Int. J. Biol. Macromol. 16: 265-275.   DOI
15 Jang J, Cho M, Chun JH, Cho MH, Park J, Oh HB, et al. 2011. The poly gamma D-glutamic acid capsule of Bacillus anthracis enhances lethal toxin activity. Infect. Immun. 79: 3846-3854.   DOI
16 Rhie GE, Roehrl MH, Mourez M, Collier RJ, Mekalanos JJ, Wang JY. 2003. A dually active anthrax vaccine that confers protection against both bacilli and toxins. Proc. Natl. Acad. Sci. USA 100: 10925-10930.   DOI
17 Kozel TR, Murphy WJ, Brandt S, Blazar BR, Lovchik JA, Thorkildson P, et al. 2004. mAbs to Bacillus anthracis capsular antigen for immunoprotection in anthrax and detection of antigenemia. Proc. Natl. Acad. Sci. USA 101: 5042-5047.   DOI
18 Gates-Hollingsworth MA, Perry MR, Chen H, Needham J, Houghton RL, Raychaudhuri S, et al. 2015. Immunoassay for capsular antigen of Bacillus anthracis enables rapid diagnosis in a rabbit model of inhalational anthrax. PLoS One 10: e0126304.   DOI
19 Diefenbach A, Jamieson AM, Liu SD, Shastri N, Raulet DH. 2000. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat. Immunol. 1: 119-126.   DOI
20 Jamieson AM, Diefenbach A, McMahon CW, Xiong N, Carlyle JR, Raulet DH. 2002. The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 17: 19-29.   DOI
21 Badgwell B, Parihar R, Magro C, Dierksheide J, Russo T, Carson WE. 2002. Natural killer cells contribute to the lethality of a murine model of Escherichia coli infection. Sugery 132: 205-212.
22 Souza-Fonseca-Guimaraes F, Adib-Conquy M, Cavaillon JM. 2012. Natural killer (NK) cells in antibacterial innate immunity: angels or devils?. Mol. Med. 18: 270-285.
23 Kerr AR, Kirkham LA, Kadioglu A, Andrew PW, Garside P, Thompson H, et al. 2005. Identification of a detrimental role for NK cells in pneumococcal pneumonia and sepsis in immunocompromised hosts. Microbes Infect. 7: 845-852.   DOI
24 Newton DW Jr, Runnels HA, Keanrns RJ. 1992. Enhanced splenic bacterial clearance and neutrophilia in anti-NK1.1- treated mice infected with Pseudomonas aeruginosa. Nat. Immun. 11: 335-344.
25 Smith H, Keppie J, Stanley JL. 1954. Observations on the cause of death in experimental anthrax. Lancet 267: 474-476.
26 Stearns-Kurosawa DJ, Lupu F, Taylor FB Jr, Kinasewitz G, Kurosawa S. 2006. Sepsis and pathophysiology of anthrax in a nonhuman primate model. Am. J. Pathol. 169: 433-444.   DOI
27 Lapaque N, Walzer T, Meresse S, Vivier E, Trowsdale J. 2009. Interactions between human NK cells and macrophages in response to Salmonella infection. J. Immunol. 182: 4339-4348.   DOI
28 Jeon JH, Lee HR, Cho MH, Park OK, Park J, Rhie GE. 2015. The poly-${\gamma}$-D-glutamic acid capsule surrogate of the Bacillus anthracis capsule is a novel Toll-like receptor 2 agonist. Infect. Immun. 83: 3847-3856.   DOI
29 Bozzano F, Picciotto A, Costa P, Marras F, Fazio V, Hirsch I, et al. 2011. Activating NK cell receptor expression/function (NKp30, NKp46, DNAM-1) during chronic viraemic HCV infection is associated with the outcome of combined treatment. Eur. J. Immunol. 41: 2905-2914.   DOI
30 Haller D, Serrant P, Granato D, Schiffrin EJ, Blum S. 2002. Activation of human NK cells by staphylococci and lactobacilli requires cell contact-dependent costimulation by autologous monocytes. Clin. Diagn. Lab. Immunol. 9: 649-657.
31 Newman KC, Riley EM. 2007. Whatever turns you on: accessory-cell-dependent activation of NK cells by pathogens. Nat. Rev. Immunol. 7: 279-291.   DOI
32 Inglesby TV, O'Toole T, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, et al. 2002. Anthrax as a biological weapon, 2002: updated recommendations for management. JAMA 287: 2236-2252.   DOI
33 Morse SA. 2014. Pathogen security-help or hindrance? Front. Bioeng. Biotechnol. 2: 83-94.
34 Guichard A, Nizet V, Bier E. 2012. New insights into the biological effects of anthrax toxins:linking cellular to organismal responses. Microbes Infect. 14: 97-118.   DOI
35 Leppla SH, Robbins JB, Schneerson R, Shiloach J. 2002. Development of an improved vaccine for anthrax. J. Clin. Invest. 110: 141-144.   DOI
36 Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. 2008. Functions of natural killer cells. Nat. Immunol. 9: 503-510.   DOI