PcpA promotes higher levels of infection and modulates recruitment of myeloid-derived suppressor cells during pneumococcal pneumonia

Journal of Immunology

Volumn 196, Issue 5, 2016, Pages 2239-2248

  Walker, Melissa M ^a   Novak, Lea ^b   Widener, Rebecca ^c   Grubbs, James Aaron ^d   King, Janice ^a   Hale, Joanetha Y ^a   Ochs, Martina M ^e   Myers, Lisa E ^e   Briles, David E ^a,f,g   Deshanex, Jessy ^d  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d University of Alabama at Birmingham   (United States)

^e SANOFI PASTEUR   (France)

^f UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^g University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; INTERLEUKIN 6; PROTEIN PCPA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; AUTACOID; BACTERIAL PROTEIN; CARRIER PROTEIN; CYTOKINE; PCPA PROTEIN, STREPTOCOCCUS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTEREMIA; BACTERIAL LOAD; BACTERIAL PNEUMONIA; BLOOD; CELL INFILTRATION; CELL RECRUITMENT; CELLULAR PARAMETERS; CONTROLLED STUDY; FEMALE; FOCAL PNEUMONIA; HISTOLOGY; IN VIVO STUDY; INFECTION CONTROL; INFLAMMATION; INNATE IMMUNITY; LIVER; LUNG; LUNG LAVAGE; MALE; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PATHOGEN CLEARANCE; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; REGULATORY T LYMPHOCYTE; SEPSIS; SPLEEN; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE; SUPPRESSOR CELL; ANIMAL; BIOSYNTHESIS; BONE MARROW CELL; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; IMMUNOMODULATION; MACROPHAGE; METABOLISM; MICROBIOLOGY; MORTALITY; MUTATION; PATHOLOGY; TIME FACTOR; TRANSGENIC MOUSE;

ANIMALS; BACTEREMIA; BACTERIAL LOAD; BACTERIAL PROTEINS; CARRIER PROTEINS; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; IMMUNOMODULATION; INFLAMMATION MEDIATORS; MACROPHAGES; MICE; MICE, TRANSGENIC; MUTATION; MYELOID CELLS; PNEUMONIA, PNEUMOCOCCAL; STREPTOCOCCUS PNEUMONIAE; TIME FACTORS; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84962033230     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402518     Document Type: Article

References (35)

1. O'Brien, K. L., L. J. Wolfson, J. P. Watt, E. Henkle, M. Deloria-Knoll, N. McCall, E. Lee, K. Mulholland, O. S. Levine, and T. Cherian, Hib and Pneumococcal Global Burden of Disease Study Team. 2009. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374: 893-902.
2. Bogaert, D., A. van Belkum, M. Sluijter, A. Luijendijk, R. de Groot, H. C. Rümke, H. A. Verbrugh, and P. W. Hermans. 2004. Colonisation by Streptococcus pneumoniae and Staphylococcus aureus in healthy children. Lancet 363: 1871-1872.
3. Mitchell, T. J. 2003. The pathogenesis of streptococcal infections: from tooth decay to meningitis. Nat. Rev. Microbiol. 1: 219-230.
4. Weiser, J. N. 2010. The pneumococcus: why a commensal misbehaves. J. Mol. Med. 88: 97-102.
5. Bergmann, S., and S. Hammerschmidt. 2006. Versatility of pneumococcal surface proteins. Microbiology 152: 295-303.
6. Sánchez-Beato, A. R., R. López, and J. L. García. 1998. Molecular characterization of PcpA: a novel choline-binding protein of Streptococcus pneumoniae. FEMS Microbiol. Lett. 164: 207-214.
7. Hava, D. L., and A. Camilli. 2002. Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol. Microbiol. 45: 1389-1406.
8. Johnston, J. W., D. E. Briles, L. E. Myers, and S. K. Hollingshead. 2006. Mn2+- dependent regulation of multiple genes in Streptococcus pneumoniae through PsaR and the resultant impact on virulence. Infect. Immun. 74: 1171-1180.
9. Glover, D. T., S. K. Hollingshead, and D. E. Briles. 2008. Streptococcus pneumoniae surface protein PcpA elicits protection against lung infection and fatal sepsis. Infect. Immun. 76: 2767-2776.
10. Brooks, W. A., L. J. Chang, X. Sheng, R. Hopfer, and P. P. R. S. Team, PPR02 Study Team. 2015. Safety and immunogenicity of a trivalent recombinant PcpA, PhtD, and PlyD1 pneumococcal protein vaccine in adults, toddlers, and infants: a phase I randomized controlled study. Vaccine 33: 4610-4617.
11. Khan, M. N., S. K. Sharma, L. M. Filkins, and M. E. Pichichero. 2012. PcpA of Streptococcus pneumoniae mediates adherence to nasopharyngeal and lung epithelial cells and elicits functional antibodies in humans. Microbes Infect. 14: 1102-1110.
12. Gillespie, S. H., and I. Balakrishnan. 2000. Pathogenesis of pneumococcal infection. J. Med. Microbiol. 49: 1057-1067.
13. Gillespie, S. H., P. H. McWhinney, and C. C. Kibbler. 1991. Pneumococcal bacteraemia. Lancet 337: 376.
14. Bergeron, Y., N. Ouellet, A. M. Deslauriers, M. Simard, M. Olivier, and M. G. Bergeron. 1998. Cytokine kinetics and other host factors in response to pneumococcal pulmonary infection in mice. Infect. Immun. 66: 912-922.
15. Cauwels, A., E. Wan, M. Leismann, and E. Tuomanen. 1997. Coexistence of CD14-dependent and independent pathways for stimulation of human monocytes by gram-positive bacteria. Infect. Immun. 65: 3255-3260.
16. Braun, J. S., R. Novak, G. Gao, P. J. Murray, and J. L. Shenep. 1999. Pneumolysin, a protein toxin of Streptococcus pneumoniae, induces nitric oxide production from macrophages. Infect. Immun. 67: 3750-3756.
17. Steinwede, K., S. Henken, J. Bohling, R. Maus, B. Ueberberg, C. Brumshagen, E. L. Brincks, T. S. Griffith, T. Welte, and U. A. Maus. 2012. TNF-related apoptosis-inducing ligand (TRAIL) exerts therapeutic efficacy for the treatment of pneumococcal pneumonia in mice. J. Exp. Med. 209: 1937-1952.
18. Paton, J. C. 1996. The contribution of pneumolysin to the pathogenicity of Streptococcus pneumoniae. Trends Microbiol. 4: 103-106.
19. Rubins, J. B., D. Charboneau, C. Fasching, A. M. Berry, J. C. Paton, J. E. Alexander, P. W. Andrew, T. J. Mitchell, and E. N. Janoff. 1996. Distinct roles for pneumolysin's cytotoxic and complement activities in the pathogenesis of pneumococcal pneumonia. Am. J. Respir. Crit. Care Med. 153: 1339-1346.
20. Dockrell, D. H., H. M. Marriott, L. R. Prince, V. C. Ridger, P. G. Ince, P. G. Hellewell, and M. K. Whyte. 2003. Alveolar macrophage apoptosis contributes to pneumococcal clearance in a resolving model of pulmonary infection. J. Immunol. 171: 5380-5388.
21. Knapp, S., J. C. Leemans, S. Florquin, J. Branger, N. A. Maris, J. Pater, N. van Rooijen, and T. van der Poll. 2003. Alveolar macrophages have a protective antiinflammatory role during murine pneumococcal pneumonia. Am. J. Respir. Crit. Care Med. 167: 171-179.
22. Maus, U. A., M. Srivastava, J. C. Paton, M. Mack, M. B. Everhart, T. S. Blackwell, J. W. Christman, D. Schlöndorff, W. Seeger, and J. Lohmeyer. 2004. Pneumolysin-induced lung injury is independent of leukocyte trafficking into the alveolar space. J. Immunol. 173: 1307-1312.
23. Winter, C., K. Taut, M. Srivastava, F. Länger, M. Mack, D. E. Briles, J. C. Paton, R. Maus, T. Welte, M. D. Gunn, and U. A. Maus. 2007. Lung-specific overexpression of CC chemokine ligand (CCL) 2 enhances the host defense to Streptococcus pneumoniae infection in mice: role of the CCL2-CCR2 axis. J. Immunol. 178: 5828-5838.
24. Taut, K., C. Winter, D. E. Briles, J. C. Paton, J. W. Christman, R. Maus, R. Baumann, T. Welte, and U. A. Maus. 2008. Macrophage turnover kinetics in the lungs of mice infected with Streptococcus pneumoniae. Am. J. Respir. Cell Mol. Biol. 38: 105-113.
25. Hahn, I., A. Klaus, A. K. Janze, K. Steinwede, N. Ding, J. Bohling, C. Brumshagen, H. Serrano, F. Gauthier, J. C. Paton, et al. 2011. Cathepsin G and neutrophil elastase play critical and nonredundant roles in lung-protective immunity against Streptococcus pneumoniae in mice. Infect. Immun. 79: 4893-4901.
26. Poe, S. L., M. Arora, T. B. Oriss, M. Yarlagadda, K. Isse, A. Khare, D. E. Levy, J. S. Lee, R. K. Mallampalli, Y. R. Chan, et al. 2013. STAT1-regulated lung MDSC-like cells produce IL-10 and efferocytose apoptotic neutrophils with relevance in resolution of bacterial pneumonia. Mucosal Immunol. 6: 189-199.
27. Deshane, J., J. W. Zmijewski, R. Luther, A. Gaggar, R. Deshane, J. F. Lai, X. Xu, M. Spell, K. Estell, C. T. Weaver, et al. 2011. Free radical-producing myeloidderived regulatory cells: potent activators and suppressors of lung inflammation and airway hyperresponsiveness. Mucosal Immunol. 4: 503-518.
28. Daniels, C. C., T. C. Briles, S. Mirza, A. P. Håkansson, and D. E. Briles. 2006. Capsule does not block antibody binding to PspA, a surface virulence protein of Streptococcus pneumoniae. Microb. Pathog. 40: 228-233.
29. Briles, D. E., S. K. Hollingshead, J. C. Paton, E. W. Ades, L. Novak, F. W. van Ginkel, and W. H. Benjamin, Jr. 2003. Immunizations with pneumococcal surface protein A and pneumolysin are protective against pneumonia in a murine model of pulmonary infection with Streptococcus pneumoniae. J. Infect. Dis. 188: 339-348.
30. Werner, J. L., M. A. Gessner, L. M. Lilly, M. P. Nelson, A. E. Metz, D. Horn, C. W. Dunaway, J. Deshane, D. D. Chaplin, C. T. Weaver, et al. 2011. Neutrophils produce interleukin 17A (IL-17A) in a dectin-1- and IL-23-dependent manner during invasive fungal infection. Infect. Immun. 79: 3966-3977.
31. Mundy-Bosse, B. L., G. B. Lesinski, A. C. Jaime-Ramirez, K. Benninger, M. Khan, P. Kuppusamy, K. Guenterberg, S. V. Kondadasula, A. R. Chaudhury, K. M. La Perle, et al. 2011. Myeloid-derived suppressor cell inhibition of the IFN response in tumor-bearing mice. Cancer Res. 71: 5101-5110.
32. Chicharro, J. L., V. Serrano, R. Ureña, A. M. Gutierrez, A. Carvajal, P. Fernández-Hernando, and A. Lucía. 1999. Trace elements and electrolytes in human resting mixed saliva after exercise. Br. J. Sports Med. 33: 204-207.
33. Briles, D. E., M. J. Crain, B. M. Gray, C. Forman, and J. Yother. 1992. Strong association between capsular type and virulence for mice among human isolates of Streptococcus pneumoniae. Infect. Immun. 60: 111-116.
34. Pruijt, J. F., P. Verzaal, R. van Os, E. J. de Kruijf, M. L. van Schie, A. Mantovani, A. Vecchi, I. J. Lindley, R. Willemze, S. Starckx, et al. 2002. Neutrophils are indispensable for hematopoietic stem cell mobilization induced by interleukin-8 in mice. Proc. Natl. Acad. Sci. USA 99: 6228-6233.
35. Gillespie, S. H. 1989. Aspects of pneumococcal infection including bacterial virulence, host response and vaccination. J. Med. Microbiol. 28: 237-248.