Bacterial exploitation of phosphorylcholine mimicry suppresses inflammation to promote airway infection

Journal of Clinical Investigation

Volumn 125, Issue 10, 2015, Pages 3878-3890

  Hergott, Christopher B ^a   Roche, Aoife M ^a   Naidu, Nikhil A ^a   Mesaros, Clementina ^a   Blair, Ian A ^a   Weiser, Jeffrey N ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIHYDRO 2,4,6 TRIMETHYL 3,5 PYRIDINEDICARBOXYLIC ACID METHYL 2 PHENYLTHIOETHYL ESTER; BACTERIAL ENZYME; CHOP REMODELING ENZYME; FORMYLMETHIONYLLEUCYLPHENYLALANINE; GLPQ ENZYME; PHOSPHODIESTERASE; PHOSPHOLIPID; PHOSPHORYLCHOLINE; THROMBOCYTE ACTIVATING FACTOR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CARRIER PROTEIN; CELL SURFACE RECEPTOR; CHOLINE-BINDING PROTEIN E, STREPTOCOCCUS PNEUMONIAE; FIBRINOGEN RECEPTOR; G PROTEIN COUPLED RECEPTOR; GLPQ PROTEIN, HAEMOPHILUS INFLUENZAE; IMMUNOGLOBULIN D; LIPOPROTEIN; THROMBOCYTE ACTIVATING FACTOR RECEPTOR;

AIRWAY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CELL WALL; BACTERIAL CLEARANCE; BACTERIAL STRAIN; BACTERIUM; CONTROLLED STUDY; HAEMOPHILUS INFLUENZAE; HUMAN; HYDROLYSIS; IMMUNE EVASION; INFLAMMATION; LEUKOCYTE ACTIVATION; MASS SPECTROMETRY; MEDIATOR; MOLECULAR MIMICRY; MOUSE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; STREPTOCOCCUS PNEUMONIAE; UPPER RESPIRATORY TRACT INFECTION; ANIMAL; C57BL MOUSE; CELL WALL; CHEMICALLY INDUCED; CHEMISTRY; DEFICIENCY; DRUG EFFECTS; ENZYMOLOGY; GENETICS; HAEMOPHILUS INFECTION; HETEROZYGOTE; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; NEUTROPENIA; NOSE CAVITY; PHYSIOLOGY; PNEUMOCOCCAL INFECTION; SPECIES DIFFERENCE;

ANIMALS; BACTERIAL PROTEINS; CARRIER PROTEINS; CARRIER STATE; CELL WALL; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; IMMUNOGLOBULIN D; LIPOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR MIMICRY; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; NASAL CAVITY; NEUTROPENIA; NEUTROPHIL ACTIVATION; NEUTROPHILS; PHAGOCYTOSIS; PHOSPHORYLCHOLINE; PLATELET ACTIVATING FACTOR; PLATELET MEMBRANE GLYCOPROTEINS; PNEUMOCOCCAL INFECTIONS; PROTEOLYSIS; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; SPECIES SPECIFICITY; STREPTOCOCCUS PNEUMONIAE;

EID: 84943260174     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI81888     Document Type: Article

References (91)

1. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13(3):159-175.
2. Amulic B, Cazalet C, Hayes GL, Metzler KD, Zychlinsky A. Neutrophil function: from mechanisms to disease. Annu Rev Immunol. 2011;30:459-489.
3. Segal AW. How neutrophils kill microbes. Annu Rev Immunol. 2004;23:197-223.
4. Mantovani A, Cassatella MA, Costantini C, Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol. 2011;11(8):519-531.
5. Short KR, Reading PC, Wang N, Diavatopoulos DA, Wijburg OL. Increased nasopharyngeal bacterial titers and local inflammation facilitate transmission of Streptococcus pneumoniae. mBio. 2011;3(5):e00255-12.
6. Urban CF, Lourido S, Zychlinsky A. How do microbes evade neutrophil killing? Cell Microbiol. 2006;8(11):1687-1696.
7. Sarantis H, Grinstein S. Subversion of phagocytosis for pathogen survival. Cell Host Microbe. 2012;12(4):419-431.
8. Sadik CD, Kim ND, Luster AD. Neutrophils cascading their way to inflammation. Trends Immunol. 2011;32(10):452-460.
9. Maekawa T, et al. Porphyromonas gingivalis manipulates complement and TLR signaling to uncouple bacterial clearance from inflammation and promote dysbiosis. Cell Host Microbe. 2014;15(6):768-778.
10. Spaan AN, Surewaard BG, Nijland R, van Strijp JA. Neutrophils versus Staphylococcus aureus: a biological tug of war. Annu Rev Microbiol. 2012;67: 629-650.
11. Wood WB, Smith MR, Watson B. Studies on the mechanism of recovery in pneumococcal pneumonia: IV. The mechanism of phagocytosis in the absence of antibody. J Exp Med. 1946;84(4):387-402.
12. Wood WB, Smith MR. Host-parasite relationships in experimental pneumonia due to pneumococcus type III. J Exp Med. 1950;92(1):85-100.
13. Knecht JC, Schiffman G, Austrian R. Some biological properties of Pneumococcus type 37 and the chemistry of its capsular polysaccharide. J Exp Med. 1970;132(3):475-487.
14. O'Brien KL, et al. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet. 2009;374(9693):893-902.
15. Griffin MR, Zhu Y, Moore MR, Whitney CG, Grijalva CG. U.S. hospitalizations for pneumonia after a decade of pneumococcal vaccination. N Engl J Med. 2013;369(2):155-163.
16. Simell B, et al. The fundamental link between pneumococcal carriage and disease. Expert Rev Vaccines. 2012;11(7):841-855.
17. Gray BM, Converse GM, Dillon HC. Epidemiologic studies of Streptococcus pneumoniae in infants: acquisition, carriage, and infection during the first 24 months of life. J Infect Dis. 1980;142(6):923-933.
18. Gwaltney JM, Sande MA, Austrian R, Hendley JO. Spread of Streptococcus pneumoniae in families. II. Relation of transfer of S. pneumoniae to incidence of colds and serum antibody. J Infect Dis. 1975;132(1):62-68.
19. McCool TL, Cate TR, Moy G, Weiser JN. The immune response to pneumococcal proteins during experimental human carriage. J Exp Med. 2002;195(3):359-365.
20. Zhang Z, Clarke TB, Weiser JN. Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J Clin Invest. 2009;119(7):1899-1909.
21. Melin M, Jarva H, Siira L, Meri S, Käyhty H, Väkeväinen M. Streptococcus pneumoniae capsular serotype 19F is more resistant to C3 deposition and less sensitive to opsonophagocytosis than serotype 6B. Infect Immun. 2009;77(2):676-684.
22. Gordon DL, Johnson GM, Hostetter MK. Ligand-receptor interactions in the phagocytosis of virulent Streptococcus pneumoniae by polymorphonuclear leukocytes. J Infect Dis. 1986;154(4):619-626.
23. Kadioglu A, Andrew PW. The innate immune response to pneumococcal lung infection: the untold story. Trends Immunol. 2004;25(3):143-149.
24. McCool TL, Weiser JN. Limited role of antibody in clearance of Streptococcus pneumoniae in a murine model of colonization. Infect Immun. 2004;72(10):5807-5813.
25. van Rossum AM, Lysenko ES, Weiser JN. Host and bacterial factors contributing to the clearance of colonization by Streptococcus pneumoniae in a murine model. Infect Immun. 2005;73(11):7718-7726.
26. Kim JO, Weiser JN. Association of intrastrain phase variation in quantity of capsular polysaccharide and teichoic acid with the virulence of Streptococcus pneumoniae. J Infect Dis. 1998;177(2):368-377.
27. Stebbins CE, Galán JE. Structural mimicry in bacterial virulence. Nature. 2001;412(6848):701-705.
28. Clark SE, Weiser JN. Microbial modulation of host immunity with the small molecule phosphorylcholine. Infect Immun. 2013;81(2):392-401.
29. Fischer W. Phosphocholine of pneumococcal teichoic acids: role in bacterial physiology and pneumococcal infection. Res Microbiol. 1999;151(6):421-427.
30. Cundell DR, Gerard NP, Gerard C, Idanpaan-Heikkila I, Tuomanen EI. Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature. 1995;377(6548):435-438.
31. Shirasaki H, et al. Expression and localization of platelet-activating factor receptor in human nasal mucosa. Ann Allergy Asthma Immunol. 2005;95(2):190-196.
32. Wu H, et al. Lipoxin A4 and platelet activating factor are involved in E. coli or LPS-induced lung inflammation in CFTR-deficient mice. PLoS One. 2013;9(3):e93003.
33. Hanahan DJ, Demopoulos CA, Liehr J, Pinckard RN. Identification of platelet activating factor isolated from rabbit basophils as acetyl glyceryl ether phosphorylcholine. J Biol Chem. 1980;255(12):5514-5516.
34. Clark PO, Hanahan DJ, Pinckard RN. Physical and chemical properties of platelet-activating factor obtained from human neutrophils and monocytes and rabbit neutrophils and basophils. Biochim Biophys Acta. 1980;628(1):69-75.
35. Shaw JO, Pinckard RN, Ferrigni KS, McManus LM, Hanahan DJ. Activation of human neutrophils with 1-O-hexadecyl/octadecyl-2-acetylsn-glycerol-3-phosphorylcholine (platelet activating factor). J Immunol. 1981;127(3):1250-1255.
36. Kitchen E, Rossi AG, Condliffe AM, Haslett C, Chilvers ER. Demonstration of reversible priming of human neutrophils using platelet-activating factor. Blood. 1996;88(11):4330-4337.
37. Brown SL, Jala VR, Raghuwanshi SK, Nasser MW, Haribabu B, Richardson RM. Activation and regulation of platelet-activating factor receptor: role of G(i) and G(q) in receptor-mediated chemotactic, cytotoxic, and cross-regulatory signals. J Immunol. 2006;177(5):3242-3249.
38. Eckels PC, et al. Amantadine inhibits platelet-activating factor induced clathrin-mediated endocytosis in human neutrophils. Am J Physiol Cell Physiol. 2009;297(4):C886-C897.
39. Shalit M, Von Allmen C, Atkins PC, Zweiman B. Platelet activating factor increases expression of complement receptors on human neutrophils. J Leukoc Biol. 1988;44(3):212-217.
40. McLaughlin NJ, et al. Platelet-activating factormediated endosome formation causes membrane translocation of p67phox and p40phox that requires recruitment and activation of p38 MAPK, Rab5a, and phosphatidylinositol 3-kinase in human neutrophils. J Immunol. 2008;180(12):8192-8203.
41. Dalia AB, Weiser JN. Minimization of bacterial size allows for complement evasion and is overcome by the agglutinating effect of antibody. Cell Host Microbe. 2011;10(5):486-496.
42. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol. 2007;83(1):64-70.
43. Matthias KA, Roche AM, Standish AJ, Shchepetov M, Weiser JN. Neutrophil-toxin interactions promote antigen delivery and mucosal clearance of Streptococcus pneumoniae. J Immunol. 2008;180(9):6246-6254.
44. Kinhult J, Egesten A, Benson M, Uddman R, Cardell LO. Increased expression of surface activation markers on neutrophils following migration into the nasal lumen. Clin Exp Allergy. 2003;33(8):1141-1146.
45. Kishimoto TK, Jutila MA, Berg EL, Butcher EC. Neutrophil Mac-1 and MEL-14 adhesion proteins inversely regulated by chemotactic factors. Science. 1989;245(4923):1238-1241.
46. Tedder TF. Cell-surface receptor shedding: a means of regulating function. Am J Respir Cell Mol Biol. 1991;5(4):305-306.
47. Albrich WC, et al. Pneumococcal colonisation density: a new marker for disease severity in HIV-infected adults with pneumonia. BMJ Open. 2013;4(8):e005953.
48. Richard AL, Siegel SJ, Erikson J, Weiser JN. TLR2 signaling decreases transmission of Streptococcus pneumoniae by limiting bacterial shedding in an infant mouse Influenza A co-infection model. PLoS Pathog. 2014;10(8):e1004339.
49. Hermoso JA, et al. Insights into pneumococcal pathogenesis from the crystal structure of the modular teichoic acid phosphorylcholine esterase Pce. Nat Struct Mol Biol. 2005;12(6):533-538.
50. Zinchuk O, Fukushima A, Zinchuk V, Fukata K, Ueno H. Direct action of platelet activating factor (PAF) induces eosinophil accumulation and enhances expression of PAF receptors in conjunctivitis. Mol Vis. 2005;11:114-123.
51. Mori M, Aihara M, Kume K, Hamanoue M, Kohsaka S, Shimizu T. Predominant expression of platelet-activating factor receptor in the rat brain microglia. J Neurosci. 1996;16(11):3590-3600.
52. Fernández-Gallardo S, Ortega MP, Priego JG, de Casa-Juana MF, Sunkel C, Sánchez Crespo M. Pharmacological actions of PCA 4248, a new platelet-activating factor receptor antagonist: in vivo studies. J Pharmacol Exp Ther. 1990;255(1):34-39.
53. Matsumura Y, Byrne SN, Nghiem DX, Miyahara Y, Ullrich SE. A role for inflammatory mediators in the induction of immunoregulatory B cells. J Immunol. 2006;177(7):4810-4817.
54. Garcia CC, et al. Platelet-activating factor receptor plays a role in lung injury and death caused by Influenza A in mice. PLoS Pathog. 2009;6(11):e1001171.
55. Dalia AB, Standish AJ, Weiser JN. Three surface exoglycosidases from Streptococcus pneumoniae, NanA, BgaA, and StrH, promote resistance to opsonophagocytic killing by human neutrophils. Infect Immun. 2010;78(5):2108-2116.
56. Vollmer W, Tomasz A. Identification of the teichoic acid phosphorylcholine esterase in Streptococcus pneumoniae. Mol Microbiol. 2001;39(6):1610-1622.
57. Futosi K, Fodor S, Mócsai A. Reprint of Neutrophil cell surface receptors and their intracellular signal transduction pathways. Int Immunopharmacol. 2013;17(4):1185-1197.
58. Krause KH, Schlegel W, Wollheim CB, Andersson T, Waldvogel FA, Lew PD. Chemotactic peptide activation of human neutrophils and HL-60 cells. Pertussis toxin reveals correlation between inositol trisphosphate generation, calcium ion transients, and cellular activation. J Clin Invest. 1985;76(4):1348-1354.
59. Santibanez TA, Shefer A, Briere EC, Cohn AC, Groom AV. Effects of a nationwide Hib vaccine shortage on vaccination coverage in the United States. Vaccine. 2012;30(5):941-947.
60. Timothy FM, Aimee LB, Andrew TS, Sanjay S. Persistent colonization by Haemophilus influenzae in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2004;170(3):266-272.
61. Zola TA, Lysenko ES, Weiser JN. Mucosal clearance of capsule-expressing bacteria requires both TLR and nucleotide-binding oligomerization domain 1 signaling. J Immunol. 2008;181(11):7909-7916.
62. Fan X, Goldfine H, Lysenko E, Weiser JN. The transfer of choline from the host to the bacterial cell surface requires glpQ in Haemophilus influenzae. Mol Microbiol. 2001;41(5):1029-1036.
63. Janson H, Melhus A, Hermansson A, Forsgren A. Protein D, the glycerophosphodiester phosphodiesterase from Haemophilus influenzae with affinity for human immunoglobulin D, influences virulence in a rat otitis model. Infect Immun. 1994;62(11):4848-4854.
64. Weiser JN. The pneumococcus: why a commensal misbehaves. J Mol Med (Berl). 2010;88(2):97-102.
65. Desa MN, Sekaran SD, Vadivelu J, Parasakthi N. Distribution of CBP genes in Streptococcus pneumoniae isolates in relation to vaccine types, penicillin susceptibility and clinical site. Epidemiol Infect. 2008;136(7):940-942.
66. Gosink KK, Mann ER, Guglielmo C, Tuomanen EI, Masure HR. Role of novel choline binding proteins in virulence of Streptococcus pneumoniae. Infect Immun. 2000;68(10):5690-5695.
67. Höltje JV, Tomasz A. Teichoic acid phosphorylcholine esterase. A novel enzyme activity in pneumococcus. J Biol Chem. 1974;249(21):7032-7034.
68. Paulson SK, Wolf JL, Novotney-Barry A, Cox CP. Pharmacologic characterization of the rabbit neutrophil receptor for platelet-activating factor. Proc Soc Exp Biol Med. 1990;195(2):247-254.
69. Stenton SC, et al. Platelet-activating factor in bronchoalveolar lavage fluid from asthmatic subjects. Eur Respir J. 1990;3(4):408-413.
70. Yan JJ, et al. Therapeutic effects of lysophosphatidylcholine in experimental sepsis. Nat Med. 2004;10(2):161-167.
71. Prescott SM, Zimmerman GA, McIntyre TM. Platelet-activating factor. J Biol Chem. 1990;265(29):17381-17384.
72. Siegel SJ, Roche AM, Weiser JN. Influenza promotes pneumococcal growth during coinfection by providing host sialylated substrates as a nutrient source. Cell Host Microbe. 2014;16(1):55-67.
73. Weiser JN, Shchepetov M, Chong ST. Decoration of lipopolysaccharide with phosphorylcholine: a phase-variable characteristic of Haemophilus influenzae. Infect Immun. 1997;65(3):943-950.
74. Weiser JN, Goldberg JB, Pan N, Wilson L, Virji M. The phosphorylcholine epitope undergoes phase variation on a 43-kilodalton protein in Pseudomonas aeruginosa and on pili of Neisseria meningitidis and Neisseria gonorrhoeae. Infect Immun. 1998;66(9):4263-4267.
75. Barbier M, et al. Lysine trimethylation of EF-Tu mimics platelet-activating factor to initiate Pseudomonas aeruginosa pneumonia. mBio. 2012;4(3):13.
76. Waller AK, Sage T, Kumar C, Carr T, Gibbins JM, Clarke SR. Staphylococcus aureus lipoteichoic acid inhibits platelet activation and thrombus formation via the Paf receptor. J Infect Dis. 2013;208(12):2046-2057.
77. Hosoki K, et al. Staphylococcus aureus directly activates eosinophils via platelet-activating factor receptor. J Leukoc Biol. 2012;92(2):333-341.
78. Liu M, et al. Group A Streptococcus secreted esterase hydrolyzes platelet-activating factor to impede neutrophil recruitment and facilitate innate immune evasion. PLoS Pathog. 2011;8(4):e1002624.
79. McIntyre TM, Prescott SM, Stafforini DM. The emerging roles of PAF acetylhydrolase. J Lipid Res. 2009;50(suppl):S255-S259.
80. Touqui L, et al. Excretion of platelet activating factor-acetylhydrolase and phospholipase A2 into nasal fluids after allergenic challenge: possible role in the regulation of platelet activating factor release. J Allergy Clin Immunol. 1994;94(1):109-119.
81. Seki M, et al. Expression and DNA microarray analysis of a platelet activating factor-related molecule in severe pneumonia in mice due to influenza virus and bacterial co-infection. Jpn J Infect Dis. 2008;62(1):6-10.
82. Investigators S, et al. Darapladib for preventing ischemic events in stable coronary heart disease. N Engl J Med. 2014;370(18):1702-1711.
83. Tettelin H, et al. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science. 2001;293(5529):498-506.
84. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat Med. 2010;16(2):228-231.
85. Brown AO, et al. Streptococcus pneumoniae translocates into the myocardium and forms unique microlesions that disrupt cardiac function. PLoS Pathog. 2014;10(9):e1004383.
86. Radin JN, Orihuela CJ, Murti G, Guglielmo C, Murray PJ, Tuomanen EI. beta-Arrestin 1 participates in platelet-activating factor receptor-mediated endocytosis of Streptococcus pneumoniae. Infect Immun. 2005;73(12):7827-7835.
87. Lee W-BB, et al. Neutrophils Promote mycobacterial trehalose dimycolate-induced lung inflammation via the mincle pathway. PLoS Pathog. 2011;8(4):e1002614.
88. McGovern NN, et al. Hypoxia selectively inhibits respiratory burst activity and killing of Staphylococcus aureus in human neutrophils. J Immunol. 2010;186(1):453-463.
89. Diavatopoulos DA, et al. Influenza A virus facilitates Streptococcus pneumoniae transmission and disease. FASEB J. 2010;24(6):1789-1798.
90. Beisswenger C, Lysenko ES, Weiser JN. Early bacterial colonization induces toll-like receptordependent transforming growth factor beta signaling in the epithelium. Infect Immun. 2009;77(5):2212-2220.
91. Standish AJ, Weiser JN. Human neutrophils kill Streptococcus pneumoniae via serine proteases. J Immunol. 2009;183(4):2602-2609.