Interleukin-1β regulates CXCL8 release and influences disease outcome in response to Streptococcus pneumoniae, defining intercellular cooperation between pulmonary epithelial cells and macrophages

Infection and Immunity

Volumn 80, Issue 3, 2012, Pages 1140-1149

  Marriott, Helen M ^a   Gascoyne, Kate A ^a,b   Gowda, Ravi ^b   Geary, Ian ^a   Nicklin, Martin J H ^a   Iannelli, Francesco ^c   Pozzi, Gianni ^c   Mitchell, Timothy J ^d   Whyte, Moira K B ^a,b   Sabroe, Ian ^a,b   Dockrell, David H ^a,b  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b SHEFFIELD TEACHING HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^c UNIVERSITY OF SIENA   (Italy)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; INTERLEUKIN 8; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA RECEPTOR; VITAMIN D;

AIRWAY; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL ACTIVITY; CELL CULTURE; CELL DIFFERENTIATION; CELL INTERACTION; CELL STIMULATION; CELL VIABILITY; CELLULAR IMMUNITY; COCULTURE; CONTROLLED STUDY; CULTURE MEDIUM; CYTOKINE RELEASE; DISEASE SEVERITY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTERCELLULAR SPACE; LUNG ALVEOLUS EPITHELIUM; LUNG ALVEOLUS MACROPHAGE; LUNG INFILTRATE; MOUSE; NEUTROPHIL; NONHUMAN; OUTCOME ASSESSMENT; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEROTYPE; SIGNAL TRANSDUCTION; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE; SUPERNATANT; UPREGULATION;

ANIMALS; CELL LINE; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; EPITHELIAL CELLS; FEMALE; HUMANS; INTERLEUKIN-1BETA; INTERLEUKIN-8; LUNG; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; PNEUMOCOCCAL INFECTIONS; RECEPTORS, INTERLEUKIN-1; STREPTOCOCCUS PNEUMONIAE;

EID: 84857681753     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05697-11     Document Type: Article

References (67)

1. Adamou JE, Wizemann TM, Barren P, Langermann S. 1998. Adherence of Streptococcus pneumoniae to human bronchial epithelial cells (BEAS-2B). Infect. Immun. 66:820-822.
2. Ali F, et al. 2003. Streptococcus pneumoniae-associated human macrophage apoptosis after bacterial internalization via complement and Fcgamma receptors correlates with intracellular bacterial load. J. Infect. Dis. 188:1119-1131.
3. Baggiolini M, Walz A, Kunkel SL. 1989. Neutrophil-activating peptide-1/interleukin 8, a novel cytokine that activates neutrophils. J. Clinical Invest. 84:1045-1049.
4. Barocchi MA, et al. 2006. A pneumococcal pilus influences virulence and host inflammatory responses. Proc. Natl. Acad. Sci. U. S. A. 103:2857-2862.
5. Beisswenger C, Lysenko ES, Weiser JN. 2009. Early bacterial colonization induces Toll-like receptor-dependent transforming growth factor beta signaling in the epithelium. Infect. Immun. 77:2212-2220.
6. Bogaert D, De Groot R, Hermans PW. 2004. Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect. Dis. 4:144-154.
7. Bootsma HJ, Egmont-Petersen M, Hermans PW. 2007. Analysis of the in vitro transcriptional response of human pharyngeal epithelial cells to adherent Streptococcus pneumoniae: evidence for a distinct response to encapsulated strains. Infect. Immun. 75:5489-5499.
8. Calbo E, Garau J. 2010. Of mice and men: innate immunity in pneumococcal pneumonia. Int. J. Antimicrob. Agents 35:107-113.
9. Chaudhuri N, et al. 2010. Diesel exhaust particles override natural injurylimiting pathways in the lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 299:L263-L271.
10. Chou RC, et al. 2010. Lipid-cytokine-chemokine cascade drives neutrophil recruitment in a murine model of inflammatory arthritis. Immunity 33:266-278.
11. Coulter KR, Wewers MD, Lowe MP, Knoell DL. 1999. Extracellular regulation of interleukin (IL)-1beta through lung epithelial cells and defective IL-1 type II receptor expression. Am. J. Resp. Cell. Mol. Biol. 20:964-975.
12. Daigneault M, Preston JA, Marriott HM, Whyte MK, Dockrell DH. 2010. The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS One 5:e8668.
13. Diamond G, Legarda D, Ryan LK. 2000. The innate immune response of the respiratory epithelium. Immunol. Rev. 173:27-38.
14. Dockrell DH, Lee M, Lynch DH, Read RC. 2001. Immune-mediated phagocytosis and killing of Streptococcus pneumoniae are associated with direct and bystander macrophage apoptosis. J. Infect. Dis. 184:713-722.
15. Dockrell DH, et al. 2003. Alveolar macrophage apoptosis contributes to pneumococcal clearance in a resolving model of pulmonary infection. J. Immunol. 171:5380-5388.
16. Eskola J, et al. 1992. Epidemiology of invasive pneumococcal infections in children in Finland. J. Am. Med. Assoc. 268:3323-3327.
17. Gingles NA, et al. 2001. Role of genetic resistance in invasive pneumococcal infection: identification and study of susceptibility and resistance in inbred mouse strains. Infect. Immun. 69:426-434.
18. Glaccum MB, et al. 1997. Phenotypic and functional characterization of mice that lack the type I receptor for IL-1. J. Immunol. 159:3364-3371.
19. Gosink KK, Mann ER, Guglielmo C, Tuomanen EI, Masure HR. 2000. Role of novel choline binding proteins in virulence of Streptococcus pneumoniae. Infect. Immun. 68:5690-5695.
20. Gribar SC, Richardson WM, Sodhi CP, Hackam DJ. 2008. No longer an innocent bystander: epithelial Toll-like receptor signaling in the development of mucosal inflammation. Mol. Med. 14:645-659.
21. Hammerschmidt S, et al. 2005. Illustration of pneumococcal polysaccharide capsule during adherence and invasion of epithelial cells. Infect. Immun. 73:4653-4667.
22. Hathaway LJ, Battig P, Muhlemann K. 2007. In vitro expression of the first capsule gene of Streptococcus pneumoniae, cpsA, is associated with serotype-specific colonization prevalence and invasiveness. Microbiology 153:2465-2471.
23. Herbold W, et al. 2010. Importance of CXC chemokine receptor 2 in alveolar neutrophil and exudate macrophage recruitment in response to pneumococcal lung infection. Infect. Immun. 78:2620-2630.
24. Heumann D, Barras C, Severin A, Glauser MP, Tomasz A. 1994. Grampositive cell walls stimulate synthesis of tumor necrosis factor alpha and interleukin-6 by human monocytes. Infect. Immun. 62:2715-2721.
25. Hippenstiel S, Opitz B, Schmeck B, Suttorp N. 2006. Lung epithelium as a sentinel and effector system in pneumonia-molecular mechanisms of pathogen recognition and signal transduction. Resp. Res. 7:97.
26. Hmama Z, et al. 1999. 1α, 25-Dihydroxyvitamin D(3)-induced myeloid cell differentiation is regulated by a vitamin D receptor-phosphatidylinositol 3-kinase signaling complex. J. Exp. Med. 190:1583-1594.
27. Jones MR, Simms BT, Lupa MM, Kogan MS, Mizgerd JP. 2005. Lung NF-kappaB activation and neutrophil recruitment require IL-1 and TNF receptor signaling during pneumococcal pneumonia. J. Immunology 175:7530-7535.
28. Kadioglu A, Weiser JN, Paton JC, Andrew PW. 2008. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat. Rev. Microbiol. 6:288-301.
29. Khor CC, et al. 2007. A Mal functional variant is associated with protection against invasive pneumococcal disease, bacteremia, malaria, and tuberculosis. Nat. Genet. 39:523-528.
30. Krakauer T. 2002. Stimulant-dependent modulation of cytokines and chemokines by airway epithelial cells: cross-talk between pulmonary epithelial and peripheral blood mononuclear cells. Clin. Diagn. Lab. Immunol. 9:126-131.
31. Ku CL, et al. 2007. Selective predisposition to bacterial infections in IRAK-4-deficient children: IRAK-4-dependent TLRs are otherwise redundant in protective immunity. J. Exp. Med. 204:2407-2422.
32. Magee AD, Yother J. 2001. Requirement for capsule in colonization by Streptococcus pneumoniae. Infect. Immun. 69:3755-3761.
33. Marks M, et al. 2007. Influence of neutropenia on the course of serotype 8 pneumococcal pneumonia in mice. Infect. Immun. 75:1586-1597.
34. Marriott HM, et al. 2008. Reactive oxygen species regulate neutrophil recruitment and survival in pneumococcal pneumonia. Am. J. Respir. Crit. Care Med. 177:887-895.
35. Mayer AK, et al. 2007. Differential recognition of TLR-dependent microbial ligands in human bronchial epithelial cells. J. Immunol. 178:3134-3142.
36. Miles AA, Misra SS, Irwin JO. 1938. The estimation of the bactericidal power of the blood. J. Hyg. 38:732-749.
37. Morris GE, et al. 2006. Cooperative molecular and cellular networks regulate Toll-like receptor-dependent inflammatory responses. FASEB J. 20:2153-2155.
38. Morris GE, et al. 2005. Agonists of Toll-like receptors 2 and 4 activate airway smooth muscle via mononuclear leukocytes. Am. J. Resp. Crit. Care Med. 171:814-822.
39. Musher DM. 1992. Infections caused by Streptococcus pneumoniae: clinical spectrum, pathogenesis, immunity, and treatment. Clin. Infect. Dis. 14:801-807.
40. Obaro S, Adegbola R. 2002. The pneumococcus: carriage, disease and conjugate vaccines. J. Med. Microbiol. 51:98-104.
41. Opitz B, et al. 2004. Nucleotide-binding oligomerization domain proteins are innate immune receptors for internalized Streptococcus pneumoniae. J. Biol. Chem. 279:36426-36432.
42. Parker LC, et al. 2008. A phosphatidylserine species inhibits a range of TLR-but not IL-1beta-induced inflammatory responses by disruption of membrane microdomains. J. Immunol. 181:5606-5617.
43. Pearce BJ, Iannelli F, Pozzi G. 2002. Construction of new unencapsulated (rough) strains of Streptococcus pneumoniae. Res. Microbiol. 153:243-247.
44. Quinton LJ, et al. 2007. Functions and regulation of NF-kappaB RelA during pneumococcal pneumonia. J. Immunol. 178:1896-1903.
45. Riesenfeld-Orn I, Wolpe S, Garcia-Bustos JF, Hoffmann MK, Tuomanen E. 1989. Production of interleukin-1 but not tumor necrosis factor by human monocytes stimulated with pneumococcal cell surface components. Infect. Immun. 57:1890-1893.
46. Rijneveld AW, et al. 2001. TNF-alpha compensates for the impaired host defense of IL-1 type I receptor-deficient mice during pneumococcal pneumonia. J. Immunol. 167:5240-5246.
47. Rijneveld AW, et al. 2003. Interleukin-1 receptor antagonist transiently impairs antibacterial defense but not survival in murine pneumococcal pneumonia. Eur. Cytokine Netw. 14:242-245.
48. Robson RL, Reed NA, Horvat RT. 2006. Differential activation of in-flammatory pathways in A549 type II pneumocytes by Streptococcus pneumoniae strains with different adherence properties. BMC Infect. Dis. 6:71.
49. Schmeck B, et al. 2006. Pneumococci induced TLR-and Rac1-dependent NF-kappaB-recruitment to the IL-8 promoter in lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 290:L730-L737.
50. Schwende H, Fitzke E, Ambs P, Dieter P. 1996. Differences in the state of differentiation of THP-1 cells induced by phorbol ester and 1,25-dihydroxyvitamin D3. J. Leukocyte Biol. 59:555-561.
51. Selinger DS, Reed WP. 1979. Pneumococcal adherence to human epithelial cells. Infect. Immun. 23:545-548.
52. Standiford TJ, et al. 1990. Interleukin-8 gene expression by a pulmonary epithelial cell line. A model for cytokine networks in the lung. J. Clin. Invest. 86:1945-1953.
53. Standiford TJ, Kunkel SL, Phan SH, Rollins BJ, Strieter RM. 1991. Alveolar macrophage-derived cytokines induce monocyte chemoattractant protein-1 expression from human pulmonary type II-like epithelial cells. J. Biol. Chem. 266:9912-9918.
54. Strieter RM, Kunkel SL, Keane MP, Standiford TJ. 1999. Chemokines in lung injury: Thomas A. Neff lecture. Chest 116:103S-110S.
55. Sun K, Salmon SL, Lotz SA, Metzger DW. 2007. Interleukin-12 promotes gamma interferon-dependent neutrophil recruitment in the lung and improves protection against respiratory Streptococcus pneumoniae infection. Infect. Immun. 75:1196-1202.
56. Sutherland AM, et al. 2011. A nonsynonymous polymorphism of IRAK4 associated with increased prevalence of Gram-positive infection and decreased response to Toll-like receptor ligands. J. Innate Immun. 3:447-458.
57. Talbot UM, Paton AW, Paton JC. 1996. Uptake of Streptococcus pneumoniae by respiratory epithelial cells. Infect. Immun. 64:3772-3777.
58. Thomas LH, Wickremasinghe MI, Sharland M, Friedland JS. 2000. Synergistic upregulation of interleukin-8 secretion from pulmonary epithelial cells by direct and monocyte-dependent effects of respiratory syncytial virus infection. J. Virol. 74:8425-8433.
59. Tong HH, Blue LE, James MA, DeMaria TF. 2000. Evaluation of the virulence of a Streptococcus pneumoniae neuraminidase-deficient mutant in nasopharyngeal colonization and development of otitis media in the chinchilla model. Infect. Immun. 68:921-924.
60. Ward JR, et al. 2009. A central role for monocytes in Toll-like receptormediated activation of the vasculature. Immunology 128:58-68.
61. Ware LB, Matthay MA. 2000. The acute respiratory distress syndrome. New Engl. J. Med. 342:1334-1349.
62. Weiser JN, et al. 2003. Antibody-enhanced pneumococcal adherence requires IgA1 protease. Proc. Natl. Acad. Sci. U. S. A. 100:4215-4220.
63. Wickremasinghe MI, Thomas LH, Friedland JS. 1999. Pulmonary epithelial cells are a source of IL-8 in the response to Mycobacterium tuberculosis: essential role of IL-1 from infected monocytes in a NF-kappa B-dependent network. J. Immunol. 163:3936-3947.
64. Winder AA, Wohlford-Lenane C, Scheetz TE. 2009. Differential effects of cytokines and corticosteroids on Toll-like receptor 2 expression and activity in human airway epithelia. Resp. Res. 10:96.
65. Witzenrath M, et al. 2011. The NLRP3 inflammasome is differentially activated by pneumolysin variants and contributes to host defense in pneumococcal pneumonia. J. Immunol. 187:434-440.
66. Xu F, et al. 2008. Modulation of the inflammatory response to Streptococcus pneumoniae in a model of acute lung tissue infection. Am. J. Resp. Cell. Mol. Biol. 39:522-529.
67. Zwijnenburg PJ, van der Poll T, Florquin S, Roord JJ, Van Furth AM. 2003. IL-1 receptor type 1 gene-deficient mice demonstrate an impaired host defense against pneumococcal meningitis. J. Immunol. 170:4724-4730.