Porins of Pseudomonas Aeruginosa Induce Release of Tumor Necrosis Factor Alpha and Interleukin-6 by Human Leukocytes

Overview

Journal Infect Immun

Publisher American Society for Microbiology

Specialty Allergy & Immunology

Date 1997 May 1

PMID 9125547

Citations 11

Authors

V Cusumano

M A Tufano

G Mancuso

M Carbone

F Rossano

M T Fera

F A Ciliberti

E Ruocco

R A Merendino

G Teti

Affiliations

Soon will be listed here.

Abstract

The aim of this study was to examine the ability of Pseudomonas aeruginosa components to induce release of cytokines from human leukocytes. Human whole-blood cultures were incubated with several concentrations of purified P. aeruginosa products, including porins, exomucopolysaccharide, lipopolysaccharide, and toxin A. Supernatants were assayed for tumor necrosis factor alpha (TNF-alpha) and interleukin-6 (IL-6) activities. All of the P. aeruginosa components except toxin A were able to stimulate the release of both cytokines. On a weight basis, porins were as effective as lipopolysaccharide and significantly more effective than exomucopolysaccharide in inducing IL-6 release (P < 0.05). Moreover, porins were more potent than either exomucopolysaccharide or lipopolysaccharide in inducing TNF-alpha release (P < 0.05). Further experiments using isolated leukocytes suggested that monocytes were the cell population predominantly responsible for the production of both cytokines. These data indicate that P. aeruginosa porins are able to induce significant cytokine production. These components may be responsible for the chronically overactive inflammatory response associated with persistent lung infection in cystic fibrosis patients.

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References

AMES G, Spudich E, Nikaido H . Protein composition of the outer membrane of Salmonella typhimurium: effect of lipopolysaccharide mutations. J Bacteriol. 1974; 117(2):406-16. PMC: 285527. DOI: 10.1128/jb.117.2.406-416.1974. View

Evans L, Linker A . Production and characterization of the slime polysaccharide of Pseudomonas aeruginosa. J Bacteriol. 1973; 116(2):915-24. PMC: 285463. DOI: 10.1128/jb.116.2.915-924.1973. View

Nakae T . Outer membrane of Salmonella. Isolation of protein complex that produces transmembrane channels. J Biol Chem. 1976; 251(7):2176-8. View

Morrison D, Betz S, Jacobs D . Isolation of a lipid A bound polypeptide responsible for "LPS-initiated" mitogenesis of C3H/HeJ spleen cells. J Exp Med. 1976; 144(3):840-6. PMC: 2190404. DOI: 10.1084/jem.144.3.840. View

Smit J, Nikaido H . Outer membrane of gram-negative bacteria. XVIII. Electron microscopic studies on porin insertion sites and growth of cell surface of Salmonella typhimurium. J Bacteriol. 1978; 135(2):687-702. PMC: 222430. DOI: 10.1128/jb.135.2.687-702.1978. View

Turner M, Warner J, Stokes C . Immunological studies in cystic fibrosis. Arch Dis Child. 1978; 53(8):631-8. PMC: 1545069. DOI: 10.1136/adc.53.8.631. View

Hodson M . Immunological abnormalities in cystic fibrosis: chicken or egg?. Thorax. 1980; 35(11):801-6. PMC: 471387. DOI: 10.1136/thx.35.11.801. View

Borregaard N . Bactericidal mechanisms of the human neutrophil. An integrated biochemical and morphological model. Scand J Haematol. 1984; 32(3):225-30. DOI: 10.1111/j.1600-0609.1984.tb01685.x. View

Suter S, Schaad U, Roux L, Nydegger U, Waldvogel F . Granulocyte neutral proteases and Pseudomonas elastase as possible causes of airway damage in patients with cystic fibrosis. J Infect Dis. 1984; 149(4):523-31. DOI: 10.1093/infdis/149.4.523. View

10.

Galdiero F, Tufano M, Sommese L, Folgore A, Tedesco F . Activation of complement system by porins extracted from Salmonella typhimurium. Infect Immun. 1984; 46(2):559-63. PMC: 261571. DOI: 10.1128/iai.46.2.559-563.1984. View

11.

Tufano M, Berlingieri M, Sommese L, Galdiero F . Immune response in mice and effects on cells by outer membrane porins from Salmonella typhimurium. Microbiologica. 1984; 7(4):353-66. View

12.

Bruce M, Poncz L, Klinger J, Stern R, Tomashefski Jr J, Dearborn D . Biochemical and pathologic evidence for proteolytic destruction of lung connective tissue in cystic fibrosis. Am Rev Respir Dis. 1985; 132(3):529-35. DOI: 10.1164/arrd.1985.132.3.529. View

13.

Espevik T, Nissen-Meyer J . A highly sensitive cell line, WEHI 164 clone 13, for measuring cytotoxic factor/tumor necrosis factor from human monocytes. J Immunol Methods. 1986; 95(1):99-105. DOI: 10.1016/0022-1759(86)90322-4. View

14.

Van Snick J, Cayphas S, Vink A, Uyttenhove C, Coulie P, Rubira M . Purification and NH2-terminal amino acid sequence of a T-cell-derived lymphokine with growth factor activity for B-cell hybridomas. Proc Natl Acad Sci U S A. 1986; 83(24):9679-83. PMC: 387204. DOI: 10.1073/pnas.83.24.9679. View

15.

Galdiero F, Gorga F, Bentivoglio C, Mancuso R, Galdiero E, Tufano M . The action of LPS porins and peptidoglycan fragments on human spermatozoa. Infection. 1988; 16(6):349-53. DOI: 10.1007/BF01644545. View

16.

Aderka D, Le J, Vilcek J . IL-6 inhibits lipopolysaccharide-induced tumor necrosis factor production in cultured human monocytes, U937 cells, and in mice. J Immunol. 1989; 143(11):3517-23. View

17.

Pier G . Immunologic properties of Pseudomonas aeruginosa mucoid exopolysaccharide (alginate). Antibiot Chemother (1971). 1989; 42:80-7. DOI: 10.1159/000417608. View

18.

Tufano M, Ianniello R, Galdiero M, De Martino L, Galdiero F . Effect of Salmonella typhimurium porins on biological activities of human polymorphonuclear leukocytes. Microb Pathog. 1989; 7(5):337-46. DOI: 10.1016/0882-4010(89)90037-5. View

19.

Misfeldt M, Legaard P, Howell S, Fornella M, LeGrand R . Induction of interleukin-1 from murine peritoneal macrophages by Pseudomonas aeruginosa exotoxin A. Infect Immun. 1990; 58(4):978-82. PMC: 258570. DOI: 10.1128/iai.58.4.978-982.1990. View

20.

Van Snick J . Interleukin-6: an overview. Annu Rev Immunol. 1990; 8:253-78. DOI: 10.1146/annurev.iy.08.040190.001345. View