Home LiteratureArticle Details
PMID: 9636192 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Resistance to endotoxic shock and reduced neutrophil migration in mice deficient for the Src-family kinases Hck and Fgr.

Lowell CA, Berton G

Abstract

Signal transduction through the leukocyte integrins is required for the processes of firm adhesion, activation, and chemotaxis of neutrophils during inflammatory reactions. Neutrophils isolated from knockout mice that are deficient in the expression of p59/61(hck) (Hck) and p58(c-fgr) (Fgr), members of the Src-family of protein tyrosine kinases, have been shown to be defective in adhesion mediated activation. Cells from these animals have impaired induction of respiratory burst and granule secretion following plating on surfaces that crosslink beta2 and beta3 integrins. To determine if the defective function of hck-/-fgr-/- neutrophils observed in vitro also results in impaired inflammatory responses in vivo, we examined responses induced by lipopolysaccharide (LPS) injection in these animals. The hck-/-fgr-/- mice showed marked resistance to the lethal effects of high-dose LPS injection despite the fact that high levels of serum tumor necrosis factor alpha and interleukin 1alpha were detected. Serum chemistry analysis revealed a marked reduction in liver and renal damage in mutant mice treated with LPS, whereas blood counts showed a marked neutrophilia that was not seen in wild-type animals. Direct examination of liver sections from mutant mice revealed reduced neutrophil migration into the tissue. These data demonstrate that defective integrin signaling in neutrophils, caused by loss of Hck and Fgr tyrosine kinase activity, results in impaired inflammation-dependent tissue injury in vivo.

MeSH Terms
Animals Cell Adhesion/immunology Chemotaxis, Leukocyte/immunology Immunity, Innate/immunology Lipopolysaccharides/toxicity Liver/pathology Mice Mice, Inbred C57BL Neutrophils/immunology Protein-Tyrosine Kinases/physiology Proto-Oncogene Proteins/physiology Proto-Oncogene Proteins c-hck Shock, Septic/immunology Signal Transduction src-Family Kinases/physiology
Chemicals
Lipopolysaccharides Proto-Oncogene Proteins Protein-Tyrosine Kinases Hck protein, mouse Proto-Oncogene Proteins c-hck proto-oncogene proteins c-fgr src-Family Kinases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Lowell C A
Department of Laboratory Medicine, University of California, San Francisco, CA 94143-0100, USA. clowell@cgl.ucsf.edu
Berton G
References (36)
36 references, click to expand
  1. Acute inflammation in gram-negative infection: endotoxin, interleukin 1, tumor necrosis factor, and neutrophils.
    Fed Proc. 1987 Jan;46(1):97-104 PMID: 3542580
  2. Lung vascular injury induced by chemotactic factors: enhancement by bacterial endotoxins.
    Fed Proc. 1986 Jan;45(1):7-12 PMID: 3510132
  3. Tumor necrosis factor is a terminal mediator in galactosamine/endotoxin-induced hepatitis in mice.
    Biochem Pharmacol. 1989 Feb 15;38(4):627-31 PMID: 2465008
  4. The biology of cachectin/TNF--a primary mediator of the host response.
    Annu Rev Immunol. 1989;7:625-55 PMID: 2540776
  5. Cytokine-induced respiratory burst of human neutrophils: dependence on extracellular matrix proteins and CD11/CD18 integrins.
    J Cell Biol. 1989 Sep;109(3):1341-9 PMID: 2475511
  6. Local production of tumor necrosis factor alpha, interleukin 1, and interleukin 6 in meningococcal meningitis. Relation to the inflammatory response.
    J Exp Med. 1989 Dec 1;170(6):1859-67 PMID: 2584928
  7. Mac-1 (CD11b/CD18) mediates adherence-dependent hydrogen peroxide production by human and canine neutrophils.
    J Immunol. 1990 Apr 1;144(7):2702-11 PMID: 2181020
  8. Neutrophils contribute to ischemia/reperfusion injury in rat liver in vivo.
    FASEB J. 1990 Dec;4(15):3355-9 PMID: 2253850
  9. Tumor necrosis factor alpha mediates lethal activity of killed gram-negative and gram-positive bacteria in D-galactosamine-treated mice.
    Infect Immun. 1991 Jun;59(6):2110-5 PMID: 2037372
  10. Neutrophil-induced liver cell injury in endotoxin shock is a CD11b/CD18-dependent mechanism.
    Am J Physiol. 1991 Dec;261(6 Pt 1):G1051-6 PMID: 1767846
  11. Neutrophil depletion protects against liver injury from bacterial endotoxin.
    Lab Invest. 1992 Mar;66(3):347-61 PMID: 1538588
  12. Mechanisms of lipopolysaccharide-induced neutrophil retention. Relative contributions of adhesive and cellular mechanical properties.
    J Immunol. 1992 Jul 1;149(1):154-62 PMID: 1376747
  13. Monoclonal antibody NIMP-R10 directed against the CD11b chain of the type 3 complement receptor can substitute for monoclonal antibody 5C6 to exacerbate listeriosis by preventing the focusing of myelomonocytic cells at infectious foci in the liver.
    J Leukoc Biol. 1992 Jul;52(1):130-2 PMID: 1640170
  14. The role of interleukin-1 in disease.
    N Engl J Med. 1993 Jan 14;328(2):106-13 PMID: 8439348
  15. Adhesion-dependent protein tyrosine phosphorylation in neutrophils treated with tumor necrosis factor.
    J Cell Biol. 1993 Feb;120(3):777-84 PMID: 8425901
  16. Effect of inhibitors of distinct signalling pathways on neutrophil Q2- generation in response to tumor necrosis factor-alpha, and antibodies against CD18 and CD11a: evidence for a common and unique pattern of sensitivity to wortmannin and protein tyrosine kinase inhibitors.
    Biochem Biophys Res Commun. 1993 Feb 15;190(3):935-40 PMID: 8094958
  17. Role of leukocyte adhesion molecules in complement-induced lung injury.
    J Immunol. 1993 Mar 15;150(6):2401-6 PMID: 8095513
  18. Role of beta 1, beta 2 integrins and ICAM-1 in lung injury after deposition of IgG and IgA immune complexes.
    J Immunol. 1993 Mar 15;150(6):2407-17 PMID: 7680691
  19. Role of beta 2 integrins and ICAM-1 in lung injury following ischemia-reperfusion of rat hind limbs.
    Am J Pathol. 1993 Aug;143(2):464-72 PMID: 8102031
  20. Leukocyte response integrin and integrin-associated protein act as a signal transduction unit in generation of a phagocyte respiratory burst.
    J Exp Med. 1993 Oct 1;178(4):1165-74 PMID: 8104228
  21. The Src family of tyrosine protein kinases in hemopoietic signal transduction.
    Stem Cells. 1993 Sep;11(5):371-80 PMID: 7694720
  22. Functional overlap in the src gene family: inactivation of hck and fgr impairs natural immunity.
    Genes Dev. 1994 Feb 15;8(4):387-98 PMID: 8125254
  23. Superantigen mediated shock: a cytokine release syndrome.
    Immunobiology. 1993 Nov;189(3-4):270-84 PMID: 8125513
  24. Leukocytosis and resistance to septic shock in intercellular adhesion molecule 1-deficient mice.
    J Exp Med. 1994 Jul 1;180(1):95-109 PMID: 7911822
  25. Deficiency of Src family kinases p59/61hck and p58c-fgr results in defective adhesion-dependent neutrophil functions.
    J Cell Biol. 1996 May;133(4):895-910 PMID: 8666673
  26. Activation of p58c-fgr and p53/56lyn in adherent human neutrophils: evidence for a role of divalent cations in regulating neutrophil adhesion and protein tyrosine kinase activities.
    J Inflamm. 1995;45(4):297-311 PMID: 8867673
  27. Neutrophil activation by adhesion: mechanisms and pathophysiological implications.
    Int J Clin Lab Res. 1996;26(3):160-77 PMID: 8905448
  28. Molecular interactions in cell adhesion complexes.
    Curr Opin Cell Biol. 1997 Feb;9(1):76-85 PMID: 9013677
  29. Signaling by adhesion in human neutrophils: activation of the p72syk tyrosine kinase and formation of protein complexes containing p72syk and Src family kinases in neutrophils spreading over fibrinogen.
    J Immunol. 1997 Feb 15;158(4):1902-10 PMID: 9029132
  30. Lipopolysaccharide (LPS)-induced macrophage activation and signal transduction in the absence of Src-family kinases Hck, Fgr, and Lyn.
    J Exp Med. 1997 May 5;185(9):1661-70 PMID: 9151903
  31. Granules of the human neutrophilic polymorphonuclear leukocyte.
    Blood. 1997 May 15;89(10):3503-21 PMID: 9160655
  32. Transcriptional activation of vascular cell adhesion molecule-1 gene in vivo and its role in the pathophysiology of neutrophil-induced liver injury in murine endotoxin shock.
    J Immunol. 1997 Jun 15;158(12):5941-8 PMID: 9190948
  33. Mechanisms of neutrophil-induced parenchymal cell injury.
    J Leukoc Biol. 1997 Jun;61(6):647-53 PMID: 9201255
  34. Molecules and mechanisms operating in septic shock: lessons from knockout mice.
    Immunol Today. 1997 Jul;18(7):329-34 PMID: 9238836
  35. Effects of bacterial endotoxins on neutrophil function.
    Rev Infect Dis. 1985 May-Jun;7(3):404-18 PMID: 3895355
  36. Lethal toxicity of lipopolysaccharide and tumor necrosis factor in normal and D-galactosamine-treated mice.
    J Exp Med. 1987 Mar 1;165(3):657-63 PMID: 3819645
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1998-06-23
Pages
7580-4
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC22689
Subset
IM
Grants
NHLBI NIH HHS · P50 HL054476 · United States
NIDDK NIH HHS · DK50267 · United States
NHLBI NIH HHS · HL54476 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com