Home LiteratureArticle Details
PMID: 2921324 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages.

The Journal of clinical investigation ·Vol. 83 ·No. 3 ·1989-03-00 ·Pages 865-75

Savill JS, Wyllie AH, Henson JE, Walport MJ, Henson PM, Haslett C

Abstract

Mechanisms governing the normal resolution processes of inflammation are poorly understood, yet their elucidation may lead to a greater understanding of the pathogenesis of chronic inflammation. The removal of neutrophils and their potentially histotoxic contents is one prerequisite of resolution. Engulfment by macrophages is an important disposal route, and changes in the senescent neutrophil that are associated with their recognition by macrophages are the subject of this investigation. Over 24 h in culture an increasing proportion of human neutrophils from peripheral blood or acutely inflamed joints underwent morphological changes characteristic of programmed cell death or apoptosis. Time-related chromatin cleavage in an internucleosomal pattern indicative of the endogenous endonuclease activation associated with programmed cell death was also demonstrated. A close correlation was observed between the increasing properties of apoptosis in neutrophils and the degree of macrophage recognition of the aging neutrophil population, and a direct relationship between these parameters was confirmed within aged neutrophil populations separated by counterflow centrifugation into fractions with varying proportions of apoptosis. Macrophages from acutely inflamed joints preferentially ingested apoptotic neutrophils and histological evidence was presented for occurrence of the process in situ. Programmed cell death is a phenomenon of widespread biological importance and has not previously been described in a cell of the myeloid line. Because it leads to recognition of intact senescent neutrophils that have not necessarily disgorged their granule contents, these processes may represent a mechanism for the removal of neutrophils during inflammation that also serves to limit the degree of tissue injury.

MeSH Terms
Arthritis/pathology,physiopathology Arthritis, Rheumatoid/pathology,physiopathology Cell Survival Cells, Cultured Chromatin/metabolism Humans Kinetics Macrophages/physiology Microscopy, Electron Neutrophils/pathology,physiology Osteoarthritis/pathology,physiopathology Phagocytosis Synovial Fluid/cytology
Chemicals
Chromatin
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Savill J S
Department of Medicine, Royal Postgraduate Medical School, Hammersmith Hospital, London, United Kingdom.
Wyllie A H
Henson J E
Walport M J
Henson P M
Haslett C
References (29)
29 references, click to expand
  1. Glucocorticoid activation of a calcium-dependent endonuclease in thymocyte nuclei leads to cell death.
    J Immunol. 1984 Jan;132(1):38-42 PMID: 6317746
  2. Internal disintegration model of cytotoxic lymphocyte-induced target damage.
    Immunol Rev. 1983;72:97-118 PMID: 6347870
  3. Hormone-induced cell death. 2. Surface changes in thymocytes undergoing apoptosis.
    Am J Pathol. 1984 Jun;115(3):426-36 PMID: 6610362
  4. Modulation of multiple neutrophil functions by preparative methods or trace concentrations of bacterial lipopolysaccharide.
    Am J Pathol. 1985 Apr;119(1):101-10 PMID: 2984939
  5. Macrophage recognition of cells undergoing programmed cell death (apoptosis).
    Immunology. 1985 Oct;56(2):351-8 PMID: 3876985
  6. Low density neutrophils in patients with systemic lupus erythematosus, rheumatoid arthritis, and acute rheumatic fever.
    Arthritis Rheum. 1986 Nov;29(11):1334-42 PMID: 2430586
  7. Tissue injury in inflammation. Oxidants, proteinases, and cationic proteins.
    J Clin Invest. 1987 Mar;79(3):669-74 PMID: 3546374
  8. Cytotoxic T lymphocytes and glucocorticoids activate an endogenous suicide process in target cells.
    Nature. 1987 May 7-13;327(6117):62-4 PMID: 3494953
  9. The pulmonary vascular sequestration of neutrophils in endotoxemia is initiated by an effect of endotoxin on the neutrophil in the rabbit.
    Am Rev Respir Dis. 1987 Jul;136(1):9-18 PMID: 3605849
  10. Monocyte retention and migration in pulmonary inflammation. Requirement for neutrophils.
    Lab Invest. 1988 Aug;59(2):200-13 PMID: 3404972
  11. ELECTRON-MICROSCOPE OBSERVATIONS ON THE PHAGOCYTOSIS OF NEUTROPHIL POLYMORPHONUCLEAR LEUCOCYTES BY MACROPHAGES.
    J Pathol Bacteriol. 1964 Jul;88:307-9 PMID: 14194992
  12. GRANULOCYTOPOIESIS. I. SENESCENCE AND RANDOM LOSS OF NEUTROPHILIC GRANULOCYTES IN HUMAN BEINGS.
    Blood. 1964 Oct;24:402-14 PMID: 14220782
  13. Unusual synovial fluid findings in Reiter's syndrome.
    Ann Intern Med. 1967 Apr;66(4):677-84 PMID: 6023534
  14. Cytological and cytochemical studies on cell death and digestion in the foetal rat foot: the role of macrophages and hydrolytic enzymes.
    J Cell Sci. 1968 Jun;3(2):245-62 PMID: 5661999
  15. Immunologic tissue injury mediated by neutrophilic leukocytes.
    Adv Immunol. 1968;9:97-162 PMID: 4236490
  16. Phagocytosis of blood cells by splenic macrophages in thrombotic thrombocytopenic purpura.
    Ann Intern Med. 1975 Jun;82(6):799-802 PMID: 1169901
  17. Intracellular control of human neutrophil secretion. I. C5a-induced stimulus-specific desensitization and the effects of cytochalasin B.
    J Immunol. 1978 Sep;121(3):851-5 PMID: 211165
  18. Joint fluid cytology in Reiter's disease.
    Ann Rheum Dis. 1978 Dec;37(6):557-60 PMID: 749702
  19. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation.
    Nature. 1980 Apr 10;284(5756):555-6 PMID: 6245367
  20. Susceptibility of soluble and matrix fibronectins to degradation by tissue proteinases, mast cell chymase and cathepsin G.
    J Biol Chem. 1981 Jan 10;256(1):471-7 PMID: 6450204
  21. Phagocytosis of neutrophils by marrow macrophages in childhood chronic benign neutropenia.
    J Pediatr. 1981 Feb;98(2):207-12 PMID: 7463215
  22. Control of vascular permeability by polymorphonuclear leukocytes in inflammation.
    Nature. 1981 Feb 19;289(5799):646-50 PMID: 7464931
  23. Cell death: the significance of apoptosis.
    Int Rev Cytol. 1980;68:251-306 PMID: 7014501
  24. Peritoneal macrophages which phagocytose autologous polymorphonuclear leucocytes in guinea-pigs. I: induction by irritants and microorgansisms and inhibition by colchicine.
    Br J Exp Pathol. 1982 Jun;63(3):278-84 PMID: 6807336
  25. Phagocytosis of senescent neutrophils by human monocyte-derived macrophages and rabbit inflammatory macrophages.
    J Exp Med. 1982 Aug 1;156(2):430-42 PMID: 7097159
  26. Hormone-induced cell death. Purification ad properties of thymocytes undergoing apoptosis after glucocorticoid treatment.
    Am J Pathol. 1982 Oct;109(1):78-87 PMID: 6289672
  27. Evidence for granulocyte-mediated macrophage activation after C. parvum immunization.
    Cell Immunol. 1983 Feb 1;75(2):367-77 PMID: 6831566
  28. Human serum induces maturation of human monocytes in vitro. Changes in cytolytic activity, intracellular lysosomal enzymes, and nonspecific esterase activity.
    Am J Pathol. 1983 Jun;111(3):331-40 PMID: 6859218
  29. Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis.
    J Pathol. 1984 Jan;142(1):67-77 PMID: 6422024
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
1989-03-00
Pages
865-75
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC303760
Subset
IM
Grants
NHLBI NIH HHS · HL-27353 · 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