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PMID: 6088394 Published · ppublish English Journal Article

In vitro inhibition of murine macrophage migration by Bordetella pertussis lymphocytosis-promoting factor.

Infection and immunity ·Vol. 45 ·No. 3 ·1984-09-00 ·Pages 718-25

Meade BD, Kind PD, Ewell JB, McGrath PP, Manclark CR

Abstract

Lymphocytosis promoting factor (LPF) of Bordetella pertussis is a protein toxin which may have a role in the pathogenesis of pertussis. Since macrophages have an important role in the control of respiratory infections, the in vitro effects of LPF on macrophages from C3H/HeN and C3H/HeJ mice and on a murine macrophage-like cell line, RAW264, were examined. LPF inhibited random migration of resident peritoneal macrophages as well as the chemotaxis of peritoneal macrophages and the cell line. Fifty percent inhibition of chemotaxis occurred at 0.2 to 0.3 ng of LPF per ml for the macrophages and at 1 to 2 ng of LPF per ml for the cell line. When LPF was either heated at 80 degrees C for 5 min or premixed with specific antibodies, it failed to inhibit migration. At 20 ng/ml, LPF inhibited chemotaxis by more than 80% and also decreased Fc-mediated phagocytosis by 25 to 35%. At this dose, LPF was not a chemoattractant for murine macrophages and did not reduce macrophage viability, adherence, or opsonized zymosan-stimulated superoxide release. When LPF-treated macrophages were added to tissue culture dishes and then examined microscopically after 4 h, the LPF-treated cells adhered but failed to spread and elongate as well as control macrophages. These data indicate that LPF specifically inhibits macrophage migration in vitro and suggest that a possible role for LPF in pathogenesis is to inhibit migration of macrophages to the site of B. pertussis infection.

MeSH Terms
Animals Bacterial Toxins/immunology Bordetella pertussis/immunology Cell Adhesion Cell Survival Chemotaxis, Leukocyte Macrophage Migration-Inhibitory Factors Macrophages/cytology,immunology Mice Mice, Inbred Strains Pertussis Toxin Phagocytosis Superoxides/metabolism Virulence Factors, Bordetella
Chemicals
Bacterial Toxins Macrophage Migration-Inhibitory Factors Virulence Factors, Bordetella Superoxides Pertussis Toxin
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Meade B D
Kind P D
Ewell J B
McGrath P P
Manclark C R
References (47)
47 references, click to expand
  1. Phagocyte strategy vs. microbial tactics.
    Rev Infect Dis. 1980 Sep-Oct;2(5):817-38 PMID: 7052569
  2. Chemotaxis by mouse macrophage cell lines.
    J Immunol. 1981 Jun;126(6):2194-9 PMID: 7229371
  3. Separation and purification of the hemagglutinins from Bordetella pertussis.
    Infect Immun. 1983 Jul;41(1):313-20 PMID: 6305841
  4. Novel biological property of pertussis toxin: chemotactic activity on human monocytes.
    Infect Immun. 1983 Jul;41(1):420-2 PMID: 6305846
  5. Pertussis toxin. Affinity purification of a new ADP-ribosyltransferase.
    J Biol Chem. 1983 Dec 10;258(23):14647-51 PMID: 6315733
  6. Cyclic AMP affects macrophage migration.
    Nat New Biol. 1972 Aug 9;238(84):176-7 PMID: 4340573
  7. immunoglobulin and histamine-sensitivity response of mice to live Bordetella pertussis.
    Infect Immun. 1973 Jul;8(1):83-90 PMID: 4352456
  8. Structure of critical point dried oncornaviruses.
    Virology. 1973 Oct;55(2):535-40 PMID: 4126410
  9. Extraction and partial purification of the histamine-sensitizing factor of Bordetella pertussis.
    J Immunol. 1974 Jul;113(1):18-26 PMID: 4134061
  10. N-formylmethionyl peptides as chemoattractants for leucocytes.
    Proc Natl Acad Sci U S A. 1975 Mar;72(3):1059-62 PMID: 1093163
  11. Isolation and properties of the leukocytosis- and lymphocytosis-promoting factor of Bordetella pertussis.
    J Exp Med. 1976 Jun 1;143(6):1483-502 PMID: 58054
  12. The beta-adrenergic receptors in pertussis.
    J Trop Med Hyg. 1976 Oct;79(10):213-7 PMID: 189057
  13. Defense mechanisms of the respiratory membrane.
    Am Rev Respir Dis. 1977 Mar;115(3):479-514 PMID: 320925
  14. Biological activities of crystalline pertussigen from Bordetella pertussis.
    Infect Immun. 1981 Sep;33(3):820-6 PMID: 6269999
  15. Effects of cell concentration on chemotactic responsiveness of mouse resident peritoneal macrophages.
    J Reticuloendothel Soc. 1981 Oct;30(4):271-82 PMID: 7310768
  16. The regulatory role of macrophages in antigenic stimulation. Part Two: symbiotic relationship between lymphocytes and macrophages.
    Adv Immunol. 1981;31:1-136 PMID: 6797272
  17. Cyclic nucleotides regulate the morphologic alterations required for chemotaxis in monocytes.
    J Immunol. 1982 Mar;128(3):1192-7 PMID: 6120193
  18. Chemotaxis of purified human monocytes in vitro: lack of accessory cell requirement.
    Infect Immun. 1982 May;36(2):591-7 PMID: 7085073
  19. The effect of Bordetella pertussis lymphocytosis-promoting factor (LPF) on antibody response in mice: its enhancing and suppressive effects.
    Jpn J Med Sci Biol. 1982 Feb;35(1):25-9 PMID: 6285047
  20. Direct modification of the membrane adenylate cyclase system by islet-activating protein due to ADP-ribosylation of a membrane protein.
    Proc Natl Acad Sci U S A. 1982 May;79(10):3129-33 PMID: 6954463
  21. Inhibition of macrophage response to brain injury. A new effect of pertussis vaccine possibly related to histamine-sensitizing factor.
    Am J Pathol. 1972 May;67(2):349-60 PMID: 4553663
  22. The mitogenic effect of the lymphocytosis promoting factor from Bordetella pertussis on human lymphocytes.
    J Clin Invest. 1977 Sep;60(3):683-92 PMID: 197121
  23. Biologic and biochemical activities of continuous macrophage cell lines P388D1 and J774.1.
    J Immunol. 1977 Dec;119(6):2060-6 PMID: 915291
  24. Agents that increase cyclic AMP inhibit accumulation of cGMP and depress human monocyte locomotion.
    J Immunol. 1978 Feb;120(2):492-6 PMID: 202654
  25. Biological properties of islets-activating protein (IAP) purified from the culture medium of Bordetella pertussis.
    J Biochem. 1978 Jan;83(1):305-12 PMID: 203575
  26. Chemotactic activity of lectins in vitro.
    Z Immunitatsforsch Immunobiol. 1978 Mar;154(2):173-85 PMID: 645177
  27. Effects of prostaglandins on the spreading, adhesion and migration of mouse peritoneal macrophages.
    Prostaglandins. 1978 Jul;16(1):39-46 PMID: 704923
  28. Prostaglandin E1 reversibly induces morphological changes in macrophages and inhibits phagocytosis.
    Exp Cell Res. 1979 Mar 15;119(2):365-71 PMID: 570928
  29. Polymorphonuclear leukocyte-inhibitory factor of Bordetella pertussis. I. Extraction and partial purification of phagocytosis- and chemotaxis-inhibitory activities.
    Biken J. 1978 Dec;21(4):121-35 PMID: 224858
  30. A 48-well micro chemotaxis assembly for rapid and accurate measurement of leukocyte migration.
    J Immunol Methods. 1980;33(3):239-47 PMID: 6989919
  31. Leukocyte locomotion and chemotaxis: effects of bacteria and viruses.
    Rev Infect Dis. 1980 Mar-Apr;2(2):293-318 PMID: 6994210
  32. Phagocyte impotence caused by an invasive bacterial adenylate cyclase.
    Science. 1982 Sep 3;217(4563):948-50 PMID: 6287574
  33. Review of the Bureau of Biologic's experience with Limulus amebocyte lysate and endotoxin.
    Prog Clin Biol Res. 1982;93:141-51 PMID: 7122587
  34. Identification of the predominant substrate for ADP-ribosylation by islet activating protein.
    J Biol Chem. 1983 Feb 25;258(4):2072-5 PMID: 6296122
  35. Loss of the inhibitory function of the guanine nucleotide regulatory component of adenylate cyclase due to its ADP ribosylation by islet-activating protein, pertussis toxin, in adipocyte membranes.
    J Biol Chem. 1983 Mar 10;258(5):3319-26 PMID: 6298231
  36. Stimulation and inhibition of adenylyl cyclases mediated by distinct regulatory proteins.
    Nature. 1983 Apr 21;302(5910):706-9 PMID: 6300694
  37. Aerosol infection of mice with Bordetella pertussis.
    Infect Immun. 1980 Jul;29(1):261-6 PMID: 6249758
  38. Bordetella pertussis respiratory tract infection in the mouse: pathophysiological responses.
    J Infect Dis. 1980 Jul;142(1):56-66 PMID: 6249873
  39. The macrophage as an effector cell.
    N Engl J Med. 1980 Sep 11;303(11):622-6 PMID: 6447249
  40. Pertussis toxin: the cause of the harmful effects and prolonged immunity of whooping cough. A hypothesis.
    Rev Infect Dis. 1979 May-Jun;1(3):401-12 PMID: 233166
  41. Slow interaction of islet-activating protein with pancreatic islets during primary culture to cause reversal of alpha-adrenergic inhibition of insulin secretion.
    J Biol Chem. 1980 Oct 25;255(20):9580-8 PMID: 6253447
  42. Calmodulin activates prokaryotic adenylate cyclase.
    Proc Natl Acad Sci U S A. 1980 Jul;77(7):3841-4 PMID: 6253992
  43. Monocyte responsiveness to chemotactic stimuli is a property of a subpopulation of cells that can respond to multiple chemoattractants.
    J Clin Invest. 1981 Jan;67(1):60-8 PMID: 7451658
  44. Polymorphonuclear leukocyte-inhibitory factor of Bordetella pertussis. III. Inhibition of Arthus reaction and peritoneal infiltration of PMN.
    Microbiol Immunol. 1980;24(10):895-905 PMID: 6258031
  45. Inhibition of mononuclear phagocyte elongation, migration, and cellular exudate formation following Bordetella pertussis vaccine administration.
    Proc Soc Exp Biol Med. 1981 Feb;166(2):249-56 PMID: 7208486
  46. Lectin-mediated induction of human neutrophil chemotaxis, chemokinesis, and cap formation.
    Infect Immun. 1980 Aug;29(2):600-8 PMID: 7216429
  47. Bordetella pertussis toxins.
    Pharmacol Ther. 1982;19(1):1-53 PMID: 6304790
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
1984-09-00
Pages
718-25
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC263356
Subset
IM
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