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PMID: 10545501 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Integrating conflicting chemotactic signals. The role of memory in leukocyte navigation.

The Journal of cell biology ·Vol. 147 ·No. 3 ·1999-11-01 ·Pages 577-88

Foxman EF, Kunkel EJ, Butcher EC

Abstract

Leukocytes navigate through complex chemoattractant arrays, and in so doing, they must migrate from one chemoattractant source to another. By evaluating directional persistence and chemotaxis during neutrophil migration under agarose, we show that cells migrating away from a local chemoattractant, against a gradient, display true chemotaxis to distant agonists, often behaving as if the local gradient were without effect. We describe two interrelated properties of migrating cells that allow this to occur. First, migrating leukocytes can integrate competing chemoattractant signals, responding as if to the vector sum of the orienting signals present. Second, migrating cells display memory of their recent environment: cells' perception of the relative strength of orienting signals is influenced by their history, so that cells prioritize newly arising or newly encountered attractants. We propose that this cellular memory, by promoting sequential chemotaxis to one attractant after another, is in fact responsible for the integration of competitive orienting signals over time, and allows combinations of chemoattractants to guide leukocytes in a step-by-step fashion to their destinations within tissues.

MeSH Terms
Adaptation, Physiological/drug effects Chemotactic Factors/pharmacology Chemotaxis, Leukocyte Environment Humans Interleukin-8/pharmacology Leukotriene B4/pharmacology Models, Biological Neutrophils/cytology,drug effects,physiology Signal Transduction/drug effects Time Factors Video Recording
Chemicals
Chemotactic Factors Interleukin-8 Leukotriene B4
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Foxman E F
Laboratory of Immunology and Vascular Biology, Stanford University Medical School, Stanford, California 94305, USA. [email protected]
Kunkel E J
Butcher E C
References (43)
43 references, click to expand
  1. Chemokines and renal disease.
    Am J Kidney Dis. 1995 Dec;26(6):982-94 PMID: 7503075
  2. Adaptation of human neutrophil responsiveness to the chemoattractant N-formylmethionylleucylphenylalanine. Heterogeneity and/or negative cooperative interaction of receptors.
    J Biol Chem. 1982 Jun 10;257(11):6280-6 PMID: 6281264
  3. Eosinophil recruitment to the lung in a murine model of allergic inflammation. The role of T cells, chemokines, and adhesion receptors.
    J Clin Invest. 1996 Nov 15;98(10):2332-45 PMID: 8941651
  4. A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen.
    Cell. 1996 Dec 13;87(6):1037-47 PMID: 8978608
  5. Chemoattractant cross-desensitization of the human neutrophil IL-8 receptor involves receptor internalization and differential receptor subtype regulation.
    J Immunol. 1997 Feb 1;158(3):1361-9 PMID: 9013980
  6. C-X-C and C-C chemokines are expressed in the cerebrospinal fluid in bacterial meningitis and mediate chemotactic activity on peripheral blood-derived polymorphonuclear and mononuclear cells in vitro.
    J Immunol. 1997 Feb 15;158(4):1956-64 PMID: 9029138
  7. Synchronous synthesis of alpha- and beta-chemokines by cells of diverse lineage in the central nervous system of mice with relapses of chronic experimental autoimmune encephalomyelitis.
    Am J Pathol. 1997 Feb;150(2):617-30 PMID: 9033275
  8. Contrasting responses to multiple chemotactic stimuli in transendothelial migration: heterologous desensitization in neutrophils and augmentation of migration in eosinophils.
    J Immunol. 1997 Mar 1;158(5):2340-9 PMID: 9036983
  9. Human chemokines: an update.
    Annu Rev Immunol. 1997;15:675-705 PMID: 9143704
  10. Impaired host defense, hematopoiesis, granulomatous inflammation and type 1-type 2 cytokine balance in mice lacking CC chemokine receptor 1.
    J Exp Med. 1997 Jun 2;185(11):1959-68 PMID: 9166425
  11. Impaired inflammatory responses in the reverse arthus reaction through genetic deletion of the C5a receptor.
    J Exp Med. 1997 Aug 29;186(5):749-56 PMID: 9271590
  12. Defects in macrophage recruitment and host defense in mice lacking the CCR2 chemokine receptor.
    J Exp Med. 1997 Nov 17;186(10):1757-62 PMID: 9362535
  13. Chemoattractant receptor cross talk as a regulatory mechanism in leukocyte adhesion and migration.
    Eur J Immunol. 1997 Oct;27(10):2571-8 PMID: 9368612
  14. Multistep navigation and the combinatorial control of leukocyte chemotaxis.
    J Cell Biol. 1997 Dec 1;139(5):1349-60 PMID: 9382879
  15. Chemotaxis in a lymphocyte cell line transfected with C-C chemokine receptor 2B: evidence that directed migration is mediated by betagamma dimers released by activation of Galphai-coupled receptors.
    Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14495-9 PMID: 9405641
  16. Chemokines--chemotactic cytokines that mediate inflammation.
    N Engl J Med. 1998 Feb 12;338(7):436-45 PMID: 9459648
  17. Galphai is not required for chemotaxis mediated by Gi-coupled receptors.
    J Biol Chem. 1999 Jan 29;274(5):2824-8 PMID: 9915816
  18. Recent advances in chemokines and chemokine receptors.
    Crit Rev Immunol. 1999;19(1):1-47 PMID: 9987599
  19. Chemotaxis in leukocytes.
    Physiol Rev. 1946 Jul;26(3):319-36 PMID: 20993553
  20. Leukocyte locomotion and chemotaxis. New methods for evaluation, and demonstration of a cell-derived chemotactic factor.
    J Exp Med. 1973 Feb 1;137(2):387-410 PMID: 4568301
  21. Mechanisms of sensing chemical gradients by polymorphonuclear leukocytes.
    Nature. 1974 May 31;249(456):450-2 PMID: 4834231
  22. Chemotaxis under agarose: a new and simple method for measuring chemotaxis and spontaneous migration of human polymorphonuclear leukocytes and monocytes.
    J Immunol. 1975 Dec;115(6):1650-6 PMID: 1102606
  23. Heterogeneity of human polymorphonuclear leukocyte receptors for leukotriene B4. Identification of a subset of high affinity receptors that transduce the chemotactic response.
    J Exp Med. 1984 Apr 1;159(4):1027-41 PMID: 6323613
  24. Behaviour of neutrophil leucocytes in uniform concentrations of chemotactic factors: contraction waves, cell polarity and persistence.
    J Cell Sci. 1985 Mar;74:75-93 PMID: 3161901
  25. Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors.
    J Cell Biol. 1977 Nov;75(2 Pt 1):606-16 PMID: 264125
  26. Videoanalysis of chemokinesis: characterization of speed, persistence and orientation in an agarose assay.
    Ann Clin Lab Sci. 1987 Nov-Dec;17(6):389-97 PMID: 3688822
  27. Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium.
    Annu Rev Cell Biol. 1988;4:649-86 PMID: 2848555
  28. Chemoattractant-stimulated GTPase activity is decreased on membranes from polymorphonuclear leukocytes incubated in chemoattractant.
    J Biol Chem. 1989 Jan 5;264(1):190-6 PMID: 2535838
  29. Interleukin 8 (monocyte-derived neutrophil chemotactic factor) dynamically regulates its own receptor expression on human neutrophils.
    J Biol Chem. 1990 Jan 5;265(1):183-9 PMID: 2403554
  30. C5a reduces formyl peptide-induced actin polymerization and phosphatidylinositol(3,4,5)trisphosphate formation, but not phosphatidylinositol (4,5) bisphosphate hydrolysis and superoxide production, in human neutrophils.
    J Immunol. 1992 Jul 15;149(2):609-14 PMID: 1320642
  31. Constitutive and stimulated MCP-1, GRO alpha, beta, and gamma expression in human airway epithelium and bronchoalveolar macrophages.
    Am J Physiol. 1994 Mar;266(3 Pt 1):L278-86 PMID: 8166297
  32. Cross-desensitization of receptors for peptide chemoattractants. Characterization of a new form of leukocyte regulation.
    J Immunol. 1994 Oct 1;153(7):3267-75 PMID: 8089498
  33. Fibrin regulates neutrophil migration in response to interleukin 8, leukotriene B4, tumor necrosis factor, and formyl-methionyl-leucyl-phenylalanine.
    J Exp Med. 1995 May 1;181(5):1763-72 PMID: 7722453
  34. Cytokine networks in the skin.
    J Invest Dermatol. 1995 Jul;105(1 Suppl):20S-24S PMID: 7615993
  35. Regulation of the expression of IL-8 receptor A/B by IL-8: possible functions of each receptor.
    J Immunol. 1995 Sep 1;155(5):2587-94 PMID: 7650389
  36. Requirement of MIP-1 alpha for an inflammatory response to viral infection.
    Science. 1995 Sep 15;269(5230):1583-5 PMID: 7667639
  37. Differential expression of GRO-alpha and IL-8 mRNA in psoriasis: a model for neutrophil migration and accumulation in vivo.
    J Invest Dermatol. 1996 Nov;107(5):778-82 PMID: 8875965
  38. A visual analysis of chemotactic and chemokinetic locomotion of human neutrophil leucocytes. Use of a new chemotaxis assay with Candida albicans as gradient source.
    Exp Cell Res. 1978 Jan;111(1):191-203 PMID: 340239
  39. Sensory adaptation of leukocytes to chemotactic peptides.
    J Cell Biol. 1979 Aug;82(2):517-27 PMID: 479314
  40. Chemotactic peptide receptor modulation in polymorphonuclear leukocytes.
    J Cell Biol. 1980 Jun;85(3):703-11 PMID: 7391138
  41. Cell polarity: an examination of its behavioral expression and its consequences for polymorphonuclear leukocyte chemotaxis.
    J Cell Biol. 1981 Jun;89(3):585-92 PMID: 7251666
  42. Kinetic analysis of chemotactic peptide receptor modulation.
    J Cell Biol. 1982 Jan;92(1):34-43 PMID: 6276415
  43. Cross-desensitization of chemoattractant receptors occurs at multiple levels. Evidence for a role for inhibition of phospholipase C activity.
    J Biol Chem. 1995 Nov 17;270(46):27829-33 PMID: 7499254
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1999-11-01
Pages
577-88
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2151176
Subset
IM
Grants
NIAID NIH HHS · 5T32-AI07290 · United States
NIGMS NIH HHS · GM07365 · United States
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