Home LiteratureArticle Details
PMID: 16903868 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Enhanced neutrophil motility by granulocyte colony-stimulating factor: the role of extracellular signal-regulated kinase and phosphatidylinositol 3-kinase.

Immunology ·Vol. 119 ·No. 3 ·2006-11-00 ·Pages 393-403

Nakamae-Akahori M, Kato T, Masuda S, Sakamoto E, Kutsuna H, Hato F, Nishizawa Y, Hino M, Kitagawa S

Abstract

The effect of granulocyte colony-stimulating factor (G-CSF) on human neutrophil motility was studied using videomicroscopy. Stimulation of neutrophils with G-CSF resulted in enhanced motility with morphological change and increased adherence. Enhanced neutrophil motility was detected within 3-5 min after G-CSF stimulation, reached a maximum at 10 min, and was sustained for approximately 35 min. The maximum migration rate was 84.4 +/- 2.9 microm/5 min. A study using the Boyden chamber method revealed that G-CSF-stimulated neutrophils exhibited random migration but not chemotaxis. Enhanced neutrophil motility and morphological change were inhibited by MEK [mitogen-activated protein kinase (MAPK)/extracellular signal-regulated kinase (ERK) kinase] inhibitors (PD98059 and U0126), and a phosphatidylinositol 3-kinase (PI3K) inhibitor (wortmannin), but not by a p38 MAPK inhibitor (SB203580). These findings are consistent with the fact that G-CSF selectively activates MEK/ERK and PI3K, but not p38, in neutrophils. MEK/ERK activation was associated with G-CSF-induced redistribution of F-actin and phosphorylated myosin light chain. Enhanced neutrophil motility was observed even in the presence of neutralizing anti-CD18 antibody, which prevented cell adherence. These findings indicate that G-CSF induces human neutrophil migration via activation of MEK/ERK and PI3K.

MeSH Terms
Adult Cell Movement/immunology Cells, Cultured Chemotaxis, Leukocyte/immunology Extracellular Signal-Regulated MAP Kinases/immunology Granulocyte Colony-Stimulating Factor/immunology Humans Microscopy, Video Myosin Light Chains/metabolism Neutrophil Activation/immunology Neutrophils/immunology Phosphatidylinositol 3-Kinases/immunology Phosphorylation Signal Transduction/immunology
Chemicals
Myosin Light Chains Granulocyte Colony-Stimulating Factor Phosphatidylinositol 3-Kinases Extracellular Signal-Regulated MAP Kinases
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Nakamae-Akahori Mika
Department of Physiology, Osaka City University Graduate School of Medicine, Abenoku, Osaka, Japan.
Kato Takayuki
Masuda Sayuri
Sakamoto Erina
Kutsuna Haruo
Hato Fumihiko
Nishizawa Yoshiki
Hino Masayuki
Kitagawa Seiichi
References (35)
35 references, click to expand
  1. Function of PI3Kgamma in thymocyte development, T cell activation, and neutrophil migration.
    Science. 2000 Feb 11;287(5455):1040-6 PMID: 10669416
  2. Recombinant human granulocyte colony-stimulating factor as an activator of human granulocytes: potentiation of responses triggered by receptor-mediated agonists and stimulation of C3bi receptor expression and adherence.
    Blood. 1989 Nov 1;74(6):2144-9 PMID: 2553162
  3. Expression of the G-CSF receptor on hematopoietic progenitor cells is not required for their mobilization by G-CSF.
    Blood. 2000 May 15;95(10):3025-31 PMID: 10807765
  4. Activation of Rhoa and ROCK are essential for detachment of migrating leukocytes.
    Mol Biol Cell. 2001 Jul;12(7):2137-45 PMID: 11452009
  5. Temporal and quantitative regulation of mitogen-activated protein kinase (MAPK) modulates cell motility and invasion.
    Oncogene. 2001 Jul 12;20(31):4209-18 PMID: 11464287
  6. Abnormal migration phenotype of mitogen-activated protein kinase-activated protein kinase 2-/- neutrophils in Zigmond chambers containing formyl-methionyl-leucyl-phenylalanine gradients.
    J Immunol. 2001 Oct 1;167(7):3953-61 PMID: 11564814
  7. In vivo activation of human neutrophil functions by administration of recombinant human granulocyte colony-stimulating factor in patients with malignant lymphoma.
    Blood. 1989 Dec;74(8):2743-8 PMID: 2479431
  8. An increase or a decrease in myosin II phosphorylation inhibits macrophage motility.
    J Cell Biol. 1991 Jul;114(2):277-83 PMID: 2071674
  9. Granulocyte colony-stimulating factor and its receptor.
    Blood. 1991 Dec 1;78(11):2791-808 PMID: 1720034
  10. Myosin light chain phosphorylation does not increase during yeast phagocytosis by macrophages.
    J Biol Chem. 1993 Aug 15;268(23):16883-6 PMID: 8349578
  11. The role of granulocyte-macrophage and granulocyte colony-stimulating factors in neutrophil transendothelial migration: comparison with interleukin-8.
    Exp Hematol. 1994 Mar;22(3):329-34 PMID: 7509293
  12. Granulocyte colony-stimulating factor (G-CSF) increases neutrophil migration across vascular endothelium independent of an effect on adhesion: comparison with granulocyte-macrophage colony-stimulating factor (GM-CSF).
    Br J Haematol. 1996 Jul;94(1):40-7 PMID: 8757506
  13. Interleukin 8-stimulated phosphatidylinositol-3-kinase activity regulates the migration of human neutrophils independent of extracellular signal-regulated kinase and p38 mitogen-activated protein kinases.
    Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3052-7 PMID: 9096344
  14. Random migration of polymorphonuclear leukocytes induced by GM-CSF involving a signal transduction pathway different from that of fMLP.
    J Leukoc Biol. 1997 Apr;61(4):500-6 PMID: 9103237
  15. Regulation of cell motility by mitogen-activated protein kinase.
    J Cell Biol. 1997 Apr 21;137(2):481-92 PMID: 9128257
  16. p38 mitogen-activated protein kinase activation is required for human neutrophil function triggered by TNF-alpha or FMLP stimulation.
    J Immunol. 1998 Feb 15;160(4):1982-9 PMID: 9469462
  17. Importance of MEK in neutrophil microbicidal responsiveness.
    J Immunol. 1998 Jan 1;160(1):434-43 PMID: 9552001
  18. Cytokine-specific activation of distinct mitogen-activated protein kinase subtype cascades in human neutrophils stimulated by granulocyte colony-stimulating factor, granulocyte-macrophage colony-stimulating factor, and tumor necrosis factor-alpha.
    Blood. 1999 Jan 1;93(1):341-9 PMID: 9864179
  19. C-reactive protein inhibits chemotactic peptide-induced p38 mitogen-activated protein kinase activity and human neutrophil movement.
    J Biol Chem. 1999 Jun 18;274(25):17968-74 PMID: 10364245
  20. Role of ERK and JNK pathways in regulating cell motility and matrix metalloproteinase 9 production in growth factor-stimulated human epidermal keratinocytes.
    J Cell Physiol. 1999 Aug;180(2):271-84 PMID: 10395297
  21. Regulation of cell contraction and membrane ruffling by distinct signals in migratory cells.
    J Cell Biol. 1999 Sep 6;146(5):1107-16 PMID: 10477763
  22. Activation of human neutrophils by granulocyte colony-stimulating factor, granulocyte-macrophage colony-stimulating factor, and tumor necrosis factor alpha: role of phosphatidylinositol 3-kinase.
    Int J Hematol. 2004 Dec;80(5):421-7 PMID: 15646653
  23. Regulation of tumor cell motility by ERK mitogen-activated protein kinases.
    Ann N Y Acad Sci. 2004 Dec;1030:208-18 PMID: 15659800
  24. Regulation of myosin II during cytokinesis in higher eukaryotes.
    Trends Cell Biol. 2005 Jul;15(7):371-7 PMID: 15935670
  25. Neutrophils lacking phosphoinositide 3-kinase gamma show loss of directionality during N-formyl-Met-Leu-Phe-induced chemotaxis.
    Proc Natl Acad Sci U S A. 2002 Mar 19;99(6):3603-8 PMID: 11904423
  26. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4.
    Nat Immunol. 2002 Jul;3(7):687-94 PMID: 12068293
  27. G-CSF is an essential regulator of neutrophil trafficking from the bone marrow to the blood.
    Immunity. 2002 Oct;17(4):413-23 PMID: 12387736
  28. Granulocyte colony-stimulating factor promotes adhesion of neutrophils.
    Am J Physiol Cell Physiol. 2003 Jan;284(1):C103-10 PMID: 12388113
  29. Expression of the inhibitor of apoptosis (IAP) family members in human neutrophils: up-regulation of cIAP2 by granulocyte colony-stimulating factor and overexpression of cIAP2 in chronic neutrophilic leukemia.
    Blood. 2003 Feb 1;101(3):1164-71 PMID: 12393423
  30. Essential role of phosphoinositide 3-kinase delta in neutrophil directional movement.
    J Immunol. 2003 Mar 1;170(5):2647-54 PMID: 12594293
  31. Actin reorganization and morphological changes in human neutrophils stimulated by TNF, GM-CSF, and G-CSF: the role of MAP kinases.
    Am J Physiol Cell Physiol. 2004 Jan;286(1):C55-64 PMID: 12954601
  32. Membrane type 1 matrix metalloproteinase regulates collagen-dependent mitogen-activated protein/extracellular signal-related kinase activation and cell migration.
    Cancer Res. 2004 Feb 1;64(3):1044-9 PMID: 14871836
  33. Activation of phosphatidylinositol 3-kinase and extracellular signal-regulated kinase is required for glial cell line-derived neurotrophic factor-induced migration and invasion of pancreatic carcinoma cells.
    Cancer Res. 2004 Aug 1;64(15):5291-300 PMID: 15289335
  34. Chemotactic activity of recombinant human granulocyte colony-stimulating factor.
    Blood. 1988 Nov;72(5):1456-60 PMID: 2460152
  35. Regulation of polymorphonuclear leukocyte phagocytosis by myosin light chain kinase after activation of mitogen-activated protein kinase.
    Blood. 2000 Apr 1;95(7):2407-12 PMID: 10733514
Article Info
Journal
Immunology
Abbr.
Immunology
ISSN
0019-2805
Published
2006-11-00
Epub
2006-00-14
Pages
393-403
Language
English
Region
England
NLM ID
0374672
PMCID
PMC1819568
Subset
IM
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