DOI: 10.1126/science.271.5251.981. Role of Rho in Chemoattractant-Activated Leukocyte Adhesion Through Integrins

Role of Rho in Chemoattractant-Activated Leukocyte Adhesion Through Integrins

10.1126/science.271.5251.981

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Heterotrimeric guanine nucleotide binding protein (G protein)-linked receptors of the chemoattractant subfamily can trigger adhesion through leukocyte integrins, and in this role they are thought to regulate immune cell-cell interactions and trafficking. In lymphoid cells transfected with formyl peptide or interleukin-8 receptors, agonist stimulation activated nucleotide exchange on the small guanosine triphosphate-binding protein RhoA in seconds. Inactivation of Rho by C3 transferase exoenzyme blocked agonist-induced lymphocyte α4β1 adhesion to vascular cell adhesion molecule-1 and neutrophil β2 integrin adhesion to fibrinogen. These findings suggest that Rho participates in signaling from chemoattractant receptors to trigger rapid adhesion in leukocytes.

Bibliography

Laudanna, C., Campbell, J. J., & Butcher, E. C. (1996). Role of Rho in Chemoattractant-Activated Leukocyte Adhesion Through Integrins. Science, 271(5251), 981â983.

Authors 3

Carlo Laudanna (first)
James J. Campbell (additional)
Eugene C. Butcher (additional)

References 23 Referenced 410

AKTORIES K, THE RHO GENE-PRODUCT EXPRESSED IN ESCHERICHIA-COLI IS A SUBSTRATE OF BOTULINUM ADP-RIBOSYLTRANSFERASE-C3, BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS 158, 209 (1989). (10.1016/S0006-291X(89)80199-8) / BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS / THE RHO GENE-PRODUCT EXPRESSED IN ESCHERICHIA-COLI IS A SUBSTRATE OF BOTULINUM ADP-RIBOSYLTRANSFERASE-C3 by AKTORIES K (1989)
BARGATZE F. R., RAPID G-PROTEIN-REGULATED ACTIVATION EVENT INVOLVED IN LYMPHOCYTE BINDING TO HIGH ENDOTHELIAL VENULES, JOURNAL OF EXPERIMENTAL MEDICINE 178, 367 (1993). (10.1084/jem.178.1.367) / JOURNAL OF EXPERIMENTAL MEDICINE / RAPID G-PROTEIN-REGULATED ACTIVATION EVENT INVOLVED IN LYMPHOCYTE BINDING TO HIGH ENDOTHELIAL VENULES by BARGATZE F. R. (1993)
BRUNS F. R., INHIBITION OF PROTEIN-KINASE-C BY CALPHOSTIN-C IS LIGHT-DEPENDENT, BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS 176, 288 (1991). (10.1016/0006-291X(91)90922-T) / BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS / INHIBITION OF PROTEIN-KINASE-C BY CALPHOSTIN-C IS LIGHT-DEPENDENT by BRUNS F. R. (1991)
CAMPBELL J. J. unpublished data.
CLARKE MSF, SYRINGE LOADING INTRODUCES MACROMOLECULES INTO LIVING MAMMALIAN-CELL CYTOSOL, JOURNAL OF CELL SCIENCE 102, 533 (1992). (10.1242/jcs.102.3.533) / JOURNAL OF CELL SCIENCE / SYRINGE LOADING INTRODUCES MACROMOLECULES INTO LIVING MAMMALIAN-CELL CYTOSOL by CLARKE MSF (1992)
COCKCROFT S, THE RECEPTORS FOR ATP AND FMETLEUPHE ARE INDEPENDENTLY COUPLED TO PHOSPHOLIPASE-C AND PHOSPHOLIPASE-A2 VIA G-PROTEIN(S) - RELATIONSHIP BETWEEN PHOSPHOLIPASE-C AND PHOSPHOLIPASE-A2 ACTIVATION AND EXOCYTOSIS IN HL60 CELLS AND HUMAN-NEUTROPHILS, BIOCHEMICAL JOURNAL 263, 715 (1989). (10.1042/bj2630715) / BIOCHEMICAL JOURNAL / THE RECEPTORS FOR ATP AND FMETLEUPHE ARE INDEPENDENTLY COUPLED TO PHOSPHOLIPASE-C AND PHOSPHOLIPASE-A2 VIA G-PROTEIN(S) - RELATIONSHIP BETWEEN PHOSPHOLIPASE-C AND PHOSPHOLIPASE-A2 ACTIVATION AND EXOCYTOSIS IN HL60 CELLS AND HUMAN-NEUTROPHILS by COCKCROFT S (1989)
DOWNWARD J, STIMULATION OF P21RAS UPON T-CELL ACTIVATION, NATURE 346, 719 (1990). (10.1038/346719a0) / NATURE / STIMULATION OF P21RAS UPON T-CELL ACTIVATION by DOWNWARD J (1990)
FURTH E. M., MONOCLONAL-ANTIBODIES TO THE P21 PRODUCTS OF THE TRANSFORMING GENE OF HARVEY MURINE SARCOMA-VIRUS AND OF THE CELLULAR RAS GENE FAMILY, JOURNAL OF VIROLOGY 43, 294 (1982). (10.1128/jvi.43.1.294-304.1982) / JOURNAL OF VIROLOGY / MONOCLONAL-ANTIBODIES TO THE P21 PRODUCTS OF THE TRANSFORMING GENE OF HARVEY MURINE SARCOMA-VIRUS AND OF THE CELLULAR RAS GENE FAMILY by FURTH E. M. (1982)
GERARD C, THE PRO-INFLAMMATORY 7-TRANSMEMBRANE SEGMENT RECEPTORS OF THE LEUKOCYTE, CURRENT OPINION IN IMMUNOLOGY 6, 140 (1994). (10.1016/0952-7915(94)90045-0) / CURRENT OPINION IN IMMUNOLOGY / THE PRO-INFLAMMATORY 7-TRANSMEMBRANE SEGMENT RECEPTORS OF THE LEUKOCYTE by GERARD C (1994)
HALL A, SMALL GTP-BINDING PROTEINS AND THE REGULATION OF THE ACTIN CYTOSKELETON, ANNUAL REVIEW OF CELL BIOLOGY 10, 31 (1994). (10.1146/annurev.cb.10.110194.000335) / ANNUAL REVIEW OF CELL BIOLOGY / SMALL GTP-BINDING PROTEINS AND THE REGULATION OF THE ACTIN CYTOSKELETON by HALL A (1994)
HONDA S, LIGAND-INDUCED ADHESION TO ACTIVATED ENDOTHELIUM AND TO VASCULAR CELL-ADHESION MOLECULE-1 IN LYMPHOCYTES TRANSFECTED WITH THE N-FORMYL PEPTIDE RECEPTOR, JOURNAL OF IMMUNOLOGY 152, 4026 (1994). (10.4049/jimmunol.152.8.4026) / JOURNAL OF IMMUNOLOGY / LIGAND-INDUCED ADHESION TO ACTIVATED ENDOTHELIUM AND TO VASCULAR CELL-ADHESION MOLECULE-1 IN LYMPHOCYTES TRANSFECTED WITH THE N-FORMYL PEPTIDE RECEPTOR by HONDA S (1994)
KOBAYASHI E, CALPHOSTIN C (UCN-1028C), A NOVEL MICROBIAL COMPOUND, IS A HIGHLY POTENT AND SPECIFIC INHIBITOR OF PROTEIN KINASE-C, BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS 159, 548 (1989). (10.1016/0006-291X(89)90028-4) / BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS / CALPHOSTIN C (UCN-1028C), A NOVEL MICROBIAL COMPOUND, IS A HIGHLY POTENT AND SPECIFIC INHIBITOR OF PROTEIN KINASE-C by KOBAYASHI E (1989)
LAUDANNA C unpublished data.
LEY K, INTRAVENOUS INTERLEUKIN-8 INHIBITS GRANULOCYTE EMIGRATION FROM RABBIT MESENTERIC VENULES WITHOUT ALTERING L-SELECTIN EXPRESSION OR LEUKOCYTE ROLLING, JOURNAL OF IMMUNOLOGY 151, 6347 (1993). (10.4049/jimmunol.151.11.6347) / JOURNAL OF IMMUNOLOGY / INTRAVENOUS INTERLEUKIN-8 INHIBITS GRANULOCYTE EMIGRATION FROM RABBIT MESENTERIC VENULES WITHOUT ALTERING L-SELECTIN EXPRESSION OR LEUKOCYTE ROLLING by LEY K (1993)
10.1126/science.1604323
NIELSON P. C., EFFECTS OF SELECTIVE PHOSPHODIESTERASE INHIBITORS ON THE POLYMORPHONUCLEAR LEUKOCYTE RESPIRATORY BURST, JOURNAL OF ALLERGY AND CLINICAL IMMUNOLOGY 86, 801 (1990). (10.1016/S0091-6749(05)80186-1) / JOURNAL OF ALLERGY AND CLINICAL IMMUNOLOGY / EFFECTS OF SELECTIVE PHOSPHODIESTERASE INHIBITORS ON THE POLYMORPHONUCLEAR LEUKOCYTE RESPIRATORY BURST by NIELSON P. C. (1990)
PATERSON F. H., MICROINJECTION OF RECOMBINANT-P21RHO INDUCES RAPID CHANGES IN CELL MORPHOLOGY, JOURNAL OF CELL BIOLOGY 111, 1001 (1990). (10.1083/jcb.111.3.1001) / JOURNAL OF CELL BIOLOGY / MICROINJECTION OF RECOMBINANT-P21RHO INDUCES RAPID CHANGES IN CELL MORPHOLOGY by PATERSON F. H. (1990)
10.1016/0092-8674(92)90163-7
ROSSI F, PHOSPHATIDIC-ACID AND NOT DIACYLGLYCEROL GENERATED BY PHOSPHOLIPASE-D IS FUNCTIONALLY LINKED TO THE ACTIVATION OF THE NADPH OXIDASE BY FMLP IN HUMAN NEUTROPHILS, BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS 168, 320 (1990). (10.1016/0006-291X(90)91711-Z) / BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS / PHOSPHATIDIC-ACID AND NOT DIACYLGLYCEROL GENERATED BY PHOSPHOLIPASE-D IS FUNCTIONALLY LINKED TO THE ACTIVATION OF THE NADPH OXIDASE BY FMLP IN HUMAN NEUTROPHILS by ROSSI F (1990)
SEKINE A, ASPARAGINE RESIDUE IN THE RHO GENE-PRODUCT IS THE MODIFICATION SITE FOR BOTULINUM ADP-RIBOSYLTRANSFERASE, JOURNAL OF BIOLOGICAL CHEMISTRY 264, 8602 (1989). (10.1016/S0021-9258(18)81834-8) / JOURNAL OF BIOLOGICAL CHEMISTRY / ASPARAGINE RESIDUE IN THE RHO GENE-PRODUCT IS THE MODIFICATION SITE FOR BOTULINUM ADP-RIBOSYLTRANSFERASE by SEKINE A (1989)
STASIA J. M., ADP-RIBOSYLATION OF A SMALL SIZE GTP-BINDING PROTEIN IN BOVINE NEUTROPHILS BY THE C3 EXOENZYME OF CLOSTRIDIUM-BOTULINUM AND EFFECT ON THE CELL MOTILITY, BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS 180, 615 (1991). (10.1016/S0006-291X(05)81110-6) / BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS / ADP-RIBOSYLATION OF A SMALL SIZE GTP-BINDING PROTEIN IN BOVINE NEUTROPHILS BY THE C3 EXOENZYME OF CLOSTRIDIUM-BOTULINUM AND EFFECT ON THE CELL MOTILITY by STASIA J. M. (1991)
TOMINAGA T, INHIBITION OF PMA-INDUCED, LFA-1-DEPENDENT LYMPHOCYTE AGGREGATION BY ADP RIBOSYLATION OF THE SMALL MOLECULAR-WEIGHT GTP BINDING-PROTEIN, RHO, JOURNAL OF CELL BIOLOGY 120, 1529 (1993). (10.1083/jcb.120.6.1529) / JOURNAL OF CELL BIOLOGY / INHIBITION OF PMA-INDUCED, LFA-1-DEPENDENT LYMPHOCYTE AGGREGATION BY ADP RIBOSYLATION OF THE SMALL MOLECULAR-WEIGHT GTP BINDING-PROTEIN, RHO by TOMINAGA T (1993)
VONANDRIAN H. U., L-SELECTIN FUNCTION IS REQUIRED FOR BETA-2-INTEGRIN-MEDIATED NEUTROPHIL ADHESION AT PHYSIOLOGICAL SHEAR RATES INVIVO, AMERICAN JOURNAL OF PHYSIOLOGY 263, 1034 (1992). / AMERICAN JOURNAL OF PHYSIOLOGY / L-SELECTIN FUNCTION IS REQUIRED FOR BETA-2-INTEGRIN-MEDIATED NEUTROPHIL ADHESION AT PHYSIOLOGICAL SHEAR RATES INVIVO by VONANDRIAN H. U. (1992)

Dates

Type	When
Created	18 years, 10 months ago (Oct. 27, 2006, 10:30 a.m.)
Deposited	1 year, 7 months ago (Jan. 12, 2024, 11:07 a.m.)
Indexed	1 month, 4 weeks ago (July 7, 2025, 1:25 a.m.)
Issued	29 years, 6 months ago (Feb. 16, 1996)
Published	29 years, 6 months ago (Feb. 16, 1996)
Published Print	29 years, 6 months ago (Feb. 16, 1996)

Funders 0

None

BibTeX

@article{Laudanna_1996, title={Role of Rho in Chemoattractant-Activated Leukocyte Adhesion Through Integrins}, volume={271}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.271.5251.981}, DOI={10.1126/science.271.5251.981}, number={5251}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Laudanna, Carlo and Campbell, James J. and Butcher, Eugene C.}, year={1996}, month=feb, pages={981–983} }

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      "article-title": "SYRINGE LOADING INTRODUCES MACROMOLECULES INTO LIVING MAMMALIAN-CELL CYTOSOL",
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      "volume": "168",
      "author": "ROSSI F",
      "year": "1990",
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    },
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      "key": "e_1_2_1_21_2",
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      "DOI": "10.1016/S0021-9258(18)81834-8",
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      "volume": "264",
      "author": "SEKINE A",
      "year": "1989",
      "unstructured": "SEKINE A, ASPARAGINE RESIDUE IN THE RHO GENE-PRODUCT IS THE MODIFICATION SITE FOR BOTULINUM ADP-RIBOSYLTRANSFERASE, JOURNAL OF BIOLOGICAL CHEMISTRY 264, 8602 (1989).",
      "journal-title": "JOURNAL OF BIOLOGICAL CHEMISTRY"
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      "volume": "180",
      "author": "STASIA J. M.",
      "year": "1991",
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      "volume": "120",
      "author": "TOMINAGA T",
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      "author": "VONANDRIAN H. U.",
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