Regulation of airway epithelial cell NF-kappa B-dependent gene expression by protein kinase C delta

Airway epithelial cells synthesize proinflammatory molecules such as IL-8, GM-CSF, RANTES, and ICAM-1, the expression of which is increased in the airways of patients with asthma. We investigated the regulation of these NF-kappa B-dependent genes by the novel protein kinase C (PKC) isoform PKC delta...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:The Journal of immunology (1950) 2003-06, Vol.170 (11), p.5681-5689
Hauptverfasser: Page, Kristen, Li, Jing, Zhou, Limei, Iasvovskaia, Svetlana, Corbit, Kevin C, Soh, Jae-Won, Weinstein, I Bernard, Brasier, Allan R, Lin, Anning, Hershenson, Marc B, Iasvoyskaia, Svetlana
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 5689
container_issue 11
container_start_page 5681
container_title The Journal of immunology (1950)
container_volume 170
creator Page, Kristen
Li, Jing
Zhou, Limei
Iasvovskaia, Svetlana
Corbit, Kevin C
Soh, Jae-Won
Weinstein, I Bernard
Brasier, Allan R
Lin, Anning
Hershenson, Marc B
Iasvoyskaia, Svetlana
description Airway epithelial cells synthesize proinflammatory molecules such as IL-8, GM-CSF, RANTES, and ICAM-1, the expression of which is increased in the airways of patients with asthma. We investigated the regulation of these NF-kappa B-dependent genes by the novel protein kinase C (PKC) isoform PKC delta in 16HBE14o- human airway epithelial cells, focusing on IL-8 expression. Transient transfection with the constitutively active catalytic subunit of PKC delta (PKC delta-CAT), and treatment with bryostatin 1, an activator of PKC delta, each increased transcription from the IL-8 promoter, whereas overexpression of PKC epsilon had minor effects. Expression of a dominant negative PKC delta mutant (PKC delta-KR) or pretreatment of cells with rottlerin, a chemical PKC delta inhibitor, attenuated TNF-alpha- and phorbol ester-induced transcription from the IL-8 promoter. Bryostatin 1 treatment increased IL-8 protein abundance in primary airway epithelial cells. Selective activation of PKC delta by bryostatin also activated NF-kappa B, as evidenced by p65 RelA and p50 NF-kappa B1 binding to DNA, NF-kappa B trans-activation, and I kappa B degradation. The sufficiency of PKC delta to induce NF-kappa B nuclear translocation and binding to DNA was confirmed in a 16HBE14o- cell line inducibly expressing PKC delta-CAT under the tet-off system. Deletion of the NF-kappa B response element severely attenuated PKC delta-induced IL-8 promoter activity. Finally, PKC delta-CAT induced transcription from the GM-CSF, RANTES, and ICAM-1 promoters. Together these data suggest that PKC delta plays a key role in the regulation of airway epithelial cell NF-kappa B-dependent gene expression.
doi_str_mv 10.4049/jimmunol.170.11.5681
format Article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_73310668</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>73310668</sourcerecordid><originalsourceid>FETCH-LOGICAL-c349t-8eaefc04cb0e4d419a15ef5e33bada39348ab25720b3f637fa3b94e1f2648fdd3</originalsourceid><addsrcrecordid>eNpFkE1Lw0AURQdRbK3-A5FZuUt9k5lMkqUWq4IoiK6Hl-RNnTZfZhK0_96UVlzdzT2Xy2HsUsBcgUpv1q6qhrop5yKGuRDzSCfiiE1FFEGgNehjNgUIw0DEOp6wM-_XAKAhVKdsIsI4SlUEU5a_0WoosXdNzRvL0XXfuOXUuv6TSoclz6ks-csy2GDbIr8LCmqpLqju-Ypq4vTTduT9Ds-2vO2anlzNN65GT3zBCyp7PGcnFktPF4ecsY_l_fviMXh-fXha3D4HuVRpHySEZHNQeQakCiVSFBHZiKTMsECZSpVgFkZxCJm0WsYWZZYqEjbUKrFFIWfser873vgayPemcn73H2tqBm9iKQVonYxFtS_mXeN9R9a0nauw2xoBZifX_Mk1o1wjhNnJHbGrw_6QVVT8Qweb8hdY5XmL</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>73310668</pqid></control><display><type>article</type><title>Regulation of airway epithelial cell NF-kappa B-dependent gene expression by protein kinase C delta</title><source>MEDLINE</source><source>Alma/SFX Local Collection</source><source>EZB Electronic Journals Library</source><creator>Page, Kristen ; Li, Jing ; Zhou, Limei ; Iasvovskaia, Svetlana ; Corbit, Kevin C ; Soh, Jae-Won ; Weinstein, I Bernard ; Brasier, Allan R ; Lin, Anning ; Hershenson, Marc B ; Iasvoyskaia, Svetlana</creator><creatorcontrib>Page, Kristen ; Li, Jing ; Zhou, Limei ; Iasvovskaia, Svetlana ; Corbit, Kevin C ; Soh, Jae-Won ; Weinstein, I Bernard ; Brasier, Allan R ; Lin, Anning ; Hershenson, Marc B ; Iasvoyskaia, Svetlana</creatorcontrib><description>Airway epithelial cells synthesize proinflammatory molecules such as IL-8, GM-CSF, RANTES, and ICAM-1, the expression of which is increased in the airways of patients with asthma. We investigated the regulation of these NF-kappa B-dependent genes by the novel protein kinase C (PKC) isoform PKC delta in 16HBE14o- human airway epithelial cells, focusing on IL-8 expression. Transient transfection with the constitutively active catalytic subunit of PKC delta (PKC delta-CAT), and treatment with bryostatin 1, an activator of PKC delta, each increased transcription from the IL-8 promoter, whereas overexpression of PKC epsilon had minor effects. Expression of a dominant negative PKC delta mutant (PKC delta-KR) or pretreatment of cells with rottlerin, a chemical PKC delta inhibitor, attenuated TNF-alpha- and phorbol ester-induced transcription from the IL-8 promoter. Bryostatin 1 treatment increased IL-8 protein abundance in primary airway epithelial cells. Selective activation of PKC delta by bryostatin also activated NF-kappa B, as evidenced by p65 RelA and p50 NF-kappa B1 binding to DNA, NF-kappa B trans-activation, and I kappa B degradation. The sufficiency of PKC delta to induce NF-kappa B nuclear translocation and binding to DNA was confirmed in a 16HBE14o- cell line inducibly expressing PKC delta-CAT under the tet-off system. Deletion of the NF-kappa B response element severely attenuated PKC delta-induced IL-8 promoter activity. Finally, PKC delta-CAT induced transcription from the GM-CSF, RANTES, and ICAM-1 promoters. Together these data suggest that PKC delta plays a key role in the regulation of airway epithelial cell NF-kappa B-dependent gene expression.</description><identifier>ISSN: 0022-1767</identifier><identifier>EISSN: 1550-6606</identifier><identifier>DOI: 10.4049/jimmunol.170.11.5681</identifier><identifier>PMID: 12759450</identifier><language>eng</language><publisher>United States</publisher><subject>Cell Line ; Cells, Cultured ; Chemokine CCL5 - genetics ; Chemokine CCL5 - physiology ; DNA-Binding Proteins - metabolism ; DNA-Binding Proteins - physiology ; Enzyme Activation - genetics ; Gene Expression Regulation - physiology ; Granulocyte-Macrophage Colony-Stimulating Factor - genetics ; Granulocyte-Macrophage Colony-Stimulating Factor - physiology ; Humans ; I-kappa B Kinase ; Intercellular Adhesion Molecule-1 - genetics ; Intercellular Adhesion Molecule-1 - physiology ; Interleukin-8 - biosynthesis ; Interleukin-8 - genetics ; Isoenzymes - biosynthesis ; Isoenzymes - physiology ; NF-kappa B - physiology ; Promoter Regions, Genetic - physiology ; Protein Kinase C - biosynthesis ; Protein Kinase C - physiology ; Protein Kinase C-delta ; Protein-Serine-Threonine Kinases - metabolism ; Protein-Serine-Threonine Kinases - physiology ; Respiratory Mucosa - cytology ; Respiratory Mucosa - enzymology ; Respiratory Mucosa - metabolism ; Respiratory Mucosa - pathology ; Trans-Activators - metabolism ; Trans-Activators - physiology ; Transcription, Genetic</subject><ispartof>The Journal of immunology (1950), 2003-06, Vol.170 (11), p.5681-5689</ispartof><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c349t-8eaefc04cb0e4d419a15ef5e33bada39348ab25720b3f637fa3b94e1f2648fdd3</citedby><cites>FETCH-LOGICAL-c349t-8eaefc04cb0e4d419a15ef5e33bada39348ab25720b3f637fa3b94e1f2648fdd3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/12759450$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Page, Kristen</creatorcontrib><creatorcontrib>Li, Jing</creatorcontrib><creatorcontrib>Zhou, Limei</creatorcontrib><creatorcontrib>Iasvovskaia, Svetlana</creatorcontrib><creatorcontrib>Corbit, Kevin C</creatorcontrib><creatorcontrib>Soh, Jae-Won</creatorcontrib><creatorcontrib>Weinstein, I Bernard</creatorcontrib><creatorcontrib>Brasier, Allan R</creatorcontrib><creatorcontrib>Lin, Anning</creatorcontrib><creatorcontrib>Hershenson, Marc B</creatorcontrib><creatorcontrib>Iasvoyskaia, Svetlana</creatorcontrib><title>Regulation of airway epithelial cell NF-kappa B-dependent gene expression by protein kinase C delta</title><title>The Journal of immunology (1950)</title><addtitle>J Immunol</addtitle><description>Airway epithelial cells synthesize proinflammatory molecules such as IL-8, GM-CSF, RANTES, and ICAM-1, the expression of which is increased in the airways of patients with asthma. We investigated the regulation of these NF-kappa B-dependent genes by the novel protein kinase C (PKC) isoform PKC delta in 16HBE14o- human airway epithelial cells, focusing on IL-8 expression. Transient transfection with the constitutively active catalytic subunit of PKC delta (PKC delta-CAT), and treatment with bryostatin 1, an activator of PKC delta, each increased transcription from the IL-8 promoter, whereas overexpression of PKC epsilon had minor effects. Expression of a dominant negative PKC delta mutant (PKC delta-KR) or pretreatment of cells with rottlerin, a chemical PKC delta inhibitor, attenuated TNF-alpha- and phorbol ester-induced transcription from the IL-8 promoter. Bryostatin 1 treatment increased IL-8 protein abundance in primary airway epithelial cells. Selective activation of PKC delta by bryostatin also activated NF-kappa B, as evidenced by p65 RelA and p50 NF-kappa B1 binding to DNA, NF-kappa B trans-activation, and I kappa B degradation. The sufficiency of PKC delta to induce NF-kappa B nuclear translocation and binding to DNA was confirmed in a 16HBE14o- cell line inducibly expressing PKC delta-CAT under the tet-off system. Deletion of the NF-kappa B response element severely attenuated PKC delta-induced IL-8 promoter activity. Finally, PKC delta-CAT induced transcription from the GM-CSF, RANTES, and ICAM-1 promoters. Together these data suggest that PKC delta plays a key role in the regulation of airway epithelial cell NF-kappa B-dependent gene expression.</description><subject>Cell Line</subject><subject>Cells, Cultured</subject><subject>Chemokine CCL5 - genetics</subject><subject>Chemokine CCL5 - physiology</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>DNA-Binding Proteins - physiology</subject><subject>Enzyme Activation - genetics</subject><subject>Gene Expression Regulation - physiology</subject><subject>Granulocyte-Macrophage Colony-Stimulating Factor - genetics</subject><subject>Granulocyte-Macrophage Colony-Stimulating Factor - physiology</subject><subject>Humans</subject><subject>I-kappa B Kinase</subject><subject>Intercellular Adhesion Molecule-1 - genetics</subject><subject>Intercellular Adhesion Molecule-1 - physiology</subject><subject>Interleukin-8 - biosynthesis</subject><subject>Interleukin-8 - genetics</subject><subject>Isoenzymes - biosynthesis</subject><subject>Isoenzymes - physiology</subject><subject>NF-kappa B - physiology</subject><subject>Promoter Regions, Genetic - physiology</subject><subject>Protein Kinase C - biosynthesis</subject><subject>Protein Kinase C - physiology</subject><subject>Protein Kinase C-delta</subject><subject>Protein-Serine-Threonine Kinases - metabolism</subject><subject>Protein-Serine-Threonine Kinases - physiology</subject><subject>Respiratory Mucosa - cytology</subject><subject>Respiratory Mucosa - enzymology</subject><subject>Respiratory Mucosa - metabolism</subject><subject>Respiratory Mucosa - pathology</subject><subject>Trans-Activators - metabolism</subject><subject>Trans-Activators - physiology</subject><subject>Transcription, Genetic</subject><issn>0022-1767</issn><issn>1550-6606</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2003</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpFkE1Lw0AURQdRbK3-A5FZuUt9k5lMkqUWq4IoiK6Hl-RNnTZfZhK0_96UVlzdzT2Xy2HsUsBcgUpv1q6qhrop5yKGuRDzSCfiiE1FFEGgNehjNgUIw0DEOp6wM-_XAKAhVKdsIsI4SlUEU5a_0WoosXdNzRvL0XXfuOXUuv6TSoclz6ks-csy2GDbIr8LCmqpLqju-Ypq4vTTduT9Ds-2vO2anlzNN65GT3zBCyp7PGcnFktPF4ecsY_l_fviMXh-fXha3D4HuVRpHySEZHNQeQakCiVSFBHZiKTMsECZSpVgFkZxCJm0WsYWZZYqEjbUKrFFIWfser873vgayPemcn73H2tqBm9iKQVonYxFtS_mXeN9R9a0nauw2xoBZifX_Mk1o1wjhNnJHbGrw_6QVVT8Qweb8hdY5XmL</recordid><startdate>20030601</startdate><enddate>20030601</enddate><creator>Page, Kristen</creator><creator>Li, Jing</creator><creator>Zhou, Limei</creator><creator>Iasvovskaia, Svetlana</creator><creator>Corbit, Kevin C</creator><creator>Soh, Jae-Won</creator><creator>Weinstein, I Bernard</creator><creator>Brasier, Allan R</creator><creator>Lin, Anning</creator><creator>Hershenson, Marc B</creator><creator>Iasvoyskaia, Svetlana</creator><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20030601</creationdate><title>Regulation of airway epithelial cell NF-kappa B-dependent gene expression by protein kinase C delta</title><author>Page, Kristen ; Li, Jing ; Zhou, Limei ; Iasvovskaia, Svetlana ; Corbit, Kevin C ; Soh, Jae-Won ; Weinstein, I Bernard ; Brasier, Allan R ; Lin, Anning ; Hershenson, Marc B ; Iasvoyskaia, Svetlana</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c349t-8eaefc04cb0e4d419a15ef5e33bada39348ab25720b3f637fa3b94e1f2648fdd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2003</creationdate><topic>Cell Line</topic><topic>Cells, Cultured</topic><topic>Chemokine CCL5 - genetics</topic><topic>Chemokine CCL5 - physiology</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>DNA-Binding Proteins - physiology</topic><topic>Enzyme Activation - genetics</topic><topic>Gene Expression Regulation - physiology</topic><topic>Granulocyte-Macrophage Colony-Stimulating Factor - genetics</topic><topic>Granulocyte-Macrophage Colony-Stimulating Factor - physiology</topic><topic>Humans</topic><topic>I-kappa B Kinase</topic><topic>Intercellular Adhesion Molecule-1 - genetics</topic><topic>Intercellular Adhesion Molecule-1 - physiology</topic><topic>Interleukin-8 - biosynthesis</topic><topic>Interleukin-8 - genetics</topic><topic>Isoenzymes - biosynthesis</topic><topic>Isoenzymes - physiology</topic><topic>NF-kappa B - physiology</topic><topic>Promoter Regions, Genetic - physiology</topic><topic>Protein Kinase C - biosynthesis</topic><topic>Protein Kinase C - physiology</topic><topic>Protein Kinase C-delta</topic><topic>Protein-Serine-Threonine Kinases - metabolism</topic><topic>Protein-Serine-Threonine Kinases - physiology</topic><topic>Respiratory Mucosa - cytology</topic><topic>Respiratory Mucosa - enzymology</topic><topic>Respiratory Mucosa - metabolism</topic><topic>Respiratory Mucosa - pathology</topic><topic>Trans-Activators - metabolism</topic><topic>Trans-Activators - physiology</topic><topic>Transcription, Genetic</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Page, Kristen</creatorcontrib><creatorcontrib>Li, Jing</creatorcontrib><creatorcontrib>Zhou, Limei</creatorcontrib><creatorcontrib>Iasvovskaia, Svetlana</creatorcontrib><creatorcontrib>Corbit, Kevin C</creatorcontrib><creatorcontrib>Soh, Jae-Won</creatorcontrib><creatorcontrib>Weinstein, I Bernard</creatorcontrib><creatorcontrib>Brasier, Allan R</creatorcontrib><creatorcontrib>Lin, Anning</creatorcontrib><creatorcontrib>Hershenson, Marc B</creatorcontrib><creatorcontrib>Iasvoyskaia, Svetlana</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>The Journal of immunology (1950)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Page, Kristen</au><au>Li, Jing</au><au>Zhou, Limei</au><au>Iasvovskaia, Svetlana</au><au>Corbit, Kevin C</au><au>Soh, Jae-Won</au><au>Weinstein, I Bernard</au><au>Brasier, Allan R</au><au>Lin, Anning</au><au>Hershenson, Marc B</au><au>Iasvoyskaia, Svetlana</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Regulation of airway epithelial cell NF-kappa B-dependent gene expression by protein kinase C delta</atitle><jtitle>The Journal of immunology (1950)</jtitle><addtitle>J Immunol</addtitle><date>2003-06-01</date><risdate>2003</risdate><volume>170</volume><issue>11</issue><spage>5681</spage><epage>5689</epage><pages>5681-5689</pages><issn>0022-1767</issn><eissn>1550-6606</eissn><abstract>Airway epithelial cells synthesize proinflammatory molecules such as IL-8, GM-CSF, RANTES, and ICAM-1, the expression of which is increased in the airways of patients with asthma. We investigated the regulation of these NF-kappa B-dependent genes by the novel protein kinase C (PKC) isoform PKC delta in 16HBE14o- human airway epithelial cells, focusing on IL-8 expression. Transient transfection with the constitutively active catalytic subunit of PKC delta (PKC delta-CAT), and treatment with bryostatin 1, an activator of PKC delta, each increased transcription from the IL-8 promoter, whereas overexpression of PKC epsilon had minor effects. Expression of a dominant negative PKC delta mutant (PKC delta-KR) or pretreatment of cells with rottlerin, a chemical PKC delta inhibitor, attenuated TNF-alpha- and phorbol ester-induced transcription from the IL-8 promoter. Bryostatin 1 treatment increased IL-8 protein abundance in primary airway epithelial cells. Selective activation of PKC delta by bryostatin also activated NF-kappa B, as evidenced by p65 RelA and p50 NF-kappa B1 binding to DNA, NF-kappa B trans-activation, and I kappa B degradation. The sufficiency of PKC delta to induce NF-kappa B nuclear translocation and binding to DNA was confirmed in a 16HBE14o- cell line inducibly expressing PKC delta-CAT under the tet-off system. Deletion of the NF-kappa B response element severely attenuated PKC delta-induced IL-8 promoter activity. Finally, PKC delta-CAT induced transcription from the GM-CSF, RANTES, and ICAM-1 promoters. Together these data suggest that PKC delta plays a key role in the regulation of airway epithelial cell NF-kappa B-dependent gene expression.</abstract><cop>United States</cop><pmid>12759450</pmid><doi>10.4049/jimmunol.170.11.5681</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0022-1767
ispartof The Journal of immunology (1950), 2003-06, Vol.170 (11), p.5681-5689
issn 0022-1767
1550-6606
language eng
recordid cdi_proquest_miscellaneous_73310668
source MEDLINE; Alma/SFX Local Collection; EZB Electronic Journals Library
subjects Cell Line
Cells, Cultured
Chemokine CCL5 - genetics
Chemokine CCL5 - physiology
DNA-Binding Proteins - metabolism
DNA-Binding Proteins - physiology
Enzyme Activation - genetics
Gene Expression Regulation - physiology
Granulocyte-Macrophage Colony-Stimulating Factor - genetics
Granulocyte-Macrophage Colony-Stimulating Factor - physiology
Humans
I-kappa B Kinase
Intercellular Adhesion Molecule-1 - genetics
Intercellular Adhesion Molecule-1 - physiology
Interleukin-8 - biosynthesis
Interleukin-8 - genetics
Isoenzymes - biosynthesis
Isoenzymes - physiology
NF-kappa B - physiology
Promoter Regions, Genetic - physiology
Protein Kinase C - biosynthesis
Protein Kinase C - physiology
Protein Kinase C-delta
Protein-Serine-Threonine Kinases - metabolism
Protein-Serine-Threonine Kinases - physiology
Respiratory Mucosa - cytology
Respiratory Mucosa - enzymology
Respiratory Mucosa - metabolism
Respiratory Mucosa - pathology
Trans-Activators - metabolism
Trans-Activators - physiology
Transcription, Genetic
title Regulation of airway epithelial cell NF-kappa B-dependent gene expression by protein kinase C delta
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-03T19%3A56%3A20IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Regulation%20of%20airway%20epithelial%20cell%20NF-kappa%20B-dependent%20gene%20expression%20by%20protein%20kinase%20C%20delta&rft.jtitle=The%20Journal%20of%20immunology%20(1950)&rft.au=Page,%20Kristen&rft.date=2003-06-01&rft.volume=170&rft.issue=11&rft.spage=5681&rft.epage=5689&rft.pages=5681-5689&rft.issn=0022-1767&rft.eissn=1550-6606&rft_id=info:doi/10.4049/jimmunol.170.11.5681&rft_dat=%3Cproquest_cross%3E73310668%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=73310668&rft_id=info:pmid/12759450&rfr_iscdi=true