DNA released from neutrophil extracellular traps (NETs) activates pancreatic stellate cells and enhances pancreatic tumor growth
Identifieur interne : 000908 ( Main/Exploration ); précédent : 000907; suivant : 000909DNA released from neutrophil extracellular traps (NETs) activates pancreatic stellate cells and enhances pancreatic tumor growth
Auteurs : Jennifer L. Miller-Ocuin [États-Unis] ; Xiaoyan Liang [États-Unis] ; Brian A. Boone [États-Unis] ; W. Reed Doerfler [États-Unis] ; Aatur D. Singhi [États-Unis] ; Daolin Tang [États-Unis] ; Rui Kang [États-Unis] ; Michael T. Lotze [États-Unis] ; Herbert J. Zeh [États-Unis]Source :
- Oncoimmunology [ 2162-4011 ] ; 2019.
Abstract
Neutrophil extracellular trap (NET) formation results in the expulsion of granulocyte proteins and DNA into the extracellular space. This process is mediated by the enzyme peptidyl arginine deiminase 4 (PADI4) and translocation of elastase to the nucleus. NET formation, marked by increased levels of extracellular DNA, promotes pancreatic cancer proliferation and metastasis. Mice deficient in Padi4 demonstrate decreased pancreatic tumor growth, associated with a reduction in circulating extracellular DNA levels, diminished pancreatic stromal activation and improved survival in murine orthotopic pancreatic adenocarcinoma. Transplantation of Padi4−/− bone marrow into genetically engineered mice with Kras driven pancreatic adenocarcinoma (Pdx1-Cre:KrasG12D/+, KC mice) limits the frequency of invasive cancers when compared with syngeneic controls. DNA from neutrophils activates pancreatic stellate cells that form dense, fibrous stroma which can promote and enable tumor proliferation. DNase treatment diminishes murine tumor growth and stromal activation to reverse the effect of NETs within the tumor microenvironment. Furthermore, deletion of the receptor for advanced glycation end products (RAGE) in pancreatic stellate cells abrogates the effects of DNA in promoting stellate cell proliferation and decreases tumor growth. Circulating neutrophil-derived DNA correlates with the stage in patients with pancreatic ductal adenocarcinoma, confirming the role of NETs in human pancreatic cancer. These findings support further investigation into targeting of NETs, PADI4 and extracellular DNA as a potential treatment strategy in patients with pancreatic cancer.
Url:
DOI: 10.1080/2162402X.2019.1605822
PubMed: 31428515
PubMed Central: 6685506
Affiliations:
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Miller-Ocuin</name><affiliation wicri:level="1"><nlm:aff id="AFF0001"><institution>Department of Surgery, University of Pittsburgh School of Medicine</institution>, Pittsburgh, PA,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Liang, Xiaoyan" sort="Liang, Xiaoyan" uniqKey="Liang X" first="Xiaoyan" last="Liang">Xiaoyan Liang</name><affiliation wicri:level="1"><nlm:aff id="AFF0001"><institution>Department of Surgery, University of Pittsburgh School of Medicine</institution>, Pittsburgh, PA,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Boone, Brian A" sort="Boone, Brian A" uniqKey="Boone B" first="Brian A." last="Boone">Brian A. 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Reed Doerfler</name><affiliation wicri:level="1"><nlm:aff id="AFF0001"><institution>Department of Surgery, University of Pittsburgh School of Medicine</institution>, Pittsburgh, PA,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Singhi, Aatur D" sort="Singhi, Aatur D" uniqKey="Singhi A" first="Aatur D." last="Singhi">Aatur D. Singhi</name><affiliation wicri:level="1"><nlm:aff id="AFF0003"><institution>Department of Pathology, University of Pittsburgh School of Medicine</institution>, Pittsburgh, PA,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Tang, Daolin" sort="Tang, Daolin" uniqKey="Tang D" first="Daolin" last="Tang">Daolin Tang</name><affiliation wicri:level="1"><nlm:aff id="AFF0001"><institution>Department of Surgery, University of Pittsburgh School of Medicine</institution>, Pittsburgh, PA,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="AFF0004"><institution>Department of Surgery, UT Southwestern Medical Center</institution>, Dallas, TX,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Kang, Rui" sort="Kang, Rui" uniqKey="Kang R" first="Rui" last="Kang">Rui Kang</name><affiliation wicri:level="1"><nlm:aff id="AFF0001"><institution>Department of Surgery, University of Pittsburgh School of Medicine</institution>, Pittsburgh, PA,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="AFF0004"><institution>Department of Surgery, UT Southwestern Medical Center</institution>, Dallas, TX,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Lotze, Michael T" sort="Lotze, Michael T" uniqKey="Lotze M" first="Michael T." last="Lotze">Michael T. Lotze</name><affiliation wicri:level="1"><nlm:aff id="AFF0001"><institution>Department of Surgery, University of Pittsburgh School of Medicine</institution>, Pittsburgh, PA,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="AFF0005"><institution>Department of Immunology, University of Pittsburgh School of Medicine</institution>, Pittsburgh, PA,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="AFF0006"><institution>Department of Bioengineering, University of Pittsburgh School of Medicine</institution>, Pittsburgh, PA,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Zeh, Herbert J" sort="Zeh, Herbert J" uniqKey="Zeh H" first="Herbert J." last="Zeh">Herbert J. Zeh</name><affiliation wicri:level="1"><nlm:aff id="AFF0001"><institution>Department of Surgery, University of Pittsburgh School of Medicine</institution>, Pittsburgh, PA,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="AFF0004"><institution>Department of Surgery, UT Southwestern Medical Center</institution>, Dallas, TX,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">Oncoimmunology</title><idno type="ISSN">2162-4011</idno><idno type="eISSN">2162-402X</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>ABSTRACT</title><p>Neutrophil extracellular trap (NET) formation results in the expulsion of granulocyte proteins and DNA into the extracellular space. This process is mediated by the enzyme peptidyl arginine deiminase 4 (PADI4) and translocation of elastase to the nucleus. NET formation, marked by increased levels of extracellular DNA, promotes pancreatic cancer proliferation and metastasis. Mice deficient in Padi4 demonstrate decreased pancreatic tumor growth, associated with a reduction in circulating extracellular DNA levels, diminished pancreatic stromal activation and improved survival in murine orthotopic pancreatic adenocarcinoma. Transplantation of Padi4<sup>−/−</sup> bone marrow into genetically engineered mice with Kras driven pancreatic adenocarcinoma (Pdx1-Cre:Kras<sup>G12D/+</sup>, KC mice) limits the frequency of invasive cancers when compared with syngeneic controls. DNA from neutrophils activates pancreatic stellate cells that form dense, fibrous stroma which can promote and enable tumor proliferation. DNase treatment diminishes murine tumor growth and stromal activation to reverse the effect of NETs within the tumor microenvironment. Furthermore, deletion of the receptor for advanced glycation end products (RAGE) in pancreatic stellate cells abrogates the effects of DNA in promoting stellate cell proliferation and decreases tumor growth. Circulating neutrophil-derived DNA correlates with the stage in patients with pancreatic ductal adenocarcinoma, confirming the role of NETs in human pancreatic cancer. These findings support further investigation into targeting of NETs, PADI4 and extracellular DNA as a potential treatment strategy in patients with pancreatic cancer.</p><p><bold>Trial Registration</bold>: This study reports correlative data from a clinical trial registered with clinicaltrials.gov, NCT01978184 (November 7, 2013).</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Brinkmann, V" uniqKey="Brinkmann V">V Brinkmann</name></author><author><name sortKey="Reichard, U" uniqKey="Reichard U">U Reichard</name></author><author><name sortKey="Goosmann, C" uniqKey="Goosmann C">C Goosmann</name></author><author><name sortKey="Fauler, B" uniqKey="Fauler B">B Fauler</name></author><author><name sortKey="Uhlemann, Y" uniqKey="Uhlemann Y">Y Uhlemann</name></author><author><name sortKey="Weiss, Ds" uniqKey="Weiss D">DS Weiss</name></author><author><name sortKey="Weinrauch, Y" uniqKey="Weinrauch Y">Y Weinrauch</name></author><author><name sortKey="Zychlinsky, A" uniqKey="Zychlinsky A">A. 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Miller-Ocuin</name></noRegion><name sortKey="Boone, Brian A" sort="Boone, Brian A" uniqKey="Boone B" first="Brian A." last="Boone">Brian A. Boone</name><name sortKey="Boone, Brian A" sort="Boone, Brian A" uniqKey="Boone B" first="Brian A." last="Boone">Brian A. Boone</name><name sortKey="Doerfler, W Reed" sort="Doerfler, W Reed" uniqKey="Doerfler W" first="W. Reed" last="Doerfler">W. Reed Doerfler</name><name sortKey="Kang, Rui" sort="Kang, Rui" uniqKey="Kang R" first="Rui" last="Kang">Rui Kang</name><name sortKey="Kang, Rui" sort="Kang, Rui" uniqKey="Kang R" first="Rui" last="Kang">Rui Kang</name><name sortKey="Liang, Xiaoyan" sort="Liang, Xiaoyan" uniqKey="Liang X" first="Xiaoyan" last="Liang">Xiaoyan Liang</name><name sortKey="Lotze, Michael T" sort="Lotze, Michael T" uniqKey="Lotze M" first="Michael T." last="Lotze">Michael T. Lotze</name><name sortKey="Lotze, Michael T" sort="Lotze, Michael T" uniqKey="Lotze M" first="Michael T." last="Lotze">Michael T. Lotze</name><name sortKey="Lotze, Michael T" sort="Lotze, Michael T" uniqKey="Lotze M" first="Michael T." last="Lotze">Michael T. Lotze</name><name sortKey="Singhi, Aatur D" sort="Singhi, Aatur D" uniqKey="Singhi A" first="Aatur D." last="Singhi">Aatur D. Singhi</name><name sortKey="Tang, Daolin" sort="Tang, Daolin" uniqKey="Tang D" first="Daolin" last="Tang">Daolin Tang</name><name sortKey="Tang, Daolin" sort="Tang, Daolin" uniqKey="Tang D" first="Daolin" last="Tang">Daolin Tang</name><name sortKey="Zeh, Herbert J" sort="Zeh, Herbert J" uniqKey="Zeh H" first="Herbert J." last="Zeh">Herbert J. Zeh</name><name sortKey="Zeh, Herbert J" sort="Zeh, Herbert J" uniqKey="Zeh H" first="Herbert J." last="Zeh">Herbert J. Zeh</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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