Tissue Factor Induced by Epithelial-Mesenchymal Transition Triggers a Procoagulant State That Drives Metastasis of Circulating Tumor Cells.
Identifieur interne : 001B89 ( PubMed/Corpus ); précédent : 001B88; suivant : 001B90Tissue Factor Induced by Epithelial-Mesenchymal Transition Triggers a Procoagulant State That Drives Metastasis of Circulating Tumor Cells.
Auteurs : Morgane Bourcy ; Meggy Suarez-Carmona ; Justine Lambert ; Marie-Emilie Francart ; Hélène Schroeder ; Céline Delierneux ; Nicolas Skrypek ; Erik W. Thompson ; Guy Jérusalem ; Geert Berx ; Marc Thiry ; Silvia Blacher ; Brett G. Hollier ; Agnès Noël ; Cécile Oury ; Myriam Polette ; Christine GillesSource :
- Cancer research [ 1538-7445 ] ; 2016.
English descriptors
- KwdEn :
- MESH :
- chemical , biosynthesis : Thromboplastin.
- pathology : Neoplastic Cells, Circulating.
- chemical , physiology : Zinc Finger E-box-Binding Homeobox 1.
- secondary : Lung Neoplasms.
- Animals, Blood Coagulation, Cell Line, Tumor, Epithelial-Mesenchymal Transition, Female, Humans, Mice, Mice, Inbred BALB C.
Abstract
Epithelial-mesenchymal transition (EMT) is prominent in circulating tumor cells (CTC), but how it influences metastatic spread in this setting is obscure. Insofar as blood provides a specific microenvironment for tumor cells, we explored a potential link between EMT and coagulation that may provide EMT-positive CTCs with enhanced colonizing properties. Here we report that EMT induces tissue factor (TF), a major cell-associated initiator of coagulation and related procoagulant properties in the blood. TF blockade by antibody or shRNA diminished the procoagulant activity of EMT-positive cells, confirming a functional role for TF in these processes. Silencing the EMT transcription factor ZEB1 inhibited both EMT-associated TF expression and coagulant activity, further strengthening the link between EMT and coagulation. Accordingly, EMT-positive cells exhibited a higher persistance/survival in the lungs of mice colonized after intravenous injection, a feature diminished by TF or ZEB1 silencing. In tumor cells with limited metastatic capability, enforcing expression of the EMT transcription factor Snail increased TF, coagulant properties, and early metastasis. Clinically, we identified a subpopulation of CTC expressing vimentin and TF in the blood of metastatic breast cancer patients consistent with our observations. Overall, our findings define a novel EMT-TF regulatory axis that triggers local activation of coagulation pathways to support metastatic colonization of EMT-positive CTCs. Cancer Res; 76(14); 4270-82. ©2016 AACR.
DOI: 10.1158/0008-5472.CAN-15-2263
PubMed: 27221703
Links to Exploration step
pubmed:27221703Le document en format XML
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Department of Biomedical Molecular Biology, Cancer Research Institute Ghent (CRIG), Ghent University, Ghent, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Thompson, Erik W" sort="Thompson, Erik W" uniqKey="Thompson E" first="Erik W" last="Thompson">Erik W. 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Department of Biomedical Molecular Biology, Cancer Research Institute Ghent (CRIG), Ghent University, Ghent, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Thiry, Marc" sort="Thiry, Marc" uniqKey="Thiry M" first="Marc" last="Thiry">Marc Thiry</name><affiliation><nlm:affiliation>GIGA-Neurosciences, Unit of Cell and Tissue Biology, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Blacher, Silvia" sort="Blacher, Silvia" uniqKey="Blacher S" first="Silvia" last="Blacher">Silvia Blacher</name><affiliation><nlm:affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Hollier, Brett G" sort="Hollier, Brett G" uniqKey="Hollier B" first="Brett G" last="Hollier">Brett G. Hollier</name><affiliation><nlm:affiliation>Australian Prostate Cancer Research Centre - Queensland, Institute of Health and Biomedical Innovation, School of Biomedical Sciences, Queensland University of Technology, Princess Alexandra Hospital, Translational Research Institute, Brisbane, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Noel, Agnes" sort="Noel, Agnes" uniqKey="Noel A" first="Agnès" last="Noël">Agnès Noël</name><affiliation><nlm:affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Oury, Cecile" sort="Oury, Cecile" uniqKey="Oury C" first="Cécile" last="Oury">Cécile Oury</name><affiliation><nlm:affiliation>GIGA-Cardiovascular Sciences, Laboratory of Thrombosis and Hemostasis, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Polette, Myriam" sort="Polette, Myriam" uniqKey="Polette M" first="Myriam" last="Polette">Myriam Polette</name><affiliation><nlm:affiliation>INSERM UMR-S 903, CHU, Biopathology Laboratory, University of Reims, Reims, France.</nlm:affiliation></affiliation></author><author><name sortKey="Gilles, Christine" sort="Gilles, Christine" uniqKey="Gilles C" first="Christine" last="Gilles">Christine Gilles</name><affiliation><nlm:affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium. cgilles@ulg.ac.be.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2016">2016</date><idno type="RBID">pubmed:27221703</idno><idno type="pmid">27221703</idno><idno type="doi">10.1158/0008-5472.CAN-15-2263</idno><idno type="wicri:Area/PubMed/Corpus">001B89</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">001B89</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Tissue Factor Induced by Epithelial-Mesenchymal Transition Triggers a Procoagulant State That Drives Metastasis of Circulating Tumor Cells.</title><author><name sortKey="Bourcy, Morgane" sort="Bourcy, Morgane" uniqKey="Bourcy M" first="Morgane" last="Bourcy">Morgane Bourcy</name><affiliation><nlm:affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Suarez Carmona, Meggy" sort="Suarez Carmona, Meggy" uniqKey="Suarez Carmona M" first="Meggy" last="Suarez-Carmona">Meggy Suarez-Carmona</name><affiliation><nlm:affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Lambert, Justine" sort="Lambert, Justine" uniqKey="Lambert J" first="Justine" last="Lambert">Justine Lambert</name><affiliation><nlm:affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Francart, Marie Emilie" sort="Francart, Marie Emilie" uniqKey="Francart M" first="Marie-Emilie" last="Francart">Marie-Emilie Francart</name><affiliation><nlm:affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Schroeder, Helene" sort="Schroeder, Helene" uniqKey="Schroeder H" first="Hélène" last="Schroeder">Hélène Schroeder</name><affiliation><nlm:affiliation>CHU, Department of Medical Oncology, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Delierneux, Celine" sort="Delierneux, Celine" uniqKey="Delierneux C" first="Céline" last="Delierneux">Céline Delierneux</name><affiliation><nlm:affiliation>GIGA-Cardiovascular Sciences, Laboratory of Thrombosis and Hemostasis, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Skrypek, Nicolas" sort="Skrypek, Nicolas" uniqKey="Skrypek N" first="Nicolas" last="Skrypek">Nicolas Skrypek</name><affiliation><nlm:affiliation>Unit of Molecular and Cellular Oncology Lab, Inflammation Research Center, VIB, Ghent, Belgium. Department of Biomedical Molecular Biology, Cancer Research Institute Ghent (CRIG), Ghent University, Ghent, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Thompson, Erik W" sort="Thompson, Erik W" uniqKey="Thompson E" first="Erik W" last="Thompson">Erik W. Thompson</name><affiliation><nlm:affiliation>Institute of Health and Biomedical Innovation and School of Biomedical Sciences Translational Research Institute, Queensland University of Technology, Brisbane, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Jerusalem, Guy" sort="Jerusalem, Guy" uniqKey="Jerusalem G" first="Guy" last="Jérusalem">Guy Jérusalem</name><affiliation><nlm:affiliation>CHU, Department of Medical Oncology, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Berx, Geert" sort="Berx, Geert" uniqKey="Berx G" first="Geert" last="Berx">Geert Berx</name><affiliation><nlm:affiliation>Unit of Molecular and Cellular Oncology Lab, Inflammation Research Center, VIB, Ghent, Belgium. Department of Biomedical Molecular Biology, Cancer Research Institute Ghent (CRIG), Ghent University, Ghent, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Thiry, Marc" sort="Thiry, Marc" uniqKey="Thiry M" first="Marc" last="Thiry">Marc Thiry</name><affiliation><nlm:affiliation>GIGA-Neurosciences, Unit of Cell and Tissue Biology, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Blacher, Silvia" sort="Blacher, Silvia" uniqKey="Blacher S" first="Silvia" last="Blacher">Silvia Blacher</name><affiliation><nlm:affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Hollier, Brett G" sort="Hollier, Brett G" uniqKey="Hollier B" first="Brett G" last="Hollier">Brett G. Hollier</name><affiliation><nlm:affiliation>Australian Prostate Cancer Research Centre - Queensland, Institute of Health and Biomedical Innovation, School of Biomedical Sciences, Queensland University of Technology, Princess Alexandra Hospital, Translational Research Institute, Brisbane, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Noel, Agnes" sort="Noel, Agnes" uniqKey="Noel A" first="Agnès" last="Noël">Agnès Noël</name><affiliation><nlm:affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Oury, Cecile" sort="Oury, Cecile" uniqKey="Oury C" first="Cécile" last="Oury">Cécile Oury</name><affiliation><nlm:affiliation>GIGA-Cardiovascular Sciences, Laboratory of Thrombosis and Hemostasis, University of Liège, Liège, Belgium.</nlm:affiliation></affiliation></author><author><name sortKey="Polette, Myriam" sort="Polette, Myriam" uniqKey="Polette M" first="Myriam" last="Polette">Myriam Polette</name><affiliation><nlm:affiliation>INSERM UMR-S 903, CHU, Biopathology Laboratory, University of Reims, Reims, France.</nlm:affiliation></affiliation></author><author><name sortKey="Gilles, Christine" sort="Gilles, Christine" uniqKey="Gilles C" first="Christine" last="Gilles">Christine Gilles</name><affiliation><nlm:affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium. cgilles@ulg.ac.be.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Cancer research</title><idno type="eISSN">1538-7445</idno><imprint><date when="2016" type="published">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Blood Coagulation</term><term>Cell Line, Tumor</term><term>Epithelial-Mesenchymal Transition</term><term>Female</term><term>Humans</term><term>Lung Neoplasms (secondary)</term><term>Mice</term><term>Mice, Inbred BALB C</term><term>Neoplastic Cells, Circulating (pathology)</term><term>Thromboplastin (biosynthesis)</term><term>Zinc Finger E-box-Binding Homeobox 1 (physiology)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="biosynthesis" xml:lang="en"><term>Thromboplastin</term></keywords><keywords scheme="MESH" qualifier="pathology" xml:lang="en"><term>Neoplastic Cells, Circulating</term></keywords><keywords scheme="MESH" type="chemical" qualifier="physiology" xml:lang="en"><term>Zinc Finger E-box-Binding Homeobox 1</term></keywords><keywords scheme="MESH" qualifier="secondary" xml:lang="en"><term>Lung Neoplasms</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Blood Coagulation</term><term>Cell Line, Tumor</term><term>Epithelial-Mesenchymal Transition</term><term>Female</term><term>Humans</term><term>Mice</term><term>Mice, Inbred BALB C</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Epithelial-mesenchymal transition (EMT) is prominent in circulating tumor cells (CTC), but how it influences metastatic spread in this setting is obscure. Insofar as blood provides a specific microenvironment for tumor cells, we explored a potential link between EMT and coagulation that may provide EMT-positive CTCs with enhanced colonizing properties. Here we report that EMT induces tissue factor (TF), a major cell-associated initiator of coagulation and related procoagulant properties in the blood. TF blockade by antibody or shRNA diminished the procoagulant activity of EMT-positive cells, confirming a functional role for TF in these processes. Silencing the EMT transcription factor ZEB1 inhibited both EMT-associated TF expression and coagulant activity, further strengthening the link between EMT and coagulation. Accordingly, EMT-positive cells exhibited a higher persistance/survival in the lungs of mice colonized after intravenous injection, a feature diminished by TF or ZEB1 silencing. In tumor cells with limited metastatic capability, enforcing expression of the EMT transcription factor Snail increased TF, coagulant properties, and early metastasis. Clinically, we identified a subpopulation of CTC expressing vimentin and TF in the blood of metastatic breast cancer patients consistent with our observations. Overall, our findings define a novel EMT-TF regulatory axis that triggers local activation of coagulation pathways to support metastatic colonization of EMT-positive CTCs. Cancer Res; 76(14); 4270-82. ©2016 AACR.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">27221703</PMID><DateCreated><Year>2016</Year><Month>09</Month><Day>22</Day></DateCreated><DateCompleted><Year>2017</Year><Month>07</Month><Day>17</Day></DateCompleted><DateRevised><Year>2017</Year><Month>10</Month><Day>30</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1538-7445</ISSN><JournalIssue CitedMedium="Internet"><Volume>76</Volume><Issue>14</Issue><PubDate><Year>2016</Year><Month>07</Month><Day>15</Day></PubDate></JournalIssue><Title>Cancer research</Title><ISOAbbreviation>Cancer Res.</ISOAbbreviation></Journal><ArticleTitle>Tissue Factor Induced by Epithelial-Mesenchymal Transition Triggers a Procoagulant State That Drives Metastasis of Circulating Tumor Cells.</ArticleTitle><Pagination><MedlinePgn>4270-82</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1158/0008-5472.CAN-15-2263</ELocationID><Abstract><AbstractText>Epithelial-mesenchymal transition (EMT) is prominent in circulating tumor cells (CTC), but how it influences metastatic spread in this setting is obscure. Insofar as blood provides a specific microenvironment for tumor cells, we explored a potential link between EMT and coagulation that may provide EMT-positive CTCs with enhanced colonizing properties. Here we report that EMT induces tissue factor (TF), a major cell-associated initiator of coagulation and related procoagulant properties in the blood. TF blockade by antibody or shRNA diminished the procoagulant activity of EMT-positive cells, confirming a functional role for TF in these processes. Silencing the EMT transcription factor ZEB1 inhibited both EMT-associated TF expression and coagulant activity, further strengthening the link between EMT and coagulation. Accordingly, EMT-positive cells exhibited a higher persistance/survival in the lungs of mice colonized after intravenous injection, a feature diminished by TF or ZEB1 silencing. In tumor cells with limited metastatic capability, enforcing expression of the EMT transcription factor Snail increased TF, coagulant properties, and early metastasis. Clinically, we identified a subpopulation of CTC expressing vimentin and TF in the blood of metastatic breast cancer patients consistent with our observations. Overall, our findings define a novel EMT-TF regulatory axis that triggers local activation of coagulation pathways to support metastatic colonization of EMT-positive CTCs. Cancer Res; 76(14); 4270-82. ©2016 AACR.</AbstractText><CopyrightInformation>©2016 American Association for Cancer Research.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Bourcy</LastName><ForeName>Morgane</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Suarez-Carmona</LastName><ForeName>Meggy</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lambert</LastName><ForeName>Justine</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Francart</LastName><ForeName>Marie-Emilie</ForeName><Initials>ME</Initials><AffiliationInfo><Affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schroeder</LastName><ForeName>Hélène</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>CHU, Department of Medical Oncology, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Delierneux</LastName><ForeName>Céline</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>GIGA-Cardiovascular Sciences, Laboratory of Thrombosis and Hemostasis, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Skrypek</LastName><ForeName>Nicolas</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Unit of Molecular and Cellular Oncology Lab, Inflammation Research Center, VIB, Ghent, Belgium. Department of Biomedical Molecular Biology, Cancer Research Institute Ghent (CRIG), Ghent University, Ghent, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Thompson</LastName><ForeName>Erik W</ForeName><Initials>EW</Initials><AffiliationInfo><Affiliation>Institute of Health and Biomedical Innovation and School of Biomedical Sciences Translational Research Institute, Queensland University of Technology, Brisbane, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jérusalem</LastName><ForeName>Guy</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>CHU, Department of Medical Oncology, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Berx</LastName><ForeName>Geert</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Unit of Molecular and Cellular Oncology Lab, Inflammation Research Center, VIB, Ghent, Belgium. Department of Biomedical Molecular Biology, Cancer Research Institute Ghent (CRIG), Ghent University, Ghent, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Thiry</LastName><ForeName>Marc</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>GIGA-Neurosciences, Unit of Cell and Tissue Biology, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Blacher</LastName><ForeName>Silvia</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hollier</LastName><ForeName>Brett G</ForeName><Initials>BG</Initials><AffiliationInfo><Affiliation>Australian Prostate Cancer Research Centre - Queensland, Institute of Health and Biomedical Innovation, School of Biomedical Sciences, Queensland University of Technology, Princess Alexandra Hospital, Translational Research Institute, Brisbane, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Noël</LastName><ForeName>Agnès</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Oury</LastName><ForeName>Cécile</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>GIGA-Cardiovascular Sciences, Laboratory of Thrombosis and Hemostasis, University of Liège, Liège, Belgium.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Polette</LastName><ForeName>Myriam</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>INSERM UMR-S 903, CHU, Biopathology Laboratory, University of Reims, Reims, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gilles</LastName><ForeName>Christine</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>GIGA-Cancer, Laboratory of Tumor and Development Biology, University of Liège, Liège, Belgium. cgilles@ulg.ac.be.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2016</Year><Month>05</Month><Day>24</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Cancer Res</MedlineTA><NlmUniqueID>2984705R</NlmUniqueID><ISSNLinking>0008-5472</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C486307">ZEB1 protein, human</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D000071799">Zinc 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