Systematic Analysis of Coronavirus Disease 2019 (COVID-19) Receptor ACE2 in Malignant Tumors: Pan-Cancer Analysis.
Identifieur interne : 000045 ( Main/Exploration ); précédent : 000044; suivant : 000046Systematic Analysis of Coronavirus Disease 2019 (COVID-19) Receptor ACE2 in Malignant Tumors: Pan-Cancer Analysis.
Auteurs : Jukun Song [République populaire de Chine] ; Jing Han [République populaire de Chine] ; Feng Liu [République populaire de Chine] ; Xianlin Chen [République populaire de Chine] ; Shenqi Qian [République populaire de Chine] ; Yadong Wang [République populaire de Chine] ; Zhenyu Jia [États-Unis] ; Xiaofeng Duan [République populaire de Chine] ; Xiangyan Zhang [République populaire de Chine] ; Jianguo Zhu [République populaire de Chine]Source :
- Frontiers in molecular biosciences [ 2296-889X ] ; 2020.
Abstract
Background
Coronavirus disease 2019 (COVID-19) was first detected in patients with pneumonia in December 2019 in China and it spread rapidly to the rest of the world becoming a global pandemic. Several observational studies have reported that cancer is a risk factor for COVID-19. On the other hand, ACE2, a receptor for the SARS-CoV-2 virus, was found to be aberrantly expressed in many tumors. However, the characterization of aberrant ACE2 expression in malignant tumors has not been elucidated. Here, we conducted a systematic analysis of the ACE2 expression profile across 31 types of tumors.
Methods
Distribution of ACE2 expression was analyzed using the GTEx, CCLE, TCGA pan-cancer databases. We evaluated the effect of ACE2 on clinical prognosis using the Kaplan-Meier survival plot and COX regression analysis. Correlation between ACE2 and immune infiltration levels was investigated in various cancer types. Additionally, the correlation between ACE2 and immune neoantigen, TMB, microsatellite instability, Mismatch Repair Genes (MMRs), HLA gene members, and DNA Methyltransferase (DNMT) was investigated. The frequency of ACE2 gene mutation in various tumors was analyzed. Functional enrichment analysis was conducted in various cancer types using the GSEA method.
Results
In normal tissues, ACE2 was highly expressed in almost all 31 organs tested. In cancer cell lines, the expression level of ACE2 was low to medium. Although aberrant expression was observed in most cancer types, high expression of ACE2 was not linked to OS, DFS, RFS, and DFI in most tumors in TCGA pan-cancer data. We found that ACE2 expression was significantly correlated with the infiltrating levels of macrophages and dendritic cells, CD4+ T cells, CD8+ T cells, and B cells in multiple tumors. A positive correlation between ACE2 expression and immune neoantigen, TMB, and microsatellite instability was found in multiple cancers. GSEA analysis which was carried out to determine the effect of ACE2 on tumors indicated that several cancer-associated pathways and immune-related pathways were hyperactivated in the high ACE2 expression group of most tumors.
Conclusion
These findings suggest that ACE2 is not correlated with prognosis in most cancer types. However, elevated ACE2 is significantly correlated with immune infiltrating levels, including those of CD8+ T cells, CD4+ T cells, macrophages, neutrophils, and DCs in multiple cancers, especially in lung and breast cancer patients. These findings suggest that ACE2 may affect the tumor environment in cancer patients with COVID-19.
DOI: 10.3389/fmolb.2020.569414
PubMed: 33195415
PubMed Central: PMC7649796
Affiliations:
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China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Respiratory and Critical Care Medicine, Guizhou Provincial People's Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Feng" sort="Liu, Feng" uniqKey="Liu F" first="Feng" last="Liu">Feng Liu</name><affiliation wicri:level="1"><nlm:affiliation>Department of B Ultrasound, Guizhou Provincial People's Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of B Ultrasound, Guizhou Provincial People's Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author><author><name sortKey="Chen, Xianlin" sort="Chen, Xianlin" uniqKey="Chen X" first="Xianlin" last="Chen">Xianlin Chen</name><affiliation wicri:level="1"><nlm:affiliation>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author><author><name sortKey="Qian, Shenqi" sort="Qian, Shenqi" uniqKey="Qian S" first="Shenqi" last="Qian">Shenqi Qian</name><affiliation wicri:level="1"><nlm:affiliation>Department of Stomatology, Changshun County Medical Group Central Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Stomatology, Changshun County Medical Group Central Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Yadong" sort="Wang, Yadong" uniqKey="Wang Y" first="Yadong" last="Wang">Yadong Wang</name><affiliation wicri:level="1"><nlm:affiliation>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author><author><name sortKey="Jia, Zhenyu" sort="Jia, Zhenyu" uniqKey="Jia Z" first="Zhenyu" last="Jia">Zhenyu Jia</name><affiliation wicri:level="2"><nlm:affiliation>Department of Botany and Plant Sciences, University of California, Riverside, Riverside, CA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Botany and Plant Sciences, University of California, Riverside, Riverside, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Duan, Xiaofeng" sort="Duan, Xiaofeng" uniqKey="Duan X" first="Xiaofeng" last="Duan">Xiaofeng Duan</name><affiliation wicri:level="1"><nlm:affiliation>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Xiangyan" sort="Zhang, Xiangyan" uniqKey="Zhang X" first="Xiangyan" last="Zhang">Xiangyan Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Department of Respiratory and Critical Care Medicine, Guizhou Provincial People's Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Respiratory and Critical Care Medicine, Guizhou Provincial People's Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author><author><name sortKey="Zhu, Jianguo" sort="Zhu, Jianguo" uniqKey="Zhu J" first="Jianguo" last="Zhu">Jianguo Zhu</name><affiliation wicri:level="1"><nlm:affiliation>Department of Urology, Guizhou Provincial People's Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Urology, Guizhou Provincial People's Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:33195415</idno><idno type="pmid">33195415</idno><idno type="doi">10.3389/fmolb.2020.569414</idno><idno type="pmc">PMC7649796</idno><idno type="wicri:Area/Main/Corpus">000005</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000005</idno><idno 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last="Han">Jing Han</name><affiliation wicri:level="1"><nlm:affiliation>Department of Respiratory and Critical Care Medicine, Guizhou Provincial People's Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Respiratory and Critical Care Medicine, Guizhou Provincial People's Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Feng" sort="Liu, Feng" uniqKey="Liu F" first="Feng" last="Liu">Feng Liu</name><affiliation wicri:level="1"><nlm:affiliation>Department of B Ultrasound, Guizhou Provincial People's Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of B Ultrasound, Guizhou Provincial People's Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author><author><name sortKey="Chen, Xianlin" sort="Chen, Xianlin" uniqKey="Chen X" first="Xianlin" last="Chen">Xianlin Chen</name><affiliation wicri:level="1"><nlm:affiliation>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author><author><name sortKey="Qian, Shenqi" sort="Qian, Shenqi" uniqKey="Qian S" first="Shenqi" last="Qian">Shenqi Qian</name><affiliation wicri:level="1"><nlm:affiliation>Department of Stomatology, Changshun County Medical Group Central Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Stomatology, Changshun County Medical Group Central Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Yadong" sort="Wang, Yadong" uniqKey="Wang Y" first="Yadong" last="Wang">Yadong Wang</name><affiliation wicri:level="1"><nlm:affiliation>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author><author><name sortKey="Jia, Zhenyu" sort="Jia, Zhenyu" uniqKey="Jia Z" first="Zhenyu" last="Jia">Zhenyu Jia</name><affiliation wicri:level="2"><nlm:affiliation>Department of Botany and Plant Sciences, University of California, Riverside, Riverside, CA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Botany and Plant Sciences, University of California, Riverside, Riverside, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Duan, Xiaofeng" sort="Duan, Xiaofeng" uniqKey="Duan X" first="Xiaofeng" last="Duan">Xiaofeng Duan</name><affiliation wicri:level="1"><nlm:affiliation>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Xiangyan" sort="Zhang, Xiangyan" uniqKey="Zhang X" first="Xiangyan" last="Zhang">Xiangyan Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Department of Respiratory and Critical Care Medicine, Guizhou Provincial People's Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Respiratory and Critical Care Medicine, Guizhou Provincial People's Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author><author><name sortKey="Zhu, Jianguo" sort="Zhu, Jianguo" uniqKey="Zhu J" first="Jianguo" last="Zhu">Jianguo Zhu</name><affiliation wicri:level="1"><nlm:affiliation>Department of Urology, Guizhou Provincial People's Hospital, Guizhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Urology, Guizhou Provincial People's Hospital, Guizhou</wicri:regionArea><wicri:noRegion>Guizhou</wicri:noRegion></affiliation></author></analytic><series><title level="j">Frontiers in molecular biosciences</title><idno type="ISSN">2296-889X</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><b>Background</b></p><p>Coronavirus disease 2019 (COVID-19) was first detected in patients with pneumonia in December 2019 in China and it spread rapidly to the rest of the world becoming a global pandemic. Several observational studies have reported that cancer is a risk factor for COVID-19. On the other hand, ACE2, a receptor for the SARS-CoV-2 virus, was found to be aberrantly expressed in many tumors. However, the characterization of aberrant ACE2 expression in malignant tumors has not been elucidated. Here, we conducted a systematic analysis of the ACE2 expression profile across 31 types of tumors.</p></div><div type="abstract" xml:lang="en"><p><b>Methods</b></p><p>Distribution of ACE2 expression was analyzed using the GTEx, CCLE, TCGA pan-cancer databases. We evaluated the effect of ACE2 on clinical prognosis using the Kaplan-Meier survival plot and COX regression analysis. Correlation between ACE2 and immune infiltration levels was investigated in various cancer types. Additionally, the correlation between ACE2 and immune neoantigen, TMB, microsatellite instability, Mismatch Repair Genes (MMRs), HLA gene members, and DNA Methyltransferase (DNMT) was investigated. The frequency of ACE2 gene mutation in various tumors was analyzed. Functional enrichment analysis was conducted in various cancer types using the GSEA method.</p></div><div type="abstract" xml:lang="en"><p><b>Results</b></p><p>In normal tissues, ACE2 was highly expressed in almost all 31 organs tested. In cancer cell lines, the expression level of ACE2 was low to medium. Although aberrant expression was observed in most cancer types, high expression of ACE2 was not linked to OS, DFS, RFS, and DFI in most tumors in TCGA pan-cancer data. We found that ACE2 expression was significantly correlated with the infiltrating levels of macrophages and dendritic cells, CD4+ T cells, CD8+ T cells, and B cells in multiple tumors. A positive correlation between ACE2 expression and immune neoantigen, TMB, and microsatellite instability was found in multiple cancers. GSEA analysis which was carried out to determine the effect of ACE2 on tumors indicated that several cancer-associated pathways and immune-related pathways were hyperactivated in the high ACE2 expression group of most tumors.</p></div><div type="abstract" xml:lang="en"><p><b>Conclusion</b></p><p>These findings suggest that ACE2 is not correlated with prognosis in most cancer types. However, elevated ACE2 is significantly correlated with immune infiltrating levels, including those of CD8+ T cells, CD4+ T cells, macrophages, neutrophils, and DCs in multiple cancers, especially in lung and breast cancer patients. These findings suggest that ACE2 may affect the tumor environment in cancer patients with COVID-19.</p></div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">33195415</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>17</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">2296-889X</ISSN><JournalIssue CitedMedium="Print"><Volume>7</Volume><PubDate><Year>2020</Year></PubDate></JournalIssue><Title>Frontiers in molecular biosciences</Title><ISOAbbreviation>Front Mol Biosci</ISOAbbreviation></Journal><ArticleTitle>Systematic Analysis of Coronavirus Disease 2019 (COVID-19) Receptor ACE2 in Malignant Tumors: Pan-Cancer Analysis.</ArticleTitle><Pagination><MedlinePgn>569414</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fmolb.2020.569414</ELocationID><Abstract><AbstractText Label="Background" NlmCategory="UNASSIGNED">Coronavirus disease 2019 (COVID-19) was first detected in patients with pneumonia in December 2019 in China and it spread rapidly to the rest of the world becoming a global pandemic. Several observational studies have reported that cancer is a risk factor for COVID-19. On the other hand, ACE2, a receptor for the SARS-CoV-2 virus, was found to be aberrantly expressed in many tumors. However, the characterization of aberrant ACE2 expression in malignant tumors has not been elucidated. Here, we conducted a systematic analysis of the ACE2 expression profile across 31 types of tumors.</AbstractText><AbstractText Label="Methods" NlmCategory="UNASSIGNED">Distribution of ACE2 expression was analyzed using the GTEx, CCLE, TCGA pan-cancer databases. We evaluated the effect of ACE2 on clinical prognosis using the Kaplan-Meier survival plot and COX regression analysis. Correlation between ACE2 and immune infiltration levels was investigated in various cancer types. Additionally, the correlation between ACE2 and immune neoantigen, TMB, microsatellite instability, Mismatch Repair Genes (MMRs), HLA gene members, and DNA Methyltransferase (DNMT) was investigated. The frequency of ACE2 gene mutation in various tumors was analyzed. Functional enrichment analysis was conducted in various cancer types using the GSEA method.</AbstractText><AbstractText Label="Results" NlmCategory="UNASSIGNED">In normal tissues, ACE2 was highly expressed in almost all 31 organs tested. In cancer cell lines, the expression level of ACE2 was low to medium. Although aberrant expression was observed in most cancer types, high expression of ACE2 was not linked to OS, DFS, RFS, and DFI in most tumors in TCGA pan-cancer data. We found that ACE2 expression was significantly correlated with the infiltrating levels of macrophages and dendritic cells, CD4+ T cells, CD8+ T cells, and B cells in multiple tumors. A positive correlation between ACE2 expression and immune neoantigen, TMB, and microsatellite instability was found in multiple cancers. GSEA analysis which was carried out to determine the effect of ACE2 on tumors indicated that several cancer-associated pathways and immune-related pathways were hyperactivated in the high ACE2 expression group of most tumors.</AbstractText><AbstractText Label="Conclusion" NlmCategory="UNASSIGNED">These findings suggest that ACE2 is not correlated with prognosis in most cancer types. However, elevated ACE2 is significantly correlated with immune infiltrating levels, including those of CD8+ T cells, CD4+ T cells, macrophages, neutrophils, and DCs in multiple cancers, especially in lung and breast cancer patients. These findings suggest that ACE2 may affect the tumor environment in cancer patients with COVID-19.</AbstractText><CopyrightInformation>Copyright © 2020 Song, Han, Liu, Chen, Qian, Wang, Jia, Duan, Zhang and Zhu.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Song</LastName><ForeName>Jukun</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Han</LastName><ForeName>Jing</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Respiratory and Critical Care Medicine, Guizhou Provincial People's Hospital, Guizhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Feng</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Department of B Ultrasound, Guizhou Provincial People's Hospital, Guizhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Xianlin</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Qian</LastName><ForeName>Shenqi</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Stomatology, Changshun County Medical Group Central Hospital, Guizhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Yadong</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jia</LastName><ForeName>Zhenyu</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>Department of Botany and Plant Sciences, University of California, Riverside, Riverside, CA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Duan</LastName><ForeName>Xiaofeng</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Department of Oral and Maxillofacial Surgery, Guizhou Provincial People's Hospital, Guizhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Xiangyan</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Department of Respiratory and Critical Care Medicine, Guizhou Provincial People's Hospital, Guizhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhu</LastName><ForeName>Jianguo</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Urology, Guizhou Provincial People's Hospital, Guizhou, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal 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last="Chen">Xianlin Chen</name><name sortKey="Duan, Xiaofeng" sort="Duan, Xiaofeng" uniqKey="Duan X" first="Xiaofeng" last="Duan">Xiaofeng Duan</name><name sortKey="Han, Jing" sort="Han, Jing" uniqKey="Han J" first="Jing" last="Han">Jing Han</name><name sortKey="Liu, Feng" sort="Liu, Feng" uniqKey="Liu F" first="Feng" last="Liu">Feng Liu</name><name sortKey="Qian, Shenqi" sort="Qian, Shenqi" uniqKey="Qian S" first="Shenqi" last="Qian">Shenqi Qian</name><name sortKey="Wang, Yadong" sort="Wang, Yadong" uniqKey="Wang Y" first="Yadong" last="Wang">Yadong Wang</name><name sortKey="Zhang, Xiangyan" sort="Zhang, Xiangyan" uniqKey="Zhang X" first="Xiangyan" last="Zhang">Xiangyan Zhang</name><name sortKey="Zhu, Jianguo" sort="Zhu, Jianguo" uniqKey="Zhu J" first="Jianguo" last="Zhu">Jianguo Zhu</name></country><country name="États-Unis"><region name="Californie"><name sortKey="Jia, Zhenyu" sort="Jia, Zhenyu" uniqKey="Jia Z" first="Zhenyu" last="Jia">Zhenyu 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