Radiosensitization of Clioquinol Combined with Zinc in the Nasopharyngeal Cancer Stem-like Cells by Inhibiting Autophagy in Vitro and in Vivo
Identifieur interne : 000F39 ( Ncbi/Merge ); précédent : 000F38; suivant : 000F40Radiosensitization of Clioquinol Combined with Zinc in the Nasopharyngeal Cancer Stem-like Cells by Inhibiting Autophagy in Vitro and in Vivo
Auteurs : Yuan Ke [République populaire de Chine] ; Chaoyan Wu [République populaire de Chine] ; Yifei Zeng [République populaire de Chine] ; Mengge Chen [République populaire de Chine] ; Yonghong Li [République populaire de Chine] ; Conghua Xie [République populaire de Chine] ; Yunfeng Zhou [République populaire de Chine] ; Yahua Zhong [République populaire de Chine] ; Haijun Yu [République populaire de Chine]Source :
- International Journal of Biological Sciences [ 1449-2288 ] ; 2020.
Abstract
Loco-regional recurrence of nasopharyngeal carcinoma (NPC) after radiation therapy is one of the main types of treatment failure. This study is aimed to explore the possible causes of inside-field recurrence of NPC patients in order to develop effective treatment methods. Our study indicated that CD44 and autophagy proteins in tumor tissues of patients with recurrent NPC are higher than that of the relapse free patients. The
Url:
DOI: 10.7150/ijbs.40305
PubMed: 32071548
PubMed Central: 7019136
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<author><name sortKey="Ke, Yuan" sort="Ke, Yuan" uniqKey="Ke Y" first="Yuan" last="Ke">Yuan Ke</name>
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<author><name sortKey="Xie, Conghua" sort="Xie, Conghua" uniqKey="Xie C" first="Conghua" last="Xie">Conghua Xie</name>
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<author><name sortKey="Zhou, Yunfeng" sort="Zhou, Yunfeng" uniqKey="Zhou Y" first="Yunfeng" last="Zhou">Yunfeng Zhou</name>
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<author><name sortKey="Zhong, Yahua" sort="Zhong, Yahua" uniqKey="Zhong Y" first="Yahua" last="Zhong">Yahua Zhong</name>
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<author><name sortKey="Yu, Haijun" sort="Yu, Haijun" uniqKey="Yu H" first="Haijun" last="Yu">Haijun Yu</name>
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<wicri:regionArea>Department of Radiation and Medical Oncology, Zhongnan Hospital of Wuhan University, Wuhan</wicri:regionArea>
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<wicri:regionArea>Hubei Key Laboratory of Tumor Biological Behaviors, Wuhan, China; Hubei Cancer Clinical Study Center, Zhongnan Hospital of Wuhan University, Wuhan</wicri:regionArea>
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<series><title level="j">International Journal of Biological Sciences</title>
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<front><div type="abstract" xml:lang="en"><p>Loco-regional recurrence of nasopharyngeal carcinoma (NPC) after radiation therapy is one of the main types of treatment failure. This study is aimed to explore the possible causes of inside-field recurrence of NPC patients in order to develop effective treatment methods. Our study indicated that CD44 and autophagy proteins in tumor tissues of patients with recurrent NPC are higher than that of the relapse free patients. The <italic>in vitro</italic>
experiments further confirmed that cancer stem cells (CSCs) were more radioresistant with enhanced autophagy activity. Treatment with clioquinol (CQ) combined with zinc could obviously enhance the radiosensitivity of CNE-2s cells through autophagy inhibition, activation of the caspase system and impairment of DNA damage repair. The<italic> in vivo</italic>
experiments have further consolidated our findings. Our results suggest that CSCs and enhanced autophagy activity may be involved in the inside-field recurrence of NPC, and CQ combined with zinc could be an important therapeutic approach for recurrent NPC.</p>
</div>
</front>
<back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Chua, Mlk" uniqKey="Chua M">MLK Chua</name>
</author>
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<author><name sortKey="Sivridis, E" uniqKey="Sivridis E">E Sivridis</name>
</author>
</analytic>
</biblStruct>
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</author>
<author><name sortKey="Shi, Z" uniqKey="Shi Z">Z Shi</name>
</author>
<author><name sortKey="Zhao, S" uniqKey="Zhao S">S Zhao</name>
</author>
<author><name sortKey="Wang, Ft" uniqKey="Wang F">FT Wang</name>
</author>
<author><name sortKey="Zhou, Tt" uniqKey="Zhou T">TT Zhou</name>
</author>
<author><name sortKey="Liu, B" uniqKey="Liu B">B Liu</name>
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</analytic>
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</author>
<author><name sortKey="Wang, B" uniqKey="Wang B">B Wang</name>
</author>
<author><name sortKey="Zhang, H" uniqKey="Zhang H">H Zhang</name>
</author>
<author><name sortKey="Katsube, T" uniqKey="Katsube T">T Katsube</name>
</author>
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</author>
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</author>
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</biblStruct>
</listBibl>
</div1>
</back>
</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Int J Biol Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">Int. J. Biol. Sci</journal-id>
<journal-id journal-id-type="publisher-id">ijbs</journal-id>
<journal-title-group><journal-title>International Journal of Biological Sciences</journal-title>
</journal-title-group>
<issn pub-type="epub">1449-2288</issn>
<publisher><publisher-name>Ivyspring International Publisher</publisher-name>
<publisher-loc>Sydney</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">32071548</article-id>
<article-id pub-id-type="pmc">7019136</article-id>
<article-id pub-id-type="doi">10.7150/ijbs.40305</article-id>
<article-id pub-id-type="publisher-id">ijbsv16p0777</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Paper</subject>
</subj-group>
</article-categories>
<title-group><article-title>Radiosensitization of Clioquinol Combined with Zinc in the Nasopharyngeal Cancer Stem-like Cells by Inhibiting Autophagy in Vitro and in<italic> Vivo</italic>
</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Ke</surname>
<given-names>Yuan</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="aff" rid="A2">2</xref>
<xref ref-type="author-notes" rid="FNA_star">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wu</surname>
<given-names>Chaoyan</given-names>
</name>
<xref ref-type="aff" rid="A3">3</xref>
<xref ref-type="author-notes" rid="FNA_star">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zeng</surname>
<given-names>Yifei</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chen</surname>
<given-names>Mengge</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Li</surname>
<given-names>Yonghong</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Xie</surname>
<given-names>Conghua</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhou</surname>
<given-names>Yunfeng</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhong</surname>
<given-names>Yahua</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yu</surname>
<given-names>Haijun</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="aff" rid="A2">2</xref>
<xref ref-type="corresp" rid="FNA_envelop">✉</xref>
</contrib>
</contrib-group>
<aff id="A1"><label>1</label>
Department of Radiation and Medical Oncology, Zhongnan Hospital of Wuhan University, Wuhan, China</aff>
<aff id="A2"><label>2</label>
Hubei Key Laboratory of Tumor Biological Behaviors, Wuhan, China; Hubei Cancer Clinical Study Center, Zhongnan Hospital of Wuhan University, Wuhan, China</aff>
<aff id="A3"><label>3</label>
Department of Integrated Traditional Chinese Medicine and Western medicine, Zhongnan Hospital of Wuhan University, Wuhan, China</aff>
<author-notes><corresp id="FNA_envelop">✉ Corresponding author: Haijun Yu, Department of Radiation and Medical Oncology, Zhongnan Hospital of Wuhan University, Wuhan, China, 169 Donghu Road, Wuhan, China,430071. E-mail: <email>haijunyu@whu.edu.cn</email>
</corresp>
<fn fn-type="equal" id="FNA_star"><p>* These authors contributed equally to this work.</p>
</fn>
<fn fn-type="COI-statement"><p>Competing Interests: The authors have declared that no competing interest exists.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2020</year>
</pub-date>
<pub-date pub-type="epub"><day>14</day>
<month>1</month>
<year>2020</year>
</pub-date>
<volume>16</volume>
<issue>5</issue>
<fpage>777</fpage>
<lpage>789</lpage>
<history><date date-type="received"><day>15</day>
<month>9</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>12</day>
<month>11</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© The author(s)</copyright-statement>
<copyright-year>2020</copyright-year>
<license license-type="open-access"><license-p>This is an open access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">https://creativecommons.org/licenses/by/4.0/</ext-link>
). See <ext-link ext-link-type="uri" xlink:href="http://ivyspring.com/terms">http://ivyspring.com/terms</ext-link>
for full terms and conditions.</license-p>
</license>
</permissions>
<abstract><p>Loco-regional recurrence of nasopharyngeal carcinoma (NPC) after radiation therapy is one of the main types of treatment failure. This study is aimed to explore the possible causes of inside-field recurrence of NPC patients in order to develop effective treatment methods. Our study indicated that CD44 and autophagy proteins in tumor tissues of patients with recurrent NPC are higher than that of the relapse free patients. The <italic>in vitro</italic>
experiments further confirmed that cancer stem cells (CSCs) were more radioresistant with enhanced autophagy activity. Treatment with clioquinol (CQ) combined with zinc could obviously enhance the radiosensitivity of CNE-2s cells through autophagy inhibition, activation of the caspase system and impairment of DNA damage repair. The<italic> in vivo</italic>
experiments have further consolidated our findings. Our results suggest that CSCs and enhanced autophagy activity may be involved in the inside-field recurrence of NPC, and CQ combined with zinc could be an important therapeutic approach for recurrent NPC.</p>
</abstract>
</article-meta>
</front>
<floats-group><fig id="F1" position="float"><label>Fig 1</label>
<caption><p>High levels of CD44, Beclin1, LC3 in 60 NPC patients. (A) Representative IHC images of CD44; case 1-3 represent NPC patients with inside-field recurrence and case 4-5 represent ones with relapse free. (B) Representative IHC images of Beclin1 and LC3. (C) Scatter plot of the protein levels of CD44, Beclin1, LC3 for the NPC patients with and without inside-field recurrence. Immunoreactivity was analyzed in 5 random areas for each pathological section and was scored as 0+(no staining), 1+(weak staining), 2+(moderate staining),3+(strong staining),4+ (very strong staining). (*, P<0.05; **, P< 0.01; ***, P<0.001).</p>
</caption>
<graphic xlink:href="ijbsv16p0777g001"></graphic>
</fig>
<fig id="F2" position="float"><label>Fig 2</label>
<caption><p>Side population cells were isolated from nasopharyngeal cancer cell (CNE-2) and characterized with stem cell properties. (A) sorting of CNE-2 cells by flow cytometry. (B) the sorting purity of the freshly sorted SP cells. (C) the CNE-2s and CNE-2ns cells were seeded in tumor sphere culture medium. (D) clone formation results and statistical analysis. (E) the CNE-2s and CNE-2ns cells lysates were analyzed by Western blotting and Realtime-qPCR with anti-CD44, anti-E-cadherin and anti-Vimentin. GAPDH served as a loading control. (All data represent the mean ± SD; n=3; *, P<0.05; **, P< 0.01; ***, P<0.001) (F) the indicated amounts of CNE-2s and CNE-2ns cells were transplanted into 6 weeks BALB/c-nu mice.</p>
</caption>
<graphic xlink:href="ijbsv16p0777g002"></graphic>
</fig>
<fig id="F3" position="float"><label>Fig 3</label>
<caption><p>Comparison of radiosensitivity and autophagy levels in CNE-2s and CNE-2ns cells. (A) colony-formation assay for CNE-2s and CNE-2ns cells using irradiated (2 Gy and 10 Gy). (B) dose-survival curves of irradiated CNE-2s and CNE-2ns cells (range, 0-10 Gy. Data represent the mean ±SD; n=3). (C) Western blotting detection of Beclin1, LC3A and LC3B in CNE-2s and CNE-2ns cells assessed 24 hours after 4 Gy IR.</p>
</caption>
<graphic xlink:href="ijbsv16p0777g003"></graphic>
</fig>
<fig id="F4" position="float"><label>Fig 4</label>
<caption><p>CQ combined with zinc enhanced the radiosensitivity of CNE-2s cells. (A) Representative crystal violet staining photos of CNE-2s cells irradiated with 2 Gy and 10 Gy. All values shown were mean ± SD of triplicate measurements and repeated three times with similar results. Clone formation assay was used to detect the radiosensitivity of CNE-2s cells with different treatments. (B) Representative images of acridine orange staining in CNE-2s. (C) Representative images of GFP-LC3 tracer protein. (D) Representative images of transmission electron microscopy to observe the structure and number of autophagosomes. (E) Western blotting analysis of Beclin1, LC3A and LC3B protein levels in CNE-2s cells.</p>
</caption>
<graphic xlink:href="ijbsv16p0777g004"></graphic>
</fig>
<fig id="F5" position="float"><label>Fig 5</label>
<caption><p>CQ combined with Zinc suppressed NF-κB activity and increased radiation induced DNA damage. (A) Immunofluorescence staining localization of phospho-p65(phos-P65) in different treatment groups of CNE-2s cells. (B) Immunofluorescence staining of phos-γH2AX. (C)Western blotting analysis of key proteins involved in DNA damage and repair in different treatment groups.</p>
</caption>
<graphic xlink:href="ijbsv16p0777g005"></graphic>
</fig>
<fig id="F6" position="float"><label>Fig 6</label>
<caption><p>CQ combined with zinc promoted radiation-induced apoptosis in CNE-2s cells. (A) cell cytometry analysis of Annexin V and PI for apoptosis in CNE-2s cells. (B)the administration treatment group had significantly more cell apoptosis than individual ones. Data were expressed as mean ± SD, n=3, * p<0.05, ***p<0.001. (C) Western blotting analysis of apoptosis-related proteins in different treatment groups.</p>
</caption>
<graphic xlink:href="ijbsv16p0777g006"></graphic>
</fig>
<fig id="F7" position="float"><label>Fig 7</label>
<caption><p>CQ combined with zinc inhibited tumor growth<italic> in vivo</italic>
. (A) Simulation position before IR. (B) Representative image of tumor growth in different treatments (I, II, III, IV, V represent control, CQ+Zinc, IR, IR + CQ + Zinc, IR + RAPA + CQ +Zinc respectively). (C) Gross view of tumor. (D) Growth curve of tumor volume. (E) Representative immunohistochemistry staining images of Beclin1 and LC3 in tumor tissue.</p>
</caption>
<graphic xlink:href="ijbsv16p0777g007"></graphic>
</fig>
<table-wrap id="T1" position="float"><label>Table 1</label>
<caption><p>Clinical characteristics of NPC patients (n = 60)</p>
</caption>
<table frame="hsides" rules="groups"><thead valign="top"><tr><th rowspan="2" colspan="1">Characteristics</th>
<th rowspan="1" colspan="1">Inside-field recurrence (n = 20)</th>
<th rowspan="1" colspan="1">Without recurrence (n = 40)</th>
</tr>
<tr><th rowspan="1" colspan="1">No. of cases (%)</th>
<th rowspan="1" colspan="1">No. of cases (%)</th>
</tr>
</thead>
<tbody valign="top"><tr><td rowspan="1" colspan="1"><bold>Gender</bold>
</td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
</tr>
<tr><td rowspan="1" colspan="1">Male</td>
<td rowspan="1" colspan="1">15(75%)</td>
<td rowspan="1" colspan="1">30(75%)</td>
</tr>
<tr><td rowspan="1" colspan="1">Female</td>
<td rowspan="1" colspan="1">5(25%)</td>
<td rowspan="1" colspan="1">10(25%)</td>
</tr>
<tr><td rowspan="1" colspan="1"><bold>WHO Histologic type</bold>
</td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
</tr>
<tr><td rowspan="1" colspan="1">IIa</td>
<td rowspan="1" colspan="1">4(20%)</td>
<td rowspan="1" colspan="1">8(20%)</td>
</tr>
<tr><td rowspan="1" colspan="1">IIb</td>
<td rowspan="1" colspan="1">16(80%)</td>
<td rowspan="1" colspan="1">32(80%)</td>
</tr>
<tr><td rowspan="1" colspan="1"><bold>T classification</bold>
</td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
</tr>
<tr><td rowspan="1" colspan="1">T1</td>
<td rowspan="1" colspan="1">2(10%)</td>
<td rowspan="1" colspan="1">5(13%)</td>
</tr>
<tr><td rowspan="1" colspan="1">T2</td>
<td rowspan="1" colspan="1">8(40%)</td>
<td rowspan="1" colspan="1">16(40%)</td>
</tr>
<tr><td rowspan="1" colspan="1">T3</td>
<td rowspan="1" colspan="1">7(35%)</td>
<td rowspan="1" colspan="1">15(38%)</td>
</tr>
<tr><td rowspan="1" colspan="1">T4</td>
<td rowspan="1" colspan="1">3(15%)</td>
<td rowspan="1" colspan="1">4(9%)</td>
</tr>
<tr><td rowspan="1" colspan="1"><bold>N classification</bold>
</td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
</tr>
<tr><td rowspan="1" colspan="1">N1</td>
<td rowspan="1" colspan="1">1(5%)</td>
<td rowspan="1" colspan="1">6(15%)</td>
</tr>
<tr><td rowspan="1" colspan="1">N2</td>
<td rowspan="1" colspan="1">16(80%)</td>
<td rowspan="1" colspan="1">28(70%)</td>
</tr>
<tr><td rowspan="1" colspan="1">N3</td>
<td rowspan="1" colspan="1">3(15%)</td>
<td rowspan="1" colspan="1">6(15%)</td>
</tr>
<tr><td rowspan="1" colspan="1"><bold>Clinical stage</bold>
</td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
</tr>
<tr><td rowspan="1" colspan="1">I</td>
<td rowspan="1" colspan="1">0(0%)</td>
<td rowspan="1" colspan="1">0(0%)</td>
</tr>
<tr><td rowspan="1" colspan="1">II</td>
<td rowspan="1" colspan="1">1(5%)</td>
<td rowspan="1" colspan="1">2(5%)</td>
</tr>
<tr><td rowspan="1" colspan="1">III</td>
<td rowspan="1" colspan="1">14(70%)</td>
<td rowspan="1" colspan="1">28(70%)</td>
</tr>
<tr><td rowspan="1" colspan="1">IVa+IVb</td>
<td rowspan="1" colspan="1">5(25%)</td>
<td rowspan="1" colspan="1">10(25%)</td>
</tr>
<tr><td rowspan="1" colspan="1"><bold>Neoadjuvant chemotherapy</bold>
</td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
</tr>
<tr><td rowspan="1" colspan="1">Yes</td>
<td rowspan="1" colspan="1">17(85%)</td>
<td rowspan="1" colspan="1">32(80%)</td>
</tr>
<tr><td rowspan="1" colspan="1">No</td>
<td rowspan="1" colspan="1">3(15%)</td>
<td rowspan="1" colspan="1">8(20%)</td>
</tr>
<tr><td rowspan="1" colspan="1"><bold>Concurrent chemotherapy</bold>
</td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
</tr>
<tr><td rowspan="1" colspan="1">Yes</td>
<td rowspan="1" colspan="1">13(65%)</td>
<td rowspan="1" colspan="1">25(62%)</td>
</tr>
<tr><td rowspan="1" colspan="1">No</td>
<td rowspan="1" colspan="1">7(35%)</td>
<td rowspan="1" colspan="1">15(38%)</td>
</tr>
<tr><td rowspan="1" colspan="1"><bold>PTV-GTVt dose</bold>
</td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
</tr>
<tr><td rowspan="1" colspan="1">≥70Gy</td>
<td rowspan="1" colspan="1">18(90%)</td>
<td rowspan="1" colspan="1">36(90%)</td>
</tr>
<tr><td rowspan="1" colspan="1"><70Gy</td>
<td rowspan="1" colspan="1">2(10%)</td>
<td rowspan="1" colspan="1">4(10%)</td>
</tr>
<tr><td rowspan="1" colspan="1"><bold>Radiotherapy modality</bold>
</td>
<td rowspan="1" colspan="1"></td>
<td rowspan="1" colspan="1"></td>
</tr>
<tr><td rowspan="1" colspan="1">IMRT</td>
<td rowspan="1" colspan="1">20(100%)</td>
<td rowspan="1" colspan="1">40(100%)</td>
</tr>
<tr><td rowspan="1" colspan="1">3D-CRT or 2D</td>
<td rowspan="1" colspan="1">0</td>
<td rowspan="1" colspan="1">0</td>
</tr>
</tbody>
</table>
</table-wrap>
</floats-group>
</pmc>
<affiliations><list><country><li>République populaire de Chine</li>
</country>
<region><li>Hubei</li>
</region>
<settlement><li>Wuhan</li>
</settlement>
</list>
<tree><country name="République populaire de Chine"><region name="Hubei"><name sortKey="Ke, Yuan" sort="Ke, Yuan" uniqKey="Ke Y" first="Yuan" last="Ke">Yuan Ke</name>
</region>
<name sortKey="Chen, Mengge" sort="Chen, Mengge" uniqKey="Chen M" first="Mengge" last="Chen">Mengge Chen</name>
<name sortKey="Chen, Mengge" sort="Chen, Mengge" uniqKey="Chen M" first="Mengge" last="Chen">Mengge Chen</name>
<name sortKey="Ke, Yuan" sort="Ke, Yuan" uniqKey="Ke Y" first="Yuan" last="Ke">Yuan Ke</name>
<name sortKey="Li, Yonghong" sort="Li, Yonghong" uniqKey="Li Y" first="Yonghong" last="Li">Yonghong Li</name>
<name sortKey="Li, Yonghong" sort="Li, Yonghong" uniqKey="Li Y" first="Yonghong" last="Li">Yonghong Li</name>
<name sortKey="Wu, Chaoyan" sort="Wu, Chaoyan" uniqKey="Wu C" first="Chaoyan" last="Wu">Chaoyan Wu</name>
<name sortKey="Xie, Conghua" sort="Xie, Conghua" uniqKey="Xie C" first="Conghua" last="Xie">Conghua Xie</name>
<name sortKey="Xie, Conghua" sort="Xie, Conghua" uniqKey="Xie C" first="Conghua" last="Xie">Conghua Xie</name>
<name sortKey="Yu, Haijun" sort="Yu, Haijun" uniqKey="Yu H" first="Haijun" last="Yu">Haijun Yu</name>
<name sortKey="Yu, Haijun" sort="Yu, Haijun" uniqKey="Yu H" first="Haijun" last="Yu">Haijun Yu</name>
<name sortKey="Zeng, Yifei" sort="Zeng, Yifei" uniqKey="Zeng Y" first="Yifei" last="Zeng">Yifei Zeng</name>
<name sortKey="Zeng, Yifei" sort="Zeng, Yifei" uniqKey="Zeng Y" first="Yifei" last="Zeng">Yifei Zeng</name>
<name sortKey="Zhong, Yahua" sort="Zhong, Yahua" uniqKey="Zhong Y" first="Yahua" last="Zhong">Yahua Zhong</name>
<name sortKey="Zhong, Yahua" sort="Zhong, Yahua" uniqKey="Zhong Y" first="Yahua" last="Zhong">Yahua Zhong</name>
<name sortKey="Zhou, Yunfeng" sort="Zhou, Yunfeng" uniqKey="Zhou Y" first="Yunfeng" last="Zhou">Yunfeng Zhou</name>
<name sortKey="Zhou, Yunfeng" sort="Zhou, Yunfeng" uniqKey="Zhou Y" first="Yunfeng" last="Zhou">Yunfeng Zhou</name>
</country>
</tree>
</affiliations>
</record>
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