Prostate Cancer Heterogeneous High-Metastatic Multi-Organ-Colonizing Chemo-Resistant Variants Selected by Serial Metastatic Passage in Nude Mice Are Highly Enriched for Multinucleate Giant Cells
In order to further understand the role of tumor heterogeneity in metastasis and chemo-resistance, high metastatic PC-3 human prostate cancer variants were selected by injecting parental PC-3 cells, expressing green fluorescent protein (GFP) in the footpad of nude mice, which then metastasize to ing...
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| description | In order to further understand the role of tumor heterogeneity in metastasis and chemo-resistance, high metastatic PC-3 human prostate cancer variants were selected by injecting parental PC-3 cells, expressing green fluorescent protein (GFP) in the footpad of nude mice, which then metastasize to inguinal lymph nodes. The PC-3-GFP cells which metastasized to the inguinal lymph nodes were collected and were re-injected to the footpad. After 6 such cycles, the PC-3-GFP cells collected from inguinal lymph nodes (PC-3-GFP-LN) were again injected to the footpad. PC-3-GFP-LN showed 100% metastasis to major lymph nodes (popliteal, inguinal, axillary, and cervical), and 100% metastasis to bone and lung. The percent of giant cell variants was enriched in PC-3-GFP-LN-6 compared to parental cells and increased with each cycle of selection, which in turn had increased metastasis. PC-3-GFP-LN-6 cells were resistant to 5-fluorouracil, doxorubicin and cisplatinum, compared to parental PC-3. However, PC-3-GFP-LN-6 was sensitive to the traditional Chinese medicine (TCM) herbal mixture LQ, similar to the parental cells. These results suggest that PC-3 tumors are heterogenous and that subpopulations of highly metastatic, drug-resistant cells can be step-wise selected using a mouse model of tumor progression. |
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The PC-3-GFP cells which metastasized to the inguinal lymph nodes were collected and were re-injected to the footpad. After 6 such cycles, the PC-3-GFP cells collected from inguinal lymph nodes (PC-3-GFP-LN) were again injected to the footpad. PC-3-GFP-LN showed 100% metastasis to major lymph nodes (popliteal, inguinal, axillary, and cervical), and 100% metastasis to bone and lung. The percent of giant cell variants was enriched in PC-3-GFP-LN-6 compared to parental cells and increased with each cycle of selection, which in turn had increased metastasis. PC-3-GFP-LN-6 cells were resistant to 5-fluorouracil, doxorubicin and cisplatinum, compared to parental PC-3. However, PC-3-GFP-LN-6 was sensitive to the traditional Chinese medicine (TCM) herbal mixture LQ, similar to the parental cells. These results suggest that PC-3 tumors are heterogenous and that subpopulations of highly metastatic, drug-resistant cells can be step-wise selected using a mouse model of tumor progression.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0140721</identifier><identifier>PMID: 26536025</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>5-Fluorouracil ; Animals ; Antineoplastic Agents - therapeutic use ; Antineoplastic Agents - toxicity ; Bone Neoplasms - pathology ; Bone Neoplasms - secondary ; Cancer ; Cancer metastasis ; Cancer therapies ; Care and treatment ; Cell cycle ; Cell Line, Tumor ; Cell Survival ; Chemotherapy ; Chinese medicine ; Cisplatin - therapeutic use ; Cisplatin - toxicity ; Cloning ; Complications and side effects ; Development and progression ; Doxorubicin ; Doxorubicin - therapeutic use ; Doxorubicin - toxicity ; Drug resistance ; Drug Resistance, Neoplasm - genetics ; Drugs, Chinese Herbal - therapeutic use ; Drugs, Chinese Herbal - toxicity ; Fluorescence ; Fluorouracil - therapeutic use ; Fluorouracil - toxicity ; Genes, Reporter ; Giant cells ; Giant Cells - cytology ; Giant Cells - pathology ; Green fluorescent protein ; Green Fluorescent Proteins - genetics ; Green Fluorescent Proteins - metabolism ; Health aspects ; Herbal medicine ; Humans ; Laboratories ; Lung Neoplasms - pathology ; Lung Neoplasms - secondary ; Lungs ; Lymph nodes ; Lymph Nodes - pathology ; Lymphatic Metastasis ; Lymphatic system ; Male ; Medicine, Chinese Traditional ; Metastases ; Metastasis ; Mice ; Mice, Nude ; Mouse devices ; Patient outcomes ; Pharmaceuticals ; Prostate cancer ; Prostatic Neoplasms - drug therapy ; Prostatic Neoplasms - metabolism ; Prostatic Neoplasms - pathology ; Subpopulations ; Surgery ; Traditional Chinese medicine ; Transplantation, Heterologous ; Tumors</subject><ispartof>PloS one, 2015-11, Vol.10 (11), p.e0140721-e0140721</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Zhang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Zhang et al 2015 Zhang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-9d763698027e22ec918e002f3eae9accf4ec4ecb0bdb6dae49e296574d40a4803</citedby><cites>FETCH-LOGICAL-c692t-9d763698027e22ec918e002f3eae9accf4ec4ecb0bdb6dae49e296574d40a4803</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4633180/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4633180/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26536025$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Nie, Daotai</contributor><creatorcontrib>Zhang, Lei</creatorcontrib><creatorcontrib>Wu, Chengyu</creatorcontrib><creatorcontrib>Hoffman, Robert M</creatorcontrib><title>Prostate Cancer Heterogeneous High-Metastatic Multi-Organ-Colonizing Chemo-Resistant Variants Selected by Serial Metastatic Passage in Nude Mice Are Highly Enriched for Multinucleate Giant Cells</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>In order to further understand the role of tumor heterogeneity in metastasis and chemo-resistance, high metastatic PC-3 human prostate cancer variants were selected by injecting parental PC-3 cells, expressing green fluorescent protein (GFP) in the footpad of nude mice, which then metastasize to inguinal lymph nodes. The PC-3-GFP cells which metastasized to the inguinal lymph nodes were collected and were re-injected to the footpad. After 6 such cycles, the PC-3-GFP cells collected from inguinal lymph nodes (PC-3-GFP-LN) were again injected to the footpad. PC-3-GFP-LN showed 100% metastasis to major lymph nodes (popliteal, inguinal, axillary, and cervical), and 100% metastasis to bone and lung. The percent of giant cell variants was enriched in PC-3-GFP-LN-6 compared to parental cells and increased with each cycle of selection, which in turn had increased metastasis. PC-3-GFP-LN-6 cells were resistant to 5-fluorouracil, doxorubicin and cisplatinum, compared to parental PC-3. However, PC-3-GFP-LN-6 was sensitive to the traditional Chinese medicine (TCM) herbal mixture LQ, similar to the parental cells. 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drug therapy</subject><subject>Prostatic Neoplasms - metabolism</subject><subject>Prostatic Neoplasms - pathology</subject><subject>Subpopulations</subject><subject>Surgery</subject><subject>Traditional Chinese medicine</subject><subject>Transplantation, Heterologous</subject><subject>Tumors</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk91u0zAUxyMEYmPwBggsISG4SHHsxElukKZqbJVWNm2wW8txTlJPrl1sBzEejyfDabupRbtAsWTr-Hf-58M5SfI6w5OMltmnWzs4I_RkZQ1McJbjkmRPksOspiRlBNOnO-eD5IX3txgXtGLseXJAWEEZJsVh8ufSWR9EADQVRoJDZxDA2R4M2MGjM9Uv0jkEMTJKovmgg0ovXC9MOrXaGvVbmR5NF7C06RV4FTkT0I1wKu4eXYMGGaBFzV08R6NGO2qXwnvRA1IGfR1aQHMlAR07WIfVd-jEOCUX0buzbhPaDFLDmO3pqI-moLV_mTzrhPbwarsfJd-_nHybnqXnF6ez6fF5KllNQlq3JaOsrjApgRCQdVYBxqSjIKAWUnY5yLga3LQNawXkNZCaFWXe5ljkFaZHyduN7kpbz7ft9zwrKSZRt6KRmG2I1opbvnJqKdwdt0LxtcG6ngsXC9fARdU0Fc1LQQua52UjihrLqqAko0SKaD5KPm-jDc0SWgkmOKH3RPdvjFrw3v7kOaM0W6f7YSvg7I8BfOBL5WVsmFg_7Zh3VtYZZnVE3_2DPl7dlupFLECZzsa4chTlxzmlLOZejFqTR6j4tbBUMv6rnYr2PYePew6RCfAr9GLwns-ur_6fvbjZZ9_vsAsQOiy81UNQ1vh9MN-AMo6Cd9A9NDnDfBy1-27wcdT4dtSi25vdB3pwup8t-hcZRiai</recordid><startdate>20151104</startdate><enddate>20151104</enddate><creator>Zhang, Lei</creator><creator>Wu, Chengyu</creator><creator>Hoffman, Robert M</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20151104</creationdate><title>Prostate Cancer Heterogeneous High-Metastatic Multi-Organ-Colonizing Chemo-Resistant Variants Selected by Serial Metastatic Passage in Nude Mice Are Highly Enriched for Multinucleate Giant Cells</title><author>Zhang, Lei ; Wu, Chengyu ; Hoffman, Robert M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-9d763698027e22ec918e002f3eae9accf4ec4ecb0bdb6dae49e296574d40a4803</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>5-Fluorouracil</topic><topic>Animals</topic><topic>Antineoplastic Agents - therapeutic use</topic><topic>Antineoplastic Agents - toxicity</topic><topic>Bone Neoplasms - pathology</topic><topic>Bone Neoplasms - secondary</topic><topic>Cancer</topic><topic>Cancer metastasis</topic><topic>Cancer therapies</topic><topic>Care and treatment</topic><topic>Cell cycle</topic><topic>Cell Line, Tumor</topic><topic>Cell Survival</topic><topic>Chemotherapy</topic><topic>Chinese medicine</topic><topic>Cisplatin - therapeutic use</topic><topic>Cisplatin - toxicity</topic><topic>Cloning</topic><topic>Complications and side effects</topic><topic>Development and progression</topic><topic>Doxorubicin</topic><topic>Doxorubicin - therapeutic use</topic><topic>Doxorubicin - toxicity</topic><topic>Drug resistance</topic><topic>Drug Resistance, Neoplasm - genetics</topic><topic>Drugs, Chinese Herbal - therapeutic use</topic><topic>Drugs, Chinese Herbal - toxicity</topic><topic>Fluorescence</topic><topic>Fluorouracil - therapeutic use</topic><topic>Fluorouracil - toxicity</topic><topic>Genes, Reporter</topic><topic>Giant cells</topic><topic>Giant Cells - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Lei</au><au>Wu, Chengyu</au><au>Hoffman, Robert M</au><au>Nie, Daotai</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Prostate Cancer Heterogeneous High-Metastatic Multi-Organ-Colonizing Chemo-Resistant Variants Selected by Serial Metastatic Passage in Nude Mice Are Highly Enriched for Multinucleate Giant Cells</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-11-04</date><risdate>2015</risdate><volume>10</volume><issue>11</issue><spage>e0140721</spage><epage>e0140721</epage><pages>e0140721-e0140721</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>In order to further understand the role of tumor heterogeneity in metastasis and chemo-resistance, high metastatic PC-3 human prostate cancer variants were selected by injecting parental PC-3 cells, expressing green fluorescent protein (GFP) in the footpad of nude mice, which then metastasize to inguinal lymph nodes. The PC-3-GFP cells which metastasized to the inguinal lymph nodes were collected and were re-injected to the footpad. After 6 such cycles, the PC-3-GFP cells collected from inguinal lymph nodes (PC-3-GFP-LN) were again injected to the footpad. PC-3-GFP-LN showed 100% metastasis to major lymph nodes (popliteal, inguinal, axillary, and cervical), and 100% metastasis to bone and lung. The percent of giant cell variants was enriched in PC-3-GFP-LN-6 compared to parental cells and increased with each cycle of selection, which in turn had increased metastasis. PC-3-GFP-LN-6 cells were resistant to 5-fluorouracil, doxorubicin and cisplatinum, compared to parental PC-3. However, PC-3-GFP-LN-6 was sensitive to the traditional Chinese medicine (TCM) herbal mixture LQ, similar to the parental cells. These results suggest that PC-3 tumors are heterogenous and that subpopulations of highly metastatic, drug-resistant cells can be step-wise selected using a mouse model of tumor progression.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26536025</pmid><doi>10.1371/journal.pone.0140721</doi><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_plos_journals_1730269883 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | 5-Fluorouracil Animals Antineoplastic Agents - therapeutic use Antineoplastic Agents - toxicity Bone Neoplasms - pathology Bone Neoplasms - secondary Cancer Cancer metastasis Cancer therapies Care and treatment Cell cycle Cell Line, Tumor Cell Survival Chemotherapy Chinese medicine Cisplatin - therapeutic use Cisplatin - toxicity Cloning Complications and side effects Development and progression Doxorubicin Doxorubicin - therapeutic use Doxorubicin - toxicity Drug resistance Drug Resistance, Neoplasm - genetics Drugs, Chinese Herbal - therapeutic use Drugs, Chinese Herbal - toxicity Fluorescence Fluorouracil - therapeutic use Fluorouracil - toxicity Genes, Reporter Giant cells Giant Cells - cytology Giant Cells - pathology Green fluorescent protein Green Fluorescent Proteins - genetics Green Fluorescent Proteins - metabolism Health aspects Herbal medicine Humans Laboratories Lung Neoplasms - pathology Lung Neoplasms - secondary Lungs Lymph nodes Lymph Nodes - pathology Lymphatic Metastasis Lymphatic system Male Medicine, Chinese Traditional Metastases Metastasis Mice Mice, Nude Mouse devices Patient outcomes Pharmaceuticals Prostate cancer Prostatic Neoplasms - drug therapy Prostatic Neoplasms - metabolism Prostatic Neoplasms - pathology Subpopulations Surgery Traditional Chinese medicine Transplantation, Heterologous Tumors |
| title | Prostate Cancer Heterogeneous High-Metastatic Multi-Organ-Colonizing Chemo-Resistant Variants Selected by Serial Metastatic Passage in Nude Mice Are Highly Enriched for Multinucleate Giant Cells |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-05T09%3A30%3A35IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Prostate%20Cancer%20Heterogeneous%20High-Metastatic%20Multi-Organ-Colonizing%20Chemo-Resistant%20Variants%20Selected%20by%20Serial%20Metastatic%20Passage%20in%20Nude%20Mice%20Are%20Highly%20Enriched%20for%20Multinucleate%20Giant%20Cells&rft.jtitle=PloS%20one&rft.au=Zhang,%20Lei&rft.date=2015-11-04&rft.volume=10&rft.issue=11&rft.spage=e0140721&rft.epage=e0140721&rft.pages=e0140721-e0140721&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0140721&rft_dat=%3Cgale_plos_%3EA433632159%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1730269883&rft_id=info:pmid/26536025&rft_galeid=A433632159&rft_doaj_id=oai_doaj_org_article_a8bb8347a353447ba590c8532132ca7a&rfr_iscdi=true |