Circadian disruption accelerates tumor growth and angio/stromagenesis through a Wnt signaling pathway
Epidemiologic studies show a high incidence of cancer in shift workers, suggesting a possible relationship between circadian rhythms and tumorigenesis. However, the precise molecular mechanism played by circadian rhythms in tumor progression is not known. To identify the possible mechanisms underlyi...
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| Veröffentlicht in: | PloS one 2010-12, Vol.5 (12), p.e15330 |
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| creator | Yasuniwa, Yoshihiro Izumi, Hiroto Wang, Ke-Yong Shimajiri, Shohei Sasaguri, Yasuyuki Kawai, Kazuaki Kasai, Hiroshi Shimada, Takashi Miyake, Koichi Kashiwagi, Eiji Hirano, Gen Kidani, Akihiko Akiyama, Masaki Han, Bin Wu, Ying Ieiri, Ichiro Higuchi, Shun Kohno, Kimitoshi |
| description | Epidemiologic studies show a high incidence of cancer in shift workers, suggesting a possible relationship between circadian rhythms and tumorigenesis. However, the precise molecular mechanism played by circadian rhythms in tumor progression is not known. To identify the possible mechanisms underlying tumor progression related to circadian rhythms, we set up nude mouse xenograft models. HeLa cells were injected in nude mice and nude mice were moved to two different cases, one case is exposed to a 24-hour light cycle (L/L), the other is a more "normal" 12-hour light/dark cycle (L/D). We found a significant increase in tumor volume in the L/L group compared with the L/D group. In addition, tumor microvessels and stroma were strongly increased in L/L mice. Although there was a hypervascularization in L/L tumors, there was no associated increase in the production of vascular endothelial cell growth factor (VEGF). DNA microarray analysis showed enhanced expression of WNT10A, and our subsequent study revealed that WNT10A stimulates the growth of both microvascular endothelial cells and fibroblasts in tumors from light-stressed mice, along with marked increases in angio/stromagenesis. Only the tumor stroma stained positive for WNT10A and WNT10A is also highly expressed in keloid dermal fibroblasts but not in normal dermal fibroblasts indicated that WNT10A may be a novel angio/stromagenic growth factor. These findings suggest that circadian disruption induces the progression of malignant tumors via a Wnt signaling pathway. |
| doi_str_mv | 10.1371/journal.pone.0015330 |
| format | Article |
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However, the precise molecular mechanism played by circadian rhythms in tumor progression is not known. To identify the possible mechanisms underlying tumor progression related to circadian rhythms, we set up nude mouse xenograft models. HeLa cells were injected in nude mice and nude mice were moved to two different cases, one case is exposed to a 24-hour light cycle (L/L), the other is a more "normal" 12-hour light/dark cycle (L/D). We found a significant increase in tumor volume in the L/L group compared with the L/D group. In addition, tumor microvessels and stroma were strongly increased in L/L mice. Although there was a hypervascularization in L/L tumors, there was no associated increase in the production of vascular endothelial cell growth factor (VEGF). DNA microarray analysis showed enhanced expression of WNT10A, and our subsequent study revealed that WNT10A stimulates the growth of both microvascular endothelial cells and fibroblasts in tumors from light-stressed mice, along with marked increases in angio/stromagenesis. Only the tumor stroma stained positive for WNT10A and WNT10A is also highly expressed in keloid dermal fibroblasts but not in normal dermal fibroblasts indicated that WNT10A may be a novel angio/stromagenic growth factor. These findings suggest that circadian disruption induces the progression of malignant tumors via a Wnt signaling pathway.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0015330</identifier><identifier>PMID: 21203463</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animal models ; Animals ; Biochemistry ; Biology ; Cancer ; Cancer research ; Cell cycle ; Circadian Rhythm ; Circadian rhythms ; Deoxyribonucleic acid ; Development and progression ; Disease Progression ; DNA ; DNA microarrays ; DNA repair ; Drug resistance ; Endothelial cells ; Environmental health ; Epidemiology ; Fibroblasts ; Gene expression ; Gene Expression Regulation, Neoplastic ; Genes ; Genetic research ; Growth ; HeLa Cells ; Hospitals ; Humans ; Light ; Male ; Medicine ; Metastasis ; Mice ; Mice, Inbred BALB C ; Mice, Nude ; Microvasculature ; Molecular biology ; Neoplasm Transplantation ; Neoplasms - pathology ; Neovascularization, Pathologic ; Nerve Tissue Proteins - metabolism ; Oncology ; Pathology ; Pharmaceutical sciences ; Signal transduction ; Signaling ; Skin ; Skin - metabolism ; Stroma ; Transcription factors ; Tumorigenesis ; Tumors ; Urine ; Vascular endothelial growth factor ; Vascular Endothelial Growth Factor A - metabolism ; Wnt protein ; Wnt Proteins - metabolism ; Workers ; Xenografts ; Xenotransplantation</subject><ispartof>PloS one, 2010-12, Vol.5 (12), p.e15330</ispartof><rights>COPYRIGHT 2010 Public Library of Science</rights><rights>2010 Yasuniwa et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://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>Yasuniwa et al. 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c757t-d6065d058b83bf559e66a52b4b106a02920bf4469532f668eee746d464b365bc3</citedby><cites>FETCH-LOGICAL-c757t-d6065d058b83bf559e66a52b4b106a02920bf4469532f668eee746d464b365bc3</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/PMC3009728/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3009728/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21203463$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yasuniwa, Yoshihiro</creatorcontrib><creatorcontrib>Izumi, Hiroto</creatorcontrib><creatorcontrib>Wang, Ke-Yong</creatorcontrib><creatorcontrib>Shimajiri, Shohei</creatorcontrib><creatorcontrib>Sasaguri, Yasuyuki</creatorcontrib><creatorcontrib>Kawai, Kazuaki</creatorcontrib><creatorcontrib>Kasai, Hiroshi</creatorcontrib><creatorcontrib>Shimada, Takashi</creatorcontrib><creatorcontrib>Miyake, Koichi</creatorcontrib><creatorcontrib>Kashiwagi, Eiji</creatorcontrib><creatorcontrib>Hirano, Gen</creatorcontrib><creatorcontrib>Kidani, Akihiko</creatorcontrib><creatorcontrib>Akiyama, Masaki</creatorcontrib><creatorcontrib>Han, Bin</creatorcontrib><creatorcontrib>Wu, Ying</creatorcontrib><creatorcontrib>Ieiri, Ichiro</creatorcontrib><creatorcontrib>Higuchi, Shun</creatorcontrib><creatorcontrib>Kohno, Kimitoshi</creatorcontrib><title>Circadian disruption accelerates tumor growth and angio/stromagenesis through a Wnt signaling pathway</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Epidemiologic studies show a high incidence of cancer in shift workers, suggesting a possible relationship between circadian rhythms and tumorigenesis. However, the precise molecular mechanism played by circadian rhythms in tumor progression is not known. To identify the possible mechanisms underlying tumor progression related to circadian rhythms, we set up nude mouse xenograft models. HeLa cells were injected in nude mice and nude mice were moved to two different cases, one case is exposed to a 24-hour light cycle (L/L), the other is a more "normal" 12-hour light/dark cycle (L/D). We found a significant increase in tumor volume in the L/L group compared with the L/D group. In addition, tumor microvessels and stroma were strongly increased in L/L mice. Although there was a hypervascularization in L/L tumors, there was no associated increase in the production of vascular endothelial cell growth factor (VEGF). DNA microarray analysis showed enhanced expression of WNT10A, and our subsequent study revealed that WNT10A stimulates the growth of both microvascular endothelial cells and fibroblasts in tumors from light-stressed mice, along with marked increases in angio/stromagenesis. Only the tumor stroma stained positive for WNT10A and WNT10A is also highly expressed in keloid dermal fibroblasts but not in normal dermal fibroblasts indicated that WNT10A may be a novel angio/stromagenic growth factor. These findings suggest that circadian disruption induces the progression of malignant tumors via a Wnt signaling pathway.</description><subject>Analysis</subject><subject>Animal models</subject><subject>Animals</subject><subject>Biochemistry</subject><subject>Biology</subject><subject>Cancer</subject><subject>Cancer research</subject><subject>Cell cycle</subject><subject>Circadian Rhythm</subject><subject>Circadian rhythms</subject><subject>Deoxyribonucleic acid</subject><subject>Development and progression</subject><subject>Disease Progression</subject><subject>DNA</subject><subject>DNA microarrays</subject><subject>DNA repair</subject><subject>Drug resistance</subject><subject>Endothelial cells</subject><subject>Environmental health</subject><subject>Epidemiology</subject><subject>Fibroblasts</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>Genes</subject><subject>Genetic research</subject><subject>Growth</subject><subject>HeLa Cells</subject><subject>Hospitals</subject><subject>Humans</subject><subject>Light</subject><subject>Male</subject><subject>Medicine</subject><subject>Metastasis</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Mice, Nude</subject><subject>Microvasculature</subject><subject>Molecular biology</subject><subject>Neoplasm Transplantation</subject><subject>Neoplasms - pathology</subject><subject>Neovascularization, Pathologic</subject><subject>Nerve Tissue Proteins - metabolism</subject><subject>Oncology</subject><subject>Pathology</subject><subject>Pharmaceutical sciences</subject><subject>Signal transduction</subject><subject>Signaling</subject><subject>Skin</subject><subject>Skin - metabolism</subject><subject>Stroma</subject><subject>Transcription factors</subject><subject>Tumorigenesis</subject><subject>Tumors</subject><subject>Urine</subject><subject>Vascular endothelial growth 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One</addtitle><date>2010-12-23</date><risdate>2010</risdate><volume>5</volume><issue>12</issue><spage>e15330</spage><pages>e15330-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Epidemiologic studies show a high incidence of cancer in shift workers, suggesting a possible relationship between circadian rhythms and tumorigenesis. However, the precise molecular mechanism played by circadian rhythms in tumor progression is not known. To identify the possible mechanisms underlying tumor progression related to circadian rhythms, we set up nude mouse xenograft models. HeLa cells were injected in nude mice and nude mice were moved to two different cases, one case is exposed to a 24-hour light cycle (L/L), the other is a more "normal" 12-hour light/dark cycle (L/D). We found a significant increase in tumor volume in the L/L group compared with the L/D group. In addition, tumor microvessels and stroma were strongly increased in L/L mice. Although there was a hypervascularization in L/L tumors, there was no associated increase in the production of vascular endothelial cell growth factor (VEGF). DNA microarray analysis showed enhanced expression of WNT10A, and our subsequent study revealed that WNT10A stimulates the growth of both microvascular endothelial cells and fibroblasts in tumors from light-stressed mice, along with marked increases in angio/stromagenesis. Only the tumor stroma stained positive for WNT10A and WNT10A is also highly expressed in keloid dermal fibroblasts but not in normal dermal fibroblasts indicated that WNT10A may be a novel angio/stromagenic growth factor. These findings suggest that circadian disruption induces the progression of malignant tumors via a Wnt signaling pathway.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21203463</pmid><doi>10.1371/journal.pone.0015330</doi><tpages>e15330</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2010-12, Vol.5 (12), p.e15330 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1296292816 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Analysis Animal models Animals Biochemistry Biology Cancer Cancer research Cell cycle Circadian Rhythm Circadian rhythms Deoxyribonucleic acid Development and progression Disease Progression DNA DNA microarrays DNA repair Drug resistance Endothelial cells Environmental health Epidemiology Fibroblasts Gene expression Gene Expression Regulation, Neoplastic Genes Genetic research Growth HeLa Cells Hospitals Humans Light Male Medicine Metastasis Mice Mice, Inbred BALB C Mice, Nude Microvasculature Molecular biology Neoplasm Transplantation Neoplasms - pathology Neovascularization, Pathologic Nerve Tissue Proteins - metabolism Oncology Pathology Pharmaceutical sciences Signal transduction Signaling Skin Skin - metabolism Stroma Transcription factors Tumorigenesis Tumors Urine Vascular endothelial growth factor Vascular Endothelial Growth Factor A - metabolism Wnt protein Wnt Proteins - metabolism Workers Xenografts Xenotransplantation |
| title | Circadian disruption accelerates tumor growth and angio/stromagenesis through a Wnt signaling pathway |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-10T12%3A30%3A14IST&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=Circadian%20disruption%20accelerates%20tumor%20growth%20and%20angio/stromagenesis%20through%20a%20Wnt%20signaling%20pathway&rft.jtitle=PloS%20one&rft.au=Yasuniwa,%20Yoshihiro&rft.date=2010-12-23&rft.volume=5&rft.issue=12&rft.spage=e15330&rft.pages=e15330-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0015330&rft_dat=%3Cgale_plos_%3EA473812122%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=1296292816&rft_id=info:pmid/21203463&rft_galeid=A473812122&rft_doaj_id=oai_doaj_org_article_754173dd31284f43b89d8c0c2c98b8b3&rfr_iscdi=true |