Pancreatic stellate cells reorganize matrix components and lead pancreatic cancer invasion via the function of Endo180
Specific cell populations leading the local invasion of cancer are called “leading cells”. However, the underlying mechanisms are unclear. Here, we identified leading cells in pancreatic cancer and determined how these cells lead and promote cancer cell invasion in the extracellular matrix (ECM). Us...
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| Veröffentlicht in: | Cancer letters 2018-01, Vol.412, p.143-154 |
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| creator | Koikawa, Kazuhiro Ohuchida, Kenoki Takesue, Shin Ando, Yohei Kibe, Shin Nakayama, Hiromichi Endo, Sho Abe, Toshiya Okumura, Takashi Horioka, Kohei Sada, Masafumi Iwamoto, Chika Moriyama, Taiki Nakata, Kohei Miyasaka, Yoshihiro Ohuchida, Riichi Manabe, Tatsuya Ohtsuka, Takao Nagai, Eishi Mizumoto, Kazuhiro Hashizume, Makoto Nakamura, Masafumi |
| description | Specific cell populations leading the local invasion of cancer are called “leading cells”. However, the underlying mechanisms are unclear. Here, we identified leading cells in pancreatic cancer and determined how these cells lead and promote cancer cell invasion in the extracellular matrix (ECM). Using three-dimensional matrix remodeling assay, we found that pancreatic stellate cells (PSCs) frequently invaded the collagen matrix with pancreatic cancer cells (PCCs), which invaded behind the invading PSCs. In addition, invading PSCs changed the alignment of collagen fibers, resulting in ECM remodeling and an increase in the parallel fibers along the direction of invading PSCs. Endo180 expression was higher in PSCs than in PCCs, Endo180 knockdown in PSCs attenuated the invasive abilities of PSCs and co-cultured PCCs, and decreased the expression level of phosphorylated myosin light chain 2 (MLC2). In mouse models, Endo180-knockdown PSCs suppressed tumor growth and changes in collagen fiber orientation in co-transplantation with PCCs. Our findings suggest that PSCs lead the local invasion of PCCs by physically remodeling the ECM, possibly via the function of Endo180, which reconstructs the actin cell skeleton by phosphorylation of MLC2.
•Pancreatic stellate cells (PSCs) lead pancreatic cancer cells (PCCs) invasion by extracellular matrix (ECM) remodeling.•Endo180 is related with invasive ability of leading PSCs via phosphorylation of myosin light chain 2 (MLC2).•Inhibition of Endo180 in PSCs suppressed the ability of ECM remodeling and consequently suppressed co-cultured PCCs invasion. |
| doi_str_mv | 10.1016/j.canlet.2017.10.010 |
| format | Article |
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•Pancreatic stellate cells (PSCs) lead pancreatic cancer cells (PCCs) invasion by extracellular matrix (ECM) remodeling.•Endo180 is related with invasive ability of leading PSCs via phosphorylation of myosin light chain 2 (MLC2).•Inhibition of Endo180 in PSCs suppressed the ability of ECM remodeling and consequently suppressed co-cultured PCCs invasion.</description><identifier>ISSN: 0304-3835</identifier><identifier>EISSN: 1872-7980</identifier><identifier>DOI: 10.1016/j.canlet.2017.10.010</identifier><identifier>PMID: 29061505</identifier><language>eng</language><publisher>Ireland: Elsevier B.V</publisher><subject>Actin ; Animal models ; Breast cancer ; Cardiac Myosins - metabolism ; Cell division ; Cell Line, Tumor ; Collagen ; Collagen - chemistry ; Endo180 ; Extracellular matrix ; Extracellular Matrix - chemistry ; Extracellular matrix remodeling ; Fabric analysis ; Fiber orientation ; Fibers ; Fibroblasts ; Humans ; Invasiveness ; Leading cells ; Medical prognosis ; Metastasis ; Myosin ; Myosin Light Chains - metabolism ; Neoplasm Invasiveness ; Pancreatic cancer ; Pancreatic Neoplasms - pathology ; Pancreatic stellate cells ; Pancreatic Stellate Cells - physiology ; Parallel fibers ; Phosphorylation ; Receptors, Mitogen - physiology ; Rodents ; Signal transduction ; Stellate cells ; Transplantation</subject><ispartof>Cancer letters, 2018-01, Vol.412, p.143-154</ispartof><rights>2017 Elsevier B.V.</rights><rights>Copyright © 2017 Elsevier B.V. All rights reserved.</rights><rights>2017. Elsevier B.V.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c586t-8d7480f876019ff007dadf57a648dd75437b44dca2849ade8d087aa850d594653</citedby><cites>FETCH-LOGICAL-c586t-8d7480f876019ff007dadf57a648dd75437b44dca2849ade8d087aa850d594653</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0304383517306444$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29061505$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Koikawa, Kazuhiro</creatorcontrib><creatorcontrib>Ohuchida, Kenoki</creatorcontrib><creatorcontrib>Takesue, Shin</creatorcontrib><creatorcontrib>Ando, Yohei</creatorcontrib><creatorcontrib>Kibe, Shin</creatorcontrib><creatorcontrib>Nakayama, Hiromichi</creatorcontrib><creatorcontrib>Endo, Sho</creatorcontrib><creatorcontrib>Abe, Toshiya</creatorcontrib><creatorcontrib>Okumura, Takashi</creatorcontrib><creatorcontrib>Horioka, Kohei</creatorcontrib><creatorcontrib>Sada, Masafumi</creatorcontrib><creatorcontrib>Iwamoto, Chika</creatorcontrib><creatorcontrib>Moriyama, Taiki</creatorcontrib><creatorcontrib>Nakata, Kohei</creatorcontrib><creatorcontrib>Miyasaka, Yoshihiro</creatorcontrib><creatorcontrib>Ohuchida, Riichi</creatorcontrib><creatorcontrib>Manabe, Tatsuya</creatorcontrib><creatorcontrib>Ohtsuka, Takao</creatorcontrib><creatorcontrib>Nagai, Eishi</creatorcontrib><creatorcontrib>Mizumoto, Kazuhiro</creatorcontrib><creatorcontrib>Hashizume, Makoto</creatorcontrib><creatorcontrib>Nakamura, Masafumi</creatorcontrib><title>Pancreatic stellate cells reorganize matrix components and lead pancreatic cancer invasion via the function of Endo180</title><title>Cancer letters</title><addtitle>Cancer Lett</addtitle><description>Specific cell populations leading the local invasion of cancer are called “leading cells”. However, the underlying mechanisms are unclear. Here, we identified leading cells in pancreatic cancer and determined how these cells lead and promote cancer cell invasion in the extracellular matrix (ECM). Using three-dimensional matrix remodeling assay, we found that pancreatic stellate cells (PSCs) frequently invaded the collagen matrix with pancreatic cancer cells (PCCs), which invaded behind the invading PSCs. In addition, invading PSCs changed the alignment of collagen fibers, resulting in ECM remodeling and an increase in the parallel fibers along the direction of invading PSCs. Endo180 expression was higher in PSCs than in PCCs, Endo180 knockdown in PSCs attenuated the invasive abilities of PSCs and co-cultured PCCs, and decreased the expression level of phosphorylated myosin light chain 2 (MLC2). In mouse models, Endo180-knockdown PSCs suppressed tumor growth and changes in collagen fiber orientation in co-transplantation with PCCs. Our findings suggest that PSCs lead the local invasion of PCCs by physically remodeling the ECM, possibly via the function of Endo180, which reconstructs the actin cell skeleton by phosphorylation of MLC2.
•Pancreatic stellate cells (PSCs) lead pancreatic cancer cells (PCCs) invasion by extracellular matrix (ECM) remodeling.•Endo180 is related with invasive ability of leading PSCs via phosphorylation of myosin light chain 2 (MLC2).•Inhibition of Endo180 in PSCs suppressed the ability of ECM remodeling and consequently suppressed co-cultured PCCs invasion.</description><subject>Actin</subject><subject>Animal models</subject><subject>Breast cancer</subject><subject>Cardiac Myosins - metabolism</subject><subject>Cell division</subject><subject>Cell Line, Tumor</subject><subject>Collagen</subject><subject>Collagen - chemistry</subject><subject>Endo180</subject><subject>Extracellular matrix</subject><subject>Extracellular Matrix - chemistry</subject><subject>Extracellular matrix remodeling</subject><subject>Fabric analysis</subject><subject>Fiber orientation</subject><subject>Fibers</subject><subject>Fibroblasts</subject><subject>Humans</subject><subject>Invasiveness</subject><subject>Leading cells</subject><subject>Medical prognosis</subject><subject>Metastasis</subject><subject>Myosin</subject><subject>Myosin Light Chains - metabolism</subject><subject>Neoplasm Invasiveness</subject><subject>Pancreatic cancer</subject><subject>Pancreatic Neoplasms - pathology</subject><subject>Pancreatic stellate cells</subject><subject>Pancreatic Stellate Cells - physiology</subject><subject>Parallel fibers</subject><subject>Phosphorylation</subject><subject>Receptors, Mitogen - physiology</subject><subject>Rodents</subject><subject>Signal transduction</subject><subject>Stellate cells</subject><subject>Transplantation</subject><issn>0304-3835</issn><issn>1872-7980</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kUuLFDEUhYMoTjv6D0QCbtxUe9OVVFIbQYbxAQO60HW4k9zSNNVJm6Qa9debokcFF64uHL5zX4expwK2AsTwcr91GGeq2x0I3aQtCLjHNsLoXadHA_fZBnqQXW96dcEelbIHACW1esgudiMMQoHasNNHjC4T1uB4qTTPWIm7VgvPlPIXjOEn8QPWHL5zlw7HFCnWwjF6PhN6fvzrb_s4yjzEE5aQIj8F5PUr8WmJrq5Cmvh19EkYeMweTDgXenJXL9nnN9efrt51Nx_evr96fdM5ZYbaGa-lgcnoAcQ4TQDao5-UxkEa77WSvb6V0jvcGTmiJ-PBaESjwKtRDqq_ZC_OfY85fVuoVHsIZT0PI6WlWDEqBYMErRv6_B90n5Yc23aNGsbRyKGXjZJnyuVUSqbJHnM4YP5hBdg1F7u351zsmsuqtlya7dld8-X2QP6P6XcQDXh1Bqh94xQo2-ICtX_6kMlV61P4_4RfZWegow</recordid><startdate>20180101</startdate><enddate>20180101</enddate><creator>Koikawa, Kazuhiro</creator><creator>Ohuchida, Kenoki</creator><creator>Takesue, Shin</creator><creator>Ando, Yohei</creator><creator>Kibe, Shin</creator><creator>Nakayama, Hiromichi</creator><creator>Endo, Sho</creator><creator>Abe, Toshiya</creator><creator>Okumura, Takashi</creator><creator>Horioka, Kohei</creator><creator>Sada, Masafumi</creator><creator>Iwamoto, Chika</creator><creator>Moriyama, Taiki</creator><creator>Nakata, Kohei</creator><creator>Miyasaka, Yoshihiro</creator><creator>Ohuchida, Riichi</creator><creator>Manabe, Tatsuya</creator><creator>Ohtsuka, Takao</creator><creator>Nagai, Eishi</creator><creator>Mizumoto, Kazuhiro</creator><creator>Hashizume, Makoto</creator><creator>Nakamura, Masafumi</creator><general>Elsevier B.V</general><general>Elsevier Limited</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>7TO</scope><scope>7U9</scope><scope>H94</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>7X8</scope></search><sort><creationdate>20180101</creationdate><title>Pancreatic stellate cells reorganize matrix components and lead pancreatic cancer invasion via the function of Endo180</title><author>Koikawa, Kazuhiro ; Ohuchida, Kenoki ; Takesue, Shin ; Ando, Yohei ; Kibe, Shin ; Nakayama, Hiromichi ; Endo, Sho ; Abe, Toshiya ; Okumura, Takashi ; Horioka, Kohei ; Sada, Masafumi ; Iwamoto, Chika ; Moriyama, Taiki ; Nakata, Kohei ; Miyasaka, Yoshihiro ; Ohuchida, Riichi ; Manabe, Tatsuya ; Ohtsuka, Takao ; Nagai, Eishi ; Mizumoto, Kazuhiro ; Hashizume, Makoto ; Nakamura, Masafumi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c586t-8d7480f876019ff007dadf57a648dd75437b44dca2849ade8d087aa850d594653</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Actin</topic><topic>Animal models</topic><topic>Breast cancer</topic><topic>Cardiac Myosins - metabolism</topic><topic>Cell division</topic><topic>Cell Line, Tumor</topic><topic>Collagen</topic><topic>Collagen - chemistry</topic><topic>Endo180</topic><topic>Extracellular matrix</topic><topic>Extracellular Matrix - chemistry</topic><topic>Extracellular matrix remodeling</topic><topic>Fabric analysis</topic><topic>Fiber orientation</topic><topic>Fibers</topic><topic>Fibroblasts</topic><topic>Humans</topic><topic>Invasiveness</topic><topic>Leading cells</topic><topic>Medical prognosis</topic><topic>Metastasis</topic><topic>Myosin</topic><topic>Myosin Light Chains - metabolism</topic><topic>Neoplasm Invasiveness</topic><topic>Pancreatic cancer</topic><topic>Pancreatic Neoplasms - pathology</topic><topic>Pancreatic stellate cells</topic><topic>Pancreatic Stellate Cells - physiology</topic><topic>Parallel fibers</topic><topic>Phosphorylation</topic><topic>Receptors, Mitogen - physiology</topic><topic>Rodents</topic><topic>Signal transduction</topic><topic>Stellate cells</topic><topic>Transplantation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Koikawa, Kazuhiro</creatorcontrib><creatorcontrib>Ohuchida, Kenoki</creatorcontrib><creatorcontrib>Takesue, Shin</creatorcontrib><creatorcontrib>Ando, Yohei</creatorcontrib><creatorcontrib>Kibe, Shin</creatorcontrib><creatorcontrib>Nakayama, Hiromichi</creatorcontrib><creatorcontrib>Endo, Sho</creatorcontrib><creatorcontrib>Abe, Toshiya</creatorcontrib><creatorcontrib>Okumura, Takashi</creatorcontrib><creatorcontrib>Horioka, Kohei</creatorcontrib><creatorcontrib>Sada, Masafumi</creatorcontrib><creatorcontrib>Iwamoto, Chika</creatorcontrib><creatorcontrib>Moriyama, Taiki</creatorcontrib><creatorcontrib>Nakata, Kohei</creatorcontrib><creatorcontrib>Miyasaka, Yoshihiro</creatorcontrib><creatorcontrib>Ohuchida, Riichi</creatorcontrib><creatorcontrib>Manabe, Tatsuya</creatorcontrib><creatorcontrib>Ohtsuka, Takao</creatorcontrib><creatorcontrib>Nagai, Eishi</creatorcontrib><creatorcontrib>Mizumoto, Kazuhiro</creatorcontrib><creatorcontrib>Hashizume, Makoto</creatorcontrib><creatorcontrib>Nakamura, Masafumi</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>MEDLINE - Academic</collection><jtitle>Cancer letters</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Koikawa, Kazuhiro</au><au>Ohuchida, Kenoki</au><au>Takesue, Shin</au><au>Ando, Yohei</au><au>Kibe, Shin</au><au>Nakayama, Hiromichi</au><au>Endo, Sho</au><au>Abe, Toshiya</au><au>Okumura, Takashi</au><au>Horioka, Kohei</au><au>Sada, Masafumi</au><au>Iwamoto, Chika</au><au>Moriyama, Taiki</au><au>Nakata, Kohei</au><au>Miyasaka, Yoshihiro</au><au>Ohuchida, Riichi</au><au>Manabe, Tatsuya</au><au>Ohtsuka, Takao</au><au>Nagai, Eishi</au><au>Mizumoto, Kazuhiro</au><au>Hashizume, Makoto</au><au>Nakamura, Masafumi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pancreatic stellate cells reorganize matrix components and lead pancreatic cancer invasion via the function of Endo180</atitle><jtitle>Cancer letters</jtitle><addtitle>Cancer Lett</addtitle><date>2018-01-01</date><risdate>2018</risdate><volume>412</volume><spage>143</spage><epage>154</epage><pages>143-154</pages><issn>0304-3835</issn><eissn>1872-7980</eissn><abstract>Specific cell populations leading the local invasion of cancer are called “leading cells”. However, the underlying mechanisms are unclear. Here, we identified leading cells in pancreatic cancer and determined how these cells lead and promote cancer cell invasion in the extracellular matrix (ECM). Using three-dimensional matrix remodeling assay, we found that pancreatic stellate cells (PSCs) frequently invaded the collagen matrix with pancreatic cancer cells (PCCs), which invaded behind the invading PSCs. In addition, invading PSCs changed the alignment of collagen fibers, resulting in ECM remodeling and an increase in the parallel fibers along the direction of invading PSCs. Endo180 expression was higher in PSCs than in PCCs, Endo180 knockdown in PSCs attenuated the invasive abilities of PSCs and co-cultured PCCs, and decreased the expression level of phosphorylated myosin light chain 2 (MLC2). In mouse models, Endo180-knockdown PSCs suppressed tumor growth and changes in collagen fiber orientation in co-transplantation with PCCs. Our findings suggest that PSCs lead the local invasion of PCCs by physically remodeling the ECM, possibly via the function of Endo180, which reconstructs the actin cell skeleton by phosphorylation of MLC2.
•Pancreatic stellate cells (PSCs) lead pancreatic cancer cells (PCCs) invasion by extracellular matrix (ECM) remodeling.•Endo180 is related with invasive ability of leading PSCs via phosphorylation of myosin light chain 2 (MLC2).•Inhibition of Endo180 in PSCs suppressed the ability of ECM remodeling and consequently suppressed co-cultured PCCs invasion.</abstract><cop>Ireland</cop><pub>Elsevier B.V</pub><pmid>29061505</pmid><doi>10.1016/j.canlet.2017.10.010</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Cancer letters, 2018-01, Vol.412, p.143-154 |
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| subjects | Actin Animal models Breast cancer Cardiac Myosins - metabolism Cell division Cell Line, Tumor Collagen Collagen - chemistry Endo180 Extracellular matrix Extracellular Matrix - chemistry Extracellular matrix remodeling Fabric analysis Fiber orientation Fibers Fibroblasts Humans Invasiveness Leading cells Medical prognosis Metastasis Myosin Myosin Light Chains - metabolism Neoplasm Invasiveness Pancreatic cancer Pancreatic Neoplasms - pathology Pancreatic stellate cells Pancreatic Stellate Cells - physiology Parallel fibers Phosphorylation Receptors, Mitogen - physiology Rodents Signal transduction Stellate cells Transplantation |
| title | Pancreatic stellate cells reorganize matrix components and lead pancreatic cancer invasion via the function of Endo180 |
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