The role of the immunoescape in colorectal cancer liver metastasis
The expression of programmed death 1 (PD-1) and programmed death-ligand 1 (PD-L1) indicate the efficacy of anti-PD-1/PD-L1 therapy in colorectal cancer (CRC), but are less useful for monitoring the efficacy of therapy of CRC liver metastasis (CRLM). This study investigated the effects of immune mole...
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| Veröffentlicht in: | PloS one 2021-11, Vol.16 (11), p.e0259940-e0259940 |
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| creator | Takasu, Chie Yamashita, Shoko Morine, Yuji Yoshikawa, Kozo Tokunaga, Takuya Nishi, Masaaki Kashihara, Hideya Yoshimoto, Toshiaki Shimada, Mitsuo |
| description | The expression of programmed death 1 (PD-1) and programmed death-ligand 1 (PD-L1) indicate the efficacy of anti-PD-1/PD-L1 therapy in colorectal cancer (CRC), but are less useful for monitoring the efficacy of therapy of CRC liver metastasis (CRLM). This study investigated the effects of immune molecules on the prognosis of CRLM. We enrolled 71 patients with CRLM who underwent curative resection for CRC. We used immunohistochemistry to analyze the expression of PD-1, PD-L1, indoleamine-pyrrole 2,3-dioxygenase (IDO), and CD163 (a marker of tumor-associated macrophages [TAMs]) in metastatic tumors. The immune molecules PD-1, PD-L1, IDO, and TAMs were expressed in 32.3%, 47.8%, 45.0%, and 47.9% of metastatic CRC samples, respectively. The 5-year overall survival rates associated with immune molecule-positive groups were significantly better than in the negative groups (PD-1: 87.7% vs 53.2%, p = 0.023; PD-L1: 82.4% vs 42.3%, p = 0.007; IDO: 80.7% vs 43.5%, p = 0.007; TAMs: 82.6% vs 48.0%, p = 0.005). Multivariate analysis revealed PD-1 expression (p = 0.032, hazard ratio: 0.19), IDO expression (p = 0.049, hazard ratio: 0.37), and tumor differentiation (p |
| doi_str_mv | 10.1371/journal.pone.0259940 |
| format | Article |
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This study investigated the effects of immune molecules on the prognosis of CRLM. We enrolled 71 patients with CRLM who underwent curative resection for CRC. We used immunohistochemistry to analyze the expression of PD-1, PD-L1, indoleamine-pyrrole 2,3-dioxygenase (IDO), and CD163 (a marker of tumor-associated macrophages [TAMs]) in metastatic tumors. The immune molecules PD-1, PD-L1, IDO, and TAMs were expressed in 32.3%, 47.8%, 45.0%, and 47.9% of metastatic CRC samples, respectively. The 5-year overall survival rates associated with immune molecule-positive groups were significantly better than in the negative groups (PD-1: 87.7% vs 53.2%, p = 0.023; PD-L1: 82.4% vs 42.3%, p = 0.007; IDO: 80.7% vs 43.5%, p = 0.007; TAMs: 82.6% vs 48.0%, p = 0.005). Multivariate analysis revealed PD-1 expression (p = 0.032, hazard ratio: 0.19), IDO expression (p = 0.049, hazard ratio: 0.37), and tumor differentiation (p<0.001, hazard ratio: 0.02) as independent prognostic indicators. PD-1 and TAMs in metastases were associated with less aggressive features such as smaller tumors. Furthermore, TAMs positively and significantly correlated with PD-1 expression (p = 0.011), PD-L1 expression (p = 0.024), and tended to correlate with IDO expression (p = 0.078). PD-1, PD-L1, IDO, and TAMs in CRLM were associated with less aggressive features and better prognosis of patients with CRC, indicating adaptive antitumor immunity vs immune tolerance. These molecules may therefore serve as prognostic markers for CRLM.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0259940</identifier><identifier>PMID: 34797860</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adaptive Immunity ; Adult ; Aged ; Aged, 80 and over ; Antigens, CD - genetics ; Antigens, CD - metabolism ; Antigens, Differentiation, Myelomonocytic - genetics ; Antigens, Differentiation, Myelomonocytic - metabolism ; B7-H1 Antigen - genetics ; B7-H1 Antigen - metabolism ; Biology and Life Sciences ; Biomarkers, Tumor - genetics ; Cancer ; CD163 antigen ; Colonic Neoplasms ; Colorectal cancer ; Colorectal carcinoma ; Colorectal Neoplasms - complications ; Colorectal Neoplasms - metabolism ; Diagnosis ; Diagnostic Tests, Routine ; Evaluation ; Female ; Gene Expression - genetics ; Health hazards ; Humans ; Immune system ; Immune Tolerance ; Immunohistochemistry ; Immunological tolerance ; Indoleamine-Pyrrole 2,3,-Dioxygenase - genetics ; Japan ; Liver ; Liver - cytology ; Liver cancer ; Liver Neoplasms ; Macrophages ; Male ; Markers ; Medical prognosis ; Medicine and Health Sciences ; Metastases ; Metastasis ; Middle Aged ; Monoclonal antibodies ; Multivariate analysis ; Neoplasm Metastasis - immunology ; Neoplasm Metastasis - physiopathology ; PD-1 protein ; PD-L1 protein ; Prognosis ; Programmed Cell Death 1 Receptor - genetics ; Programmed Cell Death 1 Receptor - metabolism ; Receptors, Cell Surface - genetics ; Receptors, Cell Surface - metabolism ; Rectal Neoplasms ; Supervision ; Surgery ; Survival ; Transcriptome - genetics ; Tryptophan 2,3-dioxygenase ; Tumor-Associated Macrophages - immunology ; Tumor-Associated Macrophages - metabolism ; Tumors</subject><ispartof>PloS one, 2021-11, Vol.16 (11), p.e0259940-e0259940</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Takasu 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>2021 Takasu et al 2021 Takasu et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c736t-de0d7990331de6a4119644de03fbb5fc247f7f4fa5fa7dbc96c9f92b72ef55ea3</citedby><cites>FETCH-LOGICAL-c736t-de0d7990331de6a4119644de03fbb5fc247f7f4fa5fa7dbc96c9f92b72ef55ea3</cites><orcidid>0000-0001-6438-2763</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8604373/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8604373/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23865,27923,27924,53790,53792,79371,79372</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34797860$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Gold, Jason S.</contributor><creatorcontrib>Takasu, Chie</creatorcontrib><creatorcontrib>Yamashita, Shoko</creatorcontrib><creatorcontrib>Morine, Yuji</creatorcontrib><creatorcontrib>Yoshikawa, Kozo</creatorcontrib><creatorcontrib>Tokunaga, Takuya</creatorcontrib><creatorcontrib>Nishi, Masaaki</creatorcontrib><creatorcontrib>Kashihara, Hideya</creatorcontrib><creatorcontrib>Yoshimoto, Toshiaki</creatorcontrib><creatorcontrib>Shimada, Mitsuo</creatorcontrib><title>The role of the immunoescape in colorectal cancer liver metastasis</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The expression of programmed death 1 (PD-1) and programmed death-ligand 1 (PD-L1) indicate the efficacy of anti-PD-1/PD-L1 therapy in colorectal cancer (CRC), but are less useful for monitoring the efficacy of therapy of CRC liver metastasis (CRLM). This study investigated the effects of immune molecules on the prognosis of CRLM. We enrolled 71 patients with CRLM who underwent curative resection for CRC. We used immunohistochemistry to analyze the expression of PD-1, PD-L1, indoleamine-pyrrole 2,3-dioxygenase (IDO), and CD163 (a marker of tumor-associated macrophages [TAMs]) in metastatic tumors. The immune molecules PD-1, PD-L1, IDO, and TAMs were expressed in 32.3%, 47.8%, 45.0%, and 47.9% of metastatic CRC samples, respectively. The 5-year overall survival rates associated with immune molecule-positive groups were significantly better than in the negative groups (PD-1: 87.7% vs 53.2%, p = 0.023; PD-L1: 82.4% vs 42.3%, p = 0.007; IDO: 80.7% vs 43.5%, p = 0.007; TAMs: 82.6% vs 48.0%, p = 0.005). Multivariate analysis revealed PD-1 expression (p = 0.032, hazard ratio: 0.19), IDO expression (p = 0.049, hazard ratio: 0.37), and tumor differentiation (p<0.001, hazard ratio: 0.02) as independent prognostic indicators. PD-1 and TAMs in metastases were associated with less aggressive features such as smaller tumors. Furthermore, TAMs positively and significantly correlated with PD-1 expression (p = 0.011), PD-L1 expression (p = 0.024), and tended to correlate with IDO expression (p = 0.078). PD-1, PD-L1, IDO, and TAMs in CRLM were associated with less aggressive features and better prognosis of patients with CRC, indicating adaptive antitumor immunity vs immune tolerance. These molecules may therefore serve as prognostic markers for CRLM.</description><subject>Adaptive Immunity</subject><subject>Adult</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Antigens, CD - genetics</subject><subject>Antigens, CD - metabolism</subject><subject>Antigens, Differentiation, Myelomonocytic - genetics</subject><subject>Antigens, Differentiation, Myelomonocytic - metabolism</subject><subject>B7-H1 Antigen - genetics</subject><subject>B7-H1 Antigen - metabolism</subject><subject>Biology and Life Sciences</subject><subject>Biomarkers, Tumor - genetics</subject><subject>Cancer</subject><subject>CD163 antigen</subject><subject>Colonic Neoplasms</subject><subject>Colorectal cancer</subject><subject>Colorectal carcinoma</subject><subject>Colorectal Neoplasms - complications</subject><subject>Colorectal Neoplasms - metabolism</subject><subject>Diagnosis</subject><subject>Diagnostic Tests, Routine</subject><subject>Evaluation</subject><subject>Female</subject><subject>Gene Expression - genetics</subject><subject>Health hazards</subject><subject>Humans</subject><subject>Immune system</subject><subject>Immune Tolerance</subject><subject>Immunohistochemistry</subject><subject>Immunological tolerance</subject><subject>Indoleamine-Pyrrole 2,3,-Dioxygenase - genetics</subject><subject>Japan</subject><subject>Liver</subject><subject>Liver - cytology</subject><subject>Liver cancer</subject><subject>Liver Neoplasms</subject><subject>Macrophages</subject><subject>Male</subject><subject>Markers</subject><subject>Medical prognosis</subject><subject>Medicine and Health Sciences</subject><subject>Metastases</subject><subject>Metastasis</subject><subject>Middle Aged</subject><subject>Monoclonal antibodies</subject><subject>Multivariate analysis</subject><subject>Neoplasm Metastasis - immunology</subject><subject>Neoplasm Metastasis - physiopathology</subject><subject>PD-1 protein</subject><subject>PD-L1 protein</subject><subject>Prognosis</subject><subject>Programmed Cell Death 1 Receptor - genetics</subject><subject>Programmed Cell Death 1 Receptor - metabolism</subject><subject>Receptors, Cell Surface - genetics</subject><subject>Receptors, Cell Surface - metabolism</subject><subject>Rectal Neoplasms</subject><subject>Supervision</subject><subject>Surgery</subject><subject>Survival</subject><subject>Transcriptome - genetics</subject><subject>Tryptophan 2,3-dioxygenase</subject><subject>Tumor-Associated Macrophages - immunology</subject><subject>Tumor-Associated Macrophages - metabolism</subject><subject>Tumors</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</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>eNqNkl2L1DAUhoso7jr6D0QLgujFjEnz1dwI6-LHwMKCrt6GND2ZyZI2Y9Iu-u_NON1lKnshLW1y8pw3OSdvUTzHaIWJwO-uwxh77Ve70MMKVUxKih4Up1iSaskrRB4ejU-KJyldI8RIzfnj4oRQIUXN0Wnx4WoLZQweymDLIY9d1419gGT0Lk_60gQfIphB-9Lo3kAsvbvJ3w4GnfLr0tPikdU-wbPpvyi-f_p4df5leXH5eX1-drE0gvBh2QJqhZSIENwC1xRjySnNUWKbhllTUWGFpVYzq0XbGMmNtLJqRAWWMdBkUbw86O58SGoqP6l95UwQxnEm1geiDfpa7aLrdPytgnbqbyDEjdJxcMaDIgxj2wJoyS1tcjOwYKKVbaNRQ5p6r_V-2m1sOmgN9EPUfiY6X-ndVm3CjcptpUSQLPBmEojh5whpUJ1LBrzXPYQxn5sjVNUMU5nRV_-g91c3URudC3C9DXlfsxdVZ7wmWNQyX_WiWN1D5aeFzpnsFetyfJbwdpaQmQF-DRs9pqTW377-P3v5Y86-PmK3oP2wTcGPgwt9moP0AJoYUopg75qMkdpb_bYbam91NVk9p704vqC7pFtvkz9vr_k6</recordid><startdate>20211119</startdate><enddate>20211119</enddate><creator>Takasu, Chie</creator><creator>Yamashita, Shoko</creator><creator>Morine, Yuji</creator><creator>Yoshikawa, Kozo</creator><creator>Tokunaga, Takuya</creator><creator>Nishi, Masaaki</creator><creator>Kashihara, Hideya</creator><creator>Yoshimoto, Toshiaki</creator><creator>Shimada, Mitsuo</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>AEUYN</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>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-6438-2763</orcidid></search><sort><creationdate>20211119</creationdate><title>The role of the immunoescape in colorectal cancer liver metastasis</title><author>Takasu, Chie ; Yamashita, Shoko ; Morine, Yuji ; Yoshikawa, Kozo ; Tokunaga, Takuya ; Nishi, Masaaki ; Kashihara, Hideya ; Yoshimoto, Toshiaki ; Shimada, Mitsuo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c736t-de0d7990331de6a4119644de03fbb5fc247f7f4fa5fa7dbc96c9f92b72ef55ea3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Adaptive Immunity</topic><topic>Adult</topic><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Antigens, CD - genetics</topic><topic>Antigens, CD - metabolism</topic><topic>Antigens, Differentiation, Myelomonocytic - genetics</topic><topic>Antigens, Differentiation, Myelomonocytic - metabolism</topic><topic>B7-H1 Antigen - genetics</topic><topic>B7-H1 Antigen - metabolism</topic><topic>Biology and Life Sciences</topic><topic>Biomarkers, Tumor - genetics</topic><topic>Cancer</topic><topic>CD163 antigen</topic><topic>Colonic Neoplasms</topic><topic>Colorectal cancer</topic><topic>Colorectal carcinoma</topic><topic>Colorectal Neoplasms - complications</topic><topic>Colorectal Neoplasms - metabolism</topic><topic>Diagnosis</topic><topic>Diagnostic Tests, Routine</topic><topic>Evaluation</topic><topic>Female</topic><topic>Gene Expression - genetics</topic><topic>Health hazards</topic><topic>Humans</topic><topic>Immune system</topic><topic>Immune Tolerance</topic><topic>Immunohistochemistry</topic><topic>Immunological tolerance</topic><topic>Indoleamine-Pyrrole 2,3,-Dioxygenase - genetics</topic><topic>Japan</topic><topic>Liver</topic><topic>Liver - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Takasu, Chie</au><au>Yamashita, Shoko</au><au>Morine, Yuji</au><au>Yoshikawa, Kozo</au><au>Tokunaga, Takuya</au><au>Nishi, Masaaki</au><au>Kashihara, Hideya</au><au>Yoshimoto, Toshiaki</au><au>Shimada, Mitsuo</au><au>Gold, Jason S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The role of the immunoescape in colorectal cancer liver metastasis</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2021-11-19</date><risdate>2021</risdate><volume>16</volume><issue>11</issue><spage>e0259940</spage><epage>e0259940</epage><pages>e0259940-e0259940</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The expression of programmed death 1 (PD-1) and programmed death-ligand 1 (PD-L1) indicate the efficacy of anti-PD-1/PD-L1 therapy in colorectal cancer (CRC), but are less useful for monitoring the efficacy of therapy of CRC liver metastasis (CRLM). This study investigated the effects of immune molecules on the prognosis of CRLM. We enrolled 71 patients with CRLM who underwent curative resection for CRC. We used immunohistochemistry to analyze the expression of PD-1, PD-L1, indoleamine-pyrrole 2,3-dioxygenase (IDO), and CD163 (a marker of tumor-associated macrophages [TAMs]) in metastatic tumors. The immune molecules PD-1, PD-L1, IDO, and TAMs were expressed in 32.3%, 47.8%, 45.0%, and 47.9% of metastatic CRC samples, respectively. The 5-year overall survival rates associated with immune molecule-positive groups were significantly better than in the negative groups (PD-1: 87.7% vs 53.2%, p = 0.023; PD-L1: 82.4% vs 42.3%, p = 0.007; IDO: 80.7% vs 43.5%, p = 0.007; TAMs: 82.6% vs 48.0%, p = 0.005). Multivariate analysis revealed PD-1 expression (p = 0.032, hazard ratio: 0.19), IDO expression (p = 0.049, hazard ratio: 0.37), and tumor differentiation (p<0.001, hazard ratio: 0.02) as independent prognostic indicators. PD-1 and TAMs in metastases were associated with less aggressive features such as smaller tumors. Furthermore, TAMs positively and significantly correlated with PD-1 expression (p = 0.011), PD-L1 expression (p = 0.024), and tended to correlate with IDO expression (p = 0.078). PD-1, PD-L1, IDO, and TAMs in CRLM were associated with less aggressive features and better prognosis of patients with CRC, indicating adaptive antitumor immunity vs immune tolerance. These molecules may therefore serve as prognostic markers for CRLM.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>34797860</pmid><doi>10.1371/journal.pone.0259940</doi><tpages>e0259940</tpages><orcidid>https://orcid.org/0000-0001-6438-2763</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2021-11, Vol.16 (11), p.e0259940-e0259940 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_2599573561 |
| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; PubMed Central; Directory of Open Access Journals; Free Full-Text Journals in Chemistry; EZB Electronic Journals Library |
| subjects | Adaptive Immunity Adult Aged Aged, 80 and over Antigens, CD - genetics Antigens, CD - metabolism Antigens, Differentiation, Myelomonocytic - genetics Antigens, Differentiation, Myelomonocytic - metabolism B7-H1 Antigen - genetics B7-H1 Antigen - metabolism Biology and Life Sciences Biomarkers, Tumor - genetics Cancer CD163 antigen Colonic Neoplasms Colorectal cancer Colorectal carcinoma Colorectal Neoplasms - complications Colorectal Neoplasms - metabolism Diagnosis Diagnostic Tests, Routine Evaluation Female Gene Expression - genetics Health hazards Humans Immune system Immune Tolerance Immunohistochemistry Immunological tolerance Indoleamine-Pyrrole 2,3,-Dioxygenase - genetics Japan Liver Liver - cytology Liver cancer Liver Neoplasms Macrophages Male Markers Medical prognosis Medicine and Health Sciences Metastases Metastasis Middle Aged Monoclonal antibodies Multivariate analysis Neoplasm Metastasis - immunology Neoplasm Metastasis - physiopathology PD-1 protein PD-L1 protein Prognosis Programmed Cell Death 1 Receptor - genetics Programmed Cell Death 1 Receptor - metabolism Receptors, Cell Surface - genetics Receptors, Cell Surface - metabolism Rectal Neoplasms Supervision Surgery Survival Transcriptome - genetics Tryptophan 2,3-dioxygenase Tumor-Associated Macrophages - immunology Tumor-Associated Macrophages - metabolism Tumors |
| title | The role of the immunoescape in colorectal cancer liver metastasis |
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