Stroma AReactive Invasion Front Areas (SARIFA) proves prognostic relevance in gastric carcinoma and is based on a tumor–adipocyte interaction indicating an altered immune response
Background Recently, we presented Stroma AReactive Invasion Front Areas (SARIFA) as a new histomorphologic negative prognostic biomarker in gastric cancer. It is defined as direct contact between tumor cells and fat cells. The aim of this study was to further elucidate the underlying genomic, transc...
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| Veröffentlicht in: | Gastric cancer : official journal of the International Gastric Cancer Association and the Japanese Gastric Cancer Association 2024-01, Vol.27 (1), p.72-85 |
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| creator | Grosser, Bianca Heyer, Christian M. Austgen, Johannes Sipos, Eva Reitsam, Nic G. Hauser, Andreas VanSchoiack, Alison Kroeppler, David Vlasenko, Dmytro Probst, Andreas Novotny, Alexander Weichert, Wilko Keller, Gisela Schlesner, Matthias Märkl, Bruno |
| description | Background
Recently, we presented Stroma AReactive Invasion Front Areas (SARIFA) as a new histomorphologic negative prognostic biomarker in gastric cancer. It is defined as direct contact between tumor cells and fat cells. The aim of this study was to further elucidate the underlying genomic, transcriptional, and immunological mechanisms of the SARIFA phenomenon.
Methods
To address these questions, SARIFA was classified on H&E-stained tissue sections of three cohorts: an external cohort (
n
= 489, prognostic validation), the TCGA-STAD cohort (
n
= 194, genomic and transcriptomic analysis), and a local cohort (
n
= 60, digital spatial profiling (whole transcriptome) and double RNA in situ hybridization/immunostaining of cytokines).
Results
SARIFA status proved to be an independent negative prognostic factor for overall survival in an external cohort of gastric carcinomas. In TCGA-STAD cohort, SARIFA is not driven by distinct genomic alterations, whereas the gene expression analyses showed an upregulation of FABP4 in SARIFA-positive tumors. In addition, the transcriptional regulations of white adipocyte differentiation, triglyceride metabolism, and catabolism were upregulated in pathway analyses. In the DSP analysis of SARIFA-positive tumors, FABP4 and the transcriptional regulation of white adipocyte differentiation were upregulated in macrophages. Additionally, a significantly lower expression of the cytokines IL6 and TNFα was observed at the invasion front.
Conclusions
SARIFA proves to be a strong negative prognostic biomarker in advanced gastric cancer, implicating an interaction of tumor cells with tumor-promoting adipocytes with crucial changes in tumor cell metabolism. SARIFA is not driven by tumor genetics but is very likely driven by an altered immune response as a causative mechanism. |
| doi_str_mv | 10.1007/s10120-023-01436-8 |
| format | Article |
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Recently, we presented Stroma AReactive Invasion Front Areas (SARIFA) as a new histomorphologic negative prognostic biomarker in gastric cancer. It is defined as direct contact between tumor cells and fat cells. The aim of this study was to further elucidate the underlying genomic, transcriptional, and immunological mechanisms of the SARIFA phenomenon.
Methods
To address these questions, SARIFA was classified on H&E-stained tissue sections of three cohorts: an external cohort (
n
= 489, prognostic validation), the TCGA-STAD cohort (
n
= 194, genomic and transcriptomic analysis), and a local cohort (
n
= 60, digital spatial profiling (whole transcriptome) and double RNA in situ hybridization/immunostaining of cytokines).
Results
SARIFA status proved to be an independent negative prognostic factor for overall survival in an external cohort of gastric carcinomas. In TCGA-STAD cohort, SARIFA is not driven by distinct genomic alterations, whereas the gene expression analyses showed an upregulation of FABP4 in SARIFA-positive tumors. In addition, the transcriptional regulations of white adipocyte differentiation, triglyceride metabolism, and catabolism were upregulated in pathway analyses. In the DSP analysis of SARIFA-positive tumors, FABP4 and the transcriptional regulation of white adipocyte differentiation were upregulated in macrophages. Additionally, a significantly lower expression of the cytokines IL6 and TNFα was observed at the invasion front.
Conclusions
SARIFA proves to be a strong negative prognostic biomarker in advanced gastric cancer, implicating an interaction of tumor cells with tumor-promoting adipocytes with crucial changes in tumor cell metabolism. SARIFA is not driven by tumor genetics but is very likely driven by an altered immune response as a causative mechanism.</description><identifier>ISSN: 1436-3291</identifier><identifier>EISSN: 1436-3305</identifier><identifier>DOI: 10.1007/s10120-023-01436-8</identifier><identifier>PMID: 37874427</identifier><language>eng</language><publisher>Singapore: Springer Nature Singapore</publisher><subject>Abdominal Surgery ; Adipocytes ; Adipocytes - metabolism ; Adipocytes - pathology ; Biomarkers ; Cancer Research ; Carcinoma ; Cytokines ; Cytokines - metabolism ; Gastric cancer ; Gastroenterology ; Gene expression ; Gene regulation ; Genomics ; Humans ; Hybridization ; Immune response ; Immunomodulation ; Macrophages ; Medical prognosis ; Medicine ; Medicine & Public Health ; Metabolism ; Oncology ; Original ; Original Article ; Prognosis ; Stomach Neoplasms - pathology ; Stroma ; Surgical Oncology ; Transcription ; Transcriptomes ; Transcriptomics ; Tumor cells ; Tumors</subject><ispartof>Gastric cancer : official journal of the International Gastric Cancer Association and the Japanese Gastric Cancer Association, 2024-01, Vol.27 (1), p.72-85</ispartof><rights>The Author(s) 2023</rights><rights>2023. The Author(s).</rights><rights>The Author(s) 2023. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c502t-e51981b1767d7d72c3982d3d292465064f5909eb0aed760c22e7b71e25e227d63</citedby><cites>FETCH-LOGICAL-c502t-e51981b1767d7d72c3982d3d292465064f5909eb0aed760c22e7b71e25e227d63</cites><orcidid>0000-0003-4957-4876</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s10120-023-01436-8$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s10120-023-01436-8$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,777,781,882,27905,27906,41469,42538,51300</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37874427$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Grosser, Bianca</creatorcontrib><creatorcontrib>Heyer, Christian M.</creatorcontrib><creatorcontrib>Austgen, Johannes</creatorcontrib><creatorcontrib>Sipos, Eva</creatorcontrib><creatorcontrib>Reitsam, Nic G.</creatorcontrib><creatorcontrib>Hauser, Andreas</creatorcontrib><creatorcontrib>VanSchoiack, Alison</creatorcontrib><creatorcontrib>Kroeppler, David</creatorcontrib><creatorcontrib>Vlasenko, Dmytro</creatorcontrib><creatorcontrib>Probst, Andreas</creatorcontrib><creatorcontrib>Novotny, Alexander</creatorcontrib><creatorcontrib>Weichert, Wilko</creatorcontrib><creatorcontrib>Keller, Gisela</creatorcontrib><creatorcontrib>Schlesner, Matthias</creatorcontrib><creatorcontrib>Märkl, Bruno</creatorcontrib><title>Stroma AReactive Invasion Front Areas (SARIFA) proves prognostic relevance in gastric carcinoma and is based on a tumor–adipocyte interaction indicating an altered immune response</title><title>Gastric cancer : official journal of the International Gastric Cancer Association and the Japanese Gastric Cancer Association</title><addtitle>Gastric Cancer</addtitle><addtitle>Gastric Cancer</addtitle><description>Background
Recently, we presented Stroma AReactive Invasion Front Areas (SARIFA) as a new histomorphologic negative prognostic biomarker in gastric cancer. It is defined as direct contact between tumor cells and fat cells. The aim of this study was to further elucidate the underlying genomic, transcriptional, and immunological mechanisms of the SARIFA phenomenon.
Methods
To address these questions, SARIFA was classified on H&E-stained tissue sections of three cohorts: an external cohort (
n
= 489, prognostic validation), the TCGA-STAD cohort (
n
= 194, genomic and transcriptomic analysis), and a local cohort (
n
= 60, digital spatial profiling (whole transcriptome) and double RNA in situ hybridization/immunostaining of cytokines).
Results
SARIFA status proved to be an independent negative prognostic factor for overall survival in an external cohort of gastric carcinomas. In TCGA-STAD cohort, SARIFA is not driven by distinct genomic alterations, whereas the gene expression analyses showed an upregulation of FABP4 in SARIFA-positive tumors. In addition, the transcriptional regulations of white adipocyte differentiation, triglyceride metabolism, and catabolism were upregulated in pathway analyses. In the DSP analysis of SARIFA-positive tumors, FABP4 and the transcriptional regulation of white adipocyte differentiation were upregulated in macrophages. Additionally, a significantly lower expression of the cytokines IL6 and TNFα was observed at the invasion front.
Conclusions
SARIFA proves to be a strong negative prognostic biomarker in advanced gastric cancer, implicating an interaction of tumor cells with tumor-promoting adipocytes with crucial changes in tumor cell metabolism. SARIFA is not driven by tumor genetics but is very likely driven by an altered immune response as a causative mechanism.</description><subject>Abdominal Surgery</subject><subject>Adipocytes</subject><subject>Adipocytes - metabolism</subject><subject>Adipocytes - pathology</subject><subject>Biomarkers</subject><subject>Cancer Research</subject><subject>Carcinoma</subject><subject>Cytokines</subject><subject>Cytokines - metabolism</subject><subject>Gastric cancer</subject><subject>Gastroenterology</subject><subject>Gene expression</subject><subject>Gene regulation</subject><subject>Genomics</subject><subject>Humans</subject><subject>Hybridization</subject><subject>Immune response</subject><subject>Immunomodulation</subject><subject>Macrophages</subject><subject>Medical prognosis</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Metabolism</subject><subject>Oncology</subject><subject>Original</subject><subject>Original Article</subject><subject>Prognosis</subject><subject>Stomach Neoplasms - pathology</subject><subject>Stroma</subject><subject>Surgical Oncology</subject><subject>Transcription</subject><subject>Transcriptomes</subject><subject>Transcriptomics</subject><subject>Tumor cells</subject><subject>Tumors</subject><issn>1436-3291</issn><issn>1436-3305</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><recordid>eNp9Uk1u1TAQjhAVLYULsECW2JRFiu3EcbJCUdUHT6qE1MLacux5wVViB9uJ1B134Cy9ECfB6WvLzwJ5MSPP9zMjfVn2iuBTgjF_FwgmFOeYFjkmZVHl9ZPs6K4pCsyePvS0IYfZ8xCuMSasIdWz7LDgNS9Lyo-y26vo3ShRewlSRbMA2tpFBuMs2nhnI2o9yIBOrtrL7aZ9iybvFghr6a0L0SjkYYBFWgXIWNTLEH36VNIrY1dhaTUyAXUygEZJVaI4j87__P5DajM5dRNXYgS_2qe5sdooGY3tExXJIU0S0YzjbCF5hcnZAC-yg50cAry8r8fZl83557OP-cWnD9uz9iJXDNOYAyNNTTrCK67To6poaqoLTRtaVgxX5Y41uIEOS9C8wopS4B0nQBlQynVVHGfv97rT3I2gFdjo5SAmb0bpb4STRvw9sear6N0iCOYVSR5J4eRewbtvM4QoRhMUDIO04OYgaF0TWrKKr9A3_0Cv3extuk_QtCZhJWXrSnSPUt6F4GH3uA3BYo2F2MdCpFiIu1iIOpFe_3nHI-UhBwlQ7AEhjWwP_rf3f2R_AWerxs0</recordid><startdate>20240101</startdate><enddate>20240101</enddate><creator>Grosser, Bianca</creator><creator>Heyer, Christian M.</creator><creator>Austgen, Johannes</creator><creator>Sipos, Eva</creator><creator>Reitsam, Nic G.</creator><creator>Hauser, Andreas</creator><creator>VanSchoiack, Alison</creator><creator>Kroeppler, David</creator><creator>Vlasenko, Dmytro</creator><creator>Probst, Andreas</creator><creator>Novotny, Alexander</creator><creator>Weichert, Wilko</creator><creator>Keller, Gisela</creator><creator>Schlesner, Matthias</creator><creator>Märkl, Bruno</creator><general>Springer Nature Singapore</general><general>Springer Nature B.V</general><scope>C6C</scope><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>7T5</scope><scope>H94</scope><scope>K9.</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4957-4876</orcidid></search><sort><creationdate>20240101</creationdate><title>Stroma AReactive Invasion Front Areas (SARIFA) proves prognostic relevance in gastric carcinoma and is based on a tumor–adipocyte interaction indicating an altered immune response</title><author>Grosser, Bianca ; Heyer, Christian M. ; Austgen, Johannes ; Sipos, Eva ; Reitsam, Nic G. ; Hauser, Andreas ; VanSchoiack, Alison ; Kroeppler, David ; Vlasenko, Dmytro ; Probst, Andreas ; Novotny, Alexander ; Weichert, Wilko ; Keller, Gisela ; Schlesner, Matthias ; Märkl, Bruno</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c502t-e51981b1767d7d72c3982d3d292465064f5909eb0aed760c22e7b71e25e227d63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Abdominal Surgery</topic><topic>Adipocytes</topic><topic>Adipocytes - metabolism</topic><topic>Adipocytes - pathology</topic><topic>Biomarkers</topic><topic>Cancer Research</topic><topic>Carcinoma</topic><topic>Cytokines</topic><topic>Cytokines - metabolism</topic><topic>Gastric cancer</topic><topic>Gastroenterology</topic><topic>Gene expression</topic><topic>Gene regulation</topic><topic>Genomics</topic><topic>Humans</topic><topic>Hybridization</topic><topic>Immune response</topic><topic>Immunomodulation</topic><topic>Macrophages</topic><topic>Medical prognosis</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Metabolism</topic><topic>Oncology</topic><topic>Original</topic><topic>Original Article</topic><topic>Prognosis</topic><topic>Stomach Neoplasms - pathology</topic><topic>Stroma</topic><topic>Surgical Oncology</topic><topic>Transcription</topic><topic>Transcriptomes</topic><topic>Transcriptomics</topic><topic>Tumor cells</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Grosser, Bianca</creatorcontrib><creatorcontrib>Heyer, Christian M.</creatorcontrib><creatorcontrib>Austgen, Johannes</creatorcontrib><creatorcontrib>Sipos, Eva</creatorcontrib><creatorcontrib>Reitsam, Nic G.</creatorcontrib><creatorcontrib>Hauser, Andreas</creatorcontrib><creatorcontrib>VanSchoiack, Alison</creatorcontrib><creatorcontrib>Kroeppler, David</creatorcontrib><creatorcontrib>Vlasenko, Dmytro</creatorcontrib><creatorcontrib>Probst, Andreas</creatorcontrib><creatorcontrib>Novotny, Alexander</creatorcontrib><creatorcontrib>Weichert, Wilko</creatorcontrib><creatorcontrib>Keller, Gisela</creatorcontrib><creatorcontrib>Schlesner, Matthias</creatorcontrib><creatorcontrib>Märkl, Bruno</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Immunology Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Gastric cancer : official journal of the International Gastric Cancer Association and the Japanese Gastric Cancer Association</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Grosser, Bianca</au><au>Heyer, Christian M.</au><au>Austgen, Johannes</au><au>Sipos, Eva</au><au>Reitsam, Nic G.</au><au>Hauser, Andreas</au><au>VanSchoiack, Alison</au><au>Kroeppler, David</au><au>Vlasenko, Dmytro</au><au>Probst, Andreas</au><au>Novotny, Alexander</au><au>Weichert, Wilko</au><au>Keller, Gisela</au><au>Schlesner, Matthias</au><au>Märkl, Bruno</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Stroma AReactive Invasion Front Areas (SARIFA) proves prognostic relevance in gastric carcinoma and is based on a tumor–adipocyte interaction indicating an altered immune response</atitle><jtitle>Gastric cancer : official journal of the International Gastric Cancer Association and the Japanese Gastric Cancer Association</jtitle><stitle>Gastric Cancer</stitle><addtitle>Gastric Cancer</addtitle><date>2024-01-01</date><risdate>2024</risdate><volume>27</volume><issue>1</issue><spage>72</spage><epage>85</epage><pages>72-85</pages><issn>1436-3291</issn><eissn>1436-3305</eissn><abstract>Background
Recently, we presented Stroma AReactive Invasion Front Areas (SARIFA) as a new histomorphologic negative prognostic biomarker in gastric cancer. It is defined as direct contact between tumor cells and fat cells. The aim of this study was to further elucidate the underlying genomic, transcriptional, and immunological mechanisms of the SARIFA phenomenon.
Methods
To address these questions, SARIFA was classified on H&E-stained tissue sections of three cohorts: an external cohort (
n
= 489, prognostic validation), the TCGA-STAD cohort (
n
= 194, genomic and transcriptomic analysis), and a local cohort (
n
= 60, digital spatial profiling (whole transcriptome) and double RNA in situ hybridization/immunostaining of cytokines).
Results
SARIFA status proved to be an independent negative prognostic factor for overall survival in an external cohort of gastric carcinomas. In TCGA-STAD cohort, SARIFA is not driven by distinct genomic alterations, whereas the gene expression analyses showed an upregulation of FABP4 in SARIFA-positive tumors. In addition, the transcriptional regulations of white adipocyte differentiation, triglyceride metabolism, and catabolism were upregulated in pathway analyses. In the DSP analysis of SARIFA-positive tumors, FABP4 and the transcriptional regulation of white adipocyte differentiation were upregulated in macrophages. Additionally, a significantly lower expression of the cytokines IL6 and TNFα was observed at the invasion front.
Conclusions
SARIFA proves to be a strong negative prognostic biomarker in advanced gastric cancer, implicating an interaction of tumor cells with tumor-promoting adipocytes with crucial changes in tumor cell metabolism. SARIFA is not driven by tumor genetics but is very likely driven by an altered immune response as a causative mechanism.</abstract><cop>Singapore</cop><pub>Springer Nature Singapore</pub><pmid>37874427</pmid><doi>10.1007/s10120-023-01436-8</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-4957-4876</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Gastric cancer : official journal of the International Gastric Cancer Association and the Japanese Gastric Cancer Association, 2024-01, Vol.27 (1), p.72-85 |
| issn | 1436-3291 1436-3305 |
| language | eng |
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| source | MEDLINE; EZB-FREE-00999 freely available EZB journals; SpringerLink Journals - AutoHoldings |
| subjects | Abdominal Surgery Adipocytes Adipocytes - metabolism Adipocytes - pathology Biomarkers Cancer Research Carcinoma Cytokines Cytokines - metabolism Gastric cancer Gastroenterology Gene expression Gene regulation Genomics Humans Hybridization Immune response Immunomodulation Macrophages Medical prognosis Medicine Medicine & Public Health Metabolism Oncology Original Original Article Prognosis Stomach Neoplasms - pathology Stroma Surgical Oncology Transcription Transcriptomes Transcriptomics Tumor cells Tumors |
| title | Stroma AReactive Invasion Front Areas (SARIFA) proves prognostic relevance in gastric carcinoma and is based on a tumor–adipocyte interaction indicating an altered immune response |
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