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The Expression of CTLA-4 in Breast Tumors and Tumor-Infiltrating Leukocytes Affects Patients’ Systemic Inflammatory Status and Varies According to Their Molecular Subtypes
Recent evidence has pointed out that the cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) expression is a poor prognosis factor. However, the implications of CTLA-4 expression on circulating inflammatory mediators are unclear for breast cancer. Tumor biopsies and blood samples were collected fro...
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| Published in: | Inflammation 2023-10, Vol.46 (5), p.1639-1652 |
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| creator | Kern, Rodrigo da Silva, Janaina Carla Negretti, Fábio Ferreira, Mariane Okamoto Coletto, Matheus Iago Oliveira de Oliveira, Stefania Tagliari Alves, Fernanda Mara Scandolara, Thalita Basso Rech, Daniel Panis, Carolina |
| description | Recent evidence has pointed out that the cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) expression is a poor prognosis factor. However, the implications of CTLA-4 expression on circulating inflammatory mediators are unclear for breast cancer. Tumor biopsies and blood samples were collected from 117 breast cancer patients. Oxidative stress parameters were evaluated in plasma samples by measuring the lipoperoxidation profile and nitric oxide metabolites (NOx). Interleukins 12 (IL-12) and 4 (IL-4) were assessed by ELISA. CTLA-4 expression was determined by immunofluorescence assessed by its labeling in tumor-infiltrating leukocytes (TILs) or breast tumors. Correlations between CTLA-4 expression in breast tumors with TCD4/TCD8 infiltrating lymphocyte and inflammation-related genes were performed using data from TIMER 2.0/TCGA databases (
n
= 2160). CTLA-4 expression in TILs significantly correlated to triple-negative breast tumors. Patients carrying CTLA-4-positive tumors exhibited lower plasmatic NOx levels, and those expressing CTLA-4 in TILs had reduced levels of IL-12 in plasma. No changes in either IL-4 or lipid peroxidation profiles were detected concerning any CTLA4 status. Compared to the Luminal A ones, oxidative stress parameters and cytokines were observed in patients bearing triple-negative tumors. CTLA-4 expression in all breast cancer subtypes positively correlated to TCD4/TCD8 lymphocyte infiltrates, as well as to the pro-inflammatory genes IL12A, IL4, NFKB1, NFKB2, NOS1, NOS2, and NOS3. CTLA-4 expression in both tumor and TILs can affect the systemic inflammatory status of breast cancer patients, especially antitumor molecules such as IL-12 and NOx that correlate to more aggressive disease. |
| doi_str_mv | 10.1007/s10753-023-01830-5 |
| format | article |
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n
= 2160). CTLA-4 expression in TILs significantly correlated to triple-negative breast tumors. Patients carrying CTLA-4-positive tumors exhibited lower plasmatic NOx levels, and those expressing CTLA-4 in TILs had reduced levels of IL-12 in plasma. No changes in either IL-4 or lipid peroxidation profiles were detected concerning any CTLA4 status. Compared to the Luminal A ones, oxidative stress parameters and cytokines were observed in patients bearing triple-negative tumors. CTLA-4 expression in all breast cancer subtypes positively correlated to TCD4/TCD8 lymphocyte infiltrates, as well as to the pro-inflammatory genes IL12A, IL4, NFKB1, NFKB2, NOS1, NOS2, and NOS3. CTLA-4 expression in both tumor and TILs can affect the systemic inflammatory status of breast cancer patients, especially antitumor molecules such as IL-12 and NOx that correlate to more aggressive disease.</description><identifier>ISSN: 0360-3997</identifier><identifier>EISSN: 1573-2576</identifier><identifier>DOI: 10.1007/s10753-023-01830-5</identifier><identifier>PMID: 37237069</identifier><language>eng</language><publisher>New York: Springer US</publisher><subject>Biomedical and Life Sciences ; Biomedicine ; Biopsy ; Breast cancer ; CTLA-4 Antigen - metabolism ; CTLA-4 protein ; Cytotoxicity ; Enzyme-linked immunosorbent assay ; Humans ; Immunofluorescence ; Immunology ; Inflammation ; Interleukin 12 ; Interleukin 4 ; Interleukin-12 - metabolism ; Interleukin-4 - metabolism ; Internal Medicine ; Leukocytes ; Lipid peroxidation ; Lymphocytes ; Lymphocytes T ; Lymphocytes, Tumor-Infiltrating - metabolism ; Lymphocytes, Tumor-Infiltrating - pathology ; Nitric oxide ; Nitric-oxide synthase ; Oxidative stress ; Pathology ; Pharmacology/Toxicology ; Prognosis ; Rheumatology ; Triple Negative Breast Neoplasms - metabolism ; Triple Negative Breast Neoplasms - pathology ; Tumors</subject><ispartof>Inflammation, 2023-10, Vol.46 (5), p.1639-1652</ispartof><rights>The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c375t-2e10023a21e1397ca2df6c5bd89ae1a34adb590cb90bfb71ea0dff46de8a1aa63</citedby><cites>FETCH-LOGICAL-c375t-2e10023a21e1397ca2df6c5bd89ae1a34adb590cb90bfb71ea0dff46de8a1aa63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,786,790,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37237069$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kern, Rodrigo</creatorcontrib><creatorcontrib>da Silva, Janaina Carla</creatorcontrib><creatorcontrib>Negretti, Fábio</creatorcontrib><creatorcontrib>Ferreira, Mariane Okamoto</creatorcontrib><creatorcontrib>Coletto, Matheus Iago Oliveira</creatorcontrib><creatorcontrib>de Oliveira, Stefania Tagliari</creatorcontrib><creatorcontrib>Alves, Fernanda Mara</creatorcontrib><creatorcontrib>Scandolara, Thalita Basso</creatorcontrib><creatorcontrib>Rech, Daniel</creatorcontrib><creatorcontrib>Panis, Carolina</creatorcontrib><title>The Expression of CTLA-4 in Breast Tumors and Tumor-Infiltrating Leukocytes Affects Patients’ Systemic Inflammatory Status and Varies According to Their Molecular Subtypes</title><title>Inflammation</title><addtitle>Inflammation</addtitle><addtitle>Inflammation</addtitle><description>Recent evidence has pointed out that the cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) expression is a poor prognosis factor. However, the implications of CTLA-4 expression on circulating inflammatory mediators are unclear for breast cancer. Tumor biopsies and blood samples were collected from 117 breast cancer patients. Oxidative stress parameters were evaluated in plasma samples by measuring the lipoperoxidation profile and nitric oxide metabolites (NOx). Interleukins 12 (IL-12) and 4 (IL-4) were assessed by ELISA. CTLA-4 expression was determined by immunofluorescence assessed by its labeling in tumor-infiltrating leukocytes (TILs) or breast tumors. Correlations between CTLA-4 expression in breast tumors with TCD4/TCD8 infiltrating lymphocyte and inflammation-related genes were performed using data from TIMER 2.0/TCGA databases (
n
= 2160). CTLA-4 expression in TILs significantly correlated to triple-negative breast tumors. Patients carrying CTLA-4-positive tumors exhibited lower plasmatic NOx levels, and those expressing CTLA-4 in TILs had reduced levels of IL-12 in plasma. No changes in either IL-4 or lipid peroxidation profiles were detected concerning any CTLA4 status. Compared to the Luminal A ones, oxidative stress parameters and cytokines were observed in patients bearing triple-negative tumors. CTLA-4 expression in all breast cancer subtypes positively correlated to TCD4/TCD8 lymphocyte infiltrates, as well as to the pro-inflammatory genes IL12A, IL4, NFKB1, NFKB2, NOS1, NOS2, and NOS3. CTLA-4 expression in both tumor and TILs can affect the systemic inflammatory status of breast cancer patients, especially antitumor molecules such as IL-12 and NOx that correlate to more aggressive disease.</description><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Biopsy</subject><subject>Breast cancer</subject><subject>CTLA-4 Antigen - metabolism</subject><subject>CTLA-4 protein</subject><subject>Cytotoxicity</subject><subject>Enzyme-linked immunosorbent assay</subject><subject>Humans</subject><subject>Immunofluorescence</subject><subject>Immunology</subject><subject>Inflammation</subject><subject>Interleukin 12</subject><subject>Interleukin 4</subject><subject>Interleukin-12 - metabolism</subject><subject>Interleukin-4 - metabolism</subject><subject>Internal Medicine</subject><subject>Leukocytes</subject><subject>Lipid peroxidation</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>Lymphocytes, Tumor-Infiltrating - metabolism</subject><subject>Lymphocytes, Tumor-Infiltrating - pathology</subject><subject>Nitric oxide</subject><subject>Nitric-oxide synthase</subject><subject>Oxidative stress</subject><subject>Pathology</subject><subject>Pharmacology/Toxicology</subject><subject>Prognosis</subject><subject>Rheumatology</subject><subject>Triple Negative Breast Neoplasms - metabolism</subject><subject>Triple Negative Breast Neoplasms - pathology</subject><subject>Tumors</subject><issn>0360-3997</issn><issn>1573-2576</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNp9kU2O1DAQhS0EYpqBC7BAltjMJuCfdpwsm9YAIzUCqRu2UcUpDxkSu7Ediey4BofgUpwENxlAYsHCsqX63qsnP0Iec_aMM6afR860kgUT-fBKskLdISuutCyE0uVdsmKyZIWsa31GHsR4wxir6kreJ2dSC6lZWa_I98NHpJdfjgFj7L2j3tLtYbcp1rR39EVAiIkeptGHSMF1y7O4crYfUoDUu2u6w-mTN3PCSDfWokmRvssTdCn--PqN7ueYcOwNzaIBxhGSDzPdJ0jTYvkBQn_SGuNDdzJMnuZQfaBv_IBmGiDQ_dSm-YjxIblnYYj46PY-J-9fXh62r4vd21dX282uMFKrVAjM_yMkCI5c1tqA6GxpVNtVNSAHuYauVTUzbc1a22qOwDpr12WHFXCAUp6Ti8X3GPznCWNqxj4aHAZw6KfYiErkBaUSPKNP_0Fv_BRcTpcprUpZZTBTYqFM8DEGtM0x9COEueGsOZXZLGU2OXbzq8xGZdGTW-upHbH7I_ndXgbkAsQ8ctcY_u7-j-1PZo-uGg</recordid><startdate>20231001</startdate><enddate>20231001</enddate><creator>Kern, Rodrigo</creator><creator>da Silva, Janaina Carla</creator><creator>Negretti, Fábio</creator><creator>Ferreira, Mariane Okamoto</creator><creator>Coletto, Matheus Iago Oliveira</creator><creator>de Oliveira, Stefania Tagliari</creator><creator>Alves, Fernanda Mara</creator><creator>Scandolara, Thalita Basso</creator><creator>Rech, Daniel</creator><creator>Panis, Carolina</creator><general>Springer US</general><general>Springer Nature B.V</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>7T5</scope><scope>7TO</scope><scope>7U9</scope><scope>H94</scope><scope>K9.</scope><scope>7X8</scope></search><sort><creationdate>20231001</creationdate><title>The Expression of CTLA-4 in Breast Tumors and Tumor-Infiltrating Leukocytes Affects Patients’ Systemic Inflammatory Status and Varies According to Their Molecular Subtypes</title><author>Kern, Rodrigo ; da Silva, Janaina Carla ; Negretti, Fábio ; Ferreira, Mariane Okamoto ; Coletto, Matheus Iago Oliveira ; de Oliveira, Stefania Tagliari ; Alves, Fernanda Mara ; Scandolara, Thalita Basso ; Rech, Daniel ; Panis, Carolina</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c375t-2e10023a21e1397ca2df6c5bd89ae1a34adb590cb90bfb71ea0dff46de8a1aa63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Biopsy</topic><topic>Breast cancer</topic><topic>CTLA-4 Antigen - metabolism</topic><topic>CTLA-4 protein</topic><topic>Cytotoxicity</topic><topic>Enzyme-linked immunosorbent assay</topic><topic>Humans</topic><topic>Immunofluorescence</topic><topic>Immunology</topic><topic>Inflammation</topic><topic>Interleukin 12</topic><topic>Interleukin 4</topic><topic>Interleukin-12 - metabolism</topic><topic>Interleukin-4 - metabolism</topic><topic>Internal Medicine</topic><topic>Leukocytes</topic><topic>Lipid peroxidation</topic><topic>Lymphocytes</topic><topic>Lymphocytes T</topic><topic>Lymphocytes, Tumor-Infiltrating - metabolism</topic><topic>Lymphocytes, Tumor-Infiltrating - pathology</topic><topic>Nitric oxide</topic><topic>Nitric-oxide synthase</topic><topic>Oxidative stress</topic><topic>Pathology</topic><topic>Pharmacology/Toxicology</topic><topic>Prognosis</topic><topic>Rheumatology</topic><topic>Triple Negative Breast Neoplasms - metabolism</topic><topic>Triple Negative Breast Neoplasms - pathology</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kern, Rodrigo</creatorcontrib><creatorcontrib>da Silva, Janaina Carla</creatorcontrib><creatorcontrib>Negretti, Fábio</creatorcontrib><creatorcontrib>Ferreira, Mariane Okamoto</creatorcontrib><creatorcontrib>Coletto, Matheus Iago Oliveira</creatorcontrib><creatorcontrib>de Oliveira, Stefania Tagliari</creatorcontrib><creatorcontrib>Alves, Fernanda Mara</creatorcontrib><creatorcontrib>Scandolara, Thalita Basso</creatorcontrib><creatorcontrib>Rech, Daniel</creatorcontrib><creatorcontrib>Panis, Carolina</creatorcontrib><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>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>MEDLINE - Academic</collection><jtitle>Inflammation</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kern, Rodrigo</au><au>da Silva, Janaina Carla</au><au>Negretti, Fábio</au><au>Ferreira, Mariane Okamoto</au><au>Coletto, Matheus Iago Oliveira</au><au>de Oliveira, Stefania Tagliari</au><au>Alves, Fernanda Mara</au><au>Scandolara, Thalita Basso</au><au>Rech, Daniel</au><au>Panis, Carolina</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Expression of CTLA-4 in Breast Tumors and Tumor-Infiltrating Leukocytes Affects Patients’ Systemic Inflammatory Status and Varies According to Their Molecular Subtypes</atitle><jtitle>Inflammation</jtitle><stitle>Inflammation</stitle><addtitle>Inflammation</addtitle><date>2023-10-01</date><risdate>2023</risdate><volume>46</volume><issue>5</issue><spage>1639</spage><epage>1652</epage><pages>1639-1652</pages><issn>0360-3997</issn><eissn>1573-2576</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Recent evidence has pointed out that the cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) expression is a poor prognosis factor. However, the implications of CTLA-4 expression on circulating inflammatory mediators are unclear for breast cancer. Tumor biopsies and blood samples were collected from 117 breast cancer patients. Oxidative stress parameters were evaluated in plasma samples by measuring the lipoperoxidation profile and nitric oxide metabolites (NOx). Interleukins 12 (IL-12) and 4 (IL-4) were assessed by ELISA. CTLA-4 expression was determined by immunofluorescence assessed by its labeling in tumor-infiltrating leukocytes (TILs) or breast tumors. Correlations between CTLA-4 expression in breast tumors with TCD4/TCD8 infiltrating lymphocyte and inflammation-related genes were performed using data from TIMER 2.0/TCGA databases (
n
= 2160). CTLA-4 expression in TILs significantly correlated to triple-negative breast tumors. Patients carrying CTLA-4-positive tumors exhibited lower plasmatic NOx levels, and those expressing CTLA-4 in TILs had reduced levels of IL-12 in plasma. No changes in either IL-4 or lipid peroxidation profiles were detected concerning any CTLA4 status. Compared to the Luminal A ones, oxidative stress parameters and cytokines were observed in patients bearing triple-negative tumors. CTLA-4 expression in all breast cancer subtypes positively correlated to TCD4/TCD8 lymphocyte infiltrates, as well as to the pro-inflammatory genes IL12A, IL4, NFKB1, NFKB2, NOS1, NOS2, and NOS3. CTLA-4 expression in both tumor and TILs can affect the systemic inflammatory status of breast cancer patients, especially antitumor molecules such as IL-12 and NOx that correlate to more aggressive disease.</abstract><cop>New York</cop><pub>Springer US</pub><pmid>37237069</pmid><doi>10.1007/s10753-023-01830-5</doi><tpages>14</tpages></addata></record> |
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| subjects | Biomedical and Life Sciences Biomedicine Biopsy Breast cancer CTLA-4 Antigen - metabolism CTLA-4 protein Cytotoxicity Enzyme-linked immunosorbent assay Humans Immunofluorescence Immunology Inflammation Interleukin 12 Interleukin 4 Interleukin-12 - metabolism Interleukin-4 - metabolism Internal Medicine Leukocytes Lipid peroxidation Lymphocytes Lymphocytes T Lymphocytes, Tumor-Infiltrating - metabolism Lymphocytes, Tumor-Infiltrating - pathology Nitric oxide Nitric-oxide synthase Oxidative stress Pathology Pharmacology/Toxicology Prognosis Rheumatology Triple Negative Breast Neoplasms - metabolism Triple Negative Breast Neoplasms - pathology Tumors |
| title | The Expression of CTLA-4 in Breast Tumors and Tumor-Infiltrating Leukocytes Affects Patients’ Systemic Inflammatory Status and Varies According to Their Molecular Subtypes |
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