Prognostic significance of serum complement activation, neutrophil extracellular traps and extracellular DNA in newly diagnosed epithelial ovarian cancer
We observed that the tumor microenvironment (TME) in metastatic epithelial ovarian cancer (EOC) and in other solid tumors can reprogram normal neutrophils to acquire a complement-dependent suppressor phenotype characterized by inhibition of stimulated T cell activation. This study aims to evaluate w...
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| Veröffentlicht in: | Gynecologic oncology 2025-02, Vol.193, p.49-57 |
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| creator | Ricciuti, Jason Liu, Qian Khan, A.N.M. Nazmul H. Joseph, Janine M. Veuskens, Bert Giridharan, Thejaswini Suzuki, Sora Emmons, Tiffany Yaffe, Michael Kuijpers, Taco W. Jongerius, Ilse Brouwer, Mieke Pouw, Richard B. Odunsi, Kunle Frederick, Peter Mager, Katherine LaVigne Lele, Shashikant Gaulin, Nicole Hakim, Christiane Edwards, Robert P. Olawaiye, Alexander B. Sukamanovich, Paniti Taylor, Sarah Elishaev, Esther Zsiros, Emese Modugno, Francesmary Moysich, Kirsten Segal, Brahm |
| description | We observed that the tumor microenvironment (TME) in metastatic epithelial ovarian cancer (EOC) and in other solid tumors can reprogram normal neutrophils to acquire a complement-dependent suppressor phenotype characterized by inhibition of stimulated T cell activation. This study aims to evaluate whether serum markers of neutrophil activation and complement at diagnosis of EOC would be associated with clinical outcomes.
We conducted a two-center prospective study of patients with newly diagnosed EOC (N = 188). Blood and ascites fluid were collected at diagnosis for biomarker analysis. Patients were evaluated for progression-free survival (PFS) and overall survival (OS).
The median OS was 47 months (95 % CI: 34–58) and the median PFS was 12 months (95 % CI: 11–15). Pre-treatment serum levels of genomic DNA (gDNA), markers of neutrophil degranulation (myeloperoxidase [MPO]) and neutrophil extracellular traps (NETs) (citrullinated histone H3 [CitH3]), and complement activation (C3b/c) were each associated with worse OS in univariate analysis. In multivariate analyses controlling for age, stage, and optimal debulking, serum gDNA, MPO, and CitH3 remained associated with worse OS, while C3b/c levels were not. In an exploratory analysis, the largest magnitude of difference in 2-year OS occurred in patients with low C3b/c and low CitH3 compared to all other patients (87 % vs 46 % survival, respectively). In ascites fluid, increased factor H, a negative regulator of complement activation, was associated with improved OS in univariate analysis.
These results point to serum gDNA, NETs, and complement activation as potential prognostic biomarkers in patients with newly diagnosed EOC.
•Immune checkpoint inhibitors have been shown to be largely ineffective as a treatment for epithelial ovarian cancer (EOC).•Neutrophils, NETs, and complement signaling have previously been implicated in inducing T cell suppression.•In this study, complement activation, NETs, extracellular gDNA (cellular damage marker), were associated with worse EOC survival.•Ascites fluid factor H, a negative regulator of complement activation, was associated with improved survival. |
| doi_str_mv | 10.1016/j.ygyno.2024.12.006 |
| format | Article |
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We conducted a two-center prospective study of patients with newly diagnosed EOC (N = 188). Blood and ascites fluid were collected at diagnosis for biomarker analysis. Patients were evaluated for progression-free survival (PFS) and overall survival (OS).
The median OS was 47 months (95 % CI: 34–58) and the median PFS was 12 months (95 % CI: 11–15). Pre-treatment serum levels of genomic DNA (gDNA), markers of neutrophil degranulation (myeloperoxidase [MPO]) and neutrophil extracellular traps (NETs) (citrullinated histone H3 [CitH3]), and complement activation (C3b/c) were each associated with worse OS in univariate analysis. In multivariate analyses controlling for age, stage, and optimal debulking, serum gDNA, MPO, and CitH3 remained associated with worse OS, while C3b/c levels were not. In an exploratory analysis, the largest magnitude of difference in 2-year OS occurred in patients with low C3b/c and low CitH3 compared to all other patients (87 % vs 46 % survival, respectively). In ascites fluid, increased factor H, a negative regulator of complement activation, was associated with improved OS in univariate analysis.
These results point to serum gDNA, NETs, and complement activation as potential prognostic biomarkers in patients with newly diagnosed EOC.
•Immune checkpoint inhibitors have been shown to be largely ineffective as a treatment for epithelial ovarian cancer (EOC).•Neutrophils, NETs, and complement signaling have previously been implicated in inducing T cell suppression.•In this study, complement activation, NETs, extracellular gDNA (cellular damage marker), were associated with worse EOC survival.•Ascites fluid factor H, a negative regulator of complement activation, was associated with improved survival.</description><identifier>ISSN: 0090-8258</identifier><identifier>ISSN: 1095-6859</identifier><identifier>EISSN: 1095-6859</identifier><identifier>DOI: 10.1016/j.ygyno.2024.12.006</identifier><identifier>PMID: 39764857</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Complement activation ; Epithelial ovarian cancer ; Extracellular genomic DNA ; NETs ; Neutrophil activation ; Survival</subject><ispartof>Gynecologic oncology, 2025-02, Vol.193, p.49-57</ispartof><rights>2024 Elsevier Inc.</rights><rights>Copyright © 2024 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c239t-f63e2f8d700bb0f2113d265b047617b760cfb777ae1a28e3cbd48994a6cbeed93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S009082582401223X$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65534</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39764857$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ricciuti, Jason</creatorcontrib><creatorcontrib>Liu, Qian</creatorcontrib><creatorcontrib>Khan, A.N.M. Nazmul H.</creatorcontrib><creatorcontrib>Joseph, Janine M.</creatorcontrib><creatorcontrib>Veuskens, Bert</creatorcontrib><creatorcontrib>Giridharan, Thejaswini</creatorcontrib><creatorcontrib>Suzuki, Sora</creatorcontrib><creatorcontrib>Emmons, Tiffany</creatorcontrib><creatorcontrib>Yaffe, Michael</creatorcontrib><creatorcontrib>Kuijpers, Taco W.</creatorcontrib><creatorcontrib>Jongerius, Ilse</creatorcontrib><creatorcontrib>Brouwer, Mieke</creatorcontrib><creatorcontrib>Pouw, Richard B.</creatorcontrib><creatorcontrib>Odunsi, Kunle</creatorcontrib><creatorcontrib>Frederick, Peter</creatorcontrib><creatorcontrib>Mager, Katherine LaVigne</creatorcontrib><creatorcontrib>Lele, Shashikant</creatorcontrib><creatorcontrib>Gaulin, Nicole</creatorcontrib><creatorcontrib>Hakim, Christiane</creatorcontrib><creatorcontrib>Edwards, Robert P.</creatorcontrib><creatorcontrib>Olawaiye, Alexander B.</creatorcontrib><creatorcontrib>Sukamanovich, Paniti</creatorcontrib><creatorcontrib>Taylor, Sarah</creatorcontrib><creatorcontrib>Elishaev, Esther</creatorcontrib><creatorcontrib>Zsiros, Emese</creatorcontrib><creatorcontrib>Modugno, Francesmary</creatorcontrib><creatorcontrib>Moysich, Kirsten</creatorcontrib><creatorcontrib>Segal, Brahm</creatorcontrib><title>Prognostic significance of serum complement activation, neutrophil extracellular traps and extracellular DNA in newly diagnosed epithelial ovarian cancer</title><title>Gynecologic oncology</title><addtitle>Gynecol Oncol</addtitle><description>We observed that the tumor microenvironment (TME) in metastatic epithelial ovarian cancer (EOC) and in other solid tumors can reprogram normal neutrophils to acquire a complement-dependent suppressor phenotype characterized by inhibition of stimulated T cell activation. This study aims to evaluate whether serum markers of neutrophil activation and complement at diagnosis of EOC would be associated with clinical outcomes.
We conducted a two-center prospective study of patients with newly diagnosed EOC (N = 188). Blood and ascites fluid were collected at diagnosis for biomarker analysis. Patients were evaluated for progression-free survival (PFS) and overall survival (OS).
The median OS was 47 months (95 % CI: 34–58) and the median PFS was 12 months (95 % CI: 11–15). Pre-treatment serum levels of genomic DNA (gDNA), markers of neutrophil degranulation (myeloperoxidase [MPO]) and neutrophil extracellular traps (NETs) (citrullinated histone H3 [CitH3]), and complement activation (C3b/c) were each associated with worse OS in univariate analysis. In multivariate analyses controlling for age, stage, and optimal debulking, serum gDNA, MPO, and CitH3 remained associated with worse OS, while C3b/c levels were not. In an exploratory analysis, the largest magnitude of difference in 2-year OS occurred in patients with low C3b/c and low CitH3 compared to all other patients (87 % vs 46 % survival, respectively). In ascites fluid, increased factor H, a negative regulator of complement activation, was associated with improved OS in univariate analysis.
These results point to serum gDNA, NETs, and complement activation as potential prognostic biomarkers in patients with newly diagnosed EOC.
•Immune checkpoint inhibitors have been shown to be largely ineffective as a treatment for epithelial ovarian cancer (EOC).•Neutrophils, NETs, and complement signaling have previously been implicated in inducing T cell suppression.•In this study, complement activation, NETs, extracellular gDNA (cellular damage marker), were associated with worse EOC survival.•Ascites fluid factor H, a negative regulator of complement activation, was associated with improved survival.</description><subject>Complement activation</subject><subject>Epithelial ovarian cancer</subject><subject>Extracellular genomic DNA</subject><subject>NETs</subject><subject>Neutrophil activation</subject><subject>Survival</subject><issn>0090-8258</issn><issn>1095-6859</issn><issn>1095-6859</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2025</creationdate><recordtype>article</recordtype><recordid>eNp9kUGP1CAYhonRuOPqLzAxHD3Y-gEtbQ8eNruummzUg54Jha-zTFqoQGedn-K_tbOzevDgCUKel_eDh5CXDEoGTL7dlYftwYeSA69KxksA-YhsGHR1Idu6e0w2AB0ULa_bM_IspR0ACGD8KTkTXSOrtm425NfXGLY-pOwMTW7r3eCM9gZpGGjCuEzUhGkecUKfqTbZ7XV2wb-hHpccw3zrRoo_c9QGx3EZdaTrfk5Ue_vP-dXnC-r8mrsbD9Q6fWzFFZpdvsXR6ZGGvY5Oe3o_QHxOngx6TPjiYT0n36_ff7v8WNx8-fDp8uKmMFx0uRikQD60tgHoexg4Y8JyWfdQNZI1fSPBDH3TNBqZ5i0K09uq7bpKS9Mj2k6ck9ene-cYfiyYsppcOk6tPYYlKcEk56KuWr6i4oSaGFKKOKg5uknHg2Kgjk7UTt07UUcninG1OllTrx4Kln5C-zfzR8IKvDsBuD5z7zCqZByuf2BdRJOVDe6_Bb8B1lGjbA</recordid><startdate>20250201</startdate><enddate>20250201</enddate><creator>Ricciuti, Jason</creator><creator>Liu, Qian</creator><creator>Khan, A.N.M. 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Nazmul H. ; Joseph, Janine M. ; Veuskens, Bert ; Giridharan, Thejaswini ; Suzuki, Sora ; Emmons, Tiffany ; Yaffe, Michael ; Kuijpers, Taco W. ; Jongerius, Ilse ; Brouwer, Mieke ; Pouw, Richard B. ; Odunsi, Kunle ; Frederick, Peter ; Mager, Katherine LaVigne ; Lele, Shashikant ; Gaulin, Nicole ; Hakim, Christiane ; Edwards, Robert P. ; Olawaiye, Alexander B. ; Sukamanovich, Paniti ; Taylor, Sarah ; Elishaev, Esther ; Zsiros, Emese ; Modugno, Francesmary ; Moysich, Kirsten ; Segal, Brahm</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c239t-f63e2f8d700bb0f2113d265b047617b760cfb777ae1a28e3cbd48994a6cbeed93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2025</creationdate><topic>Complement activation</topic><topic>Epithelial ovarian cancer</topic><topic>Extracellular genomic DNA</topic><topic>NETs</topic><topic>Neutrophil activation</topic><topic>Survival</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ricciuti, Jason</creatorcontrib><creatorcontrib>Liu, Qian</creatorcontrib><creatorcontrib>Khan, A.N.M. 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Nazmul H.</au><au>Joseph, Janine M.</au><au>Veuskens, Bert</au><au>Giridharan, Thejaswini</au><au>Suzuki, Sora</au><au>Emmons, Tiffany</au><au>Yaffe, Michael</au><au>Kuijpers, Taco W.</au><au>Jongerius, Ilse</au><au>Brouwer, Mieke</au><au>Pouw, Richard B.</au><au>Odunsi, Kunle</au><au>Frederick, Peter</au><au>Mager, Katherine LaVigne</au><au>Lele, Shashikant</au><au>Gaulin, Nicole</au><au>Hakim, Christiane</au><au>Edwards, Robert P.</au><au>Olawaiye, Alexander B.</au><au>Sukamanovich, Paniti</au><au>Taylor, Sarah</au><au>Elishaev, Esther</au><au>Zsiros, Emese</au><au>Modugno, Francesmary</au><au>Moysich, Kirsten</au><au>Segal, Brahm</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Prognostic significance of serum complement activation, neutrophil extracellular traps and extracellular DNA in newly diagnosed epithelial ovarian cancer</atitle><jtitle>Gynecologic oncology</jtitle><addtitle>Gynecol Oncol</addtitle><date>2025-02-01</date><risdate>2025</risdate><volume>193</volume><spage>49</spage><epage>57</epage><pages>49-57</pages><issn>0090-8258</issn><issn>1095-6859</issn><eissn>1095-6859</eissn><abstract>We observed that the tumor microenvironment (TME) in metastatic epithelial ovarian cancer (EOC) and in other solid tumors can reprogram normal neutrophils to acquire a complement-dependent suppressor phenotype characterized by inhibition of stimulated T cell activation. This study aims to evaluate whether serum markers of neutrophil activation and complement at diagnosis of EOC would be associated with clinical outcomes.
We conducted a two-center prospective study of patients with newly diagnosed EOC (N = 188). Blood and ascites fluid were collected at diagnosis for biomarker analysis. Patients were evaluated for progression-free survival (PFS) and overall survival (OS).
The median OS was 47 months (95 % CI: 34–58) and the median PFS was 12 months (95 % CI: 11–15). Pre-treatment serum levels of genomic DNA (gDNA), markers of neutrophil degranulation (myeloperoxidase [MPO]) and neutrophil extracellular traps (NETs) (citrullinated histone H3 [CitH3]), and complement activation (C3b/c) were each associated with worse OS in univariate analysis. In multivariate analyses controlling for age, stage, and optimal debulking, serum gDNA, MPO, and CitH3 remained associated with worse OS, while C3b/c levels were not. In an exploratory analysis, the largest magnitude of difference in 2-year OS occurred in patients with low C3b/c and low CitH3 compared to all other patients (87 % vs 46 % survival, respectively). In ascites fluid, increased factor H, a negative regulator of complement activation, was associated with improved OS in univariate analysis.
These results point to serum gDNA, NETs, and complement activation as potential prognostic biomarkers in patients with newly diagnosed EOC.
•Immune checkpoint inhibitors have been shown to be largely ineffective as a treatment for epithelial ovarian cancer (EOC).•Neutrophils, NETs, and complement signaling have previously been implicated in inducing T cell suppression.•In this study, complement activation, NETs, extracellular gDNA (cellular damage marker), were associated with worse EOC survival.•Ascites fluid factor H, a negative regulator of complement activation, was associated with improved survival.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>39764857</pmid><doi>10.1016/j.ygyno.2024.12.006</doi><tpages>9</tpages></addata></record> |
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| subjects | Complement activation Epithelial ovarian cancer Extracellular genomic DNA NETs Neutrophil activation Survival |
| title | Prognostic significance of serum complement activation, neutrophil extracellular traps and extracellular DNA in newly diagnosed epithelial ovarian cancer |
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