High Densities of Tumor-Associated Plasma Cells Predict Improved Prognosis in Triple Negative Breast Cancer
Breast cancer is the most common malignancy affecting women, but the heterogeneity of the condition is a significant obstacle to effective treatment. Triple negative breast cancers (TNBCs) do not express HER2 or the receptors for estrogen or progesterone, and so often have a poor prognosis. Tumor-in...
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Published in | Frontiers in immunology Vol. 9; p. 1209 |
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Main Authors | , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Frontiers Media S.A
30.05.2018
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Abstract | Breast cancer is the most common malignancy affecting women, but the heterogeneity of the condition is a significant obstacle to effective treatment. Triple negative breast cancers (TNBCs) do not express HER2 or the receptors for estrogen or progesterone, and so often have a poor prognosis. Tumor-infiltrating T cells have been well-characterized in TNBC, and increased numbers are associated with better outcomes; however, the potential roles of B cells and plasma cells have been large. Here, we conducted a retrospective correlative study on the expression of B cell/plasma cell-related genes, and the abundance and localization of B cells and plasma cells within TNBCs, and clinical outcome. We analyzed 269 TNBC samples and used immunohistochemistry to quantify tumor-infiltrating B cells and plasma cells, coupled with NanoString measurement of expression of immunoglobulin metagenes. Multivariate analysis revealed that patients bearing TNBCs with above-median densities of CD38
plasma cells had significantly better disease-free survival (DFS) (HR = 0.44; 95% CI 0.26-0.77;
= 0.004) but not overall survival (OS), after adjusting for the effects of known prognostic factors. In contrast, TNBCs with higher immunoglobulin gene expression exhibited improved prognosis (OS
= 0.029 and DFS
= 0.005). The presence of B cells and plasma cells was positively correlated (
< 0.0001,
= 0.558), while immunoglobulin gene IGKC, IGHM, and IGHG1 mRNA expression correlated specifically with the density of CD38
plasma cells (IGKC
< 0.0001,
= 0.647; IGHM
< 0.0001,
= 0.580; IGHG1
< 0.0001,
= 0.655). Interestingly, after adjusting the multivariate analysis for the effect of intratumoral CD38
plasma cell density, the expression levels of all three genes lost significant prognostic value, suggesting a biologically important role of plasma cells. Last but not least, the addition of intratumoral CD38
plasma cell density to clinicopathological features significantly increased the prognostic value for both DFS (ΔLRχ
= 17.28,
= 1.71E-08) and OS (ΔLRχ
= 10.03,
= 6.32E-08), compared to clinicopathological features alone. The best combination was achieved by integrating intratumoral CD38
plasma cell density and IGHG1 which conferred the best added prognostic value for DFS (ΔLRχ
= 27.38,
= 5.22E-10) and OS (ΔLRχ
= 21.29,
= 1.03E-08). Our results demonstrate that the role of plasma cells in TNBC warrants further study to elucidate the relationship between their infiltration of tumors and disease recurrence. |
---|---|
AbstractList | Breast cancer is the most common malignancy affecting women, but the heterogeneity of the condition is a significant obstacle to effective treatment. Triple negative breast cancers (TNBCs) do not express HER2 or the receptors for estrogen or progesterone, and so often have a poor prognosis. Tumor-infiltrating T cells have been well-characterized in TNBC, and increased numbers are associated with better outcomes; however, the potential roles of B cells and plasma cells have been large. Here, we conducted a retrospective correlative study on the expression of B cell/plasma cell-related genes, and the abundance and localization of B cells and plasma cells within TNBCs, and clinical outcome. We analyzed 269 TNBC samples and used immunohistochemistry to quantify tumor-infiltrating B cells and plasma cells, coupled with NanoString measurement of expression of immunoglobulin metagenes. Multivariate analysis revealed that patients bearing TNBCs with above-median densities of CD38
plasma cells had significantly better disease-free survival (DFS) (HR = 0.44; 95% CI 0.26-0.77;
= 0.004) but not overall survival (OS), after adjusting for the effects of known prognostic factors. In contrast, TNBCs with higher immunoglobulin gene expression exhibited improved prognosis (OS
= 0.029 and DFS
= 0.005). The presence of B cells and plasma cells was positively correlated (
< 0.0001,
= 0.558), while immunoglobulin gene IGKC, IGHM, and IGHG1 mRNA expression correlated specifically with the density of CD38
plasma cells (IGKC
< 0.0001,
= 0.647; IGHM
< 0.0001,
= 0.580; IGHG1
< 0.0001,
= 0.655). Interestingly, after adjusting the multivariate analysis for the effect of intratumoral CD38
plasma cell density, the expression levels of all three genes lost significant prognostic value, suggesting a biologically important role of plasma cells. Last but not least, the addition of intratumoral CD38
plasma cell density to clinicopathological features significantly increased the prognostic value for both DFS (ΔLRχ
= 17.28,
= 1.71E-08) and OS (ΔLRχ
= 10.03,
= 6.32E-08), compared to clinicopathological features alone. The best combination was achieved by integrating intratumoral CD38
plasma cell density and IGHG1 which conferred the best added prognostic value for DFS (ΔLRχ
= 27.38,
= 5.22E-10) and OS (ΔLRχ
= 21.29,
= 1.03E-08). Our results demonstrate that the role of plasma cells in TNBC warrants further study to elucidate the relationship between their infiltration of tumors and disease recurrence. Breast cancer is the most common malignancy affecting women, but the heterogeneity of the condition is a significant obstacle to effective treatment. Triple negative breast cancers (TNBCs) do not express HER2 or the receptors for estrogen or progesterone, and so often have a poor prognosis. Tumor-infiltrating T cells have been well-characterized in TNBC, and increased numbers are associated with better outcomes; however, the potential roles of B cells and plasma cells have been large. Here, we conducted a retrospective correlative study on the expression of B cell/plasma cell-related genes, and the abundance and localization of B cells and plasma cells within TNBCs, and clinical outcome. We analyzed 269 TNBC samples and used immunohistochemistry to quantify tumor-infiltrating B cells and plasma cells, coupled with NanoString measurement of expression of immunoglobulin metagenes. Multivariate analysis revealed that patients bearing TNBCs with above-median densities of CD38+ plasma cells had significantly better disease-free survival (DFS) (HR = 0.44; 95% CI 0.26–0.77; p = 0.004) but not overall survival (OS), after adjusting for the effects of known prognostic factors. In contrast, TNBCs with higher immunoglobulin gene expression exhibited improved prognosis (OS p = 0.029 and DFS p = 0.005). The presence of B cells and plasma cells was positively correlated (p < 0.0001, R = 0.558), while immunoglobulin gene IGKC, IGHM, and IGHG1 mRNA expression correlated specifically with the density of CD38+ plasma cells (IGKC p < 0.0001, R = 0.647; IGHM p < 0.0001, R = 0.580; IGHG1 p < 0.0001, R = 0.655). Interestingly, after adjusting the multivariate analysis for the effect of intratumoral CD38+ plasma cell density, the expression levels of all three genes lost significant prognostic value, suggesting a biologically important role of plasma cells. Last but not least, the addition of intratumoral CD38+ plasma cell density to clinicopathological features significantly increased the prognostic value for both DFS (ΔLRχ2 = 17.28, p = 1.71E−08) and OS (ΔLRχ2 = 10.03, p = 6.32E−08), compared to clinicopathological features alone. The best combination was achieved by integrating intratumoral CD38+ plasma cell density and IGHG1 which conferred the best added prognostic value for DFS (ΔLRχ2 = 27.38, p = 5.22E−10) and OS (ΔLRχ2 = 21.29, p = 1.03E−08). Our results demonstrate that the role of plasma cells in TNBC warrants further study to elucidate the relationship between their infiltration of tumors and disease recurrence. Breast cancer is the most common malignancy affecting women, but the heterogeneity of the condition is a significant obstacle to effective treatment. Triple negative breast cancers (TNBCs) do not express HER2 or the receptors for estrogen or progesterone, and so often have a poor prognosis. Tumor-infiltrating T cells have been well-characterized in TNBC, and increased numbers are associated with better outcomes; however, the potential roles of B cells and plasma cells have been large. Here, we conducted a retrospective correlative study on the expression of B cell/plasma cell-related genes, and the abundance and localization of B cells and plasma cells within TNBCs, and clinical outcome. We analyzed 269 TNBC samples and used immunohistochemistry to quantify tumor-infiltrating B cells and plasma cells, coupled with NanoString measurement of expression of immunoglobulin metagenes. Multivariate analysis revealed that patients bearing TNBCs with above-median densities of CD38 + plasma cells had significantly better disease-free survival (DFS) (HR = 0.44; 95% CI 0.26–0.77; p = 0.004) but not overall survival (OS), after adjusting for the effects of known prognostic factors. In contrast, TNBCs with higher immunoglobulin gene expression exhibited improved prognosis (OS p = 0.029 and DFS p = 0.005). The presence of B cells and plasma cells was positively correlated ( p < 0.0001, R = 0.558), while immunoglobulin gene IGKC, IGHM, and IGHG1 mRNA expression correlated specifically with the density of CD38 + plasma cells (IGKC p < 0.0001, R = 0.647; IGHM p < 0.0001, R = 0.580; IGHG1 p < 0.0001, R = 0.655). Interestingly, after adjusting the multivariate analysis for the effect of intratumoral CD38 + plasma cell density, the expression levels of all three genes lost significant prognostic value, suggesting a biologically important role of plasma cells. Last but not least, the addition of intratumoral CD38 + plasma cell density to clinicopathological features significantly increased the prognostic value for both DFS (ΔLRχ 2 = 17.28, p = 1.71E−08) and OS (ΔLRχ 2 = 10.03, p = 6.32E−08), compared to clinicopathological features alone. The best combination was achieved by integrating intratumoral CD38 + plasma cell density and IGHG1 which conferred the best added prognostic value for DFS (ΔLRχ 2 = 27.38, p = 5.22E−10) and OS (ΔLRχ 2 = 21.29, p = 1.03E−08). Our results demonstrate that the role of plasma cells in TNBC warrants further study to elucidate the relationship between their infiltration of tumors and disease recurrence. |
Author | Chia, Noel Iqbal, Jabed Yeong, Joe Ong, Clara Chong Hui Lim, Elaine Putti, Thomas Choudary Lee, Bernett Li, Huihua Tan, Puay Hoon Thike, Aye Aye Dent, Rebecca Lim, Jeffrey Chun Tatt Lye, Weng Kit |
AuthorAffiliation | 1 Division of Pathology, Singapore General Hospital , Singapore , Singapore 3 Division of Medicine, Singapore General Hospital , Singapore , Singapore 6 Department of Pathology, Yong Loo Lin School of Medicine, National University of Singapore , Singapore , Singapore 7 National Cancer Center , Singapore , Singapore 5 Centre for Quantitative Medicine, Duke-NUS Medical School , Singapore , Singapore 2 Singapore Immunology Network (SIgN), Agency of Science, Technology and Research (ASTAR) , Singapore , Singapore 4 Faculty of Medicine, University of New South Wales , Sydney, NSW , Australia |
AuthorAffiliation_xml | – name: 3 Division of Medicine, Singapore General Hospital , Singapore , Singapore – name: 7 National Cancer Center , Singapore , Singapore – name: 4 Faculty of Medicine, University of New South Wales , Sydney, NSW , Australia – name: 5 Centre for Quantitative Medicine, Duke-NUS Medical School , Singapore , Singapore – name: 2 Singapore Immunology Network (SIgN), Agency of Science, Technology and Research (ASTAR) , Singapore , Singapore – name: 6 Department of Pathology, Yong Loo Lin School of Medicine, National University of Singapore , Singapore , Singapore – name: 1 Division of Pathology, Singapore General Hospital , Singapore , Singapore |
Author_xml | – sequence: 1 givenname: Joe surname: Yeong fullname: Yeong, Joe organization: Singapore Immunology Network (SIgN), Agency of Science, Technology and Research (ASTAR), Singapore, Singapore – sequence: 2 givenname: Jeffrey Chun Tatt surname: Lim fullname: Lim, Jeffrey Chun Tatt organization: Division of Pathology, Singapore General Hospital, Singapore, Singapore – sequence: 3 givenname: Bernett surname: Lee fullname: Lee, Bernett organization: Singapore Immunology Network (SIgN), Agency of Science, Technology and Research (ASTAR), Singapore, Singapore – sequence: 4 givenname: Huihua surname: Li fullname: Li, Huihua organization: Division of Medicine, Singapore General Hospital, Singapore, Singapore – sequence: 5 givenname: Noel surname: Chia fullname: Chia, Noel organization: Faculty of Medicine, University of New South Wales, Sydney, NSW, Australia – sequence: 6 givenname: Clara Chong Hui surname: Ong fullname: Ong, Clara Chong Hui organization: Division of Pathology, Singapore General Hospital, Singapore, Singapore – sequence: 7 givenname: Weng Kit surname: Lye fullname: Lye, Weng Kit organization: Centre for Quantitative Medicine, Duke-NUS Medical School, Singapore, Singapore – sequence: 8 givenname: Thomas Choudary surname: Putti fullname: Putti, Thomas Choudary organization: Department of Pathology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore – sequence: 9 givenname: Rebecca surname: Dent fullname: Dent, Rebecca organization: National Cancer Center, Singapore, Singapore – sequence: 10 givenname: Elaine surname: Lim fullname: Lim, Elaine organization: National Cancer Center, Singapore, Singapore – sequence: 11 givenname: Aye Aye surname: Thike fullname: Thike, Aye Aye organization: Division of Pathology, Singapore General Hospital, Singapore, Singapore – sequence: 12 givenname: Puay Hoon surname: Tan fullname: Tan, Puay Hoon organization: Division of Pathology, Singapore General Hospital, Singapore, Singapore – sequence: 13 givenname: Jabed surname: Iqbal fullname: Iqbal, Jabed organization: Division of Pathology, Singapore General Hospital, Singapore, Singapore |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29899747$$D View this record in MEDLINE/PubMed |
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ContentType | Journal Article |
Copyright | Copyright © 2018 Yeong, Lim, Lee, Li, Chia, Ong, Lye, Putti, Dent, Lim, Thike, Tan and Iqbal. 2018 Yeong, Lim, Lee, Li, Chia, Ong, Lye, Putti, Dent, Lim, Thike, Tan and Iqbal |
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Keywords | triple negative breast cancer tumor immunology B cells immunohistochemistry plasma cells |
Language | English |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by: Petranel Theresa Ferrao, University of Melbourne, Australia Specialty section: This article was submitted to Cancer Immunity and Immunotherapy, a section of the journal Frontiers in Immunology Reviewed by: Pin Wu, Zhejiang University, China; Marleen Kok, Netherlands Cancer Institute (NKI), Netherlands |
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Title | High Densities of Tumor-Associated Plasma Cells Predict Improved Prognosis in Triple Negative Breast Cancer |
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