Skip to main content
Top
Published in: Breast Cancer Research and Treatment 1/2019

01-08-2019 | Biomarkers | Review

Prognostic role of immune infiltrates in breast ductal carcinoma in situ

Authors: Xiao-Yang Chen, Joe Yeong, Aye Aye Thike, Boon Huat Bay, Puay Hoon Tan

Published in: Breast Cancer Research and Treatment | Issue 1/2019

Login to get access

Abstract

Purpose

Ductal carcinoma in situ (DCIS) of the breast is often regarded as a non-obligate precursor to invasive breast carcinoma but current diagnostic tools are unable to accurately predict the invasive potential of DCIS. Infiltration of immune cells into the tumour and its microenvironment is often an early event at the site of tumourigenesis. These immune infiltrates may be potential predictive and/or prognostic biomarkers for DCIS. This review aims to discuss recent findings pertaining to the potential prognostic significance of immune infiltrates as well as their evaluation in DCIS.

Methods

A literature search on PubMed was conducted up to 28th January 2019. Search terms used were “DCIS”, “ductal carcinoma in situ”, “immune”, “immunology”, “TIL”, “TIL assessment”, and “tumour-infiltrating lymphocyte”. Search filters for “Most Recent” and “English” were applied. Information from published papers related to the research topic were synthesised and summarised for this review.

Results

Studies have revealed that immune infiltrates play a role in the biology and microenvironment of DCIS, as well as treatment response. There is currently no consensus on the evaluation of TILs in DCIS for clinical application.

Conclusions

This review highlights the recent findings on the potential influence and prognostic value of immunological processes on DCIS progression, as well as the evaluation of TILs in DCIS. Further characterisation of the immune milieu of DCIS is recommended to better understand the immune response in DCIS progression and recurrence.
Literature
2.
go back to reference Koh VC, Lim JC, Thike AA, Cheok PY, Thu MM, Tan VK, Tan BK, Ong KW, Ho GH, Tan WJ, Tan Y, Salahuddin AS, Busmanis I, Chong AP, Iqbal J, Thilagaratnam S, Wong JS, Tan PH (2015) Characteristics and behaviour of screen-detected ductal carcinoma in situ of the breast: comparison with symptomatic patients. Breast Cancer Res Treat 152(2):293–304. https://doi.org/10.1007/s10549-015-3472-6 CrossRefPubMed Koh VC, Lim JC, Thike AA, Cheok PY, Thu MM, Tan VK, Tan BK, Ong KW, Ho GH, Tan WJ, Tan Y, Salahuddin AS, Busmanis I, Chong AP, Iqbal J, Thilagaratnam S, Wong JS, Tan PH (2015) Characteristics and behaviour of screen-detected ductal carcinoma in situ of the breast: comparison with symptomatic patients. Breast Cancer Res Treat 152(2):293–304. https://​doi.​org/​10.​1007/​s10549-015-3472-6 CrossRefPubMed
4.
go back to reference Wellings SR, Jensen HM (1973) On the origin and progression of ductal carcinoma in the human breast. J Natl Cancer Inst 50(5):1111–1118CrossRefPubMed Wellings SR, Jensen HM (1973) On the origin and progression of ductal carcinoma in the human breast. J Natl Cancer Inst 50(5):1111–1118CrossRefPubMed
10.
go back to reference Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP, Yang F, Talantov D, Timmermans M, Meijer-van Gelder ME, Yu J, Jatkoe T, Berns EM, Atkins D, Foekens JA (2005) Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet (London, England) 365(9460):671–679. https://doi.org/10.1016/s0140-6736(05)17947-1 CrossRef Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP, Yang F, Talantov D, Timmermans M, Meijer-van Gelder ME, Yu J, Jatkoe T, Berns EM, Atkins D, Foekens JA (2005) Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet (London, England) 365(9460):671–679. https://​doi.​org/​10.​1016/​s0140-6736(05)17947-1 CrossRef
13.
go back to reference Fleischer T, Frigessi A, Johnson KC, Edvardsen H, Touleimat N, Klajic J, Riis ML, Haakensen VD, Wärnberg F, Naume B, Helland Å, Børresen-Dale A-L, Tost J, Christensen BC, Kristensen VNJGB (2014) Genome-wide DNA methylation profiles in progression to in situ and invasive carcinoma of the breast with impact on gene transcription and prognosis. Genome Biol 15(8):435. https://doi.org/10.1186/s13059-014-0435-x CrossRefPubMedPubMedCentral Fleischer T, Frigessi A, Johnson KC, Edvardsen H, Touleimat N, Klajic J, Riis ML, Haakensen VD, Wärnberg F, Naume B, Helland Å, Børresen-Dale A-L, Tost J, Christensen BC, Kristensen VNJGB (2014) Genome-wide DNA methylation profiles in progression to in situ and invasive carcinoma of the breast with impact on gene transcription and prognosis. Genome Biol 15(8):435. https://​doi.​org/​10.​1186/​s13059-014-0435-x CrossRefPubMedPubMedCentral
17.
go back to reference Pang J-MB, Savas P, Fellowes AP, Mir Arnau G, Kader T, Vedururu R, Hewitt C, Takano EA, Byrne DJ, Choong DYH, Millar EKA, Lee CS, O’Toole SA, Lakhani SR, Cummings MC, Mann GB, Campbell IG, Dobrovic A, Loi S, Gorringe KL, Fox SB (2017) Breast ductal carcinoma in situ carry mutational driver events representative of invasive breast cancer. Mod Pathol 30(7):952. https://doi.org/10.1038/modpathol.2017.21 CrossRefPubMed Pang J-MB, Savas P, Fellowes AP, Mir Arnau G, Kader T, Vedururu R, Hewitt C, Takano EA, Byrne DJ, Choong DYH, Millar EKA, Lee CS, O’Toole SA, Lakhani SR, Cummings MC, Mann GB, Campbell IG, Dobrovic A, Loi S, Gorringe KL, Fox SB (2017) Breast ductal carcinoma in situ carry mutational driver events representative of invasive breast cancer. Mod Pathol 30(7):952. https://​doi.​org/​10.​1038/​modpathol.​2017.​21 CrossRefPubMed
18.
go back to reference Ottesen GL, Christensen IJ, Larsen JK, Larsen J, Christiansen J, Baldetorp B, Linden T, Hansen B, Andersen JA (1997) DNA ploidy analysis in breast carcinoma. Comparison of unfixed and fixed tissue analyzed by image and flow cytometry. Anal Quant Cytol Histol 19(5):413–422PubMed Ottesen GL, Christensen IJ, Larsen JK, Larsen J, Christiansen J, Baldetorp B, Linden T, Hansen B, Andersen JA (1997) DNA ploidy analysis in breast carcinoma. Comparison of unfixed and fixed tissue analyzed by image and flow cytometry. Anal Quant Cytol Histol 19(5):413–422PubMed
19.
go back to reference Giardina C, Serio G, Lepore G, Lettini T, Dalena AM, Pennella A, D’Eredita G, Valente T, Ricco R (2003) Pure ductal carcinoma in situ and in situ component of ductal invasive carcinoma of the breast. A preliminary morphometric study. J Exp Clin Cancer Res 22(2):279–288PubMed Giardina C, Serio G, Lepore G, Lettini T, Dalena AM, Pennella A, D’Eredita G, Valente T, Ricco R (2003) Pure ductal carcinoma in situ and in situ component of ductal invasive carcinoma of the breast. A preliminary morphometric study. J Exp Clin Cancer Res 22(2):279–288PubMed
23.
go back to reference Fisher ER, Gregorio RM, Fisher B, Redmond C, Vellios F, Sommers SC (1975) The pathology of invasive breast cancer. A syllabus derived from findings of the National Surgical Adjuvant Breast Project (protocol no. 4). Cancer 36(1):1–85CrossRefPubMed Fisher ER, Gregorio RM, Fisher B, Redmond C, Vellios F, Sommers SC (1975) The pathology of invasive breast cancer. A syllabus derived from findings of the National Surgical Adjuvant Breast Project (protocol no. 4). Cancer 36(1):1–85CrossRefPubMed
33.
go back to reference Gil Del Alcazar CR, Huh SJ, Ekram MB, Trinh A, Liu LL, Beca F, Zi X, Kwak M, Bergholtz H, Su Y, Ding L, Russnes HG, Richardson AL, Babski K, Min Hui Kim E, McDonnell CH 3rd, Wagner J, Rowberry R, Freeman GJ, Dillon D, Sorlie T, Coussens LM, Garber JE, Fan R, Bobolis K, Allred DC, Jeong J, Park SY, Michor F, Polyak K (2017) Immune escape in breast cancer during in situ to invasive carcinoma transition. Cancer Discov 7(10):1098–1115. https://doi.org/10.1158/2159-8290.Cd-17-0222 CrossRefPubMedPubMedCentral Gil Del Alcazar CR, Huh SJ, Ekram MB, Trinh A, Liu LL, Beca F, Zi X, Kwak M, Bergholtz H, Su Y, Ding L, Russnes HG, Richardson AL, Babski K, Min Hui Kim E, McDonnell CH 3rd, Wagner J, Rowberry R, Freeman GJ, Dillon D, Sorlie T, Coussens LM, Garber JE, Fan R, Bobolis K, Allred DC, Jeong J, Park SY, Michor F, Polyak K (2017) Immune escape in breast cancer during in situ to invasive carcinoma transition. Cancer Discov 7(10):1098–1115. https://​doi.​org/​10.​1158/​2159-8290.​Cd-17-0222 CrossRefPubMedPubMedCentral
41.
go back to reference Hendry S, Salgado R, Gevaert T, Russell PA, John T, Thapa B, Christie M, van de Vijver K, Estrada MV, Gonzalez-Ericsson PI, Sanders M, Solomon B, Solinas C, Van den Eynden G, Allory Y, Preusser M, Hainfellner J, Pruneri G, Vingiani A, Demaria S, Symmans F, Nuciforo P, Comerma L, Thompson EA, Lakhani S, Kim SR, Schnitt S, Colpaert C, Sotiriou C, Scherer SJ, Ignatiadis M, Badve S, Pierce RH, Viale G, Sirtaine N, Penault-Llorca F, Sugie T, Fineberg S, Paik S, Srinivasan A, Richardson A, Wang Y, Chmielik E, Brock J, Johnson DB, Balko J, Wienert S, Bossuyt V, Michiels S, Ternes N, Burchardi N, Luen SJ, Savas P, Klauschen F, Watson PH, Nelson BH, Criscitiello C, O’Toole S, Larsimont D, de Wind R, Curigliano G, Andre F, Lacroix-Triki M, van de Vijver M, Rojo F, Floris G, Bedri S, Sparano J, Rimm D, Nielsen T, Kos Z, Hewitt S, Singh B, Farshid G, Loibl S, Allison KH, Tung N, Adams S, Willard-Gallo K, Horlings HM, Gandhi L, Moreira A, Hirsch F, Dieci MV, Urbanowicz M, Brcic I, Korski K, Gaire F, Koeppen H, Lo A, Giltnane J, Rebelatto MC, Steele KE, Zha J, Emancipator K, Juco JW, Denkert C, Reis-Filho J, Loi S, Fox SB (2017) Assessing tumor-infiltrating lymphocytes in solid tumors: a practical review for pathologists and proposal for a standardized method from the International Immunooncology Biomarkers Working Group: Part 1: Assessing the host immune response, TILs in invasive breast carcinoma and ductal carcinoma in situ, metastatic tumor deposits and areas for further research. Adv Anat Pathol 24(5):235–251. https://doi.org/10.1097/pap.0000000000000162 CrossRefPubMedPubMedCentral Hendry S, Salgado R, Gevaert T, Russell PA, John T, Thapa B, Christie M, van de Vijver K, Estrada MV, Gonzalez-Ericsson PI, Sanders M, Solomon B, Solinas C, Van den Eynden G, Allory Y, Preusser M, Hainfellner J, Pruneri G, Vingiani A, Demaria S, Symmans F, Nuciforo P, Comerma L, Thompson EA, Lakhani S, Kim SR, Schnitt S, Colpaert C, Sotiriou C, Scherer SJ, Ignatiadis M, Badve S, Pierce RH, Viale G, Sirtaine N, Penault-Llorca F, Sugie T, Fineberg S, Paik S, Srinivasan A, Richardson A, Wang Y, Chmielik E, Brock J, Johnson DB, Balko J, Wienert S, Bossuyt V, Michiels S, Ternes N, Burchardi N, Luen SJ, Savas P, Klauschen F, Watson PH, Nelson BH, Criscitiello C, O’Toole S, Larsimont D, de Wind R, Curigliano G, Andre F, Lacroix-Triki M, van de Vijver M, Rojo F, Floris G, Bedri S, Sparano J, Rimm D, Nielsen T, Kos Z, Hewitt S, Singh B, Farshid G, Loibl S, Allison KH, Tung N, Adams S, Willard-Gallo K, Horlings HM, Gandhi L, Moreira A, Hirsch F, Dieci MV, Urbanowicz M, Brcic I, Korski K, Gaire F, Koeppen H, Lo A, Giltnane J, Rebelatto MC, Steele KE, Zha J, Emancipator K, Juco JW, Denkert C, Reis-Filho J, Loi S, Fox SB (2017) Assessing tumor-infiltrating lymphocytes in solid tumors: a practical review for pathologists and proposal for a standardized method from the International Immunooncology Biomarkers Working Group: Part 1: Assessing the host immune response, TILs in invasive breast carcinoma and ductal carcinoma in situ, metastatic tumor deposits and areas for further research. Adv Anat Pathol 24(5):235–251. https://​doi.​org/​10.​1097/​pap.​0000000000000162​ CrossRefPubMedPubMedCentral
44.
49.
go back to reference Pruneri G, Lazzeroni M, Bagnardi V, Tiburzio GB, Rotmensz N, DeCensi A, Guerrieri-Gonzaga A, Vingiani A, Curigliano G, Zurrida S, Bassi F, Salgado R, Van den Eynden G, Loi S, Denkert C, Bonanni B, Viale G (2017) The prevalence and clinical relevance of tumor-infiltrating lymphocytes (TILs) in ductal carcinoma in situ of the breast. Ann Oncol 28(2):321–328. https://doi.org/10.1093/annonc/mdw623 CrossRefPubMed Pruneri G, Lazzeroni M, Bagnardi V, Tiburzio GB, Rotmensz N, DeCensi A, Guerrieri-Gonzaga A, Vingiani A, Curigliano G, Zurrida S, Bassi F, Salgado R, Van den Eynden G, Loi S, Denkert C, Bonanni B, Viale G (2017) The prevalence and clinical relevance of tumor-infiltrating lymphocytes (TILs) in ductal carcinoma in situ of the breast. Ann Oncol 28(2):321–328. https://​doi.​org/​10.​1093/​annonc/​mdw623 CrossRefPubMed
51.
go back to reference Man YG, Tai L, Barner R, Vang R, Saenger JS, Shekitka KM, Bratthauer GL, Wheeler DT, Liang CY, Vinh TN, Strauss BL (2003) Cell clusters overlying focally disrupted mammary myoepithelial cell layers and adjacent cells within the same duct display different immunohistochemical and genetic features: implications for tumor progression and invasion. Breast Cancer Res 5(6):R231–R241. https://doi.org/10.1186/bcr653 CrossRefPubMedPubMedCentral Man YG, Tai L, Barner R, Vang R, Saenger JS, Shekitka KM, Bratthauer GL, Wheeler DT, Liang CY, Vinh TN, Strauss BL (2003) Cell clusters overlying focally disrupted mammary myoepithelial cell layers and adjacent cells within the same duct display different immunohistochemical and genetic features: implications for tumor progression and invasion. Breast Cancer Res 5(6):R231–R241. https://​doi.​org/​10.​1186/​bcr653 CrossRefPubMedPubMedCentral
55.
go back to reference Loi S, Michiels S, Salgado R, Sirtaine N, Jose V, Fumagalli D, Kellokumpu-Lehtinen PL, Bono P, Kataja V, Desmedt C, Piccart MJ, Loibl S, Denkert C, Smyth MJ, Joensuu H, Sotiriou C (2014) Tumor infiltrating lymphocytes are prognostic in triple negative breast cancer and predictive for trastuzumab benefit in early breast cancer: results from the FinHER trial. Ann Oncol 25(8):1544–1550. https://doi.org/10.1093/annonc/mdu112 CrossRefPubMed Loi S, Michiels S, Salgado R, Sirtaine N, Jose V, Fumagalli D, Kellokumpu-Lehtinen PL, Bono P, Kataja V, Desmedt C, Piccart MJ, Loibl S, Denkert C, Smyth MJ, Joensuu H, Sotiriou C (2014) Tumor infiltrating lymphocytes are prognostic in triple negative breast cancer and predictive for trastuzumab benefit in early breast cancer: results from the FinHER trial. Ann Oncol 25(8):1544–1550. https://​doi.​org/​10.​1093/​annonc/​mdu112 CrossRefPubMed
57.
58.
go back to reference Ben-Hur H, Cohen O, Schneider D, Gurevich P, Halperin R, Bala U, Mozes M, Zusman I (2002) The role of lymphocytes and macrophages in human breast tumorigenesis: an immunohistochemical and morphometric study. Anticancer Res 22(2b):1231–1238PubMed Ben-Hur H, Cohen O, Schneider D, Gurevich P, Halperin R, Bala U, Mozes M, Zusman I (2002) The role of lymphocytes and macrophages in human breast tumorigenesis: an immunohistochemical and morphometric study. Anticancer Res 22(2b):1231–1238PubMed
59.
60.
go back to reference Loi S, Sirtaine N, Piette F, Salgado R, Viale G, Van Eenoo F, Rouas G, Francis P, Crown JP, Hitre E, de Azambuja E, Quinaux E, Di Leo A, Michiels S, Piccart MJ, Sotiriou C (2013) Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: bIG 02-98. J Clin Oncol 31(7):860–867. https://doi.org/10.1200/jco.2011.41.0902 CrossRefPubMed Loi S, Sirtaine N, Piette F, Salgado R, Viale G, Van Eenoo F, Rouas G, Francis P, Crown JP, Hitre E, de Azambuja E, Quinaux E, Di Leo A, Michiels S, Piccart MJ, Sotiriou C (2013) Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: bIG 02-98. J Clin Oncol 31(7):860–867. https://​doi.​org/​10.​1200/​jco.​2011.​41.​0902 CrossRefPubMed
66.
go back to reference Bilik R, Mor C, Hazaz B, Moroz C (1989) Characterization of T-lymphocyte subpopulations infiltrating primary breast cancer. Cancer Immunol Immunother 28(2):143–147CrossRefPubMed Bilik R, Mor C, Hazaz B, Moroz C (1989) Characterization of T-lymphocyte subpopulations infiltrating primary breast cancer. Cancer Immunol Immunother 28(2):143–147CrossRefPubMed
69.
go back to reference Senovilla L, Vitale I, Martins I, Tailler M, Pailleret C, Michaud M, Galluzzi L, Adjemian S, Kepp O, Niso-Santano M, Shen S, Marino G, Criollo A, Boileve A, Job B, Ladoire S, Ghiringhelli F, Sistigu A, Yamazaki T, Rello-Varona S, Locher C, Poirier-Colame V, Talbot M, Valent A, Berardinelli F, Antoccia A, Ciccosanti F, Fimia GM, Piacentini M, Fueyo A, Messina NL, Li M, Chan CJ, Sigl V, Pourcher G, Ruckenstuhl C, Carmona-Gutierrez D, Lazar V, Penninger JM, Madeo F, Lopez-Otin C, Smyth MJ, Zitvogel L, Castedo M, Kroemer G (2012) An immunosurveillance mechanism controls cancer cell ploidy. Science 337(6102):1678–1684. https://doi.org/10.1126/science.1224922 CrossRefPubMed Senovilla L, Vitale I, Martins I, Tailler M, Pailleret C, Michaud M, Galluzzi L, Adjemian S, Kepp O, Niso-Santano M, Shen S, Marino G, Criollo A, Boileve A, Job B, Ladoire S, Ghiringhelli F, Sistigu A, Yamazaki T, Rello-Varona S, Locher C, Poirier-Colame V, Talbot M, Valent A, Berardinelli F, Antoccia A, Ciccosanti F, Fimia GM, Piacentini M, Fueyo A, Messina NL, Li M, Chan CJ, Sigl V, Pourcher G, Ruckenstuhl C, Carmona-Gutierrez D, Lazar V, Penninger JM, Madeo F, Lopez-Otin C, Smyth MJ, Zitvogel L, Castedo M, Kroemer G (2012) An immunosurveillance mechanism controls cancer cell ploidy. Science 337(6102):1678–1684. https://​doi.​org/​10.​1126/​science.​1224922 CrossRefPubMed
72.
go back to reference Gobert M, Treilleux I, Bendriss-Vermare N, Bachelot T, Goddard-Leon S, Arfi V, Biota C, Doffin AC, Durand I, Olive D, Perez S, Pasqual N, Faure C, Ray-Coquard I, Puisieux A, Caux C, Blay JY, Menetrier-Caux C (2009) Regulatory T cells recruited through CCL22/CCR72 are selectively activated in lymphoid infiltrates surrounding primary breast tumors and lead to an adverse clinical outcome. Can Res 69(5):2000–2009. https://doi.org/10.1158/0008-5472.Can-08-2360 CrossRef Gobert M, Treilleux I, Bendriss-Vermare N, Bachelot T, Goddard-Leon S, Arfi V, Biota C, Doffin AC, Durand I, Olive D, Perez S, Pasqual N, Faure C, Ray-Coquard I, Puisieux A, Caux C, Blay JY, Menetrier-Caux C (2009) Regulatory T cells recruited through CCL22/CCR72 are selectively activated in lymphoid infiltrates surrounding primary breast tumors and lead to an adverse clinical outcome. Can Res 69(5):2000–2009. https://​doi.​org/​10.​1158/​0008-5472.​Can-08-2360 CrossRef
74.
go back to reference Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, Zhu Y, Wei S, Kryczek I, Daniel B, Gordon A, Myers L, Lackner A, Disis ML, Knutson KL, Chen L, Zou W (2004) Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 10(9):942–949. https://doi.org/10.1038/nm1093 CrossRefPubMed Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, Zhu Y, Wei S, Kryczek I, Daniel B, Gordon A, Myers L, Lackner A, Disis ML, Knutson KL, Chen L, Zou W (2004) Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 10(9):942–949. https://​doi.​org/​10.​1038/​nm1093 CrossRefPubMed
83.
85.
go back to reference Urdiales-Viedma M, Nogales-Fernandez F, Martos-Padilla S, Sanchez-Cantalejo E (1986) Breast tumors: immunoglobulins in axillary lymph nodes. Tumori J 72(6):575–579CrossRef Urdiales-Viedma M, Nogales-Fernandez F, Martos-Padilla S, Sanchez-Cantalejo E (1986) Breast tumors: immunoglobulins in axillary lymph nodes. Tumori J 72(6):575–579CrossRef
86.
go back to reference DiLillo DJ, Hamaguchi Y, Ueda Y, Yang K, Uchida J, Haas KM, Kelsoe G, Tedder TF (2008) Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J Immunol 180(1):361–371CrossRefPubMed DiLillo DJ, Hamaguchi Y, Ueda Y, Yang K, Uchida J, Haas KM, Kelsoe G, Tedder TF (2008) Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J Immunol 180(1):361–371CrossRefPubMed
87.
go back to reference Otero DC, Anzelon AN, Rickert RC (2003) CD19 function in early and late B cell development: I. Maintenance of follicular and marginal zone B cells requires CD19-dependent survival signals. J Immunol 170(1):73–83CrossRefPubMed Otero DC, Anzelon AN, Rickert RC (2003) CD19 function in early and late B cell development: I. Maintenance of follicular and marginal zone B cells requires CD19-dependent survival signals. J Immunol 170(1):73–83CrossRefPubMed
90.
go back to reference Wijdenes J, Vooijs WC, Clement C, Post J, Morard F, Vita N, Laurent P, Sun RX, Klein B, Dore JM (1996) A plasmocyte selective monoclonal antibody (B-B4) recognizes syndecan-1. Br J Haematol 94(2):318–323CrossRefPubMed Wijdenes J, Vooijs WC, Clement C, Post J, Morard F, Vita N, Laurent P, Sun RX, Klein B, Dore JM (1996) A plasmocyte selective monoclonal antibody (B-B4) recognizes syndecan-1. Br J Haematol 94(2):318–323CrossRefPubMed
91.
go back to reference Barbareschi M, Maisonneuve P, Aldovini D, Cangi MG, Pecciarini L, Angelo Mauri F, Veronese S, Caffo O, Lucenti A, Palma PD, Galligioni E, Doglioni C (2003) High syndecan-1 expression in breast carcinoma is related to an aggressive phenotype and to poorer prognosis. Cancer 98(3):474–483. https://doi.org/10.1002/cncr.11515 CrossRefPubMed Barbareschi M, Maisonneuve P, Aldovini D, Cangi MG, Pecciarini L, Angelo Mauri F, Veronese S, Caffo O, Lucenti A, Palma PD, Galligioni E, Doglioni C (2003) High syndecan-1 expression in breast carcinoma is related to an aggressive phenotype and to poorer prognosis. Cancer 98(3):474–483. https://​doi.​org/​10.​1002/​cncr.​11515 CrossRefPubMed
93.
go back to reference Kato M, Wang H, Kainulainen V, Fitzgerald ML, Ledbetter S, Ornitz DM, Bernfield M (1998) Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2. Nat Med 4(6):691–697CrossRefPubMed Kato M, Wang H, Kainulainen V, Fitzgerald ML, Ledbetter S, Ornitz DM, Bernfield M (1998) Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2. Nat Med 4(6):691–697CrossRefPubMed
99.
go back to reference Raes G, Brys L, Dahal BK, Brandt J, Grooten J, Brombacher F, Vanham G, Noel W, Bogaert P, Boonefaes T, Kindt A, Van den Bergh R, Leenen PJ, De Baetselier P, Ghassabeh GH (2005) Macrophage galactose-type C-type lectins as novel markers for alternatively activated macrophages elicited by parasitic infections and allergic airway inflammation. J Leukoc Biol 77(3):321–327. https://doi.org/10.1189/jlb.0304212 CrossRefPubMed Raes G, Brys L, Dahal BK, Brandt J, Grooten J, Brombacher F, Vanham G, Noel W, Bogaert P, Boonefaes T, Kindt A, Van den Bergh R, Leenen PJ, De Baetselier P, Ghassabeh GH (2005) Macrophage galactose-type C-type lectins as novel markers for alternatively activated macrophages elicited by parasitic infections and allergic airway inflammation. J Leukoc Biol 77(3):321–327. https://​doi.​org/​10.​1189/​jlb.​0304212 CrossRefPubMed
102.
go back to reference Sica A, Saccani A, Mantovani A (2002) Tumor-associated macrophages: a molecular perspective. Int Immunopharmacol 2(8):1045–1054CrossRefPubMed Sica A, Saccani A, Mantovani A (2002) Tumor-associated macrophages: a molecular perspective. Int Immunopharmacol 2(8):1045–1054CrossRefPubMed
103.
109.
go back to reference Salgado R, Denkert C, Demaria S, Sirtaine N, Klauschen F, Pruneri G, Wienert S, Van den Eynden G, Baehner FL, Penault-Llorca F, Perez EA, Thompson EA, Symmans WF, Richardson AL, Brock J, Criscitiello C, Bailey H, Ignatiadis M, Floris G, Sparano J, Kos Z, Nielsen T, Rimm DL, Allison KH, Reis-Filho JS, Loibl S, Sotiriou C, Viale G, Badve S, Adams S, Willard-Gallo K, Loi S (2015) The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014. Ann Oncol 26(2):259–271. https://doi.org/10.1093/annonc/mdu450 CrossRefPubMed Salgado R, Denkert C, Demaria S, Sirtaine N, Klauschen F, Pruneri G, Wienert S, Van den Eynden G, Baehner FL, Penault-Llorca F, Perez EA, Thompson EA, Symmans WF, Richardson AL, Brock J, Criscitiello C, Bailey H, Ignatiadis M, Floris G, Sparano J, Kos Z, Nielsen T, Rimm DL, Allison KH, Reis-Filho JS, Loibl S, Sotiriou C, Viale G, Badve S, Adams S, Willard-Gallo K, Loi S (2015) The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014. Ann Oncol 26(2):259–271. https://​doi.​org/​10.​1093/​annonc/​mdu450 CrossRefPubMed
111.
go back to reference Dieci MV, Radosevic-Robin N, Fineberg S, van den Eynden G, Ternes N, Penault-Llorca F, Pruneri G, D’Alfonso TM, Demaria S, Castaneda C, Sanchez J, Badve S, Michiels S, Bossuyt V, Rojo F, Singh B, Nielsen T, Viale G, Kim SR, Hewitt S, Wienert S, Loibl S, Rimm D, Symmans F, Denkert C, Adams S, Loi S, Salgado R (2017) Update on tumor-infiltrating lymphocytes (TILs) in breast cancer, including recommendations to assess TILs in residual disease after neoadjuvant therapy and in carcinoma in situ: a report of the International Immuno-Oncology Biomarker Working Group on breast cancer. Semin Cancer Biol. https://doi.org/10.1016/j.semcancer.2017.10.003 CrossRefPubMed Dieci MV, Radosevic-Robin N, Fineberg S, van den Eynden G, Ternes N, Penault-Llorca F, Pruneri G, D’Alfonso TM, Demaria S, Castaneda C, Sanchez J, Badve S, Michiels S, Bossuyt V, Rojo F, Singh B, Nielsen T, Viale G, Kim SR, Hewitt S, Wienert S, Loibl S, Rimm D, Symmans F, Denkert C, Adams S, Loi S, Salgado R (2017) Update on tumor-infiltrating lymphocytes (TILs) in breast cancer, including recommendations to assess TILs in residual disease after neoadjuvant therapy and in carcinoma in situ: a report of the International Immuno-Oncology Biomarker Working Group on breast cancer. Semin Cancer Biol. https://​doi.​org/​10.​1016/​j.​semcancer.​2017.​10.​003 CrossRefPubMed
Metadata
Title
Prognostic role of immune infiltrates in breast ductal carcinoma in situ
Authors
Xiao-Yang Chen
Joe Yeong
Aye Aye Thike
Boon Huat Bay
Puay Hoon Tan
Publication date
01-08-2019
Publisher
Springer US
Keyword
Biomarkers
Published in
Breast Cancer Research and Treatment / Issue 1/2019
Print ISSN: 0167-6806
Electronic ISSN: 1573-7217
DOI
https://doi.org/10.1007/s10549-019-05272-2

Other articles of this Issue 1/2019

Breast Cancer Research and Treatment 1/2019 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine