Skip to main content
Erschienen in: Cancer Immunology, Immunotherapy 6/2013

01.06.2013 | Original Article

Elevated level of peripheral CD8+CD28 T lymphocytes are an independent predictor of progression-free survival in patients with metastatic breast cancer during the course of chemotherapy

verfasst von: Guohong Song, Xiaoli Wang, Jun Jia, Yanhua Yuan, Fengling Wan, Xinna Zhou, Huabing Yang, Jun Ren, Jiezhun Gu, Herbert Kim Lyerly

Erschienen in: Cancer Immunology, Immunotherapy | Ausgabe 6/2013

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Suppression of cellular immunity resulting from tumorigenesis and/or therapy might promote cancer cells’ growth, progression and invasion. Here, we explored whether T lymphocyte subtypes from peripheral blood of metastatic breast cancer (MBC) female patients could be used as alternative surrogate markers for cancer progress. Additionally, plasma levels of interleukin (IL)-2, IL-4, IL-6, IL-10, IFN-γ, and transforming growth factor-β1 were quantitated from MBC and healthy volunteers.

Experimental design

This study included 89 female MBC patients during the post-salvage chemotherapy follow-up and 50 age- and sex-matched healthy volunteers as control. The percentages of T lymphocyte subpopulations from peripheral blood and plasma levels of cytokines were measured.

Results

Both CD8+CD28 and CD4+CD25+ were elevated in MBC patients compared to the control cohort (P < 0.05). In contrast, CD3+ and CD8+CD28+cells were significantly lower in MBC patients (P < 0.0001, P = 0.045, respectively). MBC patients had elevated levels of immunosuppressive cytokines IL-6 and IL-10. Patients with elevated CD8+CD28 and CD4+CD25+ cells showed increased levels of IL-6, and only patients with elevated CD8+CD28 had decreased interferon-γ. Univariate analysis indicated increased CD3+CD4+ or CD8+CD28+correlated with prolonged progression-free survival (PFS), while elevated CD8+CD28associated with shorten PFS. The percent of CD8+CD28 T lymphocytes is an independent predictor for PFS through multivariate analysis.

Conclusions

This study suggests that progressive elevated levels of CD8+CD28 suppressor T lymphocytes represent a novel independent predictor of PFS during post-chemotherapy follow-up.
Literatur
1.
Zurück zum Zitat Marr LA, Gilham DE, Campbell JD, Fraser AR (2012) Immunology in the clinic review series; focus on cancer: double trouble for tumours: bi-functional and redirected T cells as effective cancer immunotherapies. Clin Exp Immunol 167(2):216–225PubMedCrossRef Marr LA, Gilham DE, Campbell JD, Fraser AR (2012) Immunology in the clinic review series; focus on cancer: double trouble for tumours: bi-functional and redirected T cells as effective cancer immunotherapies. Clin Exp Immunol 167(2):216–225PubMedCrossRef
2.
Zurück zum Zitat Chow MT, Möller A, Smyth MJ (2012) Inflammation and immune surveillance in cancer. Semin Cancer Biol 22(1):23–32PubMedCrossRef Chow MT, Möller A, Smyth MJ (2012) Inflammation and immune surveillance in cancer. Semin Cancer Biol 22(1):23–32PubMedCrossRef
3.
Zurück zum Zitat Shiao SL, Ganesan AP, Rugo HS, Coussens LM (2011) Immune microenvironments in solid tumors: new targets for therapy. Genes Dev 25(24):2559–2572PubMedCrossRef Shiao SL, Ganesan AP, Rugo HS, Coussens LM (2011) Immune microenvironments in solid tumors: new targets for therapy. Genes Dev 25(24):2559–2572PubMedCrossRef
4.
Zurück zum Zitat Leber MF, Efferth T (2009) Molecular principles of cancer invasion and metastasis. Int J Oncol 34(4):881–895PubMed Leber MF, Efferth T (2009) Molecular principles of cancer invasion and metastasis. Int J Oncol 34(4):881–895PubMed
5.
Zurück zum Zitat Miller FR (1993) Immune mechanisms in the sequential steps of metastasis. Crit Rev Oncog 4(3):293–311PubMed Miller FR (1993) Immune mechanisms in the sequential steps of metastasis. Crit Rev Oncog 4(3):293–311PubMed
6.
Zurück zum Zitat Solomayer EF, Feuerer M, Bai L, Umansky V, Beckhove P, Meyberg GC, Bastert G, Schirrmacher V, Diel IJ (2003) Influence of adjuvant hormone therapy and chemotherapy on the immune system analyzed in the bone marrow of patients with breast cancer. Clin Cancer Res 9(1):174–180PubMed Solomayer EF, Feuerer M, Bai L, Umansky V, Beckhove P, Meyberg GC, Bastert G, Schirrmacher V, Diel IJ (2003) Influence of adjuvant hormone therapy and chemotherapy on the immune system analyzed in the bone marrow of patients with breast cancer. Clin Cancer Res 9(1):174–180PubMed
7.
Zurück zum Zitat Ceschia T, Beorchia A, Guglielmi R, Mandoliti G, Fongione S, Cereghini M, Tonutti E, Sala PG, Pizzi G (1991) Influence of radiotherapy on lymphocyte subpopulations. Radiol Med 81(4):532–536PubMed Ceschia T, Beorchia A, Guglielmi R, Mandoliti G, Fongione S, Cereghini M, Tonutti E, Sala PG, Pizzi G (1991) Influence of radiotherapy on lymphocyte subpopulations. Radiol Med 81(4):532–536PubMed
8.
Zurück zum Zitat Zou W (2006) Regulatory T cells, tumor immunity and immunotherapy. Nat Rev Immunol 6(4):295–307PubMedCrossRef Zou W (2006) Regulatory T cells, tumor immunity and immunotherapy. Nat Rev Immunol 6(4):295–307PubMedCrossRef
9.
Zurück zum Zitat Woo EY, Chu CS, Goletz TJ, Schlienger K, Yeh H, Coukos G et al (2001) Regulatory CD4+CD25+ T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res 61(12):4766–4772PubMed Woo EY, Chu CS, Goletz TJ, Schlienger K, Yeh H, Coukos G et al (2001) Regulatory CD4+CD25+ T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res 61(12):4766–4772PubMed
10.
Zurück zum Zitat Ichihara F, Kono K, Takahashi A, Kawaida H, Sugai H, Fujii H (2003) Increased populations of regulatory T cells in peripheral blood and tumor-infiltrating lymphocytes in patients with gastric and esophageal cancers. Clin Cancer Res 9(12):4404–4408PubMed Ichihara F, Kono K, Takahashi A, Kawaida H, Sugai H, Fujii H (2003) Increased populations of regulatory T cells in peripheral blood and tumor-infiltrating lymphocytes in patients with gastric and esophageal cancers. Clin Cancer Res 9(12):4404–4408PubMed
11.
Zurück zum Zitat Gilberto F, Filaci G, Fravega M, Negrini S, Procopio F, Fenoglio D et al (2004) Nonantigen specific CD8+ T suppressor lymphocytes originate from CD8+CD28− T cells and inhibit both T-cell proliferation and CTL function. Hum Immunol 65(2):142–156CrossRef Gilberto F, Filaci G, Fravega M, Negrini S, Procopio F, Fenoglio D et al (2004) Nonantigen specific CD8+ T suppressor lymphocytes originate from CD8+CD28 T cells and inhibit both T-cell proliferation and CTL function. Hum Immunol 65(2):142–156CrossRef
12.
Zurück zum Zitat Leong PP, Mohammad R, Ibrahim N, Ithnin H, Abdullah M, Davis WC et al (2006) Phenotyping of lymphocytes expressing regulatory and effector markers in infiltrating ductal carcinoma of the breast. Immunol Lett 102(2):229–236PubMedCrossRef Leong PP, Mohammad R, Ibrahim N, Ithnin H, Abdullah M, Davis WC et al (2006) Phenotyping of lymphocytes expressing regulatory and effector markers in infiltrating ductal carcinoma of the breast. Immunol Lett 102(2):229–236PubMedCrossRef
13.
Zurück zum Zitat Wang RF (2008) CD8 + regulatory T cells, their suppressive mechanisms, and regulation in cancer. Hum Immunol 69(11):811–814PubMedCrossRef Wang RF (2008) CD8 + regulatory T cells, their suppressive mechanisms, and regulation in cancer. Hum Immunol 69(11):811–814PubMedCrossRef
14.
Zurück zum Zitat Aandahl EM, Torgersen KM, Taskén K (2008) CD8+ regulatory T cells-A distinct T-cell lineage or a transient T-cell phenotype? Hum Immunol 69(11):696–699PubMedCrossRef Aandahl EM, Torgersen KM, Taskén K (2008) CD8+ regulatory T cells-A distinct T-cell lineage or a transient T-cell phenotype? Hum Immunol 69(11):696–699PubMedCrossRef
15.
Zurück zum Zitat Filaci G, Fenoglio D, Fravega M, Ansaldo G, Borgonovo G, Traverso P et al (2007) CD8+CD28− T regulatory lymphocytes inhibiting T cell proliferative and cytotoxic functions infiltrate human cancers. J Immunol 179(7):4323–4334PubMed Filaci G, Fenoglio D, Fravega M, Ansaldo G, Borgonovo G, Traverso P et al (2007) CD8+CD28 T regulatory lymphocytes inhibiting T cell proliferative and cytotoxic functions infiltrate human cancers. J Immunol 179(7):4323–4334PubMed
16.
Zurück zum Zitat Melichar B, Tousková M, Solichová D, Králicková P, Kopecký G (2001) CD4 + T-lymphocytopenia and systemic immune activation in patients with primary and secondary liver tumours. Scand J Clin Lab Invest 61(5):363–370PubMedCrossRef Melichar B, Tousková M, Solichová D, Králicková P, Kopecký G (2001) CD4 + T-lymphocytopenia and systemic immune activation in patients with primary and secondary liver tumours. Scand J Clin Lab Invest 61(5):363–370PubMedCrossRef
17.
Zurück zum Zitat Lissoni P, Brivio F, Ferrante R, Vigore L, Vaghi M, Fumagalli E et al (2000) Circulating immature and mature dendritic cells in relation to lymphocyte subsets in patients with gastrointestinal tract cancer. Int J Biol Markers 15(1):22–25PubMed Lissoni P, Brivio F, Ferrante R, Vigore L, Vaghi M, Fumagalli E et al (2000) Circulating immature and mature dendritic cells in relation to lymphocyte subsets in patients with gastrointestinal tract cancer. Int J Biol Markers 15(1):22–25PubMed
18.
Zurück zum Zitat Melichar B, Jandik P, Krejsek J, Solichova D, Drahosova M, Skopec F et al (1996) Mitogen-induced lymphocyte proliferation and systemic immune activation in cancer patients. Tumori 82(3):218–220PubMed Melichar B, Jandik P, Krejsek J, Solichova D, Drahosova M, Skopec F et al (1996) Mitogen-induced lymphocyte proliferation and systemic immune activation in cancer patients. Tumori 82(3):218–220PubMed
19.
Zurück zum Zitat Okita R, Saeki T, Takashima S, Yamaguchi Y, Toge T (2005) CD4 + CD25 + regulatory T cells in the peripheral blood of patients with breast cancer and non-small cell lung cancer. Oncol Rep 14(5):1269–1273PubMed Okita R, Saeki T, Takashima S, Yamaguchi Y, Toge T (2005) CD4 + CD25 + regulatory T cells in the peripheral blood of patients with breast cancer and non-small cell lung cancer. Oncol Rep 14(5):1269–1273PubMed
20.
Zurück zum Zitat Meloni F, Morosini M, Solari N, Passadore I, Nascimbene C, Novo M et al (2006) Foxp3 Expressing CD4 + CD25 + and CD8 + CD28 − T Regulatory Cells in the Peripheral Blood of Patients with Lung Cancer and Pleural Mesothelioma. Hum Immunol 67(1–2):1–12PubMedCrossRef Meloni F, Morosini M, Solari N, Passadore I, Nascimbene C, Novo M et al (2006) Foxp3 Expressing CD4 + CD25 + and CD8 + CD28 − T Regulatory Cells in the Peripheral Blood of Patients with Lung Cancer and Pleural Mesothelioma. Hum Immunol 67(1–2):1–12PubMedCrossRef
21.
Zurück zum Zitat Fu J, Xu D, Liu Z, Shi M, Zhao P, Fu B et al (2007) Increased regulatory T cells correlate with CD8 T-cell impairment and poor survival in hepatocellular carcinoma patients. Gastroenterology 132(7):2328–2339PubMedCrossRef Fu J, Xu D, Liu Z, Shi M, Zhao P, Fu B et al (2007) Increased regulatory T cells correlate with CD8 T-cell impairment and poor survival in hepatocellular carcinoma patients. Gastroenterology 132(7):2328–2339PubMedCrossRef
22.
Zurück zum Zitat Holcombe RF, Jacobson J, Dakhil SR, Stewart RM, Betzing KS, Kannan K et al (1999) Association of immune parameters with clinical outcome in stage III colon cancer: results of Southwest Oncology Group Protocol 9009. Cancer Immunol Immunother 48(9):533–539PubMedCrossRef Holcombe RF, Jacobson J, Dakhil SR, Stewart RM, Betzing KS, Kannan K et al (1999) Association of immune parameters with clinical outcome in stage III colon cancer: results of Southwest Oncology Group Protocol 9009. Cancer Immunol Immunother 48(9):533–539PubMedCrossRef
23.
Zurück zum Zitat Zaloudik J, Lauerova L, Janakova L, Talac R, Simickova M, Nekulova M et al (1999) Significance of pre-treatment immunological parameters in colorectal cancer patients with unresectable metastases to the liver. Hepatogastroenterology 46(25):220–227PubMed Zaloudik J, Lauerova L, Janakova L, Talac R, Simickova M, Nekulova M et al (1999) Significance of pre-treatment immunological parameters in colorectal cancer patients with unresectable metastases to the liver. Hepatogastroenterology 46(25):220–227PubMed
24.
Zurück zum Zitat Vesely P, Tousková M, Melichar B (2005) Phenotype of peripheral blood leukocytes and survival of patients with metastatic colorectal cancer. Int J Biol Markers 20(2):126–133PubMed Vesely P, Tousková M, Melichar B (2005) Phenotype of peripheral blood leukocytes and survival of patients with metastatic colorectal cancer. Int J Biol Markers 20(2):126–133PubMed
25.
Zurück zum Zitat Liu F, Lang R, Zhao J, Zhang X, Pringle GA, Fan Y et al (2011) CD8+ cytotoxic T cell and FOXP3+ regulatory T cell infiltration in relation to breast cancer survival and molecular subtypes. Breast Cancer Res Treat 130(2):645–655PubMedCrossRef Liu F, Lang R, Zhao J, Zhang X, Pringle GA, Fan Y et al (2011) CD8+ cytotoxic T cell and FOXP3+ regulatory T cell infiltration in relation to breast cancer survival and molecular subtypes. Breast Cancer Res Treat 130(2):645–655PubMedCrossRef
26.
Zurück zum Zitat Tiwari M (2010) From tumor immunology to cancer immunotherapy: miles to go. J Cancer Res Ther 6(4):427–431PubMedCrossRef Tiwari M (2010) From tumor immunology to cancer immunotherapy: miles to go. J Cancer Res Ther 6(4):427–431PubMedCrossRef
28.
Zurück zum Zitat Kim R, Emi M, Tanabe K, Arihiro K (2006) Tumor-driven evolution of immunosuppressive networks during malignant progression. Cancer Res 66(11):5527–5536PubMedCrossRef Kim R, Emi M, Tanabe K, Arihiro K (2006) Tumor-driven evolution of immunosuppressive networks during malignant progression. Cancer Res 66(11):5527–5536PubMedCrossRef
29.
Zurück zum Zitat Suzuki K, KadotaK Sima CS, Nitadori J, Rusch VW, Travis WD et al (2013) Clinical impact of immune microenvironment in stage I lung adenocarcinoma: tumor interleukin-12 receptor β2(IL-12Rβ2), IL-7R, and stromal FoxP3/CD3 ratio are independent predictors of recurrence. J Clin Oncol 31(4):490–498PubMedCrossRef Suzuki K, KadotaK Sima CS, Nitadori J, Rusch VW, Travis WD et al (2013) Clinical impact of immune microenvironment in stage I lung adenocarcinoma: tumor interleukin-12 receptor β2(IL-12Rβ2), IL-7R, and stromal FoxP3/CD3 ratio are independent predictors of recurrence. J Clin Oncol 31(4):490–498PubMedCrossRef
30.
Zurück zum Zitat Saison J, Demaret J, Venet F, Chidiac C, Malcus C, Poitevin-Later F et al (2013) CD4+CD25+CD127- assessment as a surrogate phenotype for FOXP3+ regulatory T cells in HIV-1 infected viremic and aviremic subjects. Cytometry B Clin Cytom 84(1):50–54PubMed Saison J, Demaret J, Venet F, Chidiac C, Malcus C, Poitevin-Later F et al (2013) CD4+CD25+CD127- assessment as a surrogate phenotype for FOXP3+ regulatory T cells in HIV-1 infected viremic and aviremic subjects. Cytometry B Clin Cytom 84(1):50–54PubMed
31.
32.
Zurück zum Zitat Watanabe MA, Oda JM, Amarante MK, Cesar Voltarelli J (2010) Regulatory T cells and breast cancer: implications for immunopathogenesis. Cancer Metastasis Rev 29(4):569–579PubMedCrossRef Watanabe MA, Oda JM, Amarante MK, Cesar Voltarelli J (2010) Regulatory T cells and breast cancer: implications for immunopathogenesis. Cancer Metastasis Rev 29(4):569–579PubMedCrossRef
33.
Zurück zum Zitat Sakaguchi S (2005) Naturally arising Foxp3-expressing CD25 + CD4 + regulatory T cells in immunological tolerance to self and nonself. Nat Immunol 6(4):345–352PubMedCrossRef Sakaguchi S (2005) Naturally arising Foxp3-expressing CD25 + CD4 + regulatory T cells in immunological tolerance to self and nonself. Nat Immunol 6(4):345–352PubMedCrossRef
34.
Zurück zum Zitat Shevach EM (2002) CD4 + CD25 + suppressor T cells: more questions than answers. Nat Rev Immunol 2(6):389–400PubMed Shevach EM (2002) CD4 + CD25 + suppressor T cells: more questions than answers. Nat Rev Immunol 2(6):389–400PubMed
35.
Zurück zum Zitat Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N et al (2003) Conversion of peripheral CD4 + CD25– naive T cells to CD4 + CD25 + regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 198(12):1875–1886PubMedCrossRef Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N et al (2003) Conversion of peripheral CD4 + CD25– naive T cells to CD4 + CD25 + regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 198(12):1875–1886PubMedCrossRef
36.
Zurück zum Zitat Liyanage UK, Moore TT, Joo HG, Tanaka Y, Herrmann V, Doherty G et al (2002) Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J Immunol 169(5):2756–2761PubMed Liyanage UK, Moore TT, Joo HG, Tanaka Y, Herrmann V, Doherty G et al (2002) Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J Immunol 169(5):2756–2761PubMed
37.
Zurück zum Zitat Sasada T, Kimura M, Yoshida Y, Kanai M, Takabayashi A (2003) CD4 + CD25 + regulatory T cells in patients with gastrointestinal malignancies: possible involvement of regulatory T cells in disease progression. Cancer 98(5):1089–1099PubMedCrossRef Sasada T, Kimura M, Yoshida Y, Kanai M, Takabayashi A (2003) CD4 + CD25 + regulatory T cells in patients with gastrointestinal malignancies: possible involvement of regulatory T cells in disease progression. Cancer 98(5):1089–1099PubMedCrossRef
38.
Zurück zum Zitat Javia LR, Rosenberg SA (2003) CD4 + CD25 + suppressor lymphocytes in the circulation of patients immunized against melanoma antigens. J Immunother 26(1):85–93PubMedCrossRef Javia LR, Rosenberg SA (2003) CD4 + CD25 + suppressor lymphocytes in the circulation of patients immunized against melanoma antigens. J Immunother 26(1):85–93PubMedCrossRef
39.
Zurück zum Zitat Somasundaram R, Jacob L, Swoboda R, Caputo L, Song H, Basak S et al (2002) Inhibition of cytolytic T lymphocyte proliferation by autologous CD4 + CD25 + regulatory T cells in a colorectal carcinoma patient is mediated by transforming growth factor. Cancer Res 62(18):5267–5272PubMed Somasundaram R, Jacob L, Swoboda R, Caputo L, Song H, Basak S et al (2002) Inhibition of cytolytic T lymphocyte proliferation by autologous CD4 + CD25 + regulatory T cells in a colorectal carcinoma patient is mediated by transforming growth factor. Cancer Res 62(18):5267–5272PubMed
40.
Zurück zum Zitat Kim R, Emi M, Tanabe K (2006) Cancer immunosuppression and autoimmune disease: beyond immunosuppressive networks for tumour immunity. Immunology 119(2):254–264PubMedCrossRef Kim R, Emi M, Tanabe K (2006) Cancer immunosuppression and autoimmune disease: beyond immunosuppressive networks for tumour immunity. Immunology 119(2):254–264PubMedCrossRef
41.
Zurück zum Zitat Qiu YR, Yang CL, Chen LB, Wang Q (2002) Analysis of CD8(+) and CD8(+)CD28(−) cell subsets in patients with hepatocellular carcinoma. Di Yi Jun Yi Da Xue Xue Bao 22(1):72–73PubMed Qiu YR, Yang CL, Chen LB, Wang Q (2002) Analysis of CD8(+) and CD8(+)CD28(−) cell subsets in patients with hepatocellular carcinoma. Di Yi Jun Yi Da Xue Xue Bao 22(1):72–73PubMed
42.
Zurück zum Zitat Tsukishiro T, Donnenberg AD, Whiteside TL (2003) Rapid turnover of the CD8(+)CD28(−) T-cell subset of effector cells in the circulation of patients with head and neck cancer. Cancer Immunol Immunother 52(10):599–607PubMedCrossRef Tsukishiro T, Donnenberg AD, Whiteside TL (2003) Rapid turnover of the CD8(+)CD28(−) T-cell subset of effector cells in the circulation of patients with head and neck cancer. Cancer Immunol Immunother 52(10):599–607PubMedCrossRef
43.
Zurück zum Zitat Strioga M, Pasukoniene V, Characiejus D (2011) CD8 + CD28- and CD8 + CD57 + Tcells and their role in health and disease. Immunology 134(1):17–32PubMedCrossRef Strioga M, Pasukoniene V, Characiejus D (2011) CD8 + CD28- and CD8 + CD57 + Tcells and their role in health and disease. Immunology 134(1):17–32PubMedCrossRef
44.
Zurück zum Zitat Pagès F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R et al (2005) Effector memory T cells, early metastasis, and survival in colorectal cancer. N Eng J Med 353(25):2654–2666CrossRef Pagès F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R et al (2005) Effector memory T cells, early metastasis, and survival in colorectal cancer. N Eng J Med 353(25):2654–2666CrossRef
45.
Zurück zum Zitat Karagöz B, Bilgi O, Gümüs M, Erikçi AA, Sayan O, Türken O et al (2010) CD8 + CD28- cells and CD4 + CD25 + regulatory T cells in the peripheral blood of advanced stage lung cancer patients. Med Oncol 27(1):29–33PubMedCrossRef Karagöz B, Bilgi O, Gümüs M, Erikçi AA, Sayan O, Türken O et al (2010) CD8 + CD28- cells and CD4 + CD25 + regulatory T cells in the peripheral blood of advanced stage lung cancer patients. Med Oncol 27(1):29–33PubMedCrossRef
46.
Zurück zum Zitat DeBenedette MA, Calderhead DM, Tcherepanova IY, Nicolette CA, Healey DG (2011) Potency of mature CD40L RNA electroporated dendritic cells correlates with IL-12 secretion by tracking multifunctional CD8(+)/CD28(+) cytotoxic T-cell responses in vitro. J Immunother 34(1):45–57PubMedCrossRef DeBenedette MA, Calderhead DM, Tcherepanova IY, Nicolette CA, Healey DG (2011) Potency of mature CD40L RNA electroporated dendritic cells correlates with IL-12 secretion by tracking multifunctional CD8(+)/CD28(+) cytotoxic T-cell responses in vitro. J Immunother 34(1):45–57PubMedCrossRef
Metadaten
Titel
Elevated level of peripheral CD8+CD28− T lymphocytes are an independent predictor of progression-free survival in patients with metastatic breast cancer during the course of chemotherapy
verfasst von
Guohong Song
Xiaoli Wang
Jun Jia
Yanhua Yuan
Fengling Wan
Xinna Zhou
Huabing Yang
Jun Ren
Jiezhun Gu
Herbert Kim Lyerly
Publikationsdatum
01.06.2013
Verlag
Springer-Verlag
Erschienen in
Cancer Immunology, Immunotherapy / Ausgabe 6/2013
Print ISSN: 0340-7004
Elektronische ISSN: 1432-0851
DOI
https://doi.org/10.1007/s00262-013-1424-8

Weitere Artikel der Ausgabe 6/2013

Cancer Immunology, Immunotherapy 6/2013 Zur Ausgabe

Update Onkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.