Skip to main content
Top
Published in: Cancer Immunology, Immunotherapy 9/2015

01-09-2015 | Original Article

Increased CCL17 serum levels are associated with improved survival in advanced melanoma

Authors: Benjamin Weide, Nicolas Allgaier, Andreas Hector, Andrea Forschner, Ulrike Leiter, Thomas K. Eigentler, Claus Garbe, Dominik Hartl

Published in: Cancer Immunology, Immunotherapy | Issue 9/2015

Login to get access

Abstract

Background

Prognostic factors of melanoma patients with distant metastases remain poorly established. This study aimed to compare the prognostic impact of putative serum biomarkers, namely S100B, YKL-40 or CCL17, in stage IV melanoma patients.

Patients and methods

Serum concentrations were analyzed by ELISA. Disease-specific survival of 80 patients according to S100B, YKL-40 or CCL17 and clinical factors were calculated by univariate Kaplan–Meier survival and multivariate analysis.

Results

Low serum levels of S100B, high concentrations of CCL17 and female gender correlated with improved survival. A trend for favorable prognosis was observed for the M categories M1a/b versus M1c according to the AJCC classification. No correlation with survival was evident for YKL-40 serum levels and age. In multivariate analysis, S100B (HR 2.1; p = 0.005) and CCL17 (HR 1.8; p = 0.029) had independent prognostic impact. Patients with a combination of normal S100B and high CCL17 had a high chance for long-term survival, which was 43 % after 3 years.

Conclusion

Serum levels of CCL17 and S100B represent independent prognostic markers for melanoma patients with distant metastases. These biomarkers were more powerful than the M category according to the AJCC classification to indicate overall survival. CCL17 represents a promising biomarker upon immune checkpoint blockade in melanoma.
Literature
1.
go back to reference Balch CM, Buzaid AC, Soong SJ, Atkins MB, Cascinelli N, Coit DG, Fleming ID, Gershenwald JE, Houghton A Jr, Kirkwood JM, McMasters KM, Mihm MF, Morton DL, Reintgen DS, Ross MI, Sober A, Thompson JA, Thompson JF (2001) Final version of the American Joint Committee on Cancer staging system for cutaneous melanoma. J Clin Oncol 19(16):3635–3648PubMed Balch CM, Buzaid AC, Soong SJ, Atkins MB, Cascinelli N, Coit DG, Fleming ID, Gershenwald JE, Houghton A Jr, Kirkwood JM, McMasters KM, Mihm MF, Morton DL, Reintgen DS, Ross MI, Sober A, Thompson JA, Thompson JF (2001) Final version of the American Joint Committee on Cancer staging system for cutaneous melanoma. J Clin Oncol 19(16):3635–3648PubMed
2.
go back to reference Sirott MN, Bajorin DF, Wong GY, Tao Y, Chapman PB, Templeton MA, Houghton AN (1993) Prognostic factors in patients with metastatic malignant melanoma. A multivariate analysis. Cancer 72(10):3091–3098CrossRefPubMed Sirott MN, Bajorin DF, Wong GY, Tao Y, Chapman PB, Templeton MA, Houghton AN (1993) Prognostic factors in patients with metastatic malignant melanoma. A multivariate analysis. Cancer 72(10):3091–3098CrossRefPubMed
3.
go back to reference Eton O, Legha SS, Moon TE, Buzaid AC, Papadopoulos NE, Plager C, Burgess AM, Bedikian AY, Ring S, Dong Q, Glassman AB, Balch CM, Benjamin RS (1998) Prognostic factors for survival of patients treated systemically for disseminated melanoma. J Clin Oncol 16(3):1103–1111PubMed Eton O, Legha SS, Moon TE, Buzaid AC, Papadopoulos NE, Plager C, Burgess AM, Bedikian AY, Ring S, Dong Q, Glassman AB, Balch CM, Benjamin RS (1998) Prognostic factors for survival of patients treated systemically for disseminated melanoma. J Clin Oncol 16(3):1103–1111PubMed
4.
go back to reference Manola J, Atkins M, Ibrahim J, Kirkwood J (2000) Prognostic factors in metastatic melanoma: a pooled analysis of Eastern Cooperative Oncology Group trials. J Clin Oncol 18(22):3782–3793PubMed Manola J, Atkins M, Ibrahim J, Kirkwood J (2000) Prognostic factors in metastatic melanoma: a pooled analysis of Eastern Cooperative Oncology Group trials. J Clin Oncol 18(22):3782–3793PubMed
5.
go back to reference Pflugfelder A, Kochs C, Blum A, Capellaro M, Czeschik C, Dettenborn T, Dill D, Dippel E, Eigentler T, Feyer P, Follmann M, Frerich B, Ganten MK, Gartner J, Gutzmer R, Hassel J, Hauschild A, Hohenberger P, Hubner J, Kaatz M, Kleeberg UR, Kolbl O, Kortmann RD, Krause-Bergmann A, Kurschat P, Leiter U, Link H, Loquai C, Loser C, Mackensen A, Meier F, Mohr P, Mohrle M, Nashan D, Reske S, Rose C, Sander C, Satzger I, Schiller M, Schlemmer HP, Strittmatter G, Sunderkotter C, Swoboda L, Trefzer U, Voltz R, Vordermark D, Weichenthal M, Werner A, Wesselmann S, Weyergraf AJ, Wick W, Garbe C, Schadendorf D (2013) Malignant melanoma S3-guideline “diagnosis, therapy and follow-up of melanoma”. J Dtsch Dermatol Ges 11 (Suppl 6):1–116, 111–126. doi:10.1111/ddg.12113_suppl Pflugfelder A, Kochs C, Blum A, Capellaro M, Czeschik C, Dettenborn T, Dill D, Dippel E, Eigentler T, Feyer P, Follmann M, Frerich B, Ganten MK, Gartner J, Gutzmer R, Hassel J, Hauschild A, Hohenberger P, Hubner J, Kaatz M, Kleeberg UR, Kolbl O, Kortmann RD, Krause-Bergmann A, Kurschat P, Leiter U, Link H, Loquai C, Loser C, Mackensen A, Meier F, Mohr P, Mohrle M, Nashan D, Reske S, Rose C, Sander C, Satzger I, Schiller M, Schlemmer HP, Strittmatter G, Sunderkotter C, Swoboda L, Trefzer U, Voltz R, Vordermark D, Weichenthal M, Werner A, Wesselmann S, Weyergraf AJ, Wick W, Garbe C, Schadendorf D (2013) Malignant melanoma S3-guideline “diagnosis, therapy and follow-up of melanoma”. J Dtsch Dermatol Ges 11 (Suppl 6):1–116, 111–126. doi:10.​1111/​ddg.​12113_​suppl
7.
8.
go back to reference Weide B, Elsasser M, Buttner P, Pflugfelder A, Leiter U, Eigentler TK, Bauer J, Witte M, Meier F, Garbe C (2012) Serum markers lactate dehydrogenase and S100B predict independently disease outcome in melanoma patients with distant metastasis. Br J Cancer 107(3):422–428. doi:10.1038/bjc.2012.306 PubMedCentralCrossRefPubMed Weide B, Elsasser M, Buttner P, Pflugfelder A, Leiter U, Eigentler TK, Bauer J, Witte M, Meier F, Garbe C (2012) Serum markers lactate dehydrogenase and S100B predict independently disease outcome in melanoma patients with distant metastasis. Br J Cancer 107(3):422–428. doi:10.​1038/​bjc.​2012.​306 PubMedCentralCrossRefPubMed
9.
go back to reference Real E, Kaiser A, Raposo G, Amara A, Nardin A, Trautmann A, Donnadieu E (2004) Immature dendritic cells (DCs) use chemokines and intercellular adhesion molecule (ICAM)-1, but not DC-specific ICAM-3-grabbing nonintegrin, to stimulate CD4+ T cells in the absence of exogenous antigen. J Immunol 173(1):50–60CrossRefPubMed Real E, Kaiser A, Raposo G, Amara A, Nardin A, Trautmann A, Donnadieu E (2004) Immature dendritic cells (DCs) use chemokines and intercellular adhesion molecule (ICAM)-1, but not DC-specific ICAM-3-grabbing nonintegrin, to stimulate CD4+ T cells in the absence of exogenous antigen. J Immunol 173(1):50–60CrossRefPubMed
10.
go back to reference Semmling V, Lukacs-Kornek V, Thaiss CA, Quast T, Hochheiser K, Panzer U, Rossjohn J, Perlmutter P, Cao J, Godfrey DI, Savage PB, Knolle PA, Kolanus W, Forster I, Kurts C (2010) Alternative cross-priming through CCL17-CCR4-mediated attraction of CTLs toward NKT cell-licensed DCs. Nat Immunol 11(4):313–320CrossRefPubMed Semmling V, Lukacs-Kornek V, Thaiss CA, Quast T, Hochheiser K, Panzer U, Rossjohn J, Perlmutter P, Cao J, Godfrey DI, Savage PB, Knolle PA, Kolanus W, Forster I, Kurts C (2010) Alternative cross-priming through CCL17-CCR4-mediated attraction of CTLs toward NKT cell-licensed DCs. Nat Immunol 11(4):313–320CrossRefPubMed
11.
go back to reference Walter S, Weinschenk T, Stenzl A, Zdrojowy R, Pluzanska A, Szczylik C, Staehler M, Brugger W, Dietrich PY, Mendrzyk R, Hilf N, Schoor O, Fritsche J, Mahr A, Maurer D, Vass V, Trautwein C, Lewandrowski P, Flohr C, Pohla H, Stanczak JJ, Bronte V, Mandruzzato S, Biedermann T, Pawelec G, Derhovanessian E, Yamagishi H, Miki T, Hongo F, Takaha N, Hirakawa K, Tanaka H, Stevanovic S, Frisch J, Mayer-Mokler A, Kirner A, Rammensee HG, Reinhardt C, Singh-Jasuja H (2012) Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival. Nat Med 18(8):1254–1261. doi:10.1038/nm.2883 CrossRefPubMed Walter S, Weinschenk T, Stenzl A, Zdrojowy R, Pluzanska A, Szczylik C, Staehler M, Brugger W, Dietrich PY, Mendrzyk R, Hilf N, Schoor O, Fritsche J, Mahr A, Maurer D, Vass V, Trautwein C, Lewandrowski P, Flohr C, Pohla H, Stanczak JJ, Bronte V, Mandruzzato S, Biedermann T, Pawelec G, Derhovanessian E, Yamagishi H, Miki T, Hongo F, Takaha N, Hirakawa K, Tanaka H, Stevanovic S, Frisch J, Mayer-Mokler A, Kirner A, Rammensee HG, Reinhardt C, Singh-Jasuja H (2012) Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival. Nat Med 18(8):1254–1261. doi:10.​1038/​nm.​2883 CrossRefPubMed
12.
go back to reference Cornforth AN, Lee GJ, Fowler AW, Carbonell DJ, Dillman RO (2009) Increases in serum TARC/CCL17 levels are associated with progression-free survival in advanced melanoma patients in response to dendritic cell-based immunotherapy. J Clin Immunol 29(5):657–664. doi:10.1007/s10875-009-9299-3 CrossRefPubMed Cornforth AN, Lee GJ, Fowler AW, Carbonell DJ, Dillman RO (2009) Increases in serum TARC/CCL17 levels are associated with progression-free survival in advanced melanoma patients in response to dendritic cell-based immunotherapy. J Clin Immunol 29(5):657–664. doi:10.​1007/​s10875-009-9299-3 CrossRefPubMed
13.
go back to reference Schmidt H, Johansen JS, Gehl J, Geertsen PF, Fode K, von der Maase H (2006) Elevated serum level of YKL-40 is an independent prognostic factor for poor survival in patients with metastatic melanoma. Cancer 106(5):1130–1139CrossRefPubMed Schmidt H, Johansen JS, Gehl J, Geertsen PF, Fode K, von der Maase H (2006) Elevated serum level of YKL-40 is an independent prognostic factor for poor survival in patients with metastatic melanoma. Cancer 106(5):1130–1139CrossRefPubMed
14.
go back to reference Egberts F, Kotthoff EM, Gerdes S, Egberts JH, Weichenthal M, Hauschild A (2012) Comparative study of YKL-40, S-100B and LDH as monitoring tools for stage IV melanoma. Eur J Cancer 48(5):695–702CrossRefPubMed Egberts F, Kotthoff EM, Gerdes S, Egberts JH, Weichenthal M, Hauschild A (2012) Comparative study of YKL-40, S-100B and LDH as monitoring tools for stage IV melanoma. Eur J Cancer 48(5):695–702CrossRefPubMed
15.
go back to reference Lasithiotakis KG, Leiter U, Gorkievicz R, Eigentler T, Breuninger H, Metzler G, Strobel W, Garbe C (2006) The incidence and mortality of cutaneous melanoma in Southern Germany: trends by anatomic site and pathologic characteristics, 1976 to 2003. Cancer 107(6):1331–1339CrossRefPubMed Lasithiotakis KG, Leiter U, Gorkievicz R, Eigentler T, Breuninger H, Metzler G, Strobel W, Garbe C (2006) The incidence and mortality of cutaneous melanoma in Southern Germany: trends by anatomic site and pathologic characteristics, 1976 to 2003. Cancer 107(6):1331–1339CrossRefPubMed
16.
go back to reference Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Atkins MB, Byrd DR, Buzaid AC, Cochran AJ, Coit DG, Ding S, Eggermont AM, Flaherty KT, Gimotty PA, Kirkwood JM, McMasters KM, Mihm MC Jr, Morton DL, Ross MI, Sober AJ, Sondak VK (2009) Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol 27(36):6199–6206. doi:10.1200/JCO.2009.23.4799 PubMedCentralCrossRefPubMed Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Atkins MB, Byrd DR, Buzaid AC, Cochran AJ, Coit DG, Ding S, Eggermont AM, Flaherty KT, Gimotty PA, Kirkwood JM, McMasters KM, Mihm MC Jr, Morton DL, Ross MI, Sober AJ, Sondak VK (2009) Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol 27(36):6199–6206. doi:10.​1200/​JCO.​2009.​23.​4799 PubMedCentralCrossRefPubMed
17.
go back to reference Volck B, Price PA, Johansen JS, Sorensen O, Benfield TL, Nielsen HJ, Calafat J, Borregaard N (1998) YKL-40, a mammalian member of the chitinase family, is a matrix protein of specific granules in human neutrophils. Proc Assoc Am Physicians 110(4):351–360PubMed Volck B, Price PA, Johansen JS, Sorensen O, Benfield TL, Nielsen HJ, Calafat J, Borregaard N (1998) YKL-40, a mammalian member of the chitinase family, is a matrix protein of specific granules in human neutrophils. Proc Assoc Am Physicians 110(4):351–360PubMed
18.
go back to reference Lee CG, Hartl D, Lee GR, Koller B, Matsuura H, Da Silva CA, Sohn MH, Cohn L, Homer RJ, Kozhich AA, Humbles A, Kearley J, Coyle A, Chupp G, Reed J, Flavell RA, Elias JA (2009) Role of breast regression protein 39 (BRP-39)/chitinase 3-like-1 in Th2 and IL-13-induced tissue responses and apoptosis. J Exp Med 206(5):1149–1166. doi:10.1084/jem.20081271 PubMedCentralCrossRefPubMed Lee CG, Hartl D, Lee GR, Koller B, Matsuura H, Da Silva CA, Sohn MH, Cohn L, Homer RJ, Kozhich AA, Humbles A, Kearley J, Coyle A, Chupp G, Reed J, Flavell RA, Elias JA (2009) Role of breast regression protein 39 (BRP-39)/chitinase 3-like-1 in Th2 and IL-13-induced tissue responses and apoptosis. J Exp Med 206(5):1149–1166. doi:10.​1084/​jem.​20081271 PubMedCentralCrossRefPubMed
19.
go back to reference Recklies AD, White C, Ling H (2002) The chitinase 3-like protein human cartilage glycoprotein 39 (HC-gp39) stimulates proliferation of human connective-tissue cells and activates both extracellular signal-regulated kinase- and protein kinase B-mediated signalling pathways. Biochem J 365(Pt 1):119–126. doi:10.1042/BJ20020075 PubMedCentralCrossRefPubMed Recklies AD, White C, Ling H (2002) The chitinase 3-like protein human cartilage glycoprotein 39 (HC-gp39) stimulates proliferation of human connective-tissue cells and activates both extracellular signal-regulated kinase- and protein kinase B-mediated signalling pathways. Biochem J 365(Pt 1):119–126. doi:10.​1042/​BJ20020075 PubMedCentralCrossRefPubMed
20.
go back to reference Renkema GH, Boot RG, Au FL, Donker-Koopman WE, Strijland A, Muijsers AO, Hrebicek M, Aerts JM (1998) Chitotriosidase, a chitinase, and the 39-kDa human cartilage glycoprotein, a chitin-binding lectin, are homologues of family 18 glycosyl hydrolases secreted by human macrophages. Eur J Biochem 251(1–2):504–509CrossRefPubMed Renkema GH, Boot RG, Au FL, Donker-Koopman WE, Strijland A, Muijsers AO, Hrebicek M, Aerts JM (1998) Chitotriosidase, a chitinase, and the 39-kDa human cartilage glycoprotein, a chitin-binding lectin, are homologues of family 18 glycosyl hydrolases secreted by human macrophages. Eur J Biochem 251(1–2):504–509CrossRefPubMed
21.
go back to reference Jensen BV, Johansen JS, Price PA (2003) High levels of serum HER-2/neu and YKL-40 independently reflect aggressiveness of metastatic breast cancer. Clin Cancer Res 9(12):4423–4434PubMed Jensen BV, Johansen JS, Price PA (2003) High levels of serum HER-2/neu and YKL-40 independently reflect aggressiveness of metastatic breast cancer. Clin Cancer Res 9(12):4423–4434PubMed
23.
go back to reference Cintin C, Johansen JS, Christensen IJ, Price PA, Sorensen S, Nielsen HJ (2002) High serum YKL-40 level after surgery for colorectal carcinoma is related to short survival. Cancer 95(2):267–274CrossRefPubMed Cintin C, Johansen JS, Christensen IJ, Price PA, Sorensen S, Nielsen HJ (2002) High serum YKL-40 level after surgery for colorectal carcinoma is related to short survival. Cancer 95(2):267–274CrossRefPubMed
24.
go back to reference Schmidt H, Johansen JS, Sjoegren P, Christensen IJ, Sorensen BS, Fode K, Larsen J, von der Maase H (2006) Serum YKL-40 predicts relapse-free and overall survival in patients with American Joint Committee on Cancer stage I and II melanoma. J Clin Oncol 24(5):798–804CrossRefPubMed Schmidt H, Johansen JS, Sjoegren P, Christensen IJ, Sorensen BS, Fode K, Larsen J, von der Maase H (2006) Serum YKL-40 predicts relapse-free and overall survival in patients with American Joint Committee on Cancer stage I and II melanoma. J Clin Oncol 24(5):798–804CrossRefPubMed
26.
go back to reference Egberts F, Pollex A, Egberts JH, Kaehler KC, Weichenthal M, Hauschild A (2008) Long-term survival analysis in metastatic melanoma: serum S100B is an independent prognostic marker and superior to LDH. Onkologie 31(7):380–384CrossRefPubMed Egberts F, Pollex A, Egberts JH, Kaehler KC, Weichenthal M, Hauschild A (2008) Long-term survival analysis in metastatic melanoma: serum S100B is an independent prognostic marker and superior to LDH. Onkologie 31(7):380–384CrossRefPubMed
27.
go back to reference Martenson ED, Hansson LO, Nilsson B, von Schoultz E, Brahme EM, Ringborg U, Hansson J (2001) Serum S-100B protein as a prognostic marker in malignant cutaneous melanoma. J Clin Oncol 19(3):824–831PubMed Martenson ED, Hansson LO, Nilsson B, von Schoultz E, Brahme EM, Ringborg U, Hansson J (2001) Serum S-100B protein as a prognostic marker in malignant cutaneous melanoma. J Clin Oncol 19(3):824–831PubMed
28.
go back to reference Donato R (2001) S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 33(7):637–668CrossRefPubMed Donato R (2001) S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 33(7):637–668CrossRefPubMed
29.
30.
go back to reference Romagnani S (2002) Cytokines and chemoattractants in allergic inflammation. Mol Immunol 38(12–13):881–885CrossRefPubMed Romagnani S (2002) Cytokines and chemoattractants in allergic inflammation. Mol Immunol 38(12–13):881–885CrossRefPubMed
33.
go back to reference Henry CJ, Ornelles DA, Mitchell LM, Brzoza-Lewis KL, Hiltbold EM (2008) IL-12 produced by dendritic cells augments CD8+ T cell activation through the production of the chemokines CCL1 and CCL17. J Immunol 181(12):8576–8584PubMedCentralCrossRefPubMed Henry CJ, Ornelles DA, Mitchell LM, Brzoza-Lewis KL, Hiltbold EM (2008) IL-12 produced by dendritic cells augments CD8+ T cell activation through the production of the chemokines CCL1 and CCL17. J Immunol 181(12):8576–8584PubMedCentralCrossRefPubMed
34.
go back to reference Inoue H, Iga M, Xin M, Asahi S, Nakamura T, Kurita R, Nakayama M, Nakazaki Y, Takayama K, Nakanishi Y, Tani K (2008) TARC and RANTES enhance antitumor immunity induced by the GM-CSF-transduced tumor vaccine in a mouse tumor model. Cancer Immunol Immunother 57(9):1399–1411. doi:10.1007/s00262-008-0476-7 CrossRefPubMed Inoue H, Iga M, Xin M, Asahi S, Nakamura T, Kurita R, Nakayama M, Nakazaki Y, Takayama K, Nakanishi Y, Tani K (2008) TARC and RANTES enhance antitumor immunity induced by the GM-CSF-transduced tumor vaccine in a mouse tumor model. Cancer Immunol Immunother 57(9):1399–1411. doi:10.​1007/​s00262-008-0476-7 CrossRefPubMed
36.
go back to reference Sugiyama D, Nishikawa H, Maeda Y, Nishioka M, Tanemura A, Katayama I, Ezoe S, Kanakura Y, Sato E, Fukumori Y, Karbach J, Jager E, Sakaguchi S (2013) Anti-CCR4 mAb selectively depletes effector-type FoxP3+ CD4+ regulatory T cells, evoking antitumor immune responses in humans. Proc Natl Acad Sci USA 110(44):17945–17950. doi:10.1073/pnas.1316796110 PubMedCentralCrossRefPubMed Sugiyama D, Nishikawa H, Maeda Y, Nishioka M, Tanemura A, Katayama I, Ezoe S, Kanakura Y, Sato E, Fukumori Y, Karbach J, Jager E, Sakaguchi S (2013) Anti-CCR4 mAb selectively depletes effector-type FoxP3+ CD4+ regulatory T cells, evoking antitumor immune responses in humans. Proc Natl Acad Sci USA 110(44):17945–17950. doi:10.​1073/​pnas.​1316796110 PubMedCentralCrossRefPubMed
37.
go back to reference Dudley ME, Yang JC, Sherry R, Hughes MS, Royal R, Kammula U, Robbins PF, Huang J, Citrin DE, Leitman SF, Wunderlich J, Restifo NP, Thomasian A, Downey SG, Smith FO, Klapper J, Morton K, Laurencot C, White DE, Rosenberg SA (2008) Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol 26(32):5233–5239. doi:10.1200/JCO.2008.16.5449 PubMedCentralCrossRefPubMed Dudley ME, Yang JC, Sherry R, Hughes MS, Royal R, Kammula U, Robbins PF, Huang J, Citrin DE, Leitman SF, Wunderlich J, Restifo NP, Thomasian A, Downey SG, Smith FO, Klapper J, Morton K, Laurencot C, White DE, Rosenberg SA (2008) Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol 26(32):5233–5239. doi:10.​1200/​JCO.​2008.​16.​5449 PubMedCentralCrossRefPubMed
38.
go back to reference Hodi FS, O’Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, Akerley W, van den Eertwegh AJ, Lutzky J, Lorigan P, Vaubel JM, Linette GP, Hogg D, Ottensmeier CH, Lebbe C, Peschel C, Quirt I, Clark JI, Wolchok JD, Weber JS, Tian J, Yellin MJ, Nichol GM, Hoos A, Urba WJ (2010) Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363(8):711–723. doi:10.1056/NEJMoa1003466 PubMedCentralCrossRefPubMed Hodi FS, O’Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, Akerley W, van den Eertwegh AJ, Lutzky J, Lorigan P, Vaubel JM, Linette GP, Hogg D, Ottensmeier CH, Lebbe C, Peschel C, Quirt I, Clark JI, Wolchok JD, Weber JS, Tian J, Yellin MJ, Nichol GM, Hoos A, Urba WJ (2010) Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363(8):711–723. doi:10.​1056/​NEJMoa1003466 PubMedCentralCrossRefPubMed
39.
go back to reference Robert C, Thomas L, Bondarenko I, O’Day S, Weber J, Garbe C, Lebbe C, Baurain JF, Testori A, Grob JJ, Davidson N, Richards J, Maio M, Hauschild A, Miller WH Jr, Gascon P, Lotem M, Harmankaya K, Ibrahim R, Francis S, Chen TT, Humphrey R, Hoos A, Wolchok JD (2011) Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 364(26):2517–2526. doi:10.1056/NEJMoa1104621 CrossRefPubMed Robert C, Thomas L, Bondarenko I, O’Day S, Weber J, Garbe C, Lebbe C, Baurain JF, Testori A, Grob JJ, Davidson N, Richards J, Maio M, Hauschild A, Miller WH Jr, Gascon P, Lotem M, Harmankaya K, Ibrahim R, Francis S, Chen TT, Humphrey R, Hoos A, Wolchok JD (2011) Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 364(26):2517–2526. doi:10.​1056/​NEJMoa1104621 CrossRefPubMed
40.
go back to reference Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, Wolchok JD, Hersey P, Joseph RW, Weber JS, Dronca R, Gangadhar TC, Patnaik A, Zarour H, Joshua AM, Gergich K, Elassaiss-Schaap J, Algazi A, Mateus C, Boasberg P, Tumeh PC, Chmielowski B, Ebbinghaus SW, Li XN, Kang SP, Ribas A (2013) Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 369(2):134–144. doi:10.1056/NEJMoa1305133 PubMedCentralCrossRefPubMed Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, Wolchok JD, Hersey P, Joseph RW, Weber JS, Dronca R, Gangadhar TC, Patnaik A, Zarour H, Joshua AM, Gergich K, Elassaiss-Schaap J, Algazi A, Mateus C, Boasberg P, Tumeh PC, Chmielowski B, Ebbinghaus SW, Li XN, Kang SP, Ribas A (2013) Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 369(2):134–144. doi:10.​1056/​NEJMoa1305133 PubMedCentralCrossRefPubMed
41.
go back to reference Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, Pitot HC, Hamid O, Bhatia S, Martins R, Eaton K, Chen S, Salay TM, Alaparthy S, Grosso JF, Korman AJ, Parker SM, Agrawal S, Goldberg SM, Pardoll DM, Gupta A, Wigginton JM (2012) Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 366(26):2455–2465. doi:10.1056/NEJMoa1200694 PubMedCentralCrossRefPubMed Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, Pitot HC, Hamid O, Bhatia S, Martins R, Eaton K, Chen S, Salay TM, Alaparthy S, Grosso JF, Korman AJ, Parker SM, Agrawal S, Goldberg SM, Pardoll DM, Gupta A, Wigginton JM (2012) Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 366(26):2455–2465. doi:10.​1056/​NEJMoa1200694 PubMedCentralCrossRefPubMed
42.
go back to reference Ji RR, Chasalow SD, Wang L, Hamid O, Schmidt H, Cogswell J, Alaparthy S, Berman D, Jure-Kunkel M, Siemers NO, Jackson JR, Shahabi V (2012) An immune-active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol Immunother 61(7):1019–1031. doi:10.1007/s00262-011-1172-6 CrossRefPubMed Ji RR, Chasalow SD, Wang L, Hamid O, Schmidt H, Cogswell J, Alaparthy S, Berman D, Jure-Kunkel M, Siemers NO, Jackson JR, Shahabi V (2012) An immune-active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol Immunother 61(7):1019–1031. doi:10.​1007/​s00262-011-1172-6 CrossRefPubMed
43.
Metadata
Title
Increased CCL17 serum levels are associated with improved survival in advanced melanoma
Authors
Benjamin Weide
Nicolas Allgaier
Andreas Hector
Andrea Forschner
Ulrike Leiter
Thomas K. Eigentler
Claus Garbe
Dominik Hartl
Publication date
01-09-2015
Publisher
Springer Berlin Heidelberg
Published in
Cancer Immunology, Immunotherapy / Issue 9/2015
Print ISSN: 0340-7004
Electronic ISSN: 1432-0851
DOI
https://doi.org/10.1007/s00262-015-1714-4

Other articles of this Issue 9/2015

Cancer Immunology, Immunotherapy 9/2015 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