Skip to main content
Top
Published in: Journal of Neuro-Oncology 2/2013

01-09-2013 | Clinical Study

A panel of four cytokines predicts the prognosis of patients with malignant gliomas

Authors: Yi Lin, Guozhen Zhang, Jing Zhang, Guangzu Gao, Min Li, Yong Chen, Jiangfei Wang, Guilin Li, Sonya-Wei Song, Xiaoguang Qiu, Yunjie Wang, Tao Jiang

Published in: Journal of Neuro-Oncology | Issue 2/2013

Login to get access

Abstract

A comprehensive evaluation of cytokine levels in patients with gliomas could provide important information for the progression and host responses of gliomas. We studied a panel of 120 cytokines and growth factors and investigated their prognostic values for glioma. A protein antibody array was first performed to study the prognostic significance of 120 cytokines in the plasma samples of 45 glioblastoma patients prior to craniotomy or biopsy procedure. An independent set of plasma samples from 260 patients with astrocytomas (80 grade II, 80 grade III, 100 grade IV) with complete clinicopathologic data and follow-ups were used for validation. Ten cytokines were identified by significance analysis of microarray, in which four were associated with poor prognosis (IL-15, MCP-1, GDNF, IL-1R4/ST2), and six were associated with good prognosis (IGFBP-6, MIP-1δ, ICAM-3, IL-7, MIP-3β, and sgp130) of the glioblastoma patients. Moreover, a 4-cytokine panel composed of IL-7, IL1R4/ST2, sgp130 and MCP-1 showed significant correlation with overall survival of the glioblastoma patients (HR 2.068; 95 % CI 1.357–3.153; p = 0.001). In the validation set, the cytokine panel was significantly correlated with overall survival in the 260 glioma patients (HR 3.480, 95 % CI 1.890–6.422) in multivariate Cox regression analysis. It also showed strong correlation with survival in patients with malignant gliomas (grade III: HR 2.790, 95 % CI 1.597–3.984, p = 0.002; grade IV: HR 1.753; 95 % CI 1.502–2.255, p < 0.001). This panel of four cytokines: IL-7, IL1R4/ST2, sgp130, and MCP-1 can serve as a prognostic marker for patients with malignant gliomas.
Appendix
Available only for authorised users
Literature
1.
go back to reference Louis D, Ohgaki H, Wiestler O, Cavenee W (2007) WHO classification of tumours of the central nervous system. IARC, Lyon Louis D, Ohgaki H, Wiestler O, Cavenee W (2007) WHO classification of tumours of the central nervous system. IARC, Lyon
2.
go back to reference Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996PubMedCrossRef Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996PubMedCrossRef
3.
go back to reference Rivera AL, Pelloski CE, Gilbert MR, Colman H, De La Cruz C, Sulman EP, Bekele BN, Aldape KD (2010) MGMT promoter methylation is predictive of response to radiotherapy and prognostic in the absence of adjuvant alkylating chemotherapy for glioblastoma. Neuro Oncol 12:116–121PubMedCrossRef Rivera AL, Pelloski CE, Gilbert MR, Colman H, De La Cruz C, Sulman EP, Bekele BN, Aldape KD (2010) MGMT promoter methylation is predictive of response to radiotherapy and prognostic in the absence of adjuvant alkylating chemotherapy for glioblastoma. Neuro Oncol 12:116–121PubMedCrossRef
4.
go back to reference Giannini C, Burger PC, Berkey BA, Cairncross JG, Jenkins RB, Mehta M, Curran WJ, Aldape K (2008) Anaplastic oligodendroglial tumors: refining the correlation among histopathology, 1p 19q deletion and clinical outcome in Intergroup Radiation Therapy Oncology Group Trial 9402. Brain Pathol 18:360–369. doi:10.1111/j.1750-3639.2008.00129.x PubMedCrossRef Giannini C, Burger PC, Berkey BA, Cairncross JG, Jenkins RB, Mehta M, Curran WJ, Aldape K (2008) Anaplastic oligodendroglial tumors: refining the correlation among histopathology, 1p 19q deletion and clinical outcome in Intergroup Radiation Therapy Oncology Group Trial 9402. Brain Pathol 18:360–369. doi:10.​1111/​j.​1750-3639.​2008.​00129.​x PubMedCrossRef
5.
go back to reference Houillier C, Wang X, Kaloshi G, Mokhtari K, Guillevin R, Laffaire J, Paris S, Boisselier B, Idbaih A, Laigle-Donadey F, Hoang-Xuan K, Sanson M, Delattre JY (2010) IDH1 or IDH2 mutations predict longer survival and response to temozolomide in low-grade gliomas. Neurology 75:1560–1566PubMedCrossRef Houillier C, Wang X, Kaloshi G, Mokhtari K, Guillevin R, Laffaire J, Paris S, Boisselier B, Idbaih A, Laigle-Donadey F, Hoang-Xuan K, Sanson M, Delattre JY (2010) IDH1 or IDH2 mutations predict longer survival and response to temozolomide in low-grade gliomas. Neurology 75:1560–1566PubMedCrossRef
6.
go back to reference Lin Y, Jiang T, Zhou K, Xu L, Chen B, Li G, Qiu X, Jiang T, Zhang W, Song SW (2009) Plasma IGFBP-2 levels predict clinical outcomes of patients with high-grade gliomas. Neuro Oncol 11:468–476PubMedCrossRef Lin Y, Jiang T, Zhou K, Xu L, Chen B, Li G, Qiu X, Jiang T, Zhang W, Song SW (2009) Plasma IGFBP-2 levels predict clinical outcomes of patients with high-grade gliomas. Neuro Oncol 11:468–476PubMedCrossRef
7.
go back to reference Hormigo A, Gu B, Karimi S, Riedel E, Panageas KS, Edgar MA, Tanwar MK, Rao JS, Fleisher M, DeAngelis LM, Holland EC (2006) YKL-40 and matrix metalloproteinase-9 as potential serum biomarkers for patients with high-grade gliomas. Clin Cancer Res 12:5698–5704. doi:10.1158/1078-0432.CCR-06-0181 PubMedCrossRef Hormigo A, Gu B, Karimi S, Riedel E, Panageas KS, Edgar MA, Tanwar MK, Rao JS, Fleisher M, DeAngelis LM, Holland EC (2006) YKL-40 and matrix metalloproteinase-9 as potential serum biomarkers for patients with high-grade gliomas. Clin Cancer Res 12:5698–5704. doi:10.​1158/​1078-0432.​CCR-06-0181 PubMedCrossRef
8.
go back to reference Jung CS, Foerch C, Schanzer A, Heck A, Plate KH, Seifert V, Steinmetz H, Raabe A, Sitzer M (2007) Serum GFAP is a diagnostic marker for glioblastoma multiforme. Brain 130:3336–3341PubMedCrossRef Jung CS, Foerch C, Schanzer A, Heck A, Plate KH, Seifert V, Steinmetz H, Raabe A, Sitzer M (2007) Serum GFAP is a diagnostic marker for glioblastoma multiforme. Brain 130:3336–3341PubMedCrossRef
9.
go back to reference Fukuda ME, Iwadate Y, Machida T, Hiwasa T, Nimura Y, Nagai Y, Takiguchi M, Tanzawa H, Yamaura A, Seki N (2005) Cathepsin D is a potential serum marker for poor prognosis in glioma patients. Cancer Res 65:5190–5194PubMedCrossRef Fukuda ME, Iwadate Y, Machida T, Hiwasa T, Nimura Y, Nagai Y, Takiguchi M, Tanzawa H, Yamaura A, Seki N (2005) Cathepsin D is a potential serum marker for poor prognosis in glioma patients. Cancer Res 65:5190–5194PubMedCrossRef
10.
go back to reference Quan N, Herkenham M (2002) Connecting cytokines and brain: a review of current issues. Histol Histopathol 17:273–288PubMed Quan N, Herkenham M (2002) Connecting cytokines and brain: a review of current issues. Histol Histopathol 17:273–288PubMed
11.
go back to reference Ray S, Britschgi M, Herbert C, Takeda-Uchimura Y, Boxer A, Blennow K, Friedman LF, Galasko DR, Jutel M, Karydas A, Kaye JA, Leszek J, Miller BL, Minthon L, Quinn JF, Rabinovici GD, Robinson WH, Sabbagh MN, So YT, Sparks DL, Tabaton M, Tinklenberg J, Yesavage JA, Tibshirani R, Wyss-Coray T (2007) Classification and prediction of clinical Alzheimer’s diagnosis based on plasma signaling proteins. Nat Med 13:1359–1362PubMedCrossRef Ray S, Britschgi M, Herbert C, Takeda-Uchimura Y, Boxer A, Blennow K, Friedman LF, Galasko DR, Jutel M, Karydas A, Kaye JA, Leszek J, Miller BL, Minthon L, Quinn JF, Rabinovici GD, Robinson WH, Sabbagh MN, So YT, Sparks DL, Tabaton M, Tinklenberg J, Yesavage JA, Tibshirani R, Wyss-Coray T (2007) Classification and prediction of clinical Alzheimer’s diagnosis based on plasma signaling proteins. Nat Med 13:1359–1362PubMedCrossRef
12.
go back to reference Muller L, Pawelec G (2003) Cytokines and antitumor immunity. Technol Cancer Res Treat 2:183–194PubMed Muller L, Pawelec G (2003) Cytokines and antitumor immunity. Technol Cancer Res Treat 2:183–194PubMed
13.
go back to reference Zeh HJ, Winikoff S, Landsittel DP, Gorelik E, Marrangoni AM, Velikokhatnaya L, Winans MT, Lee K, Moser A, Bartlett D, Lotze MT, Siegfried JM, Whitcomb D, Papacristou G, Slivka A, Bigbee WL, Lokshin AE (2005) Multianalyte profiling of serum cytokines for detection of pancreatic cancer. Cancer Biomark 1:259–269PubMed Zeh HJ, Winikoff S, Landsittel DP, Gorelik E, Marrangoni AM, Velikokhatnaya L, Winans MT, Lee K, Moser A, Bartlett D, Lotze MT, Siegfried JM, Whitcomb D, Papacristou G, Slivka A, Bigbee WL, Lokshin AE (2005) Multianalyte profiling of serum cytokines for detection of pancreatic cancer. Cancer Biomark 1:259–269PubMed
14.
go back to reference Gorelik E, Landsittel DP, Marrangoni AM, Modugno F, Velikokhatnaya L, Winans MT, Bigbee WL, Herberman RB, Lokshin AE (2005) Multiplexed immunobead-based cytokine profiling for early detection of ovarian cancer. Cancer Epidemiol Biomarkers Prev 14:981–987PubMedCrossRef Gorelik E, Landsittel DP, Marrangoni AM, Modugno F, Velikokhatnaya L, Winans MT, Bigbee WL, Herberman RB, Lokshin AE (2005) Multiplexed immunobead-based cytokine profiling for early detection of ovarian cancer. Cancer Epidemiol Biomarkers Prev 14:981–987PubMedCrossRef
15.
go back to reference Pusztai L, Mendoza TR, Reuben JM, Martinez MM, Willey JS, Lara J, Syed A, Fritsche HA, Bruera E, Booser D, Valero V, Arun B, Ibrahim N, Rivera E, Royce M, Cleeland CS, Hortobagyi GN (2004) Changes in plasma levels of inflammatory cytokines in response to paclitaxel chemotherapy. Cytokine 25:94–102PubMedCrossRef Pusztai L, Mendoza TR, Reuben JM, Martinez MM, Willey JS, Lara J, Syed A, Fritsche HA, Bruera E, Booser D, Valero V, Arun B, Ibrahim N, Rivera E, Royce M, Cleeland CS, Hortobagyi GN (2004) Changes in plasma levels of inflammatory cytokines in response to paclitaxel chemotherapy. Cytokine 25:94–102PubMedCrossRef
16.
go back to reference Kaminska J, Nowacki MP, Kowalska M, Rysinska A, Chwalinski M, Fuksiewicz M, Michalski W, Chechlinska M (2005) Clinical significance of serum cytokine measurements in untreated colorectal cancer patients: soluble tumor necrosis factor receptor type I—an independent prognostic factor. Tumour Biol 26:186–194PubMedCrossRef Kaminska J, Nowacki MP, Kowalska M, Rysinska A, Chwalinski M, Fuksiewicz M, Michalski W, Chechlinska M (2005) Clinical significance of serum cytokine measurements in untreated colorectal cancer patients: soluble tumor necrosis factor receptor type I—an independent prognostic factor. Tumour Biol 26:186–194PubMedCrossRef
17.
go back to reference Linkov F, Lisovich A, Yurkovetsky Z, Marrangoni A, Velikokhatnaya L, Nolen B, Winans M, Bigbee W, Siegfried J, Lokshin A, Ferris RL (2007) Early detection of head and neck cancer: development of a novel screening tool using multiplexed immunobead-based biomarker profiling. Cancer Epidemiol Biomarkers Prev 16:102–107PubMedCrossRef Linkov F, Lisovich A, Yurkovetsky Z, Marrangoni A, Velikokhatnaya L, Nolen B, Winans M, Bigbee W, Siegfried J, Lokshin A, Ferris RL (2007) Early detection of head and neck cancer: development of a novel screening tool using multiplexed immunobead-based biomarker profiling. Cancer Epidemiol Biomarkers Prev 16:102–107PubMedCrossRef
18.
go back to reference Katsumata N, Eguchi K, Fukuda M, Yamamoto N, Ohe Y, Oshita F, Tamura T, Shinkai T, Saijo N (1996) Serum levels of cytokines in patients with untreated primary lung cancer. Clin Cancer Res 2:553–559PubMed Katsumata N, Eguchi K, Fukuda M, Yamamoto N, Ohe Y, Oshita F, Tamura T, Shinkai T, Saijo N (1996) Serum levels of cytokines in patients with untreated primary lung cancer. Clin Cancer Res 2:553–559PubMed
19.
go back to reference Enewold L, Mechanic LE, Bowman ED, Zheng YL, Yu Z, Trivers G, Alberg AJ, Harris CC (2009) Serum concentrations of cytokines and lung cancer survival in African Americans and Caucasians. Cancer Epidemiol Biomarkers Prev 18:215–222PubMedCrossRef Enewold L, Mechanic LE, Bowman ED, Zheng YL, Yu Z, Trivers G, Alberg AJ, Harris CC (2009) Serum concentrations of cytokines and lung cancer survival in African Americans and Caucasians. Cancer Epidemiol Biomarkers Prev 18:215–222PubMedCrossRef
20.
go back to reference Jiang Y, Valente AJ, Williamson MJ, Zhang L, Graves DT (1990) Post-translational modification of a monocyte-specific chemoattractant synthesized by glioma, osteosarcoma, and vascular smooth muscle cells. J Biol Chem 265:18318–18321PubMed Jiang Y, Valente AJ, Williamson MJ, Zhang L, Graves DT (1990) Post-translational modification of a monocyte-specific chemoattractant synthesized by glioma, osteosarcoma, and vascular smooth muscle cells. J Biol Chem 265:18318–18321PubMed
21.
go back to reference Kasahara T, Mukaida N, Yamashita K, Yagisawa H, Akahoshi T, Matsushima K (1991) IL-1 and TNF-alpha induction of IL-8 and monocyte chemotactic and activating factor (MCAF) mRNA expression in a human astrocytoma cell line. Immunology 74:60–67PubMed Kasahara T, Mukaida N, Yamashita K, Yagisawa H, Akahoshi T, Matsushima K (1991) IL-1 and TNF-alpha induction of IL-8 and monocyte chemotactic and activating factor (MCAF) mRNA expression in a human astrocytoma cell line. Immunology 74:60–67PubMed
22.
go back to reference Nitta T, Sato K, Allegretta M, Brocke S, Lim M, Mitchell DJ, Steinman L (1992) Expression of granulocyte colony stimulating factor and granulocyte-macrophage colony stimulating factor genes in human astrocytoma cell lines and in glioma specimens. Brain Res 571:19–25PubMedCrossRef Nitta T, Sato K, Allegretta M, Brocke S, Lim M, Mitchell DJ, Steinman L (1992) Expression of granulocyte colony stimulating factor and granulocyte-macrophage colony stimulating factor genes in human astrocytoma cell lines and in glioma specimens. Brain Res 571:19–25PubMedCrossRef
23.
go back to reference Kuratsu J, Yoshizato K, Yoshimura T, Leonard EJ, Takeshima H, Ushio Y (1993) Quantitative study of monocyte chemoattractant protein-1 (MCP-1) in cerebrospinal fluid and cyst fluid from patients with malignant glioma. J Natl Cancer Inst 85:1836–1839PubMedCrossRef Kuratsu J, Yoshizato K, Yoshimura T, Leonard EJ, Takeshima H, Ushio Y (1993) Quantitative study of monocyte chemoattractant protein-1 (MCP-1) in cerebrospinal fluid and cyst fluid from patients with malignant glioma. J Natl Cancer Inst 85:1836–1839PubMedCrossRef
24.
go back to reference Gousias K, Markou M, Arzoglou V, Voulgaris S, Vartholomatos G, Kostoula A, Voulgari P, Polyzoidis K, Kyritsis AP (2010) Frequent abnormalities of the immune system in gliomas and correlation with the WHO grading system of malignancy. J Neuroimmunol 226:136–142PubMedCrossRef Gousias K, Markou M, Arzoglou V, Voulgaris S, Vartholomatos G, Kostoula A, Voulgari P, Polyzoidis K, Kyritsis AP (2010) Frequent abnormalities of the immune system in gliomas and correlation with the WHO grading system of malignancy. J Neuroimmunol 226:136–142PubMedCrossRef
25.
go back to reference Paik S, Shak S, Tang G, Kim C, Baker J, Cronin M, Baehner FL, Walker MG, Watson D, Park T, Hiller W, Fisher ER, Wickerham DL, Bryant J, Wolmark N (2004) A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 351:2817–2826PubMedCrossRef Paik S, Shak S, Tang G, Kim C, Baker J, Cronin M, Baehner FL, Walker MG, Watson D, Park T, Hiller W, Fisher ER, Wickerham DL, Bryant J, Wolmark N (2004) A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 351:2817–2826PubMedCrossRef
26.
go back to reference Lynch DH, Namen AE, Miller RE (1991) In vivo evaluation of the effects of interleukins 2, 4 and 7 on enhancing the immunotherapeutic efficacy of anti-tumor cytotoxic T lymphocytes. Eur J Immunol 21:2977–2985PubMedCrossRef Lynch DH, Namen AE, Miller RE (1991) In vivo evaluation of the effects of interleukins 2, 4 and 7 on enhancing the immunotherapeutic efficacy of anti-tumor cytotoxic T lymphocytes. Eur J Immunol 21:2977–2985PubMedCrossRef
27.
go back to reference Sica D, Rayman P, Stanley J, Edinger M, Tubbs RR, Klein E, Bukowski R, Finke JH (1993) Interleukin 7 enhances the proliferation and effector function of tumor-infiltrating lymphocytes from renal-cell carcinoma. Int J Cancer 53:941–947PubMedCrossRef Sica D, Rayman P, Stanley J, Edinger M, Tubbs RR, Klein E, Bukowski R, Finke JH (1993) Interleukin 7 enhances the proliferation and effector function of tumor-infiltrating lymphocytes from renal-cell carcinoma. Int J Cancer 53:941–947PubMedCrossRef
28.
go back to reference Narazaki M, Yasukawa K, Saito T, Ohsugi Y, Fukui H, Koishihara Y, Yancopoulos GD, Taga T, Kishimoto T (1993) Soluble forms of the interleukin-6 signal-transducing receptor component gp130 in human serum possessing a potential to inhibit signals through membrane-anchored gp130. Blood 82:1120–1126PubMed Narazaki M, Yasukawa K, Saito T, Ohsugi Y, Fukui H, Koishihara Y, Yancopoulos GD, Taga T, Kishimoto T (1993) Soluble forms of the interleukin-6 signal-transducing receptor component gp130 in human serum possessing a potential to inhibit signals through membrane-anchored gp130. Blood 82:1120–1126PubMed
29.
go back to reference Weiergraber O, Hemmann U, Kuster A, Muller-Newen G, Schneider J, Rose-John S, Kurschat P, Brakenhoff JP, Hart MH, Stabel S et al (1995) Soluble human interleukin-6 receptor. Expression in insect cells, purification and characterization. Eur J Biochem 234:661–669PubMedCrossRef Weiergraber O, Hemmann U, Kuster A, Muller-Newen G, Schneider J, Rose-John S, Kurschat P, Brakenhoff JP, Hart MH, Stabel S et al (1995) Soluble human interleukin-6 receptor. Expression in insect cells, purification and characterization. Eur J Biochem 234:661–669PubMedCrossRef
30.
go back to reference Chalaris A, Garbers C, Rabe B, Rose-John S, Scheller J (2011) The soluble Interleukin 6 receptor: generation and role in inflammation and cancer. Eur J Cell Biol 90:484–494PubMedCrossRef Chalaris A, Garbers C, Rabe B, Rose-John S, Scheller J (2011) The soluble Interleukin 6 receptor: generation and role in inflammation and cancer. Eur J Cell Biol 90:484–494PubMedCrossRef
31.
go back to reference Rabe B, Chalaris A, May U, Waetzig GH, Seegert D, Williams AS, Jones SA, Rose-John S, Scheller J (2008) Transgenic blockade of interleukin 6 transsignaling abrogates inflammation. Blood 111:1021–1028PubMedCrossRef Rabe B, Chalaris A, May U, Waetzig GH, Seegert D, Williams AS, Jones SA, Rose-John S, Scheller J (2008) Transgenic blockade of interleukin 6 transsignaling abrogates inflammation. Blood 111:1021–1028PubMedCrossRef
32.
go back to reference Kropf P, Herath S, Klemenz R, Muller I (2003) Signaling through the T1/ST2 molecule is not necessary for Th2 differentiation but is important for the regulation of type 1 responses in nonhealing Leishmania major infection. Infect Immun 71:1961–1971PubMedCrossRef Kropf P, Herath S, Klemenz R, Muller I (2003) Signaling through the T1/ST2 molecule is not necessary for Th2 differentiation but is important for the regulation of type 1 responses in nonhealing Leishmania major infection. Infect Immun 71:1961–1971PubMedCrossRef
33.
go back to reference Amatucci A, Novobrantseva T, Gilbride K, Brickelmaier M, Hochman P, Ibraghimov A (2007) Recombinant ST2 boosts hepatic Th2 response in vivo. J Leukoc Biol 82:124–132PubMedCrossRef Amatucci A, Novobrantseva T, Gilbride K, Brickelmaier M, Hochman P, Ibraghimov A (2007) Recombinant ST2 boosts hepatic Th2 response in vivo. J Leukoc Biol 82:124–132PubMedCrossRef
34.
go back to reference Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, Zurawski G, Moshrefi M, Qin J, Li X, Gorman DM, Bazan JF, Kastelein RA (2005) IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23:479–490PubMedCrossRef Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, Zurawski G, Moshrefi M, Qin J, Li X, Gorman DM, Bazan JF, Kastelein RA (2005) IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23:479–490PubMedCrossRef
35.
go back to reference Takezako N, Hayakawa M, Hayakawa H, Aoki S, Yanagisawa K, Endo H, Tominaga S (2006) ST2 suppresses IL-6 production via the inhibition of IkappaB degradation induced by the LPS signal in THP-1 cells. Biochem Biophys Res Commun 341:425–432PubMedCrossRef Takezako N, Hayakawa M, Hayakawa H, Aoki S, Yanagisawa K, Endo H, Tominaga S (2006) ST2 suppresses IL-6 production via the inhibition of IkappaB degradation induced by the LPS signal in THP-1 cells. Biochem Biophys Res Commun 341:425–432PubMedCrossRef
36.
go back to reference Moffatt MF, Gut IG, Demenais F, Strachan DP, Bouzigon E, Heath S, von Mutius E, Farrall M, Lathrop M, Cookson WO (2010) A large-scale, consortium-based genomewide association study of asthma. N Engl J Med 363:1211–1221PubMedCrossRef Moffatt MF, Gut IG, Demenais F, Strachan DP, Bouzigon E, Heath S, von Mutius E, Farrall M, Lathrop M, Cookson WO (2010) A large-scale, consortium-based genomewide association study of asthma. N Engl J Med 363:1211–1221PubMedCrossRef
37.
go back to reference Wiemels JL, Wiencke JK, Sison JD, Miike R, McMillan A, Wrensch M (2002) History of allergies among adults with glioma and controls. Int J Cancer 98:609–615PubMedCrossRef Wiemels JL, Wiencke JK, Sison JD, Miike R, McMillan A, Wrensch M (2002) History of allergies among adults with glioma and controls. Int J Cancer 98:609–615PubMedCrossRef
38.
go back to reference Yoshimura T, Robinson EA, Tanaka S, Appella E, Kuratsu J, Leonard EJ (1989) Purification and amino acid analysis of two human glioma-derived monocyte chemoattractants. J Exp Med 169:1449–1459PubMedCrossRef Yoshimura T, Robinson EA, Tanaka S, Appella E, Kuratsu J, Leonard EJ (1989) Purification and amino acid analysis of two human glioma-derived monocyte chemoattractants. J Exp Med 169:1449–1459PubMedCrossRef
39.
go back to reference Takeshima H, Kuratsu J, Takeya M, Yoshimura T, Ushio Y (1994) Expression and localization of messenger RNA and protein for monocyte chemoattractant protein-1 in human malignant glioma. J Neurosurg 80:1056–1062PubMedCrossRef Takeshima H, Kuratsu J, Takeya M, Yoshimura T, Ushio Y (1994) Expression and localization of messenger RNA and protein for monocyte chemoattractant protein-1 in human malignant glioma. J Neurosurg 80:1056–1062PubMedCrossRef
40.
go back to reference Salcedo R, Ponce ML, Young HA, Wasserman K, Ward JM, Kleinman HK, Oppenheim JJ, Murphy WJ (2000) Human endothelial cells express CCR2 and respond to MCP-1: direct role of MCP-1 in angiogenesis and tumor progression. Blood 96:34–40PubMed Salcedo R, Ponce ML, Young HA, Wasserman K, Ward JM, Kleinman HK, Oppenheim JJ, Murphy WJ (2000) Human endothelial cells express CCR2 and respond to MCP-1: direct role of MCP-1 in angiogenesis and tumor progression. Blood 96:34–40PubMed
41.
go back to reference Platten M, Kretz A, Naumann U, Aulwurm S, Egashira K, Isenmann S, Weller M (2003) Monocyte chemoattractant protein-1 increases microglial infiltration and aggressiveness of gliomas. Ann Neurol 54:388–392PubMedCrossRef Platten M, Kretz A, Naumann U, Aulwurm S, Egashira K, Isenmann S, Weller M (2003) Monocyte chemoattractant protein-1 increases microglial infiltration and aggressiveness of gliomas. Ann Neurol 54:388–392PubMedCrossRef
Metadata
Title
A panel of four cytokines predicts the prognosis of patients with malignant gliomas
Authors
Yi Lin
Guozhen Zhang
Jing Zhang
Guangzu Gao
Min Li
Yong Chen
Jiangfei Wang
Guilin Li
Sonya-Wei Song
Xiaoguang Qiu
Yunjie Wang
Tao Jiang
Publication date
01-09-2013
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 2/2013
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-013-1171-x

Other articles of this Issue 2/2013

Journal of Neuro-Oncology 2/2013 Go to the issue