Skip to main content
Erschienen in: Cancer Immunology, Immunotherapy 2/2018

20.10.2017 | Original Article

Clinicopathologic implications of CD8+/Foxp3+ ratio and miR-574-3p/PD-L1 axis in spinal chordoma patients

verfasst von: Ming-Xiang Zou, Ke-Miao Guo, Guo-Hua Lv, Wei Huang, Jing Li, Xiao-Bin Wang, Yi Jiang, Xiao-Ling She

Erschienen in: Cancer Immunology, Immunotherapy | Ausgabe 2/2018

Einloggen, um Zugang zu erhalten

Abstract

Currently, little is known about the interactions between microRNAs (miRNAs) and the PD-1/PD-L1 signaling pathway in chordoma, and data discussing the role of the immune milieu in chordoma prognosis are limited. We aimed to analyze the relationship between PD-L1, miR-574-3p, microenvironmental tumor-infiltrating lymphocytes (TILs) and clinicopathological features of spinal chordoma patients. PD-L1 expression and TILs (including Foxp3+, CD8+, PD-1+ and PD-L1+) were assessed by immunohistochemistry in tumor specimens of 54 spinal chordoma patients. MiRNAs microarray and bioinformatical analysis were used to identify miRNAs potentially regulating PD-L1 expression, which were further validated by quantitative RT-PCR. miR-574-3p was identified to potentially regulate PD-L1 expression in chordoma, which inversely correlated with PD-L1. Positive PD-L1 expression on tumor cells was associated with advanced stages (P = 0.041) and TILs infiltration (P = 0.005), whereas decreased miR-574-3p level correlated with higher muscle invasion (P = 0.012), more severe tumor necrosis (P = 0.022) and poor patient survival. Importantly, a patient subgroup with PD-L1+/miR-574-3plow chordoma phenotype was significantly associated with worse local recurrence-free survival (LRFS) (P = 0.026). PD-1+ TILs density was associated with surrounding muscle invasion (P = 0.014), and independently portended poor LRFS (P = 0.040), while PD-L1+ TILs showed tendencies of less aggressive clinical outcomes. Multivariate analysis of OS only found CD8+/Foxp3+ ratio to be independent prognostic factor (P = 0.022). These findings may be useful to stratify patients into prognostic groups and provide a rationale for the use of checkpoint blockade therapy, possibly by administering miR-574-3p mimics, in spinal chordoma.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Hu H, Yang HL, Lu J, Chen KW, Qiu YH, Liu W, Luo ZP (2012) Association of telomerase expression with recurrence of sacral chordoma. Ann Oncol 23(10):2772CrossRefPubMed Hu H, Yang HL, Lu J, Chen KW, Qiu YH, Liu W, Luo ZP (2012) Association of telomerase expression with recurrence of sacral chordoma. Ann Oncol 23(10):2772CrossRefPubMed
2.
Zurück zum Zitat Samson IR, Springfield DS, Suit HD, Mankin HJ (1993) Operative treatment of sacrococcygeal chordoma. A review of twenty-one cases. J Bone Joint Surg Am 75(10):1476–1484CrossRefPubMed Samson IR, Springfield DS, Suit HD, Mankin HJ (1993) Operative treatment of sacrococcygeal chordoma. A review of twenty-one cases. J Bone Joint Surg Am 75(10):1476–1484CrossRefPubMed
3.
Zurück zum Zitat Walcott BP, Nahed BV, Mohyeldin A, Coumans JV, Kahle KT, Ferreira MJ (2012) Chordoma: current concepts, management, and future directions. Lancet Oncol 13(2):e69–e76CrossRefPubMed Walcott BP, Nahed BV, Mohyeldin A, Coumans JV, Kahle KT, Ferreira MJ (2012) Chordoma: current concepts, management, and future directions. Lancet Oncol 13(2):e69–e76CrossRefPubMed
4.
Zurück zum Zitat Bompas E, Le Cesne A, Tresch-Bruneel E, Lebellec L, Laurence V, Collard O, Saada-Bouzid E, Isambert N, Blay JY, Amela EY, Salas S, Chevreau C, Bertucci F, Italiano A, Clisant S, Penel N (2015) Sorafenib in patients with locally advanced and metastatic chordomas: a phase II trial of the French Sarcoma Group (GSF/GETO). Ann Oncol 26(10):2168–2173CrossRefPubMedPubMedCentral Bompas E, Le Cesne A, Tresch-Bruneel E, Lebellec L, Laurence V, Collard O, Saada-Bouzid E, Isambert N, Blay JY, Amela EY, Salas S, Chevreau C, Bertucci F, Italiano A, Clisant S, Penel N (2015) Sorafenib in patients with locally advanced and metastatic chordomas: a phase II trial of the French Sarcoma Group (GSF/GETO). Ann Oncol 26(10):2168–2173CrossRefPubMedPubMedCentral
5.
Zurück zum Zitat McMaster ML, Goldstein AM, Bromley CM, Ishibe N, Parry DM (2001) Chordoma: incidence and survival patterns in the United States, 1973–1995. Cancer Causes Control 12(1):1–11CrossRefPubMed McMaster ML, Goldstein AM, Bromley CM, Ishibe N, Parry DM (2001) Chordoma: incidence and survival patterns in the United States, 1973–1995. Cancer Causes Control 12(1):1–11CrossRefPubMed
6.
Zurück zum Zitat Bydon M, Papadimitriou K, Witham T, Wolinsky JP, Bydon A, Sciubba D, Gokaslan Z (2012) Novel therapeutic targets in chordoma. Expert Opin Ther Targets 16(11):1139–1143CrossRefPubMed Bydon M, Papadimitriou K, Witham T, Wolinsky JP, Bydon A, Sciubba D, Gokaslan Z (2012) Novel therapeutic targets in chordoma. Expert Opin Ther Targets 16(11):1139–1143CrossRefPubMed
7.
Zurück zum Zitat Kayani B, Hanna SA, Sewell MD, Saifuddin A, Molloy S, Briggs TW (2014) A review of the surgical management of sacral chordoma. Eur J Surg Oncol 40(11):1412–1420CrossRefPubMed Kayani B, Hanna SA, Sewell MD, Saifuddin A, Molloy S, Briggs TW (2014) A review of the surgical management of sacral chordoma. Eur J Surg Oncol 40(11):1412–1420CrossRefPubMed
8.
Zurück zum Zitat Fuchs B, Dickey ID, Yaszemski MJ, Inwards CY, Sim FH (2005) Operative management of sacral chordoma. J Bone Joint Surg Am 87(10):2211–2216PubMed Fuchs B, Dickey ID, Yaszemski MJ, Inwards CY, Sim FH (2005) Operative management of sacral chordoma. J Bone Joint Surg Am 87(10):2211–2216PubMed
9.
Zurück zum Zitat Kayani B, Sewell MD, Tan KA, Hanna SA, Williams R, Pollock R, Skinner J, Briggs TW (2015) Prognostic factors in the operative management of sacral chordomas. World Neurosurg 84(5):1354–1361CrossRefPubMed Kayani B, Sewell MD, Tan KA, Hanna SA, Williams R, Pollock R, Skinner J, Briggs TW (2015) Prognostic factors in the operative management of sacral chordomas. World Neurosurg 84(5):1354–1361CrossRefPubMed
10.
Zurück zum Zitat Baratti D, Gronchi A, Pennacchioli E, Lozza L, Colecchia M, Fiore M, Santinami M (2003) Chordoma: natural history and results in 28 patients treated at a single institution. Ann Surg Oncol 10(3):291–296CrossRefPubMed Baratti D, Gronchi A, Pennacchioli E, Lozza L, Colecchia M, Fiore M, Santinami M (2003) Chordoma: natural history and results in 28 patients treated at a single institution. Ann Surg Oncol 10(3):291–296CrossRefPubMed
11.
Zurück zum Zitat Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, Roche PC, Lu J, Zhu G, Tamada K, Lennon VA, Celis E, Chen L (2002) Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 8(8):793–800CrossRefPubMed Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, Roche PC, Lu J, Zhu G, Tamada K, Lennon VA, Celis E, Chen L (2002) Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 8(8):793–800CrossRefPubMed
12.
Zurück zum Zitat Iwai Y, Ishida M, Tanaka Y, Okazaki T, Honjo T, Minato N (2002) Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl Acad Sci USA 99(19):12293–12297CrossRefPubMedPubMedCentral Iwai Y, Ishida M, Tanaka Y, Okazaki T, Honjo T, Minato N (2002) Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl Acad Sci USA 99(19):12293–12297CrossRefPubMedPubMedCentral
13.
Zurück zum Zitat Marcq E, Pauwels P, van Meerbeeck JP, Smits EL (2015) Targeting immune checkpoints: new opportunity for mesothelioma treatment? Cancer Treat Rev 41(10):914–924CrossRefPubMed Marcq E, Pauwels P, van Meerbeeck JP, Smits EL (2015) Targeting immune checkpoints: new opportunity for mesothelioma treatment? Cancer Treat Rev 41(10):914–924CrossRefPubMed
14.
Zurück zum Zitat Senbabaoglu Y, Gejman RS, Winer AG, Liu M, Van Allen EM, de Velasco G, Miao D, Ostrovnaya I, Drill E, Luna A, Weinhold N, Lee W, Manley BJ, Khalil DN, Kaffenberger SD, Chen Y, Danilova L, Voss MH, Coleman JA, Russo P, Reuter VE, Chan TA, Cheng EH, Scheinberg DA, Li MO, Choueiri TK, Hsieh JJ, Sander C, Hakimi AA (2016) Tumor immune microenvironment characterization in clear cell renal cell carcinoma identifies prognostic and immunotherapeutically relevant messenger RNA signatures. Genome Biol 17(1):231CrossRefPubMedPubMedCentral Senbabaoglu Y, Gejman RS, Winer AG, Liu M, Van Allen EM, de Velasco G, Miao D, Ostrovnaya I, Drill E, Luna A, Weinhold N, Lee W, Manley BJ, Khalil DN, Kaffenberger SD, Chen Y, Danilova L, Voss MH, Coleman JA, Russo P, Reuter VE, Chan TA, Cheng EH, Scheinberg DA, Li MO, Choueiri TK, Hsieh JJ, Sander C, Hakimi AA (2016) Tumor immune microenvironment characterization in clear cell renal cell carcinoma identifies prognostic and immunotherapeutically relevant messenger RNA signatures. Genome Biol 17(1):231CrossRefPubMedPubMedCentral
15.
16.
Zurück zum Zitat Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, Lee W, Yuan J, Wong P, Ho TS, Miller ML, Rekhtman N, Moreira AL, Ibrahim F, Bruggeman C, Gasmi B, Zappasodi R, Maeda Y, Sander C, Garon EB, Merghoub T, Wolchok JD, Schumacher TN, Chan TA (2015) Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348(6230):124–128CrossRefPubMedPubMedCentral Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, Lee W, Yuan J, Wong P, Ho TS, Miller ML, Rekhtman N, Moreira AL, Ibrahim F, Bruggeman C, Gasmi B, Zappasodi R, Maeda Y, Sander C, Garon EB, Merghoub T, Wolchok JD, Schumacher TN, Chan TA (2015) Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348(6230):124–128CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Gooden MJ, de Bock GH, Leffers N, Daemen T, Nijman HW (2011) The prognostic influence of tumour-infiltrating lymphocytes in cancer: a systematic review with meta-analysis. Br J Cancer 105(1):93–103CrossRefPubMedPubMedCentral Gooden MJ, de Bock GH, Leffers N, Daemen T, Nijman HW (2011) The prognostic influence of tumour-infiltrating lymphocytes in cancer: a systematic review with meta-analysis. Br J Cancer 105(1):93–103CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat deLeeuw RJ, Kost SE, Kakal JA, Nelson BH (2012) The prognostic value of FoxP3+ tumor-infiltrating lymphocytes in cancer: a critical review of the literature. Clin Cancer Res 18(11):3022–3029CrossRefPubMed deLeeuw RJ, Kost SE, Kakal JA, Nelson BH (2012) The prognostic value of FoxP3+ tumor-infiltrating lymphocytes in cancer: a critical review of the literature. Clin Cancer Res 18(11):3022–3029CrossRefPubMed
19.
Zurück zum Zitat Zou MX, Peng AB, Lv GH, Wang XB, Li J, She XL, Jiang Y (2016) Expression of programmed death-1 ligand (PD-L1) in tumor-infiltrating lymphocytes is associated with favorable spinal chordoma prognosis. Am J Transl Res 8(7):3274–3287PubMedPubMedCentral Zou MX, Peng AB, Lv GH, Wang XB, Li J, She XL, Jiang Y (2016) Expression of programmed death-1 ligand (PD-L1) in tumor-infiltrating lymphocytes is associated with favorable spinal chordoma prognosis. Am J Transl Res 8(7):3274–3287PubMedPubMedCentral
20.
Zurück zum Zitat Feng Y, Shen J, Gao Y, Liao Y, Cote G, Choy E, Chebib I, Mankin H, Hornicek F, Duan Z (2015) Expression of programmed cell death ligand 1 (PD-L1) and prevalence of tumor-infiltrating lymphocytes (TILs) in chordoma. Oncotarget 6(13):11139–11149CrossRefPubMedPubMedCentral Feng Y, Shen J, Gao Y, Liao Y, Cote G, Choy E, Chebib I, Mankin H, Hornicek F, Duan Z (2015) Expression of programmed cell death ligand 1 (PD-L1) and prevalence of tumor-infiltrating lymphocytes (TILs) in chordoma. Oncotarget 6(13):11139–11149CrossRefPubMedPubMedCentral
21.
Zurück zum Zitat Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297CrossRefPubMed Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297CrossRefPubMed
22.
Zurück zum Zitat Inui M, Martello G, Piccolo S (2010) MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 11(4):252–263CrossRefPubMed Inui M, Martello G, Piccolo S (2010) MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 11(4):252–263CrossRefPubMed
23.
24.
Zurück zum Zitat Gulluoglu S, Tuysuz EC, Kuskucu A, Ture U, Atalay B, Sahin F, Bayrak OF (2016) The potential function of microRNA in chordomas. Gene 585(1):76–83CrossRefPubMed Gulluoglu S, Tuysuz EC, Kuskucu A, Ture U, Atalay B, Sahin F, Bayrak OF (2016) The potential function of microRNA in chordomas. Gene 585(1):76–83CrossRefPubMed
25.
Zurück zum Zitat Zou MX, Lv GH, Wang XB, Li J (2016) Prognostic biomarkers in spinal chordoma: a systematic review. J Neuropathol Exp Neurol 75(12):1184–1187CrossRefPubMed Zou MX, Lv GH, Wang XB, Li J (2016) Prognostic biomarkers in spinal chordoma: a systematic review. J Neuropathol Exp Neurol 75(12):1184–1187CrossRefPubMed
26.
Zurück zum Zitat Galon J, Pages F, Marincola FM, Angell HK, Thurin M, Lugli A, Zlobec I, Berger A, Bifulco C, Botti G, Tatangelo F, Britten CM, Kreiter S, Chouchane L, Delrio P, Arndt H, Asslaber M, Maio M, Masucci GV, Mihm M, Vidal-Vanaclocha F, Allison JP, Gnjatic S, Hakansson L, Huber C, Singh-Jasuja H, Ottensmeier C, Zwierzina H, Laghi L, Grizzi F, Ohashi PS, Shaw PA, Clarke BA, Wouters BG, Kawakami Y, Hazama S, Okuno K, Wang E, O’Donnell-Tormey J, Lagorce C, Pawelec G, Nishimura MI, Hawkins R, Lapointe R, Lundqvist A, Khleif SN, Ogino S, Gibbs P, Waring P, Sato N, Torigoe T, Itoh K, Patel PS, Shukla SN, Palmqvist R, Nagtegaal ID, Wang Y, D’Arrigo C, Kopetz S, Sinicrope FA, Trinchieri G, Gajewski TF, Ascierto PA, Fox BA (2012) Cancer classification using the Immunoscore: a worldwide task force. J Transl Med 10:205CrossRefPubMedPubMedCentral Galon J, Pages F, Marincola FM, Angell HK, Thurin M, Lugli A, Zlobec I, Berger A, Bifulco C, Botti G, Tatangelo F, Britten CM, Kreiter S, Chouchane L, Delrio P, Arndt H, Asslaber M, Maio M, Masucci GV, Mihm M, Vidal-Vanaclocha F, Allison JP, Gnjatic S, Hakansson L, Huber C, Singh-Jasuja H, Ottensmeier C, Zwierzina H, Laghi L, Grizzi F, Ohashi PS, Shaw PA, Clarke BA, Wouters BG, Kawakami Y, Hazama S, Okuno K, Wang E, O’Donnell-Tormey J, Lagorce C, Pawelec G, Nishimura MI, Hawkins R, Lapointe R, Lundqvist A, Khleif SN, Ogino S, Gibbs P, Waring P, Sato N, Torigoe T, Itoh K, Patel PS, Shukla SN, Palmqvist R, Nagtegaal ID, Wang Y, D’Arrigo C, Kopetz S, Sinicrope FA, Trinchieri G, Gajewski TF, Ascierto PA, Fox BA (2012) Cancer classification using the Immunoscore: a worldwide task force. J Transl Med 10:205CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat Zou MX, Lv GH, Li J, She XL, Jiang Y (2016) Upregulated human telomerase reverse transcriptase (hTERT) expression is associated with spinal chordoma growth, invasion and poor prognosis. Am J Transl Res 8(2):516–529PubMedPubMedCentral Zou MX, Lv GH, Li J, She XL, Jiang Y (2016) Upregulated human telomerase reverse transcriptase (hTERT) expression is associated with spinal chordoma growth, invasion and poor prognosis. Am J Transl Res 8(2):516–529PubMedPubMedCentral
28.
Zurück zum Zitat Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ (2007) Cancer statistics. CA Cancer J Clin 57(1):43–66CrossRefPubMed Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ (2007) Cancer statistics. CA Cancer J Clin 57(1):43–66CrossRefPubMed
29.
Zurück zum Zitat Fisher CG, Saravanja DD, Dvorak MF, Rampersaud YR, Clarkson PW, Hurlbert J, Fox R, Zhang H, Lewis S, Riaz S, Ferguson PC, Boyd MC (2011) Surgical management of primary bone tumors of the spine: validation of an approach to enhance cure and reduce local recurrence. Spine (Phila Pa 1976) 36(10):830–836CrossRef Fisher CG, Saravanja DD, Dvorak MF, Rampersaud YR, Clarkson PW, Hurlbert J, Fox R, Zhang H, Lewis S, Riaz S, Ferguson PC, Boyd MC (2011) Surgical management of primary bone tumors of the spine: validation of an approach to enhance cure and reduce local recurrence. Spine (Phila Pa 1976) 36(10):830–836CrossRef
30.
Zurück zum Zitat Chen K, Mo J, Zhou M, Wang G, Wu G, Chen H, Zhang K, Yang H (2014) Expression of PTEN and mTOR in sacral chordoma and association with poor prognosis. Med Oncol 31(4):886CrossRefPubMed Chen K, Mo J, Zhou M, Wang G, Wu G, Chen H, Zhang K, Yang H (2014) Expression of PTEN and mTOR in sacral chordoma and association with poor prognosis. Med Oncol 31(4):886CrossRefPubMed
31.
Zurück zum Zitat Zhou M, Chen K, Yang H, Wang G, Lu J, Ji Y, Wu C, Chen C (2014) Expression of insulin-like growth factor II mRNA-binding protein 3 (IMP3) in sacral chordoma. J Neurooncol 116(1):77–82CrossRefPubMed Zhou M, Chen K, Yang H, Wang G, Lu J, Ji Y, Wu C, Chen C (2014) Expression of insulin-like growth factor II mRNA-binding protein 3 (IMP3) in sacral chordoma. J Neurooncol 116(1):77–82CrossRefPubMed
32.
Zurück zum Zitat Meng T, Yin H, Li B, Li Z, Xu W, Zhou W, Cheng M, Wang J, Zhou L, Yang X, Liu T, Yan W, Song D, Xiao J (2015) Clinical features and prognostic factors of patients with chordoma in the spine: a retrospective analysis of 153 patients in a single center. Neuro Oncol 17(5):725–732CrossRefPubMed Meng T, Yin H, Li B, Li Z, Xu W, Zhou W, Cheng M, Wang J, Zhou L, Yang X, Liu T, Yan W, Song D, Xiao J (2015) Clinical features and prognostic factors of patients with chordoma in the spine: a retrospective analysis of 153 patients in a single center. Neuro Oncol 17(5):725–732CrossRefPubMed
33.
Zurück zum Zitat Zou MX, Huang W, Wang XB, Li J, Lv GH, Wang B, Deng YW (2015) Reduced expression of miRNA-1237-3p associated with poor survival of spinal chordoma patients. Eur Spine J 24(8):1738–1746CrossRefPubMed Zou MX, Huang W, Wang XB, Li J, Lv GH, Wang B, Deng YW (2015) Reduced expression of miRNA-1237-3p associated with poor survival of spinal chordoma patients. Eur Spine J 24(8):1738–1746CrossRefPubMed
34.
Zurück zum Zitat Zou MX, Huang W, Wang XB, Lv GH, Li J, Deng YW (2014) Identification of miR-140-3p as a marker associated with poor prognosis in spinal chordoma. Int J Clin Exp Pathol 7(8):4877–4885PubMedPubMedCentral Zou MX, Huang W, Wang XB, Lv GH, Li J, Deng YW (2014) Identification of miR-140-3p as a marker associated with poor prognosis in spinal chordoma. Int J Clin Exp Pathol 7(8):4877–4885PubMedPubMedCentral
35.
Zurück zum Zitat Wang A, Wang HY, Liu Y, Zhao MC, Zhang HJ, Lu ZY, Fang YC, Chen XF, Liu GT (2015) The prognostic value of PD-L1 expression for non-small cell lung cancer patients: a meta-analysis. Eur J Surg Oncol 41(4):450–456CrossRefPubMed Wang A, Wang HY, Liu Y, Zhao MC, Zhang HJ, Lu ZY, Fang YC, Chen XF, Liu GT (2015) The prognostic value of PD-L1 expression for non-small cell lung cancer patients: a meta-analysis. Eur J Surg Oncol 41(4):450–456CrossRefPubMed
36.
Zurück zum Zitat Zhang Y, Kang S, Shen J, He J, Jiang L, Wang W, Guo Z, Peng G, Chen G, He J, Liang W (2015) Prognostic significance of programmed cell death 1 (PD-1) or PD-1 ligand 1 (PD-L1) expression in epithelial-originated cancer: a meta-analysis. Medicine (Baltimore) 94(6):e515CrossRef Zhang Y, Kang S, Shen J, He J, Jiang L, Wang W, Guo Z, Peng G, Chen G, He J, Liang W (2015) Prognostic significance of programmed cell death 1 (PD-1) or PD-1 ligand 1 (PD-L1) expression in epithelial-originated cancer: a meta-analysis. Medicine (Baltimore) 94(6):e515CrossRef
38.
Zurück zum Zitat Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408CrossRefPubMed Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408CrossRefPubMed
39.
Zurück zum Zitat Zhu Y, Li M, Mu D, Kong L, Zhang J, Zhao F, Li Z, Liu X, Bo C, Yu J (2016) CD8+/FOXP3+ ratio and PD-L1 expression associated with survival in pT3N0M0 stage esophageal squamous cell cancer. Oncotarget 7(44):71455–71465CrossRefPubMedPubMedCentral Zhu Y, Li M, Mu D, Kong L, Zhang J, Zhao F, Li Z, Liu X, Bo C, Yu J (2016) CD8+/FOXP3+ ratio and PD-L1 expression associated with survival in pT3N0M0 stage esophageal squamous cell cancer. Oncotarget 7(44):71455–71465CrossRefPubMedPubMedCentral
40.
Zurück zum Zitat Berghoff AS, Fuchs E, Ricken G, Mlecnik B, Bindea G, Spanberger T, Hackl M, Widhalm G, Dieckmann K, Prayer D, Bilocq A, Heinzl H, Zielinski C, Bartsch R, Birner P, Galon J, Preusser M (2016) Density of tumor-infiltrating lymphocytes correlates with extent of brain edema and overall survival time in patients with brain metastases. Oncoimmunology 5(1):e1057388CrossRefPubMed Berghoff AS, Fuchs E, Ricken G, Mlecnik B, Bindea G, Spanberger T, Hackl M, Widhalm G, Dieckmann K, Prayer D, Bilocq A, Heinzl H, Zielinski C, Bartsch R, Birner P, Galon J, Preusser M (2016) Density of tumor-infiltrating lymphocytes correlates with extent of brain edema and overall survival time in patients with brain metastases. Oncoimmunology 5(1):e1057388CrossRefPubMed
41.
Zurück zum Zitat Bellmunt J, Mullane SA, Werner L, Fay AP, Callea M, Leow JJ, Taplin ME, Choueiri TK, Hodi FS, Freeman GJ, Signoretti S (2015) Association of PD-L1 expression on tumor-infiltrating mononuclear cells and overall survival in patients with urothelial carcinoma. Ann Oncol 26(4):812–817CrossRefPubMed Bellmunt J, Mullane SA, Werner L, Fay AP, Callea M, Leow JJ, Taplin ME, Choueiri TK, Hodi FS, Freeman GJ, Signoretti S (2015) Association of PD-L1 expression on tumor-infiltrating mononuclear cells and overall survival in patients with urothelial carcinoma. Ann Oncol 26(4):812–817CrossRefPubMed
42.
Zurück zum Zitat Teng F, Meng X, Wang X, Yuan J, Liu S, Mu D, Zhu H, Kong L, Yu J (2016) Expressions of CD8+ TILs, PD-L1 and Foxp3+ TILs in stage I NSCLC guiding adjuvant chemotherapy decisions. Oncotarget 7(39):64318–64329CrossRefPubMedPubMedCentral Teng F, Meng X, Wang X, Yuan J, Liu S, Mu D, Zhu H, Kong L, Yu J (2016) Expressions of CD8+ TILs, PD-L1 and Foxp3+ TILs in stage I NSCLC guiding adjuvant chemotherapy decisions. Oncotarget 7(39):64318–64329CrossRefPubMedPubMedCentral
43.
Zurück zum Zitat Kollmann D, Ignatova D, Jedamzik J, Chang YT, Jomrich G, Paireder M, Kristo I, Kazakov D, Michal M, Cozzio A, Hoetzenecker W, Schatton T, Asari R, Preusser M, Guenova E, Schoppmann SF (2017) Expression of programmed cell death protein 1 by tumor-infiltrating lymphocytes and tumor cells is associated with advanced tumor stage in patients with Esophageal Adenocarcinoma. Ann Surg Oncol 24(9):2698–2706CrossRefPubMedPubMedCentral Kollmann D, Ignatova D, Jedamzik J, Chang YT, Jomrich G, Paireder M, Kristo I, Kazakov D, Michal M, Cozzio A, Hoetzenecker W, Schatton T, Asari R, Preusser M, Guenova E, Schoppmann SF (2017) Expression of programmed cell death protein 1 by tumor-infiltrating lymphocytes and tumor cells is associated with advanced tumor stage in patients with Esophageal Adenocarcinoma. Ann Surg Oncol 24(9):2698–2706CrossRefPubMedPubMedCentral
44.
Zurück zum Zitat Li S, Xu F, Li H, Zhang J, Zhong A, Huang B, Lai M (2017) S100A8+ stroma cells predict a good prognosis and inhibit aggressiveness in colorectal carcinoma. Oncoimmunology 6(1):e1260213CrossRefPubMed Li S, Xu F, Li H, Zhang J, Zhong A, Huang B, Lai M (2017) S100A8+ stroma cells predict a good prognosis and inhibit aggressiveness in colorectal carcinoma. Oncoimmunology 6(1):e1260213CrossRefPubMed
45.
Zurück zum Zitat Gabrielson A, Wu Y, Wang H, Jiang J, Kallakury B, Gatalica Z, Reddy S, Kleiner D, Fishbein T, Johnson L, Island E, Satoskar R, Banovac F, Jha R, Kachhela J, Feng P, Zhang T, Tesfaye A, Prins P, Loffredo C, Marshall J, Weiner L, Atkins M, He AR (2016) Intratumoral CD3 and CD8 T-cell densities associated with relapse-free survival in HCC. Cancer Immunol Res 4(5):419–430CrossRefPubMedPubMedCentral Gabrielson A, Wu Y, Wang H, Jiang J, Kallakury B, Gatalica Z, Reddy S, Kleiner D, Fishbein T, Johnson L, Island E, Satoskar R, Banovac F, Jha R, Kachhela J, Feng P, Zhang T, Tesfaye A, Prins P, Loffredo C, Marshall J, Weiner L, Atkins M, He AR (2016) Intratumoral CD3 and CD8 T-cell densities associated with relapse-free survival in HCC. Cancer Immunol Res 4(5):419–430CrossRefPubMedPubMedCentral
46.
Zurück zum Zitat Budczies J, Klauschen F, Sinn BV, Gyorffy B, Schmitt WD, Darb-Esfahani S, Denkert C (2012) Cutoff finder: a comprehensive and straightforward Web application enabling rapid biomarker cutoff optimization. PLoS One 7(12):e51862CrossRefPubMedPubMedCentral Budczies J, Klauschen F, Sinn BV, Gyorffy B, Schmitt WD, Darb-Esfahani S, Denkert C (2012) Cutoff finder: a comprehensive and straightforward Web application enabling rapid biomarker cutoff optimization. PLoS One 7(12):e51862CrossRefPubMedPubMedCentral
47.
Zurück zum Zitat Lim JS, Sundar R, Chénard-Poirier M, Lopez J, Yap TA (2017) Emerging biomarkers for PD-1 pathway cancer therapy. Biomark Med 11(1):53–67CrossRefPubMed Lim JS, Sundar R, Chénard-Poirier M, Lopez J, Yap TA (2017) Emerging biomarkers for PD-1 pathway cancer therapy. Biomark Med 11(1):53–67CrossRefPubMed
48.
Zurück zum Zitat Yuasa T, Masuda H, Yamamoto S, Numao N, Yonese J (2017) Biomarkers to predict prognosis and response to checkpoint inhibitors. Int J Clin Oncol 22(4):629–634CrossRefPubMedPubMedCentral Yuasa T, Masuda H, Yamamoto S, Numao N, Yonese J (2017) Biomarkers to predict prognosis and response to checkpoint inhibitors. Int J Clin Oncol 22(4):629–634CrossRefPubMedPubMedCentral
49.
Zurück zum Zitat Ji Z, Long H, Hu Y, Qiu X, Chen X, Li Z, Fan D, Ma B, Fan Q (2010) Expression of MDR1, HIF-1alpha and MRP1 in sacral chordoma and chordoma cell line CM-319. J Exp Clin Cancer Res 29:158CrossRefPubMedPubMedCentral Ji Z, Long H, Hu Y, Qiu X, Chen X, Li Z, Fan D, Ma B, Fan Q (2010) Expression of MDR1, HIF-1alpha and MRP1 in sacral chordoma and chordoma cell line CM-319. J Exp Clin Cancer Res 29:158CrossRefPubMedPubMedCentral
50.
Zurück zum Zitat Li X, Ji Z, Ma Y, Qiu X, Fan Q, Ma B (2012) Expression of hypoxia-inducible factor-1alpha, vascular endothelial growth factor and matrix metalloproteinase-2 in sacral chordomas. Oncol Lett 3(6):1268–1274CrossRefPubMedPubMedCentral Li X, Ji Z, Ma Y, Qiu X, Fan Q, Ma B (2012) Expression of hypoxia-inducible factor-1alpha, vascular endothelial growth factor and matrix metalloproteinase-2 in sacral chordomas. Oncol Lett 3(6):1268–1274CrossRefPubMedPubMedCentral
51.
Zurück zum Zitat Lee DH, Zhang Y, Kassam AB, Park MJ, Gardner P, Prevedello D, Henry S, Horbinski C, Beumer JH, Tawbi H, Williams BJ, Shaffrey ME, Egorin MJ, Abounader R, Park DM (2015) Combined PDGFR and HDAC inhibition overcomes PTEN disruption in chordoma. PLoS One 10(8):e0134426CrossRefPubMedPubMedCentral Lee DH, Zhang Y, Kassam AB, Park MJ, Gardner P, Prevedello D, Henry S, Horbinski C, Beumer JH, Tawbi H, Williams BJ, Shaffrey ME, Egorin MJ, Abounader R, Park DM (2015) Combined PDGFR and HDAC inhibition overcomes PTEN disruption in chordoma. PLoS One 10(8):e0134426CrossRefPubMedPubMedCentral
52.
Zurück zum Zitat Barsoum IB, Smallwood CA, Siemens DR, Graham CH (2014) A mechanism of hypoxia-mediated escape from adaptive immunity in cancer cells. Cancer Res 74(3):665–674CrossRefPubMed Barsoum IB, Smallwood CA, Siemens DR, Graham CH (2014) A mechanism of hypoxia-mediated escape from adaptive immunity in cancer cells. Cancer Res 74(3):665–674CrossRefPubMed
53.
Zurück zum Zitat Noman MZ, Desantis G, Janji B, Hasmim M, Karray S, Dessen P, Bronte V, Chouaib S (2014) PD-L1 is a novel direct target of HIF-1alpha, and its blockade under hypoxia enhanced MDSC-mediated T cell activation. J Exp Med 211(5):781–790CrossRefPubMedPubMedCentral Noman MZ, Desantis G, Janji B, Hasmim M, Karray S, Dessen P, Bronte V, Chouaib S (2014) PD-L1 is a novel direct target of HIF-1alpha, and its blockade under hypoxia enhanced MDSC-mediated T cell activation. J Exp Med 211(5):781–790CrossRefPubMedPubMedCentral
54.
Zurück zum Zitat Spranger S, Gajewski TF (2016) Tumor-intrinsic oncogene pathways mediating immune avoidance. Oncoimmunology 5(3):e1086862CrossRefPubMed Spranger S, Gajewski TF (2016) Tumor-intrinsic oncogene pathways mediating immune avoidance. Oncoimmunology 5(3):e1086862CrossRefPubMed
55.
Zurück zum Zitat Su Y, Ni Z, Wang G, Cui J, Wei C, Wang J, Yang Q, Xu Y, Li F (2012) Aberrant expression of microRNAs in gastric cancer and biological significance of miR-574-3p. Int Immunopharmacol 13(4):468–475CrossRefPubMedPubMedCentral Su Y, Ni Z, Wang G, Cui J, Wei C, Wang J, Yang Q, Xu Y, Li F (2012) Aberrant expression of microRNAs in gastric cancer and biological significance of miR-574-3p. Int Immunopharmacol 13(4):468–475CrossRefPubMedPubMedCentral
56.
Zurück zum Zitat Tatarano S, Chiyomaru T, Kawakami K, Enokida H, Yoshino H, Hidaka H, Nohata N, Yamasaki T, Gotanda T, Tachiwada T, Seki N, Nakagawa M (2012) Novel oncogenic function of mesoderm development candidate 1 and its regulation by MiR-574-3p in bladder cancer cell lines. Int J Oncol 40(4):951–959CrossRefPubMed Tatarano S, Chiyomaru T, Kawakami K, Enokida H, Yoshino H, Hidaka H, Nohata N, Yamasaki T, Gotanda T, Tachiwada T, Seki N, Nakagawa M (2012) Novel oncogenic function of mesoderm development candidate 1 and its regulation by MiR-574-3p in bladder cancer cell lines. Int J Oncol 40(4):951–959CrossRefPubMed
57.
Zurück zum Zitat Chiyomaru T, Yamamura S, Fukuhara S, Hidaka H, Majid S, Saini S, Arora S, Deng G, Shahryari V, Chang I, Tanaka Y, Tabatabai ZL, Enokida H, Seki N, Nakagawa M, Dahiya R (2013) Genistein up-regulates tumor suppressor microRNA-574-3p in prostate cancer. PLoS One 8(3):e58929CrossRefPubMedPubMedCentral Chiyomaru T, Yamamura S, Fukuhara S, Hidaka H, Majid S, Saini S, Arora S, Deng G, Shahryari V, Chang I, Tanaka Y, Tabatabai ZL, Enokida H, Seki N, Nakagawa M, Dahiya R (2013) Genistein up-regulates tumor suppressor microRNA-574-3p in prostate cancer. PLoS One 8(3):e58929CrossRefPubMedPubMedCentral
58.
Zurück zum Zitat Ujihira T, Ikeda K, Suzuki T, Yamaga R, Sato W, Horie-Inoue K, Shigekawa T, Osaki A, Saeki T, Okamoto K, Takeda S, Inoue S (2015) MicroRNA-574-3p, identified by microRNA library-based functional screening, modulates tamoxifen response in breast cancer. Sci Rep 5:7641CrossRefPubMedPubMedCentral Ujihira T, Ikeda K, Suzuki T, Yamaga R, Sato W, Horie-Inoue K, Shigekawa T, Osaki A, Saeki T, Okamoto K, Takeda S, Inoue S (2015) MicroRNA-574-3p, identified by microRNA library-based functional screening, modulates tamoxifen response in breast cancer. Sci Rep 5:7641CrossRefPubMedPubMedCentral
59.
Zurück zum Zitat Zhao L, Yu H, Yi S, Peng X, Su P, Xiao Z, Liu R, Tang A, Li X, Liu F, Shen S (2016) The tumor suppressor miR-138-5p targets PD-L1 in colorectal cancer. Oncotarget 7(29):45370–45384CrossRefPubMedPubMedCentral Zhao L, Yu H, Yi S, Peng X, Su P, Xiao Z, Liu R, Tang A, Li X, Liu F, Shen S (2016) The tumor suppressor miR-138-5p targets PD-L1 in colorectal cancer. Oncotarget 7(29):45370–45384CrossRefPubMedPubMedCentral
60.
Zurück zum Zitat Fritzsching B, Fellenberg J, Moskovszky L, Sapi Z, Krenacs T, Machado I, Poeschl J, Lehner B, Szendroi M, Bosch AL, Bernd L, Csoka M, Mechtersheimer G, Ewerbeck V, Kinscherf R, Kunz P (2015) CD8+/FOXP3+-ratio in osteosarcoma microenvironment separates survivors from non-survivors: a multicenter validated retrospective study. Oncoimmunology 4(3):e990800CrossRefPubMedPubMedCentral Fritzsching B, Fellenberg J, Moskovszky L, Sapi Z, Krenacs T, Machado I, Poeschl J, Lehner B, Szendroi M, Bosch AL, Bernd L, Csoka M, Mechtersheimer G, Ewerbeck V, Kinscherf R, Kunz P (2015) CD8+/FOXP3+-ratio in osteosarcoma microenvironment separates survivors from non-survivors: a multicenter validated retrospective study. Oncoimmunology 4(3):e990800CrossRefPubMedPubMedCentral
61.
Zurück zum Zitat Asano Y, Kashiwagi S, Goto W, Kurata K, Noda S, Takashima T, Onoda N, Tanaka S, Ohsawa M, Hirakawa K (2016) Tumour-infiltrating CD8 to FOXP3 lymphocyte ratio in predicting treatment responses to neoadjuvant chemotherapy of aggressive breast cancer. Br J Surg 103(7):845–854CrossRefPubMed Asano Y, Kashiwagi S, Goto W, Kurata K, Noda S, Takashima T, Onoda N, Tanaka S, Ohsawa M, Hirakawa K (2016) Tumour-infiltrating CD8 to FOXP3 lymphocyte ratio in predicting treatment responses to neoadjuvant chemotherapy of aggressive breast cancer. Br J Surg 103(7):845–854CrossRefPubMed
62.
Zurück zum Zitat Roychoudhuri R, Eil RL, Restifo NP (2015) The interplay of effector and regulatory T cells in cancer. Curr Opin Immunol 33:101–111CrossRefPubMed Roychoudhuri R, Eil RL, Restifo NP (2015) The interplay of effector and regulatory T cells in cancer. Curr Opin Immunol 33:101–111CrossRefPubMed
63.
Zurück zum Zitat Kim JR, Moon YJ, Kwon KS, Bae JS, Wagle S, Kim KM, Park HS, Lee H, Moon WS, Chung MJ, Kang MJ, Jang KY (2013) Tumor infiltrating PD1-positive lymphocytes and the expression of PD-L1 predict poor prognosis of soft tissue sarcomas. PLoS One 8(12):e82870CrossRefPubMedPubMedCentral Kim JR, Moon YJ, Kwon KS, Bae JS, Wagle S, Kim KM, Park HS, Lee H, Moon WS, Chung MJ, Kang MJ, Jang KY (2013) Tumor infiltrating PD1-positive lymphocytes and the expression of PD-L1 predict poor prognosis of soft tissue sarcomas. PLoS One 8(12):e82870CrossRefPubMedPubMedCentral
64.
Zurück zum Zitat Kang MJ, Kim KM, Bae JS, Park HS, Lee H, Chung MJ, Moon WS, Lee DG, Jang KY (2013) Tumor-infiltrating PD1-positive lymphocytes and FoxP3-positive regulatory T cells predict distant metastatic relapse and survival of clear cell renal cell carcinoma. Transl Oncol 6(3):282–289CrossRefPubMedPubMedCentral Kang MJ, Kim KM, Bae JS, Park HS, Lee H, Chung MJ, Moon WS, Lee DG, Jang KY (2013) Tumor-infiltrating PD1-positive lymphocytes and FoxP3-positive regulatory T cells predict distant metastatic relapse and survival of clear cell renal cell carcinoma. Transl Oncol 6(3):282–289CrossRefPubMedPubMedCentral
65.
Zurück zum Zitat Zhao T, Li C, Wu Y, Li B, Zhang B (2017) Prognostic value of PD-L1 expression in tumor infiltrating immune cells in cancers: a meta-analysis. PLoS One 12(4):e0176822CrossRefPubMedPubMedCentral Zhao T, Li C, Wu Y, Li B, Zhang B (2017) Prognostic value of PD-L1 expression in tumor infiltrating immune cells in cancers: a meta-analysis. PLoS One 12(4):e0176822CrossRefPubMedPubMedCentral
66.
Zurück zum Zitat Altman DG, Lausen B, Sauerbrei W, Schumacher M (1994) Dangers of using “optimal” cutpoints in the evaluation of prognostic factors. J Natl Cancer Inst 86(11):829–835CrossRefPubMed Altman DG, Lausen B, Sauerbrei W, Schumacher M (1994) Dangers of using “optimal” cutpoints in the evaluation of prognostic factors. J Natl Cancer Inst 86(11):829–835CrossRefPubMed
67.
Zurück zum Zitat Mazumdar M, Glassman JR (2000) Categorizing a prognostic variable: review of methods, code for easy implementation and applications to decision-making about cancer treatments. Stat Med 19(1):113–132CrossRefPubMed Mazumdar M, Glassman JR (2000) Categorizing a prognostic variable: review of methods, code for easy implementation and applications to decision-making about cancer treatments. Stat Med 19(1):113–132CrossRefPubMed
68.
Zurück zum Zitat Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pagès C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoué F, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH, Pagès F (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313(5795):1960–1964CrossRefPubMed Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pagès C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoué F, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH, Pagès F (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313(5795):1960–1964CrossRefPubMed
69.
Zurück zum Zitat Liu K, Yang K, Wu B, Chen H, Chen X, Chen X, Jiang L, Ye F, He D, Lu Z, Xue L, Zhang W, Li Q, Zhou Z, Mo X, Hu J (2015) Tumor-infiltrating immune cells are associated with prognosis of gastric cancer. Medicine (Baltimore) 94(39):e1631CrossRef Liu K, Yang K, Wu B, Chen H, Chen X, Chen X, Jiang L, Ye F, He D, Lu Z, Xue L, Zhang W, Li Q, Zhou Z, Mo X, Hu J (2015) Tumor-infiltrating immune cells are associated with prognosis of gastric cancer. Medicine (Baltimore) 94(39):e1631CrossRef
Metadaten
Titel
Clinicopathologic implications of CD8+/Foxp3+ ratio and miR-574-3p/PD-L1 axis in spinal chordoma patients
verfasst von
Ming-Xiang Zou
Ke-Miao Guo
Guo-Hua Lv
Wei Huang
Jing Li
Xiao-Bin Wang
Yi Jiang
Xiao-Ling She
Publikationsdatum
20.10.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
Cancer Immunology, Immunotherapy / Ausgabe 2/2018
Print ISSN: 0340-7004
Elektronische ISSN: 1432-0851
DOI
https://doi.org/10.1007/s00262-017-2080-1

Weitere Artikel der Ausgabe 2/2018

Cancer Immunology, Immunotherapy 2/2018 Zur Ausgabe

Update Onkologie

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