Pro-inflammatory chemokine-chemokine receptor interactions within the Ewing sarcoma microenvironment determine CD8+ T-lymphocyte infiltration and affect tumour progression

Journal of Pathology

Volumn 223, Issue 3, 2011, Pages 347-357

  Berghuis, Dagmar ^a   Santos, Susy J ^a   Baelde, Hans J ^a   Taminiau, Antonie H M ^a   Maarten Egeler, R ^a   Schilham, Marco W ^a   Hogendoorn, Pancras C W ^a   Lankester, Arjan C ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Bone soft tissue tumour; Chemokines; Ewing sarcoma; Flow cytometry; Immunotherapy; Infiltrating T lymphocytes; Multicolour immunohistochemistry; Patient prognosis; Quantitative PCR; Tumour microenvironment

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR3; CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR3; CUTANEOUS T CELL ATTRACTING CHEMOKINE; CXCL1 CHEMOKINE; CXCL13 CHEMOKINE; CXCL3 CHEMOKINE; CXCL9 CHEMOKINE; EOTAXIN; EOTAXIN 3; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 3; RANTES; SECONDARY LYMPHOID TISSUE CHEMOKINE;

ADAPTIVE IMMUNITY; ARTICLE; CANCER GROWTH; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CELL MIGRATION; CELL SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; EWING SARCOMA; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; TUMOR MICROENVIRONMENT;

ADOLESCENT; ADULT; BONE NEOPLASMS; CD8-POSITIVE T-LYMPHOCYTES; CHILD; CHILD, PRESCHOOL; DISEASE PROGRESSION; GENE EXPRESSION PROFILING; HUMANS; INFLAMMATION MEDIATORS; INTERFERON-GAMMA; LYMPHOCYTES, TUMOR-INFILTRATING; NEOPLASM PROTEINS; POLYMERASE CHAIN REACTION; RECEPTORS, CCR5; RECEPTORS, CHEMOKINE; RECEPTORS, CXCR3; SARCOMA, EWING'S; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT;

EID: 78650618910     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2819     Document Type: Article

References (51)

1. Ushigome S, Machinami R, Sorensen PH,. Ewing sarcoma/primitive neuroectodermal tumour. In World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of Soft Tissue and Bone, Fletcher CDM, Unni KK, Mertens F, (eds). IARC Press: Lyon, 2002; 298-300.
2. Riggi N, Cironi L, Suva ML, et al., Sarcomas: genetics, signalling, and cellular origins. Part 1: the fellowship of TET. J Pathol 2007; 213: 4-20. (Pubitemid 47354561)
3. Szuhai K, Ijszenga M, de Jong D, et al., The NFATc2 gene is involved in a novel cloned translocation in a Ewing sarcoma variant that couples its function in immunology to oncology. Clin Cancer Res 2009; 15: 2259-2268.
4. Juergens C, Weston C, Lewis I, et al., Safety assessment of intensive induction with vincristine, ifosfamide, doxorubicin, and etoposide (VIDE) in the treatment of Ewing tumors in the EURO-E.W.I.N.G. 99 clinical trial. Pediatr Blood Cancer 2006; 47: 22-29. (Pubitemid 43787904)
5. Le Deley MC, Delattre O, Schaefer KL, et al., Impact of EWS-ETS fusion type on disease progression in Ewing's sarcoma/peripheral primitive neuroectodermal tumor: prospective results from the cooperative Euro-E.W.I.N.G. 99 trial. J Clin Oncol 2010; 28: 1982-1988.
6. van Doorninck JA, Ji L, Schaub B, et al., Current treatment protocols have eliminated the prognostic advantage of type 1 fusions in Ewing sarcoma: a report from the Children's Oncology Group. J Clin Oncol 2010; 28: 1989-1994.
7. Lorusso G, Ruegg C,. The tumor microenvironment and its contribution to tumor evolution toward metastasis. Histochem Cell Biol 2008; 130: 1091-1103.
8. Mueller MM, Fusenig NE, Friends or foes - bipolar effects of the tumour stroma in cancer. Nature Rev Cancer 2004; 4: 839-849.
9. de Visser KE,. Spontaneous immune responses to sporadic tumors: tumor-promoting, tumor-protective or both? Cancer Immunol Immunother 2008; 57: 1531-1539.
10. Smyth MJ, Dunn GP, Schreiber RD,. Cancer immunosurveillance and immunoediting: the roles of immunity in suppressing tumor development and shaping tumor immunogenicity. Adv Immunol 2006; 90: 1-50.
11. Galon J, Costes A, Sanchez-Cabo F, et al., Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006; 313: 1960-1964. (Pubitemid 44498003)
12. Sato E, Olson SH, Ahn J, et al., Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8 + /regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci U S A 2005; 102: 18538-18543. (Pubitemid 43011261)
13. Clemente CG, Mihm MC Jr, Bufalino R, et al., Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer 1996; 77: 1303-1310. (Pubitemid 26102328)
14. Mantovani A, Allavena P, Sozzani S, et al., Chemokines in the recruitment and shaping of the leukocyte infiltrate of tumors. Semin Cancer Biol 2004; 14: 155-160. (Pubitemid 38586740)
15. Ohtani H, Jin Z, Takegawa S, et al., Abundant expression of CXCL9 (MIG) by stromal cells that include dendritic cells and accumulation of CXCR3+ T cells in lymphocyte-rich gastric carcinoma. J Pathol 2009; 217: 21-31.
16. Harlin H, Meng Y, Peterson AC, et al., Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res 2009; 69: 3077-3085.
17. Berghuis D, de Hooge AS, Santos SJ, et al., Reduced human leukocyte antigen expression in advanced-stage Ewing sarcoma: implications for immune recognition. J Pathol 2009; 218: 222-231.
18. Meyer-Wentrup F, Richter G, Burdach S,. Identification of an immunogenic EWS-FLI1-derived HLA-DR-restricted T helper cell epitope. Pediatr Hematol Oncol 2005; 22: 297-308. (Pubitemid 40770481)
19. Liu XF, Helman LJ, Yeung C, et al., XAGE-1, a new gene that is frequently expressed in Ewing's sarcoma. Cancer Res 2000; 60: 4752-4755.
20. de Hooge ASK, Berghuis D, Santos SJ, et al., Expression of cellular FLICE inhibitory protein, caspase-8, and protease inhibitor-9 in Ewing sarcoma and implications for susceptibility to cytotoxic pathways. Clin Cancer Res 2007; 13: 206-214. (Pubitemid 46121870)
21. Verhoeven DH, de Hooge AS, Mooiman EC, et al., NK cells recognize and lyse Ewing sarcoma cells through NKG2D and DNAM-1 receptor dependent pathways. Mol Immunol 2008; 45: 3917-3925.
22. Cho D, Shook DR, Shimasaki N, et al., Cytotoxicity of activated natural killer cells against pediatric solid tumors. Clin Cancer Res 2010; 15: 3901-3909.
23. Staege MS, Hansen G, Baersch G, et al., Functional and molecular characterization of interleukin-2 transgenic Ewing tumor cells for in vivo immunotherapy. Pediatr Blood Cancer 2004; 43: 23-34. (Pubitemid 38738268)
24. Zhang H, Merchant MS, Chua KS, et al., Tumor expression of 4-1BB ligand sustains tumor lytic T cells. Cancer Biol Ther 2003; 2: 579-586.
25. De Angulo G, Hernandez M, Morales-Arias J, et al., Early lymphocyte recovery as a prognostic indicator for high-risk Ewing sarcoma. J Pediatr Hematol Oncol 2007; 29: 48-52. (Pubitemid 46143025)
26. Dagher R, Long LM, Read EJ, et al., Pilot trial of tumor-specific peptide vaccination and continuous infusion interleukin-2 in patients with recurrent Ewing sarcoma and alveolar rhabdomyosarcoma: an inter-institute NIH study. Med Pediatr Oncol 2002; 38: 158-164. (Pubitemid 34171069)
27. Mackall CL, Rhee EH, Read EJ, et al., A pilot study of consolidative immunotherapy in patients with high-risk pediatric sarcomas. Clin Cancer Res 2008; 14: 4850-4858.
28. Suminoe A, Matsuzaki A, Hattori H, et al., Immunotherapy with autologous dendritic cells and tumor antigens for children with refractory malignant solid tumors. Pediatr Transplant 2009; 13: 746-753.
29. Vakkila J, Jaffe R, Michelow M, et al., Pediatric cancers are infiltrated predominantly by macrophages and contain a paucity of dendritic cells: a major nosologic difference with adult tumors. Clin Cancer Res 2006; 12: 2049-2054.
30. Theoleyre S, Mori K, Cherrier B, et al., Phenotypic and functional analysis of lymphocytes infiltrating osteolytic tumors: use as a possible therapeutic approach of osteosarcoma. BMC Cancer 2005; 5 (123.): 123. (Pubitemid 41461012)
31. Ottaviano L, Schaefer KL, Gajewski M, et al., Molecular characterization of commonly used cell lines for bone tumor research: a trans-European EuroBoNet effort. Genes Chromosomes Cancer 2010; 49: 40-51.
32. Szuhai K, Ijszenga M, Tanke HJ, et al., Molecular cytogenetic characterization of four previously established and two newly established Ewing sarcoma cell lines. Cancer Genet Cytogenet 2006; 166: 173-179.
33. van Vlierberghe RL, Sandel MH, Prins FA, et al., Four-color staining combining fluorescence and brightfield microscopy for simultaneous immune cell phenotyping and localization in tumor tissue sections. Microsc Res Tech 2005; 67: 15-21.
34. Abramoff MD, Magelhaes PJ, Ram SJ,. Image processing with ImageJ. Biophotonics Int 2004; 11: 36-42.
35. Vandesompele J, De Preter K, Pattyn F, et al., Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002; 3:RESEARCH0034.
36. Eisen MB, Spellman PT, Brown PO, et al., Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 1998; 95: 14863-14868.
37. Page RD,. Visualizing phylogenetic trees using TreeView. Curr Protoc Bioinformatics 2002; Chapter 6: Unit 6.2.
38. Rivoltini L, Arienti F, Orazi A, et al., Phenotypic and functional analysis of lymphocytes infiltrating paediatric tumours, with a characterization of the tumour phenotype. Cancer Immunol Immunother 1992; 34: 241-251.
39. Kawai O, Ishii G, Kubota K, et al., Predominant infiltration of macrophages and CD8(+) T cells in cancer nests is a significant predictor of survival in stage IV nonsmall cell lung cancer. Cancer 2008; 113: 1387-1395.
40. Dunn GP, Koebel CM, Schreiber RD,. Interferons, immunity and cancer immunoediting. Nature Rev Immunol 2006; 6: 836-848.
41. Ikeda H, Old LJ, Schreiber RD,. The roles of IFN gamma in protection against tumor development and cancer immunoediting. Cytokine Growth Factor Rev 2002; 13: 95-109. (Pubitemid 34229385)
42. Wenzel J, Tomiuk S, Zahn S, et al., Transcriptional profiling identifies an interferon-associated host immune response in invasive squamous cell carcinoma of the skin. Int J Cancer 2008; 123: 2605-2615.
43. Lissat A, Vraetz T, Tsokos M, et al., Interferon-gamma sensitizes resistant Ewing's sarcoma cells to tumor necrosis factor apoptosis-inducing ligand-induced apoptosis by up-regulation of caspase-8 without altering chemosensitivity. Am J Pathol 2007; 170: 1917-1930. (Pubitemid 47339266)
44. Gortz A, Nibbs RJ, McLean P, et al., The chemokine ESkine/CCL27 displays novel modes of intracrine and paracrine function. J Immunol 2002; 169: 1387-1394. (Pubitemid 34809183)
45. Torres R, Ramirez JC,. A chemokine targets the nucleus: Cxcl12-gamma isoform localizes to the nucleolus in adult mouse heart. PLoS One 2009; 4: e7570.
46. Iijima W, Ohtani H, Nakayama T, et al., Infiltrating CD8+ T cells in oral lichen planus predominantly express CCR5 and CXCR3 and carry respective chemokine ligands RANTES/CCL5 and IP-10/CXCL10 in their cytolytic granules: a potential self-recruiting mechanism. Am J Pathol 2003; 163: 261-268. (Pubitemid 36759610)
47. Gottlieb AB, Luster AD, Posnett DN, et al., Detection of a gamma interferon-induced protein IP-10 in psoriatic plaques. J Exp Med 1988; 168: 941-948.
48. Ganss R, Ryschich E, Klar E, et al., Combination of T-cell therapy and trigger of inflammation induces remodeling of the vasculature and tumor eradication. Cancer Res 2002; 62: 1462-1470. (Pubitemid 34407808)
49. Lugade AA, Sorensen EW, Gerber SA, et al., Radiation-induced IFN-gamma production within the tumor microenvironment influences antitumor immunity. J Immunol 2008; 180: 3132-3139.
50. Zitvogel L, Apetoh L, Ghiringhelli F, et al., Immunological aspects of cancer chemotherapy. Nature Rev Immunol 2008; 8: 59-73.
51. Llombart-Bosch A, Carda C, Peydro-Olaya A, et al., Soft tissue Ewing's sarcoma. Characterization in established cultures and xenografts with evidence of a neuroectodermic phenotype. Cancer 1990; 66: 2589-2601.