pVHL/HIF-regulated CD70 expression is associated with infiltration of CD27+ lymphocytes and increased serum levels of soluble CD27 in clear cell renal cell carcinoma

Clinical Cancer Research

Volumn 21, Issue 4, 2015, Pages 889-898

  Ruf, Melanie ^a   Mittmann, Christiane ^a   Nowicka, Anna M ^a   Hartmann, Arndt ^b   Hermanns, Thomas ^a   Poyet, Cedric ^a   Van Den Broek, Maries ^c   Sulser, Tullio ^a   Moch, Holger ^a   Schraml, Peter ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; CD70 ANTIGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; VON HIPPEL LINDAU PROTEIN; CD70 PROTEIN, HUMAN; HIF1A PROTEIN, HUMAN; SMALL INTERFERING RNA; VHL PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; GENE MUTATION; GENETIC ANALYSIS; HIF1ALPHA GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; KIDNEY CARCINOMA; LYMPHOCYTIC INFILTRATION; MAJOR CLINICAL STUDY; METASTASIS; OUTCOME ASSESSMENT; PRIMARY TUMOR; PROMOTER REGION; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TUMOR GENE; UPREGULATION; VHL GENE; BIOSYNTHESIS; BLOOD; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; KIDNEY TUMOR; METABOLISM; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOLUBILITY; T LYMPHOCYTE; TISSUE MICROARRAY; TUMOR ASSOCIATED LEUKOCYTE;

ANTIGENS, CD27; ANTIGENS, CD70; CARCINOMA, RENAL CELL; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; KIDNEY NEOPLASMS; LYMPHOCYTES, TUMOR-INFILTRATING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SOLUBILITY; T-LYMPHOCYTES; TISSUE ARRAY ANALYSIS; TRANSFECTION; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 84923118889     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-1425     Document Type: Article

References (50)

1. Rechsteiner MP, von Teichman A, Nowicka A, Sulser T, Schraml P, Moch H. VHL gene mutations and their effects on hypoxia inducible factor HIFalpha: identification of potential driver and passenger mutations. Cancer Res 2011; 71: 5500-11.
2. Frew IJ, Krek W. pVHL: a multipurpose adaptor protein. Sci Signal 2008; 1: pe30.
3. Shen C, Kaelin WG Jr. The VHL/HIF axis in clear cell renal carcinoma. Semin Cancer Biol 2013; 23: 18-25.
4. Boysen G, Bausch-Fluck D, Thoma CR, Nowicka AM, Stiehl DP, Cima I, et al. Identification and functional characterizationofpVHL-dependentcell surface proteins in renal cell carcinoma. Neoplasia 2012; 14: 535-46.
5. Goodwin RG, Alderson MR, Smith CA, Armitage RJ, VandenBos T, Jerzy R, et al. Molecular and biological characterizationofa ligand for CD27 defines a new family of cytokines with homology to tumor necrosis factor. Cell 1993; 73: 447-56.
6. Watts TH TNF/TNFR family members in costimulation of T cell responses. Annu Rev Immunol 2005; 23: 23-68.
7. Croft M. The role of TNF superfamily members in T-cell function and diseases. Nat Rev Immunol 2009; 9: 271-85.
8. Nolte MA, van Olffen RW, van Gisbergen KP, van Lier RA Timing and tuning of CD27-CD70 interactions: the impact of signal strength in setting the balance between adaptive responses and immunopathology. Immunol Rev 2009; 229: 216-31.
9. Grewal IS CD70 as a therapeutic target in human malignancies. Expert Opin Ther Targets 2008; 12: 341-51.
10. Junker K, Hindermann W, von Eggeling F, Diegmann J, Haessler K, Schubert J. CD70: anew tumor specific biomarker for renal cell carcinoma. J Urol 2005; 173: 2150-3.
11. Adam PJ, Terrett JA, Steers G, Stockwin L, Loader JA, Fletcher GC, et al. CD70 (TNFSF7) is expressed at high prevalence in renal cell carcinomas and is rapidly internalised on antibody binding. Br J Cancer 2006; 95: 298-306.
12. Law CL, Gordon KA, Toki BE, Yamane AK, Hering MA, Cerveny CG, et al. Lymphocyte activation antigen CD70 expressedbyrenalcell carcinomaisa potential therapeutic target for anti-CD70 antibody-drug conjugates. Cancer Res 2006; 66: 2328-37.
13. Jilaveanu LB, Sznol J, Aziz SA, Duchen D, Kluger HM, Camp RL. CD70 expression patterns in renal cell carcinoma. Hum Pathol 2012; 43: 1394-9.
14. Diegmann J, Junker K, Loncarevic IF, Michel S, Schimmel B, von Eggeling F. Immune escape for renal cell carcinoma: CD70 mediates apoptosis in lymphocytes. Neoplasia 2006; 8: 933-8.
15. Wang QJ, Hanada K, Robbins PF, Li YF, Yang JC. Distinctive features of the differentiated phenotype and infiltration of tumor-reactive lymphocytes in clear cell renal cell carcinoma. Cancer Res 2012; 72: 6119-29.
16. Ingold B, Wild PJ, Nocito A, Amin MB, Storz M, Heppner FL, et al. Renal cell carcinoma marker reliably discriminates central nervous system haeman-gioblastoma from brain metastases of renal cell carcinoma. Histopathology 2008; 52: 674-81.
17. Wyler L, Napoli CU, Ingold B, Sulser T, Heikenwalder M, Schraml P, et al. Brain metastasis in renal cancer patients: metastatic pattern, tumour-associated macrophages and chemokine/chemoreceptor expression. Br J Cancer 2014; 110: 686-94.
18. Herrmann E, Trojan L, Becker F, Wulfing C, Schrader AJ, Barth P, et al. Prognostic factors of papillary renal cell carcinoma: results from a multi-institutional series after pathological review. J Urol 2010; 183: 460-6.
19. Dahinden C, Ingold B, Wild P, Boysen G, Luu VD, Montani M, et al. Mining tissue microarray data to uncover combinations of biomarker expression patterns that improve intermediate staging and grading of clear cell renal cell cancer. Clin Cancer Res 2010; 16: 88-98.
20. Beleut M, Zimmermann P, Baudis M, Bruni N, Buhlmann P, Laule O, et al. Integrative genome-wide expression profiling identifies three distinct molecular subgroups of renal cell carcinoma with different patient outcome. BMC Cancer 2012; 12: 310.
21. Staller P, Sulitkova J, Lisztwan J, Moch H, Oakeley EJ, Krek W. Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL. Nature 2003; 425: 307-11.
22. Hergovich A, Lisztwan J, Thoma CR, Wirbelauer C, Barry RE, Krek W. Priming-dependent phosphorylation and regulation of the tumor suppressor pVHL by glycogen synthase kinase 3. Mol Cell Biol 2006; 26: 5784-96.
23. Pawlowski R, Muhl SM, Sulser T, Krek W, Moch H, Schraml P. Loss of PBRM1 expression is associated with renal cell carcinoma progression. Int J Cancer 2013; 132:E11-7.
24. Casagrande S, Ruf M, Rechsteiner M, Morra L, Brun-Schmid S, von Teichman A, et al. The protein tyrosine phosphatase receptor type J is regulated by the pVHL-HIF axis in clear cell renal cell carcinoma. J Pathol 2013; 229: 525-34.
25. Raval RR, Lau KW, Tran MG, Sowter HM, Mandriota SJ, Li JL, et al. Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol Cell Biol 2005; 25: 5675-86.
26. Metzen E, Stiehl DP, Doege K, Marxsen JH, Hellwig-Burgel T, Jelkmann W. Regulation of the prolyl hydroxylase domain protein 2 (phd2/egln-1) gene: identification of a functional hypoxia-responsive element. Biochem J 2005; 387: 711-7.
27. Shen C, Beroukhim R, Schumacher SE, Zhou J, Chang M, Signoretti S, et al. Genetic and functional studies implicateHIF1alphaasa14q kidney cancer suppressor gene. Cancer Discov 2011; 1: 222-35.
28. Wischhusen J, Jung G, Radovanovic I, Beier C, Steinbach JP, Rimner A, et al. Identification of CD70-mediated apoptosis of immune effector cells as a novel immune escape pathway of human glioblastoma. Cancer Res 2002; 62: 2592-9.
29. Hintzen RQ, de Jong R, Hack CE, Chamuleau M, de Vries EF, ten Berge IJ, et al. A soluble form of the human T cell differentiation antigen CD27 is released after triggering of the TCR/CD3 complex. J Immunol 1991; 147: 29-35.
30. Loenen WA, De Vries E, Gravestein LA, Hintzen RQ, Van Lier RA, Borst J. The CD27 membrane receptor, a lymphocyte-specific member of the nerve growth factor receptor family, gives rise to a soluble form by protein processing that does not involve receptor endocytosis. Eur J Immunol 1992; 22: 447-55.
31. Herman JG, Latif F, Weng Y, Lerman MI, Zbar B, Liu S, et al. Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc Natl Acad Sci U S A 1994; 91: 9700-4.
32. Schodel J, Oikonomopoulos S, Ragoussis J, Pugh CW, Ratcliffe PJ, Mole DR. High-resolution genome-wide mapping of HIF-binding sites by ChIPseq. Blood 2011; 117:e207-17.
33. Yu SE, Park SH, Jang YK. Epigenetic silencing of TNFSF7 (CD70) by DNA methylation during progression to breast cancer. Mol Cells 2010; 29: 217-21.
34. Wouters BG, Koritzinsky M. Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat Rev Cancer 2008; 8: 851-64.
35. Hedrich CM, Rauen T. Epigenetic patterns in systemic sclerosis and their contribution to attenuated CD70 signaling cascades. Clin Immunol 2012; 143: 1-3.
36. + T cells. J Autoimmun 2010; 35: 58-69.
37. Fu L, Wang G, Shevchuk MM, Nanus DM, Gudas LJ. Generation of a mouse model of Von Hippel-Lindau kidney disease leading to renal cancers by expression of a constitutively active mutant of HIF1alpha. Cancer Res 2011; 71: 6848-56.
38. Fu L, Wang G, Shevchuk MM, Nanus DM, Gudas LJ. Activation of HIF2alpha in kidney proximal tubule cells causes abnormal glycogen deposition but not tumorigenesis. Cancer Res 2013; 73: 2916-25.
39. Gordan JD, Lal P, Dondeti VR, Letrero R, Parekh KN, Oquendo CE, et al. HIF-alpha effects on c-Myc distinguish two subtypes of sporadic VHL-deficient clear cell renal carcinoma. Cancer Cell 2008; 14: 435-46.
40. Nilsson A, de Milito A, Mowafi F, Winberg G, Bjork O, Wolpert EZ, et al. Expression of CD27-CD70 on early B cell progenitors in the bone marrow: implication for diagnosis and therapy of childhood ALL. Exp Hematol 2005; 33: 1500-7.
41. Yoshino K, Kishibe K, Nagato T, Ueda S, Komabayashi Y, Takahara M, et al. Expression of CD70 in nasal natural killer/T cell lymphoma cell lines and patients; its role for cell proliferation through binding to soluble CD27. BrJ Haematol 2013; 160: 331-42.
42. Huang J, Jochems C, Anderson AM, Talaie T, Jales A, Madan RA, et al. Soluble CD27-pool in humans may contribute to T cell activation and tumor immunity. J Immunol 2013; 190: 6250-8.
43. Chahlavi A, Rayman P, Richmond AL, Biswas K, Zhang R, Vogelbaum M, et al. Glioblastomas induce T-lymphocyte death by two distinct pathways involving gangliosides and CD70. Cancer Res 2005; 65: 5428-38.
44. Aulwurm S, Wischhusen J, Friese M, Borst J, Weller M. Immune stimulatory effects of CD70 override CD70-mediated immune cell apoptosisin rodent glioma models and confer long-lasting antiglioma immunity in vivo. Int J Cancer 2006; 118: 1728-35.
45. Tesselaar K, Arens R, van Schijndel GM, Baars PA, van der Valk MA, Borst J, et al. Lethal Tcell immunodeficiency induced bychronic costimulation via CD27-CD70 interactions. Nat Immunol 2003; 4: 49-54.
46. Thomas LJ, He LZ, Marsh H, Keler T. Targeting human CD27 with an agonist antibody stimulates T-cell activation and antitumor immunity. Oncoimmunology 2014; 3:e27255.
47. Conti A, Santoni M, Amantini C, Burattini L, Berardi R, Santoni G, et al. Progress of Molecular Targeted Therapies for Advanced Renal Cell Carcinoma. Biomed Res Int 2013; 2013: 419176.
48. Jeffrey SC, Burke PJ, Lyon RP, Meyer DW, Sussman D, Anderson M, et al. A potent anti-CD70 antibody-drug conjugate combining a dimeric pyrrolobenzodiazepine drug with site-specific conjugation technology. Bioconjug Chem 2013; 24: 1256-63.
49. + T cell tolerance and permits effective immunity. Immunity 2008; 29: 934-46.
50. + T cell responses by pathogens typically depends on CD70-mediated interactions with dendritic cells. Eur J Immunol 2007; 37: 716-28.