Molecular characterization of clear cell renal cell carcinoma identifies CSNK2A1, SPP1 and DEFB1 as promising novel prognostic markers

APMIS

Volumn 124, Issue 5, 2016, Pages 372-383

  Rabjerg, Maj ^a   Bjerregaard, Henriette ^b   Halekoh, Ulrich ^c   Jensen, Boye L ^d   Walter, Steen ^a   Marcussen, Niels ^a  

^a ODENSE UNIVERSITY HOSPITAL   (Denmark)

^b NOVO NORDISK A S   (Denmark)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

CcRCC; CSNK2A1; DEFB1; Prognosis; SPP1; Taqman Array

Indexed keywords

BEVACIZUMAB; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MESSENGER RNA; PAZOPANIB; PROTEIN TYROSINE KINASE INHIBITOR; SORAFENIB; SUNITINIB; TUMOR MARKER; VASCULOTROPIN INHIBITOR; BETA DEFENSIN; CASEIN KINASE 2, ALPHA, HUMAN; CASEIN KINASE II; DEFB1 PROTEIN, HUMAN; OSTEOPONTIN; SPP1 PROTEIN, HUMAN;

ADULT; ARTICLE; CANCER PROGNOSIS; CSNK2A1 GENE; DEFB1 GENE; DISEASE SPECIFIC SURVIVAL; FEMALE; FOLLOW UP; GENE; GENE EXPRESSION; GENE PRODUCT; HUMAN; HUMAN TISSUE; KIDNEY CARCINOMA; MAJOR CLINICAL STUDY; MALE; NEPHRECTOMY; OVERALL SURVIVAL; PREDICTOR VARIABLE; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; SPP1 GENE; AGED; BIOSYNTHESIS; CARCINOMA, RENAL CELL; COHORT ANALYSIS; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENETICS; KIDNEY NEOPLASMS; MIDDLE AGED; MOLECULAR GENETICS; PATHOLOGY; PROGNOSIS; SURVIVAL ANALYSIS; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; BETA-DEFENSINS; BIOMARKERS, TUMOR; CARCINOMA, RENAL CELL; CASEIN KINASE II; COHORT STUDIES; FEMALE; FOLLOW-UP STUDIES; GENE EXPRESSION PROFILING; HUMANS; KIDNEY NEOPLASMS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; OSTEOPONTIN; PROGNOSIS; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA; SURVIVAL ANALYSIS;

EID: 84959161032     PISSN: 09034641     EISSN: 16000463     Source Type: Journal    
DOI: 10.1111/apm.12519     Document Type: Article

References (59)

1. Eble JN, Sauter G, Epstein JI, Sesterhenn I. WHO Classification of Tumours: Tumours of the Urinary System and Male Genital Organs. Lyon: IARCPress, 2004: 9-88.
2. Ljungberg B, Bensalah K, Canfield S, Dabestani S, Hofmann F, Hora M, et al. EAU guidelines on renal cell carcinoma: 2014 update. Eur Urol 2015;67:913-24.
3. Chawla SN, Crispen PL, Hanlon AL, Greenberg RE, Chen DY, Uzzo RG. The natural history of observed enhancing renal masses: meta-analysis and review of the world literature. J Urol 2006;175:425-31.
4. Zisman A, Pantuck AJ, Wieder J, Chao DH, Dorey F, Said JW, et al. Risk group assessment and clinical outcome algorithm to predict the natural history of patients with surgically resected renal cell carcinoma. J Clin Oncol 2002;20:4559-66.
5. Grandinetti CA, Goldspiel BR. Sorafenib and sunitinib: novel targeted therapies for renal cell cancer. Pharmacotherapy 2007;27:1125-44.
6. Frank I, Blute ML, Cheville JC, Lohse CM, Weaver AL, Zincke H. An outcome prediction model for patients with clear cell renal cell carcinoma treated with radical nephrectomy based on tumor stage, size, grade and necrosis: the SSIGN score. J Urol 2002;168:2395-400.
7. Delahunt B, McKenney JK, Lohse CM, Leibovich BC, Thompson RH, Boorjian SA, et al. A novel grading system for clear cell renal cell carcinoma incorporating tumor necrosis. Am J Surg Pathol 2013;37:311-22.
8. Varela I, Tarpey P, Raine K, Huang D, Ong CK, Stephens P, et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 2011;469:539-42.
9. Dalgliesh GL, Furge K, Greenman C, Chen L, Bignell G, Butler A, et al. Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes. Nature 2010;463:360-3.
10. Guo G, Gui Y, Gao S, Tang A, Hu X, Huang Y, et al. Frequent mutations of genes encoding ubiquitin-mediated proteolysis pathway components in clear cell renal cell carcinoma. Nat Genet 2012;44:17-9.
11. Moch H, Schraml P, Bubendorf L, Mirlacher M, Kononen J, Gasser T, et al. High-throughput tissue microarray analysis to evaluate genes uncovered by cDNA microarray screening in renal cell carcinoma. Am J Pathol 1999;154:981-6.
12. Young AN, Amin MB, Moreno CS, Lim SD, Cohen C, Petros JA, et al. Expression profiling of renal epithelial neoplasms: a method for tumor classification and discovery of diagnostic molecular markers. Am J Pathol 2001;158:1639-51.
13. Skubitz KM, Skubitz AP. Differential gene expression in renal-cell cancer. J Lab Clin Med 2002;140:52-64.
14. Yamazaki K, Sakamoto M, Ohta T, Kanai Y, Ohki M, Hirohashi S. Overexpression of KIT in chromophobe renal cell carcinoma. Oncogene 2003;22:847-52.
15. Takahashi M, Yang XJ, Sugimura J, Backdahl J, Tretiakova M, Qian CN, et al. Molecular subclassification of kidney tumors and the discovery of new diagnostic markers. Oncogene 2003;22:6810-8.
16. Jones J, Otu H, Spentzos D, Kolia S, Inan M, Beecken WD, et al. Gene signatures of progression and metastasis in renal cell cancer. Clin Cancer Res 2005;11:5730-9.
17. Schuetz AN, Yin-Goen Q, Amin MB, Moreno CS, Cohen C, Hornsby CD, et al. Molecular classification of renal tumors by gene expression profiling. J Mol Diagn 2005;7:206-18.
18. Yao M, Tabuchi H, Nagashima Y, Baba M, Nakaigawa N, Ishiguro H, et al. Gene expression analysis of renal carcinoma: adipose differentiation-related protein as a potential diagnostic and prognostic biomarker for clear-cell renal carcinoma. J Pathol 2005;205:377-87.
19. Sultmann H, von Heydebreck A, Huber W, Kuner R, Buness A, Vogt M, et al. Gene expression in kidney cancer is associated with cytogenetic abnormalities, metastasis formation, and patient survival. Clin Cancer Res 2005;11(2 Pt 1):646-55.
20. Bjerregaard H. Quantitative real-time PCR TaqMan low density array in renal cell carcinoma. Potential tecnique in Subtyping and Prognosis. [Master]: Odense: University of Southern Denmark, 2009.
21. Rabjerg M, Olivan-Viguera A, Hansen LK, Jensen L, Sevelsted-Moller L, Walter S, et al. High expression of KCa3.1 in patients with clear cell renal carcinoma predicts high metastatic risk and poor survival. PLoS ONE 2015;10:e0122992.
22. GeNorm. http://medgen.ugent.be/~jvdesomp/genorm/ Ref type: Data File 2013.
23. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002;3:RESEARCH0034.
24. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 2007;8:R19.
25. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001;29:e45.
26. Lausen B, Schumacher M. Maximally selected rank statistics. Biometrics 1992;48:73-85.
27. Hothorn T, Lausen B. On the exact distribution of maximally selected rank statistics. Comput Stat Data Anal 2003;43:121-37.
28. Guerra B, Issinger OG. Protein kinase CK2 and its role in cellular proliferation, development and pathology. Electrophoresis 1999;20:391-408.
29. Tawfic S, Yu S, Wang H, Faust R, Davis A, Ahmed K. Protein kinase CK2 signal in neoplasia. Histol Histopathol 2001;16:573-82.
30. Bibby AC, Litchfield DW. The multiple personalities of the regulatory subunit of protein kinase CK2: CK2 dependent and CK2 independent roles reveal a secret identity for CK2beta. Int J Biol Sci 2005;1:67-79.
31. Stalter G, Siemer S, Becht E, Ziegler M, Remberger K, Issinger OG. Asymmetric expression of protein kinase CK2 subunits in human kidney tumors. Biochem Biophys Res Commun 1994;202:141-7.
32. Gang X, Wang Y, Wang Y, Zhao Y, Ding L, Zhao J, et al. Suppression of casein kinase 2 sensitizes tumor cells to antitumor TRAIL therapy by regulating the phosphorylation and localization of p65 in prostate cancer. Oncol Rep 2015;34:1599-604.
33. Laramas M, Pasquier D, Filhol O, Ringeisen F, Descotes JL, Cochet C. Nuclear localization of protein kinase CK2 catalytic subunit (CK2alpha) is associated with poor prognostic factors in human prostate cancer. Eur J Cancer 2007;43:928-34.
34. Agarwal M, Nitta RT, Li G. Casein Kinase 2: a novel player in glioblastoma therapy and cancer stem cells. J Mol Genet Med 2013;8:pii: 1000094.
35. Bae JS, Park SH, Kim KM, Kwon KS, Kim CY, Lee HK, et al. CK2alpha phosphorylates DBC1 and is involved in the progression of gastric carcinoma and predicts poor survival of gastric carcinoma patients. Int J Cancer 2015;136:797-809.
36. Kim JS, Eom JI, Cheong JW, Choi AJ, Lee JK, Yang WI, et al. Protein kinase CK2alpha as an unfavorable prognostic marker and novel therapeutic target in acute myeloid leukemia. Clin Cancer Res 2007;13:1019-28.
37. Zou J, Luo H, Zeng Q, Dong Z, Wu D, Liu L. Protein kinase CK2alpha is overexpressed in colorectal cancer and modulates cell proliferation and invasion via regulating EMT-related genes. J Transl Med 2011;9:97.
38. Hessenauer A, Schneider CC, Gotz C, Montenarh M. CK2 inhibition induces apoptosis via the ER stress response. Cell Signal 2011;23:145-51.
39. Pierre F, Chua PC, O'Brien SE, Siddiqui-Jain A, Bourbon P, Haddach M, et al. Discovery and SAR of 5-(3-chlorophenylamino)benzo[c][2, 6]naphthyridine-8-carboxylic acid (CX-4945), the first clinical stage inhibitor of protein kinase CK2 for the treatment of cancer. J Med Chem 2011;54:635-54.
40. Kim J, Kim SH. Druggability of the CK2 inhibitor CX-4945 as an anticancer drug and beyond. Arch Pharm Res 2012;35:1293-6.
41. Filhol O, Nueda A, Martel V, Gerber-Scokaert D, Benitez MJ, Souchier C, et al. Live-cell fluorescence imaging reveals the dynamics of protein kinase CK2 individual subunits. Mol Cell Biol 2003;23:975-87.
42. Rodan GA. Osteopontin overview. Ann N Y Acad Sci 1995;760:1-5.
43. Rittling SR, Chambers AF. Role of osteopontin in tumour progression. Br J Cancer 2004;90:1877-81.
44. Wai PY, Kuo PC. The role of Osteopontin in tumor metastasis. J Surg Res 2004;121:228-41.
45. Shimada Y, Watanabe G, Kawamura J, Soma T, Okabe M, Ito T, et al. Clinical significance of osteopontin in esophageal squamous cell carcinoma: comparison with common tumor markers. Oncology 2005;68:285-92.
46. Liu H, Chen A, Guo F, Yuan L. Influence of osteopontin short hairpin RNA on the proliferation and invasion of human renal cancer cells. J Huazhong Univ Sci Technolog Med Sci 2010;30:61-8.
47. Matusan K, Dordevic G, Stipic D, Mozetic V, Lucin K. Osteopontin expression correlates with prognostic variables and survival in clear cell renal cell carcinoma. J Surg Oncol 2006;94:325-31.
48. Sun CQ, Arnold R, Fernandez-Golarz C, Parrish AB, Almekinder T, He J, et al. Human beta-defensin-1, a potential chromosome 8p tumor suppressor: control of transcription and induction of apoptosis in renal cell carcinoma. Cancer Res 2006;66:8542-9.
49. Na X, Wu G, Ryan CK, Schoen SR, di'Santagnese PA, Messing EM. Overproduction of vascular endothelial growth factor related to von Hippel-Lindau tumor suppressor gene mutations and hypoxia-inducible factor-1 alpha expression in renal cell carcinomas. J Urol 2003;170(2 Pt 1):588-92.
50. Jacobsen J, Grankvist K, Rasmuson T, Bergh A, Landberg G, Ljungberg B. Expression of vascular endothelial growth factor protein in human renal cell carcinoma. BJU Int 2004;93:297-302.
51. Guethbrandsdottir G, Hjelle KM, Frugard J, Bostad L, Aarstad HJ, Beisland C. Preoperative high levels of serum vascular endothelial growth factor are a prognostic marker for poor outcome after surgical treatment of renal cell carcinoma. Scand J Urol 2015;49:388-94.
52. Vano YA, Tartour E, Fournier LS, Beuselinck B, Mejean A, Oudard S. Prognostic factors in patients with advanced renal cell carcinoma treated with VEGF-targeted agents. Expert Rev Anticancer Ther 2014;14:523-42.
53. Rini BI, Michaelson MD, Rosenberg JE, Bukowski RM, Sosman JA, Stadler WM, et al. Antitumor activity and biomarker analysis of sunitinib in patients with bevacizumab-refractory metastatic renal cell carcinoma. J Clin Oncol 2008;26:3743-8.
54. Escudier B, Eisen T, Stadler WM, Szczylik C, Oudard S, Staehler M, et al. Sorafenib for treatment of renal cell carcinoma: final efficacy and safety results of the phase III treatment approaches in renal cancer global evaluation trial. J Clin Oncol 2009;27:3312-8.
55. Eng L, Azad AK, Habbous S, Pang V, Xu W, Maitland-van der Zee AH, et al. Vascular endothelial growth factor pathway polymorphisms as prognostic and pharmacogenetic factors in cancer: a systematic review and meta-analysis. Clin Cancer Res 2012;18:4526-37.
56. Ma N, Li LW, Cheng JL. Predictive value of vascular endothelial growth factor polymorphisms on the clinical outcome of renal cell carcinoma patients. Oncol Lett 2015;9:651-6.
57. Motzer RJ, Hutson TE, Hudes GR, Figlin RA, Martini JF, English PA, et al. Investigation of novel circulating proteins, germ line single-nucleotide polymorphisms, and molecular tumor markers as potential efficacy biomarkers of first-line sunitinib therapy for advanced renal cell carcinoma. Cancer Chemother Pharmacol 2014;74:739-50.
58. Pena-Llopis S, Vega-Rubin-de-Celis S, Liao A, Leng N, Pavia-Jimenez A, Wang S, et al. BAP1 loss defines a new class of renal cell carcinoma. Nat Genet 2012;44:751-9.
59. Hakimi AA, Ostrovnaya I, Reva B, Schultz N, Chen YB, Gonen M, et al. Adverse outcomes in clear cell renal cell carcinoma with mutations of 3p21 epigenetic regulators BAP1 and SETD2: a report by MSKCC and the KIRC TCGA research network. Clin Cancer Res 2013;19:3259-67.