An overview of renal cell cancer: Pathology and genetics

Seminars in Cancer Biology

Volumn 23, Issue 1, 2013, Pages 3-9

  Moch, Holger ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

Dialysis associated carcinoma; Molecular pathology; Translocation renal cancer; VHL gene; WHO classification

Indexed keywords

CYTOKERATIN;

CANCER CLASSIFICATION; CANCER GENETICS; CANCER PROGNOSIS; CARCINOGENESIS; CHROMOSOME DELETION; CHROMOSOME LOSS; CHROMOSOME TRANSLOCATION; CHROMOSOME XP; CLINICAL FEATURE; CYTOGENETICS; DIAGNOSTIC TEST; DIFFERENTIAL DIAGNOSIS; DISTANT METASTASIS; EPITHELIUM TUMOR; FAMILIAL CANCER; FLUORESCENCE IN SITU HYBRIDIZATION; GENE FUSION; GENE MUTATION; GENETIC ANALYSIS; GENETIC SELECTION; HISTOLOGY; HISTOPATHOLOGY; HUMAN; KARYOTYPING; KIDNEY CARCINOMA; KIDNEY COLLECTING TUBULE; KIDNEY EPITHELIUM; KIDNEY TUBULE EPITHELIUM; KIDNEY TUMOR; LIPID COMPOSITION; LIVER METASTASIS; MALIGNANT TRANSFORMATION; NEUROBLASTOMA; ONCOCYTOMA; PAPILLARY CARCINOMA; PSAMMOMA BODY; REVIEW; SARCOMATOID CARCINOMA; SOMATIC MUTATION; SPINDLE CELL CARCINOMA; TUMOR SUPPRESSOR GENE; TUMOR VOLUME; WORLD HEALTH ORGANIZATION;

CARCINOMA, RENAL CELL; CHROMOSOME ABERRATIONS; HUMANS; KIDNEY NEOPLASMS; PROGNOSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84873093984     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2012.06.006     Document Type: Review

References (100)

1. Kovacs G., Akhtar M., Beckwith B.J., Bugert P., Cooper C.S., Delahunt B., et al. The Heidelberg classification of renal cell tumours. Journal of Pathology 1997, 183:131-133.
2. Algaba F., Akaza H., Lopez-Beltran A., Martignoni G., Moch H., Montironi R., et al. Pathology of renal cancer. 1st EAU-ICD international consultation on kidney cancer 2010, 47-72. Z. Kirkali, P. Mulders (Eds.).
3. Eble J., Sauter G., Epstein J., Sesterhenn I. Tumours of the kidney. Tumours of the urinary system and male genital organs. WHO classification of tumours 2004, IARC Press, Lyon.
4. Cheville J.C., Lohse C.M., Zincke H., Weaver A.L., Blute M.L. Comparisons of outcome and prognostic features among histologic subtypes of renal cell carcinoma. American Journal of Surgical Pathology 2003, 27:612-624.
5. Moch H., Gasser T., Amin M.B., Torhorst J., Sauter G., Mihatsch M.J. Prognostic utility of the recently recommended histologic classification and revised TNM staging system of renal cell carcinoma: a Swiss experience with 588 tumors. Cancer 2000, 89:604-614.
6. Motzer R.J., Bukowski R.M. Targeted therapy for metastatic renal cell carcinoma. Journal of Clinical Oncology 2006, 24:5601-5608.
7. Grignon D., Eble J., Bonsib S., Moch H. Clear Cell Renal Cell Carcinoma. World Health Organization classification of tumours. Pathology and genetics of tumours of the urinary system and male genital organs 2004, 23-25. IARC Press, Lyon. J. Eble, G. Sauter, J. Epstein, A. et (Eds.).
8. Eble J.N., Bonsib S.M. Extensively cystic renal neoplasms: cystic nephroma, cystic partially differentiated nephroblastoma, multilocular cystic renal cell carcinoma, and cystic hamartoma of renal pelvis. Seminars in Diagnostic Pathology 1998, 15:2-20.
9. de Peralta-Venturina M., Moch H., Amin M., Tamboli P., Hailemariam S., Mihatsch M., et al. Sarcomatoid differentiation in renal cell carcinoma: a study of 101 cases. American Journal of Surgical Pathology 2001, 25:275-284.
10. Sconocchia G., Spagnoli G.C., Del Principe D., Ferrone S., Anselmi M., Wongsena W., et al. Defective infiltration of natural killer cells in MICA/B-positive renal cell carcinoma involves beta(2)-integrin-mediated interaction. Neoplasia 2009, 11:662-671.
11. Morra L., Rechsteiner M., Casagrande S., Duc Luu V., Santimaria R., Diener P.A., et al. Relevance of periostin splice variants in renal cell carcinoma. American Journal of Pathology 2011, 179:1513-1521.
12. Kovacs G. Papillary renal cell carcinoma. A morphologic and cytogenetic study of 11 cases. American Journal of Pathology 1989, 134:27-34.
13. Mancilla-Jimenez R., Stanley R.J., Blath R.A. Papillary renal cell carcinoma. Cancer 1976, 38:2469-2480.
14. Amin M., Corless C., Renshaaw A., Tickoo S., Kubus J., Schultz D. Papillary (chromophil) renal cell carcinoma: histomorphologic characteristics and evaluation of conventional pathologic prognostic parameters in 62 cases. American Journal of Surgical Pathology 1997, 21:621-635.
15. Delahunt B., Eble J. Papillary renal cell carcinoma: a clinicopathologic and immunohistochemical study of 105 tumors. Modern Pathology 1997, 10:537-544.
16. Hes O., Brunelli M., Michal M., Cossu Rocca P., Hora M., Chilosi M., et al. Oncocytic papillary renal cell carcinoma: a clinicopathologic, immunohistochemical, ultrastructural, and interphase cytogenetic study of 12 cases. Annals of diagnostic pathology 2006, 10:133-139.
17. Storkel S., Steart P.V., Drenckhahn D., Thoenes W. The human chromophobe cell renal carcinoma: its probable relation to intercalated cells of the collecting duct. Virchows Archiv. B. Cell Pathology 1989, 56:237-245.
18. Thoenes W., Störkel S., Rumpelt H., Moll R., Baum H., Werner S. Chromophobe cell renal carcinoma and its variants-a report on 32 cases. Journal of Pathology 1988, 155:277-287.
19. Akhtar M., Tulbah A., Kardar A.H., Ali M.A. Sarcomatoid renal cell carcinoma: the chromophobe connection. American Journal of Surgical Pathology 1997, 21:1188-1195.
20. Renshaw A.A., Richie J.P. Subtypes of renal cell carcinoma. Different onset and sites of metastatic disease. American Journal of Clinical Pathology 1999, 111:539-543.
21. Amin M.B., Paner G.P., Alvarado-Cabrero I., Young A.N., Stricker H.J., Lyles R.H., et al. Chromophobe renal cell carcinoma: histomorphologic characteristics and evaluation of conventional pathologic prognostic parameters in 145 cases. American Journal of Surgical Pathology 2008, 32:1822-1834.
22. Amin M.B., Crotty T.B., Tickoo S.K., Farrow G.M. Renal oncocytoma: a reappraisal of morphologic features with clinicopathologic findings in 80 cases. American Journal of Surgical Pathology 1997, 21:1-12.
23. Fleming S., Lewi H.J. Collecting duct carcinoma of the kidney. Histopathology 1986, 10:1131-1141.
24. Kirkali Z., Celebi I., Akan G., Yorukoglu K. Bellini duct (collecting duct) carcinoma of the kidney. Urology 1996, 47:921-923.
25. Srigley J.R., Eble J.N. Collecting duct carcinoma of kidney. Seminars in Diagnostic Pathology 1998, 15:54-67.
26. Avery R.A., Harris J.E., Davis C.J., Borgaonkar D.S., Byrd J.C., Weiss R.B. Renal medullary carcinoma. Cancer 1996, 78:128-132.
27. Davis C.J., Mostofi F.K., Sesterhenn I.A. Renal medullary carcinoma. American Journal of Surgical Pathology 1995, 19:1-11.
28. Argani P., Antonescu C.R., Couturier J., Fournet J.C., Sciot R., Debiec-Rychter M., et al. PRCC-TFE3 renal carcinomas: morphologic, immunohistochemical, ultrastructural, and molecular analysis of an entity associated with the t(X;1)(p11.2;q21). American Journal of Surgical Pathology 2002, 26:1553-1566.
29. Argani P., Antonescu C.R., Illei P.B., Lui M.Y., Timmons C.F., Newbury R., et al. Primary renal neoplasms with the ASPL-TFE3 gene fusion of alveolar soft part sarcoma: a distinctive tumor entity previously included among renal cell carcinomas of children and adolescents. American Journal of Pathology 2001, 159:179-192.
30. Argani P., Lae M., Hutchinson B., Reuter V.E., Collins M.H., Perentesis J., et al. Renal carcinomas with the t(6;11)(p21;q12): clinicopathologic features and demonstration of the specific alpha-TFEB gene fusion by immunohistochemistry, RT-PCR, and DNA PCR. American Journal of Surgical Pathology 2005, 29:230-240.
31. Argani P., Lal P., Hutchinson B., Lui M.Y., Reuter V.E., Ladanyi M. Aberrant nuclear immunoreactivity for TFE3 in neoplasms with TFE3 gene fusions: a sensitive and specific immunohistochemical assay. American Journal of Surgical Pathology 2003, 27:750-761.
32. Bruder E., Passera O., Harms D., Leuschner I., Ladanyi M., Argani P., et al. Morphologic and molecular characterization of renal cell carcinoma in children and young adults. American Journal of Surgical Pathology 2004, 28:1117-1132.
33. Argani P., Olgac S., Tickoo S.K., Goldfischer M., Moch H., Chan D.Y., et al. Xp11 translocation renal cell carcinoma in adults: expanded clinical, pathologic, and genetic spectrum. American Journal of Surgical Pathology 2007, 31:1149-1160.
34. Medeiros L.J., Palmedo G., Krigman H.R., Kovacs G., Beckwith J.B. Oncocytoid renal cell carcinoma after neuroblastoma: a report of four cases of a distinct clinicopathologic entity. American Journal of Surgical Pathology 1999, 23:772-780.
35. Rakozy C., Schmahl G.E., Bogner S., Storkel S. Low-grade tubular-mucinous renal neoplasms: morphologic, immunohistochemical, and genetic features. Modern Pathology 2002, 15:1162-1171.
36. Fine S.W., Argani P., DeMarzo A.M., Delahunt B., Sebo T.J., Reuter V.E., et al. Expanding the histologic spectrum of mucinous tubular and spindle cell carcinoma of the kidney. American Journal of Surgical Pathology 2006, 30:1554-1560.
37. Srigley J.R., Delahunt B. Uncommon and recently described renal carcinomas. Modern Pathology: An Official Journal of the United States and Canadian Academy of Pathology, Inc. 2009, 22(Suppl. 2):S2-S23.
38. Amin M.B., Maclennan G.T., Gupta R., Grignon D., Paraf F., Vieillefond A., et al. Tubulocystic carcinoma of the kidney: clinicopathologic analysis of 31 cases of a distinctive rare subtype of renal cell carcinoma. American Journal of Surgical Pathology 2009, 33:384-392.
39. Amin M.B., Gupta R., Ondrej H., McKenney J.K., Michal M., Young A.N., et al. Primary thyroid-like follicular carcinoma of the kidney: report of 6 cases of a histologically distinctive adult renal epithelial neoplasm. American Journal of Surgical Pathology 2009, 33:393-400.
40. Tickoo S.K., Deperalta-Venturina M.N., Harik L.R., Worcester H.D., Salama M.E., Young A.N., et al. Spectrum of epithelial neoplasms in end-stage renal disease: an experience from 66 tumor-bearing kidneys with emphasis on histologic patterns distinct from those in sporadic adult renal neoplasia. American Journal of Surgical Pathology 2006, 30:141-153.
41. Linehan W.M., Gnarra J.R., Lerman M.I., Latif F., Zbar B. Genetic basis of renal cell cancer. Important Advances in Oncology 1993, 47-70.
42. Neumann H.P., Bender B.U., Berger D.P., Laubenberger J., Schultze-Seemann W., Wetterauer U., et al. Prevalence, morphology and biology of renal cell carcinoma in von Hippel-Lindau disease compared to sporadic renal cell carcinoma. Journal of Urology 1998, 160:1248-1254.
43. Schmidt L., Duh F.M., Chen F., Kishida T., Glenn G., Choyke P., et al. Germline and somatic mutations in the tyrosine kinase domain of the MET proto-oncogene in papillary renal carcinomas. Nature Genetics 1997, 16:68-73.
44. Schmidt L., Junker K., Nakaigawa N., Kinjerski T., Weirich G., Miller M., et al. Novel mutations of the MET proto-oncogene in papillary renal carcinomas. Oncogene 1999, 18:2343-2350.
45. Carpten J.D., Robbins C.M., Villablanca A., Forsberg L., Presciuttini S., Bailey-Wilson J., et al. HRPT2, encoding parafibromin, is mutated in hyperparathyroidism-jaw tumor syndrome. Nature Genetics 2002, 32:676-680.
46. Teh B.T., Farnebo F., Kristoffersson U., Sundelin B., Cardinal J., Axelson R., et al. Autosomal dominant primary hyperparathyroidism and jaw tumor syndrome associated with renal hamartomas and cystic kidney disease: linkage to 1q21-q32 and loss of the wild type allele in renal hamartomas. Journal of Clinical Endocrinology and Metabolism 1996, 81:4204-4211.
47. Nickerson M.L., Warren M.B., Toro J.R., Matrosova V., Glenn G., Turner M.L., et al. Mutations in a novel gene lead to kidney tumors, lung wall defects, and benign tumors of the hair follicle in patients with the Birt-Hogg-Dube syndrome. Cancer Cell 2002, 2:157-164.
48. Zbar B., Alvord W.G., Glenn G., Turner M., Pavlovich C.P., Schmidt L., et al. Risk of renal and colonic neoplasms and spontaneous pneumothorax in the Birt-Hogg-Dube syndrome. Cancer Epidemiology, Biomarkers and Prevention 2002, 11:393-400.
49. Latif F., Tory K., Gnarra J., Yao M., Duh F.M., Orcutt M.L., et al. Identification of the von Hippel-Lindau disease tumor suppressor gene. Science 1993, 260:1317-1320.
50. Gnarra J.R., Tory K., Weng Y., Schmidt L., Wei M.H., Li H., et al. Mutations of the VHL tumour suppressor gene in renal carcinoma. Nature Genetics 1994, 7:85-90.
51. Varela I., Tarpey P., Raine K., Huang D., Ong C.K., Stephens P., et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 2011, 469:539-542.
52. Morrissey C., Martinez A., Zatyka M., Agathanggelou A., Honorio S., Astuti D., et al. Epigenetic inactivation of the RASSF1A 3p21. 3 tumor suppressor gene in both clear cell and papillary renal cell carcinoma. Cancer Research 2001, 61:7277-7281.
53. Lovell M., Lott S.T., Wong P., El-Naggar A., Tucker S., Killary A.M. The genetic locus NRC-1 within chromosome 3p12 mediates tumor suppression in renal cell carcinoma independently of histological type, tumor microenvironment, and VHL mutation. Cancer Research 1999, 59:2182-2189.
54. von Teichman A., Comperat E., Behnke S., Storz M., Moch H., Schraml P. VHL mutations and dysregulation of pVHL- and PTEN-controlled pathways in multilocular cystic renal cell carcinoma. Modern Pathology: An Official Journal of the United States and Canadian Academy of Pathology, Inc. 2011, 24:571-578.
55. Schraml P., Struckmann K., Bednar R., Fu W., Gasser T., Wilber K., et al. CDKNA2A mutation analysis, protein expression, and deletion mapping of chromosome 9p in conventional clear-cell renal carcinomas: evidence for a second tumor suppressor gene proximal to CDKN2A. American Journal of Pathology 2001, 158:593-601.
56. Schraml P., Struckmann K., Hatz F., Sonnet S., Kully C., Gasser T., et al. VHL mutations and their correlation with tumour cell proliferation, microvessel density, and patient prognosis in clear cell renal cell carcinoma. Journal of Pathology 2002, 196:186-193.
57. Schullerus D., Herbers J., Chudek J., Kanamaru H., Kovacs G. Loss of heterozygosity at chromosomes 8p, 9p, and 14q is associated with stage and grade of non-papillary renal cell carcinomas. Journal of Pathology 1997, 183:151-155.
58. Schullerus D., von Knobloch R., Chudek J., Herbers J., Kovacs G. Microsatellite analysis reveals deletion of a large region at chromosome 8p in conventional renal cell carcinoma. International Journal of Cancer 1999, 80:22-24.
59. Bissig H., Richter J., Desper R., Meier V., Schraml P., Schäffer A., et al. Evaluation of the clonal relationship between primary and metastatic renal cell carcinoma by comparative genomic hybridization. American Journal of Pathology 1999, 155:267-274.
60. Mertz K.D., Demichelis F., Sboner A., Hirsch M.S., Dal Cin P., Struckmann K., et al. Association of cytokeratin 7 and 19 expression with genomic stability and favorable prognosis in clear cell renal cell cancer. International Journal of Cancer 2008, 123:569-576.
61. Jiang F., Desper R., Papadimitriou C.H., Schaffer A.A., Kallioniemi O.P., Richter J., et al. Construction of evolutionary tree models for renal cell carcinoma from comparative genomic hybridization data. Cancer Research 2000, 60:6503-6509.
62. Jiang F., Moch H., Richter J., Egenter C., Gasser T., Bubendorf L., et al. Comparative genomic hybridization reveals frequent chromosome 13q and 4q losses in renal carcinomas with sarcomatoid transformation. Journal of Pathology 1998, 185:382-388.
63. Minner S., Rump D., Tennstedt P., Simon R., Burandt E., Terracciano L., et al. Epidermal growth factor receptor protein expression and genomic alterations in renal cell carcinoma. Cancer 2012, 118:1268-1275.
64. Moch H., Presti J.C., Sauter G., Buchholz N., Jordan P., Mihatsch M.J., et al. Genetic aberrations detected by comparative genomic hybridization are associated with clinical outcome in renal cell carcinoma. Cancer Research 1996, 56:27-30.
65. Moch H., Sauter G., Buchholz N., Gasser T.C., Bubendorf L., Waldman F.M., et al. Epidermal growth factor receptor expression is associated with rapid tumor cell proliferation in renal cell carcinoma. Human Pathology 1997, 28:1255-1259.
66. Moch H., Sauter G., Gasser T.C., Bubendorf L., Richter J., Presti J.C., et al. EGF-r gene copy number changes in renal cell carcinoma detected by fluorescence in situ hybridization. Journal of Pathology 1998, 184:424-429.
67. Moch H., Sauter G., Gasser T.C., Buchholz N., Bubendorf L., Richter J., et al. p53 protein expression but not mdm-2 protein expression is associated with rapid tumor cell proliferation and prognosis in renal cell carcinoma. Urological Research 1997, 25(Suppl. 1):S25-S30.
68. Jiang F., Richter J., Schraml P., Bubendorf L., Gasser T., Sauter G., et al. Chromosomal imbalances in papillary renal cell carcinoma: genetic differences between histological subtypes. American Journal of Pathology 1998, 153:1467-1473.
69. Kovacs G., Fuzesi L., Emanual A., Kung H.F. Cytogenetics of papillary renal cell tumors. Genes, Chromosomes and Cancer 1991, 3:249-255.
70. Presti J., Moch H., Reuter V., Huynh D., Waldman F. Chromosome 1 and 14 loss in renal oncocytomas. Genes, Chromosomes and Cancer 1996, 17:199-204.
71. Speicher M., Schoell B., Du Manoir S., Schröck E., Ried T., Cremer T., et al. Specific loss of chromosomes 1, 2, 6, 10, 13, 17, and 21 in chromophobe renal cell carcinomas revealed by comparative genomic hybridization. American Journal of Pathology 1994, 145:356-364.
72. Schoenberg M., Cairns P., Brooks J.D., Marshall F.F., Epstein J.I., Isaacs W.B., et al. Frequent loss of chromosome arms 8p and 13q in collecting duct carcinoma (CDC) of the kidney. Genes, Chromosomes and Cancer 1995, 12:76-80.
73. Srigley J., Kapusta L., Reuter V., Amin M., Grignon D., Eble J., et al. Phenotypic, molecular and ultrastructural studies of a novel low grade renal epithelial neoplasm possibly related to the loop of Henle. Modern Pathology 2002, 15:182A.
74. Yang X.J., Zhou M., Hes O., Shen S., Li R., Lopez J., et al. Tubulocystic carcinoma of the kidney: clinicopathologic and molecular characterization. American Journal of Surgical Pathology 2008, 32:177-187.
75. Zhou M., Yang X.J., Lopez J.I., Shah R.B., Hes O., Shen S.S., et al. Renal tubulocystic carcinoma is closely related to papillary renal cell carcinoma: implications for pathologic classification. American Journal of Surgical Pathology 2009, 33:1840-1849.
76. Gobbo S., Eble J.N., Grignon D.J., Martignoni G., Maclennan G.T., Shah R.B., et al. Clear cell papillary renal cell carcinoma: a distinct histopathologic and molecular genetic entity. American Journal of Surgical Pathology 2008, 32:1239-1245.
77. Thoenes W., Storkel S., Rumpelt H.J. Histopathology and classification of renal cell tumors (adenomas, oncocytomas and carcinomas). The basic cytological and histopathological elements and their use for diagnostics. Pathology, Research and Practice 1986, 181:125-143.
78. Verdorfer I., Culig Z., Hobisch A., Bartsch G., Hittmair A., Duba H.C., et al. Characterisation of a collecting duct carcinoma by cytogenetic analysis and comparative genomic hybridisation. International Journal of Oncology 1998, 13:461-464.
79. Zerban H., Nogueira E., Riedasch G., Bannasch P. Renal oncocytoma: origin from the collecting duct. Virchows Archiv B 1987, 52:375-387.
80. Ortmann M., Vierbuchen M., Fischer R. Renal oncocytoma. II. Lectin and immunohistochemical features indicating an origin from the collecting duct. Virchows Archiv. B. Cell Pathology 1988, 56:175-184.
81. Mandriota S.J., Turner K.J., Davies D.R., Murray P.G., Morgan N.V., Sowter H.M., et al. HIF activation identifies early lesions in VHL kidneys: evidence for site-specific tumor suppressor function in the nephron. Cancer Cell 2002, 1:459-468.
82. Montani M., Heinimann K., von Teichman A., Rudolph T., Perren A., Moch H. VHL-gene deletion in single renal tubular epithelial cells and renal tubular cysts: further evidence for a cyst-dependent progression pathway of clear cell renal carcinoma in von Hippel-Lindau disease. American Journal of Surgical Pathology 2010, 34:806-815.
83. Thoma C.R., Frew I.J., Hoerner C.R., Montani M., Moch H., Krek W. pVHL and GSK3beta are components of a primary cilium-maintenance signalling network. Nature Cell Biology 2007, 9:588-595.
84. Thoma C.R., Frew I.J., Krek W. The VHL tumor suppressor: riding tandem with GSK3beta in primary cilium maintenance. Cell Cycle 2007, 6:1809-1813.
85. Schraml P., Frew I.J., Thoma C.R., Boysen G., Struckmann K., Krek W., et al. Sporadic clear cell renal cell carcinoma but not the papillary type is characterized by severely reduced frequency of primary cilia. Modern Pathology 2009, 22:31-36.
86. Vasei M., Modjtahedi H., Ale-Booyeh O., Mosallaei A., Kaibafzadeh A.M., Shahriari M., et al. Amplification and expression of EGFR and ERBB2 in Wilms tumor. Cancer Genetics and Cytogenetics 2009, 194:88-95.
87. Bonsib S.M. T2 clear cell renal cell carcinoma is a rare entity: a study of 120 clear cell renal cell carcinomas. Journal of Urology 2005, 174:1199-1202. [Discussion 1202].
88. Bonsib S.M. Renal lymphatics, and lymphatic involvement in sinus vein invasive (pT3b) clear cell renal cell carcinoma: a study of 40 cases. Modern Pathology 2006, 19:746-753.
89. Bonsib S.M. Renal veins and venous extension in clear cell renal cell carcinoma. Modern Pathology 2007, 20:44-53.
90. Fuhrman S., Lasky L., Limas C. Prognostic significance of morphologic parameters in renal cell carcinoma. American Journal of Surgical Pathology 1982, 6:655-663.
91. Delahunt B., Sika-Paotonu D., Bethwaite P.B., William Jordan T., Magi-Galluzzi C., Zhou M., et al. Grading of clear cell renal cell carcinoma should be based on nucleolar prominence. American Journal of Surgical Pathology 2011, 35:1134-1139.
92. Delahunt B., Sika-Paotonu D., Bethwaite P.B., McCredie M.R., Martignoni G., Eble J.N., et al. Fuhrman grading is not appropriate for chromophobe renal cell carcinoma. American Journal of Surgical Pathology 2007, 31:957-960.
93. Paner G.P., Amin M.B., Alvarado-Cabrero I., Young A.N., Stricker H.J., Moch H., et al. A novel tumor grading scheme for chromophobe renal cell carcinoma: prognostic utility and comparison with Fuhrman nuclear grade. American Journal of Surgical Pathology 2010, 34:1233-1240.
94. Eichelberg C., Junker K., Ljungberg B., Moch H. Diagnostic and prognostic molecular markers for renal cell carcinoma: a critical appraisal of the current state of research and clinical applicability. European Urology 2009, 55:851-863.
95. Beroukhim R., Brunet J.P., Di Napoli A., Mefiz K.D., Seeley A., Pires M.M., et al. Patterns of gene expression and copy-number alterations in von-Hippel-Lindau disease-associated and sporadic clear cell carcinoma of the kidney. Cancer Research 2009, 69:4674-4681.
96. 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. American Journal of Pathology 1999, 154:981-986.
97. Struckmann K., Mertz K., Steu S., Storz M., Staller P., Krek W., et al. pVHL co-ordinately regulates CXCR4/CXCL12 and MMP2/MMP9 expression in human clear-cell renal cell carcinoma. Journal of Pathology 2008, 214:464-471.
98. Luu V.D., Boysen G., Struckmann K., Casagrande S., von Teichman A., Wild P.J., et al. Loss of VHL and hypoxia provokes PAX2 up-regulation in clear cell renal cell carcinoma. Clinical Cancer Research 2009, 15:3297-3304.
99. Staller P., Sulitkova J., Lisztwan J., Moch H., Oakeley E.J., Krek W. Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL. Nature 2003, 425:307-311.
100. Dahinden C., Ingold B., Wild P., Boysen G., Luu V.D., 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. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2010, 16:88-98.