Molecular pathology of chromophobe renal cell carcinoma: A review

International Journal of Urology

Volumn 17, Issue 7, 2010, Pages 592-600

  Yusenko, Maria V ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

chromophobe renal cell carcinoma; diagnosis; electron microscopy; histology; molecular markers

Indexed keywords

CALGRANULIN A; CARBONATE DEHYDRATASE II; CAVEOLIN 1; CD82 ANTIGEN; CLAUDIN 7; CYCLIN D1; CYTOKERATIN 7; EPITHELIAL CELL ADHESION MOLECULE; EPITHELIAL MEMBRANE ANTIGEN; MEMBRANE METALLOENDOPEPTIDASE; TRANSCRIPTION FACTOR PAX2;

ADRENAL CORTEX TUMOR; ANTIBODY SPECIFICITY; CANCER DIAGNOSIS; CELL ULTRASTRUCTURE; CHROMOSOME 10; CHROMOSOME 13; CHROMOSOME 17; CHROMOSOME 2; CHROMOSOME 21; CHROMOSOME LOSS; COMPUTED TOMOGRAPHY SCANNER; DIAGNOSTIC ACCURACY; DIAGNOSTIC IMAGING; DIFFERENTIAL DIAGNOSIS; DIPLOIDY; DNA MICROARRAY; DNA PROBE; ENDOREDUPLICATION; GENE EXPRESSION; GENOME ANALYSIS; HISTOPATHOLOGY; HUMAN; KIDNEY CARCINOMA; MOLECULAR DYNAMICS; MUTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; ONCOCYTOMA; POLYPLOIDY; PRIORITY JOURNAL; PROGNOSIS; REVIEW; TUMOR LOCALIZATION; TUMOR VOLUME; ULTRASOUND;

CARCINOMA, RENAL CELL; HUMANS; KIDNEY NEOPLASMS;

EID: 77953857889     PISSN: 09198172     EISSN: 14422042     Source Type: Journal    
DOI: 10.1111/j.1442-2042.2010.02558.x     Document Type: Review

References (88)

1. Bannasch P, Schacht U, Storch E. Morphogenese und Mikromorphologie epithelialer Nierentumoren bei Nitrosomorpholin-vergifteten Ratten. I. Induktion und Histologie der Tumouren. Z. Krebsforsch. 1974 81: 311 331.
2. Thoenes W, Storkel S, Rumpelt HJ. Human chromophobe cell renal carcinoma. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 1985 48: 207 217.
3. Thoenes W, Störkel S, Rumpelt HJ et al. Chromophobe cell renal carcinoma and its variants: a report on 32 cases. J. Pathol. 1988 155: 277 287.
4. Cindolo L, de la Taille A, Schips L et al. Chromophobe renal cell carcinoma: comprehensive analysis of 104 cases from multicenter European database. Urology 2005 654: 681 686.
5. Akhtar M, Kardar H, Linjawi T et al. Chromophobe cell carcinoma of the kidney, a clinicopathological study of 21 cases. Am. J. Surg. Pathol. 1995 19: 1245 1256.
6. Crotty TB, Farrow GM, Lieber MM. Chromophobe cell renal carcinoma: clinicopathological feature of 50 cases. J. Urol. 1995 154: 964 967.
7. Zini L, Leroy X, Lemaitre L et al. Tumour necrosis in chromophobe renal cell carcinoma: clinical data to distinguish aggressive variants. Eur. J. Surg. Oncol. 2007 34: 687 691.
8. Jinzaki M, Tanimoto A, Mukai M et al. Double-phase helical CT of small renal parenchymal neoplasms: correlation with pathologic findings and tumor angiogenesis. J. Comput. Assist. Tomogr. 2000 24: 835 842.
9. Prasad SR, Narra VR, Shah R et al. Segmental disorders of the nephron: histological and imaging perspective. Br. J. Radiol. 2007 80: 593 602.
10. Störkel S, Martignoni G, van der Berg E. Chromophobe Renal Cell Carcinoma, in World Health Organization Classification of Tumours: Pathology and Genetics of Tumours of the Urinary System and Male Genital Organs. IARC Press
11. Cheville JC, Lohse CM, Zincke H et al. Comparisons of outcome and prognostic features among histologic subtypes of renal cell carcinoma. Am. J. Surg. Pathol. 2003 27: 612 624. (Pubitemid 36514472)
12. Kovacs G, Soudah B, Hoene E. Binucleated cells in a human renal cell carcinoma with 34 chromosomes. Cancer Genet. Cytogenet. 1988 31: 211 215.
13. Wiatrowska BA, Zakowski MF. Fine-needle aspiration biopsy of chromophobe renal cell carcinoma and oncocytoma comparison of cytomorphologic features. Cancer 1999 87: 161 167.
14. Okoń K. Pathology of renal tumours in adults. Molecular biology, histopathological diagnosis and prognosis. Pol. J. Pathol. 2008 59: 129 176.
15. Tickoo SK, Amin MB. Discriminant nuclear features of renal oncocytoma and chromophobe renal cell carcinoma. Analysis of their potential utility in the differential diagnosis. Am. J. Clin. Pathol. 1998 1106: 782 787.
16. Moreno SM, Banitez IA, Martinez MA et al. Ultrastructural studies in a series of 18 cases of chromophobe renal cell carcinoma. Ultrastruct. Pathol. 2005 29: 377 387.
17. Thoenes W, Baum HP, Storkel S et al. Cytoplasmic microvesicles in chromophobe cell renal carcinoma demonstrated by freeze fracture. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 1987 54: 127 130.
18. Storkel S, Steart PV, Drenckhahn D et al. The human chromophobe cell renal carcinoma: its probable relation to intercalated cells of the collecting duct. Virchows Arch. B Cell Pathol. 1989 56: 237 245.
19. Krishnan B, Troung LD. Renal epithelial neoplasms: the diagnostic implications of electron microscopic study in 55 cases. Hum. Pathol. 2002 33: 68 79.
20. Bonsib SM. Renal chromophobe carcinoma: the relationship between cytoplasmic vesicles and colloidal iron stain. J. Urol. Pathol. 1996 4: 9 14.
21. Tickoo SK, Amin MB, Zarbo RJ. Colloidal iron staining in renal epithelial neoplasms, including chromophobe renal cell carcinoma: emphasis on technique and patterns of staining. Am. J. Surg. Pathol. 1998 22: 419 424.
22. Cochand-Priollet B, Molinie V, Bougaran J et al. Renal chromophobe cell carcinoma and oncocytoma. A comparative morphologic, histochemical, and immunohistochemical study of 124 cases. Arch. Pathol. Lab. Med. 1997 121: 1081 1086.
23. Skinnider BF, Jones EC. Renal oncocytoma and chromophobe renal cell carcinoma: a comparison of colloidal iron staining and electron microscopy. Am. J. Clin. Pathol. 1999 111: 796 803.
24. Akhtar M, Al-Sohaibani MO, Haleem A et al. Flow cytometric DNA analysis of chromophobe cell carcinoma of the kidney. J. Urol. Pathol. 1996 4: 15 23.
25. Holzmann K, Blin N, Welter C et al. Telomeric associations and loss of telomeric DNA repeats in renal tumours. Genes Chromosomes Cancer 1993 6: 178 181.
26. Müller M, Heicappell R, Krause H et al. Telomerase activity in malignant and benign renal tumours. Eur. Urol. 1999 35: 249 255.
27. Kovacs A, Kovacs G. Low chromosome number in chromophobe renal cell carcinomas. Genes Chromosomes Cancer 1992 4: 267 268.
28. Speicher MR, Schoell B, du Manoir S et al. Specific loss of chromosomes 1, 2, 6, 10, 13, 17, and 21 in chromophobe renal cell carcinomas revealed by comparative genomic hybridization. Am. J. Pathol. 1994 145: 356 364.
29. Bugert P, Kovacs G. Molecular differential diagnosis of renal cell carcinomas by microsatellite analysis. Am. J. Pathol. 1996 149: 2081 2088.
30. Bugert P, Gaul C, Weber K et al. Specific genetic changes of diagnostic importance in chromophobe renal cell carcinomas. Lab. Invest. 1997 76: 203 208.
31. Herbers J, Schullerus D, Chudek J et al. Lack of genetic changes at specific genomic sites separates renal oncocytomas from renal cell carcinomas. J. Pathol. 1998 184: 58 62.
32. Shuin T, Kondo K, Sakai N et al. A case of chromophobe renal cell carcinoma associated with low chromosome number and microsatellite instability. Cancer Genet. Cytogenet. 1996 86: 69 71.
33. Iqbal MA, Akhtar M, Ali MA. Cytogenetic findings in renal cell carcinoma. Hum. Pathol. 1996 27: 949 954.
34. Iqbal MA, Akhtar M, Ulmer C et al. FISH analysis in chromophobe renal-cell carcinoma. Diagn. Cytopathol. 2000 22: 3 6.
35. Brunelli M, Eble JN, Zhang S et al. Eosinophilic and classic chromophobe renal cell carcinomas have similar frequent losses of multiple chromosomes from among chromosomes 1, 2, 6, 10, and 17, and this pattern of genetic abnormality is not present in renal oncocytoma. Mod. Pathol. 2005 18: 161 169.
36. Wilhelm M, Veltman JA, Olshen A et al. Array based CGH for the differential diagnosis of renal cell cancer. Cancer Res. 2002 62: 957 960.
37. Akhtar M, Chantziantoniou N. Flow cytometric and quantitative image cell analysis of DNA ploidy in renal chromophobe cell carcinoma. Hum. Pathol. 1998 29: 1181 1188.
38. Monzon FA, Hagenkord JM, Lyons-Weiler MA et al. Whole genome SNP arrays as a potential diagnostic tool for the detection of characteristic chromosomal aberrations in renal epithelial tumors. Mod. Pathol. 2008 21: 599 608.
39. Hagenkord JM, Parwani AV, Lyons-Weiler MA et al. Virtual karyotyping with SNP microarrays reduces uncertainty in the diagnosis of renal epithelial tumors. Diagn. Pathol. 2008 3: 44.
40. Yusenko MV, Kuiper RP, Boethe T et al. High-resolution DNA copy number and gene expression analyses distinguish chromophobe renal cell carcinoma and renal oncocytomas. BMC Cancer 2009 9: 152.
41. Contractor H, Zariwala M, Bugert P et al. Mutation of the p53 tumour suppressor gene occurs preferentially in chromophobe type of renal cell tumours. J. Pathol. 1997 181: 136 139.
42. Sükösd F, Digon B, Fischer J et al. Allelic loss at 10q23.3 but lack of mutation of PTEN/MMAC1 in chromophobe renal cell carcinoma. Cancer Genet. Cytogenet. 2001 128: 161 163.
43. Pavlovich CP, Walther MM, Eyler RA et al. Renal tumours in Birt-Hogg-Dube syndrome. Am. J. Surg. Pathol. 2002 26: 1542 1552.
44. Nagy A, Zubakov D, Stupar Z et al. Lack of mutation of the folliculin gene in sporadic chromophobe RCC and renal oncocytoma. Int. J. Cancer 2004 109: 472 475.
45. Kovacs A, Störkel S, Thoenes W et al. Mitochondrial and chromosomal DNA alterations in human chromophobe renal cell carcinomas. J. Pathol. 1992 167: 273 277.
46. Nagy A, Wilhelm M, Sükösd F et al. Somatic mitochondrial DNA mutations in human chromophobe renal cell carcinomas. Genes Chromosomes Cancer 2002 35: 256 260.
47. Boer JM, Huber WK, Sultmann H et al. Identification and classification of differentially expressed genes in renal cell carcinoma by expression profiling on a global human 31,500-element cDNA array. Genome Res. 2001 11: 1861 1870.
48. Young AN, Amin MB, Moreno CS et al. Expression profiling of renal epithelial neoplasms: a method for tumour classification and discovery of diagnostic molecular markers. Am. J. Pathol. 2001 585: 1639 1651.
49. Gieseg MA, Cody T, Man MZ et al. Expression profiling of human renal carcinoma with functional taxonomic analysis. BMC Bioinformatics 2002 3: 1 13.
50. Takahashi M, Yang XY, Sugimura J et al. Molecular subclassification of kidney tumours and the discovery of new diagnostic markers. Oncogene 2003 22: 6810 6818.
51. Higgins JPT, Shinghal R, Gill H et al. Gene expression patterns in renal cell carcinoma assessed by complementary DNA microarray. Am. J. Pathol. 2003 1623: 925 932.
52. Schuetz AN, Yin-Goen Q, Amin MB et al. Molecular classification of renal tumours by gene expression profiling. J. Mol. Diagn. 2005 7: 206 218.
53. Jones J, Out H, Spentzos D et al. Gene signatures of progression and metastasis in renal cell cancer. Clin. Cancer Res. 2005 11: 5730 5739.
54. Rohan S, Tu JJ, Kao J et al. Gene expression profiling separates chromophobe renal cell carcinoma from oncocytoma and identifies vesicular transport and cell junction proteins as differentially expressed genes. Clin. Cancer Res. 2006 12: 6937 6945.
55. Yang XJ, Sugimura J, Schafernak KT et al. Classification of renal neoplasms based on molecular signatures. J. Urol. 2006 175: 2302 2306.
56. Yusenko MV, Zubakov D, Kovacs G. Gene expression profiling of chromophobe renal cell carcinomas and renal oncocytomas by Affymetrix GeneChip using pooled and individual tumours. Int. J. Biol. Sci. 2009 5: 517 527.
57. Kim SS, Choi YD, Jin XM et al. Immunohistochemical stain for cytokeratin 7, S100A1 and claudin 8 is valuable in differential diagnosis of chromophobe renal cell carcinoma from renal oncocytoma. Histopathology 2009 54: 633 635.
58. Furge KA, Lucas KA, Takahashi M et al. Robust classification of renal cell carcinoma based on gene expression data and predicted cytogenetic profiles. Cancer Res. 2004 64: 4117 4121.
59. Garcia E, Li M. Caveolin-1 immunohistochemical analysis in differentiating chromophobe renal cell carcinoma from renal oncocytoma. Am. J. Clin. Pathol. 2006 125: 392 398.
60. Leroy X, Moukassa D, Copin MC et al. Utility of cytokeratin 7 for distinguishing chromophobe renal cell carcinoma from renal oncocytoma. Eur. Urol. 2000 37: 484 487.
61. Mathers ME, Pollock AM, Marsh C et al. Cytokeratin 7: a useful adjunct in the diagnosis of chromophobe renal cell carcinoma. Histopathology 2002 40: 563 567.
62. Mazal PR, Exner M, Haitel A et al. Expression of kidney specific cadherin distinguishes chromophobe renal cell carcinoma from renal oncocytoma. Hum. Pathol. 2005 36: 22 8.
63. Adley BP, Papavero V, Sugimura J et al. Diagnostic value of cytokeratin 7 and parvalbumin in differentiating chromophobe renal cell carcinoma from renal oncocytoma. Anal. Quant. Cytol. Histol. 2006 28: 228 236.
64. Memeo L, Jhang J, Assad AM et al. Immunohistochemical analysis for cytokeratin 7, KIT, and PAX2: value in the differential diagnosis of chromophobe cell carcinoma. Am. J. Clin. Pathol. 2007 1272: 225 229.
65. Liu L, Qian J, Singh H et al. Immunohistochemical analysis of chromophobe renal cell carcinoma, renal oncocytoma, and clear cell carcinoma: an optimal and practical panel for differential diagnosis. Arch. Pathol. Lab. Med. 2007 1318: 1290 1297.
66. Choi YD, Kim KS, Ryu S et al. Claudin-7 is highly expressed in chromophobe renal cell carcinoma and renal oncocytoma. J. Korean Med. Sci. 2007 222: 305 310.
67. Hornsby CD, Cohen C, Amin MB et al. Claudin-7 immunohistochemistry in renal tumours: a candidate marker for chromophobe renal cell carcinoma identified by gene expression profiling. Arch. Pathol. Lab. Med. 2007 131: 1541 1546.
68. Osunkoya AO, Cohen C, Lawson D et al. Claudin-7 and claudin-8: immunohistochemical markers for the differential diagnosis of chromophobe renal cell carcinoma and renal oncocytoma. Hum. Pathol. 2009 40: 206 210.
69. Pan CC, Chen PC, Chiang H. Overexpression of KIT (CD117) in chromophobe renal cell carcinoma and renal oncocytoma. Am. J. Clin. Pathol. 2004 121: 878 883.
70. Went P, Dirnhofer S, Salvisberg T et al. Expression of epithelial cell adhesion molecule (EpCam) in renal epithelial tumours. Am. J. Surg. Pathol. 2005 29: 83 8.
71. Khoury JD, Abrahams NA, Levin HS et al. The utility of epithelial membrane antigen and vimentin in the diagnosis of chromophobe renal cell carcinoma. Ann. Diagn. Pathol. 2002 6: 154 158.
72. Avery AK, Beckstead J, Renshaw AA, Corless CL. Use of antibodies to RCC and CD10 in the differential diagnosis of renal neoplasms. Am. J. Surg. Pathol. 2000 24: 203 210.
73. Lin BT, Brynes RK, Gelb AB et al. Cyclin D1 expression in renal carcinomas and oncocytomas: an immunohistochemical study. Mod. Pathol. 1998 11: 1075 1081.
74. Lin F, Yang W, Betten M et al. Expression of S-100 protein in renal cell neoplasms. Hum. Pathol. 2006 37: 462 470.
75. Li G, Barthelemy A, Feng G et al. S100A1: a powerful marker to differentiate chromophobe renal cell carcinoma from renal oncocytoma. Histopathology 2007 50: 642 647.
76. Rocca PC, Brunelli M, Gobbo S et al. Diagnostic utility of S100A1 expression in renal cell neoplasms: an immunohistochemical and quantitative RT-PCR study. Mod. Pathol. 2007 20: 722 728.
77. Kauffman EC, Barocas DA, Chen YT et al. Differential expression of KAI1 metastasis suppressor protein in renal cell tumor histological subtypes. J. Urol. 2009 181: 2305 2311.
78. Yusenko MV, Kovacs G. Identifying CD82 (KAI1) as a marker for human chromophobe renal cell carcinoma. Histopathology 2009 55: 687 695.
79. Klatte T, Han KR, Said JW et al. Pathobiology and prognosis of chromophobe renal cell carcinoma. Urol. Oncol. 2008 6: 604 609.
80. Amin MB, Tamboli P, Javidan J et al. Prognostic impact of histologic subtyping of adult renal epithelial neoplasms: an experience of 405 cases. Am. J. Surg. Pathol. 2002 26: 281 291.
81. Renshaw AA, Henske EP, Loughlin KR et al. Aggressive variants of chromophobe renal cell carcinoma. Cancer 1996 78: 1756 1761.
82. Motzer RJ, Bacik J, Mariani T et al. Treatment outcome and survival associated with metastatic renal cell carcinoma of non-clear-cell histology. J. Clin. Oncol. 2002 20: 2376 2381.
83. Akhtar M, Kfoury H, Linjawi T et al. Sarcomatoid chromophobe cell carcinoma of the kidney. J. Urol. Pathol. 1996 4: 155 166.
84. Renshaw AA, Richie JP. Subtypes of renal cell carcinoma. Different onset and sites of metastatic disease. Am. J. Clin. Pathol. 1999 111: 539 543.
85. Badoual C, Tissier F, Lagorce-Pages C et al. Pulmonary metastases from a chromophobe renal cell carcinoma: 10 years' evolution. Histopathology 2002 40: 300 302.
86. Fuhrman SA, Lasky LC, Limas C. Prognostic significance of morphologic parameters in renal cell carcinoma. Am. J. Surg. Pathol. 1982 6: 655 663.
87. de Peralta-Venturina M, Moch H, Amin M et al. Sarcomatoid differentiation in renal cell carcinoma: a study of 101 cases. Am. J. Surg. Pathol. 2001 25: 275 284. (Pubitemid 32174196)
88. Brunelli M, Gobbo S, Cossu-Rocca P et al. Chromosomal gains in the sarcomatoid transformation of chromophobe renal cell carcinoma. Mod. Pathol. 2007 20: 303 309.