Renal Cell Neoplasia Tables: Recurrent Cytogenomic Alterations

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Table 1 - Recurrent Genomic Alterations in Renal Cell Neoplasia Detected by Chromosomal Microarray (Literature Review). Genetic alterations and their associated clinical significance in major types of renal cell neoplasia. Table derived from Liu et al., 2020 [PMID 32434132] with permission from Cancer Genetics.

WHO Classification
Subtype Clear Cell RCC Papillary RCC

Type 1

Papillary RCC

Type 2

(heterogeneous group)

MiTF-Translocation RCC Chromophobe RCC Oncocytoma
Percentage 70-75% 15-20% 15-20% 1-5% 5% 5%
Origin Proximal    Tubules Collecting   Ducts
Copy Number Alterations [level of evidencea; clinical significanceb]
Whole genome Mostly gains Mostly losses No CNAs (~50%) [1; R]
chr1 1p- (10%) [2; R] 1p- (25%) [2; R] 1p- (30%) [3; R] -1 (90%) [1; D]c -1/1p- soly (50%) [1; R]
chr2 +2 (18%) [2; R] -2 (80%) [1; D]c
chr3 -3/3p- (VHL, KDM6A,

KDM5C, SETD2, PBRM1)

(90%) [1; D]

+3 (40%) [2; R] 3p-/cnLOH(3p) (21%) [2; R], 3p+ (12%) [3; R], 3q+ (21%) [3; R] -3 (25%) [3; R]
chr4 4p- (10%) [2; R] -4 (21%) [3; R] +4 (10%) [3; R]
chr5 5p+ (24%) [2; R],

5q+ (SQSTM1) (40-60%) [2; R]

5q+/+5 (20%) [2; R] -5 (25%) [3; R]
chr6 6q- (20%) [2; R] -6 (17%) [3; R] 6p21 (TFEB) amp [2; D, P] -6 (90%) [1; D]c
chr7 +7 (25%) [2; R] +7/+7,+7 (84%) [1; D]c +7 (25%) [1; D] +7 (30%) [3; R]
chr8 8p- (25%) [2; R] +8 (MYC) (10-33%) [3; R] -8 (15%) [3; R]c
chr9 9p- (20%) [1; P]

9q- (20%) [2; R]

9p- (19%) [2; R],

9q- (17%) [3; R]

9p- (30%) [3; R] -9 (35%) [3; R]
chr10 10q- (10%) [2; R] 10q- (17%) [3; R] -10 (90%) [1; D]c
chr11 11q- (19%) [3; R] -11 (10%) [3; R]
chr12 +12 (15%) [2; R] +12 (52%) [2; R] +12 (15%) [3; R] +12 (35%) [3; R]
chr13 +13 (13%) [2; R] -13 (20%) [3; R] -13 (85%) [1; D]c
chr14 14q- (HIF1A) (40%) [1; P] -14 (28%) [2; R] -14 (10%) [2; R]
chr15 -15 (15%) [3; R] -15 (15%) [3; R]
chr16 16p+ (12%) [2; R],

16q+ (10%) [2; R]

+16 (55%) [2; R] 16p+ (40%) [2; R],

16q+ (35%) [2; R]

chr17 +17 (84%) [1; D]c 17p- (8%) [3; R],

+17/17q+ (50%) [1; D]

17p- (20%) [3; R],

17q+ (40%) [3; R]

-17 (90%) [1; D]c
chr18 -18 (10%) [2; R] -18 (26%) [2; R] -18 (15%) [3; R]
chr19
chr20 +20 (13%) [2; R] +20 (40%) [2; R]
chr21 -21 (19%) [3; R] -21 (70%) [1; D]c -21 (15%) [3; R]
chr22 -22 (40%) [2; R]
X -X (10%) [3;R]
Y -Y (40%) [1; R with -1]c
Rearrangements [level of evidence; clinical significance]
TERT promoter (5p15) (<10%) [3; R] TFE3 (Xp11), TFEB (6p21) (100%) [1; D, P] TERT promoter (5p15) (12%) [3; R] CCND1 (11q13) (40%) [2; D]
Mutations (SNVs, Indels) [level of evidence; clinical significance]
Mutated

in >20%

PBRM1 [2; R], VHL (also promoter methylation) [1; D] TP53 [2; R]
Mutated

in 10-20%

BAP1 [1; P], SETD2 [2; R] MET [1; D]
Mutated

in 5-10%

KDM5C, MTOR, PTEN, TP53 [2; R] CDKN2A (also promoter hypermethylation) [2; P], MET [1; D] PTEN [2; R]
Mutated

in 2-5%

ARID1A, CDKN2A, KDMT2C/KDMT2D, LRP1B, PIK3CA, PTEN, STAG2, TCEB1, TERT CDKN2A/CDKN2B, KDM6A, MLL3, NF2, NFE2L2, SMARCB1, TERT BAP1, FAT1, KDM6A, NF2, NFE2L2, PBRM1, SETD2, STAG2, TERT, TP53 ARID1A, FAAH2, FAT1/FAT4, FLT4, MICALCL, NIN, PDHB, PDXDC1, TSC1/TSC2, ZNF765 ERCC2, C2CD4C
Mitochondrial  DNA MT-ND5 [3,D] MT-COX1, MT-COX2, MT-COX3, MT-ND5, MT-CYTB [2,D]
Germline susceptibility
Germline susceptibility
  • mainly VHL (von Hippel-Lindau Syndrome)
  • PTEN (Cowden Syndrome)
  • FLCN (Birt-Hogg-Dube syndrome)
  • TSC1 and TSC2 (tuberous sclerosis)
  • SDHB (most common), SDHC (less common), SDHA (rare), SDHD (rare) (succinate dehydrogenase deficient RCC)
  • MET (Hereditary papillary RCC)
  • FH (Hereditary leiomyomatosis and RCC)
FCLN (Birt-Hogg-Dube syndrome) FCLN (Birt-Hogg-Dube syndrome)
References [9[1], 14[2], 17[3], 24[4], 27[5], 29[6], 32[7], 35[8], 49[9], 156-168[10][11][12][13][14][15][16][17][18][19][20][21][22]] [10[23], 42[24], 67-71[25][26][27][28][29], 73[30], 74[31], 98[32], 169-174[33][34][35][36][37][38]] [10[1], 121[39], 122[40], 124[41], 125[42], 175[43]] [11[44], 12[45], 103[46], 105[47], 106[48], 108[49], 109[50], 129[51], 137[52], 176[53], 177[54]] [12[45], 76[55], 102[56], 103[46], 105[47], 129[51], 132[57], 135-137[58][59][52], 140[60], 178-180[61][62][63]]

Note: a level of evidence (ranges from level 1 to 3 as specified in the methods). Level 1, established clinical significance and present in current WHO classification and/or professional practice guidelines such as NCCN, ASCO, CAP guidelines or FDA approval; Level 2, recurrent clinical significance based on large studies with outcomes; and Level 3, recurrent but uncertain clinical significance based on smaller studies and multiple case reports.

          b clinical significance, D-diagnosis, P-prognosis, R-recurrence

          c alterations in combination

Reference

1. Liu YJ, Houldsworth J, Emmadi R, Dyer L, Wolff DJ. Assessing Genomic Copy Number Alterations as Best Practice for Renal Cell Neoplasia: An Evidence-Based Review from the Cancer Genomics Consortium Workgroup. Cancer Genet. 2020 Jun;244:40-54. doi: 10.1016/j.cancergen.2020.04.004. Epub 2020 May 1. PMID 32434132.

  1. 1.0 1.1 Cancer Genome Atlas Research Network (2013-07-04). "Comprehensive molecular characterization of clear cell renal cell carcinoma". Nature. 499 (7456): 43–49. doi:10.1038/nature12222. ISSN 1476-4687. PMC 3771322. PMID 23792563.
  2. Klatte, Tobias; et al. (2009-02-10). "Cytogenetic profile predicts prognosis of patients with clear cell renal cell carcinoma". Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology. 27 (5): 746–753. doi:10.1200/JCO.2007.15.8345. ISSN 1527-7755. PMID 19124809.
  3. Mitchell, Thomas J.; et al. (04 19, 2018). "Timing the Landmark Events in the Evolution of Clear Cell Renal Cell Cancer: TRACERx Renal". Cell. 173 (3): 611–623.e17. doi:10.1016/j.cell.2018.02.020. ISSN 1097-4172. PMC 5927631. PMID 29656891. Check date values in: |date= (help)
  4. Chen, Meng; et al. (2009-11-15). "Genome-wide profiling of chromosomal alterations in renal cell carcinoma using high-density single nucleotide polymorphism arrays". International Journal of Cancer. 125 (10): 2342–2348. doi:10.1002/ijc.24642. ISSN 1097-0215. PMC 2768265. PMID 19521957.
  5. Gerlinger, Marco; et al. (2012-03-08). "Intratumor heterogeneity and branched evolution revealed by multiregion sequencing". The New England Journal of Medicine. 366 (10): 883–892. doi:10.1056/NEJMoa1113205. ISSN 1533-4406. PMC 4878653. PMID 22397650.
  6. Sato, Yusuke; et al. (2013-08). "Integrated molecular analysis of clear-cell renal cell carcinoma". Nature Genetics. 45 (8): 860–867. doi:10.1038/ng.2699. ISSN 1546-1718. PMID 23797736. Check date values in: |date= (help)
  7. Beroukhim, Rameen; et al. (2009-06-01). "Patterns of gene expression and copy-number alterations in von-hippel lindau disease-associated and sporadic clear cell carcinoma of the kidney". Cancer Research. 69 (11): 4674–4681. doi:10.1158/0008-5472.CAN-09-0146. ISSN 1538-7445. PMC 2745239. PMID 19470766.
  8. Arai, Eri; et al. (2008-09-01). "Genetic clustering of clear cell renal cell carcinoma based on array-comparative genomic hybridization: its association with DNA methylation alteration and patient outcome". Clinical Cancer Research: An Official Journal of the American Association for Cancer Research. 14 (17): 5531–5539. doi:10.1158/1078-0432.CCR-08-0443. ISSN 1078-0432. PMID 18765545.
  9. Kroeger, Nils; et al. (2013-04-15). "Deletions of chromosomes 3p and 14q molecularly subclassify clear cell renal cell carcinoma". Cancer. 119 (8): 1547–1554. doi:10.1002/cncr.27947. ISSN 1097-0142. PMID 23335244.
  10. Crino, Peter B.; et al. (2006-09-28). "The tuberous sclerosis complex". The New England Journal of Medicine. 355 (13): 1345–1356. doi:10.1056/NEJMra055323. ISSN 1533-4406. PMID 17005952.
  11. Dalgliesh, Gillian L.; et al. (2010-01-21). "Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes". Nature. 463 (7279): 360–363. doi:10.1038/nature08672. ISSN 1476-4687. PMC 2820242. PMID 20054297.
  12. Kaimakliotis, Hristos Z.; et al. (2014-05). "Plasmacytoid bladder cancer: variant histology with aggressive behavior and a new mode of invasion along fascial planes". Urology. 83 (5): 1112–1116. doi:10.1016/j.urology.2013.12.035. ISSN 1527-9995. PMID 24582117. Check date values in: |date= (help)
  13. Kaku, Haruki; et al. (2004-07). "Positive correlation between allelic loss at chromosome 14q24-31 and poor prognosis of patients with renal cell carcinoma". Urology. 64 (1): 176–181. doi:10.1016/j.urology.2004.03.015. ISSN 1527-9995. PMID 15245966. Check date values in: |date= (help)
  14. Kluzek, Katarzyna; et al. (2017-04-25). "Genetic characterization of Polish ccRCC patients: somatic mutation analysis of PBRM1, BAP1 and KDMC5, genomic SNP array analysis in tumor biopsy and preliminary results of chromosome aberrations analysis in plasma cell free DNA". Oncotarget. 8 (17): 28558–28574. doi:10.18632/oncotarget.15331. ISSN 1949-2553. PMC 5438672. PMID 28212566.
  15. Köhn, Linda; et al. (2015-05). "Specific genomic aberrations predict survival, but low mutation rate in cancer hot spots, in clear cell renal cell carcinoma". Applied immunohistochemistry & molecular morphology: AIMM. 23 (5): 334–342. doi:10.1097/PAI.0000000000000087. ISSN 1533-4058. PMC 4431677. PMID 24992170. Check date values in: |date= (help)
  16. Latif, F.; et al. (1993-05-28). "Identification of the von Hippel-Lindau disease tumor suppressor gene". Science (New York, N.Y.). 260 (5112): 1317–1320. doi:10.1126/science.8493574. ISSN 0036-8075. PMID 8493574.
  17. Moore, L. E.; et al. (2012-06-25). "Genomic copy number alterations in clear cell renal carcinoma: associations with case characteristics and mechanisms of VHL gene inactivation". Oncogenesis. 1: e14. doi:10.1038/oncsis.2012.14. ISSN 2157-9024. PMC 3412648. PMID 23552698.
  18. Peña-Llopis, Samuel; et al. (2012-06-10). "BAP1 loss defines a new class of renal cell carcinoma". Nature Genetics. 44 (7): 751–759. doi:10.1038/ng.2323. ISSN 1546-1718. PMC 3788680. PMID 22683710.
  19. Piva, Francesco; et al. (2015). "BAP1, PBRM1 and SETD2 in clear-cell renal cell carcinoma: molecular diagnostics and possible targets for personalized therapies". Expert Review of Molecular Diagnostics. 15 (9): 1201–1210. doi:10.1586/14737159.2015.1068122. ISSN 1744-8352. PMID 26166446.
  20. Rechsteiner, Markus P.; et al. (2011-08-15). "VHL gene mutations and their effects on hypoxia inducible factor HIFα: identification of potential driver and passenger mutations". Cancer Research. 71 (16): 5500–5511. doi:10.1158/0008-5472.CAN-11-0757. ISSN 1538-7445. PMID 21715564.
  21. Ricketts, Christopher J.; et al. (2012-12). "Succinate dehydrogenase kidney cancer: an aggressive example of the Warburg effect in cancer". The Journal of Urology. 188 (6): 2063–2071. doi:10.1016/j.juro.2012.08.030. ISSN 1527-3792. PMC 3856891. PMID 23083876. Check date values in: |date= (help)
  22. Zhang, Zhongfa; et al. (2010). "A Comprehensive Study of Progressive Cytogenetic Alterations in Clear Cell Renal Cell Carcinoma and a New Model for ccRCC Tumorigenesis and Progression". Advances in Bioinformatics: 428325. doi:10.1155/2010/428325. ISSN 1687-8035. PMC 2909727. PMID 20671976.
  23. Cancer Genome Atlas Research Network; et al. (2016-01-14). "Comprehensive Molecular Characterization of Papillary Renal-Cell Carcinoma". The New England Journal of Medicine. 374 (2): 135–145. doi:10.1056/NEJMoa1505917. ISSN 1533-4406. PMC 4775252. PMID 26536169.
  24. Antonelli, Alessandro; et al. (2010-06). "Cytogenetic features, clinical significance and prognostic impact of type 1 and type 2 papillary renal cell carcinoma". Cancer Genetics and Cytogenetics. 199 (2): 128–133. doi:10.1016/j.cancergencyto.2010.02.013. ISSN 1873-4456. PMID 20471516. Check date values in: |date= (help)
  25. Jiang, F.; et al. (1998-11). "Chromosomal imbalances in papillary renal cell carcinoma: genetic differences between histological subtypes". The American Journal of Pathology. 153 (5): 1467–1473. doi:10.1016/S0002-9440(10)65734-3. ISSN 0002-9440. PMC 1853413. PMID 9811338. Check date values in: |date= (help)
  26. Klatte, Tobias; et al. (2009-02-15). "Cytogenetic and molecular tumor profiling for type 1 and type 2 papillary renal cell carcinoma". Clinical Cancer Research: An Official Journal of the American Association for Cancer Research. 15 (4): 1162–1169. doi:10.1158/1078-0432.CCR-08-1229. ISSN 1078-0432. PMID 19228721.
  27. Sanders, Melinda E.; et al. (2002-09). "Unique patterns of allelic imbalance distinguish type 1 from type 2 sporadic papillary renal cell carcinoma". The American Journal of Pathology. 161 (3): 997–1005. doi:10.1016/S0002-9440(10)64260-5. ISSN 0002-9440. PMC 1867241. PMID 12213728. Check date values in: |date= (help)
  28. Yu, Wenjuan; et al. (2013-06). "Clinicopathological, genetic, ultrastructural characterizations and prognostic factors of papillary renal cell carcinoma: new diagnostic and prognostic information". Acta Histochemica. 115 (5): 452–459. doi:10.1016/j.acthis.2012.10.009. ISSN 1618-0372. PMID 23219441. Check date values in: |date= (help)
  29. Schraml, P.; et al. (2000-03). "Allelic loss at the D9S171 locus on chromosome 9p13 is associated with progression of papillary renal cell carcinoma". The Journal of Pathology. 190 (4): 457–461. doi:10.1002/(SICI)1096-9896(200003)190:43.0.CO;2-C. ISSN 0022-3417. PMID 10699995. Check date values in: |date= (help)
  30. Hughson, M. D.; et al. (1998-10-15). "Clear-cell and papillary carcinoma of the kidney: an analysis of chromosome 3, 7, and 17 abnormalities by microsatellite amplification, cytogenetics, and fluorescence in situ hybridization". Cancer Genetics and Cytogenetics. 106 (2): 93–104. doi:10.1016/s0165-4608(98)00068-5. ISSN 0165-4608. PMID 9797772.
  31. Velickovic, M.; et al. (2001-06-15). "VHL and FHIT locus loss of heterozygosity is common in all renal cancer morphotypes but differs in pattern and prognostic significance". Cancer Research. 61 (12): 4815–4819. ISSN 0008-5472. PMID 11406557.
  32. Przybycin, Christopher G.; et al. (2013-07). "Hereditary syndromes with associated renal neoplasia: a practical guide to histologic recognition in renal tumor resection specimens". Advances in Anatomic Pathology. 20 (4): 245–263. doi:10.1097/PAP.0b013e318299b7c6. ISSN 1533-4031. PMID 23752087. Check date values in: |date= (help)
  33. Hes, Ondrej; et al. (2006-06). "Oncocytic papillary renal cell carcinoma: a clinicopathologic, immunohistochemical, ultrastructural, and interphase cytogenetic study of 12 cases". Annals of Diagnostic Pathology. 10 (3): 133–139. doi:10.1016/j.anndiagpath.2005.12.002. ISSN 1092-9134. PMID 16730306. Check date values in: |date= (help)
  34. Lefèvre, Marine; et al. (2005-12). "Adult papillary renal tumor with oncocytic cells: clinicopathologic, immunohistochemical, and cytogenetic features of 10 cases". The American Journal of Surgical Pathology. 29 (12): 1576–1581. doi:10.1097/01.pas.0000184821.09871.ec. ISSN 0147-5185. PMID 16327429. Check date values in: |date= (help)
  35. Jones, Timothy D.; et al. (2005-10-15). "Molecular genetic evidence for the independent origin of multifocal papillary tumors in patients with papillary renal cell carcinomas". Clinical Cancer Research: An Official Journal of the American Association for Cancer Research. 11 (20): 7226–7233. doi:10.1158/1078-0432.CCR-04-2597. ISSN 1078-0432. PMID 16243792.
  36. Sweeney, Paul; et al. (2002-07). "Biological significance of c-met over expression in papillary renal cell carcinoma". The Journal of Urology. 168 (1): 51–55. ISSN 0022-5347. PMID 12050491. Check date values in: |date= (help)
  37. Kattar, M. M.; et al. (1997-11). "Clinicopathologic and interphase cytogenetic analysis of papillary (chromophilic) renal cell carcinoma". Modern Pathology: An Official Journal of the United States and Canadian Academy of Pathology, Inc. 10 (11): 1143–1150. ISSN 0893-3952. PMID 9388066. Check date values in: |date= (help)
  38. Kovacs, G.; et al. (1991-07). "Cytogenetics of papillary renal cell tumors". Genes, Chromosomes & Cancer. 3 (4): 249–255. doi:10.1002/gcc.2870030403. ISSN 1045-2257. PMID 1958590. Check date values in: |date= (help)
  39. Mendel, Lionel; et al. (03 2018). "Comprehensive study of three novel cases of TFEB-amplified renal cell carcinoma and review of the literature: Evidence for a specific entity with poor outcome". Genes, Chromosomes & Cancer. 57 (3): 99–113. doi:10.1002/gcc.22513. ISSN 1098-2264. PMID 29127730. Check date values in: |date= (help)
  40. Skala, Stephanie L.; et al. (01 2018). "Detection of 6 TFEB-amplified renal cell carcinomas and 25 renal cell carcinomas with MITF translocations: systematic morphologic analysis of 85 cases evaluated by clinical TFE3 and TFEB FISH assays". Modern Pathology: An Official Journal of the United States and Canadian Academy of Pathology, Inc. 31 (1): 179–197. doi:10.1038/modpathol.2017.99. ISSN 1530-0285. PMID 28840857. Check date values in: |date= (help)
  41. Pan, Chin-Chen; et al. (2013-07). "High chromosomal copy number alterations in Xp11 translocation renal cell carcinomas detected by array comparative genomic hybridization are associated with aggressive behavior". The American Journal of Surgical Pathology. 37 (7): 1116–1119. doi:10.1097/PAS.0b013e318293d872. ISSN 1532-0979. PMID 23759936. Check date values in: |date= (help)
  42. Malouf, Gabriel G.; et al. (2013-09-01). "Genomic heterogeneity of translocation renal cell carcinoma". Clinical Cancer Research: An Official Journal of the American Association for Cancer Research. 19 (17): 4673–4684. doi:10.1158/1078-0432.CCR-12-3825. ISSN 1557-3265. PMC 3882157. PMID 23817689.
  43. Argani, Pedram; et al. (11 2016). "TFEB-amplified Renal Cell Carcinomas: An Aggressive Molecular Subset Demonstrating Variable Melanocytic Marker Expression and Morphologic Heterogeneity". The American Journal of Surgical Pathology. 40 (11): 1484–1495. doi:10.1097/PAS.0000000000000720. ISSN 1532-0979. PMC 5069163. PMID 27565001. Check date values in: |date= (help)
  44. Davis, Caleb F.; et al. (2014-09-08). "The somatic genomic landscape of chromophobe renal cell carcinoma". Cancer Cell. 26 (3): 319–330. doi:10.1016/j.ccr.2014.07.014. ISSN 1878-3686. PMC 4160352. PMID 25155756.
  45. 45.0 45.1 Chen, Fengju; et al. (2016-03-15). "Multilevel Genomics-Based Taxonomy of Renal Cell Carcinoma". Cell Reports. 14 (10): 2476–2489. doi:10.1016/j.celrep.2016.02.024. ISSN 2211-1247. PMC 4794376. PMID 26947078.
  46. 46.0 46.1 Krill-Burger, John M.; et al. (2012-06). "Renal cell neoplasms contain shared tumor type-specific copy number variations". The American Journal of Pathology. 180 (6): 2427–2439. doi:10.1016/j.ajpath.2012.01.044. ISSN 1525-2191. PMC 3378847. PMID 22483639. Check date values in: |date= (help)
  47. 47.0 47.1 Yusenko, Maria V.; et al. (2009-05-18). "High-resolution DNA copy number and gene expression analyses distinguish chromophobe renal cell carcinomas and renal oncocytomas". BMC cancer. 9: 152. doi:10.1186/1471-2407-9-152. ISSN 1471-2407. PMC 2686725. PMID 19445733.
  48. Kang, Xue-Ling; et al. (2015). "Chromosomal imbalances revealed in primary renal cell carcinomas by comparative genomic hybridization". International Journal of Clinical and Experimental Pathology. 8 (4): 3636–3647. ISSN 1936-2625. PMC 4466932. PMID 26097545.
  49. Sperga, Maris; et al. (2013-10). "Chromophobe renal cell carcinoma--chromosomal aberration variability and its relation to Paner grading system: an array CGH and FISH analysis of 37 cases". Virchows Archiv: An International Journal of Pathology. 463 (4): 563–573. doi:10.1007/s00428-013-1457-6. ISSN 1432-2307. PMID 23913167. Check date values in: |date= (help)
  50. Casuscelli, Jozefina; et al. (2017-06-15). "Genomic landscape and evolution of metastatic chromophobe renal cell carcinoma". JCI insight. 2 (12). doi:10.1172/jci.insight.92688. ISSN 2379-3708. PMC 5470887. PMID 28614790.
  51. 51.0 51.1 Gowrishankar, Banumathy; et al. (2014-12). "Subtyping of renal cortical neoplasms in fine needle aspiration biopsies using a decision tree based on genomic alterations detected by fluorescence in situ hybridization". BJU international. 114 (6): 881–890. doi:10.1111/bju.12643. ISSN 1464-410X. PMC 4257075. PMID 24467611. Check date values in: |date= (help)
  52. 52.0 52.1 Tan, Min-Han; et al. (2010-05-12). "Genomic expression and single-nucleotide polymorphism profiling discriminates chromophobe renal cell carcinoma and oncocytoma". BMC cancer. 10: 196. doi:10.1186/1471-2407-10-196. ISSN 1471-2407. PMC 2883967. PMID 20462447.
  53. Abbosh, Philip; et al. (12 2018). "Molecular and Genomic Profiling to Identify Actionable Targets in Chromophobe Renal Cell Cancer". European Urology Focus. 4 (6): 969–971. doi:10.1016/j.euf.2017.01.003. ISSN 2405-4569. PMID 28753842. Check date values in: |date= (help)
  54. Hammer, B. E. (1989-03). "Proton decoupled 13C NMR imaging". Magnetic Resonance Imaging. 7 (2): 235–240. doi:10.1016/0730-725x(89)90710-8. ISSN 0730-725X. PMID 2541301. Check date values in: |date= (help)
  55. Durinck, Steffen; et al. (2015-01). "Spectrum of diverse genomic alterations define non-clear cell renal carcinoma subtypes". Nature Genetics. 47 (1): 13–21. doi:10.1038/ng.3146. ISSN 1546-1718. PMC 4489427. PMID 25401301. Check date values in: |date= (help)
  56. Gowrishankar, Banumathy; et al. (2015-05). "A genomic algorithm for the molecular classification of common renal cortical neoplasms: development and validation". The Journal of Urology. 193 (5): 1479–1485. doi:10.1016/j.juro.2014.11.099. ISSN 1527-3792. PMID 25498568. Check date values in: |date= (help)
  57. Joshi, Shilpy; et al. (2015-12-01). "The Genomic Landscape of Renal Oncocytoma Identifies a Metabolic Barrier to Tumorigenesis". Cell Reports. 13 (9): 1895–1908. doi:10.1016/j.celrep.2015.10.059. ISSN 2211-1247. PMC 4779191. PMID 26655904.
  58. Lindgren, Valerie; et al. (2004-02). "Cytogenetic analysis of a series of 13 renal oncocytomas". The Journal of Urology. 171 (2 Pt 1): 602–604. doi:10.1097/01.ju.0000109172.07081.16. ISSN 0022-5347. PMID 14713769. Check date values in: |date= (help)
  59. Paner, Gladell P.; et al. (2007-01). "High incidence of chromosome 1 abnormalities in a series of 27 renal oncocytomas: cytogenetic and fluorescence in situ hybridization studies". Archives of Pathology & Laboratory Medicine. 131 (1): 81–85. doi:10.1043/1543-2165(2007)131[81:HIOCAI]2.0.CO;2. ISSN 1543-2165. PMID 17227127. Check date values in: |date= (help)
  60. Boris, Ronald S.; et al. (2011-06). "The impact of germline BHD mutation on histological concordance and clinical treatment of patients with bilateral renal masses and known unilateral oncocytoma". The Journal of Urology. 185 (6): 2050–2055. doi:10.1016/j.juro.2011.02.051. ISSN 1527-3792. PMC 3164767. PMID 21496834. Check date values in: |date= (help)
  61. Michalova, Kvetoslava; et al. (2018-08). "Papillary renal cell carcinoma with cytologic and molecular genetic features overlapping with renal oncocytoma: Analysis of 10 cases". Annals of Diagnostic Pathology. 35: 1–6. doi:10.1016/j.anndiagpath.2018.01.010. ISSN 1532-8198. PMID 30072012. Check date values in: |date= (help)
  62. He, Huiying; et al. (2018-12). ""High-grade oncocytic renal tumor": morphologic, immunohistochemical, and molecular genetic study of 14 cases". Virchows Archiv: An International Journal of Pathology. 473 (6): 725–738. doi:10.1007/s00428-018-2456-4. ISSN 1432-2307. PMID 30232607. Check date values in: |date= (help)
  63. Dvorakova, Marie; et al. (2010-05-24). "Renal oncocytoma: a comparative clinicopathologic study and fluorescent in-situ hybridization analysis of 73 cases with long-term follow-up". Diagnostic Pathology. 5: 32. doi:10.1186/1746-1596-5-32. ISSN 1746-1596. PMC 2881070. PMID 20497539.