JOURNAL OF CLINICAL ONCOLOGY DIAGNOSIS IN ONCOLOGY

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1 VOLUME 28 NUMER 34 DECEMER JOURNL OF CLINICL ONCOLOGY DIGNOSIS IN ONCOLOGY Renal Cell Carcinoma With t(6;11) Translocation: Patient Case With a Novel lpha- Fusion Point Renal cell carcinoma (RCC) with t(6;11) translocation is an extremely rare disease entity; to our knowledge, only 18 patient cases have been reported as of now ecause of its infrequence, it is not well known and can be easily misdiagnosed as another kind of renal cell tumor. We present a patient case in which angiomyolipoma was the initial diagnosis by the referring institution. In this patient, a novel lpha- fusion point associated with RCC with t(6;11) translocation was detected. The patient, a 26-year-old man, sought medical observation because of painless gross hematuria. Laboratory data showed no abnormality of peripheral blood. bdominal ultrasonography and computed tomography scan revealed a 4-cm left renal mass. In October 2009, he underwent an uncomplicated left radical nephrectomy. This patient case was sent to our department for consultation by a provincial hospital with a sample of the left renal mass consisting of 10 hematoxylin and eosin slides and two corresponding paraffin blocks. The patient was not treated with chemotherapy or radiation therapy after surgery. t 6 months after surgery, he was free of disease and undergoing follow-up. Grossly, a cm mass was revealed in the upper pole of the left kidney on the cut surface. The mass was well circumscribed, nodular, and tan-brown in color. Neither necrosis nor hemorrhage was identified. This information was acquired from the initial hospital. Histologically, the submitted paraffin-embedded tissue blocks were cut into 3- m sections and stained with hematoxylin and eosin for inspection by light microscope, along with the 10 original slides. The tumor consisted of large and small epithelioid cells arranged in a nested alveolar or acinar pattern and separated by thin capillaries (Fig 1). The large cells had well-defined cell borders, clear or granular eosinophilic abundant cytoplasm, and round nuclei with small nucleoli. The small cells had narrow eosinophilic cytoplasm, and dark nuclei were characteristically clustered around hyaline basement membrane material within large acini (Fig 1). Psammomatous calcification and hemosiderin were not identified. Mitoses were rare. Necrosis was absent. Immunohistochemically, both types of tumor cells were diffusely positive for vimentin and Melan- and widely stained with E1/E3, CK8, and Cam5.2 anticytokeratin antibodies (Figs 1C and 1D). The immunostains for human melanoma black 45 (HM45) and PNL2 were focally positive only in the large cells. Cytoplasmic decorating for CD10 was focally positive in isolated cells. Nuclear staining with transcription factor (TF) E antibody was present in the majority of tumor cells (Fig 1E). The proliferation rate of Ki-67 antibody was 2%. Immunostains for TFE3, smooth muscle actin, CK7, epithelial membrane antigen (EM), S-100 protein, -inhibin, estrogen receptor, progesterone receptor, synaptophysin, and chromogranin were negative. Under electron microscope, rudimentary organelles were seen within the neoplastic cytoplasm (Fig 2, arrow) and poorly formed lumens, cell tight junctions, and microvilli were detected among neoplastic cells (Fig 2, arrows). No premelanosomes or melanosomes were identified. Detection of lpha- fusion by reverse transcription polymerase chain reaction (RT-PCR) and DN-PCR was respectively performed as described by rgani et al, 4 employing the same primers: alpha forward, 5 -GGTGGTTTGGTGG-3 ; reverser, 5 -CTCCGGTGGCTGCCCTTCCCCTCC-3. PCR-amplified products were gel purified by DN purification kit (Qiagen, Venlo, the Netherlands), and sequencing was followed with an I 3730XL automated sequencer (pplied iosystems, Foster City, C). The primers used for sequencing were the same as the amplification primers. gene exon and intron structures were obtained from the Ensembl project (Hinxton, United Kingdom). Housekeeping gene PGK transcript was examined in this case (data not shown). Unfortunately, the expected product of lpha- fusion was not obtained via RT-PCR. However, the expected product of lpha- fusion, 879 bp, was obtained by DN-PCR on genomic DN. The negative control lacking DN was negative (Fig 3). Sequencing analysis revealed the lpha- fusion point to be between lpha at nucleotide 1810 (Genbank accession number F203815) and at nucleotide 94 numbered from the 5 end of exon3 of (Figs 3 and 3C). On basis of pathologic, immunohistochemical, ultrastructural, and genetic features, diagnosis of RCC with t(6;11) translocation was made. The translocation of t(6;11)(p21;q12 or q13) in RCC causes fusion of the lpha gene on 11q12 or q13 with the gene on 6p21, resulting in overexpression of native protein. 1 The first report of RCC with t(6;11) translocation was published in To our knowledge, only 18 patient cases have been reported in the literature In 17 of these, clinical history was available; they involved six male and 11 female patients, with a mean age of 24.5 years (median, 22 years; range, 6 to 54 years). ccording to available clinical history, RCC with t(6;11) translocation is predominantly seen in children and young adults, with older adults making up a small minority of patients. Only two (11.7%) of the 17 patients were older than age 40 years. The patient in our case was 26 years old. Microscopically, RCC with t(6;11) translocation consists mainly of two types of cells: large epithelioid cells with clear or eosinophilic cytoplasms and small cells with narrow cytoplasms and dense chromatin. Remarkably, the small cells surround basement membrane material located in large acini. 3,4,6,9,10 Our patient case involved histologic features similar to those reported in others, but cysts with hyaline-papillary structures and large vessels with collagenized walls did not exist. Published literature shows that the most distinctive immunohistochemical feature of RCC with t(6;11) translocation is detectable Journal of Clinical Oncology, Vol 28, No 34 (December 1), 2010: pp e709-e by merican Society of Clinical Oncology e709

2 Zhan et al C D E Fig 1. nuclear staining for native protein.1-8,10 rgani et al4 detected strong nuclear labeling in all seven RCCs with t(6;11) translocation investigated, whereas 1,089 other unrelated neoplasms and normal tissues did not show nuclear labeling. Interestingly, HM45 and Melan- are commonly positive in RCC with t(6;11) translocation.1,3-7,9,10 rgani et al4 postulated that the expression of e by merican Society of Clinical Oncology HM45 and Melan- in RCC with t(6;11) translocation reflected aberrant transcriptional activity of the abnormally expressed protein, because has a DN binding domain identical to that of microphthalmia-associated transcription factor. Expression of, HM45, and Melan- was also found in our patient case. Most RCCs with t(6;11) translocation are negative for cytokeratins (eg, E1/E3, JOURNL OF CLINICL ONCOLOGY

3 Diagnosis in Oncology Fig 2. Cam5.2) and EM. 2-4,6,7 Only four patient cases, including ours, have been positive for E1/E3, 5,7,10 and two have been positive for EM. 7 The reason for different expression of epithelial markers in RCC with t(6;11) translocation remains unclear. Immunostains of this disease entity for TFE3, microphthalmia-associated transcription factor, RCC, smooth muscle actin, S-100 protein, and desmin have always been negative in reported patient cases (Table 1). Ultrastructurally, in our patient case, junctions between neoplasm cells as well as rudimentary microvilli on the surfaces of neoplasm cells were detected. The cell junctions and rudimentary microvilli were consistent with those of conventional clear cell RCCs, which indicates this disease entity is derived from the epithelium or shows epithelial differentiation. Our patient case involved the same features of cell junctions and rudimentary microvilli as those described in the literature. 2,3 Genetically, rgani et al 4 demonstrated that the lack of splice signals in lpha, an intronless gene, resulted in identical DN-PCR and RT-PCR products of the lpha- fusion gene. In the lpha gene, the breakpoint was at nucleotide 1810 (Fig 3D, arrow) and fell in the 1.2 kb breakpoint cluster region (breakpoints 1070 and 1419, reported by Kuiper et al 1 ; breakpoints 1580, 1672, 1760, 1795, and 2274, reported by rgani et al 4 ; and breakpoint 1631, reported by Fusion Point lpha C Fusion Point D lpha lpha 1,070 1,580 1,419 1,631 1,672 1,760 1,795 1,810 2,274 TG Fig by merican Society of Clinical Oncology e711

4 Zhan et al Table 1. Clinical and Immunohistochemical Features of Reported Patient Cases ge Immunophenotype Patient (years) Sex Reference TFE3 HM45 Melan- MITF CD10 RCC E1/E3 Cam5.2 CK7 CK8 EM SM S-100 Desmin 1 14 F Kuiper et al 1 N N N N N N N N 2 42 F Kuiper et al 1 N N N N N N N N N N N N N N N 3 17 F Kuiper et al 1 N N N N N N N N N N N N N N N 4 18 F Davis et al 2 N N N N N N N 5 18 M rgani et al 3 N 6 10 M rgani et al 3 N 7 20 F rgani et al 4 N N N N N N N N 8 9 F rgani et al 4 N N N N N N N N N N N N 9 33 M rgani et al 4 N N N N N 10 6 F rgani et al 5 N N N N N N N N N N N F Pecciarini et al 6 N N N N N N F Camparo et al 7 N N N N N N N M Camparo et al 7 N N N N N N N 14 N N Geller et al 8 N N N N N N N N N N N N N M Hora et al 9 N N N N N N N N N N N N F Hora et al 9 N N N N N N N N N N N N F Hora et al 9 N N N N N N N N N N N N M Suárez-Vilela N N N et al 10 Our patient 26 M N N N Total 14 of 14 0 of of of 15 0 of 4 7 of 11 0 of 4 4 of 11 2 of 6 1 of 8 2 of 2 2 of 8 0 of 5 0 of 7 0 of 5 NOTE. Davis et al 2 published two patient cases, but one was included in the report by rgani et al. 3 Geller et al 8 published two patient cases, but one was included in the report by rgani et al. 4 bbreviations:, transcription factor E; TFE3, transcription factor E3; HM45, human melanoma black 45; MITF, microphthalmia-associated transcription factor; RCC, renal cell carcinoma; EM, epithelial membrane antigen; SM, smooth muscle actin; N, not available. Pecciarini et al 6 ). In the gene, the breakpoint was at 94 nucleotides numbered from the 5 end of exon3 of (Fig 3D, arrow) and fell in the 289 bp breakpoint cluster region (breakpoints 237 and 96, reported by Kuiper et al 1 ; breakpoints 162, 144, 139, 122, and 70, reported by rgani et al 4 ; and breakpoint 359, reported by Pecciarini et al 6 ). For our patient, we used the same primers for DN-PCR and RT-PCR as those described by rgani et al. 4 The expected product of lpha- fusion was obtained via DN-PCR, whereas RT-PCR failed to do so. We think the reason for the RT-PCR failure was likely because RN extracted from paraffin-embedded tissue is usually partially degenerated. 4 The fusion of lpha- was detected in our patient case by sequencing analysis of the DN-PCR product. Interestingly, a novel fusion point of lpha- was detected. RCC with t(6;11) translocation may express epithelial and melanocytic markers, inevitably requiring differentiation from clear cell RCCs, papillary RCCs, and angiomyolipomas. RCC with t(6;11) translocation also shares many features with renal carcinoma associated with Xp11.2 translocations, so differentiation between these two diseases is also necessary. bipolar pattern, specific nuclear labeling for, and molecular detection of lpha- fusion gene can help in distinguishing RCC with t(6;11) translocation from other neoplasms of the kidney. Prognostically, RCC with t(6;11) translocation seems to be indolent. Of the reported 13 patients for whom treatment information was available, 10 underwent radical nephrectomy, 1,3,4,6,7,9,10 three received partial nephrectomy, 2,4,9 and none underwent postoperative chemotherapy or radiation therapy after surgery. Only one patient presented with metastasis and died 3 months after nephrectomy, 7 whereas there was no evidence of recurrence or metastasis in the others during follow-up from 3 to 84 months. Identification of the exact biobehavioral criteria for this disease entity must be determined on the basis of more patient cases. He-Qin Zhan, Chao-Fu Wang, Xiong-Zeng Zhu, and Xiao-Li Xu Fudan University Shanghai Cancer Center; and Shanghai Medical College, Fudan University, Shanghai, China UTHORS DISCLOSURES OF POTENTIL CONFLICTS OF INTEREST The author(s) indicated no potential conflicts of interest. REFERENCES 1. Kuiper RP, Schepens M, Thijssen J, et al: Upregulation of the transcription factor in t(6;11)(p21;q13)-positive renal cell carcinomas due to promoter substitution. Hum Mol Genet 12: , Davis IJ, Hsi L, rroyo JD, et al: Cloning of an lpha- fusion in renal tumours harboring the t(6;11)(p21;q13) chromosome translocation. Proc Natl cad Sci U S 100: , rgani P, Hawkins, Griffin C, et al: distinctive pediatric renal neoplasm characterised by epitheolid morphology, basement membrane production, focal HM45 immunoreactivity, and t(6;11)(p21.1;q12) chromosome translocation. m J Pathol 158: , rgani P, Laé M, Hutchinson, et al: Renal carcinomas with the t(6; 11)(p21; q12): Clinicopathologic features and demonstration of the specific alpha- fusion gene by immunohistochemistry, RT-PCR, and DN PCR. m J Surg Pathol 29: , rgani P, Laé M, allard ET, et al: Translocation carcinomas of the kidney after chemotherapy in childhood. J Clin Oncol 24: , Pecciarini L, Cangi MG, Lo Cunsolo C, et al: Characterization of t(6;11)(p21; q12) in a renal-cell carcinoma of an adult patient. Genes Chromosomes Cancer 46: , Camparo P, Vasiliu V, Molinie V, et al: Renal translocation carcinomas: Clinicopathologic, immunohistochemical and gene expression profiling analysis e by merican Society of Clinical Oncology JOURNL OF CLINICL ONCOLOGY

5 Diagnosis in Oncology of 31 cases with a review of the literature. m J Surg Pathol 32: , Geller JI, rgani P, deniran, et al: Translocation renal cell carcinoma: Lack of negative impact due to lymph node spread. Cancer 112: , Hora M, Hes O, Urge T, et al: distinctive translocation carcinoma of the kidney [ rossete-like forming, t(6;11), HM45-positive renal tumor]. Int Urol Nephrol 41: , Suárez-Vilela D, Izquierdo-García F, Méndez-Álvarez JR, et al: Renal translocation carcinoma with expression of : Presentation of a case with distinctive histological and immunohistochemical features. Int J Surg Pathol [epub ahead of print on ugust 16, 2009] DOI: /JCO ; published online ahead of print at on September 7, 2010 cknowledgment We thank Shanghai Majorio Technologies for assistance with sequencing and Wen-Tao Huang for assistance with reverse transcription polymerase chain reaction. He-Qin Zhan and Chao-Fu Wang contributed equally to this work by merican Society of Clinical Oncology e713

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