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A Comprehensive Analysis of PAX8 Expression in Human Epithelial Tumors Anna R

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A Comprehensive Analysis of PAX8 Expression in Human Epithelial Tumors Anna R ORIGINAL ARTICLE A Comprehensive Analysis of PAX8 Expression in Human Epithelial Tumors Anna R. Laury, MD,*w Ruth Perets, MD, PhD,z Huiying Piao,z Jeffrey F. Krane, MD, PhD,*w Justine A. Barletta, MD,*w Christopher French, MD,*w Lucian R. Chirieac, MD,*w Rosina Lis, MD,z Massimo Loda, MD,*w z Jason L. Hornick, MD, PhD,*w Ronny Drapkin, MD, PhD,*w z and Michelle S. Hirsch, MD, PhD*wy including but not limited to those from the prostate, colon, Abstract: PAX8 is a paired-box gene important in embryogen- stomach, liver, adrenal gland, and head and neck, and small esis of the thyroid, Mu¨llerian, and renal/upper urinary tracts, cell carcinomas from the lung, cervix, and ovary, were PAX8 and expression of PAX8 has been previously described in negative. PAX8 specificity was confirmed by Western blot carcinomas from each of these sites. However, a large study analysis, as expression was detected only in ovarian and RCC including a wide variety of epithelial neoplasms from multiple cell lines. These results show that PAX8 is a highly sensitive organ sites other than the thyroid, kidney, or Mu¨llerian system marker for thyroid, renal, Mu¨llerian, and thymic tumors. has not been performed. The goal of this study was to evaluate Importantly, all lung adenocarcinomas, breast and adrenal the utility of PAX8 immunostaining based on the evaluation of neoplasms, and the majority of gastrointestinal tumors were a wide range of epithelial tumors. PAX8 immunohistochemistry negative for PAX8. Therefore, PAX8 is an excellent marker for was performed on 1357 tumors (486 tumors in whole-tissue confirming primary tumor site. In a subset of cases, additional sections and 871 tumors in tissue microarrays, predominantly markers, including but not limited to thyroid transcription epithelial) from multiple organs. Only nuclear staining was factor-1, RCC, and Wilms tumor-1, may be needed to distinguish scored as positive, and tumors were evaluated for the extent and between the 3 most common PAX8-positive tumors. intensity of staining. Western blot analysis with PAX8 was also performed on multiple tumor cell lines. Nuclear PAX8 staining Key Words: PAX8, immunohistochemistry, carcinoma, Mu¨ller- was present in 91% (60 of 66) of thyroid tumors, 90% (158 of ian, renal, thyroid, ovarian, thymus 176) of renal cell carcinomas (RCCs), 81% (13 of 16) of renal (Am J Surg Pathol 2011;35:816–826) oncocytomas, 99% (164 of 165) of high-grade ovarian serous carcinomas, 71% (32 of 49) of nonserous ovarian epithelial neoplasms, 91% (10 of 11) of cervical epithelial lesions, and 98% (152 of 155) of endometrial adenocarcinomas. Of the n addition to morphologic features, immunohistochem- remaining 719 evaluated tumors, only 30 cases (4%), including Iistry is routinely used to determine the primary site of 12 thymic neoplasms, 3 bladder urothelial carcinomas, 4 lung many metastatic tumors, especially those that are poorly squamous cell carcinomas, 2 esophageal adenocarcinomas, differentiated or have unusual morphology. Traditionally, 1 pancreatic adenocarcinoma, 2 cholangiocarcinomas, 1 ovarian the combined use of CK7 and CK20 is helpful in Sertoli-Leydig cell tumor, 1 ovarian sex cord stromal tumor, distinguishing lung, breast, Mu¨llerian, or head and neck 3 testicular mixed germ cell tumors, and 1 acinic cell carcinoma, (CK7 positive, CK20 negative) versus gastrointestinal showed at least weak or focal PAX8 positivity. The unexpected (CK20 positive, CK7 negative, or CK20 and CK7 finding was diffuse, moderate staining of PAX8 in a subset of positive) primaries. However, these 2 markers alone are thymomas and thymic carcinomas. The 689 remaining tumors, neither sensitive nor specific. The use of lineage-specific markers, such as thyroid transcription factor-1 (TTF-1), 14,32 17,26,46 y Wilms tumor-1 (WT-1), mammoglobin, octa- From the *Department of Pathology; Women’s and Perinatal mer-binding transcription factor 4,15 and renal cell Pathology Division, Department of Pathology, Brigham and 3 Women’s Hospital; zDepartment of Medical Oncology, Center for carcinoma (RCC), provides additional help in narrowing Molecular Oncologic Pathology, Dana Farber Cancer Institute; and down primary tumor site or cell differentiation; however, wHarvard Medical School, Boston, MA. there still exist cases in which the low sensitivity of these Supported in part by a Harvard Medical School Center of Excellence in markers limits their utility. Women’s Health Grant (MSH), a Dana Farber Cancer Institute Friends Award (MSH), and by the Ann Schreiber Program of PAX8 is a member of the paired-box family of genes Excellence Grant from the Ovarian Cancer Research Fund (RP). that is expressed during organogenesis of the thyroid Presented in part at the 99th Annual Meeting of the United States and gland, Mu¨llerian tract, and kidney.7,37,38 PAX8 has Canadian Academy of Pathology, Washington DC, 2010. also been shown to be expressed in a subset of renal,44 Correspondence: Michelle S. Hirsch, MD, PhD, Department of bladder,43 and thyroid neoplasms,36 and in ovarian Pathology, Brigham and Women’s Hospital, 75 Francis Street, 6,21,26,35 Amory-3, Boston, MA 02115 (e-mail: [email protected]). malignancies. The absence of PAX8 expression Copyright r 2011 by Lippincott Williams & Wilkins in breast carcinoma35 and malignant mesothelioma21 is 816 | www.ajsp.com Am J Surg Pathol Volume 35, Number 6, June 2011 Am J Surg Pathol Volume 35, Number 6, June 2011 PAX8 in Epithelial Tumors especially useful when the differential diagnosis includes TABLE 1. PAX8 Expression in Human Tumors from Multiple ovarian carcinoma. In well-differentiated neuroendocrine Organs tumors, PAX8 may be helpful in determining primary No. Total No. Cases site, and in predicting favorable outcome in a subset Tumor Type Positive (%Positive) of pancreatic endocrine tumors.25,41 These studies not- withstanding, a single comprehensive evaluation of PAX8 Genitourinary RCC expression across a wide variety of benign and malignant Clear cell RCC 115 123 (93) epithelial tumors from multiple organ sites has not been Papillary RCC 19 25 (76) reported. Chromophobe RCC 4 5 (80) Therefore, the purpose of this study was to evaluate CDC 1 2 (50) Xp11 translocation carcinoma 5 6 (83) the utility of PAX8 expression in a large number of Mucinous tubular and spindle 3 3 (100) neoplasms (predominantly epithelial) using immunohis- cell CA tochemistry and a combination of tissue microarray Clear cell tubulopapillary RCC 4 4 (100) (TMA) and whole-tissue sections. Tubulocystic RCC 1 1 (100) NOS or metastatic 5 6 (83) Renal angiomyoadenomatous tumor 1 1 (100) MATERIALS AND METHODS Angiomyolipoma 0 6 (0) Oncocytoma 13 16 (81) Case Selection Bladder urothelial carcinoma 3 17 (18) After approval from the Institutional Review Board Clear cell adenocarcinoma of bladder/ 2 2 (100) ureter at Brigham & Women’s Hospital, 1357 cases were evaluated Prostate adenocarcinoma 0 86 (0) using whole-tissue (N = 486) and TMA (N = 871) sections; Gastrointestinal some of the latter cases have been described else- Gastric ACA 0 22 (0) where.4,8,21,24 Tissues were obtained from the head and Gastric (M) 0 10 (0) Colon ACA 0 41 (0) neck, lung, breast, thyroid, parathyroid, thymus, adrenal Colon (M) 0 11 (0) gland, kidney, esophagus, stomach, pancreas, small bowel, Colon (SQ) 0 2 (0) large bowel, appendix, testis, ovary, endometrium, cervix, Anal (SQ) 0 2 (0) and bladder. The list of individual tumor types from each Appendiceal (M) 0 30 (0) organ is presented in Table 1. Normal tissues adjacent to Gallbladder ACA 0 1 (0) Cholangiocarcinoma 2 2 (100) neoplasms and also control tissues in the TMAs were Esophageal ACA 2 8 (25) evaluated concurrently (Fig. 1). Esophageal (M) 0 2 (0) Esophageal (SQ) 0 7 (0) Immunohistochemistry Pancreatic ACA 1 12 (8) Immunohistochemistry was performed using the Pancreatic (M) 0 4 (0) Pancreatic (solid pseudopapillary) 0 1 (0) Envision Plus/Horseradish Peroxidase system (Dako, Hepatocellular carcinoma 0 6 (0) Carpinteria, CA) and a polyclonal antibody to PAX8 Breast (1:800 dilution; Proteintech Group Inc, Chicago, IL) as Invasive ductal carcinoma 0 91 (0) previously described.21 In brief, paraffin-embedded sec- Invasive lobular carcinoma 0 19 (0) Mixed carcinoma 0 19 (0) tions were incubated in hydrogen peroxidase and absolute Head and neck alcohol for 30 minutes to block endogenous peroxidase Squamous cell carcinoma 0 5 (0) activity. Antigen retrieval was performed using pressure Squamous dysplasia 0 6 (0) cooker pretreatment in a citrate buffer (pH = 6.0). Tissue Acinic cell carcinoma 1 3 (33) sections were subsequently incubated with the primary Adenoid cystic carcinoma 0 13 (0) Basal cell adenoma/carcinoma (salivary 0 4 (0) antibody for 40 minutes at 251C. After tris-buffered saline gland) (rinses, the tissue was incubated using the Envision Plus Mucoepidermoid carcinoma 0 8 (0) secondary antibody for 30 minutes, followed by diamino- Olfactory neuroblastoma 0 3 (0) benzidine for 5 minutes. Appropriate positive (tonsil Polymorphous low grade ACA 0 3 (0) Pleomorphic adenoma 0 4 (0) lymphocytes) and negative (incubation with secondary Carcinoma ex pleomorphic adenoma 0 1 (0) antibody only) controls were stained in parallel for each Sinonasal adenocarcinoma 0 2 (0) round of immunohistochemistry. PAX8 was evaluated for High grade salivary gland ACA 0 4 (0) nuclear staining only. Immunoreactivity with normal B Salivary duct carcinoma 0 5 (0) lymphocytes was used as an internal positive control and Myoepithelial carcinoma 0 2 (0) Salivary carcinomas/ACA, NOS 0 12 (0) as an intensity reference when present. Atypical carcinoid (larynx) 0 6 (0) Clear cell odontogenic carcinoma 0 1 (0) Western Blot Analysis PD carcinoma, NOS 0 3 (0) Eighteen established renal, ovarian, prostatic, Lung Adenocarcinoma 0 120 (0) breast, colonic, cervical, and brain tumor cell lines were Squamous cell carcinoma 4 12 (33) also used to evaluate PAX8 protein expression.
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