MOC-31 Exhibits Superior Reactivity Compared With Ber-EP4 in Invasive Lobular and Ductal Carcinoma of the Breast. A Tissue Microarray Study

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1 RESEARCH ARTICLE MOC-31 Exhibits Superior Reactivity Compared With Ber-EP4 in Invasive Lobular and Ductal Carcinoma of the Breast A Tissue Microarray Study Reetesh K. Pai, MD and Robert B. West, MD Abstract: Distinguishing between reactive mesothelial proliferations and adenocarcinoma is often very difficult. Ancillary studies, in particular immunohistochemistry, are often critical in detecting malignant epithelial cells, especially in serous effusion specimens. MOC-31 and Ber-EP4 are antibodies which target the epithelial cell adhesion molecule (Ep-CAM, TACSTD1) expressed in epithelial cells, and both are useful in distinguishing metastatic adenocarcinoma from reactive mesothelial cells. However, the reactivity of MOC-31 and Ber-EP4 with breast carcinoma, one of the more common carcinomas involving serous effusions, has not been extensively studied. We analyzed the immunohistochemical expression of MOC-31 and Ber-EP4 using tissue microarrays containing invasive ductal carcinoma (191 cases), invasive lobular carcinoma (44 cases), and 102 other carcinoma types comprising primary carcinomas of lung, gynecologic tract, pancreas, colon, gastric, esophageal, prostate, head and neck, hepatic, and renal origin. For MOC-31, 184 of 191 (96%) invasive ductal carcinomas and 39 of 44 (89%) invasive lobular carcinomas exhibited diffuse positive staining. In contrast, for Ber-EP4, 121 of 183 (66%) invasive ductal carcinomas and 11 of 40 (27.5%) invasive lobular carcinomas exhibited diffuse positive staining. With the exception of 1 case of esophageal adenocarcinoma, all other adenocarcinomas (86 of 87 cases) exhibited diffuse staining with both Ber-EP4 and MOC-31. MOC-31 and Ber-EP4 exhibited identical staining with all other carcinoma types. Our findings indicate that MOC- 31 is superior to Ber-EP4 in detecting both invasive lobular and ductal carcinoma of the breast. Key Words: MOC-31, Ber-EP4, TACSTD1, breast, carcinoma (Appl Immunohistochem Mol Morphol 2009;17: ) Distinguishing between reactive mesothelial proliferations and adenocarcinoma is often very difficult. Reactive mesothelial cells may at times exhibit significant Received for publication July 2, 2008; accepted August 28, From the Department of Pathology, Stanford University, Stanford, CA. Reprints: Reetesh K. Pai, MD, Department of Pathology, Stanford University, 300 Pasteur Drive, Room H-2110, Stanford, CA ( Copyright r 2009 by Lippincott Williams & Wilkins cytologic atypia raising concern for carcinoma. Alternatively, carcinoma may occasionally be cytologically bland and lack overt features of malignancy. The challenge in distinguishing benign mesothelial cells from carcinoma is made more difficult when evaluating cytologic specimens given the limited sample size. Lobular carcinoma of the breast is particularly notorious for mimicking reactive mesothelial cells in cytologic preparations. A marker that can reliably label malignant epithelial cells would have tremendous diagnostic utility. Immunohistochemical staining with MOC-31 and Ber-EP4 has been shown to be useful in distinguishing metastatic adenocarcinoma from reactive mesothelial cells. 1 4 Both Ber-EP4 and MOC-31 antibodies target the extracellular domain of epithelial cell adhesion molecule (Ep-CAM) which is involved with cell-cell adhesion of epithelial cells, 5 and thus do not react with mesothelial cells. 1,2 Although these antibodies have been found to react with most epithelial cells and epithelial neoplasms, the reactivity of these antibodies with a significant number of ductal and lobular breast carcinoma subtypes has not been previously reported. The purpose of this study is to evaluate the differences in reactivity between MOC-31 and Ber-EP4 in invasive lobular and ductal carcinoma of the breast. MATERIALS AND METHODS Construction of Tissue Microarrays Two tissue microarrays containing 277 and 125 tissue cores, for a total of 402 tissue cores, each measuring 0.6 mm, were created using a tissue arrayer (Beecher Instruments, Silver Spring, MD) according to a previously described method. 6 Representative areas from each case were selected for the microarrays from paraffin blocks based on hematoxylin and eosin-stained sections. The tissue microarrays contained cases of primary breast carcinoma including invasive ductal carcinoma (191) and invasive lobular carcinoma (44). The breast carcinomas were divided into ductal and lobular subtypes based on conventional light microscopic morphologic features. 7 For the small subset of cases in which the distinction between carcinoma subtypes was difficult using conventional light microscopy, E-cadherin immunohistochemical staining 202 Appl Immunohistochem Mol Morphol Volume 17, Number 3, May 2009

2 Appl Immunohistochem Mol Morphol Volume 17, Number 3, May 2009 MOC-31 and Ber-EP4 in Invasive Breast Carcinoma (clone A2C7, Zymed, 1:600 dilution) was employed to differentiate between lobular and ductal carcinoma. 7,8 In addition, 102 other carcinoma types comprising primary carcinomas of lung, gynecologic tract, pancreas, colon, gastric, esophageal, prostate, head and neck, hepatic, and renal origin were included. Tissue cores of normal human epithelial, mesenchymal, and lymphoid tissue were included as positive and negative controls. MOC-31 and Ber-EP4 Immunohistochemistry Immunohistochemical stains were performed on 4-mm sections from tissue array blocks, which were deparaffinized in xylene and hydrated in graded alcohols. Antigen retrieval was performed in 0.01 M sodium citrate buffer using a pressure cooker (30 min at 1151C for Ber- EP4) or a waterbath (30 min at 951C for MOC-31). Immunohistochemical staining for Ber-EP4 (1:400 dilution; Dako) and MOC-31 (1:120 dilution; Dako) was performed with the Dako Autostainer (Dako Corporation, Carpinteria, CA). Detection was carried out using Dako Envision. Internal positive and negative controls were available for both antibodies from the numerous tissue cores of normal human epithelium and mesenchymal tissue present in our tissue microarrays. For both antibodies, staining was scored as diffuse (>20% of tumor cells), focal (5% to 20% of tumor cells), negative, or uninterpretable due to lack of lesional tissue in the tissue core on the basis of either membranous and/ or cytoplasmic staining. Faint cytoplasmic staining or reactivity in <5% of cells was interpreted as negative. This scoring system was devised based on the author s experience with MOC-31 and Ber-EP4 in evaluating effusion specimens for metastatic carcinoma in routine clinical practice. Labeling of greater than 20% of the cells of interest in an effusion specimen provides support for a neoplastic epithelial cell proliferation. Focal staining is not entirely diagnostic of neoplasia and generally requires additional studies to confirm the presence of carcinoma. Scoring systems with similar cutoffs have been published for these antibodies. 9 Estrogen and Progesterone Receptor and HER2 Characterization of Breast Carcinoma Cases Estrogen (clone 1d5, Dako, 1:80 dilution) and progesterone receptor (clone PgR36, Dako, 1:80 dilution) immunohistochemistry was performed in 210 breast carcinoma cases and scored as positive (any labeling) or negative (no labeling). Fluorescence in situ hybridization (FISH) was performed in 167 breast carcinoma cases using the dual-color PathVysion Her-2 DNA probe kit containing a HER2 locus-specific probe (LSI HER2) and a control probe specific for the pericentromeric region of chromosome no. 17 (D17Z1). A total of 25 interphase nuclei were scored for the number of HER2 and D17Z1 signals. A ratio <1.8 is considered to be negative, between 1.8 and 2.2 ambiguous, and >2.2 positive for HER2 amplification based on Food and Drug Administration-approved criteria. Cells with innumerable (>10) HER2 signals are scored as having 10 signals. RESULTS MOC-31 and Ber-EP4 had vastly different reactivities with invasive lobular and ductal carcinoma of the breast (Table 1). For MOC-31, 184 of 191 (96%) invasive ductal carcinomas and 39 of 44 (89%) invasive lobular carcinomas exhibited diffuse positive staining (Fig. 1). In contrast, for Ber-EP4, 121 of 183 (66%) invasive ductal carcinomas and 11 of 40 (27.5%) invasive lobular carcinomas exhibited diffuse positive staining (Fig. 2). For both MOC-31 and Ber-EP4, immunostaining was typically intense and predominantly membranous. Variable cytoplasmic reactivity was also noted in most cases in addition to membranous staining. With the exception of 1 case of esophageal adenocarcinoma, all other adenocarcinomas exhibited diffuse staining with both Ber-EP4 and MOC-31 (Table 2). Immunostaining was usually intensely membranous with variable cytoplasmic reactivity. Hepatocellular carcinoma, conventional renal cell carcinoma, and head and neck squamous cell carcinoma commonly lacked expression of Ber-EP4 and MOC-31 (Table 2). Given the very low numbers of MOC-31 negative breast carcinoma cases, it is not possible to adequately compare the differences between MOC-31 and Ber- Ep4 negative breast carcinomas with respect to tumor grade, estrogen receptor status, progesterone receptor status, and HER2 amplification by FISH. Of the breast carcinoma cases in which clinicopathologic data were available, Ber-EP4 negative invasive ductal carcinomas were typically grade 1 or 2 tumors (31 of 33 cases), which expressed estrogen receptor (33 of 33 positive) and progesterone receptor (28 of 33 positive) and lacked HER2 amplification by FISH (Table 3). In contrast, the majority of the Ber-EP4 negative invasive lobular carcinomas (9 of 16 cases) were grade 2 or 3 suggesting that higher-grade invasive lobular carcinomas may lose Ber-EP4 expression. TABLE 1. Summary of Immunohistochemical Staining of Breast Carcinoma With MOC-31 and Ber-EP4 Carcinoma Type Diffuse Positive MOC-31 Focal Positive Diffuse Positive Ber-EP4 Focal Positive Invasive lobular 39/44 (89) 1/44 (2) 4/44 (9) 11/40 (27.5) 3/40 (7.5) 26/40 (65) Invasive ductal 184/191 (96) 2/191 (1) 5/191 (3) 121/183 (66) 16/183 (9) 46/183 (25) r 2009 Lippincott Williams & Wilkins 203

3 Pai and West Appl Immunohistochem Mol Morphol Volume 17, Number 3, May 2009 FIGURE 1. Diffuse membranous staining of invasive ductal carcinoma of the breast is identified with MOC-31 (A) in contrast to negative staining with Ber-EP4 in this case (B). Fewer cases of invasive ductal carcinoma (121 of 183 cases) exhibited diffuse membranous staining with Ber-EP4 (C) (150 magnification). DISCUSSION Ber-EP4 and MOC-31 are monoclonal antibodies directed against the Ep-CAM which mediates cell-cell adhesion of epithelial cells. 5,11 14 Cell-cell adhesions are mediated by the extracellular domain of the protein containing 2 epidermal growth factor-like domains whereas the intracellular domain interacts with actin cytoskeleton of epithelial cells. 5,15 Both Ber-EP4 and MOC-31 are known to react with the extracellular epidermal growth factor-like I domain of Ep-CAM. 5,16 Given that Ep-CAM is expressed in most of epithelial tissues, Ber-EP4 and MOC31 immunohistochemistry can serve as a useful tool in labeling malignant epithelial cells. MOC-31 is an antibody originally raised against a smallcelllungcarcinomacellline. 14 Although originally targeted against small cell carcinoma, numerous studies of the reactivity of MOC-31 in adenocarcinoma from various anatomic sites have been reported, primarily in the cytopathology literature. 1,17 19 Most studies have shown MOC-31 to be highly sensitive in detecting malignant epithelial cells in effusion specimens. 1,19 However, most reports in the literature include only a small number of cases and do not differentiate between lobular and ductal breast carcinoma subtypes. In their original characterization, Latza et al 11 found that Ber-EP4 reacted with all normal epithelial FIGURE 2. Diffuse membranous staining of invasive lobular carcinoma of the breast is identified with MOC-31 (A) in contrast to negative staining with Ber-EP4 in this case (B). Fewer cases of invasive lobular carcinoma (11 of 40 cases) exhibited diffuse membranous staining with Ber-EP4 (C) (150 magnification). TABLE 2. Summary of Immunohistochemical Staining of MOC-31 and Ber-EP4 With Other Carcinoma Types MOC-31 Ber-EP4 Carcinoma Type Diffuse Positive Diffuse Positive Lung adenocarcinoma 11/11 0/11 10/11* 0/11 Lung squamous cell 5/5 0/5 3/5* 0/5 Lung small cell 6/6 0/6 6/6 0/6 Ovarian surface epithelial 16/16 0/16 17/17 0/17 Uterine endometrioid 11/11 0/11 11/11 0/11 Uterine cervical 4/4 0/4 4/4 0/4 adenocarcinoma Pancreas adenocarcinoma 8/8 0/8 8/8 0/8 Colon adenocarcinoma 10/10 0/10 11/11 0/11 Gastric adenocarcinoma 9/9 0/9 9/9 0/9 Esophageal 4/5 1/5 4/5 1/5 adenocarcinoma Esophageal squamous cell 3/4 1/4 3/4 1/4 Prostate 13/13 0/13 13/13 0/13 Head/neck squamous cell 4/13 9/13 3/13 10/13 Hepatocellular 1/7 6/7 1/7 6/7 Urothelial 14/14 0/14 11/14 3/14 Conventional renal cell 2/8 6/8 2/8 6/8 Papillary renal cell 6/6 0/6 5/6 1/6 Chromophobe renal cell 4/4 0/4 4/4 0/4 *One case of lung adenocarcinoma and 2 cases of lung squamous cell carcinoma exhibited focal staining with Ber-EP4. cells with the exception of parietal cells of gastric glands, apical cell layers of squamous epithelium, and adult hepatocytes. 20 Importantly, normal or reactive mesothelial cells and nonepithelial tissue did not react with Ber- EP4. 2,11 Although absent in normal superficial squamous epithelium, increased Ep-CAM expression has been shown in squamous cell carcinomas. 20 In a subsequent report, Ber-EP4 was found to react with 72 of 83 (87%) adenocarcinomas; however, 8 of 25 cases of invasive breast carcinoma, including 5 ductal carcinomas and 3 lobular carcinomas, were nonreactive. 2 Although this early study suggested diminished reactivity of breast carcinomas with Ber-EP4, only a small number of cases were analyzed making it difficult to reach definite conclusions. To our knowledge, no subsequent study including a large number of cases has examined the reactivity of Ber-EP4 with breast carcinoma. Our tissue microarray data strongly suggest that MOC-31 is superior to Ber-EP4 in detecting both invasive lobular and ductal carcinoma of the breast. 2 Although most studies have shown MOC-31 to diffusely react with breast carcinoma, Delahaye et al 21 reported diffuse MOC- 31 staining in only 8 of 17 cases (47%) of metastatic breast carcinoma in serous effusions. Technical issues likely account for this discordant finding. First, it is not clear whether the antibody used by Delahaye et al is the same one used in this study. Second, and most importantly, Delahaye et al employed immunocytochemical staining performed on cytologic smear preparations in contrast to formalin-fixed paraffin-embedded tissue 204 r 2009 Lippincott Williams & Wilkins

4 Appl Immunohistochem Mol Morphol Volume 17, Number 3, May 2009 MOC-31 and Ber-EP4 in Invasive Breast Carcinoma TABLE 3. Comparison of Tumor Characteristics of Invasive Ductal and Lobular Carcinomas With MOC-31 and Ber-EP4 Reactivities Characteristic MOC-31 negative Ductal Carcinomas Ber-EP4 negative Ductal Carcinomas MOC-31 negative Lobular Carcinomas Ber-EP4 negative Lobular Carcinomas Grade /3 11/33 1/1 7/16 2 1/3 20/33 0/1 7/16 3 0/3 2/33 0/1 2/16 Estrogen receptor Positive 3/3 33/33 N/A 8/10 0/3 0/33 2/10 Progesterone receptor Positive 2/3 28/33 N/A 7/10 1/3 5/33 3/10 Her2 fluorescence in situ hybridization <1.8 3/3 28/31 N/A 7/ /3 0/31 1/8 >2.2 0/3 3/31 0/8 Mean size in cm (range) 1.9 ( ) 2.0 ( ) ( ) N/A indicates not available. sections, which were used in our study. In our experience, immunocytochemical staining is prone to significant interpretative error and obtaining appropriately reactive positive and negative controls for these studies is difficult. Despite this one exception, our results are comparable with other studies and indicate that MOC-31 is a highly sensitive marker of epithelial malignancy, including invasive ductal and lobular carcinoma of the breast. 1,17,19,22 MOC31 may be particularly helpful in evaluating cytologic specimens for the presence of metastatic lobular carcinoma of the breast. Because breast carcinoma is one of the more common causes of malignant effusions, the diminished reactivity of Ber-EP4 with breast carcinoma represents a significant shortcoming for this antibody. However, additional studies are necessary to further elucidate the differences in reactivities of these antibodies in cytologic preparations. The reason for the difference between MOC-31 and Ber-EP4 staining, particularly with lobular carcinoma of the breast, is unclear. Given that both antibodies react with the extracellular domain of Ep-CAM, one would expect similar reactivities with these antibodies. Various cell adhesion molecule systems have been identified in human epithelial tissues. 5 In addition to Ep-CAM, the cadherin family of proteins plays a crucial role in cell-cell adhesion in epithelial cells, and most epithelial cells typically coexpress Ep-CAM and E-cadherin. 23,24 Of interest, lobular breast carcinoma is known to exhibit decreased expression of E-cadherin, due to a mutation in E-cadherin, by immunohistochemistry. 25,26 Recently, Ep- CAM has been shown to modulate cell-cell interactions mediated by E-cadherin. 24,27 Overexpression of Ep-CAM during cell division leads to dissociation of cadherins with accumulation of E-cadherin/b-catenin complexes in the cell cytoplasm. 24 After cell division, Ep-CAM expression declines and higher levels of E-cadherin mediate intercellular adhesion. 5 These findings suggest significant cross-signaling between the Ep-CAM and classic adherens-based adhesion systems in epithelial cells during epithelial cell proliferation. One can postulate that the loss of E-cadherin mediated cell adhesion in lobular carcinoma results in the alteration of the Ep-CAM based adhesion system and may lead to the selectively diminished expression of the Ep-CAM antigen recognized by the monoclonal antibody Ber-EP4. Our results also suggest that, in contrast to MOC-31, Ber-EP4 expression is diminished with increasing grade of lobular carcinoma. However, further studies are necessary to evaluate the presence and function of Ep-CAM in invasive lobular carcinoma. REFERENCES 1. Morgan RL, De Young BR, McGaughy VR, et al. MOC-31 aids in the differentiation between adenocarcinoma and reactive mesothelial cells. Cancer. 1999;87: Sheibani K, Shin SS, Kezirian J, et al. Ber-EP4 antibody as a discriminant in the differential diagnosis of malignant mesothelioma versus adenocarcinoma. Am J Surg Pathol. 1991;15: Yaziji H, Battifora H, Barry TS, et al. Evaluation of 12 antibodies for distinguishing epithelioid mesothelioma from adenocarcinoma: identification of a three-antibody immunohistochemical panel with maximal sensitivity and specificity. Mod Pathol. 2006;19: Marchevsky AM, Wick MR. Evidence-based guidelines for the utilization of immunostains in diagnostic pathology: pulmonary adenocarcinoma versus mesothelioma. Appl Immunohistochem Mol Morphol. 2007;15: Winter MJ, Nagtegaal ID, van Krieken JH, et al. The epithelial cell adhesion molecule (Ep-CAM) as a morphoregulatory molecule is a tool in surgical pathology. Am J Pathol. 2003;163: Kononen J, Bubendorf L, Kallioniemi A, et al. Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat Med. 1998;4: Ellis IOSS, Schnitt SJ, Sastre-Garau X, et al. Invasive breast carcinoma. In: Tavassoli FA, Devilee P, eds. WHO Pathology and Genetics: Tumours of the Breast and Female Genital Organs. Lyon, France: IARC Press; 2003: Longacre TA, Ennis M, Quenneville LA, et al. Interobserver agreement and reproducibility in classification of invasive breast carcinoma: an NCI breast cancer family registry study. Mod Pathol. 2006;19: King JE, Thatcher N, Pickering CA, et al. Sensitivity and specificity of immunohistochemical markers used in the diagnosis of epithelioid mesothelioma: a detailed systematic analysis using published data. Histopathology. 2006;48: Elston CW, Ellis IO. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience r 2009 Lippincott Williams & Wilkins 205

5 Pai and West Appl Immunohistochem Mol Morphol Volume 17, Number 3, May 2009 from a large study with long-term follow-up. Histopathology. 1991;19: Latza U, Niedobitek G, Schwarting R, et al. Ber-EP4: new monoclonal antibody which distinguishes epithelia from mesothelial. J Clin Pathol. 1990;43: Litvinov SV, Bakker HA, Gourevitch MM, et al. Evidence for a role of the epithelial glycoprotein 40 (Ep-CAM) in epithelial cell-cell adhesion. Cell Adhes Commun. 1994;2: Beiske K, Myklebust AT, Aamdal S, et al. Detection of bone marrow metastases in small cell lung cancer patients. Comparison of immunologic and morphologic methods. Am J Pathol. 1992;141: Myklebust AT, Beiske K, Pharo A, et al. Selection of anti-sclc antibodies for diagnosis of bone marrow metastasis. Br J Cancer Suppl. 1991;14: Balzar M, Bakker HA, Briaire-de-Bruijn IH, et al. Cytoplasmic tail regulates the intercellular adhesion function of the epithelial cell adhesion molecule. Mol Cell Biol. 1998;18: Gosens MJ, van Kempen LC, van de Velde CJ, et al. Loss of membranous Ep-CAM in budding colorectal carcinoma cells. Mod Pathol. 2007;20: Edwards C, Oates J. OV 632 and MOC 31 in the diagnosis of mesothelioma and adenocarcinoma: an assessment of their use in formalin fixed and paraffin wax embedded material. J Clin Pathol. 1995;48: Ruitenbeek T, Gouw AS, Poppema S. Immunocytology of body cavity fluids. MOC-31, a monoclonal antibody discriminating between mesothelial and epithelial cells. Arch Pathol Lab Med. 1994;118: Lyons-Boudreaux V, Mody DR, Zhai J, et al. Cytologic malignancy versus benignancy: how useful are the newer markers in body fluid cytology? Arch Pathol Lab Med. 2008;132: Litvinov SV, van Driel W, van Rhijn CM, et al. Expression of Ep- CAM in cervical squamous epithelia correlates with an increased proliferation and the disappearance of markers for terminal differentiation. Am J Pathol. 1996;148: Delahaye M, van der Ham F, van der Kwast TH. Complementary value of five carcinoma markers for the diagnosis of malignant mesothelioma, adenocarcinoma metastasis, and reactive mesothelium in serous effusions. Diagn Cytopathol. 1997;17: Sosolik RC, McGaughy VR, De Young BR. Anti-MOC-31: a potential addition to the pulmonary adenocarcinoma versus mesothelioma immunohistochemistry panel. Mod Pathol. 1997;10: Nathke IS, Hinck LE, Nelson WJ. Epithelial cell adhesion and development of cell surface polarity: possible mechanisms for modulation of cadherin function, organization and distribution. J Cell Sci Suppl. 1993;17: Litvinov SV, Balzar M, Winter MJ, et al. Epithelial cell adhesion molecule (Ep-CAM) modulates cell-cell interactions mediated by classic cadherins. J Cell Biol. 1997;139: Droufakou S, Deshmane V, Roylance R, et al. Multiple ways of silencing E-cadherin gene expression in lobular carcinoma of the breast. Int J Cancer. 2001;92: Moll R, Mitze M, Frixen UH, et al. Differential loss of E-cadherin expression in infiltrating ductal and lobular breast carcinomas. Am J Pathol. 1993;143: Winter MJ, Nagelkerken B, Mertens AE, et al. Expression of Ep-CAM shifts the state of cadherin-mediated adhesions from strong to weak. Exp Cell Res. 2003;285: r 2009 Lippincott Williams & Wilkins

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