Skip to main content
Top
Published in: Virchows Archiv 6/2013

01-12-2013 | Original Article

Monoclonal antibody HBME-1 reacts with a minor subset of B cells with villous surface and can be useful in the diagnosis of hairy cell leukemia and other indolent lymphoproliferations of villous B lymphocytes

Authors: László Krenács, Judit Tóth-Lipták, Judit Demeter, Klára Piukovics, Zita Borbényi, Péter Gogolák, Eszter Sári, Enikő Bagdi

Published in: Virchows Archiv | Issue 6/2013

Login to get access

Abstract

The Hector Battifora mesothelial epitope-1 (HBME-1) monoclonal antibody has been generated against human mesothelioma cells and recognizes a biochemically unknown membrane epitope. We have accidentally found that the HBME-1 reacts with scattered lymphocytes showing villous surface in hyperplastic lymphoid tissue. To evaluate its reactivity pattern, we have performed a consecutive immunohistochemical study in nonneoplastic bone marrow and lymphoid samples (n = 40), as well as in malignant lymphoproliferations (n = 427), including hairy cell leukemia (HCL) (n = 72), HCL variant (HCL-v) (n = 13), splenic diffuse red pulp small B cell lymphoma (SDRPL) (n = 8), splenic B cell marginal zone lymphoma (SMZL) (n = 59), and splenic B cell lymphoma/leukemia, not further classifiable on bone marrow morphology (SBCL) (n = 37) cases. The staining pattern of HBME-1 was compared to DBA.44. HBME-1+ villous lymphocytes were constantly detected in low number in nonneoplastic lymphoid tissues. With multicolor immunofluorescence staining, HBME-1+ lymphocytes showed a CD20+/CD79a+/IgM+ B cell phenotype. In B cell lymphoproliferations of villous lymphocytes, HBME-1 reactivity was demonstrated in 96 % of HCL, 39 % of HCL-v, 50 % of SDRPL, 12 % of SMZL, and 19 % of SBCL cases. Nodal and extranodal marginal zone lymphoma cases were positive in 12 % of the cases. A small minority (4 %) of the other B cell lymphomas and no T cell lymphoma revealed tumor cell reactivity with HBME-1. In conclusion, our study has established that HBME-1 reacts with a minor subset of B lymphocytes and a small proportion of B cell lymphomas, which has not been described previously. We suggest that HBME-1 can be a useful marker in the diagnosis of HCL and other indolent lymphoproliferations of villous B lymphocytes.
Appendix
Available only for authorised users
Literature
2.
go back to reference Ascoli V, Carnovale-Scalzo C, Taccogna S, Nardi F (1997) Utility of HBME-1 immunostaining in serous effusions. Cytopathology 8:328–335PubMedCrossRef Ascoli V, Carnovale-Scalzo C, Taccogna S, Nardi F (1997) Utility of HBME-1 immunostaining in serous effusions. Cytopathology 8:328–335PubMedCrossRef
4.
go back to reference Del Giudice I, Matutes E, Morilla R, Morilla A, Owusu-Ankomah K, Rafiq F, A’Hern R, Delgado J, Bazerbashi MB, Catovsky D (2004) The diagnostic value of CD123 in B-cell disorders with hairy or villous lymphocytes. Haematologica 89:303–308PubMed Del Giudice I, Matutes E, Morilla R, Morilla A, Owusu-Ankomah K, Rafiq F, A’Hern R, Delgado J, Bazerbashi MB, Catovsky D (2004) The diagnostic value of CD123 in B-cell disorders with hairy or villous lymphocytes. Haematologica 89:303–308PubMed
5.
go back to reference de Matos LL, Del Giglio AB, Matsubayashi CO, de Lima FM, Del Giglio A, da Silva Pinhal MA (2012) Expression of CK-19, galectin-3 and HBME-1 in the differentiation of thyroid lesions: systematic review and diagnostic meta-analysis. Diagn Pathol 7:97. doi:10.1186/1746-1596-7-97 PubMedCrossRef de Matos LL, Del Giglio AB, Matsubayashi CO, de Lima FM, Del Giglio A, da Silva Pinhal MA (2012) Expression of CK-19, galectin-3 and HBME-1 in the differentiation of thyroid lesions: systematic review and diagnostic meta-analysis. Diagn Pathol 7:97. doi:10.​1186/​1746-1596-7-97 PubMedCrossRef
6.
go back to reference Dische FE, Darby AJ, Howard ER (1978) Malignant synovioma: electron microscopical findings in three patients and review of the literature. J Pathol 124:149–155PubMedCrossRef Dische FE, Darby AJ, Howard ER (1978) Malignant synovioma: electron microscopical findings in three patients and review of the literature. J Pathol 124:149–155PubMedCrossRef
7.
go back to reference Falini B, Tiacci E, Liso A, Basso K, Sabattini E, Pacini R, Foa R, Pulsoni A, Dalla Favera R, Pileri S (2004) Simple diagnostic assay for hairy cell leukaemia by immunocytochemical detection of annexin A1 (ANXA1). Lancet 363:1869–1870PubMedCrossRef Falini B, Tiacci E, Liso A, Basso K, Sabattini E, Pacini R, Foa R, Pulsoni A, Dalla Favera R, Pileri S (2004) Simple diagnostic assay for hairy cell leukaemia by immunocytochemical detection of annexin A1 (ANXA1). Lancet 363:1869–1870PubMedCrossRef
8.
go back to reference Foucar K, Falini B, Catovsky D, Stein H (2008) Hairy cell leukaemia. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (eds) WHO classification of tumours of haematopoietic and lymphoid tissues, vol 2, 4th edn, WHO classification of tumours. IARC, Lyon, pp 188–190 Foucar K, Falini B, Catovsky D, Stein H (2008) Hairy cell leukaemia. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (eds) WHO classification of tumours of haematopoietic and lymphoid tissues, vol 2, 4th edn, WHO classification of tumours. IARC, Lyon, pp 188–190
9.
go back to reference Frisch B, Bartl R (eds) (1999) Biopsy interpretation of bone and bone marrow, 2nd edn. Arnold, London–Sidney–Auckland, p 350 Frisch B, Bartl R (eds) (1999) Biopsy interpretation of bone and bone marrow, 2nd edn. Arnold, London–Sidney–Auckland, p 350
11.
go back to reference Hounieu H, Chittal SM, al Saati T, de Mascarel A, Sabattini E, Pileri S, Falini B, Ralfkiaer E, Le Tourneau A, Selves J et al (1992) Hairy cell leukemia. Diagnosis of bone marrow involvement in paraffin-embedded sections with monoclonal antibody DBA.44. Am J Clin Pathol 98:26–33PubMed Hounieu H, Chittal SM, al Saati T, de Mascarel A, Sabattini E, Pileri S, Falini B, Ralfkiaer E, Le Tourneau A, Selves J et al (1992) Hairy cell leukemia. Diagnosis of bone marrow involvement in paraffin-embedded sections with monoclonal antibody DBA.44. Am J Clin Pathol 98:26–33PubMed
12.
go back to reference Hoyer JD, Li CY, Yam LT, Hanson CA, Kurtin PJ (1997) Immunohistochemical demonstration of acid phosphatase isoenzyme 5 (tartrate-resistant) in paraffin sections of hairy cell leukemia and other hematologic disorders. Am J Clin Pathol 108:308–315PubMed Hoyer JD, Li CY, Yam LT, Hanson CA, Kurtin PJ (1997) Immunohistochemical demonstration of acid phosphatase isoenzyme 5 (tartrate-resistant) in paraffin sections of hairy cell leukemia and other hematologic disorders. Am J Clin Pathol 108:308–315PubMed
13.
go back to reference Isaacson PG, Piris MA, Berger F, Swerdlow SH, Thieblemont C, Pittaluga S, Harris NL (2008) Splenic B-cell marginal zone lymphoma. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (eds) WHO classification of tumours of haematopoietic and lymphoid tissues, vol 2, WHO classification of tumours. IARC, Lyon, pp 185–187 Isaacson PG, Piris MA, Berger F, Swerdlow SH, Thieblemont C, Pittaluga S, Harris NL (2008) Splenic B-cell marginal zone lymphoma. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (eds) WHO classification of tumours of haematopoietic and lymphoid tissues, vol 2, WHO classification of tumours. IARC, Lyon, pp 185–187
14.
go back to reference Janckila AJ, Cardwell EM, Yam LT, Li CY (1995) Hairy cell identification by immunohistochemistry of tartrate-resistant acid phosphatase. Blood 85:2839–2844PubMed Janckila AJ, Cardwell EM, Yam LT, Li CY (1995) Hairy cell identification by immunohistochemistry of tartrate-resistant acid phosphatase. Blood 85:2839–2844PubMed
15.
go back to reference Kanellis G, Mollejo M, Montes-Moreno S, Rodriguez-Pinilla SM, Cigudosa JC, Algara P, Montalban C, Matutes E, Wotherspoon A, Piris MA (2009) Splenic diffuse red pulp small B-cell lymphoma: revision of a series of cases reveals characteristic clinico-pathological features. Haematologica 95:1122–1129. doi:10.3324/haematol.2009.013714 CrossRef Kanellis G, Mollejo M, Montes-Moreno S, Rodriguez-Pinilla SM, Cigudosa JC, Algara P, Montalban C, Matutes E, Wotherspoon A, Piris MA (2009) Splenic diffuse red pulp small B-cell lymphoma: revision of a series of cases reveals characteristic clinico-pathological features. Haematologica 95:1122–1129. doi:10.​3324/​haematol.​2009.​013714 CrossRef
16.
go back to reference Marafioti T, Jones M, Facchetti F, Diss TC, Du MQ, Isaacson PG, Pozzobon M, Pileri SA, Strickson AJ, Tan SY, Watkins F, Mason DY (2003) Phenotype and genotype of interfollicular large B cells, a subpopulation of lymphocytes often with dendritic morphology. Blood 102:2868–2876PubMedCrossRef Marafioti T, Jones M, Facchetti F, Diss TC, Du MQ, Isaacson PG, Pozzobon M, Pileri SA, Strickson AJ, Tan SY, Watkins F, Mason DY (2003) Phenotype and genotype of interfollicular large B cells, a subpopulation of lymphocytes often with dendritic morphology. Blood 102:2868–2876PubMedCrossRef
17.
go back to reference Matutes E, Morilla R, Owusu-Ankomah K, Houliham A, Meeus P, Catovsky D (1994) The immunophenotype of hairy cell leukemia (HCL). Proposal for a scoring system to distinguish HCL from B-cell disorder with hairy or villous lymphocytes. Leuk Lymphoma 14:57–61PubMed Matutes E, Morilla R, Owusu-Ankomah K, Houliham A, Meeus P, Catovsky D (1994) The immunophenotype of hairy cell leukemia (HCL). Proposal for a scoring system to distinguish HCL from B-cell disorder with hairy or villous lymphocytes. Leuk Lymphoma 14:57–61PubMed
18.
go back to reference Matutes E, Wotherspoon A, Brito-Babapulle V, Catovsky D (2001) The natural history and clinico-pathological features of the variant form of hairy cell leukemia. Leukemia 15:184–186PubMedCrossRef Matutes E, Wotherspoon A, Brito-Babapulle V, Catovsky D (2001) The natural history and clinico-pathological features of the variant form of hairy cell leukemia. Leukemia 15:184–186PubMedCrossRef
19.
go back to reference Miettinen M, Kovatich AJ (1995) HMBE-1 a monoclonal antibody useful in the differential diagnosis of mesothelioma, adenocarcinoma, and soft-tissue and bone tumors. Appl Immunohistochem 3:115–322 Miettinen M, Kovatich AJ (1995) HMBE-1 a monoclonal antibody useful in the differential diagnosis of mesothelioma, adenocarcinoma, and soft-tissue and bone tumors. Appl Immunohistochem 3:115–322
20.
go back to reference Miettinen M, Karkkainen P (1996) Differential reactivity of HBME-1 and CD15 antibodies in benign and malignant thyroid tumours: preferential reactivity with malignant tumours. Virchows Arch 429:213–219PubMed Miettinen M, Karkkainen P (1996) Differential reactivity of HBME-1 and CD15 antibodies in benign and malignant thyroid tumours: preferential reactivity with malignant tumours. Virchows Arch 429:213–219PubMed
21.
go back to reference Miettinen M, Limon J, Niezabitowski A, Lasota J (2001) Calretinin and other mesothelioma markers in synovial sarcoma: analysis of antigenic similarities and differences with malignant mesothelioma. Am J Surg Pathol 25:610–617PubMedCrossRef Miettinen M, Limon J, Niezabitowski A, Lasota J (2001) Calretinin and other mesothelioma markers in synovial sarcoma: analysis of antigenic similarities and differences with malignant mesothelioma. Am J Surg Pathol 25:610–617PubMedCrossRef
22.
go back to reference Miranda RN, Briggs RC, Kinney MC, Veno PA, Hammer RD, Cousar JB (2000) Immunohistochemical detection of cyclin D1 using optimized conditions is highly specific for mantle cell lymphoma and hairy cell leukemia. Mod Pathol 13:1308–1314PubMedCrossRef Miranda RN, Briggs RC, Kinney MC, Veno PA, Hammer RD, Cousar JB (2000) Immunohistochemical detection of cyclin D1 using optimized conditions is highly specific for mantle cell lymphoma and hairy cell leukemia. Mod Pathol 13:1308–1314PubMedCrossRef
23.
go back to reference Morgan EA, Yu H, Pinkus JL, Pinkus GS (2013) Immunohistochemical detection of hairy cell leukemia in paraffin sections using a highly effective CD103 rabbit monoclonal antibody. Am J Clin Pathol 139:220–230. doi:10.1309/AJCPHW7RULIZT2GB PubMedCrossRef Morgan EA, Yu H, Pinkus JL, Pinkus GS (2013) Immunohistochemical detection of hairy cell leukemia in paraffin sections using a highly effective CD103 rabbit monoclonal antibody. Am J Clin Pathol 139:220–230. doi:10.​1309/​AJCPHW7RULIZT2GB​ PubMedCrossRef
24.
go back to reference Nesland JM, Sobrinho-Simoes M, Johannessen JV (1987) Scanning electron microscopy of the human thyroid gland and its disorders. Scanning Microsc 1:1797–1810PubMed Nesland JM, Sobrinho-Simoes M, Johannessen JV (1987) Scanning electron microscopy of the human thyroid gland and its disorders. Scanning Microsc 1:1797–1810PubMed
25.
go back to reference O’Hara BJ, Paetau A, Miettinen M (1998) Keratin subsets and monoclonal antibody HBME-1 in chordoma: immunohistochemical differential diagnosis between tumors simulating chordoma. Hum Pathol 29:119–126PubMedCrossRef O’Hara BJ, Paetau A, Miettinen M (1998) Keratin subsets and monoclonal antibody HBME-1 in chordoma: immunohistochemical differential diagnosis between tumors simulating chordoma. Hum Pathol 29:119–126PubMedCrossRef
26.
go back to reference Ordóñez NG (1998) Role of immunohistochemistry in distinguishing epithelial peritoneal mesotheliomas from peritoneal and ovarian serous carcinomas. Am J Surg Pathol 22:1203–1214PubMedCrossRef Ordóñez NG (1998) Role of immunohistochemistry in distinguishing epithelial peritoneal mesotheliomas from peritoneal and ovarian serous carcinomas. Am J Surg Pathol 22:1203–1214PubMedCrossRef
27.
go back to reference Pardo-Mindan FJ, Guillen FJ, Villas C, Vazquez JJ (1981) A comparative ultrastructural study of chondrosarcoma, chordoid sarcoma, and chordoma. Cancer 47:2611–2619PubMedCrossRef Pardo-Mindan FJ, Guillen FJ, Villas C, Vazquez JJ (1981) A comparative ultrastructural study of chondrosarcoma, chordoid sarcoma, and chordoma. Cancer 47:2611–2619PubMedCrossRef
28.
go back to reference Piris M, Foucar K, Mollejo M, Campo E, Falini B (2008) Splenic B-cell lymphoma/leukaemia, unclassifiable. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (eds) WHO classification of tumours of haematopoietic and lymphoid tissues, vol 2, 4th edn, WHO classification of tumours. IARC, Lyon, pp 191–193 Piris M, Foucar K, Mollejo M, Campo E, Falini B (2008) Splenic B-cell lymphoma/leukaemia, unclassifiable. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (eds) WHO classification of tumours of haematopoietic and lymphoid tissues, vol 2, 4th edn, WHO classification of tumours. IARC, Lyon, pp 191–193
29.
go back to reference Ponzoni M, Kanellis G, Pouliou E, Baliakas P, Scarfò L, Ferreri AJ, Doglioni C, Bikos V, Dagklis A, Anagnostopoulos A, Ghia P, Stamatopoulos K, Papadaki T (2012) Bone marrow histopathology in the diagnostic evaluation of splenic marginal-zone and splenic diffuse red pulp small B-cell lymphoma: a reliable substitute for spleen histopathology? Am J Surg Pathol 36:1609–1618. doi:10.1097/PAS.0b013e318271243d PubMedCrossRef Ponzoni M, Kanellis G, Pouliou E, Baliakas P, Scarfò L, Ferreri AJ, Doglioni C, Bikos V, Dagklis A, Anagnostopoulos A, Ghia P, Stamatopoulos K, Papadaki T (2012) Bone marrow histopathology in the diagnostic evaluation of splenic marginal-zone and splenic diffuse red pulp small B-cell lymphoma: a reliable substitute for spleen histopathology? Am J Surg Pathol 36:1609–1618. doi:10.​1097/​PAS.​0b013e318271243d​ PubMedCrossRef
30.
go back to reference Raju U, Fine G, Greenawald KA, Ohorodnik JM (1989) Primary papillary serous neoplasia of the peritoneum: a clinicopathologic and ultrastructural study of eight cases. Hum Pathol 20:426–436PubMedCrossRef Raju U, Fine G, Greenawald KA, Ohorodnik JM (1989) Primary papillary serous neoplasia of the peritoneum: a clinicopathologic and ultrastructural study of eight cases. Hum Pathol 20:426–436PubMedCrossRef
31.
go back to reference Robbins BA, Ellison DJ, Spinosa JC, Carey CA, Lukes RJ, Poppema S, Saven A, Piro LD (1993) Diagnostic application of two-color flow cytometry in 161 cases of hairy cell leukemia. Blood 82:1277–1287PubMed Robbins BA, Ellison DJ, Spinosa JC, Carey CA, Lukes RJ, Poppema S, Saven A, Piro LD (1993) Diagnostic application of two-color flow cytometry in 161 cases of hairy cell leukemia. Blood 82:1277–1287PubMed
33.
go back to reference Sainati L, Matutes E, Mulligan S, de Oliveira MP, Rani S, Lampert IA, Catovsky D (1990) A variant form of hairy cell leukemia resistant to alpha-interferon: clinical and phenotypic characteristics of 17 patients. Blood 76:157–162PubMed Sainati L, Matutes E, Mulligan S, de Oliveira MP, Rani S, Lampert IA, Catovsky D (1990) A variant form of hairy cell leukemia resistant to alpha-interferon: clinical and phenotypic characteristics of 17 patients. Blood 76:157–162PubMed
34.
go back to reference Sheibani K, Esteban JM, Bailey A, Battifora H, Weiss LM (1992) Immunopathologic and molecular studies as an aid to the diagnosis of malignant mesothelioma. Hum Pathol 23:107–116PubMedCrossRef Sheibani K, Esteban JM, Bailey A, Battifora H, Weiss LM (1992) Immunopathologic and molecular studies as an aid to the diagnosis of malignant mesothelioma. Hum Pathol 23:107–116PubMedCrossRef
36.
go back to reference Tiacci E, Schiavoni G, Martelli MP, Boveri E, Pacini R, Tabarrini A, Zibellini S, Santi A, Pettirossi V, Fortini E, Ascani S, Arcaini L, Inghirami G, Paulli M, Falini B (2013) Constant activation of the RAF-MEK-ERK pathway as a diagnostic and therapeutic target in hairy cell leukemia. Haematologica 98:635–639. doi:10.3324/haematol.2012.078071 PubMedCrossRef Tiacci E, Schiavoni G, Martelli MP, Boveri E, Pacini R, Tabarrini A, Zibellini S, Santi A, Pettirossi V, Fortini E, Ascani S, Arcaini L, Inghirami G, Paulli M, Falini B (2013) Constant activation of the RAF-MEK-ERK pathway as a diagnostic and therapeutic target in hairy cell leukemia. Haematologica 98:635–639. doi:10.​3324/​haematol.​2012.​078071 PubMedCrossRef
37.
go back to reference Venkatraman L, McDonald KA, Bagdi E, Krenacs L, Piggott N, McIntosh G, Dogan A (2005) Characterisation of a new monoclonal antibody recognising CD11c in paraffin-embedded tissue. Mod Pathol 18:255A–256A, 1183 Suppl.1 Venkatraman L, McDonald KA, Bagdi E, Krenacs L, Piggott N, McIntosh G, Dogan A (2005) Characterisation of a new monoclonal antibody recognising CD11c in paraffin-embedded tissue. Mod Pathol 18:255A–256A, 1183 Suppl.1
38.
go back to reference Went PT, Zimpfer A, Pehrs AC, Sabattini E, Pileri SA, Maurer R, Terracciano L, Tzankov A, Sauter G, Dirnhofer S (2005) High specificity of combined TRAP and DBA.44 expression for hairy cell leukemia. Am J Surg Pathol 29:474–478PubMedCrossRef Went PT, Zimpfer A, Pehrs AC, Sabattini E, Pileri SA, Maurer R, Terracciano L, Tzankov A, Sauter G, Dirnhofer S (2005) High specificity of combined TRAP and DBA.44 expression for hairy cell leukemia. Am J Surg Pathol 29:474–478PubMedCrossRef
Metadata
Title
Monoclonal antibody HBME-1 reacts with a minor subset of B cells with villous surface and can be useful in the diagnosis of hairy cell leukemia and other indolent lymphoproliferations of villous B lymphocytes
Authors
László Krenács
Judit Tóth-Lipták
Judit Demeter
Klára Piukovics
Zita Borbényi
Péter Gogolák
Eszter Sári
Enikő Bagdi
Publication date
01-12-2013
Publisher
Springer Berlin Heidelberg
Published in
Virchows Archiv / Issue 6/2013
Print ISSN: 0945-6317
Electronic ISSN: 1432-2307
DOI
https://doi.org/10.1007/s00428-013-1490-5

Other articles of this Issue 6/2013

Virchows Archiv 6/2013 Go to the issue