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Original Article Flow Cytometric Analysis of Immunoglobulin Heavy Chain Expression in B-Cell Lymphoma and Reactive Lymphoid Hyperplasia

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Original Article Flow Cytometric Analysis of Immunoglobulin Heavy Chain Expression in B-Cell Lymphoma and Reactive Lymphoid Hyperplasia Int J Clin Exp Pathol 2012;5(2):110-118 www.ijcep.com /ISSN: 1936-2625/IJCEP1112008 Original Article Flow cytometric analysis of immunoglobulin heavy chain expression in B-cell lymphoma and reactive lymphoid hyperplasia David D Grier1*, Samer Z Al-Quran*, Diana M Cardona2, Ying Li, Raul C Braylan3 Department of Pathology, University of Florida, College of Medicine, Gainesville, FL, USA; 1Current address: Depart- ment of Pathology, Wake Forest University School of Medicine, Winston-Salem, NC; 2Current address: Department of Pathology, Duke University Medical Center, Durham, NC; 3Current address: The Hematology Laboratory, NIH/Clinical Center, Bethesda, MD, USA; *Drs. Al-Quran and Grier contributed equally to this work and share first authorship. Received December 27, 2011; accepted January 12, 2012; Epub February 12, 2012; Published February 28, 2012 Abstract: The diagnosis of B-cell lymphoma (BCL) is often dependent on the detection of clonal immunoglobulin (Ig) light chain expression. In some BCLs, the determination of clonality based on Ig light chain restriction may be difficult. The aim of our study was to assess the utility of flow cytometric analysis of surface Ig heavy chain (HC) expression in lymphoid tissues in distinguishing lymphoid hyperplasias from BCLs, and also differentiating various BCL subtypes. HC expression on B-cells varied among different types of hyperplasias. In follicular hyperplasia, IgM and IgD expres- sion was high in mantle cells while germinal center cells showed poor HC expression. In other hyperplasias, B cell compartments were blurred but generally showed high IgD and IgM expression. Compared to hyperplasias, BCLs var- ied in IgM expression. Small lymphocytic lymphomas had lower IgM expression than mantle cell lymphomas. Of im- portance, IgD expression was significantly lower in BCLs than in hyperplasias, a finding that can be useful in differen- tiating lymphoma from reactive processes. Keywords: Flow cytometry, lymphoid tissue, immunoglobulin heavy chains, lymphoma, reactive hyperplasia Introduction expression in reactive lymphoid hyperplasias and determined the potential utility of this The assessment of immunoglobulin (Ig) light analysis in the diagnosis and classification of chains (LC) expression by flow cytometry (FCM) BCL. or immunohistochemistry has been used exten- sively in the study of lymphoid hyperplasias and Materials and methods lymphomas and light chain expression restric- tion is a critical diagnostic element in the recog- Patients and samples nition of B-cell lymphoma [1-7]. Assessment of Ig heavy chains (HC) expression has also been The records of our Hematopathology Laboratory utilized in the diagnosis of B-cell non-Hodgkin were searched for specimens of lymph nodes lymphomas (BCL) [8-13]. However, most studies and other lymphoid tissues, including spleen, have been based on immunohistochemistry and and soft tissue infiltrates, submitted for routine molecular techniques involving gene rearrange- diagnostic flow cytometric analysis. One hun- ments of the HC variable regions. The flow cy- dred and twenty three tissue biopsies and exci- tometric analysis of surface Ig HC expression sions were selected. They included BCL and has not been examined thoroughly in either lym- reactive lymphoid hyperplasias, in which Ig HC phoid hyperplasias or as a diagnostic tool in flow cytometric analysis was performed. These BCL [14-18] cases were diagnosed as such based on mor- phology, immunohistochemistry, FCM, and mo- In this study, we measured the levels of Ig HC lecular studies, if required. The lymphomas Ig heavy chain analysis in lymphoid tissue Table 1. Reagents used for flow cytometric analysis Antigen Flurochrome Clone Manufacturer CD19 PerCP SJ 25C1 BD CD20 APC L27 BD IgA FITC Polyclonal CAL IgG PE G18-145 Pharm IgM FITC Polyclonal CAL IgD PE IA6-2 Pharm Kappa FITC Polyclonal DAKO Lambda FITC Polyclonal DAKO IgG Goat isotype control FITC Polyclonal CAL IgG1 mouse isotype control PE X40 BD IgG2a mouse isotype control PE X39 BD IgG1 mouse isotype control FITC X40 BD IgG2a mouse isotype control FITC X39 BD PerCP: Peridinin-chlorophyll-protein, APC: Protein A Phycoprobe, FITC: Fluorescein isothiocyanate, PE: Phycoprobe R-phycoerythrin BD: Becton Dickinson, San Jose, CA. CAL: Caltag Laboratories, Invetrogen Immunodetection, Carlsbad, CA. Pharm: BD Biosciences Pharmingen, San Jose, CA. DAKO; DakoCytomation, Denmark. Table 2. Reagent combinations used for flow cytometric analysis. Tube FITC PE PerCP APC 1 IgG1 mouse isotype control IgG2 mouse isotype control IgG1 IgG1 2 IgG2 mouse isotype control IgG1 mouse isotype control IgG1 IgG2 IgG Goat isotype control None Anti-CD19 Anti-CD20 3 Anti-IgA Goat F(ab’)2 antihuman Anti-IgG Mouse antihuman Anti-CD19 Anti-CD20 4 Anti-IgM Goat F(ab’)2 antihuman Anti-IgD Mouse antihuman Anti-CD19 Anti-CD20 FITC: Fluorescein isothiocyanate, PE: Phycoprobe R-phycoerythrin, PerCP: Peridinin-chlorophyll-protein, APC: Protein A Phycoprobe were classified according to established criteria MO)-precoated wells in Falcon 96-well U-bottom [19]. The research protocol was approved by the assay plates (BD Labware, Franklin Lakes, NJ). Institutional Review Board. A comprehensive panel of antibodies was used, but for the purposes of this study only those Flow cytometric immunophenotyping listed in Table 1 were analyzed. The reagent combinations used are shown in Table 2. The Lymphoid tissues were received fresh and proc- reagent mixture was added to each microtiter essed within 24 hours of the biopsy procedure. well. For cell staining, approximately 3 × 105 Cell suspensions were prepared by mincing the cells were added to the coated wells containing tissue with scalpels in RPMI medium supple- the diluted fluorochrome-conjugated antibody mented with antibiotics, and filtering through a and incubated for 15 min on ice in the dark. wire mesh screen (#80 mesh). In hemocontami- Subsequently, the cells were washed twice with nated samples, erythrocyte lysing was per- 100 microL of phosphate buffer solution and formed by ammonium chloride treatment. The were centrifuged at 500 g for 5 min and the cells were then washed twice in a PBS solution supernatant was discarded. After the last cen- containing 0.1% NaN3. After the final wash trifugation and disposal of supernatant, cells step, cells were re-suspended in RPMI medium were transferred to microtubes in a final volume (Mediatech, Inc., Manassas, VA) with 10% bo- of 250 microL of PBS and analyzed on a four vine serum containing a mixture of antibiotics. color FACScalibur flow cytometer (BD Biosci- ences [BD], San Jose, CA) equipped with both a Surface labeling of the cells was performed in 488-nm argon laser and a 635-nm diode laser. albumin (Sigma Chemical Company, Saint Louis, Daily calibration of the instrument was per- 111 Int J Clin Exp Pathol 2012;5(2):110-118 Ig heavy chain analysis in lymphoid tissue formed using standardized CaliBRITE Beads ent B-cell subpopulations were distinguished by (BD) with FACSComp Software (BD), and com- CD20 expression (Figure 1C), a finding that re- pensation was performed using appropriately flects a prominent follicular hyperplasia in his- stained normal peripheral blood samples. The tologic sections [22]. The discrimination be- data were acquired using CellQuest software tween these two B-cell populations using CD20 (BD). Data analysis was performed using FSC was not always possible using CD19, which was Express 3 (De Novo Software, Los Angeles, CA). expressed more homogenously among B-cells and did not allow an adequate resolution of The expression levels of IgG, IgA, IgM, and IgD different B-cell types (Figure 1D). The less in- were determined on CD20- and CD19- express- tense CD20(+) cells correspond to the follicular ing B cells. In the BCL, the neoplastic B cells mantle cells [22], which also express variable were identified on the basis of their restricted levels of CD23, dim CD5 and no CD10 (data not kappa or lambda Ig LC, or the absence of Ig LC shown). On the other hand, the more intense expression [14, 20, 21]. In cases of partial neo- CD20(+) cells that represent germinal center plastic involvement, a separate analysis of cells [22] are of larger size, as determined by monoclonal and polyclonal B-cells was per- forward light scatter signals (Figure 1C), and formed also based on the Ig LC expression. The express variable but clearly detectable CD10 Mean Fluorescence Intensity (MFI) for each HC and CD38 (data not shown). In these hyperplas- expression in the selected B-cell populations tic cases with two discrete B-cell populations, Ig was determined by calculating a ratio between HC expression was analyzed independently on the mean channel fluorescence for the antibody the mantle and germinal center cells using labeled cells (IgA, IgG, IgM, or IgD) and the CD20 and CD10 expression as well as cell size mean channel fluorescence for the appropriate as discriminators. The mantle cells showed high Ig isotype-matched controls. expression of IgM and IgD while IgG and IgA expression was much weaker or not detectable Statistical analysis on these cells (Figure 1E). Although variable, IgD expression on the mantle cells was particularly Statistical analysis was performed using the intense, as clearly demonstrated in Figure 2 Mann-Whitney test using GraphPad Prism while the Ig HC expression on germinal center (GraphPad Software, San Diego, CA). cells was relatively low for all Ig classes (Figure 1F) and difficult to measure. Thus, for compari- Results son with BCL, the measurements of HC expres- sion in these cases were obtained on the man- Sample characteristics tle B cells. The samples consisted of 60 reactive lymphoid B-cell lymphomas: In BCL, the expression of a hyperplasias and 63 BCL, which included 13 dominant Ig HC was highly variable, and in diffuse large cell lymphomas (LCL), 16 small some cases there was no detectable Ig HC ex- lymphocytic lymphomas (SLL), 18 follicular lym- pression. In general, BCL without detectable LC phomas (FL), 9 mantle cell lymphomas (MCL), 4 expression demonstrated lack of HC expression marginal zone lymphomas (MZL) and 3 Burkitt (data not shown); however, three lymphomas lymphomas (BL).
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