Original Article
ZAP-70 Expression as a Surrogate for Immunoglobulin-Variable-Region Mutations in Chronic Lymphocytic Leukemia
N Engl J Med 2003; 348:1764-1775May 1, 2003
- Abstract
Background
The mutational status of immunoglobulin heavy-chain variable-region (IgVH ) genes in the leukemic cells of chronic lymphocytic leukemia (CLL) is an important prognostic factor in the disease. We investigated whether the expression of ZAP-70 by CLL cells correlated with the IgVH mutational status, disease progression, and survival.
Methods
The expression of ZAP-70 was analyzed in T-cell and B-cell lines and in peripheral-blood samples from 56 patients with CLL with the use of flow cytometry, Western blotting, and immunohistochemistry. The results were correlated with the IgVH mutational status and clinical outcome.
Results
ZAP-70 was detected by flow-cytometric analysis in cells of T-cell lineage and in leukemic cells from 32 of 56 patients with CLL. In all patients in whom at least 20 percent of the leukemic cells were positive for ZAP-70, IgVH was unmutated, whereas IgVH mutations were found in 21 of 24 patients in whom less than 20 percent of the leukemic cells were positive for ZAP-70 (P<0.001). Concordant results were obtained when ZAP-70 expression was assessed by immunohistochemistry or Western blotting. The level of ZAP-70 expression did not change over time (median, 37 months) in sequential samples from 30 patients with CLL. Patients with Binet stage A CLL who had at least 20 percent ZAP-70–positive leukemic cells had more rapid progression and poorer survival than those with less than 20 percent ZAP-70–positive cells.
Conclusions
Among patients with CLL, expression of ZAP-70, as detected by flow-cytometric analysis, correlated with IgVH mutational status, disease progression, and survival.
Media in This Article
Figure 1
Western Blot Analysis of the Expression of ZAP-70 in a T-Cell Line, a Peripheral-Blood Sample from Patient 17 with Chronic Lymphocytic Leukemia (CLL), and 10 B-Cell Lines (Panel A); Seven Patients with CLL According to the Presence or Absence of Mutations in the Immunoglobulin Heavy-Chain Variable-Region (IgVH ) Genes (Panel B); and Normal Peripheral-Blood T Cells (Panel C).Figure 2
Immunofluorescence and Flow-Cytometric Analysis of the Expression of ZAP-70.Article Activity
- Article
The staging systems developed by Rai et al.1 and Binet et al.2 are standard methods of assessing prognosis in chronic lymphocytic leukemia (CLL). However, since these systems cannot identify stable or progressive forms of the disease, there has been a continual effort to identify other prognostic factors in CLL.3-6
About 50 to 70 percent of patients with CLL have evidence of somatic hypermutation in the immunoglobulin heavy-chain variable-region (IgVH ) genes of the leukemic cells.7-11 These patients probably constitute a subgroup in whom the leukemic cells have passed through the germinal center, the site of IgVH hypermutation.12 It is important to note that patients with unmutated IgVH genes usually have an advanced stage of CLL and unfavorable cytogenetic features, require therapy, and have a short survival. In contrast, patients with leukemic cells that have mutant IgVH genes usually present in an early clinical stage, frequently have 13q14 chromosomal deletions, do not have alterations of p53, do not require therapy, and have a long survival.11,13,14 For these reasons, knowledge of the mutational status of IgVH is of considerable value in assessing the prognosis in CLL. Most general laboratories, however, are unable to determine IgVH sequences. Moreover, even when the technique is available, it is too costly and time consuming to include in the standard workup of CLL. These considerations have made finding a surrogate for IgVH mutational status in CLL an important priority.
Investigations using DNA microarrays15,16 have shown that CLL cells exhibit a characteristic gene-expression profile in which the expression of a small subgroup of genes, including those encoding ZAP-70, IM1286077, and C-type lectin, correlates with the mutational status of IgVH genes.16,17 ZAP-70, a member of the Syk–ZAP-70 protein tyrosine kinase family, is normally expressed in T cells and natural killer cells and has a critical role in the initiation of T-cell signaling.18-22 This finding led us to hypothesize that the expression of ZAP-70 could not only predict IgVH mutational status but also serve as a prognostic factor in CLL. We therefore analyzed ZAP-70 protein in CLL cells from a series of patients using Western blotting, immunohistochemistry, and flow cytometry and correlated the results with the mutational status of the IgVH genes and the clinical outcome.
Methods
Patients and Sample Collection
Fifty-six patients who had received a diagnosis of CLL at our institution were selected on the basis of the availability of frozen samples for biologic studies. Lymph-node–biopsy specimens were available from eight patients. Progression was defined as a change to a more advanced clinical stage or the need for treatment. The time to progression and survival were calculated from the time of diagnosis. The median age was 60 years (range, 37 to 81), and the median duration of follow-up (from diagnosis) was 63 months.
Mononuclear cells from peripheral-blood samples were isolated on a Ficoll–Hypaque gradient (Seromed).23 In three samples, CD19+ cells were isolated with use of anti-CD19 fluorescein isothiocyanate, followed by separation with anti–fluorescein isothiocyanate Microbeads (Miltenyi Biotec). Lymph-node–biopsy specimens from six additional patients who had received a diagnosis of mantle-cell lymphoma according to the criteria of the World Health Organization24 were included in the analysis.
Preparation of RNA, Complementary DNA, and Genomic DNA
Total RNA was isolated with use of Ultraspec RNA (Biotecx Laboratories) according to the manufacturer's instructions. Complementary DNA (cDNA) was synthesized from 1 μg of RNA with the use of Moloney–murine leukemia virus reverse transcriptase (Invitrogen, Life Technologies). High-molecular-weight DNA was extracted from mononuclear cells isolated on a Ficoll gradient with use of a salting-out procedure.25
Amplification of IgVH Genes
We amplified cDNA using a set of six heavy-chain variable-region (VH) family-specific primers (VH1 through VH6) that anneal to sequences in the leader region26 along with primers complementary to the constant region (IgM and IgG).7 When amplification with these primers failed, an alternative set of primers specific to framework I region and the heavy-chain joining (JH) region was used.27 For the amplification of genomic DNA, approximately 100 ng of DNA was used in a total volume of 50 μl.11
IgVH Mutational Status
Polymerase-chain-reaction (PCR) products were purified either directly with use of the Concert rapid PCR purification system (GIBCO BRL), or by gel excision with use of the QIAEX II agarose-gel extraction kit (Qiagen). Products were directly sequenced from both strands with use of the Big Dye Terminator Cycle Sequencing Ready Reaction (versions 2.0 and 3.0, Applied Biosystems) according to the manufacturer's instructions. Sequencing analysis and alignments were performed with use of DNAPLOT software and the VBASE data library.28 Samples in which fewer than 2 percent of base pairs differed from those of the consensus sequence were considered unmutated.8
Western Blotting
Western blotting of cell lysates was carried out as previously described.23 Cell lysates from the following cell lines were also included: Jurkat (a T-cell line derived from lymphoblastic lymphoma), JVM-2 (B-cell prolymphocytic leukemia), Granta 519 and REC (mantle-cell lymphoma), DHL-16 and DOHH-2 (follicular lymphoma), Ly1.2 and Ly3 (diffuse large-B-cell lymphoma), and Namalwa, Raji, Daudi, and Ramos (Burkitt's lymphoma). Blots were incubated with anti–ZAP-70 antibody (Upstate Biotechnology) and anti–α-tubulin (Calbiochem). Lysates from Jurkat cells, a T-cell line with a high level of expression of ZAP-70 protein,18 were used as a positive control. To analyze the influence of normal T cells present in the CLL samples, we mixed different concentrations of mononuclear cells from healthy blood donors with REC cells, a B-cell line that does not express ZAP-70.
Immunohistochemistry
We also analyzed the expression of ZAP-70 in paraffin-embedded sections of lymph-node–biopsy specimens from eight patients with CLL and six patients with mantle-cell lymphoma using an anti–ZAP-70 antibody (ZAP-70-LR, Santa Cruz Biotechnology). We evaluated the level of ZAP-70 expression in tumor cells, T cells, and residual germinal-center areas.
Flow Cytometry
Mononuclear cells, as well as whole blood, from 56 patients with CLL and 10 healthy blood donors used as normal controls were fixed and permeabilized with use of the Fix & Perm kit (Caltag Laboratories) according to the manufacturer's instructions. Then 1.5 μg of anti–ZAP-70 antibody per 500,000 cells was incubated for 20 minutes at room temperature, washed twice in phosphate-buffered saline (Biomerieux), incubated for 20 minutes with goat antimouse immunoglobulin fluorescein isothiocyanate (Dako), washed, and then incubated with normal mouse serum for five minutes. Finally, CD3–phycoerythrin, CD56–phycoerythrin, CD19– peridinin chlorophyll protein cychrome 5.5, and CD5–allophycocyanine (BD Biosciences) were added, and the samples were incubated for 15 minutes. Samples were analyzed with a flow cytometer (FACS Calibur, BD Biosciences) with a gate on the fluorescence 2 detector to ensure that at least 1000 T cells and natural killer cells were analyzed in each sample. In samples from healthy control subjects, at least 5000 B cells were also analyzed. Analysis of stained samples was carried out with use of CellQuest software (BD Biosciences).
Lymphocytes were gated to avoid the inclusion of debris, monocytes, and doublets. The resultant cells were then gated to select CD3+CD56+ cells (T and natural killer cells), used as an internal control for ZAP-70 expression, and CD19+CD5+ (CLL cells). Biparametric dot graphs of cells that were stained for ZAP-70 and CD3 plus CD56 were independently plotted for T cells and natural killer cells and CLL cells. A marker that included T cells and natural killer cells (in the upper right quadrant of each graph) was used to calculate the percentage of CLL cells that were positive for ZAP-70. The percentage of CD19+ cells that also expressed CD38 was quantified as previously described.8
Statistical Analysis
Correlations between ZAP-70, CD38, and mutational status were analyzed with use of Wilcoxon's and Fisher's exact tests and a multiple regression analysis. To identify the level of ZAP-70 expression that could best be used to discriminate mutated from unmutated cells, we used a receiver-operating-characteristic plot.29 Correlations between the clinical characteristics and the expression of ZAP-70 were also analyzed with use of Wilcoxon's or Fisher's exact test. Survival and time to progression were estimated according to the method of Kaplan and Meier and compared between groups by means of the log-rank test. All P values were two-sided, and the type I error was set at 5 percent. Statistical analyses were performed with use of SPSS software.30
Results
Somatic Mutations in IgVH Genes
All sequences of IgVH genes in the leukemic cells from the 56 patients were in-frame rearrangements, and only two premature stop codons were observed. We found somatic mutations (up to 98 percent homology with germ-line sequences) in 21 of 56 patients (38 percent), including 7 that had 95.6 to 97.3 percent homology with germ-line sequences (Table 1Table 1
Main Biologic and Clinical Characteristics of the Patients.).Western Blot Analysis of ZAP-70 Expression
ZAP-70 expression was analyzed in 12 human cell lines corresponding to different stages of B-cell differentiation. Peripheral-blood lymphocytes from healthy blood donors (data not shown) and the Jurkat T-cell line were used as positive controls. The protein was not detected in any of the B-cell lines, except the Ramos cell line, in which it was expressed weakly (Figure 1AFigure 1
Western Blot Analysis of the Expression of ZAP-70 in a T-Cell Line, a Peripheral-Blood Sample from Patient 17 with Chronic Lymphocytic Leukemia (CLL), and 10 B-Cell Lines (Panel A); Seven Patients with CLL According to the Presence or Absence of Mutations in the Immunoglobulin Heavy-Chain Variable-Region (IgVH ) Genes (Panel B); and Normal Peripheral-Blood T Cells (Panel C).).Of 32 samples from the patients with CLL, 16 had a high level of expression of ZAP-70 on Western blotting and the remaining 16 had a low level of expression (Figure 1B). The presence of more than 2 percent T cells in the blood samples influenced the result, especially when the proportion was 10 percent or higher (Figure 1C). However, samples from all but two patients with CLL contained less than 15 percent T cells on Western blotting (mean [±SD], 4.5±5.5 percent); Patient 45 had more than 20 percent T cells in the sample.
Immunohistochemical Analysis of ZAP-70 Expression
We analyzed lymph-node–biopsy specimens from eight patients with CLL, none of whom had IgVH mutations, and six patients with mantle-cell lymphoma, which is characterized by proliferation of CD5+ B cells but not usually by IgVH mutations. All lymph-node–biopsy specimens from the patients with CLL were positive for ZAP-70, with a diffuse pattern reflecting the infiltration by leukemic cells. T cells in the biopsy specimens showed stronger immunoreactivity than the CLL cells. Residual germinal centers were negative for ZAP-70. All mantle-cell lymphomas were negative for ZAP-70, whereas T cells in the tissue had a high level of expression of ZAP-70.
Flow-Cytometric analysis of ZAP-70 Expression
In samples of normal blood, flow-cytometric analysis disclosed a population with high and homogeneous expression of ZAP-70 (Figure 2AFigure 2
Immunofluorescence and Flow-Cytometric Analysis of the Expression of ZAP-70.). This population corresponded to T cells and natural killer cells. In these samples, the proportion of normal B cells (from healthy blood donors) expressing as much ZAP-70 as T cells and natural killer cells was 0 to 6.5 percent (mean, 4±2.5). No significant differences in ZAP-70 expression were observed between CD5– and CD5+ B-cell subpopulations (Figure 2B).The method used to quantify the percentage of CLL cells expressing as much ZAP-70 as T cells is shown in Figure 2C. Leukemic cells from 56 patients with CLL were analyzed for ZAP-70 expression by flow cytometry. In these samples, T cells and natural killer cells also displayed high and homogeneous levels of expression of ZAP-70. In contrast to normal CD5+ B cells, CD5+ CLL cells from 32 of 56 patients expressed high levels of ZAP-70 (Figure 2D).
In all but one patient (Patient 45), there was complete concordance of ZAP-70 expression as assessed by flow cytometry, Western blotting, and immunohistochemistry (Table 1). These discrepant results in Patient 45 (Figure 1B and Table 1) could be explained by the high number of T cells (20 percent) in the patient's sample. ZAP-70 expression was also analyzed in 30 of 56 patients from whom two sequential samples were available. The median time between the collections of the samples was 37 months (range, 11 to 64). None of these 30 patients had significant changes in ZAP-70 expression over time.
Correlation between ZAP-70 Protein and IgVH Mutational Status
There was a strong correlation between the presence of IgVH mutations and the percentage of leukemic cells that expressed ZAP-70, as assessed by flow cytometry. In the receiver-operating-characteristic analysis, a value of 17.5 percent ZAP-70–positive CLL cells was the best cutoff for assigning IgVH mutational status. We used a cutoff value of 20 percent for simplicity. Patients with unmutated IgVH genes had higher percentages of ZAP-70–positive CLL cells than did patients with IgVH mutations (48±21 percent vs. 6±4 percent, P<0.001). Samples from all 21 patients with IgVH mutations contained less than 20 percent ZAP-70–positive CLL cells, and all but 3 patients without IgVH mutations (91 percent) had 20 percent or more ZAP-70–positive CLL cells (Figure 3AFigure 3
Correlation of the Level of Expression of ZAP-70 and Immunoglobulin Heavy-Chain Variable-Region (IgVH ) Mutational Status (Panel A) and IgVH Sequence Homology (Panel B). and Figure 3B). Conversely, all the patients with increased proportions of ZAP-70–positive cells did not have somatic mutations, and 88 percent of patients with low numbers of ZAP-70–positive cells had IgVH mutations. Overall, the probability of the absence of somatic mutations in the presence of more than 20 percent ZAP-70–positive CLL cells (positive predictive value) was 100 percent (95 percent confidence interval, 89 to 100), whereas the probability of IgVH mutations in the presence of a low percentage of ZAP-70–positive cells (negative predictive value) was 87.5 percent (95 percent confidence interval, 68 to 97). The sensitivity and specificity of the flow-cytometric analysis were 91 percent (95 percent confidence interval, 77 to 98) and 100 percent (95 percent confidence interval, 84 to 100), respectively.To verify ZAP-70 expression in the three patients in whom IgVH status and flow-cytometric results were discordant, Western blot analysis was performed on isolated fractions of CD19+ cells with a purity greater than 98 percent (CD19 is a surface marker of B cells). A weak signal was observed in all three samples (data not shown), validating the low levels of expression of ZAP-70 observed on flow cytometry.
ZAP-70 and CD38 Expression
Data for the expression of CD38 were available for 45 patients (CD38 is a marker that has been proposed as a surrogate for IgVH mutational status). Of these 45 patients, 18 had no more than 30 percent CD38+ cells (Table 1). There were significant differences in the mean percentages of CD38+ CLL cells between patients with IgVH mutations and those without IgVH mutations (20 percent vs. 60 percent, P<0.001). In addition, 22 of 28 patients without IgVH mutations (79 percent) had at least 30 percent CD38+ cells, whereas 12 of 17 (71 percent) with somatic mutations had less than 30 percent CD38+ cells. Moreover, the percentage of CD38+ cells was at least 30 percent in 21 of 25 patients (84 percent) with at least 20 percent ZAP-70–positive cells and less than 30 percent in 14 of 20 patients (70 percent) with less than 20 percent ZAP-70–positive cells. The level of CD38 expression was also low in the two patients with discordant results of ZAP-70 expression and IgVH mutations (Table 1). In a multiple regression analysis, only ZAP-70 expression (P<0.001), and not CD38 expression, maintained its correlation with IgVH mutational status.
Prognostic Importance of the Percentage of ZAP-70–Positive Cells
None of the standard variables were associated with ZAP-70 expression, including Binet's and Rai's clinical stages, the lymphocyte count, and the lymphocyte doubling time. However, an increased percentage of ZAP-70–positive cells was associated with a short time to progression. Among 44 patients with Binet stage A, the median time to progression was 29 months for the 26 patients with at least 20 percent ZAP-70–positive cells, whereas the median was not reached among the 18 patients with less than 20 percent ZAP-70–positive cells (P=0.009) (Figure 4AFigure 4
Kaplan–Meier Estimates of the Actuarial Risk of Disease Progression (Panel A) and the Likelihood of Survival (Panel B) among Patients with Binet Stage A Chronic Lymphocytic Leukemia, According to the Level of Expression of ZAP-70.).When survival was calculated from the time of diagnosis, the 26 patients with Binet stage A CLL and at least 20 percent ZAP-70–positive cells had a median survival of 90 months, whereas the median survival was not reached in the 18 patients with Binet stage A and less than 20 percent ZAP-70–positive cells (P=0.01) (Figure 4B). However, when all patients were analyzed (Binet stage A, B, and C), the percentage of ZAP-70–positive cells was not significantly correlated with survival (P=0.06). The percentage of CD38+ cells (with a cutoff of 30 percent) did not predict progression or survival (data not shown). Finally, as expected, IgVH mutational status also correlated with progression and survival (data not shown).
Discussion
The management of CLL is based on each patient's individual risk, because the disease has a widely variable clinical course. An important determinant of the prognosis is the mutational status of IgVH genes in the leukemic cells, which correlates with the clinical outcome better than and independently of classic prognostic factors.8,11,31 Methods to identify IgVH mutations are, however, not widely available in clinical practice. Our study confirms that the leukemic cells without IgVH mutations in patients with CLL express high levels of ZAP-70, whereas the leukemic cells with IgVH mutations in patients with CLL have barely detectable levels of ZAP-70.16,17 Moreover, using flow cytometry, we found that none of the patients with CLL and at least 20 percent ZAP-70–positive cells had IgVH somatic mutations, whereas all but three patients with less than 20 percent ZAP-70–positive cells had mutated IgVH genes. Flow-cytometric analysis of ZAP-70 expression was a sensitive and specific surrogate for mutational status of IgVH genes; this method should be readily available in general laboratories.
The mechanisms accounting for the relation between ZAP-70 expression and the mutational status of IgVH are unknown. We also have no explanation for the inconsistency between mutational status and ZAP-70 levels in three of our patients. A discrepancy between ZAP-70 expression, as assessed by Western blotting, and the IgVH mutational status was also found in 1 of 22 patients in another series.17
Apart from CLL cells, ZAP-70 was expressed only in T cells and tumors of T-cell lineage, whereas it was barely detectable in normal CD19+CD5+ cells. It was not detected by Western blotting or immunohistochemistry in any of the B-cell lines or biopsy specimens of mantle-cell lymphoma. Nevertheless, ZAP-70 messenger RNA has been found in other B-cell lines with the use of reverse-transcriptase–PCR (RT-PCR) analysis.16 Our results indicate that, among B-cell and T-cell lymphoproliferative disorders, a high level of ZAP-70 expression is restricted to T-cell proliferative diseases and a subgroup of CLL.
The use of flow cytometry to assess the level of ZAP-70 expression offers advantages over other systems of analysis. With flow cytometry, it is possible to analyze the percentage of ZAP-70–positive cells selectively in subpopulations of CLL cells, T cells, and natural killer cells. By contrast, Western blotting and RT-PCR can overestimate the level of expression of ZAP-70 owing to the presence of T cells in the sample.16,17
The value of CD38 as a surrogate for IgVH mutations is controversial.32,33 Moreover, the level of CD38 expression may vary over the course of the disease.34 In our series, the level of CD38 expression did not correlate with disease progression or survival. In contrast, the level of expression of ZAP-70 did not change over time, and the presence of ZAP-70 was associated with rapid progression and poor survival.
In conclusion, the expression of ZAP-70 by CLL cells, as ascertained by flow-cytometric analysis, is a simple and reliable surrogate for the identification of IgVH mutations. Moreover, ZAP-70 expression by itself can be used as a prognostic marker. For these reasons, ZAP-70 analysis should be included in the workup of patients with CLL.
Supported in part by grants from the José Carreras International Foundation against Leukemia (EM/02 and CR/02), Fondo de Investigaciones Sanitarias (02/0250 and 01/1581), and Ministerio de Ciencia y Tecnologia (SAF-02-3261). Ms. Crespo is a recipient of a grant from Fondo de Investigaciones Sanitarias, Spain.
Ms. Crespo and Drs. Bosch and Villamor contributed equally to the article.
We are indebted to Professor Freda K. Stevenson for technical advice in the analysis of the somatic mutations of IgVH , to Montse Sánchez for immunohistochemical analysis, and to Penelope Elvy and Eoin McGrath for their assistance in the preparation of the manuscript.
Source Information
From the Department of Hematology (M.C., F.B., A.L.-G., E.M.) and the Hematopathology Unit (N.V., B.B., D.C., M.R., S.M., E.C.), Institut d'Investigacions Biomèdiques August Pi i Sunyer, Hospital Clínic, Barcelona, Spain.
Address reprint requests to Dr. Bosch at the Department of Hematology, Hospital Clínic, Villarroel 170, Barcelona 08036, Spain, or at fbosch@clinic.ub.es.
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