Original Article
Langerhans'-Cell Histiocytosis (Histiocytosis X) -- A Clonal Proliferative Disease
N Engl J Med 1994; 331:154-160July 21, 1994
- Abstract
Background
The lesions of Langerhans'-cell histiocytosis (histiocytosis X), a proliferative histiocytic disorder of unknown cause, contain histiocytes similar in phenotype to dendritic Langerhans' cells. The disease ranges in severity from a fatal leukemia-like disorder to an isolated lytic lesion of bone. Intermediate forms of the disease are usually characterized by multiorgan involvement, diabetes insipidus, and a chronic course.
Methods
To determine whether Langerhans' histiocytosis is a polyclonal reactive disease or a clonal disorder, we used X-linked polymorphic DNA probes (HUMARA, PGK, M27β[DXS255], and HPRT) to assess clonality in lesional tissues and control leukocytes from 10 female patients with various forms of the disease. Lymphoid clonality was also assessed by analysis of rearrangements at immunoglobulin and T-cell-receptor gene loci.
Results
The HUMARA assay detected clonal cells in the lesions of 9 of the 10 patients: 3 patients had acute disseminated disease, 3 had unifocal disease, and 3 had intermediate forms. The percentage of clonal cells closely approximated the percentage of CD1a-positive histiocytes in each lesion. Clonality was also confirmed in two of nine cases with the PGK or M27β probe. Extreme constitutional lyonization precluded assessment of clonality in the 10th case. Lymphoid clonality was ruled out in all cases.
Conclusions
The detection of clonal histiocytes in all forms of Langerhans'-cell histiocytosis indicates that this disease is probably a clonal neoplastic disorder with highly variable biologic behavior. Thus, genetic mutations that promote clonal expansion of Langerhans' cells or their precursors may now be identified.
Media in This Article
Figure 1
The HUMARA Clonality Assay.Figure 2
Assessment of Clonality in Patient 1 by the HUMARA PCR Assay.Article Activity
- Article
Langerhans'-cell histiocytosis (LCH) encompasses several disorders previously known as histiocytosis X, Letterer-Siwe disease, Hand-Schuller-Christian syndrome, eosinophilic granuloma of bone, and self-healing reticulohistiocytosis1,2. The clinical varieties of LCH range from a lethal leukemia-like disorder that primarily affects infants to a curable solitary lytic lesion of bone. Intermediate forms characterized by lesions of bone, skin, and mucous membranes, various degrees of organ dysfunction, and diabetes insipidus have an indolent course. In contrast to the clinical heterogeneity of LCH, the pathologic features of all forms of the disease are more uniform. The lesions consist of histiocytes that resemble in morphology and phenotype the dendritic antigen-presenting Langerhans' cells of the skin and other organs1,3-6. Like their normal counterparts, pathologic Langerhans' cells are positive for HLA-DR, CD1a, S100, and the Fc receptor; some contain Langerhans' cell (Birbeck) granules1. Although LCH was described a century ago,7 its cause and pathogenesis are still unknown. The prevailing opinion is that LCH is a reactive disorder rather than a neoplastic process8. However, this assumption has never been definitively tested.
An important distinguishing feature of a neoplasm is its origin from a single clone of cells9. A reactive process, by contrast, is polyclonal. Clonality can be assessed in any cell lineage in the majority of female subjects by molecular analysis of patterns of X-chromosome inactivation (reviewed by Vogelstein et al.10,11 and Busque and Gilliland12). In female subjects, each somatic cell randomly inactivates one X chromosome early in embryogenesis and transmits its pattern of inactivation (lyonization) to all progeny cells. Methods of assessing the clonality of cells from a female subject follow the principle of lyonization. DNA probes that can detect polymorphisms at a particular X-linked locus allow a distinction to be made between the maternal X chromosome and the paternal X chromosome. The active X chromosome may be distinguished from the inactive X chromosome by its state of methylation or by gene expression. Ideally, half the cells in a polyclonal tissue will have inactivated the paternally derived X chromosome, and half the maternally derived X chromosome. A monoclonal, or “clonal,” population of cells, by contrast, exclusively inactivates one X chromosome.
Three X-linked polymorphic loci have been used to analyze clonality: the loci for phosphoglycerate kinase (PGK)10,11 and hypoxanthine phosphoribosyltransferase (HPRT)10,11 and the hypervariable locus DXS255 (M27β)13-17. However, a low frequency of polymorphisms limits the usefulness of HPRT and PGK because of the low incidence of polymorphisms at these loci in the two X chromosomes,11,12 whereas variable methylation may restrict the utility of M27β15,16. These shortcomings have been overcome with the X-linked human androgen-receptor (HUMARA) gene; analysis of clonality at this locus produces superior results because of its high rate of heterozygosity (informativeness) (>90 percent) and consistent patterns of methylation12,18,19. An aspect of lyonization that complicates the analysis is that nonrandom patterns of X-chromosome inactivation may occur in up to 25 percent of female subjects (skewed lyonization). Thus, their normal tissues may mimic the molecular pattern of a clonal population of cells12,20. It is therefore essential to compare patterns of X-chromosome inactivation in pathologic tissues with the patterns in normal cells derived from a similar embryologic lineage in each subject.
To determine whether LCH is a clonal or a polyclonal disorder, we used HUMARA, HPRT, PGK, and M27β probes to evaluate clonality in lesional cells and peripheral leukocytes from 10 female patients with various forms of LCH.
Methods
Case Histories
Female patients with LCH were chosen for our study on the basis of the availability of appropriate fresh or frozen lesional tissues obtained for diagnosis and control samples of peripheral blood. Informed consent was obtained in all cases. The presence of CD1a-positive histiocytes and Langerhans'-cell granules confirmed the diagnosis of LCH in each case21. When frozen tissues were available (for all 10 patients except Patients 4 and 5), the percentage of CD1a-positive cells relative to the total number of nucleated cells in the lesion was determined by counting 500 cells in each of two fields in an immunoperoxidase-stained frozen section taken from the same tissue used for molecular analysis4,5. The lesions studied had been obtained before treatment in all patients except one (Patient 6), from whom tissue was obtained after radiation to a site remote from the sample.
Three patients presented with “acute disseminated LCH”22 involving the skin, liver, spleen, and lymph nodes (Patients 1, 2, and 3). Lymph-node biopsies provided diagnostic material and tissue for molecular studies. All three patients received intensive multiagent chemotherapy; Patient 1 died 10 months after diagnosis, and Patients 2 and 3 have survived 9 and 40 months after diagnosis, respectively.
Four patients presented with the intermediate form of LCH, with multiple bone lesions and various degrees of organ dysfunction (Patients 4, 5, 6, and 7). Diagnostic biopsies of osseous lesions provided tissue for molecular studies. A lymph-node biopsy was performed in Patient 7 during the course of disease after cranial irradiation and multiagent chemotherapy, and this specimen was also analyzed for clonality. Patient 4 died two years after diagnosis despite multiagent chemotherapy and local irradiation of affected mastoid processes. Patient 5 has remained free of any evidence of disease after therapy with vinblastine and prednisone. Patients 6 and 7 have active disease; Patient 7 has diabetes insipidus associated with a progressive hypothalamic tumor.
Three patients presented with LCH confined to a single bony lesion (Patients 8, 9, and 10). Specimens obtained during diagnostic biopsy of this tissue were used for clonality studies. These three patients were treated with curettage and are disease-free 16, 13, and 12 months after diagnosis, respectively.
Assessment of Lymphoid Clonality
To detect clonal lymphoid cells, rearrangements of genes encoding the variable region of immunoglobulin heavy chain and the beta, gamma, and delta chains of the T-cell-antigen receptor were identified in DNA from the patients' lesions according to established methods with a sensitivity of 2 percent23.
Molecular Assessment of Clonality with HPRT, PGK, and M27β Probes
Lesional DNA was analyzed for clonality at the HPRT,10,11 PGK,10,11 and DXS255(M27β)13,14,17 loci with established Southern blotting techniques (reviewed by Busque and Gilliland12). Alleles were quantitated by laser densitometric scanning of autoradiographs; allelic ratios for M27β and PGK were calculated as previously described17,20. Clonality at the PGK locus was also assessed with a polymerase-chain-reaction (PCR) assay24.
Molecular Assessment of Clonality at the HUMARA Locus
Clonality at the HUMARA locus was assessed by PCR amplification according to a modification of the technique of Allen et al.18 (Figure 1Figure 1
The HUMARA Clonality Assay.). A total of 10 ng to 1 μg of DNA was digested overnight at 37 °C in a 20-microliter reaction mixture containing RsaI (20 units) or RsaI with 40 units of HpaII. The restriction enzymes were then inactivated by heating at 95 °C for 10 minutes. For the PCR, 2 microliters of the digested DNA was combined with 23 microliters of PCR reaction mixture, for a final concentration of 50 mmol of potassium chloride per liter, 10 mmol of TRIS (pH 8.3) per liter, 1.5 mmol of magnesium chloride per liter, 0.01 percent gelatin, 200 μmol of each deoxynucleotide triphosphate per liter, 5 pmol of each primer, 0.5 pmol of primer 1 labeled with γ[P32]-ATP kinase, 0.05 unit of Taq polymerase, and 5 percent dimethylsulfoxide. The sequences of the primers used for amplification in the HUMARA assay were 5'GCTGTGAAGGTTGCTGTTCCTCAT3' (primer 1) and 5'TCCAGAATCTGTTCCAGAGCGTGC3' (primer 2). Initial denaturation was performed for 3 minutes at 94 °C, followed by 28 cycles of 45 seconds at 94 °C, 30 seconds at 60 °C, and 30 seconds at 72 °C. After amplification, 12.5 microliters of sequencing-denaturing loading buffer was added to each tube; the samples were heated at 94 °C for five minutes and then quenched with ice. The samples were loaded on denaturing-sequencing gels composed of 4 percent 19:1 acrylamide:bisacrylamide in 30 percent formamide, 4 M urea, and TRIS borate EDTA buffer. The gels were run at 80 W for 4 hours, dried, and left on PhosphorImager screens (Molecular Dynamics) for 24 hours. Allele intensity was quantitated with ImageQuant 3.15 software.For each sample, a corrected ratio was calculated by dividing the ratio of the predigested sample (allele 1/allele 2) obtained after digesting DNA with RsaI and HpaII, by the ratio of the non-predigested sample (allele 1/allele 2) obtained after digesting DNA with RsaI alone. The use of this ratio corrected for the preferential amplification of one allele that might occur if the alleles differed markedly in the length of their repeats, or if the allele on the active X chromosome was more readily amplified. A final clonality ratio for each patient was determined by dividing the corrected ratio of the lesional DNA by that of the control DNA, thereby normalizing values for unequal lyonization. The percentage of clonal cells was estimated by comparing the final ratio with a standard curve of allelic ratios plotted against percentages of clonal cells. Experiments mixing polyclonal and clonal cells have demonstrated that the percentage of clonal cells can be estimated with an error of ±10 percent, and that a clonal population of cells can be detected if they constitute more than 10 to 15 percent of cells in a polyclonal background (unpublished data). All assays were performed in triplicate, with the assayer blinded to the percentage of lesional histiocytes.
Results
Patterns of X-chromosome inactivation in lesional tissue were compared with those in control leukocytes in peripheral blood from the 10 female patients with LCH. The HUMARA locus was informative in all 10 patients (Table 1Table 1
Molecular Analysis of Clonality in Patients with LCH.). By contrast, the HPRT locus was uninformative in all patients tested (Patients 1 through 8; data not shown), and the PGK locus was informative in only one (Patient 8). Similarly, clonality could be reliably assessed with M27β in only one patient (Patient 1); variable methylation, inability to resolve overlapping alleles, or inadequacy of the amounts of DNA for Southern blotting led to uninterpretable results in the other patients. Lesional DNA from all patients lacked clonal rearrangements of the immunoglobulin heavy chain or T-cell-receptor beta-, gamma-, and delta-chain genes, precluding the presence of a lymphoid clone in each patient (data not shown).Acute Disseminated LCH
Clonal cells were detected in affected lymph nodes with the HUMARA assay (Figure 1) in all three patients with the acute disseminated form of LCH. In Patient 1, the ratio of the two HUMARA alleles (one from the maternal and one from the paternal X chromosome) in the control DNA was 1.09, a value close to the ideal ratio of 1.0 for a completely random pattern of X-chromosome inactivation (Table 1 and Figure 2AFigure 2
Assessment of Clonality in Patient 1 by the HUMARA PCR Assay.). In contrast, when the HUMARA locus in DNA from this patient's lymph node was amplified by PCR, there was preferential amplification of the larger HUMARA allele, which contains a longer triplet-repeat expansion (Figure 2B). The HUMARA-allele ratio in the lymph node, which was effaced by histiocytes, was 5.12, a value reflecting nonrandom X-chromosome inactivation and consistent with a predominantly clonal population. The final corrected clonality ratio, 4.7, was converted to a percentage of clonal cells, 65 percent (error, ±10 percent) (Table 1; see the Methods section). This value was similar to the percentage of CD1a-positive histiocytes in the lesion (70 percent) (Table 1). The close agreement between the molecular and histochemical results, along with the absence of a clonal lymphoid population, is strong evidence that the clonal cells in this lesion were the CD1a-positive histiocytes.Clonality was also confirmed with the M27β probe in Patient 1 (Table 1 and Figure 3Figure 3
Analysis of Clonality at the M27β Locus in Patient 1.). Although both M27β alleles in the control DNA were digested with methylation-sensitive restriction enzymes, indicating random X-chromosome inactivation (Figure 3A, lane 3), the two alleles were not digested equally, as in previous studies15,16. However, comparison of the digestion patterns in control DNA with those in lesional DNA did reveal very different patterns of X-chromosome inactivation. In lesional DNA, the upper M27β allele was substantially digested, whereas the lower allele was undigested (Figure 3B, lane 3). This pattern is consistent with preferential inactivation (methylation) of the lower allele and the presence of a clonal population of cells. The M27β-allele ratio was 1.9:1 in control DNA and greater than 10:1 in lesional DNA (Table 1).Clonality was also demonstrated in Patients 2 and 3, with the HUMARA assay (Table 1 and Figure 4Figure 4
Assessment of Clonality in Patient 2 by the HUMARA PCR Assay.). Although control DNA from Patient 2 had a nonrandom pattern of X-chromosome inactivation (corrected ratio for HUMARA alleles, 1.57), DNA from this patient's lymph node showed a markedly skewed pattern (corrected ratio, 4.9), indicating that a clonal population constituted 50 ±10 percent of the lymph-node cells. These data were consistent with the virtual effacement of this patient's lymph node by CD1a-positive histiocytes (Figure 5AFigure 5
Immunoperoxidase Staining of CD1a-Positive Langerhans' Histiocytes in Lymph Nodes from Patient 2 (Panel A, x200) and Patient 3 (Panel B, x200).). In contrast to the specimens from Patients 1 and 2, the lymph node from Patient 3 showed only focal sinusoidal involvement by CD1apositive histiocytes (Figure 5B). Nonetheless, a clonal population of cells constituting 25 ±10 percent of total cells could be detected with the HUMARA assay.Intermediate Forms of LCH
Specimens from Patients 4, 5, 6, and 7 were cytologically heterogeneous and contained relatively small numbers of CD1a-positive histiocytes admixed with eosinophils and other cells. However, in three of these four patients clonal cells could be detected in lesional tissues with the HUMARA assay (Table 1). With frozen tissues, the percentage of clonal cells determined with the HUMARA assay was close to the percentage of CD1a-positive histiocytes (Table 1). Control samples from Patients 4 and 5 had nonrandom patterns of X-chromosome inactivation, but the lesional tissues clearly contained clonal cell populations. In Patient 7, clonal cells were detected in a bone-biopsy specimen obtained before treatment and in an affected lymph node obtained three years after the biopsy. Both clonal populations had inactivated the same X chromosome, implying that the same clone persisted during the course of this patient's illness.
Clonality could not be determined definitively in Patient 6, a known carrier of X-linked spinobulbar muscular atrophy, because of extreme constitutional lyonization. This disease results from expansion of the polymorphic cysteine-alanine-glycine (CAG) repeat in the first exon of the HUMARA locus itself25. However, although control DNA displayed marked skewing (corrected ratio, 3.23), lesional DNA was skewed in the opposite direction (corrected ratio, 2.7), suggesting the presence of a clonal cell population.
Unifocal LCH
The HUMARA assay also detected clonal cells in bone-biopsy specimens from the three patients with solitary bone lesions (Table 1, Patients 8, 9, and 10). Despite skewed lyonization in normal DNA from Patient 8, the HUMARA assay revealed skewing in favor of the opposite HUMARA allele in lesional DNA (as in Patient 6). Clonality was also found in this patient with the PGK assay (Table 1). In each of the three patients, there was a close agreement between the percentage of clonal cells determined with the HUMARA assay and the percentage of CD1a-positive histiocytes in the lesion.
Discussion
Langerhans'-cell histiocytosis, an enigmatic disorder, has been variously classified as a neoplastic process, a reactive disorder, or an aberrant immune response1. A wide spectrum of disease and variable clinical behavior are characteristic. Although histopathological examination cannot predict clinical outcome, recent studies have shown that Langerhans' cells within the lesions of LCH are intrinsically proliferative26. In our study of 10 female patients with various forms of LCH whose ages ranged from 3 months to 25 years, molecular analysis revealed evidence of clonal cells in all 9 patients in whom results could be interpreted with confidence. The HUMARA PCR-based assay proved to be a powerful method of assessing clonality. In contrast to other X-linked polymorphic loci, the HUMARA locus had a high rate of informativeness, which allowed clonality to be determined in all patients. Quantitation of HUMARA alleles with PhosphorImager analysis gave the assay remarkable sensitivity, an essential feature in studies of cytologically heterogeneous lesions, such as those in LCH. The excellent agreement between the percentage of clonal cells detected with the HUMARA assay and the percentage of CD1a-positive histiocytes in each lesion, together with the absence of clonal lymphoid cells, strongly supports the conclusion that the clonal cells in LCH are the CD1a-positive Langerhans' cells. Our results thus show that LCH is a clonal histiocytic disease rather than a reactive polyclonal disorder.
It is notable that all three forms of LCH had a clonal pattern. The detection of clonal histiocytes in children with the acute disseminated form of disease was not unforeseen; this “leukemia-like” form of LCH behaves like a neoplastic process, with mortality rates approaching 60 to 65 percent among infants8,22,27,28. However, the presence of clonal histiocytes in intermediate forms of LCH was surprising. In this type of LCH the survival rate is 60 to 70 percent among children two years old or younger and 80 percent among children more than two years old8,27,28; spontaneous regression has rarely been reported8,29. The finding of clonal histiocytes in unifocal LCH was also unexpected, since this form of disease is the most clinically benign.
Although the possibility that LCH has a viral pathogenesis is of considerable interest, McClain et al.,30 using molecular methods to detect the genomes of Epstein-Barr virus, human herpesvirus type 6, and seven other viruses, found no trace of viral DNA in 50 cases of LCH. Leahy et al.31 have implicated human herpesvirus type 6, but their study requires confirmation. Recent ultrastructural studies also found no evidence of virus32. However, the remote possibility remains that LCH could result from a virally induced clonal proliferation of dendritic Langerhans' cells.
More compelling is the possibility that LCH is a clonal neoplastic disorder that arises from somatic mutations that cause the clonal expansion of Langerhans' cells or their precursors in bone marrow and organs. The extreme rarity of familial cases makes it unlikely that a predisposing mutation could be inherited in LCH as in other childhood neoplasms. Since our studies revealed that clonal histiocytes occur in all forms of LCH, clonality alone will not suffice to predict biologic behavior and clinical course. Indeed, clonal cells have been detected in several disorders that may not be overtly “malignant.”33-36 However, if each form of LCH were to have distinct mutations, then molecular assessment at the time of diagnosis might allow one to predict the clinical course and to direct appropriate therapy.
Supported by the Histiocytosis Association of America, the Dedicated Health Research Fund of the State of New Mexico, the All Children's Hospital Foundation Histiocytosis Research Fund, and the National Cancer Institute of Canada.
We are indebted to the Toughill and Kontoyannis families, the Histiocytosis Association of America, and the Nikolas Symposia for the creation of research forums and funding for the histiocytoses; to our collaborators for submitting case materials and clinical histories -- Vickey Gresik, M.D. (Department of Pathology, Texas Children's Hospital, Baylor School of Medicine, Houston), Peter Isaacson, M.D. (Department of Histopathology, University College, London Medical School, London), Ron Jaffe, M.D. (Department of Pathology, Children's Hospital of Pittsburgh, Pittsburgh), James Navin, M.D. (Department of Laboratories, Kapiolani Medical Center for Women and Children, Honolulu), and Charles Palmer, M.D. (Presbyterian Hospital, Albuquerque, N.M.); and to Loretta Kanapilly-Chavez and Brian Schnell, M.D., for technical assistance.
Source Information
From the Departments of Pathology and Pediatrics, the Center for Molecular and Cellular Diagnostics, and the Cancer Center, University of New Mexico School of Medicine, Albuquerque (C.L.W., B.B.G., M.H.D.); the Division of Hematology-Oncology, Brigham and Women's Hospital, Harvard Medical School, Boston (L.B., D.G.G.); the Department of Pathology and Laboratory Medicine, All Children's Hospital, St. Petersburg, Fla. (B.E.F.); and the Department of Pediatrics, Texas Children's Hospital, Baylor College of Medicine, Houston (K.L.M.)
Address reprint requests to Dr. Willman at the University of New Mexico Cancer Center, 900 Camino de Salud, N.E., Albuquerque, NM 87131.
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