Original Article
A Gain-of-Function Mutation of JAK2 in Myeloproliferative Disorders
N Engl J Med 2005; 352:1779-1790April 28, 2005
- Abstract
Background
Polycythemia vera, essential thrombocythemia, and idiopathic myelofibrosis are clonal myeloproliferative disorders arising from a multipotent progenitor. The loss of heterozygosity (LOH) on the short arm of chromosome 9 (9pLOH) in myeloproliferative disorders suggests that 9p harbors a mutation that contributes to the cause of clonal expansion of hematopoietic cells in these diseases.
Methods
We performed microsatellite mapping of the 9pLOH region and DNA sequencing in 244 patients with myeloproliferative disorders (128 with polycythemia vera, 93 with essential thrombocythemia, and 23 with idiopathic myelofibrosis).
Results
Microsatellite mapping identified a 9pLOH region that included the Janus kinase 2 (JAK2) gene. In patients with 9pLOH, JAK2 had a homozygous G→T transversion, causing phenylalanine to be substituted for valine at position 617 of JAK2 (V617F). All 51 patients with 9pLOH had the V617F mutation. Of 193 patients without 9pLOH, 66 were heterozygous for V617F and 127 did not have the mutation. The frequency of V617F was 65 percent among patients with polycythemia vera (83 of 128), 57 percent among patients with idiopathic myelofibrosis (13 of 23), and 23 percent among patients with essential thrombocythemia (21 of 93). V617F is a somatic mutation present in hematopoietic cells. Mitotic recombination probably causes both 9pLOH and the transition from heterozygosity to homozygosity for V617F. Genetic evidence and in vitro functional studies indicate that V617F gives hematopoietic precursors proliferative and survival advantages. Patients with the V617F mutation had a significantly longer duration of disease and a higher rate of complications (fibrosis, hemorrhage, and thrombosis) and treatment with cytoreductive therapy than patients with wild-type JAK2.
Conclusions
A high proportion of patients with myeloproliferative disorders carry a dominant gain-of-function mutation of JAK2.
Media in This Article
Figure 1
Mapping of the Minimal 9pLOH Region in Patients with Myeloproliferative Disorders.Figure 2
The JAK2 Mutation in Patients with Myeloproliferative Disorders.Article Activity
- Article
The myeloproliferative disorders are a heterogeneous group of diseases characterized by excessive production of blood cells by hematopoietic precursors. In addition to thrombotic and hemorrhagic complications, leukemic transformation can occur.1 Typically, the myeloproliferative disorders encompass four related entities2: chronic myelogenous leukemia (CML), polycythemia vera, essential thrombocythemia, and idiopathic myelofibrosis. Clonal hematopoiesis is a key feature of these disorders.3-5 The lesion is believed to involve the hematopoietic stem cell, since all myeloid lineages and, frequently, the B-cell lineage are monoclonal. T cells, however, are polyclonal.4,6
Progenitor cells in polycythemia vera form erythroid colonies in the absence of exogenous erythropoietin. These endogenous erythroid colonies7 have been used in an auxiliary diagnostic assay to distinguish polycythemia vera from secondary erythrocytosis,8 but they also occur in some cases of essential thrombocythemia and idiopathic myelofibrosis. More important, the presence of endogenous erythroid colonies is a hallmark of abnormal in vitro growth of hematopoietic progenitors, and this finding has been the basis of many studies of signaling by cytokine receptors of hematopoietic cells. These receptors transduce signals by activating members of the Janus kinase (JAK) family of proteins, which phosphorylate cytoplasmic targets, including the signal transducers and activators of transcription (STATs).9 Constitutive activation of the STAT3 protein has been found in 30 percent of patients with polycythemia vera,10 and a decrease in the level of the thrombopoietin receptor protein in platelets is a feature of both polycythemia vera and essential thrombocythemia.11,12 Only the late steps of differentiation of endogenous erythroid colonies in polycythemia vera are erythropoietin-independent, and they can be blocked by inhibitors of JAK2, phosphatidylinositol 3' kinase, or kinases of the Src family.13 Recently, the tyrosine kinase inhibitor imatinib mesylate has been reported to produce clinical responses in patients with polycythemia vera.14,15 These data suggest the involvement of a kinase in the pathogenesis of myeloproliferative disorders.
Cytogenetic abnormalities occur in only 10 to 15 percent of patients with myeloproliferative disorders.16-18 The most common abnormalities are deletions in chromosome 20q.19,20 Fluorescence in situ hybridization and comparative genomic hybridization suggested a role for chromosome 9p.20-23 Using genome-wide microsatellite screening, we identified loss of heterozygosity (LOH) on the short arm of chromosome 9 (9pLOH) in six patients with polycythemia vera24; using microsatellite markers within the LOH region, we found 9pLOH in 13 of 43 patients with polycythemia vera and 1 of 15 patients with essential thrombocythemia.24,25 Markers from the 9pLOH region did not cosegregate with the phenotype in four families with polycythemia vera, suggesting that a somatic event causes 9pLOH.26 In the present study, we increased the number of microsatellite markers in order to map a minimal genomic region shared by all patients with 9pLOH and myeloproliferative disorders to identify potential candidate genes.
Methods
Subjects
We evaluated 244 patients with myeloproliferative disorders from Switzerland and Italy: 128 patients with polycythemia vera, 93 with essential thrombocythemia, and 23 with idiopathic myelofibrosis.25,27,28 We studied 41 healthy persons, 9 patients with chronic myelogenous leukemia, and 11 patients with secondary erythrocytosis as controls. The study was approved by the local ethics committees, and all samples were obtained after subjects provided written informed consent. In addition, we used DNA from 30 archival samples. The diagnostic criteria of the World Health Organization (WHO) were followed for all Swiss patients, whereas the Polycythemia Vera Study Group (PVSG) criteria were used for all Italian patients.29-31 The main difference between the two classifications is the use of bone marrow histologic findings as a diagnostic criterion in the WHO classification to distinguish early stages of idiopathic myelofibrosis from essential thrombocythemia or polycythemia vera. The presence of endogenous erythroid colonies is a major WHO criterion and a minor PVSG criterion.
Isolation of Cells and DNA
Granulocytes were isolated,24 and analysis of cytospin preparations verified that the purity exceeded 90 percent. Peripheral-blood CD4+ T cells were isolated by means of magnetic sorting (Miltenyi Biotech). Peripheral-blood mononuclear cells (PBMCs) were prepared with the use of Ficoll gradient centrifugation. Buccal mucosal cells were obtained with cytologic brushes, and hair-follicle DNA was prepared from plucked hair. Genomic DNA was isolated with the use of the QIAmp DNA Blood Mini Kit (Qiagen).
Detection of LOH
LOH was detected by means of fluorescence microsatellite polymerase-chain-reaction (PCR) analysis with the use of primer sequences from public databases (listed in the Supplementary Appendix, available with the complete text of this article at www.nejm.org). The samples were analyzed on a DNA genetic analyzer (model 3100, Applied Biosystems). LOH was considered to be present if one allele showed a reduction in the peak fluorescence intensity of more than 90 percent in granulocytes, but two alleles were present in nonclonal tissues (T cells, PBMCs, buccal mucosa, or hair-follicle cells) from the same patient.
Analysis of the Number of Gene Copies
The number of copies of chromosome 9p in granulocyte DNA was determined with the use of quantitative PCR by comparing two single-copy loci: one in exon 14 of JAK2 and an uncharacterized gene on chromosome 13. The primers and details of these assays are provided in the Supplementary Appendix.
JAK2 Sequencing
We sequenced the JAK2 complementary DNA (cDNA) with reverse-transcriptase (RT) PCR using seven pairs of overlapping primers described in the Supplementary Appendix (sequence information is available on request).
DNA Constructs
The mutant JAK2 cDNA was amplified by RT-PCR with the use of granulocyte RNA from a patient who was homozygous for the mutation. The Supplementary Appendix gives details of the primers and cloning into vectors.
Proliferation Assays
The mouse interleukin 3–dependent cell line BaF3 and the human thrombopoietin-dependent cell line UT-7/TPO (kindly provided by Dr. N. Komatsu) were transfected by electroporation with the wild-type JAK2 (plasmid murine stem-cell virus [pMSCV]–Jak2) and mutant JAK2 (pMSCV-V617F-Jak2) constructs. The Supplementary Appendix gives details of the assays for proliferation and cell viability.
Immunoprecipitation and Western Blotting
BaF3 cells were incubated in a culture medium (RPMI) containing 10 percent fetal-calf serum in the absence of interleukin-3 for 12 hours at 37°C, whereupon various concentrations of interleukin-3 were added for 15 minutes. Cell lysates were prepared as previously described.32 Immunoprecipitation and immunoblotting were carried out with the use of polyclonal antibodies against JAK2 (Upstate) and STAT5 (Santa Cruz) and the phosphotyrosine-specific mouse monoclonal antibody 4G10 (Upstate).
Statistical Analysis
We used the chi-square or Fisher's exact test where appropriate to compare categorical variables among the groups, which were categorized according to mutational status (heterozygous, homozygous, or wild type), and the Mann–Whitney U test or Kruskal–Wallis test to compare continuous variables among the groups. For some analyses, the heterozygous and the homozygous groups of patients were pooled and compared with patients without JAK2 mutations.
Results
Fine Mapping of the Common 9pLOH Region
Using 10 microsatellite markers covering chromosome 9p, we found 9pLOH in granulocytes from 51 of 244 patients with myeloproliferative disorders (21 percent), but not in those from any of the control subjects: 41 healthy subjects, 9 patients with CML, and 11 patients with secondary erythrocytosis. The frequency of 9pLOH was 34 percent among patients with polycythemia vera, 22 percent among patients with idiopathic myelofibrosis, and 3 percent among patients with essential thrombocythemia. The size of the chromosomal region showing LOH varied, but the telomeric region of chromosome 9p was always involved (Figure 1AFigure 1
Mapping of the Minimal 9pLOH Region in Patients with Myeloproliferative Disorders.). By aligning the LOH regions of all 51 patients with 9pLOH, we identified a 6.2-Mbp interval common to all patients that extended from the telomere to marker D9S1852 and contained the gene for the tyrosine kinase JAK2 (Figure 1B). Since JAK2 mediates signaling through several hematopoietic cytokine receptors, we considered JAK2 an attractive candidate gene.9pLOH and a G→T Mutation in the Coding Region of JAK2
The coding region of JAK2 in all 51 patients with 9pLOH had a G→T transversion that changed a valine to a phenylalanine at position 617 (V617F; GenBank accession number AY973037) (Table 1Table 1
Frequency of the JAK2 V617F Mutation. and Figure 2Figure 2The JAK2 Mutation in Patients with Myeloproliferative Disorders.). All patients with 9pLOH are expected to be homozygous (both alleles mutated) or hemizygous (one allele mutated and the other absent) for the V617F mutation. However, in eight patients, the findings were compatible with the presence of heterozygosity (one allele was mutated, and the other was wild type) (Table 1). Our definition of LOH allows 10 percent of granulocytes without 9pLOH to be present in a given sample and the ratios of G and T peak intensities in sequencing chromatograms cannot be used to quantify allelic ratios. It is therefore likely that an admixture of granulocytes with wild-type or heterozygous V617F genotypes caused the apparent heterozygosity in these eight patients. Of the remaining 193 patients without 9pLOH, 34 percent were heterozygous for V617F and 66 percent were homozygous for the wild-type allele; none were homozygous for V617F (Table 1). The V617F mutation was absent in 71 healthy controls, 11 patients with secondary erythrocytosis, and 9 patients with CML (Table 1).The mutation was present in 65 percent of patients with polycythemia vera, as compared with 57 percent of those with idiopathic myelofibrosis (P=0.72) and 23 percent of those with essential thrombocythemia (P<0.001) (Table 1). Homozygosity for V617F was underrepresented among patients with essential thrombocythemia, as compared with patients with polycythemia vera and patients with idiopathic myelofibrosis, and was linked to the presence of 9pLOH.
The median duration of disease was significantly longer among patients with myeloproliferative disorders who were homozygous for the V617F mutation than among those who were heterozygous for the mutation (48 months [range, 0 to 576] vs. 23 months [range, 0 to 252], P<0.02 by the Mann–Whitney U test). This difference is compatible with the existence of a two-step process to acquire homozygosity. Interestingly, patients with myeloproliferative disorders who had wild-type JAK2 had the shortest duration of disease (15 months; range, 0 to 330; P=0.05 for the comparison with heterozygous patients).
Identification of a Somatic Mutation in Myeloproliferative Disorders
We sequenced DNA from T cells, PBMCs, or nonhematopoietic tissues from 89 patients with the V617F mutation. We could not detect the mutant JAK2 allele in these control tissues, a result consistent with the existence of a somatic mutation. In two patients, we detected the V617F mutation in buccal mucosa cells, but since samples of buccal mucosa can be contaminated with blood, we analyzed hair-follicle cells from these patients and found only the wild-type JAK2 sequence (Figure 2C).
Cause of 9pLOH
The 9pLOH in myeloproliferative disorders could result from deletions of the telomeric portions of chromosome 9p or mitotic recombination between chromatids of homologous 9p chromosomes (Figure 3AFigure 3
Mechanisms of 9pLOH.). In the case of a deletion, we would expect to find only one copy of DNA for the deleted region, whereas two copies should be expected in the event of mitotic recombination (Figure 3A). To evaluate these possibilities, we used quantitative PCR to determine the number of copies of JAK2 and, as a control, the number of copies of a single-copy gene on chromosome 13. Of 33 patients with 9pLOH, all had two copies of chromosome 9p (Figure 3B). This result argues against deletions as the cause of 9pLOH and makes mitotic recombination the most likely mechanism. We also analyzed parental chromosomes of two patients with 9pLOH. In one (Patient 50), the maternally derived chromosome 9p was lost, whereas in the other (Patient 116), the paternal chromosome 9p was missing (Figure 3C). Thus, either maternal or paternal chromosome 9p can be lost, suggesting that genomic imprinting is not involved in the expansion of cells with 9pLOH.Proliferative and Survival Advantage Afforded by V617F
To investigate whether the V617F mutation has functional consequences, we analyzed data on endogenous erythroid colonies in 180 patients with myeloproliferative disorders. Endogenous erythroid colonies were present in 77 of 87 patients with the V617F mutation, whereas only 57 of 93 patients without the mutation had them (P<0.001 by Fisher's exact test). Next, we expressed the JAK2 V617F protein in the mouse interleukin-3–dependent cell line BaF3 (Figure 4Figure 4
Functional Effects of the JAK2 V617F Mutation in Stably Transfected Murine Interleukin-3–Dependent BaF3 Cells.). These transfected cells were hypersensitive to low concentrations of interleukin-3 and were more numerous (elevated baseline value) than control cells in the absence of interleukin-3 (Figure 4A). The same results were obtained in four independent experiments and in analogous experiments with BaF3 cells that were doubly transfected with the erythropoietin receptor gene and JAK2 and in V617F-transfected thrombopoietin-dependent UT-7/TPO human cells (data not shown).Interleukin-3, erythropoietin, and thrombopoietin signaling is dependent on JAK2.33,34 Differences in cell viability were apparent when the transfected BaF3 cell lines were maintained in serum-containing medium in the absence of interleukin-3 (Figure 4B). This result suggests that the transfected JAK2 mutant increased survival of the cells in the absence of the cytokine. Since the proliferation assay measures the numbers of cells after three days of culture, the results obtained in the absence of interleukin-3 in Figure 4A can be compared with those of the viability curves on day 3 in Figure 4B: both show approximately twice the number of viable mutant cells as control cells. When kept under the same conditions for more than 10 days, BaF3 cells transfected with the JAK2 V617F survived, and their numbers increased by a factor of 100, whereas cells transfected with the wild-type JAK2 or the vector control died (Figure 4C).
We also examined the phosphorylation of JAK2 and STAT5 proteins under the same conditions as in the proliferation assays (Figure 4D). JAK2 phosphorylation was only slightly increased in the absence of or at low concentrations of interleukin-3. A more pronounced difference was detected in the phosphorylation of STAT5, one of the principal protein substrates of JAK2 (Figure 4D). At higher interleukin-3 concentrations, these differences disappeared. The differences in signaling mirrored the differences in growth and survival observed at the same cytokine concentrations. Thus, the presence of JAK2 V617F conferred a proliferative and survival advantage by rendering the cells more sensitive to incoming stimulatory signals.
Correlations with Clinical Data
Possible associations between the V617F mutation and clinical features were retrospectively analyzed in 244 patients. The only significant differences between patients who were heterozygous and those who were homozygous for the V617F mutation were the above-mentioned increase in the median duration of disease and the correlation between 9pLOH and homozygosity for the mutation. Therefore, we limited our comparison to patients with the V617F mutation and those without the mutation (Table 2Table 2
Characteristics Associated with the JAK2 V617F Mutation.). Significantly more patients with the mutation than without the mutation had complications (secondary fibrosis, hemorrhage, and thrombosis) and had received cytoreductive treatment. Of five patients with leukemic transformation, four had the V617F mutation (P=0.20).Discussion
Fine mapping of the 9pLOH region in patients with myeloproliferative disorders identified a 6.2-Mbp genomic interval that contains the gene for the tyrosine kinase JAK2 (Figure 1). This gene, JAK2, was a strong candidate for causing clonal expansion of hematopoietic progenitors in myeloproliferative disorders because of its essential function in hematopoiesis.33,34 We found a G→T transversion that results in a change in a single amino acid, V617F, in the pseudokinase domain of JAK2 (Figure 2 and Table 1). V617F is not a polymorphism, since it was absent from 142 chromosomes of healthy people and is not recorded in the databases of single-nucleotide polymorphisms. Moreover, we did not detect the V617F mutation in 11 patients with secondary erythrocytosis or 9 patients with CML.
We found conclusive evidence that V617F is a somatic mutation in hematopoietic cells. We cannot exclude the possibility of germ-line mutations in some cases of familial myeloproliferative disorders, although chromosome 9p was previously excluded by linkage analysis in four families with polycythemia vera.26 The frequency of the V617F mutation was highest among patients with polycythemia vera and lowest among patients with essential thrombocythemia (Table 1). Essential thrombocythemia is the most heterogeneous myeloproliferative disorder, with a substantial proportion of patients showing polyclonal hematopoiesis.4,6,35 The low frequency of 9pLOH in this disease might reflect the low mitotic activity in the essential-thrombocythemia progenitor or stem-cell pool.
It is remarkable that we found an identical somatic G→T transversion in JAK2 in 117 unrelated patients, or 48 percent of the patients with myeloproliferative disorders (Table 1). The V617F mutation is located in the pseudokinase domain of JAK2 (Figure 2B), a region that inhibits JAK2 kinase activity.36,37 Mutations affecting this domain are associated with malignant transformation of hematopoietic cells in drosophila.38
BaF3 and UT-7/TPO cells that were transfected with the mutant JAK2 gene were hypersensitive to low concentrations of interleukin-3 and erythropoietin and thrombopoietin, respectively. In the presence of serum, transfected BaF3 cells showed increased survival, proliferation, and phosphorylation of JAK2 and STAT5, even in the absence of interleukin-3 (Figure 4). This result suggests that other cytokines in serum at low concentrations are most likely sufficient to maintain the viability and proliferation of cells expressing JAK2 V617F. Similarly, the growth of endogenous erythroid colonies in myeloproliferative disorders also depends on the presence of serum.39
The effect of the JAK2 V617F mutation on the proliferation of BaF3 cells was less dramatic than that of the TEL-JAK2 fusion protein found in acute lymphoblastic leukemias.40 The relatively subtle effect of the V617F mutation fits well with the mild and indolent nature of the clonal proliferation observed in myeloproliferative disorders. Hypersensitivity to insulin-like growth factor, thrombopoietin, interleukin-3, and other cytokines has been described in hematopoietic progenitor cells from patients with myeloproliferative disorders.39,41-43 How the V617F mutation sustains the increased phosphorylation of JAK2 in the presence of serum, but in the absence of interleukin-3, and the factor or factors in serum that mediate this effect remain unknown. Nevertheless, the functional relevance of the V617F mutation is supported by the finding that endogenous erythroid colonies were present in 89 percent of patients with V617F and the close association between homozygosity for the V617F mutation and 9pLOH, which demonstrates the survival advantage of such homozygous hematopoietic cells.
The gene-dosage analysis suggests that mitotic recombination between chromatids of homologous chromosomes 9p is the most likely mechanism leading to 9pLOH (Figure 3). The absence of homozygosity for the V617F mutation in patients with myeloproliferative disorders who do not have 9pLOH suggests that a transition from heterozygosity to homozygosity by means of a mechanism that is independent of mitotic recombination is rare. Mitotic recombination is a frequent genetic mechanism in the inactivation of tumor-suppressor genes in solid tumors,44-46 but not in malignant diseases of the hematopoietic system.47
Our data suggest two possible pathogenetic mechanisms of the JAK2 V617F mutation. In one (model A in Figure 5Figure 5
Possible Roles of the JAK2 V617F Mutation in Myeloproliferative Diseases.), the heterozygous JAK2 V617F mutation alone or in combination with one or more preexisting somatic mutations causes the myeloproliferative-disorder phenotype in approximately 50 percent of patients. A somatic mutation in an as yet unknown gene would be responsible for the phenotype in the other patients (not shown). This model does not explain the presence of the V617F mutation in several myeloproliferative disorders. Perhaps the genetic background or additional somatic mutations in hematopoietic cells alter the effects of the V617F mutation on the phenotype. In model B, JAK2 V617F occurs after the appearance of the myeloproliferative-disorder phenotype as a mutation associated with disease progression but is not necessary or sufficient to cause the phenotype (Figure 5). In this model, patients with myeloproliferative disorders without the JAK2 mutation have an early stage of the disease. One prediction of this model is that the duration of disease should be shortest in patients without the JAK2 mutation and longest in those who are homozygous for the V617F mutation, as we observed. In both models, the transition from heterozygosity to homozygosity for the mutation represents clonal evolution. Our data indicate that mitotic recombination in patients with 9pLOH produces a daughter cell that is homozygous for the V617F mutation and can outcompete the parental cells that are heterozygous (Figure 3A and Figure 5).Evaluation of the clinical data (Table 2) revealed significant correlations between the presence of the V617F mutation and the frequency of complications (secondary fibrosis, hemorrhage, and thrombosis). These correlations could be a consequence of the longer duration of disease in patients with the JAK2 mutation or could be linked to a more aggressive phenotype, perhaps owing to an increased responsiveness to cytokines. Patients with the V617F mutation were older than those without the mutation, and a higher proportion had received cytoreductive therapy at the time of sample collection. The increased frequency of cytoreductive therapy does not necessarily imply the presence of a more aggressive disease and could be based on age alone, according to widely accepted therapeutic guidelines.
Taken together, our data suggest that the V617F mutation in JAK2 is a dominant gain-of-function mutation that contributes to the expansion of the myeloproliferative-disorder clone. The V617F mutation could form the basis for a new molecular classification of myeloproliferative disorders. Furthermore, in view of the invariant nature of the JAK2 mutation, small molecules could be developed that specifically target the mutated protein in patients with myeloproliferative disorders.
Supported in part by a grant (3100-066 949.01) from the Swiss National Science Foundation, grants (OCS-01163-09-2001 and OCS-01411-08-2003) from the Swiss Cancer League, and a grant from the Stiftung für Hämatologische Forschung (all to Dr. Skoda); by a grant from the Krebsliga beider Basel (to Dr. Kralovics); and by a grant from the Associazione Italiana per la Ricerca sul Cancro, Milan (to Dr. Cazzola).
We are indebted to the patients and their physicians for contributing to the study, to Gary Gilliland for sharing data before publication, to Guido Sauter for providing cells with monosomy 9, and to Alois Gratwohl, Jürg Schwaller, Markus Heim, and Ed Palmer for helpful comments on the manuscript.
Source Information
From the Department of Research, Experimental Hematology (R.K., S.-S.T., R.T., R.C.S.), and the Departments of Hematology (A.S.B., J.R.P.) and Laboratory Medicine (A.T.), University Hospital Basel, Basel, Switzerland; and the Division of Hematology, University of Pavia Medical School and Istituto di Ricovero e Cura a Carattere Scientifico, Policlinico San Matteo, Pavia, Italy (F.P., M.C.).
Address reprint requests to Dr. Skoda at the Department of Research, University Hospital Basel, Hebelstr. 20, CH-4031 Basel, Switzerland, or at radek.skoda@unibas.ch.
- References
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- Citing Articles (789)
Citing Articles
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Jun Xia, Mi-ze Lu, Yuan-qiang Jiang, Guo-hua Yang, Yun Zhuang, Hong-li Sun, Yun-feng Shen. (2012) JAK2 V617F, MPL W515L and JAK2 exon 12 mutations in Chinese patients with primary myelofibrosis. Chinese Journal of Cancer Research 24:1, 72-76
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Rafael Ramos da Silva, Betânia Lucena Domingues Hatzlhofer, Cíntia Gonsalves de Faria Machado, Aleide Santos de Melo Lima, Dulcinéia Martins de Albuquerque, Magnun Nueldo Nunes dos Santos, Kleber Yotsumoto Fertrin, Fernando Ferreira Costa, Aderson da Silva Araújo, Marcos Andre Cavalcanti Bezerra. (2012) JAK2 V617F Mutation Prevalence in Myeloproliferative Neoplasms in Pernambuco, Brazil. Genetic Testing and Molecular Biomarkers120203074333006
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Tomohiro Iwasaki, Hirokazu Kawai, Koushi Oseki, Tadayuki Togashi, Kazuhiko Shioji, Satoshi Yamamoto, Yoshinobu Sato, Kenji Suzuki, Ken Toba, Minoru Nomoto, Katsuyoshi Hatakeyama, Yutaka Aoyagi. (2012) Japanese case of Budd-Chiari syndrome due to hepatic vein thrombosis successfully treated with liver transplantation. Hepatology Research 42:2, 213-218
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Aiko Sato-Otsubo, Masashi Sanada, Seishi Ogawa. (2012) Single-Nucleotide Polymorphism Array Karyotyping in Clinical Practice: Where, When, and How?. Seminars in Oncology 39:1, 13-25
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Anna M. Jankowska, Hadrian Szpurka. (2012) Mutational Determinants of Epigenetic Instablity in Myeloid Malignancies. Seminars in Oncology 39:1, 80-96
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Hideki Muramatsu, Hideki Makishima, Jaroslaw P. Maciejewski. (2012) Chronic Myelomonocytic Leukemia and Atypical Chronic Myeloid Leukemia: Novel Pathogenetic Lesions. Seminars in Oncology 39:1, 67-73
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Ching-Liang Ho, Yi-Ying Wu, Hsiu-Man Hung, Ping-Ying Chang, Wei-You Kao, Yeu-Chin Chen, Tsu-Yi Chao. (2012) Rapid identification of heterozygous or homozygous JAK2V617F mutations in myeloproliferative neoplasms using melting curve analysis. Journal of the Formosan Medical Association
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Mathilde Födermayr, Otto Zach, Maria Huber, Sigrid Machherndl-Spandl, Soraya Wölfl, Hans-Christian Bösmüller, Sonja Hasenschwandtner, Sonja Burgstaller, Otto Krieger, Dieter Lutz, Ansgar Weltermann, Hanns Hauser. (2012) The clinical impact of DNA methylation frequencies of JAK2 negative regulators in patients with essential Thrombocythemia. Leukemia Research
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Giovanni Barosi, Letizia Lupo, Vittorio Rosti. (2012) Management of Myeloproliferative Neoplasms: From Academic Guidelines to Clinical Practice. Current Hematologic Malignancy Reports
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Sabine Druillennec, Coralie Dorard, Alain Eychène. (2012) Alternative Splicing in Oncogenic Kinases: From Physiological Functions to Cancer. Journal of Nucleic Acids 2012, 1-14
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Mayur Parihar, J. Ashok Kumar, Usha Sitaram, Poonkuzhali Balasubramanian, Aby Abraham, Auro Viswabandya, Biju George, Vikram Mathews, Alok Srivastava, Vivi M. Srivastava. (2012) Cytogenetic analysis of acute myeloid leukemia with t(8;21) from a tertiary care center in India with correlation between clinicopathologic characteristics and molecular analysis. Leukemia & Lymphoma 53:1, 103-109
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Francesco Passamonti, Margherita Maffioli, Domenica Caramazza. (2012) New generation small-molecule inhibitors in myeloproliferative neoplasms. Current Opinion in Hematology1
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Junko H Ohyashiki, Masayuki Yoneta, Hisashi Hisatomi, Tamiko Iwabuchi, Tomohiro Umezu, Kazuma Ohyashiki. (2012) The C allele of the JAK2 rs4495487 is an additional candidate locus that contributes to myeloproliferative neoplasm predisposition in the Japanese population. BMC Medical Genetics 13:1, 6
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Elodie Pronier, François Delhommeau. (2011) Role of TET2 Mutations in Myeloproliferative Neoplasms. Current Hematologic Malignancy Reports
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Su-Jiang Zhang, Omar Abdel-Wahab. (2011) Disordered Epigenetic Regulation in the Pathophysiology of Myeloproliferative Neoplasms. Current Hematologic Malignancy Reports
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Madappa N. Kundranda, Raoul Tibes, Ruben A. Mesa. (2011) Transformation of a Chronic Myeloproliferative Neoplasm to Acute Myelogenous Leukemia: Does Anything Work?. Current Hematologic Malignancy Reports
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F Passamonti. (2011) How to manage polycythemia vera. Leukemia
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Elisa Rumi, Ashot Harutyunyan, Chiara Elena, Daniela Pietra, Thorsten Klampfl, Klaudia Bagienski, Tiina Berg, Ilaria Casetti, Cristiana Pascutto, Francesco Passamonti, Robert Kralovics, Mario Cazzola. (2011) Identification of genomic aberrations associated with disease transformation by means of high-resolution SNP array analysis in patients with myeloproliferative neoplasm. American Journal of Hematology 86:12, 974-979
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Raoul Tibes, Ruben Mesa. (2011) JAK2 inhibitors in the treatment of myeloproliferative neoplasms: rationale and clinical data. Clinical Investigation 1:12, 1681-1693
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Soji Morishita, Norio Komatsu, Keita Kirito, Aya H. Koda, Yuji Sekiguchi, Satoshi Tsuneda, Naohiro Noda. (2011) Alternately binding probe competitive PCR as a simple, cost-effective, and accurate quantification method for JAK2V617F allele burden in myeloproliferative neoplasms. Leukemia Research 35:12, 1632-1636
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Jie Qian, Jennifer L. Mason, Beverly P. Holskin, Kristen A. Murray, Sheryl L. Meyer, Mark A. Ator, Thelma S. Angeles. (2011) Comparison of Two Homogeneous Cell-Based Kinase Assays for JAK2 V617F: SureFire ® pSTAT5 and GeneBLAzer ® Fluorescence Resonance Energy Transfer Assays. ASSAY and Drug Development Technologies111201124825001
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Vaibhav Kapuria, Alexander Levitzki, William G. Bornmann, David Maxwell, Waldemar Priebe, Roderick J. Sorenson, Hollis D. Showalter, Moshe Talpaz, Nicholas J. Donato. (2011) A novel small molecule deubiquitinase inhibitor blocks Jak2 signaling through Jak2 ubiquitination. Cellular Signalling 23:12, 2076-2085
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Y. ZHONG, J. WU, R. MA, H. CAO, Z. WANG, J. DING, L. CHENG, J. FENG, B. CHEN. (2011) Association of Janus kinase 2 (JAK2) polymorphisms with acute leukemia susceptibility. International Journal of Laboratory Hematologyno-no
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Bingfei Dong, Yang Zhang, Xueqi Fu, Guangyi Wang. (2011) Absence of JAK2V617F mutation in Chinese deep vein thrombosis patients without myeloproliferative neoplasms. Thrombosis Research
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Rebekah Baskin, Meghanath Gali, Sung O. Park, Zhizhuang Joe Zhao, György M. Keserű, Kirpal S. Bisht, Peter P. Sayeski. (2011) Identification of novel SAR properties of the Jak2 small molecule inhibitor G6: Significance of the para-hydroxyl orientation. Bioorganic & Medicinal Chemistry Letters
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N. C. P. Cross. (2011) Genetic and Epigenetic Complexity in Myeloproliferative Neoplasms. Hematology 2011:1, 208-214
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F. Cervantes. (2011) Management of Essential Thrombocythemia. Hematology 2011:1, 215-221
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W. Wu, X.-H. Sun. (2011) Janus kinase 3: the controller and the controlled. Acta Biochimica et Biophysica Sinica
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Laurie B. Schenkel, Xin Huang, Alan Cheng, Holly L. Deak, Elizabeth Doherty, Renee Emkey, Yan Gu, Hakan Gunaydin, Joseph L. Kim, Josie Lee, Robert Loberg, Philip Olivieri, Jeanne Pistillo, Jin Tang, Qian Wan, Hui-Ling Wang, Shen-Wu Wang, Mary C. Wells, Bin Wu, Violeta Yu, Liqin Liu, Stephanie Geuns-Meyer. (2011) Discovery of Potent and Highly Selective Thienopyridine Janus Kinase 2 Inhibitors. Journal of Medicinal Chemistry111116112723000
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P. Guglielmelli, F. Biamonte, J. Score, C. Hidalgo-Curtis, F. Cervantes, M. Maffioli, T. Fanelli, T. Ernst, N. Winkelman, A. V. Jones, K. Zoi, A. Reiter, A. Duncombe, L. Villani, A. Bosi, G. Barosi, N. C. P. Cross, A. M. Vannucchi. (2011) EZH2 mutational status predicts poor survival in myelofibrosis. Blood 118:19, 5227-5234
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David Mitchell, Kevin P. Cole, Patrick M. Pollock, David M. Coppert, Timothy P. Burkholder, Joshua R. Clayton. (2011) Development and a Practical Synthesis of the JAK2 Inhibitor LY2784544. Organic Process Research & Development111109092804006
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Marshall J. Orloff, Jon I. Isenberg, Henry O. Wheeler, Pat O. Daily, Barbara Girard. (2011) Budd–Chiari Syndrome Revisited: 38 Years’ Experience with Surgical Portal Decompression. Journal of Gastrointestinal Surgery
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E.-F. Gautier, M. Picard, C. Laurent, C. Marty, J.-L. Villeval, C. Demur, F. Delhommeau, E. Hexner, S. Giraudier, N. Bonnevialle, B. Ducommun, C. Recher, G. Laurent, S. Manenti, V. Mansat-De Mas. (2011) The cell cycle regulator CDC25A is a target for JAK2V617F oncogene. Blood
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John Anastasi. (2011) The myeloproliferative neoplasms including the eosinophilia-related myeloproliferations associated with tyrosine kinase mutations: changes and issues in classification and diagnosis criteria. Seminars in Diagnostic Pathology 28:4, 304-313
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A Harutyunyan, B Gisslinger, T Klampfl, T Berg, K Bagienski, H Gisslinger, R Kralovics. (2011) Rare germline variants in regions of loss of heterozygosity may influence clinical course of hematological malignancies. Leukemia 25:11, 1782-1784
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Jungwon Huh, Chul Won Jung, Jong Won Kim, Hee-Jin Kim, Sun-Hee Kim, Myung Geun Shin, Yeo Kyeoung Kim, Hyeoung Joon Kim, Jang Soo Suh, Joon Ho Moon, Sang Kyung Sohn, Goong Hyun Nam, Jong-eun Lee, Dong Hwan Dennis Kim. (2011) Genome-wide high density single-nucleotide polymorphism array-based karyotyping improves detection of clonal aberrations including der(9) deletion, but does not predict treatment outcomes after imatinib therapy in chronic myeloid leukemia. Annals of Hematology 90:11, 1255-1264
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Brady L. Stein, John D. Crispino, Alison R. Moliterno. (2011) Janus kinase inhibitors. Current Opinion in Oncology1
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Cristina Royo, Itziar Salaverria, Elena M. Hartmann, Andreas Rosenwald, Elías Campo, Sílvia Beà. (2011) The complex landscape of genetic alterations in mantle cell lymphoma. Seminars in Cancer Biology 21:5, 322-334
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Andreas Kreft, Thomas Kindler, Erik Springer, Charles James Kirkpatrick. (2011) JAK2-V617F-mutated myeloproliferative neoplasms reveal different allele burden within hematopoietic cell lineages: a microdissection study of bone marrow trephine biopsies. Virchows Archiv 459:5, 521-527
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J. HOEKSTRA, E. L. BRESSER, J. H. SMALBERG, M. C. W. SPAANDER, F. W. G. LEEBEEK, H. L. A. JANSSEN. (2011) Long-term follow-up of patients with portal vein thrombosis and myeloproliferative neoplasms. Journal of Thrombosis and Haemostasis 9:11, 2208-2214
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János László Iványi, Éva Marton, Márk Plander. (2011) A JAK2<sup>V617F</sup>-mutáció jelentősége krónikus myeloproliferativ neoplasiás betegeinkben. Orvosi Hetilap 152:45, 1795-1803
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Ihab El-Hemaidi, Susan E. Robinson. (2011) Management of haematological malignancy in pregnancy. Best Practice & Research Clinical Obstetrics & Gynaecology
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Jongwon Lim, Brandon Taoka, Ryan D. Otte, Kerrie Spencer, Christopher J. Dinsmore, Michael D. Altman, Grace Chan, Craig Rosenstein, Sujata Sharma, Hua-Poo Su, Alexander A. Szewczak, Lin Xu, Hong Yin, Joan Zugay-Murphy, C. Gary Marshall, Jonathan R. Young. (2011) Discovery of 1-Amino-5 H -pyrido[4,3- b ]indol-4-carboxamide Inhibitors of Janus Kinase 2 (JAK2) for the Treatment of Myeloproliferative Disorders. Journal of Medicinal Chemistry 54:20, 7334-7349
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G Wernig, M G Kharas, A Mullally, D S Leeman, R Okabe, T George, D O Clary, D G Gilliland. (2011) EXEL-8232, a small-molecule JAK2 inhibitor, effectively treats thrombocytosis and extramedullary hematopoiesis in a murine model of myeloproliferative neoplasm induced by MPLW515L. Leukemia
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N. E. Elliott, S. M. Cleveland, V. Grann, J. Janik, T. A. Waldmann, U. P. Dave. (2011) FERM domain mutations induce gain of function in JAK3 in adult T-cell leukemia/lymphoma. Blood 118:14, 3911-3921
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Alfonso Quintás-Cardama, Taghi Manshouri, Zeev Estrov, David Harris, Ying Zhang, Amos Gaikwad, Hagop M. Kantarjian, Srdan Verstovsek. (2011) Preclinical characterization of atiprimod, a novel JAK2 AND JAK3 inhibitor. Investigational New Drugs 29:5, 818-826
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Marie-Cécile Valera, Olivier Parant, Christophe Vayssiere, Jean-François Arnal, Bernard Payrastre. (2011) Essential thrombocythemia and pregnancy. European Journal of Obstetrics & Gynecology and Reproductive Biology 158:2, 141-147
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Paulo Lisboa Bittencourt, Cláudia Alves Couto, Daniel Dias Ribeiro. (2011) Portal Vein Thrombosis and Budd–Chiari Syndrome. Hematology/Oncology Clinics of North America 25:5, 1049-1066
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Qiang Wen, Benjamin Goldenson, John D. Crispino. (2011) Normal and malignant megakaryopoiesis. Expert Reviews in Molecular Medicine 13,
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F Cervantes. (2011) How I treat splenomegaly in myelofibrosis. Blood Cancer Journal 1:10, e37
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Anurima Majumder, Andrew T. Magis, Sung O. Park, Nicholas C. Figueroa, Rebekah Baskin, Annet Kirabo, Robert W. Allan, Zhizhuang Joe Zhao, Kirpal S. Bisht, György M. Keserű, Peter P. Sayeski. (2011) A46, a benzothiophene-derived compound, suppresses Jak 2-mediated pathologic cell growth. Experimental Hematology
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Anurima Majumder, Annet Kirabo, Kanchana Karrupiah, Shigeharu Tsuda, Jennifer Caldwell-Busby, Arturo J. Cardounel, György M. Keserű, Peter P. Sayeski. (2011) Cell Death Induced by the Jak2 Inhibitor, G6, Correlates with Cleavage of Vimentin Filaments. Biochemistry 50:36, 7774-7786
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Annette Leon, John F. Staropoli, Jesus M. Hernandez, Janina A. Longtine, Frank C. Kuo, Paola Dal Cin. (2011) Translocation t(1;9) is a recurrent cytogenetic abnormality associated with progression of essential thrombocythemia patients displaying the JAK2 V617F mutation. Leukemia Research 35:9, 1188-1192
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Cornelis J.J. Huijsmans, Jeroen Poodt, Paul H.M. Savelkoul, Mirjam H.A. Hermans. (2011) Sensitive Detection and Quantification of the JAK2V617F Allele by Real-Time PCR. The Journal of Molecular Diagnostics 13:5, 558-564
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Alen Ostojic, Radovan Vrhovac, Srdan Verstovsek. (2011) Ruxolitinib: a new JAK1/2 inhibitor that offers promising options for treatment of myelofibrosis. Future Oncology 7:9, 1035-1043
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Qifang Zhang, Jamie L. Sturgill, Maciej Kmieciak, Karol Szczepanek, Marta Derecka, Catherine Koebel, Laura J. Graham, Yun Dai, Shuang Chen, Steven Grant, Joanna Cichy, Kazuya Shimoda, Ana Gamero, Masoud Manjili, Harry Bear, Daniel Conrad, Andrew C. Larner. (2011) The Role of Tyk2 in Regulation of Breast Cancer Growth. Journal of Interferon & Cytokine Research 31:9, 671-677
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Kh. Dhanachandra Singh, Muthusamy Karthikeyan, Palani Kirubakaran, Selvaraman Nagamani. (2011) Pharmacophore filtering and 3D-QSAR in the discovery of new JAK2 inhibitors. Journal of Molecular Graphics and Modelling 30, 186-197
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C. H. Riley, M. K. Jensen, M. K. Brimnes, H. C. Hasselbalch, O. W. Bjerrum, P. t. Straten, I. M. Svane. (2011) Increase in circulating CD4+CD25+Foxp3+ T cells in patients with Philadelphia-negative chronic myeloproliferative neoplasms during treatment with IFN- . Blood 118:8, 2170-2173
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W. Vainchenker, F. Delhommeau, S. N. Constantinescu, O. A. Bernard. (2011) New mutations and pathogenesis of myeloproliferative neoplasms. Blood 118:7, 1723-1735
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Daniela Ungureanu, Jinhua Wu, Tuija Pekkala, Yashavanthi Niranjan, Clifford Young, Ole N Jensen, Chong-Feng Xu, Thomas A Neubert, Radek C Skoda, Stevan R Hubbard, Olli Silvennoinen. (2011) The pseudokinase domain of JAK2 is a dual-specificity protein kinase that negatively regulates cytokine signaling. Nature Structural & Molecular Biology 18:9, 971-976
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H Jäkel, C Weinl, L Hengst. (2011) Phosphorylation of p27Kip1 by JAK2 directly links cytokine receptor signaling to cell cycle control. Oncogene 30:32, 3502-3512
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S. Anand, F. Stedham, E. Gudgin, P. Campbell, P. Beer, A. R. Green, B. J. P. Huntly. (2011) Increased basal intracellular signaling patterns do not correlate with JAK2 genotype in human myeloproliferative neoplasms. Blood 118:6, 1610-1621
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Alexandra Iliadi, Margarita Petropoulou, Penelope C. Ioannou, Theodore K. Christopoulos, Nikolaos I. Anagnostopoulos, Emmanuel Kanavakis, Jan Traeger-Synodinos. (2011) Absolute Quantification of the Alleles in Somatic Point Mutations by Bioluminometric Methods based on Competitive Polymerase Chain Reaction in the Presence of a Locked Nucleic Acid Blocker or an Allele-Specific Primer. Analytical Chemistry110809102303042
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A. Benmoussa, H. Dehbi, S. Fehri, A. Quessar, S. Nadifi. (2011) JAK2-V617F mutation in Moroccan patients with myeloproliferative disorders: Contribution, diagnosis and therapeutic prospects. Pathologie Biologie 59:4, e89-e92
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Catherine L. Carmichael, Warren S. Alexander. (2011) Mouse models of diseases of megakaryocyte and platelet homeostasis. Mammalian Genome 22:7-8, 449-465
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Linda M. Scott. (2011) The JAK2 exon 12 mutations: A comprehensive review. American Journal of Hematology 86:8, 668-676
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John Mascarenhas, Nitin Roper, Pratima Chaurasia, Ronald Hoffman. (2011) Epigenetic abnormalities in myeloproliferative neoplasms: a target for novel therapeutic strategies. Clinical Epigenetics 2:2, 197-212
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Kiran Naqvi, Srdan Verstovsek, Hagop Kantarjian, Farhad Ravandi. (2011) A potential role of ruxolitinib in leukemia. Expert Opinion on Investigational Drugs 20:8, 1159-1166
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C. Maktouf, A. Bounemra, S. Mahjoub, F. Msadek, A. Khlif, M. Karoui, S. Hdiji, S. Zriba, N. Ben Romdhane, M. Elloumi. (2011) Evaluation of serum VEGF levels in untreated erythrocytosis patients. Pathologie Biologie 59:4, 240-242
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K A Monaghan, T Khong, C J Burns, A Spencer. (2011) The novel JAK inhibitor CYT387 suppresses multiple signalling pathways, prevents proliferation and induces apoptosis in phenotypically diverse myeloma cells. Leukemia
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M Nakatake, B Monte-Mor, N Debili, N Casadevall, V Ribrag, E Solary, W Vainchenker, I Plo. (2011) JAK2V617F negatively regulates p53 stabilization by enhancing MDM2 via La expression in myeloproliferative neoplasms. Oncogene
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S. Anand, F. Stedham, P. Beer, E. Gudgin, C. A. Ortmann, A. Bench, W. Erber, A. R. Green, B. J. P. Huntly. (2011) Effects of the JAK2 mutation on the hematopoietic stem and progenitor compartment in human myeloproliferative neoplasms. Blood 118:1, 177-181
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T. Klampfl, A. Harutyunyan, T. Berg, B. Gisslinger, M. Schalling, K. Bagienski, D. Olcaydu, F. Passamonti, E. Rumi, D. Pietra, R. Jager, L. Pieri, P. Guglielmelli, I. Iacobucci, G. Martinelli, M. Cazzola, A. M. Vannucchi, H. Gisslinger, R. Kralovics. (2011) Genome integrity of myeloproliferative neoplasms in chronic phase and during disease progression. Blood 118:1, 167-176
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Y. Zheng, H. Qin, S. J. Frank, L. Deng, D. W. Litchfield, A. Tefferi, A. Pardanani, F.-T. Lin, J. Li, B. Sha, E. N. Benveniste. (2011) A CK2-dependent mechanism for activation of the JAK-STAT signaling pathway. Blood 118:1, 156-166
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Vibe Skov, Thomas Stauffer Larsen, Mads Thomassen, Caroline Hasselbalch Riley, Morten K. Jensen, Ole Weis Bjerrum, Torben A. Kruse, Hans Carl Hasselbalch. (2011) Whole-blood transcriptional profiling of interferon-inducible genes identifies highly upregulated IFI27 in primary myelofibrosis. European Journal of Haematology 87:1, 54-60
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Alfonso Quintás-Cardama, Srdan Verstovsek. (2011) New JAK2 inhibitors for myeloproliferative neoplasms. Expert Opinion on Investigational Drugs 20:7, 961-972
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Katayoon Kasaian, Steven JM Jones. (2011) A new frontier in personalized cancer therapy: mapping molecular changes. Future Oncology 7:7, 873-894
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Raoul Tibes, Ruben A. Mesa. (2011) Myeloproliferative neoplasms 5 years after discovery of JAK2V617F: what is the impact of JAK2 inhibitor therapy?. Leukemia & Lymphoma 52:7, 1178-1187
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Olivier Rager, Marie Parrens, Josette Brière, Éric Lippert, Noël Milpied, Jean-Luc Pellegrin, Jean-François Viallard. (2011) Intérêt de la biopsie ostéomédullaire dans la thrombocytémie essentielle. La Presse Médicale
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K. Shide, T. Kameda, V. Markovtsov, H. K. Shimoda, E. Tonkin, S. Fang, C. Liu, M. Gelman, W. Lang, J. Romero, J. McLaughlin, S. Bhamidipati, J. Clough, C. Low, A. Reitsma, S. Siu, P. Pine, G. Park, A. Torneros, M. Duan, R. Singh, D. G. Payan, T. Matsunaga, Y. Hitoshi, K. Shimoda. (2011) R723, a selective JAK2 inhibitor, effectively treats JAK2V617F-induced murine myeloproliferative neoplasm. Blood 117:25, 6866-6875
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Ryan C Russell, Roxana I Sufan, Bing Zhou, Pardeep Heir, Severa Bunda, Stephanie S Sybingco, Samantha N Greer, Olga Roche, Samuel A Heathcote, Vinca W K Chow, Lukasz M Boba, Terri D Richmond, Michele M Hickey, Dwayne L Barber, David A Cheresh, M Celeste Simon, Meredith S Irwin, William Y Kim, Michael Ohh. (2011) Loss of JAK2 regulation via a heterodimeric VHL-SOCS1 E3 ubiquitin ligase underlies Chuvash polycythemia. Nature Medicine 17:7, 845-853
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