Maffei Rossana, Paolini Ambra, Conte Benedetta, Riva Giovanni, Nasillo Vincenzo, Cretì Federica, Martinelli Silvia, Giacobbi Francesca, Corradini Giorgia, Pilato Flora, Bernabei Daniela, Lancellotti Cesare, Debbia Giulia, Morselli Monica, Potenza Leonardo, Giusti Davide, Colaci Elisabetta, Bettelli Francesca, Bresciani Paola, Cuoghi Angela, Gilioli Andrea, Messerotti Andrea, Pioli Valeria, Maccaferri Monica, Leonardi Giovanna, Manfredini Rossella, Marasca Roberto, Eccher Albino, Luppi Mario, Forghieri Fabio, Candoni Anna, Tagliafico Enrico
Department of Laboratory Medicine and Pathology, Diagnostic Hematology and Clinical Genomics, Azienda Ospedaliero-Universitaria, Policlinico, and AUSL Modena, Italy.
Hematology Unit, Department of Medical and Surgical Sciences, University of Modena and Reggio Emilia, Azienda Ospedaliero-Universitaria, Policlinico, Modena, Italy.
Ann Hematol. 2025 Jan;104(1):263-274. doi: 10.1007/s00277-025-06232-1. Epub 2025 Feb 5.
The colony-stimulating factor 3 receptor (CSF3R) plays an essential role in differentiation, growth, and survival of granulocytes. Driver mutations in CSF3R gene represent a diagnostic marker of chronic neutrophilic leukemia (CNL). Less commonly, these mutations are observed in other myeloid neoplasms but their pathogenetic and prognostic role is still unclear. Here, we analyzed a large cohort of myeloid neoplasms to evaluate the incidence of CSF3R mutations and co-mutational profile. Mutational analysis was performed using targeted NGS myeloid panel in a consecutive cohort of 360 patients with myeloid neoplasms. Mutations in CSF3R were identified in 20/360 (5.6%) cases. A CSF3R gene mutation was present in 13/179 AML cases (7.3%), in 2/27 (7.4%) CMML cases, in 1/94 (1.1%) MDS cases and in 4/60 (6.7%) other myeloid neoplasms. The frequencies of patients with CSF3R mutations lowered to 2.8% in all cases and 3.4% in AML, excluding cases with variants of uncertain significance (VUS). A total of 23 mutations of CSF3R gene were detected, half localized in the extracellular domain, 5 in the transmembrane region (type I) and 6 mutations in the cytoplasmic domain (type II). In AML, CSF3R mutations were more frequent in patients harboring CBF alterations (25.0%) and CEBPA mutations (11.8%). Two cases with AML harboring pathogenic CSF3R variants were primary refractory to induction therapy. CMML cases with T618I variant showed a myeloproliferative phenotype. Overall, our findings support the notion that CSF3R variants, particularly type I and II pathogenic mutations, may modulate the phenotypic features of leukemic cells in myeloid neoplasia.
集落刺激因子3受体(CSF3R)在粒细胞的分化、生长和存活中起重要作用。CSF3R基因的驱动突变是慢性嗜中性粒细胞白血病(CNL)的诊断标志物。较少见的是,这些突变也见于其他髓系肿瘤,但其致病和预后作用仍不清楚。在此,我们分析了一大组髓系肿瘤患者,以评估CSF3R突变的发生率和共突变情况。对360例连续的髓系肿瘤患者,使用靶向二代测序髓系检测板进行突变分析。在360例患者中有20例(5.6%)检测到CSF3R突变。179例急性髓系白血病(AML)中有13例(7.3%)存在CSF3R基因突变,27例慢性粒单核细胞白血病(CMML)中有2例(7.4%),94例骨髓增生异常综合征(MDS)中有1例(1.1%),60例其他髓系肿瘤中有4例(6.7%)。排除意义未明变异(VUS)病例后,所有病例中CSF3R突变患者的频率降至2.8%,AML中为3.4%。共检测到23个CSF3R基因突变,其中一半位于细胞外结构域,5个位于跨膜区(I型),6个位于胞质结构域(II型)。在AML中,伴有CBF改变(25.0%)和CEBPA突变(11.8%)的患者中CSF3R突变更常见。2例携带致病性CSF3R变异的AML患者对诱导治疗原发耐药。携带T618I变异的CMML病例表现出骨髓增殖表型。总体而言,我们的研究结果支持以下观点,即CSF3R变异,特别是I型和II型致病突变,可能会调节髓系肿瘤中白血病细胞的表型特征。