Differential PAX5 levels promote malignant B-cell infiltration, progression and drug resistance, and predict a poor prognosis in MCL patients independent of CCND1

Leukemia. 2016 Mar;30(3):580-93. doi: 10.1038/leu.2015.140. Epub 2015 May 15.

Abstract

Reduced Paired box 5 (PAX5) levels have important roles in the pathogenesis of human B-cell acute lymphoblastic leukemia. However, the role of PAX5 in human lymphoma remains unclear. We generated PAX5-silenced cells using mantle cell lymphoma (MCL) as a model system. These PAX5(-) MCL cells exhibited unexpected phenotypes, including increased proliferation in vitro, enhanced tumor infiltration in vivo, robust adhesion to the bone marrow stromal cells and increased retention of quiescent stem-like cells. These phenotypes were attributed to alterations in the expression of genes including p53 and Rb, and to phosphoinositide 3-kinase/mammalian target of rapamycin and phosphorylated signal transducer and activator of transcription 3 pathway hyperactivation. On PAX5 silencing, the MCL cells displayed upregulated interleukin (IL)-6 expression and increased responses to paracrine IL-6. Moreover, decreased PAX5 levels in CD19+ MCL cells correlated with their increased infiltration and progression; thus, PAX5 levels can be used as a prognostic marker independent of cyclin D1 in advanced MCL patients. Importantly, high-throughput screening of 3800 chemical compounds revealed that PAX5(-) MCL cells are highly drug-resistant compared with PAX5 wild-type MCL cells. Collectively, the results of our study support a paradigm shift regarding the functions of PAX5 in human B-cell cancer and encourage future efforts to design effective therapies against MCL.

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • B-Lymphocytes / metabolism*
  • B-Lymphocytes / pathology
  • Cell Adhesion
  • Cell Line, Tumor
  • Cell Movement
  • Cell Proliferation
  • Cyclin D1 / genetics
  • Cyclin D1 / metabolism
  • Drug Resistance, Neoplasm / genetics*
  • Gene Expression Regulation, Neoplastic*
  • High-Throughput Screening Assays
  • Humans
  • Interleukin-6 / genetics
  • Interleukin-6 / metabolism
  • Lymphoma, Mantle-Cell / diagnosis
  • Lymphoma, Mantle-Cell / drug therapy
  • Lymphoma, Mantle-Cell / genetics*
  • Lymphoma, Mantle-Cell / mortality
  • Mesenchymal Stem Cells / metabolism
  • Mesenchymal Stem Cells / pathology
  • Mice
  • PAX5 Transcription Factor / antagonists & inhibitors
  • PAX5 Transcription Factor / genetics*
  • PAX5 Transcription Factor / metabolism
  • Phosphatidylinositol 3-Kinases / genetics
  • Phosphatidylinositol 3-Kinases / metabolism
  • Prognosis
  • Retinoblastoma Protein / genetics
  • Retinoblastoma Protein / metabolism
  • STAT3 Transcription Factor / genetics
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction
  • TOR Serine-Threonine Kinases / genetics
  • TOR Serine-Threonine Kinases / metabolism
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents
  • CCND1 protein, human
  • IL6 protein, human
  • Interleukin-6
  • PAX5 Transcription Factor
  • PAX5 protein, human
  • Retinoblastoma Protein
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Tumor Suppressor Protein p53
  • Cyclin D1
  • MTOR protein, human
  • TOR Serine-Threonine Kinases