Notch signaling mediates G1/S cell-cycle progression in T cells via cyclin D3 and its dependent kinases

Blood. 2009 Feb 19;113(8):1689-98. doi: 10.1182/blood-2008-03-147967. Epub 2008 Nov 10.

Abstract

Notch signaling plays a role in normal lymphocyte development and function. Activating Notch1-mutations, leading to aberrant downstream signaling, have been identified in human T-cell acute lymphoblastic leukemia (T-ALL). While this highlights the contribution of Notch signaling to T-ALL pathogenesis, the mechanisms by which Notch regulates proliferation and survival in normal and leukemic T cells are not fully understood. Our findings identify a role for Notch signaling in G(1)-S progression of cell cycle in T cells. Here we show that expression of the G(1) proteins, cyclin D3, CDK4, and CDK6, is Notch-dependent both in vitro and in vivo, and we outline a possible mechanism for the regulated expression of cyclin D3 in activated T cells via CSL (CBF-1, mammals; suppressor of hairless, Drosophila melanogaster; Lag-1, Caenorhabditis elegans), as well as a noncanonical Notch signaling pathway. While cyclin D3 expression contributes to cell-cycle progression in Notch-dependent human T-ALL cell lines, ectopic expression of CDK4 or CDK6 together with cyclin D3 shows partial rescue from gamma-secretase inhibitor (GSI)-induced G(1) arrest in these cell lines. Importantly, cyclin D3 and CDK4 are highly overexpressed in Notch-dependent T-cell lymphomas, justifying the combined use of cell-cycle inhibitors and GSI in treating human T-cell malignancies.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes / enzymology*
  • CD4-Positive T-Lymphocytes / pathology
  • Cell Line, Tumor
  • Cyclin D3
  • Cyclin-Dependent Kinase 4 / genetics
  • Cyclin-Dependent Kinase 4 / metabolism*
  • Cyclin-Dependent Kinase 6 / genetics
  • Cyclin-Dependent Kinase 6 / metabolism*
  • Cyclins / metabolism*
  • G1 Phase / physiology
  • Gene Expression Regulation, Leukemic
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Lymphoma, T-Cell / enzymology
  • Lymphoma, T-Cell / pathology
  • Mice
  • Mice, Inbred C57BL
  • NF-kappa B / metabolism
  • Phosphorylation / physiology
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / enzymology*
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / pathology
  • Promoter Regions, Genetic / physiology
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism
  • Receptor, Notch1 / genetics
  • Receptor, Notch1 / metabolism*
  • Receptor, Notch2 / genetics
  • Receptor, Notch2 / metabolism
  • Receptor, Notch3
  • Receptor, Notch4
  • Receptors, Notch / genetics
  • Receptors, Notch / metabolism
  • Retinoblastoma Protein / metabolism
  • S Phase / physiology
  • Signal Transduction / physiology

Substances

  • CCND3 protein, human
  • Ccnd3 protein, mouse
  • Cyclin D3
  • Cyclins
  • NF-kappa B
  • Notch1 protein, mouse
  • Notch2 protein, mouse
  • Notch3 protein, mouse
  • Proto-Oncogene Proteins
  • Receptor, Notch1
  • Receptor, Notch2
  • Receptor, Notch3
  • Receptor, Notch4
  • Receptors, Notch
  • Retinoblastoma Protein
  • Notch4 protein, mouse
  • Cdk4 protein, mouse
  • Cdk6 protein, mouse
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinase 6