ROR1 can interact with TCL1 and enhance leukemogenesis in Eμ-TCL1 transgenic mice

Proc Natl Acad Sci U S A. 2014 Jan 14;111(2):793-8. doi: 10.1073/pnas.1308374111. Epub 2013 Dec 30.

Abstract

Receptor tyrosine kinase-like orphan receptor 1 (ROR1) is an oncoembryonic antigen found on chronic lymphocytic leukemia (CLL) B cells, but not on normal adult tissues. We generated transgenic (Tg) mice with human ROR1 regulated by the murine Ig promoter/enhancer. In contrast to nontransgenic littermates, such animals had B-cell-restricted expression of ROR1 and could develop clonal expansions of ROR1(bright)CD5(+)B220(low) B cells resembling human CLL at ≥ 15 mo of age. Because immune-precipitation and mass spectrometry studies revealed that ROR1 could complex with T-cell leukemia 1 (TCL1) in CLL, we crossed these animals with Eµ-TCL1-Tg (TCL1) mice. Progeny with both transgenes (ROR1 × TCL1) developed CD5(+)B220(low) B-cell lymphocytosis and leukemia at a significantly younger median age than did littermates with either transgene alone. ROR1 × TCL1 leukemia B cells had higher levels of phospho-AKT than TCL1 leukemia cells and expressed high levels of human ROR1, which we also found complexed with TCL1. Transcriptome analyses revealed that ROR1 × TCL1 leukemia cells had higher expression of subnetworks implicated in embryonic and tumor-cell proliferation, but lower expression of subnetworks involved in cell-cell adhesion or cell death than did TCL1 leukemia cells. ROR1 × TCL1 leukemia cells also had higher proportions of Ki-67-positive cells, lower proportions of cells undergoing spontaneous apoptosis, and produced more aggressive disease upon adoptive transfer than TCL1 leukemia cells. However, treatment with an anti-ROR1 mAb resulted in ROR1 down-modulation, reduced phospho-AKT, and impaired engraftment of ROR1 × TCL1 leukemia cells. Our data demonstrate that ROR1 accelerates development/progression of leukemia and may be targeted for therapy of patients with CLL.

Keywords: AKT; immune therapy; monoclonal antibody; mouse model.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Age Factors
  • Animals
  • Antibodies, Monoclonal / pharmacology
  • Apoptosis / physiology
  • B-Lymphocytes / metabolism
  • Carcinogenesis / metabolism*
  • Cell Adhesion / physiology
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Leukemia, Lymphocytic, Chronic, B-Cell / genetics
  • Leukemia, Lymphocytic, Chronic, B-Cell / metabolism*
  • Mice
  • Mice, Transgenic
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism*
  • Proto-Oncogene Proteins c-akt / metabolism
  • Receptor Tyrosine Kinase-like Orphan Receptors / immunology
  • Receptor Tyrosine Kinase-like Orphan Receptors / metabolism*

Substances

  • Antibodies, Monoclonal
  • Proto-Oncogene Proteins
  • Tcl1 protein, mouse
  • ROR1 protein, human
  • Receptor Tyrosine Kinase-like Orphan Receptors
  • Proto-Oncogene Proteins c-akt

Associated data

  • GEO/GSE51420