Abstract
T-cell acute lymphoblastic leukaemia (T-ALL) is a blood malignancy afflicting mainly children and adolescents. T-ALL patients present at diagnosis with increased white cell counts and hepatosplenomegaly, and are at an increased risk of central nervous system (CNS) relapse. For that reason, T-ALL patients usually receive cranial irradiation in addition to intensified intrathecal chemotherapy. The marked increase in survival is thought to be worth the considerable side-effects associated with this therapy. Such complications include secondary tumours, neurocognitive deficits, endocrine disorders and growth impairment. Little is known about the mechanism of leukaemic cell infiltration of the CNS, despite its clinical importance. Here we show, using T-ALL animal modelling and gene-expression profiling, that the chemokine receptor CCR7 (ref. 5) is the essential adhesion signal required for the targeting of leukaemic T-cells into the CNS. Ccr7 gene expression is controlled by the activity of the T-ALL oncogene Notch1 and is expressed in human tumours carrying Notch1-activating mutations. Silencing of either CCR7 or its chemokine ligand CCL19 (ref. 6) in an animal model of T-ALL specifically inhibits CNS infiltration. Furthermore, murine CNS-targeting by human T-ALL cells depends on their ability to express CCR7. These studies identify a single chemokine-receptor interaction as a CNS 'entry' signal, and open the way for future pharmacological targeting. Targeted inhibition of CNS involvement in T-ALL could potentially decrease the intensity of CNS-targeted therapy, thus reducing its associated short- and long-term complications.
MeSH Terms
Animals
Cell Adhesion
Cell Line, Tumor
Central Nervous System/metabolism,pathology
Chemokine CCL19/deficiency,metabolism
Chemokine CCL21/metabolism
Humans
Leukemia, T-Cell/metabolism,pathology
Mice
Mice, Inbred C57BL
Precursor T-Cell Lymphoblastic Leukemia-Lymphoma/metabolism,pathology
Receptor, Notch1/genetics,metabolism
Receptors, CCR7/deficiency,metabolism
Signal Transduction
Chemicals
CCR7 protein, human
Ccl19 protein, mouse
Ccr7 protein, mouse
Chemokine CCL19
Chemokine CCL21
Receptor, Notch1
Receptors, CCR7
Authors & Affiliations
22 authors, click to expand affiliations / ORCID
Buonamici Silvia
Department of Pathology and New York University Cancer Institute, New York 10016, USA.
Trimarchi Thomas
Ruocco Maria Grazia
Reavie Linsey
Cathelin Severine
Mar Brenton G
Klinakis Apostolos
Lukyanov Yevgeniy
Tseng Jen-Chieh
Sen Filiz
Gehrie Eric
Li Mengling
Newcomb Elizabeth
Zavadil Jiri
Meruelo Daniel
Lipp Martin
Ibrahim Sherif
Efstratiadis Argiris
Zagzag David
Bromberg Jonathan S
Dustin Michael L
Aifantis Iannis
References (29)
29 references, click to expand
-
In vivo imaging of leukocyte trafficking in blood vessels and tissues.
Curr Opin Immunol. 2004 Aug;16(4):406-17
PMID: 15245733
-
Chemokines in and out of the central nervous system: much more than chemotaxis and inflammation.
J Leukoc Biol. 2008 Sep;84(3):587-94
PMID: 18467654
-
Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia.
Science. 2004 Oct 8;306(5694):269-71
PMID: 15472075
-
CCR7 and its ligands: balancing immunity and tolerance.
Nat Rev Immunol. 2008 May;8(5):362-71
PMID: 18379575
-
The SCFFBW7 ubiquitin ligase complex as a tumor suppressor in T cell leukemia.
J Exp Med. 2007 Aug 6;204(8):1825-35
PMID: 17646408
-
Notch 1 activation in the molecular pathogenesis of T-cell acute lymphoblastic leukaemia.
Nat Rev Cancer. 2006 May;6(5):347-59
PMID: 16612405
-
Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs.
Annu Rev Immunol. 2005;23:127-59
PMID: 15771568
-
Stable T cell-dendritic cell interactions precede the development of both tolerance and immunity in vivo.
Nat Immunol. 2005 Jul;6(7):707-14
PMID: 15924144
-
Tumor-specific in vivo transfection with HSV-1 thymidine kinase gene using a Sindbis viral vector as a basis for prodrug ganciclovir activation and PET.
J Nucl Med. 2006 Jul;47(7):1136-43
PMID: 16818948
-
Expression of CCR7 in multiple sclerosis: implications for CNS immunity.
Ann Neurol. 2004 May;55(5):627-38
PMID: 15122702
-
A stable human-derived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes.
Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11400-6
PMID: 8876147
-
T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases.
Nature. 2004 Jan 8;427(6970):154-9
PMID: 14712275
-
Current management and challenges of malignant disease in the CNS in paediatric leukaemia.
Lancet Oncol. 2008 Mar;9(3):257-68
PMID: 18308251
-
CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs.
Cell. 1999 Oct 1;99(1):23-33
PMID: 10520991
-
FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to gamma-secretase inhibitors.
J Exp Med. 2007 Aug 6;204(8):1813-24
PMID: 17646409
-
A multistep adhesion cascade for lymphoid progenitor cell homing to the thymus.
Proc Natl Acad Sci U S A. 2006 May 2;103(18):7006-11
PMID: 16641096
-
Natalizumab for multiple sclerosis.
N Engl J Med. 2007 Jun 21;356(25):2622-9
PMID: 17582072
-
Requirement for cyclin D3 in lymphocyte development and T cell leukemias.
Cancer Cell. 2003 Dec;4(6):451-61
PMID: 14706337
-
Human cerebrospinal fluid central memory CD4+ T cells: evidence for trafficking through choroid plexus and meninges via P-selectin.
Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8389-94
PMID: 12829791
-
Treatment of acute lymphoblastic leukemia.
N Engl J Med. 2006 Jan 12;354(2):166-78
PMID: 16407512
-
Autologous chemotaxis as a mechanism of tumor cell homing to lymphatics via interstitial flow and autocrine CCR7 signaling.
Cancer Cell. 2007 Jun;11(6):526-38
PMID: 17560334
-
Targeting the NF-kappaB signaling pathway in Notch1-induced T-cell leukemia.
Nat Med. 2007 Jan;13(1):70-7
PMID: 17173050
-
Phenotypic and functional analysis of T cells homing into the CSF of subjects with inflammatory diseases of the CNS.
J Leukoc Biol. 2003 May;73(5):584-90
PMID: 12714572
-
Igf1r as a therapeutic target in a mouse model of basal-like breast cancer.
Proc Natl Acad Sci U S A. 2009 Feb 17;106(7):2359-64
PMID: 19174523
-
Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization.
J Exp Med. 1999 Feb 1;189(3):451-60
PMID: 9927507
-
The many roles of chemokines and chemokine receptors in inflammation.
N Engl J Med. 2006 Feb 9;354(6):610-21
PMID: 16467548
-
Mutational loss of PTEN induces resistance to NOTCH1 inhibition in T-cell leukemia.
Nat Med. 2007 Oct;13(10):1203-10
PMID: 17873882
-
Molecular pathogenesis of T-cell leukaemia and lymphoma.
Nat Rev Immunol. 2008 May;8(5):380-90
PMID: 18421304
-
Involvement of chemokine receptors in breast cancer metastasis.
Nature. 2001 Mar 1;410(6824):50-6
PMID: 11242036