Abstract
Tumour-initiating cells capable of self-renewal and differentiation, which are responsible for tumour growth, have been identified in human haematological malignancies and solid cancers. If such minority populations are associated with tumour progression in human patients, specific targeting of tumour-initiating cells could be a strategy to eradicate cancers currently resistant to systemic therapy. Here we identify a subpopulation enriched for human malignant-melanoma-initiating cells (MMIC) defined by expression of the chemoresistance mediator ABCB5 (refs 7, 8) and show that specific targeting of this tumorigenic minority population inhibits tumour growth. ABCB5+ tumour cells detected in human melanoma patients show a primitive molecular phenotype and correlate with clinical melanoma progression. In serial human-to-mouse xenotransplantation experiments, ABCB5+ melanoma cells possess greater tumorigenic capacity than ABCB5- bulk populations and re-establish clinical tumour heterogeneity. In vivo genetic lineage tracking demonstrates a specific capacity of ABCB5+ subpopulations for self-renewal and differentiation, because ABCB5+ cancer cells generate both ABCB5+ and ABCB5- progeny, whereas ABCB5- tumour populations give rise, at lower rates, exclusively to ABCB5- cells. In an initial proof-of-principle analysis, designed to test the hypothesis that MMIC are also required for growth of established tumours, systemic administration of a monoclonal antibody directed at ABCB5, shown to be capable of inducing antibody-dependent cell-mediated cytotoxicity in ABCB5+ MMIC, exerted tumour-inhibitory effects. Identification of tumour-initiating cells with enhanced abundance in more advanced disease but susceptibility to specific targeting through a defining chemoresistance determinant has important implications for cancer therapy.
MeSH Terms
ATP Binding Cassette Transporter, Subfamily B
ATP Binding Cassette Transporter, Subfamily B, Member 1/genetics,metabolism
Animals
Cell Division
Cell Line, Tumor
Cell Lineage
Disease Progression
Gene Expression Regulation, Neoplastic
Humans
Melanoma/genetics,metabolism,pathology
Mice
Mice, Inbred BALB C
Mice, Inbred NOD
Mice, Nude
Mice, SCID
Neoplasm Transplantation
Neoplastic Stem Cells/metabolism,pathology,transplantation
Tissue Array Analysis
Transplantation, Heterologous
Chemicals
ABCB5 protein, human
ATP Binding Cassette Transporter, Subfamily B
ATP Binding Cassette Transporter, Subfamily B, Member 1
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Schatton Tobias
Transplantation Research Center, Children's Hospital Boston and Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA.
Murphy George F
Frank Natasha Y
Yamaura Kazuhiro
Waaga-Gasser Ana Maria
Gasser Martin
Zhan Qian
Jordan Stefan
Duncan Lyn M
Weishaupt Carsten
Fuhlbrigge Robert C
Kupper Thomas S
Sayegh Mohamed H
Frank Markus H
References (30)
30 references, click to expand
-
Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential.
Eur J Cancer. 2007 Mar;43(5):935-46
PMID: 17320377
-
Molecular plasticity of human melanoma cells.
Oncogene. 2003 May 19;22(20):3070-5
PMID: 12789282
-
Prospective identification of tumorigenic breast cancer cells.
Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):3983-8
PMID: 12629218
-
Identification and expansion of human colon-cancer-initiating cells.
Nature. 2007 Jan 4;445(7123):111-5
PMID: 17122771
-
A tumorigenic subpopulation with stem cell properties in melanomas.
Cancer Res. 2005 Oct 15;65(20):9328-37
PMID: 16230395
-
A cell initiating human acute myeloid leukaemia after transplantation into SCID mice.
Nature. 1994 Feb 17;367(6464):645-8
PMID: 7509044
-
Stem cells, cancer, and cancer stem cells.
Nature. 2001 Nov 1;414(6859):105-11
PMID: 11689955
-
Direct visualisation and quantification of cellular cytotoxicity using two colour flourescence.
J Immunol Methods. 1992 Nov 25;156(1):47-54
PMID: 1431162
-
Comparative oncogenomics identifies NEDD9 as a melanoma metastasis gene.
Cell. 2006 Jun 30;125(7):1269-81
PMID: 16814714
-
Identification of distinct changes in gene expression after modulation of melanoma tumor antigen p97 (melanotransferrin) in multiple models in vitro and in vivo.
Carcinogenesis. 2007 Oct;28(10):2172-83
PMID: 17449903
-
Glioma stem cells promote radioresistance by preferential activation of the DNA damage response.
Nature. 2006 Dec 7;444(7120):756-60
PMID: 17051156
-
Activated leukocyte cell adhesion molecule/CD166, a marker of tumor progression in primary malignant melanoma of the skin.
Am J Pathol. 2000 Mar;156(3):769-74
PMID: 10702391
-
Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells.
Nature. 2006 Dec 7;444(7120):761-5
PMID: 17151667
-
Increased expression of stem cell markers in malignant melanoma.
Mod Pathol. 2007 Jan;20(1):102-7
PMID: 17143262
-
Tumour stem cells and drug resistance.
Nat Rev Cancer. 2005 Apr;5(4):275-84
PMID: 15803154
-
ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma.
Cancer Res. 2005 May 15;65(10):4320-33
PMID: 15899824
-
Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell.
Nat Med. 1997 Jul;3(7):730-7
PMID: 9212098
-
Tumor growth need not be driven by rare cancer stem cells.
Science. 2007 Jul 20;317(5836):337
PMID: 17641192
-
Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic.
Cancer Res. 2005 Jul 15;65(14):6207-19
PMID: 16024622
-
Identification of human brain tumour initiating cells.
Nature. 2004 Nov 18;432(7015):396-401
PMID: 15549107
-
Therapeutic potential of chimeric anti-(ganglioside GD3) antibody KM871: antitumor activity in xenograft model of melanoma and effector function analysis.
Cancer Immunol Immunother. 2000 Jul;49(4-5):253-8
PMID: 10941908
-
Malignant melanoma: genetics and therapeutics in the genomic era.
Genes Dev. 2006 Aug 15;20(16):2149-82
PMID: 16912270
-
Regulation of myogenic progenitor proliferation in human fetal skeletal muscle by BMP4 and its antagonist Gremlin.
J Cell Biol. 2006 Oct 9;175(1):99-110
PMID: 17015616
-
Expression of the neuroectodermal intermediate filament nestin in human melanomas.
Cancer Res. 1994 Jan 15;54(2):354-6
PMID: 8275467
-
A proof-of-principle study of epigenetic therapy added to neoadjuvant doxorubicin cyclophosphamide for locally advanced breast cancer.
PLoS One. 2006 Dec 20;1:e98
PMID: 17183730
-
Murine IgG1 complexes trigger immune effector functions predominantly via Fc gamma RIII (CD16).
J Immunol. 1998 Sep 15;161(6):3026-32
PMID: 9743367
-
A human colon cancer cell capable of initiating tumour growth in immunodeficient mice.
Nature. 2007 Jan 4;445(7123):106-10
PMID: 17122772
-
Membrane transporters and channels: role of the transportome in cancer chemosensitivity and chemoresistance.
Cancer Res. 2004 Jun 15;64(12):4294-301
PMID: 15205344
-
Regulation of progenitor cell fusion by ABCB5 P-glycoprotein, a novel human ATP-binding cassette transporter.
J Biol Chem. 2003 Nov 21;278(47):47156-65
PMID: 12960149
-
Embryonic and tumorigenic pathways converge via Nodal signaling: role in melanoma aggressiveness.
Nat Med. 2006 Aug;12(8):925-32
PMID: 16892036