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PMID: 18202660 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Identification of cells initiating human melanomas.

Nature ·Vol. 451 ·No. 7176 ·2008-01-17 ·Pages 345-9

Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, Zhan Q, Jordan S, Duncan LM, Weishaupt C, Fuhlbrigge RC, Kupper TS, Sayegh MH, Frank MH

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
  1. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential.
    Eur J Cancer. 2007 Mar;43(5):935-46 PMID: 17320377
  2. Molecular plasticity of human melanoma cells.
    Oncogene. 2003 May 19;22(20):3070-5 PMID: 12789282
  3. Prospective identification of tumorigenic breast cancer cells.
    Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):3983-8 PMID: 12629218
  4. Identification and expansion of human colon-cancer-initiating cells.
    Nature. 2007 Jan 4;445(7123):111-5 PMID: 17122771
  5. A tumorigenic subpopulation with stem cell properties in melanomas.
    Cancer Res. 2005 Oct 15;65(20):9328-37 PMID: 16230395
  6. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice.
    Nature. 1994 Feb 17;367(6464):645-8 PMID: 7509044
  7. Stem cells, cancer, and cancer stem cells.
    Nature. 2001 Nov 1;414(6859):105-11 PMID: 11689955
  8. Direct visualisation and quantification of cellular cytotoxicity using two colour flourescence.
    J Immunol Methods. 1992 Nov 25;156(1):47-54 PMID: 1431162
  9. Comparative oncogenomics identifies NEDD9 as a melanoma metastasis gene.
    Cell. 2006 Jun 30;125(7):1269-81 PMID: 16814714
  10. 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
  11. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response.
    Nature. 2006 Dec 7;444(7120):756-60 PMID: 17051156
  12. 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
  13. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells.
    Nature. 2006 Dec 7;444(7120):761-5 PMID: 17151667
  14. Increased expression of stem cell markers in malignant melanoma.
    Mod Pathol. 2007 Jan;20(1):102-7 PMID: 17143262
  15. Tumour stem cells and drug resistance.
    Nat Rev Cancer. 2005 Apr;5(4):275-84 PMID: 15803154
  16. ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma.
    Cancer Res. 2005 May 15;65(10):4320-33 PMID: 15899824
  17. 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
  18. Tumor growth need not be driven by rare cancer stem cells.
    Science. 2007 Jul 20;317(5836):337 PMID: 17641192
  19. 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
  20. Identification of human brain tumour initiating cells.
    Nature. 2004 Nov 18;432(7015):396-401 PMID: 15549107
  21. 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
  22. Malignant melanoma: genetics and therapeutics in the genomic era.
    Genes Dev. 2006 Aug 15;20(16):2149-82 PMID: 16912270
  23. 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
  24. Expression of the neuroectodermal intermediate filament nestin in human melanomas.
    Cancer Res. 1994 Jan 15;54(2):354-6 PMID: 8275467
  25. 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
  26. Murine IgG1 complexes trigger immune effector functions predominantly via Fc gamma RIII (CD16).
    J Immunol. 1998 Sep 15;161(6):3026-32 PMID: 9743367
  27. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice.
    Nature. 2007 Jan 4;445(7123):106-10 PMID: 17122772
  28. Membrane transporters and channels: role of the transportome in cancer chemosensitivity and chemoresistance.
    Cancer Res. 2004 Jun 15;64(12):4294-301 PMID: 15205344
  29. 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
  30. Embryonic and tumorigenic pathways converge via Nodal signaling: role in melanoma aggressiveness.
    Nat Med. 2006 Aug;12(8):925-32 PMID: 16892036
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2008-01-17
Pages
345-9
Language
English
Region
England
NLM ID
0410462
PMCID
PMC3660705
Subset
IM
Grants
NIAMS NIH HHS · P30 AR042689 · United States
NCI NIH HHS · R01 CA113796-01A1 · United States
NHLBI NIH HHS · R01 HL084815 · United States
NINDS NIH HHS · K08 NS051349 · United States
NCI NIH HHS · R01 CA113796 · United States
NIAMS NIH HHS · P30 AR042689-159006 · United States
NHLBI NIH HHS · R01 HL084815-17 · United States
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