Skin squamous cell carcinoma propagating cells increase with tumour progression and invasiveness

EMBO Journal

Volumn 31, Issue 24, 2012, Pages 4563-4575

  Lapouge, Gaëlle ^a   Beck, Benjamin ^a   Nassar, Dany ^a   Dubois, Christine ^a   Dekoninck, Sophie ^a   Blanpain, Cédric ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

cancer stem cells; carcinoma; papilloma; skin cancers

Indexed keywords

CD34 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INVASION; CANCER STEM CELL; CELL POPULATION; CLONOGENESIS; CONTROLLED STUDY; DILUTION; ENDOTHELIUM CELL; FIBROBLAST; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN CARCINOMA; STEM CELL TRANSPLANTATION; TUMOR CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT;

ANIMALS; ANTIGENS, CD34; CARCINOMA, SQUAMOUS CELL; CELL PROLIFERATION; DISEASE PROGRESSION; DNA PRIMERS; FLOW CYTOMETRY; HISTOLOGICAL TECHNIQUES; MICE; MICE, SCID; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; PAPILLOMA; REAL-TIME POLYMERASE CHAIN REACTION; SKIN NEOPLASMS; STEM CELL TRANSPLANTATION; TAMOXIFEN;

MUS;

EID: 84871003153     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.312     Document Type: Article

References (36)

1. Abel EL, Angel JM, Kiguchi K, DiGiovanni J (2009) Multi-stage chemical carcinogenesis in mouse skin: fundamentals and applications. Nat Protoc 4: 1350-1362
2. Alam M, Ratner D (2001) Cutaneous squamous-cell carcinoma. N Engl J Med 344: 975-983 (Pubitemid 32240317)
3. Ansieau S, Bastid J, Doreau A, Morel AP, Bouchet BP, Thomas C, Fauvet F, Puisieux I, Doglioni C, Piccinin S, Maestro R, Voeltzel T, Selmi A, Valsesia-Wittmann S, Caron de Fromentel C, Puisieux A (2008) Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 14: 79-89 (Pubitemid 351890463)
4. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, Clevers H (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007 (Pubitemid 350014593)
5. Barrett LE, Granot Z, Coker C, Iavarone A, Hambardzumyan D, Holland EC, Nam HS, Benezra R (2012) Self-renewal does not predict tumor growth potential in mouse models of high-grade glioma. Cancer Cell 21: 11-24
6. Beck B, Driessens G, Goossens S, Youssef KK, Kuchnio A, Caauwe A, Sotiropoulou PA, Loges S, Lapouge G, Candi A, Mascre G, Drogat B, Dekoninck S, Haigh JJ, Carmeliet P, Blanpain C (2011) A vascular niche and a VEGF-Nrp1 loop regulate the initiation and stemness of skin tumours. Nature 478: 399-403
7. Blanpain C, Lowry WE, Geoghegan A, Polak L, Fuchs E (2004) Selfrenewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118: 635-648 (Pubitemid 39179715)
8. Boiko AD, Razorenova OV, van de Rijn M, Swetter SM, Johnson DL, Ly DP, Butler PD, Yang GP, Joshua B, Kaplan MJ, Longaker MT, Weissman IL (2010) Human melanoma-initiating cells express neural crest nerve growth factor receptor CD271. Nature 466: 133-137
9. Caulin C, Bauluz C, Gandarillas A, Cano A, Quintanilla M (1993) Changes in keratin expression during malignant progression of transformed mouse epidermal keratinocytes. Exp Cell Res 204: 11-21 (Pubitemid 23203080)
10. Driessens G, Beck B, Caauwe A, Simons BD, Blanpain C (2012) Defining the mode of tumour growth by clonal analysis. Nature 488: 527-530
11. Frame S, Crombie R, Liddell J, Stuart D, Linardopoulos S, Nagase H, Portella G, Brown K, Street A, Akhurst R, Balmain A (1998) Epithelial carcinogenesis in the mouse: correlating the genetics and the biology. Philos Trans R Soc Lond B Biol Sci 353: 839-845 (Pubitemid 28314366)
12. Gershwin ME, Merchant B, Gelfand MC, Vickers J, Steinberg AD, Hansen CT (1975) The natural history and immunopathology of outbred athymic (nude) mice. Clin Immunol Immunopathol 4: 324-340
13. Hu Y, Smyth GK (2009) ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods 347: 70-78
14. Jonkers J, Meuwissen R, van der Gulden H, Peterse H, van der Valk M, Berns A (2001) Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat Genet 29: 418-425 (Pubitemid 34326692)
15. Kemp CJ (2005) Multistep skin cancer in mice as a model to study the evolution of cancer cells. Semin Cancer Biol 15: 460-473 (Pubitemid 41318046)
16. Kemp CJ, Donehower LA, Bradley A, Balmain A (1993) Reduction of p53 gene dosage does not increase initiation or promotion but enhances malignant progression of chemically induced skin tumors. Cell 74: 813-822 (Pubitemid 23270601)
17. Lapouge G, Youssef KK, Vokaer B, Achouri Y, Michaux C, Sotiropoulou PA, Blanpain C (2011) Identifying the cellular origin of squamous skin tumors. Proc Natl Acad Sci USA 108: 7431-7436
18. Lobo NA, Shimono Y, Qian D, Clarke MF (2007) The biology of cancer stem cells. Annu Rev Cell Dev Biol 23: 675-699
19. Malanchi I, Peinado H, Kassen D, Hussenet T, Metzger D, Chambon P, Huber M, Hohl D, Cano A, Birchmeier W, Huelsken J (2008) Cutaneous cancer stem cell maintenance is dependent on betacatenin signalling. Nature 452: 650-653 (Pubitemid 351483363)
20. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715 (Pubitemid 351636299)
21. Means AL, Xu Y, Zhao A, Ray KC, Gu G (2008) A CK19(CreERT) knockin mouse line allows for conditional DNA recombination in epithelial cells in multiple endodermal organs. Genesis 46: 318-323 (Pubitemid 352008880)
22. Nguyen LV, Vanner R, Dirks P, Eaves CJ (2012) Cancer stem cells: an evolving concept. Nat Rev Cancer 12: 133-143
23. O'Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445: 106-110 (Pubitemid 46067310)
24. Owens DM, Watt FM (2003) Contribution of stem cells and differentiated cells to epidermal tumours. Nat Rev Cancer 3: 444-451 (Pubitemid 37328848)
25. Pardal R, Clarke MF, Morrison SJ (2003) Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 3: 895-902 (Pubitemid 37500174)
26. Perez-Losada J, Balmain A (2003) Stem-cell hierarchy in skin cancer. Nat Rev Cancer 3: 434-443 (Pubitemid 37328847)
27. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ (2008) Efficient tumour formation by single human melanoma cells. Nature 456: 593-598
28. Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414: 105-111 (Pubitemid 33041634)
29. Rheinwald JG, Green H (1977) Epidermal growth factor and the multiplication of cultured human epidermal keratinocytes. Nature 265: 421-424 (Pubitemid 8023596)
30. Schepers AG, Snippert HJ, Stange DE, van den Born M, van Es JH, van de Wetering M, Clevers H (2012) Lineage tracing reveals Lgr5\+ stem cell activity in mouse intestinal adenomas. Science 337: 730-735
31. Schober M, Fuchs E (2011) Tumor-initiating stem cells of squamous cell carcinomas and their control by TGF-beta and integrin/focal adhesion kinase (FAK) signaling. Proc Natl Acad Sci USA 108: 10544-10549
32. Shackleton M, Quintana E, Fearon ER, Morrison SJ (2009) Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell 138: 822-829
33. Shultz LD, Lyons BL, Burzenski LM, Gott B, Chen X, Chaleff S, Kotb M, Gillies SD, King M, Mangada J, Greiner DL, Handgretinger R (2005) Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J Immunol 174: 6477-6489 (Pubitemid 40663843)
34. Tuveson DA, Shaw AT, Willis NA, Silver DP, Jackson EL, Chang S, Mercer KL, Grochow R, Hock H, Crowley D, Hingorani SR, Zaks T, King C, Jacobetz MA, Wang L, Bronson RT, Orkin SH, DePinho RA, Jacks T (2004) Endogenous oncogenic K-ras(G12D) stimulates proliferation and widespread neoplastic and developmental defects. Cancer Cell 5: 375-387 (Pubitemid 38482073)
35. Vasioukhin V, Degenstein L, Wise B, Fuchs E (1999) The magical touch: genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc Natl Acad Sci USA 96: 8551-8556 (Pubitemid 29354829)
36. White AC, Tran K, Khuu J, Dang C, Cui Y, Binder SW, Lowry WE (2011) Defining the origins of Ras/p53-mediated squamous cell carcinoma. Proc Natl Acad Sci USA 108: 7425-7430