Evidence for the transmission of neoplastic properties from transformed to normal human stem cells

Oncogene

Volumn 30, Issue 46, 2011, Pages 4632-4644

  Werbowetski Ogilvie, T E ^a,c   Schnerch, A ^a   Rampalli, S ^a   Mills, C E ^b   Lee, J B ^a   Hong, S H ^a   Levadoux Martin, M ^a   Bhatia, M ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c UNIVERSITY OF MANITOBA   (Canada)

Author keywords

differentiation; human stem cells; selfrenewal; transformation

Indexed keywords

ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; EPIGENETICS; GENE EXPRESSION; HEMATOPOIESIS; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; PRIORITY JOURNAL;

CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINE, TRANSFORMED; CELL TRANSFORMATION, NEOPLASTIC; COCULTURE TECHNIQUES; EMBRYONIC STEM CELLS; GENE EXPRESSION; GENE EXPRESSION REGULATION; HEMATOPOIETIC STEM CELLS; HUMANS; NEOPLASTIC STEM CELLS; PLURIPOTENT STEM CELLS;

EID: 81255185568     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.175     Document Type: Article

References (57)

1. Azcoitia V, Aracil M, Martinez AC, Torres M. (2005). The homeo-domain protein Meis1 is essential for definitive hematopoiesis and vascular patterning in the mouse embryo. Dev Biol 280: 307-320. (Pubitemid 40692134)
2. Baker DE, Harrison NJ, Maltby E, Smith K, Moore HD, Shaw PJ et al. (2007). Adaptation to culture of human embryonic stem cells and oncogenesis in vivo. Nat Biotechnol 25: 207-215. (Pubitemid 46227120)
3. Bedford L, Walker R, Kondo T, van Cruchten I, King ER, Sablitzky F. (2005). Id4 is required for the correct timing of neural differentiation. Dev Biol 280: 386-395. (Pubitemid 40692139)
4. Bendall SC, Stewart MH, Menendez P, George D, Vijayaragavan K, Werbowetski-Ogilvie T et al. (2007). IGF and FGF cooperatively establish the regulatory stem cell niche of pluripotent human cells in vitro. Nature 448: 1015-1021. (Pubitemid 47345578)
5. Besser D. (2004). Expression of nodal, lefty-a, and lefty-B in undifferentiated human embryonic stem cells requires activation of Smad2/3. J Biol Chem 279: 45076-45084. (Pubitemid 39430922)
6. Bhowmick NA, Chytil A, Plieth D, Gorska AE, Dumont N, Shappell S et al. (2004a). TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303: 848-851. (Pubitemid 38174665)
7. Bhowmick NA, Neilson EG, Moses HL. (2004b). Stromal fibroblasts in cancer initiation and progression. Nature 432: 332-337. (Pubitemid 39551661)
8. Bragdon B, Moseychuk O, Saldanha S, King D, Julian J, Nohe A. (2011). Bone morphogenetic proteins: a critical review. Cell Signal 23: 609-620.
9. Carpenter MK, Inokuma MS, Denham J, Mujtaba T, Chiu C-P, Rao MS. (2001a). Enrichment of neurons and neural precursors from human embryonic stem cells. Exp Neurol 172: 383-397. (Pubitemid 34075087)
10. Carpenter MK, Inokuma MS, Denham J, Mujtaba T, Chiu CP, Rao MS. (2001b). Enrichment of neurons and neural precursors from human embryonic stem cells. Exp Neurol 172: 383-397. (Pubitemid 34075087)
11. Chadwick K, Wang L, Li L, Menendez P, Murdoch B, Rouleau A et al. (2003). Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood 102: 906-915. (Pubitemid 36917782)
12. Damjanov I, Andrews PW. (2007). The terminology of teratocarcino-mas and teratomas. Nat Biotechnol 25: 1212; discussion 1212.
13. Davidson KC, Jamshidi P, Daly R, Hearn MT, Pera MF, Dottori M. (2007). Wnt3a regulates survival, expansion, and maintenance of neural progenitors derived from human embryonic stem cells. Mol Cell Neurosci 36: 408-415. (Pubitemid 47633203)
14. de la Cova C, Abril M, Bellosta P, Gallant P, Johnston LA. (2004). Drosophila myc regulates organ size by inducing cell competition. Cell 117: 107-116. (Pubitemid 38469902)
15. Dvash T, Sharon N, Yanuka O, Benvenisty N. (2007). Molecular analysis of LEFTY-expressing cells in early human embryoid bodies. Stem Cells 25: 465-472. (Pubitemid 46232802)
16. El Wakil A, Francius C, Wolff A, Pleau-Varet J, Nardelli J. (2006). The GATA2 transcription factor negatively regulates the proliferation of neuronal progenitors. Development 133: 2155-2165. (Pubitemid 43986126)
17. Erez N, Truitt M, Olson P, Hanahan D. (2010). Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell 17: 135-147.
18. Hogan C, Dupre-Crochet S, Norman M, Kajita M, Zimmermann C, Pelling AE et al. (2009). Characterization of the interface between normal and transformed epithelial cells. Nat Cell Biol 11: 460-467.
19. Hu MC, Qiu WR, Wang X, Meyer CF, Tan TH. (1996). Human HPK1, a novel human hematopoietic progenitor kinase that activates the JNK/SAPK kinase cascade. Genes Dev 10: 2251-2264. (Pubitemid 26322362)
20. Huse JT, Holland EC. (2010). Targeting brain cancer: advances in the molecular pathology of malignant glioma and medulloblastoma. Nat Rev Cancer 10: 319-331.
21. Ivins S, Pemberton K, Guidez F, Howell L, Krumlauf R, Zelent A. (2003). Regulation of Hoxb2 by APL-associated PLZF protein. Oncogene 22: 3685-3697. (Pubitemid 36760731)
22. Ji J, Werbowetski-Ogilvie TE, Zhong B, Hong SH, Bhatia M. (2009). Pluripotent transcription factors possess distinct roles in normal versus transformed human stem cells. PLoS One 4: e8065.
23. Joyce JA. (2005). Therapeutic targeting of the tumor microenviron-ment. Cancer Cell 7: 513-520.
24. Kajita M, Hogan C, Harris AR, Dupre-Crochet S, Itasaki N, Kawakami K et al. (2010). Interaction with surrounding normal epithelial cells influences signalling pathways and behaviour of Src-transformed cells. J Cell Sci 123: 171-180.
25. Kiefer F, Tibbles LA, Anafi M, Janssen A, Zanke BW, Lassam N et al. (1996). HPK1, a hematopoietic protein kinase activating the SAPK/JNK pathway. Embo J 15: 7013-7025. (Pubitemid 27023272)
26. Kihm AJ, Kong Y, Hong W, Russell JE, Rouda S, Adachi K et al. (2002). An abundant erythroid protein that stabilizes free alpha-haemoglobin. Nature 417: 758-763. (Pubitemid 34640631)
27. Kitajima K, Masuhara M, Era T, Enver T, Nakano T. (2002). GATA-2 and GATA-2/ER display opposing activities in the development and differentiation of blood progenitors. Embo J 21: 3060-3069. (Pubitemid 34670390)
28. Lensch MW, Ince TA. (2007). The terminology of teratocarcinomas and teratomas. Nat Biotechnol 25: 1211; author reply 1211-2.
29. Li C, Wong WH. (2001). Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection. PNAS 98: 31-36. (Pubitemid 32095858)
30. Mishra P, Banerjee D, Ben-Baruch A. (2011). Chemokines at the crossroads of tumor-fibroblast interactions that promote malignancy. J Leukoc Biol 89: 31-39.
31. Moreno E. (2008). Is cell competition relevant to cancer? Nat Rev Cancer 8: 141-147. (Pubitemid 351161318)
32. Moreno E, Basler K. (2004). dMyc transforms cells into super-competitors. Cell 117: 117-129. (Pubitemid 38469903)
33. Murdoch B, Chadwick K, Martin M, Shojaei F, Shah KV, Gallacher L et al. (2003). Wnt-5A augments repopulating capacity and primitive hematopoietic development of human blood stem cells in vivo. Proc Natl Acad Sci USA 100: 3422-3427. (Pubitemid 36356599)
34. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R et al. (2005). Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angio-genesis through elevated SDF-1/CXCL12 secretion. Cell 121: 335-348. (Pubitemid 40692295)
35. Postovit LM, Margaryan NV, Seftor EA, Kirschmann DA, Lipavsky A, Wheaton WW et al. (2008). Human embryonic stem cell microenvironment suppresses the tumorigenic pheno-type of aggressive cancer cells. Proc Natl Acad Sci USA 105: 4329-4334. (Pubitemid 351754380)
36. Raman D, Baugher PJ, Thu YM, Richmond A. (2007). Role of chemokines in tumor growth. Cancer Lett 256: 137-165. (Pubitemid 47418345)
37. Rosen JM, Jordan CT. (2009). The increasing complexity of the cancer stem cell paradigm. Science 324: 1670-1673.
38. Smith JR, Vallier L, Lupo G, Alexander M, Harris WA, Pedersen RA. (2008). Inhibition of Activin/Nodal signaling promotes specification of human embryonic stem cells into neuroectoderm. Dev Biol 313: 107-117. (Pubitemid 350298306)
39. Snyder A, Fraser ST, Baron MH. (2004). Bone morphogenetic proteins in vertebrate hematopoietic development. J Cell Biochem 93: 224-232. (Pubitemid 44264200)
40. Staal FJ, Sen JM. (2008). The canonical Wnt signaling pathway plays an important role in lymphopoiesis and hematopoiesis. Eur J Immunol 38: 1788-1794.
41. Steele-Perkins G, Plachez C, Butz KG, Yang G, Bachurski CJ, Kinsman SL et al. (2005). The transcription factor gene Nfib is essential for both lung maturation and brain development. Mol Cell Biol 25: 685-698. (Pubitemid 40096589)
42. Stewart MH, Bosse M, Chadwick K, Menendez P, Bendall SC, Bhatia M. (2006). Clonal isolation of hESCs reveals heterogeneity within the pluripotent stem cell compartment. Nat Methods 3: 807-815. (Pubitemid 44445828)
43. Trimboli AJ, Cantemir-Stone CZ, Li F, Wallace JA, Merchant A, Creasap N et al. (2009). Pten in stromal fibroblasts suppresses mammary epithelial tumours. Nature 461: 1084-1091.
44. Tsai FY, Keller G, Kuo FC, Weiss M, Chen J, Rosenblatt M et al. (1994). An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 371: 221-226. (Pubitemid 24293019)
45. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659. (Pubitemid 47214727)
46. Vijayaragavan K, Szabo E, Bosse M, Ramos-Mejia V, Moon RT, Bhatia M. (2009). Noncanonical Wnt signaling orchestrates early developmental events toward hematopoietic cell fate from human embryonic stem cells. Cell Stem Cell 4: 248-262.
47. Wang L, Li L, Shojaei F, Levac K, Cerdan C, Menendez P et al. (2004). Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangio-blastic properties. Immunity 21: 31-41. (Pubitemid 38925265)
48. Werbowetski-Ogilvie TE, Bosse M, Stewart M, Schnerch A, Ramos-Mejia V, Rouleau A et al. (2009). Characterization of human embryonic stem cells with features of neoplastic progression. Nat Biotechnol 27: 91-97.
49. Wicha MS, Liu S, Dontu G. (2006a). Cancer stem cells: an old idea-a paradigm shift. Cancer Res 66: 1883-1890.
50. Wicha MS, Liu S, Dontu G. (2006b). Cancer stem cells: an old idea-a paradigm shift. Cancer Res 66: 1883-1890; discussion 1895-6.
51. Wong P, Iwasaki M, Somervaille TC, So CW, Cleary ML. (2007). Meis1 is an essential and rate-limiting regulator of MLL leukemia stem cell potential. Genes Dev 21: 2762-2774. (Pubitemid 350070722)
52. Yenerel MN, Sundell IB, Weese J, Bulger M, Gilligan DM. (2005). Expression of adducin genes during erythropoiesis: a novel erythroid promoter for ADD2. Exp Hematol 33: 758-766. (Pubitemid 40826589)
53. Yilmaz OH, Valdez R, Theisen BK, Guo W, Ferguson DO, Wu H et al. (2006). Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 441: 475-482. (Pubitemid 44050144)
54. Yu L, Liu C, Vandeusen J, Becknell B, Dai Z, Wu YZ et al. (2005). Global assessment of promoter methylation in a mouse model of cancer identifies ID4 as a putative tumor-suppressor gene in human leukemia. Nat Genet 37: 265-274. (Pubitemid 41716253)
55. Yuan A, Farber EL, Rapoport AL, Tejada D, Deniskin R, Akhmedov NB et al. (2009). Transfer of microRNAs by embryonic stem cell microvesicles. PLoS One 4: e4722.
56. Zangenberg M, Grubach L, Aggerholm A, Silkjaer T, Juhl-Christen-sen C, Nyvold CG et al. (2009). The combined expression of HOXA4 and MEIS1 is an independent prognostic factor in patients with AML. Eur J Haematol 83: 439-448.
57. Zhang J, Grindley JC, Yin T, Jayasinghe S, He XC, Ross JT et al. (2006). PTEN maintains hematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 441: 518-522. (Pubitemid 44050154)