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Stem cells and solid cancers

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Abstract

Recently, there have been significant advances in our knowledge of stem cells found in tissues that can develop solid tumours. In particular, novel stem cell markers have been identified for the first time identifying multipotential cells: a required characteristic of a stem cell. The scarcity of cancer stem cells has been questioned. Current dogma states that they are rare, but novel research has suggested that this may not be the case. Here, we review the latest literature on stem cells, particularly cancer stem cells within solid tumours. We discuss current thinking on how stem cells develop into cancer stem cells and how they protect themselves from doing so and do they express unique markers that can be used to detect stem cells. We attempt to put into perspective these latest advances in stem cell biology and their potential for cancer therapy.

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References

  1. Radtke F, Clevers H (2005) Self-renewal and cancer of the gut: two sides of a coin. Science 307:1904–1909

    PubMed  CAS  Google Scholar 

  2. Tomlinson I, Bodmer W (1999) Selection, the mutation rate and cancer: ensuring that the tail does not wag the dog. Nat Med 5:11–12

    PubMed  CAS  Google Scholar 

  3. Pierce GB, Nakane PK, Martinez-Hernandez A et al (1977) Ultrastructural comparison of differentiation of stem cells of murine adenocarcinomas of colon and breast with their normal counterparts. J Natl Cancer Inst 58:1329–1345

    PubMed  CAS  Google Scholar 

  4. Hamburger AW, Salmon SE (1977) Primary bioassay of human tumor stem cells. Science 197:461–463

    PubMed  CAS  Google Scholar 

  5. Till JE, Mc CE (1961) A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res 14:213–222

    PubMed  CAS  Google Scholar 

  6. Mayhall EA, Paffett-Lugassy N, Zon LI (2004) The clinical potential of stem cells. Curr Opin Cell Biol 16:713–720

    PubMed  CAS  Google Scholar 

  7. Cheng H, Leblond CP (1974) Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian Theory of the origin of the four epithelial cell types. Am J Anat 141:537–561

    PubMed  CAS  Google Scholar 

  8. Cheng H, Leblond CP (1974) Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. I. Columnar cell. Am J Anat 141:461–479

    PubMed  CAS  Google Scholar 

  9. Cheng H, Leblond CP (1974) Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. III. Entero-endocrine cells. Am J Anat 141:503–519

    PubMed  CAS  Google Scholar 

  10. Niemann C, Watt FM (2002) Designer skin: lineage commitment in postnatal epidermis. Trends Cell Biol 12:185–192

    PubMed  CAS  Google Scholar 

  11. Rossi DJ, Jamieson CH, Weissman IL (2008) Stems cells and the pathways to aging and cancer. Cell 132:681–696

    PubMed  CAS  Google Scholar 

  12. Stemple DL, Anderson DJ (1993) Lineage diversification of the neural crest: in vitro investigations. Dev Biol 159:12–23

    PubMed  CAS  Google Scholar 

  13. Beltrami AP, Barlucchi L, Torella D et al (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114:763–776

    PubMed  CAS  Google Scholar 

  14. Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495

    PubMed  CAS  Google Scholar 

  15. Alonso L, Fuchs E (2003) Stem cells of the skin epithelium. Proc Natl Acad Sci U S A 100(Suppl 1):11830–11835

    PubMed  CAS  Google Scholar 

  16. Bjerknes M, Cheng H (1981) The stem-cell zone of the small intestinal epithelium. IV. Effects of resecting 30% of the small intestine. Am J Anat 160:93–103

    PubMed  CAS  Google Scholar 

  17. Bjerknes M, Cheng H (1981) The stem-cell zone of the small intestinal epithelium. III. Evidence from columnar, enteroendocrine, and mucous cells in the adult mouse. Am J Anat 160:77–91

    PubMed  CAS  Google Scholar 

  18. Bjerknes M, Cheng H (1981) The stem-cell zone of the small intestinal epithelium. II. Evidence from paneth cells in the newborn mouse. Am J Anat 160:65–75

    PubMed  CAS  Google Scholar 

  19. Bjerknes M, Cheng H (1981) The stem-cell zone of the small intestinal epithelium. I. Evidence from Paneth cells in the adult mouse. Am J Anat 160:51–63

    PubMed  CAS  Google Scholar 

  20. Bjerknes M, Cheng H (1981) The stem-cell zone of the small intestinal epithelium. V. Evidence for controls over orientation of boundaries between the stem-cell zone, proliferative zone, and the maturation zone. Am J Anat 160:105–112

    PubMed  CAS  Google Scholar 

  21. Forbes S, Vig P, Poulsom R et al (2002) Hepatic stem cells. J Pathol 197:510–518

    PubMed  Google Scholar 

  22. Bonner-Weir S, Sharma A (2002) Pancreatic stem cells. J Pathol 197:519–526

    PubMed  Google Scholar 

  23. Watt FM, Hogan BL (2000) Out of Eden: stem cells and their niches. Science 287:1427–1430

    PubMed  CAS  Google Scholar 

  24. Crosnier C, Stamataki D, Lewis J (2006) Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet 7:349–359

    PubMed  CAS  Google Scholar 

  25. Madison BB, Braunstein K, Kuizon E et al (2005) Epithelial hedgehog signals pattern the intestinal crypt–villus axis. Development 132:279–289

    PubMed  CAS  Google Scholar 

  26. van den Brink GR, Bleuming SA, Hardwick JC et al (2004) Indian Hedgehog is an antagonist of Wnt signaling in colonic epithelial cell differentiation. Nat Genet 36:277–282

    PubMed  Google Scholar 

  27. Kiger AA, Jones DL, Schulz C et al (2001) Stem cell self-renewal specified by JAK–STAT activation in response to a support cell cue. Science 294:2542–2545

    PubMed  CAS  Google Scholar 

  28. Tulina N, Matunis E (2001) Control of stem cell self-renewal in Drosophila spermatogenesis by JAK–STAT signaling. Science 294:2546–2549

    PubMed  CAS  Google Scholar 

  29. Spradling A, Drummond-Barbosa D, Kai T (2001) Stem cells find their niche. Nature 414:98–104

    PubMed  CAS  Google Scholar 

  30. Brinster RL, Zimmermann JW (1994) Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A 91:11298–11302

    PubMed  CAS  Google Scholar 

  31. Ohlstein B, Spradling A (2006) The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439:470–474

    PubMed  CAS  Google Scholar 

  32. Barker N, Clevers H (2007) Tracking down the stem cells of the intestine: strategies to identify adult stem cells. Gastroenterology 133:1755–1760

    PubMed  CAS  Google Scholar 

  33. Bjerknes M, Cheng H (1999) Clonal analysis of mouse intestinal epithelial progenitors. Gastroenterology 116:7–14

    PubMed  CAS  Google Scholar 

  34. Greaves LC, Preston SL, Tadrous PJ et al (2006) Mitochondrial DNA mutations are established in human colonic stem cells, and mutated clones expand by crypt fission. Proc Natl Acad Sci U S A 103:714–719

    PubMed  CAS  Google Scholar 

  35. Gutierrez-Gonzalez L, Deheragoda M, Elia G et al (2009) Analysis of the clonal architecture of the human small intestine establishes a common stem cell for all lineages and reveals a mechanism for the fixation and spread of mutations. J Pathol 217:489–496. doi:10.1002/path.2502

    PubMed  CAS  Google Scholar 

  36. McDonald SA, Greaves LC, Gutierrez-Gonzalez L et al (2008) Mechanisms of field cancerization in the human stomach: the expansion and spread of mutated gastric stem cells. Gastroenterology 134:500–510

    PubMed  CAS  Google Scholar 

  37. Yatabe Y, Tavare S, Shibata D (2001) Investigating stem cells in human colon by using methylation patterns. Proc Natl Acad Sci U S A 98:10839–10844

    PubMed  CAS  Google Scholar 

  38. Barker N, van Es JH, Kuipers J et al (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449:1003–1007

    PubMed  CAS  Google Scholar 

  39. Cai WB, Roberts SA, Potten CS et al (1997) The number of clonogenic cells in crypts in three regions of murine large intestine. Int J Radiat Biol 71:573–579

    PubMed  CAS  Google Scholar 

  40. Sangiorgi E, Capecchi MR (2008) Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 40:915–920

    PubMed  CAS  Google Scholar 

  41. Wright NA, Alison MR (1984) The biology of epithelial cell populations. Oxford University Press, Oxford

    Google Scholar 

  42. Brabletz S, Schmalhofer O, Brabletz T (2009) Gastrointestinal stem cells in development and cancer. J Pathol 217:307–317

    PubMed  CAS  Google Scholar 

  43. Jensen UB, Lowell S, Watt FM (1999) The spatial relationship between stem cells and their progeny in the basal layer of human epidermis: a new view based on whole-mount labelling and lineage analysis. Development 126:2409–2418

    PubMed  CAS  Google Scholar 

  44. Pepper JW, Sprouffske K, Maley CC (2007) Animal cell differentiation patterns suppress somatic evolution. PLoS Comput Biol 3:e250

    PubMed  Google Scholar 

  45. Cairns J (1975) Mutation selection and the natural history of cancer. Nature 255:197–200

    PubMed  CAS  Google Scholar 

  46. Potten CS, Owen G, Booth D (2002) Intestinal stem cells protect their genome by selective segregation of template DNA strands. J Cell Sci 115:2381–2388

    PubMed  CAS  Google Scholar 

  47. Smith GH (2005) Label-retaining epithelial cells in mouse mammary gland divide asymmetrically and retain their template DNA strands. Development 132:681–687

    PubMed  CAS  Google Scholar 

  48. Shinin V, Gayraud-Morel B, Gomes D et al (2006) Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 8:677–687

    PubMed  CAS  Google Scholar 

  49. Lansdorp PM (2007) Immortal strands? Give me a break. Cell 129:1244–1247

    PubMed  CAS  Google Scholar 

  50. Kiel MJ, He S, Ashkenazi R et al (2007) Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU. Nature 449:238–242

    PubMed  CAS  Google Scholar 

  51. van Leeuwen IM, Byrne HM, Jensen OE et al (2006) Crypt dynamics and colorectal cancer: advances in mathematical modelling. Cell Prolif 39:157–181

    PubMed  Google Scholar 

  52. Goodell MA, Brose K, Paradis G et al (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183:1797–1806

    PubMed  CAS  Google Scholar 

  53. Alison MR, Poulsom R, Otto WR et al (2003) Plastic adult stem cells: will they graduate from the school of hard knocks? J Cell Sci 116:599–603

    PubMed  Google Scholar 

  54. Hirschmann-Jax C, Foster AE, Wulf GG et al (2005) A distinct “side population” of cells in human tumor cells: implications for tumor biology and therapy. Cell Cycle 4:203–205

    PubMed  CAS  Google Scholar 

  55. Morita Y, Ema H, Yamazaki S et al (2006) Non-side-population hematopoietic stem cells in mouse bone marrow. Blood 108:2850–2856

    PubMed  CAS  Google Scholar 

  56. Storms RW, Trujillo AP, Springer JB et al (1999) Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl Acad Sci U S A 96:9118–9123

    PubMed  CAS  Google Scholar 

  57. Cheung AM, Wan TS, Leung JC et al (2007) Aldehyde dehydrogenase activity in leukemic blasts defines a subgroup of acute myeloid leukemia with adverse prognosis and superior NOD/SCID engrafting potential. Leukemia 21:1423–1430

    PubMed  CAS  Google Scholar 

  58. Giangreco A, Shen H, Reynolds SD et al (2004) Molecular phenotype of airway side population cells. Am J Physiol Lung Cell Mol Physiol 286:L624–630

    PubMed  CAS  Google Scholar 

  59. Vig P, Russo FP, Edwards RJ et al (2006) The sources of parenchymal regeneration after chronic hepatocellular liver injury in mice. Hepatology 43:316–324

    PubMed  Google Scholar 

  60. Barker N (2008) The canonical Wnt/beta-catenin signalling pathway. Methods Mol Biol 468:5–15

    PubMed  CAS  Google Scholar 

  61. van de Wetering M, Sancho E, Verweij C et al (2002) The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111:241–250

    PubMed  Google Scholar 

  62. van Es JH, Jay P, Gregorieff A et al (2005) Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol 7:381–386

    PubMed  Google Scholar 

  63. Sato T, Vries RG, Snippert HJ, et al (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. doi:10.1038/nature07935

  64. Bea S, Tort F, Pinyol M et al (2001) BMI-1 gene amplification and overexpression in hematological malignancies occur mainly in mantle cell lymphomas. Cancer Res 61:2409–2412

    Google Scholar 

  65. Baylin SB, Herman JG, Graff JR et al (1998) Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv Cancer Res 72:141–196

    PubMed  CAS  Google Scholar 

  66. Kim HK, Song KS, Kim HO et al (2003) Circulating numbers of endothelial progenitor cells in patients with gastric and breast cancer. Cancer Lett 198:83–88

    PubMed  CAS  Google Scholar 

  67. Reinisch C, Kandutsch S, Uthman A et al (2006) BMI-1: a protein expressed in stem cells, specialized cells and tumors of the gastrointestinal tract. Histol Histopathol 21:1143–1149

    PubMed  CAS  Google Scholar 

  68. Potten CS, Booth C, Pritchard DM (1997) The intestinal epithelial stem cell: the mucosal governor. Int J Exp Pathol 78:219–243

    PubMed  CAS  Google Scholar 

  69. Nakamura M, Okano H, Blendy JA et al (1994) Musashi, a neural RNA-binding protein required for Drosophila adult external sensory organ development. Neuron 13:67–81

    PubMed  CAS  Google Scholar 

  70. Potten CS, Booth C, Tudor GL et al (2003) Identification of a putative intestinal stem cell and early lineage marker; musashi-1. Differentiation 71:28–41

    PubMed  CAS  Google Scholar 

  71. Murayama M, Okamoto R, Tsuchiya K et al (2009) Musashi-1 suppresses expression of Paneth cell-specific genes in human intestinal epithelial cells. J Gastroenterol 44:173–182

    PubMed  CAS  Google Scholar 

  72. May R, Riehl TE, Hunt C et al (2008) Identification of a novel putative gastrointestinal stem cell and adenoma stem cell marker, doublecortin and CaM kinase-like-1, following radiation injury and in adenomatous polyposis coli/multiple intestinal neoplasia mice. Stem Cells 26:630–637

    PubMed  Google Scholar 

  73. Horwitz E, Prockop D, Fitzpatrick L et al (1999) Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 5:309–313

    PubMed  CAS  Google Scholar 

  74. Alison M, Islam S, Lim S (2009) Stem cells in liver regeneration, fibrosis and cancer: the good, the bad and the ugly. J Pathol 217:282–298

    PubMed  CAS  Google Scholar 

  75. Kuwahara R, Kofman AV, Landis CS et al (2008) The hepatic stem cell niche: identification by label-retaining cell assay. Hepatology 47:1994–2002

    PubMed  Google Scholar 

  76. Tang Y, Kitisin K, Jogunoori W et al (2008) Progenitor/stem cells give rise to liver cancer due to aberrant TGF-beta and IL-6 signaling. Proc Natl Acad Sci U S A 105:2445–2450

    PubMed  CAS  Google Scholar 

  77. Sell S, Pierce GB (1994) Maturation arrest of stem cell differentiation is a common pathway for the cellular origin of teratocarcinomas and epithelial cancers. Lab Invest 70:6–22

    PubMed  CAS  Google Scholar 

  78. Berenblum I (1949) The carcinogenic action of 9, 10-dimethyl-1, 2-benzanthracene on the skin and subcutaneous tissues of the mouse, rabbit, rat and guinea pig. J Natl Cancer Inst 10:167–174

    PubMed  CAS  Google Scholar 

  79. Barker N, Ridgway RA, van Es JH et al (2009) Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457:608–611

    PubMed  CAS  Google Scholar 

  80. Zhu L, Gibson P, Currle DS et al (2009) Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature 457:603–607

    PubMed  CAS  Google Scholar 

  81. Dalerba P, Dylla SJ, Park IK et al (2007) Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci U S A 104:10158–10163

    PubMed  CAS  Google Scholar 

  82. Ricci-Vitiani L, Lombardi DG, Pilozzi E et al (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445:111–115

    PubMed  CAS  Google Scholar 

  83. Hermann PC, Huber SL, Herrler T et al (2007) Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1:313–323

    PubMed  CAS  Google Scholar 

  84. Li C, Heidt DG, Dalerba P et al (2007) Identification of pancreatic cancer stem cells. Cancer Res 67:1030–1037

    PubMed  CAS  Google Scholar 

  85. Borovski T, Vermeulen L, Sprick MR et al (2009) One renegade cancer stem cell? Cell Cycle 8(6):803–808

    PubMed  CAS  Google Scholar 

  86. Mani SA, Guo W, Liao MJ et al (2008) The epithelial–mesenchymal transition generates cells with properties of stem cells. Cell 133:704–715

    PubMed  CAS  Google Scholar 

  87. Alison MR, Islam S (2009) Attributes of adult stem cells. J Pathol 217:144–160

    PubMed  CAS  Google Scholar 

  88. Vasiliou V, Nebert DW (2005) Analysis and update of the human aldehyde dehydrogenase (ALDH) gene family. Hum Genomics 2:138–143

    PubMed  CAS  Google Scholar 

  89. Dylla SJ, Beviglia L, Park IK et al (2008) Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS ONE 3:e2428

    PubMed  Google Scholar 

  90. Molofsky AV, He S, Bydon M et al (2005) Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways. Genes Dev 19:1432–1437

    PubMed  CAS  Google Scholar 

  91. Alison MR, Murphy G, Leedham S (2008) Stem cells and cancer: a deadly mix. Cell Tissue Res 331:109–124

    PubMed  Google Scholar 

  92. Mizrak D, Brittan M, Alison MR (2008) CD133: molecule of the moment. J Pathol 214:3–9

    PubMed  CAS  Google Scholar 

  93. Bauer N, Fonseca AV, Florek M et al (2008) New insights into the cell biology of hematopoietic progenitors by studying prominin-1 (CD133). Cells Tissues Organs 188:127–138

    PubMed  CAS  Google Scholar 

  94. Burkert J, Wright NA, Alison MR (2006) Stem cells and cancer: an intimate relationship. J Pathol 209:287–297

    PubMed  CAS  Google Scholar 

  95. Shmelkov SV, Butler JM, Hooper AT et al (2008) CD133 expression is not restricted to stem cells, and both CD133+ and CD133− metastatic colon cancer cells initiate tumors. J Clin Invest 118:2111–2120

    PubMed  CAS  Google Scholar 

  96. Ferlay J, Autier P, Boniol M et al (2007) Estimates of the cancer incidence and mortality in Europe in 2006. Ann Oncol 18:581–592

    PubMed  CAS  Google Scholar 

  97. Singh SK, Clarke ID, Terasaki M et al (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821–5828

    PubMed  CAS  Google Scholar 

  98. Goodell MA (2002) Multipotential stem cells and ‘side population’ cells. Cytotherapy 4:507–508

    PubMed  CAS  Google Scholar 

  99. Triel C, Vestergaard ME, Bolund L et al (2004) Side population cells in human and mouse epidermis lack stem cell characteristics. Exp Cell Res 295:79–90

    PubMed  CAS  Google Scholar 

  100. Haraguchi N, Utsunomiya T, Inoue H et al (2006) Characterization of a side population of cancer cells from human gastrointestinal system. Stem Cells 24:506–513

    PubMed  CAS  Google Scholar 

  101. Alison MR, Poulsom R, Brittan M et al (2006) Isolation of gut SP cells does not automatically enrich for stem cells. Gastroenterology 130:1012–1013 author reply 1013–1014

    PubMed  Google Scholar 

  102. Barker N, Ridgway RA, van Es JH et al (2008) Crypt stem cells as the cells-of-origin of intestinal cancer. Nature

  103. Preston SL, Wong WM, Chan AO et al (2003) Bottom-up histogenesis of colorectal adenomas: origin in the monocryptal adenoma and initial expansion by crypt fission. Cancer Res 63:3819–3825

    PubMed  CAS  Google Scholar 

  104. McClanahan T, Koseoglu S, Smith K et al (2006) Identification of overexpression of orphan G protein-coupled receptor GPR49 in human colon and ovarian primary tumors. Cancer Biol Ther 5:419–426

    Article  PubMed  CAS  Google Scholar 

  105. Carney DN, Gazdar AF, Bunn PA Jr et al (1982) Demonstration of the stem cell nature of clonogenic tumor cells from lung cancer patients. Stem Cells 1:149–164

    PubMed  CAS  Google Scholar 

  106. Chen YC, Hsu HS, Chen YW et al (2008) Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS ONE 3:e2637

    PubMed  Google Scholar 

  107. Eramo A, Lotti F, Sette G et al (2008) Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 15:504–514

    PubMed  CAS  Google Scholar 

  108. Levina V, Marrangoni AM, DeMarco R et al (2008) Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties. PLoS ONE 3:e3077

    PubMed  Google Scholar 

  109. Sung JM, Cho HJ, Yi H et al (2008) Characterization of a stem cell population in lung cancer A549 cells. Biochem Biophys Res Commun 371:163–167

    PubMed  CAS  Google Scholar 

  110. Ma S, Chan KW, Hu L et al (2007) Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology 132:2542–2556

    PubMed  CAS  Google Scholar 

  111. Ma S, Chan KW, Lee TK et al (2008) Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol Cancer Res 6:1146–1153

    PubMed  CAS  Google Scholar 

  112. Song W, Li H, Tao K et al (2008) Expression and clinical significance of the stem cell marker CD133 in hepatocellular carcinoma. Int J Clin Pract 62:1212–1218

    PubMed  CAS  Google Scholar 

  113. Ma S, Lee TK, Zheng BJ et al (2008) CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene 27:1749–1758

    PubMed  CAS  Google Scholar 

  114. Kelly PN, Dakic A, Adams JM et al (2007) Tumor growth need not be driven by rare cancer stem cells. Science 317:337

    PubMed  CAS  Google Scholar 

  115. Schatton T, Murphy GF, Frank NY et al (2008) Identification of cells initiating human melanomas. Nature 451:345–349

    PubMed  CAS  Google Scholar 

  116. Quintana E, Shackleton M, Sabel MS et al (2008) Efficient tumour formation by single human melanoma cells. Nature 456:593–598

    PubMed  CAS  Google Scholar 

  117. Yoo MH, Hatfield DL (2008) The cancer stem cell theory: is it correct? Mol Cells 26:514–516

    PubMed  CAS  Google Scholar 

  118. Yu Q, Su B, Liu D et al (2007) Antisense RNA-mediated suppression of Bmi-1 gene expression inhibits the proliferation of lung cancer cell line A549. Oligonucleotides 17:327–335

    PubMed  CAS  Google Scholar 

  119. Grosveld GC (2009) Gamma-secretase inhibitors: Notch so bad. Nat Med 15:20–21

    PubMed  CAS  Google Scholar 

  120. Subramanian J, Govindan R (2008) Small cell, big problem! Stem cells, root cause? Clin Lung Cancer 9:252–253

    PubMed  Google Scholar 

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Acknowledgement

SACM is funded by CORE (Formerly Digestive Disorders Foundation).

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We declare that we have no conflict of interest.

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Authors and Affiliations

  1. Centre for Gastroenterology, Institute of Cell and Molecular Science, Barts and the London School of Medicine and Dentistry, Blizard Building, 4 Newark Street, Whitechapel, London, E1 2AT, UK

    Stuart A. C. McDonald

  2. Histopathology Unit, Cancer Research UK, London Research Institute, London, UK

    Stuart A. C. McDonald, Trevor A. Graham, Stefanie Schier, Nicholas A. Wright & Malcolm R. Alison

  3. Centre for Diabetes, Institute of Cell and Molecular Science, Barts and the London School of Medicine and Dentistry, London, UK

    Malcolm R. Alison

  4. Institute of Cell and Molecular Science, Barts and the London School of Medicine and Dentistry, London, UK

    Nicholas A. Wright

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  1. Stuart A. C. McDonald
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Correspondence to Stuart A. C. McDonald.

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Stuart A. C. McDonald, Trevor A. Graham and Stefanie Schier contributed equally to this work.

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McDonald, S.A.C., Graham, T.A., Schier, S. et al. Stem cells and solid cancers. Virchows Arch 455, 1–13 (2009). https://doi.org/10.1007/s00428-009-0783-1

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