Stem cell plasticity and tumour formation

European Journal of Cancer

Volumn 42, Issue 9, 2006, Pages 1247-1256

  Alison, Malcolm R ^a,b   Lovell, Matthew J ^b   Direkze, Natalie C ^b   Wright, Nicholas A ^b   Poulsom, Richard ^b  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Cell fusion; Desmoplasia; Endothelial progenitor cells; Haematopoietic stem cells; Mesenchymal stem cells; Myofibroblasts; Neovascularisation; Transdifferentiation; Tumour stroma

Indexed keywords

ARTICLE; BONE MARROW CELL; CANCER STEM CELL; CARCINOGENESIS; CELL FUSION; CELL REGENERATION; CELL TYPE; HUMAN; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PARENCHYMA; PRIORITY JOURNAL;

ANIMALS; BONE MARROW CELLS; CELL FUSION; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; MICE; NEOPLASMS; STEM CELLS;

EID: 33646945621     PISSN: 09598049     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejca.2006.01.034     Document Type: Article

References (95)

1. Sanai N., Tramontin A.D., Quinones-Hinojosa A., et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427 (2004) 740-744
2. Beltrami A.P., Barlucchi L., Torella D., et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114 (2003) 763-776
3. Silberg D.G., Sullivan J., and Kang E. Cdx2 ectopic expression induces gastric intestinal metaplasia in transgenic mice. Gastroenterology 122 (2002) 689-696
4. Beck F., Chawengsaksophak K., Luckett J., et al. A study of regional gut endoderm potency by analysis of Cdx2 null mutant chimaeric mice. Dev Biol 255 (2003) 399-406
5. Hashimoto N., Jin H., Liu T., Chensue S.W., and Phan S.H. Bone marrow-derived progenitor cells in pulmonary fibrosis. J Clin Invest 113 (2004) 243-252
6. Forbes S.J., Russo F.P., Rey V., et al. A significant proportion of myofibroblasts are of bone marrow origin in human liver fibrosis. Gastroenterology 126 (2004) 955-963
7. Direkze N.C., Hodivala-Dilke K., Jeffery R., et al. Bone marrow contribution to tumor-associated myofibroblasts and fibroblasts. Cancer Res 64 (2004) 8942-8945
8. Stenback F., Peto R., and Shubik P. Initiation and promotion at different ages and doses in 2200 mice. I. Methods, and the apparent persistence of initiated cells. Br J Cancer 44 (1981) 1-14
9. Reya T., Morrison S.J., Clarke M.F., and Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 414 (2001) 105-111
10. Bonnet D., and Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3 (1997) 730-737
11. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., and Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100 (2003) 3983-3988
12. Singh S.K., Clarke I.D., Terasaki M., et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 63 (2003) 5821-5828
13. Singh S.K., Hawkins C., Clarke I.D., et al. Identification of human brain tumour initiating cells. Nature 432 (2004) 396-401
14. Alison M.R., Poulsom R., Otto W.R., et al. Recipes for adult stem cell plasticity: fusion cuisine or readymade?. J Clin Path 57 (2004) 113-120
15. Tran S.D., Pillemer S.R., Dutra A., et al. Differentiation of human bone marrow-derived cells into buccal epithelial cells in vivo: a molecular analytical study. Lancet 361 (2003) 1084-1088
16. Ianus A., Holz G.G., Theise N.D., et al. In vivo derivation of glucose-competent pancreatic endocrine cells from bone marrow without evidence of cell fusion. J Clin Invest 111 (2003) 843-850
17. Lagasse E., Connors H., Al-Dhalimy M., et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nature Med 6 (2000) 1229-1234
18. Wang X., Willenbring H., Akkari Y., et al. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 422 (2003) 897-901
19. Willenbring H., Bailey A.S., Foster M., et al. Myelomonocytic cells are sufficient for therapeutic cell fusion in liver. Nat Med 10 (2004) 744-748
20. Camargo F.D., Finegold M., and Goodell M.A. Hematopoietic myelomonocytic cells are the major source of hepatocyte fusion partners. J Clin Invest 113 (2004) 1266-1270
21. Alvarez-Dolado M., Pardal R., Garcia-Verdugo J.M., et al. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425 (2003) 968-973
22. Harris R.G., Herzog E.L., Bruscia E.M., Grove J.E., Van Arnam J.S., and Krause D.S. Lack of a fusion requirement for development of bone marrow-derived epithelia. Science 305 (2004) 90-93
23. Shen C.N., Slack J.M., and Tosh D. Molecular basis of transdifferentiation of pancreas to liver. Nat Cell Biol 2 (2000) 879-887
24. Jang Y.Y., Collector M.I., Baylin S.B., Diehl A.M., and Sharkis S.J. Hematopoietic stem cells convert into liver cells within days without fusion. Nat Cell Biol 6 (2004) 532-539
25. Bjornson C., Rietze R., Reynolds B., et al. Turning brain into blood: a hematopoietic fate adopted by neural stem cells in vivo. Science 283 (1999) 534-537
26. Morshead C.M., Benveniste P., Iscove N.N., et al. Hematopoietic competence is a rare property of neural stem cells that may depend on genetic and epigenetic alterations. Nat Med 8 (2002) 268-273
27. Alison M.R., Vig P., Russo F., et al. Hepatic stem cells: from inside and outside the liver?. Cell Prolif 37 (2004) 1-21
28. Orlic D., Kajstura J., Chimenti S., et al. Bone marrow cells regenerate infarcted myocardium. Nature 410 (2001) 701-704
29. Murry C.E., Soonpaa M.H., Reinecke H., et al. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428 (2004) 664-668
30. Balsam L.B., Wagers A.J., Christensen J.L., Kofidis T., Weissman I.L., and Robbins R.C. Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature 428 (2004) 668-673
31. Kajstura J., Rota M., Whang B., et al. Bone marrow cells differentiate in cardiac cell lineages after infarction independently of cell fusion. Circ Res 96 (2005) 127-137
32. Perin E.C., Dohmann H.F., Borojevic R., et al. Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation 107 (2003) 2294-2302
33. Wollert K.C., Meyer G.P., Lotz J., et al. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet 364 (2004) 141-148
34. Hess D., Li L., Martin M., et al. Bone marrow-derived stem cells initiate pancreatic regeneration. Nat Biotechnol 21 (2003) 763-770
35. Mezey E., Chandross K., Harta G., et al. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 290 (2000) 1779-1782
36. Mezey E., Key S., Vogelsang G., et al. Transplanted bone marrow generates new neurons in human brains. Proc Natl Acad Sci USA 100 (2003) 1364-1369
37. Castro R.F., Jackson K.A., Goodell M.A., et al. Failure of bone marrow cells to transdifferentiate into neural cells in vivo. Science 297 (2002) 1299
38. Mezey E., Nagy A., Szalayova I., et al. Comment on 'Failure of bone marrow cells to transdifferentiate into neural cells in vivo'. Science 299 (2003) 1184 [author reply 1184]
39. Massengale M., Wagers A.J., Vogel H., and Weissman I.L. Hematopoietic cells maintain hematopoietic fates upon entering the brain. J Exp Med 201 (2005) 1579-1589
40. Bonilla S., Silva A., Valdes L., Geijo E., Garcia-Verdugo J.M., and Martinez S. Functional neural stem cells derived from adult bone marrow. Neuroscience 133 (2005) 85-95
41. Rabb H. Paracrine and differentiation mechanisms underlying stem cell therapy for the damaged kidney. Am J Physiol Renal Physiol 289 (2005) F29-F30
42. Ritz E. Amelioration of acute renal failure by stem cell therapy - paracrine secretion versus transdifferentiation into resident cells. J Am Soc Nephrol 16 (2005) 1153-1155
43. Morigi M., Imberti B., Zoja C., et al. Mesenchymal stem cells are renotropic, helping to repair the kidney and improve function in acute renal failure. J Am Soc Nephrol 15 (2004) 1794-1804
44. Togel F., Hu Z., Weiss K., Isaac J., Lange C., and Westenfelder C. Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol 289 (2005) F31-F42
45. Fang T.-C., Alison M.R., Cook H.T., Jeffery R., Wright N.A., and Poulsom R. Proliferation of bone marrow-derived cells contributes to regeneration after folic acid-induced acute tubular injury. J Am Soc Nephrol 16 (2005) 1723-1732
46. Krause D.S., Theise N.D., Collector M.I., et al. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 105 (2001) 369-377
47. Wagers A.M., Sherwood R.I., Christensen J.L., et al. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297 (2002) 2256-2259
48. Korbling M., Katz R.L., Khanna A., et al. Hepatocytes and epithelial cells of donor origin in recipients of peripheral-blood stem cells. New Engl J Med 346 (2002) 738-746
49. Okamoto R., Yajima T., Yamazaki M., et al. Damaged epithelia regenerated by bone marrow-derived cells in the human gastrointestinal tract. Nat Med 8 (2002) 1011-1017
50. Matsumoto T., Okamoto R., Yajima T., et al. Increase of bone marrow-derived secretory lineage epithelial cells during regeneration in the human intestine. Gastroenterology 128 (2005) 1851-1867
51. Borue X., Lee S., Grove J., et al. Bone marrow-derived cells contribute to epithelial engraftment during wound healing. Am J Pathol 165 (2004) 1767-1772
52. Brittan M., Braun K.M., Reynolds L.E., et al. Bone marrow cells engraft within the epidermis and proliferate in vivo with no evidence of cell fusion. J Path 205 (2005) 1-13
53. Houghton J., and Wang T.C. Helicobacter pylori and gastric cancer: a new paradigm for inflammation-associated epithelial cancers. Gastroenterology 128 (2005) 1567-1578
54. Houghton J., Stoicov C., Nomura S., et al. Gastric cancer originating from bone marrow-derived cells. Science 306 (2004) 1568-1571
55. Aractingi S., Kanitakis J., Euvrard S., et al. Skin carcinoma arising from donor cells in a kidney transplant recipient. Cancer Res 65 (2005) 1755-1760
56. Ogle B.M., Cascalho M., and Platt J.L. Biological implications of cell fusion. Nature Reviews Mol Cell Biol 6 (2005) 567-574
57. Iwami Y., Masuda H., and Asahara T. Endothelial progenitor cells: past, state of the art, and future. J Cell Mol Med 8 (2004) 488-497
58. Hristov M., and Weber C. Endothelial progenitor cells: characterization, pathophysiology, and possible clinical relevance. J Cell Mol Med 8 (2004) 498-508
59. Khakoo A.Y., and Finkel T. Endothelial progenitor cells. Annu Rev Med 56 (2005) 79-101
60. Davidoff A.M., Ng C.Y., Brown P., et al. Bone marrow-derived cells contribute to tumor neovasculature and, when modified to express an angiogenesis inhibitor, can restrict tumor growth in mice. Clin Cancer Res 7 (2001) 2870-2879
61. Dwenger A., Rosenthal F., Machein M., Waller C., and Spyridonidis A. Transplanted bone marrow cells preferentially home to the vessels of in situ generated murine tumors rather than of normal organs. Stem Cells 22 (2004) 86-92
62. Peters B.A., Diaz L.A., Polyak K., et al. Contribution of bone marrow-derived endothelial cells to human tumor vasculature. Nat Med 11 (2005) 261-262
63. Powell D.W., Mifflin R.C., Valentich J.D., Crowe S.E., Saada J.I., and West A.B. Myofibroblasts. I. Paracrine cells important in health and disease. Am J Physiol 277 (1999) C1-C9
64. Direkze N.C., Forbes S.J., Brittan M., et al. Multiple organ engraftment by bone-marrow-derived myofibroblasts and fibroblasts in bone-marrow transplanted mice. Stem Cells 21 (2003) 514-520
65. Mori L., Bellini A., Stacey M.A., Schmidt M., and Mattoli S. Fibrocytes contribute to the myofibroblast population in wounded skin and originate from the bone marrow. Exp Cell Res 304 (2005) 81-90
66. Epperly M.W., Guo H., Gretton J.E., and Greenberger J.S. Bone marrow origin of myofibroblasts in irradiation pulmonary fibrosis. Am J Respir Cell Mol Biol 29 (2003) 213-224
67. Brittan M., Chance V., Elia G., et al. A regenerative role for bone marrow following experimental colitis: contribution to neovasculogenesis and myofibroblasts. Gastroenterology 128 (2005) 1984-1995
68. Brittan M., Hunt T., Jeffery R., et al. Bone marrow derivation of pericryptal myofibroblasts in the mouse and human small intestine and colon. Gut 50 (2002) 752-757
69. Ishii G., Sangai T., et al. Bone-marrow-derived myofibroblasts contribute to the cancer-induced stromal reaction. Biochem Biophys Res Commun 309 (2003) 232-240
70. Sangai T., Ishii G., Kodama K., et al. Effect of differences in cancer cells and tumor growth sites on recruiting bone marrow-derived endothelial cells and myofibroblasts in cancer-induced stroma. Int J Cancer 115 (2005) 885-892
71. Prockop D.J. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276 (1997) 71-74
72. Abe R., Donnelly S.C., Peng T., Bucala R., and Metz C. Peripheral blood fibrocytes: differentiation pathway and migration to wound sites. J Immunol 166 (2001) 7556-7562
73. Neaud V., Faouzi S., Guirouilh J., et al. Human hepatic myofibroblasts increase invasiveness of hepatocellular carcinoma cells: evidence for a role of hepatocyte growth factor. Hepatology 26 (1997) 1458-1466
74. von Schweinitz D., Faundez A., Teichmann B., et al. Hepatocyte growth-factor-scatter factor can stimulate post-operative tumor-cell proliferation in childhood hepatoblastoma. Int J Cancer 85 (2000) 151-159
75. Ohuchida K., Mizumoto K., Murakami M., et al. Radiation to stromal fibroblasts increases invasiveness of pancreatic cancer cells through tumor stromal interactions. Cancer Res 64 (2004) 3215-3222
76. Ng I.O., Lai E.C., Ng M.M., and Fan S.T. Tumor encapsulation in hepatocellular carcinoma. A pathologic study of 189 cases. Cancer 70 (1992) 45-49
77. Ayala G., Tuxhorn J.A., Wheeler T.M., et al. Reactive stroma as a predictor of biochemical-free recurrence in prostate cancer. Clin Cancer Res 9 (2003) 4792-4801
78. Ioachim E., Michael M., Stavropoulos N.E., Kitsiou E., Salmas M., and Malamou Mitsi V. A clinicopathological study of the expression of extracellular matrix components in urothelial carcinoma. BJU Int 95 (2005) 655-659
79. Poulsom R., Hanby A.M., Pignatelli M., et al. Expression of gelatinase A and TIMP-2 mRNAs in desmoplastic fibroblasts in both mammary carcinomas and basal cell carcinomas of the skin. J Clin Pathol 46 (1993) 429-436
80. Poulsom R., Pignatelli M., Stetler-Stevenson W.G., et al. Stromal expression of 72 kda type IV collagenase (MMP-2) and TIMP-2 mRNAs in colorectal neoplasia. Am J Pathol 141 (1992) 389-396
81. Studeny M., Marini F.C., Champlin R.E., Zompetta C., Fidler I.J., and Andreeff M. Bone marrow-derived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors. Cancer Res 62 (2002) 3603-3608
82. Studeny M., Marini F.C., Dembinski J.L., et al. Mesenchymal stem cells: potential precursors for tumor stroma and targeted-delivery vehicles for anticancer agents. J Natl Cancer Inst 96 (2004) 1593-1603
83. Desmouliere A., Guyot C., and Gabbiani G. The stroma reaction myofibroblast: a key player in the control of tumor cell behavior. Int J Dev Biol 48 (2004) 509-517
84. Kogler G., Sensken S., Airey J.A., et al. A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J Exp Med 200 (2004) 123-135
85. Mitchell K.E., Weiss M.L., Mitchell B.M., et al. Matrix cells from Wharton's jelly form neurons and glia. Stem Cells 21 (2003) 50-60
86. Jiang Y., Jahagirdar B.N., Reinhardt R.L., et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418 (2002) 41-49
87. Kucia M., Ratajczak J., and Ratajczak M.Z. Are bone marrow stem cells plastic or heterogenous - that is the question. Exp Hematol 33 (2005) 613-623
88. Kucia M., Reca R., Jala V.R., Dawn B., Ratajczak J., and Ratajczak M.Z. Bone marrow as a home of heterogenous populations of nonhematopoietic stem cells. Leukemia 19 (2005) 1118-1127
89. Cao Y., Sun Z., Liao L., Meng Y., Han Q., and Zhao R.C. Human adipose tissue-derived stem cells differentiate into endothelial cells in vitro and improve postnatal neovascularization in vivo. Biochem Biophys Res Commun 332 (2005) 370-379
90. Fernandes K.J., McKenzie I.A., Mill P., et al. A dermal niche for multipotent adult skin-derived precursor cells. Nat Cell Biol 6 (2004) 1082-1093
91. Prindull G., and Zipori D. Environmental guidance of normal and tumour cell plasticity: epithelial mesenchymal transitions as a paradigm. Blood 103 (2004) 2892-2899
92. Thompson E.W., Newgreen D.F., and Tarin D. Carcinoma invasion and metastasis: a role for epithelial-mesenchymal transition. Cancer Res 65 (2005) 5991-5995
93. Ahmad A., Hanby A.M., Dublin E.A., et al. Stromelysin 3: an independent prognostic factor for relapse-free survival in node-positive breast cancer and demonstration of novel breast carcinoma cell expression. Am J Pathol 152 (1998) 721-728
94. Tarin D., Thompson E.W., and Newgreen D.F. The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res 65 (2005) 5996-6000 [discussion 6000-1]
95. Johnson J., Bagley J., Skaznik-Wikiel M., et al. Oocyte generation in adult Mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell 122 (2005) 303-315