Oncogenic challenges in stem cells and the link to cancer initiation

Archives of Pharmacal Research

Volumn 35, Issue 2, 2012, Pages 235-244

  Lee, Ji Seon ^a   Bae, Gab Yong ^a   Lee, Mi Ok ^a   Cha, Hyuk Jin ^a  

^a Sogang University   (South Korea)

Author keywords

Cancer; Oncogenic challenge; Oncogenic susceptibility; Origin of cancer; Stem cells

Indexed keywords

CANCER STEM CELL; CELL DIFFERENTIATION; EWING SARCOMA; HEMATOPOIETIC STEM CELL; HUMAN; INTESTINE CANCER; LEUKEMIA; NONHUMAN; ONCOGENE; REVIEW; SKIN CANCER; ADULT STEM CELL; AGING; ANIMAL; BIOLOGICAL MODEL; CELL AGING; CELL TRANSFORMATION; METABOLISM; NEOPLASM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADULT STEM CELLS; AGING; ANIMALS; CELL AGING; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; MODELS, BIOLOGICAL; NEOPLASMS; NEOPLASTIC STEM CELLS;

EID: 84862640587     PISSN: 02536269     EISSN: 19763786     Source Type: Journal    
DOI: 10.1007/s12272-012-0204-x     Document Type: Review

References (92)

1. Alcantara Llaguno, S., Chen, J., Kwon, C., Jackson, E., Li, Y., Burns, D., Alvarez-Buylla, A., and Parada, L. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell, 15, 45-56 (2009).
2. Amariglio, N., Hirshberg, A., Scheithauer, B. W., Cohen, Y., Loewenthal, R., Trakhtenbrot, L., Paz, N., Koren-Michowitz, M., Waldman, D., Leider-Trejo, L., Toren, A., Constantini, S., and Rechavi, G. Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med., 6, e1000029 (2009).
3. Asai, T., Liu, Y., Bae, N., and Nimer, S. D. The p53 tumor suppressor protein regulates hematopoietic stem cell fate. J. Cell Physiol., DOI 10.1002/jcp.22561 (2010).
4. Bachoo, R. M., Maher, E. A., Ligon, K. L., Sharpless, N. E., Chan, S. S., You, M. J., Tang, Y., Defrances, J., Stover, E., Weissleder, R., Rowitch, D. H., Louis, D. N., and Depinho, R. A. Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. Cancer Cell, 1, 269-277 (2002).
5. Barker, N., Ridgway, R. A., Van Es, J. H., Van De Wetering, M., Begthel, H., Van Den Born, M., Danenberg, E., Clarke, A. R., Sansom, O. J., and Clevers, H. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature, 457, 608-611 (2009).
6. Barker, N., Huch, M., Kujala, P., Van De Wetering, M., Snippert, H. J., Van Es, J. H., Sato, T., Stange, D. E., Begthel, H., Van Den Born, M., Danenberg, E., Van Den Brink, S., Korving, J., Abo, A., Peters, P. J., Wright, N., Poulsom, R., and Clevers, H. Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem. Cell, 6, 25-36 (2010).
7. Bienz, M. and Clevers, H., Linking colorectal cancer to Wnt signaling. Cell, 103, 311-320 (2000).
8. Bleau, A. M., Hambardzumyan, D., Ozawa, T., Fomchenko, E. I., Huse, J. T., Brennan, C. W., and Holland, E. C., PTEN/ PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell, 4, 226-235 (2009).
9. Blum, B. and Benvenisty, N., The tumorigenicity of human embryonic stem cells. Adv. Cancer Res., 100, 133-158 (2008).
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, 730-737 (1997).
11. Bouras, T., Pal, B., Vaillant, F., Harburg, G., Asselin-Labat, M. L., Oakes, S. R., Lindeman, G. J., and Visvader, J. E., Notch signaling regulates mammary stem cell function and luminal cell-fate commitment. Cell Stem Cell, 3, 429-441 (2008).
12. Bruggeman, S. W., Valk-Lingbeek, M. E., Van Der Stoop, P. P., Jacobs, J. J., Kieboom, K., Tanger, E., Hulsman, D., Leung, C., Arsenijevic, Y., Marino, S., and Van Lohuizen, M., Ink4a and Arf differentially affect cell proliferation and neural stem cell self-renewal in Bmi1-deficient mice. Genes Dev., 19, 1438-1443 (2005).
13. Bruggeman, S. W., Hulsman, D., Tanger, E., Buckle, T., Blom, M., Zevenhoven, J., Van Tellingen, O., and Van Lohuizen, M., Bmi1 controls tumor development in an Ink4a/Arfindependent manner in a mouse model for glioma. Cancer Cell, 12, 328-341 (2007).
14. Campisi, J., Cancer and ageing: rival demons? Nat. Rev. Cancer, 3, 339-349 (2003).
15. Cha, H., Lowe, J. M., Li, H., Lee, J. S., Belova, G. I., Bulavin, D. V., and Fornace, A. J., Jr., Wip1 directly dephosphorylates gamma-H2AX and attenuates the DNA damage response. Cancer Res., 70, 4112-4122 (2010).
16. Chen, W., Kumar, A. R., Hudson, W. A., Li, Q., Wu, B., Staggs, R. A., Lund, E. A., Sam, T. N., and Kersey, J. H., Malignant transformation initiated by Mll-AF9: gene dosage and critical target cells. Cancer Cell, 13, 432-440 (2008).
17. Colmegna, I., Diaz-Borjon, A., Fujii, H., Schaefer, L., Goronzy, J. J., and Weyand, C. M., Defective proliferative capacity and accelerated telomeric loss of hematopoietic progenitor cells in rheumatoid arthritis. Arthritis Rheum., 58, 990-1000 (2008).
18. Demidov, O. N., Timofeev, O., Lwin, H. N., Kek, C., Appella, E., and Bulavin, D. V., Wip1 phosphatase regulates p53-dependent apoptosis of stem cells and tumorigenesis in the mouse intestine. Cell Stem Cell, 1, 180-190 (2007).
19. Dexter, D. L. and Calabresi, P., Intraneoplastic diversity. Biochim. Biophys. Acta, 695, 97-112 (1982).
20. Fialkow, P. J., Denman, A. M., Jacobson, R. J., and Lowenthal, M. N., Chronic myelocytic leukemia. Origin of some lymphocytes from leukemic stem cells. J. Clin. Invest., 62, 815-823 (1978).
21. Fidler, I. J. and Poste, G., The biologic diversity of cancer metastases. Hosp. Pract. (Off Ed), 17, 57-64 (1982).
22. Finkel, T., Serrano, M., and Blasco, M. A., The common biology of cancer and ageing. Nature, 448, 767-774 (2007).
23. Floor, S., Van Staveren, W. C., Larsimont, D., Dumont, J. E., and Maenhaut, C., Cancer cells in epithelial-to-mesenchymal transition and tumor-propagating-cancer stem cells: distinct, overlapping or same populations. Oncogene, 30, 4609-4621 (2011).
24. Gibson, P., Tong, Y., Robinson, G., Thompson, M. C., Currle, D. S., Eden, C., Kranenburg, T. A., Hogg, T., Poppleton, H., Martin, J., Finkelstein, D., Pounds, S., Weiss, A., Patay, Z., Scoggins, M., Ogg, R., Pei, Y., Yang, Z. J., Brun, S., Lee, Y., Zindy, F., Lindsey, J. C., Taketo, M. M., Boop, F. A., Sanford, R. A., Gajjar, A., Clifford, S. C., Roussel, M. F., Mckinnon, P. J., Gutmann, D. H., Ellison, D. W., Wechsler-Reya, R., and Gilbertson, R. J., Subtypes of medulloblastoma have distinct developmental origins. Nature, 468, 1095-1099 (2010).
25. Gidekel Friedlander, S. Y., Chu, G. C., Snyder, E. L., Girnius, N., Dibelius, G., Crowley, D., Vasile, E., Depinho, R. A., and Jacks, T., Context-dependent transformation of adult pancreatic cells by oncogenic K-Ras. Cancer Cell, 16, 379-389 (2009).
26. Goldstein, A. S., Huang, J., Guo, C., Garraway, I. P., and Witte, O. N., Identification of a cell of origin for human prostate cancer. Science, 329, 568-571 (2010).
27. Hahn, W. C. and Weinberg, R. A., Rules for making human tumor cells. N. Engl. J. Med., 347, 1593-1603 (2002).
28. Heppner, G. H., Tumor heterogeneity. Cancer Res., 44, 2259-2265 (1984).
29. Heuser, M., Yun, H., Berg, T., Yung, E., Argiropoulos, B., Kuchenbauer, F., Park, G., Hamwi, I., Palmqvist, L., Lai, C. K., Leung, M., Lin, G., Chaturvedi, A., Thakur, B. K., Iwasaki, M., Bilenky, M., Thiessen, N., Robertson, G., Hirst, M., Kent, D., Wilson, N. K., Gottgens, B., Eaves, C., Cleary, M. L., Marra, M., Ganser, A., and Humphries, R. K., Cell of origin in AML: susceptibility to MN1-induced transformation is regulated by the MEIS1/AbdB-like HOX protein complex. Cancer Cell, 20, 39-52 (2011).
30. Holland, E. C., Celestino, J., Dai, C., Schaefer, L., Sawaya, R. E., and Fuller, G. N., Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat. Genet., 25, 55-57 (2000).
31. Hope, K. J., Jin, L., and Dick, J. E., Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nat. Immunol., 5, 738-743 (2004).
32. Huntly, B. J., Shigematsu, H., Deguchi, K., Lee, B. H., Mizuno, S., Duclos, N., Rowan, R., Amaral, S., Curley, D., Williams, I. R., Akashi, K., and Gilliland, D. G., MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell, 6, 587-596 (2004).
33. Jacques, T. S., Swales, A., Brzozowski, M. J., Henriquez, N. V., Linehan, J. M., Mirzadeh, Z., C, O. M., Naumann, H., Alvarez-Buylla, A., and Brandner, S., Combinations of genetic mutations in the adult neural stem cell compartment determine brain tumour phenotypes. EMBO J., 29, 222-235 (2010).
34. Johnson, A. D., Pambuccian, S. E., Andrade, R. S., Dolan, M. M., and Aslan, D. L., Ewing sarcoma and primitive neuroectodermal tumor of the esophagus: report of a case and review of literature. Int. J. Surg. Pathol., 18, 388-393 (2010).
35. Kelly, P. N., Dakic, A., Adams, J. M., Nutt, S. L., and Strasser, A., Tumor growth need not be driven by rare cancer stem cells. Science, 317, 337 (2007).
36. Kim, C. F., Jackson, E. L., Woolfenden, A. E., Lawrence, S., Babar, I., Vogel, S., Crowley, D., Bronson, R. T., and Jacks, T., Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell, 121, 823-835 (2005).
37. Korsten, H., Ziel-Van Der Made, A., Ma, X., Van Der Kwast, T., and Trapman, J., Accumulating progenitor cells in the luminal epithelial cell layer are candidate tumor initiating cells in a Pten knockout mouse prostate cancer model. PLoS ONE, 4, e5662 (2009).
38. Kuhn, H., Dickinson-Anson, H., and Gage, F., Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci., 16, 2027-2033 (1996).
39. Lawson, D. A., Zong, Y., Memarzadeh, S., Xin, L., Huang, J., and Witte, O. N., Basal epithelial stem cells are efficient targets for prostate cancer initiation. Proc. Natl. Acad. Sci. U. S. A., 107, 2610-2615 (2010).
40. Le Guezennec, X. and Bulavin, D. V., WIP1 phosphatase at the crossroads of cancer and aging. Trends Biochem. Sci., 35, 109-114 (2009).
41. Lee, J. S., Lee, M. O., Moon, B. H., Shim, S. H., Fornace, A. J., Jr., and Cha, H. J., Senescent growth arrest in mesenchymal stem cells is bypassed by Wip1-mediated downregulation of intrinsic stress signaling pathways. Stem Cells, 27, 1963-1975 (2009).
42. Lee, J. S., Lee, H. J., Moon, B. H., Song, S. H., Lee, M. O., Shim, S. H., Kim, H. S., Lee, M. C., Kwon, J. T., Fornace, A. J., Jr., Kim, S. U., and Cha, H. J., Generation of cancerous neural stem cells forming glial tumor by oncogenic stimulation. Stem Cell Rev., DOI 10.1007/s12015-011-9280-4 (2011a).
43. Lee, M. O., Lee, H. J., Kim, M. A., Kim, E. K., Lee, J. H., Heo, J. H., Lee, S. H., Cho, S. H., Fornace, A. J., Jr., Jeong, H. C., and Cha, H. J., p16Ink4a suppression of lung adenocarcinoma by Bmi-1 in the presence of p38 activation. J. Thorac. Oncol., 6, 423-431 (2011b).
44. Li, L. and Neaves, W. B., Normal stem cells and cancer stem cells: the niche matters. Cancer Res., 66, 4553-4557 (2006).
45. Lim, E., Vaillant, F., Wu, D., Forrest, N. C., Pal, B., Hart, A. H., Asselin-Labat, M. L., Gyorki, D. E., Ward, T., Partanen, A., Feleppa, F., Huschtscha, L. I., Thorne, H. J., Kconfab, Fox, S. B., Yan, M., French, J. D., Brown, M. A., Smyth, G. K., Visvader, J. E., and Lindeman, G. J., Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat. Med., 15, 907-913 (2009).
46. Lin, T., Chao, C., Saito, S., Mazur, S. J., Murphy, M. E., Appella, E., and Xu, Y., p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat. Cell Biol., 7, 165-171 (2005).
47. Lindberg, N., Kastemar, M., Olofsson, T., Smits, A., and Uhrbom, L., Oligodendrocyte progenitor cells can act as cell of origin for experimental glioma. Oncogene, 28, 2266-2275 (2009).
48. Ma, X., Ziel-Van Der Made, A. C., Autar, B., Van Der Korput, H. A., Vermeij, M., Van Duijn, P., Cleutjens, K. B., De Krijger, R., Krimpenfort, P., Berns, A., Van Der Kwast, T. H., and Trapman, J., Targeted biallelic inactivation of Pten in the mouse prostate leads to prostate cancer accompanied by increased epithelial cell proliferation but not by reduced apoptosis. Cancer Res., 65, 5730-5739 (2005).
49. Mani, S. A., Guo, W., Liao, M. J., Eaton, E. N., Ayyanan, A., Zhou, A. Y., Brooks, M., Reinhard, F., Zhang, C. C., Shipitsin, M., Campbell, L. L., Polyak, K., Brisken, C., Yang, J., and Weinberg, R. A., The epithelial- mesenchymal transition generates cells with properties of stem cells. Cell, 133, 704-715 (2008).
50. Marumoto, T., Tashiro, A., Friedmann-Morvinski, D., Scadeng, M., Soda, Y., Gage, F. H., and Verma, I. M., Development of a novel mouse glioma model using lentiviral vectors. Nat. Med., 15, 110-116 (2009).
51. Meletis, K., Wirta, V., Hede, S. M., Nister, M., Lundeberg, J., and Frisen, J., p53 suppresses the self-renewal of adult neural stem cells. Development, 133, 363-369 (2006).
52. Miyagawa, Y., Okita, H., Nakaijima, H., Horiuchi, Y., Sato, B., Taguchi, T., Toyoda, M., Katagiri, Y. U., Fujimoto, J., Hata, J., Umezawa, A., and Kiyokawa, N., Inducible expression of chimeric EWS/ETS proteins confers Ewing's family tumor-like phenotypes to human mesenchymal progenitor cells. Mol. Cell Biol., 28, 2125-2137 (2008).
53. Molofsky, A., Pardal, R., Iwashita, T., Park, I., Clarke, M., and Morrison, S., Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature, 425, 962-967 (2003).
54. Molofsky, A., He, S., Bydon, M., Morrison, S., and Pardal, R., 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 (2005).
55. Molofsky, A., Slutsky, S., Joseph, N., He, S., Pardal, R., Krishnamurthy, J., Sharpless, N., and Morrison, S., Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature, 443, 448-452 (2006).
56. Molyneux, G., Geyer, F. C., Magnay, F. A., Mccarthy, A., Kendrick, H., Natrajan, R., Mackay, A., Grigoriadis, A., Tutt, A., Ashworth, A., Reis-Filho, J. S., and Smalley, M. J., BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell Stem Cell, 7, 403-417 (2010).
57. Moon, R. T. and Miller, J. R., The APC tumor suppressor protein in development and cancer. Trends Genet., 13, 256-258 (1997).
58. Mulholland, D. J., Xin, L., Morim, A., Lawson, D., Witte, O., and Wu, H., Lin-Sca-1+CD49fhigh stem/progenitors are tumor-initiating cells in the Pten-null prostate cancer model. Cancer Res., 69, 8555-8562 (2009).
59. Oliveras, A., Soler, M. J., Martinez-Estrada, O. M., Vazquez, S., Marco-Feliu, D., Vila, J. S., Vilaro, S., and Lloveras, J., Endothelial progenitor cells are reduced in refractory hypertension. J. Hum. Hypertens, 22, 183-190 (2008).
60. Park, I. K., Qian, D., Kiel, M., Becker, M. W., Pihalja, M., Weissman, I. L., Morrison, S. J., and Clarke, M. F., Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature, 423, 302-305 (2003).
61. Polyak, K. and Weinberg, R. A., Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat. Rev. Cancer, 9, 265-273 (2009).
62. Quintana, E., Shackleton, M., Sabel, M. S., Fullen, D. R., Johnson, T. M., and Morrison, S. J., Efficient tumour formation by single human melanoma cells. Nature, 456, 593-598 (2008).
63. Rando, T. A., The immortal strand hypothesis: segregation and reconstruction. Cell, 129, 1239-1243 (2007).
64. Rich, J. N., Guo, C., Mclendon, R. E., Bigner, D. D., Wang, X. F., and Counter, C. M., A genetically tractable model of human glioma formation. Cancer Res., 61, 3556-3560 (2001).
65. Riggi, N., Cironi, L., Provero, P., Suva, M. L., Kaloulis, K., Garcia-Echeverria, C., Hoffmann, F., Trumpp, A., and Stamenkovic, I., Development of Ewing's sarcoma from primary bone marrow-derived mesenchymal progenitor cells. Cancer Res., 65, 11459-11468 (2005).
66. Riggi, N., Suva, M. L., De Vito, C., Provero, P., Stehle, J. C., Baumer, K., Cironi, L., Janiszewska, M., Petricevic, T., Suva, D., Tercier, S., Joseph, J. M., Guillou, L., and Stamenkovic, I., EWS-FLI-1 modulates miRNA145 and SOX2 expression to initiate mesenchymal stem cell reprogramming toward Ewing sarcoma cancer stem cells. Genes Dev., 24, 916-932 (2010).
67. Riis, M. L., Luders, T., Nesbakken, A. J., Vollan, H. S., Kristensen, V., and Bukholm, I. R., Expression of BMI-1 and Mel-18 in breast tissue-A diagnostic marker in patients with breast cancer. BMC Cancer, 10, 686 (2010).
68. Rossi, D. J., Jamieson, C. H., and Weissman, I. L., Stems cells and the pathways to aging and cancer. Cell, 132, 681-696 (2008).
69. Rosso, A., Balsamo, A., Gambino, R., Dentelli, P., Falcioni, R., Cassader, M., Pegoraro, L., Pagano, G., and Brizzi, M. F., p53 Mediates the accelerated onset of senescence of endothelial progenitor cells in diabetes. J. Biol. Chem., 281, 4339-4347 (2006).
70. Ruzankina, Y., Pinzon-Guzman, C., Asare, A., Ong, T., Pontano, L., Cotsarelis, G., Zediak, V. P., Velez, M., Bhandoola, A., and Brown, E. J., Deletion of the developmentally essential gene ATR in adult mice leads to age-related phenotypes and stem cell loss. Cell Stem Cell, 1, 113-126 (2007).
71. Sahin, E. and Depinho, R. A., Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature, 464, 520-528 (2010).
72. Sanai, N., Alvarez-Buylla, A., and Berger, M. S., Neural stem cells and the origin of gliomas. N. Engl. J. Med., 353, 811-822 (2005).
73. Sangiorgi, E. and Capecchi, M. R., Bmi1 is expressed in vivo in intestinal stem cells. Nat. Genet., 40, 915-920 (2008).
74. Scadden, D. T., The stem-cell niche as an entity of action. Nature, 441, 1075-1079 (2006).
75. Schuller, U., Heine, V. M., Mao, J., Kho, A. T., Dillon, A. K., Han, Y. G., Huillard, E., Sun, T., Ligon, A. H., Qian, Y., Ma, Q., Alvarez-Buylla, A., Mcmahon, A. P., Rowitch, D. H., and Ligon, K. L., Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell, 14, 123-134 (2008).
76. Sharpless, N. and Depinho, R., How stem cells age and why this makes us grow old. Nat. Rev. Mol. Cell Biol., 8, 703-713 (2007).
77. Sherr, C. J., The INK4a/ARF network in tumour suppression. Nat. Rev. Mol. Cell Biol., 2, 731-737 (2001).
78. Shibata, K. R., Aoyama, T., Shima, Y., Fukiage, K., Otsuka, S., Furu, M., Kohno, Y., Ito, K., Fujibayashi, S., Neo, M., Nakayama, T., Nakamura, T., and Toguchida, J., Expression of the p16INK4A gene is associated closely with senescence of human mesenchymal stem cells and is potentially silenced by DNA methylation during in vitro expansion. Stem Cells, 25, 2371-2382 (2007).
79. So, C. W., Karsunky, H., Passegue, E., Cozzio, A., Weissman, I. L., and Cleary, M. L., MLL-GAS7 transforms multipotent hematopoietic progenitors and induces mixed lineage leukemias in mice. Cancer Cell, 3, 161-171 (2003).
80. Sutter, R., Shakhova, O., Bhagat, H., Behesti, H., Sutter, C., Penkar, S., Santuccione, A., Bernays, R., Heppner, F. L., Schuller, U., Grotzer, M., Moch, H., Schraml, P., and Marino, S., Cerebellar stem cells act as medulloblastomainitiating cells in a mouse model and a neural stem cell signature characterizes a subset of human medulloblastomas. Oncogene, 29, 1845-1856 (2010).
81. Tirode, F., Laud-Duval, K., Prieur, A., Delorme, B., Charbord, P., and Delattre, O., Mesenchymal stem cell features of Ewing tumors. Cancer Cell, 11, 421-429 (2007).
82. Vermeulen, L., Sprick, M. R., Kemper, K., Stassi, G., and Medema, J. P., Cancer stem cells-old concepts, new insights. Cell Death Differ., 15, 947-958 (2008).
83. Villeda, S. A., Luo, J., Mosher, K. I., Zou, B., Britschgi, M., Bieri, G., Stan, T. M., Fainberg, N., Ding, Z., Eggel, A., Lucin, K. M., Czirr, E., Park, J. S., Couillard-Despres, S., Aigner, L., Li, G., Peskind, E. R., Kaye, J. A., Quinn, J. F., Galasko, D. R., Xie, X. S., Rando, T. A., and Wyss-Coray, T., The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature, 477, 90-94 (2011).
84. Visvader, J. E. and Lindeman, G. J., Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat. Rev. Cancer, 8, 755-768 (2008).
85. Vonlanthen, S., Heighway, J., Altermatt, H. J., Gugger, M., Kappeler, A., Borner, M. M., Van Lohuizen, M., and Betticher, D. C., The bmi-1 oncoprotein is differentially expressed in non-small cell lung cancer and correlates with INK4A-ARF locus expression. Br. J. Cancer, 84, 1372-1376 (2001).
86. Wang, X., Kruithof-De Julio, M., Economides, K. D., Walker, D., Yu, H., Halili, M. V., Hu, Y. P., Price, S. M., Abate-Shen, C., and Shen, M. M., A luminal epithelial stem cell that is a cell of origin for prostate cancer. Nature, 461, 495-500 (2009).
87. Warner, J., Wang, J., Hope, K., Jin, L., and Dick, J., Concepts of human leukemic development. Oncogene, 23, 7164-7177 (2004).
88. Wong, E., Le Guezennec, X., Demidov, O., Marshall, N., Wang, S., Krishnamurthy, J., Sharpless, N., Dunn, N., and Bulavin, D., p38MAPK controls expression of multiple cell cycle inhibitors and islet proliferation with advancing age. Dev. Cell, 17, 142-149 (2009).
89. Xu, N., Papagiannakopoulos, T., Pan, G., Thomson, J. A., and Kosik, K. S., MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell, 137, 647-658 (2009).
90. Youssef, K. K., Van Keymeulen, A., Lapouge, G., Beck, B., Michaux, C., Achouri, Y., Sotiropoulou, P. A., and Blanpain, C., Identification of the cell lineage at the origin of basal cell carcinoma. Nat. Cell Biol., 12, 299-305 (2010).
91. Zhu, L., Gibson, P., Currle, D. S., Tong, Y., Richardson, R. J., Bayazitov, I. T., Poppleton, H., Zakharenko, S., Ellison, D. W., and Gilbertson, R. J., Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature, 457, 603-607 (2009a).
92. Zhu, Y., Zhang, C., Lu, L., Demidov, O., Sun, L., Yang, L., Bulavin, D., and Xiao, Z., Wip1 regulates the generation of new neural cells in the adult olfactory bulb through p53-dependent cell cycle control. Stem Cells, 27, 1433-1442 (2009b).