Quiescent, slow-cycling stem cell populations in cancer: A review of the evidence and discussion of significance

Journal of Oncology

Volumn , Issue , 2011, Pages

  Lyle, Stephen ^a   Moore, Nathan ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER RECURRENCE; CANCER RESISTANCE; CANCER STEM CELL; CELL CYCLE REGULATION; CELL ISOLATION; CELL LABELING; CELL MATURATION; CELL POPULATION; HUMAN; NONHUMAN; REVIEW;

EID: 78349252704     PISSN: 16878450     EISSN: 16878469     Source Type: Journal    
DOI: 10.1155/2011/396076     Document Type: Review

References (85)

1. Hanahan D., Weinberg R. A., The hallmarks of cancer Cell 2000 100 1 57 70
2. Blanpain C., Fuchs E., Epidermal homeostasis: a balancing act of stem cells in the skin Nature Reviews Molecular Cell Biology 2009 10 3 207 217
3. Kangsamaksin T., Heui J. P., Trempus C. S., Morris R. J., A perspective on murine keratinocyte stem cells as targets of chemically induced skin cancer Molecular Carcinogenesis 2007 46 8 579 584
4. Dean M., Cancer stem cells: redefining the paradigm of cancer treatment strategies Molecular Interventions 2006 6 3 140 148
5. Woodward W. A., Chen M. S., Behbod F., Rosen J. M., On mammary stem cells Journal of Cell Science 2005 118, part 16 3585 3594
6. Ricci-Vitiani L., Fabrizi E., Palio E., De Maria R., Colon cancer stem cells Journal of Molecular Medicine 2009 87 11 1097 1104
7. Reya T., Morrison S. J., Clarke M. F., Weissman I. L., Stem cells, cancer, and cancer stem cells Nature 2001 414 6859 105 111
8. Al-Hajj M., Wicha M. S., Benito-Hernandez A., Morrison S. J., Clarke M. F., Prospective identification of tumorigenic breast cancer cells Proceedings of the National Academy of Sciences of the United States of America 2003 100 7 3983 3988 (Pubitemid 36418143)
9. Jordan C. T., Guzman M. L., Noble M., Cancer stem cells New England Journal of Medicine 2006 355 12 1253 1261
10. Ricci-Vitiani L., Pagliuca A., Palio E., Zeuner A., de Maria R., Colon cancer stem cells Gut 2008 57 4 538 548
11. Visvader J. E., Lindeman G. J., Cancer stem cells in solid tumours: accumulating evidence and unresolved questions Nature Reviews Cancer 2008 8 10 755 768
12. Bonnet D., Dick J. E., Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell Nature Medicine 1997 3 7 730 737
13. Collins A. T., Berry P. A., Hyde C., Stower M. J., Maitland N. J., Prospective identification of tumorigenic prostate cancer stem cells Cancer Research 2005 65 23 10946 10951
14. Li C., Heidt D. G., Dalerba P., Burant C. F., Zhang L., Adsay V., Wicha M., Clarke M. F., Simeone D. M., Identification of pancreatic cancer stem cells Cancer Research 2007 67 3 1030 1037
15. O'Brien C. A., Pollett A., Gallinger S., Dick J. E., A human colon cancer cell capable of initiating tumour growth in immunodeficient mice Nature 2007 445 7123 106 110
16. Ricci-Vitiani L., Lombardi D. G., Pilozzi E., Biffoni M., Todaro M., Peschle C., De Maria R., Identification and expansion of human colon-cancer-initiating cells Nature 2007 445 7123 111 115
17. Chu P., Clanton D. J., Snipas T. S., Julia L., Mitchell E., Nguyen M.-L., Hare E., Peach R. J., Characterization of a subpopulation of colon cancer cells with stem cell-like properties International Journal of Cancer 2009 124 6 1312 1321
18. Gao M. -Q., Choi Y. -P., Kang S., Youn J. H., Cho N. -H., CD24+ cells from hierarchically organized ovarian cancer are enriched in cancer stem cells Oncogene 2010 29 18 2672 2680
19. Singh S. K., Hawkins C., Clarke I. D., Squire J. A., Bayani J., Hide T., Henkelman R. M., Cusimano M. D., Dirks P. B., Identification of human brain tumour initiating cells Nature 2004 432 7015 396 401
20. Shmelkov S. V., Butler J. M., Hooper A. T., Hormigo A., Kushner J., Milde T., St Clair R., Baljevic M., White I., Jin D. K., Chadburn A., Murphy A. J., Valenzuela D. M., Gale N. W., Thurston G., Yancopoulos G. D., D'Angelica M., Kemeny N., Lyden D., Rafii S., CD133 expression is not restricted to stem cells, and both CD133 + and CD133-metastatic colon cancer cells initiate tumors Journal of Clinical Investigation 2008 118 6 2111 2120
21. Kemper K., Sprick M. R., De Bree M., Scopelliti A., Vermeulen L., Hoek M., Zeilstra J., Pals S. T., Mehmet H., Stassi G., Medema J. P., The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation Cancer Research 2010 70 2 719 729
22. Diehn M., Clarke M. F., Cancer stem cells and radiotherapy: new insights into tumor radioresistance Journal of the National Cancer Institute 2006 98 24 1755 1757
23. Cotsarelis G., Sun T.-T., Lavker R. M., Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis Cell 1990 61 7 1329 1337
24. Lyle S., Christofidou-Solomidou M., Liu Y., Elder D. E., Albelda S., Cotsarelis G., The C8/144B monoclonal antibody recognizes cytokeratin 15 and defines the location of human hair follicle stem cells Journal of Cell Science 1998 111, part 21 3179 3188
25. Clayton E., Doup D. P., Klein A. M., Winton D. J., Simons B. D., Jones P. H., A single type of progenitor cell maintains normal epidermis Nature 2007 446 7132 185 189
26. Welm B. E., Tepera S. B., Venezia T., Graubert T. A., Rosen J. M., Goodell M. A., Sca-1(pos) cells in the mouse mammary gland represent an enriched progenitor cell population Developmental Biology 2002 245 1 42 56
27. Shackleton M., Vaillant F., Simpson K. J., Stingl J., Smyth G. K., Asselin-Labat M.-L., Wu L., Lindeman G. J., Visvader J. E., Generation of a functional mammary gland from a single stem cell Nature 2006 439 7072 84 88
28. Potten C. S., Kellett M., Roberts S. A., Rew D. A., Wilson G. D., Measurement of in vivo proliferation in human colorectal mucosa using bromodeoxyuridine Gut 1992 33 1 71 78
29. Barker N., Van Es J. H., Kuipers J., Kujala P., Van Den Born M., Cozijnsen M., Haegebarth A., Korving J., Begthel H., Peters P. J., Clevers H., Identification of stem cells in small intestine and colon by marker gene Lgr5 Nature 2007 449 7165 1003 1007
30. Leong K. G., Wang B.-E., Johnson L., Gao W.-Q., Generation of a prostate from a single adult stem cell Nature 2008 456 7223 804 810
31. Uchida N., Buck D. W., He D., Reitsma M. J., Masek M., Phan T. V., Tsukamoto A. S., Gage F. H., Weissman I. L., Direct isolation of human central nervous system stem cells Proceedings of the National Academy of Sciences of the United States of America 2000 97 26 14720 14725
32. Osawa M., Hanada K.-I., Hamada H., Nakauchi H., Long-term lymphohematopoietic reconstitution by a single CD34- low/negative hematopoietic stem cell Science 1996 273 5272 242 245 (Pubitemid 26285891)
33. Morrison S. J., Weissman I. L., The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype Immunity 1994 1 8 661 673
34. Watt F. M., Jensen K. B., Epidermal stem cell diversity and quiescence EMBO Molecular Medicine 2009 1 5 260 267
35. Coller H. A., Sang L., Roberts J. M., A new description of cellular quiescence. PLoS Biology 2006 4 3 e83
36. Sang L., Coller H. A., Roberts J. M., Control of the reversibility of cellular quiescence by the transcriptional repressor HES1 Science 2008 321 5892 1095 1100
37. Viatour P., Somervaille T. C., Venkatasubrahmanyam S., Kogan S., McLaughlin M. E., Weissman I. L., Butte A. J., Passegu E., Sage J., Hematopoietic stem cell quiescence is maintained by compound contributions of the retinoblastoma gene family Cell Stem Cell 2008 3 4 416 428
38. Lyle S., Christofidou-Solomidou M., Liu Y., Elder D. E., Albelda S., Cotsarelis G., Human hair follicle bulge cells are biochemically distinct and possess an epithelial stem cell phenotype Journal of Investigative Dermatology Symposium Proceedings 1999 4 3 296 301
39. Morris R. J., Liu Y., Marles L., Yang Z., Trempus C., Li S., Lin J. S., Sawicki J. A., Cotsarelis G., Capturing and profiling adult hair follicle stem cells Nature Biotechnology 2004 22 4 411 417
40. Roh C., Roche M., Guo Z., Photopoulos C., Tao Q., Lyle S., Multi-potentiality of a new immortalized epithelial stem cell line derived from human hair follicles In Vitro Cellular and Developmental Biology Animal 2008 44 7 236 244
41. Tumbar T., Guasch G., Greco V., Blanpain C., Lowry W. E., Rendl M., Fuchs R., Defining the epithelial stem cell niche in skin Science 2004 303 5656 359 363 (Pubitemid 38095773)
42. Jaks V., Barker N., Kasper M., Van Es J. H., Snippert H. J., Clevers H., Toftgrd R., Lgr5 marks cycling, yet long-lived, hair follicle stem cells Nature Genetics 2008 40 11 1291 1299
43. Potten C. S., Stem cells in gastrointestinal epithelium: numbers, characteristics and death Philosophical Transactions of the Royal Society B: Biological Sciences 1998 353 1370 821 830
44. Nishimura S., Wakabayashi N., Toyoda K., Kashima K., Mitsufuji S., Expression of Musashi-1 in human normal colon crypt cells: a possible stem cell marker of human colon epithelium Digestive Diseases and Sciences 2003 48 8 1523 1529
45. Potten C. S., Booth C., Tudor G. L., Booth D., Brady G., Hurley P., Ashton G., Clarke R., Sakakibara S.-I., Okano H., Identification of a putative intestinal stem cell and early lineage marker; musashi-1 Differentiation 2003 71 1 28 41
46. Fujimoto K., Beauchamp R. D., Whitehead R. H., Identification and isolation of candidate human colonic clonogenic cells based on cell surface integrin expression Gastroenterology 2002 123 6 1941 1948
47. Visvader J. E., Lindeman G. J., Mammary stem cells and mammopoiesis Cancer Research 2006 66 20 9798 9801
48. Pece S., Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content Cell 2010 140 1 62 73
49. Morshead C. M., Reynolds B. A., Craig C. G., McBurney M. W., Staines W. A., Morassutti D., Weiss S., Van Der Kooy D., Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells Neuron 1994 13 5 1071 1082
50. Tsujimura A., Koikawa Y., Salm S., Takao T., Coetzee S., Moscatelli D., Shapiro E., Lepor H., Sun T.-T., Lynette Wilson E., Proximal location of mouse prostate epithelial stem cells: a model of prostatic homeostasis Journal of Cell Biology 2002 157 7 1257 1265
51. Teng C., Guo Y., Zhang H., Zhang H., Ding M., Deng H., Identification and characterization of label-retaining cells in mouse pancreas Differentiation 2007 75 8 702 712
52. Bieniek R., Lazar A. J. F., Photopoulos C., Lyle S., Sebaceous tumours contain a subpopulation of cells expressing the keratin 15 stem cell marker British Journal of Dermatology 2007 156 2 378 380
53. Fillmore C. M., Kuperwasser C., Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy Breast Cancer Research 2008 10 2 R25
54. Roesch A., Fukunaga-Kalabis M., Schmidt E. C., Zabierowski S. E., Brafford P. A., Vultur A., Basu D., Gimotty P., Vogt T., Herlyn M., A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth Cell 2010 141 4 583 594
55. Dembinski J. L., Krauss S., Characterization and functional analysis of a slow cycling stem cell-like subpopulation in pancreas adenocarcinoma Clinical and Experimental Metastasis 2009 26 7 611 623
56. Mani S. A., Guo W., Liao M.-J., Eaton E. NG., Ayyanan A., Zhou A. Y., Brooks M., Reinhard F., Zhang C. C., Shipitsin M., Campbell L. L., Polyak K., Brisken C., Yang J., Weinberg R. A., The epithelial-mesenchymal transition generates cells with properties of stem cells Cell 2008 133 4 704 715
57. Ben-Porath I., Thomson M. W., Carey V. J., Ge R., Bell G. W., Regev A., Weinberg R. A., An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors Nature Genetics 2008 40 5 499 507
58. Reya T., Clevers H., Wnt signalling in stem cells and cancer Nature 2005 434 7035 843 850 (Pubitemid 40558990)
59. Turton N. J., Judah D. J., Riley J., Davies R., Lipson D., Styles J. A., Smith A. G., Gant T. W., Gene expression and amplification in breast carcinoma cells with intrinsic and acquired doxorubicin resistance Oncogene 2001 20 11 1300 1306
60. Qiu W., Carson-Walter E. B., Liu H., Epperly M., Greenberger J. S., Zambetti G. P., Zhang L., Yu J., PUMA regulates intestinal progenitor cell radiosensitivity and gastrointestinal syndrome Cell Stem Cell 2008 2 6 576 583
61. Eyler C. E., Rich J. N., Survival of the fittest: cancer stem cells in therapeutic resistance and angiogenesis Journal of Clinical Oncology 2008 26 17 2839 2845
62. Bao S., Wu Q., McLendon R. E., Hao Y., Shi Q., Hjelmeland A. B., Dewhirst M. W., Bigner D. D., Rich J. N., Glioma stem cells promote radioresistance by preferential activation of the DNA damage response Nature 2006 444 7120 756 760
63. Cheng T., Rodrigues N., Shen H., Yang Y.-G., Dombkowski D., Sykes M., Scadden D. T., Hematopoietic stem cell quiescence maintained by p21(cip1/waf1) Science 2000 287 5459 1804 1809
64. Dekaney C. M., Gulati A. S., Garrison A. P., Helmrath M. A., Henning S. J., Regeneration of intestinal stem/progenitor cells following doxorubicin treatment of mice American Journal of Physiology-Gastrointestinal and Liver Physiology 2009 297 3 G461 G470
65. Merritt A. J., Potten C. S., Watson A. J. M., Loh D. Y., Nakayama -i. K., Nakayama K., Hickman J. A., Differential expression of bcl-2 in intestinal epithelia. Correlation with attenuation of apoptosis in colonic crypts and the incidence of colonic neoplasia Journal of Cell Science 1995 108, part 6 2261 2271
66. Selleri S., Arnaboldi F., Palazzo M., Hussein U., Balsari A., Rumio C., Caveolin-1 is expressed on multipotent cells of hair follicles and might be involved in their resistance to chemotherapy British Journal of Dermatology 2005 153 3 506 513
67. Naumov G. N., Townson J. L., MacDonald I. C., Wilson S. M., Bramwell V. H. C., Groom A. C., Chambers A. F., Ineffectiveness of doxorubicin treatment on solitary dormant mammary carcinoma cells or late-developing metastases Breast Cancer Research and Treatment 2003 82 3 199 206
68. Hambardzumyan D., Becher O. J., Rosenblum M. K., Pandolfi P. P., Manova-Todorova K., Holland E. C., PI3K pathway regulates survival of cancer stem cells residing in the perivascular niche following radiation in medulloblastoma in vivo Genes and Development 2008 22 4 436 448
69. Thames H. D., Ruifrok A. C. C., Milas L., Hunter N., Mason K. A., Terry N. H. A., White R. A., Accelerated repopulation during fractionated irradiation of a murine ovarian carcinoma: downregulation of apoptosis as a possible mechanism International Journal of Radiation Oncology Biology Physics 1996 35 5 951 962
70. Todaro M., Alea M. P., Scopelliti A., Medema J. P., Stassi G., IL-4-mediated drug resistance in colon cancer stem cells Cell Cycle 2008 7 3 309 313
71. Phillips T. M., McBride W. H., Pajonk F., The response of CD24-/low/CD44+ breast cancer-initiating cells to radiation Journal of the National Cancer Institute 2006 98 24 1777 1785
72. Perucca P., Cazzalini O., Madine M., Savio M., Laskey R. A., Vannini V., Prosperi E., Stivala L. A., Loss of p21CDKN1A impairs entry to quiescence and activates a DNA damage response in normal fibroblasts induced to quiescence Cell Cycle 2009 8 1 105 114
73. Sage J., Miller A. L., Prez-Mancera P. A., Wysocki J. M., Jacks T., Acute mutation of retinoblastoma gene function is sufficient for cell cycle re-entry Nature 2003 424 6945 223 228
74. Forsberg E. C., Passegu E., Prohaska S. S., Wagers A. J., Koeva M., Stuart J. M., Weissman I. L., Molecular signatures of quiescent, mobilized and leukemia-initiating hematopoietic stem cells PLoS ONE 2010 5 1
75. Kippin T. E., Martens D. J., van der Kooy D., p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity Genes and Development 2005 19 6 756 767
76. Shimojo H., Ohtsuka T., Kageyama R., Oscillations in notch signaling regulate maintenance of neural progenitors Neuron 2008 58 1 52 64
77. Liu S., Dontu G., Mantle I. D., Patel S., Ahn N.-S., Jackson K. W., Suri P., Wicha M. S., Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells Cancer Research 2006 66 12 6063 6071
78. Horsley V., Aliprantis A. O., Polak L., Glimcher L. H., Fuchs E., NFATc1 balances quiescence and proliferation of skin stem cells Cell 2008 132 2 299 310
79. Mueller S., Cadenas E., Schnthal A. H., p21(WAF1) regulates anchorage-independent growth of HCT116 colon carcinoma cells via E-cadherin expression Cancer Research 2000 60 1 156 163
80. 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., Clevers H., Crypt stem cells as the cells-of-origin of intestinal cancer Nature 2009 457 7229 608 611
81. Vermeulen L., De Sousa E Melo F., Van Der Heijden M., Cameron K., De Jong J. H., Borovski T., Tuynman J. B., Todaro M., Merz C., Rodermond H., Sprick M. R., Kemper K., Richel D. J., Stassi G., Medema J. P., Wnt activity defines colon cancer stem cells and is regulated by the microenvironment Nature Cell Biology 2010 12 5 468 476
82. Abbas T., Dutta A., P21 in cancer: intricate networks and multiple activities Nature Reviews Cancer 2009 9 6 400 414
83. Shen K. C., Heng H., Wang Y., Lu S., Liu G., Deng C.-X., Brooks S. C., Wang Y. A., ATM and p21 cooperate to suppress aneuploidy and subsequent tumor development Cancer Research 2005 65 19 8747 8753
84. Jackson R. J., Adnane J., Coppola D., Cantor A., Sebti S. M., Pledger W. J., Loss of the cell cycle inhibitors p21Cip1 and p27Kip1 enhances tumorigenesis in knockout mouse models Oncogene 2002 21 55 8486 8497
85. Philipp J., Vo K., Gurley K. E., Seidel K., Kemp C. J., Tumor suppression by p27(kip1) and p21(Cip1) during chemically induced skin carcinogenesis Oncogene 1999 18 33 4689 4698