Label retaining cells in cancer - The dormant root of evil?

Cancer Letters

Volumn 341, Issue 1, 2013, Pages 73-79

  Schillert, Anja ^a   Trumpp, Andreas ^a   Sprick, Martin R ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Cancer stem cells; Cellular plasticity; Disseminated tumor cells; Dormancy; Stem cells; Tumor relapse

Indexed keywords

ADULT STEM CELL; BREAST CANCER; CANCER CELL; CANCER PATIENT; CANCER RECURRENCE; CELL DIFFERENTIATION; CELL FUNCTION; CELL RENEWAL; CELLULAR DORMANCY; COLORECTAL CANCER; DORMANCY; HEMATOPOIETIC SYSTEM; HUMAN; INTESTINE; INTESTINE CELL; INTESTINE STEM CELL; MELANOMA; NONHUMAN; OVARY CANCER; PANCREAS CANCER; PRIORITY JOURNAL; REGULATORY MECHANISM; SHORT SURVEY; SKIN; TUMOR DORMANCY; TUMOR MICROENVIRONMENT;

EID: 84887188562     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.04.019     Document Type: Review

References (86)

1. Hedley B.D., Chambers A.F. Tumor dormancy and metastasis. Adv. Cancer Res. 2009, 102:67-101.
2. Aguirre-Ghiso J.A. Models, mechanisms and clinical evidence for cancer dormancy. Nat. Rev. Cancer 2007, 7:834-846.
3. Demicheli R., Abbattista A., Miceli R., Valagussa P., Bonadonna G. Time distribution of the recurrence risk for breast cancer patients undergoing mastectomy: further support about the concept of tumor dormancy. Breast Cancer Res. Treat. 1996, 41:177-185.
4. Meltzer A. Dormancy and breast cancer. J. Surg. Oncol. 1990, 43:181-188.
5. Marches R., Scheuermann R., Uhr J. Cancer dormancy: from mice to man. Cell Cycle 2006, 5:1772-1778.
6. Demicheli R., Terenziani M., Valagussa P., Moliterni A., Zambetti M., Bonadonna G. Local recurrences following mastectomy: support for the concept of tumor dormancy. J. Natl. Cancer Inst. 1994, 86:45-48.
7. Folkman J., Kalluri R. Cancer without disease. Nature 2004, 427:787.
8. Tumbar T., Guasch G., Greco V., Blanpain C., Lowry W.E., Rendl M., Fuchs E. Defining the epithelial stem cell niche in skin. Science 2004, 303:359-363.
9. Moore N., Lyle S. Quiescent, slow-cycling stem cell populations in cancer: a review of the evidence and discussion of significance. J. Oncol. 2011.
10. Wikman H., Vessella R., Pantel K. Cancer micrometastasis and tumour dormancy. APMIS 2008, 116:754-770.
11. Kuilman T., Michaloglou C., Mooi W.J., Peeper D.S. The essence of senescence. Genes Dev. 2010, 24:2463-2479.
12. Weissman I.L. Stem cells: units of development, units of regeneration, and units in evolution. Cell 2000, 100:157-168.
13. 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, 61:1329-1337.
14. 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. J. Cell Sci. 1998, 111(Pt 21):3179-3188.
15. Clayton E., Doupe 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, 446:185-189.
16. Snippert H.J., Haegebarth A., Kasper M., Jaks V., van Es J.H., Barker N., van de Wetering M., van den Born M., Begthel H., Vries R.G., Stange D.E., Toftgard R., Clevers H. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science 2010, 327:1385-1389.
17. 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, 33:71-78.
18. 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, 449:1003-1007.
19. Potten C.S., Kovacs L., Hamilton E. Continuous labelling studies on mouse skin and intestine. Cell Tissue Kinet. 1974, 7:271-283.
20. Sangiorgi E., Capecchi M.R. Bmi1 is expressed in vivo in intestinal stem cells. Nat. Genet. 2008, 40:915-920.
21. Cheng H., Leblond C.P. 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. 1974, 141:537-561.
22. Bjerknes M., Cheng H. Clonal analysis of mouse intestinal epithelial progenitors. Gastroenterology 1999, 116:7-14.
23. 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. Dev. Biol. 2002, 245:42-56.
24. 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, 439:84-88.
25. 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. Proc. Natl. Acad. Sci. USA 2000, 97:14720-14725.
26. Leong K.G., Wang B.E., Johnson L., Gao W.Q. Generation of a prostate from a single adult stem cell. Nature 2008, 456:804-808.
27. Osawa M., Hanada K., Hamada H., Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 1996, 273:242-245.
28. Morrison S.J., Weissman I.L. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1994, 1:661-673.
29. Orford K.W., Scadden D.T. Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat. Rev. Genet. 2008, 9:115-128.
30. Coller H.A., Sang L., Roberts J.M. A new description of cellular quiescence. PLoS Biol. 2006, 4:e83.
31. Sang L., Coller H.A., Roberts J.M. Control of the reversibility of cellular quiescence by the transcriptional repressor HES1. Science 2008, 321:1095-1100.
32. Viatour P., Somervaille T.C., Venkatasubrahmanyam S., Kogan S., McLaughlin M.E., Weissman I.L., Butte A.J., Passegue E., Sage J. Hematopoietic stem cell quiescence is maintained by compound contributions of the retinoblastoma gene family. Cell Stem Cell 2008, 3:416-428.
33. Park Y., Gerson S.L. DNA repair defects in stem cell function and aging. Annu. Rev. Med. 2005, 56:495-508.
34. Cheshier S.H., Morrison S.J., Liao X., Weissman I.L. In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 1999, 96:3120-3125.
35. Foudi A., Hochedlinger K., Van Buren D., Schindler J.W., Jaenisch R., Carey V., Hock H. Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat. Biotechnol. 2009, 27:84-90.
36. Passegue E., Wagers A.J., Giuriato S., Anderson W.C., Weissman I.L. Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J. Exp. Med. 2005, 202:1599-1611.
37. Yoshihara H., Arai F., Hosokawa K., Hagiwara T., Takubo K., Nakamura Y., Gomei Y., Iwasaki H., Matsuoka S., Miyamoto K., Miyazaki H., Takahashi T., Suda T. Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 2007, 1:685-697.
38. Wilson A., Laurenti E., Oser G., van der Wath R.C., Blanco-Bose W., Jaworski M., Offner S., Dunant C.F., Eshkind L., Bockamp E., Lio P., Macdonald H.R., Trumpp A. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008, 135:1118-1129.
39. Essers M.A., Offner S., Blanco-Bose W.E., Waibler Z., Kalinke U., Duchosal M.A., Trumpp A. IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 2009, 458:904-908.
40. Abkowitz J.L., Linenberger M.L., Newton M.A., Shelton G.H., Ott R.L., Guttorp P. Evidence for the maintenance of hematopoiesis in a large animal by the sequential activation of stem-cell clones. Proc. Natl. Acad. Sci. USA 1990, 87:9062-9066.
41. Haug J.S., He X.C., Grindley J.C., Wunderlich J.P., Gaudenz K., Ross J.T., Paulson A., Wagner K.P., Xie Y., Zhu R., Yin T., Perry J.M., Hembree M.J., Redenbaugh E.P., Radice G.L., Seidel C., Li L. N-cadherin expression level distinguishes reserved versus primed states of hematopoietic stem cells. Cell Stem Cell 2008, 2:367-379.
42. Cairnie A.B., Lamerton L.F., Steel G.G. Cell proliferation studies in the intestinal epithelium of the rat. I. Determination of the kinetic parameters. Exp. Cell. Res. 1965, 39:528-538.
43. Potten C.S. Extreme sensitivity of some intestinal crypt cells to X and gamma irradiation. Nature 1977, 269:518-521.
44. Scoville D.H., Sato T., He X.C., Li L. Current view: intestinal stem cells and signaling. Gastroenterology 2008, 134:849-864.
45. Li L., Clevers H. Coexistence of quiescent and active adult stem cells in mammals. Science 2010, 327:542-545.
46. Medema J.P., Vermeulen L. Microenvironmental regulation of stem cells in intestinal homeostasis and cancer. Nature 2011, 474:318-326.
47. Tian H., Biehs B., Warming S., Leong K.G., Rangell L., Klein O.D., de Sauvage F.J. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 2011, 478:255-259.
48. Takeda N., Jain R., LeBoeuf M.R., Wang Q., Lu M.M., Epstein J.A. Interconversion between intestinal stem cell populations in distinct niches. Science 2011, 334:1420-1424.
49. Montgomery R.K., Carlone D.L., Richmond C.A., Farilla L., Kranendonk M.E., Henderson D.E., Baffour-Awuah N.Y., Ambruzs D.M., Fogli L.K., Algra S., Breault D.T. Mouse telomerase reverse transcriptase (mTert) expression marks slowly cycling intestinal stem cells. Proc. Natl. Acad. Sci. USA 2011, 108:179-184.
50. Yan K.S., Chia L.A., Li X., Ootani A., Su J., Lee J.Y., Su N., Luo Y., Heilshorn S.C., Amieva M.R., Sangiorgi E., Capecchi M.R., Kuo C.J. The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations. Proc. Natl. Acad. Sci. USA 2012, 109:466-471.
51. Powell A.E., Wang Y., Li Y., Poulin E.J., Means A.L., Washington M.K., Higginbotham J.N., Juchheim A., Prasad N., Levy S.E., Guo Y., Shyr Y., Aronow B.J., Haigis K.M., Franklin J.L., Coffey R.J. The Pan-ErbB negative regulator Lrig1 is an intestinal stem cell marker that functions as a tumor suppressor. Cell 2012, 149:146-158.
52. Akashi T., Shirasawa T., Hirokawa K. Gene expression of CD24 core polypeptide molecule in normal rat tissues and human tumor cell lines. Virchows Arch. 1994, 425:399-406.
53. Gracz A.D., Ramalingam S., Magness S.T. Sox9 expression marks a subset of CD24-expressing small intestine epithelial stem cells that form organoids in vitro. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298:G590-600.
54. von Furstenberg R.J., Gulati A.S., Baxi A., Doherty J.M., Stappenbeck T.S., Gracz A.D., Magness S.T., Henning S.J. Sorting mouse jejunal epithelial cells with CD24 yields a population with characteristics of intestinal stem cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 300:G409-417.
55. Laederich M.B., Funes-Duran M., Yen L., Ingalla E., Wu X., Carraway K.L., Sweeney C. The leucine-rich repeat protein LRIG1 is a negative regulator of ErbB family receptor tyrosine kinases. J. Biol. Chem. 2004, 279:47050-47056.
56. Itzkovitz S., Lyubimova A., Blat I.C., Maynard M., van Es J., Lees J., Jacks T., Clevers H., van Oudenaarden A. Single-molecule transcript counting of stem-cell markers in the mouse intestine. Nat. Cell Biol. 2012, 14:106-114.
57. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
58. Lobo N.A., Shimono Y., Qian D., Clarke M.F. The biology of cancer stem cells. Annu. Rev. Cell Dev. Biol. 2007, 23:675-699.
59. Trumpp A., Wiestler O.D. Mechanisms of disease: cancer stem cells - targeting the evil twin. Nat. Clin. Pract. Oncol. 2008, 5:337-347.
60. Vermeulen L., Sprick M.R., Kemper K., Stassi G., Medema J.P. Cancer stem cells - old concepts, new insights. Cell Death Differ. 2008, 15:947-958.
61. 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, 29:2672-2680.
62. Correa R.J., Peart T., Valdes Y.R., DiMattia G.E., Shepherd T.G. Modulation of AKT activity is associated with reversible dormancy in ascites-derived epithelial ovarian cancer spheroids. Carcinogenesis 2012, 33:49-58.
63. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 2003, 100:3983-3988.
64. 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 Res. 2007, 67:1030-1037.
65. 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 Res. 2008, 10:R25.
66. Moore N., Houghton J., Lyle S. Slow-cycling therapy-resistant cancer cells. Stem Cell Dev. 2011.
67. Pece S., Tosoni D., Confalonieri S., Mazzarol G., Vecchi M., Ronzoni S., Bernard L., Viale G., Pelicci P.G., Di Fiore P.P. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 2010, 140:62-73.
68. 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, 141:583-594.
69. Dembinski J.L., Krauss S. Characterization and functional analysis of a slow cycling stem cell-like subpopulation in pancreas adenocarcinoma. Clin. Exp. Metast. 2009, 26:611-623.
70. Sharma S.V., Lee D.Y., Li B., Quinlan M.P., Takahashi F., Maheswaran S., McDermott U., Azizian N., Zou L., Fischbach M.A., Wong K.K., Brandstetter K., Wittner B., Ramaswamy S., Classon M., Settleman J. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 2010, 141:69-80.
71. Sosa M.S., Avivar-Valderas A., Bragado P., Wen H.C., Aguirre-Ghiso J.A. ERK1/2 and p38alpha/beta signaling in tumor cell quiescence: opportunities to control dormant residual disease. Clin. Cancer Res. 2011, 17:5850-5857.
72. Bragado P., Sosa M.S., Keely P., Condeelis J., Aguirre-Ghiso J.A. Microenvironments dictating tumor cell dormancy. Recent results in cancer research. Fortschritte der Krebsforschung. Progres dans les recherches sur le cancer 2012, 195:25-39.
73. Lander A.D., Kimble J., Clevers H., Fuchs E., Montarras D., Buckingham M., Calof A.L., Trumpp A., Oskarsson T. What does the concept of the stem cell niche really mean today?. BMC Biol. 2012, 10:19.
74. Borovski T., De Sousa E.M.F., Vermeulen L., Medema J.P. Cancer stem cell niche: the place to be. Cancer Res. 2011, 71:634-639.
75. Vessella R.L., Pantel K., Mohla S. Tumor cell dormancy: an NCI workshop report. Cancer Biol. Ther. 2007, 6:1496-1504.
76. Pantel K., Woelfle U. Detection and molecular characterisation of disseminated tumour cells: implications for anti-cancer therapy. Biochim. Biophys. Acta 2005, 1756:53-64.
77. Braun S., Vogl F.D., Naume B., Janni W., Osborne M.P., Coombes R.C., Schlimok G., Diel I.J., Gerber B., Gebauer G., Pierga J.Y., Marth C., Oruzio D., Wiedswang G., Solomayer E.F., Kundt G., Strobl B., Fehm T., Wong G.Y., Bliss J., Vincent-Salomon A., Pantel K. A pooled analysis of bone marrow micrometastasis in breast cancer. N. Engl. J. Med. 2005, 353:793-802.
78. Morgan T.M., Lange P.H., Porter M.P., Lin D.W., Ellis W.J., Gallaher I.S., Vessella R.L. Disseminated tumor cells in prostate cancer patients after radical prostatectomy and without evidence of disease predicts biochemical recurrence. Clin. Cancer Res. 2009, 15:677-683.
79. Leinung S., Wurl P., Weiss C.L., Roder I., Schonfelder M. Cytokeratin-positive cells in bone marrow in comparison with other prognostic factors in colon carcinoma. Langenbecks Arch. Surg. 2000, 385:337-343.
80. Pantel K., Schlimok G., Braun S., Kutter D., Lindemann F., Schaller G., Funke I., Izbicki J.R., Riethmuller G. Differential expression of proliferation-associated molecules in individual micrometastatic carcinoma cells. J. Natl. Cancer Inst. 1993, 85:1419-1424.
81. Balic M., Lin H., Young L., Hawes D., Giuliano A., McNamara G., Datar R.H., Cote R.J. Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype. Clin. Cancer Res. 2006, 12:5615-5621.
82. Naumov G.N., Townson J.L., MacDonald I.C., Wilson S.M., Bramwell V.H., Groom A.C., Chambers A.F. Ineffectiveness of doxorubicin treatment on solitary dormant mammary carcinoma cells or late-developing metastases. Breast Cancer Res. Treat. 2003, 82:199-206.
83. Wimberger P., Heubner M., Otterbach F., Fehm T., Kimmig R., Kasimir-Bauer S. Influence of platinum-based chemotherapy on disseminated tumor cells in blood and bone marrow of patients with ovarian cancer. Gynecol. Oncol. 2007, 107:331-338.
84. Christensen J.L., Weissman I.L. Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells. Proc. Natl. Acad. Sci. USA 2001, 98:14541-14546.
85. Pasquier E., Kavallaris M., Andre N. Metronomic chemotherapy: new rationale for new directions. Nat. Rev. Clin. Oncol. 2010, 7:455-465.
86. Trumpp A., Essers M., Wilson A. Awakening dormant haematopoietic stem cells. Nat. Rev. Immunol. 2010, 10:201-209.