Cellular quiescence in mammary stem cells and breast tumor stem cells: Got testable hypotheses?

Journal of Mammary Gland Biology and Neoplasia

Volumn 14, Issue 1, 2009, Pages 19-27

  Harmes, David C ^a   DiRenzo, James ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Breast cancer; Hedgehog; Mammary stem cell; Notch; Quiescence; Stem cell; Therapeutic resistance

Indexed keywords

CD24 ANTIGEN; FLUOROURACIL; HERMES ANTIGEN; LAPATINIB; NOTCH RECEPTOR; PACLITAXEL;

ADULT STEM CELL; BREAST TUMOR; CANCER RECURRENCE; CANCER RESISTANCE; CANCER STEM CELL; CARCINOGENICITY; CELL CYCLE ARREST; CELL RENEWAL; DNA DAMAGE; GENE EXPRESSION PROFILING; HUMAN; IONIZING RADIATION; NONHUMAN; REVIEW; SENESCENCE; TRANSCRIPTION REGULATION;

ANIMALS; BREAST NEOPLASMS; HUMANS; MAMMARY GLANDS, ANIMAL; MAMMARY GLANDS, HUMAN; NEOPLASTIC STEM CELLS; STEM CELLS; TRANSCRIPTION, GENETIC;

EID: 62549160352     PISSN: 10833021     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10911-009-9111-2     Document Type: Review

References (59)

1. Stingl J, Raouf A, Eirew P, Eaves CJ. Deciphering the mammary epithelial cell hierarchy. Cell Cycle. 2006;5(14):1519-22.
2. Shackleton M, Vaillant F, Simpson KJ, et al. Generation of a functional mammary gland from a single stem cell. Nature. 2006;439(7072):84-8. doi: 10.1038/nature04372.
3. Stingl J, Eirew P, Ricketson I, et al. Purification and unique properties of mammary epithelial stem cells. Nature. 2006;439(7079):993-7.
4. Giebel B. Cell polarity and asymmetric cell division within human hematopoietic stem and progenitor cells. Cells Tissues Organs. 2008;188(1-2):116-26. doi: 10.1159/000112842.
5. Lin H. Cell biology of stem cells: An enigma of asymmetry and self-renewal. J Cell Biol. 2008;180(2):257-60. doi: 10.1083/ jcb.200712159.
6. Coller HA, Sang L, Roberts JM. A new description of cellular quiescence. PLoS Biol. 2006;4(3):e83. doi: 10.1371/journal.pbio.0040083.
7. Sang L, Coller HA, Roberts JM. Control of the reversibility of cellular quiescence by the transcriptional repressor HES1. Science. 2008;321(5892):1095-100. doi: 10.1126/science.1155998.
8. Barker N, van de Wetering M, Clevers H. The intestinal stem cell. Genes Dev. 2008;22(14):1856-64. doi: 10.1101/gad.1674008.
9. Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature. 2005;434(7035):843-50. doi: 10.1038/nature03319.
10. Moll I, Zieger W, Schmelz M. Proliferative Merkel cells were not detected in human skin. Arch Dermatol Res. 1996;288(4):184-7. doi: 10.1007/BF02505222.
11. Davenport A, Hale RJ, Hunt CR, Bigley G, McMahon RF. Expression of Ki-67 and cytokeratin 20 in hyperplastic polyps of the colorectum. J Clin Pathol. 2003;56(3):200-4. doi: 10.1136/jcp.56.3.200.
12. Flores I, Cayuela ML, Blasco MA. Effects of telomerase and telomere length on epidermal stem cell behavior. Science. 2005;309(5738):1253-6. doi: 10.1126/science.1115025.
13. Yasumoto S, Kunimura C, Kikuchi K, et al. Telomerase activity in normal human epithelial cells. Oncogene. 1996;13(2):433-9.
14. Sarin KY, Cheung P, Gilison D, et al. Conditional telomerase induction causes proliferation of hair follicle stem cells. Nature. 2005;436(7053):1048-52. doi: 10.1038/nature03836.
15. Smalley M, Ashworth A. Stem cells and breast cancer: A field in transit. Nat Rev Cancer. 2003;3(11):832-44. doi: 10.1038/nrc1212.
16. Kolquist KA, Ellisen LW, Counter CM, et al. Expression of TERT in early premalignant lesions and a subset of cells in normal tissues. Nat Genet. 1998;19(2):182-6. doi: 10.1038/554.
17. Welm BE, Tepera SB, Venezia T, Graubert TA, Rosen JM, Goodell MA. Sca-1(pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Dev Biol. 2002;245(1):42-56. doi: 10.1006/ dbio.2002.0625.
18. Woodward WA, Chen MS, Behbod F, Rosen JM. On mammary stem cells. J Cell Sci. 2005;118(Pt 16):3585-94. doi: 10.1242/jcs.02532.
19. Horsley V, Aliprantis AO, Polak L, Glimcher LH, Fuchs E. NFATc1 balances quiescence and proliferation of skin stem cells. Cell. 2008;132(2):299-310. doi: 10.1016/j.cell.2007.11.047.
20. Kobielak K, Pasolli HA, Alonso L, Polak L, Fuchs E. Defining BMP functions in the hair follicle by conditional ablation of BMP receptor IA. J Cell Biol. 2003;163(3):609-23. doi: 10.1083/jcb.200309042.
21. Suda T, Arai F, Hirao A. Hematopoietic stem cells and their niche. Trends Immunol. 2005;26(8):426-33. doi: 10.1016/j.it.2005.06.006.
22. Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nat Rev Cancer. 2003;3(12):895-902. doi: 10.1038/ nrc1232.
23. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003;100(7):3983-8. doi: 10.1073/pnas.0530291100.
24. Passegue E, Wagers AJ. Regulating quiescence: New insights into hematopoietic stem cell biology. Dev Cell. 2006;10(4):415-7. doi: 10.1016/j.devcel.2006.03.002.
25. Walkley CR, Fero ML, Chien WM, Purton LE, McArthur GA. Negative cell-cycle regulators cooperatively control self-renewal and differentiation of haematopoietic stem cells. Nat Cell Biol. 2005;7(2):172-8. doi: 10.1038/ncb1214.
26. Li N, Singh S, Cherukuri P, et al. Reciprocal intraepithelial interactions between TP63 and hedgehog signaling regulate quiescence and activation of progenitor elaboration by mammary stem cells. Stem Cells. 2008;26(5):1253-64. doi: 10.1634/stemcells.2007-0691.
27. Dontu G, Abdallah WM, Foley JM, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 2003;17(10):1253-70. doi: 10.1101/gad.1061803.
28. Fillmore CM, 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(2):R25. doi: 10.1186/bcr1982.
29. Ginestier C, Hur MH, Charafe-Jauffret E, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 2007;1(5):555-67. doi: 10.1016/ j.stem.2007.08.014.
30. Zetterberg A, Larsson O. Kinetic analysis of regulatory events in G1 leading to proliferation or quiescence of Swiss 3T3 cells. Proc Natl Acad Sci U S A. 1985;82(16):5365-9. doi: 10.1073/pnas.82.16.5365.
31. Coller HA. What's taking so long? S-phase entry from quiescence versus proliferation. Nat Rev Mol Cell Biol. 2007;8(8):667-70.
32. Kingsbury SR, Loddo M, Fanshawe T, et al. Repression of DNA replication licensing in quiescence is independent of geminin and may define the cell cycle state of progenitor cells. Exp Cell Res. 2005;309(1):56-67. doi: 10.1016/j.yexcr.2005.05.027.
33. Dyson N, Buchkovich K, Whyte P, Harlow E. Cellular proteins that are targetted by DNA tumor viruses for transformation. Princess Takamatsu Symp. 1989;20:191-8.
34. Sage J, Miller AL, Perez-Mancera PA, Wysocki JM, Jacks T. Acute mutation of retinoblastoma gene function is sufficient for cell cycle re-entry. Nature. 2003;424(6945):223-8. doi: 10.1038/nature01764.
35. Viatour P, Somervaille TC, Venkatasubrahmanyam S, et al. Hematopoietic stem cell quiescence is maintained by compound contributions of the retinoblastoma gene family. Cell Stem Cell. 2008;3(4):416-28. doi: 10.1016/j.stem.2008.07.009.
36. Litovchick L, Sadasivam S, Florens L, et al. Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol Cell. 2007;26(4):539-51. doi: 10.1016/j.molcel.2007.04.015.
37. Nielsen NH, Emdin SO, Cajander J, Landberg G. Deregulation of cyclin E and D1 in breast cancer is associated with inactivation of the retinoblastoma protein. Oncogene. 1997;14(3):295-304. doi: 10.1038/ sj.onc.1200833.
38. Pietilainen T, Lipponen P, Aaltomaa S, Eskelinen M, Kosma VM, Syrjanen K. Expression of retinoblastoma gene protein (Rb) in breast cancer as related to established prognostic factors and survival. Eur J Cancer. 1995;31A(3):329-33. doi: 10.1016/0959-8049(94)00463-F.
39. Bosco EE, Knudsen ES. RB in breast cancer: At the crossroads of tumorigenesis and treatment. Cell Cycle. 2007;6(6):667-71.
40. Bosco EE, Wang Y, Xu H, et al. The retinoblastoma tumor suppressor modifies the therapeutic response of breast cancer. J Clin Invest. 2007;117(1):218-28. doi: 10.1172/JCI28803.
41. Ceccarelli C, Santini D, Chieco P, et al. Retinoblastoma (RB1) gene product expression in breast carcinoma. Correlation with Ki-67 growth fraction and biopathological profile. J Clin Pathol. 1998;51(11):818-24. doi: 10.1136/jcp.51.11.818.
42. Zang S, Ji C, Qu X, et al. A study on Notch signaling in human breast cancer. Neoplasma. 2007;54(4):304-10.
43. Buono KD, Robinson GW, Martin C, et al. The canonical Notch/RBP-J signaling pathway controls the balance of cell lineages in mammary epithelium during pregnancy. Dev Biol. 2006;293(2):565-80. doi: 10.1016/ j.ydbio.2006.02.043.
44. Bouras T, Pal B, Vaillant F, et al. Notch signaling regulates mammary stem cell function and luminal cell-fate commitment. Cell Stem Cell. 2008;3(4):429-41. doi: 10.1016/j.stem.2008.08.001.
45. Liu H, Adler AS, Segal E, Chang HY. A transcriptional program mediating entry into cellular quiescence. PLoS Genet. 2007;3(6):e91. doi: 10.1371/ journal.pgen.0030091.
46. Lee TC, Ziff EB. Mxi1 is a repressor of the c-Myc promoter and reverses activation by USF. J Biol Chem. 1999;274(2):595-606. doi: 10.1074/ jbc.274.2.595.
47. Taj MM, Tawil RJ, Engstrom LD, et al. Mxi1, a Myc antagonist, suppresses proliferation of DU145 human prostate cells. Prostate. 2001;47(3):194-204. doi: 10.1002/pros.1063.
48. Wechsler DS, Shelly CA, Petroff CA, Dang CV. MXI1, a putative tumor suppressor gene, suppresses growth of human glioblastoma cells. Cancer Res. 1997;57(21):4905-12.
49. Liu S, Dontu G, Mantle ID, et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006;66(12):6063-71. doi: 10.1158/0008-5472.CAN-06-0054.
50. Moraes RC, Zhang X, Harrington N, et al. Constitutive activation of smoothened (SMO) in mammary glands of transgenic mice leads to increased proliferation, altered differentiation and ductal dysplasia. Development. 2007;134(6):1231-42. doi: 10.1242/dev.02797.
51. Fuchs E. Beauty is skin deep: The fascinating biology of the epidermis and its appendages. Harvey Lect. 1998;94:47-77.
52. Raouf A, Zhao Y, To K, et al. Transcriptome analysis of the normal human mammary cell commitment and differentiation process. Cell Stem Cell. 2008;3(1):109-18. doi: 10.1016/j.stem.2008.05.018.
53. Glazer RI, Wang X, Yuan H, Yin Y. Mammary stem and progenitor cell regulation. Cancer Biomark. 2007;3(4-5):171-81.
54. Hu C, Dievart A, Lupien M, Calvo E, Tremblay G, Jolicoeur P. Overexpression of activated murine Notch1 and Notch3 in transgenic mice blocks mammary gland development and induces mammary tumors. Am J Pathol. 2006;168(3):973-90. doi: 10.2353/ajpath.2006.050416.
55. Phillips TM, McBride WH, Pajonk F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst. 2006;98(24):1777-85.
56. Meissner K, Heydrich B, Jedlitschky G, et al. The ATP-binding cassette transporter ABCG2 (BCRP), a marker for side population stem cells, is expressed in human heart. J Histochem Cytochem. 2006;54(2):215-21. doi: 10.1369/jhc.5A6750.2005.
57. Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K, Tang DG. Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2-cancer cells are similarly tumorigenic. Cancer Res. 2005;65(14):6207-19. doi: 10.1158/0008-5472.CAN-05-0592.
58. Eyler CE, Rich JN. Survival of the fittest: Cancer stem cells in therapeutic resistance and angiogenesis. J Clin Oncol. 2008;26(17):2839-45. doi: 10.1200/JCO.2007.15.1829.
59. Li X, Lewis MT, Huang J, et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst. 2008;100(9):672-9. doi: 10.1093/jnci/djn123.