Therapeutic implications of cancer stem cells

Current Opinion in Genetics and Development

Volumn 14, Issue 1, 2004, Pages 43-47

  Al Hajj, Muhammad ^a   Becker, Michael W ^a   Wicha, Max ^a   Weissman, Irving ^b   Clarke, Michael F ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER; CELL PROLIFERATION; CELL RENEWAL; HUMAN; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; STATISTICAL SIGNIFICANCE; STEM CELL; STEM CELL TRANSPLANTATION;

EID: 0842281433     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2003.11.007     Document Type: Review

References (45)

1. Bixby S., Kruger G.M., Mosher J.T., Joseph N.M., Morrison S.J. Cell-intrinsic differences between stem cells from different regions of the peripheral nervous system regulate the generation of neural diversity. Neuron. 35:2002;643-656.
2. Akashi K., Traver D., Miyamoto T., Weissman I.L. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature. 404:2000;193-195.
3. Akashi K, Weissman IL: Developmental Biology of Hematopoiesis. Edited by Zon LI: New York: Oxford University Press; 2001.
4. Baum C.M., Weissman I.L., Tsukamoto A.S., Buckle A.M., Peault B. Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci USA. 89:1992;2804-2808.
5. Spink K.E., Polakis P., Weis W.I. Structural basis of the Axin-adenomatous polyposis coli interaction. EMBO J. 19:2000;2270-2279.
6. Taipale J., Beachy P.A. The hedgehog and Wnt signalling pathways in cancer. Nature. 411:2001;349-354.
7. Bhardwaj G., Murdoch B., Wu D., Baker D.P., Williams K.P., Chadwick K., Ling L.E., Karanu F.N., Bhatia M. Sonic hedgehog induces the proliferation of primitive human hematopoietic cells via BMP regulation. Nat Immunol. 2:2001;172-180.
8. Austin T.W., Solar G.P., Ziegler F.C., Liem L., Matthews W. A role for the Wnt gene family in hematopoiesis: expansion of multilineage progenitor cells. Blood. 89:1997;3624-3635.
9. Reya T., Duncan A.W., Ailles L., Domen J., Scherer D.C., Willert K., Hintz L., Nusse R., Weissman I.L. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature. 423:2003;409-414 The authors demonstrate the importance of the Wnt-β catenin signaling pathway in HSC self-renewal. Murine HSCs were infected with a retrovirus expressing an activated form of β-catenin. Expression of the activated β-catenin in HSCs led to stem-cell expansion in tissue culture as measured by both analysis of phenotype and in vivo function. In addition, they showed that expression of inhibitors of the Wnt signaling resulted in decreased HSC proliferation in vitro as well as a reduced ability of HSCs to reconstitute recipient mice on transplantation. This series of elegant experiments demonstrates that the Wnt signaling pathway is critical for normal HSC homeostasis in vitro and in vivo.
10. •], these studies document a clear role for the Wnt-β catenin signaling pathway in normal HSC homeostasis. In addition, the purified Wnt3a protein has significant potential for use in expansion and genetic engineering of HSCs.
11. Andl T., Reddy S.T., Gaddapara T., Millar S.E. WNT signals are required for the initiation of hair follicle development. Dev Cell. 2:2002;643-653.
12. Jamora C., DasGupta R., Kocieniewski P., Fuchs E. Links between signal transduction, transcription and adhesion in epithelial bud development. Nature. 422:2003;317-322.
13. Jacob J., Kieboom K., Marino S., Depinho R., van Lohuizen M. The oncogene and polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature. 397:1999;164-168.
14. -/- bone marrow cells. These results support a role for Bmi-1 in self-renewal decisions of adult HSCs.
15. van der Lugt N.M., Domen J., Linders K., van Roon M., Robanus-Maandag E., te Riele H., van der Valk M., Deschamps J., Sofroniew M., van Lohuizen M. Posterior transformation, neurological abnormalities, and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 proto-oncogene. Genes Dev. 8:1994;757-769.
16. -/- cells. This study supports an essential role for Bmi-1 in regulating stem-cell homeostasis in both normal and leukaemic stem cells.
17. Li L., Connelly M.C., Wetmore C., Curran T., Morgan J.I. Mouse embryos cloned from brain tumors. Cancer Res. 63:2003;2733-2736.
18. Knudson A.G. Jr., Strong L.C., Anderson D.E. Heredity and cancer in man. Prog Med Genet. 9:1973;113-158.
19. Morrison S.J., Qian D., Jerebek L., Thiel B.A., Park I.-K., Ford P.S., Kiel M.J., Schork N.J., Weissman I.L., Clarke M.F. A genetic determinant that specifically regulates the frequency of hematopoietic stem cells. J Immunol. 168:2002;635-642.
20. Bhatia M., Wang J.C., Kapp U., Bonnet D., Dick J.E. Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc Natl Acad Sci USA. 94:1997;5320-5325.
21. Bonnet D., Dick J. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 3:1997;730-737.
22. Blair A., Hogge D.E., Ailles L.E., Lansdorp P.M., Sutherland H.J. Lack of expression of Thy-1 (CD90) on acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo. Blood. 89:1997;3104-3112.
23. Jordan C.T., Upchurch D., Szilvassy S.J., Guzman M.L., Howard D.S., Pettigrew A.L., Meyerrose T., Rossi R., Grimes B., Rizzieri D.A.et al. The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia. 14:2000;1777-1784.
24. Peault B., Weissman I.L., Buckle A.M., Tsukamoto A., Baum C. Thy-1-expressing CD34+ human cells express multiple hematopoietic potentialities in vitro and in SCID-hu mice. Nouv Rev Fr Hematol. 35:1993;91-93.
25. Holyoake T., Jiang X., Eaves C., Eaves A. Isolation of a highly quiescent subpopulation of primitive leukemic cells in chronic myeloid leukemia. Blood. 94:1999;2056-2064.
26. Takahashi N., Miura I., Saitoh K., Miura A.B. Lineage involvement of stem cells bearing the philadelphia chromosome in chronic myeloid leukemia in the chronic phase as shown by a combination of fluorescence-activated cell sorting and fluorescence in situ hybridization. Blood. 92:1998;4758-4763.
27. Bedi A., Zehnbauer B.A., Collector M.I., Barber J.P., Zicha M.S., Sharkis S.J., Jones R.J. BCR-ABL gene rearrangement and expression of primitive hematopoietic progenitors in chronic myeloid leukemia. Blood. 81:1993;2898-2902.
28. Jaiswal S., Traver D., Miyamoto T., Akashi K., Lagasse E., Weissman I.L. Expression of BCR/ABL and BCL-2 in myeloid progenitors leads to myeloid leukemias. Proc Natl Acad Sci USA. 100:2003;10002-10007.
29. Gudjonsson T., Villadsen R., Nielsen H.L., Ronnov-Jessen L., Bissell M.J., Petersen O.W. Isolation, immortalization, and characterization of a human breast epithelial cell line with stem cell properties. Genes Dev. 16:2002;693-706.
30. Aigner S., Sthoeger Z.M., Fogel M., Weber E., Zarn J., Ruppert M., Zeller Y., Vestweber D., Stahel R., Sammar M.et al. CD24, a mucin-type glycoprotein, is a ligand for P-selectin on human tumor cells. Blood. 89:1997;3385-3395.
31. Stingl J., Eaves C., Kuusk U., Emerman J. Phenotypic and functional characterization in vitro of a multipotent epithelial cell present in the normal adult human breast. Differentiation. 63:1998;201-213.
32. - cells were able to form tumors upon transplantation, whereas tens of thousands of the other phenotypic populations of cancer cells could not. Phenotypic analysis of the xenograft tumors demonstrated that the mouse tumors consisted of heterogeneous populations of tumorigenic and non-tumorigenic cancer cells similar to those seen in the original patient specimen. These data demonstrate the presence of a cell hierarchy within a breast cancer tumor in which only a fraction of the cells have the ability to proliferate extensively, whereas others have only a limited proliferative potential. This suggests that the tumorigenic (cancer stem) cells can both self-renew as well as form non-tumorigenic cancer cells.
33. Costello R.T., Mallet F., Gaugler B., Sainty D., Arnoulet C., Gastaut J.A., Olive D. Human acute myeloid leukemia CD34+/CD38- progenitor cells have decreased sensitivity to chemotherapy and Fas-induced apoptosis, reduced immunogenicity, and impaired dendritic cell transformation capacities. Cancer Res. 60:2000;4403-4411.
34. Guzman M.L., Swiderski C.F., Howard D.S., Grimes B.A., Rossi R.M., Szilvassy S.J., Jordan C.T. Preferential induction of apoptosis for primary human leukemic stem cells. Proc Natl Acad Sci USA. 99:2002;16220-16225.
35. Zhou S., Schuetz J.D., Bunting K.D., Colapietro A.M., Sampath J., Morris J.J., Lagutina I., Grosveld G.C., Osawa M., Nakauchi H.et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med. 7:2001;1028-1034.
36. Zhou S., Morris J.J., Barnes Y., Lan L., Schuetz J.D., Sorrentino B.P. Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo. Proc Natl Acad Sci USA. 99:2002;12339-12344.
37. Gottesman M.M., Fojo T., Bates S.E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer. 2:2002;48-58.
38. Wulf G.G., Wang R.Y., Kuehnle I., Weidner D., Marini F., Brenner M.K., Andreeff M., Goodell M.A. A leukemic stem cell with intrinsic drug efflux capacity in acute myeloid leukemia. Blood. 98:2001;1166-1173.
39. Druker B.J., Tamura S., Buchdunger E., Ohno S., Segal G.M., Fanning S., Zimmermann J., Lydon N.B. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med. 2:1996;561-566.
40. O'Brien S.G., Guilhot F., Larson R.A., Gathmann I., Baccarani M., Cervantes F., Cornelissen J.J., Fischer T., Hochhaus A., Hughes T.et al. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med. 348:2003;994-1004.
41. Hughes T., Branford S. Molecular monitoring of chronic myeloid leukemia. Semin Hematol. 40:2003;62-68.
42. Bhatia R., Holtz M., Niu N., Gray R., Snyder D.S., Sawyers C.L., Arber D.A., Slovak M.L., Forman S.J. Persistence of malignant hematopoietic progenitors in chronic myelogenous leukemia patients in complete cytogenetic remission following imatinib mesylate treatment. Blood. 101:2003;4701-4707.
43. Akashi K., He X., Chen J., Iwasaki H., Niu C., Steenhard B., Zhang J., Haug J., Li L. Transcriptional accessibility for genes of multiple tissues and hematopoietic lineages is hierarchically controlled during early hematopoiesis. Blood. 101:2003;383-389.
44. Braun S., Pantel K. Prognostic significance of micrometastatic bone marrow involvement. Breast Cancer Res Treat. 52:1998;201-216.
45. DiStefano A., Tashima C.K., Yap H.Y., Hortobagyi G.N. Bone marrow metastases without cortical bone involvement in breast cancer patients. Cancer. 44:1979;196-198.