Regulation of apoptosis pathways in cancer stem cells

Cancer Letters

Volumn 338, Issue 1, 2013, Pages 168-173

  Fulda, Simone ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Apoptosis; Bcl 2; Cancer stem cells; Death receptors; IAP proteins

Indexed keywords

3 BENZYL 7 CYANO 2,3,4,5 TETRAHYDRO 1 (1H IMIDAZOL 4 YLMETHYL) 4 (2 THIENYLSULFONYL) 1H 1,4 BENZODIAZEPINE; 4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CASPASE 3; CASPASE 8; CD133 ANTIGEN; CD34 ANTIGEN; CD38 ANTIGEN; CISPLATIN; CYTARABINE; DAUNORUBICIN; DEATH RECEPTOR; DEATH RECEPTOR 5; FAS ANTIGEN; FLICE INHIBITORY PROTEIN; GEMCITABINE; IDARUBICIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN 1; ISOFLAVONE DERIVATIVE; MONOCLONAL ANTIBODY; NV 128; PROTEIN BCL 2; SURVIVIN; TRAIL RECEPTOR 2 AGONIST 5 MONOCLONAL ANTIBODY; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; VISMODEGIB; X LINKED INHIBITOR OF APOPTOSIS;

ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; CANCER COMBINATION CHEMOTHERAPY; CANCER STEM CELL; CELL RENEWAL; CELL SUBPOPULATION; CELL SURVIVAL; CHRONIC MYELOID LEUKEMIA; DRUG MECHANISM; DRUG TARGETING; ENZYME ACTIVATION; GENE SILENCING; HUMAN; INTRACELLULAR SIGNALING; MEMBRANE PERMEABILITY; MESENCHYMAL STEM CELL; MITOCHONDRIAL MEMBRANE; MOLECULAR DYNAMICS; MONOTHERAPY; NONHUMAN; PANCREAS CANCER; PHENOTYPE; PRIORITY JOURNAL; SHORT SURVEY; TUMOR MICROENVIRONMENT;

EID: 84882902651     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.03.014     Document Type: Review

References (84)

1. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997, 3:730-737.
2. 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.
3. Spangrude G.J., Heimfeld S., Weissman I.L. Purification and characterization of mouse hematopoietic stem cells. Science 1988, 241:58-62.
4. Goodell M.A., Brose K., Paradis G., Conner A.S., Mulligan R.C. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J. Exp. Med. 1996, 183:1797-1806.
5. 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, 432:396-401.
6. 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, 445:111-115.
7. 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, 445:106-110.
8. 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.
9. Zhou J., Zhang H., Gu P., Bai J., Margolick J.B., Zhang Y. NF-kappaB pathway inhibitors preferentially inhibit breast cancer stem-like cells. Breast Cancer Res. Treat. 2008, 111:419-427.
10. Domen J., Gandy K.L., Weissman I.L. Systemic overexpression of BCL-2 in the hematopoietic system protects transgenic mice from the consequences of lethal irradiation. Blood 1998, 91:2272-2282.
11. Domen J., Cheshier S.H., Weissman I.L. The role of apoptosis in the regulation of hematopoietic stem cells: overexpression of Bcl-2 increases both their number and repopulation potential. J. Exp. Med. 2000, 191:253-264.
12. Kruyt F.A., Schuringa J.J. Apoptosis and cancer stem cells: implications for apoptosis targeted therapy. Biochem. Pharmacol. 2010, 80:423-430.
13. Vermeulen L., Todaro M., de Sousa Mello F., Sprick M.R., Kemper K., Perez Alea M., Richel D.J., Stassi G., Medema J.P. Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc. Natl. Acad. Sci. USA 2008, 105:13427-13432.
14. Visvader J.E., Lindeman G.J. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat. Rev. Cancer 2008, 8:755-768.
15. Dick J.E. Stem cell concepts renew cancer research. Blood 2008, 112:4793-4807.
16. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
17. 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 2003, 423:409-414.
18. Taussig D.C., Miraki-Moud F., Anjos-Afonso F., Pearce D.J., Allen K., Ridler C., Lillington D., Oakervee H., Cavenagh J., Agrawal S.G., Lister T.A., Gribben J.G., Bonnet D. Anti-CD38 antibody-mediated clearance of human repopulating cells masks the heterogeneity of leukemia-initiating cells. Blood 2008, 112:568-575.
19. Lapidot T., Sirard C., Vormoor J., Murdoch B., Hoang T., Caceres-Cortes J., Minden M., Paterson B., Caligiuri M.A., Dick J.E. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367:645-648.
20. Kavalerchik E., Goff D., Jamieson C.H. Chronic myeloid leukemia stem cells. J. Clin. Oncol. 2008, 26:2911-2915.
21. Kakarala M., Wicha M.S. Implications of the cancer stem-cell hypothesis for breast cancer prevention and therapy. J. Clin. Oncol. 2008, 26:2813-2820.
22. Eramo A., Lotti F., Sette G., Pilozzi E., Biffoni M., Di Virgilio A., Conticello C., Ruco L., Peschle C., De Maria R. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ. 2008, 15:504-514.
23. Peacock C.D., Watkins D.N. Cancer stem cells and the ontogeny of lung cancer. J. Clin. Oncol. 2008, 26:2883-2889.
24. Takaishi S., Okumura T., Wang T.C. Gastric cancer stem cells. J. Clin. Oncol. 2008, 26:2876-2882.
25. Prince M.E., Sivanandan R., Kaczorowski A., Wolf G.T., Kaplan M.J., Dalerba P., Weissman I.L., Clarke M.F., Ailles L.E. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc. Natl. Acad. Sci. USA 2007, 104:973-978.
26. Vazquez A., Bond E.E., Levine A.J., Bond G.L. The genetics of the p53 pathway, apoptosis and cancer therapy. Nat. Rev. Drug Discov. 2008, 7:979-987.
27. Maitland N.J., Collins A.T. Prostate cancer stem cells: a new target for therapy. J. Clin. Oncol. 2008, 26:2862-2870.
28. Boman B.M., Huang E. Human colon cancer stem cells: a new paradigm in gastrointestinal oncology. J. Clin. Oncol. 2008, 26:2828-2838.
29. Ma S., Lee T.K., Zheng B.J., Chan K.W., Guan X.Y. CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene 2008, 27:1749-1758.
30. Yang Z.F., Ngai P., Ho D.W., Yu W.C., Ng M.N., Lau C.K., Li M.L., Tam K.H., Lam C.T., Poon R.T., Fan S.T. Identification of local and circulating cancer stem cells in human liver cancer. Hepatology 2008, 47:919-928.
31. Sell S., Leffert H.L. Liver cancer stem cells. J. Clin. Oncol. 2008, 26:2800-2805.
32. Zobalova R., McDermott L., Stantic M., Prokopova K., Dong L.F., Neuzil J. CD133-positive cells are resistant to TRAIL due to up-regulation of FLIP. Biochem. Biophys. Res. Commun. 2008, 373:567-571.
33. Schatton T., Murphy G.F., Frank N.Y., Yamaura K., Waaga-Gasser A.M., Gasser M., Zhan Q., Jordan S., Duncan L.M., Weishaupt C., Fuhlbrigge R.C., Kupper T.S., Sayegh M.H., Frank M.H. Identification of cells initiating human melanomas. Nature 2008, 451:345-349.
34. Huff C.A., Matsui W. Multiple myeloma cancer stem cells. J. Clin. Oncol. 2008, 26:2895-2900.
35. Kim C.F., Dirks P.B. Cancer and stem cell biology: how tightly intertwined?. Cell Stem Cell 2008, 3:147-150.
36. Ginestier C., Hur M.H., Charafe-Jauffret E., Monville F., Dutcher J., Brown M., Jacquemier J., Viens P., Kleer C.G., Liu S., Schott A., Hayes D., Birnbaum D., Wicha M.S., Dontu G. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007, 1:555-567.
37. Hermann P.C., Huber S.L., Herrler T., Aicher A., Ellwart J.W., Guba M., Bruns C.J., Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007, 1:313-323.
38. Tung D.C., Chao K.S. Targeting hedgehog in cancer stem cells: how a paradigm shift can improve treatment response. Future Oncol. 2007, 3:569-574.
39. Eyler C.E., Rich J.N. Survival of the fittest: cancer stem cells in therapeutic resistance and angiogenesis. J. Clin. Oncol. 2008, 26:2839-2845.
40. Korkaya H., Wicha M.S. Selective targeting of cancer stem cells: a new concept in cancer therapeutics. BioDrugs 2007, 21:299-310.
41. Taylor R.C., Cullen S.P., Martin S.J. Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell Biol. 2008, 9:231-241.
42. Ashkenazi A. Targeting the extrinsic apoptosis pathway in cancer. Cytokine Growth Factor Rev. 2008, 19:325-331.
43. Fulda S., Galluzzi L., Kroemer G. Targeting mitochondria for cancer therapy. Nat. Rev. Drug Discov. 2010, 9:447-464.
44. Fulda S., Vucic D. Targeting IAP proteins for therapeutic intervention in cancer. Nat. Rev. Drug Discov. 2012, 11:109-124.
45. Kelly P.N., Strasser A. The role of Bcl-2 and its pro-survival relatives in tumourigenesis and cancer therapy. Cell Death Differ. 2011, 18:1414-1424.
46. Lowe S.W., Cepero E., Evan G. Intrinsic tumour suppression. Nature 2004, 432:307-315.
47. Ashkenazi A. Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat. Rev. Cancer 2002, 2:420-430.
48. Capper D., Gaiser T., Hartmann C., Habel A., Mueller W., Herold-Mende C., von Deimling A., Siegelin M.D. Stem-cell-like glioma cells are resistant to TRAIL/Apo2L and exhibit down-regulation of caspase-8 by promoter methylation. Acta Neuropathol. 2009, 117:445-456.
49. Qi L., Bellail A.C., Rossi M.R., Zhang Z., Pang H., Hunter S., Cohen C., Moreno C.S., Olson J.J., Li S., Hao C. Heterogeneity of primary glioblastoma cells in the expression of caspase-8 and the response to TRAIL-induced apoptosis. Apoptosis 2011, 16:1150-1164.
50. Zobalova R., Stantic M., Prokopova K., Dong L.F., Neuzil J. Cancer cells with high expression of CD133 exert FLIP upregulation and resistance to TRAIL-induced apoptosis. Biofactors 2008, 34:231-235.
51. Piggott L., Omidvar N., Perez S.M., Eberl M., Clarkson R.W. Suppression of apoptosis inhibitor c-FLIP selectively eliminates breast cancer stem cell activity in response to the anti-cancer agent, TRAIL. Breast Cancer Res. 2011, 13:R88.
52. Sussman R.T., Ricci M.S., Hart L.S., Sun S.Y., El-Deiry W.S. Chemotherapy-resistant side-population of colon cancer cells has a higher sensitivity to TRAIL than the non-SP, a higher expression of c-Myc and TRAIL-receptor DR4. Cancer Biol. Ther. 2007, 6:1490-1495.
53. Yin S., Xu L., Bandyopadhyay S., Sethi S., Reddy K.B. Cisplatin and TRAIL enhance breast cancer stem cell death. Int. J. Oncol. 2011, 39:891-898.
54. Plasilova M., Zivny J., Jelinek J., Neuwirtova R., Cermak J., Necas E., Andera L., Stopka T. TRAIL (Apo2L) suppresses growth of primary human leukemia and myelodysplasia progenitors. Leukemia 2002, 16:67-73.
55. Unterkircher T., Cristofanon S., Vellanki S.H., Nonnenmacher L., Karpel-Massler G., Wirtz C.R., Debatin K.M., Fulda S. Bortezomib primes glioblastoma, including glioblastoma stem cells, for TRAIL by increasing tBid stability and mitochondrial apoptosis. Clin. Cancer Res. 2011, 17:4019-4030.
56. Kahana S., Finniss S., Cazacu S., Xiang C., Lee H.K., Brodie S., Goldstein R.S., Roitman V., Slavin S., Mikkelsen T., Brodie C. Proteasome inhibitors sensitize glioma cells and glioma stem cells to TRAIL-induced apoptosis by PKCepsilon-dependent downregulation of AKT and XIAP expressions. Cell. Signal. 2011, 23:1348-1357.
57. Loebinger M.R., Sage E.K., Davies D., Janes S.M. TRAIL-expressing mesenchymal stem cells kill the putative cancer stem cell population. Br. J. Cancer 2010, 103:1692-1697.
58. Szegezdi E., O'Reilly A., Davy Y., Vawda R., Taylor D.L., Murphy M., Samali A., Mehmet H. Stem cells are resistant to TRAIL receptor-mediated apoptosis. J. Cell Mol. Med. 2009, 13:4409-4414.
59. Rajeshkumar N.V., Rasheed Z.A., Garcia-Garcia E., Lopez-Rios F., Fujiwara K., Matsui W.H., Hidalgo M. A combination of DR5 agonistic monoclonal antibody with gemcitabine targets pancreatic cancer stem cells and results in long-term disease control in human pancreatic cancer model. Mol. Cancer Ther. 2010, 9:2582-2592.
60. A.I. Londono-Joshi, P.G. Oliver, Y. Li, C.H. Lee, A. Forero-Torres, A.F. Lobuglio, D.J. Buchsbaum, Basal-like breast cancer stem cells are sensitive to anti-DR5 mediated cytotoxicity, Breast Cancer Res. Treat. (2011) September 14 (Epub ahead of print).
61. Singh B.N., Fu J., Srivastava R.K., Shankar S. Hedgehog signaling antagonist GDC-0449 (vismodegib) inhibits pancreatic cancer stem cell characteristics: molecular mechanisms. PLoS One 2011, 6:e27306.
62. Bertrand J., Begaud-Grimaud G., Bessette B., Verdier M., Battu S., Jauberteau M.O. Cancer stem cells from human glioma cell line are resistant to Fas-induced apoptosis. Int. J. Oncol. 2009, 34:717-727.
63. Liu G., Yuan X., Zeng Z., Tunici P., Ng H., Abdulkadir I.R., Lu L., Irvin D., Black K.L., Yu J.S. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol. Cancer 2006, 5:67.
64. Vellanki S.H., Grabrucker A., Liebau S., Proepper C., Eramo A., Braun V., Boeckers T., Debatin K.M., Fulda S. Small-molecule XIAP inhibitors enhance gamma-irradiation-induced apoptosis in glioblastoma. Neoplasia 2009, 11:743-752.
65. S. Loeder, M. Fakler, H. Schoeneberger, S. Cristofanon, J. Leibacher, N. Vanlangenakker, M.J. Bertrand, P. Vandenabeele, I. Jeremias, K.M. Debatin, S. Fulda, RIP1 is required for IAP inhibitor-mediated sensitization of childhood acute leukemia cells to chemotherapy-induced apoptosis, Leukemia (2011) December 16 (E-pub ahead of print).
66. Fukuda S., Foster R.G., Porter S.B., Pelus L.M. The antiapoptosis protein survivin is associated with cell cycle entry of normal cord blood CD34(+) cells and modulates cell cycle and proliferation of mouse hematopoietic progenitor cells. Blood 2002, 100:2463-2471.
67. Leung C.G., Xu Y., Mularski B., Liu H., Gurbuxani S., Crispino J.D. Requirements for survivin in terminal differentiation of erythroid cells and maintenance of hematopoietic stem and progenitor cells. J. Exp. Med. 2007, 204:1603-1611.
68. Pennartz S., Belvindrah R., Tomiuk S., Zimmer C., Hofmann K., Conradt M., Bosio A., Cremer H. Purification of neuronal precursors from the adult mouse brain: comprehensive gene expression analysis provides new insights into the control of cell migration, differentiation, and homeostasis. Mol. Cell Neurosci. 2004, 25:692-706.
69. Taubert H., Wurl P., Greither T., Kappler M., Bache M., Bartel F., Kehlen A., Lautenschlager C., Harris L.C., Kaushal D., Fussel S., Meye A., Bohnke A., Schmidt H., Holzhausen H.J., Hauptmann S. Stem cell-associated genes are extremely poor prognostic factors for soft-tissue sarcoma patients. Oncogene 2007, 26:7170-7174.
70. Elhasid R., Larisch S. ARTS-based anticancer therapy: taking aim at cancer stem cells. Future Oncol. 2011, 7:1185-1194.
71. Garcia-Fernandez M., Kissel H., Brown S., Gorenc T., Schile A.J., Rafii S., Larisch S., Steller H. Sept4/ARTS is required for stem cell apoptosis and tumor suppression. Genes Dev. 2010, 24:2282-2293.
72. Tagscherer K.E., Fassl A., Campos B., Farhadi M., Kraemer A., Bock B.C., Macher-Goeppinger S., Radlwimmer B., Wiestler O.D., Herold-Mende C., Roth W. Apoptosis-based treatment of glioblastomas with ABT-737, a novel small molecule inhibitor of Bcl-2 family proteins. Oncogene 2008, 27:6646-6656.
73. Madjd Z., Mehrjerdi A.Z., Sharifi A.M., Molanaei S., Shahzadi S.Z., Asadi-Lari M. CD44+ cancer cells express higher levels of the anti-apoptotic protein Bcl-2 in breast tumours. Cancer Immun.: A J. Acad. Cancer Immunol. 2009, 9:4.
74. Alvero A.B., Montagna M.K., Holmberg J.C., Craveiro V., Brown D., Mor G. Targeting the mitochondria activates two independent cell death pathways in ovarian cancer stem cells. Mol. Cancer Ther. 2011, 10:1385-1393.
75. K. Kemper, H. Rodermond, S. Colak, C. Grandela, J.P. Medema, Targeting colorectal cancer stem cells with inducible caspase-9, Apoptosis (2012) January 6 (E-pub ahead of print).
76. Pellicano F., Copland M., Jorgensen H.G., Mountford J., Leber B., Holyoake T.L. BMS-214662 induces mitochondrial apoptosis in chronic myeloid leukemia (CML) stem/progenitor cells, including CD34+38- cells, through activation of protein kinase Cbeta. Blood 2009, 114:4186-4196.
77. Hayden M.S., Ghosh S. Shared principles in NF-kappaB signaling. Cell 2008, 132:344-362.
78. Perkins N.D. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat. Rev. Mol. Cell Biol. 2007, 8:49-62.
79. Baud V., Karin M. Is NF-kappaB a good target for cancer therapy? hopes and pitfalls. Nat. Rev. Drug Discov. 2009, 8:33-40.
80. Guzman M.L., Neering S.J., Upchurch D., Grimes B., Howard D.S., Rizzieri D.A., Luger S.M., Jordan C.T. Nuclear factor-kappaB is constitutively activated in primitive human acute myelogenous leukemia cells. Blood 2001, 98:2301-2307.
81. 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 2002, 99:16220-16225.
82. Guzman M.L., Rossi R.M., Neelakantan S., Li X., Corbett C.A., Hassane D.C., Becker M.W., Bennett J.M., Sullivan E., Lachowicz J.L., Vaughan A., Sweeney C.J., Matthews W., Carroll M., Liesveld J.L., Crooks P.A., Jordan C.T. An orally bioavailable parthenolide analog selectively eradicates acute myelogenous leukemia stem and progenitor cells. Blood 2007, 110:4427-4435.
83. Cao Y., Luo J.L., Karin M. IkappaB kinase alpha kinase activity is required for self-renewal of ErbB2/Her2-transformed mammary tumor-initiating cells. Proc. Natl. Acad. Sci. USA 2007, 104:15852-15857.
84. Vilimas T., Mascarenhas J., Palomero T., Mandal M., Buonamici S., Meng F., Thompson B., Spaulding C., Macaroun S., Alegre M.L., Kee B.L., Ferrando A., Miele L., Aifantis I. Targeting the NF-kappaB signaling pathway in Notch1-induced T-cell leukemia. Nat. Med. 2007, 13:70-77.