Apoptosis and cancer stem cells: Implications for apoptosis targeted therapy

Biochemical Pharmacology

Volumn 80, Issue 4, 2010, Pages 423-430

  Kruyt, Frank A E ^a   Schuringa, Jan Jacob ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Anoikis; Epithelial mesenchymal transition; Microenvironment; Plasticity; Resistance; Tumor initiating cells

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; 5 AZA 2' DEOXYCYTIDINE; ANTINEOPLASTIC AGENT; CASPASE 8; CD133 ANTIGEN; CHEMOKINE; CYTOKINE; DACTINOMYCIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LC 1; MG 123; N [1,4,8,11 TETRAAZACYCLOTETRADECANYL 1,4 PHENYLENEBIS(METHYLENE)] 2 (AMINOMETHYL)PYRIDINE; PARTHENOLIDE; PERIFOSINE; PROTEIN BCL 2; SORAFENIB; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS; X LINKED INHIBITOR OF APOPTOSIS INHIBITOR;

ACUTE GRANULOCYTIC LEUKEMIA; ANOIKIS; APOPTOSIS; CANCER GROWTH; CANCER RESISTANCE; CANCER STEM CELL; CELL DIFFERENTIATION; CELL HYPOXIA; CELL PROLIFERATION; CELL RENEWAL; CELL SURVIVAL; DRUG MECHANISM; DRUG POTENTIATION; EPITHELIUM CELL; GLIOBLASTOMA; HEMATOLOGIC MALIGNANCY; HUMAN; MALIGNANT TRANSFORMATION; MESENCHYME CELL; METASTASIS; NEURAL STEM CELL; NONHUMAN; NOTE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN TARGETING; RNA INTERFERENCE; SOLID TUMOR; TARGET CELL;

ANOIKIS; APOPTOSIS; CELL DIFFERENTIATION; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE THERAPY; HELA CELLS; HUMANS; NEOPLASTIC STEM CELLS; PROTO-ONCOGENE PROTEINS C-BCL-2; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 77953914498     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.04.010     Document Type: Note

References (102)

1. Reed J.C. Drug insight: cancer therapy strategies based on restoration of endogenous cell death mechanisms. Nat Clin Pract Oncol 2006, 3(7):388-398.
2. Ashkenazi A. Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nat Rev Drug Discov 2008, 7(12):1001-1012.
3. Kruyt F.A. TRAIL and cancer therapy. Cancer Lett 2008, 263(1):14-25.
4. Budihardjo I., Oliver H., Lutter M., Luo X., Wang X. Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol 1999, 15:269-290.
5. Brunelle J.K., Letai A. Control of mitochondrial apoptosis by the Bcl-2 family. J Cell Sci 2009, 122(Pt 4):437-441.
6. Shore G.C., Viallet J. Modulating the bcl-2 family of apoptosis suppressors for potential therapeutic benefit in cancer. Hematology Am Soc Hematol Educ Program 2005, 226-230.
7. Oltersdorf T., Elmore S.W., Shoemaker A.R., Armstrong R.C., Augeri D.J., Belli B.A., et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005, 435(7042):677-681.
8. LaCasse E.C., Mahoney D.J., Cheung H.H., Plenchette S., Baird S., Korneluk R.G. IAP-Oncogene 2008, 27(48):6252-6275.
9. Lowe S.W., Cepero E., Evan G. Intrinsic tumour suppression. Nature 2004, 432(7015):307-315.
10. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
11. Dalerba P., Cho R.W., Clarke M.F. Cancer stem cells: models and concepts. Annu Rev Med 2007, 58:267-284.
12. Barker N., van Es J.H., Kuipers J., Kujala P., van den Born M., Cozijnsen M., et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449:1003-1007.
13. Barker N., Ridgway R.A., van Es J.H., van de Wetering M., Begthel H., van den Born M., et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009, 457:608-611.
14. Barker N., van de Wetering M., Clevers H. The intestinal stem cell. Genes Dev 2008, 22:1856-1864.
15. Alcantara Llaguno S., Chen J., Kwon C.H., Jackson E.L., Li Y., Burns D.K., et al. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 2009, 15:45-56. Erratum in: Cancer Cell 2009;15(3):240.
16. Wang J.C., Dick J.E. Cancer stem cells: lessons from leukemia. Trends Cell Biol 2005, 15(9):494-501.
17. Ailles L.E., Weissman I.L. Cancer stem cells in solid tumours. Curr Opin Biotechnol 2007, 18(5):460-466.
18. Cho R.W., Clarke M.F. Recent advances in cancer stem cells. Curr Opin Genet Dev 2008, 18(1):48-53.
19. 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(7):730-737.
20. Dean M., Fojo T., Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005, 5(4):275-284.
21. Douville J., Beaulieu R., Balicki D. ALDH1 as a functional marker of cancer stem and progenitor cells. Stem Cells Dev 2009, 18:17-25.
22. Clarke M.F., Dick J.E., Dirks P.B., Eaves C.J., Jamieson C.H., Jones D.L., et al. Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006, 66(19):9339-9344.
23. Hill R.P. Identifying cancer stem cells in solid tumors: case not proven. Cancer Res 2006, 66(4):1891-1895.
24. Kennedy J.A., Barabé F., Poeppl A.G., Wang J.C., Dick J.E. Comment on " Tumor growth need not be driven by rare cancer stem cells" Science 2007, 318(5857):1722.
25. Quintana E., Shackleton M., Sabel M.S., Fullen D.R., Johnson T.M., Morrison S.J. Efficient tumour formation by single human melanoma cells. Nature 2008, 456(7222):593-598.
26. Bidlingmaier S., Zhu X., Liu B. The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells. J Mol Med 2008, 86(9):1025-1032.
27. Snippert H.J., van Es J.H., van den Born M., Begthel H., Stange D.E., Barker N., et al. Prominin-1/CD133 marks stem cells and early progenitors in mouse small intestine. Gastroenterology 2009, 136(7). 2187-94.
28. Pece S., Tosoni D., Confalonieri S., Mazzarol G., Vecchi M., Ronzoni S., et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 2010, 140(1):62-73.
29. Al-Haij 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(7):3983-3988. Erratum in: Proc Natl Acad Sci USA 2003;100(11) 6890.
30. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414(6859):105-111.
31. Hombach-Klonisch S., Paranjothy T., Wiechec E., Pocar P., Mustafa T., Seifert A., et al. Cancer stem cells as targets for cancer therapy: selected cancers as examples. Arch Immunol Ther Exp (Warsz) 2008, 56(3):165-180.
32. Thiery J.P., Sleeman J.P. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 2006, 7(2):131-142.
33. Polyak K., Weinberg R.A. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009, 9(4):265-273.
34. Liu G., Yuan X., Zeng Z., Tunici P., Ng H., Abdulkadir I.R., et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006, 5:67.
35. Capper D., Gaiser T., Hartmann C., Habel A., Mueller W., Herold-Mende C., et al. Stem-cell-like glioma cells are resistant to TRAIL/Apo2L and exhibit down-regulation of caspase-8 by promoter methylation. Acta Neuropathol 2009, 117(4):445-456.
36. De Zio D., Giunta L., Corvaro M., Ferraro E., Cecconi F. Expanding roles of programmed cell death in mammalian neurodevelopment. Semin Cell Dev Biol 2005, 16(2):281-294.
37. Ricci-Vitiani L., Pedini F., Mollinari C., Condorelli G., Bonci D., Bez A., et al. Absence of caspase 8 and high expression of PED protect primitive neural cells from cell death. J Exp Med 2004, 200(10):1257-1266.
38. Peng H., Huang Y., Duan Z., Erdmann N., Xu D., Herek S., et al. Cellular IAP1 regulates TRAIL-induced apoptosis in human fetal cortical neural progenitor cells. J Neurosci Res 2005, 82(3):295-305.
39. Corsini N.S., Sancho-Martinez I., Laudenklos S., Glagow D., Kumar S., Letellier E., et al. The death receptor CD95 activates adult neural stem cells for working memory formation and brain repair. Cell Stem Cell 2009, 5(2):178-190.
40. Johnsen J.I., Kogner P., Albihn A., Hendriksson M.A. Embryonal neural tumours and cell death. Apoptosis 2009, 14(4):424-438.
41. Lindsten T., Golden J.A., Zong W.X., Minarcik J., Harris M.H., Thompson C.B. The proapoptotic activities of Bax and Bak limit the size of the neural stem cell pool. J Neurosci 2003, 23(35):11112-11119.
42. Tagscherer K.E., Fassl A., Campos B., Farhadi M., Kraemer A., Böck B.C., et al. Apoptosis-based treatment of glioblastomas with ABT-737, a novel small molecule inhibitor of Bcl-2 family proteins. Oncogene 2008, 27(52):6646-6656.
43. Vellanki S.H., Grabrucker A., Liebau S., Proepper C., Eramo A., Braun V., et al. Small-molecule XIAP inhibitors enhance gamma-irradiation-induced apoptosis in glioblastoma. Neoplasia 2009, 11(8):743-752.
44. Del Poeta G., Bruno A., Del Principe M.I., Venditti A., Maurillo L., Buccisano F., et al. Deregulation of the mitochondrial apoptotic machinery and development of molecular targeted drugs in acute myeloid leukemia. Curr Cancer Drug Targets 2008, 8(3):207-222.
45. Mohr A., Zwacka R.M., Jarmy G., Büneker C., Schrezenmeier H., Döhner K., et al. Caspase-8L expression protects CD34+ hematopoietic progenitor cells and leukemic cells from CD95-mediated apoptosis. Oncogene 2005, 24(14):2421-2429.
46. Tazzari P.L., Tabellini G., Ricci F., Papa V., Bortul R., Chiarini F., et al. Synergistic proapoptotic activity of recombinant TRAIL plus the Akt inhibitor Perifosine in acute myelogenous leukemia cells. Cancer Res 2008, 68(22):9394-9403.
47. Konopleva M., Contractor R., Tsao T., Samudio I., Ruvolo P.P., Kitada S., et al. Mechanisms of apoptosis sensitivity and resistance to the BH3 mimetic ABT-737 in acute myeloid leukemia. Cancer Cell 2006, 10(5):375-388.
48. Zoblova 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(4):567-571.
49. 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(9):1490-1495.
50. Moore K.A., Lemischka I.R. Stem cells and their niches. Science 2006, 311(5769):1880-1885.
51. Li L., Neaves W.B. Normal stem cells and cancer stem cells: the niche matters. Cancer Res 2006, 66(9):4553-4557. Erratum in: Cancer Res 2006;66(12):6458.
52. Sneddon J.B., Werb Z. Location, location, location: the cancer stem cell niche. Cell Stem Cell 2007, 1(6):607-611.
53. Konopleva M., Tabe Y., Zeng Z., Andreeff M. Therapeutic targeting of microenvironmental interactions in leukemia: mechanisms and approaches. Drug Resist Updat 2009, 12(4-5):103-113.
54. Iwasaki H., Suda T. Cancer stem cells and their niche. Cancer Sci 2009, 100(7):1166-1172.
55. Sipkins D.A., Wei X., Wu J.W., Runnels J.M., Côté D., Means T.K., et al. In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature 2005, 435(7044):969-973.
56. De Toni F., Racaud-Sultan C., Chicanne G., Mas V.M., Cariven C., Mesange F., et al. A crosstalk between the Wnt and the adhesion-dependent signaling pathways governs the chemosensitivity of acute myeloid leukemia. Oncogene 2006, 25(22):3113-3122.
57. Calabrese C., Poppleton H., Kocak M., Hogg T.L., Fuller C., Hamner B., et al. A perivascular niche for brain tumor stem cells. Cancer Cell 2007, 11(1):69-82.
58. Oishi K., Kamakura S., Isazawa Y., Yoshimatsu T., Kuida K., Nakafuku M., et al. Notch promotes survival of neural precursor cells via mechanisms distinct from those regulating neurogenesis. Dev Biol 2004, 276(1):172-184.
59. Fan X., Matsui W., Khaki L., Stearns D., Chun J., Li Y.M., et al. Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res 2006, 66(15):7445-7452.
60. Sade H., Krishna S., Sarin A. The anti-apoptotic effect of Notch-1 requires p56lck-dependent, Akt/PKB-mediated signaling in T cells. J Biol Chem 2004, 279(4):2937-2944.
61. Qin J.Z., Stennett L., Bacon P., Bodner B., Hendrix M.J., Seftor R.E., et al. p53-independent NOXA induction overcomes apoptotic resistance of malignant melanomas. Mol Cancer Ther 2004, 3(8):895-902.
62. Doubravská L., Símová S., Cermak L., Valenta T., Korínek V., Andera L. Wnt-expressing rat embryonic fibroblasts suppress Apo2L/TRAIL-induced apoptosis of human leukemia cells. Apoptosis 2008, 13(4):573-587.
63. De Toni E.N., Thieme S.E., Herbst A., Behrens A., Stieber P., Jung A., et al. OPG is regulated by beta-catenin and mediates resistance to TRAIL-induced apoptosis in colon cancer. Clin Cancer Res 2008, 14(15):4713-4718.
64. Lapham A., Adams J.E., Paterson A., Lee M., Brimmell M., Packham G. The Bcl-w promoter is activated by beta-catenin/TCF4 in human colorectal carcinoma cells. Gene 2009, 432(1-2):112-117.
65. Todaro M., Alea M.P., Di Stefano A.B., Cammareri P., Vermeulen L., Iovino F., et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 2007, 1(4):389-402.
66. Prasad S., Ravindran J., Aggarwal B.B. NF-kappaB and cancer: how intimate is this relationship. Mol Cell Biochem 2010, 336:25-37.
67. Turco M.C., Romano M.F., Petrella A., Bisogni R., Tassone P., Venuta S. NF-kappaB/Rel-mediated regulation of apoptosis in hematologic malignancies and normal hematopoietic progenitors. Leukemia 2004, 18(1):11-17.
68. Guzman M.L., Neering S.J., Upchurch D., Grimes B., Howard D.S., Rizzieri D.A., et al. Nuclear factor-kappaB is constitutively activated in primitive human acute myelogenous leukemia cells. Blood 2001, 98(8):2301-2307.
69. Birkenkamp K.U., Geugien M., Schepers H., Westra J., Lemmink H.H., Vellenga E. Constitutive NF-kappaB DNA-binding activity in AML is frequently mediated by a Ras/PI3-K/PKB-dependent pathway. Leukemia 2004, 18(1):103-112.
70. Schepers H., Eggen B.J., Schuringa J.J., Vellenga E. Constitutive activation of NF-kappa B is not sufficient to disturb normal steady-state hematopoiesis. Haematologica 2006, 91(12):1710-1711.
71. Guzman M.L., Rossi R.M., Karnischky L., Li X., Peterson D.R., Howard D.S., et al. The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood 2005, 105(11):4163-4169.
72. Neelakantan S., Nasim S., Guzman M.L., Jordan C.T., Crooks P.A. Aminoparthenolides as novel anti-leukemic agents: discovery of the NF-kappaB inhibitor, DMAPT (LC-1). Bioorg Med Chem Lett 2009, 19(15):4346-4349.
73. Westhoff M.A., Fulda S. Adhesion-mediated apoptosis resistance in cancer. Drug Resist Updat 2009, 12(4-5):127-136.
74. Ley R., Balmanno K., Hadfield K., Weston C., Cook S.J. Activation of the ERK1/2 signaling pathway promotes phosphorylation and proteasome-dependent degradation of the BH3-only protein, Bim. J Biol Chem 2003, 278(21).
75. Boucher M.J., Morisset J., Vachon P.H., Reed J.C., Lainé J., Rivard N. MEK/ERK signaling pathway regulates the expression of Bcl-2, Bcl-X(L), and Mcl-1 and promotes survival of human pancreatic cancer cells. J Cell Biochem 2000, 79(3):355-369.
76. Manning B.D., Cantley L.C. AKT/PKB signaling: navigating downstream. Cell 2007, 129(7):1261-1274.
77. Westhoff M.A., Zhou S., Bachem M.G., Debatin K.M., Fulda S. Identification of a novel switch in the dominant forms of cell adhesion-mediated drug resistance in glioblastoma cells. Oncogene 2008, 27(39):5169-5181.
78. Bao S., Wu Q., Li Z., Sathornsumetee S., Wang H., McLendon R.E., et al. Targeting cancer stem cells through L1CAM suppresses glioma growth. Cancer Res 2008, 68(15):6043-6048.
79. Wang M.W., Consoli U., Lane C.M., Durett A., Lauppe M.J., Champlin R., et al. Rescue from apoptosis in early (CD34-selected) versus late (non-CD34-selected) human hematopoietic cells by very late antigen 4- and vascular cell adhesion molecule (VCAM) 1-dependent adhesion to bone marrow stromal cells. Cell Growth Differ 1998, 9(2):105-112.
80. Petit I., Karajannis M.A., Vincent L., Young L., Butler J., Hooper A.T., et al. The microtubule-targeting agent CA4P regresses leukemic xenografts by disrupting interaction with vascular cells and mitochondrial-dependent cell death. Blood 2008, 111(4):1951-1961.
81. Zeng Z., Shi Y.X., Samudio I.J., Wang R.Y., Ling X., Frolova O., et al. Targeting the leukemia microenvironment by CXCR4 inhibition overcomes resistance to kinase inhibitors and chemotherapy in AML. Blood 2009, 113(24):6215-6224.
82. Panchision D.M. The role of oxygen in regulating neural stem cells in development and disease. J Cell Physiol 2009, 220(3):562-568.
83. Semenza G.L. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003, 3(10):721-732.
84. Shroff E.H., Snyder C., Chandel N.S. Role of Bcl-2 family members in anoxia induced cell death. Cell Cycle 2007, 6(7):807-809.
85. Chen N., Chen X., Huang R., Zeng H., Gong J., Meng W., et al. BCL-xL is a target gene regulated by hypoxia-inducible factor-1{alpha}. J Biol Chem 2009, 284(15):10004-10012.
86. Diehn M., Cho R.W., Lobo N.A., Kalisky T., Dorie M.J., Kulp A.N., et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009, 458(7239):780-783.
87. Wang J., Yi J. Cancer cell killing via ROS: to increase or decrease, that is the question. Cancer Biol Ther 2008, 7(12):1875-1884.
88. Reinehr R., Becker S., Eberle A., Grether-Beck S., Häussinger D. Involvement of NADPH oxidase isoforms and Src family kinases in CD95-dependent hepatocyte apoptosis. J Biol Chem 2005, 280(29):27179-27194.
89. Kim Y.H., Jung E.M., Lee T.J., Kim S.H., Choi Y.H., Park J.W., et al. Rosiglitazone promotes tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by reactive oxygen species-mediated up-regulation of death receptor 5 and down-regulation of c-FLIP. Free Radic Biol Med 2008, 44(6):1055-1068.
90. Kim S., Lee T.J., Leem J., Choi K.S., Park J.W., Kwon T.K. Sanguinarine-induced apoptosis: generation of ROS, down-regulation of Bcl-2, c-FLIP, and synergy with TRAIL. J Cell Biochem 2008, 104(3):895-907.
91. Eccles S.A., Welch D.R. Metastasis: recent discoveries and novel treatment strategies. Lancet 2007, 369(9574):1742-1757.
92. Simpson C.D., Anyiwe K., Schimmer A.D. Anoikis resistance and tumor metastasis. Cancer Lett 2008, 272(2):177-185.
93. Mawji I.A., Simpson C.D., Gronda M., Williams M.A., Hurren R., Henderson C.J., et al. A chemical screen identifies anisomycin as an anoikis sensitizer that functions by decreasing FLIP protein synthesis. Cancer Res 2007, 67(17):8307-8315.
94. Stupack D.G., Teitz T., Potter M.D., Mikolon D., Houghton P.J., Kidd V.J., et al. Potentiation of neuroblastoma metastasis by loss of caspase-8. Nature 2006, 439(7072):95-99.
95. Laguinge L.M., Samara R.N., Wang W., El-Deiry W.S., Corner G., Augenlicht L., et al. DR5 receptor mediates anoikis in human colorectal carcinoma cell lines. Cancer Res 2008, 68(3):909-917.
96. Woods N.T., Yamaguchi H., Lee F.Y., Bhalla K.N., Wang H.G. Anoikis, initiated by Mcl-1 degradation and Bim induction, is deregulated during oncogenesis. Cancer Res 2007, 67(22):10744-10752.
97. Berezovskaya O., Schimmer A.D., Glinskii A.B., Pinilla C., Hoffman R.M., Reed J.C., et al. Increased expression of apoptosis inhibitor protein XIAP contributes to anoikis resistance of circulating human prostate cancer metastasis precursor cells. Cancer Res 2005, 65(6):2378-2386.
98. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133(4):704-715.
99. Onder T.T., Gupta P.B., Mani S.A., Yang J., Lander E.S., Weinberg R.A. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 2008, 68(10):3645-3654.
100. Wu W.S., Heinrichs S., Xu D., Garrison S.P., Zambetti G.P., Adams J.M., et al. Slug antagonizes p53-mediated apoptosis of hematopoietic progenitors by repressing puma. Cell 2005, 123(4):641-653.
101. Kurrey N.K., Jalgaonkar S.P., Joglekar A.V., Ghanate A.D., Chaskar P.D., Doiphode R.Y., et al. Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells 2009, 27(9):2059-2068.
102. Marotta L.L., Polyak K. Cancer stem cells: a model in the making. Curr Opin Genet Dev 2009 Feb, 19(1):44-50.