Histone deacetylase inhibition as an anticancer telomerase-targeting strategy

International Journal of Cancer

Volumn 129, Issue 12, 2011, Pages 2765-2774

  Rahman, Ruman ^a   Grundy, Richard ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

epigenetics; histone deacetylase inhibitors; hTERT; telomerase

Indexed keywords

AMIDOHYDROLASE INHIBITOR; BUTYRIC ACID; GEMCITABINE; HISTONE DEACETYLASE INHIBITOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMATINIB; IMETELSTAT; MGCD 103; PANOBINOSTAT; ROMIDEPSIN; TELOMERASE REVERSE TRANSCRIPTASE; TRANSFORMING GROWTH FACTOR BETA; TRICHOSTATIN A; UNCLASSIFIED DRUG; VALPROIC ACID; VASCULOTROPIN; VORINOSTAT; ANTINEOPLASTIC AGENT; TELOMERASE; TERT PROTEIN, HUMAN;

ACETYLATION; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CELL CULTURE; CANCER INHIBITION; CANCER STEM CELL TRANSPLANTATION; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL TRIAL (TOPIC); CUTANEOUS T CELL LYMPHOMA; DEACETYLATION; DRUG BINDING SITE; DRUG TARGETING; DRUG TOLERABILITY; EPIGENETICS; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PANCREAS CANCER; PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SYNTHESIS INHIBITION; REVIEW; SOLID TUMOR; STEM CELL TRANSPLANTATION; TRANSCRIPTION REGULATION; TUMOR RESISTANCE; CANCER STEM CELL; CELL DEATH; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; METABOLISM; MOLECULARLY TARGETED THERAPY; TUMOR CELL CULTURE;

ANTINEOPLASTIC AGENTS; CELL DEATH; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HISTONE DEACETYLASE INHIBITORS; HUMANS; MOLECULAR TARGETED THERAPY; NEOPLASTIC STEM CELLS; TELOMERASE; TUMOR CELLS, CULTURED;

EID: 84855178148     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.26241     Document Type: Review

References (95)

1. Richon VM, O'Brien JP,. Histone deacetylase inhibitors: a new class of potential therapeutic agents for cancer treatment. Clin Cancer Res 2002; 8: 662-4. (Pubitemid 34742091)
2. Khaw AK, Silasudjana M, Banerjee B, Suzuki M, Baskar R, Hande MP,. Inhibition of telomerase activity and human telomerase reverse transcriptase gene expression by histone deacetylase inhibitor in human brain cancer cells. Mutat Res 2007; 625: 134-44. (Pubitemid 350016112)
3. Li XN, Shu Q, Su JM, Perlaky L, Blaney SM, Lau CC,. Valproic acid induces growth arrest, apoptosis, and senescence in medulloblastomas by increasing histone hyperacetylation and regulating expression of p21Cip1, CDK4, and CMYC. Mol Cancer Ther 2005; 4: 1912-22. (Pubitemid 43056974)
4. Gargiulo G, Minucci S,. Epigenomic profiling of cancer cells. Int J Biochem Cell Biol 2009; 41: 127-35.
5. Johnstone RW, Ruefli AA, Lowe SW,. Apoptosis: a link between cancer genetics and chemotherapy. Cell 2002; 108: 153-64. (Pubitemid 34161136)
6. Marks PA, Rifkind RA, Richon VM, Breslow R,. Inhibitors of histone deacetylase are potentially effective anticancer agents. Clin Cancer Res 2001; 7: 759-60. (Pubitemid 32708707)
7. Metivier R, Penot G, Hubner MR, Reid G, Brand H, Kos M, Gannon F,. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 2003; 115: 751-63. (Pubitemid 38030303)
8. Buchwald M, Kramer OH, Heinzel T,. HDACi-targets beyond chromatin. Cancer Lett 2009; 280: 160-7.
9. Dokmanovic M, Clarke C, Marks PA,. Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res 2007; 5: 981-9. (Pubitemid 350080267)
10. Gregoretti IV, Lee YM, Goodson HV,. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J Mol Biol 2004; 338: 17-31. (Pubitemid 38429783)
11. Dokmanovic M, Marks PA,. Prospects: histone deacetylase inhibitors. J Cell Biochem 2005; 96: 293-304. (Pubitemid 41437862)
12. Marks PA, Breslow R,. Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat Biotechnol 2007; 25: 84-90. (Pubitemid 46087907)
13. Rosato RR, Grant S,. Histone deacetylase inhibitors: insights into mechanisms of lethality. Expert Opin Ther Targets 2005; 9: 809-24. (Pubitemid 41131680)
14. Minucci S, Pelicci PG,. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 2006; 6: 38-51. (Pubitemid 43054973)
15. Xu WS, Parmigiani RB, Marks PA,. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 2007; 26: 5541-52. (Pubitemid 47255934)
16. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M,. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009; 325: 834-40.
17. Sakuma T, Uzawa K, Onda T, Shiiba M, Yokoe H, Shibahara T, Tanzawa H,. Aberrant expression of histone deacetylase 6 in oral squamous cell carcinoma. Int J Oncol 2006; 29: 117-24.
18. Wilson AJ, Byun DS, Popova N, Murray LB, L'Italien K, Sowa Y, Arango D, Velcich A, Augenlicht LH, Mariadason JM,. Histone deacetylase 3 (HDAC3) and other class I HDACs regulate colon cell maturation and p21 expression and are deregulated in human colon cancer. J Biol Chem 2006; 281: 13548-58. (Pubitemid 43855268)
19. Zhang Z, Chen CQ, Manev H,. DNA methylation as an epigenetic regulator of neural 5-lipoxygenase expression: evidence in human NT2 and NT2-N cells. J Neurochem 2004; 88: 1424-30. (Pubitemid 38366918)
20. Zhu P, Martin E, Mengwasser J, Schlag P, Janssen KP, Gottlicher M,. Induction of HDAC2 expression upon loss of APC in colorectal tumorigenesis. Cancer Cell 2004; 5: 455-63. (Pubitemid 38610247)
21. Kim HR, Kim EJ, Yang SH, Jeong ET, Park C, Lee JH, Youn MJ, So HS, Park R,. Trichostatin A induces apoptosis in lung cancer cells via simultaneous activation of the death receptor-mediated and mitochondrial pathway? Exp Mol Med 2006; 38: 616-24. (Pubitemid 46103583)
22. Qu W, Kang YD, Zhou MS, Fu LL, Hua ZH, Wang LM,. Experimental study on inhibitory effects of histone deacetylase inhibitor MS-275 and TSA on bladder cancer cells. Urol Oncol 2009; 28: 648-54.
23. Wu Y, Guo SW,. Histone deacetylase inhibitors trichostatin A and valproic acid induce cell cycle arrest and p21 expression in immortalized human endometrial stromal cells. Eur J Obstet Gynecol Reprod Biol 2008; 137: 198-203. (Pubitemid 351423449)
24. Yin D, Ong JM, Hu J, Desmond JC, Kawamata N, Konda BM, Black KL, Koeffler HP,. Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor: effects on gene expression and growth of glioma cells in vitro and in vivo. Clin Cancer Res 2007; 13: 1045-52. (Pubitemid 46340384)
25. Camphausen K, Cerna D, Scott T, Sproull M, Burgan WE, Cerra MA, Fine H, Tofilon PJ,. Enhancement of in vitro and in vivo tumor cell radiosensitivity by valproic acid. Int J Cancer 2005; 114: 380-6. (Pubitemid 40279957)
26. Dowdy SC, Jiang S, Zhou XC, Hou X, Jin F, Podratz KC, Jiang SW,. Histone deacetylase inhibitors and paclitaxel cause synergistic effects on apoptosis and microtubule stabilization in papillary serous endometrial cancer cells. Mol Cancer Ther 2006; 5: 2767-76. (Pubitemid 44849003)
27. Ecke I, Petry F, Rosenberger A, Tauber S, Monkemeyer S, Hess I, Dullin C, Kimmina S, Pirngruber J, Johnsen SA, Uhmann A, Nitzki F, et al. Antitumor effects of a combined 5-aza-2′deoxycytidine and valproic acid treatment on rhabdomyosarcoma and medulloblastoma in Ptch mutant mice. Cancer Res 2009; 69: 887-95.
28. Kim IA, Shin JH, Kim IH, Kim JH, Kim JS, Wu HG, Chie EK, Ha SW, Park CI, Kao GD,. Histone deacetylase inhibitor-mediated radiosensitization of human cancer cells: class differences and the potential influence of p53. Clin Cancer Res 2006; 12: 940-9. (Pubitemid 43259877)
29. Gottlicher M, Minucci S, Zhu P, Kramer OH, Schimpf A, Giavara S, Sleeman JP, Lo Coco F, Nervi C, Pelicci PG, Heinzel T,. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 2001; 20: 6969-78. (Pubitemid 34062289)
30. Qiu L, Burgess A, Fairlie DP, Leonard H, Parsons PG, Gabrielli BG,. Histone deacetylase inhibitors trigger a G2 checkpoint in normal cells that is defective in tumor cells. Mol Biol Cell 2000; 11: 2069-83. (Pubitemid 30408065)
31. Rasheed WK, Johnstone RW, Prince HM,. Histone deacetylase inhibitors in cancer therapy. Expert Opin Investig Drugs 2007; 16: 659-78. (Pubitemid 46729100)
32. Duvic M, Vu J,. Vorinostat: a new oral histone deacetylase inhibitor approved for cutaneous T-cell lymphoma. Expert Opin Investig Drugs 2007; 16: 1111-20. (Pubitemid 47074165)
33. Zain J, O'Connor OA,. Targeting histone deacetyalses in the treatment of B- and T-cell malignancies. Invest New Drugs 2010; 28 (Suppl 1): S58-S78.
34. Tan J, Cang S, Ma Y, Petrillo RL, Liu D,. Novel histone deacetylase inhibitors in clinical trials as anti-cancer agents. J Hematol Oncol 2010; 3: 5.
35. Hurwitz H,. Phase I/II: the oral isotype-selective HDAC inhibitor MGCD0103 in combination with gemcitabine (Gem) in patients (pts) with refractory solid tumors. J Clin Oncol 2008; 26: 4625.
36. Johnstone RW,. Histone-deacetylase inhibitors: novel drugs for the treatment of cancer. Nat Rev Drug Discov 2002; 1: 287-99. (Pubitemid 37361445)
37. Carew JS, Giles FJ, Nawrocki ST,. Histone deacetylase inhibitors: mechanisms of cell death and promise in combination cancer therapy. Cancer Lett 2008; 269: 7-17.
38. Imai T, Adachi S, Nishijo K, Ohgushi M, Okada M, Yasumi T, Watanabe K, Nishikomori R, Nakayama T, Yonehara S, Toguchida J, Nakahata T,. FR901228 induces tumor regression associated with induction of Fas ligand and activation of Fas signaling in human osteosarcoma cells. Oncogene 2003; 22: 9231-42. (Pubitemid 38122035)
39. Rosato RR, Almenara JA, Dai Y, Grant S,. Simultaneous activation of the intrinsic and extrinsic pathways by histone deacetylase (HDAC) inhibitors and tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) synergistically induces mitochondrial damage and apoptosis in human leukemia cells. Mol Cancer Ther 2003; 2: 1273-84.
40. Sonnemann J, Hartwig M, Plath A, Saravana Kumar K, Muller C, Beck JF,. Histone deacetylase inhibitors require caspase activity to induce apoptosis in lung and prostate carcinoma cells. Cancer Lett 2006; 232: 148-60. (Pubitemid 43170964)
41. Sonnemann J, Kumar KS, Heesch S, Muller C, Hartwig C, Maass M, Bader P, Beck JF,. Histone deacetylase inhibitors induce cell death and enhance the susceptibility to ionizing radiation, etoposide, and TRAIL in medulloblastoma cells. Int J Oncol 2006; 28: 755-66.
42. Deroanne CF, Bonjean K, Servotte S, Devy L, Colige A, Clausse N, Blacher S, Verdin E, Foidart JM, Nusgens BV, Castronovo V,. Histone deacetylases inhibitors as anti-angiogenic agents altering vascular endothelial growth factor signaling. Oncogene 2002; 21: 427-36. (Pubitemid 34123805)
43. Qian DZ, Kachhap SK, Collis SJ, Verheul HM, Carducci MA, Atadja P, Pili R,. Class II histone deacetylases are associated with VHL-independent regulation of hypoxia-inducible factor 1α. Cancer Res 2006; 66: 8814-21. (Pubitemid 44449199)
44. Kim MS, Kwon HJ, Lee YM, Baek JH, Jang JE, Lee SW, Moon EJ, Kim HS, Lee SK, Chung HY, Kim CW, Kim KW,. Histone deacetylases induce angiogenesis by negative regulation of tumor suppressor genes. Nat Med 2001; 7: 437-43. (Pubitemid 32298546)
45. Kim TH, Barrera LO, Ren B,. ChIP-chip for genome-wide analysis of protein binding in mammalian cells. Curr Protoc Mol Biol 2007; Chapter 21:Unit 21.13.
46. Masutomi K, Yu EY, Khurts S, Ben-Porath I, Currier JL, Metz GB, Brooks MW, Kaneko S, Murakami S, DeCaprio JA, Weinberg RA, Stewart SA, et al. Telomerase maintains telomere structure in normal human cells. Cell 2003; 114: 241-53. (Pubitemid 36936917)
47. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL, Shay JW,. Specific association of human telomerase activity with immortal cells and cancer. Science 1994; 266: 2011-15.
48. Liu JP,. Studies of the molecular mechanisms in the regulation of telomerase activity. FASEB J 1999; 13: 2091-104.
49. Won J, Yim J, Kim TK,. Sp1 and Sp3 recruit histone deacetylase to repress transcription of human telomerase reverse transcriptase (hTERT) promoter in normal human somatic cells. J Biol Chem 2002; 277: 38230-8. (Pubitemid 35154677)
50. Horikawa I, Cable PL, Afshari C, Barrett JC,. Cloning and characterization of the promoter region of human telomerase reverse transcriptase gene. Cancer Res 1999; 59: 826-30. (Pubitemid 29086735)
51. Oh S, Song YH, Kim UJ, Yim J, Kim TK,. In vivo and in vitro analyses of Myc for differential promoter activities of the human telomerase (hTERT) gene in normal and tumor cells. Biochem Biophys Res Commun 1999; 263: 361-5. (Pubitemid 29467201)
52. Wu KJ, Grandori C, Amacker M, Simon-Vermot N, Polack A, Lingner J, Dalla-Favera R,. Direct activation of TERT transcription by c-MYC. Nat Genet 1999; 21: 220-4. (Pubitemid 29070372)
53. Cong YS, Bacchetti S,. Histone deacetylation is involved in the transcriptional repression of hTERT in normal human cells. J Biol Chem 2000; 275: 35665-8.
54. Janknecht R,. On the road to immortality: hTERT upregulation in cancer cells. FEBS Lett 2004; 564: 9-13. (Pubitemid 38490693)
55. Luscher B,. Function and regulation of the transcription factors of the Myc/Max/Mad network. Gene 2001; 277: 1-14. (Pubitemid 32972106)
56. Greenberg RA, O'Hagan RC, Deng H, Xiao Q, Hann SR, Adams RR, Lichtsteiner S, Chin L, Morin GB, DePinho RA,. Telomerase reverse transcriptase gene is a direct target of c-Myc but is not functionally equivalent in cellular transformation. Oncogene 1999; 18: 1219-26. (Pubitemid 29085995)
57. Takakura M, Kyo S, Kanaya T, Hirano H, Takeda J, Yutsudo M, Inoue M,. Cloning of human telomerase catalytic subunit (hTERT) gene promoter and identification of proximal core promoter sequences essential for transcriptional activation in immortalized and cancer cells. Cancer Res 1999; 59: 551-7. (Pubitemid 29076049)
58. Gunes C, Lichtsteiner S, Vasserot AP, Englert C,. Expression of the hTERT gene is regulated at the level of transcriptional initiation and repressed by Mad1. Cancer Res 2000; 60: 2116-21. (Pubitemid 30225170)
59. Xu D, Popov N, Hou M, Wang Q, Bjorkholm M, Gruber A, Menkel AR, Henriksson M,. Switch from Myc/Max to Mad1/Max binding and decrease in histone acetylation at the telomerase reverse transcriptase promoter during differentiation of HL60 cells. Proc Natl Acad Sci USA 2001; 98: 3826-31. (Pubitemid 32249856)
60. Casillas MA, Brotherton SL, Andrews LG, Ruppert JM, Tollefsbol TO,. Induction of endogenous telomerase (hTERT) by c-Myc in WI-38 fibroblasts transformed with specific genetic elements. Gene 2003; 316: 57-65. (Pubitemid 37249353)
61. Kyo S, Takakura M, Taira T, Kanaya T, Itoh H, Yutsudo M, Ariga H, Inoue M,. Sp1 cooperates with c-Myc to activate transcription of the human telomerase reverse transcriptase gene (hTERT). Nucleic Acids Res 2000; 28: 669-77. (Pubitemid 30068249)
62. Hou M, Wang X, Popov N, Zhang A, Zhao X, Zhou R, Zetterberg A, Bjorkholm M, Henriksson M, Gruber A, Xu D,. The histone deacetylase inhibitor trichostatin A derepresses the telomerase reverse transcriptase (hTERT) gene in human cells. Exp Cell Res 2002; 274: 25-34.
63. Yang H, Kyo S, Takatura M, Sun L,. Autocrine transforming growth factor beta suppresses telomerase activity and transcription of human telomerase reverse transcriptase in human cancer cells. Cell Growth Differ 2001; 12: 119-27. (Pubitemid 32194901)
64. Bayne S, Liu JP,. Hormones and growth factors regulate telomerase activity in ageing and cancer. Mol Cell Endocrinol 2005; 240: 11-22. (Pubitemid 41133367)
65. Li H, Xu D, Li J, Berndt MC, Liu JP,. Transforming growth factor beta suppresses human telomerase reverse transcriptase (hTERT) by Smad3 interactions with c-Myc and the hTERT gene. J Biol Chem 2006; 281: 25588-600. (Pubitemid 44401948)
66. Chen CR, Kang Y, Siegel PM, Massague J,. E2F4/5 and p107 as Smad cofactors linking the TGFβ receptor to c-myc repression. Cell 2002; 110: 19-32. (Pubitemid 34874603)
67. Yagi K, Furuhashi M, Aoki H, Goto D, Kuwano H, Sugamura K, Miyazono K, Kato M,. c-myc is a downstream target of the Smad pathway. J Biol Chem 2002; 277: 854-61. (Pubitemid 34952127)
68. Feng XH, Liang YY, Liang M, Zhai W, Lin X,. Direct interaction of c-Myc with Smad2 and Smad3 to inhibit TGFβ-mediated induction of the CDK inhibitor p15(Ink4B). Mol Cell 2002; 9: 133-43. (Pubitemid 34127777)
69. Lacerte A, Korah J, Roy M, Yang XJ, Lemay S, Lebrun JJ,. Transforming growth factor-β inhibits telomerase through SMAD3 and E2F transcription factors. Cell Signal 2008; 20: 50-9. (Pubitemid 350138369)
70. Harley CB,. Telomerase and cancer therapeutics. Nat Rev Cancer 2008; 8: 167-79. (Pubitemid 351305939)
71. Shay JW, Wright WE,. Telomeres and telomerase in normal and cancer stem cells. FEBS Lett 2010; 584: 3819-25.
72. Suenaga M, Soda H, Oka M, Yamaguchi A, Nakatomi K, Shiozawa K, Kawabata S, Kasai T, Yamada Y, Kamihira S, Tei C, Kohno S,. Histone deacetylase inhibitors suppress telomerase reverse transcriptase mRNA expression in prostate cancer cells. Int J Cancer 2002; 97: 621-5. (Pubitemid 34087800)
73. Woo HJ, Lee SJ, Choi BT, Park YM, Choi YH,. Induction of apoptosis and inhibition of telomerase activity by trichostatin A, a histone deacetylase inhibitor, in human leukemic U937 cells. Exp Mol Pathol 2007; 82: 77-84. (Pubitemid 46038263)
74. Nakamura M, Saito H, Ebinuma H, Wakabayashi K, Saito Y, Takagi T, Nakamoto N, Ishii H,. Reduction of telomerase activity in human liver cancer cells by a histone deacetylase inhibitor. J Cell Physiol 2001; 187: 392-401. (Pubitemid 32378364)
75. Wu P, Meng L, Wang H, Zhou J, Xu G, Wang S, Xi L, Chen G, Wang B, Zhu T, Lu Y, Ma D,. Role of hTERT in apoptosis of cervical cancer induced by histone deacetylase inhibitor. Biochem Biophys Res Commun 2005; 335: 36-44. (Pubitemid 41350760)
76. Cesare AJ, Reddel RR,. Alternative lengthening of telomeres: models, mechanisms and implications. Nat Rev Genet 2010; 11: 319-30.
77. Rahman R, Osteso-Ibanez T, Hirst RA, Levesley J, Kilday JP, Quinn S, Peet A, O'Callaghan C, Coyle B, Grundy RG,. Histone deacetylase inhibition attenuates cell growth with associated telomerase inhibition in high-grade childhood brain tumor cells. Mol Cancer Ther 2010; 9: 2568-81.
78. Gui CY, Ngo L, Xu WS, Richon VM, Marks PA,. Histone deacetylase (HDAC) inhibitor activation of p21WAF1 involves changes in promoter-associated proteins, including HDAC1. Proc Natl Acad Sci USA 2004; 101: 1241-6. (Pubitemid 38182673)
79. Li H, Wu X,. Histone deacetylase inhibitor, Trichostatin A, activates p21WAF1/CIP1 expression through downregulation of c-myc and release of the repression of c-myc from the promoter in human cervical cancer cells. Biochem Biophys Res Commun 2004; 324: 860-7. (Pubitemid 39345594)
80. Castelo-Branco P, Zhang C, Lipman T, Fujitani M, Hansford L, Clarke I, Harley CB, Tressler R, Malkin D, Walker E, Kaplan DR, Dirks P, et al. Neural tumor-initiating cells have distinct telomere maintenance and can be safely targeted for telomerase inhibition. Clin Cancer Res 2011; 17: 111-21.
81. Marian CO, Cho SK, McEllin BM, Maher EA, Hatanpaa KJ, Madden CJ, Mickey BE, Wright WE, Shay JW, Bachoo RM,. The telomerase antagonist, imetelstat, efficiently targets glioblastoma tumor-initiating cells leading to decreased proliferation and tumor growth. Clin Cancer Res 2010; 16: 154-63.
82. Shervington A, Lu C, Patel R, Shervington L,. Telomerase downregulation in cancer brain stem cell. Mol Cell Biochem 2009; 331: 153-9.
83. Joseph I, Tressler R, Bassett E, Harley C, Buseman CM, Pattamatta P, Wright WE, Shay JW, Go NF,. The telomerase inhibitor imetelstat depletes cancer stem cells in breast and pancreatic cancer cell lines. Cancer Res 2010; 70: 9494-504.
84. Xu T, He K, Wang L, Goldkorn A,. Prostate tumor cells with cancer progenitor properties have high telomerase activity and are rapidly killed by telomerase interference. Prostate 2011. doi: 10.1002/pros.21355. [Epub ahead of print].
85. Gerber JM, Qin L, Kowalski J, Smith BD, Griffin CA, Vala MS, Collector MI, Perkins B, Zahurak M, Matsui W, Gocke CD, Sharkis SJ, et al. Characterization of chronic myeloid leukemia stem cells. Am J Hematol 2011; 86: 31-7.
86. Brennan SK, Wang Q, Tressler R, Harley C, Go N, Bassett E, Huff CA, Jones RJ, Matsui W,. Telomerase inhibition targets clonogenic multiple myeloma cells through telomere length-dependent and independent mechanisms. PLoS One 2010; 5: pii. e12487.
87. Coller HA, Sang L, Roberts JM,. A new description of cellular quiescence. PLoS Biol 2006; 4: e83.
88. Sang L, Coller HA, Roberts JM,. Control of the reversibility of cellular quiescence by the transcriptional repressor HES1. Science 2008; 321: 1095-100.
89. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, Wu L, Lindeman GJ, Visvader JE,. Generation of a functional mammary gland from a single stem cell. Nature 2006; 439: 84-8. (Pubitemid 43053633)
90. Bieniek R, Lazar AJ, Photopoulos C, Lyle S,. Sebaceous tumours contain a subpopulation of cells expressing the keratin 15 stem cell marker. Br J Dermatol 2007; 156: 378-80. (Pubitemid 46095971)
91. Gao MQ, Choi YP, Kang S, Youn JH, Cho NH,. CD24+ cells from hierarchically organized ovarian cancer are enriched in cancer stem cells. Oncogene 2010; 29: 2672-80.
92. Cleary ML,. Regulating the leukaemia stem cell. Best Pract Res Clin Haematol 2009; 22: 483-7.
93. Dembinski JL, Krauss S,. Characterization and functional analysis of a slow cycling stem cell-like subpopulation in pancreas adenocarcinoma. Clin Exp Metastasis 2009; 26: 611-23.
94. Zhang B, Strauss AC, Chu S, Li M, Ho Y, Shiang KD, Snyder DS, Huettner CS, Shultz L, Holyoake T, Bhatia R,. Effective targeting of quiescent chronic myelogenous leukemia stem cells by histone deacetylase inhibitors in combination with imatinib mesylate. Cancer Cell 2010; 17: 427-42.
95. Sikandar S, Dizon D, Shen X, Li Z, Besterman J, Lipkin SM,. The class I HDAC inhibitor MGCD0103 induces cell cycle arrest and apoptosis in colon cancer initiating cells by upregulating Dickkopf-1 and non-canonical Wnt signaling. Oncotarget 2010; 1: 596-605.