Molecular targeting of TRF2 suppresses the growth and tumorigenesis of glioblastoma stem cells

GLIA

Volumn 62, Issue 10, 2014, Pages 1687-1698

  Bai, Yun ^a,b   Lathia, Justin D ^c   Zhang, Peisu ^b   Flavahan, William ^c   Rich, Jeremy N ^c   Mattson, Mark P ^b  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Cancer stem cells; Glioblastoma; Telomeres; Transcriptional repression

Indexed keywords

BETA TUBULIN; LENTIVIRUS VECTOR; MESSENGER RNA; PROTEIN P53; SHORT HAIRPIN RNA; TELOMERIC REPEAT BINDING FACTOR 2; TEMOZOLOMIDE; ALKYLATING AGENT; DACARBAZINE; NERVE CELL ADHESION MOLECULE L1; RE1-SILENCING TRANSCRIPTION FACTOR; REPRESSOR PROTEIN; SMALL INTERFERING RNA; TERF2 PROTEIN, HUMAN; TUBB3 PROTEIN, HUMAN; TUBULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; CANCER INHIBITION; CANCER STEM CELL; CELL COUNT; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CELL RENEWAL; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; GENE MUTATION; GENE TARGETING; GLIA CELL; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MOUSE; NERVE CELL; NERVE FIBER; NEUROBLASTOMA CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; RNA INTERFERENCE; RNA SEQUENCE; STEM CELL; TELOMERE HOMEOSTASIS; VIRAL GENE DELIVERY SYSTEM; ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; BRAIN NEOPLASMS; CANCER TRANSPLANTATION; CARCINOGENESIS; DRUG EFFECTS; GENE VECTOR; GENETICS; METABOLISM; MOLECULARLY TARGETED THERAPY; NUDE MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; BRAIN NEOPLASMS; CARCINOGENESIS; CELL DIFFERENTIATION; CELL LINE, TUMOR; DACARBAZINE; GENETIC VECTORS; GLIOBLASTOMA; HUMANS; MICE, INBRED BALB C; MICE, NUDE; MOLECULAR TARGETED THERAPY; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; NEURAL CELL ADHESION MOLECULE L1; REPRESSOR PROTEINS; RNA, MESSENGER; RNA, SMALL INTERFERING; TELOMERIC REPEAT BINDING PROTEIN 2; TUBULIN;

EID: 84906322141     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22708     Document Type: Article

References (67)

1. Amoureux MC, Coulibaly B, Chinot O, Loundou A, Metellus P, Rougon G, Figarella-Branger D. 2010. Polysialic acid neural cell adhesion molecule (PSA-NCAM) is an adverse prognosis factor in glioblastoma, and regulates olig2 expression in glioma cell lines. BMC Cancer 10:91.
2. Ballas N, Grunseich C, Lu DD, Speh JC, Mandel G. 2005. REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 121:645-657.
3. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. 2006. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756-760.
4. Bibel M, Richter J, Schrenk K, Tucker KL, Staiger V, Korte M, Goetz M, Barde YA. 2004. Differentiation of mouse embryonic stem cells into a defined neuronal lineage. Nat Neurosci 7:1003-1009.
5. Biroccio A, Rizzo A, Elli R, Koering CE, Belleville A, Benassi B, Leonetti C, Stevens MF, D'Incalci M, Zupi G, Gilson E. 2006. TRF2 inhibition triggers apoptosis and reduces tumourigenicity of human melanoma cells. Eur J Cancer 42:1881-1888.
6. Blanco R, Muñoz P, Flores JM, Klatt P, Blasco MA. 2007. Telomerase abrogation dramatically accelerates TRF2-induced epithelial carcinogenesis. Genes Dev 21:206-220.
7. Blough MD Beauchamp DC, Westgate MR, Kelly JJ, Cairncross JG. 2011. Effect of aberrant p53 function on temozolomide sensitivity of glioma cell lines and brain tumor initiating cells from glioblastoma. J Neurooncol 102:1-7.
8. Buscemi G, Zannini L, Fontanella E, Lecis D, Lisanti S, Delia D. 2009. The shelterin protein TRF2 inhibits Chk2 activity at telomeres in the absence of DNA damage. Curr Biol 19:874-879.
9. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA. 2008. A transcriptome database for astrocytes, neurons, and oligodendrocytes: A new resource for understanding brain development and function. J Neurosci 28:264-278.
10. Cheng L, Wu Q, Huang Z, Guryanova OA, Huang Q, Shou W, Rich JN, Bao S. 2011. L1CAM regulates DNA damage checkpoint response of glioblastoma stem cells through NBS1. EMBO J 30:800-813.
11. Cherry JF, Carlson AL, Benarba FL, Sommerfeld SD, Verma D, Loers G, Kohn J, Schachner M, Moghe PV. 2012. Oriented, multimeric biointerfaces of the L1 cell adhesion molecule: An approach to enhance neuronal and neural stem cell functions on 2-D and 3-D polymer substrates. Biointerphases 7(1-4):22.
12. Chong JA, Tapia-Ramírez J, Kim S, Toledo-Aral JJ, Zheng Y, Boutros MC, Altshuller YM, Frohman MA, Kraner SD, Mandel G. 1995. REST: A mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80:949-957.
13. Conti L, Crisafulli L, Caldera V, Tortoreto M, Brilli E, Conforti P, Zunino F, Magrassi L, Schiffer D, Cattaneo E. 2012. REST controls self-renewal and tumorigenic competence of human glioblastoma cells. PLoS One 7:e38486.
14. Coulson JM. 2005. Transcriptional regulation: cancer, neurons and the REST. Curr Biol 15:R665-R668.
15. Cui YF, Hargus G, Xu JC, Schmid JS, Shen YQ, Glatzel M, Schachner M, Bernreuther C. 2010. Embryonic stem cell-derived L1 overexpressing neural aggregates enhance recovery in Parkinsonian mice. Brain 133:189-204.
16. Cui YF, Xu JC, Hargus G, Jakovcevski I, Schachner M, Bernreuther C. 2011. Embryonic stem cell-derived L1 overexpressing neural aggregates enhance recovery after spinal cord injury in mice. PLoS One 6:e17126.
17. Dasari VR, Kaur K, Velpula KK, Gujrati M, Fassett D, Klopfenstein JD, Dinh DH, Rao JS. 2010. Upregulation of PTEN in glioma cells by cord blood mesenchymal stem cells inhibits migration via downregulation of the PI3K/Akt pathway. PLoS One 5:e10350.
18. de Lange T. 2005. Shelterin: The protein complex that shapes and safeguards human telomeres. Genes Dev 19:2100-2110.
19. Diehl MC, Idowu MO, Kimmelshue KN, York TP, Jackson-Cook CK, Turner KC, Holt SE, Elmore LW. 2011. Elevated TRF2 in advanced breast cancers with short telomeres. Breast Cancer Res Treat 127:623-630.
20. Dong W, Shen R, Wang Q, Gao Y, Qi X, Jiang H, Yao J, Lin X, Wu Y, Wang L. 2009. Sp1 upregulates expression of TRF2 and TRF2 inhibition reduces tumorigenesis in human colorectal carcinoma cells. Cancer Biol Ther 8:2166-2174.
21. Flavahan WA, Wu Q, Hitomi M, Rahim N, Kim Y, Sloan AE, Weil RJ, Nakano I, Sarkaria JN, Stringer BW, Day BW, Li M, Lathia JD, Rich JN, Hjelmeland AB. 2013. Brain tumor initiating cells adapt to restricted nutrition through preferential glucose uptake. Nat Neurosci 16:1373-1382.
22. Fujita K, Horikawa I, Mondal AM, Jenkins LM, Appella E, Vojtesek B, Bourdon JC, Lane DP, Harris CC. 2010. Positive feedback between p53 and TRF2 during telomere-damage signalling and cellular senescence. Nat Cell Biol 12:1205-1212.
23. Gabay L, Lowell S, Rubin LL, Anderson DJ. 2003. Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40:485-499.
24. Guichet PO, Bieche I, Teigell M, Serguera C, Rothhut B, Rigau V, Scamps F, Ripoll C, Vacher S, Taviaux S, Chevassus H, Duffau H, Mallet J, Susini A, Joubert D, Bauchet L, Hugnot JP. 2013. Cell death and neuronal differentiation of glioblastoma stem-like cells induced by neurogenic transcription factors. Glia 61:225-239.
25. Gürsel DB, Berry N, Boockvar JA. 2012. The contribution of Notch signaling to glioblastoma via activation of cancer stem cell self-renewal: The role of the endothelial network. Neurosurgery 70:N19-N21.
26. Haar CP, Hebbar P, Wallace GC IV, Das A, Vandergrift WA III, Smith JA, Giglio P, Patel SJ, Ray SK, Banik NL. 2012. Drug resistance in glioblastoma: A mini review. Neurochem Res 37:1192-1200.
27. Hayashi MT, Cesare AJ, Fitzpatrick JA, Lazzerini-Denchi E, Karlseder J. 2012. A telomere-dependent DNA damage checkpoint induced by prolonged mitotic arrest. Nat Struct Mol Biol 19:387-394.
28. Hermisson M, Klumpp A, Wick W, Wischhusen J, Nagel G, Roos W, Kaina B, Weller M. 2006. O6-methylguanine DNA methyltransferase and p53 status predict temozolomide sensitivity in human malignant glioma cells. J Neurochem 96:766-776.
29. Kallunki P, Edelman GM Jones, FS. 1997. Tissue-specific expression of the L1 cell adhesion molecule is modulated by the neural restrictive silencer element. J Cell Biol 138:1343-1354.
30. Kamal MM, Sathyan P, Singh SK, Zinn PO, Marisetty AL, Liang S, Gumin J, El-Mesallamy HO, Suki D, Colman H, Fuller GN, Lang FF, Majumder S. 2012. REST regulates oncogenic properties of glioblastoma stem cells. Stem Cells 30:405-414.
31. Karlseder J, Hoke K, Mirzoeva OK, Bakkenist C, Kastan MB, Petrini JH, de Lange T. 2004. The telomeric protein TRF2 binds the ATM kinase and can inhibit the ATM-dependent DNA damage response. PLoS Biol 2:E240.
32. Lathia JD, Gallagher J, Myers JT, Li M, Vasanji A, McLendon RE, Hjelmeland AB, Huang AY, Rich JN. 2011a. Direct in vivo evidence for tumor propagation by glioblastoma cancer stem cells. PLoS One 6:e24807.
33. Lathia JD, Hitomi M, Gallagher J, Gadani SP, Adkins J, Vasanji A, Liu L, Eyler CE, Heddleston JM, Wu Q, Minhas S, Soeda A, Hoeppner DJ, Ravin R, McKay RD, McLendon RE, Corbeil D, Chenn A, Hjelmeland AB, Park DM, Rich JN. 2011b. Distribution of CD133 reveals glioma stem cells self-renew through symmetric and asymmetric cell divisions. Cell Death Dis 1;2:e200.
34. Li Z, Bao S, Wu Q, Wang H, Eyler C, Sathornsumetee S, Shi Q, Cao Y, Lathia J, McLendon RE, Hjelmeland AB, Rich JN. 2009. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 15:501-513.
35. Lietz M, Bach K, Thiel G. 2001. Biological activity of RE-1 silencing transcription factor (REST) towards distinct transcriptional activators. Eur J Neurosci 14:1303-1312.
36. Ligon KL, Alberta JA, Kho AT, Weiss J, Kwaan MR, Nutt CL, Louis DN, Stiles CD, Rowitch DH. 2004. The oligodendroglial lineage marker OLIG2 is universally expressed in diffuse gliomas. J Neuropathol Exp Neurol 63:499-509.
37. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS. 2006. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 5:67.
38. Lottaz C, Beier D, Meyer K, Kumar P, Hermann A, Schwarz J, Junker M, Oefner PJ, Bogdahn U, Wischhusen J, Spang R, Storch A, Beier CP. 2010. Transcriptional profiles of CD133+ and CD133- glioblastoma-derived cancer stem cell lines suggest different cells of origin. Cancer Res 70:2030-2040.
39. Maness PF, Schachner M. 2007. Neural recognition molecules of the immunoglobulin superfamily: Signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10:19-26.
40. Marian CO, Cho SK, McEllin BM, Maher EA, Hatanpaa KJ, Madden CJ, Mickey BE, Wright WE, Shay JW, Bachoo RM. 2010. The telomerase antagonist, imetelstat, efficiently targets glioblastoma tumor-initiating cells leading to decreased proliferation and tumor growth. Clin Cancer Res 16:154-163.
41. Merle P, Evrard B, Petitjean A, Lehn JM, Teulade-Fichou MP, Chautard E, De Cian A, Guittat L, Tran PL, Mergny JL, Verrelle P, Tchirkov A. 2011. Telomere targeting with a new G4 ligand enhances radiation-induced killing of human glioblastoma cells. Mol Cancer Ther 10:1784-1795.
42. Nagasawa DT, Chow F, Yew A, Kim W, Cremer N, Yang I. 2012. Temozolomide and other potential agents for the treatment of glioblastoma multiforme. Neurosurg Clin N Am 23:307-322.
43. Ning H, Li T, Zhao L, Li T, Li J, Liu J, Liu Z, Fan D. 2006. TRF2 promotes multidrug resistance in gastric cancer cells. Cancer Biol Ther 5:950-956.
44. Otto SJ, McCorkle SR, Hover J, Conaco C, Han JJ, Impey S, Yochum GS, Dunn JJ, Goodman RH, Mandel G. 2007. A new binding motif for the transcriptional repressor REST uncovers large gene networks devoted to neuronal functions. J Neurosci 27:6729-6739.
45. Preusser M, de Ribaupierre S, Wöhrer A, Erridge SC, Hegi M, Weller M, Stupp R. 2011. Current concepts and management of glioblastoma. Ann Neurol 70:9-21.
46. Rhee W, Ray S, Yokoo H, Hoane ME, Lee CC, Mikheev AM, Horner PJ, Rostomily RC. 2009. Quantitative analysis of mitotic Olig2 cells in adult human brain and gliomas: Implications for glioma histogenesis and biology. Glia 57:510-523.
47. Sato A, Sunayama J, Matsuda K, Seino S, Suzuki K, Watanabe E, Tachibana K, Tomiyama A, Kayama T, Kitanaka C. 2011. MEK-ERK signaling dictates DNA-repair gene MGMT expression and temozolomide resistance of stem-like glioblastoma cells via the MDM2-p53 axis. Stem Cells 29:1942-1951.
48. Schäfer MK, Frotscher M. 2012. Role of L1CAM for axon sprouting and branching. Cell Tissue Res 349:39-48.
49. Schilling SH, Hjelmeland AB, Radiloff DR, Liu IM, Wakeman TP, Fielhauer JR, Foster EH, Lathia JD, Rich JN, Wang XF, Datto MB. 2009. NDRG4 is required for cell cycle progression and survival in glioblastoma cells. J Biol Chem 284:25160-25169.
50. Siesser PF, Maness PF. 2009. L1 cell adhesion molecules as regulators of tumor cell invasiveness. Cell Adh Migr 3:275-277.
51. Silvestre DC, Pineda JR, Hoffschir F, Studler JM, Mouthon MA, Pflumio F, Junier MP, Chneiweiss H, Boussin FD. 2011. Alternative lengthening of telomeres in human glioma stem cells. Stem Cells 29:440-451.
52. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. 2003. Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821-5828.
53. Srivenugopal KS, Shou J, Mullapudi SR, Lang FF Jr, Rao JS, Ali-Osman F. 2001. Enforced expression of wild-type p53 curtails the transcription of the O(6)-methylguanine-DNA methyltransferase gene in human tumor cells and enhances their sensitivity to alkylating agents. Clin Cancer Res 7:1398-1409.
54. Stagno D'Alcontres M, Mendez-Bermudez A, Foxon JL, Royle NJ, Salomoni P. 2007. Lack of TRF2 in ALT cells causes PML-dependent p53 activation and loss of telomeric DNA. J Cell Biol 179: 855-867.
55. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA, Gijtenbeek J, Marosi C, Vecht CJ, Mokhtari K, Wesseling P, Villa S, Eisenhauer E, Gorlia T, Weller M, Lacombe D, Cairncross JG, Mirimanoff RO; European Organisation for Research and Treatment of Cancer Brain Tumour and Radiation Oncology Groups; National Cancer Institute of Canada Clinical Trials Group. 2009. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 10:459-466.
56. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, randes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO; European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group. 2005. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987-996.
57. Sun YM, Greenway DJ, Johnson R, Street M, Belyaev ND, Deuchars J, Bee T, Wilde S, Buckley NJ. 2005. Distinct profiles of REST interactions with its target genes at different stages of neuronal development. Mol Biol Cell 16:5630-5638.
58. Suzuki T, Izumoto S, Fujimoto Y, Maruno M, Ito Y, Yoshimine T. 2005. Clinicopathological study of cellular proliferation and invasion in gliomatosis cerebri: Important role of neural cell adhesion molecule L1 in tumour invasion. J Clin Pathol 58:166-171.
59. Tamura K, Aoyagi M, Wakimoto H, Ando N, Nariai T, Yamamoto M, Ohno K. 2010. Accumulation of CD133-positive glioma cells after high-dose irradiation by Gamma Knife surgery plus external beam radiation. J Neurosurg 113:310-318.
60. Thomas RP, Recht L, Nagpal S. 2013. Advances in the management of glioblastoma: The role of temozolomide and MGMT testing. Clin Pharmacol 5:1-9.
61. Wagoner MP, Roopra A. 2012. A REST derived gene signature stratifies glioblastomas into chemotherapy resistant and responsive disease. BMC Genomics 13:686.
62. Wakimoto H, Kesari S, Farrell CJ, Curry WT Jr, Zaupa C, Aghi M, Kuroda T, Stemmer-Rachamimov A, Shah K, Liu TC, Jeyaretna DS, Debasitis J, Pruszak J, Martuza RL, Rabkin SD. 2009. Human glioblastoma-derived cancer stem cells: Establishment of invasive glioma models and treatment with oncolytic herpes simplex virus vectors. Cancer Res 69:3472-3481.
63. Wang J, Wakeman TP, Lathia JD, Hjelmeland AB, Wang XF, White RR, Rich JN, Sullenger BA. 2010. Notch promotes radioresistance of glioma stem cells. Stem Cells 28:17-28.
64. Xue H, Wu S, Papadeas ST, Spusta S, Swistowska AM, MacArthur CC, Mattson MP, Maragakis NJ, Capecchi MR, Rao MS, Zeng X, Liu Y. 2009. A targeted neuroglial reporter line generated by homologous recombination in human embryonic stem cells. Stem Cells 27:1836-1846.
65. Yan X, Ma L, Yi D, Yoon JG, Diercks A, Foltz G, Price ND, Hood LE, Tian Q. 2011. A CD133-related gene expression signature identifies an aggressive glioblastoma subtype with excessive mutations. Proc Natl Acad Sci USA 108:1591-1596.
66. Zhang P, Pazin MJ, Schwartz CM, Becker KG, Wersto RP, Dilley CM, Mattson MP. 2008. Nontelomeric TRF2-REST interaction modulates neuronal gene silencing and fate of tumor and stem cells. Curr Biol 18:1489-1494.
67. Zheng H, Ying H, Yan H, Kimmelman AC, Hiller DJ, Chen AJ, Perry SR, Tonon G, Chu GC, Ding Z, Stommel JM, Dunn KL, Wiedemeyer R, You MJ, Brennan C, Wang YA, Ligon KL, Wong WH, Chin L, DePinho RA. 2008. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 455:1129-1133.