Induction of autophagy promotes differentiation of glioma-initiating cells and their radiosensitivity

International Journal of Cancer

Volumn 129, Issue 11, 2011, Pages 2720-2731

  Zhuang, Wenzhuo ^a   Li, Bingzong ^a   Long, Linmei ^a   Chen, Liesong ^a   Huang, Qiang ^a   Liang, Zhongqin ^a  

^a SOOCHOW UNIVERSITY   (China)

Author keywords

autophagy; differentiation; glioma initiating cells; radiosensitization

Indexed keywords

3 METHYLADENINE; BETA TUBULIN; CD133 ANTIGEN; GLIAL FIBRILLARY ACIDIC PROTEIN; NESTIN; RAPAMYCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CACHEXIA; CANCER MORTALITY; CANCER SURVIVAL; CARCINOGENICITY; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CELL RENEWAL; CELL TRANSPLANTATION; CELL VIABILITY; CHEMORADIOTHERAPY; CLONOGENESIS; CONTROLLED STUDY; GLIOBLASTOMA; GLIOMA CELL; GLIOMA INITIATING CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOSENSITIVITY; RADIOSENSITIZATION; TUMOR GROWTH;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; AUTOPHAGY; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL PROLIFERATION; GLIOBLASTOMA; HUMANS; MICE; NEOPLASTIC STEM CELLS; RADIATION TOLERANCE; SIROLIMUS; TUMOR CELLS, CULTURED; TUMOR STEM CELL ASSAY; X-RAYS;

EID: 80053302394     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25975     Document Type: Article

References (50)

1. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, Hahn WC, Ligon KL, Louis DN, Brennan C, Chin L, DePinho RA, et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 2007; 21: 2683-710. (Pubitemid 350070717)
2. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, Park JK, Fine HA,. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 2006; 9: 391-403. (Pubitemid 43668737)
3. Stiles CD, Rowitch DH,. Glioma stem cells: a midterm exam. Neuron 2008; 58: 832-46. (Pubitemid 351842757)
4. Lee J, Son MJ, Woolard K, Donin NM, Li A, Cheng CH, Kotliarova S, Kotliarov Y, Walling J, Ahn S, Kim M, Totonchy M, et al. Epigenetic-mediated dysfunction of the bone morphogenetic protein pathway inhibits differentiation of glioblastoma-initiating cells. Cancer Cell 2008; 13: 69-80. (Pubitemid 350309742)
5. Penuelas S, Anido J, Prieto-Sanchez RM, Folch G, Barba I, Cuartas I, Garcia-Dorado D, Poca MA, Sahuquillo J, Baselga J, Seoane J,. TGF-beta increases glioma-initiating cell self-renewal through the induction of LIF in human glioblastoma. Cancer Cell 2009; 15: 315-27.
6. Zheng H, Ying H, Yan H, Kimmelman AC, Hiller DJ, Chen AJ, Perry SR, Tonon G, Chu GC, Ding Z, Stommel JM, Dunn KL, et al. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 2008; 455: 1129-33.
7. Liang C, Feng P, Ku B, Dotan I, Canaani D, Oh BH, Jung JU,. Autophagic and tumour suppressor activity of a novel Beclin 1-binding protein UVRAG. Nat Cell Biol 2006; 8: 688-99.
8. Iida A, Emi M, Matsuoka R, Hiratsuka E, Okui K, Ohashi H, Inazawa J, Fukushima Y, Imai T, Nakamura Y,. Identification of a gene disrupted by inv(11)(q13.5;q25) in a patient with left-right axis malformation. Hum Genet 2000; 106: 277-87. (Pubitemid 30201274)
9. Pires-DaSilva A, Gruss P,. Gene trap insertion into a novel gene expressed during mouse limb development. Dev Dyn 1998; 212: 318-25. (Pubitemid 28265151)
10. Qu X, Zou Z, Sun Q, Luby-Phelps K, Cheng P, Hogan RN, Gilpin C, Levine B,. Autophagy gene-dependent clearance of apoptotic cells during embryonic development. Cell 2007; 128: 931-46. (Pubitemid 46341412)
11. Wang J,. Beclin 1 bridges autophagy, apoptosis and differentiation. Autophagy 2008; 4: 947-8.
12. Daido S, Yamamoto A, Fujiwara K, Sawaya R, Kondo S, Kondo Y,. Inhibition of the DNA-dependent protein kinase catalytic subunit radiosensitizes malignant glioma cells by inducing autophagy. Cancer Res 2005; 65: 4368-75. (Pubitemid 40775676)
13. Ito H, Daido S, Kanzawa T, Kondo S, Kondo Y,. Radiation-induced autophagy is associated with LC3 and its inhibition sensitizes malignant glioma cells. Int J Oncol 2005; 26: 1401-10.
14. Paglin S, Lee NY, Nakar C, Fitzgerald M, Plotkin J, Deuel B, Hackett N, McMahill M, Sphicas E, Lampen N, Yahalom J,. Rapamycin-sensitive pathway regulates mitochondrial membrane potential, autophagy, and survival in irradiated MCF-7 cells. Cancer Res 2005; 65: 11061-70. (Pubitemid 41713377)
15. Takeuchi H, Kondo Y, Fujiwara K, Kanzawa T, Aoki H, Mills GB, Kondo S,. Synergistic augmentation of rapamycin-induced autophagy in malignant glioma cells by phosphatidylinositol 3-kinase/protein kinase B inhibitors. Cancer Res 2005; 65: 3336-46. (Pubitemid 40524618)
16. Guba M, von Breitenbuch P, Steinbauer M, Koehl G, Flegel S, Hornung M, Bruns CJ, Zuelke C, Farkas S, Anthuber M, Jauch KW, Geissler EK,. Rapamycin inhibits primary and metastatic tumor growth by antiangiogenesis: involvement of vascular endothelial growth factor. Nat Med 2002; 8: 128-35. (Pubitemid 34155123)
17. Shinohara ET, Cao C, Niermann K, Mu Y, Zeng F, Hallahan DE, Lu B,. Enhanced radiation damage of tumor vasculature by mTOR inhibitors. Oncogene 2005; 24: 5414-22. (Pubitemid 43080085)
18. Galanis E, Buckner JC, Maurer MJ, Kreisberg JI, Ballman K, Boni J, Peralba JM, Jenkins RB, Dakhil SR, Morton RF, Jaeckle KA, Scheithauer BW, et al. Phase II trial of temsirolimus (CCI-779) in recurrent glioblastoma multiforme: a North Central Cancer Treatment Group Study. J Clin Oncol 2005; 23: 5294-304. (Pubitemid 46206983)
19. Cloughesy TF, Yoshimoto K, Nghiemphu P, Brown K, Dang J, Zhu S, Hsueh T, Chen Y, Wang W, Youngkin D, Liau L, Martin N, et al. Antitumor activity of rapamycin in a phase I trial for patients with recurrent PTEN-deficient glioblastoma. PLoS Med 2008; 5: e8.
20. Chang SM, Wen P, Cloughesy T, Greenberg H, Schiff D, Conrad C, Fink K, Robins HI, De Angelis L, Raizer J, Hess K, Aldape K, et al. Phase II study of CCI-779 in patients with recurrent glioblastoma multiforme. Invest New Drugs 2005; 23: 357-61. (Pubitemid 40980358)
21. Doherty L, Gigas DC, Kesari S, Drappatz J, Kim R, Zimmerman J, Ostrowsky L, Wen PY,. Pilot study of the combination of EGFR and mTOR inhibitors in recurrent malignant gliomas. Neurology 2006; 67: 156-8. (Pubitemid 44305484)
22. Lomonaco SL, Finniss S, Xiang C, Decarvalho A, Umansky F, Kalkanis SN, Mikkelsen T, Brodie C,. The induction of autophagy by gamma-radiation contributes to the radioresistance of glioma stem cells. Int J Cancer 2009; 125: 717-22.
23. Huang Q, Zhang QB, Dong J, Wu YY, Shen YT, Zhao YD, Zhu YD, Diao Y, Wang AD, Lan Q,. Glioma stem cells are more aggressive in recurrent tumors with malignant progression than in the primary tumor, and both can be maintained long-term in vitro. BMC Cancer 2008; 8: 304.
24. Li J, Qin Z, Liang Z,. The prosurvival role of autophagy in Resveratrol-induced cytotoxicity in human U251 glioma cells. BMC Cancer 2009; 9: 215.
25. Zhang XD, Wang Y, Wang Y, Zhang X, Han R, Wu JC, Liang ZQ, Gu ZL, Han F, Fukunaga K, Qin ZH,. p53 mediates mitochondria dysfunction-triggered autophagy activation and cell death in rat striatum. Autophagy 2009; 5: 339-50.
26. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F, Vescovi A,. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004; 64: 7011-21. (Pubitemid 39331011)
27. Gunther HS, Schmidt NO, Phillips HS, Kemming D, Kharbanda S, Soriano R, Modrusan Z, Meissner H, Westphal M, Lamszus K,. Glioblastoma-derived stem cell-enriched cultures form distinct subgroups according to molecular and phenotypic criteria. Oncogene 2008; 27: 2897-909. (Pubitemid 351620450)
28. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB,. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821-8. (Pubitemid 37187480)
29. Shigemitsu K, Tsujishita Y, Hara K, Nanahoshi M, Avruch J, Yonezawa K,. Regulation of translational effectors by amino acid and mammalian target of rapamycin signaling pathways. Possible involvement of autophagy in cultured hepatoma cells. J Biol Chem 1999; 274: 1058-65. (Pubitemid 29058080)
30. Abeliovich H, Dunn WA, Jr, Kim J, Klionsky DJ,. Dissection of autophagosome biogenesis into distinct nucleation and expansion steps. J Cell Biol 2000; 151: 1025-34.
31. Kanazawa T, Taneike I, Akaishi R, Yoshizawa F, Furuya N, Fujimura S, Kadowaki M,. Amino acids and insulin control autophagic proteolysis through different signaling pathways in relation to mTOR in isolated rat hepatocytes. J Biol Chem 2004; 279: 8452-9. (Pubitemid 38294738)
32. Kalamidas SA, Kondomerkos DJ, Kotoulas OB, Hann AC,. Electron microscopic and biochemical study of the effects of rapamycin on glycogen autophagy in the newborn rat liver. Microsc Res Tech 2004; 63: 215-19. (Pubitemid 38316395)
33. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T,. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19: 5720-8.
34. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN,. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444: 756-60. (Pubitemid 44949604)
35. Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu JC, Sasaki YF,. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 2000; 35: 206-21. (Pubitemid 30196665)
36. Balajee AS, Geard CR,. Replication protein A and gamma-H2AX foci assembly is triggered by cellular response to DNA double-strand breaks. Exp Cell Res 2004; 300: 320-34. (Pubitemid 39314422)
37. Carr AM,. DNA structure dependent checkpoints as regulators of DNA repair. DNA Repair (Amst) 2002; 1: 983-94. (Pubitemid 35335824)
38. Abraham RT,. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 2001; 15: 2177-96. (Pubitemid 32843830)
39. Zhou BB, Elledge SJ,. The DNA damage response: putting checkpoints in perspective. Nature 2000; 408: 433-9.
40. Seaberg RM, van der Kooy D,. Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J Neurosci 2002; 22: 1784-93. (Pubitemid 35386296)
41. Vescovi AL, Galli R, Reynolds BA,. Brain tumour stem cells. Nat Rev Cancer 2006; 6: 425-36.
42. Sanai N, Alvarez-Buylla A, Berger MS,. Neural stem cells and the origin of gliomas. N Engl J Med 2005; 353: 811-22.
43. Beier D, Hau P, Proescholdt M, Lohmeier A, Wischhusen J, Oefner PJ, Aigner L, Brawanski A, Bogdahn U, Beier CP,. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res 2007; 67: 4010-15. (Pubitemid 46815044)
44. Wang J, Sakariassen PO, Tsinkalovsky O, Immervoll H, Boe SO, Svendsen A, Prestegarden L, Rosland G, Thorsen F, Stuhr L,. CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int J Cancer 2008; 122; 761-8.
45. Kondo Y, Kanzawa T, Sawaya R, Kondo S,. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 2005; 5: 726-34. (Pubitemid 41486365)
46. Hippert MM, O'Toole PS, Thorburn A,. Autophagy in cancer: good, bad, or both? Cancer Res 2006; 66: 9349-51.
47. Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ,. Potential therapeutic applications of autophagy. Nat Rev Drug Discov 2007; 6: 304-12. (Pubitemid 46505881)
48. Zhao Y, Huang Q, Yang J, Lou M, Wang A, Dong J, Qin Z, Zhang T,. Autophagy impairment inhibits differentiation of glioma stem/progenitor cells. Brain Res 2010; 1313: 250-8.
49. Cecconi F, Levine B,. The role of autophagy in mammalian development: cell makeover rather than cell death. Dev Cell 2008; 15: 344-57.
50. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, Bamber BA, Bassham DC, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4: 151-75. (Pubitemid 351231180)