Smac mimetic promotes glioblastoma cancer stem-like cell differentiation by activating NF-κB

Cell Death and Differentiation

Volumn 21, Issue 5, 2014, Pages 735-747

  Tchoghandjian, A ^a   Jennewein, C ^a   Eckhardt, I ^a   Momma, S ^a   Figarella Branger, D ^b   Fulda, S ^a  

^a GOETHE UNIVERSITY   (Germany)

^b INSERM   (France)

Author keywords

differentiation; glioblastoma; IAP proteins; NF B; Smac mimetic

Indexed keywords

BETA TUBULIN; BV 6; CD133 ANTIGEN; GLIAL FIBRILLARY ACIDIC PROTEIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN; MESSENGER RNA; PEPTIDOMIMETIC AGENT; PROTEIN P100; PROTEIN P50; PROTEIN P52; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; BV6 PEPTIDE; OLIGOPEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CANCER MODEL; CANCER STEM CELL; CANCER SURVIVAL; CARCINOGENICITY; CELL DIFFERENTIATION; CELL STRUCTURE; CLONOGENESIS; CONTROLLED STUDY; GENE EXPRESSION; GENE OVEREXPRESSION; GENE TRANSLOCATION; GENETIC TRANSCRIPTION; GLIOBLASTOMA; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; REPRESSOR GENE; SIGNAL TRANSDUCTION; ANIMAL; APOPTOSIS; BRAIN NEOPLASMS; DISEASE MODEL; DRUG EFFECTS; DRUG SCREENING; HUMAN; METABOLISM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE;

MUS;

ANIMALS; APOPTOSIS; BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; GLIOBLASTOMA; HUMANS; MICE; MICE, NUDE; NEOPLASTIC STEM CELLS; NF-KAPPA B; OLIGOPEPTIDES; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84898037741     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2013.200     Document Type: Article

References (49)

1. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007; 114: 97-109. (Pubitemid 47103521)
2. Preusser M, de Ribaupierre S, Wohrer A, Erridge SC, Hegi M, Weller M et al. Current concepts and management of glioblastoma. Ann Neurol 2011; 70: 9-21.
3. Charles NA, Holland EC, Gilbertson R, Glass R, Kettenmann H. The brain tumor microenvironment. Glia 2011; 59: 1169-1180.
4. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004; 64: 7011-7021. (Pubitemid 39331011)
5. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T et al. Identification of human brain tumour initiating cells. Nature 2004; 432: 396-401. (Pubitemid 39551674)
6. Venere M, Fine HA, Dirks PB, Rich JN. Cancer stem cells in gliomas: identifying and understanding the apex cell in cancer's hierarchy. Glia 2011; 59: 1148-1154.
7. Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012; 488: 522-526.
8. Yuki K, Natsume A, Yokoyama H, Kondo Y, Ohno M, Kato T et al. Induction of oligodendrogenesis in glioblastoma-initiating cells by IFN-mediated activation of STAT3 signaling. Cancer Lett 2009; 284: 71-79.
9. Campos B, Wan F, Farhadi M, Ernst A, Zeppernick F, Tagscherer KE et al. Differentiation therapy exerts antitumor effects on stem-like glioma cells. Clin Cancer Res 2010; 16: 2715-2728.
10. Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, Broggi G et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006; 444: 761-765. (Pubitemid 44949605)
11. Silber J, Lim DA, Petritsch C, Persson AI, Maunakea AK, Yu M et al. miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med 2008; 6: 14.
12. Gal H, Pandi G, Kanner AA, Ram Z, Lithwick-Yanai G, Amariglio N et al. MIR-451 and Imatinib mesylate inhibit tumor growth of Glioblastoma stem cells. Biochem Biophys Res Commun 2008; 376: 86-90.
13. Wagenknecht B, Glaser T, Naumann U, Kugler S, Isenmann S, Bahr M et al. Expression and biological activity of X-linked inhibitor of apoptosis (XIAP) in human malignant glioma. Cell Death Differ 1999; 6: 370-376. (Pubitemid 29186881)
14. Nagata M, Nakayama H, Tanaka T, Yoshida R, Yoshitake Y, Fukuma D et al. Overexpression of cIAP2 contributes to 5-FU resistance and a poor prognosis in oral squamous cell carcinoma. Br J Cancer 2011; 105: 1322-1330.
15. Fulda S, Vucic D, Targeting IAP. proteins for therapeutic intervention in cancer. Nat Rev Drug Discov 2012; 11: 109-124.
16. Oeckinghaus A, Hayden MS, Ghosh S. Crosstalk in NF-kappaB signaling pathways. Nat Immunol 2011; 12: 695-708.
17. Varfolomeev E, Goncharov T, Fedorova AV, Dynek JN, Zobel K, Deshayes K et al. c-IAP1 and c-IAP2 are critical mediators of tumor necrosis factor alpha (TNFalpha)-induced NF-kappaB activation. J Biol Chem 2008; 283: 24295-24299.
18. Bertrand MJ, Milutinovic S, Dickson KM, Ho WC, Boudreault A, Durkin J et al. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol Cell 2008; 30: 689-700. (Pubitemid 351818251)
19. Vallabhapurapu S, Matsuzawa A, Zhang W, Tseng PH, Keats JJ, Wang H et al. Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappaB signaling. Nat Immunol 2008; 9: 1364-1370.
20. Zarnegar BJ, Wang Y, Mahoney DJ, Dempsey PW, Cheung HH, He J et al. Noncanonical NF-kappaB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat Immunol 2008; 9: 1371-1378.
21. Vellanki SH, 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: 743-752.
22. Berger R, Jennewein C, Marschall V, Karl S, Cristofanon S, Wagner L et al. NF-{kappa}B is required for Smac mimetic-mediated sensitization of glioblastoma cells for {gamma}-irradiation-induced apoptosis. Mol Cancer Ther 2011; 10: 1867-1875.
23. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 2007; 131: 669-681. (Pubitemid 350087204)
24. Plenchette S, Cathelin S, Rebe C, Launay S, Ladoire S, Sordet O et al. Translocation of the inhibitor of apoptosis protein c-IAP1 from the nucleus to the Golgi in hematopoietic cells undergoing differentiation: a nuclear export signal-mediated event. Blood 2004; 104: 2035-2043. (Pubitemid 39297854)
25. Long RM, Morrissey C, Walsh S, Hamilton HJ, Farrell N, O'Neill A et al. Alterations in the expression of inhibitors of apoptosis during differentiation of prostate epithelial cells. BJU Int 2007; 100: 445-449. (Pubitemid 47036571)
26. Tchoghandjian A, Baeza N, Colin C, Cayre M, Metellus P, Beclin C et al. A2B5 cells from human glioblastoma have cancer stem cell properties. Brain Pathol 2010; 20: 211-221.
27. Stock K, Kumar J, Synowitz M, Petrosino S, Imperatore R, Smith ES et al. Neural precursor cells induce cell death of high-grade astrocytomas through stimulation of TRPV1. Nat Med 2012; 18: 1232-1238.
28. Liptay S, Schmid RM, Nabel EG, Nabel GJ. Transcriptional regulation of NF-kappa B2: evidence for kappa B-mediated positive and negative autoregulation. Mol Cell Biol 1994; 14: 7695-7703. (Pubitemid 24373521)
29. Vaira S, Johnson T, Hirbe AC, Alhawagri M, Anwisye I, Sammut B et al. RelB is the NF-kappaB subunit downstream of NIK responsible for osteoclast differentiation. Proc Natl Acad Sci USA 2008; 105: 3897-3902. (Pubitemid 351723496)
30. Muller-Sienerth N, Dietz L, Holtz P, Kapp M, Grigoleit GU, Schmuck C et al. SMAC mimetic BV6 induces cell death in monocytes and maturation of monocyte-derived dendritic cells. PLoS One 2011; 6: e21556.
31. Abhari BA, Cristofanon S, Kappler R, von Schweinitz D, Humphreys R, Fulda S. RIP1 is required for IAP inhibitor-mediated sensitization for TRAIL-induced apoptosis via a RIP1/FADD/caspase-8 cell death complex. Oncogene 2013; 32: 3263-3273.
32. Bae MK, Kim SR, Lee HJ, Wee HJ, Yoo MA, Ock Oh S et al. Aspirin-induced blockade of NF-kappaB activity restrains up-regulation of glial fibrillary acidic protein in human astroglial cells. Biochim Biophys Acta 2006; 1763: 282-289.
33. Nogueira L, Ruiz-Ontanon P, Vazquez-Barquero A, Lafarga M, Berciano MT, Aldaz B et al. Blockade of the NFkappaB pathway drives differentiating glioblastoma-initiating cells into senescence both in vitro and in vivo. Oncogene 2011; 30: 3537-3548.
34. Sabolek M, Herborg A, Schwarz J, Storch A. Dexamethasone blocks astroglial differentiation from neural precursor cells. Neuroreport 2006; 17: 1719-1723. (Pubitemid 44621571)
35. Ozeki A, Suzuki K, Suzuki M, Ozawa H, Yamashita S. Acceleration of astrocytic differentiation in neural stem cells surviving X-irradiation. Neuroreport 2012; 23: 290-293.
36. De Molfetta GA, Luciola Zanette D, Alexandre Panepucci R, Dos Santos AR, da Silva Jr WA, Antonio Zago M. Role of NFKB2 on the early myeloid differentiation of CD34 hematopoietic stem/progenitor cells. Differentiation 2010; 80: 195-203.
37. Enwere EK, Holbrook J, Lejmi-Mrad R, Vineham J, Timusk K, Sivaraj B et al. TWEAK and cIAP1 regulate myoblast fusion through the noncanonical NF-kappaB signaling pathway. Sci Signal 2012; 5: ra75.
38. Young KM, Bartlett PF, Coulson EJ. Neural progenitor number is regulated by nuclear factor-kappaB p65 and p50 subunit-dependent proliferation rather than cell survival. J Neurosci Res 2006; 83: 39-49. (Pubitemid 43062008)
39. Guttridge DC, Albanese C, Reuther JY, Pestell RG, Baldwin Jr AS. NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol 1999; 19: 5785-5799. (Pubitemid 29339933)
40. Widera D, Mikenberg I, Kaltschmidt B, Kaltschmidt C. Potential role of NF-kappaB in adult neural stem cells: the underrated steersman? Int J Dev Neurosci 2006; 24: 91-102. (Pubitemid 43294615)
41. Yang C, Atkinson SP, Vilella F, Lloret M, Armstrong L, Mann DA et al. Opposing putative roles for canonical and noncanonical NFkappaB signaling on the survival, proliferation, and differentiation potential of human embryonic stem cells. Stem Cells 2010; 28: 1970-1980.
42. Liu M, Sakamaki T, Casimiro MC, Willmarth NE, Quong AA, Ju X et al. The canonical NF-kappaB pathway governs mammary tumorigenesis in transgenic mice and tumor stem cell expansion. Cancer Res 2010; 70: 10464-10473.
43. Fulda S, Wick W, Weller M, Debatin KM. Smac agonists sensitize for Apo2L/TRAIL-or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat Med 2002; 8: 808-815.
44. Wagner L, Marschall V, Karl S, Cristofanon S, Zobel K, Deshayes K et al. Smac mimetic sensitizes glioblastoma cells to Temozolomide-induced apoptosis in a RIP1-and NF-kappaB-dependent manner. Oncogene 2013; 32: 988-997.
45. Tchoghandjian A, Jennewein C, Eckhardt I, Rajalingam K, Fulda S. Identification of non-canonical NF-kappaB signaling as a critical mediator of Smac mimetic-stimulated migration and invasion of glioblastoma cells. Cell Death Dis 2013; 4: e564.
46. Vogler M, Durr K, Jovanovic M, Debatin KM, Fulda S. Regulation of TRAIL-induced apoptosis by XIAP in pancreatic carcinoma cells. Oncogene 2007; 26: 248-257. (Pubitemid 46095735)
47. Kasperczyk H, La Ferla-Bruhl K, Westhoff MA, Behrend L, Zwacka RM, Debatin K-M et al. Betulinic acid as new activator of NF-kappaB: molecular mechanisms and implications for cancer therapy. Oncogene 2005; 24: 6945-6956. (Pubitemid 41509417)
48. Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, Yanagisawa M et al. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 2001; 1: 749-758. (Pubitemid 33586130)
49. Karl S, Pritschow Y, Volcic M, Hacker S, Baumann B, Wiesmuller L et al. Identification of a novel pro-apopotic function of NF-kappaB in the DNA damage response. J Cell Mol Med 2009; 13: 4239-4256.