Nucleolin antagonist triggers autophagic cell death in human glioblastoma primary cells and decreased in vivo tumor growth in orthotopic brain tumor model

Oncotarget

Volumn 6, Issue 39, 2015, Pages 42091-42104

  Benedetti, Elisabetta ^a   Antonosante, Andrea ^a   d'Angelo, Michele ^a   Cristiano, Loredana ^a   Galzio, Renato ^a   Destouches, Damien ^b,c   Florio, Tiziana Marilena ^a   Dhez, Anne Chloé ^a   Astarita, Carlo ^f   Cinque, Benedetta ^a   Fidoamore, Alessia ^a   Rosati, Floriana ^d   Cifone, Maria Grazia ^a   Ippoliti, Rodolfo ^a   Giordano, Antonio ^e,f   Courty, José ^b,c   Cimini, Annamaria ^a,f,g  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^c La Réparation et la Régénération Tissulaires ^*  (France)

^d UNIVERSITY OF SIENA   (Italy)

^e UNIVERSITY OF SIENA   (Italy)

^f TEMPLE UNIVERSITY   (United States)

^g LABORATORI NAZIONALI DEL GRAN SASSO   (Italy)

Author keywords

Autophagy; Glioblastoma; Targeted therapy

Indexed keywords

ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; CYCLIN B2; CYCLIN D1; N6L; NUCLEOLIN; PROTEIN LC 3II; PROTEIN P62; UNCLASSIFIED DRUG; ALKYLATING AGENT; DACARBAZINE; N6L PEPTIDE; PEPTIDE; PHOSPHOPROTEIN; RNA BINDING PROTEIN; TEMOZOLOMIDE;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; AUTOPHAGY; BRAIN TUMOR; CANCER CELL DESTRUCTION; CANCER INHIBITION; CANCER SURVIVAL; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; DRUG SENSITIVITY; FEMALE; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN TARGETING; SURVIVAL TIME; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BRAIN NEOPLASMS; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECTS; DRUG POTENTIATION; DRUG SCREENING; FLUORESCENCE MICROSCOPY; G1 PHASE CELL CYCLE CHECKPOINT; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED; NUDE MOUSE; PATHOLOGY; TUMOR CELL CULTURE; TUMOR CELL LINE; TUMOR VOLUME;

ADULT; AGED; ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; AUTOPHAGY; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DACARBAZINE; DRUG SYNERGISM; FEMALE; G1 PHASE CELL CYCLE CHECKPOINTS; GLIOBLASTOMA; HUMANS; KAPLAN-MEIER ESTIMATE; MICE, INBRED BALB C; MICE, NUDE; MICROSCOPY, FLUORESCENCE; MIDDLE AGED; PEPTIDES; PHOSPHOPROTEINS; RNA-BINDING PROTEINS; TUMOR BURDEN; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84951868493     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5990     Document Type: Article

References (29)

1. Berger CM, Gaume X, Bouvet P. The roles of nucleolin subcellular localization in cancer. Biochimie. 2015; 113:78-85.
2. Derenzini M, Sirri V, Pession A, Trerè D, Roussel P, Ochs RL, Hernandez-Verdun D. Quantitative changes of the two major AgNOR proteins, nucleolin and protein B23, related to stimulation of rDNA transcription. Exp Cell Res. 1995; 219:276-282.
3. de Verdugo UR, Selinka HC, Huber M, Kramer B, Kellermann J, Hofschneider PH, Kandolf R. Characterization of a 100-kilodalton binding protein for the six serotypes of coxsackie B viruses. J Virol. 1995; 69:6751-6757.
4. Koutsioumpa M, Papadimitriou E. Cell surface nucleolin as a target for anti-cancer therapies. Recent Pat Anticancer Drug Discov. 2014; 9:137-152.
5. Said EA, Courty J, Svab J, Delbé J, Krust B, Hovanessian AG. Pleiotrophin inhibits HIV infection by binding the cell surface-expressed nucleolin. FEBS J. 2005; 272:4646-4659.
6. Shibata Y, Muramatsu T, Hirai M, Inui T, Kimura T, Saito H, McCormick LM, Bu G, Kadomatsu K. Nuclear targeting by the growth factor midkine. Mol Cell Biol. 2002; 22:6788-6796.
7. Huang Y, Shi H, Zhou H, Song X, Yuan S, Luo Y. The angiogenic function of nucleolin is mediated by vascular endothelial growth factor and nonmuscle myosin. Blood. 2006; 107:3564-3571.
8. Shi H, Huang Y, Zhou H, Song X, Yuan S, Fu Y, Luo Y. Nucleolin is a receptor that mediates antiangiogenic and antitumor activity of endostatin. Blood. 2007; 110:2899-2906.
9. Bates PJ, Laber DA, Miller DM, Thomas SD, Trent JO. Discovery and development of the G-rich oligonucleotide AS1411 as a novel treatment for cancer. Exp Mol Pathol. 2009; 86:151-164.
10. Hu Q, Gu G, Liu Z, Jiang M, Kang T, Miao D, Tu Y, Pang Z, Song Q, Yao L, Xia H, Chen H, Jiang X, Gao X, Chen J. F3 peptide-functionalized PEG-PLA nanoparticles co-administrated with tLyp-1 peptide for anti-glioma drug delivery. Biomaterials. 2013; 34:1135-1145.
11. Krust B, Khoury DE, Nondier I, Soundaramourty C, Hovanessian AG. Targeting surface nucleolin with multivalent HB-19 and related Nucant pseudopeptides results in distinct inhibitory mechanisms depending on the malignant tumor cell type. BMC Cancer. 2011; 11:333.
12. Destouches D, Page N, Hamma-Kourbali Y, Machi V, Chaloin O, Frechault S, Birmpas C, Katsoris P, Beyrath J, Albanese P, Maurer M, Carpentier G, Strub JM, Van Dorsselaer A, Muller S, Bagnard D, Briand JP, Courty J. A simple approach to cancer therapy afforded by multivalent pseudopeptides that target cell-surface nucleoproteins. Cancer Res. 2011; 71:3296-3305.
13. Kibbey MC, Johnson B, Petryshyn R, Jucker M, Kleinman HK. A 110-kD nuclear shuttling protein, nucleolin, binds to the neurite-promoting IKVAV site of laminin-1 J Neurosci Res. 1995; 42:314-22.
14. Galzio R, Rosati F, Benedetti E, Cristiano L, Aldi S, Mei S, D'Angelo B, Gentile R, Laurenti G, Cifone MG, Giordano A, Cimini A. Glycosilated nucleolin as marker for human gliomas. J Cell Biochem. 2012; 113:571-579.
15. Kleihues P, Louis DN, Scheithauer BW, Rorke LB, Reifenberger G, Burger PC, Cavenee WK. The WHO classification of tumors of the nervous system. J Neuropathol Exp Neurol. 2002; 61:215-225.
16. Brockmann MA, Ulbricht U, Grüner K, Fillbrandt R, Westphal M, Lamszus K. Glioblastoma and cerebral microvascular endothelial cell migration in response to tumor-associated growth factors. Neurosurgery. 2003; 52:1391-1399.
17. Lund-Johansen M, Bjerkvig R, Humphrey PA, Bigner SH, Bigner DD, Laerum OD. Effect of epidermal growth factor on glioma cell growth, migration, and invasion in vitro. Cancer Res. 1990; 50:6039-6044.
18. Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol. 2005; 171:603-614.
19. Huang R, Xu Y, Wan W, Shou X, Qian J, You Z, Liu B, Chang C, Zhou T, Lippincott-Schwartz J, Liu W. Deacetylation of nuclear LC3 drives autophagy initiation under starvation. Mol Cell. 2015; 57:456-466.
20. Destouches D, El Khoury D, Hamma-Kourbali Y, Krust B, Albanese P, Katsoris P, Guichard G, Briand JP, Courty J, Hovanessian AG. Suppression of tumor growth and angiogenesis by a specific antagonist of the cell-surface expressed nucleolin. PLoS One. 2008; 3:e2518.
21. Tasdemir E, Maiuri MC, Galluzzi L, Vitale I, Djavaheri-Mergny M, D'Amelio M, Criollo A, Morselli E, Zhu C, Harper F, Nannmark U, Samara C, Pinton P, et al. Regulation of autophagy by cytoplasmic p53. Nat Cell Biol. 2008; 10:676-687.
22. Galluzzi L, Pietrocola F, Bravo-San Pedro JM, Amaravadi RK, Baehrecke EH, Cecconi F, Codogno P, Debnath J, Gewirtz DA, Karantza V, Kimmelman A, Kumar S, Levine B, et al. Autophagy in malignant transformation and cancer progression. EMBO J. 2015; 34:856-880.
23. Duran A, Linares JF, Galvez AS, Wikenheiser K, Flores JM, Diaz-Meco MT, Moscat J. The signaling adaptor p62 is an important NF-kappaB mediator in tumorigenesis. Cancer Cell. 2008; 13:343-354.
24. Mathew R, Karp CM, Beaudoin B, Vuong N, Chen G, Chen HY, Bray K, Reddy A, Bhanot G, Gelinas C, Dipaola RS, Karantza-Wadsworth V, White E. Autophagy suppresses tumorigenesis through elimination of p62. Cell. 2009; 137:1062-1075.
25. Takamura A, Komatsu M, Hara T, Sakamoto A, Kishi C, Waguri S, Eishi Y, Hino O, Tanaka K, Mizushima N. Autophagy-deficient mice develop multiple liver tumors. Genes Dev. 2011; 25:795-800.
26. Di Segni A, Farin K, Pinkas-Kramarski R. Identification of nucleolin as new ErbB receptors-interacting protein. PLoS One. 2008; 3:e2310.
27. Farin K, Schokoroy S, Haklai R, Cohen-Or I, Elad-Sfadia G, Reyes-Reyes ME, Bates PJ, Cox AD, Kloog Y, Pinkas-Kramarski R. Oncogenic synergism between ErbB1, nucleolin, and mutant Ras. Cancer Res. 2011; 71:2140-2151.
28. Ulasov IV, Shah N, Kaverina NV, Lee H, Lin B, Lieber A, Kadagidze ZG, Yoon JG, Schroeder B, Hothi P, Ghosh D, Baryshnikov AY, Cobbs CS. Tamoxifen improves cytopathic effect of oncolytic adenovirus in primary glioblastoma cells mediated through autophagy. Oncotarget. 2015; 6:3977-87.
29. Goldshmit Y, Trangle SS, Kloog Y, Pinkas-Kramarski R. Interfering with the interaction between ErbB1, nucleolin and Ras as a potential treatment for glioblastoma. Oncotarget. 2014; 5:8602-13.