Regulatory effects of a Mnk2-eIF4E feedback loop during mTORC1 targeting of human medulloblastoma cells

Oncotarget

Volumn 5, Issue 18, 2014, Pages 8442-8451

  Eckerdt, Frank ^a   Beauchamp, Elspeth ^a,b   Bell, Jonathan ^a   Iqbal, Asneha ^a,c   Su, Bing ^d,e   Fukunaga, Rikiro ^f   Lulla, Rishi R ^a,c   Goldman, Stewart ^a,c   Platanias, Leonidas C ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

^c CHILDREN'S MEMORIAL HOSPITAL   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^f OSAKA MEDICAL COLLEGE   (Japan)

Author keywords

Medulloblastoma; Mnk; Rapamycin; TOR

Indexed keywords

4 (4 AMINO 5 (7 METHOXY 1H INDOL 2 YL)IMIDAZO[5,1 F][1,2,4]TRIAZIN 7 YL)CYCLOHEXANECARBOXYLIC ACID; FK 506 BINDING PROTEIN; INITIATION FACTOR 4E; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN KINASE B; RAPAMYCIN; ANTINEOPLASTIC ANTIBIOTIC; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MKNK2 PROTEIN, HUMAN; MULTIPROTEIN COMPLEX; PROTEIN KINASE INHIBITOR; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE; TARGET OF RAPAMYCIN KINASE;

ARTICLE; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; COLONY FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; MEDULLOBLASTOMA CELL LINE; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; CEREBELLUM TUMOR; DOSE RESPONSE; DRUG EFFECTS; DRUG RESISTANCE; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; MEDULLOBLASTOMA; METABOLISM; PATHOLOGY; PHOSPHORYLATION; RNA INTERFERENCE; TUMOR CELL LINE;

ANTIBIOTICS, ANTINEOPLASTIC; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CEREBELLAR NEOPLASMS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; EUKARYOTIC INITIATION FACTOR-4E; FEEDBACK, PHYSIOLOGICAL; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEDULLOBLASTOMA; MULTIPROTEIN COMPLEXES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES; TRANSFECTION;

EID: 84908005763     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2319     Document Type: Article

References (41)

1. Pui CH, Gajjar AJ, Kane JR, Qaddoumi IA and Pappo AS. Challenging issues in pediatric oncology. Nat Rev Clin Oncol. 2011; 8(9):540-549.
2. Jones DT, Jager N, Kool M, Zichner T, Hutter B, Sultan M, Cho YJ, Pugh TJ, Hovestadt V, Stutz AM, Rausch T, Warnatz HJ, Ryzhova M, Bender S, Sturm D, Pleier S, et al. Dissecting the genomic complexity underlying medulloblastoma. Nature. 2012; 488(7409):100-105.
3. Robinson G, Parker M, Kranenburg TA, Lu C, Chen X, Ding L, Phoenix TN, Hedlund E, Wei L, Zhu X, Chalhoub N, Baker SJ, Huether R, Kriwacki R, Curley N, Thiruvenkatam R, et al. Novel mutations target distinct subgroups of medulloblastoma. Nature. 2012; 488(7409):43-48.
4. Pugh TJ, Weeraratne SD, Archer TC, Pomeranz Krummel DA, Auclair D, Bochicchio J, Carneiro MO, Carter SL, Cibulskis K, Erlich RL, Greulich H, Lawrence MS, Lennon NJ, McKenna A, Meldrim J, Ramos AH, et al. Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature. 2012; 488(7409):106-110.
5. Northcott PA, Jones DT, Kool M, Robinson GW, Gilbertson RJ, Cho YJ, Pomeroy SL, Korshunov A, Lichter P, Taylor MD and Pfister SM. Medulloblastomics: the end of the beginning. Nat Rev Cancer. 2012; 12(12):818-834.
6. Buonamici S, Williams J, Morrissey M, Wang A, Guo R, Vattay A, Hsiao K, Yuan J, Green J, Ospina B, Yu Q, Ostrom L, Fordjour P, Anderson DL, Monahan JE, Kelleher JF, et al. Interfering with resistance to smoothened antagonists by inhibition of the PI3K pathway in medulloblastoma. Sci Transl Med. 2010; 2(51):51ra70.
7. Bjornsti MA and Houghton PJ. The TOR pathway: a target for cancer therapy. Nat Rev Cancer. 2004; 4(5):335-348.
8. Beauchamp EM and Platanias LC. The evolution of the TOR pathway and its role in cancer. Oncogene. 2013; 32(34):3923-3932.
9. Proud CG. Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem J. 2007; 403(2):217-234.
10. Platanias LC. Mechanisms of type-I-and type-II-interferon-mediated signalling. Nat Rev Immunol. 2005; 5(5):375-386.
11. Hou J, Lam F, Proud C and Wang S. Targeting Mnks for cancer therapy. Oncotarget. 2012; 3(2):118-131.
12. De Benedetti A and Graff JR. eIF-4E expression and its role in malignancies and metastases. Oncogene. 2004; 23(18):3189-3199.
13. Fan S, Ramalingam SS, Kauh J, Xu Z, Khuri FR and Sun SY. Phosphorylated eukaryotic translation initiation factor 4 (eIF4E) is elevated in human cancer tissues. Cancer Biol Ther. 2009; 8(15):1463-1469.
14. Silvera D, Formenti SC and Schneider RJ. Translational control in cancer. Nat Rev Cancer. 2010; 10(4):254-266.
15. Topisirovic I, Ruiz-Gutierrez M and Borden KL. Phosphorylation of the eukaryotic translation initiation factor eIF4E contributes to its transformation and mRNA transport activities. Cancer Res. 2004; 64(23):8639-8642.
16. Wendel HG, Silva RL, Malina A, Mills JR, Zhu H, Ueda T, Watanabe-Fukunaga R, Fukunaga R, Teruya-Feldstein J, Pelletier J and Lowe SW. Dissecting eIF4E action in tumorigenesis. Genes Dev. 2007; 21(24):3232-3237.
17. Altman JK, Glaser H, Sassano A, Joshi S, Ueda T, Watanabe-Fukunaga R, Fukunaga R, Tallman MS and Platanias LC. Negative regulatory effects of Mnk kinases in the generation of chemotherapy-induced antileukemic responses. Mol Pharmacol. 2010; 78(4):778-784.
18. Altman JK, Szilard A, Konicek BW, Iversen PW, Kroczynska B, Glaser H, Sassano A, Vakana E, Graff JR and Platanias LC. Inhibition of Mnk kinase activity by cercosporamide and suppressive effects on acute myeloid leukemia precursors. Blood. 2013; 121(18):3675-3681.
19. Sun SY, Rosenberg LM, Wang X, Zhou Z, Yue P, Fu H and Khuri FR. Activation of Akt and eIF4E survival pathways by rapamycin-mediated mammalian target of rapamycin inhibition. Cancer Res. 2005; 65(16):7052-7058.
20. Wang X, Yue P, Chan CB, Ye K, Ueda T, Watanabe-Fukunaga R, Fukunaga R, Fu H, Khuri FR and Sun SY. Inhibition of mammalian target of rapamycin induces phosphatidylinositol 3-kinase-dependent and Mnk-mediated eukaryotic translation initiation factor 4E phosphorylation. Mol Cell Biol. 2007; 27(21):7405-7413.
21. Carayol N, Vakana E, Sassano A, Kaur S, Goussetis DJ, Glaser H, Druker BJ, Donato NJ, Altman JK, Barr S and Platanias LC. Critical roles for mTORC2-and rapamycin-insensitive mTORC1-complexes in growth and survival of BCR-ABL-expressing leukemic cells. Proc Natl Acad Sci U S A. 2010; 107(28):12469-12474.
22. Sarbassov DD, Guertin DA, Ali SM and Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science. 2005; 307(5712):1098-1101.
23. Altman JK, Sassano A, Kaur S, Glaser H, Kroczynska B, Redig AJ, Russo S, Barr S and Platanias LC. Dual mTORC2/mTORC1 targeting results in potent suppressive effects on acute myeloid leukemia (AML) progenitors. Clin Cancer Res. 2011; 17(13):4378-4388.
24. Benjamin D, Colombi M, Moroni C and Hall MN. Rapamycin passes the torch: a new generation of mTOR inhibitors. Nat Rev Drug Discov. 2011; 10(11):868-880.
25. Dibble CC, Asara JM and Manning BD. Characterization of Rictor phosphorylation sites reveals direct regulation of mTOR complex 2 by S6K1. Mol Cell Biol. 2009; 29(21):5657-5670.
26. Julien LA, Carriere A, Moreau J and Roux PP. mTORC1-activated S6K1 phosphorylates Rictor on threonine 1135 and regulates mTORC2 signaling. Mol Cell Biol. 2010; 30(4):908-921.
27. Liu P, Gan W, Inuzuka H, Lazorchak AS, Gao D, Arojo O, Liu D, Wan L, Zhai B, Yu Y, Yuan M, Kim BM, Shaik S, Menon S, Gygi SP, Lee TH, et al. Sin1 phosphorylation impairs mTORC2 complex integrity and inhibits downstream Akt signalling to suppress tumorigenesis. Nat Cell Biol. 2013; 15(11):1340-1350.
28. Jacinto E, Facchinetti V, Liu D, Soto N, Wei S, Jung SY, Huang Q, Qin J and Su B. SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell. 2006; 127(1):125-137.
29. Sharma B, Joshi S, Sassano A, Majchrzak B, Kaur S, Aggarwal P, Nabet B, Bulic M, Stein BL, McMahon B, Baker DP, Fukunaga R, Altman JK, Licht JD, Fish EN and Platanias LC. Sprouty proteins are negative regulators of interferon (IFN) signaling and IFN-inducible biological responses. J Biol Chem. 2012; 287(50):42352-42360.
30. Waskiewicz AJ, Flynn A, Proud CG and Cooper JA. Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2. EMBO J. 1997; 16(8):1909-1920.
31. Ueda T, Watanabe-Fukunaga R, Fukuyama H, Nagata S and Fukunaga R. Mnk2 and Mnk1 are essential for constitutive and inducible phosphorylation of eukaryotic initiation factor 4E but not for cell growth or development. Mol Cell Biol. 2004; 24(15):6539-6549.
32. Joshi S, Kaur S, Redig AJ, Goldsborough K, David K, Ueda T, Watanabe-Fukunaga R, Baker DP, Fish EN, Fukunaga R and Platanias LC. Type I interferon (IFN)-dependent activation of Mnk1 and its role in the generation of growth inhibitory responses. Proc Natl Acad Sci U S A. 2009; 106(29):12097-12102.
33. Geoerger B, Kerr K, Tang CB, Fung KM, Powell B, Sutton LN, Phillips PC and Janss AJ. Antitumor activity of the rapamycin analog CCI-779 in human primitive neuroectodermal tumor/medulloblastoma models as single agent and in combination chemotherapy. Cancer Res. 2001; 61(4):1527-1532.
34. Mohan AL, Friedman MD, Ormond DR, Tobias M, Murali R and Jhanwar-Uniyal M. PI3K/mTOR signaling pathways in medulloblastoma. Anticancer Res. 2012; 32(8):3141-3146.
35. Stead RL and Proud CG. Rapamycin enhances eIF4E phosphorylation by activating MAP kinase-interacting kinase 2a (Mnk2a). FEBS Lett. 2013; 587(16):2623-2628.
36. Wang X, Venugopal C, Manoranjan B, McFarlane N, O'Farrell E, Nolte S, Gunnarsson T, Hollenberg R, Kwiecien J, Northcott P, Taylor MD, Hawkins C and Singh SK. Sonic hedgehog regulates Bmi1 in human medulloblastoma brain tumor-initiating cells. Oncogene. 2012; 31(2):187-199.
37. Aldosari N, Wiltshire RN, Dutra A, Schrock E, McLendon RE, Friedman HS, Bigner DD and Bigner SH. Comprehensive molecular cytogenetic investigation of chromosomal abnormalities in human medulloblastoma cell lines and xenograft. Neuro Oncol. 2002; 4(2):75-85.
38. Northcott PA, Korshunov A, Pfister SM and Taylor MD. The clinical implications of medulloblastoma subgroups. Nat Rev Neurol. 2012; 8(6):340-351.
39. Joshi S, Sharma B, Kaur S, Majchrzak B, Ueda T, Fukunaga R, Verma AK, Fish EN and Platanias LC. Essential role for Mnk kinases in type II interferon (IFNgamma) signaling and its suppressive effects on normal hematopoiesis. J Biol Chem. 2011; 286(8):6017-6026.
40. Kaur S, Kroczynska B, Sharma B, Sassano A, Arslan AD, Majchrzak-Kita B, Stein BL, McMahon B, Altman JK, Su B, Calogero RA, Fish EN and Platanias LC. Critical roles for Rictor/Sin1 complexes in IFN-dependent gene transcription and generation of antiproliferative responses. J Biol Chem. 2014.
41. Kaur S, Lal L, Sassano A, Majchrzak-Kita B, Srikanth M, Baker DP, Petroulakis E, Hay N, Sonenberg N, Fish EN and Platanias LC. Regulatory effects of mammalian target of rapamycin-activated pathways in type I and II interferon signaling. J Biol Chem. 2007; 282(3):1757-1768.