TRM6/61 connects PKCα with translational control through tRNA i Met stabilization: Impact on tumorigenesis

Oncogene

Volumn 35, Issue 14, 2016, Pages 1785-1796

  Macari, F ^a,b   El Houfi, Y ^a,b   Boldina, G ^c,d,e,f   Xu, H ^g   Khoury Hanna, S ^a,b   Ollier, J ^a,b   Yazdani, L ^a,b   Zheng, G ^h   Bieche I ^c   Legrand, N ^a,b   Paulet, D ⁱ   Durrieu, S ^j   Bystrom A ^g   Delbecq, S ^b   Lapeyre, B ^k   Bauchet, L ^l   Pannequin, J ^a,b   Hollande, F ^a,b,m   Pan, T ^h   Teichmann, M ^j   Vagner, S ^c,d,e,f   David, A ^a,b   Choquet, A ^a,b   Joubert, D ^a,b   more..

^a INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^b UNIV MONTPELLIER   (France)

^c INSTITUT CURIE   (France)

^d CNRS UMR3348   (France)

^e UNIVERSITÉ PARIS SACLAY   (France)

^f PSL RESEARCH UNIVERSITY   (France)

^g UMEÅ UNIVERSITY   (Sweden)

^h UNIVERSITY OF CHICAGO   (United States)

ⁱ LIRMM   (France)

^j UNIVERSITÉ DE BORDEAUX   (France)

^k CNRS   (France)

^l GUI DE CHAULIAC HOSPITAL   (France)

^m UNIVERSITY OF MELBOURNE   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; MESSENGER RNA; METHIONINE TRANSFER RNA; PROTEIN KINASE C ALPHA; TRANSFER RNA METHYLTRANSFERASE; TRANSFER RNA METHYLTRANSFERASE TRM6/61; TRANSFER RNA METHYLTRANSFERASE TRM61; UNCLASSIFIED DRUG; METHIONINE; PRKCA PROTEIN, HUMAN; TRANSFER RNA; TRM61 PROTEIN, HUMAN; TUMOR MARKER;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL DEATH; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME REGULATION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GLIOBLASTOMA; GLIOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; RNA METHYLATION; RNA STABILITY; SIGNAL TRANSDUCTION; TRANSLATION INITIATION; TRANSLATION REGULATION; APOPTOSIS; BIOSYNTHESIS; GENETICS; HUMAN; PATHOLOGY; TUMOR CELL LINE;

APOPTOSIS; BIOMARKERS, TUMOR; CARCINOGENESIS; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; METHIONINE; PROTEIN KINASE C-ALPHA; RNA, TRANSFER; TRNA METHYLTRANSFERASES;

EID: 84938630715     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.244     Document Type: Article

References (49)

1. Jackson RJ, Hellen CU, Pestova TV. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 2010; 11: 113-127.
2. Sonenberg N, Hinnebusch AG. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 2009; 136: 731-745.
3. Ron D, Harding HP. eIF2α phosphorylation in cellular stress responses and disease. Cold Spring Harbor Laboratory Press: New York, 2007.
4. Lu PD, Harding HP, Ron D. Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J Cell Biol 2004; 167: 27-33.
5. Thakor N, Holcik M. IRES-mediated translation of cellular messenger RNA operates in eIF2alpha- independent manner during stress. Nucleic Acids Res 2012; 40: 541-552.
6. Koromilas AE. Roles of the translation initiation factor eIF2alpha serine 51 phosphorylation in cancer formation and treatment. Biochim Biophys Acta 2014; 1849: 871-880.
7. Anderson J, Phan L, Cuesta R, Carlson BA, Pak M, Asano K et al. The essential Gcd10p-Gcd14p nuclear complex is required for 1-methyladenosine modification and maturation of initiator methionyl-tRNA. Genes Dev 1998; 12: 3650-3662.
8. Anderson J, Phan L, Hinnebusch AG. The Gcd10p/Gcd14p complex is the essential two-subunit tRNA(1-methyladenosine) methyltransferase of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2000; 97: 5173-5178.
9. Roovers M, Wouters J, Bujnicki JM, Tricot C, Stalon V, Grosjean H et al. A primordial RNA modification enzyme: the case of tRNA (m1A) methyltransferase. Nucleic Acids Res 2004; 32: 465-476.
10. Towns WL, Begley TJ, Transfer RNA. methytransferases and their corresponding modifications in budding yeast and humans: activities, predications, and potential roles in human health. DNA Cell Biol 2012; 31: 434-454.
11. Pavon-Eternod M, Gomes S, Rosner MR, Pan T. Overexpression of initiator methionine tRNA leads to global reprogramming of tRNA expression and increased proliferation in human epithelial cells. RNA 2013; 19: 461-466.
12. Quittau-Prevostel C, Delaunay N, Collazos A, Vallentin A, Joubert D. Targeting of PKCalpha and epsilon in the pituitary: a highly regulated mechanism involving a GD(E)E motif of the V3 region. J Cell Sci 2004; 117: 63-72.
13. Diouf B, Collazos A, Labesse G, Macari F, Choquet A, Clair P et al. A 20-amino acid module of protein kinase C{epsilon} involved in translocation and selective targeting at cell-cell contacts. J Biol Chem 2009; 284: 18808-18815.
14. Collazos A, Diouf B, Guerineau NC, Quittau-Prevostel C, Peter M, Coudane F et al. A spatiotemporally coordinated cascade of protein kinase C activation controls isoform-selective translocation. Mol Cell Biol 2006; 26: 2247-2261.
15. Rosse C, Linch M, Kermorgant S, Cameron AJ, Boeckeler K, Parker PJ. PKC and the control of localized signal dynamics. Nat Rev Mol Cell Biol 2010; 11: 103-112.
16. Gravitt KR, Ward NE, Fan D, Skibber JM, Levin B, O'Brian CA. Evidence that protein kinase C-alpha activation is a critical event in phorbol ester-induced multiple drug resistance in human colon cancer cells. Biochem Pharmacol 1994; 48: 375-381.
17. Budworth J, Gant TW, Gescher A. Co-ordinate loss of protein kinase C and multidrug resistance gene expression in revertant MCF-7/Adr breast carcinoma cells. Br J Cancer 1997; 75: 1330-1335.
18. Lee SK, Shehzad A, Jung JC, Sonn JK, Lee JT, Park JW et al. Protein kinase Calpha protects against multidrug resistance in human colon cancer cells. Mol Cells 2012; 34: 61-69.
19. Benzil DL, Finkelstein SD, Epstein MH, Finch PW. Expression pattern of alpha-protein kinase C in human astrocytomas indicates a role in malignant progression. Cancer Res 1992; 52: 2951-2956.
20. Misra-Press A, Fields AP, Samols D, Goldthwait DA. Protein kinase C isoforms in human glioblastoma cells. Glia 1992; 6: 188-197.
21. Xiao H, Goldthwait DA, Mapstone T. The identification of four protein kinase C isoforms in human glioblastoma cell lines: PKC alpha, gamma, epsilon, and zeta. J Neurosurg 1994; 81: 734-740.
22. Zellner A, Fetell MR, Bruce JN, De Vivo DC, O'Driscoll KR. Disparity in expression of protein kinase C alpha in human glioma versus glioma-derived primary cell lines: therapeutic implications. Clin Cancer Res 1998; 4: 1797-1802.
23. Mandil R, Ashkenazi E, Blass M, Kronfeld I, Kazimirsky G, Rosenthal G et al. Protein kinase Calpha and protein kinase Cdelta play opposite roles in the proliferation and apoptosis of glioma cells. Cancer Res 2001; 61: 4612-4619.
24. Cameron AJ, Procyk KJ, Leitges M, Parker PJ. PKC alpha protein but not kinase activity is critical for glioma cell proliferation and survival. Int J Cancer 2008; 123: 769-779.
25. Ahmad S, Mineta T, Martuza RL, Glazer RI. Antisense expression of protein kinase C alpha inhibits the growth and tumorigenicity of human glioblastoma cells. Neurosurgery 1994; 35: 904-908 (discussion 908-909).
26. Torres AG, Batlle E, Ribas de Pouplana L. Role of tRNA modifications in human diseases. Trends Mol Med 2014; 20: 306-314.
27. Ozanick S, Krecic A, Andersland J, Anderson JT. The bipartite structure of the tRNA m1A58 methyltransferase from S. cerevisiae is conserved in humans. RNA 2005; 11: 1281-1290.
28. Gruber JR, Desai S, Blusztajn JK, Niles RM. Retinoic acid specifically increases nuclear PKC alpha and stimulates AP-1 transcriptional activity in B16 mouse melanoma cells. Exp Cell Res 1995; 221: 377-384.
29. Saikia M, Fu Y, Pavon-Eternod M, He C, Pan T. Genome-wide analysis of N1-methyl-adenosine modification in human tRNAs. RNA 2010; 16: 1317-1327.
30. Kadaba S, Krueger A, Trice T, Krecic AM, Hinnebusch AG, Anderson J. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes Dev 2004; 18: 1227-1240.
31. Ozanick SG, Wang X, Costanzo M, Brost RL, Boone C, Anderson JT. Rex1p deficiency leads to accumulation of precursor initiator tRNAMet and polyadenylation of substrate RNAs in Saccharomyces cerevisiae. Nucleic Acids Res 2009; 37: 298-308.
32. David A, Dolan BP, Hickman HD, Knowlton JJ, Clavarino G, Pierre P et al. Nuclear translation visualized by ribosome-bound nascent chain puromycylation. J Cell Biol 2012; 197: 45-57.
33. David A, Netzer N, Strader MB, Das SR, Chen CY, Gibbs J et al. RNA binding targets aminoacyl-tRNA synthetases to translating ribosomes. J Biol Chem 2011; 286: 20688-20700.
34. Pavon-Eternod M, Gomes S, Geslain R, Dai Q, Rosner MR, Pan T. tRNA overexpression in breast cancer and functional consequences. Nucleic Acids Res 2009; 37: 7268-7280.
35. 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.
36. Reme T, Hugnot JP, Bieche I, Rigau V, Burel-Vandenbos F, Prevot V et al. A Molecular Predictor Reassesses Classification of Human Grade II/III Gliomas. PLoS One 2013; 8: e66574.
37. Balmain A, Harris CC. Carcinogenesis in mouse and human cells: parallels and paradoxes. Carcinogenesis 2000; 21: 371-377.
38. Whalen SG, Gingras AC, Amankwa L, Mader S, Branton PE, Aebersold R et al. Phosphorylation of eIF-4E on serine 209 by protein kinase C is inhibited by the translational repressors, 4E-binding proteins. J Biol Chem 1996; 271: 11831-11837.
39. Guan L, Song K, Pysz MA, Curry KJ, Hizli AA, Danielpour D et al. Protein kinase C-mediated down-regulation of cyclin D1 involves activation of the translational repressor 4E-BP1 via a phosphoinositide 3-kinase/Akt-independent, protein phosphatase 2 A-dependent mechanism in intestinal epithelial cells. J Biol Chem 2007; 282: 14213-14225.
40. Hou J, Lam F, Proud C, Wang S. Targeting Mnks for cancer therapy. Oncotarget 2012; 3: 118-131.
41. Welsh GI, Price NT, Bladergroen BA, Bloomberg G, Proud CG. Identification of novel phosphorylation sites in the beta-subunit of translation initiation factor eIF-2. Biochem Biophys Res Commun 1994; 201: 1279-1288.
42. Andaya A, Jia W, Sokabe M, Fraser CS, Hershey JW, Leary JA. Phosphorylation of human eukaryotic initiation factor 2 gamma: novel site identification and targeted PKC involvement. J Proteome Res 2011; 10: 4613-4623.
43. Alain T, Morita M, Fonseca BD, Yanagiya A, Siddiqui N, Bhat M et al. eIF4E/4E-BP ratio predicts the efficacy of mTOR targeted therapies. Cancer Res 2012; 72: 6468-6476.
44. Boussemart L, Malka-Mahieu H, Girault I, Allard D, Hemmingsson O, Tomasic G et al. eIF4F is a nexus of resistance to anti-BRAF and anti-MEK cancer therapies. Nature 2014; 513: 105-109.
45. Zindy P, Berge Y, Allal B, Filleron T, Pierredon S, Cammas A et al. Formation of the eIF4F translation-initiation complex determines sensitivity to anticancer drugs targeting the EGFR and HER2 receptors. Cancer Res 2011; 71: 4068-4073.
46. Marques JM, Rodrigues RJ, Valbuena S, Rozas JL, Selak S, Marin P et al. CRMP2 tethers kainate receptor activity to cytoskeleton dynamics during neuronal maturation. J Neurosci 2013; 33: 18298-18310.
47. Shevchenko A, Wilm M, Vorm O, Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 1996; 68: 850-858.
48. Chen C, Huang B, Eliasson M, Ryden P, Bystrom AS. Elongator complex influences telomeric gene silencing and DNA damage response by its role in wobble uridine tRNA modification. PLoS Genet 2011; 7: e1002258.
49. Bjork GR, Jacobsson K, Nilsson K, Johansson MJ, Bystrom AS, Persson OP. A primordial tRNA modification required for the evolution of life? EMBO J 2001; 20: 231-239.