Regulation of mRNA translation during mitosis

被引:130
作者
Tanenbaum, Marvin E. [1 ]
Stern-Ginossar, Noam [1 ,2 ,3 ]
Weissman, Jonathan S. [1 ,2 ,3 ]
Vale, Ronald D. [1 ]
机构
[1] Univ Calif San Francisco, Howard Hughes Med Inst, Dept Cellular & Mol Pharmacol, San Francisco, CA 94117 USA
[2] Ctr RNA Syst Biol, Berkeley, CA USA
[3] Univ Calif San Francisco, Calif Inst Quantitat Biomed Res, San Francisco, CA 94143 USA
关键词
RIBOSOME ENTRY SITE; ANAPHASE-PROMOTING COMPLEX/CYCLOSOME; CELL-CYCLE PROGRESSION; PROTEIN-SYNTHESIS; MAMMALIAN-CELLS; IN-VIVO; S-PHASE; INITIATION; REVEALS; PHOSPHORYLATION;
D O I
10.7554/eLife.07957
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Passage through mitosis is driven by precisely-timed changes in transcriptional regulation and protein degradation. However, the importance of translational regulation during mitosis remains poorly understood. Here, using ribosome profiling, we find both a global translational repression and identified similar to 200 mRNAs that undergo specific translational regulation at mitotic entry. In contrast, few changes in mRNA abundance are observed, indicating that regulation of translation is the primary mechanism of modulating protein expression during mitosis. Interestingly, 91% of the mRNAs that undergo gene-specific regulation in mitosis are translationally repressed, rather than activated. One of the most pronounced translationally-repressed genes is Emi1, an inhibitor of the anaphase promoting complex (APC) which is degraded during mitosis. We show that full APC activation requires translational repression of Emi1 in addition to its degradation. These results identify gene-specific translational repression as a means of controlling the mitotic proteome, which may complement post-translational mechanisms for inactivating protein function.
引用
收藏
页数:19
相关论文
共 56 条
[41]   Preferential translation of internal ribosome entry site-containing mRNAs during the mitotic cycle in mammalian cells [J].
Qin, XL ;
Sarnow, P .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2004, 279 (14) :13721-13728
[42]   Mitotic Raptor Promotes mTORC1 Activity, G2/M Cell Cycle Progression, and Internal Ribosome Entry Site-Mediated mRNA Translation [J].
Ramirez-Valle, Francisco ;
Badura, Michelle L. ;
Braunstein, Steve ;
Narasimhan, Manisha ;
Schneider, Robert J. .
MOLECULAR AND CELLULAR BIOLOGY, 2010, 30 (13) :3151-3164
[43]   Emi1 is a mitotic regulator that interacts with Cdc20 and inhibits the anaphase promoting complex [J].
Reimann, JDR ;
Freed, E ;
Hsu, JY ;
Kramer, ER ;
Peters, JM ;
Jackson, PK .
CELL, 2001, 105 (05) :645-655
[44]   A role for hnRNP C1/C2 and Unr in internal initiation of translation during mitosis [J].
Schepens, Bert ;
Tinton, Sandrine A. ;
Bruynooghe, Yanik ;
Parthoens, Eef ;
Haegman, Mira ;
Beyaert, Rudi ;
Cornelis, Sigrid .
EMBO JOURNAL, 2007, 26 (01) :158-169
[45]   Global quantification of mammalian gene expression control [J].
Schwanhaeusser, Bjoern ;
Busse, Dorothea ;
Li, Na ;
Dittmar, Gunnar ;
Schuchhardt, Johannes ;
Wolf, Jana ;
Chen, Wei ;
Selbach, Matthias .
NATURE, 2011, 473 (7347) :337-342
[46]   CDK1 substitutes for mTOR kinase to activate mitotic cap-dependent protein translation [J].
Shuda, Masahiro ;
Velasquez, Celestino ;
Cheng, Erdong ;
Cordek, Daniel G. ;
Kwun, Hyun Jin ;
Chang, Yuan ;
Moore, Patrick S. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2015, 112 (19) :5875-5882
[47]   Regulation of mRNA translation during cellular division [J].
Sivan, Gilad ;
Stein, Orna Elroy .
CELL CYCLE, 2008, 7 (06) :741-744
[48]   Mitotic Modulation of Translation Elongation Factor 1 Leads to Hindered tRNA Delivery to Ribosomes [J].
Sivan, Gilad ;
Aviner, Ranen ;
Elroy-Stein, Orna .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2011, 286 (32) :27927-27935
[49]   The Translational Landscape of the Mammalian Cell Cycle [J].
Stumpf, Craig R. ;
Moreno, Melissa V. ;
Olshen, Adam B. ;
Taylor, Barry S. ;
Ruggero, Davide .
MOLECULAR CELL, 2013, 52 (04) :574-582
[50]   Poly(A)-tail profiling reveals an embryonic switch in translational control [J].
Subtelny, Alexander O. ;
Eichhorn, Stephen W. ;
Chen, Grace R. ;
Sive, Hazel ;
Bartel, David P. .
NATURE, 2014, 508 (7494) :66-+