A dual program for translation regulation in cellular proliferation and differentiation

Hila Gingold; Disa Tehler; Nanna R Christoffersen; Morten M Nielsen; Fazila Asmar; Susanne M Kooistra; Nicolaj S Christophersen; Lise Lotte Christensen; Michael Borre; Karina D Sørensen; Lars D Andersen; Claus L Andersen; Esther Hulleman; Tom Wurdinger; Elisabeth Ralfkiær; Kristian Helin; Kirsten Grønbæk; Torben Orntoft; Sebastian M Waszak; Orna Dahan; Jakob Skou Pedersen; Anders H Lund; Yitzhak Pilpel

doi:10.1016/j.cell.2014.08.011

A dual program for translation regulation in cellular proliferation and differentiation

Authors:

Gingold, Hila ;
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Department of Molecular Genetics, The Weizmann Institute of Science, Rehovot 76100, Israel.
Tehler, Disa ;
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Biotech Research and Innovation Centre, University of Copenhagen, 2200 Copenhagen, Denmark.
Christoffersen, Nanna R ;
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Biotech Research and Innovation Centre, University of Copenhagen, 2200 Copenhagen, Denmark.
Nielsen, Morten M ;
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Department of Clinical Medicine - Molekylær Medicinsk afdeling (MOMA), Department of Clinical Medicine, Health, Aarhus University
Asmar, Fazila ;
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Department of Hematology, Rigshospitalet, University of Copenhagen, 2100 Copenhagen, Denmark.
Kooistra, Susanne M ;
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Biotech Research and Innovation Centre, University of Copenhagen, 2200 Copenhagen, Denmark.
Christophersen, Nicolaj S ;
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Biotech Research and Innovation Centre, University of Copenhagen, 2200 Copenhagen, Denmark.
Christensen, Lise Lotte ;
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Department of Analytic Chemistry, Faculty of Agricultural Sciences, Aarhus University, Aarhus University
Borre, Michael ;
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Department of Clinical Medicine - Department of Urology, Department of Clinical Medicine, Health, Aarhus University
Sørensen, Karina D ;
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0000-0002-4902-5490
Department of Clinical Medicine - Molekylær Medicinsk afdeling (MOMA), Department of Clinical Medicine, Health, Aarhus University
Andersen, Lars D ;
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0000-0001-7061-9851
Department of Clinical Medicine - Molekylær Medicinsk afdeling (MOMA), Department of Clinical Medicine, Health, Aarhus University
Andersen, Claus L ;
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Department of Clinical Medicine - Molekylær Medicinsk afdeling (MOMA), Department of Clinical Medicine, Health, Aarhus University
Hulleman, Esther ;
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Department of Pediatric Oncology, Neuro-oncology Research Group, Cancer Center Amsterdam, VU University Medical Center, 1007 MB Amsterdam, the Netherlands.
Wurdinger, Tom ;
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Department of Neurosurgery, Neuro-oncology Research Group, Cancer Center Amsterdam, VU University Medical Center, 1007 MB Amsterdam, the Netherlands; Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA.
Ralfkiær, Elisabeth ;
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Department of Pathology, Rigshospitalet, University of Copenhagen, 2100 Copenhagen, Denmark.
Helin, Kristian ;
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Department of Clinical Medicine - Department of Experimental Clinical Oncology, Department of Clinical Medicine, Health, Aarhus University
Grønbæk, Kirsten ;
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Department of Hematology, Rigshospitalet, University of Copenhagen, 2100 Copenhagen, Denmark.
Orntoft, Torben ;
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Department of Clinical Medicine - Molekylær Medicinsk afdeling (MOMA), Department of Clinical Medicine, Health, Aarhus University
Waszak, Sebastian M ;
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École Polytechnique Fédérale de Lausanne
Dahan, Orna ;
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Department of Molecular Genetics, The Weizmann Institute of Science, Rehovot 76100, Israel.
Pedersen, Jakob Skou ;
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Department of Clinical Medicine - Molekylær Medicinsk afdeling (MOMA), Department of Clinical Medicine, Health, Aarhus University
Lund, Anders H ;
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Faculty of Science, Aarhus University, Aarhus University
Pilpel, Yitzhak
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Department of Molecular Genetics, The Weizmann Institute of Science, Rehovot 76100, Israel. Electronic address: pilpel@weizmann.ac.il.

DOI:

10.1016/j.cell.2014.08.011

Abstract:

A dichotomous choice for metazoan cells is between proliferation and differentiation. Measuring tRNA pools in various cell types, we found two distinct subsets, one that is induced in proliferating cells, and repressed otherwise, and another with the opposite signature. Correspondingly, we found that genes serving cell-autonomous functions and genes involved in multicellularity obey distinct codon usage. Proliferation-induced and differentiation-induced tRNAs often carry anticodons that correspond to the codons enriched among the cell-autonomous and the multicellularity genes, respectively. Because mRNAs of cell-autonomous genes are induced in proliferation and cancer in particular, the concomitant induction of their codon-enriched tRNAs suggests coordination between transcription and translation. Histone modifications indeed change similarly in the vicinity of cell-autonomous genes and their corresponding tRNAs, and in multicellularity genes and their tRNAs, suggesting the existence of transcriptional programs coordinating tRNA supply and demand. Hence, we describe the existence of two distinct translation programs that operate during proliferation and differentiation.

Type:

Journal article

Language:

English

Published in:

Cell, 2014, Vol 158, Issue 6, p. 1281-92

Keywords:

Journal Article; Research Support, Non-U.S. Gov't; Anticodon; Cell Differentiation; Cell Line, Tumor; Cell Proliferation; Cell Transformation, Neoplastic; Codon; Histones; Humans; Neoplasms; Protein Biosynthesis; RNA, Messenger; RNA, Transfer; Transcriptome

Main Research Area:

Medical science

Publication Status:

Published

Review type:

Peer Review

Submission year:

2014

Scientific Level:

Scientific

ID:

270966144

A dual program for translation regulation in cellular proliferation and differentiation

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