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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Lund Group, BRIC Research Groups, BRIC, Københavns Universitet
Christoffersen, Nanna R ;
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Lund Group, BRIC Research Groups, BRIC, Københavns Universitet
Nielsen, Morten M ;
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Department of Immunology and Microbiology, Department of Immunology and Microbiology, Faculty of Health and Medical Sciences, Københavns Universitet
Asmar, Fazila ;
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Department of Clinical Medicine, Faculty of Health and Medical Sciences, Københavns Universitet
Kooistra, Susanne M ;
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Helin Group, BRIC Research Groups, BRIC, Københavns Universitet
Christophersen, Nicolaj S ;
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Helin Group, BRIC Research Groups, BRIC, Københavns Universitet
Christensen, Lise Lotte ;
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Section of Diagnostic Sciences, Department of Clinical Medicine, Faculty of Health and Medical Sciences, Københavns Universitet
Borre, Michael ;
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Graduate School of Health and Medical Sciences, Graduate School of Health and Medical Sciences, Faculty of Health and Medical Sciences, Københavns Universitet
Sørensen, Karina D ;
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Department for Molecular Medicine, Aarhus University Hospital
Andersen, Lars D ;
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Department for Molecular Medicine, Aarhus University Hospital
Andersen, Claus L ;
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Department for Molecular Medicine, Aarhus University Hospital
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 Clinical Medicine, Department of Clinical Medicine, Faculty of Health and Medical Sciences, Københavns Universitet
Helin, Kristian ;
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0000-0003-1975-6097
Helin Group, BRIC Research Groups, BRIC, Københavns Universitet
Grønbæk, Kirsten ;
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Department of Clinical Medicine, Department of Clinical Medicine, Faculty of Health and Medical Sciences, Københavns Universitet
Orntoft, Torben ;
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Department for Molecular Medicine, Aarhus University Hospital
Waszak, Sebastian M ;
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Institute of Bioengineering, School of Life Sciences, École Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland.
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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Graduate School of Health and Medical Sciences, Faculty of Health and Medical Sciences, Københavns Universitet
Lund, Anders H. ;
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0000-0002-7407-3398
Lund Group, BRIC Research Groups, BRIC, Københavns Universitet
Pilpel, Yitzhak
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Department of Molecular Genetics, The Weizmann Institute of Science, Rehovot 76100, Israel.

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:

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

Main Research Area:

Science/technology

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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