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; Thomas Wurdinger; Elisabeth Ralfkiær; Kirsten Grønbæk; Kristian Helin; Torben Ørntoft; 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

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, Thomas Wurdinger, Elisabeth Ralfkiær, Kirsten Grønbæk, Kristian Helin, Torben Ørntoft , Sebastian M. Waszak, Orna DahanJakob Skou Pedersen, Anders H. Lund, Yitzhak Pilpel

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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.

Original language	English
Pages (from-to)	1281-1292
Journal	Cell
Volume	158
Issue number	6
DOIs	https://doi.org/10.1016/j.cell.2014.08.011
Publication status	Published - 11 Sept 2014
Externally published	Yes

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Gingold, H., Tehler, D., Christoffersen, N. R., Nielsen, M. M., Asmar, F., Kooistra, S. M., Christophersen, N. S., Christensen, L. L., Borre, M., Sørensen , K. D., Andersen, L. D., Andersen, C. L., Hulleman, E., Wurdinger, T., Ralfkiær, E., Grønbæk, K., Helin, K., Ørntoft , T., Waszak, S. M., ... Pilpel, Y. (2014). A dual program for translation regulation in cellular proliferation and differentiation. Cell, 158(6), 1281-1292. https://doi.org/10.1016/j.cell.2014.08.011

@article{5107db8271b045208d30cbf15954b579,

title = "A dual program for translation regulation in cellular proliferation and differentiation",

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.",

author = "Hila Gingold and Disa Tehler and Christoffersen, {Nanna R.} and Nielsen, {Morten M.} and Fazila Asmar and Kooistra, {Susanne M.} and Christophersen, {Nicolaj S.} and Christensen, {Lise Lotte} and Michael Borre and S{\o}rensen, {Karina D.} and Andersen, {Lars D.} and Andersen, {Claus L.} and Esther Hulleman and Thomas Wurdinger and Elisabeth Ralfki{\ae}r and Kirsten Gr{\o}nb{\ae}k and Kristian Helin and Torben {\O}rntoft and Waszak, {Sebastian M.} and Orna Dahan and Pedersen, {Jakob Skou} and Lund, {Anders H.} and Yitzhak Pilpel",

year = "2014",

month = sep,

day = "11",

doi = "10.1016/j.cell.2014.08.011",

language = "English",

volume = "158",

pages = "1281--1292",

journal = "Cell",

issn = "0092-8674",

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Gingold, H, Tehler, D, Christoffersen, NR, Nielsen, MM, Asmar, F, Kooistra, SM, Christophersen, NS, Christensen, LL, Borre, M, Sørensen , KD, Andersen, LD, Andersen, CL, Hulleman, E, Wurdinger, T, Ralfkiær, E, Grønbæk, K, Helin, K, Ørntoft , T, Waszak, SM, Dahan, O, Pedersen, JS, Lund, AH & Pilpel, Y 2014, 'A dual program for translation regulation in cellular proliferation and differentiation', Cell, vol. 158, no. 6, pp. 1281-1292. https://doi.org/10.1016/j.cell.2014.08.011

TY - JOUR

T1 - A dual program for translation regulation in cellular proliferation and differentiation

AU - Gingold, Hila

AU - Tehler, Disa

AU - Christoffersen, Nanna R.

AU - Nielsen, Morten M.

AU - Asmar, Fazila

AU - Kooistra, Susanne M.

AU - Christophersen, Nicolaj S.

AU - Christensen, Lise Lotte

AU - Borre, Michael

AU - Sørensen , Karina D.

AU - Andersen, Lars D.

AU - Andersen, Claus L.

AU - Hulleman, Esther

AU - Wurdinger, Thomas

AU - Ralfkiær, Elisabeth

AU - Grønbæk, Kirsten

AU - Helin, Kristian

AU - Ørntoft , Torben

AU - Waszak, Sebastian M.

AU - Dahan, Orna

AU - Pedersen, Jakob Skou

AU - Lund, Anders H.

AU - Pilpel, Yitzhak

PY - 2014/9/11

Y1 - 2014/9/11

N2 - 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.

AB - 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.

U2 - 10.1016/j.cell.2014.08.011

DO - 10.1016/j.cell.2014.08.011

M3 - Article

SN - 0092-8674

VL - 158

SP - 1281

EP - 1292

JO - Cell

JF - Cell

IS - 6

ER -

A dual program for translation regulation in cellular proliferation and differentiation

Abstract

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