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

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 DahanJakob Skou Pedersen, Anders H. Lund, Yitzhak Pilpel

220 Citations (Scopus)

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
Journal	Cell
Volume	158
Issue number	6
Pages (from-to)	1281-92
Number of pages	12
ISSN	0092-8674
DOIs	https://doi.org/10.1016/j.cell.2014.08.011
Publication status	Published - 11 Sept 2014

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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., Helin, K., Grønbæk, K., Orntoft, T., Waszak, S. M., ... Pilpel, Y. (2014). A Dual Program for Translation Regulation in Cellular Proliferation and Differentiation. Cell, 158(6), 1281-92. https://doi.org/10.1016/j.cell.2014.08.011

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, Helin, K, Grønbæk, K, Orntoft, 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. 1281-92. https://doi.org/10.1016/j.cell.2014.08.011

@article{0628c2315ea14891a8fe77099dc0f547,

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 Tom Wurdinger and Elisabeth Ralfki{\ae}r and Kristian Helin and Kirsten Gr{\o}nb{\ae}k and Torben Orntoft and Waszak, {Sebastian M} and Orna Dahan and Pedersen, {Jakob Skou} and Lund, {Anders H.} and Yitzhak Pilpel",

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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, Tom

AU - Ralfkiær, Elisabeth

AU - Helin, Kristian

AU - Grønbæk, Kirsten

AU - Orntoft, Torben

AU - Waszak, Sebastian M

AU - Dahan, Orna

AU - Pedersen, Jakob Skou

AU - Lund, Anders H.

AU - Pilpel, Yitzhak

PY - 2014/9/11

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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

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VL - 158

SP - 1281

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JO - Cell

JF - Cell

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ER -

A Dual Program for Translation Regulation in Cellular Proliferation and Differentiation

Abstract

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