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Hierarchical regulation of mRNA partitioning between the cytoplasm and the endoplasmic reticulum of mammalian cells.

Publication ,  Journal Article
Chen, Q; Jagannathan, S; Reid, DW; Zheng, T; Nicchitta, CV
Published in: Mol Biol Cell
July 15, 2011

The mRNA transcriptome is currently thought to be partitioned between the cytosol and endoplasmic reticulum (ER) compartments by binary selection; mRNAs encoding cytosolic/nucleoplasmic proteins are translated on free ribosomes, and mRNAs encoding topogenic signal-bearing proteins are translated on ER-bound ribosomes, with ER localization being conferred by the signal-recognition particle pathway. In subgenomic and genomic analyses of subcellular mRNA partitioning, we report an overlapping subcellular distribution of cytosolic/nucleoplasmic and topogenic signal-encoding mRNAs, with mRNAs of both cohorts displaying noncanonical subcellular partitioning patterns. Unexpectedly, the topogenic signal-encoding mRNA transcriptome was observed to partition in a hierarchical, cohort-specific manner. mRNAs encoding resident proteins of the endomembrane system were clustered at high ER-enrichment values, whereas mRNAs encoding secretory pathway cargo were broadly represented on free and ER-bound ribosomes. Two distinct modes of mRNA association with the ER were identified. mRNAs encoding endomembrane-resident proteins were bound via direct, ribosome-independent interactions, whereas mRNAs encoding secretory cargo displayed predominantly ribosome-dependent modes of ER association. These data indicate that mRNAs are partitioned between the cytosol and ER compartments via a hierarchical system of intrinsic and encoded topogenic signals and identify mRNA cohort-restricted modes of mRNA association with the ER.

Duke Scholars

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Published In

Mol Biol Cell

DOI

EISSN

1939-4586

Publication Date

July 15, 2011

Volume

22

Issue

14

Start / End Page

2646 / 2658

Location

United States

Related Subject Headings

  • Transcriptome
  • Subcellular Fractions
  • Ribosomes
  • RNA, Messenger
  • Proteins
  • Plasmacytoma
  • Myelolipoma
  • Mice
  • Metabolic Networks and Pathways
  • Membranes
 

Citation

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Chen, Q., Jagannathan, S., Reid, D. W., Zheng, T., & Nicchitta, C. V. (2011). Hierarchical regulation of mRNA partitioning between the cytoplasm and the endoplasmic reticulum of mammalian cells. Mol Biol Cell, 22(14), 2646–2658. https://doi.org/10.1091/mbc.E11-03-0239
Chen, Qiang, Sujatha Jagannathan, David W. Reid, Tianli Zheng, and Christopher V. Nicchitta. “Hierarchical regulation of mRNA partitioning between the cytoplasm and the endoplasmic reticulum of mammalian cells.Mol Biol Cell 22, no. 14 (July 15, 2011): 2646–58. https://doi.org/10.1091/mbc.E11-03-0239.
Chen Q, Jagannathan S, Reid DW, Zheng T, Nicchitta CV. Hierarchical regulation of mRNA partitioning between the cytoplasm and the endoplasmic reticulum of mammalian cells. Mol Biol Cell. 2011 Jul 15;22(14):2646–58.
Chen, Qiang, et al. “Hierarchical regulation of mRNA partitioning between the cytoplasm and the endoplasmic reticulum of mammalian cells.Mol Biol Cell, vol. 22, no. 14, July 2011, pp. 2646–58. Pubmed, doi:10.1091/mbc.E11-03-0239.
Chen Q, Jagannathan S, Reid DW, Zheng T, Nicchitta CV. Hierarchical regulation of mRNA partitioning between the cytoplasm and the endoplasmic reticulum of mammalian cells. Mol Biol Cell. 2011 Jul 15;22(14):2646–2658.

Published In

Mol Biol Cell

DOI

EISSN

1939-4586

Publication Date

July 15, 2011

Volume

22

Issue

14

Start / End Page

2646 / 2658

Location

United States

Related Subject Headings

  • Transcriptome
  • Subcellular Fractions
  • Ribosomes
  • RNA, Messenger
  • Proteins
  • Plasmacytoma
  • Myelolipoma
  • Mice
  • Metabolic Networks and Pathways
  • Membranes