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The Caenorhabditis elegans anchor cell transcriptome: ribosome biogenesis drives cell invasion through basement membrane.

Publication ,  Journal Article
Costa, DS; Kenny-Ganzert, IW; Chi, Q; Park, K; Kelley, LC; Garde, A; Matus, DQ; Park, J; Yogev, S; Goldstein, B; Gibney, TV; Pani, AM; Sherwood, DR
Published in: Development (Cambridge, England)
May 2023

Cell invasion through basement membrane (BM) barriers is important in development, immune function and cancer progression. As invasion through BM is often stochastic, capturing gene expression profiles of actively invading cells in vivo remains elusive. Using the stereotyped timing of Caenorhabditis elegans anchor cell (AC) invasion, we generated an AC transcriptome during BM breaching. Through a focused RNAi screen of transcriptionally enriched genes, we identified new invasion regulators, including translationally controlled tumor protein (TCTP). We also discovered gene enrichment of ribosomal proteins. AC-specific RNAi, endogenous ribosome labeling and ribosome biogenesis analysis revealed that a burst of ribosome production occurs shortly after AC specification, which drives the translation of proteins mediating BM removal. Ribosomes also enrich near the AC endoplasmic reticulum (ER) Sec61 translocon and the endomembrane system expands before invasion. We show that AC invasion is sensitive to ER stress, indicating a heightened requirement for translation of ER-trafficked proteins. These studies reveal key roles for ribosome biogenesis and endomembrane expansion in cell invasion through BM and establish the AC transcriptome as a resource to identify mechanisms underlying BM transmigration.

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Published In

Development (Cambridge, England)

DOI

EISSN

1477-9129

ISSN

0950-1991

Publication Date

May 2023

Volume

150

Issue

9

Start / End Page

dev201570

Related Subject Headings

  • Transcriptome
  • Ribosomes
  • Caenorhabditis elegans Proteins
  • Caenorhabditis elegans
  • Basement Membrane
  • Animals
  • 42 Health sciences
  • 32 Biomedical and clinical sciences
  • 31 Biological sciences
  • 11 Medical and Health Sciences
 

Citation

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Costa, D. S., Kenny-Ganzert, I. W., Chi, Q., Park, K., Kelley, L. C., Garde, A., … Sherwood, D. R. (2023). The Caenorhabditis elegans anchor cell transcriptome: ribosome biogenesis drives cell invasion through basement membrane. Development (Cambridge, England), 150(9), dev201570. https://doi.org/10.1242/dev.201570
Costa, Daniel S., Isabel W. Kenny-Ganzert, Qiuyi Chi, Kieop Park, Laura C. Kelley, Aastha Garde, David Q. Matus, et al. “The Caenorhabditis elegans anchor cell transcriptome: ribosome biogenesis drives cell invasion through basement membrane.Development (Cambridge, England) 150, no. 9 (May 2023): dev201570. https://doi.org/10.1242/dev.201570.
Costa DS, Kenny-Ganzert IW, Chi Q, Park K, Kelley LC, Garde A, et al. The Caenorhabditis elegans anchor cell transcriptome: ribosome biogenesis drives cell invasion through basement membrane. Development (Cambridge, England). 2023 May;150(9):dev201570.
Costa, Daniel S., et al. “The Caenorhabditis elegans anchor cell transcriptome: ribosome biogenesis drives cell invasion through basement membrane.Development (Cambridge, England), vol. 150, no. 9, May 2023, p. dev201570. Epmc, doi:10.1242/dev.201570.
Costa DS, Kenny-Ganzert IW, Chi Q, Park K, Kelley LC, Garde A, Matus DQ, Park J, Yogev S, Goldstein B, Gibney TV, Pani AM, Sherwood DR. The Caenorhabditis elegans anchor cell transcriptome: ribosome biogenesis drives cell invasion through basement membrane. Development (Cambridge, England). 2023 May;150(9):dev201570.
Journal cover image

Published In

Development (Cambridge, England)

DOI

EISSN

1477-9129

ISSN

0950-1991

Publication Date

May 2023

Volume

150

Issue

9

Start / End Page

dev201570

Related Subject Headings

  • Transcriptome
  • Ribosomes
  • Caenorhabditis elegans Proteins
  • Caenorhabditis elegans
  • Basement Membrane
  • Animals
  • 42 Health sciences
  • 32 Biomedical and clinical sciences
  • 31 Biological sciences
  • 11 Medical and Health Sciences