Cell-Specific Transcriptional Profiling of Ciliated Sensory Neurons Reveals Regulators of Behavior and Extracellular Vesicle Biogenesis

Juan Wang, Rachel Kaletsky, Malan Silva, April Williams, Leonard A. Haas, Rebecca J. Androwski, Jessica N. Landis, Cory Patrick, Alina Rashid, Dianaliz Santiago-Martinez, Maria Gravato-Nobre, Jonathan Hodgkin, David H. Hall, Coleen T. Murphy, Maureen M. Barr

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

Cilia and extracellular vesicles (EVs) are signaling organelles [1]. Cilia act as cellular sensory antennae, with defects resulting in human ciliopathies. Cilia both release and bind to EVs [1]. EVs are sub-micron-sized particles released by cells and function in both short- and long-range intercellular communication. In C. Elegans and mammals, the autosomal dominant polycystic kidney disease (ADPKD) gene products polycystin-1 and polycystin-2 localize to both cilia and EVs, act in the same genetic pathway, and function in a sensory capacity, suggesting ancient conservation [2]. A fundamental understanding of EV biology and the relationship between the polycystins, cilia, and EVs is lacking. To define properties of a ciliated EV-releasing cell, we performed RNA-seq on 27 GFP-labeled EV-releasing neurons (EVNs) isolated from adult C. Elegans. We identified 335 significantly overrepresented genes, of which 61 were validated by GFP reporters. The EVN transcriptional profile uncovered new pathways controlling EV biogenesis and polycystin signaling and also identified EV cargo, which included an antimicrobial peptide and ASIC channel. Tumor-necrosis-associated factor (TRAF) homologs trf-1 and trf-2 and the p38 mitogen-activated protein kinase (MAPK) pmk-1 acted in polycystin-signaling pathways controlling male mating behaviors. pmk-1 was also required for EV biogenesis, independent of the innate immunity MAPK signaling cascade. This first high-resolution transcriptome profile of a subtype of ciliated sensory neurons isolated from adult animals reveals the functional components of an EVN.

Original languageEnglish (US)
Pages (from-to)3232-3238
Number of pages7
JournalCurrent Biology
Volume25
Issue number24
DOIs
StatePublished - Dec 21 2015

Fingerprint

sensory neurons
TRPP Cation Channels
cilia
Sensory Receptor Cells
Neurons
Cilia
neurons
mitogen-activated protein kinase
Acid Sensing Ion Channels
Genes
cells
Mammals
p38 Mitogen-Activated Protein Kinases
Mitogen-Activated Protein Kinases
cell communication
antimicrobial peptides
Tumors
Conservation
Animals
mating behavior

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Cell-Specific Transcriptional Profiling of Ciliated Sensory Neurons Reveals Regulators of Behavior and Extracellular Vesicle Biogenesis. / Wang, Juan; Kaletsky, Rachel; Silva, Malan; Williams, April; Haas, Leonard A.; Androwski, Rebecca J.; Landis, Jessica N.; Patrick, Cory; Rashid, Alina; Santiago-Martinez, Dianaliz; Gravato-Nobre, Maria; Hodgkin, Jonathan; Hall, David H.; Murphy, Coleen T.; Barr, Maureen M.

In: Current Biology, Vol. 25, No. 24, 21.12.2015, p. 3232-3238.

Research output: Contribution to journalArticle

Wang, J, Kaletsky, R, Silva, M, Williams, A, Haas, LA, Androwski, RJ, Landis, JN, Patrick, C, Rashid, A, Santiago-Martinez, D, Gravato-Nobre, M, Hodgkin, J, Hall, DH, Murphy, CT & Barr, MM 2015, 'Cell-Specific Transcriptional Profiling of Ciliated Sensory Neurons Reveals Regulators of Behavior and Extracellular Vesicle Biogenesis', Current Biology, vol. 25, no. 24, pp. 3232-3238. https://doi.org/10.1016/j.cub.2015.10.057
Wang, Juan ; Kaletsky, Rachel ; Silva, Malan ; Williams, April ; Haas, Leonard A. ; Androwski, Rebecca J. ; Landis, Jessica N. ; Patrick, Cory ; Rashid, Alina ; Santiago-Martinez, Dianaliz ; Gravato-Nobre, Maria ; Hodgkin, Jonathan ; Hall, David H. ; Murphy, Coleen T. ; Barr, Maureen M. / Cell-Specific Transcriptional Profiling of Ciliated Sensory Neurons Reveals Regulators of Behavior and Extracellular Vesicle Biogenesis. In: Current Biology. 2015 ; Vol. 25, No. 24. pp. 3232-3238.
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