Cilioplasm is a cellular compartment for calcium signaling in response to mechanical and chemical stimuli

Xingjian Jin, Ashraf M. Mohieldin, Brian S. Muntean, Jill A. Green, Jagesh V. Shah, Kirk Mykytyn, Surya M. Nauli

Research output: Contribution to journalArticlepeer-review

96 Scopus citations

Abstract

Primary cilia with a diameter of ~200 nm have been implicated in development and disease. Calcium signaling within a primary cilium has never been directly visualized and has therefore remained a speculation. Fluid-shear stress and dopamine receptor type-5 (DR5) agonist are among the few stimuli that require cilia for intracellular calcium signal transduction. However, it is not known if these stimuli initiate calcium signaling within the cilium or if the calcium signal originates in the cytoplasm. Using an integrated single-cell imaging technique, we demonstrate for the first time that calcium signaling triggered by fluid-shear stress initiates in the primary cilium and can be distinguished from the subsequent cytosolic calcium response through the ryanodine receptor. Importantly, this flow-induced calcium signaling depends on the ciliary polycystin-2 calcium channel. While DR5-specific agonist induces calcium signaling mainly in the cilioplasm via ciliary CaV1.2, thrombin specifically induces cytosolic calcium signaling through the IP3 receptor. Furthermore, a non-specific calcium ionophore triggers both ciliary and cytosolic calcium responses. We suggest that cilia not only act as sensory organelles but also function as calcium signaling compartments. Cilium-dependent signaling can spread to the cytoplasm or be contained within the cilioplasm. Our study thus provides the first model to understand signaling within the cilioplasm of a living cell.

Original languageEnglish (US)
Pages (from-to)2165-2178
Number of pages14
JournalCellular and Molecular Life Sciences
Volume71
Issue number11
DOIs
StatePublished - Jun 2014
Externally publishedYes

Keywords

  • Chemosensing
  • Ciliopathy
  • Mechanosensing
  • Microscope
  • Microwire
  • Polycystic kidney

ASJC Scopus subject areas

  • Molecular Medicine
  • Molecular Biology
  • Pharmacology
  • Cellular and Molecular Neuroscience
  • Cell Biology

Fingerprint

Dive into the research topics of 'Cilioplasm is a cellular compartment for calcium signaling in response to mechanical and chemical stimuli'. Together they form a unique fingerprint.

Cite this