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Cholesterol accessibility at the ciliary membrane controls hedgehog signaling

by Kinnebrew, Maia , Johnson, Kristen A , Radhakrishnan, Arun , Patel, Bhaven B , Siebold, Christian , Covey, Douglas F , Rohatgi, Rajat , Iverson, Ellen J , McDonald, Jeffrey G , Luchetti, Giovanni , Eckert, Kaitlyn M , Kong, Jennifer H , Pusapati, Ganesh V

in Animals / Biochemistry / Biosynthesis / Birth defects / Cell Biology / Cell membranes / Cholesterol / Cholesterol - metabolism / Cilia / Cilia - metabolism / Clustered Regularly Interspaced Short Palindromic Repeats / Congenital defects / CRISPR / Developmental Biology / Enzymes / Genes / Genomes / Health aspects / Hedgehog protein / Hedgehog Proteins - metabolism / hedgehog signaling / Humans / Influence / Ligands / Lipids / Medicine / Metabolism / patched / Patched protein / Phospholipids / primary cilium / Protein transport / Proteins / Research Advance / Scientific equipment industry / Signal Transduction / smoothened / Sphingomyelin / Statistical analysis / Sterols

2019

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Cholesterol accessibility at the ciliary membrane controls hedgehog signaling

2019

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Cholesterol accessibility at the ciliary membrane controls hedgehog signaling

2019

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Journal Article

Cholesterol accessibility at the ciliary membrane controls hedgehog signaling

Kinnebrew, Maia,

Johnson, Kristen A,

Radhakrishnan, Arun,

Patel, Bhaven B,

Siebold, Christian,

Covey, Douglas F,

Rohatgi, Rajat,

Iverson, Ellen J,

McDonald, Jeffrey G,

Luchetti, Giovanni,

Eckert, Kaitlyn M,

Kong, Jennifer H,

Pusapati, Ganesh V

2019

Overview

Previously we proposed that transmission of the hedgehog signal across the plasma membrane by Smoothened is triggered by its interaction with cholesterol (Luchetti et al., 2016). But how is cholesterol, an abundant lipid, regulated tightly enough to control a signaling system that can cause birth defects and cancer? Using toxin-based sensors that distinguish between distinct pools of cholesterol, we find that Smoothened activation and hedgehog signaling are driven by a biochemically-defined, small fraction of membrane cholesterol, termed accessible cholesterol. Increasing cholesterol accessibility by depletion of sphingomyelin, which sequesters cholesterol in complexes, amplifies hedgehog signaling. Hedgehog ligands increase cholesterol accessibility in the membrane of the primary cilium by inactivating the transporter-like protein Patched 1. Trapping this accessible cholesterol blocks hedgehog signal transmission across the membrane. Our work shows that the organization of cholesterol in the ciliary membrane can be modified by extracellular ligands to control the activity of cilia-localized signaling proteins.

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eLife Science Publications, Ltd,eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd

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