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The compass in our ears

Sensory "hair cells" in our inner ear convert sound waves into electrical signals that reflect polar directions ...


Humans inherited the capacity to hear sounds thanks to structures that evolved millions of years ago. Sensory "hair cells" in our inner ear have an amazing ability to convert sound waves into electrical signals and transmit them to our brain for processing.

Each individual hair cell develops a motion sensor in the form of a brush of hair-like protrusions called hair bundles. These bundles are precisely organized and reflect directionality turning much like a magnetized needle in a compass. Neighboring hair cells all orient their bundles in concert, just the same way a collection of compasses all point to magnetic north pole.

Both single cells and organs use directionality. "Planar cell polarity" proteins establish north and south pole in an organ, while Gpsm2/LGN-Gai proteins act in single hair cells to give them directionality. How these two systems reconcile for normal hearing function has been a mystery so far.
Daple is a promising candidate in the coordination of both single cell and organ directionality.

Now, a collaboration between researchers at Jackson Laboratory (JAX) and Rockefeller University, has identified Daple protein as it interacts with both systems. Researchers, Basile Tarchini of JAX, and A.J. Hudspeth of Howard Hughes Medical Institute, along with student Kimberly Siletti of Rockefeller University, found that mice lacking Daple protein have misoriented and misshapen hair bundles. The defects in pattern indicate both organs as well as single cells will have defects. In earlier work, Tarchini and colleagues had established the signaling role of Gpsm2/LGN- Gai in modeling the staircase-like architecture of hair-bundles.

The study is published in the Dec. 11, 2017, Proceedings of the National Academy of Sciences PNAS.

Significance
Each hair cell of our auditory and vestibular systems transduces stimuli into electrical signals through its mechanosensitive hair bundle. Because the bundle is responsive along only a single axis, its orientation is crucial. Two systems determine hair-bundle polarity: planar cell polarity proteins, which establish axes along which hair cells are oriented, and the proteins G?i and LGN. Investigating how these two systems are coordinated so that each hair bundle is appropriately aligned, we identified Daple. In mutants lacking Daple, hair bundles are misoriented and misshapen, a phenotype suggestive of both organ-wide and cell-intrinsic defects. Our study indicates how Daple interacts with proteins of the two systems and proposes a model for its role in determining hair-bundle polarity.

Abstract
The establishment of planar polarization by mammalian cells necessitates the integration of diverse signaling pathways. In the inner ear, at least two systems regulate the planar polarity of sensory hair bundles. The core planar cell polarity (PCP) proteins coordinate the orientations of hair cells across the epithelial plane. The cell-intrinsic patterning of hair bundles is implemented independently by the G protein complex classically known for orienting the mitotic spindle. Although the primary cilium also participates in each of these pathways, its role and the integration of the two systems are poorly understood. We show that Dishevelled-associating protein with a high frequency of leucine residues (Daple) interacts with PCP and cell-intrinsic signals. Regulated by the cell-intrinsic pathway, Daple is required to maintain the polarized distribution of the core PCP protein Dishevelled and to position the primary cilium at the abneural edge of the apical surface. Our results suggest that the primary cilium or an associated structure influences the domain of cell-intrinsic signals that shape the hair bundle. Daple is therefore essential to orient and pattern sensory hair bundles.

Authors: Kimberly Siletti, Basile Tarchinic, and A. J. Hudspeth

Key words: auditory system cochlea hair cell planar cell polarity primary cilium

The Jackson Laboratory is an independent, nonprofit biomedical research institution based in Bar Harbor, Maine. JAX has a National Cancer Institute-designated Cancer Center in Sacramento, California, and a genomic medicine institute in Farmington, Conneticut. Employing more than 2,000 staff, its mission is to discover precise genomic solutions for disease and empower the global biomedical community in the shared quest to improve human health.

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Scanning Electron Microscope (SEM) image of an array of ciliary bundles in the frog inner ear.
Image credit: University of Virginia Health System.


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