Synergistic action of nectins and cadherins generates the mosaic cellular pattern of the olfactory epithelium

Author:

Katsunuma Sayaka12,Honda Hisao34,Shinoda Tomoyasu5,Ishimoto Yukitaka6,Miyata Takaki5,Kiyonari Hiroshi78,Abe Takaya8,Nibu Ken-ichi2,Takai Yoshimi1910,Togashi Hideru1

Affiliation:

1. Division of Molecular and Cellular Biology, Department of Biochemistry and Molecular Biology, Kobe University Graduate School of Medicine, Kobe 650-0017, Japan

2. Department of Otolaryngology-Head and Neck Surgery, Kobe University Graduate School of Medicine, Kobe 650-0017, Japan

3. Division of Neural Differentiation and Regeneration, Department of Physiology and Cell Biology, Kobe University Graduate School of Medicine, Kobe 650-0017, Japan

4. Laboratory for Morphogenetic Signaling, RIKEN Center for Developmental Biology, Kobe 650-0047, Japan

5. Department of Anatomy and Cell Biology, Nagoya University Graduate School of Medicine, Nagoya 466-8550, Japan

6. Department of Machine Intelligence and Systems Engineering, Akita Prefectural University, Akita 015-0055, Japan

7. Animal Resource Development Unit, RIKEN Center for Life Science Technologies, Kobe 650-0047, Japan

8. Genetic Engineering Team, Division of Bio-function Dynamics Imaging, RIKEN Center for Life Science Technologies, Kobe 650-0047, Japan

9. Division of Pathogenetic Signaling, Department of Biochemistry and Molecular Biology, Kobe University Graduate School of Medicine, Kobe 650-0047, Japan

10. CREST, Japan Science and Technology Agency, Kobe 650-0047, Japan

Abstract

In the olfactory epithelium (OE), olfactory cells (OCs) and supporting cells (SCs), which express different cadherins, are arranged in a characteristic mosaic pattern in which OCs are enclosed by SCs. However, the mechanism underlying this cellular patterning is unclear. Here, we show that the cellular pattern of the OE is established by cellular rearrangements during development. In the OE, OCs express nectin-2 and N-cadherin, and SCs express nectin-2, nectin-3, E-cadherin, and N-cadherin. Heterophilic trans-interaction between nectin-2 on OCs and nectin-3 on SCs preferentially recruits cadherin via α-catenin to heterotypic junctions, and the differential distributions of cadherins between junctions promote cellular intercalations, resulting in the formation of the mosaic pattern. These observations are confirmed by model cell systems, and various cellular patterns are generated by the combinatorial expression of nectins and cadherins. Collectively, the synergistic action of nectins and cadherins generates mosaic pattern, which cannot be achieved by a single mechanism.

Funder

Japan Society for the Promotion of Science

Takeda Science Foundation

Publisher

Rockefeller University Press

Subject

Cell Biology

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