eLife (Oct 2024)
Cell-cell interaction determines cell fate of mesoderm-derived cell in tongue development through Hh signaling
- Maiko Kawasaki,
- Katsushige Kawasaki,
- Finsa Tisna Sari,
- Takehisa Kudo,
- Jun Nihara,
- Madoka Kitamura,
- Takahiro Nagai,
- Vanessa Utama,
- Yoko Ishida,
- Fumiya Meguro,
- Alex Kesuma,
- Akira Fujita,
- Takayuki Nishimura,
- Yuan Kogure,
- Satoshi Maruyama,
- Jun-ichi Tanuma,
- Yoshito Kakihara,
- Takeyasu Maeda,
- Sarah Ghafoor,
- Roman H Khonsari,
- Pierre Corre,
- Paul T Sharpe,
- Martyn Cobourne,
- Brunella Franco,
- Atsushi Ohazama
Affiliations
- Maiko Kawasaki
- ORCiD
- Division of Oral Anatomy, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Katsushige Kawasaki
- Division of Oral Anatomy, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan; Center for Advanced Oral Science, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Finsa Tisna Sari
- Division of Oral Anatomy, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Takehisa Kudo
- Division of Oral Anatomy, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan; Division of Orthodontics, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Jun Nihara
- Division of Orthodontics, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Madoka Kitamura
- Division of Oral Anatomy, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan; Division of Orthodontics, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Takahiro Nagai
- Division of Oral Anatomy, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Vanessa Utama
- Division of Oral Anatomy, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Yoko Ishida
- Center for Advanced Oral Science, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Fumiya Meguro
- Division of Oral Anatomy, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Alex Kesuma
- Division of Oral Anatomy, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Akira Fujita
- Division of Orthodontics, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Takayuki Nishimura
- Division of Oral Anatomy, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Yuan Kogure
- Division of Oral Anatomy, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Satoshi Maruyama
- Division of Oral Pathology, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Jun-ichi Tanuma
- Division of Oral Pathology, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Yoshito Kakihara
- Division of Dental Pharmacology, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Takeyasu Maeda
- ORCiD
- Center for Advanced Oral Science, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- Sarah Ghafoor
- Centre for Craniofacial & Regenerative Biology, Faculty of Dentistry, Oral & Craniofacial Sciences, King’s College London, Guy’s Hospital, London, United Kingdom
- Roman H Khonsari
- Centre for Craniofacial & Regenerative Biology, Faculty of Dentistry, Oral & Craniofacial Sciences, King’s College London, Guy’s Hospital, London, United Kingdom
- Pierre Corre
- Service de Chirurgie Maxillofaciale et tomatology, Centre Hospitalier Universitaire de Nantes,1 place Alexis Ricordeau 44000, Nantes, France
- Paul T Sharpe
- ORCiD
- Centre for Craniofacial & Regenerative Biology, Faculty of Dentistry, Oral & Craniofacial Sciences, King’s College London, Guy’s Hospital, London, United Kingdom
- Martyn Cobourne
- ORCiD
- Centre for Craniofacial & Regenerative Biology, Faculty of Dentistry, Oral & Craniofacial Sciences, King’s College London, Guy’s Hospital, London, United Kingdom
- Brunella Franco
- Telethon Institute of Genetics and Medicine (TIGEM), Pozzuoli, Naples, Italy; Medical Genetics, Department of Translational Medical Sciences, Federico II University of Naples, Italy, Naples, Italy; Scuola Superiore Meridionale, School for Advanced Studies, Genomics and Experimental Medicine program,, Naples, Italy
- Atsushi Ohazama
- ORCiD
- Division of Oral Anatomy, Faculty of Dentistry & Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan
- DOI
- https://doi.org/10.7554/eLife.85042
- Journal volume & issue
-
Vol. 13
Abstract
Dysfunction of primary cilia leads to genetic disorder, ciliopathies, which shows various malformations in many vital organs such as brain. Multiple tongue deformities including cleft, hamartoma, and ankyloglossia are also seen in ciliopathies, which yield difficulties in fundamental functions such as mastication and vocalization. Here, we found these tongue anomalies in mice with mutation of ciliary protein. Abnormal cranial neural crest-derived cells (CNCC) failed to evoke Hh signal for differentiation of mesoderm-derived cells into myoblasts, which resulted in abnormal differentiation of mesoderm-derived cells into adipocytes. The ectopic adipose subsequently arrested tongue swelling formation. Ankyloglossia was caused by aberrant cell migration due to lack of non-canonical Wnt signaling. In addition to ciliopathies, these tongue anomalies are often observed as non-familial condition in human. We found that these tongue deformities could be reproduced in wild-type mice by simple mechanical manipulations to disturb cellular processes which were disrupted in mutant mice. Our results provide hints for possible future treatment in ciliopathies.
Keywords
- cell differentiation
- cell migration
- cell-cell interaction
- cranial neural crest-derived cells
- X-inactivation