Core planar cell polarity genes VANGL1 and VANGL2 in predisposition to congenital vertebral malformations

Author:

Feng Xin1234,Ye Yongyu5,Zhang Jianan16,Zhang Yuanqiang7,Zhao Sen28,Mak Judith C. W.9ORCID,Otomo Nao1011,Zhao Zhengye28,Niu Yuchen812,Yonezawa Yoshiro1011,Li Guozhuang28,Lin Mao13ORCID,Li Xiaoxin812,Cheung Prudence Wing Hang6,Xu Kexin28,Takeda Kazuki1011,Wang Shengru2,Xie Junjie14,Kotani Toshiaki10,Choi Vanessa N. T.4,Song You-Qiang414ORCID,Yang Yang28,Luk Keith Dip Kei6ORCID,Lee Kin Shing15,Li Ziquan28,Li Pik Shan15,Leung Connie Y. H.15ORCID,Lin Xiaochen14,Wang Xiaolu16,Qiu Guixing28, ,Watanabe Kota10, ,Wu Zhihong12,Posey Jennifer E.16,Ikegawa Shiro11,Lupski James R.16171819ORCID,Cheung Jason Pui Yin620ORCID,Zhang Terry Jianguo238,Gao Bo14202122ORCID,Wu Nan238ORCID,Qiu Guixing,Wu Nan,Zhang Jianguo,Wu Zhihong,Wang Shengru,Liu Sen,Li Ziquan,Yang Yang,Zhao Zhengye,Chen Guilin,Li Guozhuang,Zhu Yuanpeng,Cai Jihao,Liu Di,Xu Kexin,Yang Jianle,Maheshati Aoran,Li Qing,Xie Jingyi,Yin Xiangjie,Wang Jie,Li Zihua,Zheng Zhifa,Fang Kun,Nie Xiangyu,Cheng Xi,Wen Wen,Yang Xinyu,Zhang Yuanqiang,Liu Lian,Wang Lianlei,Chen Na,Lin Jiachen,Lin Mao,Zhao Lina,Liu Fei,Niu Yuchen,Liu Qing,Gao Guangxi,Li Shuai,Bai Yueyan,Zhao Sen,Ye Yongyu,Zhao Hengqiang,Chen Zefu,Liu Jiaqi,Yan Zihui,Yu Chenxi,Shao Jiashen,Otomo Nao,Yonezawa Yoshiro,Takeda Kazuki,Ogura Yoji,Kawakami Noriaki,Koatani Toshiaki,Suzuki Teppei,Uno Koki,Sudo Hideki,Inami Satoshi,Taneichi Hiroshi,Shigematsu Hideki,Watanabe Kei,Sugawara Ryo,Taniguchi Yuki,Minami Shohei,Nakamura Masaya,Matsumoto Morio,Ikegawa Shiro,Watanabe Kota

Affiliation:

1. School of Biomedical Sciences, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China

2. Department of Orthopedic Surgery, State Key Laboratory of Complex Severe and Rare Diseases, all at Peking Union Medical College Hospital, Peking Union Medical College and Chinese Academy of Medical Sciences, Beijing 100730, China

3. Key laboratory of big data for spinal deformities, Chinese Academy of Medical Sciences, Beijing 100730, China

4. School of Biomedical Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong Special Administrative Region, China

5. Department of Orthopedic Surgery, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou 510080, China

6. Department of Orthopaedics and Traumatology, School of Clinical Medicine, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong Special Administrative Region, China

7. Department of Orthopaedic Surgery, Qilu Hospital, Cheeloo College of Medicine, Shandong University, Jinan 250012, China

8. Beijing Key Laboratory for Genetic Research of Skeletal Deformity, Beijing 100730, China

9. Department of Pharmacology and Pharmacy, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong Special Administrative Region, China

10. Department of Orthopedic Surgery, Keio University School of Medicine, Tokyo 160-8582, Japan

11. Laboratory of Bone and Joint Diseases, RIKEN Center for Integrative Medical Sciences, Tokyo 108-8639, Japan

12. Department of Medical Research Center, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College and Chinese Academy of Medical Sciences, Beijing 100730, China

13. Department of Orthopedic Surgery, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou 310003, China

14. Department of Medicine, The University of Hong Kong-Shenzhen Hospital, Shenzhen 518009, China

15. Center for Comparative Medicine Research, The University of Hong Kong, Hong Kong Special Administrative Region, China

16. Department of Molecular and Human Genetics, Baylor College of Medicine, Houston 77030, TX

17. Human Genome Sequencing Center, Baylor College of Medicine, Houston 77030, TX

18. Texas Children’s Hospital, Houston 77030, TX

19. Department of Pediatrics, Baylor College of Medicine, Houston 77030, TX

20. Department of Orthopedics and Traumatology, The University of Hong Kong-Shenzhen Hospital, Shenzhen 518009, China

21. Centre for Translational Stem Cell Biology, Hong Kong Special Administrative Region, China

22. Key Laboratory of Regenerative Medicine, Ministry of Education, School of Biomedical Sciences, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China

Abstract

Congenital scoliosis (CS), affecting approximately 0.5 to 1 in 1,000 live births, is commonly caused by congenital vertebral malformations (CVMs) arising from aberrant somitogenesis or somite differentiation. While Wnt/ß-catenin signaling has been implicated in somite development, the function of Wnt/planar cell polarity (Wnt/PCP) signaling in this process remains unclear. Here, we investigated the role of Vangl1 and Vangl2 in vertebral development and found that their deletion causes vertebral anomalies resembling human CVMs. Analysis of exome sequencing data from multiethnic CS patients revealed a number of rare and deleterious variants in VANGL1 and VANGL2 , many of which exhibited loss-of-function and dominant-negative effects. Zebrafish models confirmed the pathogenicity of these variants. Furthermore, we found that Vangl1 knock-in (p.R258H) mice exhibited vertebral malformations in a Vangl gene dose- and environment-dependent manner. Our findings highlight critical roles for PCP signaling in vertebral development and predisposition to CVMs in CS patients, providing insights into the molecular mechanisms underlying this disorder.

Funder

MOST | National Natural Science Foundation of China

China Postdoctoral Science Foundation

Health and Medical Research Fund

Publisher

Proceedings of the National Academy of Sciences

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