Tags

Type your tag names separated by a space and hit enter

The ribosome biogenesis protein Esf1 is essential for pharyngeal cartilage formation in zebrafish.
FEBS J 2018; 285(18):3464-3484FJ

Abstract

Craniofacial malformations are common congenital birth defects and usually caused by abnormal development of the cranial neural crest cells. Some nucleolar ribosome biogenesis factors are implicated in neural crest disorders also known as neurocristopathies. However, the underlying mechanisms linking ribosome biogenesis and neural crest cell (NCC) development remain to be elucidated. Here we report a novel zebrafish model with a CRISPR/Cas9-generated esf1 mutation, which exhibits severe NCC-derived pharyngeal cartilage loss and defects in the eyes, brain, and heart. The expression of several typical NCC markers, including sox10, dlx2a, nrp2b, crestin, vgll2a, and sox9a, was reduced in the head of the esf1 mutants, which indicates that esf1 plays a role in the development of zebrafish NCCs. We demonstrate that, similar to the yeast, loss of esf1 in zebrafish leads to defects in 18S rRNA biogenesis and ribosome biogenesis. We also show strong upregulation of p53 signaling as well as apoptosis, and poor proliferation in mutants. Inactivation of p53 rescues the early tissue defects and pharyngeal cartilage loss observed in esf1 mutants, indicating that increased cell death and pharyngeal cartilage defects observed in esf1 mutants are mediated via upregulated p53 signaling pathways. Based on transplantation analysis, we found esf1 functions in NCC in a cell autonomous fashion. Together, our results suggest that esf1 is required for NCC development and pharyngeal cartilage formation. These studies provide a potential model for investigating the relationship between ribosome biogenesis defects and craniofacial neurocristopathies.

Authors+Show Affiliations

Key Laboratory of Marine Drugs (Ocean University of China), Chinese Ministry of Education, Qingdao, China. School of Medicine and Pharmacy, Ocean University of China, Qingdao, China. Laboratory for Marine Drugs and Biological Products, Qingdao National Laboratory for Marine Science and Technology, China.CAS Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China.Key Laboratory of Marine Drugs (Ocean University of China), Chinese Ministry of Education, Qingdao, China. School of Medicine and Pharmacy, Ocean University of China, Qingdao, China. Laboratory for Marine Drugs and Biological Products, Qingdao National Laboratory for Marine Science and Technology, China. CAS Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China.Key Laboratory of Marine Drugs (Ocean University of China), Chinese Ministry of Education, Qingdao, China. School of Medicine and Pharmacy, Ocean University of China, Qingdao, China. Laboratory for Marine Drugs and Biological Products, Qingdao National Laboratory for Marine Science and Technology, China.Key Laboratory of Marine Drugs (Ocean University of China), Chinese Ministry of Education, Qingdao, China. School of Medicine and Pharmacy, Ocean University of China, Qingdao, China. Laboratory for Marine Drugs and Biological Products, Qingdao National Laboratory for Marine Science and Technology, China.Key Laboratory of Marine Drugs (Ocean University of China), Chinese Ministry of Education, Qingdao, China. School of Medicine and Pharmacy, Ocean University of China, Qingdao, China. Laboratory for Marine Drugs and Biological Products, Qingdao National Laboratory for Marine Science and Technology, China.Key Laboratory of Marine Drugs (Ocean University of China), Chinese Ministry of Education, Qingdao, China. School of Medicine and Pharmacy, Ocean University of China, Qingdao, China. Laboratory for Marine Drugs and Biological Products, Qingdao National Laboratory for Marine Science and Technology, China.Key Laboratory of Marine Drugs (Ocean University of China), Chinese Ministry of Education, Qingdao, China. School of Medicine and Pharmacy, Ocean University of China, Qingdao, China. Laboratory for Marine Drugs and Biological Products, Qingdao National Laboratory for Marine Science and Technology, China.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

30073783

Citation

Chen, Jian-Yang, et al. "The Ribosome Biogenesis Protein Esf1 Is Essential for Pharyngeal Cartilage Formation in Zebrafish." The FEBS Journal, vol. 285, no. 18, 2018, pp. 3464-3484.
Chen JY, Tan X, Wang ZH, et al. The ribosome biogenesis protein Esf1 is essential for pharyngeal cartilage formation in zebrafish. FEBS J. 2018;285(18):3464-3484.
Chen, J. Y., Tan, X., Wang, Z. H., Liu, Y. Z., Zhou, J. F., Rong, X. Z., ... Li, Y. (2018). The ribosome biogenesis protein Esf1 is essential for pharyngeal cartilage formation in zebrafish. The FEBS Journal, 285(18), pp. 3464-3484. doi:10.1111/febs.14622.
Chen JY, et al. The Ribosome Biogenesis Protein Esf1 Is Essential for Pharyngeal Cartilage Formation in Zebrafish. FEBS J. 2018;285(18):3464-3484. PubMed PMID: 30073783.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - The ribosome biogenesis protein Esf1 is essential for pharyngeal cartilage formation in zebrafish. AU - Chen,Jian-Yang, AU - Tan,Xungang, AU - Wang,Zheng-Hua, AU - Liu,Yun-Zhang, AU - Zhou,Jian-Feng, AU - Rong,Xiao-Zhi, AU - Lu,Ling, AU - Li,Yun, Y1 - 2018/08/24/ PY - 2017/11/06/received PY - 2018/06/10/revised PY - 2018/08/01/accepted PY - 2018/8/4/pubmed PY - 2019/6/8/medline PY - 2018/8/4/entrez KW - apoptosis KW - neural crest cells KW - p53 KW - pharyngeal cartilage SP - 3464 EP - 3484 JF - The FEBS journal JO - FEBS J. VL - 285 IS - 18 N2 - Craniofacial malformations are common congenital birth defects and usually caused by abnormal development of the cranial neural crest cells. Some nucleolar ribosome biogenesis factors are implicated in neural crest disorders also known as neurocristopathies. However, the underlying mechanisms linking ribosome biogenesis and neural crest cell (NCC) development remain to be elucidated. Here we report a novel zebrafish model with a CRISPR/Cas9-generated esf1 mutation, which exhibits severe NCC-derived pharyngeal cartilage loss and defects in the eyes, brain, and heart. The expression of several typical NCC markers, including sox10, dlx2a, nrp2b, crestin, vgll2a, and sox9a, was reduced in the head of the esf1 mutants, which indicates that esf1 plays a role in the development of zebrafish NCCs. We demonstrate that, similar to the yeast, loss of esf1 in zebrafish leads to defects in 18S rRNA biogenesis and ribosome biogenesis. We also show strong upregulation of p53 signaling as well as apoptosis, and poor proliferation in mutants. Inactivation of p53 rescues the early tissue defects and pharyngeal cartilage loss observed in esf1 mutants, indicating that increased cell death and pharyngeal cartilage defects observed in esf1 mutants are mediated via upregulated p53 signaling pathways. Based on transplantation analysis, we found esf1 functions in NCC in a cell autonomous fashion. Together, our results suggest that esf1 is required for NCC development and pharyngeal cartilage formation. These studies provide a potential model for investigating the relationship between ribosome biogenesis defects and craniofacial neurocristopathies. SN - 1742-4658 UR - https://www.unboundmedicine.com/medline/citation/30073783/The_ribosome_biogenesis_protein_Esf1_is_essential_for_pharyngeal_cartilage_formation_in_zebrafish_ L2 - https://doi.org/10.1111/febs.14622 DB - PRIME DP - Unbound Medicine ER -