Coordination of two enhancers drives expression of olfactory trace amine-associated receptors

Aimei Fei, Wanqing Wu, Longzhi Tan, Cheng Tang, Zhengrong Xu, Xiaona Huo, Hongqiang Bao, Yalei Kong, Mark Johnson, Griffin Hartmann, Mustafa Talay, Cheng Yang, Clemens Riegler, Kristian J. Herrera, Florian Engert, X. Sunney Xie, Gilad Barnea, Stephen D. Liberles, Hui Yang and Qian Li ()
Additional contact information
Aimei Fei: Shanghai Jiao Tong University School of Medicine
Wanqing Wu: Shanghai Jiao Tong University School of Medicine
Longzhi Tan: Harvard University
Cheng Tang: Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences
Zhengrong Xu: Shanghai Jiao Tong University School of Medicine
Xiaona Huo: Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences
Hongqiang Bao: Shanghai Jiao Tong University School of Medicine
Yalei Kong: Shanghai Jiao Tong University School of Medicine
Mark Johnson: Brown University
Griffin Hartmann: Brown University
Mustafa Talay: Brown University
Cheng Yang: Shanghai Jiao Tong University School of Medicine
Clemens Riegler: Harvard University
Kristian J. Herrera: Harvard University
Florian Engert: Harvard University
X. Sunney Xie: Harvard University
Gilad Barnea: Brown University
Stephen D. Liberles: Harvard Medical School
Hui Yang: Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences
Qian Li: Shanghai Jiao Tong University School of Medicine

Nature Communications, 2021, vol. 12, issue 1, 1-19

Abstract: Abstract Olfactory sensory neurons (OSNs) are functionally defined by their expression of a unique odorant receptor (OR). Mechanisms underlying singular OR expression are well studied, and involve a massive cross-chromosomal enhancer interaction network. Trace amine-associated receptors (TAARs) form a distinct family of olfactory receptors, and here we find that mechanisms regulating Taar gene choice display many unique features. The epigenetic signature of Taar genes in TAAR OSNs is different from that in OR OSNs. We further identify that two TAAR enhancers conserved across placental mammals are absolutely required for expression of the entire Taar gene repertoire. Deletion of either enhancer dramatically decreases the expression probabilities of different Taar genes, while deletion of both enhancers completely eliminates the TAAR OSN populations. In addition, both of the enhancers are sufficient to drive transgene expression in the partially overlapped TAAR OSNs. We also show that the TAAR enhancers operate in cis to regulate Taar gene expression. Our findings reveal a coordinated control of Taar gene choice in OSNs by two remote enhancers, and provide an excellent model to study molecular mechanisms underlying formation of an olfactory subsystem.

Date: 2021
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DOI: 10.1038/s41467-021-23823-4

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