eATP sensing by the purinergic receptor PA2072 for allosteric modulation in intracellular c-di-GMP signaling

Y Yan Zhang X Xiaojing Gao (Department of Biochemistry and Molecular Biology, School of Basic Medicine, Ningxia Medical University) Y Yunjie Xiao (Tianjin Key Laboratory of Function and Application of Biological Macromolecular Structures, School of Life Sciences, Tianjin University) Y Yajing Duan (Tianjin Key Laboratory of Function and Application of Biological Macromolecular Structures, School of Life Sciences, Tianjin University) W Wangxin Xiao (Tianjin Key Laboratory of Function and Application of Biological Macromolecular Structures, School of Life Sciences, Tianjin University) Y Yangyang Xu (Tianjin Key Laboratory of Function and Application of Biological Macromolecular Structures, School of Life Sciences, Tianjin University) T Tingting Yang (The MOE Basic Research and Innovation Center for the Targeted Therapeutics of Solid Tumors, School of Basic Medical Sciences, The Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi, China.) H Huimin Zhang C Cheng Chen S Shuo Shi X Xun-Cheng Su (State Key Laboratory of Elemento-Organic Chemistry, Frontiers Science Center for New Organic Matter, College of Chemistry) X Xinghua Jin (School of Pharmaceutical Science and Technology, Tianjin University) J Jiaqing Zhao (Research Center for Medical Science and Technology, Ningxia Medical University) H Haitao Yang G Guowei Yin (Scientific Research Center, The Seventh Affiliated Hospital, Sun Yat-sen University) W Wensu Yuan (Tianjin Key Laboratory of Function and Application of Biological Macromolecular Structures, School of Life Sciences, Tianjin University) Z Zefang Wang (Key Laboratory of Material Simulation Methods & Software of Ministry of Education, College of Physics) W Weidong Huang (Department of Biochemistry and Molecular Biology, School of Basic Medicine, Ningxia Medical University) Z Zhi Lin (Department of Chemistry and Chemical Biology)

Abstract

Extracellular ATP (eATP) has emerged as a crucial signaling molecule across eukaryotic and prokaryotic domains, modulating diverse cellular functions by activating purinergic receptors to initiate intracellular signaling cascades. However, the structural and molecular mechanisms underlying eATP sensing and signaling by prokaryotic receptors remain largely unknown. Here, we demonstrate that the receptor PA2072 in Pseudomonas aeruginosa is responsible for recognizing eATP to down-regulate intracellular cyclic di-GMP levels. The periplasmic CHASE4 domain of PA2072 specifically binds and hydrolyzes eATP, exhibiting ATPase activity both in the presence and absence of a divalent cation cofactor. Structural elucidation of the PA2072 CHASE4 domain in its monomeric and complex states unveils an exquisite molecular switch governed by the oligomeric state. ATP hydrolysis by the catalytically active monomeric form is coupled to homodimerization, concomitantly deactivating its ATPase activity and initiating intracellular phosphodiesterase activity. These findings open avenues for understanding interkingdom eATP signaling and developing targeted therapeutic interventions.

Article Details

Volume / Issue Vol. 122, Issue 45
Published November 11, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (19)

Y

Yan Zhang

X

Xiaojing Gao

Department of Biochemistry and Molecular Biology, School of Basic Medicine, Ningxia Medical University

Y

Yunjie Xiao

Tianjin Key Laboratory of Function and Application of Biological Macromolecular Structures, School of Life Sciences, Tianjin University

Y

Yajing Duan

Tianjin Key Laboratory of Function and Application of Biological Macromolecular Structures, School of Life Sciences, Tianjin University

W

Wangxin Xiao

Tianjin Key Laboratory of Function and Application of Biological Macromolecular Structures, School of Life Sciences, Tianjin University

Y

Yangyang Xu

Tianjin Key Laboratory of Function and Application of Biological Macromolecular Structures, School of Life Sciences, Tianjin University

T

Tingting Yang

The MOE Basic Research and Innovation Center for the Targeted Therapeutics of Solid Tumors, School of Basic Medical Sciences, The Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi, China.

H

Huimin Zhang

C

Cheng Chen

S

Shuo Shi

X

Xun-Cheng Su

State Key Laboratory of Elemento-Organic Chemistry, Frontiers Science Center for New Organic Matter, College of Chemistry

X

Xinghua Jin

School of Pharmaceutical Science and Technology, Tianjin University

J

Jiaqing Zhao

Research Center for Medical Science and Technology, Ningxia Medical University

H

Haitao Yang

G

Guowei Yin

Scientific Research Center, The Seventh Affiliated Hospital, Sun Yat-sen University

W

Wensu Yuan

Tianjin Key Laboratory of Function and Application of Biological Macromolecular Structures, School of Life Sciences, Tianjin University

Z

Zefang Wang

Key Laboratory of Material Simulation Methods & Software of Ministry of Education, College of Physics

W

Weidong Huang

Department of Biochemistry and Molecular Biology, School of Basic Medicine, Ningxia Medical University

Z

Zhi Lin

Department of Chemistry and Chemical Biology