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Structure paper

TitleCoupling enzymatic activity and gating in an ancient TRPM chanzyme and its molecular evolution.
Journal, issue, pagesNat Struct Mol Biol, Year 2024
Publish dateMay 21, 2024
AuthorsYihe Huang / Sushant Kumar / Junuk Lee / Wei Lü / Juan Du /
PubMed AbstractChannel enzymes represent a class of ion channels with enzymatic activity directly or indirectly linked to their channel function. We investigated a TRPM2 chanzyme from choanoflagellates that ...Channel enzymes represent a class of ion channels with enzymatic activity directly or indirectly linked to their channel function. We investigated a TRPM2 chanzyme from choanoflagellates that integrates two seemingly incompatible functions into a single peptide: a channel module activated by ADP-ribose with high open probability and an enzyme module (NUDT9-H domain) consuming ADP-ribose at a remarkably slow rate. Using time-resolved cryogenic-electron microscopy, we captured a complete series of structural snapshots of gating and catalytic cycles, revealing the coupling mechanism between channel gating and enzymatic activity. The slow kinetics of the NUDT9-H enzyme module confers a self-regulatory mechanism: ADPR binding triggers NUDT9-H tetramerization, promoting channel opening, while subsequent hydrolysis reduces local ADPR, inducing channel closure. We further demonstrated how the NUDT9-H domain has evolved from a structurally semi-independent ADP-ribose hydrolase module in early species to a fully integrated component of a gating ring essential for channel activation in advanced species.
External linksNat Struct Mol Biol / PubMed:38773335
MethodsEM (single particle)
Resolution1.97 - 4.08 Å
Structure data

40721

8sr7

EMDB-40721, PDB-8sr7:
Cryo-EM structure of TRPM2 chanzyme in the presence of Magnesium, Adenosine monophosphate, and Ribose-5-phosphate
Method: EM (single particle) / Resolution: 1.97 Å

40722

8sr8

EMDB-40722, PDB-8sr8:
Cryo-EM structure of TRPM2 chanzyme in the presence of EDTA (apo state)
Method: EM (single particle) / Resolution: 2.77 Å

40723

8sr9

EMDB-40723, PDB-8sr9:
Cryo-EM structure of TRPM2 chanzyme in the presence of Magnesium
Method: EM (single particle) / Resolution: 3.05 Å

40724

8sra

EMDB-40724, PDB-8sra:
Cryo-EM structure of TRPM2 chanzyme in the presence of Calcium
Method: EM (single particle) / Resolution: 2.93 Å

40725

8srb

EMDB-40725, PDB-8srb:
Cryo-EM structure of TRPM2 chanzyme in the presence of EDTA and ADP-ribose
Method: EM (single particle) / Resolution: 2.82 Å

40726

8src

EMDB-40726, PDB-8src:
Cryo-EM structure of TRPM2 chanzyme in the presence of Calcium and ADP-ribose
Method: EM (single particle) / Resolution: 2.92 Å

EMDB-40865: NUDT9-H domain focused cryo-EM map of TRPM2 chanzyme in the presence of Calcium and ADP-ribose
Method: EM (single particle) / Resolution: 3.69 Å

EMDB-40866: NUDT9-H domain focused cryo-EM map of TRPM2 chanzyme in the presence of Magnesium, Adenosine monophosphate, and Ribose-5-phosphate
Method: EM (single particle) / Resolution: 2.8 Å

EMDB-40867: NUDT9-H domain focused cryo-EM map of TRPM2 chanzyme in the presence of Magnesium, Adenosine monophosphate, and Ribose-5-phosphate
Method: EM (single particle) / Resolution: 3.83 Å

EMDB-40868: NUDT9-H domain focused cryo-EM map of TRPM2 chanzyme in the presence of Magnesium and ADP-ribose, open state
Method: EM (single particle) / Resolution: 3.13 Å

EMDB-40869: NUDT9-H domain focused cryo-EM map of TRPM2 chanzyme in the presence of Magnesium and ADP-ribose, closed state
Method: EM (single particle) / Resolution: 2.8 Å

EMDB-40870: NUDT9-H domain focused cryo-EM map of TRPM2 chanzyme in the presence of Magnesium, ADP-ribose, Adenosine monophosphate, and Ribose-5-phosphate, closed state
Method: EM (single particle) / Resolution: 2.8 Å

EMDB-40871: NUDT9-H domain focused cryo-EM map of TRPM2 chanzyme (E1114A) in the presence of Magnesium and ADP-ribose, open state
Method: EM (single particle) / Resolution: 4.08 Å

EMDB-40872: NUDT9-H domain focused cryo-EM map of TRPM2 chanzyme (E1114A) in the presence of Magnesium and ADP-ribose, closed state
Method: EM (single particle) / Resolution: 3.27 Å

EMDB-40875: Raw consensus map of TRPM2 chanzyme in the presence of Magnesium, Adenosine monophosphate, and Ribose-5-phosphate
Method: EM (single particle) / Resolution: 1.97 Å

EMDB-40876: Raw consensus map of TRPM2 chanzyme in the presence of Magnesium
Method: EM (single particle) / Resolution: 3.16 Å

EMDB-40877: Raw consensus map of TRPM2 chanzyme in the presence of Calcium
Method: EM (single particle) / Resolution: 3.03 Å

EMDB-40878: Raw consensus map of TRPM2 chanzyme in the presence of EDTA and ADP-ribose
Method: EM (single particle) / Resolution: 3.3 Å

EMDB-40879: Raw consensus map of TRPM2 chanzyme in the presence of Magnesium and ADP-ribose, open state
Method: EM (single particle) / Resolution: 2.93 Å

EMDB-40880: Raw consensus map of TRPM2 chanzyme in the presence of Magnesium and ADP-ribose, closed state
Method: EM (single particle) / Resolution: 3.87 Å

EMDB-40881: Raw consensus map of TRPM2 chanzyme in the presence of Magnesium, ADP-ribose, Adenosine monophosphate, and Ribose-5-phosphate, closed state
Method: EM (single particle) / Resolution: 3.71 Å

EMDB-40883: Raw consensus map of TRPM2 chanzyme in the presence of Magnesium, Adenosine monophosphate, and Ribose-5-phosphate
Method: EM (single particle) / Resolution: 2.8 Å

EMDB-40887: Raw consensus map of TRPM2 chanzyme (E1114A) in the presence of Magnesium and ADP-ribose, open state
Method: EM (single particle) / Resolution: 3.87 Å

EMDB-40888: Raw consensus map of TRPM2 chanzyme (E1114A) in the presence of Magnesium and ADP-ribose, closed state
Method: EM (single particle) / Resolution: 2.82 Å

EMDB-40893: Raw consensus map of TRPM2 chanzyme in the presence of Calcium and ADP-ribose.
Method: EM (single particle) / Resolution: 2.99 Å

EMDB-40895: Raw consensus map of TRPM2 chanzyme in the presence of EDTA (apo state)
Method: EM (single particle) / Resolution: 3.02 Å

Chemicals

ChemComp-RP5:
5-O-phosphono-beta-D-ribofuranose

ChemComp-AMP:
ADENOSINE MONOPHOSPHATE / AMP*YM / Adenosine monophosphate

ChemComp-MG:
Unknown entry

ChemComp-CLR:
CHOLESTEROL / Cholesterol

ChemComp-HOH:
WATER / Water

ChemComp-CA:
Unknown entry

ChemComp-APR:
ADENOSINE-5-DIPHOSPHORIBOSE

Source
  • salpingoeca rosetta (eukaryote)
KeywordsTRANSPORT PROTEIN / TRPM2 Chanzyme / Channel-enzyme

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