Serine phosphorylation facilitates protein degradation by the human mitochondrial ClpXP protease

Y Yue Feng M Monica M. Goncalves Y Yulia Jitkova A Alexander F. A. Keszei (Princess Margaret Cancer Center) Y Yongran Yan (Princess Margaret Cancer Centre, University Health Network) C Chaitra Sarathy (Princess Margaret Cancer Centre, University Health Network) J Jonathan St-Germain (Princess Margaret Cancer Centre, University Health Network) T Tristan M. G. Kenney (Princess Margaret Cancer Centre, University Health Network) M Matthew Tcheng V Vincent Trudel (Department of Chemistry, University of Toronto) R Ross S. Mancini (Krembil Brain Institute, University Health Network) R Rahul Upadhyay (Krembil Brain Institute, University Health Network) R Rose Hurren (Princess Margaret Cancer Centre, University Health Network) M Marcela Gronda (Princess Margaret Cancer Centre, University Health Network) M Matthew Schultz (Princess Margaret Cancer Centre, University Health Network) K Kaylen Soriano (Princess Margaret Cancer Centre, University Health Network) K Kaitlin Lees (Princess Margaret Cancer Centre, University Health Network) N Neil C. Pomroy (Princess Margaret Cancer Centre, University Health Network) S S. Quinn W. Currie G Gilbert G. Privé (Princess Margaret Cancer Centre, University Health Network) M Mark A. Reed (Department of Chemistry, University of Toronto) A Andrei K. Yudin (Davenport Research Laboratories, University of Toronto, 80 St. George Street, Toronto, Ontario M5S 3H6, Canada) L Linda Z. Penn (Princess Margaret Cancer Centre, University Health Network) C Cheryl H. Arrowsmith B Brian Raught M Mohammad T. Mazhab-Jafari (Princess Margaret Cancer Center) S Siavash Vahidi A Aaron D. Schimmer

Abstract

ClpXP is a two-component mitochondrial matrix protease. The caseinolytic mitochondrial matrix peptidase chaperone subunit X (ClpX) recognizes and translocates protein substrates into the degradation chamber of the caseinolytic protease P (ClpP) for proteolysis. ClpXP degrades damaged respiratory chain proteins and is necessary for cancer cell survival. Despite the critical role of ClpXP in mitochondrial protein quality control, the specific degrons, or modifications that tag substrate proteins for degradation by human ClpXP, are still unknown. We demonstrated that phosphorylated serine (pSer) targets substrates to ClpX and facilitates their degradation by ClpXP in biochemical assays. In contrast, ClpP hyperactivated by the small-molecule drug ONC201 lost the preference for phosphorylated substrates. Hydrogen deuterium exchange mass spectrometry combined with biochemical assays showed that pSer binds the RKL loop of ClpX. ClpX variants with substitutions in the RKL loop failed to recognize phosphorylated substrates. In intact cells, ClpXP also preferentially degraded substrates with pSer. Moreover, ClpX substrates with the pSer were selectively found in aggregated mitochondrial proteins. Our work uncovers a mechanism for substrate recognition by ClpXP, with implications for targeting acute myeloid leukemia and other disorders involving ClpXP dysfunction.

Article Details

Volume / Issue Vol. 122, Issue 5
Published February 04, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (28)

Y

Yue Feng

M

Monica M. Goncalves

Y

Yulia Jitkova

A

Alexander F. A. Keszei

Princess Margaret Cancer Center

Y

Yongran Yan

Princess Margaret Cancer Centre, University Health Network

C

Chaitra Sarathy

Princess Margaret Cancer Centre, University Health Network

J

Jonathan St-Germain

Princess Margaret Cancer Centre, University Health Network

T

Tristan M. G. Kenney

Princess Margaret Cancer Centre, University Health Network

M

Matthew Tcheng

V

Vincent Trudel

Department of Chemistry, University of Toronto

R

Ross S. Mancini

Krembil Brain Institute, University Health Network

R

Rahul Upadhyay

Krembil Brain Institute, University Health Network

R

Rose Hurren

Princess Margaret Cancer Centre, University Health Network

M

Marcela Gronda

Princess Margaret Cancer Centre, University Health Network

M

Matthew Schultz

Princess Margaret Cancer Centre, University Health Network

K

Kaylen Soriano

Princess Margaret Cancer Centre, University Health Network

K

Kaitlin Lees

Princess Margaret Cancer Centre, University Health Network

N

Neil C. Pomroy

Princess Margaret Cancer Centre, University Health Network

S

S. Quinn W. Currie

G

Gilbert G. Privé

Princess Margaret Cancer Centre, University Health Network

M

Mark A. Reed

Department of Chemistry, University of Toronto

A

Andrei K. Yudin

Davenport Research Laboratories, University of Toronto, 80 St. George Street, Toronto, Ontario M5S 3H6, Canada

L

Linda Z. Penn

Princess Margaret Cancer Centre, University Health Network

C

Cheryl H. Arrowsmith

B

Brian Raught

M

Mohammad T. Mazhab-Jafari

Princess Margaret Cancer Center

S

Siavash Vahidi

A

Aaron D. Schimmer