p53 enhances DNA repair and suppresses cytoplasmic chromatin fragments and inflammation in senescent cells

K Karl N. Miller B Brightany Li H Hannah R. Pierce-Hoffman S Shreeya Patel X Xue Lei (Cancer Genome and Epigenetics Program, Sanford Burnham Prebys Medical Discovery Institute) A Adarsh Rajesh M Marcos G. Teneche A Aaron P. Havas A Armin Gandhi C Carolina Cano Macip J Jun Lyu S Stella G. Victorelli S Seung-Hwa Woo A Anthony B. Lagnado M Michael A. LaPorta T Tianhui Liu (School of Sciences, Great Bay University 1 , Dongguan 523000,) N Nirmalya Dasgupta S Sha Li (State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences) A Andrew Davis A Anatoly Korotkov E Erik Hultenius Z Zichen Gao Y Yoav Altman R Rebecca A. Porritt G Guillermina Garcia C Carolin Mogler A Andrei Seluanov V Vera Gorbunova S Susan M. Kaech X Xiao Tian Z Zhixun Dou C Chongyi Chen J João F. Passos P Peter D. Adams

Abstract

Abstract Genomic instability and inflammation are distinct hallmarks of aging, but the connection between them is poorly understood. Here we report a mechanism directly linking genomic instability and inflammation in senescent cells through a mitochondria-regulated molecular circuit involving p53 and cytoplasmic chromatin fragments (CCF) that are enriched for DNA damage signaling marker γH2A.X. We show that p53 suppresses CCF accumulation and its downstream inflammatory phenotype. p53 activation suppresses CCF formation linked to enhanced DNA repair and genome integrity. Activation of p53 in aged mice by pharmacological inhibition of MDM2 reverses transcriptomic signatures of aging and age-associated accumulation of monocytes and macrophages in liver. Mitochondrial ablation in senescent cells suppresses CCF formation and activates p53 in an ATM-dependent manner, suggesting that mitochondria-dependent formation of γH2A.X + CCF dampens nuclear DNA damage signaling and p53 activity. These data provide evidence for a mitochondria-regulated p53 signaling circuit in senescent cells that controls DNA repair, genome integrity, and senescence- and age-associated inflammation, with relevance to therapeutic targeting of age-associated disease.

Article Details

Volume / Issue Vol. 16, Issue 1
Published March 05, 2025
ISSN 2041-1723
Publisher Nature Portfolio

Journal Info

Nature Communications

Nature Portfolio

ISSN: 2041-1723 Open Access Life Sciences

Authors (34)

K

Karl N. Miller

B

Brightany Li

H

Hannah R. Pierce-Hoffman

S

Shreeya Patel

X

Xue Lei

Cancer Genome and Epigenetics Program, Sanford Burnham Prebys Medical Discovery Institute

A

Adarsh Rajesh

M

Marcos G. Teneche

A

Aaron P. Havas

A

Armin Gandhi

C

Carolina Cano Macip

J

Jun Lyu

S

Stella G. Victorelli

S

Seung-Hwa Woo

A

Anthony B. Lagnado

M

Michael A. LaPorta

T

Tianhui Liu

School of Sciences, Great Bay University 1 , Dongguan 523000,

N

Nirmalya Dasgupta

S

Sha Li

State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences

A

Andrew Davis

A

Anatoly Korotkov

E

Erik Hultenius

Z

Zichen Gao

Y

Yoav Altman

R

Rebecca A. Porritt

G

Guillermina Garcia

C

Carolin Mogler

A

Andrei Seluanov

V

Vera Gorbunova

S

Susan M. Kaech

X

Xiao Tian

Z

Zhixun Dou

C

Chongyi Chen

J

João F. Passos

P

Peter D. Adams