Progression of herpesvirus infection remodels mitochondrial organization and metabolism

Leclerc, Simon; Gupta, Alka; Ruokolainen, Visa; Chen, Jian-Hua; Kunnas, Kari; Ekman, Axel A.; Niskanen, Henri; Belevich, Ilya; Vihinen, Helena; Turkki, Paula; Perez-Berna, Ana J.; Kapishnikov, Sergey; Mäntylä, Elina; Harkiolaki, Maria; Dufour, Eric; Hytönen, Vesa; Pereiro, Eva; McEnroe, Tony; Fahy, Kenneth; Kaikkonen, Minna U.; Jokitalo, Eija; Larabell, Carolyn A.; Weinhardt, Venera; Mattola, Salla; Aho, Vesa; Vihinen-Ranta, Maija

doi:10.1371/journal.ppat.1011829

Title: Progression of herpesvirus infection remodels mitochondrial organization and metabolism

Journal Article · 15 April 2024 · PLoS Pathogens

DOI: https://doi.org/10.1371/journal.ppat.1011829 · OSTI ID:2396667

Leclerc, Simon ^[1]; Gupta, Alka ^[1]; Ruokolainen, Visa ^[1]; Chen, Jian-Hua ^[2]; Kunnas, Kari ^[1]; Ekman, Axel A. ^[3]; Niskanen, Henri ^[4]; Belevich, Ilya ^[5]; Vihinen, Helena ^[5]; Turkki, Paula ^[6]; Perez-Berna, Ana J. ^[7]; Kapishnikov, Sergey ^[8]; Mäntylä, Elina ^[6]; Harkiolaki, Maria ^[9]; Dufour, Eric ^[6]; Hytönen, Vesa ^[6]; Pereiro, Eva ^[10]; McEnroe, Tony ^[8]; Fahy, Kenneth ^[8]; Kaikkonen, Minna U. ^[4] more »

Univ. of Jyvaskyla (Finland)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Univ. of Jyvaskyla (Finland); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Univ. of Eastern Finland, Kuopio (Finland)
Univ. of Helsinki (Finland)
Tampere Univ. (Finland)
ALBA Synchrotron Light Source, Cerdanyola del Valles (Spain)
SiriusXT Limited, Dublin (Ireland)
Harwell Science and Innovation Campus, Didcot (United Kingdom); The Henry Wellcome Building for Genomic Medicine, Oxford (United Kingdom)
ALBA Synchrotron Light Source, Cerdanyola del Valles (Spain)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of California, San Francisco, CA (United States)
Univ. of Heidelberg (Germany)

Viruses target mitochondria to promote their replication, and infection-induced stress during the progression of infection leads to the regulation of antiviral defenses and mitochondrial metabolism which are opposed by counteracting viral factors. The precise structural and functional changes that underlie how mitochondria react to the infection remain largely unclear. Here we show extensive transcriptional remodeling of protein-encoding host genes involved in the respiratory chain, apoptosis, and structural organization of mitochondria as herpes simplex virus type 1 lytic infection proceeds from early to late stages of infection. High-resolution microscopy and interaction analyses unveiled infection-induced emergence of rough, thin, and elongated mitochondria relocalized to the perinuclear area, a significant increase in the number and clustering of endoplasmic reticulum-mitochondria contact sites, and thickening and shortening of mitochondrial cristae. Finally, metabolic analyses demonstrated that reactivation of ATP production is accompanied by increased mitochondrial Ca²⁺ content and proton leakage as the infection proceeds. Overall, the significant structural and functional changes in the mitochondria triggered by the viral invasion are tightly connected to the progression of the virus infection.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2396667

Journal Information:: PLoS Pathogens, Journal Name: PLoS Pathogens Journal Issue: 4 Vol. 20; ISSN 1553-7374

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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