Literature DB >> 36171294

An LKB1-mitochondria axis controls TH17 effector function.

Klara Piletic1, Daniel J Puleston1, Matteo Villa1, Francesc Baixauli1, Cameron S Field1, Lea J Flachsmann1, Andrea Quintana1, Nisha Rana1, Joy Edwards-Hicks1, Mai Matsushita1, Michal A Stanczak1, Katarzyna M Grzes1, Agnieszka M Kabat1, Mario Fabri1,2, George Caputa1, Beth Kelly1, Mauro Corrado1, Yaarub Musa1, Katarzyna J Duda1, Gerhard Mittler1, David O'Sullivan1, Hiromi Sesaki3, Thomas Jenuwein1, Joerg M Buescher1, Edward J Pearce1,4,5, David E Sanin1,4, Erika L Pearce6,7,8.   

Abstract

CD4+ T cell differentiation requires metabolic reprogramming to fulfil the bioenergetic demands of proliferation and effector function, and enforce specific transcriptional programmes1-3. Mitochondrial membrane dynamics sustains mitochondrial processes4, including respiration and tricarboxylic acid (TCA) cycle metabolism5, but whether mitochondrial membrane remodelling orchestrates CD4+ T cell differentiation remains unclear. Here we show that unlike other CD4+ T cell subsets, T helper 17 (TH17) cells have fused mitochondria with tight cristae. T cell-specific deletion of optic atrophy 1 (OPA1), which regulates inner mitochondrial membrane fusion and cristae morphology6, revealed that TH17 cells require OPA1 for its control of the TCA cycle, rather than respiration. OPA1 deletion amplifies glutamine oxidation, leading to impaired NADH/NAD+ balance and accumulation of TCA cycle metabolites and 2-hydroxyglutarate-a metabolite that influences the epigenetic landscape5,7. Our multi-omics approach revealed that the serine/threonine kinase liver-associated kinase B1 (LKB1) couples mitochondrial function to cytokine expression in TH17 cells by regulating TCA cycle metabolism and transcriptional remodelling. Mitochondrial membrane disruption activates LKB1, which restrains IL-17 expression. LKB1 deletion restores IL-17 expression in TH17 cells with disrupted mitochondrial membranes, rectifying aberrant TCA cycle glutamine flux, balancing NADH/NAD+ and preventing 2-hydroxyglutarate production from the promiscuous activity of the serine biosynthesis enzyme phosphoglycerate dehydrogenase (PHGDH). These findings identify OPA1 as a major determinant of TH17 cell function, and uncover LKB1 as a sensor linking mitochondrial cues to effector programmes in TH17 cells.
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.

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Year:  2022        PMID: 36171294     DOI: 10.1038/s41586-022-05264-1

Source DB:  PubMed          Journal:  Nature        ISSN: 0028-0836            Impact factor:   69.504


  65 in total

Review 1.  Mitochondria and Epigenetics - Crosstalk in Homeostasis and Stress.

Authors:  Olli Matilainen; Pedro M Quirós; Johan Auwerx
Journal:  Trends Cell Biol       Date:  2017-03-06       Impact factor: 20.808

Review 2.  Mitochondrial fission, fusion, and stress.

Authors:  Richard J Youle; Alexander M van der Bliek
Journal:  Science       Date:  2012-08-31       Impact factor: 47.728

3.  Metabolic control of TH17 and induced Treg cell balance by an epigenetic mechanism.

Authors:  Tao Xu; Kelly M Stewart; Xiaohu Wang; Kai Liu; Min Xie; Jae Kyu Ryu; Ke Li; Tianhua Ma; Haixia Wang; Lu Ni; Saiyong Zhu; Nan Cao; Dongwei Zhu; Yu Zhang; Katerina Akassoglou; Chen Dong; Edward M Driggers; Sheng Ding
Journal:  Nature       Date:  2017-08-02       Impact factor: 49.962

Review 4.  Mitochondrial Dynamics and Its Involvement in Disease.

Authors:  David C Chan
Journal:  Annu Rev Pathol       Date:  2019-10-04       Impact factor: 23.472

5.  Distinct modes of mitochondrial metabolism uncouple T cell differentiation and function.

Authors:  Will Bailis; Justin A Shyer; Jun Zhao; Juan Carlos Garcia Canaveras; Fatimah J Al Khazal; Rihao Qu; Holly R Steach; Piotr Bielecki; Omair Khan; Ruaidhri Jackson; Yuval Kluger; Louis J Maher; Joshua Rabinowitz; Joe Craft; Richard A Flavell
Journal:  Nature       Date:  2019-06-19       Impact factor: 49.962

Review 6.  The cell biology of mitochondrial membrane dynamics.

Authors:  Marta Giacomello; Aswin Pyakurel; Christina Glytsou; Luca Scorrano
Journal:  Nat Rev Mol Cell Biol       Date:  2020-02-18       Impact factor: 94.444

7.  Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency.

Authors:  Sara Cogliati; Christian Frezza; Maria Eugenia Soriano; Tatiana Varanita; Ruben Quintana-Cabrera; Mauro Corrado; Sara Cipolat; Veronica Costa; Alberto Casarin; Ligia C Gomes; Ester Perales-Clemente; Leonardo Salviati; Patricio Fernandez-Silva; Jose A Enriquez; Luca Scorrano
Journal:  Cell       Date:  2013-09-19       Impact factor: 41.582

Review 8.  T cell metabolism drives immunity.

Authors:  Michael D Buck; David O'Sullivan; Erika L Pearce
Journal:  J Exp Med       Date:  2015-08-10       Impact factor: 14.307

Review 9.  Metabolism, Activity, and Targeting of D- and L-2-Hydroxyglutarates.

Authors:  Dan Ye; Kun-Liang Guan; Yue Xiong
Journal:  Trends Cancer       Date:  2018-01-05

Review 10.  Mitochondrial TCA cycle metabolites control physiology and disease.

Authors:  Inmaculada Martínez-Reyes; Navdeep S Chandel
Journal:  Nat Commun       Date:  2020-01-03       Impact factor: 14.919

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