Intracellular to Interorgan Mitochondrial Communication in Striated Muscle in Health and Disease

Neoma T Boardman; Giulia Trani; Marco Scalabrin; Vanina Romanello; Rob C I Wüst

doi:10.1210/endrev/bnad004

Intracellular to Interorgan Mitochondrial Communication in Striated Muscle in Health and Disease

Endocr Rev. 2023 Jul 11;44(4):668-692. doi: 10.1210/endrev/bnad004.

Authors

Neoma T Boardman¹, Giulia Trani^{2

3}, Marco Scalabrin^{2

3}, Vanina Romanello^{2

3}, Rob C I Wüst⁴

Affiliations

¹ Cardiovascular Research Group, Department of Medical Biology, Faculty of Health Sciences, UiT-The Arctic University of Norway, 9019 Tromsø, Norway.
² Veneto Institute of Molecular Medicine, 35129 Padova, Italy.
³ Department of Biomedical Sciences, University of Padova, 35100 Padova, Italy.
⁴ Department of Human Movement Sciences, Faculty of Behavioural and Movement Sciences, Amsterdam Movement Sciences, Vrije Universiteit Amsterdam, 1081 BT Amsterdam, The Netherlands.

Abstract

Mitochondria sense both biochemical and energetic input in addition to communicating signals regarding the energetic state of the cell. Increasingly, these signaling organelles are recognized as key for regulating different cell functions. This review summarizes recent advances in mitochondrial communication in striated muscle, with specific focus on the processes by which mitochondria communicate with each other, other organelles, and across distant organ systems. Intermitochondrial communication in striated muscle is mediated via conduction of the mitochondrial membrane potential to adjacent mitochondria, physical interactions, mitochondrial fusion or fission, and via nanotunnels, allowing for the exchange of proteins, mitochondrial DNA, nucleotides, and peptides. Within striated muscle cells, mitochondria-organelle communication can modulate overall cell function. The various mechanisms by which mitochondria communicate mitochondrial fitness to the rest of the body suggest that extracellular mitochondrial signaling is key during health and disease. Whereas mitochondria-derived vesicles might excrete mitochondria-derived endocrine compounds, stimulation of mitochondrial stress can lead to the release of fibroblast growth factor 21 (FGF21) and growth differentiation factor 15 (GDF15) into the circulation to modulate whole-body physiology. Circulating mitochondrial DNA are well-known alarmins that trigger the immune system and may help to explain low-grade inflammation in various chronic diseases. Impaired mitochondrial function and communication are central in common heart and skeletal muscle pathologies, including cardiomyopathies, insulin resistance, and sarcopenia. Lastly, important new advances in research in mitochondrial endocrinology, communication, medical horizons, and translational aspects are discussed.

Keywords: FGF21; GDF15; mitochondria-organelle interactions; mitochondrial cristae; mitochondrial dynamics; myokines; respiratory supercomplexes.

Publication types

Review

MeSH terms

Humans
Mitochondria* / metabolism
Muscle, Skeletal* / metabolism