The structural basis for intermitochondrial communications is fundamentally different in cardiac and skeletal muscle

Abstract

This review focuses on recent discoveries in skeletal and cardiac muscles indicating that mitochondria behave as an interactive cohort with inter-organelle communication and specific reactions to stress signals. Our new finding is that intermitochondrial communications in cardiac and skeletal muscles rely on two distinct methods. In cardiac muscle, mitochondria are discrete entities and are fairly well immobilized in a structural context. The organelles have developed a unique method of communication, via nanotunnels, which allow temporary connection from one mitochondrion to another over distances of up to several micrometres, without overall movement of the individual organelles and loss of their identity. Skeletal muscle mitochondria, in contrast, are dynamic. Through fusion, fission and elongation, they form connections that include constrictions and connecting ducts (distinct from nanotunnels) and lose individual identity in the formation of extensive networks. Connecting elements in skeletal muscle are distinct from nanotunnels in cardiac muscle.

Organelle Membrane Extensions in Mammalian Cells

“…Other organelles in plant cells, e.g., the vacuoles or nuclei, have also been reported to extend tubules but are not well studied [10,11]. There is now evidence that similar dynamic structures exist in mammalian cells, which have been reported for peroxisomes [12] (peroxisomal membrane protrusions; reviewed in [13]) and mitochondria [14,15] (e.g., mitochondrial dynamic tubulation, mitochondrial nanotunnels, nanotubes; reviewed in [16]) (Figure 1). The formation of transient and dynamic tubules, therefore, appears to be a common subcellular phenomenon.…”

“…These nanotunnels are narrow double-membraned structures (90-210 nm in diameter, up to 30 µm in length), which can contain matrix and cristae in their lumen (Figure 1). It has been suggested that the nanotunnels in cardiomyocytes differ from intermitochondrial connections in skeletal muscle [15]. Exchange events are proposed to involve kissing junctions, where membrane extensions are in close contact with the membrane of another mitochondrion, which could eventually allow the movements of proteins through a transient pore, or fusion events, which allow mixing of matrices.…”

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

“…Mitochondrial nanotunnels are more common in cardiac muscle than in skeletal muscle ( 13 ) and are not observed in mitochondria from other organs ( 13 , 19 ). Thus, without changing mitochondrial position, nanotunnels likely contribute to slower, albeit efficient, content exchange between mitochondria in the heart ( 34 , 35 , 41 ) and would be advantageous in striated tissue where the mitochondria are constrained within the muscle fibers. In particular, cardiac nanotunnels have been observed in pools of mitochondria residing close to capillaries (also called paravascular mitochondria ( 1 )), connecting to form an intermitochondrial junction with one or more adjacent mitochondria ( 19 ).…”

Excitation-contraction coupling in mammalian skeletal muscle: Blending old and last-decade research

“…Although previously considered isolated organelles, mitochondria can communicate among them in different cell types (Huang et al, 2013;Lavorato et al, 2017;Vincent et al, 2017;Lavorato et al, 2020). In skeletal muscle by means of fusion-fission, remodeling events or "kissing junctions", they form elongated structures with narrow connecting ducts, and less frequently nanotunnels, acting as an independent and highly dynamic network which connects the matrixes of non-adjacent Frontiers in Physiology frontiersin.org 13 mitochondria (Vincent et al, 2016;Vincent et al, 2017;Vincent et al, 2019;Lavorato et al, 2020;Rahman and Quadrilatero, 2021). There has also been described synapses-like structures between adjacent mitochondria (Picard, 2015) that would help integrate information about the network (Picard et al, 2015).…”