Mitochondrial regular arrangement in muscle cells: a “crystal-like” pattern

Abstract

The aim of this work was to characterize quantitatively the arrangement of mitochondria in heart and skeletal muscles. We studied confocal images of mitochondria in nonfixed cardiomyocytes and fibers from soleus and white gastrocnemius muscles of adult rats. The arrangement of intermyofibrillar mitochondria was analyzed by estimating the densities of distribution of mitochondrial centers relative to each other (probability density function). In cardiomyocytes (1,820 mitochondrial centers marked), neighboring mitochondria are aligned along a rectangle, with distance between the centers equal to 1.97 Ϯ 0.43 and 1.43 Ϯ 0.43 m in the longitudinal and transverse directions, respectively. In soleus (1,659 mitochondrial centers marked) and white gastrocnemius (621 pairs of mitochondria marked), mitochondria are mainly organized in pairs at the I-band level. Because of this organization, there are two distances characterizing mitochondrial distribution in the longitudinal direction in these muscles. The distance between mitochondrial centers in the longitudinal direction within the same I band is 0.91 Ϯ 0.11 and 0.61 Ϯ 0.07 m in soleus and white gastrocnemius, respectively. The distance between mitochondrial centers in different I bands is ϳ3.7 and ϳ3.3 m in soleus and gastrocnemius, respectively. In the transverse direction, the mitochondria are packed considerably closer to each other in soleus than in white gastrocnemius, with the distance equal to 0.75 Ϯ 0.22 m in soleus and 1.09 Ϯ 0.41 m in gastrocnemius. Our results show that intermyofibrillar mitochondria are arranged in a highly ordered crystal-like pattern in a muscle-specific manner with relatively small deviation in the distances between neighboring mitochondria. This is consistent with the concept of the unitary nature of the organization of the muscle energy metabolism. confocal microscopy; quantitative analysis; cardiac and skeletal muscles; probability density function; unitary structure of cells RECENT STUDIES HAVE SHOWN the existence of multiple specific functional interactions among mitochondria, sarcoplasmic reticulum (SR), and myofibrils in permeabilized muscle fibers (5,14,30,34). Namely, endogenous ATP has been shown to be more efficient than exogenous ATP in maintaining calcium uptake into SR (14). In addition, kinetic studies have shown a direct supply of endogenous ADP from ATPases to mitochondria (30, 34). Such interaction can be explained by the existence of localized intracellular diffusion restrictions (28, 39). A mild treatment of the fibers with trypsin leads to the removal of these diffusion restrictions, and at the same time, distribution of mitochondria in the fiber is changed from regular arrangement in the control to random distribution after the treatment (28). Similarly, in ischemic hearts, various alterations in mitochondrial function such as the significant decrease in maximal respiration rate and half-saturation constant for ADP were observed in parallel with the changes in structural organization of the cardiac muscle cells (7,1...

Physiological diversity of mitochondrial oxidative phosphorylation

“…For instance, the classic measurement of mitochondrial section area on electron micrographs is limited by the very complex three-dimensional organization of mitochondria as a global network (16,31,51), the morphometric parameters of which also vary widely on energy status (17-19, 23, 35). Accordingly, in our study, there was an important variability of mitochondrial morphology between tissues: in heart and skeletal muscle, they presented essentially with a regular quasi-crystalline organization (46), whereas in liver and kidney they looked more irregular and less compacted by tissue architecture. In brain, the mitochondria looked more like a collection of small and numerous ovoid sections.…”

Imaging superoxide flash and metabolism-coupled mitochondrial permeability transition in living animals

“…Fluorescent cardiac mitochondria were observed between the Z-lines of sarcomeres and arranged as longitudinal bundles along the myofibrils ( Figure 1B) [17,18]. In skeletal muscle, mt-cpYFP staining of I band-delimited mitochondria [18,19] gave rise to transverse doublet bands at 2.6 µm intervals ( Figure 1C) that overlapped with staining by tetramethylrhodamine methyl ester (TMRM), a mitochondrial membrane potential (∆Ψm) indicator (Supplementary information, Figure S3). Unlike striated muscles, axons within the sciatic nerve trunk were filled with slender mitochondria (Figure 1D), many of which were engaged in anterograde or retrograde trafficking.…”

Quality Control of Mitochondrial Proteostasis

“…For example, in cultured fibroblasts mitochondria form extensive reticular networks, whereas in neuronal cells, mitochondria can be found enriched at areas of high-energy demand, including presynaptic termini, axon initial segments, and growth cones. Furthermore, in muscle cells, mitochondria adopt a very uniform intermyofibrillar conformation (Vendelin et al 2005). The dynamic nature of mitochondria provides an explanation as to how they adopt varying organizations in different cell populations.…”