The locations of mitochondria in mammalian photoreceptors: relation to retinal vasculature.
Adult mammalian photoreceptors are elongated cells, and their mitochondria are sequestered to the ends of the cell, to the inner segments and (in some species) to axon terminals in the outer plexiform layer (OPL). We hypothesised that mitochondria migrate to these locations towards sources of oxygen, from the choroid and (in some species) from the deep capillaries of the retinal circulation. Six mammalian species were surveyed, using electron and light microscopy, including immunohistochemistry for the mitochondrial enzyme cytochrome oxidase (CO). In all 6 species, mitochondria were absent from photoreceptor somas and were numerous in inner segments. Mitochondria were prominent in axon terminals in 3 species (mouse, rat, human) with a retinal circulation and were absent from those terminals in 3 species (wallaby, rat, guinea pig) with avascular retinas. Further, in a human developmental series, it was evident that mitochondria migrate within rods and cones, towards and eventually past the outer limiting membrane (OLM), into the inner segment. In Müller and RPE cells also, mitochondria concentrated at the external surface of the cells. Neurones located in the inner layers of avascular retinas have mitochondria, but their expression of CO is low. Mitochondrial locations in photoreceptors, Müller and RPE cells are economically explained as the result of migration within the cell towards sources of oxygen. In photoreceptors, this migration results in a separation of mitochondria from the nuclear genome; this separation may be a factor in the vulnerability of photoreceptors to mutations, toxins and environmental stresses, which other retinal neurones survive.
ARC Centre of Excellence in Visual Science and Research School of Biological Sciences, The Australian National University, Canberra ACT 2601, Australia. stone@rsbs.anu.edu.au
Jonathan
J
Stone
Diana
D
van Driel
Krisztina
K
Valter
Sandra
S
Rees
Jan
J
Provis
D000328:Adult; D000818:Animals; D002451:Cell Compartmentation / Q000235:genetics; D016764:Cell Polarity / Q000235:genetics; D002633:Chemotaxis / Q000502:physiology; D003576:Electron Transport Complex IV / Q000378:metabolism; D005333:Fetus; D006168:Guinea Pigs; D006801:Humans; D007614:Macropodidae; D051379:Mice; D008810:Mice, Inbred C57BL; D046529:Microscopy, Electron, Transmission; D008928:Mitochondria / Q000378:metabolism / Q000648:ultrastructure*; D009457:Neuroglia / Q000378:metabolism / Q000648:ultrastructure; D010101:Oxygen Consumption / Q000502:physiology; D020419:Photoreceptor Cells, Vertebrate / Q000378:metabolism / Q000648:ultrastructure*; D010857:Pigment Epithelium of Eye / Q000378:metabolism / Q000648:ultrastructure; D017729:Presynaptic Terminals / Q000378:metabolism / Q000648:ultrastructure; D011817:Rabbits; D051381:Rats; D017207:Rats, Sprague-Dawley; D012161:Retinal Artery / Q000648:ultrastructure; D013045:Species Specificity
D003576:Electron Transport Complex IV