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Strategies for maximizing ATP supply in the microsporidian Encephalitozoon cuniculi : direct binding of mitochondria to the parasitophorous vacuole and clustering of the mitochondrial porin VDAC

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Date
04/2014
Author
Hacker, Christian
Howell, Matthew
Bhella, David
Lucocq, John Milton
Funder
The Wellcome Trust
Grant ID
089803/B/09/Z
Keywords
Adenosine Triphosphate
Animals
Cell Line
Encephalitozoon cuniculi
Energy Metabolism
Imaging, Three-Dimensional
Microscopy, Electron
Mitochondria
Rabbits
Vacuoles
Voltage-Dependent Anion Channels
QR355 Virology
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Abstract
Microsporidia are obligate intracellular parasites with extremely reduced genomes and a dependence on host-derived ATP. The microsporidium Encephalitozoon cuniculi proliferates within a membranous vacuole and we investigated how the ATP supply is optimized at the vacuole–host interface. Using spatial EM quantification (stereology), we found a single layer of mitochondria coating substantial proportions of the parasitophorous vacuole. Mitochondrial binding occurred preferentially over the vegetative ‘meront’ stages of the parasite, which bulged into the cytoplasm, thereby increasing the membrane surface available for mitochondrial interaction. In a broken cell system mitochondrial binding was maintained and was typified by electron dense structures (< 10 nm long) bridging between outer mitochondrial and vacuole membranes. In broken cells mitochondrial binding was sensitive to a range of protease treatments. The function of directly bound mitochondria, as measured by the membrane potential sensitive dye JC-1, was indistinguishable from other mitochondria in the cell although there was a generalized depression of the membrane potential in infected cells. Finally, quantitative immuno-EM revealed that the ATP-delivering mitochondrial porin, VDAC, was concentrated atthe mitochondria-vacuole interaction site. Thus E. cuniculi appears to maximize ATP supply by direct binding of mitochondria to the parasitophorous vacuole bringing this organelle within 0.020 microns of the growing vegetative form of the parasite. ATP-delivery is further enhanced by clustering of ATP transporting porins in those regions of the outer mitochondrial membrane lying closest to the parasite.
Citation
Hacker , C , Howell , M , Bhella , D & Lucocq , J M 2014 , ' Strategies for maximizing ATP supply in the microsporidian Encephalitozoon cuniculi : direct binding of mitochondria to the parasitophorous vacuole and clustering of the mitochondrial porin VDAC ' , Cellular Microbiology , vol. 16 , no. 4 , pp. 565-579 . https://doi.org/10.1111/cmi.12240
Publication
Cellular Microbiology
Status
Peer reviewed
DOI
https://doi.org/10.1111/cmi.12240
ISSN
1462-5814
Type
Journal article
Rights
© 2013 The Authors. Cellular Microbiology published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
Description
The authors were supported by a programme grant from the Wellcome Trust (WT089803MA)
Collections
  • University of St Andrews Research
URI
http://hdl.handle.net/10023/4281

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