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

Volumn 16, Issue 4, 2014, Pages 565-579

  Hacker, Christian ^a   Howell, Matthew ^a   Bhella, David ^b   Lucocq, John ^a  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b MRC UNIVERSITY OF GLASGOW CENTRE FOR VIRUS RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; MITOCHONDRIAL PROTEIN; PORIN; VOLTAGE DEPENDENT ANION CHANNEL;

ARTICLE; CELL MEMBRANE; CELL ORGANELLE; CELL PROLIFERATION; CELL VACUOLE; CONTROLLED STUDY; COXIELLA BURNETII; CYTOPLASM; ELECTRON MICROSCOPY; ENCEPHALITOZOON; ENCEPHALITOZOON CUNICULI; ENDOPLASMIC RETICULUM; FUNGUS GROWTH; MICROSPORIDIA; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL VOLUME; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; STEREOLOGY; TRACHIPLEISTOPHORA HOMINIS;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL LINE; ENCEPHALITOZOON CUNICULI; ENERGY METABOLISM; IMAGING, THREE-DIMENSIONAL; MICROSCOPY, ELECTRON; MITOCHONDRIA; RABBITS; VACUOLES; VOLTAGE-DEPENDENT ANION CHANNELS;

EID: 84896390333     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12240     Document Type: Article

References (41)

1. Beckers, C.J., Keller, D.S., and Balch, W.E. (1987) Semi-intact cells permeable to macromolecules: use in reconstitution of protein transport from the endoplasmic reticulum to the Golgi complex. Cell 50: 523-534.
2. Canning, E.U., and Hollister, W.S. (1992) Human infections with microsporidia. Rev Med Microbiol 3: 35-42.
3. Colombini, M. (2012) VDAC structure, selectivity, and dynamics. Biochim Biophys Acta 1818: 1457-1465.
4. Cornman, R.S., Chen, Y.P., Schatz, M.C., Street, C., Zhao, Y., Descany, B., etal. (2009) Genomic analyses of the microsporidian Nosemaceranae, an emergent pathogen of honey bees. PLoS Pathog 5: e1000466.
5. Costa, F.S., and Weiss, L.M. (2000) Drug treatment of microsporidiosis. Drug Resist Updat 3: 384-399.
6. Desportes-Livage, I. (2000) Biology of microsporidia. Contrib Microbiol 6: 140-165.
7. Didier, E.S., and Weiss, L.M. (2006) Microsporidiosis: current status. Curr Opin Infect Dis 19: 485-492.
8. Didier, E.S., and Weiss, L.M. (2011) Microsporidiosis: not just in AIDS patients. Curr Opin Infect Dis 24: 490-495.
9. Didier, E.S., Maddry, J.A., Brindley, P.J., Stovall, M.E., and Didier, P.J. (2005) Therapeutic strategies for human microsporidia infections. Expert Rev Anti Infect Ther 3: 419-434.
10. Franzen, C. (2005) How do microsporidia invade cells? Folia Parasitol (Praha) 52: 36-40.
11. van der Giezen, M., Tovar, J., and Clark, C.G. (2005) Mitochondrion-derived organelles in protists and fungi. Int Rev Cytol 244: 175-225.
12. Goldberg, A.V., Molik, S., Tsaousis, A.D., Neumann, K., Kuhnke, G., Delbac, F., etal. (2008) Localization and functionality of microsporidian iron-sulphur cluster assembly proteins. Nature 452: 624-628.
13. Heinz, E., Williams, T.A., Nakjang, S., Noël, C.J., Swan, D.C., Goldberg, A.V., etal. (2012) The genome of the obligate intracellular parasite Trachipleistophora hominis: new insights into microsporidian genome dynamics and reductive evolution. PLoS Pathog 8: e1002979.
14. Hollister, W.S., Canning, E.U., Weidner, E., Field, A.S., Kench, J., and Marriott, D.J. (1996) Development and ultrastructure of Trachipleistophora hominis n.g., n.sp. after in vitro isolation from an AIDS patient and inoculation into athymic mice. Parasitology 112 (Part 1): 143-154.
15. James, T.Y., Pelin, A., Bonen, L., Ahrendt, S., Sain, D., Corradi, N., and Stajich, J.E. (2013) Shared signatures of parasitism and phylogenomics unite cryptomycota and microsporidia. Curr Biol 23: 1548-1553.
16. Katinka, M.D., Duprat, S., Cornillot, E., Metenier, G., Thomarat, F., Prensier, G., etal. (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414: 450-453.
17. Keeling, P.J. (2001) Parasites go the full monty. Nature 414: 401-402.
18. Kremer, J.R., Mastronarde, D.N., and McIntosh, J.R. (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116: 71-76.
19. Lom, J., and Nielsen, F. (2003) Fish Microsporidia: fine structural diversity and phylogeny. Int J Parasitol 33: 107-127.
20. Lucocq, J. (2012) Can data provenance go the full monty? Trends Cell Biol 22: 229-230.
21. McCullough, S., and Lucocq, J. (2005) Endoplasmic reticulum positioning and partitioning in mitotic HeLa cells. J Anat 206: 415-425.
22. Magno, R.C., Straker, L.C., de Souza, W., and Attias, M. (2005) Interrelations between the parasitophorous vacuole of Toxoplasma gondii and host cell organelles. Microsc Microanal 11: 166-174.
23. Mancini, M., Anderson, B.O., Caldwell, E., Sedghinasab, M., Paty, P.B., and Hockenbery, D.M. (1997) Mitochondrial proliferation and paradoxical membrane depolarization during terminal differentiation and apoptosis in a human colon carcinoma cell line. J Cell Biol 138: 449-469.
24. Pedersen, P.L., Mathupala, S., Rempel, A., Geschwind, J.F., and Ko, Y.H. (2002) Mitochondrial bound type II hexokinase: a key player in the growth and survival of many cancers and an ideal prospect for therapeutic intervention. Biochim Biophys Acta 1555: 14-20.
25. Perry, S.W., Norman, J.P., Barbieri, J., Brown, E.B., and Gelbard, H.A. (2011) Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. Biotechniques 50: 98-115.
26. Rasband, W.S. (1997-2013) ImageJ. Bethesda, MD: US National Institutes of Health [WWW document]. URL http://imagej.nih.gov/ij/.
27. Richards, T.A., Hirt, R.P., Williams, B.A., and Embley, T.M. (2003) Horizontal gene transfer and the evolution of parasitic protozoa. Protist 154: 17-32.
28. Rostovtseva, T.K., Sheldon, K.L., Hassanzadeh, E., Monge, C., Saks, V., Bezrukov, S.M., and Sackett, D.L. (2008) Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration. Proc Natl Acad Sci U S A 105: 18746-18751.
29. Rönnebäumer, K., Gross, U., and Bohne, W. (2008) The nascent parasitophorous vacuole membrane of Encephalitozoon cuniculi is formed by host cell lipids and contains pores which allow nutrient uptake. Eukaryot Cell 7: 1001-1008.
30. Scanlon, M., Leitch, G.J., Visvesvara, G.S., and Shaw, A.P. (2004) Relationship between the host cell mitochondria and the parasitophorous vacuole in cells infected with Encephalitozoon microsporidia. J Eukaryot Microbiol 51: 81-87.
31. Sinai, A.P., Webster, P., and Joiner, K.A. (1997) Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. J Cell Sci 110 (Part 17): 2117-2128.
32. Smiley, S.T., Reers, M., Mottola-Hartshorn, C., Lin, M., Chen, A., Smith, T.W., etal. (1991) Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci U S A 88: 3671-3675.
33. Smythe, E., Pypaert, M., Lucocq, J., and Warren, G. (1989) Formation of coated vesicles from coated pits in broken A431 cells. J Cell Biol 108: 843-853.
34. Tokuyasu, K.T. (1973) A technique for ultracryotomy of cell suspensions and tissues. J Cell Biol 57: 551-565.
35. Tsaousis, A.D., Kunji, E.R., Goldberg, A.V., Lucocq, J.M., Hirt, R.P., and Embley, T.M. (2008) A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453: 553-556.
36. Weidner, E., Canning, E.U., Rutledge, C.R., and Meek, C.L. (1999) Mosquito (Diptera: Culicidae) host compatibility and vector competency for the human myositic parasite Trachipleistophora hominis (Phylum Microspora). J Med Entomol 36: 522-525.
37. Williams, B.A., and Keeling, P.J. (2003) Cryptic organelles in parasitic protists and fungi. Adv Parasitol 54: 9-68.
38. Williams, B.A., and Keeling, P.J. (2011) Microsporidia - highly reduced and derived relatives of Fungi. In Evolution of Fungi and Fungal-like Organisms, Heidleberg. Poeggeler, S., and Woestemeyer, J. (eds). Springer, pp. 25-36.
39. Williams, B.A., Haferkamp, I., and Keeling, P.J. (2008) An ADP/ATP-specific mitochondrial carrier protein in the microsporidian Antonospora locustae. J Mol Biol 375: 1249-1257.
40. Wilson, J.E. (1995) Hexokinases. Rev Physiol Biochem Pharmacol 126: 65-198.
41. Wittner, M.W., and Weiss, L.M. (1999) The Microsporidia and Microsporidiosis. Washington DC: ASM Press.