Relationship between the Host Cell Mitochondria and the Parasitophorous Vacuole in Cells Infected with <i>Encephalitozoon</i> Microsporidia

Scanlon, Mary; Leitch, Gordon J.; Visvesvara, Govinda S.; Shaw, Andrew

doi:10.1111/j.1550-7408.2004.tb00166.x

Cited by 40 publications

(41 citation statements)

References 20 publications

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“…This is similar to the situation seen in Encephalitozoon-infected cells where mitochondria are organized around the parasitophorous vacuole (e.g. Scanlon et al 2004) and in Toxoplasma-infected cells where both endoplasmic reticulum and mitochondria are in intimate contact with the parasitophorous vacuole (Sinai et al 1997). In the smaller and most highly organized multinucleate cells there was a clear cortex, devoid of parasites.…”

Section: Discussionsupporting

confidence: 71%

“…We previously described an assay that could be used in viable microsporidia-infected cells in which calcein was employed to negatively stain parasite stages and in which MitoTracker was used to probe host cell mitochondria (Scanlon et al 2004). Fig.…”

Section: Resultsmentioning

confidence: 99%

“…In one experiment the distribution of intracellular parasite stages and host cell mitochondria was determined in viable V. corneae-infected E6 cells using the method described previously (Leitch et al 1997, Scanlon et al 2004. Briefly, host cells were loaded with the fluorescent probe, calcein, which in the host cell is found as an impermeable free acid incapable of passing the parasite plasma membrane, and MitoTracker-CMXRos which labels mitochondria.…”

Section: Methodsmentioning

confidence: 99%

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Multinucleate host cells induced by Vittaforma corneae (Microsporidia)

Leitch¹,

Shaw²,

Colden-Stanfield³

et al. 2005

FOLIA PARASIT

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Abstract. The microsporidium Vittaforma corneae (Shadduck, Meccoli, Davis et Font, 1990) develops within the target cell cytoplasm. In the present study, green monkey kidney (E6) cells infected at 30°C, 35°C or 37°C with V. corneae developed enlarged multinucleate structures of up to 200 µm in any horizontal dimension made up either of a single cell or of multiple fused cells. A number of epithelial cell types (SW-480, HT-29, Caco-2 and HCT-8) were infected with V. corneae but did not induce the same highly organized structures, suggesting that for the structure to develop, the host cell must be capable of continued mitosis, and not be differentiated or be detaching from the surface matrix. Live cell imaging of infected E6 cells revealed large, multinucleate infected cells characterized by a central focus from which radiated parasite stages and host cell mitochondria. Immunocytochemistry identifying γ and α tubulin suggested that a single centrally-located microtubule organizing centre governed the distribution of parasite stages and host cell organelles, with mitochondria and parasites being eventually transported towards the periphery of the structure. Whole cell patch clamp analysis of infected cells indicated an average five-fold increase in total membrane capacitance, consistent with an enlarged single cell. Scanning electron microscopy revealed cell-like protrusions around the periphery of the structure with the intervening space being made up of parasites and cell debris. Clearly in the case of V. corneae-infected E6 cells the parasite-host cell relationship involves subverting the host cell cytoskeleton and cell volume control, providing the parasite with the same protected niche as does a xenoma.

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Section: Discussionsupporting

confidence: 71%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Multinucleate host cells induced by Vittaforma corneae (Microsporidia)

Leitch¹,

Shaw²,

Colden-Stanfield³

et al. 2005

FOLIA PARASIT

Self Cite

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“…Recruitment of mitochondria to the LCV is a feature shared with the parasitophorous vacuoles of Chlamydia psittaci (54, 62), Toxoplasma gondii (74), and Encephalitozoon microsporidia (71). As far as we know, the molecular mechanism of recruitment has been described only in the case of T. gondii, where the N terminus of ROP2, a T. gondii protein localized to the parasitophorous vacuole membrane, has characteristics of a mitochondrial targeting signal sequence and is exposed to the host cytosol (73).…”

Section: Discussionmentioning

confidence: 99%

The Purified and Recombinant Legionella pneumophila Chaperonin Alters Mitochondrial Trafficking and Microfilament Organization

Chong¹,

Lima²,

Allan³

et al. 2009

Infect Immun

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A portion of the total cellular pool of the Legionella pneumophila chaperonin, HtpB, is found on the bacterial cell surface, where it can mediate invasion of nonphagocytic cells. HtpB continues to be abundantly produced and released by internalized L. pneumophila and may thus have postinvasion functions. We used here two functional models (protein-coated beads and expression of recombinant proteins in CHO cells) to investigate the competence of HtpB in mimicking early intracellular trafficking events of L. pneumophila, including the recruitment of mitochondria, cytoskeletal alterations, the inhibition of phagosome-lysosome fusion, and association with the endoplasmic reticulum. Microscopy and flow cytometry studies indicated that HtpB-coated beads recruited mitochondria in CHO cells and U937-derived macrophages and induced transient changes in the organization of actin microfilaments in CHO cells. Ectopic expression of HtpB in the cytoplasm of transfected CHO cells also led to modifications in actin microfilaments similar to those produced by HtpBcoated beads but did not change the distribution of mitochondria. Association of phagosomes containing HtpB-coated beads with the endoplasmic reticulum was not consistently detected by either fluorescence or electron microscopy studies, and only a modest delay in the fusion of TrOv-labeled lysosomes with phagosomes containing HtpB-coated beads was observed. HtpB is the first Legionella protein and the first chaperonin shown to, by means of our functional models, induce mitochondrial recruitment and microfilament rearrangements, two postinternalization events that typify the early trafficking of virulent L. pneumophila.

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“…Transport processes (including ADP/ATP transport) on the surface of microsporidia were recently reviewed (554). Microsporidia appear to recruit host mitochondria around their surface, apparently in line with their life-style as ATP-stealing energy parasites (439,554).…”

Section: Figmentioning

confidence: 99%

Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes

Müller

Mentel

Hellemond

et al. 2012

Microbiol Mol Biol Rev

683

904

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SUMMARY Major insights into the phylogenetic distribution, biochemistry, and evolutionary significance of organelles involved in ATP synthesis (energy metabolism) in eukaryotes that thrive in anaerobic environments for all or part of their life cycles have accrued in recent years. All known eukaryotic groups possess an organelle of mitochondrial origin, mapping the origin of mitochondria to the eukaryotic common ancestor, and genome sequence data are rapidly accumulating for eukaryotes that possess anaerobic mitochondria, hydrogenosomes, or mitosomes. Here we review the available biochemical data on the enzymes and pathways that eukaryotes use in anaerobic energy metabolism and summarize the metabolic end products that they generate in their anaerobic habitats, focusing on the biochemical roles that their mitochondria play in anaerobic ATP synthesis. We present metabolic maps of compartmentalized energy metabolism for 16 well-studied species. There are currently no enzymes of core anaerobic energy metabolism that are specific to any of the six eukaryotic supergroup lineages; genes present in one supergroup are also found in at least one other supergroup. The gene distribution across lineages thus reflects the presence of anaerobic energy metabolism in the eukaryote common ancestor and differential loss during the specialization of some lineages to oxic niches, just as oxphos capabilities have been differentially lost in specialization to anoxic niches and the parasitic life-style. Some facultative anaerobes have retained both aerobic and anaerobic pathways. Diversified eukaryotic lineages have retained the same enzymes of anaerobic ATP synthesis, in line with geochemical data indicating low environmental oxygen levels while eukaryotes arose and diversified.

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Relationship between the Host Cell Mitochondria and the Parasitophorous Vacuole in Cells Infected with Encephalitozoon Microsporidia

Cited by 40 publications

References 20 publications

Multinucleate host cells induced by Vittaforma corneae (Microsporidia)

Multinucleate host cells induced by Vittaforma corneae (Microsporidia)

The Purified and Recombinant Legionella pneumophila Chaperonin Alters Mitochondrial Trafficking and Microfilament Organization

Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes

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