Invasion of Host Cells by Microsporidia

Han, Bing; Takvorian, Peter M.; Weiss, Louis M.

doi:10.3389/fmicb.2020.00172

Cited by 88 publications

(82 citation statements)

References 161 publications

(229 reference statements)

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“…NbPTP6 had six potential O-glycosylation sites and one potential N-glycosylation site, which was similar to the NbPTP1 protein. Previously, O-glycosylation of EhPTP1 was found to affect the ability of E. hellem to infect host cells [26][27][28]. Moreover, NbPTP1 could bind with ConA, proving the existence of glycosylation modification [1,23,28,29].…”

Section: Discussionmentioning

confidence: 95%

Identification and characterization a novel polar tube protein (NbPTP6) from the microsporidian Nosema bombycis

Wang

Fan

et al. 2020

Parasites Vectors

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Background Microsporidians are opportunistic pathogens with a wide range of hosts, including invertebrates, vertebrates and even humans. Microsporidians possess a highly specialized invasion structure, the polar tube. When spores encounter an appropriate environmental stimulation, the polar tube rapidly everts out of the spore, forming a 50–500 µm hollow tube that serves as a conduit for sporoplasm passage into host cells. The polar tube is mainly composed of polar tube proteins (PTPs). So far, five major polar tube proteins have been isolated from microsporidians. Nosema bombycis, the first identified microsporidian, infects the economically important insect silkworm and causes heavy financial loss to the sericulture industry annually. Results A novel polar tube protein of N. bombycis (NbPTP6) was identified. NbPTP6 was rich in histidine (H) and serine (S), which contained a signal peptide of 16 amino acids at the N-terminus. NbPTP6 also had 6 potential O-glycosylation sites and 1 potential N-glycosylation site. The sequence alignment analysis revealed that NbPTP6 was homologous with uncharacterized proteins from other microsporidians (Encephalitozoon cuniculi, E. hellem and N. ceranae). Additionally, the NbPTP6 gene was expressed in mature N. bombycis spores. Indirect immunofluorescence analysis (IFA) result showed that NbPTP6 is localized on the whole polar tube of the germinated spores. Moreover, IFA, enzyme-linked immunosorbent (ELISA) and fluorescence-activated cell sorting (FACS) assays results revealed that NbPTP6 had cell-binding ability. Conclusions Based on our results, we have confirmed that NbPTP6 is a novel microsporidian polar tube protein. This protein could adhere with the host cell surface, so we speculated it might play an important role in the process of microsporidian infection.

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Section: Discussionmentioning

confidence: 95%

Identification and characterization a novel polar tube protein (NbPTP6) from the microsporidian Nosema bombycis

Wang

Fan

et al. 2020

Parasites Vectors

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“…In humans, microsporidia are commonly found in immunocompromised patients, and lead to opportunistic infections, such as intestinal [13], ocular [14], respiratory [15], and systemic diseases [16]. As obligate intracellular parasites with reduced genomes [17], they are dependent on the host for replication [18,19]. Prior to exiting the host cell, microsporidia form spores, which are the only form of the organism that can survive outside of a host.…”

Section: Introductionmentioning

confidence: 99%

3-Dimensional organization and dynamics of the microsporidian polar tube invasion machinery

et al. 2020

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Microsporidia, a divergent group of single-celled eukaryotic parasites, harness a specialized harpoon-like invasion apparatus called the polar tube (PT) to gain entry into host cells. The PT is tightly coiled within the transmissible extracellular spore, and is about 20 times the length of the spore. Once triggered, the PT is rapidly ejected and is thought to penetrate the host cell, acting as a conduit for the transfer of infectious cargo into the host. The organization of this specialized infection apparatus in the spore, how it is deployed, and how the nucleus and other large cargo are transported through the narrow PT are not well understood. Here we use serial block-face scanning electron microscopy to reveal the 3-dimensional architecture of the PT and its relative spatial orientation to other organelles within the spore. Using high-speed optical microscopy, we also capture and quantify the entire PT germination process of three human-infecting microsporidian species in vitro: Anncaliia algerae, Encephalitozoon hellem and E. intestinalis. Our results show that the emerging PT experiences very high accelerating forces to reach velocities exceeding 300 μm�s-1 , and that firing kinetics differ markedly between species. Live-cell imaging reveals that the nucleus, which is at least 7 times larger than the diameter of the PT, undergoes extreme deformation to fit through the narrow tube, and moves at speeds comparable to PT extension. Our study sheds new light on the 3-dimensional organization, dynamics, and mechanism of PT extrusion, and shows how infectious cargo moves through the tube to initiate infection.

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“…Microsporidia infect a wide range of hosts, including nematodes 6,7 , insects 8,9 , and vertebrates 10,11 , including humans 12 . As obligate intracellular parasites with a reduced genome 13 , they are dependent on the host for replication 14,15 . Prior to exiting the host cell, microsporidia form spores, which are the only form of the organism that can survive outside of a host.…”

mentioning

confidence: 99%

“…To initiate infection of a new cell, these parasites have evolved a unique, harpoon-like invasion apparatus called the polar tube (PT) [15][16][17] that is present in all microsporidian species. The PT is tightly coiled within the dormant spore, resembling a spring 18,19 .…”

mentioning

confidence: 99%

3-Dimensional Organization and Dynamics of the Microsporidian Polar Tube Invasion Machinery

Jaroenlak

Cammer

Davydov

et al. 2020

Preprint

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Microsporidia, a divergent group of single-celled eukaryotic parasites, harness a specialized harpoon-like invasion apparatus called the polar tube (PT) to gain entry into host cells. The PT is tightly coiled within the transmissible extracellular spore, and is about 20 times the length of the spore. Once triggered, the PT is rapidly ejected and is thought to penetrate the host cell, acting as a conduit for the transfer of infectious cargo into the host. The organization of this specialized infection apparatus in the spore, how it is deployed, and how the nucleus and other large cargo are transported through the narrow PT are not well understood. Here we use serial block-face scanning electron microscopy to reveal the 3-dimensional architecture of the PT and its relative spatial orientation to other organelles within the spore. Using high-speed optical microscopy, we also capture and quantify the entire PT germination process in vitro. Our results show that the emerging PT experiences very high accelerating forces to reach velocities exceeding 300 μm⋅s -1 , and that firing kinetics differ markedly between species. Live-cell imaging reveals that the nucleus, which is approximately 7 times larger than the diameter of the PT, undergoes extreme deformation to fit through the narrow tube, and moves at speeds comparable to PT extension. Our study sheds new light on the 3-dimensional organization, dynamics, and mechanism of PT extrusion, and shows how infectious cargo moves through the tube to initiate infection.

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Invasion of Host Cells by Microsporidia

Cited by 88 publications

References 161 publications

Identification and characterization a novel polar tube protein (NbPTP6) from the microsporidian Nosema bombycis

Identification and characterization a novel polar tube protein (NbPTP6) from the microsporidian Nosema bombycis

3-Dimensional organization and dynamics of the microsporidian polar tube invasion machinery

3-Dimensional Organization and Dynamics of the Microsporidian Polar Tube Invasion Machinery

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