Tupanvirus-infected amoebas are induced to aggregate with uninfected cells promoting viral dissemination

Oliveira, Graziele Pereira; Silva, Lorena; Leão, Thiago Lima; Mougari, Said; Fonseca, Flávio Guimarães da; Kroon, Erna Geessien; Scola, Bernard La; Abrahão, Jônatas Santos

doi:10.1038/s41598-018-36552-4

Cited by 26 publications

(53 citation statements)

References 29 publications

(34 reference statements)

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“…Kyotovirus causes cell-rounding in infected amoeba, as previously reported in other members of the family Marseilleviridae (Boyer et al, 2009;Dos Santos et al, 2016). On the other hand, kashiwazakivirus and hokutovirus lead infected amoeba cells to form "bunches, " as previously reported in tupanviruses (Oliveira et al, 2019). It is not yet understood how "bunches" form after kashiwazaki-and hokutovirus infections, from both amoebal ethological and viral aspects.…”

Section: Introductionmentioning

confidence: 58%

“…After infection with a giant virus, Acanthamoeba cells show various morphological and behavioral changes, termed cytopathic effects (CPE), and are then killed. Recent studies have indicated that amoeba cells infected with giant viruses show various CPEs, such as cellrounding, encystment, lysis, and formation of cell aggregates called "bunches" (Reteno et al, 2015;Aoki et al, 2019;Oliveira et al, 2019;Yoshikawa et al, 2019). Among these CPEs, cellrounding or lysis are the common CPEs to check and confirm the infection of amoeba with giant viruses.…”

Section: Introductionmentioning

confidence: 99%

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Kinetic Analysis of the Motility of Giant Virus-Infected Amoebae Using Phase-Contrast Microscopic Images

et al. 2020

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Tracking cell motility is a useful tool for the study of cell physiology and microbiology. Although phase-contrast microscopy is commonly used, the existence of optical artifacts called "halo" and "shade-off" have inhibited image analysis of moving cells. Here we show kinetic image analysis of Acanthamoeba motility using a newly developed computer program named "Phase-contrast-based Kinetic Analysis Algorithm for Amoebae (PKA3)," which revealed giant-virus-infected amoebae-specific motilities and aggregation profiles using time-lapse phase-contrast microscopic images. This program quantitatively detected the time-dependent, sequential changes in cellular number, size, shape, and direction and distance of cell motility. This method expands the potential of kinetic analysis of cultured cells using versatile phase-contrast images. Furthermore, this program could be a useful tool for investigating detailed kinetic mechanisms of cell motility, not only in virus-infected amoebae but also in other cells, including cancer cells, immune response cells, and neurons.

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Section: Introductionmentioning

confidence: 58%

Section: Introductionmentioning

confidence: 99%

Kinetic Analysis of the Motility of Giant Virus-Infected Amoebae Using Phase-Contrast Microscopic Images

et al. 2020

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“…We observed that the formation of the CPE seems be slower in V. vermiformis than to that previously observed in A. castellanii (Abrahão et al, 2018). We observed that TPV induces in V. vermiformis cell rounding and early cluster formation, the typical “bunches” formed by TPV in amoeba (Oliveira et al, 2019), being visible only around 12 h.p.i., being most evident at 16 and 24 h.p.i. At 36–72 h p.i., we observed bunches disaggregation and lysis (Supplementary Figure S1A).…”

Section: Resultsmentioning

confidence: 79%

“…Tupanviruses were isolated from extreme environments in Brazil and showed unprecedented characteristics, including the ability to replicate in different genera of protozoa (Abrahão et al, 2018). Our data suggest that TPV cycle in V. vermiformis is slower and less productive than TPV replication in A. castellanii (Oliveira et al, 2019; Supplementary Figure S1). The reason why we observe a delay in the evolution of TPV CPE in V. vermiformis requires more investigation as well.…”

Section: Discussionmentioning

confidence: 84%

Microscopic Analysis of the Tupanvirus Cycle in Vermamoeba vermiformis

et al. 2019

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Since Acanthamoeba polyphaga mimivirus (APMV) was identified in 2003, several other giant viruses of amoebae have been isolated, highlighting the uniqueness of this group. In this context, the tupanviruses were recently isolated from extreme environments in Brazil, presenting virions with an outstanding tailed structure and genomes containing the most complete set of translation genes of the virosphere. Unlike other giant viruses of amoebae, tupanviruses present a broad host range, being able to replicate not only in Acanthamoeba sp. but also in other amoebae, such as Vermamoeba vermiformis , a widespread, free-living organism. Although the Tupanvirus cycle in A. castellanii has been analyzed, there are no studies concerning the replication of tupanviruses in other host cells. Here, we present an in-depth microscopic study of the replication cycle of Tupanvirus in V. vermiformis . Our results reveal that Tupanvirus can enter V. vermiformis and generate new particles with similar morphology to when infecting A. castellanii cells. Tupanvirus establishes a well-delimited electron-dense viral factory in V. vermiformis , surrounded by lamellar structures, which appears different when compared with different A. castellanii cells. Moreover, viral morphogenesis occurs entirely in the host cytoplasm within the viral factory, from where complete particles, including the capsid and tail, are sprouted. Some of these particles have larger tails, which we named “supertupans.” Finally, we observed the formation of defective particles, presenting abnormalities of the tail and/or capsid. Taken together, the data presented here contribute to a better understanding of the biology of tupanviruses in previously unexplored host cells.

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“…The tupanvirus' infection is characterized by the formation of bunches, aggregate of infected amoebae with uninfected cells. This is the first time this way of increasing viral progeny has been observed in a giant viral infection (Oliveira et al, 2019). Furthermore, it is also the first virus to infect a broad range of hosts, such as Tetrahymena sp., Acanthamoeba castellanii neff, Vermamoeba vermiformis, or Willaertia magna (Abrahão et al, 2018;Silva et al, 2019).…”

Section: Introductionmentioning

confidence: 77%

How Tupanvirus Degrades the Ribosomal RNA of Its Amoebal Host? The Ribonuclease T2 Track

Rolland¹,

Scola²,

Levasseur³

2020

Front. Microbiol.

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Tupanviruses are giant viruses recently discovered in Brazil from extreme environments: Tupanvirus soda lake (TPV-SL) and Tupanvirus deep ocean (TPV-DO). Unexpected features in Tupanviruses is the cytotoxic effect observed during infection, where the virus degrades the ribosomal RNA (rRNA) of its amoebal host. Interestingly, only TPV-SL causes this rRNA shutdown. We performed a genomic comparison of the two strains to determine potential modifications explaining the absence of rRNA degradation by TPV-DO. Whole genome comparisons were performed as well as more in-depth analysis at the gene level. We also calculated selective pressure on the orthologous genes between the two viruses. Our computational and evolutionary investigations revealed a potential target: a ribonuclease T2. These enzymes are known to be involved in cellular RNA catabolism such as in lysosomal degradation of rRNA. Our results suggest a functional ribonuclease localized in acid compartment closely related to ribonuclease T2 from eukaryotes. Silencing of the RNAse T2 gene of TPV-SL abolished its rRNA shutdown ability thereby correlating in silico assumption to the experimental evidence. In conclusion, all our results pointed to RNAse T2 as a target for explaining the difference for rRNA degradation ability between both strains.

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Tupanvirus-infected amoebas are induced to aggregate with uninfected cells promoting viral dissemination

Cited by 26 publications

References 29 publications

Kinetic Analysis of the Motility of Giant Virus-Infected Amoebae Using Phase-Contrast Microscopic Images

Kinetic Analysis of the Motility of Giant Virus-Infected Amoebae Using Phase-Contrast Microscopic Images

Microscopic Analysis of the Tupanvirus Cycle in Vermamoeba vermiformis

How Tupanvirus Degrades the Ribosomal RNA of Its Amoebal Host? The Ribonuclease T2 Track

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