Protein Tyrosine Phosphatase-Induced Hyperactivity Is a Conserved Strategy of a Subset of BaculoViruses to Manipulate Lepidopteran Host Behavior

Houte, Stineke van; Ros, V.I.D.; Mastenbroek, Tom G.; Vendrig, Nadia J.; Hoover, Kelli; Spitzen, Jeroen; Oers, Monique M. van

doi:10.1371/journal.pone.0046933

Cited by 70 publications

(162 citation statements)

References 52 publications

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“…One of the most prominent cases comes from a line of research conducted on hairworms (Nematomorpha). These endoparasites infect a wide range of arthropod hosts (Poulin, 2010(Poulin, , 2011aThomas et al, 2010), inducing intense hydrophilic behaviors in their otherwise hydrophobic hosts (Thomas et al, 2002;Poulin, 2011a). A dramatic case of this induced behavioral switch, comes from the cricket Nemobius sylvestris.…”

Section: Proteomic and Genomic Host Manipulation Proteomic Manipulationmentioning

confidence: 99%

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Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation

Herbison

2017

Front. Ecol. Evol.

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Scientific and public interest in host manipulation by parasites has surged over the past few decades, resulting in an exponential growth of cases where potential behavioral manipulation has been identified. However, these studies dwarf the number of genuine attempts to elucidate the mechanistic processes behind this behavioral manipulation. Ultimately, this imbalance has slowed progress in the study of the mechanisms underlying host manipulation. As it stands, research suggests that the mechanisms of host manipulation fall into three categories: immunological, genomic/proteomic and neuropharmacological, and forth potential category: symbioant-mediated manipulation. After exploration of the literature pertaining to these four pathways, four major trends become evident. First and foremost, there is a severe disconnect between the observed molecular and behavioral shifts in a parasitized host. Indeed, very rarely a study demonstrates that molecular changes observed in a host are the result of active manipulation by the resident parasite, or that these molecular changes directly result in behavioral manipulation that increases the parasite's fitness. Secondly, parasites may often employ multiple pathways in unison to achieve control over their hosts. Despite this, current scientific approaches usually focus on each manipulation pathway in isolation rather than integrating them. Thirdly, the relative amount of host-parasite systems yet to be investigated in terms of molecular manipulation is staggering. Finally, as a result of the aforementioned trends, guiding mechanisms or principles for the multiple types of behavioral manipulation are yet to be found. Researchers should look to identify the manipulative factors required to generate the molecular changes seen in hosts, while also considering the "multi-pronged" approach parasites are taking to manipulate behavior. Assessing gene expression and its products during transitional periods in parasites may be a key methodological approach for tackling these recent trends in the host manipulation literature.

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Section: Proteomic and Genomic Host Manipulation Proteomic Manipulationmentioning

confidence: 99%

“…However, two baculovirus species that alter the locomotive activity of their hosts, appear to bypass gene regulation in favor of releasing protein tyrosine phosphatase (PTP), a dephosphorylation enzyme, into the host (Kamita et al, 2005;van Houte et al, 2012). Consequently, the PTP is thought to dephosphorylate PKG.…”

Section: Genomic Manipulationmentioning

confidence: 99%

Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation

Herbison

2017

Front. Ecol. Evol.

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“…A total of 19,230 (27.3%) unigenes were assigned at least one GO term, among which 16,527 (23.5%), 15,347 (21.8%), and 15,990 (22.7%) unigenes were assigned GO terms in the categories of cellular components, molecular functions, and biological processes, respectively. In addition, a substantial number of unigenes (14,777, or approximately 21%) were assigned GO terms in two or more categories.…”

Section: Assembly and Annotation Of The T Ni Tnms42 Transcriptomementioning

confidence: 99%

“…In addition to genes that regulate and/or mediate viral transcription, translation, and DNA replication, the virus also encodes a variety of genes that modify cellular and organismal physiology, architecture, and defenses. These viral manipulations include effects on development and behavior of the host insect through hormonal control and perhaps other mechanisms (11)(12)(13)(14), a profound modification of cellular physiology and architecture (15)(16)(17), and host tissue breakdown, which results in release of the virus into the environment (18)(19)(20)(21). The AcMNPV infection is completed in a relatively short time period (approximately 24 to 48 h), producing infectious budded and occluded viruses.…”

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confidence: 99%

Transcriptome Responses of the Host Trichoplusia ni to Infection by the Baculovirus Autographa californica Multiple Nucleopolyhedrovirus

Chen

Zhong

Fei

et al. 2014

J Virol

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Productive infection of Trichoplusia ni cells by the baculovirus Autographa californica multiple nucleopolyhedrovirus (AcMNPV) leads to expression of ϳ156 viral genes and results in dramatic cell remodeling. How the cell transcriptome responds to viral infection was unknown due to the lack of a reference genome and transcriptome for T. ni. We used an ϳ60-Gb RNA sequencing (RNA-seq) data set from infected and uninfected T. ni cells to generate and annotate a de novo transcriptome assembly of approximately 70,322 T. ni unigenes (assembled transcripts), representing the 48-h infection cycle. Using differential gene expression analysis, we found that the majority of host transcripts were downregulated after 6 h postinfection (p.i.) and throughout the remainder of the infection. In contrast, 5.7% (4,028) of the T. ni unigenes were upregulated during the early period (0 to 6 h p.i.), followed by a decrease through the remainder of the infection cycle. Also, a small subset of genes related to metabolism and stress response showed a significant elevation of transcript levels at 18 and 24 h p.i. but a decrease thereafter. We also examined the responses of genes belonging to a number of specific pathways of interest, including stress responses, apoptosis, immunity, and protein trafficking. We identified specific pathway members that were upregulated during the early phase of the infection. Combined with the parallel analysis of AcMNPV expression, these results provide both a broad and a detailed view of how baculovirus infection impacts the host cell transcriptome to evade cellular defensive responses, to modify cellular biosynthetic pathways, and to remodel cell structure. IMPORTANCEBaculoviruses are insect-specific DNA viruses that are highly pathogenic to their insect hosts. In addition to their use for biological control of certain insects, baculoviruses also serve as viral vectors for numerous biotechnological applications, such as mammalian cell transduction and protein expression for vaccine production. While there is considerable information regarding viral gene expression in infected cells, little is known regarding responses of the host cell to baculovirus infection. In these studies, we assembled a cell transcriptome from the host Trichoplusia ni and used that transcriptome to analyze changes in host cell gene expression throughout the infection cycle. The study was performed in parallel with a prior study of changes in viral gene expression. Combined, these studies provide an unprecedented new level of detail and an overview of events in the infection cycle, and they will stimulate new experimental approaches to understand, modify, and utilize baculoviruses for a variety of applications.

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“…Insects infected with Helicoverpa zea nudivirus 2 are sterilized [19]; however, continued mating is vital for virus transmission and infected females have enhanced sexual behaviour, that increases transmission [20]. A recent study on Autographa californica NPV (AcMNPV), with the lepidopteran host, Spodoptera exigua, confirmed the role of the ptp gene in the induction of hyperactivity in baculovirus infected larvae [24 ], but not in climbing behaviour [25]. Demonstrating that pathogen-induced behavioural changes are adaptive and do increase transmission can be challenging.…”

Section: Pathogen-induced Changes In Transmission Behaviourmentioning

confidence: 98%

Insect virus transmission: different routes to persistence

Cory

2015

Current Opinion in Insect Science

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Protein Tyrosine Phosphatase-Induced Hyperactivity Is a Conserved Strategy of a Subset of BaculoViruses to Manipulate Lepidopteran Host Behavior

Cited by 70 publications

References 52 publications

Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation

Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation

Transcriptome Responses of the Host Trichoplusia ni to Infection by the Baculovirus Autographa californica Multiple Nucleopolyhedrovirus

Insect virus transmission: different routes to persistence

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