Zebrafish encoded 3-O-sulfotransferase-2 generated heparan sulfate serves as a receptor during HSV-1 entry and spread

Baldwin, John R.; Antoine, Thessicar E.; Shukla, Deepak; Tiwari, Vaibhav

doi:10.1016/j.bbrc.2013.02.020

Cited by 11 publications

(20 citation statements)

References 29 publications

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“…[5][6][7][8] Quite interestingly, zebrafish Danio rerio widely expresses 3-OSTs, which are required for embryonic development and also for generating HSV receptors. [9][10][11][12][13][14] Supporting the idea that zebrafish 3-OSTs can generate the receptors, we have found evidence that similar to the human 3-OST-3 isoform, zebrafish encoded 3-OST-3 also allows HSV-1 entry. 9 In addition, zebrafish embryos are susceptible to HSV infection and the zebrafish model is now emerging as a new model system for host-pathogen interactions, largely because the zebrafish larvae are transparent and thus, highly suited for in vivo imaging and cost effective high throughput screening.…”

supporting

confidence: 66%

“…10,14 The in situ hybridization data further showed extensive 3-OST brain expression localized in the specific brain subdivisions.…”

mentioning

confidence: 84%

“…7,8 Recently, our group provided the first evidence of zebrafish encoded 3-OST modified HS receptor mimicking human 3-OST generated HS in allowing HSV-1 entry and spread. [9][10][11] Our results raised the possibility that zebrafish can provide a reasonable ground to study the role of 3-OST generated receptors in HSV-1 infection by making 3-OST isoform-specific knockouts. Zebrafish embryos can be microinjected with moroholinos at 1-4 cell stage to target the specific 3-OST gene.…”

mentioning

confidence: 88%

“…Using Chinese hamster ovary (CHO-K1) cells transiently expressing zebrafish encoded 3-OST-2 and 3-OST-3 isoforms resulted in HSV-1 infection. 9,10 More direct and visual evidence of HSV-1 infection was demonstrated by using green fluorescent protein (GFP)-tagged HSV-1 (K26GFP) virions, which clearly infected CHO-K1 cells expressing zebrafish encoded 3-OST-3. The infection was also confirmed by high resolution electron microscopy.…”

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confidence: 99%

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Zebrafish: Modeling for Herpes Simplex Virus Infections

et al. 2014

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For many years, zebrafish have been the prototypical model for studies in developmental biology. In recent years, zebrafish has emerged as a powerful model system to study infectious diseases, including viral infections. Experiments conducted with herpes simplex virus type-1 in adult zebrafish or in embryo models are encouraging as they establish proof of concept with viral-host tropism and possible screening of antiviral compounds. In addition, the presence of human homologs of viral entry receptors in zebrafish such as 3-O sulfated heparan sulfate, nectins, and tumor necrosis factor receptor superfamily member 14-like receptor bring strong rationale for virologists to test their in vivo significance in viral entry in a zebrafish model and compare the structure-function basis of virus zebrafish receptor interaction for viral entry. On the other end, a zebrafish model is already being used for studying inflammation and angiogenesis, with or without genetic manipulations, and therefore can be exploited to study viral infection-associated pathologies. The major advantage with zebrafish is low cost, easy breeding and maintenance, rapid lifecycle, and a transparent nature, which allows visualizing dissemination of fluorescently labeled virus infection in real time either at a localized region or the whole body. Further, the availability of multiple transgenic lines that express fluorescently tagged immune cells for in vivo imaging of virus infected animals is extremely attractive. In addition, a fully developed immune system and potential for receptor-specific knockouts further advocate the use of zebrafish as a new tool to study viral infections. In this review, we focus on expanding the potential of zebrafish model system in understanding human infectious diseases and future benefits.

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supporting

confidence: 66%

“…10,14 The in situ hybridization data further showed extensive 3-OST brain expression localized in the specific brain subdivisions.…”

mentioning

confidence: 84%

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confidence: 88%

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confidence: 99%

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Zebrafish: Modeling for Herpes Simplex Virus Infections

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“…Successful cloning of the ZF enzymes was verified by enzymatic digestion with restriction endonucleases (Fig. 2B to E) as previously described (14,16,17).Zebrafish 3-OST-6, but not 3-OST-1, -5, and -7, supports HSV-1 entry into resistant CHO-K1 cells. We investigated whether the ZF 3-OST enzymes can support HSV-1 entry into…”

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confidence: 69%

Comprehensive Analysis of Herpes Simplex Virus 1 (HSV-1) Entry Mediated by Zebrafish 3- O -Sulfotransferase Isoforms: Implications for the Development of a Zebrafish Model of HSV-1 Infection

Yakoub

Rawal

Maus

et al. 2014

J Virol

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Here, we performed a comprehensive analysis of the role of ZF 3-OST isoforms (3-OST-1, 3-OST-5, 3-OST-6, and 3-OST-7) in HSV-1 entry. We found that a group of 3-OST gene family isoforms (3-OST-2, -3, -4, and -6) with conserved catalytic and substrate-binding residues of the enzyme mediates HSV-1 entry and spread, while the other group (3-OST-1, -5, and -7) lacks these properties. These results demonstrate that HSV-1 entry can be recapitulated by certain ZF 3-OST enzymes, a significant step toward the establishment of a ZF model of HSV-1 infection and tissue-specific tropism. Herpes simplex virus 1 (HSV-1) entry into the host cells requires interactions between viral envelope glycoprotein D (gD) and host cell receptors (1). An important gD receptor is 3-O-sulfated heparan sulfate (3-OS HS) (2, 3). Synthesis and modifications of HS is a multistep process (4-8), of which the last step involves O-sulfation at different positions of the molecule, catalyzed by various sulfotransferases (4). 3-O-Sulfotransferases (3-OST-1, -2, -3A, -3B, -4, -5, and -6 isoforms; also called Hs3st1, -2, -3A, -3B, -4, -5, and -6, respectively) catalyze sulfation at the C-3 of the glucosamine units of HS, generating specific proteinbinding sites for HSV-1 gD (2, 3, 9, 10).Recent studies of zebrafish (ZF) provided a functional analysis of 3-OST-generated HS (11-15). Out of the characterized eight 3-OST family members in ZF, seven genes show homology to known 3-OST genes in mice and humans (11). These ZF enzyme isoforms are differentially expressed in a tissue-specific manner, suggesting the possibility of creating a tool to study HSV tissuespecific tropism, whose study is hampered by the lack of available convenient tools. Our previous preliminary studies suggested that ZF 3-OST may mediate HSV entry (15). In this study, we investigated the ability of ZF 3-OST-1, -5, -6, and -7 isoforms, comparatively to their human analogue, to facilitate HSV-1 entry and cell-cell fusion. Our previous studies have shown that ZF-encoded 3-OST isoforms (3-OST-2, -3, and -4) allow HSV-1 entry into host cells (14,16,17). Here, we provide a comprehensive analysis of the differential abilities of the remaining ZF 3-OST isoforms to mediate HSV-1 entry and propose a unique model for future studies of HSV-1 tropism using ZF as a convenient tool.Analysis and cloning of zebrafish-encoded 3-OST enzymes. To characterize ZF 3-OST isoforms relative to their human counterparts, we first performed an amino acid sequence alignment of the ZF-encoded 3-OST enzymes to the previously characterized human 3-OST-3A and 3-OST-3B isoforms (2, 11). Interestingly, we found that the amino acid sequences of the ZF 3-OST enzymes show various degrees of homology to the human 3-OST-3 isoforms (Fig. 1). Comparing the conservation of the catalytic residues of the enzymes characterized for human 3-OST-3, we found that ZF enzymes 3-OST-2, -3, -4, and -6 show 100% conservation of the catalytic residues; these were designated group I members ( Fig. 1A and B). The other isoforms (3-OST-1, -5, and...

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Initial Contact: The First Steps in Herpesvirus Entry

Azab

Osterrieder

2017

Advances in Anatomy, Embryology and Cell Biology

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The entry process of herpesviruses into host cells is complex and highly variable. It involves a sequence of well-orchestrated events that begin with virus attachment to glycan-containing proteinaceous structures on the cell surface. This initial contact tethers virus particles to the cell surface and results in a cascade of molecular interactions, including the tight interaction of viral envelope glycoproteins to specific cell receptors. These interactions trigger intracellular signaling and finally virus penetration after fusion of the viral envelope with cellular membranes. Based on the engaged cellular receptors and co-receptors, and the subsequent signaling cascades, the entry pathway will be decided on the spot. A number of viral glycoproteins and many cellular receptors and molecules have been identified as players in one or several of these events during virus entry. This chapter will review viral glycoproteins, cellular receptors and signaling cascades associated with the very first interactions of herpesviruses with their target cells.

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Zebrafish encoded 3-O-sulfotransferase-2 generated heparan sulfate serves as a receptor during HSV-1 entry and spread

Cited by 11 publications

References 29 publications

Zebrafish: Modeling for Herpes Simplex Virus Infections

Zebrafish: Modeling for Herpes Simplex Virus Infections

Comprehensive Analysis of Herpes Simplex Virus 1 (HSV-1) Entry Mediated by Zebrafish 3- O -Sulfotransferase Isoforms: Implications for the Development of a Zebrafish Model of HSV-1 Infection

Initial Contact: The First Steps in Herpesvirus Entry

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