Characterization of the Host Response to Pichinde Virus Infection in the Syrian Golden Hamster by Species-Specific Kinome Analysis

The Syrian golden hamster has been increasingly used to study viral hemorrhagic fever (VHF) pathogenesis and countermeasure efficacy. As VHFs are a global health concern, well-characterized animal models are essential for both the development of therapeutics and vaccines as well as for increasing our understanding of the molecular events that underlie viral pathogenesis. However, the paucity of reagents or platforms that are available for studying hamsters at a molecular level limits the ability to extract biological information from this important animal model. As such, there is a need to develop platforms/technologies for characterizing host responses of hamsters at a molecular level. To this end, we developed hamster-specific kinome peptide arrays to characterize the molecular host response of the Syrian golden hamster. After validating the functionality of the arrays using immune agonists of defined signaling mechanisms (lipopolysaccharide (LPS) and tumor necrosis factor (TNF)-α), we characterized the host response in a hamster model of VHF based on Pichinde virus (PICV 1The abbreviations used are:PICVPichinde virusBHK-21baby hamster kidneyICAM-1intracellular adhesion moleculeILinterleukinIPAIngenuity Pathway AnalysisJNKc-Jun N-terminal kinaseLASVLassa virusLPSlipopolysaccharideNF-κBnuclear factor kappa-light-chain-enhancer of activated B cellsORAover-representation analysisTLRToll-like receptorTNFtumor necrosis factorVCAM-1vascular cell adhesion molecule 1VEGFvascular endothelial growth factorVHFviral hemorrhagic fever.) infection by performing temporal kinome analysis of lung tissue. Our analysis revealed key roles for vascular endothelial growth factor (VEGF), interleukin (IL) responses, nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) signaling, and Toll-like receptor (TLR) signaling in the response to PICV infection. These findings were validated through phosphorylation-specific Western blot analysis. Overall, we have demonstrated that hamster-specific kinome arrays are a robust tool for characterizing the species-specific molecular host response in a VHF model. Further, our results provide key insights into the hamster host response to PICV infection and will inform future studies with high-consequence VHF pathogens. The Syrian golden hamster has been increasingly used to study viral hemorrhagic fever (VHF) pathogenesis and countermeasure efficacy. As VHFs are a global health concern, well-characterized animal models are essential for both the development of therapeutics and vaccines as well as for increasing our understanding of the molecular events that underlie viral pathogenesis. However, the paucity of reagents or platforms that are available for studying hamsters at a molecular level limits the ability to extract biological information from this important animal model. As such, there is a need to develop platforms/technologies for characterizing host responses of hamsters at a molecular level. To this end, we developed hamster-specific kinome peptide arrays to characterize the molecular host response of the Syrian golden hamster. After validating the functionality of the arrays using immune agonists of defined signaling mechanisms (lipopolysaccharide (LPS) and tumor necrosis factor (TNF)-α), we characterized the host response in a hamster model of VHF based on Pichinde virus (PICV 1The abbreviations used are:PICVPichinde virusBHK-21baby hamster kidneyICAM-1intracellular adhesion moleculeILinterleukinIPAIngenuity Pathway AnalysisJNKc-Jun N-terminal kinaseLASVLassa virusLPSlipopolysaccharideNF-κBnuclear factor kappa-light-chain-enhancer of activated B cellsORAover-representation analysisTLRToll-like receptorTNFtumor necrosis factorVCAM-1vascular cell adhesion molecule 1VEGFvascular endothelial growth factorVHFviral hemorrhagic fever.) infection by performing temporal kinome analysis of lung tissue. Our analysis revealed key roles for vascular endothelial growth factor (VEGF), interleukin (IL) responses, nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) signaling, and Toll-like receptor (TLR) signaling in the response to PICV infection. These findings were validated through phosphorylation-specific Western blot analysis. Overall, we have demonstrated that hamster-specific kinome arrays are a robust tool for characterizing the species-specific molecular host response in a VHF model. Further, our results provide key insights into the hamster host response to PICV infection and will inform future studies with high-consequence VHF pathogens. Pichinde virus baby hamster kidney intracellular adhesion molecule interleukin Ingenuity Pathway Analysis c-Jun N-terminal kinase Lassa virus lipopolysaccharide nuclear factor kappa-light-chain-enhancer of activated B cells over-representation analysis Toll-like receptor tumor necrosis factor vascular cell adhesion molecule 1 vascular endothelial growth factor viral hemorrhagic fever. Viruses of the Arenaviridae family cause persistent and asymptomatic infections of rodents throughout the world (1Albariño C.G. Posik D.M. Ghiringhelli P.D. Lozano M.E. Romanowski V. Arenavirus phylogeny: a new insight.Virus Genes. 1998; 16: 39-46Crossref PubMed Scopus (22) Google Scholar). However, infection with select members of the Arenaviridae can result in viral hemorrhagic fever (VHF) in humans and non-human primates. Lassa virus (LASV), a Risk Group 4 Select Agent, is responsible for severe febrile illness in 15–20% of those infected (2McCormick J.B. Clinical, epidemiologic, and therapeutic aspects of Lassa fever.Med. Microbiol. Immunol. 1986; 175: 153-155Crossref PubMed Scopus (49) Google Scholar, 3Richmond J.K. Baglole D.J. Lassa fever: Epidemiology, clinical features, and social consequences.BMJ. 2003; 327: 1271-1275Crossref PubMed Scopus (233) Google Scholar). While pathophysiological studies for LASV are limited to high-containment laboratories, Pichinde virus (PICV), a South American arenavirus, has been investigated as a potential surrogate for LASV and can be handled under biosafety level 2 conditions (4Jahrling P.B. Hesse R.A. Rhoderick J.B. Elwell M.A. Moe J.B. Pathogenesis of a Pichinde virus strain adapted to produce lethal infections in guinea pigs.Infect. Immun. 1981; 32: 872-880Crossref PubMed Google Scholar). Further, the histopathological effects of PICV infection of guinea pigs and hamsters are similar to those induced by LASV in humans (4Jahrling P.B. Hesse R.A. Rhoderick J.B. Elwell M.A. Moe J.B. Pathogenesis of a Pichinde virus strain adapted to produce lethal infections in guinea pigs.Infect. Immun. 1981; 32: 872-880Crossref PubMed Google Scholar, 5Lukashevich I.S. The search for animal models for Lassa fever vaccine development.Expert Rev. Vacc. 2013; 12: 71-86Crossref PubMed Scopus (32) Google Scholar, 6Gowen B.B. Julander J.G. London N.R. Wong M.H. Larson D. Morrey J.D. Li D.Y. Bray M. Assessing changes in vascular permeability in a hamster model of viral hemorrhagic fever.Virol. J. 2010; 7: 240Crossref PubMed Scopus (33) Google Scholar). Thus, PICV is attractive as a surrogate virus for modeling the hemorrhagic disease process of LASV. Recently, there has been interest in the use of the Syrian golden hamster as a model for high-consequence pathogens (7Ebihara H. Zivcec M. Gardner D. Falzarano D. LaCasse D. H. Syrian golden hamster model hemorrhagic 2013; PubMed Scopus Google Scholar, V. D. H. of the Syrian hamster as a new model of virus disease and viral hemorrhagic PubMed Scopus Google Scholar, M. D. H. H. of to immune responses in the Syrian golden hamster Immun. PubMed Scopus Google Scholar). to and guinea hamsters the effects of VHF infections in non-human with to has been that VHF infection studies in hamsters will those of and guinea pigs (7Ebihara H. Zivcec M. Gardner D. Falzarano D. LaCasse D. H. Syrian golden hamster model hemorrhagic 2013; PubMed Scopus Google Scholar, V. D. H. of the Syrian hamster as a new model of virus disease and viral hemorrhagic PubMed Scopus Google Scholar, M. D. H. H. of to immune responses in the Syrian golden hamster Immun. PubMed Scopus Google Scholar). However, are limited by the of available hamster-specific molecular reagents M. D. H. H. of to immune responses in the Syrian golden hamster Immun. PubMed Scopus Google Scholar). Thus, there is a need for that can characterize the molecular host response of the potential to global health by high-consequence there is limited information the of host cell signaling in the molecular pathogenesis of pathogens. As the molecular events with disease are essential to understanding pathogenesis and is important to the changes that infection. the of host responses, of host is the well-characterized with to cell signaling as well as the host cells for the PubMed Scopus Google Scholar). While are host responses at the level of host cell a events provide the host with a to to changes through the of cell signaling as with changes in or Further, there is increasing interest in the use of kinome for the of therapeutic and D. J. as for and host cell PubMed Scopus Google Scholar). are a for the development of therapeutics with kinase for the of by the and D. H. with kinase PubMed Scopus Google Scholar). Further, the of kinase as therapeutics for disease a of on the of D. H. with kinase PubMed Scopus Google Scholar, The of and PubMed Scopus Google Scholar). Recently, there has been for the of signaling events in the host response to pathogens J. V. D. D. H. P.B. virus growth signaling and of in PubMed Scopus Google Scholar, J. P.B. virus infection host cell signaling responses as to PubMed Scopus (32) Google Scholar, Li Toll-like receptor signaling in potential therapeutic Immun. 2013; PubMed Scopus Google Scholar, J. the kinome for and therapeutic arrays for global and for clinical of Scholar). of the Arenaviridae are to host immune signaling of activated with Pichinde virus pathogenesis by using PubMed Scopus Google Scholar, in and by infection of in and in PubMed Scopus Google Scholar). As immune responses are through signaling is essential to the host response at this level. have to characterize have been limited by the of of species-specific reagents and the of information the molecular responses of activated with Pichinde virus pathogenesis by using PubMed Scopus Google Scholar). Thus, there has been into the molecular response of hamster to high-consequence pathogens I.S. The search for animal models for Lassa fever vaccine development.Expert Rev. Vacc. 2013; 12: 71-86Crossref PubMed Scopus (32) Google Scholar, 6Gowen B.B. Julander J.G. London N.R. Wong M.H. Larson D. Morrey J.D. Li D.Y. Bray M. Assessing changes in vascular permeability in a hamster model of viral hemorrhagic fever.Virol. J. 2010; 7: 240Crossref PubMed Scopus (33) Google Scholar). we a analysis for characterizing hamster-specific kinome responses that our we have demonstrated the of hamster-specific kinome arrays for species-specific host responses to immune agonists of signaling lipopolysaccharide (LPS) and tumor necrosis factor we have characterized temporal host responses in the of hamsters and demonstrated for the that vascular endothelial growth factor (VEGF), interleukin (IL) responses, nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) signaling, and Toll-like receptor (TLR) signaling of the host response to PICV infection in the of the Syrian golden hamster. Further, we demonstrated that the of and cell signaling with of cell adhesion molecule events were to disease in as with our a for the global analysis of host responses of the Syrian golden hamster to and the potential to use from this to characterize the of signaling for therapeutic strain by The virus through hamsters and the from in and by of cells were in with cells were in and were at in a and were used in this study for the of changes in in hamster lung tissue. used as a for were based of the were on were in and cells were for 1 with by of a and cells were for were with and with with hamster kidney cells were for in the to at a cell of 1 or were to the cells for 4 and were and to kinome Syrian golden hamsters were infected by with of strain were in of on and that a viral at in and at of hamster used in this study with by the and and under lung and in or for 1 1 were using the for using and by at for After the were to a The of the hamster based on used by our that with in the and The on this were from a of biological with a on in immune As this in this we a hamster-specific of this peptide on the used as a the hamster As the Syrian hamster has been we a hamster of the Syrian hamster that were available in the with the available from the hamster. 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PubMed Scopus Google Scholar). results demonstrated the ability of the hamster-specific kinome arrays to the of hamster immune responses at the level of cell signaling over-representation analysis of kinome from and signaling signaling receptor signaling signaling signaling through signaling signaling signaling and signaling receptor signaling of in B by cell receptor signaling signaling by and of signaling by signaling signaling family signaling signaling receptor signaling receptor signaling signaling signaling signaling of the family of and by activated signaling cell receptor signaling signaling signaling in a new the of the we the hamster-specific kinome arrays to characterize the temporal host response to PICV infection in in Syrian golden hamsters the molecular pathogenesis of PICV in hamster host of PICV infection in hamsters have demonstrated that vascular permeability on in the lung of hamsters (4Jahrling P.B. Hesse R.A. Rhoderick J.B. Elwell M.A. Moe J.B. Pathogenesis of a Pichinde virus strain adapted to produce lethal infections in guinea pigs.Infect. Immun. 1981; 32: 872-880Crossref PubMed Google Scholar, 5Lukashevich I.S. The search for animal models for Lassa fever vaccine development.Expert Rev. Vacc. 2013; 12: 71-86Crossref PubMed Scopus (32) Google Scholar, 6Gowen B.B. Julander J.G. London N.R. Wong M.H. Larson D. Morrey J.D. Li D.Y. Bray M. Assessing changes in vascular permeability in a hamster model of viral hemorrhagic fever.Virol. J. 2010; 7: 240Crossref PubMed Scopus (33) Google Scholar). However, the molecular events this have been Thus, we characterized the hamster host response in lung in and hamsters and have demonstrated that of hamsters results in disease that is characterized by the of virus in and by on PICV by of cells and of the of vascular and virus by and the of disease B.B. Julander J.G. London N.R. Wong M.H. Larson D. Morrey J.D. Li D.Y. Bray M. 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J. 2010; 7: 240Crossref PubMed Scopus (33) Google Scholar). the of and is to be with the of endothelial cells in infection H. of kinase is to or effects of on and permeability in endothelial 2010; PubMed Scopus Google Scholar). the of in lung is in with a of PICV in hamsters that in at infection B.B. Julander J.G. London N.R. Wong M.H. Larson D. Morrey J.D. Li D.Y. Bray M. Assessing changes in vascular permeability in a hamster model of viral hemorrhagic fever.Virol. J. 2010; 7: 240Crossref PubMed Scopus (33) Google Scholar). Further, the of has been with vascular permeability in the endothelial growth factor vascular permeability is by adhesion J. PubMed Scopus Google Scholar). provide for the of to be with the of adhesion in PICV infection. As the for humans and hamsters is important that molecular as kinome analysis species-specific have demonstrated that the with events that in our kinome analysis with those using blot analysis. 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