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• W2778585524 abstract "Infections by ranaviruses such as Frog virus 3 (Fv3), are significantly contributing to worldwide amphibian population declines. Notably, amphibian macrophages (Mϕs) are important to both the Fv3 infection strategies and the immune defense against this pathogen. However, the mechanisms underlying amphibian Mϕ Fv3 susceptibility and resistance remain unknown. Mϕ differentiation is mediated by signaling through the colony-stimulating factor-1 receptor (CSF-1R) which is now known to be bound not only by CSF-1, but also by the unrelated interleukin-34 (IL-34) cytokine. Pertinently, amphibian (Xenopus laevis) Mϕs differentiated by CSF-1 and IL-34 are highly susceptible and resistant to Fv3, respectively. Accordingly, in the present work, we elucidate the facets of this Mϕ Fv3 susceptibility and resistance. Because cellular resistance to viral replication is marked by expression of antiviral restriction factors, it was intuitive to find that IL-34-Mϕs possess significantly greater mRNA levels of select restriction factor genes than CSF-1-Mϕs. Xenopodinae amphibians have highly expanded repertoires of antiviral interferon (IFN) cytokine gene families, and our results indicated that in comparison with the X. laevis CSF-1-Mϕs, the IL-34-Mϕs express substantially greater transcripts of representative IFN genes, belonging to distinct gene family clades, as well as their cognate receptor genes. Finally, we demonstrate that IL-34-Mϕ–conditioned supernatants confer IFN-mediated anti-Fv3 protection to the virally susceptible X. laevis kidney (A6) cell line. Together, this work underlines the differentiation pathways leading to Fv3-susceptible and -resistant amphibian Mϕ populations and defines the molecular mechanisms responsible for these differences. Infections by ranaviruses such as Frog virus 3 (Fv3), are significantly contributing to worldwide amphibian population declines. Notably, amphibian macrophages (Mϕs) are important to both the Fv3 infection strategies and the immune defense against this pathogen. However, the mechanisms underlying amphibian Mϕ Fv3 susceptibility and resistance remain unknown. Mϕ differentiation is mediated by signaling through the colony-stimulating factor-1 receptor (CSF-1R) which is now known to be bound not only by CSF-1, but also by the unrelated interleukin-34 (IL-34) cytokine. Pertinently, amphibian (Xenopus laevis) Mϕs differentiated by CSF-1 and IL-34 are highly susceptible and resistant to Fv3, respectively. Accordingly, in the present work, we elucidate the facets of this Mϕ Fv3 susceptibility and resistance. Because cellular resistance to viral replication is marked by expression of antiviral restriction factors, it was intuitive to find that IL-34-Mϕs possess significantly greater mRNA levels of select restriction factor genes than CSF-1-Mϕs. Xenopodinae amphibians have highly expanded repertoires of antiviral interferon (IFN) cytokine gene families, and our results indicated that in comparison with the X. laevis CSF-1-Mϕs, the IL-34-Mϕs express substantially greater transcripts of representative IFN genes, belonging to distinct gene family clades, as well as their cognate receptor genes. Finally, we demonstrate that IL-34-Mϕ–conditioned supernatants confer IFN-mediated anti-Fv3 protection to the virally susceptible X. laevis kidney (A6) cell line. Together, this work underlines the differentiation pathways leading to Fv3-susceptible and -resistant amphibian Mϕ populations and defines the molecular mechanisms responsible for these differences. Amphibian population die-offs resulting from the Frog virus 3 (Fv3) 3The abbreviations used are: Fv3frog virus 3CSF-1colony-stimulating factor-1IFNinterferonILinterleukinMϕmacrophageBarbaricitinibmomorpholinoMOImultiplicity of infectionqPCRquantitative PCR. ranavirus (family Iridoviridae) infections are significantly contributing to the worldwide amphibian declines (1Carey C. Cohen N. Rollins-Smith L. Amphibian declines: an immunological perspective.Dev. Comp. Immunol. 1999; 23 (10512457): 459-47210.1016/S0145-305X(99)00028-2Crossref PubMed Scopus (388) Google Scholar, 2Daszak P. Berger L. Cunningham A.A. Hyatt A.D. Green D.E. Speare R. Emerging infectious diseases and amphibian population declines.Emerg. Infect. Dis. 1999; 5 (10603206): 735-74810.3201/eid0506.990601Crossref PubMed Scopus (757) Google Scholar). Although much remains to be learned regarding the facets of amphibian immunity against these viral agents, macrophages (Mϕs) are now known to be integral to both the Fv3 infection strategy and to the amphibian host immune responses against this pathogen (3Grayfer L. Andino Fde J. Chen G. Chinchar G.V. Robert J. Immune evasion strategies of ranaviruses and innate immune responses to these emerging pathogens.Viruses. 2012; 4 (22852041): 1075-109210.3390/v4071075Crossref PubMed Scopus (47) Google Scholar, 4Grayfer L. Robert J. Amphibian macrophage development and antiviral defenses.Dev. Comp. Immunol. 2016; 58 (26705159): 60-6710.1016/j.dci.2015.12.008Crossref PubMed Scopus (29) Google Scholar). Indeed, the capacity of the anuran (frogs and toads) amphibian Xenopus laevis to mount effective anti-Fv3 responses depends on appropriate Mϕ differentiation (5Grayfer L. Robert J. Divergent antiviral roles of amphibian (Xenopus laevis) macrophages elicited by colony-stimulating factor-1 and interleukin-34.J. Leukoc. Biol. 2014; 96 (25190077): 1143-115310.1189/jlb.4A0614-295RCrossref PubMed Scopus (38) Google Scholar, 6Grayfer L. Robert J. Distinct functional roles of amphibian (Xenopus laevis) colony-stimulating factor-1- and interleukin-34-derived macrophages.J. Leukoc. Biol. 2015; 98 (26136505): 641-64910.1189/jlb.4AB0315-117RRCrossref PubMed Scopus (37) Google Scholar). As Mϕ differentiation depends on the activation of the colony-stimulating factor-1 (CSF-1) receptor, it is compelling that in addition to CSF-1 (7Wang T. Hanington P.C. Belosevic M. Secombes C.J. Two macrophage colony-stimulating factor genes exist in fish that differ in gene organization and are differentially expressed.J. Immunol. 2008; 181 (18714003): 3310-332210.4049/jimmunol.181.5.3310Crossref PubMed Scopus (85) Google Scholar8Pixley F.J. Stanley E.R. CSF-1 regulation of the wandering macrophage: complexity in action.Trends Cell Biol. 2004; 14 (15519852): 628-63810.1016/j.tcb.2004.09.016Abstract Full Text Full Text PDF PubMed Scopus (610) Google Scholar, 9Hanington P.C. Wang T. Secombes C.J. Belosevic M. Growth factors of lower vertebrates: characterization of goldfish (Carassius auratus L.) macrophage colony-stimulating factor-1.J. Biol. Chem. 2007; 282 (17827160): 31865-3187210.1074/jbc.M706278200Abstract Full Text Full Text PDF PubMed Scopus (45) Google Scholar10Garceau V. Smith J. Paton I.R. Davey M. Fares M.A. Sester D.P. Burt D.W. Hume D.A. Pivotal advance: avian colony-stimulating factor 1 (CSF-1), interleukin-34 (IL-34), and CSF-1 receptor genes and gene products.J. Leukoc. Biol. 2010; 87 (20051473): 753-76410.1189/jlb.0909624Crossref PubMed Scopus (135) Google Scholar), this receptor may be engaged by the unrelated interleukin-34 (IL-34) (11Belosevic M. Hanington P.C. Barreda D.R. Development of goldfish macrophages in vitro.Fish Shellfish Immunol. 2006; 20 (15936214): 152-17110.1016/j.fsi.2004.10.010Crossref PubMed Scopus (40) Google Scholar12Droin N. Solary E. Editorial: CSF1R, CSF-1, and IL-34, a “menage a trois” conserved across vertebrates.J. Leukoc. Biol. 2010; 87 (20430779): 745-74710.1189/jlb.1209780Crossref PubMed Scopus (49) Google Scholar, 13Lin H. Lee E. Hestir K. Leo C. Huang M. Bosch E. Halenbeck R. Wu G. Zhou A. Behrens D. Hollenbaugh D. Linnemann T. Qin M. Wong J. Chu K. et al.Discovery of a cytokine and its receptor by functional screening of the extracellular proteome.Science. 2008; 320 (18467591): 807-81110.1126/science.1154370Crossref PubMed Scopus (556) Google Scholar14Wei S. Nandi S. Chitu V. Yeung Y.G. Yu W. Huang M. Williams L.T. Lin H. Stanley E.R. Functional overlap but differential expression of CSF-1 and IL-34 in their CSF-1 receptor-mediated regulation of myeloid cells.J. Leukoc. Biol. 2010; 88 (20504948): 495-50510.1189/jlb.1209822Crossref PubMed Scopus (276) Google Scholar), presumably contributing to the functional heterogeneity seen across vertebrate Mϕs. Our recent findings suggest that whereas the X. laevis Mϕs generated by CSF-1 render animals more susceptible to Fv3, the IL-34-derived Mϕ possess potent antiviral capacities and confer frog resistance to this viral pathogen (5Grayfer L. Robert J. Divergent antiviral roles of amphibian (Xenopus laevis) macrophages elicited by colony-stimulating factor-1 and interleukin-34.J. Leukoc. Biol. 2014; 96 (25190077): 1143-115310.1189/jlb.4A0614-295RCrossref PubMed Scopus (38) Google Scholar, 6Grayfer L. Robert J. Distinct functional roles of amphibian (Xenopus laevis) colony-stimulating factor-1- and interleukin-34-derived macrophages.J. Leukoc. Biol. 2015; 98 (26136505): 641-64910.1189/jlb.4AB0315-117RRCrossref PubMed Scopus (37) Google Scholar). However, the molecular mechanisms conferring CSF-1-Mϕ susceptibility and IL-34-Mϕ resistance to Fv3 remain to be fully defined. frog virus 3 colony-stimulating factor-1 interferon interleukin macrophage baricitinib morpholino multiplicity of infection quantitative PCR. Because antiviral interferon (IFN) cytokines represent a major pillar of vertebrate antiviral defenses (7Wang T. Hanington P.C. Belosevic M. Secombes C.J. Two macrophage colony-stimulating factor genes exist in fish that differ in gene organization and are differentially expressed.J. Immunol. 2008; 181 (18714003): 3310-332210.4049/jimmunol.181.5.3310Crossref PubMed Scopus (85) Google Scholar, 9Hanington P.C. Wang T. Secombes C.J. Belosevic M. Growth factors of lower vertebrates: characterization of goldfish (Carassius auratus L.) macrophage colony-stimulating factor-1.J. Biol. Chem. 2007; 282 (17827160): 31865-3187210.1074/jbc.M706278200Abstract Full Text Full Text PDF PubMed Scopus (45) Google Scholar, 10Garceau V. Smith J. Paton I.R. Davey M. Fares M.A. Sester D.P. Burt D.W. Hume D.A. Pivotal advance: avian colony-stimulating factor 1 (CSF-1), interleukin-34 (IL-34), and CSF-1 receptor genes and gene products.J. Leukoc. Biol. 2010; 87 (20051473): 753-76410.1189/jlb.0909624Crossref PubMed Scopus (135) Google Scholar11Belosevic M. Hanington P.C. Barreda D.R. Development of goldfish macrophages in vitro.Fish Shellfish Immunol. 2006; 20 (15936214): 152-17110.1016/j.fsi.2004.10.010Crossref PubMed Scopus (40) Google Scholar), it is particularly notable that amphibians hold a key stage in the evolution of these soluble effectors. Mammals, birds, and reptiles possess three types of IFNs, type I, II, and III IFNs (15Sadler A.J. Williams B.R. Interferon-inducible antiviral effectors.Nat. Rev. Immunol. 2008; 8 (18575461): 559-56810.1038/nri2314Crossref PubMed Scopus (1584) Google Scholar), of which the type II IFNs mediate a variety of immunological roles, whereas the type I and type III IFNs predominantly participate in antiviral immunity (16Zou J. Secombes C.J. Teleost fish interferons and their role in immunity.Dev. Comp. Immunol. 2011; 35 (21781984): 1376-138710.1016/j.dci.2011.07.001Crossref PubMed Scopus (301) Google Scholar). The type I IFNs of these higher vertebrates are encoded by intronless genes, whereas their type III IFNs (also known as IFNλs/IFNLs) are encoded by five exon/four intron gene transcripts (16Zou J. Secombes C.J. Teleost fish interferons and their role in immunity.Dev. Comp. Immunol. 2011; 35 (21781984): 1376-138710.1016/j.dci.2011.07.001Crossref PubMed Scopus (301) Google Scholar). Conversely, teleost and cartilaginous fish do not appear to possess type III IFNs and encode type I IFNs with five-exon, four-intron organization (16Zou J. Secombes C.J. Teleost fish interferons and their role in immunity.Dev. Comp. Immunol. 2011; 35 (21781984): 1376-138710.1016/j.dci.2011.07.001Crossref PubMed Scopus (301) Google Scholar). Intriguingly, Xenopodinae amphibians possess type I IFN genes with the five-exon, four-intron intron gene organization of the fish counterparts; intronless type I IFNs akin to those seen in higher vertebrates; and intronless and five exon/four intron-containing type III IFN genes (17Sang Y. Liu Q. Lee J. Ma W. McVey D.S. Blecha F. Expansion of amphibian intronless interferons revises the paradigm for interferon evolution and functional diversity.Sci. Rep. 2016; 6 (27356970): 2907210.1038/srep29072Crossref PubMed Scopus (39) Google Scholar, 18Gan Z. Chen S.N. Huang B. Hou J. Nie P. Intronless and intron-containing type I IFN genes coexist in amphibian Xenopus tropicalis: insights into the origin and evolution of type I IFNs in vertebrates.Dev. Comp. Immunol. 2017; 67 (27780747): 166-17610.1016/j.dci.2016.10.007Crossref PubMed Scopus (37) Google Scholar). Most notably, we recently demonstrated that X. laevis intron-containing type I and type III IFNs play important roles in anti-Fv3 responses (19Grayfer L. De Jesús Andino F. Robert J. The amphibian (Xenopus laevis) type I interferon response to frog virus 3: new insight into ranavirus pathogenicity.J. Virol. 2014; 88 (24623410): 5766-577710.1128/JVI.00223-14Crossref PubMed Scopus (55) Google Scholar, 20Grayfer L. De Jesús Andino F. Robert J. Prominent amphibian (Xenopus laevis) tadpole type III interferon response to the frog virus 3 ranavirus.J. Virol. 2015; 89 (25717104): 5072-508210.1128/JVI.00051-15Crossref PubMed Scopus (39) Google Scholar21Wendel E.S. Yaparla A. Koubourli D.V. Grayfer L. Amphibian (Xenopus laevis) tadpoles and adult frogs mount distinct interferon responses to the Frog Virus 3 ranavirus.Virology. 2017; 503 (28081430): 12-2010.1016/j.virol.2017.01.001Crossref PubMed Scopus (24) Google Scholar). Aside from antiviral IFN responses, the capacity of distinct cell types to support or minimize the replication of invading viral pathogens often correlates with their respective gene expression of antiviral restriction factors (24Badia R. Angulo G. Riveira-Muñoz E. Pujantell M. Puig T. Ramirez C. Torres-Torronteras J. Marti R. Pauls E. Clotet B. Ballana E. Esté J.A. Inhibition of herpes simplex virus type 1 by the CDK6 inhibitor PD-0332991 (palbociclib) through the control of SAMHD1.J. Antimicrob. Chemother. 2016; 71 (26542306): 387-39410.1093/jac/dkv363Crossref PubMed Scopus (31) Google Scholar25Ballana E. Esté J.A. SAMHD1: at the crossroads of cell proliferation, immune responses, and virus restriction.Trends Microbiol. 2015; 23 (26439297): 680-69210.1016/j.tim.2015.08.002Abstract Full Text Full Text PDF PubMed Scopus (62) Google Scholar, 26Lang F. Li X. Vladimirova O. Hu B. Chen G. Xiao Y. Singh V. Lu D. Li L. Han H. Wickramasinghe J.M. Smith S.T. Zheng C. Li Q. Lieberman P.M. et al.CTCF interacts with the lytic HSV-1 genome to promote viral transcription.Sci. Rep. 2017; 7 (28045091): 3986110.1038/srep39861Crossref PubMed Scopus (28) Google Scholar27Li D.J. Verma D. Mosbruger T. Swaminathan S. CTCF and Rad21 act as host cell restriction factors for Kaposi's sarcoma-associated herpesvirus (KSHV) lytic replication by modulating viral gene transcription.PLoS Pathog. 2014; 10 (24415941): e100388010.1371/journal.ppat.1003880Crossref PubMed Scopus (51) Google Scholar). Collectively, these cellular proteins present enormous structural and functional diversities and provide the first cellular lines of defense against viral infections by targeting and ablating distinct viral replication mechanisms (24Badia R. Angulo G. Riveira-Muñoz E. Pujantell M. Puig T. Ramirez C. Torres-Torronteras J. Marti R. Pauls E. Clotet B. Ballana E. Esté J.A. Inhibition of herpes simplex virus type 1 by the CDK6 inhibitor PD-0332991 (palbociclib) through the control of SAMHD1.J. Antimicrob. Chemother. 2016; 71 (26542306): 387-39410.1093/jac/dkv363Crossref PubMed Scopus (31) Google Scholar25Ballana E. Esté J.A. SAMHD1: at the crossroads of cell proliferation, immune responses, and virus restriction.Trends Microbiol. 2015; 23 (26439297): 680-69210.1016/j.tim.2015.08.002Abstract Full Text Full Text PDF PubMed Scopus (62) Google Scholar, 26Lang F. Li X. Vladimirova O. Hu B. Chen G. Xiao Y. Singh V. Lu D. Li L. Han H. Wickramasinghe J.M. Smith S.T. Zheng C. Li Q. Lieberman P.M. et al.CTCF interacts with the lytic HSV-1 genome to promote viral transcription.Sci. Rep. 2017; 7 (28045091): 3986110.1038/srep39861Crossref PubMed Scopus (28) Google Scholar27Li D.J. Verma D. Mosbruger T. Swaminathan S. CTCF and Rad21 act as host cell restriction factors for Kaposi's sarcoma-associated herpesvirus (KSHV) lytic replication by modulating viral gene transcription.PLoS Pathog. 2014; 10 (24415941): e100388010.1371/journal.ppat.1003880Crossref PubMed Scopus (51) Google Scholar). Whereas the expression of some of these restriction factors is enhanced by IFNs, others are constitutively expressed (24Badia R. Angulo G. Riveira-Muñoz E. Pujantell M. Puig T. Ramirez C. Torres-Torronteras J. Marti R. Pauls E. Clotet B. Ballana E. Esté J.A. Inhibition of herpes simplex virus type 1 by the CDK6 inhibitor PD-0332991 (palbociclib) through the control of SAMHD1.J. Antimicrob. Chemother. 2016; 71 (26542306): 387-39410.1093/jac/dkv363Crossref PubMed Scopus (31) Google Scholar25Ballana E. Esté J.A. SAMHD1: at the crossroads of cell proliferation, immune responses, and virus restriction.Trends Microbiol. 2015; 23 (26439297): 680-69210.1016/j.tim.2015.08.002Abstract Full Text Full Text PDF PubMed Scopus (62) Google Scholar, 26Lang F. Li X. Vladimirova O. Hu B. Chen G. Xiao Y. Singh V. Lu D. Li L. Han H. Wickramasinghe J.M. Smith S.T. Zheng C. Li Q. Lieberman P.M. et al.CTCF interacts with the lytic HSV-1 genome to promote viral transcription.Sci. Rep. 2017; 7 (28045091): 3986110.1038/srep39861Crossref PubMed Scopus (28) Google Scholar27Li D.J. Verma D. Mosbruger T. Swaminathan S. CTCF and Rad21 act as host cell restriction factors for Kaposi's sarcoma-associated herpesvirus (KSHV) lytic replication by modulating viral gene transcription.PLoS Pathog. 2014; 10 (24415941): e100388010.1371/journal.ppat.1003880Crossref PubMed Scopus (51) Google Scholar). To delineate the mechanisms responsible for IL-34–derived Mϕ antiviral resistance, and CSF-1-differentiated Mϕ susceptibility to Fv3, we compared these cell populations for their gene expression of select intron-containing and intronless type I and type III IFNs as well as the respective IFN receptor genes. Additionally, we examined the restriction factor gene expression levels of these Mϕ populations and compared the ability of Fv3 to replicate within CSF- and IL-34–derived Mϕs. Moreover, we examined the ability of CSF-1-Mϕ– and IL-34-Mϕ–conditioned supernatants to restrict Fv3 growth in an otherwise highly Fv3-susceptible X. laevis kidney epithelial cell line (A6). We previously demonstrated that X. laevis Mϕs differentiated with IL-34 are resistant to Fv3 infection, whereas CSF-1-derived Mϕs are significantly more susceptible to this virus (5Grayfer L. Robert J. Divergent antiviral roles of amphibian (Xenopus laevis) macrophages elicited by colony-stimulating factor-1 and interleukin-34.J. Leukoc. Biol. 2014; 96 (25190077): 1143-115310.1189/jlb.4A0614-295RCrossref PubMed Scopus (38) Google Scholar, 6Grayfer L. Robert J. Distinct functional roles of amphibian (Xenopus laevis) colony-stimulating factor-1- and interleukin-34-derived macrophages.J. Leukoc. Biol. 2015; 98 (26136505): 641-64910.1189/jlb.4AB0315-117RRCrossref PubMed Scopus (37) Google Scholar). Accordingly, to examine whether CSF-1-Mϕs support greater Fv3 replication than IL-34-Mϕs, we differentiated IL-34- and CSF-1-Mϕs from X. laevis bone marrow cells, challenged them with Fv3, and assessed the viral loads and expression of Fv3 82R (immediate early, IE), Fv3 95R (delayed early, E), and Fv3 93L (late, L) genes in these respective Mϕ populations. As previously noted, CSF-1-Mϕs possessed significantly greater Fv3 loads than detected in the IL-34-Mϕs (Fig. 1A). Moreover, CSF-1-Mϕs possessed substantially greater magnitudes of Fv3-82R, -95R, and -93L gene expression than detected in IL-34-Mϕs (Fig. 1B). Of the examined Fv3 genes, 93L exhibited the greatest expression differences between CSF-1- and IL-34-Mϕ (Fig. 1B). Because our results indicated that IL-34-Mϕs are more restrictive to Fv3 infection while the expression of appropriate restriction factors is crucial to adequate cellular arrest of viral replication (24Badia R. Angulo G. Riveira-Muñoz E. Pujantell M. Puig T. Ramirez C. Torres-Torronteras J. Marti R. Pauls E. Clotet B. Ballana E. Esté J.A. Inhibition of herpes simplex virus type 1 by the CDK6 inhibitor PD-0332991 (palbociclib) through the control of SAMHD1.J. Antimicrob. Chemother. 2016; 71 (26542306): 387-39410.1093/jac/dkv363Crossref PubMed Scopus (31) Google Scholar25Ballana E. Esté J.A. SAMHD1: at the crossroads of cell proliferation, immune responses, and virus restriction.Trends Microbiol. 2015; 23 (26439297): 680-69210.1016/j.tim.2015.08.002Abstract Full Text Full Text PDF PubMed Scopus (62) Google Scholar, 26Lang F. Li X. Vladimirova O. Hu B. Chen G. Xiao Y. Singh V. Lu D. Li L. Han H. Wickramasinghe J.M. Smith S.T. Zheng C. Li Q. Lieberman P.M. et al.CTCF interacts with the lytic HSV-1 genome to promote viral transcription.Sci. Rep. 2017; 7 (28045091): 3986110.1038/srep39861Crossref PubMed Scopus (28) Google Scholar27Li D.J. Verma D. Mosbruger T. Swaminathan S. CTCF and Rad21 act as host cell restriction factors for Kaposi's sarcoma-associated herpesvirus (KSHV) lytic replication by modulating viral gene transcription.PLoS Pathog. 2014; 10 (24415941): e100388010.1371/journal.ppat.1003880Crossref PubMed Scopus (51) Google Scholar), we next examined whether IL-34-Mϕ resistance to Fv3 could be attributed to more robust expression of such restriction factors. In comparison with CSF-1-Mϕs, IL-34-Mϕs exhibited a significantly greater expression levels of the apobec2 (apolipoprotein B mRNA-editing enzyme-2) and trim28 (tripartite motif–containing 28) restriction factors (Fig. 2A), which are known to suppress viral replication (22Shi K. Carpenter M.A. Banerjee S. Shaban N.M. Kurahashi K. Salamango D.J. McCann J.L. Starrett G.J. Duffy J.V. Demir Ö. Amaro R.E. Harki D.A. Harris R.S. Aihara H. Structural basis for targeted DNA cytosine deamination and mutagenesis by APOBEC3A and APOBEC3B.Nat. Struct. Mol. Biol. 2017; 24 (27991903): 131-139Crossref PubMed Scopus (152) Google Scholar, 23Wolf D. Hug K. Goff S.P. TRIM28 mediates primer binding site-targeted silencing of Lys1,2 tRNA-utilizing retroviruses in embryonic cells.Proc. Natl. Acad. Sci. U.S.A. 2008; 105 (18713861): 12521-1252610.1073/pnas.0805540105Crossref PubMed Scopus (49) Google Scholar). Moreover, Fv3 is a dsDNA virus, and our result showed that IL-34-Mϕs also possessed more robust gene expression of samhd1 (SAM domain and HD domain-containing protein 1) and ctcf (CCCTC-binding factor) restriction factors, both of which are known to specifically target dsDNA viruses (24Badia R. Angulo G. Riveira-Muñoz E. Pujantell M. Puig T. Ramirez C. Torres-Torronteras J. Marti R. Pauls E. Clotet B. Ballana E. Esté J.A. Inhibition of herpes simplex virus type 1 by the CDK6 inhibitor PD-0332991 (palbociclib) through the control of SAMHD1.J. Antimicrob. Chemother. 2016; 71 (26542306): 387-39410.1093/jac/dkv363Crossref PubMed Scopus (31) Google Scholar25Ballana E. Esté J.A. SAMHD1: at the crossroads of cell proliferation, immune responses, and virus restriction.Trends Microbiol. 2015; 23 (26439297): 680-69210.1016/j.tim.2015.08.002Abstract Full Text Full Text PDF PubMed Scopus (62) Google Scholar, 26Lang F. Li X. Vladimirova O. Hu B. Chen G. Xiao Y. Singh V. Lu D. Li L. Han H. Wickramasinghe J.M. Smith S.T. Zheng C. Li Q. Lieberman P.M. et al.CTCF interacts with the lytic HSV-1 genome to promote viral transcription.Sci. Rep. 2017; 7 (28045091): 3986110.1038/srep39861Crossref PubMed Scopus (28) Google Scholar27Li D.J. Verma D. Mosbruger T. Swaminathan S. CTCF and Rad21 act as host cell restriction factors for Kaposi's sarcoma-associated herpesvirus (KSHV) lytic replication by modulating viral gene transcription.PLoS Pathog. 2014; 10 (24415941): e100388010.1371/journal.ppat.1003880Crossref PubMed Scopus (51) Google Scholar) (Fig. 2A). By contrast, CSF-1- and IL-34-Mϕs had comparable mRNA levels of cyclophilin B (cypb) and rad21 (Fig. 2A). We showed previously that, like other vertebrate CSF-1 receptor ligands (28Dwyer A.R. Mouchemore K.A. Steer J.H. Sunderland A.J. Sampaio N.G. Greenland E.L. Joyce D.A. Pixley F.J. Src family kinase expression and subcellular localization in macrophages: implications for their role in CSF-1-induced macrophage migration.J. Leukoc. Biol. 2016; 100 (26747837): 163-17510.1189/jlb.2A0815-344RRCrossref PubMed Scopus (15) Google Scholar, 29Grayfer L. Hanington P.C. Belosevic M. Macrophage colony-stimulating factor (CSF-1) induces pro-inflammatory gene expression and enhances antimicrobial responses of goldfish (Carassius auratus L.) macrophages.Fish Shellfish Immunol. 2009; 26 (19130890): 406-41310.1016/j.fsi.2008.12.001Crossref PubMed Scopus (40) Google Scholar), the frog CSF-1 and IL-34 chemoattract Mϕ precursors and induce their functional differentiation (5Grayfer L. Robert J. Divergent antiviral roles of amphibian (Xenopus laevis) macrophages elicited by colony-stimulating factor-1 and interleukin-34.J. Leukoc. Biol. 2014; 96 (25190077): 1143-115310.1189/jlb.4A0614-295RCrossref PubMed Scopus (38) Google Scholar, 6Grayfer L. Robert J. Distinct functional roles of amphibian (Xenopus laevis) colony-stimulating factor-1- and interleukin-34-derived macrophages.J. Leukoc. Biol. 2015; 98 (26136505): 641-64910.1189/jlb.4AB0315-117RRCrossref PubMed Scopus (37) Google Scholar). In this respect, intraperitoneal injection of frogs with either recombinant CSF-1 or IL-34 results in peritoneal accumulation of Mϕs that morphologically (85–90%) represent the respective CSF-1- or IL-34-Mϕ populations (5Grayfer L. Robert J. Divergent antiviral roles of amphibian (Xenopus laevis) macrophages elicited by colony-stimulating factor-1 and interleukin-34.J. Leukoc. Biol. 2014; 96 (25190077): 1143-115310.1189/jlb.4A0614-295RCrossref PubMed Scopus (38) Google Scholar, 6Grayfer L. Robert J. Distinct functional roles of amphibian (Xenopus laevis) colony-stimulating factor-1- and interleukin-34-derived macrophages.J. Leukoc. Biol. 2015; 98 (26136505): 641-64910.1189/jlb.4AB0315-117RRCrossref PubMed Scopus (37) Google Scholar). Moreover, and akin to their bone marrow-derived counterparts, the peritonea-derived IL-34- and CSF-1-Mϕs are respectively highly resistant and susceptible to Fv3 (5Grayfer L. Robert J. Divergent antiviral roles of amphibian (Xenopus laevis) macrophages elicited by colony-stimulating factor-1 and interleukin-34.J. Leukoc. Biol. 2014; 96 (25190077): 1143-115310.1189/jlb.4A0614-295RCrossref PubMed Scopus (38) Google Scholar, 6Grayfer L. Robert J. Distinct functional roles of amphibian (Xenopus laevis) colony-stimulating factor-1- and interleukin-34-derived macrophages.J. Leukoc. Biol. 2015; 98 (26136505): 641-64910.1189/jlb.4AB0315-117RRCrossref PubMed Scopus (37) Google Scholar). To examine the extent to which restriction factor expression correlates with the Fv3 susceptibility of these Mϕ populations, we examined the expression of the same panel of restriction factor–encoding genes as above, in peritonea-derived CSF-1- and IL-34-Mϕs (Fig. 2B). Of the examined genes and in comparison with peritonea-derived CSF-1-Mϕs, the peritoneal IL-34-Mϕs only expressed greater levels of apobec2 (Fig. 2B). Xenopodinae encode highly expanded repertoires of phylogenetically distinct intron containing and intronless type I and type III IFNs (ifn, ifnx, ifnl, and ifnlx, respectively (17Sang Y. Liu Q. Lee J. Ma W. McVey D.S. Blecha F. Expansion of amphibian intronless interferons revises the paradigm for interferon evolution and functional diversity.Sci. Rep. 2016; 6 (27356970): 2907210.1038/srep29072Crossref PubMed Scopus (39) Google Scholar, 18Gan Z. Chen S.N. Huang B. Hou J. Nie P. Intronless and intron-containing type I IFN genes coexist in amphibian Xenopus tropicalis: insights into the origin and evolution of type I IFNs in vertebrates.Dev. Comp. Immunol. 2017; 67 (27780747): 166-17610.1016/j.dci.2016.10.007Crossref PubMed Scopus (37) Google Scholar)). Accordingly, to define the possible mechanisms conferring the disparities in IL-34- and CSF-1-Mϕ-Fv3 resistance, we generated CSF-1- and IL-34-Mϕs, challenged them with Fv3, and examined their gene expression of type I and III IFNs belonging to each of the distinct clades, described in recent reports (17Sang Y. Liu Q. Lee J. Ma W. McVey D.S. Blecha F. Expansion of amphibian intronless interferons revises the paradigm for interferon evolution and functional diversity.Sci. Rep. 2016; 6 (27356970): 2907210.1038/srep29072Crossref PubMed Scopus (39) Google Scholar, 18Gan Z. Chen S.N. Huang B. Hou J. Nie P. Intronless and intron-containing type I IFN genes coexist in amphibian Xenopus tropicalis: insights into the origin and evolution of type I IFNs in vertebrates.Dev. Comp. Immunol. 2017; 67 (27780747): 166-17610.1016/j.dci.2016.10.007Crossref PubMed Scopus (37) Google Scholar). In comparison with the CSF-1-Mϕ cultures, IL-34-Mϕs exhibited significantly greater gene expression of intron-containing type I IFNs (ifn1 and ifn7; Fig. 3A), intronless type I IFNs (ifnx2, ifnx6, ifnx11, ifnx13, and ifnx20; Fig. 3, B–D), and intron-containing and intronless type III IFNs (ifnlx1/2, ifnl3, and ifnl4, respectively; Fig. 3, D and E). Virally challenging CSF-1-Mϕ did not result in significant changes to their gene expression of any of the examined IFNs (Fig. 3, A–E). Fv3 challenge completely abrogated the gene expression of IL-34-Mϕ ifn1 (Fig. 3A) and had no significant affect on ifn7, ifnx2, ifnx6, ifnx11, ifnx13, ifnx20, or ifnl4 gene expression (Fi" @default.
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• W2778585524 date "2018-02-01" @default.
• W2778585524 modified "2023-10-12" @default.
• W2778585524 title "Differentiation-dependent antiviral capacities of amphibian (Xenopus laevis) macrophages" @default.
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