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Journal of Virology, April 2000, p. 3815-3831, Vol. 74, No. 8
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

The Genome of Fowlpox Virus

C. L. Afonso, E. R. Tulman, Z. Lu, L. Zsak, G. F. Kutish, and D. L. Rock*

Plum Island Animal Disease Center, Agricultural Research Service, U.S. Department of Agriculture, Greenport, New York 11944

Received 15 December 1999/Accepted 26 January 2000


    ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References

Here we present the genomic sequence, with analysis, of a pathogenic fowlpox virus (FPV). The 288-kbp FPV genome consists of a central coding region bounded by identical 9.5-kbp inverted terminal repeats and contains 260 open reading frames, of which 101 exhibit similarity to genes of known function. Comparison of the FPV genome with those of other chordopoxviruses (ChPVs) revealed 65 conserved gene homologues, encoding proteins involved in transcription and mRNA biogenesis, nucleotide metabolism, DNA replication and repair, protein processing, and virion structure. Comparison of the FPV genome with those of other ChPVs revealed extensive genome colinearity which is interrupted in FPV by a translocation and a major inversion, the presence of multiple and in some cases large gene families, and novel cellular homologues. Large numbers of cellular homologues together with 10 multigene families largely account for the marked size difference between the FPV genome (260 to 309 kbp) and other known ChPV genomes (178 to 191 kbp). Predicted proteins with putative functions involving immune evasion included eight natural killer cell receptors, four CC chemokines, three G-protein-coupled receptors, two beta  nerve growth factors, transforming growth factor beta , interleukin-18-binding protein, semaphorin, and five serine proteinase inhibitors (serpins). Other potential FPV host range proteins included homologues of those involved in apoptosis (e.g., Bcl-2 protein), cell growth (e.g., epidermal growth factor domain protein), tissue tropism (e.g., ankyrin repeat-containing gene family, N1R/p28 gene family, and a T10 homologue), and avian host range (e.g., a protein present in both fowl adenovirus and Marek's disease virus). The presence of homologues of genes encoding proteins involved in steroid biogenesis (e.g., hydroxysteroid dehydrogenase), antioxidant functions (e.g., glutathione peroxidase), vesicle trafficking (e.g., two alpha -type soluble NSF attachment proteins), and other, unknown conserved cellular processes (e.g., Hal3 domain protein and GSN1/SUR4) suggests that significant modification of host cell function occurs upon viral infection. The presence of a cyclobutane pyrimidine dimer photolyase homologue in FPV suggests the presence of a photoreactivation DNA repair pathway. This diverse complement of genes with likely host range functions in FPV suggests significant viral adaptation to the avian host.


    INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References

Within the Chordopoxvirinae subfamily (poxviruses of vertebrates) of the family Poxviridae, only members of the Avipoxvirus genus infect nonmammalian hosts (118). Avipoxviruses are a large family of cytoplasmic DNA viruses which infect more than 60 species of wild birds representing 20 families (169). Variability in restriction enzyme profiles of viral DNA suggests significant genomic differences among family members (169). Cross-infection studies also suggest genetic differences among viruses, which are reflected as a wide range of pathogenic effects (absence of clinical disease, local pox lesions, local and generalized infection, and generalized infection with death) and a lack of cross protection, depending on the specific virus-host combination (46, 169).

Fowlpox virus (FPV), the prototypical member of the Avipoxvirus genus, infects chickens and turkeys. Poxvirus diseases of poultry and other domestic birds (canaries and pigeons) have significant economic impact worldwide, with losses resulting from a drop in egg production in layers, reduced growth rates in broilers, blindness, and in some cases death (46, 170). Two forms of disease are associated with different routes of infection. The most common, the cutaneous form, occurs following infection by biting arthropods that serve as mechanical vectors for viral transmission. The disease is characterized by an inflammatory process with hyperplasia of the epidermis and feather follicles, scab formation, and desquamation of the degenerated epithelium, and it predisposes the host to secondary bacterial infections. The second, or diphtheric, form involves droplet infection of the mucous membranes of the mouth, the pharynx, the larynx, and sometimes the trachea. The prognosis with this form of the disease is poor because lesions often cause death by asphyxiation (169-171).

Vaccination with live-attenuated viruses (FPV and canarypox virus [CaPV]) and nonattenuated viruses (pigeonpox virus) is used to control this disease (59, 77, 136, 182). Fowlpox and pigeonpox vaccines are applied by comb scarification, by the wing-web stick method, or by feather follicle immunization. Vaccination confers protective immunity 10 to 14 days after infection. Problems related to safety and efficacy of commercial FPV vaccines remain (9, 24, 29, 65).

Multivalent recombinant FPV vaccines as well as FPV vaccines which incorporate immune response modifiers have been constructed (28, 96). Recombinant FPV vaccines expressing foreign antigens have been used to immunize animals against other avian and mammalian diseases (26, 83, 112, 121, 124, 125, 187). Because FPV and CaPV undergo abortive replication in mammalian cells, their use as host range-restricted mammalian expression vectors has been suggested (164, 165).

The FPV genome, containing 260 to 309 kbp of double-stranded DNA, is larger than other described chordopoxvirus (ChPV) genomes (45, 115, 120). Past work on FPV genomics, much of which used highly tissue culture-passaged FPV strains, has provided genetic information on approximately one-third of the viral genome, including some viral genes with putative immune evasion and host range functions (16, 18, 20, 57, 93, 127, 150, 163, 166, 191). The rational design of safer and more effective FPV vaccines and FPV-based expression vectors will require complete information on viral genes associated with viral virulence and host range and a more complete understanding of how these genes function in viral pathogenesis, immune evasion, and avian host range. Here we report the genomic sequence and analysis of a highly pathogenic strain of FPV.


    MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References

FPV DNA isolation, cloning, and sequencing. FPV genomic DNA was extracted from primary chicken embryo fibroblasts infected with a pathogenic FPV strain (fowlpox challenge virus; Animal Health Inspection Service Center for Veterinary Biologics, Ames, Iowa). Random DNA fragments were obtained by incomplete enzymatic digestion with Tsp509I endonuclease (New England Biolabs, Beverly, Mass.). DNA fragments of 1.5 to 2.5 kbp were isolated after separation on agarose gels, cloned into the dephosphorylated EcoRI site of pUC19 plasmids, and grown in Escherichia coli DH10B cells (Gibco BRL, Gaithersburg, Md.). Double-stranded pUC19 plasmids were purified by the alkaline lysis method in accordance with the manufacturer's instruction (5'right-arrow3', Inc., Boulder, Colo.). DNA templates were sequenced from both ends with M13 forward and reverse primers, using dideoxy chain terminator sequencing chemistries (135) and an Applied Biosystems (ABI) PRISM 377 automated DNA sequencer (Perkin-Elmer, Foster City, Calif.). ABI sequence software (version 3.3) was used for lane tracking and trace extraction. Chromatogram traces were base called with Phred (64), which also produced a quality file containing a predicted probability of error at each base position. The sequences were assembled with Phrap (63), with the quality files and default settings being used to produce a consensus sequence, with some subsequent manual editing being performed by the Consed sequence editor (72). An identical sequence was assembled with the TIGR assembler, using quality files and clone length constraints (160). Gap closure was achieved by primer walking of gap-spanning clones and sequencing of PCR products. The final DNA consensus sequence represented on average sixfold redundancy at each base position.

DNA sequence analysis. Genome DNA composition, structure, repeats, and restriction enzyme patterns were analyzed as previously described (1). Open reading frames (ORFs) longer than 30 amino acids with a methionine start codon (155, 156) were evaluated for coding potential by the use of the Hexamer (ftp.sanger.ac.uk/pub/rd) and Glimmer (134) computer programs. Minor ORFs were excluded. Gene families were analyzed and annotated as previously described (1). Early-promoter sequences were predicted as follows. Fifteen-base DNA motifs with similarity to the vaccinia virus (VV) early-promoter consensus sequence (51, 118) were selected from regions located upstream of initiation codons of 30 FPV homologues of VV virus early genes. These motifs were used to generate a scoring matrix (PROFILEMAKE) (55), and this matrix was used to search 100 bases upstream of all FPV ORFs (MOTIFSEARCH) (55). Positive ORFs found by MOTIFSEARCH (P = 0.001) were further verified by visual inspection, and those that had substitutions at the most-conserved residues were excluded (14 genes).

Virus abbreviations. Virus names are abbreviated in this article as follows: African swine fever virus, ASFV; Amsacta moorei entomopoxvirus, AmEPV; canarypox virus, CaPV; chordopoxvirus, ChPV; cowpox virus, CPV; ectromelia virus, ECT; entomopoxvirus, EPV; fowlpox virus, FPV; Heliothis armigera entomopoxvirus, HaEPV; lumpy skin disease virus, LSV; Lymantria dispar nuclear polyhedrosis virus, LdNPV; molluscum contagiosum virus, MCV; myxoma virus, MYX; orf virus, OV; Paramecium bursaria chlorella virus, PBCV; rabbit fibroma virus, RFV; rabbitpox virus, RPV; reticuloendotheliosis virus, REV; swinepox virus, SPV; tanapoxvirus, TPV; vaccinia virus, VV; and variola virus, VAR.

Nucleotide and protein sequence databases. Accession numbers presented are from the GenBank, SwissProt, or PIR database unless otherwise noted.

Nucleotide sequence accession number. The FPV genome sequence has been deposited in GenBank under accession no. AF198100.


    RESULTS AND DISCUSSION
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References

Organization of the FPV genome. The FPV genome was assembled into a contiguous sequence of 288,539 bp, which is slightly smaller in size than previous estimates of 299 to 309 kbp for low-passage-number FPV field strains (45, 115). Because the hairpin loops were not sequenced, the left-most nucleotide of the assembled sequence was arbitrarily designated base 1. The nucleotide composition is 69% A+T and is uniformly distributed over the entire length of the FPV genome. Six small regions (102 to 315 bp in length) with higher C+G content (50%) are located in the terminal genomic regions (nucleotides 3219 to 5618 and 28222 to 285321). The total composition of all FPV ORFs reflects a bias for residues with A- and T-rich codons. Ile, Leu, Lys, Asn, Tyr, and Phe constitute 45% of all encoded amino acids.

FPV encodes 260 putative genes of 60 to 1,949 amino acids in length (Fig. 1; Table 1). Predicted ORFs represent an 85% coding density, with an average ORF length of 943 nucleotides. One hundred and one FPV ORFs have been assigned similarity or putative function based on homologies with other viral or cellular genes. FPV has a genomic organization similar to that of other known ChPVs (71, 108, 141, 142). There is no evidence of introns, both strands are protein encoding, and ORFs frequently occur in head-to-tail tandem arrays (Fig. 1). Fifty-two ORFs partially overlap other ORFs. Within the terminal 50 kbp of the genome, most ORFs (74% of them in these regions) are transcriptionally oriented toward their respective termini. As seen in other poxviruses, the FPV genome contains a central coding region bounded by two identical inverted terminal repeat (ITR) regions of approximately 9.5 kbp each (Fig. 1). The 3' 148 codons of ORFs FPV010 and FPV251 mark the boundary between the ITR and the central coding region (Fig. 1). The terminal 1,877 nucleotides are noncoding.


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  		FIG. 1.   Linear map of the FPV genome. ORFs are numbered from left to right based on the position of the methionine initiation codon. ORFs transcribed to the right are located above horizontal lines; ORFs transcribed to the left are below. VV homologues are indicated with red italicized numbers. Genes with similar functions and members of gene families are colored according to the figure key. ITRs are represented as gray bars below the ORF map. Boxed regions 1 to 3 indicate novel coding regions at junction sites of major genome rearrangements, and they correspond to similarly numbered regions shown in Fig. 4.

                              
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  		TABLE 1.   FPV ORFs

The remnant of an integrated avian reticuloendotheliosis virus (REV) genome in the FPV genome is represented by 253 nucleotides (232464 to 232717) that are similar (98% identity) to the long terminal repeat of a chicken B lymphoma-derived REV (accession no. M22223). However, REV env, gag, and pol genes were not found as has been reported for some FPV strains (76). The same long terminal repeat (98% identity over 200 nucleotides) is also found in several strains of Marek's disease virus (MDV), a herpesvirus of chickens. The fragmented remains of a ubiquitin gene are present in the FPV genome from nucleotides 74550 to 74220. Interestingly, the best match to this gene is chicken ubiquitin (accession no. M1110), which exhibits 54% identity over 76 amino acids with one frameshift, two in-frame stops, and two gaps.

ITRs. The FPV genome contains identical ITRs of 9,520 nucleotides at both termini (Fig. 1). Within each ITR, a 1.7-kbp region contains 42 copies of a 31- to 32-bp tandem repeat (70 to 95% identical) between nucleotides 198 and 1835 as well as between nucleotides 286703 to 288340. Sizing of seven cloned fragments spanning this tandem-repeat region produced specific size classes of 1.7, 2.4, 3.3, 5.1, and 5.8 kbp in length, indicative of length polymorphism. Therefore, individual FPV genomes could be at least 8 kbp longer than the genomic sequence assembled here. Each ITR also contains 10 ORFs. These ITR sequence data are consistent with previous descriptions of FPV ITR regions (36, 166).

Gene expression regulatory elements. FPV ORFs contain typical poxvirus promoter sequences upstream of their translation initiation codons. Sequences with similarity to the VV early-promoter consensus sequence (AAAAATGAAAAAAAA) have previously been noted in the 5' untranslated regions of known and predicted FPV early genes (90, 91, 191). Fifty-six FPV ORFs contain putative early promoters (Table 1). Of these, 22 contain a poxvirus early transcriptional stop sequence (TTTTTXT, where X is any nucleotide) near the translational stop codon (50 bases upstream to 100 bases downstream) and lack the early stop sequence elsewhere in the ORF (189). As seen in other poxviruses, many genes with potential early promoters are members of gene families and/or putative host range genes (Table 1). Three of five homologues of VV intermediate genes (FPV088, FPV126, and FPV165) contain the VV intermediate-promoter sequence (AAAXAAX11-13TAAA) (10, 11, 118), and one (FPV049) contains a single-base substitution (AAAXAG). A total of 55 putative late FPV ORFs, including many of the conserved virion-associated poxvirus genes (Table 1), contain the VV late-promoter sequence (TAAATG) at the ATG codon (131). The TAAATG late promoter has been previously described to be located upstream of FPV late genes (17, 91, 163, 191), and it is known that early-late and late promoters can be exchanged between FPV and VV with no loss of temporal specificity (27).

Transcription and mRNA biogenesis. FPV contains 26 genes involved in poxvirus transcriptional processes (Table 1). These include RNA polymerase subunits; mRNA transcription initiation, elongation, and termination factors; and the enzymes that direct posttranscriptional processing of viral mRNA (118). FPV RNA polymerase subunits include homologues of VV RPO147 (FPV137), RPO132 (FPV189), RAP94 (FPV141), RPO35 (FPV193), RPO30 (FPV100), RPO22 (FPV135), RPO19 (FPV169), RPO18 (FPV056), and RPO7 (FPV118). Homologues of all previously described early (E), intermediate (I), and late (L) poxvirus transcription factors (TFs) are found in FPV, including the following: VETFS (FPV057), VETFL (FPV171), VITF-3 (FPV172 and FPV188), VLTF-1 (FPV126), VLTF-2 (FPV049), VLTF-3 (FPV165), and VLTF-4 (FPV142) (87, 191). FPV079 and FPV183 encode elongation factors for late transcription (VV G2R and A18R) (22, 44, 186). Both transcriptional terminator NPH-1 (FPV052) and the RNA helicase NPH-II (FPV082) are present. FPV146 and FPV051 encode both subunits of the mRNA capping enzyme, and FPV102 and FPV134 encode both subunits of the poly(A) polymerase. FPV053 and FPV054 contain MutT-like motifs and are similar to VV D10R and D9R (85). D10R has recently been shown to be a negative regulator of viral transcription (149).

Nucleotide metabolism. FPV contains homologues of thymidine kinase (FPV086), dUTP pyrophosphatase (FPV038), glutaredoxin (FPV077), two deoxycytidine kinases (dCKs; FPV059 and FPV151), and a putative DNase II (FPV032) (Table 1). Genes encoding dCK and DNase II are unique to FPV and have been previously described (86, 93). Interestingly, sequencing of the complete genome has revealed a second dCK gene (FPV151). These two FPV dCK genes are 42% identical to each other and exhibit 32% amino acid identity to cellular dCK (Table 1). The DNase II homologue, FPV032, is truncated compared to the previously described FPV gene, FPCEL-1 (93). FPV032 represents the largest subunit (alpha 2) of cellular DNase II and includes the conserved histidine at the potential active site (99, 174). The function of this gene in the viral replication cycle is unknown; however, FPCEL-1 is not essential for viral growth in vitro (93). Cellular DNase II is thought to function in DNA catabolism during apoptosis (89, 168). FPV lacks other known poxvirus genes thought to be involved in nucleotide metabolism, including thymidylate kinase, thymidylate synthase, ribonucleotide reductase, guanylate kinase, and thioredoxin. This specific complement of nucleotide metabolism genes in FPV suggests that they have significance for cell and/or tissue tropism.

DNA replication and repair. FPV contains homologues of ChPV genes involved in DNA replication and repair (118) (Table 1). These include a DNA ligase (FPV043), ATP-GTP binding protein (FPV058), uracil DNA glycosylase (FPV062), DNA polymerase (FPV094) (19), DNA topoisomerase (FPV143), processivity factor (FPV185), and replication-essential protein kinase (FPV212).

Interestingly, FPV158 is a homologue of class II cyclobutane pyrimidine dimer (CPD) photolyases. Although the gene has been previously described in the Entomopoxvirinae (1), this is the first description of a photolyase in a ChPV. FPV158 is most similar to marsupial photolyase (56% identity over 462 amino acids) (188) and is slightly less similar to Melanoplus sanguinipes entomopoxvirus (EPV) photolyase (54% identity over 448 amino acids) (1). Both class II photolyase Prosite signatures (PS01083 and PS01084) are present with a single conservative substitution at residue 302. Although the function of this FPV gene is unknown, CPD photolyase is a photoreactive enzyme that efficiently repairs UV-induced CPD lesions in DNA, using visible light as an energy source (75). Since EPVs have insect hosts and FPV is mechanically vectored by insects (48), the presence of a photolyase gene in both viral genomes is suggestive of a relationship between a viral phase in insects and/or the environment and the need for this type of virus-encoded DNA repair.

Protein modification. FPV contains at least six genes with putative protein modification functions (Table 1). The homologues encoded include three serine/threonine protein kinases (PKs) (FPV111, FPV212, and FPV226), one tyrosine PK (FPV203), a tyrosine/serine protein phosphatase (FPV138), and a metalloprotease (FPV081). FPV212 and FPV226 are similar to the serine/threonine PKs B1R and B12R of VV. FPV111 is similar to VV F10L, a serine/threonine PK essential for phosphorylation of virus proteins during virion assembly (14, 54). FPV203 shows similarity to the product of a tyrosine PK-like ORF found in rabbit fibroma virus (RFV) (109); however, neither of these poxvirus proteins contains the critical Asp residue at the predicted active site (Prosite PS00109). FPV138 is a homologue of the VV H1L tyrosine/serine protein phosphatase, which is involved in VV assembly (54). FPV081 is a homologue of the VV protease G1L. This protein contains the characteristic amino-terminal His-XX-Glu-His inverted metalloprotease motif, and it may function in viral protein processing and virion morphogenesis (178).

Structural proteins. FPV encodes homologues of at least 31 known VV structural proteins, and the majority of them are associated with the intracellular mature virus particle (IMV) (Table 1). FPV homologues of VV core proteins include FPV069 (D3R), FPV083 (I7L), FPV090 (I1L), FPV103 (F17R), FPV120 (G7L), FPV131 (L4R), FPV148 (D2L), FPV167 (A3L), FPV168 (A4L), FPV174 (A10L), and FPV176 (A12L) (15, 25). FPV homologues of VV IMV membrane-associated proteins include FPV050 (D13L), FPV085 (I5L), FPV128 (L1R), FPV140 (H3L), FPV178 (A13L), FPV179 (A14L), and FPV182 (A17L). FPV lacks homologues of VV IMV membrane proteins A27L, which is required for extracellular enveloped virion (EEV) envelopment and egress and for heparan sulfate binding (41, 130), and D8L, a cell surface binding protein (103). FPV structural proteins FPV120, FPV131, FPV167, FPV174, FPV176, and FPV182, like their VV homologues, contain the conserved AG proteolytic cleavage sites, which suggests that aspects of structural protein processing are conserved in FPV (173). FPV197 is the homologue of VV ATP-GTP binding protein A32L, which likely functions in virion assembly and DNA packaging (38).

FPV contains three genes that encode proteins potentially associated with EEVs (118, 123). FPV108, FPV109, and FPV198 are similar to VV F13L, F12L, and A34R, respectively (35). Missing from FPV are obvious homologues of VV EEV genes B5R, A33R, A36R, and A56R. EEV membrane proteins are involved with EEV formation, release, and infectivity (23, 111, 181). Since these functions may be associated with aspects of host range, the lack of well-conserved homologues of these genes in FPV is not surprising.

Homologues of five genes representing two conserved poxvirus gene families with putative structural functions are present in FPV. The genes encoding FPV112 and FPV128, homologues of VV F9L and L1R, respectively, comprise one gene family (142). The genes encoding FPV127, FPV136, and FPV181, homologues of VV G9R, J5L, and A16L, respectively, comprise a second, small gene family. G9R and A16L proteins are myristylated and potentially soluble (105), and J5L is thought to be an essential gene (190). Invariant cysteine residues and putative transmembrane domains unique to each family are conserved in these FPV ORFs (142).

FPV190 and FPV191 are homologues of poxvirus A-type inclusion (ATI) proteins (Table 1), insoluble proteins that constitute the protein matrix of ATIs. Cytoplasmic ATIs are thought to protect mature virions from environmental insults, and they may be of significance for FPV transmission in nature (40, 82, 128, 133).

Host-related functions. FPV contains a significant number of putative host range genes that exhibit similarity to cellular genes and to other known poxvirus genes. This diverse complement of host range genes, some of which are novel, is suggestive of significant adaptation to the avian host. These genes may function in host immune evasion, immune modulation, and aspects of cell and/or tissue tropism or perform other cellular functions. Most of these genes are found in terminal regions of the FPV genome, although several groupings of them are more centrally located.

Immune evasion functions. FPV080 is a homologue of the eukaryotic transforming growth factor beta  (TGF-beta ) (Table 1; Fig. 2A). To our knowledge, this is the first TGF-beta gene found in a virus genome. Similarities to eukaryotic TGF-beta include the 112-amino-acid peptide region of the active protein, Prosite signature PS00250 (with one mismatch), and cysteines necessary for intra- and interchain disulfide bond formation. TGF-beta is a multifunctional peptide that both stimulates connective tissue cell growth and differentiation, particularly during neovascularization and wound healing, and suppresses proliferation of most other cell types (58). TGF-beta also exhibits a range of immunomodulatory effects, including suppression of cellular and humoral immune mechanisms, specifically generation and/or activity of cytotoxic T lymphocytes, natural killer (NK) cells, and lymphokine-activated killer cells, generation and/or activity of lymphokines (interleukin-1 [IL-1], IL-6, tumor necrosis factor, and IL-2); and production of polyclonal antibodies (58). Chemoattractant and proinflammatory properties have also been associated with TGF-beta (58). A role for FPV080 in suppression of the host immune response and/or cell growth and differentiation is likely.


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  		FIG. 2.   Multiple amino acid sequence alignments of proteins encoded by putative FPV immune evasion genes. Boldfaced letters represent conserved cysteine residues, asterisks mark Prosite signatures, and shaded residues indicate identity to amino acids of FPV proteins. Amino acid positions are indicated on the right. (A) Alignment of FPV080 with TGF-beta genes. The Prosite signature is PS00250. Frog, Xenopus laevis, accession no. P17247; chicken, Gallus gallus, accession no. P30371; rat, Rattus norvegicus, accession no. P17246; fish, Oncorhynchus mykiss, accession no. AJ007836; fruit fly, Drosophila melanogaster, accession no. M77012. (B) Alignment of FPV072 and FPV076 sequences with those of NGFs. The Prosite signature is PS00248. Rat, Rattus norvegicus, accession no. P25247; chicken, Gallus gallus, accession no. P05200; snake, Bungarus multicinctus, accession no. P34128; frog, Xenopus laevis, accession no. P211617. (C) Alignment of FPV060, FPV061, FPV116, and FPV121 sequences with those of viral and cellular CC chemokines. Herpesvirus, Kaposi's sarcoma-associated herpes-like virus, accession no. U74585; human, Homo sapiens, accession no. P22362; MCV148, molluscum contagiosum virus, accession no. U60315.

FPV072 and FPV076 are similar to cellular beta  nerve growth factor (beta -NGF) (Table 1; Fig. 2B). This is the first example of a virus encoding beta -NGF-like genes. Both FPV proteins contain the six cysteine residues involved in intrachain disulfide bonding and the Prosite beta -NGF family signature (PS00248) (Fig. 2B). beta -NGF, a member of the neurotrophin protein family, stimulates neuronal survival, division, and differentiation and promotes survival of memory B lymphocytes and mast cells (30, 97, 167). Recently, beta -NGF has been shown to be an autocrine survival factor for human immunodeficiency virus type 1-infected macrophages (68). An FPV-encoded beta -NGF may be involved in promoting infected-cell survival. In addition, beta -NGF has proinflammatory and immunomodulatory effects (5). beta -NGF, which is produced by fibroblasts and keratinocytes in response to injury, induces differentiation, activation, and degranulation of mast cells and modifies expression of mast cell-derived immunoregulatory mediators and cytokines (34, 104, 138, 176, 177, 183). Conceivably, a virus-encoded beta -NGF antagonist could have a role in inhibiting antiviral immune responses in FPV-infected skin and respiratory tract. Given that mast cells are initiators and amplifiers of innate immune responses, the presence of beta -NGF homologues in FPV suggests that interference with early innate immune responses may be important for viral infection.

FPV060, FPV061, FPV116, and FPV121 exhibit similarity to the CC class of small soluble chemokines found in vertebrates (Table 1). The FPV genes contain the conserved pattern of four cysteines which are necessary for disulfide bond formation (Prosite PS00472), as well as other conserved residues (Fig. 2C). The FPV genes are similar in size (120 to 181 amino acids) to other known CC chemokines. Three of the products contain potential signal sequences at the N terminus, indicating that they may be secreted proteins. In general, CC chemokines attract T lymphocytes and NK cells to sites of infection (113). Other ChPVs modulate CC chemokine activity by secreting novel proteins that specifically bind CC chemokines and inhibit their effects in vitro and in vivo. These inhibitors are widespread among mammalian poxviruses, including VV, variola virus (VAR), cowpox virus (CPV), RFV, myxoma virus (MYX), and rabbitpox virus but is notably absent from FPV (4, 73, 94, 151). In molluscum contagiosum virus (MCV), a CC chemokine-like protein, MC148R, functions as a broad-spectrum CC and CXC chemokine antagonist (49). FPV's large repertoire of CC chemokine homologues functioning as antagonists could result in broad-range inhibition of normal CC chemokine function during host antiviral immune responses. Alternatively, as is the case for the viral macrophage-inhibitory protein 1 chemokine encoded by human herpesvirus 8, FPV chemokine homologues may function as agonists to modify normal host immune responses (47, 61).

FPV contains three genes encoding proteins with homology to G-protein-coupled receptors (Table 1). FPV021 and FPV027 are most similar to a monkey chemokine receptor protein (GPR1), while FPV206 is most closely related to the human Epstein-Barr virus-induced G-protein-coupled receptor (21). The highest level of amino acid similarity to cellular genes occurs at the seven transmembrane domains, the first cytoplasmic domain, and the second extracellular domain. The conserved acidic amino acid-Arg-aromatic amino acid triplets in the amino-terminal portion of the second aromatic loop, which have been implicated in the interaction with G proteins, are conserved in FPV021 and conservatively substituted in FPV027 and FPV206 (8). As with other G-protein-coupled receptors, the FPV proteins contain potential glycosylation sites at their carboxyl termini. G-protein-coupled receptors are integral membrane proteins that transduce extracellular signals to the intracellular environment through activation of the phosphatidylinositol-calcium second-messenger system (139). These receptors have been identified in the capripoxviruses and in swinepox virus, where their function is not known (37, 107). However, G-protein-coupled receptors encoded by several herpesvirus genomes are able to bind chemokines and invoke signal transduction responses that affect viral replication and pathogenesis in the host (2, 7, 13, 67).

FPV073 exhibits similarity to mammalian and ChPV IL-18-binding protein and contains potential N-glycosylation sites and a signal peptide (Table 1) (142, 184). Cellular and MCV IL-18bp homologues have been found to inhibit IL-18-dependent gamma interferon production (3, 185). IL-18 is a multifunctional proinflammatory cytokine of the IL-1 family that induces gamma interferon production, Th-1 responses, and NK cell activity, and it is important for effective host responses to VV infection in mice (50, 56, 79, 114, 161, 162). An anti-inflammatory function for FPV073 is likely.

FPV047 most closely resembles mammalian K/L-type semaphorins and the alcelaphine herpesvirus semaphorin homologue (accession no. U18243) (33% identity over 597 amino acids) (Table 1). Like the K/L-type semaphorin and alcelaphine herpesvirus semaphorin, FPV064 contains a potential amino-terminal signal sequence, a large semaphorin K/L domain, an immunoglobulin (Ig) domain, and a hydrophobic carboxyl terminus (62, 95). VV also encodes a K/L-like semaphorin homologue (A39R); however, the semaphorin domain is truncated and the Ig domain is absent (84). Semaphorins are a large family of secreted and membrane-associated proteins that act as axon guidance molecules during embryonic development and may affect organogenesis, vascularization, and angiogenesis (154). In addition, the CD100 semaphorin protein found on the surface of T lymphocytes functions in cell activation (52). The secreted VV A39R protein binds a plexin-like receptor found on lymphocytes and induces cytokine production and ICAM up-regulation in monocytes (43). The FPV semaphorin homologue may have a similar immunomodulatory function.

FPV contains eight ORFs (FPV001, FPV003, FPV008, FPV235, FPV239, FPV253, FPV258, and FPV260) with homology to C-type lectins NKG2 and CD94 proteins present on NK cells and CD69 protein present on lymphocytes (Table 1). Similar proteins have been described in poxviruses (VV and CPV) and African swine fever virus (ASFV) (122, 145, 179). Although the functions of these viral proteins are unknown, the VV C-type lectin protein, A40R, localizes to infected cell plasma membranes (179). C-type lectin cellular NK cell receptors bind class I major histocompatibility complex antigens and promote or inhibit immune activity through intracellular signaling pathways (66, 132, 175). It is conceivable that the expression of these proteins in FPV-infected cells interferes with normal immune surveillance or host responses.

FPV encodes five homologues of serine proteinase inhibitors (serpins) (FPV010, FPV040, FPV044, FPV204, and FPV251) (Table 1). All contain the serpin Prosite signature (PS00284) and exhibit 21 to 29% amino acid identity to each other. Serpin genes have been found in most ChPVs (rabbitpox virus, RFV, VV, VAR, CPV, MYX, and ectromelia virus [ECT]), where they perform host range functions involving anti-inflammatory activity and/or regulation of cellular apoptosis in specific cells through inhibition of IL-1beta -converting enzyme, the cytotoxic-T-lymphocyte-derived protease granzyme B, and other caspases within the apoptosis-regulatory cascade (172).

Other host range functions. The gene encoding FPV039 is the first reported poxvirus member of the Bcl-2 gene family. FPV039 resembles MCL1, a protein induced during monocyte/macrophage differentiation in myeloid leukemia cell lines, and BFL1 (29% identity over 134 amino acids), an antiapoptosis protein expressed specifically in the bone marrow, spleen, and thymus (88, 100) (Table 1; Fig. 3A). FPV039 contains one BH1 domain and one modified BH2 domain (Prosites PS01080 and PS01258) but lacks additional BH3 and BH4 domains. As with other viral Bcl-2 homologues, FPV039 may prevent a cellular apoptotic response to viral infection (12).


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  		FIG. 3.   Multiple amino acid sequence alignments of proteins encoded by putative FPV host range genes. Asterisks mark Prosite signatures; shaded residues exhibit identity to amino acids to FPV proteins. Amino acid positions are indicated. (A) Alignment of FPV039 sequence with those viral and cellular Bcl-2 homologues. ASFV, accession no. Q07819; rat, Rattus norvegicus, accession no. AF115380; human, Homo sapiens, accession no. Q07820; mouse, Mus musculus, accession no. Q07440. (B) Alignment of FPV070 sequence with homologues of the mouse T10 protein. Celegans, Caenorhabditis elegans, accession no. Z78016; mouse, Mus musculus, accession no. X74504; yeast, S. cerevisiae, accession no. P53275. (C) Alignment of FPV250 sequence with those of proteins from avian viruses. Fowladeno, fowl adenovirus, accession no. AF007578; Gallidherp, Marek's disease virus, accession no. L22174.

FPV070 is a homologue of the mouse T10 gene and a yeast protein of unknown function (Table 1; Fig. 3B). This gene has not been previously found in a viral genome. T10 encodes a protein which is specifically expressed at high levels in epithelial cells of the trachea, esophagus, lung, and velopharyngeal region during early embryogenesis (74). The diphtheric form of FPV infection in chickens involves viral infection of the mucous membranes of the mouth, pharynx, and larynx and sometimes the trachea (169-171). An FPV T10 homologue may perform a host range function in epithelial cells of the respiratory tract.

FPV217 and FPV250 have similarities to genes of unknown function present in other viruses (Table 1; Fig. 3C). FPV217 is similar to a gene in Lymantria dispar nuclear polyhedrosis virus. FP250 is similar to putative proteins encoded by MDV and fowl adenovirus (44% identical over 99 amino acids) (32, 146). The presence of this homologue in three different avian DNA viruses suggests a significant avian host range function.

FPV211 contains an epidermal growth factor (EGF)-like domain which includes the six cysteine residues involved in disulfide bond formation, a potential signal peptide, and a transmembrane domain (Table 1). The similarity of FPV211 to secreted poxvirus EGF-like growth factors is based solely on the presence of the EGF domain. Poxvirus EGF-like growth factors are not essential for virus replication in vitro, influence virulence in vivo, and stimulate cell proliferation at sites of viral replication (110). FPV211 may contribute to the hyperplasia observed in FPV-infected tissue (169).

FPV contains 31 ORFs with ankyrin repeat motifs (Table 1). This large gene family is clustered at both ends of the genome, with two additional ORFs (FPV115 and FPV162) being found in more central locations (Fig. 1). Proteins encoded by FPV ankyrin family genes contain 1 to 12 copies of the ankyrin repeat motif (102), range in size from 104 to 747 amino acids, and are from 20 to 45% identical to each other depending on ORF size and alignment length. This level of amino acid identity is higher than that to ankyrin repeats of proteins found in a wide phylogenetic range of organisms. The ankyrin gene copy number may differ in FPV strains. Sequence from a genomic region in the right end of a highly passaged FPV strain contains nine fewer ankyrin genes than the number found here (166). Poxvirus ankyrin repeat genes have been associated with host range functions in MYX, CPV, and VV, and they may inhibit virus-induced apoptosis (70, 80, 119, 126, 153, 159). Ankyrin repeat motifs are clearly involved in mediating protein-protein interactions (101, 140). In CPV, which has a relatively broad host range, at least 16 ankyrin repeat genes have been identified (145). Loss or disruption of many of these genes in other orthopoxviruses that have a more restricted host range has suggested that loss of ankyrin genes may be associated with the narrowing of host range (6, 145).

FPV contains 10 ORFs (FPV075, FPV124, FPV150, FPV155, FPV157, FPV159, FPV161, FPV163, FPV236, and FPV248) with homology to N1R of RFV, p28 of ECT, and other ChPV and EPV genes (Table 1). Amino acid identity among FPV NR1/p28 family members is 20 to 38% and includes a conserved amino-terminal region with an invariant tryptophan residue. This domain is necessary for localization of RFV N1R to viral factories (31). FPV150 and FPV157, together with RFV N1R, ECT p28, and CPV and VAR homologues, contain a carboxyl-terminal C3HC4 RING finger. RING fingers are cysteine-rich zinc-binding motifs that are present in functionally diverse proteins, mediate protein-protein interactions, and help direct protein ubiquitination (81, 137). ECT p28 is a host range factor required for viral replication in mouse macrophages and for viral virulence in mice (143, 144); thus, a role in viral virulence and/or host range is likely for some members of this FPV family.

FPV064 encodes a homologue of cellular and MCV (MC066L) glutathione peroxidase (Table 1). FPV064 contains the glutathione peroxidase signature sequence (Prosites PS00460 and PS00763) including the active site for selenocysteine encoded by the opal codon (UGA). Cellular glutathione peroxidases reduce hydroxyperoxides with glutathione and are believed to provide protection from oxidative stress caused by ingested or endogenously formed hydroxyperoxides (157). MC066L protects human keratinocytes against cytotoxic effects of UV radiation and hydrogen peroxide and may permit efficient viral replication under conditions of environmental stress (148). A similar function for FPV064 is likely.

Cellular functions. FPV114 shares a 180-amino-acid conserved domain with proteins found in plants (accession no. U80192), yeast (accession no. P36024 and X88900), roundworms (accession no. Z81069), and bacteria (accession no. P24285, P30197, Q04810, and D90910). FPV114 is most closely related to the yeast Hal3 and SIS2 genes and a putative Hal3 homologue from the plant Arabidopsis thaliana (Table 1). These proteins function as inhibitory subunits of cellular protein phosphatases, and they promote salt tolerance and affect growth (53). FPV114, roundworm, and bacterial homologues lack the amino- and carboxyl-terminal domains found in the yeast protein. Bacterial homologues function in DNA/pantothenate and lantibiotic metabolism (39, 92). The wide phylogenetic distribution of FPV114 homologues suggests that their function is highly conserved.

FPV048 encodes a 261-amino-acid protein that is similar to the members of the GNS1/SUR4 family of integral membrane proteins (Table 1). Similarities to the GNS1/SUR4 gene family include a defined motif (BLOCKs database signature BL01188) and a conserved protein structure consisting of an N-terminal region with two transmembrane domains, a central hydrophilic loop, a C-terminal region with one to three transmembrane domains, and the Prosite family signature (PS01188). The yeast GNS1 and SUR4 genes function in glucose metabolism, and they are suspected to have pleiotrophic functions in the cellular response to nutrient availability (60, 69, 129).

FPV011 and FPV033 are similar to the eukaryotic alpha -type soluble NSF attachment protein (alpha -SNAP) (Table 1). FPV033 has been previously described, but this is the first report of a second FPV alpha -SNAP homologue (93). FPV011 and FPV033 are similar in size (278 and 267 amino acids long, respectively) and exhibit 34% amino acid identity to each other over 249 amino acids. alpha -SNAPs are involved in vesicular trafficking, mediating intracellular membrane fusion by recruiting soluble NSF to membrane receptors (158). alpha -SNAPs and their yeast homologues (Sec17) are required for vesicular transport through the Golgi complex and for exocytosis (42, 117). The fact that FPV033 is not essential for growth in vitro suggests that it has a host range function (93).

FPV093 is the homologue of VV E10R, a protein that is conserved in many cytoplasmic DNA viruses and eukaryotes and contains a pattern of cysteine residues typical of glutaredoxin and thioredoxin redox-active centers (78). The homologue of this protein in ASFV, 9GL, has recently been shown to be involved in virion maturation and viral growth in swine macrophages (98).

FPV030 exhibits homology to human PC-1, which has alkaline phosphodiesterase and nucleotide pyrophosphatase activities and has been previously found in FPV (33, 93). The function of this conserved but nonessential FPV gene is unknown; however, it has been suggested that it may provide an external source of nucleotides or regulate signal transduction (93).

FPV046 encodes a homologue of 3-beta -hydroxysteroid dehydrogenase (3beta HSDH), previously described in FPV and other poxviruses (VV and MCV) (Table 1) (116, 142, 150). In VV, 3beta HSDH has steroidogenic activity in vitro and is involved in viral virulence in vivo (116). Cellular 3beta HSDH catalyzes the oxidative conversion of both delta (5)-ene-3-beta -hydroxysteroid and ketosteroids, performing a crucial role in the biosynthesis of all classes of steroid hormones.

Two unrelated FPV ORFs, FPV029 and FPV071, have striking similarity to genes present in a diverse phylogenetic range of organisms (Table 1). FPV029 is similar to proteins of unknown function from yeast (accession no. P34222), bacteria (accession no. U67463 and AE000927), a roundworm (accession no. AF067936), a plant (accession no. AL031804), the fruit fly (accession no. AE0015722), and humans (accession no. AF151905). All of these proteins show several conserved domains, and the bacterial genes and the FPV037 ORF have similar lengths. FPV071 is similar to genes of unknown function from yeast (accession no. P40506), humans (accession no. AI391502), tomato (accession no. AI771876), and fruit fly (accession no. AF132150).

Gene families of unknown function. FPV097, FPV098, FPV099, FPV107, FPV122, and FPV123 are homologues of VAR B22R (Table 1). B22R homologues are also present in CPV, ECT, and MCV but are absent from VV (6, 71). FPV gene family members exhibit 34 to 52% amino acid identity to each other and 32 to 36% identity to the other poxvirus homologues, with the highest level of similarity being in the carboxyl-terminal regions. Several features make these FPV B22R homologues notable. They represent the largest genes in FPV (1,766 to 1,949 amino acids), and they comprise 12% of the viral genome. FPV contains multiple B22R homologues, while other poxviruses either contain a single copy of the gene or lack it (71, 108, 142). FPV B22R homologues are present in a central genomic region, while orthopoxvirus homologues are located in the terminal regions of their respective genomes (Fig. 1) (71, 108). Although no function has yet been assigned to any of these ORFs, it has been suggested that they are type II membrane proteins (108, 145).

FPV017, FPV055, FPV125, FPV199, and FPV200 have similarity to V-type Ig domains of diverse proteins (Table 1). All five proteins contain conserved Ig domain cysteines and surrounding residues. FPV017 and FPV199 are notably similar to each other (25% amino acid identity), as are FPV055 and FPV125 (37% identity over 270 amino acids). Cellular members of the Ig superfamily include secreted and membrane-bound receptors and cell adhesion proteins (180). Ig domain-containing proteins, including hemagglutinin, cytokine receptor, and HLA antigen homologues, are present in other poxviruses (141, 142, 147, 152).

FPV067, FPV087, FPV147, FPV152, FPV156, and FPV209 comprise the His-X-X-Thr motif gene family (HT motif). These genes exhibit 18 to 34% identity over 69 to 102 amino acids and contain the HT motif at residues 19 to 33 or 51 to 65. FPV147, FPV152, and FPV209 also have HX4-5T motifs upstream of the primary HT motif. The HT family ORFs have no significant similarity to other sequences in the database.

FPV006 and FPV255 are 35% identical to FPV020 over 283 amino acids. All three FPV ORFs are similar to VV C10L and C4L and homologues present in CPV and VAR (Table 1). Like their orthopoxvirus homologues, these FPV ORFs are located in the terminal genomic regions. Although their function has not been determined, C10L and C4L are dispensable for virus growth in cell culture (126).

Relationship of FPV to other ChPVs. FPV resembles other ChPVs in overall genome structure and composition (the presence of a central conserved core of genes, ITRs, and large numbers of homologues). However, compared to those of other ChPVs, the genome of FPV exhibits large-scale genomic rearrangement, more extensive gene families, and the presence of novel host range genes. Genomic comparisons of FPV and VV have shown major rearrangement of blocks of genes (115). Analysis of the complete FPV genomic sequence reveals that FPV contains at least two major genomic rearrangements in the conserved colinear core of genes present in VV, VAR, and MCV (71, 108, 142) (Fig. 4). A 12-kbp FPV genomic region containing ORFs FPV049 to FPV058 (comparable to VV A1L to D5R) is inverted and translocated toward the left end of the genome relative to VV. A 56-kbp FPV genomic region containing ORFs FPV077 to FPV112 (comparable to VV G4L to F9L) is inverted relative to VV. At the junction sites of these major rearrangements there are novel coding regions of 5 to 17.5 kbp (see boxed areas 1 to 3 in Fig. 1 and regions 1 to 3 in Fig. 4). Genes within these junction regions are predominantly homologues of cellular genes and/or are members of gene families. This clustering of cellular homologues and gene families in central genomic locations has not been previously observed in the subfamily Chordopoxvirinae, in which these types of genes are generally found in terminal variable regions of the genome (71, 106, 141). This observation suggests that blocks of genes may have translocated from terminal variable regions of the genome to central regions during large-scale rearrangements of FPV. FPV genome colinearity with genomes of other ChPVs is also interrupted at multiple sites by insertions or deletions of individual genes and multiple copies of B22R gene family members (Fig. 1 and 4 and Table 1).


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  		FIG. 4.   Comparison of gene orders of FPV and MCV homologues. Symbols represent homologous genes. Green circles, colinear genes; red diamonds, inverted genes; blue squares, inverted and translocated genes; black triangles, noncolinear genes. Noncolinear genes include FPV046 (hydroxysteroid dehydrogenase) and FPV064 (glutathione peroxidase), as well as FPV097, FPV098, FPV099, FPV107, FPV122, and FPV123 (VAR B22R homologues). Areas numbered 1 to 3 indicate novel coding regions at junction sites of major genome rearrangement and correspond to similarly numbered boxes in Fig. 1.

The FPV genome (260 to 309 kbp) is larger than other completely sequenced ChPV genomes (178 to 191 kbp). This size difference is due largely to the presence of multiple and, in some cases, large gene families. In other ChPVs, gene families contain fewer members (e.g., genes encoding ankyrin and serpins) or are represented as a single gene (e.g., genes encoding N1R/p28, B22R, CC chemokine, and NKG2-like proteins). Notably, the FPV ankyrin repeat family (31 genes), N1R/p28 family (10 genes), and B22R family (6 genes) comprise 32% of the total genome. In addition, cellular homologues novel to FPV are often found in multiple copies (e.g., beta -NGF, alpha -SNAP, and dCK). It has been suggested that the size of the ankyrin repeat multigene family may affect poxvirus host range (145). The large number of FPV multigene family members, together with the wide avian host range of FPV, provides support for the role of gene families in host range (169).

Conclusions. FPV genome analysis provides basic knowledge of viral functions, including mRNA biogenesis, DNA replication and repair, nucleotide metabolism, protein processing, manipulation of cellular responses, viral virulence, and host range, which underlie FPV interactions with its avian host and the environment. An improved understanding of these interactions will permit the engineering of novel vaccine viruses and expression vectors with enhanced efficacy and greater versatility. Additionally, the identification and characterization of FPV virulence and host range genes will contribute novel concepts to our overall understanding of pathogen-host interactions, information that is likely to have a broad impact on future strategies for controlling avian infectious diseases in general.


    ACKNOWLEDGMENTS

We thank Scott Taylor for providing the NVSL challenge strain of FPV; A. Ciupryk and G. Smoliga for excellent technical assistance; and W. H. Martinez, F. P. Horn, and R. G. Breeze for interest and encouragement.


    FOOTNOTES

* Corresponding author. Mailing address: Plum Island Animal Disease Center, P.O. Box 848, Greenport, NY 11944-0848. Phone: (516) 323-3330. Fax: (516) 323-2507. E-mail: drock{at}cshore.com.


    REFERENCES
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References

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