- Open Access
Antibody dependent enhancement of frog virus 3 infection
© Eaton et al; licensee BioMed Central Ltd. 2010
- Received: 6 December 2009
- Accepted: 18 February 2010
- Published: 18 February 2010
Viruses included in the family Iridoviridae are large, icosahedral, dsDNA viruses that are subdivided into 5 genera. Frog virus 3 (FV3) is the type species of the genus Ranavirus and the best studied iridovirus at the molecular level. Typically, antibodies directed against a virus act to neutralize the virus and limit infection. Antibody dependent enhancement occurs when viral antibodies enhance infectivity of the virus rather than neutralize it.
Here we show that anti-FV3 serum present at the time of FV3 infection enhances infectivity of the virus in two non-immune teleost cell lines. We found that antibody dependent enhancement of FV3 was dependent on the Fc portion of anti-FV3 antibodies but not related to complement. Furthermore, the presence of anti-FV3 serum during an FV3 infection in a non-immune mammalian cell line resulted in neutralization of the virus. Our results suggest that a cell surface receptor specific to teleost cell lines is responsible for the enhancement.
This report represents the first evidence of antibody dependent enhancement in iridoviruses. The data suggests that anti-FV3 serum can either neutralize or enhance viral infection and that enhancement is related to a novel antibody dependent enhancement pathway found in teleosts that is Fc dependent.
- Dengue Virus
- Antibody Dependent Enhancement
- Mammalian Fibroblast
- Ranavirus Infection
- Iridovirus Infection
Following a viral infection an immune response is elicited by the host, which includes both an innate and adaptive response. During the adaptive immune response, antibodies are produced that are designed to recognize and neutralize a pathogen. Typically, viral antibodies neutralize a virus by preventing the attachment of specific cell surface receptors with viral glycoproteins, while also activating the complement system. However, not all antibodies serve to reduce infectivity. Antibody dependent enhancement (ADE) occurs when viral antibodies enhance infectivity of a virus by promoting the attachment of viral particles to cells. Virus specific antibodies bind to viral particles to form complexes that can bypass normal routes of viral attachment and entry. The virus+antibody complex allows for increased viral entry or infection of cells that would not normally become infected. Virus+antibody complexes therefore result in a more efficient infection than with virus alone.
There are several mechanisms of how ADE can occur. The most common mechanism of ADE is Fc receptor (FcR)-dependent . In FcR-dependent ADE the virus+antibody complex binds to cells containing FcRs on their surface. The interaction is mediated between the exposed Fc region of the antibody (from the virus+antibody complex) and the FcR on the cell surface. FcRs are found on a wide variety of cells of the immune system, including macrophages, B cells, neutrophils, monocytes, and granulocytes [2, 3]. However, since not all cells that exhibit ADE are immune cells, another mechanism must be responsible for ADE in non-FcR bearing cells. Complement-mediated ADE is not exclusive to FcR bearing cells because complement receptors are found on a large variety of cell types . Complement-mediated ADE occurs via binding between the Fc region of antibodies and C1q . This can result in a variety of outcomes including the activation of complement, which causes complement C3 fragment and viral surface proteins to bind and promote viral attachment. C1q can also enhance virus attachment by binding to C1qR on the cell surface, which brings the virus into close proximity to cells.
ADE can result in increased viral pathogenesis because it enhances a virus's ability to bind to cells. It therefore can result in increased severity of disease. This was first shown with dengue virus where a second infection resulted in an increased number of infected cells and higher levels of virus production [5, 6]. An in vitro study suggested that the mechanism behind ADE in dengue virus was FcR-dependent [7–9]. Dengue virus titer was enhanced dramatically through the binding of the virus+antibody complex to FcRs found on cells of the immune system [7–9].
While ADE has been demonstrated for many RNA viruses, only a few DNA virus families, including poxviruses  and herpesviruses [11–13] have been shown to use ADE as a mechanism of infection. While it is suggested that they most likely use FcR-dependent ADE , little is actually known about the mechanism of ADE in the large DNA viruses. We decided to determine if viruses from the family Iridoviridae use ADE as a mechanism of infection. Viruses in the family Iridoviridae are large (~120-200 nm), icosahedral viruses that contain a linear, double-stranded DNA genome. Iridovirus infections appear to be restricted to invertebrates (Iridovirus, Chloriridovirus) and poikilothermic vertebrates (Lymphocystivirus, Ranavirus, Megalocytivirus) . Although iridoviruses are large DNA viruses, very little is known about their biology. Using frog virus 3 (FV3; Ranavirus) as a model virus, we propose to investigate whether ADE occurs in viruses of the family Iridoviridae, specifically in the Ranavirus genus.
ADE increases FV3 infection in teleost cells
Anti-FV3 serum neutralizes infection in BGMK cells
Addition of pre-immune serum to BF-2 cells inhibits ADE of FV3 infectivity
Protein A eliminates ADE of FV3 infectivity
ADE of FV3 infectivity is complement-independent
To determine whether FV3 ADE was complement-dependent, anti-FV3 serum and pre-immune serum were heat-inactivated to inactivate complement, or incubated with either EGTA or zymosan A. EGTA is a chelator that inhibits the classical complement pathway, while zymosan A disrupts the alternative complement pathway. Treated anti-FV3 serum or pre-immune serum was incubated with FV3 before addition to BF-2 cells. Forty-eight hours post-overlay plaques were counted. Infection by the FV3+anti-FV3 serum complexes treated with heat-inactivation, EGTA, or zymosan A did not reduce the ADE of FV3 infectivity as compared to the untreated FV3+anti-FV3 serum control (Figure 4B, Additional file 5A, 5B, 5C). Regardless of whether high or low levels of complement activity were present at the time of infection, enhancement was not affected by complement inhibitors suggesting that inactivation of complement does not disrupt ADE of FV3 infectivity.
Fc binding proteins on teleost cells
While ADE has been previously reported for some large DNA viruses, including herpesviruses [11–13] and poxviruses , no studies to date have demonstrated ADE as a mechanism to enhance infections in iridoviruses. This paper provides the first evidence of ADE in iridoviruses, specifically in the Ranavirus genus.
In this study, anti-FV3 serum demonstrated the ability to either neutralize or enhance an FV3 infection depending on the cell line. Although the infection was less efficient in mammalian cells, FV3 exhibited the ability to enter the cell and spread as was revealed by the presence of numerous plaques post-infection. The addition of anti-FV3 serum to an FV3 infection in BGMK cells dramatically reduced plaque number and size demonstrating the ability of the anti-FV3 serum to neutralize the infection in a mammalian cell line. However, the opposite effect was seen in teleost (BF-2 and FHM) cell lines. ADE often occurs with neutralizing antibodies at sub-neutralizing concentrations and differences in the interaction between virus and antibody can lead to either neutralization or enhancement of a viral infection . Furthermore, enhancement of an infection is particularly sensitive to this interaction and can also involve the target cell. Our data suggests that the anti-FV3 serum used in this study possess both neutralizing and enhancing activity, depending on various factors including the cell type and the concentration of antibody.
Ranaviruses, including FV3, have been isolated from a variety of species including fish and amphibians. While FV3 has never been isolated from fish in vivo, other closely related (over 98% sequence identity of the major capsid protein ) ranaviruses, including epizootic haematopoietic necrosis virus (EHNV) and Bohle virus (BIV) infect fish and infection can result in high levels of morbidity and mortality [18–20]. FV3 shows high levels of infectivity in fish cell lines in vitro [21–23]; therefore two fish cells lines (BF-2 and FHM) were used during this study. While there are many differences from mammalian immune systems, the immune systems of fish and amphibians are fundamentally similar to mammals with both innate immunity and adaptive immune functions [24, 25]. However, immunoglobins of lower vertebrates are currently poorly understood as compared to those of mammals. Fish were the first group to have demonstrated antibody activity and have one predominant Ig isotype, an IgM-like tetrameric molecule . Amphibians have several isotypes including IgY, which is the predominant isotype in amphibians and is considered the functional equivalent to mammalian IgG [27–29]. However, the adaptive immune system of mammals is fundamentally similar to that of lower vertebrates and is characterized by T cell receptors, Ig, and the major histocompatibility complex (MHC). Lower vertebrates also rely heavily on non-specific defense systems for pathogen defense and therefore the innate immune system of lower vertebrates, including complement, is diverse and similar to that of higher vertebrates. We therefore suspect that the mechanisms behind ADE in fish and amphibians will be similar to that of mammals. While we feel the mechanisms behind ADE to be similar between fish, amphibians, and mammals, there are some inherent differences between the immune systems of each species. It will be important to confirm these experiments in the future using sera from either immunized frogs or fish.
Common mechanisms behind ADE can be dependent on either complement or FcRs. Our results suggest that complement pathways (classical or alternative) do not play a role in the enhancement of FV3 infection by anti-FV3 serum. However, protein A eliminated any enhancement of the anti-FV3 serum suggesting the mechanism behind FV3 ADE to be FcR-dependent. Many virus families, including other DNA viruses, enhance viral infection through the binding of the Fc region of anti-viral antibodies to FcR on the surface of cells of the immune system [30–37]. However, this result is intriguing because both cell lines that exhibited ADE (BF-2 and FHM) in this study are non-immune (fibroblast and epithelial, respectively) cell lines that should lack FcR on the cell surface [2, 3, 9]. While recent research suggests that teleosts and amphibians possess both FcR homologs and novel immune-type receptors (NITRs) [38–42], little is known about their tissue distribution and role in innate immunity. FcRs in humans are a variety of sizes that can range from 40 kDa to over 70 kDa [43–46], while one previously identified FcR in fish was predicted to be ~33 kDa in size . We identified two proteins (38 kDa and 95 kDa) in teleost cells (but not in a mammalian cell line) that bound to the Fc region of rabbit antibodies. The molecular weight of these proteins does not rule out the possibility that they may function as novel FcRs in teleosts. While we do not specifically know what the anti-FV3 serum is binding to mediate ADE, the results suggest that proteins specific to teleost cells bind to the Fc region of antibodies potentially mediating ADE.
Iridovirus infections of increased pathogenicity have been recently observed in several wild and cultivated fish and amphibian species [17, 47, 48]. Specifically, ranavirus infections pose a potential threat to amphibians and have been implicated in the widespread decline of worldwide amphibian populations [48, 49]. There have recently been increasing reports of ranavirus infections, with both the severity of infections and the number of species infected increasing [17, 50–55]. While evidence suggests that an iridovirus infection mounts a strong immune response [56, 57], this does not eliminate the possibility that viral infection can be enhanced under certain circumstances. Although humoral immunity is required for protection against viruses, antibodies at sub-neutralizing concentrations may enhance, rather than protect against infection . It is also possible that the virus utilizes ADE as a method for more efficient entry. Regardless of whether a strong immune response is mounted, ADE may promote increased entry or entry into cells not usually infected. In particular, ADE in immunocompromised individuals may allow for increased infection. Furthermore, the link between ADE in vitro and in vivo currently remains elusive. For instance, ADE of dengue viruses has been well documented and extensively characterized in vitro, but in vivo studies remain unclear and controversial [58–60]. It will be important for future experiments to confirm these in vitro studies using live fish and frogs. Ranavirus infections are spreading rapidly worldwide, however, the reasons behind this rapid spread are currently unknown and are most likely complex. While FV3 ADE has yet to be demonstrated in vivo, a strong second infection of FV3 may explain the increased severity and prevalence of ranavirus infections. Therefore, ADE may represent a potential hypothesis for the recent emergence and increased severity of ranavirus infections.
This study demonstrates for the first time that FV3, an iridovirus, utilizes ADE to increase infection in vitro. The anti-FV3 serum used in this study both enhanced and neutralized a viral infection depending on cell type and concentration. The mechanism behind enhancement was found to be independent of complement but dependent upon the Fc region of anti-FV3 antibodies. The addition of protein A to either anti-FV3 serum or teleost cells completely abolished ADE. This result was surprisingly because two non-immune cell lines most likely lacking FcR were used during this experiment. Our results suggests that the Fc region of anti-FV3 antibodies may promote viral entry through novel Fc binding activity on teleost cells.
Cell lines and virus
Bluegill fry (BF-2) cells were obtained from American Type Culture Collection (ATCC, Manassas, VA) and were grown at 28°C in 5% CO2 in Eagle's Minimal Essential medium with Earle's balanced salts (EMEM; HyClone, Ottawa, ON) and 2 mM L-glutamine supplemented with 10% fetal bovine serum (FBS), 1.0 mM sodium pyruvate, 0.1 mM nonessential amino acids, and antibiotics (100 U/mL penicillin and 100 g/mL streptomycin). Baby green monkey kidney (BGMK) cells were obtained from ATCC and were maintained in Dulbecco's modified Eagle's medium (DMEM; HyClone) supplemented with 7% FBS, 2 mM L-glutamine, penicillin (100 U/mL), and streptomycin (100 g/mL) at 37°C with 5% CO2. We have previously characterized an FV3 infection in BGMK cells . Fathead minnow (FHM) cells were also obtained from ATCC and were maintained at 30°C in minimum essential medium with Hanks' salts (MEM; Invitrogen, Burlington, ON) supplemented with 10% FBS, penicillin (100 U/mL), and streptomycin (100 g/mL). FV3 was obtained from ATCC and rabbit anti-FV3 serum and rabbit pre-immune serum were kindly provided by V.G. Chinchar (University of Mississippi Medical Center, Jackson, MS). Once BGMK cells were infected with FV3 they were incubated at 28°C with 5% CO2.
ADE plaque assay
FV3 (~50 PFU) was mixed with either rabbit anti-FV3 serum or control rabbit pre-immune serum (0 ng, 10 ng, 50 ng, 100 ng, 200 ng, and 300 ng total serum protein) for a final volume of 100 μL in media and was incubated for 1 hour at 4°C. The FV3+anti-FV3 serum or FV3+pre-serum complexes were then added to BF-2, FHM, or BGMK cells grown to 90% confluence in 6-well plates. BF-2 and BGMK cells were overlaid with 2% agarose 2 hours post-infection. Forty-eight hours post-overlay cells were either stained with crystal violet (0.05%) or underwent indirect immunofluorescence and plaques were counted. FHM cells were incubated for 24 hours and indirect immunofluorescence was carried out and plaques were counted.
Pre-immune serum challenge
Rabbit anti-FV3 serum (50 ng total serum protein) or rabbit pre-immune serum (50 ng total serum protein) were mixed with FV3 (~50 PFU) in a final volume of 100 μL in EMEM and were incubated for 1 hour at 4°C. Pre-immune serum was added to BF-2 cells grown to 90% confluence in 6-well dishes for final concentrations of 0 ng/μL, 0.1 ng/μL, 0.5 ng/μL, and 1 ng/μL. FV3+anti-FV3 serum or FV3+pre-immune serum complexes were added to BF-2 cells containing pre-immune serum and were incubated for 2 hours. Cells were overlaid with 2% agarose and 48 hours post-overlay crystal violet (0.05%) was added to cells and plaques were counted.
Inhibition of Fc and complement
Rabbit anti-FV3 serum (0-150 ng total serum protein) or rabbit pre-immune serum (0-150 ng total serum protein) were incubated with protein A (300 μg/mL; Sigma, Oakville, ON) or EGTA (0.05 M) for 30 minutes at room temperature, zymosan A (20 mg/mL; Sigma) for 1 hour at 37°C, or were heat-inactivated at 56°C for 30 minutes. Approximately 50 PFU of FV3 was added and the FV3+anti-FV3 serum or FV3+pre-immune serum complexes were brought up to a final volume of 100 μL with serum-free EMEM. An ADE plaque assay in BF-2 cells was then performed. Protein A (300 μg/mL) was incubated with BF-2 cells for 30 minutes at room temperature. Cells were washed several times with PBS and 50 PFU of FV3 previously incubated with 0-150 ng anti-FV3 serum or pre-immune serum for one hour at 4°C were added to the cells. An ADE plaque assay using 0 ng, 10 ng, 50 ng, 100 ng, and 150 ng of rabbit anti-FV3 serum or control rabbit pre-immune serum was then performed.
Cells were fixed for 10 minutes in 3.7% paraformaldehyde in phosphate buffer saline (PBS). Following several washes, cells were incubated in block buffer (5% bovine serum albumin (BSA) (w/v), 50 mM Tris HCl (pH 7.4), 150 mM NaCl, 0.5% NP-40 (v/v)) overnight at 4°C. Cells were incubated with rabbit anti-FV3 serum (dilution: 1/1000) for one hour at room temperature. Cells were then incubated in FITC-conjugated goat anti-rabbit immunoglobulin G (IgG) (dilution: 1/100) (Jackson ImmunoResearch Inc., West Grove, PA) and Texas Red®-X Phalloidin (dilution 1/40) (Invitrogen) for one hour at room temperature. Finally, cells were incubated for 2 minutes in the nucleic acid stain DAPI (Invitrogen) diluted to 300 nM in PBS. Immunofluorescence was detected using a Leica DM6000 B fluorescent microscope (Leica, Wetzlar, Germany). Images were assembled using Adobe Photoshop CS4 (Adobe, San Jose, CA).
BGMK, BF-2, and FHM cells grown to 100% confluence in a 6-well dish were scraped into the media and centrifuged at 10,000 × g for 5 minutes. The supernatant was removed and the cells were re-suspended in Laemmli reducing buffer . Cell lysates were boiled and proteins were separated on a 10% polyacrylamide gel using sodium dodecyl sulfate (SDS) running buffer (125 mM Tris, 1.25 M glycine, 0.5% SDS). Following electrophoresis, the proteins were transferred from the gel to a polyvinylidene difluoride (PVDF) membrane using a semi-dry transfer apparatus (FisherBiotech, Pittsburgh, PA). The membrane was blocked overnight at 4°C in TBST buffer (140 mM NaCl, 24 mM Tris (pH 7.4), 0.2% Tween® 20, 3 mM KCl) containing 5% non-fat milk powder. The membrane was incubated without primary serum, rabbit pre-immune serum (dilution 1:1000), rabbit pre-immune serum pre-incubated with 300 μg/mL protein A for 30 minutes at room temperature (dilution 1:1000), or a second unrelated rabbit pre-immune serum (dilution 1:1000) for 1 hour shaking at room temperature. The membrane was washed several times then incubated for 1 hour shaking at room temperature in peroxidase-conjugated AffiniPure F(ab')2 fragment goat anti-rabbit IgG (Jackson ImmunoResearchInc.) diluted 1/10,000. The membrane was washed several times and proteins were detected by applying Chemiluminescence Reagent Plus (Perkin-Elmer, Boston, MA) to the membrane as per the manufacture's protocol. The images were then viewed using a Genius2 Bio Imaging System (Syngene, Frederick, MD).
We thank Dr. V.G. Chinchar of the University of Mississippi Medical Center for generously providing the rabbit anti-FV3 serum and rabbit pre-immune serum. This work is supported by Discovery Grants (Natural Science and Engineering Research Council (NSERC) of Canada) to C.R.B. H.E.E. is the recipient of a NSERC postgraduate scholarship.
- Takada A, Kawaoka Y: Antibody-dependent enhancement of viral infection: molecular mechanisms and in vivo implications. Rev Med Virol 2003, 13: 387-398. 10.1002/rmv.405PubMedView ArticleGoogle Scholar
- Ravetch JV, Kinet JP: Fc receptors. Annu Rev Immunol 1991, 9: 457-492.PubMedView ArticleGoogle Scholar
- Daeron M: Fc receptor biology. Annu Rev Immunol 1997, 15: 203-234. 10.1146/annurev.immunol.15.1.203PubMedView ArticleGoogle Scholar
- Ross GD: Complement receptors. In Encyclopedia of Immunology. Edited by: Roitt IM, Delves PJ. San Diego: Academic Press; 1992:388-391.Google Scholar
- Sangkawibha N, Rojanasuphot S, Ahandrik S, Viriyapongse S, Jatanasen S, Salitul V, Phanthumachinda B, Halstead SB: Risk factors in dengue shock syndrome: a prospective epidemiologic study in Rayong, Thailand. I. The 1980 outbreak. Am J Epidemiol 1984, 120: 653-669.PubMedGoogle Scholar
- Halstead SB: Dengue haemorrhagic fever--a public health problem and a field for research. Bull World Health Organ 1980, 58: 1-21.PubMedPubMed CentralGoogle Scholar
- Klimstra WB, Williams JC, Ryman KD, Heidner HW: Targeting Sindbis virus-based vectors to Fc receptor-positive cell types. Virology 2005, 338: 9-21. 10.1016/j.virol.2005.04.039PubMedView ArticleGoogle Scholar
- Rulli NE, Suhrbier A, Hueston L, Heise MT, Tupanceska D, Zaid A, Wilmes A, Gilmore K, Lidbury BA, Mahalingam S: Ross River virus: molecular and cellular aspects of disease pathogenesis. Pharmacol Ther 2005, 107: 329-342. 10.1016/j.pharmthera.2005.03.006PubMedView ArticleGoogle Scholar
- Sullivan NJ: Antibody-mediated enhancement of viral disease. Curr Top Microbiol Immunol 2001, 260: 145-169.PubMedGoogle Scholar
- Hawkes RA, Lafferty KJ: The enchancement of virus infectivity by antibody. Virology 1967, 33: 250-261. 10.1016/0042-6822(67)90144-4PubMedView ArticleGoogle Scholar
- Ghiasi H, Perng GC, Nesburn AB, Wechsler SL: Antibody-dependent enhancement of HSV-1 infection by anti-gK sera. Virus Res 2000, 68: 137-144. 10.1016/S0168-1702(00)00165-9PubMedView ArticleGoogle Scholar
- Inada T, Chong KT, Mims CA: Enhancing antibodies, macrophages and virulence in mouse cytomegalovirus infection. J Gen Virol 1985, 66: 871-878. 10.1099/0022-1317-66-4-871PubMedView ArticleGoogle Scholar
- Sixbey JW, Yao QY: Immunoglobulin A-induced shift of Epstein-Barr virus tissue tropism. Science 1992, 255: 1578-1580. 10.1126/science.1312750PubMedView ArticleGoogle Scholar
- Chinchar VG, Essbauer S, He JG, Hyatt A, Miyazaki T, Seligy V, Williams T: Family Iridoviridae . In Virus Taxonomy Eight Report of the International Committee on Taxonomy of Viruses. Edited by: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA. San Diego: Academic Press; 2005:145-162.Google Scholar
- Granoff A: Viruses of amphibia. Curr Top Microbiol Immunol 1969, 50: 107-137.PubMedGoogle Scholar
- Burton DR, Williamson RA, Parren PW: Antibody and virus: binding and neutralization. Virology 2000, 270: 1-3. 10.1006/viro.2000.0239PubMedView ArticleGoogle Scholar
- Hyatt AD, Gould AR, Zupanovic Z, Cunningham AA, Hengstberger S, Whittington RJ, Kattenbelt J, Coupar BE: Comparative studies of piscine and amphibian iridoviruses. Arch Virol 2000, 145: 301-331. 10.1007/s007050050025PubMedView ArticleGoogle Scholar
- Langdon JS, Humphrey JD, Williams LM, Hyatt AD, Westbury HA: First virus isolation from Australian fish: an iridovirus-like pathogen from redfin perch, Perca fluviatilis L. J Fish Dis 1986, 9: 263-268. 10.1111/j.1365-2761.1986.tb01011.xView ArticleGoogle Scholar
- Langdon JS: Experimental transmission and pathogenicity of epizootic hematopoietic necrosis virus (EHNV) in redfin perch, Perca fluviatilis L., and 11 other species of teleosts. J Fish Dis 1989, 12: 295-310. 10.1111/j.1365-2761.1989.tb00318.xView ArticleGoogle Scholar
- Moody N, Owens L: Experimental demonstration of the pathogenicity of frog virus, Bohle iridovirus, for a fish species, barramundi, Lates calcarifer . Dis Aquat Organ 1994, 18: 95-102. 10.3354/dao018095View ArticleGoogle Scholar
- Goorha R: Frog virus 3 DNA replication occurs in two stages. J Virol 1982, 43: 519-528.PubMedPubMed CentralGoogle Scholar
- Gravell M, Naegele RF: Nongenetic reactivation of frog polyhedral cytoplasmic deoxyribovirus (PCDV). Virology 1970, 40: 170-174. 10.1016/0042-6822(70)90390-9PubMedView ArticleGoogle Scholar
- Naegele RF, Granoff A: Viruses and renal carcinoma of Rana pipiens. XI. Isolation of frog virus 3 temperature-sensitive mutants; complementation and genetic recombination. Virology 1971, 44: 286-295. 10.1016/0042-6822(71)90260-1PubMedView ArticleGoogle Scholar
- Du L, Du Pasquier L, Schwager J, Flajnik MF: The immune system of Xenopus . Annu Rev Immunol 1989, 7: 251-275.View ArticleGoogle Scholar
- Tort L, Balasch JC, Mackenzie S: Fish immune system: A crossroads between immune and adaptive responses. Immunologia 2003, 22: 277-286.Google Scholar
- Kaattari SL, Piganelli JD: The specific immune system: humoral defense. In The Immune System of Fish: Organism, Pathogen, and Environment. Volume 15. Edited by: Iwama G, Nakanishi T. San Diego: Academic Press Inc; 1996.Google Scholar
- Fellah JS, Kerfourn F, Wiles MV, Schwager J, Charlemagne J: Phylogeny of immunoglobulin heavy chain isotypes: structure of the constant region of Ambystoma mexicanum upsilon chain deduced from cDNA sequence. Immunogenetics 1993, 38: 311-317. 10.1007/BF00210471PubMedView ArticleGoogle Scholar
- Hadji-Azimi I: Anuran immunoglobulins. A review. Dev Comp Immunol 1979, 3: 233-243.PubMedView ArticleGoogle Scholar
- Mussmann R, Wilson M, Marcuz A, Courtet M, Du Pasquier L: Membrane exon sequences of the three Xenopus Ig classes explain the evolutionary origin of mammalian isotypes. Eur J Immunol 1996, 26: 409-414. 10.1002/eji.1830260221PubMedView ArticleGoogle Scholar
- Dworak LJ, Wolfinbarger JB, Bloom ME: Aleutian mink disease parvovirus infection of K562 cells is antibody-dependent and is mediated via an Fc(gamma)RII receptor. Arch Virol 1997, 142: 363-373. 10.1007/s007050050082PubMedView ArticleGoogle Scholar
- Halstead SB, O'Rourke EJ: Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J Exp Med 1977, 146: 201-217. 10.1084/jem.146.1.201PubMedPubMed CentralView ArticleGoogle Scholar
- Joseph T, Kibenge MT, Kibenge FS: Antibody-mediated growth of infectious salmon anaemia virus in macrophage-like fish cell lines. J Gen Virol 2003, 84: 1701-1710. 10.1099/vir.0.19087-0PubMedView ArticleGoogle Scholar
- Kanno H, Wolfinbarger JB, Bloom ME: Aleutian mink disease parvovirus infection of mink peritoneal macrophages and human macrophage cell lines. J Virol 1993, 67: 2075-2082.PubMedPubMed CentralGoogle Scholar
- Lidbury BA, Mahalingam S: Specific ablation of antiviral gene expression in macrophages by antibody-dependent enhancement of Ross River virus infection. J Virol 2000, 74: 8376-8381. 10.1128/JVI.74.18.8376-8381.2000PubMedPubMed CentralView ArticleGoogle Scholar
- Ochiai H, Kurokawa M, Matsui S, Yamamoto T, Kuroki Y, Kishimoto C, Shiraki K: Infection enhancement of influenza A NWS virus in primary murine macrophages by anti-hemagglutinin monoclonal antibody. J Med Virol 1992, 36: 217-221. 10.1002/jmv.1890360312PubMedView ArticleGoogle Scholar
- Olsen CW, Corapi WV, Ngichabe CK, Baines JD, Scott FW: Monoclonal antibodies to the spike protein of feline infectious peritonitis virus mediate antibody-dependent enhancement of infection of feline macrophages. J Virol 1992, 66: 956-965.PubMedPubMed CentralGoogle Scholar
- Porterfield JS: Antibody-dependent enhancement of viral infectivity. Adv Virus Res 1986, 31: 335-355. full_textPubMedView ArticleGoogle Scholar
- Evenhuis J, Bengten E, Snell C, Quiniou SM, Miller NW, Wilson M: Characterization of additional novel immune type receptors in channel catfish, Ictalurus punctatus. Immunogenetics 2007, 59: 661-671. 10.1007/s00251-007-0230-xPubMedView ArticleGoogle Scholar
- Hawke NA, Yoder JA, Haire RN, Mueller MG, Litman RT, Miracle AL, Stuge T, Shen L, Miller N, Litman GW: Extraordinary variation in a diversified family of immune-type receptor genes. Proc Natl Acad Sci USA 2001, 98: 13832-13837. 10.1073/pnas.231418598PubMedPubMed CentralView ArticleGoogle Scholar
- Stafford JL, Wilson M, Nayak D, Quiniou SM, Clem LW, Miller NW, Bengten E: Identification and characterization of a FcR homolog in an ectothermic vertebrate, the channel catfish (Ictalurus punctatus). J Immunol 2006, 177: 2505-2517.PubMedView ArticleGoogle Scholar
- Yoder JA, Mueller MG, Wei S, Corliss BC, Prather DM, Willis T, Litman RT, Djeu JY, Litman GW: Immune-type receptor genes in zebrafish share genetic and functional properties with genes encoded by the mammalian leukocyte receptor cluster. Proc Natl Acad Sci USA 2001, 98: 6771-6776. 10.1073/pnas.121101598PubMedPubMed CentralView ArticleGoogle Scholar
- Strong SJ, Mueller MG, Litman RT, Hawke NA, Haire RN, Miracle AL, Rast JP, Amemiya CT, Litman GW: A novel multigene family encodes diversified variable regions. Proc Natl Acad Sci USA 1999, 96: 15080-15085. 10.1073/pnas.96.26.15080PubMedPubMed CentralView ArticleGoogle Scholar
- Albrechtson M, Yeaman GR, Kerr MA: Characterization of the IgA receptor from human polymorphonuclear leucocytes. Immunology 1988., 64:Google Scholar
- Calabi F, Neuberger MS: Molecular Genetics of Immunoglobulin. In New Comprehensive Biochemistry. Volume 17. Edited by: Neuberger A, Van Deenen LLM. New York: Elsevier Science Publishers; 1987.Google Scholar
- Delespesse G, Sarfati M, Hofstetter H, Frost H, Kilchherr E, Suter U: Human Fc epsilon R II and IgE-binding factors. Int Arch Allergy Appl Immunol 1989, 88: 18-22. 10.1159/000234741PubMedView ArticleGoogle Scholar
- Monteiro RC, Kubagawa H, Cooper MD: Cellular distribution, regulation, and biochemical nature of an Fc alpha receptor in humans. J Exp Med 1990, 171: 597-613. 10.1084/jem.171.3.597PubMedView ArticleGoogle Scholar
- Ahne W, Bremont M, Hedrick R, Hyatt A, Whittington R: Special topic review: iridoviruses associated with epizootic haematopoietic necrosis (EHN) in aquaculture. World J Microb Biot 1997, 13: 367-373. 10.1023/A:1018563930712View ArticleGoogle Scholar
- Daszak P, Berger L, Cunningham AA, Hyatt AD, Green DE, Speare R: Emerging infectious diseases and amphibian population declines. Emerg Infect Dis 1999, 5: 735-748. 10.3201/eid0506.990601PubMedPubMed CentralView ArticleGoogle Scholar
- Carey C, Cohen N, Rollins-Smith L: Amphibian declines: an immunological perspective. Dev Comp Immunol 1999, 23: 459-472. 10.1016/S0145-305X(99)00028-2PubMedView ArticleGoogle Scholar
- Chinchar VG: Ranaviruses (family Iridoviridae): emerging cold-blooded killers. Arch Virol 2002, 147: 447-470. 10.1007/s007050200000PubMedView ArticleGoogle Scholar
- Cunningham AA, Langton TE, Bennett PM, Lewin JF, Drury SE, Gough RE, Macgregor SK: Pathological and microbiological findings from incidents of unusual mortality of the common frog (Rana temporaria). Philos Trans R Soc Lond B Biol Sci 1996, 351: 1539-1557. 10.1098/rstb.1996.0140PubMedView ArticleGoogle Scholar
- De Voe R, Geissler K, Elmore S, Rotstein D, Lewbart G, Guy J: Ranavirus-associated morbidity and mortality in a group of captive eastern box turtles ( Terrapene carolina carolina ). J Zoo Wild Med 2004, 35: 534-543. 10.1638/03-037View ArticleGoogle Scholar
- Jancovich JK, Davidson EW, Morado JF, Jacobs BL, Collins JP: Isolation of a lethal virus from the endangered tiger salamander Ambystoma tigrinum stebbins . Dis Aquat Organ 1997, 31: 161-167. 10.3354/dao031161View ArticleGoogle Scholar
- Jancovich JK, Davidson EW, Parameswaran N, Mao J, Chinchar VG, Collins JP, Jacobs BL, Storfer A: Evidence for emergence of an amphibian iridoviral disease because of human-enhanced spread. Mol Ecol 2005, 14: 213-224. 10.1111/j.1365-294X.2004.02387.xPubMedView ArticleGoogle Scholar
- Zhang QY, Xiao F, Li ZQ, Gui JF, Mao J, Chinchar VG: Characterization of an iridovirus from the cultured pig frog Rana grylio with lethal syndrome. Dis Aquat Organ 2001, 48: 27-36. 10.3354/dao048027PubMedView ArticleGoogle Scholar
- Maniero GD, Morales H, Gantress J, Robert J: Generation of a long-lasting, protective, and neutralizing antibody response to the ranavirus FV3 by the frog Xenopus. Dev Comp Immunol 2006, 30: 649-657. 10.1016/j.dci.2005.09.007PubMedView ArticleGoogle Scholar
- Morales HD, Robert J: Characterization of primary and memory CD8 T-cell responses against ranavirus (FV3) in Xenopus laevis. J Virol 2007, 81: 2240-2248. 10.1128/JVI.01104-06PubMedPubMed CentralView ArticleGoogle Scholar
- Goncalvez AP, Engle RE, St Claire M, Purcell RH, Lai CJ: Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc Natl Acad Sci USA 2007, 104: 9422-9427. 10.1073/pnas.0703498104PubMedPubMed CentralView ArticleGoogle Scholar
- Halstead SB: In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J Infect Dis 1979, 140: 527-533.PubMedView ArticleGoogle Scholar
- Rosen L: Disease exacerbation caused by sequential dengue infections: myth or reality? Rev Infect Dis 1989,11(Suppl 4):S840-842.PubMedView ArticleGoogle Scholar
- Eaton H, Metcalf J, Brunetti CR: Expression of frog virus 3 genes is impaired in mammalian cell lines. Virol J 2008, 5: 83. 10.1186/1743-422X-5-83PubMedPubMed CentralView ArticleGoogle Scholar
- Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227: 680-685. 10.1038/227680a0PubMedView ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.