The neutralization of pseudorabies virus by anti-α-galactocyl natural antibody in normal serum

Hayashi, Shunichi; Ogawa, Seiji; Takashima, Yasuhiro; Otsuka, Hidenori

doi:10.1016/j.virusres.2003.09.008

Cited by 18 publications

(38 citation statements)

References 21 publications

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“…We also found that a similar phenomenon was observed when PRV grown in several cell lines was incubated with human serum [13]. PRV grown in several cell lines also showed different resistant levels against rabbit serum [13].It has been known that human immunodeficiency virus type 1 acquires cell membrane complement regulatory factors on its envelope from cells during the budding process, thereby escaping from complement attack [18]. Therefore it was assumed that RK-13-grown PRV acquired complement regulatory factors from the host rabbit cells and these were less effective against swine complement attack.…”

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confidence: 80%

supporting

confidence: 80%

“…We speculated that neutralization of PRV was caused by activation of complement via the alternative pathway because of the apparent absence of anti-PRV antibodies in swine serum [17]. We also found that a similar phenomenon was observed when PRV grown in several cell lines was incubated with human serum [13]. PRV grown in several cell lines also showed different resistant levels against rabbit serum [13].…”

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confidence: 55%

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Pseudorabies Virus Propagated in Rabbit Kidney-Derived RK13 Cells is Neutralized by Natural IgM Antibodies in Normal Swine Serum which Specifically Lyse Host Cells

Hayashi

Takashima

Otsuka

2005

The Journal of Veterinary Medical Science

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ABSTRACT. Pseudorabies virus (PRV) propagated in rabbit kidney-derived RK-13 cells (PRV-RK) was neutralized by serum obtained from specific pathogen-free pigs through the activation of complement. The virus-neutralizing activity of swine serum was lost after treatment with ethylene glycol-bis-aminoethylether-N,N,N',N'-tetraacetic acid (EGTA) or ethylenediaminetetraacetic acid (EDTA). Anti-C1q and anti-IgM antibodies also inhibited virus-neutralizing activity. Though IgG-depleted swine serum neutralized PRV, IgM and IgG-free swine serum lost virus-neutralizing activity. Pre-incubation of swine serum with RK-13 cells, but not with swine kidney-derived CPK cells, at 4°C eliminated the virus-neutralizing activity to PRV-RK. Results indicated that swine serum contained natural IgM against an antigen(s) on the RK-13 cell surface and that this surface antigen was integrated into the PRV envelope during the budding process. Thus the natural IgM in swine serum reacted with the RK-13 antigen on the viral envelope, activated the complement cascade and neutralized the PRV-RK. KEY WORDS: complement, natural antibodies, PRV.J. Vet. Med. Sci. 67(3): 229-234, 2005 We previously reported that pseudorabies virus (PRV) grown in rabbit kidney-derived RK-13 cells was neutralized by swine serum while the same virus grown in porcine kidney-derived CPK cells was resistant [17]. However, the virus-neutralizing activity of swine serum was lost when serum was heat-inactivated at 56°C for 30 min. We speculated that neutralization of PRV was caused by activation of complement via the alternative pathway because of the apparent absence of anti-PRV antibodies in swine serum [17]. We also found that a similar phenomenon was observed when PRV grown in several cell lines was incubated with human serum [13]. PRV grown in several cell lines also showed different resistant levels against rabbit serum [13].It has been known that human immunodeficiency virus type 1 acquires cell membrane complement regulatory factors on its envelope from cells during the budding process, thereby escaping from complement attack [18]. Therefore it was assumed that RK-13-grown PRV acquired complement regulatory factors from the host rabbit cells and these were less effective against swine complement attack. On the other hand PRV grown in CPK cells acquired swine complement regulatory factors which are more effective regulators against swine complement and thus were resistant to swine complement attack [17].However, further study revealed that RK-13 cells were lysed by swine serum via the activation of complement classical pathway (Hayashi et al., in preparation). It was found that swine serum contained natural IgM antibodies that specifically reacted with an antigen or antigens on the RK-13 cell surface. Therefore a question arose whether the anti-RK-13 natural IgM in swine serum is responsible for the neutralization of PRV grown in RK-13 cells.In this study, using swine serum and PRV propagated in RK-13 cells (PRV-RK), we investigated the mechanism for the virus-neu...

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confidence: 80%

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confidence: 80%

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confidence: 55%

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Pseudorabies Virus Propagated in Rabbit Kidney-Derived RK13 Cells is Neutralized by Natural IgM Antibodies in Normal Swine Serum which Specifically Lyse Host Cells

Hayashi

Takashima

Otsuka

2005

The Journal of Veterinary Medical Science

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“…For some viruses, including porcine endogenous retrovirus, pseudorabies virus, and lymphocytic choriomeningitis virus, neutralization by nonimmune human serum is triggered by natural antibodies binding to Gal␣1-3Gal epitopes on virus (21,37,43,47,50). However, we previously reported that naturally occurring antibodies to Gal␣1-3Gal are not involved in neutralizing HSV-1 virus (12).…”

Section: Discussionmentioning

confidence: 99%

Herpes Simplex Virus Type 1 and 2 Glycoprotein C Prevents Complement-Mediated Neutralization Induced by Natural Immunoglobulin M Antibody

Hook

Lubinski

Jiang

et al. 2006

J Virol

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Glycoprotein C (gC) of herpes simplex virus type 1 (HSV-1) and type 2 (HSV-2) binds complement component C3b and protects virus from complement-mediated neutralization. Differences in complement interacting domains exist between gC of HSV-1 (gC1) and HSV-2 (gC2), since the amino terminus of gC1 blocks complement C5 from binding to C3b, while gC2 fails to interfere with this activity. We previously reported that neutralization of HSV-1 gC-null virus by HSV antibody-negative human serum requires activation of C5 but not of downstream components of the classical complement pathway. In this report, we evaluated whether activation of C5 is sufficient to neutralize HSV-2 gC-null virus, or whether formation of the membrane attack complex by C6 to C9 is required for neutralization. We found that activation of the classical complement pathway up to C5 was sufficient to neutralize HSV-2 gC-null virus by HSV antibody-negative human serum. We evaluated the mechanisms by which complement activation occurred in seronegative human serum. Interestingly, natural immunoglobulin M antibodies bound to virus, which triggered activation of C1q and the classical complement pathway. HSV antibody-negative sera obtained from four individuals differed over an approximately 10-fold range in their potency for complement-mediated virus neutralization. These findings indicate that humans differ in the ability of their innate immune systems to neutralize HSV-1 or HSV-2 gC-null virus and that a critical function of gC1 and gC2 is to prevent C5 activation.Viruses employ a variety of mechanisms to evade both innate and adaptive immunity. Herpes simplex virus type 1 (HSV-1) establishes latency within the sensory ganglia of the peripheral nervous system, and interferes with the induction of interferon and immunity mediated by antibody and complement (5, 35, 39). HSV-1 also blocks cytotoxic T-lymphocyte activation by preventing antigen presentation by the major histocompatibility complex class I (15, 22, 51). HSV-1 encodes the immediate-early protein ICP47, which prevents the transport of antigenic peptides into the endoplasmic reticulum and subsequent loading onto major histocompatibility complex class I molecules.HSV-1 glycoproteins E (gE) and I (gI) together form a high-affinity Fc receptor (2,4,6,10,25,26). This receptor binds the Fc region of HSV-specific immunoglobulin G (IgG) antibodies in a process called antibody bipolar bridging (10). Antibody bipolar bridging blocks functions mediated by IgG, including antibody-dependent complement neutralization, antibody-dependent cellular cytotoxicity, and phagocytosis (7,10,40,49). In a murine flank model of infection, antibody is significantly more effective at protecting animals against disease caused by an HSV-1 mutant deficient in Fc receptor activity than by wild-type virus (40).HSV-1 glycoprotein C binds complement component C3b and inhibits the interaction of C5 and properdin (P) with C3b, blocking activation of both the classical and alternative complement pathways (11,23,32). HSV-1 gC prevent...

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“…Parasite growth is inhibited by antibody-dependent complement-mediated damage (11,13,14). Fresh sera with functional complement activity from catarrhines can also inactivate ␣Gal-expressing viruses, including various retroviruses (15)(16)(17)(18)(19) and other enveloped viruses, such as lymphocytic choriomeningitis virus (20,21) and pseudorabies virus (22). Sera from other mammals, including New World monkeys, rats, mice, and guinea pigs, do not lyse ␣Gal-expressing viruses, as these species do not naturally make anti-Gal (15)(16)(17).…”

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Possible Role of a Cell Surface Carbohydrate in Evolution of Resistance to Viral Infections in Old World Primates

Rodriguez

Welsh

2013

J Virol

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bDue to inactivation of the ␣1,3-galactosyltransferase gene (GGTA1, or the ␣1,3GT gene) approximately 28 million years ago, the carbohydrate ␣Gal (Gal␣1,3Gal␤1,4GlcNAc) is not expressed on the cells of Old World monkeys and apes (including humans) but is expressed in all other mammals. The proposed selective advantage of this mutation for these primates is the ability to produce anti-Gal antibodies, which may be an effective immune component in neutralizing ␣Gal-expressing pathogens. However, loss of ␣1,3GT expression may have been advantageous by providing natural resistance against viral pathogens that exploited the ␣1,3GT pathway or cell surface ␣Gal for infection. Infections of paired cell lines with differential expression of ␣1,3GT showed that Sindbis viruses (SINV) preferentially replicate in ␣1,3GT-positive cells, whereas herpes simplex viruses type 1 and type 2 (HSV-1 and HSV-2) preferentially grow in cells lacking ␣1,3GT. Viral growth and spread correlated with the ability of the different viruses to successfully initiate infection in the presence or absence of ␣1,3GT expression. GT knockout (KO) suckling mice infected with SINV strains (AR339 and S.A.AR86) experienced significant delay in onset of disease symptoms and mortality compared to wild-type (WT) B6 suckling mice. In contrast, HSV-2-infected GT KO mice had higher viral titers in spleen and liver and exhibited significantly more focal hepatic necrosis than WT B6 mice. This study demonstrates that ␣1,3GT activity plays a role in the course of infections for certain viruses. Furthermore, this study has implications for the evolution of resistance to viral infections in primates.

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The neutralization of pseudorabies virus by anti-α-galactocyl natural antibody in normal serum

Cited by 18 publications

References 21 publications

Pseudorabies Virus Propagated in Rabbit Kidney-Derived RK13 Cells is Neutralized by Natural IgM Antibodies in Normal Swine Serum which Specifically Lyse Host Cells

Pseudorabies Virus Propagated in Rabbit Kidney-Derived RK13 Cells is Neutralized by Natural IgM Antibodies in Normal Swine Serum which Specifically Lyse Host Cells

Herpes Simplex Virus Type 1 and 2 Glycoprotein C Prevents Complement-Mediated Neutralization Induced by Natural Immunoglobulin M Antibody

Possible Role of a Cell Surface Carbohydrate in Evolution of Resistance to Viral Infections in Old World Primates

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