Antibody-dependent enhancement

Antibody-dependent enhancement (ADE), sometimes less precisely called immune enhancement or disease enhancement, is a phenomenon in which binding of a virus to suboptimal antibodies enhances its entry into host cells, followed by its replication.[1] ADE can be induced when the strength of antibody-antigen interaction is below the certain threshold.[2][3] This phenomenon might lead to both increased virus infectivity and virulence. The viruses that can cause ADE frequently share some common features such as antigenic diversity, abilities to replicate and establish persistence in immune cells.[1] ADE can occur during the development of a primary or secondary viral infection, as well as after vaccination with a subsequent virus challenge.[1][4] It has been observed mainly with positive-strand RNA viruses. Among them are Flaviviruses such as Dengue virus,[5] Yellow fever virus, Zika virus,[6][7] Coronaviruses, including alpha- and betacoronaviruses,[8][9] Orthomyxoviruses such as influenza,[10] Retroviruses such as HIV,[11] and Orthopneumoviruses such as RSV.[12][13][14]

"Immune enhancement" redirects here. For immune enhancement in another sense, see autologous immune enhancement therapy.
In antibody-dependent enhancement, antibodies (the blue Y-shaped structures in the graphic) bind to both viral particles (labeled DENV) and Fc gamma receptors (labeled FcγR) expressed on immune cells, increasing the likelihood that the viruses will infect those cells.

ADE occurs because some virus-specific antibodies enhance the virus entry into immune cells through interaction with Fc or/and complement receptors.[1] Cells expressing this receptor (FcγRII / CD32) are represented by monocytes, macrophages, some categories of dendritic cells and B-cells. The mechanism that involves phagocytosis of immune complexes via FcγRII / CD32 receptor is better understood.[15] Antibody-dependent enhancement can hamper vaccine development, as a vaccine may cause the production of antibodies which, via ADE, worsen the disease the vaccine is designed to protect against. This is a decisive issue during late clinical stages of vaccine development against COVID-19.[16][17] Some vaccine candidates that targeted coronaviruses, RSV virus and Dengue virus elicited ADE, and were terminated from further development.

In coronavirus infection

The phenomenon of antibody-dependent enhancement of infection has been described for alpha- and betacoronaviruses.[18][19]

Mechanism

There are various hypotheses about how ADE triggered by coronaviruses occurs, and it is likely that more than one mechanism exists. The mechanism that involves interaction of the Spike protein of coronaviruses with FcRII/CD32 receptors of the immune cells is most well supported by experimental data. The data suggest that virus-antibody/Fc-receptor complex functionally mimics viral receptor in mediating viral entry.[20]

Viral antigen

In coronaviruses ADE can be promoted by antibodies to the spike (S) protein.[8][21][19][22][23] This observation was done for alphacoronaviruses such as FIPV[23][22][24] as well as for betacoronaviruses such as SARS-CoV-1[19][25] and MERS-CoV.[20] Only antibodies targeting this protein, but not other viral proteins, are able to form complexes with coronaviruses that are phagocytosed by immune cells and provoke viral replication, instead of viral destruction. Anti-Spike immune serum increases infection of human monocyte-derived macrophages by SARS-CoV.[21] It was shown that human immunodominant SARS coronavirus epitopes trigger both enhancing and neutralizing effects in non-human primates.[19]

Cellular receptors

Experimental evidence suggests that betacoronaviruses via FcyRII/CD32 receptors can enter immune cells. The antibody-virus complex is phagocytosed by CD32 + cells after binding with FcγRII receptor.[8][26][27][21][19] It was specifically shown that the expression of two types of receptors by immune cells: FcγRIIa and FcγRIIb (but not FcγRI or FcγRIIIa) induces ADE by SARS-CoV-1.[28] Along with this finding authors of another study, while observing SARS patients, found that the severity of the disease correlates with the FcγRIIa allelic polymorphism. In patients with FcγRIIa allelic isoform that can interact with both IgG1 and IgG2, the disease is more severe compared to patients with the FcγRIIa isoform capable of binding only IgG2.[29]

Types of infected immune cells

Antibodies targeted S-protein of SARS-CoV-1 promote virus entry into CD32+ cells such as B-cells,[30][31] monocytes[26][27][25] and macrophages.[26][27][30] In these cells, the virus replicates but does not promote a productive infection. This may be due to the fact that these cells of myeloid lineage do not express enough of serine proteases required for the virion activation. However, viral replication, even without the formation of infectious virions, can lead to a massive death of immune cells bearing the Fc𝛾RIIγ receptor.

Antibodies

In some experiments it was shown that ADE was mainly caused by antibodies of the IgG2a subclass, while the tested antibodies of the IgG1 subclass did not cause such an effect.[24]

Alphacoronavirus
See also: Alphacoronavirus

The feline infectious peritonitis virus (FIPV) is an alphacoronavirus that is a very common pathogen in both domestic and wild cats.[32] FIPV can cause antibody-dependent enhancement (ADE). Thus, vaccination against FIPV increases the disease seriousness.[33] It was shown that infection of macrophages by FIPV in vitro can be triggered by non-neutralising monoclonal antibodies targeting the Spike (S)-protein, and this phenomenon can also occur with diluted neutralizing antibodies.[22] ADE explains why half of cats develop peritonitis after being passively immunized with antivirus antibodies and being challenged with the same FIPV serotype.[8] In several countries an attenuated virus vaccine is available in a form of nasal drops; however, its application is still considered controversial by many experts, both in terms of safety and efficacy.[34]

Betacoronavirus
See also: Betacoronavirus
Antibody-dependent enhancement during coronavirus infection
S-protein and N-protein models of SARS-CoV-2 virus. Both models are reproduced with modifications from Ricke et al.[3] It is likely that the amino acids variability of the S-protein represents a result of antigenic drift.

There are multiple examples of ADE triggered by betacoronaviruses. The ADE related immunopathology upon viral exposure has been a major challenge for coronavirus vaccine development[35] and may similarly impact SARS-CoV-2 vaccine research.[36] The phenomenon has been demonstrated in both cell cultures and animal models. ADE related acute lung injury has been documented in both severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS) animal models.[20] It can occur during a primary infection, reinfection or infection after vaccination. For example, rabbits intranasally infected with MERS-CoV developed a pulmonary infection characterized by viremia and perivascular inflammation of the lung along with an antibody response that lacked neutralizing antibodies.[37] The rabbits produced neutralizing antibodies after the initial virus challenge, however re-exposure to MERS-CoV triggered more severe lung disease.[37] Similar observation were done with re-infected or vaccinated mice with SARS-CoV. Thus, mice were capable to develop neutralizing antibodies after re-infection with SARS-CoV itself or after vaccination with four types of vaccines. However, they all developed immunopathologic-type lung damage after SARS-CoV virus challenge, despite being protected from the virus compared to control.[35] Similar problems were observed with hamsters [31] and non-human primates. For example, vaccinated macaques due to ADE suffered from acute lung injury after the virus challenge despite having the lower viral loads after vaccination.[38][39] In these animals lung injury occurred with both type of vaccinations such as inactivated virus[38] or vector construct based on modified vaccinia Ankara virus that encoded full-length SARS-CoV spike (S) protein.[39] However, ferrets, after vaccination with a similar construct that was followed by the virus challenge developed severe hepatitis instead of a lung damage.[40]

Potential link between COVID-19 pathophysiology and conformational change of S-protein

Potential linkage between pathogenesis of SARS, COVID-19 and ADE

The pathogenesis of SARS and COVID-19 diseases, may be associated with ADE, manifested in the infection of monocytes, macrophages and B-cells. Some researchers[3] believe that ADE is a key step in COVID-19 evolution from the mild to severe form with critical symptoms. ADE may explain the observed dysregulation of immune system, including apoptosis of immune cells, T-cell lymphopenia an inflammatory cascade with accumulation of macrophages and neutrophils in the lungs, and a a cytokine storm. Previously, other researchers have also put forward a similar hypothesis regarding SARS.[30][41]. ADE goes along with reduction of Th1 cytokines IL2, TNF-α and IFN-γ and increase of Th2 cytokines IL-10, IL-6, PGE-2 and INF-α, as well as with inhibition of STAT pathway.[42] This process can trigger generalized infection of immune cells in multiple organs and cytokine storm.[43][44]

Also, an ongoing question in the COVID-19 pandemic is whether—and if so, to what extent—COVID-19 receives ADE from prior infection with other coronaviruses.[45]

IgG antibodies targeting the S-protein of SARS-CoV-1

The following observations made on a small group of six patients, three of whom recovered and three died, also support the idea that antibodies to the S-protein can harm patients by causing ADE.[46] A comparative analysis of the specific humoral response showed that in patients who died from SARS-CoV-1 infection, neutralizing antibodies to the S-protein were produced much faster than in recovered people. So, it was revealed that on the 15th day of illness in patients who subsequently died, the titer of antibodies to the S-protein was significantly higher than in those who subsequently recovered. At the same time, although the titer of neutralizing antibodies during the course of the disease in patients who subsequently died grew faster than the titer in subsequently recovered patients, it also decreased faster. At the same time, in patients who subsequently recovered, the antibody titer increased more slowly, but rose to a higher level and stayed at this level longer. This dynamics of changes in antibody titers was characteristic of both IgM and IgG antibodies. It can be assumed that patients who subsequently died developed an antibody-dependent increase in viral infection in severe form and the rapid production of antibodies to the S-protein, which could not neutralize the virus, contributed to this. It is possible that the slower titer rise contributed to the production of antibodies with a higher binding constant corresponding to stronger antigen-antibody complexes, with higher affinity and avidity.[46] A significant excess of the level of antibodies in severe patients compared with non-severe patients was also observed in a sample of 325 patients in another study. [47] Other researchers received similar data on a sample of 347 SARS patients. Moreover, it was found that in patients who subsequently died, antibodies appeared first.[48]

IgG antibodies targeting the S-protein of SARS-CoV-2

Similar to SARS-CoV-1 virus results were obtained when measuring the amount of IgG antibodies to the S-protein of the SARS-CoV-2 virus found in the serum of hospitalized patients. An earlier appearance of IgG antibodies in patients with severe illness compared with those in whom it was mild was observed in a sample of 285 people.[49] Interestingly, with respect to IgM antibodies, a different dynamic was observed, they were found either in the same or in lower titer in patients with a more severe form of the disease.[49][50] In a sample of 173 patients, the effect of a significant excess of the level of antibodies in severely ill patients compared with non-severe patients was shown two weeks after symptoms onset.[51] In addition, a positive and significant correlation was found between the antibodies titer in the blood and the concentration of inflammatory markers such as C-reactive protein and lactate dehydrogenase. The data were obtained from 29 patients .[52] At the same time, a significant inverse correlation was found between the antibody titer and the number of lymphocytes.[52]

In influenza infection

Prior receipt of 2008–09 TIV (Trivalent Inactivated Influenza Vaccine) was associated with an increased risk of medically attended pH1N1 illness during the spring-summer 2009 in Canada. The occurrence of bias (selection, information) or confounding cannot be ruled out. Further experimental and epidemiological assessment is warranted. Possible biological mechanisms and immunoepidemiologic implications are considered.[53]

Natural infection and the attenuated vaccine induce antibodies that enhance the update of the homologous virus and H1N1 virus isolated several years later, demonstrating that a primary influenza A virus infection results in the induction of infection enhancing antibodies.[54]

ADE was suspected in infections with influenza A virus subtype H7N9, but knowledge is limited.

In dengue virus infection
Further information: Dengue fever and Dengue virus

The most widely known example of ADE occurs in the setting of infection with dengue virus, a single-stranded positive-polarity RNA virus of the family Flaviviridae. It causes a disease of varying severity in humans, from dengue fever (DF), which is usually self-limited, to dengue hemorrhagic fever and dengue shock syndrome, either of which may be life-threatening.[55] It is estimated that as many as 390 million individuals are infected with dengue virus annually.[56]

The phenomenon of ADE may be observed when a person who has previously been infected with one serotype of the dengue virus becomes infected months or years later with a different serotype. In such cases, the clinical course of the disease is more severe, and these people have higher viremia compared with those in whom ADE has not occurred. This explains the observation that while primary (first) infections cause mostly minor disease (dengue fever) in children, secondary infection (re-infection at a later date) is more likely to be associated with dengue hemorrhagic fever and/or dengue shock syndrome in both children and adults.[57]

There are four antigenically different serotypes of dengue virus (dengue virus 1–4).[58] In 2013 a fifth serotype was reported.[59] Infection with dengue virus induces the production of neutralizing homotypic immunoglobulin G (IgG) antibodies which provide lifelong immunity against the infecting serotype. Infection with dengue virus also produces some degree of cross-protective immunity against the other three serotypes.[60] Neutralizing heterotypic (cross-reactive) IgG antibodies are responsible for this cross-protective immunity, which typically persists for a period of several months to a few years. These heterotypic antibody titers decrease over long time periods (4 to 20 years).[61] While heterotypic IgG antibody titers decrease, homotypic IgG antibody titers increase over long time periods. This could be due to the preferential survival of long-lived memory B cells producing homotypic antibodies.[61]

In addition to inducing neutralizing heterotypic antibodies, infection with the dengue virus can also induce heterotypic antibodies that neutralize the virus only partially or not at all.[62] The production of such cross-reactive but non-neutralizing antibodies could be the reason for more severe secondary infections. It is thought that by binding to but not neutralizing the virus, these antibodies cause it to behave as a "trojan horse",[63][64][65] where it is delivered into the wrong compartment of dendritic cells that have ingested the virus for destruction.[66][67] Once inside the white blood cell, the virus replicates undetected, eventually generating very high virus titers which cause severe disease.[68]

A study conducted by Modhiran et al.[69] attempted to explain how non-neutralizing antibodies down-regulate the immune response in the host cell through the Toll-like receptor signaling pathway. Toll-like receptors are known to recognize extra- and intracellular viral particles and to be a major basis of the cytokines production. In vitro experiments showed that the inflammatory cytokines and type 1 interferon production were reduced when the ADE-dengue virus complex bound to the Fc receptor of THP-1 cells. This can be explained by both a decrease of Toll-like receptor production and a modification of its signaling pathway. On one hand, an unknown protein induced by the stimulated Fc receptor reduces the Toll-like receptor transcription and translation, which reduces the capacity of the cell to detect viral proteins. On the other hand, many proteins (TRIF, TRAF6, TRAM, TIRAP, IKKα, TAB1, TAB2, NF-κB complex) involved in the Toll-like receptor signaling pathway are down-regulated, which led to a decrease of the cytokine production. Two of them, TRIF and TRAF6, are respectively down-regulated by 2 proteins SARM and TANK up-regulated by the stimulated Fc receptors.

To illustrate the phenomenon of ADE, consider the following example: an epidemic of dengue fever occurred in Cuba, lasting from 1977 to 1979. The infecting serotype was dengue virus-1. This epidemic was followed by two more outbreaks of dengue fever—one in 1981 and one in 1997; dengue virus-2 was the infecting serotype in both of these later epidemics. 205 cases of dengue hemorrhagic fever and dengue shock syndrome occurred during the 1997 outbreak, all in people older than 15 years. All but three of these cases were demonstrated to have been previously infected by the dengue virus-1 serotype during the epidemic of 1977–1979.[70] Furthermore, people who had been infected with dengue virus-1 during the 1977-79 outbreak and secondarily infected with dengue virus-2 in 1997 had a 3-4 fold increased probability of developing severe disease than those secondarily infected with dengue virus-2 in 1981.[61] This scenario can be explained by the presence of neutralizing heterotypic IgG antibodies in sufficient titers in 1981, the titers of which had decreased by 1997 to the point where they no longer provided significant cross-protective immunity.

In HIV-1 virus infection

ADE of infection has also been reported in HIV. Like dengue virus, non-neutralizing level of antibodies have been found to enhance the viral infection through interactions of the complement system and receptors.[71] The increase in infection has been reported to be over 350 fold which is comparable to ADE in other viruses like dengue virus.[71] ADE in HIV can be complement-mediated or Fc receptor-mediated. Complements in the presence of HIV-1 positive sera have been found to enhance the infection of MT-2 T-cell line. The Fc-receptor mediated enhancement was reported when HIV infection was enhanced by sera from HIV-1 positive guinea pig enhanced the infection of peripheral blood mononuclear cells without the presence of any complements.[72] Complement component receptors CR2, CR3 and CR4 have been found to mediate this Complement-mediated enhancement of infection.[71][73] The infection of HIV-1 leads to activation of complements. Fragments of these complements can assist viruses with infection by facilitating viral interactions with host cells that express complement receptors.[74] The deposition of complement on the virus brings the gp120 protein close to CD4 molecules on the surface of the cells, thus leading to facilitated viral entry.[74] Viruses pre-exposed to non-neutralizing complement system have also been found to enhance infections in interdigitating dendritic cells. Opsonized viruses have not only shown enhanced entry but also favorable signaling cascades for HIV replication in interdigitating dendritic cells.[75]

HIV-1 has also shown enhancement of infection in HT-29 cells when the viruses were pre-opsonized with complements C3 and C9 in seminal fluid. This enhanced rate of infection was almost 2 times greater than infection of HT-29 cells with virus alone.[76] Subramanian et al., reported that almost 72% of serum samples out of 39 HIV positive individuals contained complements that were known to enhance the infection. They also suggested that the presence of neutralizing antibody or antibody-dependent cellular cytotoxicity-mediating antibodies in the serum contains infection-enhancing antibodies.[77] The balance between the neutralizing antibodies and infection-enhancing antibodies changes as the disease progresses. During advanced stages of the disease the proportion of infection-enhancing antibodies are generally higher than neutralizing antibodies.[78] Increase in viral protein synthesis and RNA production have been reported to occur during the complement-mediated enhancement of infection. Cells that are challenged with non-neutralizing levels of complements have been found have accelerated release of reverse transcriptase and the viral progeny.[79] The interaction of anti-HIV antibodies with non-neutralizing complement exposed viruses also aid in binding of the virus and the erythrocytes which can lead to more efficient delivery of viruses to the immune-compromised organs.[73]

ADE in HIV has raised questions about the risk of infections to volunteers who have taken sub-neutralizing levels of vaccine just like any other viruses that exhibit ADE. Gilbert et al., in 2005 reported that there was no ADE of infection when they used rgp120 vaccine in phase 1 and 2 trials.[80] It has been emphasized that much research needs to be done in the field of the immune response to HIV-1, information from these studies can be used to produce a more effective vaccine.

Mechanism

There are several possibilities to explain the phenomenon:

  1. A viral surface protein studded with antibodies against a virus of one serotype binds to a similar virus with a different serotype. The binding is meant to neutralize the virus surface protein from attaching to the cell, but the virus-antibody complex also binds to the Fc-region antibody receptor (FcγR) on the cell membrane. This brings the virus into close proximity to the virus-specific receptor, and the cell internalizes the virus through the normal infection route.[81]
  2. A virus surface protein may be attached to antibodies of a different serotype, activating the classical pathway of the complement system. The complement cascade system instead binds C1Q complex attached to the virus surface protein via the antibodies, which in turn bind C1q receptor found on cells, bringing the virus and the cell close enough for a specific virus receptor to bind the virus, beginning infection. This mechanism has not been shown specifically for dengue virus infection, but may occur with Ebola virus infection in vitro.[82]
  3. When an antibody to a virus is present for a different serotype, it is unable to neutralize the virus, which is then ingested into the cell as a sub-neutralized virus particle. These viruses are phagocytosed as antigen-antibody complexes, and degraded by macrophages. Upon ingestion the antibodies no longer even sub-neutralize the body due to the denaturing condition at the step for acidification of phagosome before fusion with lysosome. The virus becomes active and begins its proliferation within the cell.

See also
  • Original antigenic sin
  • Other ways in which antibodies can (unusually) make an infection worse instead of better
    • Blocking antibody, which can be either good or bad, depending on circumstances
    • Hook effect, most relevant to in vitro tests but known to have some in vivo relevances

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