Reverse Engineering Provides Insights on the Evolution of Subgroups A to E Avian Sarcoma and Leukosis Virus Receptor Specificity †
Abstract
:1. Introduction
- (1)
- Many of the viral fusion glycoproteins are trimers of heterodimers. Each heterodimer consists of a globular, receptor binding domain (blue spheres) and a fusion protein that consists of a fusion peptide, two regions of tertiary structure (N, C), and a region to anchor the heterodimer in the viral membrane. The trimer of dimers usually undergoes a late protease cleavage resulting in a trapped, metastable, fusion-active conformation that requires a trigger to begin the fusion process.
- (2)
- After interaction with the appropriate trigger, the fusion-active glycoprotein undergoes an extensive conformation change producing an extended intermediate form that delivers the hydrophobic fusion peptide (blue box) to bury in the target cellular membrane, linking the viral and cellular membranes. Multiple extended viral glycoprotein intermediates are thought to be necessary to form a fusion pore. The globular domains are not shown for clarity.
- (3)
- The extended intermediates are energetically favored to collapse.
- (4)
- This collapse forms the stable six-helix bundle (6HB) and draws the two membranes together.
- (5)
- The apposition of the two membranes causes disruption and mixing of the lipid leaflets, a state called hemifusion.
- (6)
- A fusion pore is the result of the final conformational changes in the viral glycoproteins forming a trimer of hairpins. Once triggered, the conformational changes in the viral fusion proteins are thought to occur in a relatively short time resulting in the trimer of hairpins, the thermodynamically favored final structure.
2. Classes of Viral Fusion Proteins
3. Viral Fusion Protein Triggers
4. ASLV Experimental System
4.1. ASLV Subgroup A to E Envelope Glycoproteins
4.2. ASLV Subgroup A to E Receptors
4.3. ASLV Receptor and Glycoprotein Immunoadhesins
4.4. RCAS Family of Replication-Competent ASLV Vectors
4.5. Receptor Usage Assays
5. Subgroup A to E ASLV Entry Mechanism
6. Reverse Engineering: Identification of ASLV Envelope Glycoprotein Residues Critical for Virus Entry Using Genetic Selection Strategies
The Cell Entry Characteristics of RCASBP(B) versus RAV-2 Wild Type Envelope Glycoproteins
7. Summary/Reprise
- Small 1–2-amino acid changes in the hr1/vr3 regions can alter receptor binding affinity and receptor usage to even preferentially exploit the subtle differences that exist between one receptor homolog and another, e.g., chicken Tva versus quail Tva; expansion to use chicken TvbS1 and quail TvbQ. In these cases, wild type binding affinity was retained for one receptor homolog while significantly reducing the binding affinity to the other homolog, while maintaining wild type levels of viral replication and titer.
- Often, the initial evolutionary step is a deletion mutation in the hr1 C5–C6 loop of the SU glycoprotein that knocks out the normal receptor binding affinity and broadens receptor usage to other cell surface proteins including other known ASLV receptors, and may or may not also broaden host range.
- Subtle differences in the amino acid sequence in the C-terminal region of the SU glycoprotein and/or the extracellular region of the TM glycoprotein can affect the specificity and efficiency of the two-step ASLV membrane fusion process. The mutations that alter the biochemical properties of the fusion process often result in an “activated” envelope glycoprotein trimer that can more easily, and with less specificity, facilitate membrane fusion and virus entry.
- In general, expansion of ASLV receptor usage away from the extreme one receptor specificity leads to a loss of viral replication fitness and lower maximum titers likely due to the glycoprotein variants causing cytotoxic effects in the cells. While the ability of a virus to use multiple different receptors would seem to be an evolutionary advantage, these studies observe a deleterious effect of an expanded receptor usage that would likely pressure for the glycoprotein to acquire additional mutations to overcome this disadvantage presumably increasing receptor specificity.
Funding
Conflicts of Interest
References
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Allele | Chicken Line | Mutation | Phenotype | Ref. |
---|---|---|---|---|
tvas | Line H6 Line 0 | Wild type | Tva receptor conferring susceptibility to ASLV(A) infection. | [57] |
tvar | Line C Line Rh-C | Single nucleotide mutation in tvas resulting in a Cys40Trp substitution. | Structural change in Tva due to alteration of the disulfide bond pattern. Drastically lowered binding affinity for ASLV(A) envelope glycoproteins. | |
tvar2 | Line 72 | Four-nucleotide insertion in tvas changing reading frame. | Predicted to lead to a complete absence of the Tva protein. | |
tvbs1 | Line 15B1 | Wild type | TvbS1 receptor conferring susceptibility to ASLV subgroups B, D, and E. | [49,58] |
tvbs3 | Line 0 | Single nucleotide mutation in tvbs1 resulting in a Cys62Ser substitution. | Structural change in TvbS1 due to alteration of the disulfide bond pattern. Drastically lower binding affinity for only ASLV(E) envelope glycoproteins. | [49,58] |
tvbr | Line 72 | Single nucleotide mutation in tvbs1 resulting in a premature stop codon. | Predicted to lead to the production of a severely truncated protein at amino acid 57 of the TvbS1 protein. | [58] |
tvbr2 | Line M | Single nucleotide mutation in tvbs1 resulting in a Cys125Ser substitution. | Structural change in TvbS1 due to alteration of the disulfide bond pattern. Lowered binding affinity for ASLV(B) and ASLV(D), and drastically lower binding affinity for ASLV(E) glycoproteins. | [52] |
tvcs | Line H6 | Wild type | Tvc receptor conferring susceptibility to ASLV(C) infection. | [54] |
tvcr | Line 15 Line 15I5 | Single nucleotide mutation in tvcs resulting in a premature stop codon. | Predicted to lead to the production of a severely truncated protein at amino acid 55 of the Tvc protein. |
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Federspiel, M.J. Reverse Engineering Provides Insights on the Evolution of Subgroups A to E Avian Sarcoma and Leukosis Virus Receptor Specificity. Viruses 2019, 11, 497. https://doi.org/10.3390/v11060497
Federspiel MJ. Reverse Engineering Provides Insights on the Evolution of Subgroups A to E Avian Sarcoma and Leukosis Virus Receptor Specificity. Viruses. 2019; 11(6):497. https://doi.org/10.3390/v11060497
Chicago/Turabian StyleFederspiel, Mark J. 2019. "Reverse Engineering Provides Insights on the Evolution of Subgroups A to E Avian Sarcoma and Leukosis Virus Receptor Specificity" Viruses 11, no. 6: 497. https://doi.org/10.3390/v11060497
APA StyleFederspiel, M. J. (2019). Reverse Engineering Provides Insights on the Evolution of Subgroups A to E Avian Sarcoma and Leukosis Virus Receptor Specificity. Viruses, 11(6), 497. https://doi.org/10.3390/v11060497