A COVID-19 Accessory Protein, SARS-CoV-2 ORF3a

Colin Shin '24 Rachel Chen '24


Contents:


I. Introduction

The novelly discovered SARS-CoV-2-encoded ORF3a is of high interest to researchers combatting the COVID-19 pandemic. SARS-CoV-2 ORF (open reading frame) 3a encodes a highly conserved, putative viroporin across SARS-Cov-2 variants. Viroporins are transmembrane channels that alter the infected cell's permeability to allow entry of permeant ions and small molecules, which can cause a plethora of homeostatic disruptions to the cell and facilitate viral release, which drastically enhances viral growth of SARS-CoV-2 (Breitinger, et al.). Viroporins have also been found to trigger inflammatory responses and suppress defensive apoptosis of coronavirus-infected cells (Ren, et al.). Based on Cryo-EM data, we can now analyze ORF3a's structure for potential insights on how it directs viral-host interactions.

II. Structural Overview

Starting at the N-terminus, the SARS-CoV-2 3a protomer has a transmembrane region, consisting of 3 alpha helices (TM1,TM2,TM3), connected to a cytosolic domain (CD) by a turn-helix-turn (1). The protrudes the viroporin into cytosol. It contains 8 beta strands in a commonly observed beta-sandwich, where pairs of antiparallel beta strands stack atop each other. B1, B2, B6, and partially B7 make the "outer" sheet; while, B3, B4, B5, B8, and half of B7 make the "inner" sheet. This is a novel fold that has not yet been observed in other proteins.

Kern, et al. has successfully reconstituted SARS-CoV-2 3a as dimers and tetramers, but the molecule could potentially oligomerize even larger. Dimeric contact is facilitated by highly complementary interactions between the CD using these specific (Kern et al.). This results in a hydrophobic core that buries up to 940 angstrom-squared of surface area per beta chain. The lumenal side will show TM1-3 of one protomer and TM1-3 of another respectively encircled in a manner.

The 124 kDa tetramer is a side-by-side arrangement of two identical dimers (Figure 1). Cyro-EM analysis suggests this contact to occur between the TM3-CD linker and the beta1-beta2 linkers of neighboring dimers, at the This small contact between loops buries only 600 angstroms-squared of protein surface. Consistently, the tetramer has been less frequently observed than the dimer. Experimentally introduced mutations to a adjacent below TM3 but above beta1 and beta2 propound that disulfide bonding also facilitates tetramerization. The bonds most likely occurs between , whose sulfhydryl proximities to each other are within the average range for disulfide bonding (alpha carbon = 3.0 - 7.5 angstroms) (Gao, et al.).

Figure 3

Figure 1. Macromolecule docking of an ORF3a tetramer, with a duplicate dimer positioned to the left of the JMOL-rendered ORF3a structure. (Source: Kern, et al.)

 

III. Ion Channel Activity

Biochemical assays reveal channels respond to potassium and calcium ions, but deactivate in response to acidic pH conditions (Kern et al.). Our rendered structure is most likely a "closed" state and would undergo conformational changes to become a functional channel.

The inward facing side of the TM's are lined with residues that create a polar cavity vertically through the center of the ORF3a structure (Figure 2). There are also openings identified as "tunnels" which connect the central polar cavity to the exterior of the protein, shown in the figure below. The upper tunnel (circumferenced by indicated ) leads into the intermembrane space; The lower tunnel (circumferenced by indicated ) leads into cytosol.

Most ion channels also contain pores as a part of its ion conduction pathway. These pores can resemble exterior divots or grooves . For ORF3a, these are presented as hydrophilic regions formed in between TM's. One particular groove is situated between TM2 and TM3, indicated by the . In the tetramerized form, these grooves in the dimer interface could potentially also create an interior cavity, as depicted in Figure 3.

Figure 1

Figure 2. Digital rendering of upper tunnel (left) and lower tunnel (right) in cyan blue in ORF3a structure. (Source: Kern, et al.)

Figure 2

Figure 3. Solvent excluded surface rendering of the TM2-3 hydrophilic groove (outlined in dashed lines). Color coding demonstrates most hydrophilic regions (dark cyan) to most hydrophobic regions (dark yellow). (Source: Kern, et al.)


IV. References

Breitinger, U., Farag, N. S., Sticht, H., and Breitinger, H.-G. (2022). Viroporins: Structure, function, and their role in the life cycle of SARS-CoV-2. The International Journal of Biochemistry and Cell Biology, 145, 106185. https://doi.org/10.1016/j.biocel.2022.106185

Gao, X., Dong, X., Li, X., Liu, Z., and Liu, H. (2020). Prediction of disulfide bond engineering sites using a machine learning method. Scientific Reports, 10, 10330. https://doi.org/10.1038/s41598-020-67230-z

Kern, D. M., Sorum, B., Mali, S. S., Hoel, C. M., Sridharan, S., Remis, J. P., Toso, D. B., Kotecha, A., Bautista, D. M., and Brohawn, S. G. (2021). Cryo-EM structure of SARS-CoV-2 ORF3a in lipid nanodiscs. Nature Structural and Molecular Biology, 28(7), 573-582. https://doi.org/10.1038/s41594-021-00619-0

Ren, Y., Shu, T., Wu, D., Mu, J., Wang, C., Huang, M., Han, Y., Zhang, X.-Y., Zhou, W., Qiu, Y., and Zhou, X. (2020). The ORF3a protein of SARS-CoV-2 induces apoptosis in cells. Cellular and Molecular Immunology, 17(8), Article 8. https://doi.org/10.1038/s41423-020-0485-9

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