C Proteins: Controllers of Orderly Paramyxovirus Replication and of the Innate Immune Response
<p>C protein expression among viruses of the <span class="html-italic">Paramyxoviridae</span> family. (<b>A</b>) Phylogenetic tree indicating subfamilies and genera. The tree is based on full genome alignment of available reference genomes in GenBank using CLUSTALW [<a href="#B18-viruses-14-00137" class="html-bibr">18</a>] and was generated with iTOL [<a href="#B19-viruses-14-00137" class="html-bibr">19</a>]. Viruses of genera in red express C proteins. (<b>B</b>) Organization of the overlapping open reading frames in the mRNAs derived from the P/V/C genes of MeV (<b>left</b>), SeV (<b>center</b>) and NiV (<b>right</b>). SeV expresses four C proteins from alternative start codons named C’, C, Y1 and Y2. (<b>C</b>) Secondary structure predictions for P and C proteins, as well as the V protein-specific carboxy-terminus (V<sub>CT</sub>). Alpha-helices are depicted in blue, beta strands in orange and unstructured (coiled) regions are shown in grey. Underlined regions in P and V proteins correspond to their unique carboxy-termini (P<sub>CT</sub> and V<sub>CT</sub>). N<sup>0</sup>BD: binding domain interacting with free nucleoprotein; TMD: tetramerization domain of P; XD: domain of P interacting with N<sub>tail</sub> of the nucleocapsid; ZnBD: Zn-binding domain of V protein that interacts with several host innate immunity factors. Figure generated with BioRender.com.</p> "> Figure 2
<p>Sequence and structure comparison of paramyxoviral C proteins. Phylogenetic analysis of the C protein sequences (<b>left</b>). Different genera are highlighted in individual colors. Prototype species underlined. Sequences were aligned using the PROMALS3D tool [<a href="#B56-viruses-14-00137" class="html-bibr">56</a>], and a phylogenetic analysis was done via the neighbor-joining clustering method using the EMBL-EBI Simple Phylogeny tool [<a href="#B57-viruses-14-00137" class="html-bibr">57</a>]. Predicted secondary structures of the different C proteins (<b>right</b>). Alpha-helices are depicted in blue, beta strands in orange and unstructured (coiled) regions are shown in grey. Translation initiation codons are indicated by arrows. Predictions were performed with the JPred tool [<a href="#B58-viruses-14-00137" class="html-bibr">58</a>]. The red box indicates the region in the SeV C protein for which a tertiary structure is available (PDB 3WWT) [<a href="#B59-viruses-14-00137" class="html-bibr">59</a>]. Figure generated with BioRender.com.</p> "> Figure 3
<p>Structural features of the SeV C protein. (<b>A</b>) SeV C protein (amino acid residues 99–204, shown in gold) in a complex with STAT1 (silver) (PDB 3WWT) [<a href="#B59-viruses-14-00137" class="html-bibr">59</a>]. Residues important for binding to ALIX (LXXW motif) are shown in red; potential Tsg101-binding residues (QWLQ-motif) are shown in blue. (<b>B</b>) SeV C protein (amino acid residues 99–204, shown in gold) in a complex with the BRO1 domain of ALIX (light blue) (PDB 6KP3) [<a href="#B61-viruses-14-00137" class="html-bibr">61</a>]. (<b>C</b>) Conserved ALIX-binding motifs in respiroviruses (top five sequences), and homologous residues in morbilliviruses (bottom four sequences). (<b>D</b>) Conserved Tsg101-binding motifs in henipaviruses (top three sequences), and homologous residues in respiroviruses (bottom 5 sequences). Figure generated with BioRender.com.</p> "> Figure 4
<p>Overview of the localization and functions of the C protein in the paramyxovirus life cycle, and antagonism of the innate immunity pathways involved in paramyxovirus sensing. (<b>Top left</b>) After cell entry, the viral polymerase transcribes mRNAs and replicates the viral genome. C proteins regulate these processes and prevent the formation of immunostimulatory DI genomes (panhandle structures). (<b>Center</b>) Type-I IFN (IFNβ) induction after the sensing of DI genomes by cellular receptors PKR, RIG-I and MDA-5. C proteins can interfere with these processes by blocking the signal transduction cascade at multiple steps in the cytoplasm and nucleus. (<b>Bottom right</b>) Type-I IFN signaling activates the JAK/STAT pathways involving STAT1 and STAT2. The SeV C protein binds and sequesters STAT1; the other C proteins inhibit STAT1 phosphorylation. (<b>Bottom left</b>) The HPIV3 C protein also blocks the inflammasome-mediated activation of IL1β. (<b>Top center</b>) The C proteins interact with ESCRT components to enhance virus particle assembly and budding. SeV C interacts with ALIX, and NiV C interacts with Tsg101. (<b>Top right</b>) Several C proteins shuttle between the cytoplasm and nucleus utilizing the nuclear pore complex (NPC). Figure generated with BioRender.com.</p> "> Figure 5
<p>Schematic representation of the replicating paramyxovirus RNP and potential roles of C proteins in enhancing polymerase processivity. The viral nucleocapsid consists of RNA (orange curved line) encapsidated with N (blue shapes). The viral polymerase consisting of L (purple) and tetrameric P (grey) extracts viral RNA from the nucleocapsid and synthesizes a complementary sequence (green curved line). P moves the polymerase along the genomic RNA by sequentially interacting with helically arranged N subunits. P also interacts with free N to encapsidate the nascent RNA strand. C proteins may enhance polymerase processivity through one or several of the four indicated mechanisms. Figure generated with BioRender.com.</p> ">
Abstract
:1. Introduction
2. C Proteins Are Expressed from Alternative Open Reading Frames in the P/V/C Genes
3. All Three Types of C Proteins Include an Intrinsically Disordered Part
4. Functional Insights from the SeV C-STAT1 Complex Structure
5. C Proteins Are Basic and Shuttle between Cytoplasm and Nucleus
6. C Proteins Enhance Virulence through Multiple Mechanisms
7. C Proteins Regulate Viral Transcription and Replication
8. C Proteins Minimize Production of Immunostimulatory DI RNA
9. C proteins Interact with the Polymerase Complex
10. C Proteins Directly Interfere with Innate Immunity Activation
10.1. Interferon Induction
10.2. Interferon Signaling
10.3. Inflammation
11. C Proteins Support Viral Particle Assembly and Budding
12. Concluding Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Genus | Species | Abbreviation | Genome Sequence | C Protein Sequence | Reference | |
---|---|---|---|---|---|---|
(GenBank) | (GenBank) | (UniProt/UniParc) | ||||
Aquapara-myxovirus | Oncorhynchus aquaparamyxovirus | PSPV | MH900516.1 | AYN62575.1 | I1TLL1 | [29] |
Salmo aquaparamyxovirus | ASPV | NC_025360.1 | YP_009094145.1 | B2BX73 | [30] | |
Henipavirus | Cedar henipavirus | CeV | NC_025351.1 | YP_009094083.1 | J7H4I1 | [31] |
Hendra henipavirus | HeV | NC_001906.3 | NP_047109.1 | O55779 | [32] | |
Nipah henipavirus | NiV | NC_002728.1 | NP_112024.1 | Q997F1 | [33] | |
Jeilongvirus | Beilong jeilongvirus | BeV | NC_007803.1 | YP_512248.1 | Q287X7 | [34] |
Jun jeilongvirus | J-V | NC_007454.1 | YP_338079.1 | Q49HN8 | [35] | |
Morbillivirus | Canine morbillivirus | CDV | NC_001921.1 | NP_047203.1 | P06941 | [36] |
Cetacean morbillivirus | CeMV | NC_005283.1 | NP_945026.1 | Q709E7 | [37] | |
Feline morbillivirus | FeMV | NC_039196.1 | YP_009512960.1 | UPI000259F006 | [38] | |
Measles morbillivirus | MeV | NC_001498.1 | NP_056920.1 | Q9YZN9 | [39] | |
Phocine morbillivirus | PMV | NC_028249.1 | YP_009177600.1 | P35940 | [40] | |
Rinderpest morbillivirus | RPV | NC_006296.2 | YP_087122.1 | P35948 | [41] | |
Small ruminant morbillivirus | PPRV | NC_006383.2 | YP_133824.1 | Q5ZER5 | [42] | |
Narmovirus | Mossman narmovirus | MoV | NC_005339.1 | NP_958051.1 | Q6WGM3 | [43] |
Myodes narmovirus | BaVV | NC_055167.1 | YP_010085011.1 | N/A | [44] | |
Nariva narmovirus | NarV | NC_017937.1 | YP_006347585.1 | B8XH61 | [45] | |
Tupaia narmovirus | TPMV | NC_002199.1 | NP_054693.1 | Q9WS38 | [46] | |
Respirovirus | Bovine respirovirus 3 | BPIV3 | NC_002161.1 | N/A | N/A | [47] |
Caprine respirovirus 3 | CPIV3 | NC_028362.1 | N/A | N/A | [48] | |
Human respirovirus 1 | HPIV1 | NC_003461.1 | NP_604436.1 | Q8QT30 | [49] | |
Human respirovirus 3 | HPIV3 | NC_001796.2 | NP_599251.1 | UPI0000161E9C | [50] | |
Murine respirovirus | SeV | NC_001552.1 | NP_056872.1 | O55527 | [51] | |
Porcine respirovirus 1 | PPIV1 | NC_025402.1 | YP_009094446.1 | S5LSI4 | [52] | |
Squirrel respirovirus | GSqRV | LS992584.1 | SYZ47172.1 | A0A383S9W5 | [53] | |
Salemvirus | Salem salemvirus | SalV | NC_025386.1 | YP_009094334.1 | Q9IZB9 | [54] |
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Siering, O.; Cattaneo, R.; Pfaller, C.K. C Proteins: Controllers of Orderly Paramyxovirus Replication and of the Innate Immune Response. Viruses 2022, 14, 137. https://doi.org/10.3390/v14010137
Siering O, Cattaneo R, Pfaller CK. C Proteins: Controllers of Orderly Paramyxovirus Replication and of the Innate Immune Response. Viruses. 2022; 14(1):137. https://doi.org/10.3390/v14010137
Chicago/Turabian StyleSiering, Oliver, Roberto Cattaneo, and Christian K. Pfaller. 2022. "C Proteins: Controllers of Orderly Paramyxovirus Replication and of the Innate Immune Response" Viruses 14, no. 1: 137. https://doi.org/10.3390/v14010137