- Open Access
6thInternational Symposium on Retroviral Nucleocapsid
© Berkhout et al; licensee BioMed Central Ltd. 2008
- Received: 18 December 2007
- Accepted: 25 February 2008
- Published: 25 February 2008
Retroviruses and LTR-retrotransposons are widespread in all living organisms and, in some instances such as for HIV, can be a serious threat to the human health. The retroviral nucleocapsid is the inner structure of the virus where several hundred nucleocapsid protein (NC) molecules coat the dimeric, genomic RNA. During the past twenty years, NC was found to play multiple roles in the viral life cycle (Fig. 1), notably during the copying of the genomic RNA into the proviral DNA by viral reverse transcriptase and integrase, and is therefore considered to be a prime target for anti-HIV therapy. The 6th NC symposium was held in the beautiful city of Amsterdam, the Netherlands, on the 20th and 21st of September 2007. All aspects of NC biology, from structure to function and to anti-HIV vaccination, were covered during this meeting.
- Stem Loop Structure
- Rous Sarcoma Virus
- Strand Transfer
- Ribosomal Scanning
- Dimerization Initiation Site
This first session on NC structure-function relationships discussed the basis of NC recognition of the genomic RNA and its potent nucleic acid chaperoning activities, discovered in the late 80's [1–6] (for reviews see [7–9]). Using single DNA molecules that are stretched and melted by force, M. Williams (Northeastern University, Boston, MA, USA) and collaborators examined the influence of HIV and HTLV-1 NC on double stranded DNA destabilization and reannealing. It was found that HIV NC behaved as a pure chaperone while HTLV-1 NC was more akin a single stranded DNA binding protein [10–12] in agreement with the recent findings of K. Musier-Forsyth (OSU, Columbus, OH, USA; see below). Based on standard assays to monitor the NC nucleic acid binding, aggregation and annealing activities, K. Musier-Forsyth and collaborators showed that the N-terminal 35 residues of HIV-1 NC were necessary and sufficient for chaperone function in vitro. Interestingly, the HIV-1 Gag polyprotein was also shown to be a nucleic acid chaperone protein, a property that is likely to facilitate genome dimerization and tRNA primer annealing during virion assembly. Results on different retroviral NC proteins showed that they exhibit significant differences in their overall chaperone activity, decreasing in the order HIV-1 ~RSV > MLV >> HTLV-1. Both K Musier-Forsyth and M Williams found that HTLV-1 NC's poor chaperone activity was caused by its acidic C-terminal domain. Using fluorescence-based techniques and the HIV-1 TAR stem-loop (SL) structure, Y Mély and his colleagues (Faculté de Pharmacie, Strasbourg, France) showed that the HIV-1 NC structural determinants, formed by the hydrophobic plateau at the top of the two zinc fingers and the flanking basic residues, are essential for its chaperoning function [13–15]. Similar structural determinants were also found to be essential for the chaperoning function of MoMLV NC that contains a unique zinc finger that is also flanked by basic residues .
NC is an obligatory constituent of the viral replication machinery whereby the genomic RNA is converted into the full-length double-stranded viral DNA by RT. This appears to be mediated by tight interactions between NC molecules, the genomic RNA that is in a dimeric form and RT. In a long standing effort to understand the role of NC in viral DNA synthesis, R Gorelick et al. (NCI-Frederick, MD, USA)  discussed their investigation of two HIV NC zinc-finger mutants, H23C and H44C, which exhibit severe replication defects . Analyses of early infection revealed that these mutations cause major defects in integration, but not reverse transcription: curiously, the rate of initiation and partial completion of reverse transcription was faster than wild-type . Examination of virus particles prior to infection revealed that both mutant virions contain significantly more viral DNA than wild-type particles. Thus these NC mutations cause premature reverse transcription, and this may provide a partial explanation for their replication defects.
J. Mak and colleagues (Macfarlane Burnet Centre, Victoria, Australia) investigated the rate of HIV-1 recombination in cell cultures by monitoring sequence-tag redistribution in the gag and pol genes. They found that rates of recombination were high, corresponding to about 6–7 per cycle in T cells and up to 12–14 in monocyte-derived macrophages.
In addition to the genomic RNA, HIV-1 virions can package a substantial amount of spliced viral RNAs, but this seems to be independent of the NC zinc fingers, as reported by M. Mougel et al. (CNRS, Montpellier, France). Reverse transcription of these spliced RNAs takes place as efficiently as that of the genomic RNA, but poorly responds to the chain terminator antiviral drug AZT. Thus, AZT treatment might well increase the representativeness of spliced HIV-1 DNAs [34, 35].
All viral RNA, the full length and the spliced forms, contain the TAR sequence at the 5' and 3' ends. NC can induce TAR dimerization as reported by E. Andersen et al (University of Aarhus, Denmark) . According to these authors, TAR dimerization is important for the obligatory first strand transfer during cDNA synthesis and this TAR dimer has a parallel orientation depending, at least in part, on the dimerization initiation site (DIS). Completion of viral DNA synthesis necessitates the second strand transfer which takes place at the level of the PBS sequence. N Morellet et al (CNRS Paris, France) investigated this strand transfer in HIV-1 by means of NMR and fluorescence studies. They found that NC, notably the zinc fingers, chaperones this reaction by modifying the conformation of the loops of both PBS (+) and (-) sequences, promoting the formation of a kissing complex and the subsequent annealing of the PBS (+) and (-) sequences.
The genomic RNA codes for the Gag and Gag-Pol polyprotein precursors which are synthesized by the host translation machinery. Several characteristics of the HIV-1 5' UTR, such as the 5' terminal TAR hairpin, its length and overall secondary structure, are likely to interfere with ribosomal scanning and suggest that translation is initiated by internal entry of ribosomes (IRES) [37, 38]. To gain further insight in the mechanism of translation initiation on the HIV-1 5'UTR, T. Abbink, K. Arts and B. Berkhout (Amsterdam, the Netherlands) introduced upstream AUGs (uAUG) at different positions in the 5'UTR and determined the effect on the expression of a downstream reporter gene under control of the gag AUG. If ribosomal scanning initiates upstream of the uAUG, translation will start on the uAUG, thereby inhibiting the expression of the downstream reporter gene. This allowed determination of the window of ribosomal scanning on the HIV-1 5' UTR. Their studies show that the inserted uAUG inhibited reporter gene expression at every position in the 5'UTR, thus indicating that the entire 5' UTR is scanned. In addition, they show that reinitiation of translation on the HIV-1 5'UTR is quite efficient if the upstream open reading frame is short (less than 20 bases). This finding is in agreement with previous findings  but different from others showing that HIV Gag translation operates by an IRES mechanism .
HIV-1 Gag polyprotein contains all of the molecular determinants required for its intracellular trafficking, and its assembly and budding in the form of virus-like particles (VLPs). The role of NC in Gag assembly has been studied for almost twenty years [1–5]. A. Rein and his colleagues (NCI-Frederick, MD, USA) have characterized the assembly properties of chimeric proteins in which the NC (and p1 and p6) domain of HIV-1 Gag is replaced by dimerizing or trimerizing leucine- or isoleucine-zipper motifs, respectively. These proteins assemble in mammalian cells into virus-like particles (VLPs) with morphology nearly, but not quite, identical to those formed by wild-type Gag. These VLPs contain at least 10-fold less RNA than wild-type VLPs. Their buoyant density is somewhat lower than that of wild-type VLPs; this difference is consistent with the hypothesis that the packing of the chimeric proteins in these VLPs is the same as that of wild-type Gag. The chimeric proteins co-assemble efficiently with wild-type Gag; thus the function of RNA in normal VLP assembly is not to act as a "string" upon which Gag protein molecules are aligned. The chimeric proteins were expressed in bacteria. They did not assemble spontaneously, but could be induced to assemble into VLPs by addition of either RNA or inositol hexakisphosphate.
D. Muriaux, J.L. Darlix and collaborators (INSERM Lyon, France) have been studying the trafficking and the assembly of HIV-1 in human cells. Viral and cellular factors are involved in these processes, in particular the NC domain of Gag, the genomic RNA, and cellular proteins of the endocytic pathways, and membrane microdomains . They found that HIV-1 can bud into intracellular vesicles in addition to the plasma membrane of T cells . The NC zinc fingers of HIV-1 Gag were found to be critical determinants of Gag assembly and localisation in endosomes . Furthermore, they reported the involvement of a tetraspanin web in T-lymphoblastic cells that serves as a platform for HIV-1 assembly (Grigorov B., V. Attuil-Audenis, F. Perugi, M. Nedelec, S. Watson, J.-L. Darlix, C. Pique, H. Conjeaud & D. Muriaux: IMPLICATIONS OF TETRASPANINS IN HIV-1 FORMATION in infected T-lymphoblastic cells., submitted).
NC protein can exist in different forms in newly made mature HIV-1 virions, namely NCp15 (NC-SP2-p6), NCp9 (NCp7-SP2) and fully processed NCp7. J.A. Thomas (NCI-Frederick, MD, USA) presented work of collaborators where they investigated the requirement for proteolytic maturation of NC by mutating the protease cleavage sites necessary for the production of mature NCp9 (NCp7-SP2) or NCp7. Interestingly, viruses tailored to make either NCp9 + p6 or NCp7 + SP2 + p6 were fully infectious and could replicate in H9 cells. In contrast, viruses that made either NCp15 or NCp7 + p1-p6 were replication defective. Because the replication block was principally manifested by a severe reduction in integration, it is likely that NCp9 has a role in the integration process  and has also been shown to facilitate in vitro concerted integration even better than NCp7 .
The 6th international Retroviral NC symposium was supported by the Office of AIDS RESEARCH (OAR, USA), SAIC FREDERICK (NCI, USA), the ROYAL DUTCH ACADEMY OF SCIENCES (The Netherlands), The Center for Infection and Immunity Amsterdam (CINIMA, the Netherlands), the city of Amsterdam (the Netherlands) the Dutch AIDS Fund (The Netherlands), ANRS (Paris, France), Clean Air Europe, Greiner bio-one Europe, SANYO Europe. Projects have been funded in whole or in part with federal funds from the National Cancer Institute, National Institutes of Health, under contract N01-CO-12400. The content of this publication does not necessarily reflect the views or policies of the Department of Health and Human Services, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government.
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