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U N C O R R Ec Ted Pr O Effect of mutations K97A and E128A on RNA binding and self assembly of papaya mosaic potexvirus coat protein Marie-He´ le` ne Tremblay1, Nathalie Majeau1, Marie-Eve Laliberte´ Gagne´ 1, Katia Lecours2, He´ le` ne Morin1, Jean-Baptiste Duvignaud1, Marile` ne Bolduc1, Nicolas Chouinard1, Christine Pare´F1, Ste´ phane Gagne´ 2 and Denis Leclerc1 1 Centre de Recherche en Infectiologie, Univeriste´ Laval, Que´ bec, Canada 2De´ partement de Biochimie, Universite´ Laval, Que´ bec, Canada O O Keywords Papaya mosaic potexvirus (PapMV) coat proteinR (CP) was expressed assembly; coat protein; nucleocapsid; (CPDN5) in Escherichia coli and showed to self assemble into nucleocapsid papaya mosaic virus; potexvirus like particles (NLPs). Twenty per cent of the purified protein was found as NLPs of 50 nm in length and 80% was foundP as a multimer of 450 kDa (Received 20 July 2005, revised 29 Septem- ber 2005, accepted 25 October 2005) (20 subunits) arranged in a disk. Two mutants in the RNA binding domain of the PapMV CP, K97A and E128A showed interesting properties. The doi:10.1111/j.1742-4658.2005.05033.x proteins of both mutants could be easily purified and CD spectra of these proteins showed secondary and tertiaryD structures similar to the WT pro- tein. The mutant K97A was unable to self assemble and bind RNA. On the contrary, the mutant E128A showed an improved affinity for RNA and self assembled more efficientlyE in NLPs. E128A NLPs were longer (150 nm) than the recombinant CPDN5 and 100% percent of the protein was found as NLPs in bacteria. E128A NLPs were more resistant to diges- tion by trypsin than theT CPDN5 but were more sensitive to denaturation by heat. We discuss the possible role of K97 and E128 in the assembly of PapMV. C Papaya mosaic potexvirus (PapMV) is a memberE of particles that are very similar to the WT virus [3]. The the potexvirus family. The virion is a flexible rod in vitro assembly of PapMV was shown to be specific 500 nm in length and 15 nm in diameter composed of and triggered by 47 nucleotides of the 5¢ noncoding 1400 subunits of viral coat protein (CP) [1] assembledR region of the virus [6]. This region is free of any dis- around a plus-strand genomic RNA of 6656 nucleo- cernable secondary structure, an important feature for tides (nt) [2]. In vitro reconstitution of PapMV nucleo- initiation of the assembly process [6]. In vitro assembly capsid-like particles (NLPs) was previouslyR studied is specific when performed at a pH of 8.0–8.5 in a buf- using CP prepared from the acetic acid degradation of fer of low ionic strength [4] and elongation proceeds in purified virus [3]. Using this method, PapMV CP can the 5¢fi3¢ direction [7]. One atom of Ca2+ is attached be isolated from the genomicO RNA and used for to each subunit, which is probably important for the in vitro assembly assays [3]. Extracted CP has been structure of the protein [8]. Alignment of PapMV CP found as a variety of aggregates ranging from 14S to with the CP of other potexviruses reveals that these 25S [4] that include a disk-likeC structure (14 S) made proteins share 35% identity [9]. The N terminus of the of 18–20 subunits. These disks are helical structures proteins is the most divergent and their length is also (two turns of the helix) similar in architecture to the variable. It can reach more than 50 amino acids in the native virus particle [3,5].N The addition of RNA to the case of potato aucuba mosaic virus. Phosphorylation isolated disks triggers the assembly of long rod-shaped of the N terminus of potato virus X CP by host Abbreviations CP, coat protein; NLP,U nucleocapsid like particles; nt, nucleotide; PapMV, Papaya mosaic potexvirus. FEBS Journal (2005) ª 2005 The Authors Journal compilation ª 2005 FEBS 1 FEBS 5033 Dispatch: 25.11.05 Journal: FEBS CE: Blackwell Journal Name Manuscript No. B Author Received: No. of pages: 12 PE: Agila RNA binding and assembly of PapMV CP M.-H. Tremblay kinases was shown to render the genomic RNA more Results translatable [10]. It is possible that the incorporation of negative charges by phosphorylation of the N termi- Alignment of the potexvirus coat proteins nus destabilizes the subunits and favours disassembly of the particles, an important step in the initiation of The alignment of the amino acids sequences of 19 infection. potexviruses CPs between amino acid 91–169 of Pap-F Until now, most of the data collected on assembly MV CP revealed a consensus sequence (Fig. 1A). This of the potexvirus family have been obtained from Pap- conserved region shows the charged residues R104, MV in vitro assembly using partially denatured and K133, K137, and R161 that are believedO to be renatured proteins extracted by the acetic acid method involved in interaction with the genomic RNA and [3]. Even though in vitro assembly using this method play an important role in assembly and packaging of has been studied extensively, the nature of the interac- the viral genome [13]. It also containsO acidic residues tions between CP subunits, and between the subunits that could be important for the interaction with the and the genomic RNA remains unknown. genomic RNA, as shown for tobacco mosaic virus In this report, we showed that NLPs produced in CP [14]. Based on these observations,R we hypothes- Escherichia coli were very similar to the WT particles. ized that charged residues in the region 91–169 are Furthermore, extensive mutation analysis in the puta- good candidates for a specific interaction with the tive RNA binding domain of PapMV led to the iden- genomic RNA and excellentP targets for site specific tification of two mutants: one that had lost its mutagenesis. By introduction of mutations in the affinity for RNA, and one that showed an improved putative RNA binding domain, we hope to confirm affinity for RNA. The biochemical properties of the for the first time in the potexvirus family that this mutants were compared with the WT recombinant region is important for binding the genomic RNA proteins. and formation ofD NLPs. E A T C B E R R Fig. 1. (A) Alignment of a consensus sequence derived from 18 known potexvirus coat protein and the papaya mosaic virus coat protein (PapMV CP) in the conserved region 90–169 of PapMV. The amino acid corresponding to position 128 of the PapMV CP is an A in most potexviruses (underlined), an E in three differentO potexviruses including PapMV (bold), and T, V, S or Q occur in this position in the other five potexvirus sequences. The consensus was made using the CP sequences of: BaMV: Bamboo mosaic virus; PlAMV: Plantago asiatica mosaic virus; TVX: Tulip virus X; CsCMV: Cassava common mosaic virus; ClYMV: Clover yellow mosaic virus; HVX: Hosta virus X; LVX: Lily virus X; CymMV: Cymbidium mosaic virus; PAMV: Potato aucuba mosaic virus; NMV: Narcissus mosaic virus; PepMV: Pepino mosaic virus; FoMV: Foxtail mosaic virus; ScaVX: ScallionC virus X; WClMV: White clover mosaic virus; SMYEV: Strawberry mild yellow edge virus; PVX: Potato virus X; AltMV: Alternanthera mosaic virus; CVX: Cactus virus X; PapMV: Papaya mosaic virus. (B) Expression and purification of recombinant CPDN5, K97A, R104K105R108 ⁄ A, E128A and E148A. Lanes 1–7: Coomassie staining profile of the recombinant proteins. lane 1: E. coli lysate before induction ofN CPDN5, lane 2: E. coli lysate of CPDN5 16 h postinduction with 1 mM IPTG, lane 3: recombinant CPDN5 purified using a Ni2+ column; lane 4: purified K97A, lane 5: purified R104K105R108 ⁄ A lane 6: purified E128A lane 7: purified E148A, lane 8: PapMV CP from virus purified from plants. Lanes 9–14: Western blotting of purified recombinant proteins revealed with IgG directed against PapMV CP. Lane 9: Purified CPDN5, lane 10: purified K97A, lane 11: R104K105R108 ⁄ A, lane 12; E128A, lane13; E148A and lane 14: purified virus from infected plants.U 2 FEBS Journal (2005) ª 2005 The Authors Journal compilation ª 2005 FEBS M.-H. Tremblay RNA binding and assembly of PapMV CP that the purified protein was indeed PapMV CP Expression of PapMV CP and its mutated forms (Fig. 1B, lane 9). Following the same procedure, we in E. coli have purified several mutated forms of the PapMV CP. We amplified the PapMV CP gene by RT ⁄ PCR and We have generated nine different mutants that har- cloned the resulting PCR fragment in the E. coli bour one, two or three A substitutions (Fig. 1A). Five expression vector pET-3d. The PapMV CP harbours mutants R118-D120-K121 ⁄ A, K133-K137 ⁄ A, D142-F two M residues at positions 1 and 6 of the CP ORF. It D145 ⁄ A, R161A and E166-E167-R168 ⁄ A produced is not clear if both of these initiation codons are used unstable proteins and were undetectable or expressed during replication of the virus. However, it has been at very low levels. It is likely that mutagenesisO in this shown that a large proportion of the CP of the purified conserved region affected the native folding of the CP. virus lacks several amino acids at the N terminus [1]. The mutants K97A, R104K105R108 ⁄ A, E128A and To ensure production of only one ORF in E. coli,we E148A could be expressed to level similarO to CPDN5 removed the N-terminal five amino acids. M6 served as and easily purified using a 6·H tag as shown with the an initiation codon in our expression system. The intro- CPDN5 (Fig. 1B; lane 4, 5, 6 and 7). However, the duction of the initiation codon in the NcoI site intro- removal of imidazole duringR the dialysis made duced an extra A that is found in all the constructs the mutants R104K105R108 ⁄ A and E148A aggregate made in this study.
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