Organization of the major and minor capsid proteins in human papillomavirus type 33 virus-like particles
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1 Journal of General Virology (5),, 0-. Printed in Great Britain 0 Organization of the major and minor capsid proteins in human papillomavirus type virus-like particles Martin Sapp, l* Christoph Volpers, Marianne Miiller and Rolf E. Streeck Institute for Medical Microbiology and Institute for Pathology, University of Mainz, D-55 Mainz, Germany The organization of the major (L) and minor (L) proteins in the human papillomavirus capsid is still largely unknown. In this study we analysed the disulphide bonding between L proteins and the association of L proteins with capsomers using virus-like particles obtained in insect cells by co-expression of the L and L genes of human papillomavirus type. About 50% of the L protein molecules in these particles (. g/cm z) formed disulphide-bonded trimers. Reduction of the intermolecular disulphide bonds by dithiothreitol (DTT) treatment caused disassembly of virus-like particles into capsomers. This indicates that disulphide bonds between capsomers at the threefold symmetry positions of the capsid are essential for the assembly of the papiuomavirus capsid. In contrast, the L protein was not engaged in intermolecular disulphide bonding. The L protein remained associated with capsomers on disassembly by treatment with DTT. When the disassembly was carried out in 0"5 u-nac, complete L protein molecules bound preferentially to capsomer oligomers, whereas truncated L protein molecules bound only to monomers. In 0. u-nacl only complete L protein molecules remained bound to capsomers. This indicates that different regions of the L protein molecule are differentially involved in the association of the papillomavirus capsid. Papillomaviruses are a subfamily of the papovaviruses. The properties shared by these viruses include a circular dsdna genome, a nonenveloped virion and an icosahedral capsid. Papillomaviruses have a specific tropism for epithelial cells and have been found in a great variety of species. More than 0 types of human papillomavirus (HPV) have been recognized but only a few, e.g. HPV-I (which induces cutaneous warts), can be isolated as virus particles. The other HPVs, e.g. HPV- or HPV- (which are associated with genital carcinoma), have only been identified by cloning their genomes from epithelial lesions. Moreover, no system exists for the efficient propagation of HPVs in vitro. The capsid of papillomaviruses and of the other papovaviruses comprises capsomers, each a pentamer of the major capsid protein, L or VP, arranged in a T= icosahedral surface lattice (Baker et al., ; Liddington et al., ; Rayment et al., ). In addition, the papillomavirus capsid carries a minor protein, L (Komly et al., ), which contributes -5 % to the capsid protein, corresponding to -0 molecules per virion (Favre et al., ; Orth et al., ). Sixty of the capsomers are hexavalent, i.e. surrounded by six capsomers each, but capsomers are * Author for correspondence. Fax + 5. pentavalent, as dictated by the icosahedral symmetry. Therefore the capsid proteins in the different capsomers are not equivalently bonded. X-ray structure analysis of polyomavirus particles (Rayment et al., ) and simian virus 0 (SV0) virions (Liddington et al., ) and analysis by cryoelectron microscopy and threedimensional image reconstruction of HPV- and bovine papillomavirus type (Baker et al., ; Hagensee et al., ) have indicated that there are six symmetrically different VP or L protein molecules. The location and function of the minor capsid protein L in the papillomavirus capsid is largely unknown. Recent evidence indicating that it may be essential for packaging DNA (Zhou et al.,, ) suggests a position close to the core of the virion. We and others have recently succeeded in producing empty virus-like particles (VLP) of various papillomavirus types by synthesizing the L protein alone or in combination with the L protein, using vaccinia virus (Zhou et al., ; Hagensee et al., ) or baculovirus recombinants (Rose et al., ; Kirnbauer et al., ; Volpers et al., ). Both spherical particles of 50-0 nm diameter and tubular structures of 5-0nm and 50-0 nm diameter of numerous lengths have been obtained. Similar structures are found in naturally occurring papillomavirus infections (Finch & Klug, 5). The particles have a density of. g/cm ~ in CsC corresponding to empty, i.e. DNA-free, papillomavirus SGM
2 0 (a) Short communication (c) (b) 5 (d) 5 0 Fig.. VLPs purified as described previously (Volpers et al., ) by sedimentation on two successive CsC gradients were dialysed against PBS supplemented with 500 mn-nacl for h. After incubation for 0 rain at room temperature in the absence (a, b) or presence (c, d) of 0 mm-dtt the samples were loaded onto an.5 ml linear sucrose gradient and spun for.5 h at 000 r.p.m, in a SW 0 rotor at C. The TCA precipitates were resuspended in sample buffer (Laemmli, 0) and boiled for 5 rain. The proteins were analysed by SDS-PAGE and subsequently transferred to nitrocellulose membranes (Towbin e t al., ). The LI (a, c) and L proteins (b, d) were detected using MAb L- directed against L amino acids 0 (Sapp et al., ) and MAb L- directed against L amino acids -0 (C. Volpers, M. Sapp, P. J. F. Snijders, J. M. M. Walboomers & R. E. Streeck, unpublished results). Bound antibodies were detected with horseradish peroxidase coupled to goat anti-mouse IgG (Jackson Immunochemicals) and enhanced chemiluminescence (Amersham). Sedimentation was from left to right. The signal for L proteins was enhanced approximately fiftyfold by using more protein and longer exposure times. capsids. They are structurally indistinguishable from H P V virions (Hagensee et al., ) and induce neutralizing antibodies (Kirnbauer et al., ). In this study we analysed the organization o f the L and L proteins in VLPs o f HPV- produced by infection o f insect cells with recombinant baculoviruses. These studies were made possible by the availability o f highaffinity M A b s to both capsid proteins (Sapp et al., ; C. Volpers, M. Sapp, P. J. F. Snijders, J. M. M. W a l b o o m e r s & R. E. Streeck, unpublished results). W h e n expressed in insect cells, both L and L proteins were tightly associated with the nuclear matrix. VLPs were extracted after mild sonication and purified by two successive CsC centrifugations (Volpers et al., ). The HPV- L protein (55 ) produced under these conditions was always f o u n d to be partially degraded into 5 k D a and 5 k D a products. Similar degradation products o f the L protein have been observed in empty particles purified from lesions (Favre et al., 5). The L protein (50, migrating as a k D a protein in S D S - P A G E ) was even more susceptible to degradation in the V L P preparations. The larger L proteins f o u n d occasionally were p r o b a b l y due to modification. I n c o r p o r a t i o n o f L proteins into VLPs has previously been demonstrated using immunoelectron microscopy (Volpers et al., ). As previously shown by two-dimensional electrophoresis under reducing and nonreducing conditions, a b o u t 5 0 % o f the LI protein molecules in VLPs form intermolecular disulphide bonds yielding a 0 k D a trimer. Only the 55 k D a and 5 k D a proteins participate in intermolecular disulphide bonding. The remaining 50 % of L protein f o u n d as m o n o m e r s consists o f both the 55 k D a and 5 k D a proteins and 5 k D a degradation products (Volpers et al., ). In contrast to the L protein no shift in the electrophoretic mobility o f the L protein was f o u n d when VLPs submitted to reducing and nonreducing conditions were analysed by SDS P A G E, using a M A b to L protein for Western blotting (data not shown). This is in agreement with an analysis o f the disulphide cross-linking in HPV- virions purified from warts ( D o o r b a r & Gallimore, ) and demonstrates that the association of L proteins with both naturally occurring virus particles and VLPs is due to noncovalent binding. To investigate whether the intermolecular disulphide bonds between L proteins are formed within a capsomer or between L proteins in adjacent capsomers, VLPs were treated for 0 min with 0 m M - D T T as a reducing agent. DTT-treated and untreated V L P s were loaded onto a.5 ml sucrose gradient (0-0 % sucrose in PBS supplemented with 500 mm-nac and 5 lag/ml BSA) and spun for -5 h at 000 r.p.m, in an SW 0 rotor at C. Fractions (50 gl) were collected f r o m the top and proteins were precipitated by T C A and analysed by Western blotting using M A b L- (Sapp et al., )
3 Short communication.s!.s :, : i 0 S II ~i ~ ~ ~ W :':' :;::,i: : ~... : (b) ' m, m 0 m i!i iiii ii! (c) (d) (e) Fig.. VLPs incubated with 0 mn-dtt for 0 min were spun through a 0-0% sucrose gradient for h at 000 r.p.m, at C. Fractions (500 gl) were collected from the top and analysed as described in Fig. for the presence of L (a) and L protein (b). Only the upper fractions, out of the total, are shown. Thyroglobulin (S), catalase (ll.s) and haemoglobin (.S) were used as markers and run in a separate tube. Untreated (c) and DTT-treated VLPs before (d) and after (e) centrifugation (fraction ) were spotted onto copper grids and negatively stained using % phosphotungstic acid. The grids were observed and photomicrographs were taken with a Philips EM0 transmission microscope. The bar represents 0 nm. and MAb J. M. M. results), L - ( C. V o l p e r s, M. S a p p, P. J. F. S n i j d e r s, described, untreated VLPs which contain tubular Walboomers tures lengths respectively & R.E. (Fig. ). Streeck, Under the unpublished conditions of numerous particles (Volpers in addition et al., ) s e d i m e n t e d to struc- spherical in a b r o a d
4 Short communication -//-ME +fl-me ! 5 -- Fig.. DTT-treated VLPs were sedimented through a sucrose cushion to remove DTT and subsequently denatured with sample buffer lacking (-/LME, lane ) or containing (+fl-me, lane )//-mercaptoethanol. Untreated VLPs (lanes and ) served as controls. Samples were analysed by SDS-PAGE and transferred to nitrocellulose. The LI protein was detected using MAb LI-. peak (Fig. a). As shown in Fig. l(b), L protein and most of the L-protein degradation products cosedimented with L protein. In contrast, L protein was found mainly in the upper fractions of the gradients after DTT treatment, indicating partial disassembly of VLPs (Fig. c). An identical shift from fast to more slowly sedimenting material was observed for L protein (Fig. d). Partial disassembly was achieved with DTT concentrations as low as -5 mm (data not shown). It should be remembered that L protein amounts to only % of L protein in VLPs. In Fig. (b, d) larger amounts of protein and longer exposure times were used only to enhance the signal for L protein. To investigate whether monomeric L protein or capsomers were produced under these conditions, the disassembled VLPs were analysed by longer sedimentation runs in sucrose gradients ( h, 000r.p.m., SW 0 rotor) and by electron microscopy. As shown in Fig. (a), most of the L protein sedimented at -S, corresponding to a molecular mass of at least 00, whereas a minor fraction of LI protein sedimented faster than S. However, no monomeric L protein was detected. According to results using electron microscopy (Fig. d), the main products after DTT treatment of VLPs were monomeric capsomers. Untreated VLPs are also shown in Fig. (c) for comparison. These data clearly demonstrate that disulphide bonds between capsomers, i.e. between L protein molecules in adjacent capsomers, are essential for VLP assembly. To investigate whether the L proteins within capsomers were cross-linked by disulphide bonds, capsomers prepared by DTT treatment of VLPs were sedimented through a sucrose cushion to remove DTT and subsequently analysed by SDS-PAGE (Fig. ). Whereas 50 % of the L protein in untreated VLPs migrated as a 0 trimer under nonreducing conditions, in agreement with our previous finding (Fig., lane ), no L oligomers were found in the capsomer preparation (Fig., lane ). These data clearly indicate that disulphide bonds between three L protein molecules are essential for the assembly of capsomers into capsids, whereas intermolecular disulphide bonds between L protein molecules are not required to form capsomers. Similarly, no disulphide bonds were observed between VP molecules within capsomers in SV0 virions (Liddington et al., ). Even though we cannot exclude the possibility that intermolecular disulphide bonds between L protein molecules within capsomers were reduced by the DTT treatment, our results strongly suggest that the L trimer present in capsids is formed from L protein molecules in three adjacent capsomers. We then set out to resolve whether the association between L and L proteins could be further defined. Although proteolysis of the L protein was extensive, making interpretation difficult, some conclusions were reached. To start with we investigated whether the L and L proteins remained associated after disassembly into capsomers. As shown in Fig. (b), a set of L protein degradation products with apparent molecular masses ranging from 5 to as well as a modified L protein present in this VLP preparation cosedimented with the major peak of the L protein representing the capsomer fraction. However, most of the non-degraded L protein sedimented with the faster sedimenting fraction. Analysis by electron microscopy of fraction, which contained most of the full-length L protein, revealed the presence of mainly capsomer di- to tetramers (Fig. e). Sedimentation of the L protein changed dramatically when the VLPs were disassembled in low salt (0. M vs 0'5 N). Whereas sedimentation of the LI protein remained basically unchanged (Fig. a), most of the L protein degradation products dissociated from the L protein under these conditions and were now found near the top of the gradient (Fig. b). The high molecular mass undegraded L protein, however, was now found associated with monomeric rather than di- to tetrameric capsomers, indicating dissociation of the L protein-containing oligomeric capsomers. This finding indicates that there are at least two types of interaction between capsomers and L proteins. The domain responsible for the salt-independent interaction is lost in the partially degraded proteins. It would be interesting to map the precise domain(s) responsible for the interaction with capsomers using defined L protein deletion mutants. Our results indicating that L L protein interactions are stabilized by salt are in agreement with previous reports that salt increases the stability of virions of the papovavirus group (Brady et al., ; Salunke et al., ). X-ray diffraction data of empty capsids and complete virions of polyomavirus (Griffith et al., ) and SV0
5 Short communication (a).s -S S (b) "~ ( Fig.. VLPs were dialysed for h against PBS, incubated for 0 min with 0 mm-dtt, subsequently loaded onto a 0-0 % sucrose gradient in PBS and spun at 000 r.p.m, for h in an SW 0 rotor. Fractions (500 gl) were collected from the top. The proteins were precipitated and analysed as described. The L (a) and L (b) proteins were detected using MAb LI- and MAb L-, respectively. Only the upper fractions, out of the total, are shown. Thyroglobulin (S), catalase (.S) and haemoglobin (.S) analysed in a separate gradient of the same run served as markers. Sedimentation was from left to right. virions (Liddington et al., ) have previously implied that each of the minor capsid proteins, VP or VP, is associated with the hollow of a capsomer, linking the nucleocore to the virus shell. Even though L proteins may serve a similar function, i.e. binding the virus DNA, the lower number of at most 0 L protein molecules per HPV capsid, as compared to about 0 molecules of minor capsid proteins found in SV0 and polyomavirus, suggests an organization that may be quite different from that of other papovaviruses. According to our data, different regions of the L protein molecule may be involved in the association with adjacent capsomers and in binding to single capsomers. A portion of the L protein molecule may thus be buried within a capsomer, whereas other portions should be accessible between capsomers. This is supported by recent reports showing that L proteins are accessible to antibody binding in complete virions (Yaegashi et al., ) and empty capsids (C. Volpers, M. Sapp, P. J. F. Snijders, J. M. M. Walboomers & R.E. Streeck, unpublished results) and, in addition, are able to induce neutralizing antibodies (Christensen et al., ; Roden et al., ). We thank Ute Kraus for excellent technical assistance. This work was supported by the Deutsche Forschungsgemeinschaft and a 'Graduiertenkolleg' scholarship to C.V. References BAKER, T.S., NEWCOMB, W.W., OLSON, N.H., COWSERT, L. M., OLSON, C. & BROWN, J. C. (). Structures of bovine and human papillomaviruses. Biophysical Journal 0, 5 5. BRADY, J. N., WINSTON, V. D. & CONSIGLI, R. A. (). Dissociation of polyoma virus by the chelation of calcium ions found associated with purified virions. Journal of Virology,. CHRISTENSEN, N. D., KREIDER, J. S., KAN, N. C. & DIANGELO, S. L. (). The open reading frame L of cottontail rabbit papillomavirus contains antibody-inducing neutralizing epitopes. Virology, 5-5. DOORBAR, J. & GALLtMORE, P. H. (). Identification of proteins encoded by the L and L open reading frames of human papillomavirus la. Journal of Virology, -. FAVRE, M., BREITBURD, F., CROISSANT, O. & ORTH, G. (5). Structural polypeptides of rabbit, bovine, and human papillomaviruses. Journal of Virology, -. FAVRE, M., BREITBURD, F., CROISSANT, O. & ORTH, G. (). Chromatin-like structures obtained after alkaline disruption of bovine and human papillomaviruses. Journal of Virology, FINCH, J.T. & KLUG, A. (5). The structure of viruses of the papilloma-polyoma type. III. Structure of rabbit papilloma virus. Journal of Molecular Biology, l.
6 Short communication GRIFFITH, J. P., GRIFFITH, D. L., RAYMENT, I., MURAKAMI, W.T. & CASPAR, D. k. D. (). Inside polyomavirus at 5 A resolution. Nature 55, 5-5. HAGENSEE, M.E., YAEGASHI, N. & GALLOWAY, D.A. (). Selfassembly of human papillomavirus type capsids by expression of the L protein alone or by coexpression of the L and L capsid proteins. Journal of Virology,. HAGENSEE, M. E., OLSON, N. H., BAKER, T. S. & GALLOWAY, D.A. (). Three-dimensional structure of vaccinia-produced human papillomavirus type capsids. Journal of Virology, KIRNBAUER, R., BOOY, F., CHENG, N., LOWRY, D. R. & SCHILLER, J. T. (). Papillomavirus L major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proceedings of the National Academy of Sciences, USA, 0-. KOMLY, C. A., BREITBURD, F., CROISSANT, 0. ~; STREECK, R. E. (). The L open reading fi'ame of human papillomavirus type la encodes a minor structural protein carrying type-specific antigens. Journal of Virology 0, -. LAEMMLI, U.K. (0). Cleavage of structural proteins during the assembly of the head of bacteriophage T. Nature, 0 5. LIDDINGTON, R. C., YAN, Y., MOULAI, J., SAHLI, R., BENJAMIN, T. L. & HARRISON, S.C. (). Structure of simian virus 0 at. A resolution. Nature 5,. ORTH, G., BREITBURD, F. & FAVRE, M. (). Evidence for antigenic determinants shared by structural polypeptides of (Shope) rabbit papillomavirus and human papillomavirus type. Virology, 55. RAYMENT, I., BAKER, T.S., CASPAR, D. L. D. & MURAKAMI, W.T. (). Polyoma virus capsid structure at -5 A resolution. Nature 5, -. RODEN, R. B. S., WESSINGER, E. M., HENDERSON, D.W., BOOY, F., KIRNBAUER, R., MUSHINSKI, J. F., LOWY, O. R. ~; SCHILLER, J. T. (). Neutralization of bovine papillomavirus by antibodies to L & L capsid proteins. Journal of" Virology, ROSE, R. C., BONNEZ, W., REICHMAN, R. C. & GARCEA, R. L. (). Expression of human papillomavirus type L protein in insect cells: in vivo and in vitro assembly of virus-like particles. Journal of Virology,. SALUNKE, D.M., CASPAR, D. L. D. & GARCEA, R.L. (). Selfassembly of purified polyomavirus capsid protein VP. Cell, 5-0. SAPP, M., KRAUS, U., VOLPERS, C., SNIJDERS, P. J. F., WALBOOMERS, J. U. M. & STREECK, R. E. (). Analysis of type-restricted and cross-reactive epitopes on virus-like particles of human papillomavirus type and in infected tissues using monoclonal antibodies to the major capsid protein. Journal of General Virology 5, 5-. TOWBIN, H., STAEHELIN, T. ~L GORDON, J. (). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences, USA, VOLPERS, C., SCHIRMACHER, P., STREECK, R. E. & SAPP, M. (). Assembly of the major and the minor capsid protein of human papillomavirus type into virus-like particles and tubular structures in insect cells. Virology 00, YAEGASHI, N., JENISON, S.A., VALENTINE, J.M., DUNN, M., TAICHMANN, L.B., BAKER, D.A. & GALLOWAY, D.A. (). Characterization of murine polyclonal antisera and monoclonal antibodies generated against intact and denatured human papillomavirus type virions. Journal of Virology 5, -. ZHOU, J., SUN, X.-Y., STENZEL, D.J. & FRAZER, I.H. (). Expression of vaccinia recombinant HPV L and L0RF proteins in epithelial cells is sufficient for assembly of HPV virionlike particles. Virology 5, 5-5. ZHOU, J., STENZEL, D. J., SUN, X.-Y. & FRAZER, I. H. (). Synthesis and assembly of infectious bovine papillomavirus particles in vitro. Journal of General Virology,. ZHOU, J., SUN, X.-Y., Louis, K. & FRAZER, I. H. (). Interaction of human papillomavirus (HPV) type capsid proteins with HPV DNA requires an intact L N-terminal sequence. Journal of Virology, -5. (Received March 5; Accepted April 5)
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