- Open Access
Two dimensional VOPBA reveals laminin receptor (LAMR1) interaction with dengue virus serotypes 1, 2 and 3
© Tio et al; licensee BioMed Central Ltd. 2005
- Received: 24 February 2005
- Accepted: 25 March 2005
- Published: 25 March 2005
The search for the dengue virus receptor has generated many candidates often identified only by molecular mass. The wide host range of the viruses in vitro combined with multiple approaches to identifying the receptor(s) has led to the notion that many receptors or attachment proteins may be involved and that the different dengue virus serotypes may utilize different receptors on the same cells as well as on different cell types.
In this study we used sequential extraction of PS Clone D cell monolayers with the detergent β-octylglucopyranoside followed by sodium deoxycholate to prepare a cell membrane-rich fraction. We then used 2 dimensional (2D) gel electrophoresis to separate the membrane proteins and applied a modified virus overlay protein binding assay (VOPBA) to show that dengue virus serotypes 1, 2 and 3 all interact with the 37 kDa/67 kDa laminin receptor (LAMR1), a common non-integrin surface protein on many cell types.
At least 3 of the 4 dengue serotypes interact with the 37 kDa/67 kDa laminin receptor, LAMR1, which may be a common player in dengue virus-cell surface interaction.
The dengue viruses have become recognized as important global pathogens causing dengue haemorrhagic fever not only in Southeast Asia but also in South and Central America and in the Caribbean.[1, 2]. There are 4 closely related dengue viruses referred to as DENV-1, DENV-2, DENV-3 and DENV-4. They are mosquito borne viruses with a single stranded positive sense RNA genome around 11 kilobases in length, and are able to infect both mosquito and human hosts. A wide range of cell types from multiple species is susceptible to infection with dengue viruses in vitro. Numerous studies have attempted to identify the cell surface receptor or receptors utilized by the dengue viruses to gain entry into susceptible cells, but multiple approaches using different cell lines and different dengue virus strains have generated many candidate DENV interacting proteins identified in some cases only by molecular mass [4–11]. Heparan sulfates and the C-type lectins DC-SIGN and L-SIGN have been shown to mediate infection by dengue viruses and most recently, studies using a standard virus overlay protein binding assay (VOPBA) have suggested that in the liver cell line HepG2, different DENV serotypes utilize different cell surface molecules. More specifically, mass spectrometric methods have been used to identify reactive bands using VOPBA and it has been suggested that DENV-2 interacts with GRP78 while DENV-1 interacts with the 37 kDa/67 kDa high affinity laminin receptor.
Identification of reference protein spots in detergent extracts of PS Clone D cell monolayer
2D VOPBA of β octyl-glucopyranoside extract
2D VOPBA of sodium deoxycholate extract of cells previously extracted with β octyl-glucopyranoside
MALDI TOF MS
Peptide mass fingerprints were obtained using Voyager DE STR (Applied Biosystems, Foster City, CA, USA) and mass lists were submitted for search against the NCBI protein database (National Institutes of Health, Bethesda, MD, USA) using the MASCOT search engine. Spectra and their corresponding mass-lists generated from analysis of the tryptic digests are provided as additional files 1,2,3,4,5.
Immunoblot confirmation of LAMR1 and lamin B1 spots on 2D gel blots
LAMR1 is expressed on the surface of PS Clone D cells
The investigation of early events in the infection of susceptible cells by dengue viruses is important in the quest to understand the ability of this group of mosquito borne viruses to infect both insect and mammalian cells, yet appear to have a restricted tissue tropism in the human host. Determination of the nature of the early interactions of the infecting viruses with molecules on the surface of susceptible cells provides for the possibility that this understanding can lead to the development of therapeutic agents that can be used to inhibit virus infection. The laminin receptor has already been described as a receptor for DENV-1 by single dimension VOPBA followed by MS/MS. The results from the MASCOT search showed multiple hits in this particular study, indicating several possibilities, including ATP synthase β chain, β actin and the laminin receptor, but the authors selected the lower scoring laminin receptor for further investigation. This was a reasonable choice since this molecule has previously been identified as a receptor for the alphaviruses Sindbis virus and Venezuelan equine encephalitis virus (VEEV) and the flavivirus tick-borne encephalitis virus (TBEV).
In our study, 2D VOPBA was used to eliminate the problem of co-migrating bands in a single dimension and the mass list generated from trypsin digestion of the most prominent reactive spot turned up numerous hits unambiguously listing the same protein, variously known as protein 40 kD, laminin-binding protein, 34/67 kDa laminin receptor, laminin receptor 1, LAMR1, Lamr1 protein, 67 kDa laminin receptor, 40S ribosomal protein SA, and so on. Contrary to earlier suggestions that LAMR1 is a DENV-1 specific receptor[14, 16], in our hands, DENV-1, DENV-2 and DENV-3 were all shown to interact with the same molecule LAMR1 although DENV-4 did not. It is thus likely that in the PS Clone D cells we have studied, at least 3 of the 4 different dengue serotypes utilize the same surface protein to gain entry into the cells. In our study we also did not find any evidence of DENV-2 binding to BiP/GRP78 as has been shown using single dimension VOPBA.
LAMR1 is a non-integrin receptor interacting with the extracellular matrix. It is generally accepted that the 37 kDa form is the precursor to the 67 kDa form although it is still not clear how this transition occurs. We have used a commercially available rabbit polyclonal antibody raised against a recombinant protein corresponding to amino acids 110–250 of human LAMR1 to show that this protein can be found in patches on the surface of PS clone D cells which are not contact inhibited in vitro. This distribution of LAMR1 is consistent with the findings of Donaldson et al, and it is thus possible that LAMR1 may be utilized as a receptor by the dengue viruses. Other groups have already shown that LAMR1 is a functional receptor for Sindbis virus, VEEV, TBEV and DENV1[16, 24–26]. We have not included functional studies in this present work, as this study is meant to be an exploratory study of dengue virus interacting proteins in PS Clone D cells using 2D VOPBA as an interrogating tool. There is no doubt that the treatment of the cell extracts limits the ability of this method to identify interactions dependent upon conformational structures, nevertheless, we managed to identify LAMR1 confirming previous observations by other investigators. We have further shown that LAMR1 interaction is not limited to DENV-1 alone, but that DENV-2 and DENV-3 also interact with LAMR1 and that this may be a common receptor for dengue virus entry into cells.
Many integrins have been shown to function as receptors for different viruses, for example the α6 integrins mediate human papillomavirus entry, β3 integrins mediates cell entry by hantaviruses., α2β1 integrin is a receptor for human echovirus 1.[30, 31], α5β1 integrin binds human parvovirus B19, α2β1 and αxβ2 mediate rotavirus infection and αvβ3 is the receptor for the flavivirus West Nile virus (WNV).. Many viruses are now known to infect cells through a multistep process involving binding to the cell surface followed by internalization, often through interacting with more than one surface molecule. Outside-in binding of integrins leads also to signal transduction, and this functional activation has been shown to be necessary for internalization as in the example of human parvovirus B19. In the case of adenoviruses, integrin clustering due to receptor binding initiates the signalling events required for internalization. The finding that DENV-1, DENV-2 and DENV-3 interact with the laminin receptor is thus consistent with this growing body of work describing the utilization by viruses of extracellular matrix protein receptors for gaining entry into cells.
In this study we have also identified dengue virus envelope protein interaction with an actin binding protein Hip55, which has been shown to be involved in endocytosis, vesicular transport and signal transduction. Hip55 has also been shown to interact with CD2v protein of African swine fever virus (ASFV) and colocalizes to areas surrounding perinuclear virus factories in ASFV infected cells. The role of Hip55 in the life cycle of dengue virus should be further investigated.
In our preparations of dengue virus antigens, DENV-4 antigen had the weakest reactivity in ELISA (data not shown) suggesting a lower titre of antigen than the other 3 serotypes, but the DENV-4 2D VOPBA did show a different reactivity pattern, picking out lamin B1 instead of LAMR1. Lamin B1 is not a plasma membrane protein but is part of the nuclear membrane[38, 39] and is thus unlikely to be an alternative receptor for DENV-4. The significance of the reaction of DENV-4 envelope protein with lamin B1 is unclear and will be the subject of further studies. It is also interesting that DENV-4 envelope also reacted with another protein involved in vesicle transport and target membrane fusion, the p47 protein cofactor of NSFL1/p97. The similarity of function of the p47 protein with that of Hip 55, which is reactive with all 4 dengue serotypes, suggests that DENV-4 may use a different pathway than DENV-1, DENV-2 and DENV-3 in the course of infection of a particular cell.
Two-dimensional VOPBA was used to identify cell membrane proteins interacting with dengue virus envelope protein. This approach identified several interactors including LAMR1, a non-integrin laminin binding protein, which has previously been suggested as a receptor for DENV-1 but not other dengue virus serotypes. Using more rigorous tools we have shown clearly that LAMR1 interacts not only with DENV-1 but also with DENV-2 and DENV-3. We have further shown that dengue virus envelope protein from all 4 serotypes also interacts with an actin binding protein Hip55 and that DENV-4 differs from the other three dengue virus serotypes in that it's envelope protein interacts with lamin B1 and p47 and does not interact with LAMR1.
Preparation of virus antigens
The 4 prototype dengue viruses were used in this study. All viruses were propagated in Aedes albopictus C6/36 cells grown in Leibovitz 15 media supplemented with 5% heat inactivated foetal calf serum, antibiotics and 10% tryptose phosphate broth. Antigens were prepared by inoculating C6/36 cell monolayers with the different DENV serotypes as described previously and harvested when syncytium formation was extensive. Cell culture fluids were clarified by centrifugation before use. Fluids similarly prepared from mock infected C6/36 cells were used as negative antigen controls.
Preparation of cell and membrane extracts
Just confluent flasks of the porcine kidney cell line PS Clone D were used in the preparation of detergent extracts for separation by 2D gel electrophoresis. Monolayers were washed twice with phosphate buffered saline (PBS) before subjecting to treatment with 1% β octyl-glucopyranoside (βOG) in a hypotonic buffer containing 10 mM HEPES, 1.5 mM MgCl2, 5 mM KCl and a protease inhibitor cocktail (Boehringer Mannheim GmbH, Germany), pH 7.5 rocking at 4°C for 1 hour. The solution was removed and designated βOG-extract.
The remaining membranes, cytoskeleton and nuclei were then washed for 1 hour at 4°C with a solution containing 2% CHAPS in the same buffer as described above. The resulting solution was discarded and the residual material solubilized by rocking at 4°C for 1 hour in the above buffer containing 1% sodium deoxycholate (NaDOC). The resulting solution was removed and designated βOG-insoluble NaDOC-extract.
All extracts were spun in a microfuge at 14,000 rpm for 10 minutes and the supernatants stored at -20°C until use.
Sample preparation for 2D gel electrophoresis
All samples were prepared for 2D gel electrophoresis using the Ready Prep 2-D Cleanup Kit (BioRad Laboratories, Hercules, CA, USA) according to the manufacturer's instructions.
2D gel electrophoresis
Protein pellets were resolubilized in IPG strip rehydration solution (8 M urea, 2% CHAPS, 40 mM DTT, 0.5% IPG buffer pH3-10, bromophenol blue) at room temperature for 30 minutes, then spun in a microfuge at 14,000 rpm for 10 min. 125 ul of the resulting supernatant was used for each IPG strip (ReadyStrips pH 3-10, 7 cm, BioRad Laboratories, Hercules, CA, USA) and rehydration was achieved at 50 uA for 15 hours at 20°C using the IPGphor IEF system (Amersham Pharmacia Biotech, Uppsala, Sweden). Subsequently IEF was carried out for 30 minutes at 500 V, 30 minutes at 1000 V and 2 to 2.5 hours at 8000 V with a step-and-hold gradient until a total of 8500 volt-hours had been achieved.
IPG strips were then washed with distilled water and then equilibrated by rocking for 20 minutes at room temperature in SDS equilibration buffer (50 mM Tris-HCl pH 8.8, 6 M urea, 30% glycerol, 2% SDS) containing 10 mg/ml DTT, allowing for at least 5 ml of buffer per strip.
Strips were then washed with distilled water and placed on the top surface of the second dimension gel which was a 10% SDS polyacrylamide gel polymerized overnight. Molecular weight markers were applied onto small pieces of chromatography paper and inserted next to each strip on the top of each gel, after which the strips and markers were sealed with 0.7% agarose in 0.125 M Tris-HCl pH 6.8. The second dimension separation of proteins by molecular mass was achieved at a constant 140 V (Mini Protean 3, BioRad Laboratories, Hercules, CA, USA).
Electrotransfer of 2D gels to nitrocellulose
The Hoefer TE series Transfor Electrophoresis Unit (Hoefer Scientific Instruments, San Francisco, CA, USA) was used to electrotransfer proteins from 2D gels to nitrocellulose membranes at 200 mA for 1 hour in ice cold Towbin buffer (25 mM Tris, 192 mM glycine, 20% methanol). Nitrocellulose blots were then stained using Ponceau S. A record of the positions of the visible protein spots on each blot was made by scanning the Ponceau S probed blot using ImageScanner (Amersham Pharmacia Biotech, Uppsala, Sweden) and the software ImageMaster Labscan v3.00 (Amersham Biosciences, UK). After scanning, the Ponceau S was stripped by washing in water and the blots were then blocked by rocking for 1 hour in PBS containing 5% skimmed milk.
Virus overlay protein binding assay (VOPBA)
The 2D blots were incubated overnight with rocking at room temperature with clarified antigen preparations and mock-infected controls. The blots were then washed with PBS and incubated with the anti-flavivirus monoclonal antibody 4G2 in another overnight incubation at room temperature. After washing with PBS, the blots were incubated with rabbit-anti-mouse Ig HRP (DAKO, Glostrup, Denmark) at 1:1000 dilution in 5% skimmed milk in PBS for 2 hrs at room temperature. The blots were then washed with PBS and reactive protein spots were visualized by developing with the chromogenic substrate, 4-chloro-1-naphthol/hydrogen peroxide. Reaction was stopped after 1 hr by washing with water. The membranes were scanned and compared with the Ponceau S images scanned previously using Adobe Photoshop version 5.0 LE (Adobe Systems Inc., San Jose, CA, USA).
In-gel trypsin digestion and analysis by MALDI-TOF MS
Reactive spots seen on the blots were identified in the Ponceau S scans which had been recorded previously and the corresponding spots in the coomassie blue-stained gel were picked and stored in UHQ water in 0.5 ml microfuge tubes at 4°C. During all steps in the digestion process the buffer used was 5 mM NH4HCO3. Gel spots were first destained with 50% HPLC grade methanol. Destained spots were dehydrated with acetonitrile for 10 minutes before incubation with 10 mM DTT for 50 minutes at 55°C. This was followed by incubation with 55 mM iodoacetamide (IAA) for 30 minutes at room temperature in the dark. The spots were then washed twice with buffer for 20 minutes each time, dehydrated with acetonitrile for 10 minutes and rehydrated with buffer. Finally the gel spots were dehydrated twice with acetonitrile for 10 minutes each time and dried completely by centrifugation under vacuum (DNA Speed-Vac DNA110, Savant Instruments Inc, Farmingdale, NY, USA) for 10 minutes. Each gel spot was then reswelled in 5 ul of 12.5 ng/ul of sequencing grade trypsin (Promega, Madison, WI, USA) in 5 mM NH4HCO3 for 45 minutes on ice. Excess trypsin solution was then removed, the spots were covered in 5 ul buffer and digestion was allowed to proceed at 37°C overnight. Digests were stored at -20°C until analysed.
Analysis by MALDI-TOF MS
For MALDI analysis, digests were thawed, spun in a microfuge at 14,000 rpm for 10 minutes. One ul of the supernatant was mixed in a 1:1 ratio with a 1:10 dilution of saturated α-cyano-4-hydroxycinnamic acid (ACCA) matrix in 0.25% trifluoroacetic acid, 50% acetonitrile, 50% water. This mixture was spotted onto MALDI target plates and spectra were acquired using Voyager-DE STR Biospectrometry workstation (Applied Biosystems, Foster City, CA, USA). Peptide mass lists were submitted for search against the NCBI database (National Institutes of Health, Bethesda, MD, USA) using the MASCOT search engine (Matrix Science, London, UK). No constraints were set for species but carbamiodomethylation of cysteine residues and possible missed-cleavages were included.
Immunostaining of 2D gel blots
The 2D blots were incubated with polyclonal rabbit antisera against LAMR1 and Lamin B1 diluted 1:200 in PBS with 5% skimmed milk at room temperature, overnight with rocking. After extensive washing with PBS, the bound antibodies were detected with anti rabbit Ig conjugated with horseradish peroxidase, and visualized using the chromogenic substrate 4-chloro-1-naphthol/hydrogen peroxide as described above. Antisera were obtained from Santa Cruz Biotechnology (Santa Cruz, CA, USA).
Surface staining of cells and photomicrography
Cells were resuspended at 1 × 105 cells per ml in Leibovitz 15 media containing 3% heat inactivated foetal calf serum, antibiotics and tryptose phosphate broth. Resuspended cells were delivered in 25 ul volumes to individual wells of multitest slides (Erie Scientific Co., Portsmouth, NH, USA) and allowed to adhere overnight in a moist box at 37°C. Cells were then washed in PBS and fixed with 3.7% paraformaldehye in PBS at pH 7.4 for 15 minutes followed by a shift to 2% paraformaldehyde in PBS at pH 8.5 for a further 15 minutes. After washing in PBS slides were air dried and stored at -20°C until use.
Prior to staining, slides were incubated in 50 mM ammonium chloride in PBS for 5 minutes, washed thoroughly and blocked in 1% foetal calf serum in PBS for 30 minutes. Immunofluorescence staining of the surface of cells was achieved by incubation for 1 hour with polyclonal rabbit antisera against LAMR1 at 1:25 dilution in PBS containing 1% foetal calf serum. After washing with PBS the cells were incubated with anti rabbit Ig conjugated with Alexa Fluor 488 (Molecular Probes, Eugene, OR, USA) at 1:1000 dilution for 30 minutes following by washing with PBS. DAPI was used to counterstain nuclei. Slides were viewed using an Axiovert 200 (Zeiss, Germany) with filter sets appropriate for FITC and DAPI.
Photomicrography was achieved using a cooled CCD monochrome 12 bit camera Evolution QEi and Image-Pro 5.0 software (Media Cybernetics Inc., Canada) was used for preparing fluorescence composite images with pseudocolour. Adobe Photoshop version 5.0 LE was used to compose and present the figure collage.
This work was funded in part by Venture Technologies Sdn Bhd and by Universiti Malaysia Sarawak.
- Gibbons RV, Vaughn DW: Dengue: an escalating problem. Bmj 2002, 324: 1563-1566. 10.1136/bmj.324.7353.1563PubMed CentralView ArticlePubMedGoogle Scholar
- Gubler DJ: The changing epidemiology of yellow fever and dengue, 1900 to 2003: full circle? Comp Immunol Microbiol Infect Dis 2004, 27: 319-330. 10.1016/j.cimid.2004.03.013View ArticlePubMedGoogle Scholar
- van Regenmortel MHV, Fauquet CM, Bishop DHL, Carsten EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeoch DJ, Pringle CR, Wickner RB: Virus Taxonomy: Seventh Report of the International Committee on Taxonomy of Viruses. San Diego, Wien, New York, Academic Press; 2000:1024.Google Scholar
- Bielefeldt-Ohmann H, Meyer M, Fitzpatrick DR, Mackenzie JS: Dengue virus binding to human leukocyte cell lines: receptor usage differs between cell types and virus strains. Virus Res 2001, 73: 81-89. 10.1016/S0168-1702(00)00233-1View ArticlePubMedGoogle Scholar
- Hung JJ, Hsieh MT, Young MJ, Kao CL, King CC, Chang W: An external loop region of domain III of dengue virus type 2 envelope protein is involved in serotype-specific binding to mosquito but not mammalian cells. J Virol 2004, 78: 378-388. 10.1128/JVI.78.1.378-388.2004PubMed CentralView ArticlePubMedGoogle Scholar
- Martinez-Barragan JJ, del Angel RM: Identification of a putative coreceptor on Vero cells that participates in dengue 4 virus infection. J Virol 2001, 75: 7818-7827. 10.1128/JVI.75.17.7818-7827.2001PubMed CentralView ArticlePubMedGoogle Scholar
- Moreno-Altamirano MM, Sanchez-Garcia FJ, Munoz ML: Non Fc receptor-mediated infection of human macrophages by dengue virus serotype 2. J Gen Virol 2002, 83: 1123-1130.View ArticlePubMedGoogle Scholar
- Ramos-Castaneda J, Imbert JL, Barron BL, Ramos C: A 65-kDa trypsin-sensible membrane cell protein as a possible receptor for dengue virus in cultured neuroblastoma cells. J Neurovirol 1997, 3: 435-440.View ArticlePubMedGoogle Scholar
- Reyes-del Valle J, del Angel RM: Isolation of putative dengue virus receptor molecules by affinity chromatography using a recombinant E protein ligand. J Virol Methods 2004, 116: 95-102. 10.1016/j.jviromet.2003.10.014View ArticlePubMedGoogle Scholar
- Salas-Benito JS, del Angel RM: Identification of two surface proteins from C6/36 cells that bind dengue type 4 virus. J Virol 1997, 71: 7246-7252.PubMed CentralPubMedGoogle Scholar
- Yazi Mendoza M, Salas-Benito JS, Lanz-Mendoza H, Hernandez-Martinez S, del Angel RM: A putative receptor for dengue virus in mosquito tissues: localization of a 45-kDa glycoprotein. Am J Trop Med Hyg 2002, 67: 76-84.PubMedGoogle Scholar
- Chen Y, Maguire T, Hileman RE, Fromm JR, Esko JD, Linhardt RJ, Marks RM: Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat Med 1997, 3: 866-871. 10.1038/nm0897-866View ArticlePubMedGoogle Scholar
- Tassaneetrithep B, Burgess TH, Granelli-Piperno A, Trumpfheller C, Finke J, Sun W, Eller MA, Pattanapanyasat K, Sarasombath S, Birx DL, Steinman RM, Schlesinger S, Marovich MA: DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 2003, 197: 823-829. 10.1084/jem.20021840PubMed CentralView ArticlePubMedGoogle Scholar
- Jindadamrongwech S, Smith DR: Virus Overlay Protein Binding Assay (VOPBA) reveals serotype specific heterogeneity of dengue virus binding proteins on HepG2 human liver cells. Intervirology 2004, 47: 370-373. 10.1159/000080882View ArticlePubMedGoogle Scholar
- Jindadamrongwech S, Thepparit C, Smith DR: Identification of GRP 78 (BiP) as a liver cell expressed receptor element for dengue virus serotype 2. Arch Virol 2004, 149: 915-927. 10.1007/s00705-003-0263-xView ArticlePubMedGoogle Scholar
- Thepparit C, Smith DR: Serotype-specific entry of dengue virus into liver cells: identification of the 37-kilodalton/67-kilodalton high-affinity laminin receptor as a dengue virus serotype 1 receptor. J Virol 2004, 78: 12647-12656. 10.1128/JVI.78.22.12647-12656.2004PubMed CentralView ArticlePubMedGoogle Scholar
- Cao W, Henry MD, Borrow P, Yamada H, Elder JH, Ravkov EV, Nichol ST, Compans RW, Campbell KP, Oldstone MB: Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 1998, 282: 2079-2081. 10.1126/science.282.5396.2079View ArticlePubMedGoogle Scholar
- Borrow P, Oldstone MB: Characterization of lymphocytic choriomeningitis virus-binding protein(s): a candidate cellular receptor for the virus. J Virol 1992, 66: 7270-7281.PubMed CentralPubMedGoogle Scholar
- Nordhoff E, Egelhofer V, Giavalisco P, Eickhoff H, Horn M, Przewieslik T, Theiss D, Schneider U, Lehrach H, Gobom J: Large-gel two-dimensional electrophoresis-matrix assisted laser desorption/ionization-time of flight-mass spectrometry: an analytical challenge for studying complex protein mixtures. Electrophoresis 2001, 22: 2844-2855. 10.1002/1522-2683(200108)22:14<2844::AID-ELPS2844>3.3.CO;2-ZView ArticlePubMedGoogle Scholar
- Egelhofer V, Bussow K, Luebbert C, Lehrach H, Nordhoff E: Improvements in protein identification by MALDI-TOF-MS peptide mapping. Anal Chem 2000, 72: 2741-2750. 10.1021/ac990686hView ArticlePubMedGoogle Scholar
- Falconar AK: Identification of an epitope on the dengue virus membrane (M) protein defined by cross-protective monoclonal antibodies: design of an improved epitope sequence based on common determinants present in both envelope (E and M) proteins. Arch Virol 1999, 144: 2313-2330. 10.1007/s007050050646View ArticlePubMedGoogle Scholar
- Perkins DN, Pappin DJ, Creasy DM, Cottrell JS: Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20: 3551-3567. 10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2View ArticlePubMedGoogle Scholar
- de Hoog CL, Foster LJ, Mann M: RNA and RNA binding proteins participate in early stages of cell spreading through spreading initiation centers. Cell 2004, 117: 649-662. 10.1016/S0092-8674(04)00456-8View ArticlePubMedGoogle Scholar
- Wang KS, Kuhn RJ, Strauss EG, Ou S, Strauss JH: High-affinity laminin receptor is a receptor for Sindbis virus in mammalian cells. J Virol 1992, 66: 4992-5001.PubMed CentralPubMedGoogle Scholar
- Ludwig GV, Kondig JP, Smith JF: A putative receptor for Venezuelan equine encephalitis virus from mosquito cells. J Virol 1996, 70: 5592-5599.PubMed CentralPubMedGoogle Scholar
- Protopopova EV, Konavalova SN, Loktev VB: [Isolation of a cellular receptor for tick-borne encephalitis virus using anti-idiotypic antibodies]. Vopr Virusol 1997, 42: 264-268.PubMedGoogle Scholar
- Donaldson EA, McKenna DJ, McMullen CB, Scott WN, Stitt AW, Nelson J: The expression of membrane-associated 67-kDa laminin receptor (67LR) is modulated in vitro by cell-contact inhibition. Mol Cell Biol Res Commun 2000, 3: 53-59. 10.1006/mcbr.2000.0191View ArticlePubMedGoogle Scholar
- Evander M, Frazer IH, Payne E, Qi YM, Hengst K, McMillan NA: Identification of the alpha6 integrin as a candidate receptor for papillomaviruses. J Virol 1997, 71: 2449-2456.PubMed CentralPubMedGoogle Scholar
- Gavrilovskaya IN, Brown EJ, Ginsberg MH, Mackow ER: Cellular entry of hantaviruses which cause hemorrhagic fever with renal syndrome is mediated by beta3 integrins. J Virol 1999, 73: 3951-3959.PubMed CentralPubMedGoogle Scholar
- Bergelson JM, Chan BM, Finberg RW, Hemler ME: The integrin VLA-2 binds echovirus 1 and extracellular matrix ligands by different mechanisms. J Clin Invest 1993, 92: 232-239.PubMed CentralView ArticlePubMedGoogle Scholar
- Bergelson JM, Shepley MP, Chan BM, Hemler ME, Finberg RW: Identification of the integrin VLA-2 as a receptor for echovirus 1. Science 1992, 255: 1718-1720.View ArticlePubMedGoogle Scholar
- Weigel-Kelley KA, Yoder MC, Srivastava A: Alpha5beta1 integrin as a cellular coreceptor for human parvovirus B19: requirement of functional activation of beta1 integrin for viral entry. Blood 2003, 102: 3927-3933. 10.1182/blood-2003-05-1522View ArticlePubMedGoogle Scholar
- Graham KL, Zeng W, Takada Y, Jackson DC, Coulson BS: Effects on rotavirus cell binding and infection of monomeric and polymeric peptides containing alpha2beta1 and alphaxbeta2 integrin ligand sequences. J Virol 2004, 78: 11786-11797. 10.1128/JVI.78.21.11786-11797.2004PubMed CentralView ArticlePubMedGoogle Scholar
- Chu JJ, Ng ML: Interaction of West Nile virus with alpha v beta 3 integrin mediates virus entry into cells. J Biol Chem 2004, 279: 54533-54541. 10.1074/jbc.M410208200View ArticlePubMedGoogle Scholar
- Chiu CY, Mathias P, Nemerow GR, Stewart PL: Structure of adenovirus complexed with its internalization receptor, alphavbeta5 integrin. J Virol 1999, 73: 6759-6768.PubMed CentralPubMedGoogle Scholar
- Kessels MM, Engqvist-Goldstein AE, Drubin DG, Qualmann B: Mammalian Abp1, a signal-responsive F-actin-binding protein, links the actin cytoskeleton to endocytosis via the GTPase dynamin. J Cell Biol 2001, 153: 351-366. 10.1083/jcb.153.2.351PubMed CentralView ArticlePubMedGoogle Scholar
- Kay-Jackson PC, Goatley LC, Cox L, Miskin JE, Parkhouse RM, Wienands J, Dixon LK: The CD2v protein of African swine fever virus interacts with the actin-binding adaptor protein SH3P7. J Gen Virol 2004, 85: 119-130. 10.1099/vir.0.19435-0View ArticlePubMedGoogle Scholar
- Moir RD, Yoon M, Khuon S, Goldman RD: Nuclear lamins A and B1: different pathways of assembly during nuclear envelope formation in living cells. J Cell Biol 2000, 151: 1155-1168. 10.1083/jcb.151.6.1155PubMed CentralView ArticlePubMedGoogle Scholar
- Goldman RD, Gruenbaum Y, Moir RD, Shumaker DK, Spann TP: Nuclear lamins: building blocks of nuclear architecture. Genes Dev 2002, 16: 533-547. 10.1101/gad.960502View ArticlePubMedGoogle Scholar
- Kondo H, Rabouille C, Newman R, Levine TP, Pappin D, Freemont P, Warren G: p47 is a cofactor for p97-mediated membrane fusion. Nature 1997, 388: 75-78. 10.1038/40411View ArticlePubMedGoogle Scholar
- Cardosa MJ, Wang SM, Sum MS, Tio PH: Antibodies against prM protein distinguish between previous infection with dengue and Japanese encephalitis viruses. BMC Microbiol 2002, 2: 9. 10.1186/1471-2180-2-9PubMed CentralView ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.