This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Parker, J. S. L.
Right arrow Articles by Parrish, C. R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Parker, J. S. L.
Right arrow Articles by Parrish, C. R.

 Previous Article  |  Next Article 

Journal of Virology, April 2001, p. 3896-3902, Vol. 75, No. 8
0022-538X/01/$04.00+0   DOI: 10.1128/JVI.75.8.3896-3902.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Canine and Feline Parvoviruses Can Use Human or Feline Transferrin Receptors To Bind, Enter, and Infect Cells

John S. L. Parker,1,dagger William J. Murphy,2 Dai Wang,1,Dagger Stephen J. O'Brien,2 and Colin R. Parrish1,*

James A. Baker Institute, College of Veterinary Medicine, Cornell University, Ithaca, New York 14853,1 and Laboratory of Genomic Diversity, National Cancer Institute, Frederick, Maryland 217022

Received 8 November 2000/Accepted 22 January 2001

Canine parvovirus (CPV) enters and infects cells by a dynamin-dependent, clathrin-mediated endocytic pathway, and viral capsids colocalize with transferrin in perinuclear vesicles of cells shortly after entry (J. S. L. Parker and C. R. Parrish, J. Virol. 74:1919-1930, 2000). Here we report that CPV and feline panleukopenia virus (FPV), a closely related parvovirus, bind to the human and feline transferrin receptors (TfRs) and use these receptors to enter and infect cells. Capsids did not detectably bind or enter quail QT35 cells or a Chinese hamster ovary (CHO) cell-derived cell line that lacks any TfR (TRVb cells). However, capsids bound and were endocytosed into QT35 cells and CHO-derived TRVb-1 cells that expressed the human TfR. TRVb-1 cells or TRVb cells transiently expressing the feline TfR were susceptible to infection by CPV and FPV, but the parental TRVb cells were not. We screened a panel of feline-mouse hybrid cells for susceptibility to FPV infection and found that only those cells that possessed feline chromosome C2 were susceptible. The feline TfR gene (TRFC) also mapped to feline chromosome C2. These data indicate that cell susceptibility for these viruses is determined by the TfR.


* Corresponding author. Mailing address: James A. Baker Institute, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853. Phone: (607) 256-5649. Fax: (607) 256-5608. E-mail: crp3{at}cornell.edu.

dagger Present address: Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, MA 02115.

Dagger Present address: Department of Molecular Biology, Princeton University, Princeton, NJ 08544.


Journal of Virology, April 2001, p. 3896-3902, Vol. 75, No. 8
0022-538X/01/$04.00+0   DOI: 10.1128/JVI.75.8.3896-3902.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Nelson, C. D. S., Minkkinen, E., Bergkvist, M., Hoelzer, K., Fisher, M., Bothner, B., Parrish, C. R. (2008). Detecting Small Changes and Additional Peptides in the Canine Parvovirus Capsid Structure. J. Virol. 82: 10397-10407 [Abstract] [Full Text]  
  • Cavalli, A., Martella, V., Desario, C., Camero, M., Bellacicco, A. L., De Palo, P., Decaro, N., Elia, G., Buonavoglia, C. (2008). Evaluation of the Antigenic Relationships among Canine Parvovirus Type 2 Variants. CVI 15: 534-539 [Abstract] [Full Text]  
  • Flanagan, M. L., Oldenburg, J., Reignier, T., Holt, N., Hamilton, G. A., Martin, V. K., Cannon, P. M. (2008). New World Clade B Arenaviruses Can Use Transferrin Receptor 1 (TfR1)-Dependent and -Independent Entry Pathways, and Glycoproteins from Human Pathogenic Strains Are Associated with the Use of TfR1. J. Virol. 82: 938-948 [Abstract] [Full Text]  
  • Palermo, L. M., Hafenstein, S. L., Parrish, C. R. (2006). Purified feline and canine transferrin receptors reveal complex interactions with the capsids of canine and feline parvoviruses that correspond to their host ranges.. J. Virol. 80: 8482-8492 [Abstract] [Full Text]  
  • Farr, G. A., Cotmore, S. F., Tattersall, P. (2006). VP2 Cleavage and the Leucine Ring at the Base of the Fivefold Cylinder Control pH-Dependent Externalization of both the VP1 N Terminus and the Genome of Minute Virus of Mice. J. Virol. 80: 161-171 [Abstract] [Full Text]  
  • Martella, V., Cavalli, A., Decaro, N., Elia, G., Desario, C., Campolo, M., Bozzo, G., Tarsitano, E., Buonavoglia, C. (2005). Immunogenicity of an Intranasally Administered Modified Live Canine Parvovirus Type 2b Vaccine in Pups with Maternally Derived Antibodies. CVI 12: 1243-1245 [Abstract] [Full Text]  
  • Rubio, M.-P., Lopez-Bueno, A., Almendral, J. M. (2005). Virulent Variants Emerging in Mice Infected with the Apathogenic Prototype Strain of the Parvovirus Minute Virus of Mice Exhibit a Capsid with Low Avidity for a Primary Receptor. J. Virol. 79: 11280-11290 [Abstract] [Full Text]  
  • Padron, E., Bowman, V., Kaludov, N., Govindasamy, L., Levy, H., Nick, P., McKenna, R., Muzyczka, N., Chiorini, J. A., Baker, T. S., Agbandje-McKenna, M. (2005). Structure of Adeno-Associated Virus Type 4. J. Virol. 79: 5047-5058 [Abstract] [Full Text]  
  • Vihinen-Ranta, M., Suikkanen, S., Parrish, C. R. (2004). Pathways of Cell Infection by Parvoviruses and Adeno-Associated Viruses. J. Virol. 78: 6709-6714 [Full Text]  
  • Hueffer, K., Palermo, L. M., Parrish, C. R. (2004). Parvovirus Infection of Cells by Using Variants of the Feline Transferrin Receptor Altering Clathrin-Mediated Endocytosis, Membrane Domain Localization, and Capsid-Binding Domains. J. Virol. 78: 5601-5611 [Abstract] [Full Text]  
  • Maxwell, I. H., Maxwell, F. (2004). Parvovirus LuIII transducing vectors packaged by LuIII versus FPV capsid proteins: the VP1 N-terminal region is not a major determinant of human cell permissiveness. J. Gen. Virol. 85: 1251-1257 [Abstract] [Full Text]  
  • Walters, R. W., Agbandje-McKenna, M., Bowman, V. D., Moninger, T. O., Olson, N. H., Seiler, M., Chiorini, J. A., Baker, T. S., Zabner, J. (2004). Structure of Adeno-Associated Virus Serotype 5. J. Virol. 78: 3361-3371 [Abstract] [Full Text]  
  • Imelli, N., Meier, O., Boucke, K., Hemmi, S., Greber, U. F. (2004). Cholesterol Is Required for Endocytosis and Endosomal Escape of Adenovirus Type 2. J. Virol. 78: 3089-3098 [Abstract] [Full Text]  
  • Govindasamy, L., Hueffer, K., Parrish, C. R., Agbandje-McKenna, M. (2003). Structures of Host Range-Controlling Regions of the Capsids of Canine and Feline Parvoviruses and Mutants. J. Virol. 77: 12211-12221 [Abstract] [Full Text]  
  • Suikkanen, S., Aaltonen, T., Nevalainen, M., Valilehto, O., Lindholm, L., Vuento, M., Vihinen-Ranta, M. (2003). Exploitation of Microtubule Cytoskeleton and Dynein during Parvoviral Traffic toward the Nucleus. J. Virol. 77: 10270-10279 [Abstract] [Full Text]  
  • Hueffer, K., Govindasamy, L., Agbandje-McKenna, M., Parrish, C. R. (2003). Combinations of Two Capsid Regions Controlling Canine Host Range Determine Canine Transferrin Receptor Binding by Canine and Feline Parvoviruses. J. Virol. 77: 10099-10105 [Abstract] [Full Text]  
  • Palermo, L. M., Hueffer, K., Parrish, C. R. (2003). Residues in the Apical Domain of the Feline and Canine Transferrin Receptors Control Host-Specific Binding and Cell Infection of Canine and Feline Parvoviruses. J. Virol. 77: 8915-8923 [Abstract] [Full Text]  
  • Lachmann, S., Rommeleare, J., Nuesch, J. P. F. (2003). Novel PKC{eta} Is Required To Activate Replicative Functions of the Major Nonstructural Protein NS1 of Minute Virus of Mice. J. Virol. 77: 8048-8060 [Abstract] [Full Text]  
  • Snyers, L., Zwickl, H., Blaas, D. (2003). Human Rhinovirus Type 2 Is Internalized by Clathrin-Mediated Endocytosis. J. Virol. 77: 5360-5369 [Abstract] [Full Text]  
  • Hueffer, K., Parker, J. S. L., Weichert, W. S., Geisel, R. E., Sgro, J.-Y., Parrish, C. R. (2003). The Natural Host Range Shift and Subsequent Evolution of Canine Parvovirus Resulted from Virus-Specific Binding to the Canine Transferrin Receptor. J. Virol. 77: 1718-1726 [Abstract] [Full Text]  
  • Ros, C., Burckhardt, C. J., Kempf, C. (2002). Cytoplasmic Trafficking of Minute Virus of Mice: Low-pH Requirement, Routing to Late Endosomes, and Proteasome Interaction. J. Virol. 76: 12634-12645 [Abstract] [Full Text]  
  • Ross, S. R., Schofield, J. J., Farr, C. J., Bucan, M. (2002). Mouse transferrin receptor 1 is the cell entry receptor for mouse mammary tumor virus. Proc. Natl. Acad. Sci. USA 99: 12386-12390 [Abstract] [Full Text]  
  • Suikkanen, S., Saajarvi, K., Hirsimaki, J., Valilehto, O., Reunanen, H., Vihinen-Ranta, M., Vuento, M. (2002). Role of Recycling Endosomes and Lysosomes in Dynein-Dependent Entry of Canine Parvovirus. J. Virol. 76: 4401-4411 [Abstract] [Full Text]  
  • Vihinen-Ranta, M., Wang, D., Weichert, W. S., Parrish, C. R. (2002). The VP1 N-Terminal Sequence of Canine Parvovirus Affects Nuclear Transport of Capsids and Efficient Cell Infection. J. Virol. 76: 1884-1891 [Abstract] [Full Text]  
  • Rubio, M.-P., Guerra, S., Almendral, J. M. (2001). Genome Replication and Postencapsidation Functions Mapping to the Nonstructural Gene Restrict the Host Range of a Murine Parvovirus in Human Cells. J. Virol. 75: 11573-11582 [Abstract] [Full Text]