Limited transferrin receptor clustering allows rapid diffusion of canine parvovirus into clathrin endocytic structures

Journal of Virology

Volumn 86, Issue 9, 2012, Pages 5330-5340

  Cureton, David K ^a   Harbison, Carole E ^b,c   Cocucci, Emanuele ^a   Parrish, Colin R ^b   Kirchhausen, Tom ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; CLATHRIN; TRANSFERRIN RECEPTOR;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CAT; CELL STRUCTURE; CELL SURFACE; CLUSTER ANALYSIS; DIFFUSION; ENDOCYTOSIS; FELINE PANLEUKOPENIA VIRUS; FLUORESCENCE MICROSCOPY; HALF LIFE TIME; INTERNALIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RECEPTOR BINDING; VIRUS CAPSID;

ANIMALS; CAPSID; CATS; CELL LINE; CELL MEMBRANE; CLATHRIN; COATED PITS, CELL-MEMBRANE; DIFFUSION; DOGS; ENDOCYTOSIS; KINETICS; PARVOVIRUS, CANINE; PROTEIN BINDING; RECEPTORS, TRANSFERRIN; RECEPTORS, VIRUS; VIRUS ASSEMBLY; VIRUS INTERNALIZATION;

CANINE PARVOVIRUS; FELIDAE; MIRIDAE;

EID: 84861307148     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.07194-11     Document Type: Article

References (51)

1. Agbandje M, McKenna R, Rossmann MG, Strassheim ML, Parrish CR. 1993. Structure determination of feline panleukopenia virus empty particles. Proteins 16:155-171.
2. Bocking T, Aguet F, Harrison SC, Kirchhausen T. 2011. Single-molecule analysis of a molecular disassemblase reveals the mechanism of Hsc70- driven clathrin uncoating. Nat. Struct. Mol. Biol. 18:295-301.
3. Booth AG, Wilson MJ. 1981. Human placental coated vesicles contain receptor-bound transferrin. Biochem. J. 196:355-362.
4. Cheng Y, Zak O, Aisen P, Harrison SC, Walz T. 2004. Structure of the human transferrin receptor-transferrin complex. Cell 116:565-576.
5. Collawn JF, et al. 1993. YTRF is the conserved internalization signal of the transferrin receptor, and a second YTRF signal at position 31-34 enhances endocytosis. J. Biol. Chem. 268:21686-21692.
6. Conner SD, Schmid SL. 2003. Regulated portals of entry into the cell. Nature 422:37-44.
7. Crandell RA, Fabricant CG, Nelson-Rees WA. 1973. Development, characterization, and viral susceptibility of a feline (Felis catus) renal cell line (CRFK). In Vitro 9:176-185.
8. Cureton DK, Massol RH, Saffarian S, Kirchhausen TL, Whelan SP. 2009. Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog. 5:e1000394.
9. Cureton DK, Massol RH, Whelan SP, Kirchhausen T. 2010. The length of vesicular stomatitis virus particles dictates a need for actin assembly during clathrin-dependent endocytosis. PLoS Pathog. 6:e1001127.
10. Ehrlich M, et al. 2004. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118:591-605.
11. Gell C, Berndt M, Enderlein J, Diez S. 2009. TIRF microscopy evanescent field calibration using tilted fluorescent microtubules. J. Microsc. 234:38-46.
12. Goodman LB, et al. 2010. Binding site on the transferrin receptor for the parvovirus capsid and effects of altered affinity on cell uptake and infection. J. Virol. 84:4969-4978.
13. Green NM. 1975. Avidin. Adv. Protein Chem. 29:85-133.
14. Hafenstein S, et al. 2007. Asymmetric binding of transferrin receptor to parvovirus capsids. Proc. Natl. Acad. Sci. U. S. A. 104:6585-6589.
15. Harbison CE, Chiorini JA, Parrish CR. 2008. The parvovirus capsid odyssey: from the cell surface to the nucleus. Trends Microbiol. 16:208-214.
16. Harbison CE, Lyi SM, Weichert WS, Parrish CR. 2009. Early steps in cell infection by parvoviruses: host-specific differences in cell receptor binding but similar endosomal trafficking. J. Virol. 83:10504-10514.
17. Harding C, Heuser J, Stahl P. 1983. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J. Cell Biol. 97:329-339.
18. Hueffer K, Govindasamy L, Agbandje-McKenna M, Parrish CR. 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.
19. Hueffer K, et al. 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.
20. Kerssemakers JW, et al. 2006. Assembly dynamics of microtubules at molecular resolution. Nature 442:709-712.
21. Kirchhausen T. 2009. Imaging endocytic clathrin structures in living cells. Trends Cell Biol. 19:596-605.
22. Kukura P, et al. 2009. High-speed nanoscopic tracking of the position and orientation of a single virus. Nat. Methods 6:923-927.
23. Lawrence CM, et al. 1999. Crystal structure of the ectodomain of human transferrin receptor. Science 286:779-782.
24. Lebron JA, West AP, Jr, Bjorkman PJ. 1999. The hemochromatosis protein HFE competes with transferrin for binding to the transferrin receptor. J. Mol. Biol. 294:239-245.
25. Liu AP, Aguet F, Danuser G, Schmid SL. 2010. Local clustering of transferrin receptors promotes clathrin-coated pit initiation. J. Cell Biol. 191:1381-1393.
26. Loerke D, et al. 2009. Cargo and dynamin regulate clathrin-coated pit maturation. PLoS Biol. 7:e57.
27. Lozach PY, et al. 2011. DC-SIGN as a receptor for phleboviruses. Cell Host Microbe 10:75-88.
28. Massol RH, Boll W, Griffin AM, Kirchhausen T. 2006. A burst of auxilin recruitment determines the onset of clathrin-coated vesicle uncoating. Proc. Natl. Acad. Sci. U. S. A. 103:10265-10270.
29. McGraw TE, Greenfield L, Maxfield FR. 1987. Functional expression of the human transferrin receptor cDNA in Chinese hamster ovary cells deficient in endogenous transferrin receptor. J. Cell Biol. 105:207-214.
30. Mercer J, Schelhaas M, Helenius A. 2010. Virus entry by endocytosis. Annu. Rev. Biochem. 79:803-833.
31. Palermo LM, Hafenstein SL, Parrish CR. 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.
32. Palermo LM, Hueffer K, Parrish CR. 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.
33. Parker JS, Murphy WJ, Wang D, O'Brien SJ, Parrish CR. 2001. Canine and feline parvoviruses can use human or feline transferrin receptors to bind, enter, and infect cells. J. Virol. 75:3896-3902.
34. Parker JS, Parrish CR. 2000. Cellular uptake and infection by canine parvovirus involves rapid dynamin-regulated clathrin-mediated endocytosis, followed by slower intracellular trafficking. J. Virol. 74:1919-1930.
35. Parrish CR. 1991. Mapping specific functions in the capsid structure of canine parvovirus and feline panleukopenia virus using infectious plasmid clones. Virology 183:195-205.
36. Parrish CR, Kawaoka Y. 2005. The origins of new pandemic viruses: the acquisition of new host ranges by canine parvovirus and influenza A viruses. Annu. Rev. Microbiol. 59:553-586.
37. Qian H, Sheetz MP, Elson EL. 1991. Single particle tracking. Analysis of diffusion and flow in two-dimensional systems. Biophys. J. 60:910-921.
38. Radoshitzky SR, et al. 2007. Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses. Nature 446:92-96.
39. Ross SR, Schofield JJ, Farr CJ, Bucan M. 2002. Mouse transferrin receptor 1 is the cell entry receptor for mouse mammary tumor virus. Proc. Natl. Acad. Sci. U. S. A. 99:12386-12390.
40. Rust MJ, Lakadamyali M, Zhang F, Zhuang X. 2004. Assembly of endocytic machinery around individual influenza viruses during viral entry. Nat. Struct. Mol. Biol. 11:567-573.
41. Saffarian S, Cocucci E, Kirchhausen T. 2009. Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol. 7:e1000191.
42. Sako Y, Kusumi A. 1995. Barriers for lateral diffusion of transferrin receptor in the plasma membrane as characterized by receptor dragging by laser tweezers: fence versus tether. J. Cell Biol. 129:1559-1574.
43. Sako Y, Kusumi A. 1994. Compartmentalized structure of the plasma membrane for receptor movements as revealed by a nanometer-level motion analysis. J. Cell Biol. 125:1251-1264.
44. Taylor MJ, Perrais D, Merrifield CJ. 2011. A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol. 9:e1000604.
45. Traub LM. 2009. Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat. Rev. Mol. Cell Biol. 10:583-596.
46. Trowbridge IS, Omary MB. 1981. Human cell surface glycoprotein related to cell proliferation is the receptor for transferrin. Proc. Natl. Acad. Sci. U. S. A. 78:3039-3043.
47. Tsao J, et al. 1991. The three-dimensional structure of canine parvovirus and its functional implications. Science 251:1456-1464.
48. van der Schaar HM, et al. 2008. Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog. 4:e1000244.
49. Ward JH, Kushner JP, Kaplan J. 1982. Transferrin receptors of human fibroblasts. Analysis of receptor properties and regulation. Biochem. J. 208:19-26.
50. Wu H, Rossmann MG. 1993. The canine parvovirus empty capsid structure. J. Mol. Biol. 233:231-244.
51. Yeung DE, et al. 1991. Monoclonal antibodies to the major nonstructural nuclear protein of minute virus of mice. Virology 181:35-45.