Impaired genome encapsidation restricts the in vitro propagation of human parvovirus B19

Journal of Virological Methods

Volumn 193, Issue 1, 2013, Pages 215-225

  Wolfisberg, Raphael ^a   Ruprecht, Nico ^a   Kempf, Christoph ^a,b   Ros, Carlos ^a,b  

^a UNIVERSITY OF BERN   (Switzerland)

^b CSL Behring AG   (Switzerland)

Author keywords

EPCs; Erythroid progenitor cells; Hypoxia; Parvovirus B19; UT7 Epo cells; VP1u

Indexed keywords

CD36 ANTIGEN; CHLOROQUINE; MESSENGER RNA; PROTEIN VP1; VIRUS DNA;

ARTICLE; CELL HYPOXIA; CONTROLLED STUDY; DNA PACKAGING; ERYTHROID PRECURSOR CELL; GENETIC TRANSFECTION; HEAT TREATMENT; HUMAN PARVOVIRUS B19; IN VITRO STUDY; NONHUMAN; PARVOVIRUS INFECTION; PRIORITY JOURNAL; VIRAL PHENOMENA AND FUNCTIONS; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS GENOME ENCAPSIDATION; VIRUS LOAD; VIRUS REPLICATION; WILD TYPE;

EPCS; ERYTHROID PROGENITOR CELLS; HYPOXIA; PARVOVIRUS B19; UT7/EPO CELLS; VP1U;

ANTIGENS, CD36; CELL LINE; ERYTHROID PRECURSOR CELLS; HUMANS; OXYGEN; PARVOVIRUS B19, HUMAN; VIRUS ASSEMBLY; VIRUS CULTIVATION; VIRUS REPLICATION;

MIRIDAE; PARVOVIRUS;

EID: 84879996549     PISSN: 01660934     EISSN: 18790984     Source Type: Journal    
DOI: 10.1016/j.jviromet.2013.06.003     Document Type: Article

References (51)

1. Bleker S., Pawlita M., Kleinschmidt J.A. Impact of capsid conformation and Rep-capsid interactions on adeno-associated virus type 2 genome packaging. J. Virol. 2006, 80:810-820.
2. Bleker S., Sonntag F., Kleinschmidt J.A. Mutational analysis of narrow pores at the fivefold symmetry axes of adeno-associated virus type 2 capsids reveals a dual role in genome packaging and activation of phospholipase A2 activity. J. Virol. 2005, 79:2528-2540.
3. Bönsch C., Zuercher C., Lieby P., Kempf C., Ros C. The globoside receptor triggers structural changes in the B19 virus capsid that facilitate virus internalization. J. Virol. 2010, 84:11737-11746.
4. Bönsch C., Kempf C., Mueller I., Manning L., Laman M., Davis T.M., Ros C. Chloroquine and its derivatives exacerbate B19V-associated anemia by promoting viral replication. PLoS Negl. Trop. Dis. 2010, 4(4):e669.
5. Bönsch C., Kempf C., Ros C. Interaction of parvovirus B19 with human erythrocytes alters virus structure and cell membrane integrity. J. Virol. 2008, 82:11784-11791.
6. Bonvicini F., Filippone C., Manaresi E., Zerbini M., Musiani M., Gallinella G. HepG2 hepatocellular carcinoma cells are a non-permissive system for B19 virus infection. J. Gen. Virol. 2008, 89:3034-3038.
7. Brown K.E., Anderson S.M., Young N.S. Erythrocyte P antigen: cellular receptor for B19 parvovirus. Science 1993, 262:114-117.
8. Brunstein J., Söderlund-Venermo M., Hedman K. Identification of a novel RNA splicing pattern as a basis of restricted cell tropism of erythrovirus B19. Virology 2000, 274:284-291.
9. Caillet-Fauquet P., Di Giambattista M., Draps M.L., Hougardy V., de Launoit Y., Laub R. An assay for parvovirus B19 neutralizing antibodies based on human hepatocarcinoma cell lines. Transfusion 2004, 44:1340-1343.
10. Caillet-Fauquet P., Draps M.L., Di Giambattista M., de Launoit Y., Laub R. Hypoxia enables B19 erythrovirus to yield abundant infectious progeny in a pluripotent erythroid cell line. J. Virol. Methods 2004, 121:145-153.
11. Chen A.Y., Kleiboeker S., Qiu J. Productive parvovirus B19 infection of primary human erythroid progenitor cells at hypoxia is regulated by STAT5A and MEK signaling but not HIFα. PLoS Pathog. 2011, 7(6):e1002088.
12. Chen A.Y., Guan W., Lou S., Liu Z., Kleiboeker S., Qiu J. Role of erythropoietin receptor signaling in parvovirus B19 replication in human erythroid progenitor cells. J. Virol. 2010, 84:12385-12396.
13. Cossart Y.E., Field A.M., Cant B., Widdows D. Parvovirus-like particles in human sera. Lancet 1975, 1:72-73.
14. Cotmore S.F., Tattersall P. Mutations at the base of the icosahedral five-fold cylinders of minute virus of mice induce 3'-to-5' genome uncoating and critically impair entry functions. J. Virol. 2012, 86:69-80.
15. Cotmore S.F., Tattersall P. Encapsidation of minute virus of mice DNA: aspects of the translocation mechanism revealed by the structure of partially packaged genomes. Virology 2005, 336:100-112.
16. Cotmore S.F., D'abramo A.M., Ticknor C.M., Tattersall P. Controlled conformational transitions in the MVM virion expose the VP1 N-terminus and viral genome without particle disassembly. Virology 1999, 254:169-181.
17. Farr G.A., Tattersall P. A conserved leucine that constricts the pore through the capsid fivefold cylinder plays a central role in parvoviral infection. Virology 2004, 323:243-256.
18. Filippone C., Franssila R., Kumar A., Saikko L., Kovanen P.E., Söderlund-Venermo M., Hedman K. Erythroid progenitor cells expanded from peripheral blood without mobilization or preselection: molecular characteristics and functional competence. PLoS One 2010, 5(3):e9496.
19. Gallinella G., Manaresi E., Zuffi E., Venturoli S., Bonsi L., Bagnara G.P., Musiani M., Zerbini M. Different patterns of restriction to B19 parvovirus replication in human blast cell lines. Virology 2000, 278:361-367.
20. Gigler A., Dorsch S., Hemauer A., Williams C., Kim S., Young N.S., Zolla-Pazner S., Wolf H., Gorny M.K., Modrow S. Generation of neutralizing human monoclonal antibodies against parvovirus B19 proteins. J. Virol. 1999, 73:1974-1979.
21. Guan W., Cheng F., Yoto Y., Kleiboeker S., Wong S., Zhi N., Pintel D.J., Qiu J. Block to the production of full-length B19 virus transcripts by internal polyadenylation is overcome by replication of the viral genome. J. Virol. 2008, 82:9951-9963.
22. Heegaard E.D., Brown K.E. Human parvovirus B19. Clin. Microbiol. Rev. 2002, 15:485-505.
23. Heegaard E.D., Hornsleth A. Parvovirus: the expanding spectrum of disease. Acta Paediatr. 1995, 84:109-117.
24. Hunter L.A., Samulski R.J. Colocalization of adeno-associated virus Rep and capsid proteins in the nuclei of infected cells. J. Virol. 1992, 66:317-324.
25. King J.A., Dubielzig R., Grimm D., Kleinschmidt J.A. DNA helicase-mediated packaging of adeno-associated virus type 2 genomes into preformed capsids. EMBO J. 2001, 20:3282-3291.
26. Kooistra K., Mesman H.J., de Waal M., Koppelman M.H., Zaaijer H.L. Epidemiology of high-level parvovirus B19 viraemia among Dutch blood donors, 2003-2009. Vox Sang. 2011, 100:261-266.
27. Kronenberg S., Bottcher B., von der Lieth C.W., Bleker S., Kleinschmidt J.A. A conformational change in the adeno-associated virus type 2 capsid leads to the exposure of hidden VP1N termini. J. Virol. 2005, 79:5296-5303.
28. Liu J.M., Green S.W., Shimada T., Young N.S. A block in full-length transcript maturation in cells nonpermissive for B19 parvovirus. J. Virol. 1992, 66:4686-4692.
29. Luo Y., Lou S., Deng X., Liu Z., Li Y., Kleiboeker S., Qiu J. Parvovirus B19 infection of human primary erythroid progenitor cells triggers ATR-Chk1 signaling, which promotes B19 virus replication. J. Virol. 2011, 85:8046-8055.
30. Mani B., Baltzer C., Valle N., Almendral J.M., Kempf C., Ros C. Low pH-dependent endosomal processing of the incoming parvovirus minute virus of mice virion leads to externalization of the VP1 N-terminal sequence (N-VP1), N-VP2 cleavage, and uncoating of the full-length genome. J. Virol. 2006, 80:1015-1024.
31. Miyagawa E., Yoshida T., Takahashi H., Yamaguchi K., Nagano T., Kiriyama Y., Okochi K., Sato H. Infection of the erythroid cell line, KU812Ep6 with human parvovirus B19 and its application to titration of B19 infectivity. J. Virol. Methods 1999, 83:45-54.
32. Moffatt S., Yaegashi N., Tada K., Tanaka N., Sugamura K. Human parvovirus B19 nonstructural (NS1) protein induces apoptosis in erythroid lineage cells. J. Virol. 1998, 72:3018-3028.
33. Mortimer P.P., Humphries R.K., Moore J.G., Purcell R.H., Young N.S. A human parvovirus-like virus inhibits haematopoietic colony formation in vitro. Nature 1983, 302:426-429.
34. Munakata Y., Saito-Ito T., Kumura-Ishii K., Huang J., Kodera T., Ishii T., Hirabayashi Y., Koyanagi Y., Sasaki T. Ku80 autoantigen as a cellular coreceptor for human parvovirus B19 infection. Blood 2005, 106:3449-3456.
35. Ozawa K., Kurtzman G., Young N. Productive infection by B19 parvovirus of human erythroid bone marrow cells in vitro. Blood 1987, 70:384-391.
36. Ozawa K., Kurtzman G., Young N. Replication of the B19 parvovirus in human bone marrow cell cultures. Science 1986, 233:883-886.
37. Pallier C., Greco A., Le Junter J., Saib A., Vassias I., Morinet F. The 3' untranslated region of the B19 parvovirus capsid protein mRNAs inhibits its own mRNA translation in nonpermissive cells. J. Virol. 1997, 71:9482-9489.
38. Pillet S., Fichelson S., Morinet F., Young N.S., Zhi N., Wong S. Human B19 erythrovirus in vitro replication: what's new?. J. Virol. 2008, 82:8951-8953.
39. Pillet S., Le Guyader N., Hofer T., NguyenKhac F., Koken M., Aubin J.T., Fichelson S., Gassmann M., Morinet F. Hypoxia enhances human B19 erythrovirus gene expression in primary erythroid cells. Virology 2004, 327:1-7.
40. Plevka P., Hafenstein S., Li L., D'Abrgamo A., Cotmore S.F., Rossmann M.G., Tattersall P. Structure of a packaging-defective mutant of minute virus of mice indicates that the genome is packaged via a pore at a 5-fold axis. J. Virol. 2011, 85:4822-4827.
41. Ros C., Gerber M., Kempf C. Conformational changes in the VP1-unique region of native human parvovirus B19 lead to exposure of internal sequences that play a role in virus neutralization and infectivity. J. Virol. 2006, 80:12017-12024.
42. Servey J.T., Reamy B.V., Hodge J. Clinical presentations of parvovirus B19 infection. Am. Fam. Physician 2007, 75:373-376.
43. Shimomura S., Komatsu N., Frickhofen N., Anderson S., Kajigaya S., Young N.S. First continuous propagation of B19 parvovirus in a cell line. Blood 1992, 79:18-24.
44. Takahashi T., Ozawa K., Takahashi K., Asano S., Takaku F. Susceptibility of human erythropoietic cells to B19 parvovirus in vitro increases with differentiation. Blood 1990, 75:603-610.
45. Timpe J., Bevington J., Casper J., Dignam J.D., Trempe J.P. Mechanisms of adeno-associated virus genome encapsidation. Curr. Gene Ther. 2005, 5:273-284.
46. Vihinen-Ranta M., Wang D., Weichert W.S., Parrish C.R. The VP1 N-terminal sequence of canine parvovirus affects nuclear transport of capsids and efficient cell infection. J. Virol. 2002, 76:1884-1891.
47. Weigel-Kelley K.A., Yoder M.C., 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.
48. Wistuba A., Kern A., Weger S., Grimm D., Kleinschmidt J.A. Subcellular compartmentalization of adeno-associated virus type 2 assembly. J. Virol. 1997, 71:1341-1352.
49. Wong S., Zhi N., Filippone C., Keyvanfar K., Kajigaya S., Brown K.E., Young N.S. Ex vivo-generated CD36+ erythroid progenitors are highly permissive to human parvovirus B19 replication. J. Virol. 2008, 82:2470-2476.
50. Wong S., Brown K.E. Development of an improved method of detection of infectious parvovirus B19. J. Clin. Virol. 2006, 35:407-413.
51. Zhi N., Zádori Z., Brown K.E., Tijssen P. Construction and sequencing of an infectious clone of the human parvovirus B19. Virology 2004, 318:142-152.