Block to the production of full-length B19 virus transcripts by internal polyadenylation is overcome by replication of the viral genome

Journal of Virology

Volumn 82, Issue 20, 2008, Pages 9951-9963

  Guan, Wuxiang ^a   Cheng, Fang ^a   Yoto, Yuko ^b,f   Kleiboeker, Steve ^c   Wong, Susan ^d   Zhi, Ning ^d   Pintel, David J ^b   Qiu, Jianming ^a,e  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b University of Missouri   (United States)

^c ViraCor Laboratories   (United States)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^e UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^f SAPPORO MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; GENOMIC RNA; VIRUS PROTEIN; VIRUS RNA; RNA PRECURSOR;

ARTICLE; CLONE; GENE REPLICATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INTRON; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PARVOVIRUS; PARVOVIRUS INFECTION; POLYADENYLATION; PRIORITY JOURNAL; RNA SPLICING; VIRUS CAPSID; VIRUS GENOME; VIRUS REPLICATION; VIRUS TRANSCRIPTION; ANIMAL; CELL LINE; DNA REPLICATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PLANT GROWTH;

MIRIDAE; PARVOVIRUS;

ANIMALS; CELL LINE; DNA REPLICATION; GENOME, VIRAL; HUMANS; PARVOVIRUS B19, HUMAN; POLYADENYLATION; RNA PRECURSORS; RNA SPLICING; RNA, VIRAL; TRANSCRIPTION, GENETIC; TROPISM; VIRUS REPLICATION;

EID: 53749095629     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01162-08     Document Type: Article

References (49)

1. Beard, C., J. St. Amand, and C. R. Astell. 1989. Transient expression of B19 parvovirus gene products in COS-7 cells transfected with B19-SV40 hybrid vectors. Virology 172:659-664.
2. Beyer, A. L., and Y. N. Osheim. 1988. Splice site selection, rate of splicing, and alternative splicing on nascent transcripts. Genes Dev. 2:754-765.
3. Bonvicini, F., C. Filippone, S. Delbarba, E. Manaresi, M. Zerbini, M. Musiani, and G. Gallinella. 2006. Parvovirus B19 genome as a single, twostate replicative and transcriptional unit. Virology 347:447-454.
4. Brown, K. E. 2005. The genus Erythrovirus, p. 25-45. In J. Kerr, M. M. Fan, M. E. Bloom, R. M. Linden, and C. R. Parrish (ed.), Parvoviruses. Hodder Arnold, London, United Kingdom.
5. Brown, K. E., S. M. Anderson, and N. S. Young. 1993. Erythrocyte P antigen: cellular receptor for B19 parvovirus. Science 262:114-117.
6. Brown, K. E., and N. Young. 1997. Human parvovirus B19: pathogenesis of disease, p. 105-119. In L. J. Anderson and N. Young (ed.), Human parvovirus B19, vol. 20. Karger, Basel, Switzerland.
7. Calvo, O., and J. L. Manley. 2003. Strange bedfellows: polyadenylation factors at the promoter. Genes Dev. 17:1321-1327.
8. Cotmore, S. F., and P. Tattersall. 1984. Characterization and molecular cloning of a human parvovirus genome. Science 226:1161-1165.
9. Cotmore, S. F., and P. Tattersall. 2006. A rolling-hairpin strategy: basic mechanisms of DNA replication in the parvoviruses, p. 171-181. In J. Kerr, S. F. Cotmore, M. E. Bloom, R. M. Linden, and C. R. Parrish (ed.), Parvoviruses. Hoddler Arond, London, United Kingdom.
10. Fong, N., and D. L. Bentley. 2001. Capping, splicing, and 3′ processing are independently stimulated by RNA polymerase II: different functions for different segments of the CTD. Genes Dev. 15:1783-1795.
11. Freyssinier, J. M., C. Lecoq-Lafon, S. Amsellem, F. Picard, R. Ducrocq, P. Mayeux, C. Lacombe, and S. Fichelson. 1999. Purification, amplification and characterization of a population of human erythroid progenitors. Br. J. Haematol. 106:912-922.
12. Gallinella, G., E. Manaresi, E. Zuffi, S. Venturoli, L. Bonsi, G. P. Bagnara, M. Musiani, and M. Zerbini. 2000. Different patterns of restriction to B19 parvovirus replication in human blast cell lines. Virology 278:361-367.
13. Giarratana, M. C., L. Kobari, H. Lapillonne, D. Chalmers, L. Kiger, T. Cynober, M. C. Marden, H. Wajcman, and L. Douay. 2005. Ex vivo generation of fully mature human red blood cells from hematopoietic stem cells. Nat. Biotechnol. 23:69-74.
14. Hirt, B. 1967. Selective extraction of polyoma DNA from infected mouse cell cultures. J. Mol. Biol. 26:365-369.
15. Ishov, A. M., and G. G. Maul. 1996. The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition. J. Cell Biol. 134:815-826.
16. Jul-Larsen, A., T. Visted, B. O. Karlsen, C. H. Rinaldo, R. Bjerkvig, P. E. Lonning, and S. O. Boe. 2004. PML-nuclear bodies accumulate DNA in response to polyomavirus BK and simian virus 40 replication. Exp. Cell Res. 298:58-73.
17. Liu, J. M., S. W. Green, T. Shimada, and N. S. Young. 1992. A block in full-length transcript maturation in cells nonpermissive for B19 parvovirus. J. Virol. 66:4686-4692.
18. Miyagawa, E., T. Yoshida, H. Takahashi, K. Yamaguchi, T. Nagano, Y. Kiriyama, K. Okochi, and H. Sato. 1999. Infection of the erythroid cell line, KU812Ep6 with human parvovirus B19 and its application to titration of B19 infectivity. J. Virol. Methods 83:45-54.
19. Moffatt, S., N. Yaegashi, K. Tada, N. Tanaka, and K. Sugamura. 1998. Human parvovirus B19 nonstructural (NS1) protein induces apoptosis in erythroid lineage cells. J. Virol. 72:3018-3028.
20. Morita, E., K. Tada, H. Chisaka, H. Asao, H. Sato, N. Yaegashi, and K. Sugamura. 2001. Human parvovirus B19 induces cell cycle arrest at G(2) phase with accumulation of mitotic cyclins. J. Virol. 75:7555-7563.
21. Mouw, M. B., and D. J. Pintel. 2000. Adeno-associated virus RNAs appear in a temporal order and their splicing is stimulated during coinfection with adenovirus. J. Virol. 74:9878-9888.
22. Munakata, Y., T. Saito-Ito, K. Kumura-Ishii, J. Huang, T. Kodera, T. Ishii, Y. Hirabayashi, Y. Koyanagi, and T. Sasaki. 2005. Ku80 autoantigen as a cellular coreceptor for human parvovirus B19 infection. Blood 106:3449-3456.
23. Naeger, L. K., R. V. Schoborg, Q. Zhao, G. E. Tullis, and D. J. Pintel. 1992. Nonsense mutations inhibit splicing of MVM RNA in cis when they interrupt the reading frame of either exon of the final spliced product. Genes Dev. 6:1107-1119.
24. Ozawa, K., J. Ayub, Y. S. Hao, G. Kurtzman, T. Shimada, and N. Young. 1987. Novel transcription map for the B19 (human) pathogenic parvovirus. J. Virol. 61:2395-2406.
25. Ozawa, K., J. Ayub, S. Kajigaya, T. Shimada, and N. Young. 1988. The gene encoding the nonstructural protein of B19 (human) parvovirus may be lethal in transfected cells. J. Virol. 62:2884-2889.
26. Ozawa, K., G. Kurtzman, and N. Young. 1986. Replication of the B19 parvovirus in human bone marrow cell cultures. Science 233:883-886.
27. Pombo, A., J. Ferreira, E. Bridge, and M. Carmo-Fonseca. 1994. Adenovirus replication and transcription sites are spatially separated in the nucleus of infected cells. EMBO J. 13:5075-5085.
28. Qiu, J., F. Cheng, L. R. Burger, and D. Pintel. 2006. The transcription profile of Aleutian mink disease virus in CRFK cells is generated by alternative processing of pre-mRNAs produced from a single promoter. J. Virol. 80:654-662.
29. Qiu, J., F. Cheng, and D. Pintel. 2006. Molecular characterization of caprine adeno-associated virus (AAV-Go. 1) reveals striking similarity to human AAV5. Virology 356:208-216.
30. Qiu, J., F. Cheng, and D. Pintel. 2007. Distance-dependent processing of adeno-associated virus type 5 RNA is controlled by 5′ exon definition. J. Virol. 81:7974-7984.
31. Qiu, J., R. Nayak, and D. J. Pintel. 2004. Alternative polyadenylation of adeno-associated virus type 5 RNA within an internal intron is governed by both a downstream element within the intron 3′ splice acceptor and an element upstream of the P41 initiation site. J. Virol. 78:83-93.
32. Qiu, J., R. Nayak, G. E. Tullis, and D. J. Pintel. 2002. Characterization of the transcription profile of adeno-associated virus type 5 reveals a number of unique features compared to previously characterized adeno-associated viruses. J. Virol. 76:12435-12447.
33. Qiu, J., and D. J. Pintel. 2002. The adeno-associated virus type 2 Rep protein regulates RNA processing via interaction with the transcription template. Mol. Cell. Biol. 22:3639-3652.
34. Qiu, J., and D. J. Pintel. 2004. Alternative polyadenylation of adeno-associated virus type 5 RNA within an internal intron is governed by the distance between the promoter and the intron and is inhibited by U1 small nuclear RNP binding to the intervening donor. J. Biol. Chem. 279:14889-14898.
35. Schoborg, R. V., and D. J. Pintel. 1991. Accumulation of MVM gene products is differentially regulated by transcription initiation, RNA processing and protein stability. Virology 181:22-34.
36. Srivastava, A., E. Bruno, R. Briddell, R. Cooper, C. Srivastava, K. van Besien, and R. Hoffman. 1990. Parvovirus B19-induced perturbation of human megakaryocytopoiesis in vitro. Blood 76:1997-2004.
37. Srivastava, A., and L. Lu. 1988. Replication of B19 parvovirus in highly enriched hematopoietic progenitor cells from normal human bone marrow. J. Virol. 62:3059-3063.
38. St. Amand, J., and C. R. Astell. 1993. Identification and characterization of a family of 11-kDa proteins encoded by the human parvovirus B19. Virology 192:121-131.
39. Takahashi, T., K. Ozawa, K. Takahashi, S. Asano, and F. Takaku. 1990. Susceptibility of human erythropoietic cells to B19 parvovirus in vitro increases with differentiation. Blood 75:603-610.
40. Tang, Q., P. Bell, P. Tegtmeyer, and G. G. Maul. 2000. Replication but not transcription of simian virus 40 DNA is dependent on nuclear domain 10. J. Virol. 74:9694-9700.
41. Tattersall, P. 2006. The evolution of parvovirus taxonomy, p. 5-14. In J. Kerr, S. F. Cotmore, M. E. Bloom, R. M. Linden, and C. R. Parrish (ed.), Parvoviruses. Hodder Arond, London, United Kingdom.
42. Weigel-Kelley, K. A., M. C. Yoder, and A. Srivastava. 2003. Alpha5beta1 integrin as a cellular coreceptor for human parvovirus B19: requirement of functional activation of beta1 integrin for viral entry. Blood 102:3927-3933.
43. Weitzman, M. D., K. J. Fisher, and J. M. Wilson. 1996. Recruitment of wild-type and recombinant adeno-associated virus into adenovirus replication centers. J. Virol. 70:1845-1854.
44. + erythroid progenitors are highly permissive to human parvovirus B19 replication. J. Virol. 82:2470-2476.
45. Word, P. 2006. Replication of adeno-associated virus DNA, p. 189-212. In J. Kerr, S. F. Cotmore, M. E. Bloom, R. M. Linden, and C. R. Parrish (ed.), Parvoviruses. Hoddler Arond, London, United Kingdom.
46. Yoto, Y., J. Qiu, and D. J. Pintel. 2006. Identification and characterization of two internal cleavage and polyadenylation sites of parvovirus B19 RNA. J. Virol. 80:1604-1609.
47. Young, P. J., K. T. Jensen, L. R. Burger, D. J. Pintel, and C. L. Lorson. 2002. Minute virus of mice NS1 interacts with the SMN protein, and they colocalize in novel nuclear bodies induced by parvovirus infection. J. Virol. 76:3892-3904.
48. Zhi, N., I. P. Mills, J. Lu, S. Wong, C. Filippone, and K. E. Brown. 2006. Molecular and functional analyses of a human parvovirus B19 infectious clone demonstrate essential roles for NS1, VP1, and the 11-kilodalton protein in virus replication and infectivity. J. Virol. 80:5941-5950.
49. Zhi, N., Z. Zadori, K. E. Brown, and P. Tijssen. 2004. Construction and sequencing of an infectious clone of the human parvovirus B19. Virology 318:142-152.