Human parvovirus B19 infection causes cell cycle arrest of human erythroid progenitors at late S phase that favors viral DNA replication

Journal of Virology

Volumn 87, Issue 23, 2013, Pages 12766-12775

  Luo, Yong ^a   Kleiboeker, Steve ^b   Deng, Xuefeng ^a   Qiu, Jianming ^a  

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

^b Viracor IBT Laboratories   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; BROXURIDINE; CELL DNA; CELL NUCLEUS DNA; VIRUS DNA;

ARTICLE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL LABELING; CONTROLLED STUDY; DNA CONTENT; DNA DAMAGE; DNA DETERMINATION; DNA REPAIR; DNA REPLICATION; DNA SYNTHESIS; ERYTHROID PRECURSOR CELL; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HUMAN PARVOVIRUS B19; NONHUMAN; PRIORITY JOURNAL; S PHASE CELL CYCLE CHECKPOINT; STAINING; VIRUS CELL INTERACTION; VIRUS MUTANT; VIRUS REPLICATION; WILD TYPE;

CELL LINE; DNA REPLICATION; DNA, VIRAL; ERYTHEMA INFECTIOSUM; ERYTHROID PRECURSOR CELLS; HUMANS; PARVOVIRUS B19, HUMAN; S PHASE CELL CYCLE CHECKPOINTS; VIRUS REPLICATION;

EID: 84887157097     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02333-13     Document Type: Article

References (58)

1. Weir E. 2005. Parvovirus B19 infection:fifth disease and more. CMAJ 172:743.
2. Young NS, Brown KE. 2004. Parvovirus B19. N. Engl. J. Med. 350:586-597.
3. Lamont R, Sobel J, Vaisbuch E, Kusanovic J, Mazaki-Tovi S, Kim S, Uldbjerg N, Romero R. 2011. Parvovirus B19 infection in human pregnancy. BJOG 118:175-186.
4. Riipinen A, Vaisanen E, Nuutila M, Sallmen M, Karikoski R, Lindbohm ML, Hedman K, Taskinen H, Soderlund-Venermo M. 2008. Parvovirus B19 infection in fetal deaths. Clin. Infect. Dis. 47:1519-1525.
5. Anderson MJ, Khousam MN, Maxwell DJ, Gould SJ, Happerfield LC, Smith WJ. 1988. Human parvovirus B19 and hydrops fetalis. Lancet i:535.
6. Tavil B, Sanal O, Turul T, Yel L, Gurgey A, Gumruk F. 2009. Parvovirus B19-induced persistent pure red cell aplasia in a child with T-cell immunodeficiency. Pediatr. Hematol. Oncol. 26:63-68.
7. Mrzljak A, Kardum-Skelin I, Cvrlje VC, Kanizaj TF, Sustercic D, Gustin D, Kocman B. 2010. Parvovirus B 19 (PVB19) induced pure red cell aplasia (PRCA) in immunocompromised patient after liver transplantation. Coll. Antropol. 34:271-274.
8. Shade RO, Blundell MC, Cotmore SF, Tattersall P, Astell CR. 1986. Nucleotide sequence and genome organization of human parvovirus B19 isolated from the serum of a child during aplastic crisis. J. Virol. 58:921-936.
9. Duncan JR, Potter CB, Cappellini MD, Kurtz JB, Anderson MJ, Weatherall DJ. 1983. Aplastic crisis due to parvovirus infection in pyruvate kinase deficiency. Lancet ii:14-16.
10. Rechavi G, Vonsover A, Manor Y, Mileguir F, Shpilberg O, Kende G, Brok-Simoni F, Mandel M, Gotlieb-Stematski T, Ben-Bassat I. 1989. Aplastic crisis due to human B19 parvovirus infection in red cell pyrimidine-5'-nucleotidase deficiency. Acta Haematol. 82:46-49.
11. Cotmore SF, Tattersall P. 1984. Characterization and molecular cloning of a human parvovirus genome. Science 226:1161-1165.
12. Ozawa K, Ayub J, Hao YS, Kurtzman G, Shimada T, Young N. 1987. Novel transcription map for the B19 (human) pathogenic parvovirus. J. Virol. 61:2395-2406.
13. Ozawa K, Kurtzman G, Young N. 1986. Replication of the B19 parvovirus in human bone marrow cell cultures. Science 233:883-886.
14. Srivastava A, Lu L. 1988. Replication of B19 parvovirus in highly enriched hematopoietic progenitor cells from normal human bone marrow. J. Virol. 62:3059-3063.
15. Morey AL, Fleming KA. 1992. Immunophenotyping of fetal haemopoietic cells permissive for human parvovirus B19 replication in vitro. Br. J. Haematol. 82:302-309.
16. Morita E, Nakashima A, Asao H, Sato H, Sugamura K. 2003. Human parvovirus B19 nonstructural protein (NS1) induces cell cycle arrest at G(1) phase. J. Virol. 77:2915-2921.
17. Morita E, Tada K, Chisaka H, Asao H, Sato H, Yaegashi N, Sugamura K. 2001. Human parvovirus B19 induces cell cycle arrest at G(2) phase with accumulation of mitotic cyclins. J. Virol. 75:7555-7563.
18. Sol N, Le JJ, Vassias I, Freyssinier JM, Thomas A, Prigent AF, Rudkin BB, Fichelson S, Morinet F. 1999. Possible interactions between the NS-1 protein and tumor necrosis factor alpha pathways in erythroid cell apoptosis induced by human parvovirus B19. J. Virol. 73:8762-8770.
19. Wong S, Zhi N, Filippone C, Keyvanfar K, Kajigaya S, Brown KE, Young NS. 2008. Ex vivo-generated CD36+ erythroid progenitors are highly permissive to human parvovirus B19 replication. J. Virol. 82:2470-2476.
20. Chen AY, Guan W, Lou S, Liu Z, Kleiboeker S, Qiu J. 2010. Role of erythropoietin receptor signaling in parvovirus B19 replication in human erythroid progenitor cells. J. Virol. 84:12385-12396.
21. Guan W, Wong S, Zhi N, Qiu J. 2009. The genome of human parvovirus B19 virus can replicate in non-permissive cells with the help of adenovirus genes and produces infectious virus. J. Virol. 83:9541-9553.
22. Chen AY, Kleiboeker S, Qiu J. 2011. Productive parvovirus B19 infection of primary human erythroid progenitor cells at hypoxia is regulated by STAT5A andMEKsignaling but not HIF alpha. PLoS Pathog. 7:e1002088. doi:10.1371/journal.ppat.1002088.
23. Zhi N, Zadori Z, Brown KE, Tijssen P. 2004. Construction and sequencing of an infectious clone of the human parvovirus B19. Virology 318:142-152.
24. Wan Z, Zhi N, Wong S, Keyvanfar K, Liu D, Raghavachari N, Munson PJ, Su S, Malide D, Kajigaya S, Young NS. 2010. Human parvovirus B19 causes cell cycle arrest of human erythroid progenitors via deregulation of the E2F family of transcription factors. J. Clin. Invest. 120:3530-3544.
25. Lou S, Luo Y, Cheng F, Huang Q, Shen W, Kleiboeker S, Tisdale JF, Liu Z, Qiu J. 2012. Human parvovirus B19 DNA replication induces a DNA damage response that is dispensable for cell cycle arrest at G2/M phase. J. Virol. 86:10748-10758.
26. Oleksiewicz MB, Alexandersen S. 1997. S-phase-dependent cell cycle disturbances caused by Aleutian mink disease parvovirus. J. Virol. 71: 1386-1396.
27. Deleu L, Pujol A, Faisst S, Rommelaere J. 1999. Activation of promoter P4 of the autonomous parvovirus minute virus of mice at early S phase is required for productive infection. J. Virol. 73:3877-3885.
28. Wolter S, Richards R, Armentrout RW. 1980. Cell cycle-dependent replication of the DNA of minute virus of mice, a parvovirus. Biochim. Biophys. Acta 607:420-431.
29. Bashir T, Horlein R, Rommelaere J, Willwand K. 2000. Cyclin A activates the DNA polymerase delta-dependent elongation machinery in vitro:a parvovirus DNA replication model. Proc. Natl. Acad. Sci. U.S.A. 97:5522-5527.
30. Luo Y, Deng X, Cheng F, Li Y, Qiu J. 2013. SMC1-mediated intra-S phase arrest facilitates BocavirusDNAreplication. J. Virol. 87:4017-4032.
31. Cotmore SF, Tattersall P. 1987. The autonomously replicating parvoviruses of vertebrates. Adv. Virus Res. 33:91-174.
32. Cotmore SF, Tattersall P. 2005. A rolling-hairpin strategy:basic mechanisms of DNA replication in the parvoviruses, p 171-181. In Kerr J, Cotmore SF, Bloom ME, Linden RM, Parrish CR (ed), Parvoviruses. Hoddler Arond, London, United Kingdom.
33. Davy C, Doorbar J. 2007. G2/M cell cycle arrest in the life cycle of viruses. Virology 368:219-226.
34. Luo Y, Lou S, Deng X, Liu Z, Li Y, Kleiboeker S, Qiu J. 2011. Parvovirus B19 infection of human primary erythroid progenitor cells triggers ATRChk1 signaling, which promotes B19 virus replication. J. Virol. 85:8046-8055.
35. Guan W, Cheng F, Yoto Y, Kleiboeker S, Wong S, Zhi N, Pintel DJ, Qiu J. 2008. Block to the production of full-length B19 virus transcripts by internal polyadenylation is overcome by replication of the viral genome. J. Virol. 82:9951-9963.
36. Hirt B. 1967. Selective extraction of polyoma DNA from infected mouse cell cultures. J. Mol. Biol. 26:365-369.
37. Gratzner HG. 1982. Monoclonal antibody to 5-bromo-and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218: 474-475.
38. Lindqvist A, Rodriguez-Bravo V, Medema RH. 2009. The decision to enter mitosis:feedback and redundancy in the mitotic entry network. J. Cell Biol. 185:193-202.
39. Goto H, Tomono Y, Ajiro K, Kosako H, Fujita M, Sakurai M, Okawa K, Iwamatsu A, Okigaki T, Takahashi T, Inagaki M. 1999. Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J. Biol. Chem. 274:25543-25549.
40. Weitzman MD, Lilley CE, Chaurushiya MS. 2010. Genomes in conflict: maintaining genome integrity during virus infection. Annu. Rev. Microbiol. 64:61-81.
41. Olive PL. 2002. The comet assay. An overview of techniques. Methods Mol. Biol. 203:179-194.
42. Shaposhnikov SA, Salenko VB, Brunborg G, Nygren J, Collins AR. 2008. Single-cell gel electrophoresis (the comet assay):loops or fragments? Electrophoresis 29:3005-3012.
43. Bashir T, Rommelaere J, Cziepluch C. 2001. In vivo accumulation of cyclin A and cellular replication factors in autonomous parvovirus minute virus of mice-associated replication bodies. J. Virol. 75:4394-4398.
44. Christensen J, Tattersall P. 2002. Parvovirus initiator protein NS1 and RPA coordinate replication fork progression in a reconstituted DNA replication system. J. Virol. 76:6518-6531.
45. Nash K, Chen W, Muzyczka N. 2008. Complete in vitro reconstitution of adeno-associated virus DNA replication requires the minichromosome maintenance complex proteins. J. Virol. 82:1458-1464.
46. Pacek M, Walter JC. 2004. A requirement for MCM7 and Cdc45 in chromosome unwinding during eukaryotic DNA replication. EMBO J. 23:3667-3676.
47. Chen AY, Zhang EY, Guan W, Cheng F, Kleiboeker S, Yankee TM, Qiu J. 2010. The small 11kDa non-structural protein of human parvovirus B19 plays a key role in inducing apoptosis during B19 virus infection of primary erythroid progenitor cells. Blood 115:1070-1080.
48. Bartek J, Lukas C, Lukas J. 2004. Checking on DNA damage in S phase. Nat. Rev. Mol. Cell Biol. 5:792-804.
49. Hermanns J, Schulze A, Jansen D, Kleinschmidt JA, Schmidt R, zur Hausen H. 1997. Infection of primary cells by adeno-associated virus type 2 results in a modulation of cell cycle-regulating proteins. J. Virol. 71: 6020-6027.
50. Op De Beeck A, Sobczak-Thepot J, Sirma H, Bourgain F, Brechot C, Caillet-Fauquet P. 2001. NS1-and minute virus of mice-induced cell cycle arrest:involvement of p53 and p21(cip1). J. Virol. 75:11071-11078.
51. Luo Y, Qiu J. 2013. Parvovirus infection induced DNA damage response. Future Virol. 8:245-257.
52. Zhi N, Mills IP, Lu J, Wong S, Filippone C, Brown KE. 2006. Molecular and functional analyses of a human parvovirus B19 infectious clone demonstrates essential roles for NS1, VP1, and the 11-kilodalton protein in virus replication and infectivity. J. Virol. 80:5941-5950.
53. Gareus R, Gigler A, Hemauer A, Leruez-Ville M, Morinet F, Wolf H, Modrow S. 1998. Characterization of cis-acting and NS1 proteinresponsive elements in the p6 promoter of parvovirus B19. J. Virol. 72: 609-616.
54. Ozawa K, Ayub J, Kajigaya S, Shimada T, Young N. 1988. The gene encoding the nonstructural protein of B19 (human) parvovirus may be lethal in transfected cells. J. Virol. 62:2884-2889.
55. Moffatt S, Yaegashi N, Tada K, Tanaka N, Sugamura K. 1998. Human parvovirus B19 nonstructural (NS1) protein induces apoptosis in erythroid lineage cells. J. Virol. 72:3018-3028.
56. Chen AY, Qiu J. 2010. Parvovirus infection-induced cell detah and cell cycle arrest. Future Virol. 5:731-741.
57. Chen AY, Luo Y, Cheng F, Sun Y, Qiu J. 2010. Bocavirus infection induces a mitochondrion-mediated apoptosis and cell cycle arrest at G2/ M-phase. J. Virol. 84:5615-5626.
58. Berthet C, Raj K, Saudan P, Beard P. 2005. How adeno-associated virus Rep78 protein arrests cells completely in S phase. Proc. Natl. Acad. Sci. U.S.A. 102:13634-13639.