Role of erythropoietin receptor signaling in parvovirus B19 replication in human erythroid progenitor cells

Journal of Virology

Volumn 84, Issue 23, 2010, Pages 12385-12396

  Chen, Aaron Yun ^a   Guan, Wuxiang ^a   Lou, Sai ^a,b   Liu, Zhengwen ^b   Kleiboeker, Steve ^c   Qiu, Jianming ^a  

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

^b XI'AN JIAOTONG UNIVERSITY   (China)

^c ViraCor Laboratories   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR; JANUS KINASE 2; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; ERYTHEMA INFECTIOSUM; ERYTHROID PRECURSOR CELL; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; HUMAN PARVOVIRUS B19; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STEM CELL EXPANSION; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS GENOME; VIRUS REPLICATION;

ANTIGENS, CD36; BLOTTING, SOUTHERN; BLOTTING, WESTERN; ERYTHROID PRECURSOR CELLS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC VECTORS; HUMANS; JANUS KINASE 2; LENTIVIRUS; PARVOVIRIDAE INFECTIONS; PARVOVIRUS B19, HUMAN; PHOSPHORYLATION; RECEPTORS, ERYTHROPOIETIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TYRPHOSTINS; VIRAL TROPISM; VIRUS REPLICATION;

PARVOVIRUS;

EID: 78049517981     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01229-10     Document Type: Article

References (64)

1. Al-Khan, A., A. Caligiuri, and J. Apuzzio. 2003. Parvovirus B-19 infection during pregnancy. Infect. Dis. Obstet. Gynecol. 11:175-179.
2. Anderson, M. J., M. N. Khousam, D. J. Maxwell, S. J. Gould, L. C. Happerfield, and W. J. Smith. 1988. Human parvovirus B19 and hydrops fetalis. Lancet i:535.
3. Asokan, A., J. B. Hamra, L. Govindasamy, M. Agbandje-McKenna, and R. J. Samulski. 2006. Adeno-associated virus type 2 contains an integrin alpha5beta1 binding domain essential for viral cell entry. J. Virol. 80:8961-8969.
4. Basic, D., S. Gupta, and R. Y. Kwong. 2010. Parvovirus b19-induced myocarditis mimicking acute myocardial infarction: clarification of diagnosis by cardiac magnetic resonance imaging. Circulation 121:e40-e42.
5. Bernuau, J., F. Durand, and D. Valla. 1999. Parvovirus B19 infection and fulminant hepatitis. Lancet 353:754-755. (Pubitemid 29103829)
6. Bock, C. T., K. Klingel, and R. Kandolf. 2010. Human parvovirus B19-associated myocarditis. N. Engl. J. Med. 362:1248-1249.
7. Bonvicini, F., C. Filippone, S. Delbarba, E. Manaresi, M. Zerbini, M. Musiani, and G. Gallinella. 2006. Parvovirus B19 genome as a single, two-state replicative and transcriptional unit. Virology 347:447-454.
8. Brown, K. E., S. M. Anderson, and N. S. Young. 1993. Erythrocyte P antigen: cellular receptor for B19 parvovirus. Science 262:114-117.
9. 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.
10. Brown, K. E., N. S. Young, and J. M. Liu. 1994. Molecular, cellular and clinical aspects of parvovirus B19 infection. Crit. Rev. Oncol. Hematol. 16:1-31.
11. 2/M phase. J. Virol. 84:5615-5626.
12. Chen, A. Y., E. Y. Zhang, W. Guan, F. Cheng, S. Kleiboeker, T. M. Yankee, and J. Qiu. 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.
13. Chisaka, H., E. Morita, N. Yaegashi, and K. Sugamura. 2003. Parvovirus B19 and the pathogenesis of anaemia. Rev. Med. Virol. 13:347-359.
14. Cotmore, S. F., and P. Tattersall. 2005. Structure and organization of the viral genome, p. 73-94. In J. Kerr, S. F. Cotmore, M. E. Bloom, R. M. Linden, and C. R. Parrish (ed.), Parvoviruses. Hodder Arnold, London, United Kingdom.
15. Dai, C. H., S. B. Krantz, and K. M. Zsebo. 1991. Human burst-forming units-erythroid need direct interaction with stem cell factor for further development. Blood 78:2493-2497.
16. de Jong, E. P., T. R. de Haan, A. C. Kroes, M. F. Beersma, D. Oepkes, and F. J. Walther. 2006. Parvovirus B19 infection in pregnancy. J. Clin. Virol. 36:1-7.
17. de Wolf, J. T., E. W. Muller, D. H. Hendriks, R. M. Halie, and E. Vellenga. 1994. Mast cell growth factor modulates CD36 antigen expression on erythroid progenitors from human bone marrow and peripheral blood associated with ongoing differentiation. Blood 84:59-64.
18. Duechting, A., C. Tschope, H. Kaiser, T. Lamkemeyer, N. Tanaka, S. Aberle, F. Lang, J. Torresi, R. Kandolf, and C. T. Bock. 2008. Human parvovirus B19 NS1 protein modulates inflammatory signaling by activation of STAT3/PIAS3 in human endothelial cells. J. Virol. 82:7942-7952.
19. Filippone, C., R. Franssila, A. Kumar, L. Saikko, P. E. Kovanen, M. Soderlund- Venermo, and K. Hedman. 2010. Erythroid progenitor cells expanded from peripheral blood without mobilization or preselection: molecular characteristics and functional competence. PLoS One 5:e9496.
20. Fu, P., X. Jiang, and M. O. Arcasoy. 2009. Constitutively active erythropoietin receptor expression in breast cancer cells promotes cellular proliferation and migration through a MAP-kinase dependent pathway. Biochem. Biophys. Res. Commun. 379:696-701.
21. Guan, W., F. Cheng, Y. Yoto, S. Kleiboeker, S. Wong, N. Zhi, D. J. Pintel, and J. Qiu. 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.
22. Guan, W., S. Wong, N. Zhi, and J. Qiu. 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.
23. Karetnyi, Y. V., P. R. Beck, R. S. Markin, A. N. Langnas, and S. J. Naides. 1999. Human parvovirus B19 infection in acute fulminant liver failure. Arch. Virol. 144:1713-1724.
24. Koury, M. J., and M. C. Bondurant. 1992. The molecular mechanism of erythropoietin action. Eur. J. Biochem. 210:649-663.
25. Lodish, H. F., S. Ghaffari, M. Socolovsky, W. Tong, and J. Zhang. 2009. Intracellular signaling by the erythropoietin receptor, p. 155-174. In S. G. Elliott, M. A. Foote, and G. Molineux (ed.), Erythropoietins, erythropoietic factors and erythropoiesis. Birkhäuser Verlag, Basel, Switzerland.
26. Longmore, G. D., and H. F. Lodish. 1991. An activating mutation in the murine erythropoietin receptor induces erythroleukemia in mice: a cytokine receptor superfamily oncogene. Cell 67:1089-1102.
27. Meydan, N., T. Grunberger, H. Dadi, M. Shahar, E. Arpaia, Z. Lapidot, J. S. Leeder, M. Freedman, A. Cohen, A. Gazit, A. Levitzki, and C. M. Roifman. 1996. Inhibition of acute lymphoblastic leukaemia by a Jak-2 inhibitor. Nature 379:645-648.
28. 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. (Pubitemid 29528543)
29. 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. (Pubitemid 28175541)
30. Morey, A. L., and K. A. Fleming. 1992. Immunophenotyping of fetal haemopoietic cells permissive for human parvovirus B19 replication in vitro. Br. J. Haematol. 82:302-309.
31. 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.
32. 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. (Pubitemid 41609180)
33. Muta, K., S. B. Krantz, M. C. Bondurant, and C. H. Dai. 1995. Stem cell factor retards differentiation of normal human erythroid progenitor cells while stimulating proliferation. Blood 86:572-580.
34. Neubauer, H., A. Cumano, M. Muller, H. Wu, U. Huffstadt, and K. Pfeffer. 1998. Jak2 deficiency defines an essential developmental checkpoint in de- finitive hematopoiesis. Cell 93:397-409. (Pubitemid 28232084)
35. Noguchi, C. T., L. Wang, H. M. Rogers, R. Teng, and Y. Jia. 2008. Survival and proliferative roles of erythropoietin beyond the erythroid lineage. Expert Rev. Mol. Med. 10:e36.
36. Ogawa, M. 1993. Differentiation and proliferation of hematopoietic stem cells. Blood 81:2844-2853. (Pubitemid 23162099)
37. Okumura, N., K. Tsuji, and T. Nakahata. 1992. Changes in cell surface antigen expressions during proliferation and differentiation of human erythroid progenitors. Blood 80:642-650.
38. 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. (Pubitemid 17097550)
39. Ozawa, K., G. Kurtzman, and N. Young. 1986. Replication of the B19 parvovirus in human bone marrow cell cultures. Science 233:883-886. (Pubitemid 16011896)
40. Papayannopoulou, T., M. Brice, and C. A. Blau. 1993. Kit ligand in synergy with interleukin-3 amplifies the erythropoietin-independent, globin-synthesizing progeny of normal human burst-forming units-erythroid in suspension cultures: physiologic implications. Blood 81:299-310.
41. Pardi, D. S., Y. Romero, L. E. Mertz, and D. D. Douglas. 1998. Hepatitis-associated aplastic anemia and acute parvovirus B19 infection: a report of two cases and a review of the literature. Am. J. Gastroenterol. 93:468-470.
42. Parganas, E., D. Wang, D. Stravopodis, D. J. Topham, J. C. Marine, S. Teglund, E. F. Vanin, S. Bodner, O. R. Colamonici, J. M. van Deursen, G. Grosveld, and J. N. Ihle. 1998. Jak2 is essential for signaling through a variety of cytokine receptors. Cell 93:385-395.
43. Pillet, S., G. N. Le, T. Hofer, F. NguyenKhac, M. Koken, J. T. Aubin, S. Fichelson, M. Gassmann, and F. Morinet. 2004. Hypoxia enhances human B19 erythrovirus gene expression in primary erythroid cells. Virology 327:1-7.
44. Pinto, J. P., S. Ribeiro, H. Pontes, S. Thowfeequ, D. Tosh, F. Carvalho, and G. Porto. 2008. Erythropoietin mediates hepcidin expression in hepatocytes through EPOR signaling and regulation of C/EBPalpha. Blood 111:5727-5733.
45. Poole, B. D., J. Zhou, A. Grote, A. Schiffenbauer, and S. J. Naides. 2006. Apoptosis of liver-derived cells induced by parvovirus B19 nonstructural protein. J. Virol. 80:4114-4121.
46. Qiu, J., F. Cheng, and D. Pintel. 2007. The abundant R2 mRNA generated by Aleutian mink disease parvovirus is tricistronic, encoding NS2, VP1, and VP2. J. Virol. 81:6993-7000.
47. Riipinen, A., E. Vaisanen, M. Nuutila, M. Sallmen, R. Karikoski, M. L. Lindbohm, K. Hedman, H. Taskinen, and M. Soderlund-Venermo. 2008. Parvovirus b19 infection in fetal deaths. Clin. Infect. Dis. 47:1519-1525.
48. Sokal, E. M., M. Melchior, C. Cornu, A. T. Vandenbroucke, J. P. Buts, B. J. Cohen, and G. Burtonboy. 1998. Acute parvovirus B19 infection associated with fulminant hepatitis of favourable prognosis in young children. Lancet 352:1739-1741.
49. Sol, N., J. J. Le, I. Vassias, J. M. Freyssinier, A. Thomas, A. F. Prigent, B. B. Rudkin, S. Fichelson, and F. Morinet. 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.
50. 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.
51. + cells. J. Exp. Med. 183:837-845.
52. 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.
53. Vainchenker, W., J. F. Deschamps, J. M. Bastin, J. Guichard, M. Titeux, J. Breton-Gorius, and A. J. McMichael. 1982. Two monoclonal antiplatelet antibodies as markers of human megakaryocyte maturation: immunofluorescent staining and platelet peroxidase detection in megakaryocyte colonies and in in vivo cells from normal and leukemic patients. Blood 59:514-521.
54. Weigel-Kelley, K. A., M. C. Yoder, and A. Srivastava. 2001. Recombinant human parvovirus B19 vectors: erythrocyte P antigen is necessary but not sufficient for successful transduction of human hematopoietic cells. J. Virol. 75:4110-4116.
55. 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.
56. + erythroid progenitors are highly permissive to human parvovirus B19 replication. J. Virol. 82:2470-2476.
57. Woolf, A. D., G. V. Campion, A. Chishick, S. Wise, B. J. Cohen, P. T. Klouda, O. Caul, and P. A. Dieppe. 1989. Clinical manifestations of human parvovirus B19 in adults. Arch. Intern. Med. 149:1153-1156.
58. Wu, H., U. Klingmuller, P. Besmer, and H. F. Lodish. 1995. Interaction of the erythropoietin and stem-cell-factor receptors. Nature 377:242-246.
59. Wu, H., X. Liu, R. Jaenisch, and H. F. Lodish. 1995. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell 83:59-67.
60. Yaegashi, N., T. Niinuma, H. Chisaka, S. Uehara, S. Moffatt, K. Tada, M. Iwabuchi, Y. Matsunaga, M. Nakayama, C. Yutani, Y. Osamura, E. Hirayama, K. Okamura, K. Sugamura, and A. Yajima. 1999. Parvovirus B19 infection induces apoptosis of erythroid cells in vitro and in vivo. J. Infect. 39:68-76.
61. 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.
62. Young, N. S., and K. E. Brown. 2004. Parvovirus B19. N. Engl. J. Med. 350:586-597.
63. Zandstra, P. W., E. Conneally, A. L. Petzer, J. M. Piret, and C. J. Eaves. 1997. Cytokine manipulation of primitive human hematopoietic cell self-renewal. Proc. Natl. Acad. Sci. U. S. A. 94:4698-4703.
64. Zhang, C. C., and H. F. Lodish. 2008. Cytokines regulating hematopoietic stem cell function. Curr. Opin. Hematol. 15:307-311.