Severe leukopenia and dysregulated erythropoiesis in SCID mice persistently infected with the parvovirus minute virus of mice

Journal of Virology

Volumn 73, Issue 3, 1999, Pages 1774-1784

  Segovia, José C ^a   Gallego, Jesús M ^b   Bueren, Juan A ^a   Almendral, José M ^b  

^a CIEMAT   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BURST FORMING UNIT E; COLONY FORMING UNIT GM; CONTROLLED STUDY; DYSERYTHROPOIESIS; ERYTHROBLAST; LEUKOPENIA; MACROPHAGE; MOUSE; NONHUMAN; PARVOVIRUS; PRIORITY JOURNAL; SCID MOUSE; VIRUS INFECTION; VIRUS REPLICATION;

EID: 0033019497     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.3.1774-1784.1999     Document Type: Article

References (72)

1. Anderson, M. J., E. Lewis, I. M. Kidd, S. M. Hall, and B. J. Cohen. 1984. An outbreak of erythema infectiosum associated with human parvovirus infection. J. Hyg. 93:85-93.
2. Anderson, M. J., P. G. Higgins, L. R. Davis, J. S. Willman, S. E. Jones, I. M. Kidd, J. R. Pattison, and D. A. J. Tyrrell. 1985. Experimental parvovirus infection in man. J. Infect. Dis. 152:257-265.
3. Ansel, J. D., and G. J. Bancroft. 1989. The biology of the SCID mutation. Immunol. Today 10:322-325.
4. Baldauf, A. Q., K. Willwand, E. Mumtsidu, J. P. F. Nüesch, and J. Rommelaere. 1997. Specific initiation of replication at the right-end telomera of the closed species of minute virus of mice replicative-form DNA. J. Virol. 71:971-980.
5. Berns, K. I. 1996. Parvoviridae: the viruses and their replication, p. 2173-2197. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Virology, 3rd ed. Lippincott-Raven Press, New York, N.Y.
6. Bloom, M. E., H. Kanno, S. Mori, and J. B. Wolfinbarger. 1994. Aleutian mink disease: puzzles and paradigms. Infect. Agents Dis. 3:279-301.
7. Bloom, M. E., R. E. Race, and J. B. Wolfinbarger. 1987. Analysis of Aleutian disease of mink parvovirus infection using strand-specific hybridization probes. Intervirology 27:102-111.
8. Bloom, M. E., S. Alexandersen, S. Mori, and J. B. Wolfinbarger. 1989. Analysis of parvovirus infections using strand-specific hybridization probes. Virus Res. 14:1-26.
9. Bonnard, G. D., E. K. Manders, D. A. Campbell, R. B. Herberman, and M. J. Collins. 1976. Immunosuppressive activity of a subline of the mouse EL-4 lymphoma. J. Exp. Med. 143:187-205.
10. Bosma, G. C., M. Fried, R. P. Custer, A. Carroll, D. M. Gibson, and M. J. Bosma. 1988. Evidence of functional lymphocytes in some (leaky) scid mice. J. Exp. Med. 167:1016-1033.
11. Bosma, G. C., R. P. Custer, and M. J. Bosma. 1983. A severe combined immunodeficiency mutation in the mouse. Nature 301:527-530.
12. Brown, D. W., R. M. Welsh, and A. A. Like. 1993. Infection of peripancreatic lymph nodes but not islets precedes Kilham rat virus-induced diabetes in BB/Wor rats. J. Virol. 10:5873-5878.
13. Brown, K. E., S. M. Anderson, and N. S. Young. 1993. Erythrocyte P antigen: cellular receptor for B19 parvovirus. Science 262:114-117.
14. Brownstein, D. G., A. L. Smith, R. O. Jacoby, E. A. Johnson, G. Hansen, and P. Tattersall. 1991. Pathogenesis of infection with a virulent allotropic variant of minute virus of mice and regulation by host genotype. Lab. Invest. 65:357-363.
15. Caillet-Fauquet, P., M. Perros, A. Brandenburger, P. Spegelaere, and J. Rommelaere. 1990. Programmed killing of human cells by means of an inducible clone of parvoviral genes encoding non-structural proteins. EMBO J. 9:2989-2995.
16. Chipman, P. R., M. Agbandje-McKenna, S. Kajigaya, K. E. Brown, N. S. Young, T. S. Baker, and M. G. Rossmann. 1996. Cryo-electron microscopy studies of empty capsids of human parvovirus B19 complexed with its cellular receptor. Proc. Natl. Acad. Sci. USA 93:7502-7506.
17. Christensen, J., S. F. Cotmore, and P. Tattersall. 1997. A novel cellular site-specific DNA-binding protein cooperates with the viral NS1 polypeptide to initiate parvovirus DNA replication. J. Virol. 71:1405-1416.
18. Chung, Y. H., H. S. Jun, Y. Kang, K. Hirasawa, B. R. Lee, N. Van Rooijen, and J. W. Yoon. 1997. Role of macrophages and macrophage-derived cytokines in the pathogenesis of Kilham rat virus-induced autoimmune diabetes in diabetes-resistant biobreeding rats. J. Immunol. 159:466-471.
19. Cohen, B. J., M. M. Bucklley, J. P. Clewley, V. E. Jones, A. H. Puttick, and R. K. Jacoby. 1986. Human parvovirus infection in early rheumatoid and inflammatory arthritis. Ann. Rheum. Dis. 45:832-838.
20. Cornelis, J. J., P. Becquart, N. Duponchel, N. Salomé, B. L. Avalosse, M. Namba, and J. Rommelaere. 1988. Transformation of human fibroblasts by ionizing radiation, a chemical carcinogen, or simian virus 40 correlates with an increase in susceptibility to the autonomous parvovirus H-1 virus and minute virus of mice. J. Virol. 62:1679-1686.
21. Cowling, G. J., and T. M. Dexter. 1992. Erythropoietin and myeloid colony stimulating factors. Trends Biotechnol. 10:349-357.
22. Doerig, C., B. Hirt, J. P. Antonietti, and P. Beard. 1990. Nonstructural protein of parvovirus B19 and minute virus of mice controls transcription. J. Virol. 64:387-396.
23. Doerig, C., B. Hirt, P. Beard, and J. P. Antonietti. 1988. Minute virus of mice non-structural proteins NS-1 is necessary and sufficient for trans-activation of the viral P39 promoter. J. Gen. Virol. 69:2563-2573.
24. Engers, H. D., J. A. Louis, R. H. Zubler, and B. Hirt. 1981. Inhibition of T-cell mediated functions by MVM(i), a parvovirus closely related to minute virus of mice. J. Immunol. 127:2280-2285.
25. Erslev, A. J. 1990. The production of erythrocytes, p. 389-397. In W. J. Williams, E. Beutler, A. J. Erslev, and M. A. Lichtman (ed.), Hematology. McGraw-Hill Publishing Co., New York, N.Y.
26. Faisst, S., S. Bartnitzke, J. R. Schlehofer, and H. zur Hausen. 1990. Persistence of parvovirus H-1 DNA in human B-and T-lymphoma cells. Virus Res. 16:211-224.
27. Frickhofen, N., J. L. Abkowitz, M. Safford, M. Berry, J. Antunez-de-Mayolo, A. Aslrow, R. Cohen, I. Halperin, L. King, D. Mintzer, B. Cohen, and N. S. Young. 1990. Persistent B19 parvovirus infection in patients infected with human immunodeficiency virus type 1 (HIV-1): a treatable cause of anemia in AIDS. Ann. Intern. Med. 113:926-933.
28. Harris, J. W. 1992. Parvovirus B19 for the hematologist. Am. J. Hematol. 39:119-130.
29. Jacoby, R. O., E. A. Johnson, F. X. Paturzo, D. J. Gaertner, J. L. Brandsma, and A. L. Smith. 1991. Persistent rat parvovirus infection in individually housed rats. Arch. Virol. 117:193-205.
30. Kelley, L. L., M. J. Koury, M. C. Bondurant, S. T. Koury, S. T. Sawyer, and A. Wickrema. 1993. Survival or death of individual proerythroblasts results from differing erythropoietin sensitivities: a mechanism for controlled rates of erythrocyte production. Blood 82:2340-2352.
31. Kimsey, P. B., H. D. Engers, B. Hirt, and V. Jongeneel. 1986. Pathogenicity of fibroblast-and lymphocyte-specific variants of minute virus of mice. J. Virol. 59:8-13.
32. Krishan, A. 1975. Rapid flow cytometric analysis of mammalian cell cycle by propidium iodide staining. J. Cell Biol. 66:188-193.
33. Kurtzman, G. J., K. Ozawa, B. Cohen, G. Hanson, R. Oseas, and N. S. Young. 1987. Chronic bone marrow failure due to persistent B19 parvovirus infection. N. Engl. J. Med. 317:287-294.
34. Kurtzman, G. J., L. Platanias, L. Lustig, N. Frickhofen, and N. S. Young. 1989. Feline parvovirus propagates in cat bone marrow cultures and inhibits hematopoietic colony formation in vitro. Blood 74:71-81.
35. Larse, S., A. Flagstad, and B. Aalbaek. 1976. Experimental feline panleukopenia in the conventional cat. Vet. Pathol. 13:216-240.
36. Lawrence, J. S., J. T. Syverton, J. S. Shaw, and F. P. Smith. 1940. Infectious feline agranulocytosis. Am. J. Pathol. 16:333-354.
37. Legendre, D., and J. Rommelaere. 1992. Terminal regions of the NS-1 protein of the parvovirus minute virus of mice are involved in cytotoxicity and promoter trans inhibition. J. Virol. 66:5705-5713.
38. Lichtman, M. A., J. K. Chamberlain, and P. A. Santillo. 1978. Factors thought to contribute to the regulation of egress of cells from marrow, p. 243-258. In R. Silber, J. LoBue, and A. S. Gordon (ed.), The year of hematology. Plenum Press, New York, N.Y.
39. Metcalf, D. 1989. The molecular control of cell division, differentiation, commitment and maturation in haemopoietic cells. Nature 339:27-30.
40. Miller, R. A., D. C. Ward, and F. H. Ruddle. 1977. Embryonal carcinoma cells (and their somatic cell hybrids) are resistant to infection by the murine parvovirus MVM, which does infect other teratocarcinoma-derived cell lines. J. Cell. Physiol. 91:393-402.
41. Moffatt, S., N. Tanaka, K. Tada, M. Nose, M. Nakamura, O. Muraoka, T. Hirano, and K. Sugamura. 1996. A cytotoxic nonstructural protein (NS1) of human parvovirus B19 induces the activation of interleukin-6 gene expression. J. Virol. 70:8485-8491.
42. Moffatt, S., N. Yaegashi, K. Tada, N. Tanaka, and K. Sugamura. 1998. Human parvovirus B19 nonstructural (NS1) protein induces apoptosis in erythroid cells. J. Virol. 72:3018-3028.
43. Mori, S., J. B. Wolfinbarger, M. Miyazawa, and M. E. Bloom. 1991. Replication of Aleutian mink disease parvovirus in lymphoid tissues of adult mink: involvement of follicular dendritic cells and macrophages. J. Virol. 65:952-956.
44. Mortimer, P. P., R. K. Humphries, J. G. Moore, R. H. Purcell, and N. S. Young. 1983. A human parvovirus-like virus inhibits haemopoietic colony formation in vitro. Nature 302:426-429.
45. Owren, P. A. 1948. Congenital hemolytic jaundice: the pathogenesis of the "hemolytic crisis." Blood 3:231-248.
46. Ozawa, K., G. Kurtzman, and N. Young. 1987. Productive infection by B19 parvovirus of human erythroid bone marrow cells in vitro. Blood 70:384-391.
47. Pattison, J. R., S. E. Jones, and J. Hodgson. 1981. Parvovirus infections and hypoplastic crises in sickle cell anaemia. Lancet i:564-665.
48. Porter, D. D., A. E. Larsen, and H. G. Porter. 1969. The pathogenesis of Aleutian disease of mink. In vivo viral replication and the host antibody response to viral antigen. J. Exp. Med. 130:575-589.
49. Potter, C. G., A. C. Potter, C. S. R. Hatton, H. M. Chapel, M. J. Anderson, J. R. Pattison, D. A. J. Tyrrell, P. G. Higgins, J. S. Willman, H. F. Parry, and P. M. Cotes. 1987. Variation of erythroid and myeloid precursors in the marrow and peripheral blood of volunteer subjects infected with human parvovirus (B19). J. Clin. Invest. 79:1486-1492.
50. Quesenberry, P. P. 1990. Hemopoietic stem cells, progenitor cells, and growth factors, p. 129-147. In W. J. Williams, E. Beutler, A. J. Erslev, and M. A. Lichtman (ed.), Hematology. McGraw-Hill Publishing Co., New York. N.Y.
51. Ramírez, J. C., A. Fairén, and J. M. Almendral. 1996. Parvovirus minute virus of mice strain i multiplication and pathogenesis in the newborn mouse brain are restricted to proliferative areas and to migratory cerebellar young neurons. J. Virol. 70:8109-8116.
52. Rhode III, S. L. 1989. Both excision and replication of cloned autonomous parvovirus DNA require the NS1 (rep) protein. J. Virol. 63:4249-4256.
53. Segovia, J. C., A. Real, J. A. Bueren, and J. M. Almendral. 1991. In vitro myelosuppressive effects of the parvovirus minute virus of mice (MVMi) on hematopoietic stem and committed progenitor cells. Blood 77:980-988.
54. Segovia, J. C., J. A. Bueren, and J. M. Almendral. 1995. Myeloid depression follows infection of susceptible newborn mice with the parvovirus minute virus of mice (strain i). J. Virol. 69:3229-3232.
55. Shivdasani, R. A., and S. H. Orkin. 1996. The transcriptional control of hematopoiesis. Blood 87:4025-4039.
56. Siegl, G. 1988. Patterns of parvovirus disease in animals, p. 43-67. In J. R. Pattison (ed.). Parvoviruses and human disease. CRC Press, Boca Raton. Fla.
57. Siegl, G., R. C. Bates, K. I. Berns, B. J. Carter, D. C. Kelly, E. Kurstak, and P. Tattersall. 1985. Characteristics and taxonomy of Parvoviridae. Intervirology 23:61-73.
58. Spalholz, B. A., and P. Tattersall. 1983. Interaction of minute virus of mice with differentiated cells: strain-dependent cell specificity is mediated by intracellular factors. J. Virol. 46:937-943.
59. Studdert, M. J. 1990. Tissue tropism of parvoviruses, p. 3-27. In P. Tijssen (ed.), Handbook of parvoviruses, vol. II. CRC Press, Boca Raton, Fla.
60. 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.
61. Tattersall, P. 1972. Replication of parvovirus minute virus of mice. 1. Dependence of virus multiplication and plaque formation on cell growth. J. Virol. 10:586-590.
62. Tattersall, P., and E. M. Gardiner. 1990. Autonomous parvovirus host-cell interactions, p. 111-121. In P. Tijssen (ed.), Handbook of parvoviruses, vol I. CRC Press, Boca Raton, Fla.
63. Tennant, R. W., K. R. Laymant, and R. E. Hand, Jr. 1969. Effect of cell physiological state on infection by rat virus. J. Virol. 4:872-878.
64. Toolan, H. W. 1990. The rodent parvoviruses, p. 159-176. In P. Tijssen (ed.), Handbook of parvoviruses, vol II. CRC Press, Boca Raton, Fla.
65. Török, T. J. 1992. Parvovirus B19 and human disease. Adv. Intern. Med. 37:431-455.
66. Williams, G. T., C. A. Smith, E. Spooncer, T. M. Dexter, and D. R. Taylor. 1990. Haemopoietic colony stimulating factors promote cell survival by suppressing apoptosis. Nature 343:76-79.
67. Wu, H., V. Klingmüller, P. Besmer, and H. Lodish. 1995. Interaction of the erythropoietin and stem cell factor receptors. Nature 377:242-246.
68. 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.
69. Yeung, D. E., G. W. Brown, P. Tam, R. H. Russnak, G. Wilson, I. Clark-Lewis, and C. R. Astell. 1991. Monoclonal antibodies to the major nonstructural nuclear protein of minute virus of mice. Virology 181:35-45.
70. Young, N. S. 1993. Viruses and bone marrow, Marcel Dekker, Inc., New York, N.Y.
71. Young, N. S. 1996. Parvoviruses, p. 2199-2220. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Virology, 3rd ed. Lippincott-Raven Press, New York, N.Y.
72. Young, N. S., M. Yoshida, and W. Sugden. 1992. Viral pathogenesis of hematologic disorders. In G. Stamatoyanapoulos, A. S. Nienhuis, P. Leder, P. Majerus, and H. Varmus (ed.), Molecular basis of blood diseases. W. B. Saunders Co., Philadelphia, Pa.