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. 1993 Sep;67(9):5698–5703. doi: 10.1128/jvi.67.9.5698-5703.1993

Comparison of the ability of lactate dehydrogenase-elevating virus and its virion RNA to infect murine leukemia virus-infected or -uninfected cell lines.

T Inada 1, H Kikuchi 1, S Yamazaki 1
PMCID: PMC237979  PMID: 8394468

Abstract

Lactate dehydrogenase-elevating virus (LDV) has a strict species specificity. Cells or cell lines other than a particular subset of mouse primary macrophages which can support LDV replication in vitro have not been identified. LDV induces neurological disorders in old C58 or AKR strains, in which the involvement of multiple copies of the endogenous N-tropic murine leukemia virus (MuLV) genome and the Fv-1 locus of the mouse has been implicated. Our previous studies have demonstrated that LDV could infect and replicate in cell lines of the mouse or other species in vitro when they were infected with MuLV. The significance of and the precise mechanism underlying this phenomenon, however, remain unclear. We demonstrated in this study the efficient infection and replication of the virus in vitro by inoculation of its RNA mixed with liposome. No significant difference either in the efficiency of RNA transfection or in the ability to support its replication was observed among the various species' cell lines examined. In addition, by RNA transfection the virus replicated with equal efficiency in MuLV-infected and -uninfected cells or in macrophages derived from mice irrespective of their age. In contrast, the pattern of the infection by virus particles was quite different; LDV replication was observed only in macrophages (particularly from newborn mice) and MuLV-infected cells. By using various LDV isolates, it was demonstrated that the capability of replication between neurovirulent, LDV type C, and the other avirulent strains was almost the same in mouse cell lines when their RNA was introduced into the cells. Higher infectivity of LDV-C to MuLV-infected cells may be due to its efficient incorporation of the particles into MuLV-infected cells.

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Selected References

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  1. Brinton-Darnell M., Plagemann P. G. Structure and chemical-physical characteristics of lactate dehydrogenase-elevating virus and its RNA. J Virol. 1975 Aug;16(2):420–433. doi: 10.1128/jvi.16.2.420-433.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brinton M. A., Gavin E. I., Fernandez A. V. Genotypic variation among six isolates of lactate dehydrogenase-elevating virus. J Gen Virol. 1986 Dec;67(Pt 12):2673–2684. doi: 10.1099/0022-1317-67-12-2673. [DOI] [PubMed] [Google Scholar]
  3. Buxton I. K., Chan S. P., Plagemann P. G. The IA antigen is not the major receptor for lactate dehydrogenase-elevating virus on macrophages from CBA and BALB/c mice. Virus Res. 1988 Feb;9(2-3):205–219. doi: 10.1016/0168-1702(88)90031-7. [DOI] [PubMed] [Google Scholar]
  4. Cafruny W. A., Plagemann P. G. Immune response to lactate dehydrogenase-elevating virus: serologically specific rabbit neutralizing antibody to the virus. Infect Immun. 1982 Sep;37(3):1007–1012. doi: 10.1128/iai.37.3.1007-1012.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cafruny W. A., Strancke C. R., Kowalchyk K., Plagemann P. G. Replication of lactate dehydrogenase-elevating virus in C58 mice and quantification of antiviral antibodies and of tissue virus levels as a function of development of paralytic disease. J Gen Virol. 1986 Jan;67(Pt 1):27–37. doi: 10.1099/0022-1317-67-1-27. [DOI] [PubMed] [Google Scholar]
  6. Contag C. H., Chan S. P., Wietgrefe S. W., Plagemann P. G. Correlation between presence of lactate dehydrogenase-elevating virus RNA and antigens in motor neurons and paralysis in infected C58 mice. Virus Res. 1986 Dec;6(3):195–209. doi: 10.1016/0168-1702(86)90069-9. [DOI] [PubMed] [Google Scholar]
  7. Contag C. H., Plagemann P. G. Age-dependent poliomyelitis of mice: expression of endogenous retrovirus correlates with cytocidal replication of lactate dehydrogenase-elevating virus in motor neurons. J Virol. 1989 Oct;63(10):4362–4369. doi: 10.1128/jvi.63.10.4362-4369.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Duffey P. S., Martinez D., Abrams G. D., Murphy W. H. Pathogenetic mechanisms in immune polioencephalomyelitis: induction of disease in immunosuppressed mice. J Immunol. 1976 Feb;116(2):475–481. [PubMed] [Google Scholar]
  9. Felgner P. L., Gadek T. R., Holm M., Roman R., Chan H. W., Wenz M., Northrop J. P., Ringold G. M., Danielsen M. Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7413–7417. doi: 10.1073/pnas.84.21.7413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Godeny E. K., Speicher D. W., Brinton M. A. Map location of lactate dehydrogenase-elevating virus (LDV) capsid protein (Vp1) gene. Virology. 1990 Aug;177(2):768–771. doi: 10.1016/0042-6822(90)90546-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gravell M., London W. T., Leon M. E., Palmer A. E., Hamilton R. S. Differences among isolates of simian hemorrhagic fever (SHF) virus. Proc Soc Exp Biol Med. 1986 Jan;181(1):112–119. doi: 10.3181/00379727-181-42231. [DOI] [PubMed] [Google Scholar]
  12. Inada T., Mims C. A. Ia antigens and Fc receptors of mouse peritoneal macrophages as determinants of susceptibility to lactic dehydrogenase virus. J Gen Virol. 1985 Jul;66(Pt 7):1469–1477. doi: 10.1099/0022-1317-66-7-1469. [DOI] [PubMed] [Google Scholar]
  13. Inada T., Mims C. A. Mouse Ia antigens are receptors for lactate dehydrogenase virus. Nature. 1984 May 3;309(5963):59–61. doi: 10.1038/309059a0. [DOI] [PubMed] [Google Scholar]
  14. Inada T., Mims C. A. Pattern of infection and selective loss of Ia positive cells in suckling and adult mice inoculated with lactic dehydrogenase virus. Arch Virol. 1985;86(3-4):151–165. doi: 10.1007/BF01309821. [DOI] [PubMed] [Google Scholar]
  15. Inada T. Replication of lactate dehydrogenase-elevating virus in various species cell lines infected with dual-, ampho- and xenotropic murine leukaemia viruses in vitro. Virus Res. 1993 Mar;27(3):267–281. doi: 10.1016/0168-1702(93)90038-o. [DOI] [PubMed] [Google Scholar]
  16. Inada T., Yamazaki S. Replication of lactate dehydrogenase-elevating virus in cells infected with murine leukaemia viruses in vitro. J Gen Virol. 1991 Oct;72(Pt 10):2437–2444. doi: 10.1099/0022-1317-72-10-2437. [DOI] [PubMed] [Google Scholar]
  17. Kascsak R. J., Carp R. I., Donnenfeld H., Bartfeld H. Kinetics of replication of lactate dehydrogenase-elevating virus in age-dependent polioencephalomyelitis. Intervirology. 1983;19(1):6–15. doi: 10.1159/000149331. [DOI] [PubMed] [Google Scholar]
  18. Kowalchyk K., Plagemann P. G. Cell surface receptors for lactate dehydrogenase-elevating virus on subpopulation of macrophages. Virus Res. 1985 Apr;2(3):211–229. doi: 10.1016/0168-1702(85)90010-3. [DOI] [PubMed] [Google Scholar]
  19. Kuo L. L., Harty J. T., Erickson L., Palmer G. A., Plagemann P. G. A nested set of eight RNAs is formed in macrophages infected with lactate dehydrogenase-elevating virus. J Virol. 1991 Sep;65(9):5118–5123. doi: 10.1128/jvi.65.9.5118-5123.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Martinez D., Brinton M. A., Tachovsky T. G., Phelps A. H. Identification of lactate dehydrogenase-elevating virus as the etiological agent of genetically restricted, age-dependent polioencephalomyelitis of mice. Infect Immun. 1980 Mar;27(3):979–987. doi: 10.1128/iai.27.3.979-987.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Martinez D., Wolanski B., Tytell A. A., Devlin R. G. Viral etiology of age-dependent polioencephalomyelitis in C58 mice. Infect Immun. 1979 Jan;23(1):133–139. doi: 10.1128/iai.23.1.133-139.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Murphy W. H., Nawrocki J. F., Pease L. R. Age-dependent paralytic viral infection in C58 mice: possible implications in human neurologic disease. Prog Brain Res. 1983;59:291–303. doi: 10.1016/S0079-6123(08)63874-1. [DOI] [PubMed] [Google Scholar]
  23. NOTKINS A. L. RECOVERY OF AN INFECTIOUS RIBONUCLEIC ACID FROM THE LACTIC DEHYDROGENASE AGENT BY TREATMENT WITH ETHER. Virology. 1964 Apr;22:563–567. doi: 10.1016/0042-6822(64)90077-7. [DOI] [PubMed] [Google Scholar]
  24. NOTKINS A. L., SCHEELE C. AN INFECTIOUS NUCLEIC ACID FROM THE LACTIC DEHYDROGENASE AGENT. Virology. 1963 Aug;20:640–642. doi: 10.1016/0042-6822(63)90291-5. [DOI] [PubMed] [Google Scholar]
  25. Nawrocki J. F., Pease L. R., Murphy W. H. Etiologic role of lactic dehydrogenase virus infection in an age-dependent neuroparalytic disease in C58 mice. Virology. 1980 May;103(1):259–264. doi: 10.1016/0042-6822(80)90147-6. [DOI] [PubMed] [Google Scholar]
  26. Onyekaba C. O., Harty J. T., Even C., Hu B. G., Plagemann P. G. Persistent infection of mice by lactate dehydrogenase-elevating virus: effects of immunosuppression on virus replication and antiviral immune responses. Virus Res. 1989 Dec;14(4):297–315. doi: 10.1016/0168-1702(89)90023-3. [DOI] [PubMed] [Google Scholar]
  27. Onyekaba C. O., Harty J. T., Plagemann P. G. Extensive cytocidal replication of lactate dehydrogenase-elevating virus in cultured peritoneal macrophages from 1-2-week-old mice. Virus Res. 1989 Dec;14(4):327–338. doi: 10.1016/0168-1702(89)90025-7. [DOI] [PubMed] [Google Scholar]
  28. Pease L. R., Abrams G. D., Murphy W. H. FV-1 restriction of age-dependent paralytic lactic dehydrogenase virus infection. Virology. 1982 Feb;117(1):29–37. doi: 10.1016/0042-6822(82)90504-9. [DOI] [PubMed] [Google Scholar]
  29. Pease L. R., Murphy W. H. Co-infection by lactic dehydrogenase virus and C-type retrovirus elicits neurological disease. Nature. 1980 Jul 24;286(5771):398–400. doi: 10.1038/286398a0. [DOI] [PubMed] [Google Scholar]
  30. Plagemann P. G., Moennig V. Lactate dehydrogenase-elevating virus, equine arteritis virus, and simian hemorrhagic fever virus: a new group of positive-strand RNA viruses. Adv Virus Res. 1992;41:99–192. doi: 10.1016/S0065-3527(08)60036-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ritzi D. M., Holth M., Smith M. S., Swart W. J., Cafruny W. A., Plagemann G. W., Stueckemann J. A. Replication of lactate dehydrogenase-elevating virus in macrophages. 1. Evidence for cytocidal replication. J Gen Virol. 1982 Apr;59(Pt 2):245–262. doi: 10.1099/0022-1317-59-2-245. [DOI] [PubMed] [Google Scholar]
  32. Rowson K. E., Mahy B. W. Lactate dehydrogenase-elevating virus. J Gen Virol. 1985 Nov;66(Pt 11):2297–2312. doi: 10.1099/0022-1317-66-11-2297. [DOI] [PubMed] [Google Scholar]
  33. Rowson K. E., Mahy B. W. Lactic dehydrogenase virus. Virol Monogr. 1975;(13):1–121. doi: 10.1007/978-3-7091-8378-6_1. [DOI] [PubMed] [Google Scholar]
  34. Stroop W. G., Weibel J., Schaefer D., Brinton M. A. Ultrastructural and immunofluorescent studies of acute and chronic lactate dehydrogenase elevating virus-induced nonparalytic poliomyelitis in mice. Proc Soc Exp Biol Med. 1985 Feb;178(2):261–274. doi: 10.3181/00379727-178-42009. [DOI] [PubMed] [Google Scholar]
  35. Takeda N., Miyamura K., Takegami T., Yamazaki S. A temperature-sensitive defect of enterovirus 70 is located at the uridylylation of the genome-linked protein VPg in vitro. Virus Genes. 1989 Aug;2(4):347–355. doi: 10.1007/BF00684042. [DOI] [PubMed] [Google Scholar]
  36. Zeegers J. J., Van der Zeijst B. A., Horzinek M. C. The structural proteins of equine arteritis virus. Virology. 1976 Aug;73(1):200–205. doi: 10.1016/0042-6822(76)90074-x. [DOI] [PubMed] [Google Scholar]

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