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PMID: 3018287 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Molecular analysis and pathogenesis of the feline aplastic anemia retrovirus, feline leukemia virus C-Sarma.

Journal of virology ·Vol. 60 ·No. 1 ·1986-10-00 ·Pages 242-50

Riedel N, Hoover EA, Gasper PW, Nicolson MO, Mullins JI

Abstract

We describe the molecular cloning of an anemogenic feline leukemia virus (FeLV), FeLV-C-Sarma, from the productively infected human rhabdomyosarcoma cell line RD(FeLV-C-S). Molecularly cloned FeLV-C-S proviral DNA yielded infectious virus (mcFeLV-C-S) after transfection of mammalian cells, and virus interference studies using transfection-derived virus demonstrated that our clone encodes FeLV belonging to the C subgroup. mcFeLV-C-S did not induce viremia in eight 8-week-old outbred specific-pathogen-free (SPF) cats. It did, however, induce viremia and a rapid, fatal aplastic anemia due to profound suppression of erythroid stem cell growth in 9 of 10 inoculated newborn, SPF cats within 3 to 8 weeks (21 to 58 days) postinoculation. Thus, the genome of mcFeLV-C-S encodes the determinants responsible for the genetically dominant induction of irreversible erythroid aplasia in outbred cats. A potential clue to the pathogenic determinants of this virus comes from previous work indicating that all FeLV isolates belonging to the C subgroup, an envelop-gene-determined property, and only those belonging to the C subgroup, are potent, consistent inducers of aplastic anemia in cats. To approach the molecular mechanism underlying the induction of this disease, we first determined the nucleotide sequence of the envelope genes and 3' long terminal repeat of FeLV-C-S and compared it with that of FeLV-B-Gardner-Arnstein (mcFeLV-B-GA), a subgroup-B feline leukemia virus that consistently induces a different disease, myelodysplastic anemia, in neonatal SPF cats. Our analysis revealed that the p15E genes and long terminal repeats of the two FeLV strains are highly homologous, whereas there are major differences in the gp70 proteins, including five regions of significant amino acid differences and apparent sequence substitution. Some of these changes are also reflected in predicted glycosylation sites; the gp70 protein of FeLV-B-GA has 11 potential glycosylation sites, only 8 of which are present in FeLV-C-S.

MeSH Terms
Anemia, Aplastic/etiology,metabolism,veterinary Animals Base Sequence Cat Diseases/etiology,metabolism Cats Genes, Viral Leukemia Virus, Feline/genetics,isolation & purification,pathogenicity Repetitive Sequences, Nucleic Acid Retroviridae Proteins/genetics Viral Envelope Proteins/genetics Viremia/etiology,veterinary Virus Cultivation
Chemicals
Retroviridae Proteins Viral Envelope Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Riedel N
Hoover E A
Gasper P W
Nicolson M O
Mullins J I
References (62)
62 references, click to expand
  1. The U3 portion of feline leukemia virus DNA identifies horizontally acquired proviruses in leukemic cats.
    Proc Natl Acad Sci U S A. 1981 Dec;78(12):7778-82 PMID: 6278488
  2. The structure and evolution of the human beta-globin gene family.
    Cell. 1980 Oct;21(3):653-68 PMID: 6985477
  3. Sequence-specific antibodies show that maturation of Moloney leukemia virus envelope polyprotein involves removal of a COOH-terminal peptide.
    Proc Natl Acad Sci U S A. 1981 Oct;78(10):6023-7 PMID: 6947213
  4. Isolation of lymphocytopathic retroviruses from San Francisco patients with AIDS.
    Science. 1984 Aug 24;225(4664):840-2 PMID: 6206563
  5. Trans-acting transcriptional activation of the long terminal repeat of human T lymphotropic viruses in infected cells.
    Science. 1984 Jul 27;225(4660):381-5 PMID: 6330891
  6. Biology of feline leukemia virus in the natural environment.
    Cancer Res. 1976 Feb;36(2 pt 2):582-8 PMID: 175919
  7. Molecular basis of host range variation in avian retroviruses.
    J Virol. 1985 Jan;53(1):32-9 PMID: 2981357
  8. Horizontally and vertically transmitted oncornaviruses of cats.
    Adv Cancer Res. 1975;21:175-248 PMID: 174397
  9. Detection of the feline leukemia virus and other mammalian oncornaviruses by immunofluorescence.
    Bibl Haematol. 1973;39:778-99 PMID: 4360195
  10. Selective effect of feline leukaemia virus on early erythroid precursors.
    Nature. 1982 Mar 11;296(5853):156-8 PMID: 6278316
  11. Identification of regulatory sequences in the prelude sequences of an H2A histone gene by the study of specific deletion mutants in vivo.
    Proc Natl Acad Sci U S A. 1980 Mar;77(3):1432-6 PMID: 6929494
  12. Analysis of the env gene of a molecularly cloned and biologically active Moloney mink cell focus-forming proviral DNA.
    J Virol. 1982 Oct;44(1):19-31 PMID: 7143566
  13. An improved assay for feline leukaemia virus pseudotypes of murine sarcoma virus.
    J Gen Virol. 1976 Apr;31(1):139-43 PMID: 177726
  14. Molecular cloning and characterization of endogenous feline leukemia virus sequences from a cat genomic library.
    J Virol. 1983 Jun;46(3):829-40 PMID: 6304345
  15. Activation of SV40 genome by 72-base pair tandem repeats of Moloney sarcoma virus.
    Nature. 1982 Feb 18;295(5850):568-72 PMID: 6276775
  16. Simple, quantitative assay for both xenotropic murine leukemia and ecotropic feline leukemia viruses.
    J Virol. 1974 Jul;14(1):177-9 PMID: 4365331
  17. Human serum "parvovirus": a specific cause of aplastic crisis in children with hereditary spherocytosis.
    J Pediatr. 1983 May;102(5):720-2 PMID: 6842330
  18. Conformation of polypeptides and proteins.
    Adv Protein Chem. 1968;23:283-438 PMID: 4882249
  19. Rous sarcoma virus encodes a transcriptional activator.
    Cell. 1985 Mar;40(3):537-46 PMID: 2982497
  20. Infectious proviral DNA in human cells infected with transformation-defective type C viruses.
    Virology. 1976 Apr;70(2):301-12 PMID: 57665
  21. "Nonrandom" DNA sequence analysis in bacteriophage M13 by the dideoxy chain-termination method.
    Proc Natl Acad Sci U S A. 1982 Jul;79(14):4298-302 PMID: 6956859
  22. Nucleotide sequence of Moloney murine leukaemia virus.
    Nature. 1981 Oct 15-21;293(5833):543-8 PMID: 6169994
  23. Subgroup classification of feline leukemia and sarcoma viruses by viral interference and neutralization tests.
    Virology. 1973 Jul;54(1):160-9 PMID: 4351607
  24. Anemia associated with feline leukemia virus infection in cats.
    J Natl Cancer Inst. 1975 Jan;54(1):209-17 PMID: 163317
  25. Nucleotide sequences of the envelope genes of two isolates of feline leukemia virus subgroup B.
    J Virol. 1984 Feb;49(2):629-32 PMID: 6319767
  26. Location and function of retroviral and SV40 sequences that enhance biochemical transformation after microinjection of DNA.
    Cell. 1983 Jul;33(3):705-16 PMID: 6307525
  27. Nucleotide sequence of the Akv env gene.
    J Virol. 1982 May;42(2):519-29 PMID: 6283170
  28. Viral transduction of c-myc gene in naturally occurring feline leukaemias.
    Nature. 1984 Apr 26-May 2;308(5962):856-8 PMID: 6325922
  29. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  30. Biochemical evidence that MCF murine leukemia viruses are envelope (env) gene recombinants.
    Proc Natl Acad Sci U S A. 1977 Oct;74(10):4676-80 PMID: 200928
  31. Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma.
    J Cell Biol. 1975 Dec;67(3):835-51 PMID: 811671
  32. Cultivation in vitro of cells derived from a human rhabdomyosarcoma.
    Cancer. 1969 Sep;24(3):520-6 PMID: 4241949
  33. A unique sequence in murine leukemia virus long terminal repeat functions as a termination signal for transcription in Escherichia coli.
    J Virol. 1983 Jan;45(1):456-61 PMID: 6337268
  34. Interaction between feline leukaemia virus subgroups in the pathogenesis of erythroid hypoplasia.
    Int J Cancer. 1984 Aug 15;34(2):283-8 PMID: 6088406
  35. Sequence analysis of Gardner-Arnstein feline leukaemia virus envelope gene reveals common structural properties of mammalian retroviral envelope genes.
    EMBO J. 1983;2(12):2239-46 PMID: 6321156
  36. Subgenomic, cellular Rous sarcoma virus RNAs contain oligonucleotides from the 3' half and the 5' terminus of virion RNA.
    Nature. 1977 Dec 15;270(5638):631-4 PMID: 201866
  37. Immunosuppressive therapy of severe aplastic anemia.
    Prog Clin Biol Res. 1984;148:259-70 PMID: 6379664
  38. The frequency of occurrence of feline leukaemia virus subgroups in cats.
    Int J Cancer. 1978 Mar 15;21(3):334-7 PMID: 204584
  39. The family of human T-lymphotropic leukemia viruses: HTLV-I as the cause of adult T cell leukemia and HTLV-III as the cause of acquired immunodeficiency syndrome.
    Blood. 1985 Feb;65(2):253-63 PMID: 2981583
  40. Eukaryotic promoters?
    Nature. 1979 May 31;279(5712):376 PMID: 16068156
  41. Tissue-specific transcription preference as a determinant of cell tropism and leukaemogenic potential of murine retroviruses.
    Nature. 1984 Nov 8-14;312(5990):159-62 PMID: 6095084
  42. Nucleotide sequences of feline sarcoma virus long terminal repeats and 5' leaders show extensive homology to those of other mammalian retroviruses.
    J Virol. 1983 Jan;45(1):466-72 PMID: 6296453
  43. Sequence arrangement and biological activity of cloned feline leukemia virus proviruses from a virus-productive human cell line.
    J Virol. 1981 May;38(2):688-703 PMID: 6264136
  44. Tumorigenic transformation of mammalian cells induced by a normal human gene homologous to the oncogene of Harvey murine sarcoma virus.
    Nature. 1982 Jun 10;297(5866):479-83 PMID: 6283358
  45. Characterization and mapping of RNase T1-resistant oligonucleotides derived from the genomes of Akv and MCF murine leukemia viruses.
    Proc Natl Acad Sci U S A. 1978 Jan;75(1):495-9 PMID: 203942
  46. The occurrence of feline leukaemia virus neutralizing antibodies in cats.
    Int J Cancer. 1978 Sep 15;22(3):351-7 PMID: 212375
  47. Horizontal transmission of feline leukemia virus under experimental conditions.
    J Natl Cancer Inst. 1977 Feb;58(2):443-4 PMID: 189052
  48. Primary structure of glycoprotein glycans: basis for the molecular biology of glycoproteins.
    Adv Carbohydr Chem Biochem. 1980;37:157-223 PMID: 6996449
  49. The presence of disulfide-linked gp70-p15(E) complexes in AKR murine leukemia virus.
    Virology. 1977 Dec;83(2):417-22 PMID: 201090
  50. Haemopoietic colony formation (BFU-E, GM-CFC) during the development of pure red cell hypoplasia induced in the cat by feline leukaemia virus.
    Leuk Res. 1983;7(2):103-16 PMID: 6304428
  51. Promoter sequences of eukaryotic protein-coding genes.
    Science. 1980 Sep 19;209(4463):1406-14 PMID: 6251548
  52. Sequence at the 3' end of globin mRNA shows homology with immunoglobulin light chain mRNA.
    Nature. 1974 Nov 29;252(5482):359-62 PMID: 4139664
  53. Feline glucose-6-phosphate dehydrogenase cellular mosaicism. Application to the study of retrovirus-induced pure red cell aplasia.
    J Clin Invest. 1985 Jan;75(1):133-40 PMID: 2981248
  54. Erythroid hypoplasia in cats inoculated with feline leukemia virus.
    J Natl Cancer Inst. 1974 Nov;53(5):1271-6 PMID: 4372379
  55. Moloney murine sarcoma proviral DNA is a transcriptional unit.
    Nature. 1980 Dec 25;288(5792):665-9 PMID: 6256637
  56. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis.
    Gene. 1983 Dec;26(1):101-6 PMID: 6323249
  57. Cellular origin and role of mink cell focus-forming viruses in murine thymic lymphomas.
    Nature. 1982 Jan 7;295(5844):25-31 PMID: 6276750
  58. Modifications of the immunofluorescence assay for feline leukemia virus group-specific antigens.
    Am J Vet Res. 1978 Dec;39(12):1877-80 PMID: 219732
  59. Nucleotide sequence of the envelope gene of Gardner-Arnstein feline leukemia virus B reveals unique sequence homologies with a murine mink cell focus-forming virus.
    J Virol. 1983 Jun;46(3):871-80 PMID: 6304347
  60. Disease-specific and tissue-specific production of unintegrated feline leukaemia virus variant DNA in feline AIDS.
    Nature. 1986 Jan 23-29;319(6051):333-6 PMID: 3001539
  61. Feline leukemia virus-induced erythroid aplasia: in vitro hemopoietic culture studies.
    Exp Hematol. 1981 Nov;9(10):990-1001 PMID: 6273200
  62. Detection, isolation, and continuous production of cytopathic retroviruses (HTLV-III) from patients with AIDS and pre-AIDS.
    Science. 1984 May 4;224(4648):497-500 PMID: 6200935
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1986-10-00
Pages
242-50
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC253922
Subset
IM
Grants
NCI NIH HHS · CA32563 · United States
Databases
GENBANK
M14331
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