Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1992 Sep;66(9):5561–5568. doi: 10.1128/jvi.66.9.5561-5568.1992

Hematopoietic target cells of anemogenic subgroup C versus nonanemogenic subgroup A feline leukemia virus.

G A Dean 1, P M Groshek 1, J I Mullins 1, E A Hoover 1
PMCID: PMC289115  PMID: 1323710

Abstract

Feline leukemia viruses (FeLVs) belonging to interference subgroup C induce fatal anemia resembling human pure red cell aplasia (PRCA). Subgroup A FeLVs, although closely related genetically to FeLVs of subgroup C, do not induce PRCA. The determinants for PRCA induction by a molecularly cloned prototype subgroup C virus (FeLV-Sarma-C [FSC]) have been localized to the N-terminal 241 amino acids of the surface glycoprotein (SU) gp70. To investigate whether the anemogenic activity of FSC reflects a unique capacity to infect erythroid progenitor cells, we used correlative immunogold, immunofluorescence, and cytological staining to study prospectively the hemopoietic cell populations infected by either FSC or FeLV-FAIDS-61E-A (F6A), a prototype of subgroup A virus. The results demonstrated that although only FSC-infected animals developed erythrocyte aplasia, the env SU and the major core protein (p27) were expressed in a surprisingly large fraction of the lymphoid, erythroid, and myeloid lineage marrow cells in both FSC- and F6A-infected cats. Between days 8 and 17 postinoculation, gp70 and p27 were detected in 43 to 73% of erythroid, 25 to 75% of lymphoid, and 35 to 50% of myeloid lineage cells, regardless of whether the cats were infected with FSC or F6A. Thus, anemogenic subgroup C and nonanemogenic subgroup A FeLVs have similar hemopoietic cell tropism and infection kinetics, despite their divergent effects on erythroid progenitor cell function. Acute anemia induction by subgroup C FeLV, therefore, does not reflect a unique tropism for marrow erythroid cells but rather indicates a unique cytopathic effect of the SU on erythroid progenitor cells.

Full text

PDF
5561

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abkowitz J. L., Holly R. D., Grant C. K. Retrovirus-induced feline pure red cell aplasia. Hematopoietic progenitors are infected with feline leukemia virus and erythroid burst-forming cells are uniquely sensitive to heterologous complement. J Clin Invest. 1987 Oct;80(4):1056–1063. doi: 10.1172/JCI113160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Abkowitz J. L., Ott R. L., Holly R. D., Adamson J. W. Lymphocytes and antibody in retrovirus-induced feline pure red cell aplasia. J Natl Cancer Inst. 1987 Jan;78(1):135–139. doi: 10.1093/jnci/78.1.135. [DOI] [PubMed] [Google Scholar]
  3. Abkowitz J. L., Ott R. L., Nakamura J. M., Steinmann L., Fialkow P. J., Adamson J. W. 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):133–140. doi: 10.1172/JCI111665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Abkowitz J. L. Retrovirus-induced feline pure red blood cell aplasia: pathogenesis and response to suramin. Blood. 1991 Apr 1;77(7):1442–1451. [PubMed] [Google Scholar]
  5. Chesebro B., Portis J. L., Wehrly K., Nishio J. Effect of murine host genotype on MCF virus expression, latency, and leukemia cell type of leukemias induced by Friend murine leukemia helper virus. Virology. 1983 Jul 15;128(1):221–233. doi: 10.1016/0042-6822(83)90332-x. [DOI] [PubMed] [Google Scholar]
  6. Costello C. Haematological abnormalities in human immunodeficiency virus (HIV) disease. J Clin Pathol. 1988 Jul;41(7):711–715. doi: 10.1136/jcp.41.7.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Donahue P. R., Hoover E. A., Beltz G. A., Riedel N., Hirsch V. M., Overbaugh J., Mullins J. I. Strong sequence conservation among horizontally transmissible, minimally pathogenic feline leukemia viruses. J Virol. 1988 Mar;62(3):722–731. doi: 10.1128/jvi.62.3.722-731.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Donahue R. E., Johnson M. M., Zon L. I., Clark S. C., Groopman J. E. Suppression of in vitro haematopoiesis following human immunodeficiency virus infection. Nature. 1987 Mar 12;326(6109):200–203. doi: 10.1038/326200a0. [DOI] [PubMed] [Google Scholar]
  9. Fischinger P. J., Blevins C. S., Nomura S. Simple, quantitative assay for both xenotropic murine leukemia and ecotropic feline leukemia viruses. J Virol. 1974 Jul;14(1):177–179. doi: 10.1128/jvi.14.1.177-179.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Folks T. M., Kessler S. W., Orenstein J. M., Justement J. S., Jaffe E. S., Fauci A. S. Infection and replication of HIV-1 in purified progenitor cells of normal human bone marrow. Science. 1988 Nov 11;242(4880):919–922. doi: 10.1126/science.2460922. [DOI] [PubMed] [Google Scholar]
  11. Ghosh A. K., Bachmann M. H., Hoover E. A., Mullins J. I. Identification of a putative receptor for subgroup A feline leukemia virus on feline T cells. J Virol. 1992 Jun;66(6):3707–3714. doi: 10.1128/jvi.66.6.3707-3714.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Grant C. K., Ernisse B. J., Jarrett O., Jones F. R. Feline leukemia virus envelope gp70 of subgroups B and C defined by monoclonal antibodies with cytotoxic and neutralizing functions. J Immunol. 1983 Dec;131(6):3042–3048. [PubMed] [Google Scholar]
  13. Hardy W. D., Jr, Hess P. W., MacEwen E. G., McClelland A. J., Zuckerman E. E., Essex M., Cotter S. M., Jarrett O. Biology of feline leukemia virus in the natural environment. Cancer Res. 1976 Feb;36(2 Pt 2):582–588. [PubMed] [Google Scholar]
  14. Hoover E. A., Kociba G. J., Hardy W. D., Jr, Yohn D. S. Erythroid hypoplasia in cats inoculated with feline leukemia virus. J Natl Cancer Inst. 1974 Nov;53(5):1271–1276. doi: 10.1093/jnci/53.5.1271. [DOI] [PubMed] [Google Scholar]
  15. ISHII S. EQUINE INFECTIOUS ANEMIA OR SWAMP FEVER. Adv Vet Sci. 1963;8:263–298. [PubMed] [Google Scholar]
  16. Jarrett O., Golder M. C., Toth S., Onions D. E., Stewart M. F. Interaction between feline leukaemia virus subgroups in the pathogenesis of erythroid hypoplasia. Int J Cancer. 1984 Aug 15;34(2):283–288. doi: 10.1002/ijc.2910340222. [DOI] [PubMed] [Google Scholar]
  17. Jarrett O., Laird H. M., Hay D. Determinants of the host range of feline leukaemia viruses. J Gen Virol. 1973 Aug;20(2):169–175. doi: 10.1099/0022-1317-20-2-169. [DOI] [PubMed] [Google Scholar]
  18. Johnson C. S., Marcelletti J., Longley C., Furmanski P. Inhibition of normal erythropoiesis in mice with Friend virus induced erythroleukemia. Exp Hematol. 1982 Oct;10(9):743–753. [PubMed] [Google Scholar]
  19. Kociba G. J., Lange R. D., Dunn C. D., Hoover E. A. Serum erythropoietin changes in cats with feline leukemia virus-induced erythroid aplasia. Vet Pathol. 1983 Sep;20(5):548–552. doi: 10.1177/030098588302000506. [DOI] [PubMed] [Google Scholar]
  20. Leiderman I. Z., Greenberg M. L., Adelsberg B. R., Siegal F. P. A glycoprotein inhibitor of in vitro granulopoiesis associated with AIDS. Blood. 1987 Nov;70(5):1267–1272. [PubMed] [Google Scholar]
  21. Lunardi-Iskandar Y., Nugeyre M. T., Georgoulias V., Barré-Sinoussi F., Jasmin C., Chermann J. C. Replication of the human immunodeficiency virus 1 and impaired differentiation of T cells after in vitro infection of bone marrow immature T cells. J Clin Invest. 1989 Feb;83(2):610–615. doi: 10.1172/JCI113924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lutz H., Pedersen N. C., Durbin R., Theilen G. H. Monoclonal antibodies to three epitopic regions of feline leukemia virus p27 and their use in enzyme-linked immunosorbent assay of p27. J Immunol Methods. 1983 Jan 28;56(2):209–220. doi: 10.1016/0022-1759(83)90413-1. [DOI] [PubMed] [Google Scholar]
  23. McElrath M. J., Pruett J. E., Cohn Z. A. Mononuclear phagocytes of blood and bone marrow: comparative roles as viral reservoirs in human immunodeficiency virus type 1 infections. Proc Natl Acad Sci U S A. 1989 Jan;86(2):675–679. doi: 10.1073/pnas.86.2.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Oliff A., Ruscetti S., Douglass E. C., Scolnick E. Isolation of transplantable erythroleukemia cells from mice infected with helper-independent Friend murine leukemia virus. Blood. 1981 Aug;58(2):244–254. [PubMed] [Google Scholar]
  25. Onions D., Jarrett O., Testa N., Frassoni F., Toth S. Selective effect of feline leukaemia virus on early erythroid precursors. Nature. 1982 Mar 11;296(5853):156–158. doi: 10.1038/296156a0. [DOI] [PubMed] [Google Scholar]
  26. Overbaugh J., Donahue P. R., Quackenbush S. L., Hoover E. A., Mullins J. I. Molecular cloning of a feline leukemia virus that induces fatal immunodeficiency disease in cats. Science. 1988 Feb 19;239(4842):906–910. doi: 10.1126/science.2893454. [DOI] [PubMed] [Google Scholar]
  27. Perkocha L. A., Rodgers G. M. Hematologic aspects of human immunodeficiency virus infection: laboratory and clinical considerations. Am J Hematol. 1988 Oct;29(2):94–105. doi: 10.1002/ajh.2830290207. [DOI] [PubMed] [Google Scholar]
  28. Riedel N., Hoover E. A., Dornsife R. E., Mullins J. I. Pathogenic and host range determinants of the feline aplastic anemia retrovirus. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2758–2762. doi: 10.1073/pnas.85.8.2758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Riedel N., Hoover E. A., Gasper P. W., Nicolson M. O., Mullins J. I. Molecular analysis and pathogenesis of the feline aplastic anemia retrovirus, feline leukemia virus C-Sarma. J Virol. 1986 Oct;60(1):242–250. doi: 10.1128/jvi.60.1.242-250.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sakaguchi M., Sato T., Groopman J. E. Human immunodeficiency virus infection of megakaryocytic cells. Blood. 1991 Feb 1;77(3):481–485. [PubMed] [Google Scholar]
  31. Sarma P. S., Jain D., Hill P. R. In vitro host range of feline leukemia virus. Bibl Haematol. 1975;(40):489–492. doi: 10.1159/000397566. [DOI] [PubMed] [Google Scholar]
  32. Sarma P. S., Log T. Subgroup classification of feline leukemia and sarcoma viruses by viral interference and neutralization tests. Virology. 1973 Jul;54(1):160–169. doi: 10.1016/0042-6822(73)90125-6. [DOI] [PubMed] [Google Scholar]
  33. Sitbon M., Evans L., Nishio J., Wehrly K., Chesebro B. Analysis of two strains of Friend murine leukemia viruses differing in ability to induce early splenomegaly: lack of relationship with generation of recombinant mink cell focus-forming viruses. J Virol. 1986 Jan;57(1):389–393. doi: 10.1128/jvi.57.1.389-393.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sitbon M., Sola B., Evans L., Nishio J., Hayes S. F., Nathanson K., Garon C. F., Chesebro B. Hemolytic anemia and erythroleukemia, two distinct pathogenic effects of Friend MuLV: mapping of the effects to different regions of the viral genome. Cell. 1986 Dec 26;47(6):851–859. doi: 10.1016/0092-8674(86)90800-7. [DOI] [PubMed] [Google Scholar]
  35. Steinberg H. N., Crumpacker C. S., Chatis P. A. In vitro suppression of normal human bone marrow progenitor cells by human immunodeficiency virus. J Virol. 1991 Apr;65(4):1765–1769. doi: 10.1128/jvi.65.4.1765-1769.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Stoler M. H., Eskin T. A., Benn S., Angerer R. C., Angerer L. M. Human T-cell lymphotropic virus type III infection of the central nervous system. A preliminary in situ analysis. JAMA. 1986 Nov 7;256(17):2360–2364. [PubMed] [Google Scholar]
  37. Takeuchi Y., Vile R. G., Simpson G., O'Hara B., Collins M. K., Weiss R. A. Feline leukemia virus subgroup B uses the same cell surface receptor as gibbon ape leukemia virus. J Virol. 1992 Feb;66(2):1219–1222. doi: 10.1128/jvi.66.2.1219-1222.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Watanabe M., Ringler D. J., Nakamura M., DeLong P. A., Letvin N. L. Simian immunodeficiency virus inhibits bone marrow hematopoietic progenitor cell growth. J Virol. 1990 Feb;64(2):656–663. doi: 10.1128/jvi.64.2.656-663.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zon L. I., Arkin C., Groopman J. E. Haematologic manifestations of the human immune deficiency virus (HIV). Br J Haematol. 1987 Jun;66(2):251–256. doi: 10.1111/j.1365-2141.1987.tb01307.x. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES