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Journal of Virology, March 2002, p. 2363-2374, Vol. 76, No. 5
0022-538X/02/$04.00+0     DOI: 10.1128/jvi.76.5.2363-2374.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Disruption of Hematopoiesis and Thymopoiesis in the Early Premalignant Stages of Infection with SL3-3 Murine Leukemia Virus

*** Karen Rulli,1 Jack Lenz,2 and Laura S. Levy1*

Department of Microbiology and Immunology, Program in Molecular Pathogenesis and Immunity, Program in Molecular and Cellular Biology, and Tulane Cancer Center, Tulane University Health Sciences Center, New Orleans, Louisiana 70112,1 Department of Molecular Genetics, Albert Einstein School of Medicine, Bronx, New York 104612

Received 6 August 2001/ Accepted 27 November 2001

A time course analysis of SL3-3 murine leukemia virus (SL3) infection in thymus and bone marrow of NIH/Swiss mice was performed to assess changes that occur during the early stages of progression to lymphoma. Virus was detectable in thymocytes, bone marrow, and spleen as early as 1 to 2 weeks postinoculation (p.i.). In bone marrow, virus infection was detected predominantly in immature myeloid or granulocytic cells. Flow cytometry revealed significant reductions of the Ter-119+ and Mac-1+ populations, and significant expansions of the Gr-1+ and CD34+ populations, between 2 and 4 weeks p.i. Analysis of colony-forming potential confirmed these findings. In the thymus, SL3 replication was associated with significant disruption in thymocyte subpopulation distribution between 4 and 7 weeks p.i. A significant thymic regression was observed just prior to the clonal outgrowth of tumor cells. Proviral long terminal repeats (LTRs) with increasing numbers of enhancer repeats were observed to accumulate exclusively in the thymus during the first 8 weeks p.i. Observations were compared to the early stages of infection with a virtually nonpathogenic SL3 mutant, termed SL3{Delta}Myb5, which was shown by real-time PCR to be replication competent. Comparison of SL3 with SL3{Delta}Myb5 implicated certain premalignant changes in tumorigenesis, including (i) increased proportions of Gr-1+ and CD34+ bone marrow progenitors, (ii) a significant increase in the proportion of CD4- CD8- thymocytes, (iii) thymic regression prior to tumor outgrowth, and (iv) accumulation of LTR enhancer variants. A model in which disrupted bone marrow hematopoiesis and thymopoiesis contribute to the development of lymphoma in the SL3-infected animal is discussed.

* Corresponding author. Mailing address: Department of Microbiology and Immunology, Tulane University School of Medicine, 1430 Tulane Ave. SL-38, New Orleans, LA 70112. Phone: (504) 587-2083. Fax: (504) 588-5144. E-mail: llevy{at}tulane.edu.

Journal of Virology, March 2002, p. 2363-2374, Vol. 76, No. 5
0022-538X/02/$04.00+0     DOI: 10.1128/jvi.76.5.2363-2374.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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