Abstract
Conditioned medium from a culture of whole human embryo cells stimulated prolonged exponential growth in suspension culture of leukocytes from a patient with acute myelogenous leukemia. Ten to 20% of the cultured cells consistently differentiated into mature granulocytes including neutrophils, eosinophils, and basophils. The proportion of lymphocytes declined after culturing, and tests for Epstein-Barr virus antigens were negative. An abnormality of a G group chromosome was observed in some metaphases from the patient's fresh bone marrow and from the cultured leukocytes, indicating growth in vitro of leukemic cells. After 4-10 weeks in culture, a budding type-C virus was continuously released by the cultured leukocytes, predominantly by undifferentiated blast cells. This virus was originally identified in three different cultures of a peripheral blood specimen obtained at the time of diagnosis. Subsequently, this virus was identified by reverse transcriptase (RNA-dependent DNA polymerase) assays and by electron microscopy in cultured leukocytes from a bone marrow specimen obtained 14 months later from the same patient. Virus produced by cultures of both specimens was closely related, if not identical, to the woolly monkey type-C virus.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Aaronson S. A., Hartley J. W., Todaro G. J. Mouse leukemia virus: "spontaneous" release by mouse embryo cells after long-term in vitro cultivation. Proc Natl Acad Sci U S A. 1969 Sep;64(1):87–94. doi: 10.1073/pnas.64.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aye M. T., Till J. E., McCulloch E. A. Growth of leukemic cells in culture. Blood. 1972 Dec;40(6):806–811. [PubMed] [Google Scholar]
- Barak Y., Shore N. A., Higgins G. R., Vadakan V. V. Functional cellular maturation in cultures of human haematopoietic cells. Br J Haematol. 1974 Aug;27(4):543–549. doi: 10.1111/j.1365-2141.1974.tb06619.x. [DOI] [PubMed] [Google Scholar]
- Baxt W., Hehlmann R., Spiegelman S. Human leukaemic cells contain reverse transcriptase associated with a high molecular weight virus-related RNA. Nat New Biol. 1972 Nov 15;240(98):72–75. doi: 10.1038/newbio240072a0. [DOI] [PubMed] [Google Scholar]
- Bradley T. R., Metcalf D. The growth of mouse bone marrow cells in vitro. Aust J Exp Biol Med Sci. 1966 Jun;44(3):287–299. doi: 10.1038/icb.1966.28. [DOI] [PubMed] [Google Scholar]
- Brown C. H., 3rd, Carbone P. P. In vitro growth of normal and leukemic human bone marrow. J Natl Cancer Inst. 1971 May;46(5):989–1000. [PubMed] [Google Scholar]
- Chervenick P. A., Boggs D. R. Bone marrow colonies: stimulation in vitro by supernatant from incubated human blood cells. Science. 1970 Aug 14;169(3946):691–692. doi: 10.1126/science.169.3946.691. [DOI] [PubMed] [Google Scholar]
- Clarkson B., Strife A., De Harven E. Continuous culture of seven new cell lines (SK-L1 to 7) from patients with acute leukemia. Cancer. 1967 Jun;20(6):926–947. doi: 10.1002/1097-0142(196706)20:6<926::aid-cncr2820200603>3.0.co;2-4. [DOI] [PubMed] [Google Scholar]
- Gabelman N., Waxman S., Smith W., Douglas S. D. Appearance of C-type virus-like particles after co-cultivation of a human tumor-cell line with rat (XC) cells. Int J Cancer. 1975 Sep 15;16(3):355–369. doi: 10.1002/ijc.2910160302. [DOI] [PubMed] [Google Scholar]
- Gallagher R. E., Gallo R. C. Type C RNA tumor virus isolated from cultured human acute myelogenous leukemia cells. Science. 1975 Jan 31;187(4174):350–353. doi: 10.1126/science.46123. [DOI] [PubMed] [Google Scholar]
- Gallagher R. E., Todaro G. J., Smith R. G., Livingston D. M., Gallo R. C. Relationship between RNA-directed DNA polymerase (reverse transcriptase) from human acute leukemic blood cells and primate type-C viruses. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1309–1313. doi: 10.1073/pnas.71.4.1309. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gallo R. C., Gallagher R. E., Miller N. R., Mondal H., Saxinger W. C., Mayer R. J., Smith R. G., Gillespie D. H. Relationships between components in primate RNA tumor viruses and in the cytoplasm of human leukemic cells: implications to leukemogenesis. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):933–961. doi: 10.1101/sqb.1974.039.01.109. [DOI] [PubMed] [Google Scholar]
- Gallo R. C., Miller N. R., Saxinger W. C., Gillespie D. Primate RNA tumor virus-like DNA synthesized endogenously by RNA-dependent DNA polymerase in virus-like particles from fresh human acute leukemic blood cells. Proc Natl Acad Sci U S A. 1973 Nov;70(11):3219–3224. doi: 10.1073/pnas.70.11.3219. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gallo R. C., Yang S. S., Ting R. C. RNA dependent DNA polymerase of human acute leukaemic cells. Nature. 1970 Dec 5;228(5275):927–929. doi: 10.1038/228927a0. [DOI] [PubMed] [Google Scholar]
- Golde D. W., Byers L. A., Cline M. J. Chronic myelogenous leukemia cell growth and maturation in liquid culture. Cancer Res. 1974 Feb;34(2):419–423. [PubMed] [Google Scholar]
- Golde D. W., Cline M. J. Regulation of granulopoiesis. N Engl J Med. 1974 Dec 26;291(26):1388–1395. doi: 10.1056/NEJM197412262912606. [DOI] [PubMed] [Google Scholar]
- Gross L. Facts and theories on viruses causing cancer and leukemia. Proc Natl Acad Sci U S A. 1974 May;71(5):2013–2017. doi: 10.1073/pnas.71.5.2013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kawakami T. G., Huff S. D., Buckley P. M., Dungworth D. L., Synder S. P., Gilden R. V. C-type virus associated with gibbon lymphosarcoma. Nat New Biol. 1972 Feb 9;235(58):170–171. doi: 10.1038/newbio235170a0. [DOI] [PubMed] [Google Scholar]
- Kotler M., Weinberg E., Haspel O., Olshevsky U., Becker Y. Particles released from arginine deprived human leukaemic cells. Nat New Biol. 1973 Aug 15;244(137):197–200. doi: 10.1038/newbio244197a0. [DOI] [PubMed] [Google Scholar]
- Levine E. M. Mycoplasma contamination of animal cell cultures: a simple, rapid detection method. Exp Cell Res. 1972 Sep;74(1):99–109. doi: 10.1016/0014-4827(72)90484-3. [DOI] [PubMed] [Google Scholar]
- Lowy D. R., Rowe W. P., Teich N., Hartley J. W. Murine leukemia virus: high-frequency activation in vitro by 5-iododeoxyuridine and 5-bromodeoxyuridine. Science. 1971 Oct 8;174(4005):155–156. doi: 10.1126/science.174.4005.155. [DOI] [PubMed] [Google Scholar]
- Lozzio C. B., Lozzio B. B. Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome. Blood. 1975 Mar;45(3):321–334. [PubMed] [Google Scholar]
- Mak T. W., Kurtz S., Manaster J., Housman D. Viral-related information in oncornavirus-lik particles isolated from cultures of marrow cells from leukemic patients in relapse and remission. Proc Natl Acad Sci U S A. 1975 Feb;72(2):623–627. doi: 10.1073/pnas.72.2.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mak T. W., Manaster J., Howatson A. F., McCulloch E. A., Till J. E. Particles with characteristics of leukoviruses in cultures of marrow cells from leukemic patients in remission and relapse. Proc Natl Acad Sci U S A. 1974 Nov;71(11):4336–4340. doi: 10.1073/pnas.71.11.4336. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McCulloch E. A., Mak T. W., Price G. B., Till J. E. Organization and communication in populations of normal and leukemic hemopoietic cells. Biochim Biophys Acta. 1974 Dec 31;355(3-4):260–299. doi: 10.1016/0304-419x(74)90013-4. [DOI] [PubMed] [Google Scholar]
- Mondal H., Gallagher R. E., Gallo R. C. RNA-directed DNA polymerase from human leukemic blood cells and from primate type-C virus-producing cells: high- and low-molecular-weight forms with variant biochemical and immunological properties. Proc Natl Acad Sci U S A. 1975 Mar;72(3):1194–1198. doi: 10.1073/pnas.72.3.1194. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moore M. A., Spitzer G., Williams N., Metcalf D., Buckley J. Agar culture studies in 127 cases of untreated acute leukemia: the prognostic value of reclassification of leukemia according to in vitro growth characteristics. Blood. 1974 Jul;44(1):1–18. [PubMed] [Google Scholar]
- Morley A., Higgs D. Lack of increased differentiation of leukemic cells in response to colony-stimulating factor. Cancer Res. 1974 Sep;34(9):2307–2310. [PubMed] [Google Scholar]
- Nooter K., Aarssen A. M., Bentvelzen P., De Groot F. G., Van Pelt F. G. Isolation of infectious C-type oncornavirus from human leukaemic bone marrow cells. Nature. 1975 Aug 14;256(5518):595–597. doi: 10.1038/256595a0. [DOI] [PubMed] [Google Scholar]
- Panem S., Prochownik E. V., Reale F. R., Kirsten W. H. Isolation of type C virions from a normal human fibroblast strain. Science. 1975 Jul 25;189(4199):297–299. doi: 10.1126/science.49927. [DOI] [PubMed] [Google Scholar]
- Paran M., Sachs L., Barak Y., Resnitzky P. In vitro induction of granulocyte differentiation in hematopoietic cells from leukemic and non-leukemic patients. Proc Natl Acad Sci U S A. 1970 Nov;67(3):1542–1549. doi: 10.1073/pnas.67.3.1542. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pluznik D. H., Sachs L. The induction of clones of normal mast cells by a substance from conditioned medium. Exp Cell Res. 1966 Oct;43(3):553–563. doi: 10.1016/0014-4827(66)90026-7. [DOI] [PubMed] [Google Scholar]
- Price G. B., Senn J. S., McCulloch E. A., Till J. E. Heterogeneity of molecules with low molecular weight isolated from media conditioned by human leukocytes and capable of stimulating colony formation by human granulopoietic progenitor cells. J Cell Physiol. 1974 Dec;84(3):383–396. doi: 10.1002/jcp.1040840307. [DOI] [PubMed] [Google Scholar]
- Prival J. T., Paran M., Gallo R. C., Wu A. M. Colony-stimulating factors in cultures of human peripheral blood cells. J Natl Cancer Inst. 1974 Dec;53(6):1583–1588. [PubMed] [Google Scholar]
- Reedman B. M., Klein G. Cellular localization of an Epstein-Barr virus (EBV)-associated complement-fixing antigen in producer and non-producer lymphoblastoid cell lines. Int J Cancer. 1973 May;11(3):499–520. doi: 10.1002/ijc.2910110302. [DOI] [PubMed] [Google Scholar]
- Robinson W. A., Kurnick J. E., Pike B. L. Colony growth of human leukemic peripheral blood cells in vitro. Blood. 1971 Oct;38(4):500–508. [PubMed] [Google Scholar]
- Sherr C. J., Todaro G. J. Primate type C virus p30 antigen in cells from humans with acute leukemia. Science. 1975 Mar 7;187(4179):855–857. doi: 10.1126/science.163489. [DOI] [PubMed] [Google Scholar]
- Shevach E. M., Jaffe E. S., Green I. Receptors for complement and immunoglobulin on human and animal lymphoid cells. Transplant Rev. 1973;16:3–28. doi: 10.1111/j.1600-065x.1973.tb00115.x. [DOI] [PubMed] [Google Scholar]
- Teich N. M., Weiss R. A., Salahuddin S. Z., Gallagher R. E., Gillespie D. H., Gallo R. C. Infective transmission and characterisation of a C-type virus released by cultured human myeloid leukaemia cells. Nature. 1975 Aug 14;256(5518):551–555. doi: 10.1038/256551a0. [DOI] [PubMed] [Google Scholar]
- Todaro G. J., Gallo R. C. Immunological relationship of DNA polymerase from human acute leukaemia cells and primate and mouse leukaemia virus reverse transcriptase. Nature. 1973 Jul 27;244(5413):206–209. doi: 10.1038/244206a0. [DOI] [PubMed] [Google Scholar]
- Wolfe L. G., Deinhardt F., Theilen G. H., Rabin H., Kawakami T., Bustad L. K. Induction of tumors in marmoset monkeys by simian sarcoma virus, type 1 (Lagothrix): a preliminary report. J Natl Cancer Inst. 1971 Nov;47(5):1115–1120. [PubMed] [Google Scholar]