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. 1991 May;65(5):2732–2735. doi: 10.1128/jvi.65.5.2732-2735.1991

Differentiation of human embryonal carcinoma cells induces human immunodeficiency virus permissiveness which is stimulated by human cytomegalovirus coinfection.

G Hirka 1, K Prakash 1, H Kawashima 1, S A Plotkin 1, P W Andrews 1, E Gönczöl 1
PMCID: PMC240639  PMID: 1850047

Abstract

Human immunodeficiency virus (HIV) replicates in differentiated but not undifferentiated NTERA-2 human embryonal carcinoma cells; neither cell type expresses CD4. Susceptibility of the differentiated cells is enhanced by coinfection with cytomegalovirus. HIV infection induces lactoseries glycolipids, suggesting a mechanism whereby HIV might interfere with normal embryogenesis.

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Selected References

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  1. Adachi A., Koenig S., Gendelman H. E., Daugherty D., Gattoni-Celli S., Fauci A. S., Martin M. A. Productive, persistent infection of human colorectal cell lines with human immunodeficiency virus. J Virol. 1987 Jan;61(1):209–213. doi: 10.1128/jvi.61.1.209-213.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adachi M., Hayami M., Kashiwagi N., Mizuta T., Ohta Y., Gill M. J., Matheson D. S., Tamaoki T., Shiozawa C., Hakomori S. Expression of Ley antigen in human immunodeficiency virus-infected human T cell lines and in peripheral lymphocytes of patients with acquired immune deficiency syndrome (AIDS) and AIDS-related complex (ARC). J Exp Med. 1988 Feb 1;167(2):323–331. doi: 10.1084/jem.167.2.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Andrews P. W., Damjanov I., Simon D., Banting G. S., Carlin C., Dracopoli N. C., Føgh J. Pluripotent embryonal carcinoma clones derived from the human teratocarcinoma cell line Tera-2. Differentiation in vivo and in vitro. Lab Invest. 1984 Feb;50(2):147–162. [PubMed] [Google Scholar]
  4. Andrews P. W., Gönczöl E., Fenderson B. A., Holmes E. H., O'Malley G., Hakomori S., Plotkin S. Human cytomegalovirus induces stage-specific embryonic antigen 1 in differentiating human teratocarcinoma cells and fibroblasts. J Exp Med. 1989 Apr 1;169(4):1347–1359. doi: 10.1084/jem.169.4.1347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Andrews P. W., Gönczöl E., Plotkin S. A., Dignazio M., Oosterhuis J. W. Differentiation of TERA-2 human embryonal carcinoma cells into neurons and HCMV permissive cells. Induction by agents other than retinoic acid. Differentiation. 1986;31(2):119–126. doi: 10.1111/j.1432-0436.1986.tb00392.x. [DOI] [PubMed] [Google Scholar]
  6. Andrews P. W. Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev Biol. 1984 Jun;103(2):285–293. doi: 10.1016/0012-1606(84)90316-6. [DOI] [PubMed] [Google Scholar]
  7. Belman A. L., Diamond G., Dickson D., Horoupian D., Llena J., Lantos G., Rubinstein A. Pediatric acquired immunodeficiency syndrome. Neurologic syndromes. Am J Dis Child. 1988 Jan;142(1):29–35. doi: 10.1001/archpedi.1988.02150010039017. [DOI] [PubMed] [Google Scholar]
  8. Bird J. M., Kimber S. J. Oligosaccharides containing fucose linked alpha(1-3) and alpha(1-4) to N-acetylglucosamine cause decompaction of mouse morulae. Dev Biol. 1984 Aug;104(2):449–460. doi: 10.1016/0012-1606(84)90101-5. [DOI] [PubMed] [Google Scholar]
  9. Blanche S., Rouzioux C., Moscato M. L., Veber F., Mayaux M. J., Jacomet C., Tricoire J., Deville A., Vial M., Firtion G. A prospective study of infants born to women seropositive for human immunodeficiency virus type 1. HIV Infection in Newborns French Collaborative Study Group. N Engl J Med. 1989 Jun 22;320(25):1643–1648. doi: 10.1056/NEJM198906223202502. [DOI] [PubMed] [Google Scholar]
  10. Blin N., Stafford D. W. A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res. 1976 Sep;3(9):2303–2308. doi: 10.1093/nar/3.9.2303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Calvani M. HIV embryopathy and neurocristopathies. Am J Dis Child. 1988 Jan;142(1):10–11. doi: 10.1001/archpedi.1988.02150010016003. [DOI] [PubMed] [Google Scholar]
  12. Casareale D., Fiala M., Chang C. M., Cone L. A., Mocarski E. S. Cytomegalovirus enhances lysis of HIV-infected T lymphoblasts. Int J Cancer. 1989 Jul 15;44(1):124–130. doi: 10.1002/ijc.2910440122. [DOI] [PubMed] [Google Scholar]
  13. Cheng-Mayer C., Rutka J. T., Rosenblum M. L., McHugh T., Stites D. P., Levy J. A. Human immunodeficiency virus can productively infect cultured human glial cells. Proc Natl Acad Sci U S A. 1987 May;84(10):3526–3530. doi: 10.1073/pnas.84.10.3526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Clapham P. R., Weber J. N., Whitby D., McIntosh K., Dalgleish A. G., Maddon P. J., Deen K. C., Sweet R. W., Weiss R. A. Soluble CD4 blocks the infectivity of diverse strains of HIV and SIV for T cells and monocytes but not for brain and muscle cells. Nature. 1989 Jan 26;337(6205):368–370. doi: 10.1038/337368a0. [DOI] [PubMed] [Google Scholar]
  15. Dalgleish A. G., Beverley P. C., Clapham P. R., Crawford D. H., Greaves M. F., Weiss R. A. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature. 1984 Dec 20;312(5996):763–767. doi: 10.1038/312763a0. [DOI] [PubMed] [Google Scholar]
  16. Damjanov I., Solter D. Experimental teratoma. Curr Top Pathol. 1974;59:69–130. doi: 10.1007/978-3-642-65857-0_2. [DOI] [PubMed] [Google Scholar]
  17. Davis M. G., Kenney S. C., Kamine J., Pagano J. S., Huang E. S. Immediate-early gene region of human cytomegalovirus trans-activates the promoter of human immunodeficiency virus. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8642–8646. doi: 10.1073/pnas.84.23.8642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Dodd J., Jessell T. M. Cell surface glycoconjugates and carbohydrate-binding proteins: possible recognition signals in sensory neurone development. J Exp Biol. 1986 Sep;124:225–238. doi: 10.1242/jeb.124.1.225. [DOI] [PubMed] [Google Scholar]
  19. Duclos H., Elfassi E., Michelson S., Arenzana-Seisdedos F., Hazan U., Munier A., Virelizier J. L. Cytomegalovirus infection and trans-activation of HIV-1 and HIV-2 LTRs in human astrocytoma cells. AIDS Res Hum Retroviruses. 1989 Apr;5(2):217–224. doi: 10.1089/aid.1989.5.217. [DOI] [PubMed] [Google Scholar]
  20. Fenderson B. A., Zehavi U., Hakomori S. A multivalent lacto-N-fucopentaose III-lysyllysine conjugate decompacts preimplantation mouse embryos, while the free oligosaccharide is ineffective. J Exp Med. 1984 Nov 1;160(5):1591–1596. doi: 10.1084/jem.160.5.1591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fritsch E. F., Temin H. M. Inhibition of viral DNA synthesis in stationary chicken embryo fibroblasts infected with avian retroviruses. J Virol. 1977 Nov;24(2):461–469. doi: 10.1128/jvi.24.2.461-469.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fukushi Y., Nudelman E., Levery S. B., Hakomori S., Rauvala H. Novel fucolipids accumulating in human adenocarcinoma. III. A hybridoma antibody (FH6) defining a human cancer-associated difucoganglioside (VI3NeuAcV3III3Fuc2nLc6). J Biol Chem. 1984 Aug 25;259(16):10511–10517. [PubMed] [Google Scholar]
  23. Gönczöl E., Andrews P. W., Plotkin S. A. Cytomegalovirus infection of human teratocarcinoma cells in culture. J Gen Virol. 1985 Mar;66(Pt 3):509–515. doi: 10.1099/0022-1317-66-3-509. [DOI] [PubMed] [Google Scholar]
  24. Gönczöl E., Andrews P. W., Plotkin S. A. Cytomegalovirus replicates in differentiated but not in undifferentiated human embryonal carcinoma cells. Science. 1984 Apr 13;224(4645):159–161. doi: 10.1126/science.6322309. [DOI] [PubMed] [Google Scholar]
  25. Harouse J. M., Kunsch C., Hartle H. T., Laughlin M. A., Hoxie J. A., Wigdahl B., Gonzalez-Scarano F. CD4-independent infection of human neural cells by human immunodeficiency virus type 1. J Virol. 1989 Jun;63(6):2527–2533. doi: 10.1128/jvi.63.6.2527-2533.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ho W. Z., Harouse J. M., Rando R. F., Gönczöl E., Srinivasan A., Plotkin S. A. Reciprocal enhancement of gene expression and viral replication between human cytomegalovirus and human immunodeficiency virus type 1. J Gen Virol. 1990 Jan;71(Pt 1):97–103. doi: 10.1099/0022-1317-71-1-97. [DOI] [PubMed] [Google Scholar]
  27. Katz S. L., Wilfert C. M. Human immunodeficiency virus infection of newborns. N Engl J Med. 1989 Jun 22;320(25):1687–1689. doi: 10.1056/NEJM198906223202509. [DOI] [PubMed] [Google Scholar]
  28. Klatzmann D., Champagne E., Chamaret S., Gruest J., Guetard D., Hercend T., Gluckman J. C., Montagnier L. T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature. 1984 Dec 20;312(5996):767–768. doi: 10.1038/312767a0. [DOI] [PubMed] [Google Scholar]
  29. Lee V. M., Andrews P. W. Differentiation of NTERA-2 clonal human embryonal carcinoma cells into neurons involves the induction of all three neurofilament proteins. J Neurosci. 1986 Feb;6(2):514–521. doi: 10.1523/JNEUROSCI.06-02-00514.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Maio J. J., Brown F. L. Regulation of expression driven by human immunodeficiency virus type 1 and human T-cell leukemia virus type I long terminal repeats in pluripotential human embryonic cells. J Virol. 1988 Apr;62(4):1398–1407. doi: 10.1128/jvi.62.4.1398-1407.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Martin G. R. Teratocarcinomas and mammalian embryogenesis. Science. 1980 Aug 15;209(4458):768–776. doi: 10.1126/science.6250214. [DOI] [PubMed] [Google Scholar]
  32. McKeating J. A., Griffiths P. D., Weiss R. A. HIV susceptibility conferred to human fibroblasts by cytomegalovirus-induced Fc receptor. Nature. 1990 Feb 15;343(6259):659–661. doi: 10.1038/343659a0. [DOI] [PubMed] [Google Scholar]
  33. Poiesz B. J., Ruscetti F. W., Gazdar A. F., Bunn P. A., Minna J. D., Gallo R. C. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7415–7419. doi: 10.1073/pnas.77.12.7415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Prakash K., Seligy V. L. A temporally expressed gene from Schwanniomyces alluvius and detection of homologous sequences in other yeasts. Gene. 1988 Dec 15;73(1):131–140. doi: 10.1016/0378-1119(88)90319-8. [DOI] [PubMed] [Google Scholar]
  35. Rando R. F., Pellett P. E., Luciw P. A., Bohan C. A., Srinivasan A. Transactivation of human immunodeficiency virus by herpesviruses. Oncogene. 1987 Mar;1(1):13–18. [PubMed] [Google Scholar]
  36. Rando R. F., Srinivasan A., Feingold J., Gonczol E., Plotkin S. Characterization of multiple molecular interactions between human cytomegalovirus (HCMV) and human immunodeficiency virus type 1 (HIV-1). Virology. 1990 May;176(1):87–97. doi: 10.1016/0042-6822(90)90233-h. [DOI] [PubMed] [Google Scholar]
  37. Skolnik P. R., Kosloff B. R., Hirsch M. S. Bidirectional interactions between human immunodeficiency virus type 1 and cytomegalovirus. J Infect Dis. 1988 Mar;157(3):508–514. doi: 10.1093/infdis/157.3.508. [DOI] [PubMed] [Google Scholar]
  38. Tateno M., Gonzalez-Scarano F., Levy J. A. Human immunodeficiency virus can infect CD4-negative human fibroblastoid cells. Proc Natl Acad Sci U S A. 1989 Jun;86(11):4287–4290. doi: 10.1073/pnas.86.11.4287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tovo P. A., Gabiano C., Favro-Paris S., Palomba E., Gajno G. Brain atrophy with intracranial calcification following congenital HIV infection. Acta Paediatr Scand. 1988 Sep;77(5):776–779. doi: 10.1111/j.1651-2227.1988.tb10752.x. [DOI] [PubMed] [Google Scholar]
  40. Urkin J., Sarov B., Naggan L., Haikin H., Sarov I. Prevalence of CMV antibodies among women of childbearing age in different social environments in southern Israel. J Med Virol. 1988 Jan;24(1):19–25. doi: 10.1002/jmv.1890240104. [DOI] [PubMed] [Google Scholar]
  41. Varmus H. E., Padgett T., Heasley S., Simon G., Bishop J. M. Cellular functions are required for the synthesis and integration of avian sarcoma virus-specific DNA. Cell. 1977 Jun;11(2):307–319. doi: 10.1016/0092-8674(77)90047-2. [DOI] [PubMed] [Google Scholar]
  42. Volpi A., Pica F., Cauletti M., Panà A., Rocchi G. Cytomegalovirus infection in day care centers in Rome, Italy: viral excretion in children and occupational risk among workers. J Med Virol. 1988 Oct;26(2):119–125. doi: 10.1002/jmv.1890260203. [DOI] [PubMed] [Google Scholar]
  43. Weller T. H. The cytomegaloviruses: ubiquitous agents with protean clinical manifestations. I. N Engl J Med. 1971 Jul 22;285(4):203–214. doi: 10.1056/NEJM197107222850406. [DOI] [PubMed] [Google Scholar]
  44. Wentworth B. B., French L. Plaque assay of cytomegalovirus strains of human origin. Proc Soc Exp Biol Med. 1970 Nov;135(2):253–258. doi: 10.3181/00379727-135-35031. [DOI] [PubMed] [Google Scholar]

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