Abstract
A persistently coronavirus-infected embryonic stem (ES) cell line A3/MHV was established by infecting an ES cell line, A3-1, with mouse hepatitis virus type-2. Although almost all A3/MHV cells were found infected, both A3/MHV and A3-1 cells expressed comparable levels of cell surface differentiation markers. In addition, A3/MHV cells retained the ability to form embryoid bodies. These results suggest that persistent coronavirus infection does not affect the differentiation of ES cells.
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- Aoyama H., Delouvée A., Thiery J. P. Cell adhesion mechanisms in gangliogenesis studied in avian embryo and in a model system. Cell Differ. 1985 Nov;17(4):247–260. doi: 10.1016/0045-6039(85)90499-3. [DOI] [PubMed] [Google Scholar]
- Asanaka M., Lai M. M. Cell fusion studies identified multiple cellular factors involved in mouse hepatitis virus entry. Virology. 1993 Dec;197(2):732–741. doi: 10.1006/viro.1993.1649. [DOI] [PubMed] [Google Scholar]
- Baybutt H. N., Wege H., Carter M. J., ter Meulen V. Adaptation of coronavirus JHM to persistent infection of murine sac(-) cells. J Gen Virol. 1984 May;65(Pt 5):915–924. doi: 10.1099/0022-1317-65-5-915. [DOI] [PubMed] [Google Scholar]
- Bradley A., Evans M., Kaufman M. H., Robertson E. Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature. 1984 May 17;309(5965):255–256. doi: 10.1038/309255a0. [DOI] [PubMed] [Google Scholar]
- Castro R. F., Perlman S. CD8+ T-cell epitopes within the surface glycoprotein of a neurotropic coronavirus and correlation with pathogenicity. J Virol. 1995 Dec;69(12):8127–8131. doi: 10.1128/jvi.69.12.8127-8131.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Doetschman T., Williams P., Maeda N. Establishment of hamster blastocyst-derived embryonic stem (ES) cells. Dev Biol. 1988 May;127(1):224–227. doi: 10.1016/0012-1606(88)90204-7. [DOI] [PubMed] [Google Scholar]
- Dveksler G. S., Basile A. A., Cardellichio C. B., Holmes K. V. Mouse hepatitis virus receptor activities of an MHVR/mph chimera and MHVR mutants lacking N-linked glycosylation of the N-terminal domain. J Virol. 1995 Jan;69(1):543–546. doi: 10.1128/jvi.69.1.543-546.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Evans M. J., Kaufman M. H. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981 Jul 9;292(5819):154–156. doi: 10.1038/292154a0. [DOI] [PubMed] [Google Scholar]
- Fleming J. O., Stohlman S. A., Harmon R. C., Lai M. M., Frelinger J. A., Weiner L. P. Antigenic relationships of murine coronaviruses: analysis using monoclonal antibodies to JHM (MHV-4) virus. Virology. 1983 Dec;131(2):296–307. doi: 10.1016/0042-6822(83)90498-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Flintoff W. F., Van Dinter S. Several rat cell lines share a common defect in their inability to internalize murine coronaviruses efficiently. J Gen Virol. 1989 Jul;70(Pt 7):1713–1724. doi: 10.1099/0022-1317-70-7-1713. [DOI] [PubMed] [Google Scholar]
- Grover A., Andrews G., Adamson E. D. Role of laminin in epithelium formation by F9 aggregates. J Cell Biol. 1983 Jul;97(1):137–144. doi: 10.1083/jcb.97.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grover A., Oshima R. G., Adamson E. D. Epithelial layer formation in differentiating aggregates of F9 embryonal carcinoma cells. J Cell Biol. 1983 Jun;96(6):1690–1696. doi: 10.1083/jcb.96.6.1690. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hilton A., Mizzen L., MacIntyre G., Cheley S., Anderson R. Translational control in murine hepatitis virus infection. J Gen Virol. 1986 May;67(Pt 5):923–932. doi: 10.1099/0022-1317-67-5-923. [DOI] [PubMed] [Google Scholar]
- Kooi C., Mizzen L., Alderson C., Daya M., Anderson R. Early events of importance in determining host cell permissiveness to mouse hepatitis virus infection. J Gen Virol. 1988 Jun;69(Pt 6):1125–1135. doi: 10.1099/0022-1317-69-6-1125. [DOI] [PubMed] [Google Scholar]
- Kubo H., Takase-Yoden S., Taguchi F. Neutralization and fusion inhibition activities of monoclonal antibodies specific for the S1 subunit of the spike protein of neurovirulent murine coronavirus JHMV c1-2 variant. J Gen Virol. 1993 Jul;74(Pt 7):1421–1425. doi: 10.1099/0022-1317-74-7-1421. [DOI] [PubMed] [Google Scholar]
- Kurihara Y., Kurihara H., Suzuki H., Kodama T., Maemura K., Nagai R., Oda H., Kuwaki T., Cao W. H., Kamada N. Elevated blood pressure and craniofacial abnormalities in mice deficient in endothelin-1. Nature. 1994 Apr 21;368(6473):703–710. doi: 10.1038/368703a0. [DOI] [PubMed] [Google Scholar]
- Kyuwa S., Cohen M., Nelson G., Tahara S. M., Stohlman S. A. Modulation of cellular macromolecular synthesis by coronavirus: implication for pathogenesis. J Virol. 1994 Oct;68(10):6815–6819. doi: 10.1128/jvi.68.10.6815-6819.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lai M. M. Coronavirus: organization, replication and expression of genome. Annu Rev Microbiol. 1990;44:303–333. doi: 10.1146/annurev.mi.44.100190.001511. [DOI] [PubMed] [Google Scholar]
- Lamontagne L. M., Dupuy J. M. Persistent infection with mouse hepatitis virus 3 in mouse lymphoid cell lines. Infect Immun. 1984 Jun;44(3):716–723. doi: 10.1128/iai.44.3.716-723.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leibowitz J. L., Bond C. W., Anderson K., Goss S. Biological and macromolecular properties of murine cells persistently infected with MHV-JHM. Arch Virol. 1984;80(4):315–332. doi: 10.1007/BF01311222. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Macintyre G., Wong F., Anderson R. A model for persistent murine coronavirus infection involving maintenance via cytopathically infected cell centres. J Gen Virol. 1989 Mar;70(Pt 3):763–768. doi: 10.1099/0022-1317-70-3-763. [DOI] [PubMed] [Google Scholar]
- Martin G. R. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7634–7638. doi: 10.1073/pnas.78.12.7634. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mizzen L., Cheley S., Rao M., Wolf R., Anderson R. Fusion resistance and decreased infectability as major host cell determinants of coronavirus persistence. Virology. 1983 Jul 30;128(2):407–417. doi: 10.1016/0042-6822(83)90266-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Muramatsu H., Hamada H., Noguchi S., Kamada Y., Muramatsu T. Cell-surface changes during in vitro differentiation of pluripotent embryonal carcinoma cells. Dev Biol. 1985 Aug;110(2):284–296. doi: 10.1016/0012-1606(85)90088-0. [DOI] [PubMed] [Google Scholar]
- Muramatsu T. Cell surface glycoproteins as markers in monitoring in vitro differentiation of embryonal carcinoma cells. Cell Differ. 1984 Dec;15(2-4):101–108. doi: 10.1016/0045-6039(84)90059-9. [DOI] [PubMed] [Google Scholar]
- Nomoto S., Muramatsu H., Ozawa M., Suganuma T., Tashiro M., Muramatsu T. An anti-carbohydrate monoclonal antibody inhibits cell-substratum adhesion of F9 embryonal carcinoma cells. Exp Cell Res. 1986 May;164(1):49–62. doi: 10.1016/0014-4827(86)90453-2. [DOI] [PubMed] [Google Scholar]
- Nédellec P., Dveksler G. S., Daniels E., Turbide C., Chow B., Basile A. A., Holmes K. V., Beauchemin N. Bgp2, a new member of the carcinoembryonic antigen-related gene family, encodes an alternative receptor for mouse hepatitis viruses. J Virol. 1994 Jul;68(7):4525–4537. doi: 10.1128/jvi.68.7.4525-4537.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pease S., Williams R. L. Formation of germ-line chimeras from embryonic stem cells maintained with recombinant leukemia inhibitory factor. Exp Cell Res. 1990 Oct;190(2):209–211. doi: 10.1016/0014-4827(90)90187-f. [DOI] [PubMed] [Google Scholar]
- Reisner Y., Gachelin G., Dubois P., Nicolas J. F., Sharon N., Jacob F. Interaction of peanut agglutinin, a lectin specific for nonreducing terminal D-galactosyl residues, with embryonal carcinoma cells. Dev Biol. 1977 Nov;61(1):20–27. doi: 10.1016/0012-1606(77)90338-4. [DOI] [PubMed] [Google Scholar]
- Sato M., Ozawa M., Hamada H., Kasai M., Tokunaga T., Muramatsu T. Cell surface markers to monitor the process of visceral endoderm differentiation from embryonal carcinoma cells: identification of the stage sensitive to high concentration of retinoic acid. J Embryol Exp Morphol. 1985 Aug;88:165–182. [PubMed] [Google Scholar]
- Sawicki S. G., Lu J. H., Holmes K. V. Persistent infection of cultured cells with mouse hepatitis virus (MHV) results from the epigenetic expression of the MHV receptor. J Virol. 1995 Sep;69(9):5535–5543. doi: 10.1128/jvi.69.9.5535-5543.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shames R. B., Jennings A. G., Sawyer R. H. Expression of the cell adhesion molecules, L-CAM and N-CAM during avian scale development. J Exp Zool. 1991 Feb;257(2):195–207. doi: 10.1002/jez.1402570208. [DOI] [PubMed] [Google Scholar]
- Shen M. M., Leder P. Leukemia inhibitory factor is expressed by the preimplantation uterus and selectively blocks primitive ectoderm formation in vitro. Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):8240–8244. doi: 10.1073/pnas.89.17.8240. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spaan W., Cavanagh D., Horzinek M. C. Coronaviruses: structure and genome expression. J Gen Virol. 1988 Dec;69(Pt 12):2939–2952. doi: 10.1099/0022-1317-69-12-2939. [DOI] [PubMed] [Google Scholar]
- Taguchi F., Yamada A., Fujiwara K. Resistance to highly virulent mouse hepatitis virus acquired by mice after low-virulence infection: enhanced antiviral activity of macrophages. Infect Immun. 1980 Jul;29(1):42–49. doi: 10.1128/iai.29.1.42-49.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tahara S. M., Dietlin T. A., Bergmann C. C., Nelson G. W., Kyuwa S., Anthony R. P., Stohlman S. A. Coronavirus translational regulation: leader affects mRNA efficiency. Virology. 1994 Aug 1;202(2):621–630. doi: 10.1006/viro.1994.1383. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vestweber D., Kemler R. Identification of a putative cell adhesion domain of uvomorulin. EMBO J. 1985 Dec 16;4(13A):3393–3398. doi: 10.1002/j.1460-2075.1985.tb04095.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wege H., Siddell S., ter Meulen V. The biology and pathogenesis of coronaviruses. Curr Top Microbiol Immunol. 1982;99:165–200. doi: 10.1007/978-3-642-68528-6_5. [DOI] [PubMed] [Google Scholar]
- Williams R. K., Jiang G. S., Holmes K. V. Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5533–5536. doi: 10.1073/pnas.88.13.5533. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yokomori K., Asanaka M., Stohlman S. A., Lai M. M. A spike protein-dependent cellular factor other than the viral receptor is required for mouse hepatitis virus entry. Virology. 1993 Sep;196(1):45–56. doi: 10.1006/viro.1993.1453. [DOI] [PubMed] [Google Scholar]