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. 1959 Sep 30;110(4):643–656. doi: 10.1084/jem.110.4.643

ELECTRON MICROSCOPIC OBSERVATIONS ON THE DEVELOPMENT OF HERPES SIMPLEX VIRUS

Councilman Morgan 1, Harry M Rose 1, Margaret Holden 1, Ellyn P Jones 1
PMCID: PMC2136996  PMID: 14424096

Abstract

Study of the J.M. strain of herpes simplex virus in human amnionic and HeLa cell tissue cultures revealed the presence of intranuclear crystals composed of viral particles with a single membrane enclosing a central body. Randomly dispersed virus with double coats was seen in the nuclear matrix and between multiple membranes at the nuclear periphery. The majority of intracytoplasmic viral particles were within walled vacuoles. It is suggested that this strain of virus differentiates and frequently crystallizes at template sites which are characterized by aggregates of granules near the nuclear margin; that particles, either singly or occasionally in small groups, become enclosed by a second peripheral membrane while still within the nucleus; that the virus can pass into the cytoplasm through reduplications of the nuclear membrane which are deposited behind the virus in such a manner as to prevent rupture of the nucleus; that most of the intracytoplasmic virus is contained within sacks formed by nuclear membranes; and that rupture of these sacks at the cell surface results in extrusion of virus without disruption of the cell. No evidence was obtained to support the hypothesis that virus develops in the cytoplasm. Examination of the H.R. and C.G. strains of herpes simplex virus in identical cell lines grown under similar conditions failed to show viral crystals, but reduplication of the nuclear membranes was evident. Study of the J.M. strain in cells of chicken embryo chorioallantoic membranes indicated that the basic mechanisms of viral development and release did not differ from those operating in HeLa and human amnionic cells.

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Selected References

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  1. BERNHARD W., BAUER A., HAREL J., OBERLING C. Les formes intracytoplasmiques du virus fibromateux de Shope; études de coupes ultrafines au microscope électronique. Bull Assoc Fr Etud Cancer. 1954;41(4):423–444. [PubMed] [Google Scholar]
  2. BLOCH D. P., MORGAN C., GODMAN G. C., HOWE C., ROSE H. M. A correlated histochemical and electron microscopic study of the intranuclear crystalline aggregates of adenovirus (RI-APC virus) in HeLa cells. J Biophys Biochem Cytol. 1957 Jan 25;3(1):1–8. doi: 10.1083/jcb.3.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BRANDT P. W. A study of the mechanism of pinocytosis. Exp Cell Res. 1958 Oct;15(2):300–313. doi: 10.1016/0014-4827(58)90032-6. [DOI] [PubMed] [Google Scholar]
  4. BUCK R. C. The fine structure of endothelium of large arteries. J Biophys Biochem Cytol. 1958 Mar 25;4(2):187–190. doi: 10.1083/jcb.4.2.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. DEMPSEY E. W. Electron microscopy of the visceral yolk-sac epithelium of the guinea pig. Am J Anat. 1953 Nov;93(3):331–363. doi: 10.1002/aja.1000930303. [DOI] [PubMed] [Google Scholar]
  6. FAWCETT D. W. Electron microscope observations on intracellular virus-like particles associated with the cells of the Lucké renal adenocarcinoma. J Biophys Biochem Cytol. 1956 Nov 25;2(6):725–741. doi: 10.1083/jcb.2.6.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. HAMLIN A., HARFORD C. G., PARKER E., VAN RAVENSWAAY T. Electron microscopy of HeLa cells infected with adenoviruses. J Exp Med. 1956 Sep 1;104(3):443–454. doi: 10.1084/jem.104.3.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. HARFORD C. G., HAMLIN A., PARKER E. Electron microscopy of HeLa cells infected with ARD virus. Trans Assoc Am Physicians. 1955;68:82–86. [PubMed] [Google Scholar]
  9. KJELLEN L., LAGERMALM G., SVEDMYR A., THORSSON K. G. Crystalline-like patterns in the nuclei of cells infected with an animal virus. Nature. 1955 Mar 19;175(4455):505–506. doi: 10.1038/175505a0. [DOI] [PubMed] [Google Scholar]
  10. LOW B. W., PINNOCK P. R. The packing structure of crystalline RI-APC virus. J Biophys Biochem Cytol. 1956 Jul 25;2(4):483–486. doi: 10.1083/jcb.2.4.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. LUSE S. A., SMITH M. G. Electron microscopy of salivary gland viruses. J Exp Med. 1958 May 1;107(5):623–632. doi: 10.1084/jem.107.5.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. MORGAN C., ELLISON S. A., ROSE H. M., MOORE D. H. Serial sections of vaccinia virus examined at one stage of development in the electron microscope. Exp Cell Res. 1955 Dec;9(3):572–578. doi: 10.1016/0014-4827(55)90086-0. [DOI] [PubMed] [Google Scholar]
  13. MORGAN C., ELLISON S. A., ROSE H. M., MOORE D. H. Structure and development of viruses as observed in the electron microscope. I. Herpes simplex virus. J Exp Med. 1954 Aug 1;100(2):195–202. doi: 10.1084/jem.100.2.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. MORGAN C., ELLISON S. A., ROSE H. M., MOORE D. H. Structure and development of viruses observed in the electron microscope. II. Vaccinia and fowl pox viruses. J Exp Med. 1954 Sep 1;100(3):301–310. doi: 10.1084/jem.100.3.301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. MORGAN C., GODMAN G. C., HOWE C., ROSE H. M. Intracellular crystals associated with viral development. Trans Assoc Am Physicians. 1958;71:281–286. [PubMed] [Google Scholar]
  16. MORGAN C., JONES E. P., HOLDEN M., ROSE H. M. Intranuclear crystals of herpes simplex virus observed with the electron microscope. Virology. 1958 Jun;5(3):568–571. doi: 10.1016/0042-6822(58)90047-3. [DOI] [PubMed] [Google Scholar]
  17. MORGAN C., ROSE H. M., MOORE D. H. An evaluation of host cell changes accompanying viral multiplication as observed in the electron microscope. Ann N Y Acad Sci. 1957 Oct 21;68(2):302–323. doi: 10.1111/j.1749-6632.1957.tb56087.x. [DOI] [PubMed] [Google Scholar]
  18. MORGAN C., ROSE H. M., MOORE D. H. Structure and development of viruses observed in the electron microscope. III. Influenza virus. J Exp Med. 1956 Aug 1;104(2):171–182. doi: 10.1084/jem.104.2.171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. MORGAN C., ROSE H. M., MOORE D. H. Use of the electron microscope in the study of intracellular virus. Bull N Y Acad Med. 1958 Feb;34(2):85–98. [PMC free article] [PubMed] [Google Scholar]
  20. REISSIG M., MELNICK J. L. The cellular changes produced in tissue cultures by herpes B virus correlated with the concurrent multiplication of the virus. J Exp Med. 1955 Mar 1;101(3):341–352. doi: 10.1084/jem.101.3.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. STOKER M. G., SMITH K. M., ROSS R. W. Electron microscope studies of HeLa cells infected with herpes virus. J Gen Microbiol. 1958 Oct;19(2):244–249. doi: 10.1099/00221287-19-2-244. [DOI] [PubMed] [Google Scholar]
  22. WATSON M. L. The nuclear envelope; its structure and relation to cytoplasmic membranes. J Biophys Biochem Cytol. 1955 May 25;1(3):257–270. doi: 10.1083/jcb.1.3.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. WILSON A. T. The egestion of phagocytized particles by leukocytes. J Exp Med. 1953 Oct;98(4):305–310. doi: 10.1084/jem.98.4.305. [DOI] [PMC free article] [PubMed] [Google Scholar]

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