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. 1985 Jul 1;101(1):60–65. doi: 10.1083/jcb.101.1.60

Monensin-resistant mouse Balb/3T3 cell mutant with aberrant penetration of vesicular stomatitis virus

PMCID: PMC2113637  PMID: 2861207

Abstract

A mutant (MO-5) resistant to monensin (an ionophoric antibiotic) derived from the mouse Balb/3T3 cell line, was a poor host for vesicular stomatitis virus (VSV) or semliki forest virus (SFV) multiplication. The yield of VSV particles in MO-5 is one 100-fold reduced as is VSV-dependent RNA synthesis. In contrast to a pH-remedial mutant, the abortive production of infectious VSV particles in MO-5 cells was not restored by low pH treatment. The pH values in the endosome and the lysosome of MO-5 cells were 5.2 and 5.4, respectively, values that were comparable to the pH value in Balb/3T3 cells. Assays with [3H]uridine-labeled VSV indicated similar binding of VSV in MO-5: percoll gradient centrifugation analysis of [35S]methionine-labeled VSV- infected Balb/3T3 showed accumulation of VSV in the lysosome fraction 20 min after VSV infection, whereas VSV can be found mainly in endosome/Golgi fraction of MO-5 cells after 40 to 60 min on the percoll gradients. Degradation of [35S]methionine-labeled VSV was observed at a significant rate in Balb/3T3 cells, but not in MO-5 cells. The monensin- resistant somatic cell may thus provide a genetic route to study the mechanism of endocytosis or transport of enveloped viruses.

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Selected References

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  1. Brown M. S., Anderson R. G., Goldstein J. L. Recycling receptors: the round-trip itinerary of migrant membrane proteins. Cell. 1983 Mar;32(3):663–667. doi: 10.1016/0092-8674(83)90052-1. [DOI] [PubMed] [Google Scholar]
  2. Dales S. Early events in cell-animal virus interactions. Bacteriol Rev. 1973 Jun;37(2):103–135. doi: 10.1128/br.37.2.103-135.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dickson R. B., Willingham M. C., Pastan I. alpha 2-macroglobulin adsorbed to colloidal gold: a new probe in the study of receptor-mediated endocytosis. J Cell Biol. 1981 Apr;89(1):29–34. doi: 10.1083/jcb.89.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dunn W. A., Hubbard A. L., Aronson N. N., Jr Low temperature selectively inhibits fusion between pinocytic vesicles and lysosomes during heterophagy of 125I-asialofetuin by the perfused rat liver. J Biol Chem. 1980 Jun 25;255(12):5971–5978. [PubMed] [Google Scholar]
  5. FitzGerald D. J., Padmanabhan R., Pastan I., Willingham M. C. Adenovirus-induced release of epidermal growth factor and pseudomonas toxin into the cytosol of KB cells during receptor-mediated endocytosis. Cell. 1983 Feb;32(2):607–617. doi: 10.1016/0092-8674(83)90480-4. [DOI] [PubMed] [Google Scholar]
  6. Goldstein J. L., Anderson R. G., Brown M. S. Coated pits, coated vesicles, and receptor-mediated endocytosis. Nature. 1979 Jun 21;279(5715):679–685. doi: 10.1038/279679a0. [DOI] [PubMed] [Google Scholar]
  7. Helenius A., Kartenbeck J., Simons K., Fries E. On the entry of Semliki forest virus into BHK-21 cells. J Cell Biol. 1980 Feb;84(2):404–420. doi: 10.1083/jcb.84.2.404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Helenius A., Marsh M., White J. Inhibition of Semliki forest virus penetration by lysosomotropic weak bases. J Gen Virol. 1982 Jan;58(Pt 1):47–61. doi: 10.1099/0022-1317-58-1-47. [DOI] [PubMed] [Google Scholar]
  9. Ikezaki K., Akiyama S., Miyazaki C., Kimura G., Kuwano M. Imidazole-resistant phenotype and virus transformation in cultured rat cells. Cancer Res. 1984 May;44(5):1791–1795. [PubMed] [Google Scholar]
  10. Ikezaki K., Akiyama S., Nakamura M., Komiyama S., Kuwano M. Isolation and characterization of vitamin A-sensitive Chinese hamster lung cell lines. J Cell Physiol. 1983 Oct;117(1):15–22. doi: 10.1002/jcp.1041170104. [DOI] [PubMed] [Google Scholar]
  11. Kakunaga T., Crow J. D. Cell variants showing differential susceptibility to ultraviolet light--induced transformation. Science. 1980 Jul 25;209(4455):505–507. doi: 10.1126/science.7394516. [DOI] [PubMed] [Google Scholar]
  12. Kielian M. C., Helenius A. Role of cholesterol in fusion of Semliki Forest virus with membranes. J Virol. 1984 Oct;52(1):281–283. doi: 10.1128/jvi.52.1.281-283.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Klausner R. D., van Renswoude J., Kempf C., Rao K., Bateman J. L., Robbins A. R. Failure to release iron from transferrin in a Chinese hamster ovary cell mutant pleiotropically defective in endocytosis. J Cell Biol. 1984 Mar;98(3):1098–1101. doi: 10.1083/jcb.98.3.1098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kuwano M., Tabuki T., Akiyama S., Mifune K., Takatsuki A., Tamura G., Ikehara Y. Isolation and characterization of Chinese hamster ovary cell mutants with altered sensitivity to high doses of tunicamycin. Somatic Cell Genet. 1981 Sep;7(5):507–521. doi: 10.1007/BF01549655. [DOI] [PubMed] [Google Scholar]
  15. Maeda T., Kawasaki K., Ohnishi S. Interaction of influenza virus hemagglutinin with target membrane lipids is a key step in virus-induced hemolysis and fusion at pH 5.2. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4133–4137. doi: 10.1073/pnas.78.7.4133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mahoney E. M., Scott W. A., Landsberger F. R., Hamill A. L., Cohn Z. A. Influence of fatty acyl substitution on the composition and function of macrophage membranes. J Biol Chem. 1980 May 25;255(10):4910–4917. [PubMed] [Google Scholar]
  17. Marsh M., Bolzau E., Helenius A. Penetration of Semliki Forest virus from acidic prelysosomal vacuoles. Cell. 1983 Mar;32(3):931–940. doi: 10.1016/0092-8674(83)90078-8. [DOI] [PubMed] [Google Scholar]
  18. Masuda A., Akiyama S., Kuwano M. Chinese hamster cell mutant resistant to ML236B (Compactin) is defective in endocytosis of low-density lipo-protein. Mol Cell Biol. 1982 Nov;2(11):1354–1361. doi: 10.1128/mcb.2.11.1354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Masuda A., Tomita K., Kuwano M. Chinese hamster cell mutants with defective endocytosis of low-density lipoprotein contain altered fatty acid composition in the membrane. Biochem Biophys Res Commun. 1984 Jul 31;122(2):627–634. doi: 10.1016/s0006-291x(84)80079-0. [DOI] [PubMed] [Google Scholar]
  20. Matlin K. S., Reggio H., Helenius A., Simons K. Infectious entry pathway of influenza virus in a canine kidney cell line. J Cell Biol. 1981 Dec;91(3 Pt 1):601–613. doi: 10.1083/jcb.91.3.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Matlin K. S., Reggio H., Helenius A., Simons K. Pathway of vesicular stomatitis virus entry leading to infection. J Mol Biol. 1982 Apr 15;156(3):609–631. doi: 10.1016/0022-2836(82)90269-8. [DOI] [PubMed] [Google Scholar]
  22. Maxfield F. R. Weak bases and ionophores rapidly and reversibly raise the pH of endocytic vesicles in cultured mouse fibroblasts. J Cell Biol. 1982 Nov;95(2 Pt 1):676–681. doi: 10.1083/jcb.95.2.676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mento S. J., Siminovitch L. Isolation and preliminary characterization of Sindbis virus-resistant Chinese hamster ovary cells. Virology. 1981 Jun;111(2):320–330. doi: 10.1016/0042-6822(81)90336-6. [DOI] [PubMed] [Google Scholar]
  24. Merion M., Schlesinger P., Brooks R. M., Moehring J. M., Moehring T. J., Sly W. S. Defective acidification of endosomes in Chinese hamster ovary cell mutants "cross-resistant" to toxins and viruses. Proc Natl Acad Sci U S A. 1983 Sep;80(17):5315–5319. doi: 10.1073/pnas.80.17.5315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Moehring J. M., Moehring T. J. Strains of CHO-K1 cells resistant to Pseudomonas exotoxin A and cross-resistant to diphtheria toxin and viruses. Infect Immun. 1983 Sep;41(3):998–1009. doi: 10.1128/iai.41.3.998-1009.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Moehring J. M., Moehring T. J. The spectrum of virus resistance of a KB cell strain resistant to diphtheria toxin. Virology. 1976 Feb;69(2):786–788. doi: 10.1016/0042-6822(76)90507-9. [DOI] [PubMed] [Google Scholar]
  27. Ohkuma S., Poole B. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3327–3331. doi: 10.1073/pnas.75.7.3327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ono M., Ando M., Shimada T., Furuno K., Kato K., Kuwano M. Isolation of chloroquine-resistant Chinese hamster V79 cell variants that are also resistant to ammonium chloride. J Biochem. 1983 Nov;94(5):1493–1503. [PubMed] [Google Scholar]
  29. Ono M., Kuwano M., Watanabe K., Funatsu G. Chinese hamster cell variants resistant to the A chain of ricin carry altered ribosome function. Mol Cell Biol. 1982 Jun;2(6):599–606. doi: 10.1128/mcb.2.6.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ono M., Takahashi K., Sato Y., Kuwano M. Phosphorylation of membrane proteins in monensin-resistant mutant of Chinese hamster ovary cell with altered insulin-receptor activity. Biochem Int. 1984 Sep;9(3):369–377. [PubMed] [Google Scholar]
  31. Ono M., Yamato H., Ando M., Kuwano M. Chinese hamster ovary cell variants resistant to monensin, an ionophoric antibiotic. I. Isolation and altered endocytosis of ricin. J Cell Physiol. 1984 May;119(2):198–203. doi: 10.1002/jcp.1041190209. [DOI] [PubMed] [Google Scholar]
  32. Pastan I. H., Willingham M. C. Journey to the center of the cell: role of the receptosome. Science. 1981 Oct 30;214(4520):504–509. doi: 10.1126/science.6170111. [DOI] [PubMed] [Google Scholar]
  33. Ray B., Wu H. C. Enhanced internalization of ricin in nigericin-pretreated Chinese hamster ovary cells. Mol Cell Biol. 1981 Jun;1(6):560–567. doi: 10.1128/mcb.1.6.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Robbins A. R., Peng S. S., Marshall J. L. Mutant Chinese hamster ovary cells pleiotropically defective in receptor-mediated endocytosis. J Cell Biol. 1983 Apr;96(4):1064–1071. doi: 10.1083/jcb.96.4.1064. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sato Y., Ono M., Takaki R., Kuwano M. Chinese hamster ovary cell variants resistant to monensin, an ionophoric antibiotic. II. Growth requirement for insulin and altered insulin-receptor activity. J Cell Physiol. 1984 May;119(2):204–210. doi: 10.1002/jcp.1041190210. [DOI] [PubMed] [Google Scholar]
  36. Schlegel R., Willingham M. C., Pastan I. H. Saturable binding sites for vesicular stomatitis virus on the surface of Vero cells. J Virol. 1982 Sep;43(3):871–875. doi: 10.1128/jvi.43.3.871-875.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Steinman R. M., Mellman I. S., Muller W. A., Cohn Z. A. Endocytosis and the recycling of plasma membrane. J Cell Biol. 1983 Jan;96(1):1–27. doi: 10.1083/jcb.96.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Straubinger R. M., Hong K., Friend D. S., Papahadjopoulos D. Endocytosis of liposomes and intracellular fate of encapsulated molecules: encounter with a low pH compartment after internalization in coated vesicles. Cell. 1983 Apr;32(4):1069–1079. doi: 10.1016/0092-8674(83)90291-x. [DOI] [PubMed] [Google Scholar]
  39. Wellner R. B., Ray B., Ghosh P. C., Wu H. C. Genetic and biochemical analysis of mutation(s) affecting ricin internalization in Chinese hamster ovary cells. J Biol Chem. 1984 Oct 25;259(20):12788–12793. [PubMed] [Google Scholar]
  40. Yamashiro D. J., Fluss S. R., Maxfield F. R. Acidification of endocytic vesicles by an ATP-dependent proton pump. J Cell Biol. 1983 Sep;97(3):929–934. doi: 10.1083/jcb.97.3.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Yoshimura A., Ohnishi S. Uncoating of influenza virus in endosomes. J Virol. 1984 Aug;51(2):497–504. doi: 10.1128/jvi.51.2.497-504.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]

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