PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of jvirolPermissionsJournals.ASM.orgJournalJV ArticleJournal InfoAuthorsReviewers
 
J Virol. 1994 October; 68(10): 6745–6750.
PMCID: PMC237095

Feline immunodeficiency virus decreases cell-cell communication and mitochondrial membrane potential.

Abstract

The in vitro effects of viral replication on mitochondrial membrane potential (MMP) and gap junctional intercellular communication (GJIC) were evaluated as two parameters of potential cellular injury. Two distinct cell types were infected with the Petaluma strain of feline immunodeficiency virus (FIV). Primary astroglia supported acute FIV infection, resulting in syncytia within 3 days of infection, whereas immortalized Crandell feline kidney (CRFK) cells of epithelial origin supported persistent FIV infection in the absence of an obvious cytopathic effect. An examination of cells under conditions that included an infection rate of more than 90% for either population revealed that the astroglia produced about four times more virus than the CRFK cells. The mitochondrial uptake of the cationic fluorescent dye rhodamine 123 in infected astroglia was less than 45% of that of normal control cells, whereas the MMP of the CRFK cells, which produced about one-fourth as much virus, was 80.8% of that of the normal cells. Cell-cell communication between adjacent cells was determined by the recovery of fluorescence following photobleaching of a single cell. In spite of the lower level of innate cell-cell communication among cultured CRFK cells than among astroglia, viral replication resulted in a 30% decrease in the GJIC of both astroglia and CRFK cells. These studies indicate that cell injury, as defined by an inhibition of MMP and GJIC, can occur as a result of persistent and acute infection with the Petaluma strain of FIV.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.6M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Barhoumi R, Bowen JA, Stein LS, Echols J, Burghardt RC. Concurrent analysis of intracellular glutathione content and gap junctional intercellular communication. Cytometry. 1993 Oct;14(7):747–756. [PubMed]
  • Brown WC, Bissey L, Logan KS, Pedersen NC, Elder JH, Collisson EW. Feline immunodeficiency virus infects both CD4+ and CD8+ T lymphocytes. J Virol. 1991 Jun;65(6):3359–3364. [PMC free article] [PubMed]
  • Brunner D, Pedersen NC. Infection of peritoneal macrophages in vitro and in vivo with feline immunodeficiency virus. J Virol. 1989 Dec;63(12):5483–5488. [PMC free article] [PubMed]
  • Bunting JR, Phan TV, Kamali E, Dowben RM. Fluorescent cationic probes of mitochondria. Metrics and mechanism of interaction. Biophys J. 1989 Nov;56(5):979–993. [PubMed]
  • Burghardt RC, Barhoumi R, Lewis EH, Bailey RH, Pyle KA, Clement BA, Phillips TD. Patulin-induced cellular toxicity: a vital fluorescence study. Toxicol Appl Pharmacol. 1992 Feb;112(2):235–244. [PubMed]
  • Cheng-Mayer C, Rutka JT, Rosenblum ML, McHugh T, Stites DP, Levy JA. Human immunodeficiency virus can productively infect cultured human glial cells. Proc Natl Acad Sci U S A. 1987 May;84(10):3526–3530. [PubMed]
  • Cloyd MW, Lynn WS. Perturbation of host-cell membrane is a primary mechanism of HIV cytopathology. Virology. 1991 Apr;181(2):500–511. [PubMed]
  • Cloyd MW, Lynn WS, Ramsey K, Baron S. Inhibition of human immunodeficiency virus (HIV-1) infection by diphenylhydantoin (dilantin) implicates role of cellular calcium in virus life cycle. Virology. 1989 Dec;173(2):581–590. [PubMed]
  • Crandell RA, Fabricant CG, Nelson-Rees WA. Development, characterization, and viral susceptibility of a feline (Felis catus) renal cell line (CRFK). In Vitro. 1973 Nov-Dec;9(3):176–185. [PubMed]
  • Dewhurst S, Bresser J, Stevenson M, Sakai K, Evinger-Hodges MJ, Volsky DJ. Susceptibility of human glial cells to infection with human immunodeficiency virus (HIV). FEBS Lett. 1987 Mar 9;213(1):138–143. [PubMed]
  • Dickson DW, Mattiace LA, Kure K, Hutchins K, Lyman WD, Brosnan CF. Microglia in human disease, with an emphasis on acquired immune deficiency syndrome. Lab Invest. 1991 Feb;64(2):135–156. [PubMed]
  • Dow SW, Dreitz MJ, Hoover EA. Feline immunodeficiency virus neurotropism: evidence that astrocytes and microglia are the primary target cells. Vet Immunol Immunopathol. 1992 Dec;35(1-2):23–35. [PubMed]
  • Dow SW, Poss ML, Hoover EA. Feline immunodeficiency virus: a neurotropic lentivirus. J Acquir Immune Defic Syndr. 1990;3(7):658–668. [PubMed]
  • Ehrenberg B, Montana V, Wei MD, Wuskell JP, Loew LM. Membrane potential can be determined in individual cells from the nernstian distribution of cationic dyes. Biophys J. 1988 May;53(5):785–794. [PubMed]
  • Fermin CD, Garry RF. Membrane alterations linked to early interactions of HIV with the cell surface. Virology. 1992 Dec;191(2):941–946. [PubMed]
  • Fletcher WH, Byus CV, Walsh DA. Receptor-mediated action without receptor occupancy: a function for cell-cell communication in ovarian follicles. Adv Exp Med Biol. 1987;219:299–323. [PubMed]
  • Fontana A, Kristensen F, Dubs R, Gemsa D, Weber E. Production of prostaglandin E and an interleukin-1 like factor by cultured astrocytes and C6 glioma cells. J Immunol. 1982 Dec;129(6):2413–2419. [PubMed]
  • Frei K, Bodmer S, Schwerdel C, Fontana A. Astrocyte-derived interleukin 3 as a growth factor for microglia cells and peritoneal macrophages. J Immunol. 1986 Dec 1;137(11):3521–3527. [PubMed]
  • Frohman EM, van den Noort S, Gupta S. Astrocytes and intracerebral immune responses. J Clin Immunol. 1989 Jan;9(1):1–9. [PubMed]
  • Giulian D, Woodward J, Young DG, Krebs JF, Lachman LB. Interleukin-1 injected into mammalian brain stimulates astrogliosis and neovascularization. J Neurosci. 1988 Jul;8(7):2485–2490. [PubMed]
  • Grewe C, Beck A, Gelderblom HR. HIV: early virus-cell interactions. J Acquir Immune Defic Syndr. 1990;3(10):965–974. [PubMed]
  • Harbour DA, Williams PD, Gruffydd-Jones TJ, Burbridge J, Pearson GR. Isolation of a T-lymphotropic lentivirus from a persistently leucopenic domestic cat. Vet Rec. 1988 Jan 23;122(4):84–86. [PubMed]
  • Ishida T, Washizu T, Toriyabe K, Motoyoshi S, Tomoda I, Pedersen NC. Feline immunodeficiency virus infection in cats of Japan. J Am Vet Med Assoc. 1989 Jan 15;194(2):221–225. [PubMed]
  • Jain A, Mårtensson J, Stole E, Auld PA, Meister A. Glutathione deficiency leads to mitochondrial damage in brain. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1913–1917. [PubMed]
  • Janzer RC, Raff MC. Astrocytes induce blood-brain barrier properties in endothelial cells. Nature. 1987 Jan 15;325(6101):253–257. [PubMed]
  • Kimelberg HK. Occurrence and functional significance of serotonin and catecholamine uptake by astrocytes. Biochem Pharmacol. 1986 Jul 15;35(14):2273–2281. [PubMed]
  • Kinchington D, Barker W, Galpin S, Apostolov K. Temperature enhancement of syncytium formation by HIV and Sendai virus. J Med Virol. 1992 Jan;36(1):44–48. [PubMed]
  • Loewenstein WR. Permeability of membrane junctions. Ann N Y Acad Sci. 1966 Jul 14;137(2):441–472. [PubMed]
  • Lynn WS, Tweedale A, Cloyd MW. Human immunodeficiency virus (HIV-1) cytotoxicity: perturbation of the cell membrane and depression of phospholipid synthesis. Virology. 1988 Mar;163(1):43–51. [PubMed]
  • Malipiero UV, Frei K, Fontana A. Production of hemopoietic colony-stimulating factors by astrocytes. J Immunol. 1990 May 15;144(10):3816–3821. [PubMed]
  • Meister A, Anderson ME. Glutathione. Annu Rev Biochem. 1983;52:711–760. [PubMed]
  • Miller MA, Garry RF, Jaynes JM, Montelaro RC. A structural correlation between lentivirus transmembrane proteins and natural cytolytic peptides. AIDS Res Hum Retroviruses. 1991 Jun;7(6):511–519. [PubMed]
  • Pedersen NC, Ho EW, Brown ML, Yamamoto JK. Isolation of a T-lymphotropic virus from domestic cats with an immunodeficiency-like syndrome. Science. 1987 Feb 13;235(4790):790–793. [PubMed]
  • Pumarola-Sune T, Navia BA, Cordon-Cardo C, Cho ES, Price RW. HIV antigen in the brains of patients with the AIDS dementia complex. Ann Neurol. 1987 May;21(5):490–496. [PubMed]
  • Rahn CA, Bombick DW, Doolittle DJ. Assessment of mitochondrial membrane potential as an indicator of cytotoxicity. Fundam Appl Toxicol. 1991 Apr;16(3):435–448. [PubMed]
  • Rey MA, Spire B, Dormont D, Barre-Sinoussi F, Montagnier L, Chermann JC. Characterization of the RNA dependent DNA polymerase of a new human T-lymphotropic retrovirus (lymphadenopathy associated virus). Biochem Biophys Res Commun. 1984 May 31;121(1):126–133. [PubMed]
  • Rodriguez M, Pierce ML, Howie EA. Immune response gene products (Ia antigens) on glial and endothelial cells in virus-induced demyelination. J Immunol. 1987 May 15;138(10):3438–3442. [PubMed]
  • Stavrou D, Mehraein P, Mellert W, Bise K, Schmidtke K, Rothemunds E, Funke I, Stocker U, Babaryka I, Zietz C, et al. Evaluation of intracerebral lesions in patients with acquired immunodeficiency syndrome. Neuropathological findings and experimental data. Neuropathol Appl Neurobiol. 1989 May-Jun;15(3):207–222. [PubMed]
  • Wade MH, Trosko JE, Schindler M. A fluorescence photobleaching assay of gap junction-mediated communication between human cells. Science. 1986 Apr 25;232(4749):525–528. [PubMed]
  • Yamamoto JK, Hansen H, Ho EW, Morishita TY, Okuda T, Sawa TR, Nakamura RM, Pedersen NC. Epidemiologic and clinical aspects of feline immunodeficiency virus infection in cats from the continental United States and Canada and possible mode of transmission. J Am Vet Med Assoc. 1989 Jan 15;194(2):213–220. [PubMed]
  • Yamamoto JK, Sparger E, Ho EW, Andersen PR, O'Connor TP, Mandell CP, Lowenstine L, Munn R, Pedersen NC. Pathogenesis of experimentally induced feline immunodeficiency virus infection in cats. Am J Vet Res. 1988 Aug;49(8):1246–1258. [PubMed]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)