Summary
This study was to determine if feline immunodeficiency virus (FIV)-infected and uninfected Crandall feline kidney (CRFK) cells exhibited a low temperature (16°C) block in membrane trafficking between transitional endoplasmic reticulum and Golgi apparatus represented by intermediate compartment formation. Cells were cultured at different temperatures and membrane changes involving the Golgi apparatus and Golgi apparatus-associated membrane structures were monitored by electron microscopy and quantitated. With 30 min of incubation, membranes of the Golgi apparatus stack increased in amount at temperatures of 16°C and below compared to temperatures above 18°C. The increase was greatest along the major polarity axis as evidenced by an increased stack height. Neither the number of cisternae per stack nor the average stack diameter (width) was affected by temperature. The response was maximal between 15 and 30 min of low temperature treatment of the cells. Results with cells infected and uninfected with feline immunodeficiency virus were similar. The increase in stack height was due primarily to an increase of membranes at the cis face (cis Golgi apparatus network). At 18°C, membranes of the trans Golgi apparatus network accumulated suggesting that import from the cis Golgi network could proceed at this temperature, whereas exit from the trans Golgi network was still at least partially blocked. Also increased at 16°C and below were numbers of transition vesicles in the space between the Golgi apparatus and the transitional endoplasmic reticulum associated with the cis Golgi apparatus face. The results suggested interruption of the orderly flux of membranes into the Golgi apparatus at 16°C and below. Moreover, the block appeared to be reversible. Upon transfer from 16°C to 37°C, there was a time-dependent decrease in the accumulations of cis compartment membrane accompanied by a corresponding equivalent increase in the membranes of the trans Golgi apparatus compartment.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Brand M, Jansen E, Ploegh HL (1985) Effect of reduced temperature on glycoprotein (Ig. HLA) processing and transport in lymphoid cells. Mol Immunol 22: 787–794
Copeland CS, Zimmer KP, Wagner KR, Healey GA, Mellman I, Helenius A (1988) Folding, trimerization and transport are sequential events in the biogenesis of influenza virus hemagglutinin. Cell 53: 197–209
Fries E, Lindstrom I (1986) The effects of low temperatures on intracellular transport of newly synthesized albumin and haptoglobin in rat hepatocytes. Biochem J 237: 33–39
Geuze JM, Morré DJ (1991) The trans Golgi reticulum. J Electron Microsc Tech 17: 24–34
Griffiths G, Pfeiffer S, Simons K, Matlin K (1985) Exit of newly synthesized membrane proteins from the trans-cisternae of the Golgi complex to the plasma membrane. J Cell Biol 101: 949–964
Holmes KV, Doller EW, Sturman LS (1981) Tunicamycin resistant glycosylation of a coronavirus glycoprotein: determination of a novel type of viral glycoprotein. Virology 115: 334–344
Lagunoff D, Wan H (1974) Temperature dependence of mast cell histamine secretion. J Cell Biol 61: 809–811
Luft JM (1961) Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol 9: 409–414
Matlin KS, Simons K (1983) Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation. Cell 34: 233–243
Morré DJ, Paulik M, Nowack D (1986) Transition vesicle formation in vitro. Protoplasma 132: 110–113
—, Minnifield N, Paulik M (1989) Identification of the 16°C compartment of the endoplasmic reticulum in rat liver and cultured hamster kidney cells. Biol Cell 67: 51–60
Noguchi T, Morré DJ (1991) Vesicular membrane transfer between endoplasmic reticulum and the Golgi apparatus of a green alga,Micrasterias americana. A 16°C block and reconstitution in a cell-free system. Protoplasma 162: 128–139
Nowack DD, Morré DM, Paulik M, Keenan T, Morré DJ (1987) Intracellular membrane flow: reconstitution of transition vesicle formation and function in a cell-free system. Proc Natl Acad Sci USA 84: 6098–6102
Paulik M, Nowack DD, Morré DJ (1988) Isolation of a vesicular intermediate in the cell-free transfer of membrane from transitional elements of the endoplasmic reticulum to Golgi apparatus cisternae of rat liver. J Biol Chem 263: 17738–17748
Phillips TR, Talbott RL, Lamont C, Muir S, Lovelace K, Elder JH (1990) Comparison of two host cell range variants of feline immunodeficiency virus. J Virol 64: 4605–4613
Saraste J, Kuismanen E (1984) Pre- and post-Golgi vacuoles operate in the transport of Semliki Forest virus membrane glycoproteins to the cell surface. Cell 38: 535–549
—, Palade GE, Farquhar MG (1986) Temperature sensitive steps in the transport of secretory proteins through the Golgi complex in exocrine pancreatic cells. Proc Natl Acad Sci USA 83: 6425–6429
Talbott RL, Sparger EE, Lovelace KM, Filch WM, Pedersen NC, Lucico PA, Elder JH (1989) Nucleotide sequence and genomic organization of feline immunodeficiency virus. Proc Natl Acad Sci USA 86: 5743–5747
Tartakoff AM (1986) Temperature and energy dependence of secretory protein transport in the exocrine pancreas. EMBO J 5: 1477–1482
Tooze J, Tooze SA, Warren G (1984) Replication of coronavirus MHV-A59 in sac(−) cells: determination of the first site of budding of progeny virions. Eur J Cell Biol 33: 291–293
Tooze SA, Tooze J, Warren G (1988) Site of addition of N-acetyl-galactosamine to the E 1 glycoprotein of mouse hepatitis virus-A 59. J Cell Biol 106: 1475–1487
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Morré, D.J., Paulik, M. Low temperature compartment formation in feline immunodeficiency virus-infected and uninfected feline kidney cells. Protoplasma 177, 15–22 (1993). https://doi.org/10.1007/BF01403394
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01403394