Abstract
A COOH-terminal double lysine motif maintains type I transmembrane proteins in the ER. Proteins tagged with this motif, eg., CD8/E19 and CD4/E19, rapidly receive post-translational modifications characteristic of the intermediate compartment and partially colocalized to this organelle. These proteins also received modifications characteristic of the Golgi but much more slowly. Lectin staining localized these Golgi modified proteins to ER indicating that this motif is a retrieval signal. Differences in the subcellular distribution and rate of post-translational modification of CD8 maintained in the ER by sequences derived from a variety of ER resident proteins suggested that the efficiency of retrieval was dependent on the sequence context of the double lysine motif and that retrieval may be initiated from multiple positions along the exocytotic pathway.
Full Text
The Full Text of this article is available as a PDF (8.1 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Beckers C. J., Keller D. S., Balch W. E. Semi-intact cells permeable to macromolecules: use in reconstitution of protein transport from the endoplasmic reticulum to the Golgi complex. Cell. 1987 Aug 14;50(4):523–534. doi: 10.1016/0092-8674(87)90025-0. [DOI] [PubMed] [Google Scholar]
- Bole D. G., Hendershot L. M., Kearney J. F. Posttranslational association of immunoglobulin heavy chain binding protein with nascent heavy chains in nonsecreting and secreting hybridomas. J Cell Biol. 1986 May;102(5):1558–1566. doi: 10.1083/jcb.102.5.1558. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bonatti S., Migliaccio G., Simons K. Palmitylation of viral membrane glycoproteins takes place after exit from the endoplasmic reticulum. J Biol Chem. 1989 Jul 25;264(21):12590–12595. [PubMed] [Google Scholar]
- Booth C., Koch G. L. Perturbation of cellular calcium induces secretion of luminal ER proteins. Cell. 1989 Nov 17;59(4):729–737. doi: 10.1016/0092-8674(89)90019-6. [DOI] [PubMed] [Google Scholar]
- Bulleid N. J., Graham A. B., Craft J. A. Microsomal epoxide hydrolase of rat liver. Purification and characterization of enzyme fractions with different chromatographic characteristics. Biochem J. 1986 Jan 15;233(2):607–611. doi: 10.1042/bj2330607. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burke B., Griffiths G., Reggio H., Louvard D., Warren G. A monoclonal antibody against a 135-K Golgi membrane protein. EMBO J. 1982;1(12):1621–1628. doi: 10.1002/j.1460-2075.1982.tb01364.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buss J. E., Sefton B. M. Direct identification of palmitic acid as the lipid attached to p21ras. Mol Cell Biol. 1986 Jan;6(1):116–122. doi: 10.1128/mcb.6.1.116. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chavrier P., Parton R. G., Hauri H. P., Simons K., Zerial M. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell. 1990 Jul 27;62(2):317–329. doi: 10.1016/0092-8674(90)90369-p. [DOI] [PubMed] [Google Scholar]
- De Brabander M. J., Van de Veire R. M., Aerts F. E., Borgers M., Janssen P. A. The effects of methyl (5-(2-thienylcarbonyl)-1H-benzimidazol-2-yl) carbamate, (R 17934; NSC 238159), a new synthetic antitumoral drug interfering with microtubules, on mammalian cells cultured in vitro. Cancer Res. 1976 Mar;36(3):905–916. [PubMed] [Google Scholar]
- Deschuyteneer M., Eckhardt A. E., Roth J., Hill R. L. The subcellular localization of apomucin and nonreducing terminal N-acetylgalactosamine in porcine submaxillary glands. J Biol Chem. 1988 Feb 15;263(5):2452–2459. [PubMed] [Google Scholar]
- Farquhar M. G. Progress in unraveling pathways of Golgi traffic. Annu Rev Cell Biol. 1985;1:447–488. doi: 10.1146/annurev.cb.01.110185.002311. [DOI] [PubMed] [Google Scholar]
- Galteau M. M., Antoine B., Reggio H. Epoxide hydrolase is a marker for the smooth endoplasmic reticulum in rat liver. EMBO J. 1985 Nov;4(11):2793–2800. doi: 10.1002/j.1460-2075.1985.tb04005.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hammarström S., Kabat E. A. Purification and characterization of a blood-group A reactive hemagglutinin from the snail Helix pomatia and a study of its combining site. Biochemistry. 1969 Jul;8(7):2696–2705. doi: 10.1021/bi00835a002. [DOI] [PubMed] [Google Scholar]
- Hauri H. P., Schweizer A. The endoplasmic reticulum-Golgi intermediate compartment. Curr Opin Cell Biol. 1992 Aug;4(4):600–608. doi: 10.1016/0955-0674(92)90078-Q. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Holmes N., Ennis P., Wan A. M., Denney D. W., Parham P. Multiple genetic mechanisms have contributed to the generation of the HLA-A2/A28 family of class I MHC molecules. J Immunol. 1987 Aug 1;139(3):936–941. [PubMed] [Google Scholar]
- Hortsch M., Meyer D. I. Immunochemical analysis of rough and smooth microsomes from rat liver. Segregation of docking protein in rough membranes. Eur J Biochem. 1985 Aug 1;150(3):559–564. doi: 10.1111/j.1432-1033.1985.tb09057.x. [DOI] [PubMed] [Google Scholar]
- Hsu V. W., Yuan L. C., Nuchtern J. G., Lippincott-Schwartz J., Hammerling G. J., Klausner R. D. A recycling pathway between the endoplasmic reticulum and the Golgi apparatus for retention of unassembled MHC class I molecules. Nature. 1991 Aug 1;352(6334):441–444. doi: 10.1038/352441a0. [DOI] [PubMed] [Google Scholar]
- Hurtley S. M., Helenius A. Protein oligomerization in the endoplasmic reticulum. Annu Rev Cell Biol. 1989;5:277–307. doi: 10.1146/annurev.cb.05.110189.001425. [DOI] [PubMed] [Google Scholar]
- Jackson M. R., McCarthy L. R., Harding D., Wilson S., Coughtrie M. W., Burchell B. Cloning of a human liver microsomal UDP-glucuronosyltransferase cDNA. Biochem J. 1987 Mar 1;242(2):581–588. doi: 10.1042/bj2420581. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jackson M. R., Nilsson T., Peterson P. A. Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum. EMBO J. 1990 Oct;9(10):3153–3162. doi: 10.1002/j.1460-2075.1990.tb07513.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kornfeld R., Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem. 1985;54:631–664. doi: 10.1146/annurev.bi.54.070185.003215. [DOI] [PubMed] [Google Scholar]
- Lewis M. J., Pelham H. R. A human homologue of the yeast HDEL receptor. Nature. 1990 Nov 8;348(6297):162–163. doi: 10.1038/348162a0. [DOI] [PubMed] [Google Scholar]
- Lewis M. J., Pelham H. R. Ligand-induced redistribution of a human KDEL receptor from the Golgi complex to the endoplasmic reticulum. Cell. 1992 Jan 24;68(2):353–364. doi: 10.1016/0092-8674(92)90476-s. [DOI] [PubMed] [Google Scholar]
- Lippincott-Schwartz J., Donaldson J. G., Schweizer A., Berger E. G., Hauri H. P., Yuan L. C., Klausner R. D. Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell. 1990 Mar 9;60(5):821–836. doi: 10.1016/0092-8674(90)90096-w. [DOI] [PubMed] [Google Scholar]
- Lippincott-Schwartz J., Yuan L. C., Bonifacino J. S., Klausner R. D. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell. 1989 Mar 10;56(5):801–813. doi: 10.1016/0092-8674(89)90685-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Littman D. R., Thomas Y., Maddon P. J., Chess L., Axel R. The isolation and sequence of the gene encoding T8: a molecule defining functional classes of T lymphocytes. Cell. 1985 Feb;40(2):237–246. doi: 10.1016/0092-8674(85)90138-2. [DOI] [PubMed] [Google Scholar]
- Maddon P. J., Littman D. R., Godfrey M., Maddon D. E., Chess L., Axel R. The isolation and nucleotide sequence of a cDNA encoding the T cell surface protein T4: a new member of the immunoglobulin gene family. Cell. 1985 Aug;42(1):93–104. doi: 10.1016/s0092-8674(85)80105-7. [DOI] [PubMed] [Google Scholar]
- Mazzarella R. A., Srinivasan M., Haugejorden S. M., Green M. ERp72, an abundant luminal endoplasmic reticulum protein, contains three copies of the active site sequences of protein disulfide isomerase. J Biol Chem. 1990 Jan 15;265(2):1094–1101. [PubMed] [Google Scholar]
- Munro S., Pelham H. R. A C-terminal signal prevents secretion of luminal ER proteins. Cell. 1987 Mar 13;48(5):899–907. doi: 10.1016/0092-8674(87)90086-9. [DOI] [PubMed] [Google Scholar]
- Nilsson T., Jackson M., Peterson P. A. Short cytoplasmic sequences serve as retention signals for transmembrane proteins in the endoplasmic reticulum. Cell. 1989 Aug 25;58(4):707–718. doi: 10.1016/0092-8674(89)90105-0. [DOI] [PubMed] [Google Scholar]
- Nilsson T., Lucocq J. M., Mackay D., Warren G. The membrane spanning domain of beta-1,4-galactosyltransferase specifies trans Golgi localization. EMBO J. 1991 Dec;10(12):3567–3575. doi: 10.1002/j.1460-2075.1991.tb04923.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pascale M. C., Malagolini N., Serafini-Cessi F., Migliaccio G., Leone A., Bonatti S. Biosynthesis and oligosaccharide structure of human CD8 glycoprotein expressed in a rat epithelial cell line. J Biol Chem. 1992 May 15;267(14):9940–9947. [PubMed] [Google Scholar]
- Pelham H. R. Control of protein exit from the endoplasmic reticulum. Annu Rev Cell Biol. 1989;5:1–23. doi: 10.1146/annurev.cb.05.110189.000245. [DOI] [PubMed] [Google Scholar]
- Pelham H. R. Evidence that luminal ER proteins are sorted from secreted proteins in a post-ER compartment. EMBO J. 1988 Apr;7(4):913–918. doi: 10.1002/j.1460-2075.1988.tb02896.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pfeffer S. R., Rothman J. E. Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi. Annu Rev Biochem. 1987;56:829–852. doi: 10.1146/annurev.bi.56.070187.004145. [DOI] [PubMed] [Google Scholar]
- Piller V., Piller F., Fukuda M. Biosynthesis of truncated O-glycans in the T cell line Jurkat. Localization of O-glycan initiation. J Biol Chem. 1990 Jun 5;265(16):9264–9271. [PubMed] [Google Scholar]
- Piller V., Piller F., Klier F. G., Fukuda M. O-glycosylation of leukosialin in K562 cells. Evidence for initiation and elongation in early Golgi compartments. Eur J Biochem. 1989 Jul 15;183(1):123–135. doi: 10.1111/j.1432-1033.1989.tb14904.x. [DOI] [PubMed] [Google Scholar]
- Rose J. K., Doms R. W. Regulation of protein export from the endoplasmic reticulum. Annu Rev Cell Biol. 1988;4:257–288. doi: 10.1146/annurev.cb.04.110188.001353. [DOI] [PubMed] [Google Scholar]
- Roth J. Cytochemical localization of terminal N-acetyl-D-galactosamine residues in cellular compartments of intestinal goblet cells: implications for the topology of O-glycosylation. J Cell Biol. 1984 Feb;98(2):399–406. doi: 10.1083/jcb.98.2.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rothman J. E. The golgi apparatus: two organelles in tandem. Science. 1981 Sep 11;213(4513):1212–1219. doi: 10.1126/science.7268428. [DOI] [PubMed] [Google Scholar]
- Saraste J., Kuismanen E. Pre- and post-Golgi vacuoles operate in the transport of Semliki Forest virus membrane glycoproteins to the cell surface. Cell. 1984 Sep;38(2):535–549. doi: 10.1016/0092-8674(84)90508-7. [DOI] [PubMed] [Google Scholar]
- Saraste J., Palade G. E., Farquhar M. G. Antibodies to rat pancreas Golgi subfractions: identification of a 58-kD cis-Golgi protein. J Cell Biol. 1987 Nov;105(5):2021–2029. doi: 10.1083/jcb.105.5.2021. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saraste J., Svensson K. Distribution of the intermediate elements operating in ER to Golgi transport. J Cell Sci. 1991 Nov;100(Pt 3):415–430. doi: 10.1242/jcs.100.3.415. [DOI] [PubMed] [Google Scholar]
- Schultz A. M., Henderson L. E., Oroszlan S. Fatty acylation of proteins. Annu Rev Cell Biol. 1988;4:611–647. doi: 10.1146/annurev.cb.04.110188.003143. [DOI] [PubMed] [Google Scholar]
- Schweizer A., Fransen J. A., Bächi T., Ginsel L., Hauri H. P. Identification, by a monoclonal antibody, of a 53-kD protein associated with a tubulo-vesicular compartment at the cis-side of the Golgi apparatus. J Cell Biol. 1988 Nov;107(5):1643–1653. doi: 10.1083/jcb.107.5.1643. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schweizer A., Fransen J. A., Matter K., Kreis T. E., Ginsel L., Hauri H. P. Identification of an intermediate compartment involved in protein transport from endoplasmic reticulum to Golgi apparatus. Eur J Cell Biol. 1990 Dec;53(2):185–196. [PubMed] [Google Scholar]
- Schweizer A., Matter K., Ketcham C. M., Hauri H. P. The isolated ER-Golgi intermediate compartment exhibits properties that are different from ER and cis-Golgi. J Cell Biol. 1991 Apr;113(1):45–54. doi: 10.1083/jcb.113.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scragg I., Celier C., Burchell B. Congenital jaundice in rats due to the absence of hepatic bilirubin UDP-glucuronyltransferase enzyme protein. FEBS Lett. 1985 Apr 8;183(1):37–42. doi: 10.1016/0014-5793(85)80949-2. [DOI] [PubMed] [Google Scholar]
- Sundelin J., Melhus H., Das S., Eriksson U., Lind P., Trägårdh L., Peterson P. A., Rask L. The primary structure of rabbit and rat prealbumin and a comparison with the tertiary structure of human prealbumin. J Biol Chem. 1985 May 25;260(10):6481–6487. [PubMed] [Google Scholar]
- Suzuki C. K., Bonifacino J. S., Lin A. Y., Davis M. M., Klausner R. D. Regulating the retention of T-cell receptor alpha chain variants within the endoplasmic reticulum: Ca(2+)-dependent association with BiP. J Cell Biol. 1991 Jul;114(2):189–205. doi: 10.1083/jcb.114.2.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tooze S. A., Tooze J., Warren G. Site of addition of N-acetyl-galactosamine to the E1 glycoprotein of mouse hepatitis virus-A59. J Cell Biol. 1988 May;106(5):1475–1487. doi: 10.1083/jcb.106.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vaux D., Tooze J., Fuller S. Identification by anti-idiotype antibodies of an intracellular membrane protein that recognizes a mammalian endoplasmic reticulum retention signal. Nature. 1990 Jun 7;345(6275):495–502. doi: 10.1038/345495a0. [DOI] [PubMed] [Google Scholar]
- Warren G. Protein transport. Signals and salvage sequences. Nature. 1987 May 7;327(6117):17–18. doi: 10.1038/327017a0. [DOI] [PubMed] [Google Scholar]
- Wieland F. T., Gleason M. L., Serafini T. A., Rothman J. E. The rate of bulk flow from the endoplasmic reticulum to the cell surface. Cell. 1987 Jul 17;50(2):289–300. doi: 10.1016/0092-8674(87)90224-8. [DOI] [PubMed] [Google Scholar]
- Zagouras P., Rose J. K. Carboxy-terminal SEKDEL sequences retard but do not retain two secretory proteins in the endoplasmic reticulum. J Cell Biol. 1989 Dec;109(6 Pt 1):2633–2640. doi: 10.1083/jcb.109.6.2633. [DOI] [PMC free article] [PubMed] [Google Scholar]