Abstract
Pulse-chase experiments in conjunction with subcellular fractionation and quantitative immunoprecipitation have been used to study the intracellular transport of four secretory proteins, albumin, transferrin, prealbumin and retinol-binding protein, in isolated rat hepatocytes. The proteins were found to be transported from the endoplasmic reticulum (ER) to the Golgi complex (GC) at greatly different rates (t1/2 = 14-137 min), indicating that transport of secretory proteins between these organelles is effected by a selective, possibly receptor-mediated process and not through bulk phase transfers. The transport from the Golgi complex to the medium was rapid for all proteins (t1/2 approximately 15 min) and possibly occurred at the same rate. Consistent with these kinetic data, the amount of a rapidly transported protein (albumin) in the GC fraction was found to be high (relative to its amount in the ER fraction) whereas the amount of a slowly transported protein (transferrin) in the GC fraction was found to be low, as determined by radioimmunoassays.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bergeron J. J., Borts D., Cruz J. Passage of serum-destined proteins through the Golgi apparatus of rat liver. An examination of heavy and light Golgi fractions. J Cell Biol. 1978 Jan;76(1):87–97. doi: 10.1083/jcb.76.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carlson J., Stenflo J. The biosynthesis of rat alpha 1-antitrypsin. J Biol Chem. 1982 Nov 10;257(21):12987–12994. [PubMed] [Google Scholar]
- Dobberstein B., Garoff H., Warren G., Robinson P. J. Cell-free synthesis and membrane insertion of mouse H-2Dd histocompatibility antigen and beta 2-microglobulin. Cell. 1979 Aug;17(4):759–769. doi: 10.1016/0092-8674(79)90316-7. [DOI] [PubMed] [Google Scholar]
- Dulley J. R., Grieve P. A. A simple technique for eliminating interference by detergents in the Lowry method of protein determination. Anal Biochem. 1975 Mar;64(1):136–141. doi: 10.1016/0003-2697(75)90415-7. [DOI] [PubMed] [Google Scholar]
- Fitting T., Kabat D. Evidence for a glycoprotein "signal" involved in transport between subcellular organelles. Two membrane glycoproteins encoded by murine leukemia virus reach the cell surface at different rates. J Biol Chem. 1982 Dec 10;257(23):14011–14017. [PubMed] [Google Scholar]
- GORDON A. H., LOUIS L. N. PREPARATION AND PROPERTIES OF RAT TRANSFERRIN. Biochem J. 1963 Sep;88:409–414. doi: 10.1042/bj0880409. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HUNTER W. M., GREENWOOD F. C. Preparation of iodine-131 labelled human growth hormone of high specific activity. Nature. 1962 May 5;194:495–496. doi: 10.1038/194495a0. [DOI] [PubMed] [Google Scholar]
- Ikehara Y., Oda K., Kato K. Conversion of proalbumin into serum albumin in the secretory vesicles of rat liver. Biochem Biophys Res Commun. 1976 Sep 7;72(1):319–326. doi: 10.1016/0006-291x(76)90996-7. [DOI] [PubMed] [Google Scholar]
- Jamieson J. D., Palade G. E. Intracellular transport of secretory proteins in the pancreatic exocrine cell. IV. Metabolic requirements. J Cell Biol. 1968 Dec;39(3):589–603. doi: 10.1083/jcb.39.3.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knipe D. M., Lodish H. F., Baltimore D. Localization of two cellular forms of the vesicular stomatitis viral glycoprotein. J Virol. 1977 Mar;21(3):1121–1127. doi: 10.1128/jvi.21.3.1121-1127.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ledford B. E., Davis D. F. Kinetics of serum protein secretion by cultured hepatoma cells. Evidence for multiple secretory pathways. J Biol Chem. 1983 Mar 10;258(5):3304–3308. [PubMed] [Google Scholar]
- Lodish H. F., Kong N., Snider M., Strous G. J. Hepatoma secretory proteins migrate from rough endoplasmic reticulum to Golgi at characteristic rates. Nature. 1983 Jul 7;304(5921):80–83. doi: 10.1038/304080a0. [DOI] [PubMed] [Google Scholar]
- Morgan E. H., Peters T., Jr Intracellular aspects of transferrin synthesis and secretion in the rat. J Biol Chem. 1971 Jun 10;246(11):3508–3511. [PubMed] [Google Scholar]
- Muto Y., Smith J. E., Milch P. O., Goodman D. S. Regulation of retinol-binding protein metabolism by vitamin A status in the rat. J Biol Chem. 1972 Apr 25;247(8):2542–2550. [PubMed] [Google Scholar]
- Ohanian S. H., Taubman S. B., Thorbecke G. J. Rates of albumin and transferrin synthesis in vitro in rat hepatoma-derived H4II-EC cells. J Natl Cancer Inst. 1969 Aug;43(2):397–406. [PubMed] [Google Scholar]
- Omura T., Takesue S. A new method for simultaneous purification of cytochrome b5 and NADPH-cytochrome c reductase from rat liver microsomes. J Biochem. 1970 Feb;67(2):249–257. doi: 10.1093/oxfordjournals.jbchem.a129248. [DOI] [PubMed] [Google Scholar]
- PETERS T., Jr The biosynthesis of rat serum albumin. I. Properties of rat albumin and its occurrence in liver cell fractions. J Biol Chem. 1962 Apr;237:1181–1185. [PubMed] [Google Scholar]
- Peterson P. A., Rask L., Ostberg L., Andersson L., Kamwendo F., Pertoft H. Studies on the transport and cellular distribution of vitamin A in normal and vitamin A-deficient rats with special reference to the vitamin A-binding plasma protein. J Biol Chem. 1973 Jun 10;248(11):4009–4022. [PubMed] [Google Scholar]
- Rask L., Geijer C., Bill A., Peterson P. A. Vitamin A supply of the cornea. Exp Eye Res. 1980 Aug;31(2):201–211. doi: 10.1016/0014-4835(80)90078-0. [DOI] [PubMed] [Google Scholar]
- Rask L., Valtersson C., Anundi H., Kvist S., Eriksson U., Dallner G., Peterson P. A. Subcellular localization in normal and vitamin A-deficient rat liver of vitamin A serum transport proteins, albumin, ceruloplasmin and class I major histocompatibility antigens. Exp Cell Res. 1983 Jan;143(1):91–102. doi: 10.1016/0014-4827(83)90112-x. [DOI] [PubMed] [Google Scholar]
- Ronne H., Ocklind C., Wiman K., Rask L., Obrink B., Peterson P. A. Ligand-dependent regulation of intracellular protein transport: effect of vitamin a on the secretion of the retinol-binding protein. J Cell Biol. 1983 Mar;96(3):907–910. doi: 10.1083/jcb.96.3.907. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roth J., Berger E. G. Immunocytochemical localization of galactosyltransferase in HeLa cells: codistribution with thiamine pyrophosphatase in trans-Golgi cisternae. J Cell Biol. 1982 Apr;93(1):223–229. doi: 10.1083/jcb.93.1.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rothman J. E., Fries E. Transport of newly synthesized vesicular stomatitis viral glycoprotein to purified Golgi membranes. J Cell Biol. 1981 Apr;89(1):162–168. doi: 10.1083/jcb.89.1.162. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rubin K., Kjellén L., Obrink B. Intercellular adhesion between juvenile liver cells. A method to measure the formation of stable lateral contacts between cells attached to a collagen gel. Exp Cell Res. 1977 Oct 15;109(2):413–422. doi: 10.1016/0014-4827(77)90021-0. [DOI] [PubMed] [Google Scholar]
- Sabatini D. D., Kreibich G., Morimoto T., Adesnik M. Mechanisms for the incorporation of proteins in membranes and organelles. J Cell Biol. 1982 Jan;92(1):1–22. doi: 10.1083/jcb.92.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scheele G. A., Palade G. E., Tartakoff A. M. Cell fractionation studies on the guinea pig pancreas. Redistribution of exocrine proteins during tissue homogenization. J Cell Biol. 1978 Jul;78(1):110–130. doi: 10.1083/jcb.78.1.110. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schreiber G., Dryburgh H., Millership A., Matsuda Y., Inglis A., Phillips J., Edwards K., Maggs J. The synthesis and secretion of rat transferrin. J Biol Chem. 1979 Dec 10;254(23):12013–12019. [PubMed] [Google Scholar]
- Smith J. E., Muto Y., Milch P. O., Goodman D. S. The effects of chylomicron vitamin A on the metabolism of retinol-binding protein in the rat. J Biol Chem. 1973 Mar 10;248(5):1544–1549. [PubMed] [Google Scholar]
- Strous G. J., Lodish H. F. Intracellular transport of secretory and membrane proteins in hepatoma cells infected by vesicular stomatitis virus. Cell. 1980 Dec;22(3):709–717. doi: 10.1016/0092-8674(80)90547-4. [DOI] [PubMed] [Google Scholar]
- Tartakoff A. M. The Golgi complex: crossroads for vesicular traffic. Int Rev Exp Pathol. 1980;22:227–251. [PubMed] [Google Scholar]
- Tartakoff A., Vassalli P. Plasma cell immunoglobulin M molecules. Their biosynthesis, assembly, and intracellular transport. J Cell Biol. 1979 Nov;83(2 Pt 1):284–299. doi: 10.1083/jcb.83.2.284. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Travis J., Bowen J., Tewksbury D., Johnson D., Pannell R. Isolation of albumin from whole human plasma and fractionation of albumin-depleted plasma. Biochem J. 1976 Aug 1;157(2):301–306. doi: 10.1042/bj1570301. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vretblad P., Hjorth R. The use of wheat-germ lectin-Sepharose for the purification of human haemopexin. Biochem J. 1977 Dec 1;167(3):759–764. doi: 10.1042/bj1670759. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wu G. E., Hozumi N., Murialdo H. Secretion of a lambda 2 immunoglobulin chain is prevented by a single amino acid substitution in its variable region. Cell. 1983 May;33(1):77–83. doi: 10.1016/0092-8674(83)90336-7. [DOI] [PubMed] [Google Scholar]
- Yokota S., Fahimi H. D. Immunocytochemical localization of albumin in the secretory apparatus of rat liver parenchymal cells. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4970–4974. doi: 10.1073/pnas.78.8.4970. [DOI] [PMC free article] [PubMed] [Google Scholar]