Abstract
Retinol stimulates the formation of transition vesicles in situ and in all free systems based on rat liver. The stimulation is on vesicle formation from transitional endoplasmic reticulum and not on vesicle fusion with donor membranes. Vesicle budding in the cell free system requires a nucleoside triphosphate and is sensitive to inhibition by thiol reagents. In this report we develop and test a model whereby a retinol-modulated NADH:protein disulfide reductase (NADH oxidase) with protein disulfide-thiol interchange activity is implicated in the vesicle budding mechanism. The protein has the ability to restore activity to scrambled, inactive RNase A and is stimulated or inhibited by retinol depending on the redox environment. Under reducing conditions and in the presence of a chemical reductant such as GSH, the partial reaction stimulated by retinol appears to be the oxidation of membrane disulfides. This is the first report of an enzymatic mechanism to explain specific retinol effects both in vivo and in vitro on membrane trafficking not given by retinoic acid.
Similar content being viewed by others
References
Morré DJ: The Golgi apparatus. Int Rev Cytol Suppl 17: 211-253, 1987
Morré DM: Intracellular actions of vitamin A. Int Rev Cytol 135: 1-38, 1992
Nowack DD, Morré DM, Paulik M, Keenan TW, Morré DJ: Intracellular membrane flow: Reconstitution of transition vesicle formation and function in a cell-free system. Proc Natl Acad Sci USA 84: 6098-6102, 1987
Balch WE: Biochemistry of interorganelle transport. J Biol Chem 264: 16965-16968, 1989
Barlowe C, Orci L, Yeung T, Hosobuchi M, Hamamoto S, Salama N, Rexach MF, Ravazzoia M, Amherdt M, Schekman R: COPII: A membrane coat formed by sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77: 895-907, 1994
Morré DJ: Hormone-and growth factor-stimulated NADH oxidase. J Bioenerg Biomemb 26: 421-433, 1994
Locke M, Huie P: Golgi complex-endoplasmic reticulum transition region has rings of beads. Science 188: 1219-1221, 1975
Nowack DD, Paulik M, Morré DJ, Morré DM: Retinol modulation of cell-free membrane transfer between endoplasmic reticulum and Golgi apparatus. Biochim Biophys Acta 1051: 250-258, 1990
Jacobs E, Morré DJ, de Cabo R, Sweeting M, Morré DM: Response of a protein disulfide isomerase like activity of transitional endoplasmic reticulum to all trans-retinol. Life Sci 59: 273-284, 1996
Chueh P-J, Morré DM, Penel C, DeHahn T, Morré DJ: The hormoneresponsive NADH oxidase of the plant plasma membrane has properties of a NADH:protein disulfide reductase. J Biol Chem 272: 11221-11227, 1997
Brightman AO, Wang J, Miu R-K: A growth factor-and hormonestimulated NADH oxidase from rat liver plasma membrane. Biochim Biophys Acta 1105: 109-117, 1992
Morré DJ, Chueh P-J, Morré DM: Capsaicin inhibits preferentially the NADH oxidase and growth of transformed cells in culture. Proc Natl Acad Sci USA 92: 1831-1835, 1995
Morré DJ: Isolation of Golgi apparatus. Meth Enzymol 22: 130-148, 1971
Morré DJ: Isolation and purification of organelles and endomembrane components from rat liver. In: M.J. Chrispeels (ed). Molecular Techniques and Approaches in Developmental Biology. Wiley, New York, 1973, pp 1-27
Lyles MM, Gilbert HF: Catalysis of the oxidative unfolding of ribonuclease A by protein disulfide isomerase: Dependence of the rate on the composition of the redox buffer. Biochemistry 30: 613-619, 1991
Hillson DA, Lambert N, Freedman RB: Formation and isomerization of disulfide bonds in proteins. Meth Enzymol 107: 281-292, 1984
Kalnitsky G, Hummel JP, Dierks C: Some factors which affect the enzymatic digestion of ribonucleic acid. J Biol Chem 234: 1512-1519, 1959
Ellman GL: Tissue sulfhydryl groups. Arch Biochem Biophys 82: 70-77, 1959
Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FD, Provenzano MD, Fugimoto EK, Goeke NM, Olson BJ, Klenk DC: Measurement of protein using bicinchoninic acid. Anal Biochem 150: 70-76, 1985
Sporn MB, Roberts AB, Goodman DS, (eds): The Retinoids. Academic Press, Orlando, Fl, Vols 1 and 2, 1984
Sherman MI: Retinoids and Cell Differentiation. CRS Press, Boca Ration, FL, 1986, p 162
Jetten AM: In: G. Guroff (ed). Growth and Maturation Factors. Wiley (Interscience), New York, 1985, 3: 221
Pawson BA, Ehmann CW, Itri LM, Sherman MI: Retinoids at the threshold: their biological significance and therapeutic potential. J Med Chem 25 (11): 1269-1277, 1982
Nyquist SE, Crane FL, Morré DJ: Vitamin A: Concentration in the rat liver Golgi apparatus. Science 173: 939-941, 1971
Wolf G: In: R.B. Alfin-Slater, D. Krischevsky (eds). Nutrition and the Adult, Micronutrients. Plenum, New York, 1980, p 97
Morré DM, Morré DJ, Walter M: Vitamin A effects on hepatic Golgi apparatus architecture. Eur J Cell Biol 25: 28-35, 1981
Morré DM, Morré DJ, Bowen S, Reutter WW, Windel K: Vitamin A excess alters membrane flow in rat liver. Eur J Cell Biol 46: 306-315, 1988
Martin BR, Morré DM: Excess vitamin A decreases the specific activity of galactosyltransferase in Golgi apparatus of rat liver. J Nutr 118: 968-975, 1988
Hayes KC, Combs HL, Faherty TB: The fine structure of vitamin A deficiency. l. Parotid duct metaplasia. Lab Invest 22: 81-89, 1970
Prutkin L: Mucous metaplasia and gap junctions in the vitamin A acidtreated skin tumor, keratoacanthoma. Cancer Res 35: 364-369, 1975
Chertow BS, Buschmann RJ, Henderson WJ: Subcellular mechanisms of parathyroid hormone secretion: Ultrastructural changes in response to calcium, vitamin A, vinblastine, and cytochalasin B. Lab Invest 32: 190-200, 1975
Morré DJ, Morré DM: Transition vesicles of the cis Golgi apparatus face of rat liver are increased by retinol. Cell Biol Rep Int 11: 89-93, 1987
Ziegel RF, Dalton AJ: Speculations based on the morphology of the Golgi system in several types of protein secreting cells. J Cell Biol 15: 45-54, 1962
Morré DJ, Mollenhauer HH, Bracker CE: In: J. Reinert, H. Ursprung (eds). Results and Problems in Cell Differentiation: Origin and Continuity of Cell Organelles. Springer-Verlag, Berlin, 1971, 2: pp 82-126
Morré DJ, Paulik M, Nowack D: Transition vesicle formation in vitro. Protoplasma 132: 110-113, 1986
Morré DM, Spring H, Trendlenburg M, Montag M, Mollenhauer BA, Mollenhauer HH, Morré DJ: Retinol stimulates Golgi apparatus activity in cultured bovine mammary gland epithelial cells. J Nutr 122: 1248-1253, 1992
Spring H, Franke WW: Transcriptionally active chromatin in loops of lampbrush chromosomes at physiological salt concentrations as revealed by electron microscopy of sections. Eur J Cell Biol 24: 298-308, 1981
Rodriguez M, Moreau P, Paulik M, Lawrence J, Morré DJ, Morré DM: NADH-activated cell-free transfer between Golgi apparatus and plasma membranes of rat liver. Biochim Biophys Acta 1107: 131-138, 1992
Thannhauser TW, Konishi Y, Scheraga HA: Sensitive quantitative analysis of disulfide bonds in polypeptides and proteins. Anal Biochem 138: 181-188, 1984
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Morré, D.M., Wang, S., Chueh, PJ. et al. A molecular basis for retinol stimulation of vesicle budding in vivo and in vitro. Mol Cell Biochem 187, 73–83 (1998). https://doi.org/10.1023/A:1006839911682
Issue Date:
DOI: https://doi.org/10.1023/A:1006839911682