Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1994 Feb 1;13(3):562–574. doi: 10.1002/j.1460-2075.1994.tb06294.x

Kin recognition between medial Golgi enzymes in HeLa cells.

T Nilsson 1, M H Hoe 1, P Slusarewicz 1, C Rabouille 1, R Watson 1, F Hunte 1, G Watzele 1, E G Berger 1, G Warren 1
PMCID: PMC394845  PMID: 8313901

Abstract

The medial Golgi enzymes, N-acetylglucosaminyltransferase I (NAGT I) and mannosidase II (Mann II), and the trans Golgi enzyme, beta-1,4-galactosyltransferase (GalT) were each retained in the endoplasmic reticulum (ER) by grafting on the cytoplasmic tail of the p33 invariant chain. Transient and stable expression of p33/NAGT I in HeLa cells caused relocation of endogenous Mann II to the ER and transient expression of p33/Mann II had a similar effect on endogenous NAGT I. Neither of these endogenous medial enzymes were affected by transient expression of p33/GalT. These data provide strong evidence for kin recognition between medial Golgi enzymes and suggest a role for them in the organization of the Golgi stack.

Full text

PDF
562

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aoki D., Lee N., Yamaguchi N., Dubois C., Fukuda M. N. Golgi retention of a trans-Golgi membrane protein, galactosyltransferase, requires cysteine and histidine residues within the membrane-anchoring domain. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4319–4323. doi: 10.1073/pnas.89.10.4319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bakke O., Dobberstein B. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell. 1990 Nov 16;63(4):707–716. doi: 10.1016/0092-8674(90)90137-4. [DOI] [PubMed] [Google Scholar]
  3. Balch W. E., Keller D. S. ATP-coupled transport of vesicular stomatitis virus G protein. Functional boundaries of secretory compartments. J Biol Chem. 1986 Nov 5;261(31):14690–14696. [PubMed] [Google Scholar]
  4. Balch W. E., Rothman J. E. Characterization of protein transport between successive compartments of the Golgi apparatus: asymmetric properties of donor and acceptor activities in a cell-free system. Arch Biochem Biophys. 1985 Jul;240(1):413–425. doi: 10.1016/0003-9861(85)90046-3. [DOI] [PubMed] [Google Scholar]
  5. Berger E. G., Aegerter E., Mandel T., Hauri H. P. Monoclonal antibodies to soluble, human milk galactosyltransferase (lactose synthase A protein). Carbohydr Res. 1986 Jun 1;149(1):23–33. doi: 10.1016/s0008-6215(00)90366-5. [DOI] [PubMed] [Google Scholar]
  6. Bischoff J., Kornfeld R. The effect of 1-deoxymannojirimycin on rat liver alpha-mannosidases. Biochem Biophys Res Commun. 1984 Nov 30;125(1):324–331. doi: 10.1016/s0006-291x(84)80371-x. [DOI] [PubMed] [Google Scholar]
  7. Blobel G., Dobberstein B. Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J Cell Biol. 1975 Dec;67(3):835–851. doi: 10.1083/jcb.67.3.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bonay P., Hughes R. C. Purification and characterization of a novel broad-specificity (alpha 1----2, alpha 1----3 and alpha 1----6) mannosidase from rat liver. Eur J Biochem. 1991 Apr 10;197(1):229–238. doi: 10.1111/j.1432-1033.1991.tb15903.x. [DOI] [PubMed] [Google Scholar]
  9. Bonner W. M., Laskey R. A. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. doi: 10.1111/j.1432-1033.1974.tb03599.x. [DOI] [PubMed] [Google Scholar]
  10. Brands R., Snider M. D., Hino Y., Park S. S., Gelboin H. V., Rothman J. E. Retention of membrane proteins by the endoplasmic reticulum. J Cell Biol. 1985 Nov;101(5 Pt 1):1724–1732. doi: 10.1083/jcb.101.5.1724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Bretz R., Stäubli W. Detergent influence on rat-liver galactosyltransferase activities towards different acceptors. Eur J Biochem. 1977 Jul 1;77(1):181–192. doi: 10.1111/j.1432-1033.1977.tb11656.x. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Burke J., Pettitt J. M., Schachter H., Sarkar M., Gleeson P. A. The transmembrane and flanking sequences of beta 1,2-N-acetylglucosaminyltransferase I specify medial-Golgi localization. J Biol Chem. 1992 Dec 5;267(34):24433–24440. [PubMed] [Google Scholar]
  14. Colley K. J., Lee E. U., Paulson J. C. The signal anchor and stem regions of the beta-galactoside alpha 2,6-sialyltransferase may each act to localize the enzyme to the Golgi apparatus. J Biol Chem. 1992 Apr 15;267(11):7784–7793. [PubMed] [Google Scholar]
  15. Dean N., Pelham H. R. Recycling of proteins from the Golgi compartment to the ER in yeast. J Cell Biol. 1990 Aug;111(2):369–377. doi: 10.1083/jcb.111.2.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dunphy W. G., Brands R., Rothman J. E. Attachment of terminal N-acetylglucosamine to asparagine-linked oligosaccharides occurs in central cisternae of the Golgi stack. Cell. 1985 Feb;40(2):463–472. doi: 10.1016/0092-8674(85)90161-8. [DOI] [PubMed] [Google Scholar]
  17. Dunphy W. G., Fries E., Urbani L. J., Rothman J. E. Early and late functions associated with the Golgi apparatus reside in distinct compartments. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7453–7457. doi: 10.1073/pnas.78.12.7453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Dunphy W. G., Rothman J. E. Compartmentation of asparagine-linked oligosaccharide processing in the Golgi apparatus. J Cell Biol. 1983 Jul;97(1):270–275. doi: 10.1083/jcb.97.1.270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Evan G. I., Lewis G. K., Ramsay G., Bishop J. M. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol Cell Biol. 1985 Dec;5(12):3610–3616. doi: 10.1128/mcb.5.12.3610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Goldberg D. E., Kornfeld S. Evidence for extensive subcellular organization of asparagine-linked oligosaccharide processing and lysosomal enzyme phosphorylation. J Biol Chem. 1983 Mar 10;258(5):3159–3165. [PubMed] [Google Scholar]
  21. Hoe M. H., Hunt R. C. Loss of one asparagine-linked oligosaccharide from human transferrin receptors results in specific cleavage and association with the endoplasmic reticulum. J Biol Chem. 1992 Mar 5;267(7):4916–4923. [PubMed] [Google Scholar]
  22. 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]
  23. Jackson M. R., Nilsson T., Peterson P. A. Retrieval of transmembrane proteins to the endoplasmic reticulum. J Cell Biol. 1993 Apr;121(2):317–333. doi: 10.1083/jcb.121.2.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Khatra B. S., Herries D. G., Brew K. Some kinetic properties of human-milk galactosyl transferase. Eur J Biochem. 1974 May 15;44(2):537–560. doi: 10.1111/j.1432-1033.1974.tb03513.x. [DOI] [PubMed] [Google Scholar]
  25. Klausner R. D., Donaldson J. G., Lippincott-Schwartz J. Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol. 1992 Mar;116(5):1071–1080. doi: 10.1083/jcb.116.5.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kumar R., Yang J., Larsen R. D., Stanley P. Cloning and expression of N-acetylglucosaminyltransferase I, the medial Golgi transferase that initiates complex N-linked carbohydrate formation. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9948–9952. doi: 10.1073/pnas.87.24.9948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Locker J. K., Griffiths G., Horzinek M. C., Rottier P. J. O-glycosylation of the coronavirus M protein. Differential localization of sialyltransferases in N- and O-linked glycosylation. J Biol Chem. 1992 Jul 15;267(20):14094–14101. doi: 10.1016/S0021-9258(19)49683-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lotteau V., Teyton L., Peleraux A., Nilsson T., Karlsson L., Schmid S. L., Quaranta V., Peterson P. A. Intracellular transport of class II MHC molecules directed by invariant chain. Nature. 1990 Dec 13;348(6302):600–605. doi: 10.1038/348600a0. [DOI] [PubMed] [Google Scholar]
  31. Louvard D., Reggio H., Warren G. Antibodies to the Golgi complex and the rough endoplasmic reticulum. J Cell Biol. 1982 Jan;92(1):92–107. doi: 10.1083/jcb.92.1.92. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Moremen K. W., Robbins P. W. Isolation, characterization, and expression of cDNAs encoding murine alpha-mannosidase II, a Golgi enzyme that controls conversion of high mannose to complex N-glycans. J Cell Biol. 1991 Dec;115(6):1521–1534. doi: 10.1083/jcb.115.6.1521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Moremen K. W., Touster O. Biosynthesis and modification of Golgi mannosidase II in HeLa and 3T3 cells. J Biol Chem. 1985 Jun 10;260(11):6654–6662. [PubMed] [Google Scholar]
  34. Moremen K. W., Touster O., Robbins P. W. Novel purification of the catalytic domain of Golgi alpha-mannosidase II. Characterization and comparison with the intact enzyme. J Biol Chem. 1991 Sep 5;266(25):16876–16885. [PubMed] [Google Scholar]
  35. 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]
  36. Munro S. Sequences within and adjacent to the transmembrane segment of alpha-2,6-sialyltransferase specify Golgi retention. EMBO J. 1991 Dec;10(12):3577–3588. doi: 10.1002/j.1460-2075.1991.tb04924.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. 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]
  39. Nilsson T., Pypaert M., Hoe M. H., Slusarewicz P., Berger E. G., Warren G. Overlapping distribution of two glycosyltransferases in the Golgi apparatus of HeLa cells. J Cell Biol. 1993 Jan;120(1):5–13. doi: 10.1083/jcb.120.1.5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Nilsson T., Slusarewicz P., Hoe M. H., Warren G. Kin recognition. A model for the retention of Golgi enzymes. FEBS Lett. 1993 Sep 6;330(1):1–4. doi: 10.1016/0014-5793(93)80906-b. [DOI] [PubMed] [Google Scholar]
  41. Nishikawa Y., Pegg W., Paulsen H., Schachter H. Control of glycoprotein synthesis. Purification and characterization of rabbit liver UDP-N-acetylglucosamine:alpha-3-D-mannoside beta-1,2-N-acetylglucosaminyltransferase I. J Biol Chem. 1988 Jun 15;263(17):8270–8281. [PubMed] [Google Scholar]
  42. Orci L., Glick B. S., Rothman J. E. A new type of coated vesicular carrier that appears not to contain clathrin: its possible role in protein transport within the Golgi stack. Cell. 1986 Jul 18;46(2):171–184. doi: 10.1016/0092-8674(86)90734-8. [DOI] [PubMed] [Google Scholar]
  43. Pathak R. K., Merkle R. K., Cummings R. D., Goldstein J. L., Brown M. S., Anderson R. G. Immunocytochemical localization of mutant low density lipoprotein receptors that fail to reach the Golgi complex. J Cell Biol. 1988 Jun;106(6):1831–1841. doi: 10.1083/jcb.106.6.1831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Pinter A., Honnen W. J. O-linked glycosylation of retroviral envelope gene products. J Virol. 1988 Mar;62(3):1016–1021. doi: 10.1128/jvi.62.3.1016-1021.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Pypaert M., Mundy D., Souter E., Labbé J. C., Warren G. Mitotic cytosol inhibits invagination of coated pits in broken mitotic cells. J Cell Biol. 1991 Sep;114(6):1159–1166. doi: 10.1083/jcb.114.6.1159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Päbo S., Bhat B. M., Wold W. S., Peterson P. A. A short sequence in the COOH-terminus makes an adenovirus membrane glycoprotein a resident of the endoplasmic reticulum. Cell. 1987 Jul 17;50(2):311–317. doi: 10.1016/0092-8674(87)90226-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Quinn P., Griffiths G., Warren G. Density of newly synthesized plasma membrane proteins in intracellular membranes II. Biochemical studies. J Cell Biol. 1984 Jun;98(6):2142–2147. doi: 10.1083/jcb.98.6.2142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Rabouille C., Strous G. J., Crapo J. D., Geuze H. J., Slot J. W. The differential degradation of two cytosolic proteins as a tool to monitor autophagy in hepatocytes by immunocytochemistry. J Cell Biol. 1993 Feb;120(4):897–908. doi: 10.1083/jcb.120.4.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. 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]
  50. Russo R. N., Shaper N. L., Taatjes D. J., Shaper J. H. Beta 1,4-galactosyltransferase: a short NH2-terminal fragment that includes the cytoplasmic and transmembrane domain is sufficient for Golgi retention. J Biol Chem. 1992 May 5;267(13):9241–9247. [PubMed] [Google Scholar]
  51. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  52. 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]
  53. Sege K., Rask L., Peterson P. A. Role of beta2-microglobulin in the intracellular processing of HLA antigens. Biochemistry. 1981 Aug 4;20(16):4523–4530. doi: 10.1021/bi00519a003. [DOI] [PubMed] [Google Scholar]
  54. Sottocasa G. L., Kuylenstierna B., Ernster L., Bergstrand A. An electron-transport system associated with the outer membrane of liver mitochondria. A biochemical and morphological study. J Cell Biol. 1967 Feb;32(2):415–438. doi: 10.1083/jcb.32.2.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Strous G. J., Berger E. G. Biosynthesis, intracellular transport, and release of the Golgi enzyme galactosyltransferase (lactose synthetase A protein) in HeLa cells. J Biol Chem. 1982 Jul 10;257(13):7623–7628. [PubMed] [Google Scholar]
  56. Strubin M., Mach B., Long E. O. The complete sequence of the mRNA for the HLA-DR-associated invariant chain reveals a polypeptide with an unusual transmembrane polarity. EMBO J. 1984 Apr;3(4):869–872. doi: 10.1002/j.1460-2075.1984.tb01898.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Swift A. M., Machamer C. E. A Golgi retention signal in a membrane-spanning domain of coronavirus E1 protein. J Cell Biol. 1991 Oct;115(1):19–30. doi: 10.1083/jcb.115.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Tang B. L., Wong S. H., Low S. H., Hong W. The transmembrane domain of N-glucosaminyltransferase I contains a Golgi retention signal. J Biol Chem. 1992 May 15;267(14):10122–10126. [PubMed] [Google Scholar]
  59. Tarentino A. L., Maley F. Purification and properties of an endo-beta-N-acetylglucosaminidase from Streptomyces griseus. J Biol Chem. 1974 Feb 10;249(3):811–817. [PubMed] [Google Scholar]
  60. Teasdale R. D., D'Agostaro G., Gleeson P. A. The signal for Golgi retention of bovine beta 1,4-galactosyltransferase is in the transmembrane domain. J Biol Chem. 1992 Feb 25;267(6):4084–4096. [PubMed] [Google Scholar]
  61. Tokuyasu K. T. Immunochemistry on ultrathin frozen sections. Histochem J. 1980 Jul;12(4):381–403. doi: 10.1007/BF01011956. [DOI] [PubMed] [Google Scholar]
  62. 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]
  63. Tulsiani D. R., Opheim D. J., Touster O. Purification and characterization of alpha-D-mannosidase from rat liver golgi membranes. J Biol Chem. 1977 May 25;252(10):3227–3233. [PubMed] [Google Scholar]
  64. 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]
  65. Vischer P., Hughes R. C. Glycosyl transferases of baby-hamster-kidney (BHK) cells and ricin-resistant mutants. N-glycan biosynthesis. Eur J Biochem. 1981 Jul;117(2):275–284. doi: 10.1111/j.1432-1033.1981.tb06334.x. [DOI] [PubMed] [Google Scholar]
  66. Watzele G., Bachofner R., Berger E. G. Immunocytochemical localization of the Golgi apparatus using protein-specific antibodies to galactosyltransferase. Eur J Cell Biol. 1991 Dec;56(2):451–458. [PubMed] [Google Scholar]
  67. Watzele G., Berger E. G. Near identity of HeLa cell galactosyltransferase with the human placental enzyme. Nucleic Acids Res. 1990 Dec 11;18(23):7174–7174. doi: 10.1093/nar/18.23.7174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Wong S. H., Low S. H., Hong W. The 17-residue transmembrane domain of beta-galactoside alpha 2,6-sialyltransferase is sufficient for Golgi retention. J Cell Biol. 1992 Apr;117(2):245–258. doi: 10.1083/jcb.117.2.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Yamamoto A., Masaki R., Tashiro Y. Is cytochrome P-450 transported from the endoplasmic reticulum to the Golgi apparatus in rat hepatocytes? J Cell Biol. 1985 Nov;101(5 Pt 1):1733–1740. doi: 10.1083/jcb.101.5.1733. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES