Elevated golgi pH impairs terminal N-glycosylation by inducing mislocalization of golgi glycosyltransferases

Journal of Cellular Physiology

Volumn 220, Issue 1, 2009, Pages 144-154

  Rivinoja, Antti ^a   Hassinen, Antti ^a   Kokkonen, Nina ^a   Kauppila, Annika ^a   Kellokumpu, Sakari ^a  

^a UNIVERSITY OF OULU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDE ALPHA(2,6)SIALYLTRANSFERASE I; BETA(1,4)GALACTOSYLTRANSFERASE; CARCINOEMBRYONIC ANTIGEN; CHLOROQUINE; GALACTOSYLTRANSFERASE; GLYCOSYLTRANSFERASE; MANNOSIDASE; MANNOSYL OLIGOSACCHARIDE (1,3-1,6)ALPHA MANNOSIDASE II; N ACETYLLACTOSAMINIDE ALPHA(2,3)SIALYLTRANSFERASE III; SIALYLTRANSFERASE; UNCLASSIFIED DRUG; HYBRID PROTEIN;

ACIDITY; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME LOCALIZATION; GLYCOSYLATION; GOLGI COMPLEX; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DOMAIN; SIALYLATION; ANIMAL; CELL STRAIN COS1; CERCOPITHECUS; DOSE RESPONSE; DRUG EFFECT; ENDOSOME; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; LYSOSOME; METABOLISM; MUTATION; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; TIME;

ANIMALS; CARCINOEMBRYONIC ANTIGEN; CERCOPITHECUS AETHIOPS; CHLOROQUINE; COS CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOSOMES; GALACTOSYLTRANSFERASES; GLYCOSYLATION; GLYCOSYLTRANSFERASES; GOLGI APPARATUS; HYDROGEN-ION CONCENTRATION; LYSOSOMES; MANNOSIDASES; MUTATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SIALYLTRANSFERASES; TIME FACTORS; TRANSFECTION;

EID: 65549131351     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21744     Document Type: Article

References (60)

1. Axelsson MA, Karlsson NG, Steel DM, Ouwendijk J, Nilsson T, Hansson GC. 2001. Neutralization of pH in the Golgi apparatus causes redistribution of glycosyltransferases and changes in the O-glycosylation of mucins. Glycobiology 11:633-644.
2. Bachert C, Lee TH, Linstedt AD. 2001. Lumenal endosomal and Golgi-retrieval determinants involved in pH-sensitive targeting of an early Golgi protein. Mol Biol Cell 12:3152-3160.
3. Berger EG. 2002. Ectopic localizations of Golgi glycosyltransferases. Glycobiology 12:29R-36R.
4. Berger EG, Grimm K, Bachi T, Bosshart H, Kleene R, Watzele M. 1993. Double immunofluorescent staining of alpha 2,6 sialyltransferase and beta 1,4 galactosyltransferase in monensin-treated cells: Evidence for different Golgi compartments? J Cell Biochem 52:275-288.
5. Bonifacino JS, Rojas R. 2006. Retrograde transport from endosomes to the trans-Golgi network. Nat Rev Mol Cell Biol 7:568-579.
6. Burger PC, Lotscher M, Sreiff M, Kleene R, Kaissling B, Berger EG. 1998. Immunocytochemical localization of alpha2,3(N)-sialyltransferase (ST3Gal III) in cell lines and rat kidney tissue sections: Evidence for Golgi and post-Golgi localization. Glycobiology 8:245-257.
7. Campbell BJ, Rowe GE, Leiper K, Rhodes JM. 2001. Increasing the intra-Golgi pH of cultured LS174T goblet-differentiated cells mimics the decreased mucin sulfation and increased thomsen-friedenreich antigen (gal beta1-3GalNac alpha-) expression seen in colon cancer. Glycobiology 11:385-393.
8. Chapman RE, Munro S. 1994. Retrieval of TGN proteins from the cell surface requires endosomal acidification. EMBO J 13:2305-2312.
9. Chen JW, Murphy TL, Willingham MC, Pastan I, August JT. 1985. Identification of two lysosomal membrane glycoproteins. J Cell Biol 101:85-95.
10. Colley KJ. 1997. Golgi localization of glycosyltransferases: More questions than answers. Glycobiology 7:1-13.
11. Crowley JF, Goldstein IJ, Arnarp J, Lonngren J. 1984. Carbohydrate binding studies on the lectin from datura stramonium seeds. Arch Biochem Biophys 231:524-533.
12. de Graffenried CL, Bertozzi CR. 2004. The roles of enzyme localisation and complex formation in glycan assembly within the Golgi apparatus. Curr Opin Cell Biol 16:356-363.
13. Demaurex N. 2002. pH homeostasis of cellular organelles. News Physiol Sci 17:1-5.
14. Diaz E, Schimmoller F, Pfeffer SR. 1997. A novel Rab9 effector required for endosome-to-TGN transport. J Cell Biol 138:283-290.
15. Elbein AD, Solf R, Dorling PR, Vosbeck K. 1981. Swainsonine: An inhibitor of glycoprotein processing. Proc Natl Acad Sci USA 78:7393-7397.
16. Ellis MA, Weisz OA. 2006. In vitro assays differentially recapitulate protein export from the trans-Golgi network. Anal Biochem 354:314-316.
17. Farquhar MG, Palade GE. 1981. The Golgi apparatus (complex)-(1954-1981)- from artifact to center stage. J Cell Biol 91:77s-103s.
18. Fenteany FH, Colley KJ. 2005. Multiple signals are required for alpha2,6-sialyltransferase (ST6Gal I) oligomerization and Golgi localization. J Biol Chem 280:5423-5429.
19. Gawlitzek M, Ryll T, Lofgren J, Sliwkowski MB. 2000. Ammoniumalters N-glycan structures of recombinant TNFR-IgG: Degradative versus biosynthetic mechanism. Bioengineering 68:637-647.
20. Gleeson PA. 1998. Targeting of proteins to the Golgi apparatus. Histochem Cell Biol 109:517-532.
21. Glick BS. 2000. Organization of the Golgi apparatus. Curr Opin Cell Biol 12:450-456.
22. Grabenhorst E, Conradt HS. 1999. The cytoplasmic, transmembrane, and stem regions of glycosyltransferases specify their in vivo functional sublocalization and stability in the Golgi. J Biol Chem 274:36107-36116.
23. Griffiths G, Quinn P, Warren G. 1983. Monensin inhibits the transport of viral membrane proteins from medial to trans Golgi cisternae in baby hamster kidney cells infected with semliki forest virus. J Cell Biol 96:835-850.
24. Griffiths G, Matteoni R, Back R, Hoflack B. 1990. Characterization of the cation-independent mannose 6-phosphate receptor-enriched prelysosomal compartment in NRK cells. J Cell Sci 95:441-461.
25. Gunther GR, Wang JL, Yahara I, Cunningham BA, Edelman GM. 1973. Concanavalin A derivatives with altered biological activities. Proc Natl Acad Sci USA 70:1012-1016.
26. Holappa K, Munoz MT, Egea G, Kellokumpu S. 2004. The AE2 anion exchanger is necessary for the structural integrity of the Golgi apparatus in mammalian cells. FEBS Lett 564:97-103.
27. Kellokumpu S, Sormunen R, Kellokumpu I. 2002. Abnormal glycosylation and altered Golgi structure in colorectal cancer: Dependence on intra-Golgi pH. FEBS Lett 516:217-224.
28. Kirsch RD, Joly E. 1998. An improved PCR-mutagenesis strategy for two-site mutagenesis or sequence swapping between related genes. Nucleic Acids Res 26:1848-1850.
29. Kobata A, Amano J. 2005. Altered glycosylation of proteins produced by malignant cells, and application for the diagnosis and immunotherapy of tumours. Immunol Cell Biol 83:429-439.
30. Kobata A, Matsuoka Y, Kuroki M, Yamashita K. 1995. The sugar chain structures of carcinoembryonic antigens and related normal antigens. Pure Appl Chem 67:1689-1698.
31. Kokkonen N, Rivinoja A, Kauppila A, Suokas M, Kellokumpu I, Kellokumpu S. 2004. Defective acidification of intracellular organelles results in aberrant secretion of cathepsin D in cancer cells. J Biol Chem 279:39982-39988.
32. Kuan SF, Byrd JC, Basbaum C, Kim YS. 1989. Inhibition of mucin glycosylation by aryl-N-acetyl-alpha-galactosaminides in human colon cancer cells. J Biol Chem 264:19271-19277.
33. Llopis J, McCaffery JM, Miyawaki A, Farquhar MG, Tsien RY. 1998. Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins. Proc Natl Acad Sci USA 95:6803-6808.
34. Losev E, Reinke CQ, Jellen J, Strongin DE, Bevis BJ, Glick BS. 2006. Golgi maturation visualized in living yeast. Nature 441:1002-1006.
35. Ma J, Colley KJ. 1996. A disulfide-bonded dimer of the Golgi beta-galactoside alpha2,6-sialyltransferase is catalytically inactive yet still retains the ability to bind galactose. J Biol Chem 271:7758-7766.
36. Machamer CE. 1991. Golgi retention signals: Do membranes hold the key? Trends Cell Biol 1:141-144.
37. Matlin KS. 1986. Ammonium chloride slows transport of the influenza virus hemagglutinin but does not cause mis-sorting in a polarized epithelial cell line. J Biol Chem 261:15172-15178.
38. Mills IG, Jones AT, Clague MJ. 1998. Involvement of the endosomal autoantigen EEA1 in homotypic fusion of early endosomes. Curr Biol 8:881-884.
39. Molinari M, Helenius A. 1999. Glycoproteins form mixed disulphides with oxidoreductases during folding in living cells. Nature 402:90-93.
40. Munro S. 1998. Localization of proteins to the Golgi apparatus. Trends Cell Biol 8:11-15.
41. Nilsson T, Slusarewicz P, Hoe MH, Warren G. 1993. Kin recognition. A model for the retention of Golgi enzymes. FEBS Lett 330:1-4.
42. Palokangas H, Ying M, Vaananen K, Saraste J. 1998. Retrograde transport from the pre-Golgi intermediate compartment and the Golgi complex is affected by the vacuolar H+-ATPase inhibitor bafilomycin A1. Mol Biol Cell 9:3561-3578.
43. Paroutis P, Touret N, Grinstein S. 2004. The pH of the secretory pathway: Measurement, determinants, and regulation. Physiology (Bethesda) 19:207-215.
44. Pecot MY, Malhotra V. 2006. The Golgi apparatus maintains its organization independent of the endoplasmic reticulum. Mol Biol Cell 17:5372-5380.
45. Prescott AR, Lucocq JM, James J, Lister JM, Ponnambalam S. 1997. Distinct compartmentalization of TGN46 and beta 1,4-galactosyltransferase in HeLa cells. Eur J Cell Biol 72:238-246.
46. Qian R, Chen C, Colley KJ. 2001. Location and mechanism of alpha 2,6-sialyltransferase dimer formation. Role of cysteine residues in enzyme dimerization, localization, activity, and processing. J Biol Chem 276:28641-28649.
47. Rabouille C, Klumperman J. 2005. Opinion: The maturing role of COPI vesicles in intra-Golgi transport. Nat Rev Mol Cell Biol 6:812-817.
48. Rabouille C, Hui N, Hunte F, Kieckbusch R, Berger EG, Warren G, Nilsson T. 1995. Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides. J Cell Sci 108:1617-1627.
49. Rivinoja A, Kokkonen N, Kellokumpu I, Kellokumpu S. 2006. Elevated Golgi pH in breast and colorectal cancer cells correlates with the expression of oncofetal carbohydrate T-antigen. J Cell Physiol 208:167-174.
50. Roth J. 2002. Protein N-glycosylation along the secretory pathway: Relationship to organelle topography and function, protein quality control, and cell interactions. Chem Rev 102:285-303.
51. Schaub BE, Berger B, Berger EG, Rohrer J. 2006. Transition of galactosyltransferase 1 from trans-Golgi cisterna to the trans-Golgi network is signal mediated. Mol Biol Cell 17:5153-5162.
52. Shibuya N, Goldstein IJ, Broekaert WF, Nsimba-Lubaki M, Peeters B, Peumans WJ. 1987. Fractionation of sialylated oligosaccharides, glycopeptides, and glycoproteins on immobilized elderberry (Sambucus nigra L.) bark lectin. Arch Biochem Biophys 254:1-8.
53. Thorens B, Vassalli P. 1986. Chloroquine and ammonium chloride prevent terminal glycosylation of immunoglobulins in plasma cells without affecting secretion. Nature 321:618-620.
54. Waldman BC, Rudnick G. 1990. UDP-GlcNAc transport across the Golgi membrane: Electroneutral exchange for dianionic UMP. Biochemistry 29:44-52.
55. Wang WC, Cummings RD. 1988. The immobilized leukoagglutinin from the seeds of maackia amurensis binds with high affinity to complex-type asn-linked oligosaccharides containing terminal sialic acid-linked alpha-2,3 to penultimate galactose residues. J Biol Chem 263:4576-4585.
56. Warhurst DC, Craig JC, Adagu IS, Meyer DJ, Lee SY. 2003. The relationship of physicochemical properties and structure to the differential antiplasmodial activity of the cinchona alkaloids. Malar J 2:26.
57. Warren G, Malhotra V. 1998. The organisation of the Golgi apparatus. Curr Opin Cell Biol 10:493-498.
58. Weisz OA. 2003. Acidification and protein traffic. Int Rev Cytol 226:259-319.
59. Wright CS. 1984. Structural comparison of the two distinct sugar binding sites in wheat germ agglutinin isolectin II. J Mol Biol 178:91-104.
60. Young WW Jr. 2004. Organization of Golgi glycosyltransferases in membranes: Complexity via complexes. J Membr Biol 198:1-13.