Proteoglycan Synthesis and Golgi Organization in Polarized Epithelial Cells

Journal of Histochemistry and Cytochemistry

Volumn 60, Issue 12, 2012, Pages 926-935

  Dick, Gunnar ^a   Akslen Hoel, Linn K ^a   Grøndahl, Frøy ^a   Kjos, Ingrid ^a   Prydz, Kristian ^a  

^a UNIVERSITY OF OSLO   (Norway)

Author keywords

Golgi; MDCK cells; polarized transport; proteoglycan

Indexed keywords

GAG PROTEIN; GLYCOPROTEIN; PROTEOGLYCAN; GLYCOSAMINOGLYCAN; PROTEOCHONDROITIN SULFATE; PROTEOHEPARAN SULFATE;

ANIMAL CELL; ARTICLE; BASOLATERAL MEMBRANE; CELL POLARITY; CELL VACUOLE; EPITHELIUM CELL; GLYCOSYLATION; GOLGI COMPLEX; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN SYNTHESIS; ANIMAL; BIOSYNTHESIS; DOG; HUMAN; MDCK CELL; METABOLISM; REVIEW; SECRETION (PROCESS); TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CELL POLARITY; CHONDROITIN SULFATE PROTEOGLYCANS; DOGS; EPITHELIAL CELLS; GLYCOSAMINOGLYCANS; GOLGI APPARATUS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; HYDROGEN-ION CONCENTRATION; MADIN DARBY CANINE KIDNEY CELLS; PROTEOGLYCANS;

EID: 84873033404     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1369/0022155412461256     Document Type: Article

References (82)

1. Almeida R,Levery SB,Mandel U,Kresse H,Schwientek T,Bennett EP,Clausen H.Cloning and expression of a proteoglycan UDP-galactose:beta-xylose beta1,4-galactosyltransferase I: A seventh member of the human beta4-galactosyltransferase gene family.J Biol Chem. 1999;274:26165-26171.
2. Appenzeller-Herzog C,Roche AC,Nufer O,Hauri HP.pH-induced conversion of the transport lectin ERGIC-53 triggers glycoprotein release.J Biol Chem. 2004;279:12943-12950.
3. Ashikov A,Routier F,Fuhlrott J,Helmus Y,Wild M,Gerardy-Schahn R,Bakker H.The human solute carrier gene SLC35B4 encodes a bifunctional nucleotide sugar transporter with specificity for UDP-xylose and UDP-N-acetylglucosamine.J Biol Chem. 2005;280:27230-27235.
4. Axelsson MA,Karlsson NG,Steel DM,Ouwendijk J,Nilsson T,Hansson GC.Neutralization of pH in the Golgi apparatus causes redistribution of glycosyltransferases and changes in the O-glycosylation of mucins.Glycobiology. 2001;11:633-644.
5. Bai X,Zhou D,Brown JR,Crawford BE,Hennet T,Esko JD.Biosynthesis of the linkage region of glycosaminoglycans: cloning and activity of galactosyltransferase II, the sixth member of the beta 1,3-galactosyltransferase family (beta 3GalT6).J Biol Chem. 2001;276:48189-48195.
6. Busse M,Feta A,Presto J,Wilen M,Gronning M,Kjellen L,Kusche-Gullberg M.Contribution of EXT1, EXT2, and EXTL3 to heparan sulfate chain elongation.J Biol Chem. 2007;282:32802-32810.
7. Caldwell JH,Howell KE.Pores galore for the Golgi.Nat Cell Biol. 2008;10:1125-1126.
8. Campbell BJ,Yu LG,Rhodes JM.Altered glycosylation in inflammatory bowel disease: a possible role in cancer development.Glycoconj J. 2001;18:851-858.
9. Caplan MJ,Stow JL,Newman AP,Madri J,Anderson HC,Farquhar MG,Palade GE,Jamieson JD.Dependence on pH of polarized sorting of secreted proteins.Nature. 1987;329:632-635.
10. Carraro-Lacroix LR,Lessa LM,Bezerra CN,Pessoa TD,Souza-Menezes J,Morales MM,Girardi AC,Malnic G.Role of CFTR and ClC-5 in modulating vacuolar H+-ATPase activity in kidney proximal tubule.Cell Physiol Biochem. 2010;26:563-576.
11. Chen C,Ma J,Lazic A,Backovic M,Colley KJ.Formation of insoluble oligomers correlates with ST6Gal I stable localization in the Golgi.J Biol Chem. 2000;275:13819-13826.
12. Deepa SS,Yamada S,Zako M,Goldberger O,Sugahara K.Chondroitin sulfate chains on syndecan-1 and syndecan-4 from normal murine mammary gland epithelial cells are structurally and functionally distinct and cooperate with heparan sulfate chains to bind growth factors: a novel function to control binding of midkine, pleiotrophin, and basic fibroblast growth factor.J Biol Chem. 2004;279:37368-37376.
13. Dick G,Grøndahl F,Prydz K.Over-expression of the 3′-phosphoadenosine 5′-phosphosulfate (PAPS) transporter 1 increases sulfation of chondroitin sulfate in the apical pathway of MDCK II cells.Glycobiology. 2008;18:53-65.
14. Dinter A,Berger EG.Golgi-disturbing agents.Histochem Cell Biol. 1998;109:571-590.
15. Edge AS,Spiro RG.Characterization of novel sequences containing 3-O-sulfated glucosamine in glomerular basement membrane heparan sulfate and localization of sulfated disaccharides to a peripheral domain.J Biol Chem. 1990;265:15874-15881.
16. Elazar Z,Orci L,Ostermann J,Amherdt M,Tanigawa G,Rothman JE.ADP-ribosylation factor and coatomer couple fusion to vesicle budding.J Cell Biol. 1994;124:415-424.
17. Erickson AC,Couchman JR.Basement membrane and interstitial proteoglycans produced by MDCK cells correspond to those expressed in the kidney cortex.Matrix Biol. 2001;19:769-778.
18. Esko JD,Weinke JL,Taylor WH,Ekborg G,Roden L,Anantharamaiah G,Gawish A.Inhibition of chondroitin and heparan sulfate biosynthesis in Chinese hamster ovary cell mutants defective in galactosyltransferase I.J Biol Chem. 1987;262:12189-12195.
19. Fiedler K,Simons K.The role of N-glycans in the secretory pathway.Cell. 1995;81:309-312.
20. Fjeldstad K,Pedersen ME,Vuong TT,Kolset SO,Nordstrand LM,Prydz K.Sulfation in the Golgi lumen of Madin-Darby canine kidney cells is inhibited by brefeldin A and depends on a factor present in the cytoplasm and on Golgi membranes.J Biol Chem. 2002;277:36272-36279.
21. Gao XD,Dean N.Distinct protein domains of the yeast Golgi GDP-mannose transporter mediate oligomer assembly and export from the endoplasmic reticulum.J Biol Chem. 2000;275:17718-17727.
22. Gawlitzek M,Ryll T,Lofgren J,Sliwkowski MB.Ammonium alters N-glycan structures of recombinant TNFR-IgG: degradative versus biosynthetic mechanisms.Biotechnol Bioeng. 2000;68:637-646.
23. Girardin EP,Hajmohammadi S,Birmele B,Helisch A,Shworak NW,de Agostini AI.Synthesis of anticoagulantly active heparan sulfate proteoglycans by glomerular epithelial cells involves multiple 3-O-sulfotransferase isoforms and a limiting precursor pool.J Biol Chem. 2005;280:38059-38070.
24. Gong F,Alzamora R,Smolak C,Li H,Naveed S,Neumann D,Hallows KR,Pastor-Soler NM.Vacuolar H+-atpase apical accumulation in kidney intercalated cells is regulated by pKa and amp-activated protein kinase.Am J Physiol Renal Physiol. 2010;298:1162-1169.
25. Götting C,Kuhn J,Zahn R,Brinkmann T,Kleesiek K.Molecular cloning and expression of human UDP-d-Xylose:proteoglycan core protein beta-d-xylosyltransferase and its first isoform XT-II.J Mol Biol. 2000;304:517-528.
26. Grøndahl F,Tveit H,Prydz K.Neutralization of endomembrane compartments in epithelial MDCK cells affects proteoglycan synthesis in the apical secretory pathway.Biochem J. 2009;418:517-528.
27. Gulberti S,Jacquinet JC,Chabel M,Ramalanjaona N,Magdalou J,Netter P,Coughtrie MW,Ouzzine M,Fournel-Gigleux S.Chondroitin sulfate N-acetylgalactosaminyltransferase-1 (CSGalNAcT-1) involved in chondroitin sulfate initiation: impact of sulfation on activity and specificity.Glycobiology. 2012;22:561-571.
28. Gulberti S,Lattard V,Fondeur M,Jacquinet JC,Mulliert G,Netter P,Magdalou J,Ouzzine M,Fournel-Gigleux S.Phosphorylation and sulfation of oligosaccharide substrates critically influence the activity of human beta1,4-galactosyltransferase 7 (GalT-I) and beta1,3-glucuronosyltransferase I (GlcAT-I) involved in the biosynthesis of the glycosaminoglycan-protein linkage region of proteoglycans.J Biol Chem. 2005;280:1417-1425.
29. Hafte TT,Fagereng GL,Prydz K,Grøndahl F,Tveit H.Protein core-dependent glycosaminoglycan modification and glycosaminoglycan-dependent polarized sorting in epithelial Madin-Darby canine kidney cells.Glycobiology. 2011;21:457-466.
30. Hassinen A,Pujol FM,Kokkonen N,Pieters C,Kihlstrom M,Korhonen K,Kellokumpu S.Functional organization of Golgi N- and O-glycosylation pathways involves pH-dependent complex formation that is impaired in cancer cells.J Biol Chem. 2011;286:38329-38340.
31. Hassinen A,Rivinoja A,Kauppila A,Kellokumpu S.Golgi N-glycosyltransferases form both homo- and heterodimeric enzyme complexes in live cells.J Biol Chem. 2010;285:17771-17777.
32. Hauri H,Appenzeller C,Kuhn F,Nufer O.Lectins and traffic in the secretory pathway.FEBS Lett. 2000;476:32-37.
33. Hill WG,Harper GS,Rozaklis T,Boucher RC,Hopwood JJ.Organ-specific over-sulfation of glycosaminoglycans and altered extracellular matrix in a mouse model of cystic fibrosis.Biochem Mol Med. 1997;62:113-122.
34. Hirschberg CB,Snider MD.Topography of glycosylation in the rough endoplasmic reticulum and Golgi apparatus.Annu Rev Biochem. 1987;56:63-87.
35. Ishida N,Kawakita M.Molecular physiology and pathology of the nucleotide sugar transporter family (SLC35).Pflugers Arch. 2004;447:768-775.
36. Izumikawa T,Koike T,Shiozawa S,Sugahara K,Tamura J,Kitagawa H.Identification of chondroitin sulfate glucuronyltransferase as chondroitin synthase-3 involved in chondroitin polymerization: chondroitin polymerization is achieved by multiple enzyme complexes consisting of chondroitin synthase family members.J Biol Chem. 2008;283:11396-11406.
37. Jönsson M,Eklund E,Fransson LA,Oldberg A.Initiation of the decorin glycosaminoglycan chain in the endoplasmic reticulum-Golgi intermediate compartment.J Biol Chem. 2003;278:21415-21420.
38. Kitagawa H,Izumikawa T,Uyama T,Sugahara K.Molecular cloning of a chondroitin polymerizing factor that cooperates with chondroitin synthase for chondroitin polymerization.J Biol Chem. 2003;278:23666-23671.
39. Kitagawa H,Tone Y,Tamura J,Neumann KW,Ogawa T,Oka S,Kawasaki T,Sugahara K.Molecular cloning and expression of glucuronyltransferase I involved in the biosynthesis of the glycosaminoglycan-protein linkage region of proteoglycans.J Biol Chem. 1998;273:6615-6618.
40. Kobialka S,Beuret N,Ben-Tekaya H,Spiess M.Glycosaminoglycan chains affect exocytic and endocytic protein traffic.Traffic. 2009;10:1845-1855.
41. Kolset SO,Prydz K,Fjeldstad K,Safaiyan F,Vuong TT,Gottfridsson E,Salmivirta M.Effect of brefeldin A on heparan sulphate biosynthesis in Madin-Darby canine kidney cells.Biochem J. 2002;362:359-366.
42. Kolset SO,Vuong TT,Prydz K.Apical secretion of chondroitin sulphate in polarized Madin-Darby canine kidney (MDCK) cells.J Cell Sci. 1999;112:1797-1801.
43. Kusche-Gullberg M,Kjellen L.Sulfotransferases in glycosaminoglycan biosynthesis.Curr Opin Struct Biol. 2003;13:605-611.
44. Lawrence R,Yabe T,Hajmohammadi S,Rhodes J,McNeely M,Liu J,Lamperti ED,Toselli PA,Lech M,Spear PG, et al.The principal neuronal gD-type 3-O-sulfotransferases and their products in central and peripheral nervous system tissues.Matrix Biol. 2007;26:442-455.
45. Ledin J,Ringvall M,Thuveson M,Eriksson I,Wilen M,Kusche-Gullberg M,Forsberg E,Kjellen L.Enzymatically active N-deacetylase/N-sulfotransferase-2 is present in liver but does not contribute to heparan sulfate N-sulfation.J Biol Chem. 2006;281:35727-35734.
46. Lippincott-Schwartz J,Yuan LC,Bonifacino JS,Klausner RD.Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER.Cell. 1989;56:801-813.
47. Lippincott-Schwartz J,Yuan L,Tipper C,Amherdt M,Orci L,Klausner RD.Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic.Cell. 1991;67:601-616.
48. Lo AC,Thinakaran G,Slunt HH,Sisodia SS.Metabolism of the amyloid precursor-like protein 2 in MDCK cells: polarized trafficking occurs independent of the chondroitin sulfate glycosaminoglycan chain.J Biol Chem. 1995;270:12641-12645.
49. Machen TE,Chandy G,Wu M,Grabe M,Moore HP.Cystic fibrosis transmembrane conductance regulator and H+ permeability in regulation of Golgi pH.JOP. 2001;2:229-236.
50. Maeda Y,Ide T,Koike M,Uchiyama Y,Kinoshita T.GPHR is a novel anion channel critical for acidification and functions of the Golgi apparatus.Nat Cell Biol. 2008;10:1135-1145.
51. McCarthy KJ,Couchman JR.Basement membrane chondroitin sulfate proteoglycans: localization in adult rat tissues.J Histochem Cytochem. 1990;38:1479-1486.
52. McCormick C,Duncan G,Goutsos KT,Tufaro F.The putative tumor suppressors EXT1 and EXT2 form a stable complex that accumulates in the Golgi apparatus and catalyzes the synthesis of heparan sulfate.Proc Natl Acad Sci U S A. 2000;97:668-673.
53. Mertens G,Van Der Schueren B,Van Den Berghe H,David G.Heparan sulfate expression in polarized epithelial cells: the apical sorting of glypican (GPI-anchored proteoglycan) is inversely related to its heparan sulfate content.J Cell Biol. 1996;132:487-497.
54. Moses J,Oldberg A,Eklund E,Fransson LA.Biosynthesis of the proteoglycan decorin-identification of intermediates in galactosaminoglycan assembly.Eur J Biochem. 1997;248:767-774.
55. Nagai N,Habuchi H,Esko JD,Kimata K.Stem domains of heparan sulfate 6-O-sulfotransferase are required for Golgi localization, oligomer formation and enzyme activity.J Cell Sci. 2004;117:3331-3341.
56. Ogawa H,Shionyu M,Sugiura N,Hatano S,Nagai N,Kubota Y,Nishiwaki K,Sato T,Gotoh M,Narimatsu H, et al.Chondroitin sulfate synthase-2/chondroitin polymerizing factor has two variants with distinct function.J Biol Chem. 2010;285:34155-34167.
57. Pacheco B,Maccarana M,Malmström A.Dermatan 4-O-sulfotransferase 1 is pivotal in the formation of iduronic acid blocks in dermatan sulfate.Glycobiology. 2009;19:1197-1203.
58. Palade G.Intracellular aspects of the process of protein synthesis.Science. 1975;189:867.
59. Palokangas H,Ying M,Vaananen K,Saraste J.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. 1998;9:3561-3578.
60. Paroutis P,Touret N,Grinstein S.The pH of the secretory pathway: measurement, determinants, and regulation.Physiology (Bethesda). 2004;19:207-215.
61. Pinhal MA,Smith B,Olson S,Aikawa J,Kimata K,Esko JD.Enzyme interactions in heparan sulfate biosynthesis: uronosyl 5-epimerase and 2-O-sulfotransferase interact in vivo.Proc Natl Acad Sci U S A. 2001;98:12984-12989.
62. Presto J,Thuveson M,Carlsson P,Busse M,Wilen M,Eriksson I,Kusche-Gullberg M,Kjellen L.Heparan sulfate biosynthesis enzymes EXT1 and EXT2 affect NDST1 expression and heparan sulfate sulfation.Proc Natl Acad Sci U S A. 2008;105:4751-4756.
63. Prydz K,Dalen KT.Synthesis and sorting of proteoglycans.J Cell Sci. 2000;113:193-205.
64. Prydz K,Dick G,Tveit H.How many ways through the Golgi maze?.Traffic. 2008;9:299-304.
65. Rivinoja A,Hassinen A,Kokkonen N,Kauppila A,Kellokumpu S.Elevated Golgi pH impairs terminal N-glycosylation by inducing mislocalization of Golgi glycosyltransferases.J Cell Physiol. 2009;220:144-154.
66. Safaiyan F,Kolset SO,Prydz K,Gottfridsson E,Lindahl U,Salmivirta M.Selective effects of sodium chlorate treatment on the sulfation of heparan sulfate.J Biol Chem. 1999;274:36267-36273.
67. Safaiyan F,Lindahl U,Salmivirta M.Structural diversity of N-sulfated heparan sulfate domains: distinct modes of glucuronyl C5 epimerization, iduronic acid 2-O-sulfation, and glucosamine 6-O-sulfation.Biochemistry. 2000;39:10823-10830.
68. Schaefer L,Hausser H,Altenburger M,Ugorcakova J,August C,Fisher LW,Schaefer RM,Kresse H.Decorin, biglycan and their endocytosis receptor in rat renal cortex.Kidney Int. 1998;54:1529-1541.
69. Schön S,Prante C,Bahr C,Kuhn J,Kleesiek K,Götting C.Cloning and recombinant expression of active full-length xylosyltransferase I (XT-I) and characterization of subcellular localization of XT-I and XT-II.J Biol Chem. 2006;281:14224-14231.
70. Seksek O,Biwersi J,Verkman AS.Direct measurement of trans-Golgi pH in living cells and regulation by second messengers.J Biol Chem. 1995;270:4967-4970.
71. Spiro RC,Freeze HH,Sampath D,Garcia JA.Uncoupling of chondroitin sulfate glycosaminoglycan synthesis by brefeldin A.J Cell Biol. 1991;115:1463-1473.
72. Sprong H,Degroote S,Nilsson T,Kawakita M,Ishida N,Van Der Sluijs P,Van Meer G.Association of the Golgi UDP-galactose transporter with UDP-galactose:ceramide galactosyltransferase allows UDP-galactose import in the endoplasmic reticulum.Mol Biol Cell. 2003;14:3482-3493.
73. Sugumaran G,Katsman M,Silbert JE.Effects of brefeldin A on the localization of chondroitin sulfate-synthesizing enzymes: activities in subfractions of the Golgi from chick embryo epiphyseal cartilage.J Biol Chem. 1992;267:8802-8806.
74. Svennevig K,Prydz K,Kolset SO.Proteoglycans in polarized epithelial Madin-Darby canine kidney cells.Biochem J. 1995;311:881-888.
75. Thorens B,Vassalli P.Chloroquine and ammonium chloride prevent terminal glycosylation of immunoglobulins in plasma cells without affecting secretion.Nature. 1986;321:618-620.
76. Toma L,Pinhal MA,Dietrich CP,Nader HB,Hirschberg CB.Transport of UDP-galactose into the Golgi lumen regulates the biosynthesis of proteoglycans.J Biol Chem. 1996;271:3897-3901.
77. Tone Y,Pedersen LC,Yamamoto T,Izumikawa T,Kitagawa H,Nishihara J,Tamura J,Negishi M,Sugahara K.2-O-phosphorylation of xylose and 6-O-sulfation of galactose in the protein linkage region of glycosaminoglycans influence the glucuronyltransferase-I activity involved in the linkage region synthesis.J Biol Chem. 2008;283:16801-16807.
78. Tveit H,Akslen LK,Fagereng GL,Tranulis MA,Prydz K.A secretory Golgi bypass route to the apical surface domain of epithelial MDCK cells.Traffic. 2009;10:1685-1695.
79. Tveit H,Dick G,Skibeli V,Prydz K.A proteoglycan undergoes different modifications en route to the apical and basolateral surfaces of Madin-Darby canine kidney cells.J Biol Chem. 2005;280:29596-29603.
80. Uhlin-Hansen L,Yanagishita M.Differential effect of brefeldin A on the biosynthesis of heparan sulfate and chondroitin/dermatan sulfate proteoglycans in rat ovarian granulosa cells in culture.J Biol Chem. 1993;268:17370-17376.
81. Vuong TT,Prydz K,Tveit H.Differences in the apical and basolateral pathways for glycosaminoglycan biosynthesis in Madin-Darby canine kidney cells.Glycobiology. 2006;16:326-332.
82. Weisz OA.Organelle acidification and disease.Traffic. 2003;4:57-64.