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Current ideas on the significance of protein glycosylation

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Abstract

Carbohydrate has been removed from a number of glycoproteins without major effect on the structure or enzyme activity of the protein. Thus carbohydrate has been suggested to underly a non-primary function for proteins, such as in relatively non-specific interactions with other carbohydrates or macromolecules, stabilization of protein conformation, or protection from proteolysis. This non-specific concept is consistent with both the general similarity in carbohydrate structure on very diverse glycoproteins and the frequent structural microheterogeneity of carbohydrate chains at given sites. The concept is supported in a general sense by the viability of cells whose glycosylation processes have been globally disrupted by mutation or pharmacological inhibitors.

In contrast to the above observations, other studies have revealed the existence of specific, selective receptors for discrete oligosaccharide structures on glycoproteins which seem to be important for compartmentalization of the glycoprotein, or the positioning of cells on which the glycoprotein is concentrated. Sometimes multivalency in the carbohydrate-receptor interaction is crucial. There are additional possible roles for carbohydrate in the transduction of information upon binding to a receptor. The possibility of specific roles for carbohydrate is supported by the existence of numerous unique carbohydrate structures, many of which have been detected as glycoantigens by monoclonal antibodies, with unique distributions in developing and differentiated cells.

This article attempts to summarize and rationalize the contradictory results. It appears that in general carbohydrate does in fact underlie only roles secondary to a protein's primary function. These secondary roles are simple non-specific ones of protection and stabilization, but often also satisfy the more sophisticated needs of spatial position control and compartmentalization in multicellular eukaryotic organisms. It is suggested that there are advantages, evolutionarily speaking, for the shared use of carbohydrate for non-specific roles and for specific roles primarily as luxury functions to be executed during the processes of cell differentiation and morphogenesis.

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References

  1. Berger EG, Buddecke E, Kamerling JP, Kobata A, Paulson JC, Vliegenthart JFG: Structure, biosynthesis and functions of glycoprotein glycans. Experientia 38:1129–1258, 1983.

    Google Scholar 

  2. Olden K, Parent JB, White SL: Carbohydrate moieties of glycoproteins. Biochim Biophys Acta 650:209–232, 1982.

    Google Scholar 

  3. Aplin JD, Hughes RC: Complex carbohydrates of the extracellular matrix. Structures, interactions and biological roles. Biochim Biophys Acta 694:375–418, 1982.

    Google Scholar 

  4. Trimble RB, Maley F, Chu FK: Glycoprotein biosynthesis in yeast. J Biol Chem 258:2562–2567, 1983.

    Google Scholar 

  5. Williams DB, Lennarz WJ: Control of asparagine-linked oligosaccharide chain processing: studies on bovine pancreatic ribonuclease B. J Biol Chem 259:5105–5114, 1984.

    Google Scholar 

  6. Pollack L, Atkinson PH: Correlation of glycosylation forms with position in amino acid sequence. J Cell Biol 97:293–300, 1983.

    Google Scholar 

  7. Lang L, Reitman M, Tang J, Roberts RM, Kornfeld S: Lysosomal enzyme phosphorylation. J Biol Chem 259:14663–14671, 1984.

    Google Scholar 

  8. Parkkinen J, Finne J: Occurrence of N-acetylglucosamine 6-phosphate in complex carbohydrates. J Biol Chem 260:10971–10975, 1985.

    Google Scholar 

  9. Lederkremer GZ, Parodi AJ: 3-O-methylation of mannose residues. J Biol Chem 259:12514–12518, 1984.

    Google Scholar 

  10. Lechner J, Wieland F, Sumper M: Transient methylation of dolichyl oligosaccharides is an obligatory step in halobacterial sulfated glycoprotein biosynthesis. J Biol Chem 260:8984–8989, 1985.

    Google Scholar 

  11. Mescher MF: Glycoproteins as cell-surface components. TIBS April 97–99, 1981.

  12. Ishihara H, Takahashi N, Ito J, Takeuchi E, Tejima S: Either high-mannose-type or hybrid type oligosaccharide is linked to the same asparagine residue in ovalbumin. Biochim Biophys Acta 669:216–221, 1981.

    Google Scholar 

  13. Uy R, Wold F: Posttranslational covalent modification of proteins. Science 198:890–896, 1977.

    Google Scholar 

  14. Kornfeld R, Kornfeld S: Assembly of asparagine-linked oligosaccharides. Ann Rev Biochem 54:631–664, 1985.

    Google Scholar 

  15. Guarnaccia SP, Shaper JH, Schnaar RL: Tunicamycin inhibits ganglioside biosynthesis in neuronal cells. Proc Natl. Acad Sci USA 80:1551–1555, 1983.

    Google Scholar 

  16. Yavin E, Richter-Landsberg C, Duksin D, Yavin Z: Tunicamycin blocks neuritogenesis and glucosamine labeling of gangliosides in developing cerebral neuron cultures. Proc Natl Acad Sci USA 81:5638–5642, 1984.

    Google Scholar 

  17. Ito F, Chou JY: Suppression of placental alkaline phosphatase biosynthesis by tunicamycin. J Biol Chem 259:14997–14999, 1984.

    Google Scholar 

  18. Gustafson GL, Milner LA: Occurrence of N-acetylglucosamine-1-phosphate in proteinase I from Dictyostelium discoideum. J Biol Chem 255:7208–7210, 1980.

    Google Scholar 

  19. Schindler M: Personal communication.

  20. Stanley P: Glycosylation mutants of animal cells. Ann Rev Genet 18:525–552, 1984.

    Google Scholar 

  21. Timpl R, Fujiwara S, Dziadek M, Aumailley M, Weber S, Engel J: Laminin, proteoglycan, nidogen and collagen IV: structural models and molecular interactions. In: Porter R, Whelan J (Eds). Basement membranes and cell movement. Ciba Foundation Symposium 108. Pitman, London, 1984, pp 2–43.

    Google Scholar 

  22. Hill HD, Reynolds JA, Hill RL: Purification, composition, molecular weight and subunit structure of ovine submaxillary mucin. J Biol Chem 252:3791–3798, 1977.

    Google Scholar 

  23. Fitzgerald LA, Denny JB, Baumbach GA, Ketcham CM, Roberts RM: Effect of altered oligosaccharide structure on. the cell surface number, distribution and turnover of the high molecular weight acidic glycoproteins of CHO cells. J Cell Sci 67:1–23, 1984.

    Google Scholar 

  24. Hall CW, Robbins AR, Krag SS: Preliminary characterization of a chinese hamster ovary cell glycosylation mutant isolated by screening for low intracellular lysosomal enzyme activity. Mol Cell Biochem (this issue).

  25. Hanover JA, Elting J, Mintz GR, Lennarz WJ: Temporal aspects of the N- and O-glycosylation of human chorionic gonadotropin. J Biol Chem 257:10172–10177, 1982.

    Google Scholar 

  26. Johnson DC, Spear PG: O-linked oligosaccharides are acquired by herpes simplex virus glycoproteins in the Golgi apparatus. Cell 32:987–997, 1983.

    Google Scholar 

  27. Carraway KL, Spielman J: Structural and functional aspects of tumor cell sialomucins. Mol Cell Biochem (this issue).

  28. Knecht DA, Dimond RL, Wheeler S, Loomis WF: Antigenic determinants shared by lysosomal proteins of Dictyostelium discoideum. J Biol Chem 259:10633–10640, 1984.

    Google Scholar 

  29. Loomis WF, Wheeler SA, Springer WR, Barondes SH: Adhesion mutants of Dictyostelium disclideum lacking the saccharide determinant recognized by two adhesion blocking monoclonal antibodies. Devel Biol 109:111–117, 1985.

    Google Scholar 

  30. Bush CA, Duben A, Ralapati S: Conformation of the glycopeptide linkage in asparagine-linked glycoproteins. Biochemistry 19:501–504, 1980.

    Google Scholar 

  31. Bush CA, Dua VK, Ralapati S, Warren CD, Spik G, Strecker G, Montreuil J: Conformation of the complex oligosaccharides of glycoproteins. J Biol Chem 257:8199–8204, 1982.

    Google Scholar 

  32. Lark MW, Culp LA: Multiple classes of heparan sulfate proteoglycans from fibroblast substratum adhesion sites. J Biol Chem 259:6773–6782, 1984.

    Google Scholar 

  33. Rose MC, Voter WA, Sage H, Brown CF, Kaufman B: Effects of deglycosylation on the architecture of ovine submaxillary mucin glycoprotein. J Biol Chem 259:3167–3172, 1984.

    Google Scholar 

  34. Schmid K: Preparation and properties of serum and plasma proteins. XXIX. Separation from human plasma of polysaccharides, peptides and proteins of low molecular weight. Crystallization of an acid glycoprotein. J Am Chem Soc 75:60–68, 1953.

    Google Scholar 

  35. Spiro RG: Studies on fetuin, a glycoprotein of fetal serum. I. Isolation, chemical composition, and physicochemical properties. J Biol Chem 235:2860–2869, 1960.

    Google Scholar 

  36. Warren L, Blithe DL, Cossu G: Variation of the carbohydrates of glycoproteins of cells growing on different surfaces. J Cell Physiol 113:17–22, 1982.

    Google Scholar 

  37. Warren L: The function of protein-bound carbohydrates in normal and pathological cells. In: Saunders et al. (Eds). Fundamental mechanisms in human cancer immunology. Elsevier North Holland, Inc., 1981, pp 99–108.

  38. Paul G, Lottspeich F, Wieland F: Asparaginyl-N-acetylgalactosamine. J Biol Chem 261:1020–1024.

  39. Bernard BA, De Luca LM, Hassell JR, Yamada KM, Olden K: Retinoic acid alters the proportion of high mannose to complex type oligosaccharides on fibronectin secreted by cultured chondrocytes. J Biol Chem 259:5310–5315, 1984.

    Google Scholar 

  40. Klebl F, Huffaker T, Tanner W: A temperature-sensitive N-glycosylation mutant of S. cerevisiae that behaves like a cell-cycle mutant. Exp Cell Res 150:309–313, 1984.

    Google Scholar 

  41. De Asua LJ, Poskocil S, Foecking MK, Otto AM: N-glycosylation of nascent proteins early in the prereplicative phase constitutes a process for controlling animal cell proliferation. Hormon Cell Reg 8:37–50, 1984.

    Google Scholar 

  42. Spiro RG, Spiro MJ, Bhoyroo VD: Studies on the regulation of the biosynthesis of glucose-containing oligosaccharide-lipids. J Biol Chem 258:9469–9476, 1983.

    Google Scholar 

  43. Reading CL: Carbohydrate structure, biological recognition, and immune function. In: Ivatt RJ (Ed). The Biology of Glycoproteins. Plenum Press, NY, pp 235–321, 1984.

  44. Warren L, Buck CA, Tuszynski GP: Glycopeptide changes and malignant transformation. A possible role for carbohydrate in malignant behavior. Biochim Biophys Acta 516:97–127, 1978.

    Google Scholar 

  45. Feizi T: Demonstration by monoclonal antibodies that carbohydrate structures of glycoproteins and glycolipids are onco-developmental antigens. Nature 314:53–57, 1985.

    Google Scholar 

  46. Hakomori S: Glycosphingolipids as differentiation-dependent, tumor-associated markers and as regulators of cell proliferation. TIBS 453–456, 1984.

  47. Schachter H: Biosynthetic controls that determine the branching and microheterogeneity of protein-bound oligosaccharides. Biochem Cell Biol 64:163–181, 1986.

    Google Scholar 

  48. Kartha S, Felix JS, Littlefield JW: Aggregation-deficient embryonal carcinoma cells: defects in peanut agglutinin (PNA) receptors. Differentiation 29:77–81, 1985.

    Google Scholar 

  49. Dennis JW, Carver JP, Schachter H: Asparagine-linked oligosaccharides in murine tumor cells: comparison of a WGA-resistant (WGAr) nonmetastatic mutant and a related WGA-sensitive (WGAs) metastatic line. J Cell Biol 99:1034–1044, 1984.

    Google Scholar 

  50. Springer GF: T and Tn, general carcinoma autoantigens. Science 224:1198–1206, 1984.

    Google Scholar 

  51. Smets LA, van Beek WP: Carbohydrates of the tumor cell surface. Biochim Biophys Acta 738:237–249, 1984.

    Google Scholar 

  52. Humphries MJ, Matsumoto K, White SL, Olden K: Oligosaccharide modification by swainsonine treatment inhibits pulmonary colonization by B16-FlO murine melanoma cells. Proc Natl Acad Sci USA 83:1752–1756, 1986.

    Google Scholar 

  53. Slack JMW, Cleine JH, Smith JC: Regional specificity of glycoconjugates in Xenopus and axolotl embryos. J Embryol Exp Morph 89:137–153, 1985.

    Google Scholar 

  54. Pennington JE, Rastan S, Roelcke D, Feizi T: Saccharide structures of the mouse embryo during the first eight days of development. J Embryol Exp Morph 90:335–361, 1985.

    Google Scholar 

  55. Sato M, Muramatsu T: Reactivity of five N-acetylgalactosamine-recognizing lectins with preimplantation embryos, early postimplantation embryos, and teratocarcinoma cells of the mouse. Differentiation 29:29–38, 1985.

    Google Scholar 

  56. Orlean P, Tanner W: Inhibition of glycoprotein synthesis in Saccharomyces cerevisiae by mating pheromones. In: Nombela (Ed). Microbial cell wall synthesis and autolysis. Elsevier Science Publishers, pp 63–71, 1984.

  57. Ozawa M, Muramatsu T, Solter D: SSEA-1, a stage-specific antigen of the mouse, is carried by the glycoprotein-bound large carbohydrate in embryonal carcinoma cells. Cell Differ 16:169–173, 1985.

    Google Scholar 

  58. Engle JC, Parodi AJ: Trypanosoma cruzi cells undergo an alteration in protein N-glycosylation upon differentiation. J Biol Chem 260:10105–10110, 1985.

    Google Scholar 

  59. Marino M, Cossu G, Neri G, Molinaro M: Appearance of a class of cell-surface fucosyl-glycopeptides in differentiated muscle cells in culture. Dev Biol 78:258–267, 1980.

    Google Scholar 

  60. Codogno P, Bernard B, Font J, Aubery M: Changes in protein glycosylation during chick embryo development. Biochim Biophys Acta 763:265–275, 1983.

    Google Scholar 

  61. Vedtofte P, Dabelsteen E, Hakomori S-I, Young WW: Changes in the expression of blood-group carbohydrates during oral mucosal development in human fetuses. Differentiation 27:221–228, 1984.

    Google Scholar 

  62. Fukuda M: Cell surface glycoconjugates as oncodifferentiation markers in hematopoietic cells. Biochim Biophys Acta 780:119–150, 1985.

    Google Scholar 

  63. Lennarz WJ: Glycoprotein synthesis and embryonic development. CRC Crit Rev Biochem 14:257–285, 1984.

    Google Scholar 

  64. Oda-Tamai S, Kato S, Hara S, Akamatsu N: Decreased transfer of oligosaccharide from oligosaccharide-lipid to protein acceptors in regenerating rat liver. J Biol Chem 260:57–63, 1985.

    Google Scholar 

  65. Hayes GR, Lucas JJ: Stimulation of lipid-linked oligosaccharide assembly duing oviduct differentiation. J Biol Chem 258:15095–15100, 1983.

    Google Scholar 

  66. Skutelsky E, Bayer EA: Cell-type-related segregation of surface galactosyl-containing components at an early developmental stage in hemopoietic bone marrow cells in the rabbit. J Cell Biol 96:184–190, 1983.

    Google Scholar 

  67. Mizoguchi A, Takasaki S, Maeda S, Kobata A: Changes in asparagine-linked sugar chains of human promyelocytic leukemic cells (HL-60) during monocytoid differentiation and myeloid differentiation. J Biol Chem 259:11943–11948, 1984.

    Google Scholar 

  68. Stein GS, Roberts RM, Davis JL, Head WJ, Stein JL, Thrall CL, Veen JV, Welch DW: Are glycoproteins and glycosaminoglycans components of the eukaryotic genome? Nature 258:639–641, 1975.

    Google Scholar 

  69. Armant DR, Kaplan HA, Lennarz WJ: N-linked glycoprotein biosynthesis in the developing mouse embryo. Devel Biol 113:228–237, 1986.

    Google Scholar 

  70. Nose M, Wigzell H: Biological significance of carbohydrate chains on monoclonal antibodies. Proc Natl Acad Sci USA 80:6632–6636, 1983.

    Google Scholar 

  71. Sairam MR. Bhargavi GN: A role for glycosylation of the α-subunit in transduction of biological signal in glycoprotein hormones. Science 229:65–67, 1985.

    Google Scholar 

  72. Kalyan NK, Bahl OP: Role of carbohydrate in human chorionic gonadotropin. J Biol Chem 258:67–74, 1983.

    Google Scholar 

  73. Rebois RV, Fishman PH: Antibodies against human chorionic gonadotropin convert the deglycosylated hormone from an antagonist to an agonist. J Biol Chem 259:8087–8090, 1984.

    Google Scholar 

  74. Bayna EM, Runyan RB, Scully NF, Reichner J, Lopez LC, Shur BD: Cell surface galactosyltransferase as a recognition molecule during development. Mol Cell Biochem (this issue).

  75. Pletcher CH, Resnick RM, Wei GJ, Bloomfield VA, Nelsestuen GL: Deglycosylated prothrombin fragment 1. J Biol Chem 255:7433–7438, 1980.

    Google Scholar 

  76. Zhu BCR, Laine RA: Polylactosamine glycosylation on human fetal placental fibronectin weakens the binding affinity of fibronectin to gelatin. J Biol Chem 260:4041–4045, 1985.

    Google Scholar 

  77. Reeves R, Chang D: Investigations of the possible functions for glycosylation in the high mobility group proteins. J Biol Chem 258:679–687, 1983.

    Google Scholar 

  78. Kan FWK, Pinto da Silva P: Preferential association of glycoproteins to the euchromatin regions of crossfractured nuclei is revealed by fracture-label. J Cell Biol 102:576–586, 1986.

    Google Scholar 

  79. Howard GA, Scnebli HP: Eukaryotic ribosomes possess a binding site for concanavalin A. Proc Natl Acad Sci USA 74:818–821, 1977.

    Google Scholar 

  80. Eylar EH: On the biological role of glycoproteins. J Theoret Biol 10:89–113, 1965.

    Google Scholar 

  81. Winterburn PJ, Phelps CF: The significance of glycosylated proteins. Nature 236:147–151, 1972.

    Google Scholar 

  82. Struck DK, Siuta PB, Lane MD, Lennarz WJ: Effect of tunicamycin on the secretion of serum proteins by primary cultures of rat and chick hepatocytes. J Biol Chem 253:5332–5337, 1978.

    Google Scholar 

  83. Sidman C: Differing requirements for glycosylation in the secretion of related glycoproteins is determined neither by the producing cell nor by the relative number of oligosaccharide units. J Biol Chem 256:9374–9376, 1981.

    Google Scholar 

  84. Docherty PA, Aronson NN: Effect of the threonine analog β-hydroxynorvaline on the glycosylation and secretion of α1-acid glycoprotein by rat hepatocytes. J Biol Chem 260:10847–10855; 1985.

    Google Scholar 

  85. Parent JB, Yeo K-T, Yeo T-K, Olden K: Differential effects of 1-deoxynojirimycin on the intracellular transport of secretory glycoproteins of human hepatoma cells in culture. Mol Cell Biochem (this issue).

  86. Repp R, Tamura T, Boschek CB, Wege H, Schwarz RT, Niemann H: The effects of processing inhibitors of N-linked oligosaccharides on the intracellular migration of glycoprotein E2 of mouse hepatitis virus and the maturation of coronavirus particles. J Biol Chem 260:15873–15879, 1985.

    Google Scholar 

  87. Ronnett GV, Knutson VP, Kohanski RA, Simpson TL, Lane MD: Role of glycosylation in processing of newly translated insulin proreceptor in 3T3-L1 adipocytes. J Biol Chem 259:4566–4575, 1984.

    Google Scholar 

  88. Breitfeld PP, Rup D, Schwartz AL: Influence of the N-linked oligosaccharides on the biosynthesis, intracellular routing, and function of the human asialoglycoprotein receptor. J Biol Chem 259:10414–10421, 1984.

    Google Scholar 

  89. Soderquist AM, Carpenter G: Glycosylation of the epidermal growth factor receptor in A-431 cells. J Biol Chem 259:12586–12594, 1984.

    Google Scholar 

  90. Burke B, Matlin K, Bause E, Legler G, Peyrieras N, Ploegh H: Inhibition of N-linked oligosaccharide trimming does not interfere with surface expression of certain integral membrane proteins. EMBO J 3:551–556, 1984.

    Google Scholar 

  91. Fitting T, Kabat D: Evidence for a glycoprotein ‘signal’ involved in transport between subcellular organelles. J Biol Chem 257:14011–14017, 1982.

    Google Scholar 

  92. Machamer CE, Florkiewicz RZ, Rose JK: A single N-linked oligosaccharide at either of the two normal sites is sufficient for transport of vesicular stomatitis virus G protein to the cell surface. Mol Cell Biol 5:3074–3083, 1985.

    Google Scholar 

  93. Firestone GL: The role of protein glycosylation in the compartmentalization and processing of mouse mammary tumor virus glycoproteins in mouse mammary tumor virus-infected rat hepatoma cells. J Biol Chem 258:6155–6161, 1983.

    Google Scholar 

  94. Schlesinger S, Malfer C, Schlesinger MJ: The formation of vesicular stomatitis virus (San Juan strain) becomes temperature-sensitive when glucose residues are retained on the oligosaccharides of the glycoprotein. J Biol Chem 259:7597–7601, 1984.

    Google Scholar 

  95. Poruchynsky MS, Tyndall C, Both GW, Sato F, Bellamy AR, Atkinson PH: Deletions into a NH2-terminal hydrophobic domain result in secretion of Rotavirus VP7, a resident endoplasmic reticulum membrane glycoprotein. J Cell Biol 101:2199–2209, 1985.

    Google Scholar 

  96. West CM, Erdos GW, Davis R: Glycoantigen expression is regulated both temporally and spatially during development in the cellular slime molds Dictyostelium discoideum and D. mucoroides. Moll Cell Biochem (this issue).

  97. Weis JJ, Fearon DT: The identification of N-linked oligosaccharides on the human CR2/Epstein-Bart virus receptor and their function in receptor metabolism, plasma membrane expression, and ligand binding. J Biol Chem 260:13824–13810, 1985.

    Google Scholar 

  98. Whitsett JA, Ross G, Weaver T, Rice W, Dion C, Hull W: Glycosylation and secretion of surfactant-associated glycoprotein A. J Biol Chem 260:15273–15279, 1985.

    Google Scholar 

  99. Duronio V, Jacobs S, Cuatrecasas P: Complete glycosylation of the insulin and insulin-like growth factor 1 receptors is not necessary for their biosynthesis and function. J Biol Chem 261:970–975, 1986.

    Google Scholar 

  100. Schauer R: Chemistry, metabolism, and biological functions of sialic acids. Adv Carbohydrate Chem Biochem 40:11131–11234, 1982.

    Google Scholar 

  101. Bernard BA, Newton SA, Olden K: Effect of size and location of the oligosaccharide chain on protease degradation of bovine pancreatic ribonuclease. J Biol Chem 258:12198–12201, 1983.

    Google Scholar 

  102. Winkler JR, Segal HL: Swainsonine inhibits glycoprotein degradation by isolated rat liver lysosomes. J Biol Chem 259:15369–15372, 1984.

    Google Scholar 

  103. Battles JR, Frazier WA, Rosen SD: Slime mold lectins. Int Rev Cyt 75:61–69, 1982.

    Google Scholar 

  104. Cooper DNW, Haywood-Reid PL, Springer WR, Barondes SH: Bacterial glycoconjugates are natural ligands for the carbohydrate binding site of discoidin I and influence its cellular compartmentalization. Devel Biol 114:416–425, 1986.

    Google Scholar 

  105. Ashwell G, Harford J: Carbohydrate-specific receptors of the liver. Ann Rev Biochem 51:531–554, 1982.

    Google Scholar 

  106. McFarlane IG: Hepatic clearance of serum glycoproteins. Clinical Sci 64:127–135, 1983.

    Google Scholar 

  107. Buck CA, Warren L: The repair of the surface structure of animal cells. J Cell Physiol 89:187–200, 1976.

    Google Scholar 

  108. Thornburg RW, Day JF, Baynes JW, Thorpe SR: Carbohydrate-mediated clearance of immune complexes from the circulation. J Biol Chem 255:6820–6825, 1980.

    Google Scholar 

  109. Day JF, Thornburg RW, Thorpe SR, Baynes JW: Carbohydrate-mediated clearance of antibody-antigen complexes from the circulation. J Biol Chem 255:2360–2365, 1980.

    Google Scholar 

  110. Sharon N: Surface carbohydrates and surface lectins are recognition determinants in phagocytosis. Immunology Today 5:143–147, 1984.

    Google Scholar 

  111. Saunders PTK, Renegar RH, Raub TJ, Baumbach GA, Atkinson PH, Blazer FW, Roberts RM. The carbohydrate structure of porcine uteroferrin and the role of the high mannose chains in promoting uptake by the reticuloendothelial cells of the fetal liver. J Biol Chem 260:3658–3665, 1985.

    Google Scholar 

  112. Snider MD, Rogers OC: Intracellular movement of cell surface receptors after endocytosis: resialylation of asialotransferrin receptor in human erythroleukemia cells. J Cell Biol 100:826–834, 1985.

    Google Scholar 

  113. Kujawa MJ, Caplan AI: Hyaluronic acid bonded to cell culture surfaces stimulated chondrogenesis in stage 24 limb mesenchyme cell cultures. Devel Biol 114:504–518, 1986.

    Google Scholar 

  114. Lev B, Ward H, Keusch GT, Pereira MEA: Lectin activation in Giardia lamblia by host protease: A novel hostparasite interaction. Science 232:71–73, 1986.

    Google Scholar 

  115. Sharon N: Carbohydrates as recognition determinants in phagocytosis and in lectin-mediated killing of target cells. Biol Cell 51:239–246, 1984.

    Google Scholar 

  116. Bock K, Breimer ME, Brignole A, Hannson GC, Karlsson K-A, Larson G. Ieffler H, Samuelsson BE, Stromberg N, Eden CS, Thurin J: Specificity of binding of a strain of uropathogenic Escherichia coli to Galα1–4Gal-containing glycosphingolipids. J Biol Chem 260:8545–8551, 1985.

    Google Scholar 

  117. Friedman MJ, Fukuda M, Laine RA: Evidence for a malarial parasite interaction site on the major transmembrane protein of the human erythrocyte. Science 228:75–77, 1985.

    Google Scholar 

  118. Gristina AG, Oga M, Webb LX, Hobgood CD: Adherent bacterial colonization in the pathogenesis of osteomyclitis. Science 228:990–993, 1985.

    CAS  PubMed  Google Scholar 

  119. Burnet FM: Mucoproteins in relation to virus action. Physiol Rev 31:131–150, 1951.

    Google Scholar 

  120. Roseman S: The synthesis of complex carbohydrates by multiglycosyltransferase systems and their potential function in intercellular adhesion. Chem Phys Lipids 5:270–297, 1970.

    Google Scholar 

  121. Shur BD: The receptor function of galactosyltransferase during cellular interactions. Mol Cell Biochem 61:143–158, 1984.

    Google Scholar 

  122. Ivatt RJ: Role of glycoproteins during early mammalian embryogenesis. In: Ivatt RJ (Ed). The Biology of Glycoproteins. Plenum Press, NY, 1985, pp 95–181.

    Google Scholar 

  123. Fenderson BA, Zehavi U, Hakomori S-I: A multivalent lacto-N-fucopentaose III-lysyllysine conjugate decompacts preimplantation mouse embryos, while the free oligosaccharide is ineffective. J Exp Med 160:1591–1596, 1984.

    Google Scholar 

  124. Lopez LC, Bayna EM, Litoff D, Shaper NL, Schaper JH, Shur DB: Receptor function of mouse sperm surface galactosyltransferase during fertilization. J Cell Biol 101:1501–1510, 1985.

    Google Scholar 

  125. Florman HM, Wassarman PM: O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity. Cell 41:313–324, 1985.

    Google Scholar 

  126. Edwards PAW: Differential cell adhesion may result from nonspecific interactions between cell surface glycoproteins. Nature 271:248–249, 1978.

    Google Scholar 

  127. Rutishauser U, Watanabe M, Silver J, Troy FA, Vimr ER: Specific alteration of N-CAM-mediated cell adhesion by an endoneuraminidase. J Cell Biol 101:1842–1849, 1985.

    Google Scholar 

  128. Gole GJ, Glaser L: A heparin-binding domain from NCAM is involved in neural cell-substratum adhesion. J Cell Biol 102:403–412, 1986.

    Google Scholar 

  129. Koide N, Nose M, Muramatsu T: Recognition of IgG by Fc receptor and complement: effects of glycosidase digestion. Biochem Biophys Res Comm 75:838–844, 1977.

    Google Scholar 

  130. Brandley BK, Schnaar RL: Cell surface carbohydrates in cell recognition and response. J Leuk Biol 40:97–111, 1986.

    Google Scholar 

  131. Rastan S, Thorpe SJ, Scudder P, Brown S, Gooi HC, Feizi T: Cell interactions in preimplantation embryos: evidence for involvement of saccharides of the poly-N acetyllactosamine series. J Embryol Exp Morph 87:115–128, 1985.

    Google Scholar 

  132. Bosmann HB, Meyers MW: Mitochondrial synthesis of glycoproteins and surface properties of mitochondrial membranes. In: Kroon AM, Saccone C (Eds). The biogenesis of mitochondria. Academic Press, New York 1974, pp 525–536.

    Google Scholar 

  133. Muller WEG: Cell membranes in sponges. Int Rev Cyt 77:129–181, 1982.

    Google Scholar 

  134. Sly WS, Fisher HD: The phosphomannosyl recognition system for intracellular and intercellular transport of lysosomal enzymes. J Cell Biochem 18:67–85, 1982.

    Google Scholar 

  135. Pierce M., Ballou CE: Cell-cell recognition in yeast, characterization of the sexual agglutination factors from Saccharomyces kluyveri. J Biol Chem 258:3576–3582, 1982.

    Google Scholar 

  136. Rosen SD, Yednock TA: Lymphocyte attachement to high endothelial venules during recirculation: a possible role for carbohydrates as recognition determinants. Mol Cell Biochem (this issue).

  137. randley BK, Ross TS, Schnaar RL: Lymphocyte adhesion to immobolized polysaccharides suggests multiple carbohydrate receptors for recirculation. Submitted for publication.

  138. Turley EA, Roth S: Spontaneous glycosylation of glycosaminoglycan substrates by adherent fibroblasts. Cell 17:109–115, 1979.

    Google Scholar 

  139. Roth J, Lentze MJ, Berger EG: Immunocytochemical demonstration of ecto-galactosyltransferase in absorptive intestinal cells. J Cell Biol 100:118–125, 1985.

    Google Scholar 

  140. Barondes SH: Soluble lectins: a new class of extracellular proteins. Science 223:1259–1264, 1984.

    Google Scholar 

  141. Tauber R, Heinze K, Reutter W: Effect of choroquine on the degradation of L-fucose and the polypeptide moiety of plasma membrane glycoproteins. Eur J Cell Biol 39:380–385, 1986.

    Google Scholar 

  142. Kreisel W, Volk BA, Buchsel R, Reutter W: Different half-lives of the carbohydrate and protein moieties of a 110000 dalton glycoprotein isolated from plasma membraned of rat liver. Proc Natl Acad Sci USA 77:1828–1831, 1980.

    Google Scholar 

  143. Castellot JJ, Choay J, Lormeau J-C, Petitou M, Sache E, Karnovsky MJ: Structural determinants of the capacity of heparin to inhibit the proliferation of vascular smooth muscle cells. II. Evidence for a pentasaccharide sequence that contains a 3–0-sulfate group. J Cell Biol 102:1979–1984, 1986.

    Google Scholar 

  144. Kelly RB: Pathways of protein secretion in eukaryotes. Science 230:25–32, 1985.

    Google Scholar 

  145. Darvill AG, Albersheim P, McNeil M, Lau JM, York WS, Stevenson TT, Thomas J, Doares S, Gollin DS, Chelf P, Davis K: Structure and function of plant cell wall polysaccharides. J Cell Sci (Suppl) 2:203–217, 1985.

    Google Scholar 

  146. Blackburn CC, Swank-Hill P, Schnaar RL: Gangliosides support neural retina cell adhesion. J Biol Chem 261:2873–2881, 1986.

    Google Scholar 

  147. Livi GP, Cardelli JA, Dimond RL: α-Mannosidase-1 mutants of Dictyostelium discoideum: early aggregationessential genes regulate enzyme precursor synthesis, modification, and processing. Differentiation 29:207–215, 1985.

    Google Scholar 

  148. Springer WR, Barondes SH: Discoidin I is implicated in cell-substratum attachment and ordered cell migration of Dictyostelium discoideum. Cell 39:557–564, 1984.

    Google Scholar 

  149. Crowley TE, Nellen W, Gomer RH, Firtel RA: Phenocopy of discoidin I-minus mutants by antisense transformation in Dictyostelium. Cell 43:633–641, 1985.

    Google Scholar 

  150. Sabatini DD, Kreibich G, Morimoto T, Adesnik M: Mechanisms for the incorporation of proteins in membranes and organelles. J Cell Biol 92:1–22, 1982.

    Google Scholar 

  151. Kinders RJ, Johnson TC: Glycopeptides prepared from mouse cerebrum inhibit protein synthesis and cell division in baby hamster kidney cells, but not in their polyoma virus-transformed analogs. Exp Cell Res 136:31–41, 1981.

    Google Scholar 

  152. Rees DA: Stereochemistry and binding behavior of carbohydrate chains. In: Biochemistry of carbohydrates. MTP Int Rev Sci, Biochem Set 1, 5:1–32, 1975.

  153. Dea CMI, Morris ER, Rees DA, Welsh A, Barnes HA, Price J: Associations of like and unlike polysaccharides: mechanism and specificity in galactomannans, intreacting bacterial polysaccharides, and related systems. Carbohy Res 57:249–272, 1977.

    Google Scholar 

  154. Allen A, Pain RH, Robson TR: Model for the structure of the gastric mucous gel. Nature 264:88–89, 1976.

    Google Scholar 

  155. Freeze HH: Interaction of Dictyostelium discoideum lysosomal enzymes with the mammalian phosphomannosyl receptor. J Biol Chem 260:8857–8864, 1985.

    Google Scholar 

  156. Green ED, Boime I, Baenziger JU: Differential processing of asn-linked oligisaccharides on pituitary glycoprotein hormones: implications for biologic function. Mol Cell Biochem (this issue).

  157. Hoflack B, Kornfeld S: Lysosomal enzyme binding to mouse P388D1 macrophage membranes lacking the 215-kDa mannose 6-phosphate receptor: evidence for the existence of a second mannose 6-phosphate receptor. Proc Natl Acad Sci USA 82:4428–4432, 1985.

    Google Scholar 

  158. Gabel CA, Goldberg DE, Kornfeld S: Identification and characterization of cells deficient in the mannose 6-phosphate receptor: evidence for an alternate pathway for lysosomal enzyme targetting. Proc Natl Acad Sci USA 80:775–779, 1983.

    Google Scholar 

  159. Yeo K-T, Parent JB, Yeo T-K, Olden K: Variability in transport rates of secretory glycoproteins through the endoplasmic reticulum and Golgi in human hepatoma cells. J Biol Chem 260:7896–7902, 1985.

    Google Scholar 

  160. Marchase RB, Hiller AM: Glucose phosphotransferase and intracellular protein trafficking. Mol Cell Biochem (this issue).

  161. Freeze HH: Modifications of lysosomal enzymes in Dictyostelium discoideum. Mol Cell Biochem (this issue).

  162. Lodish HF, Kong N: Glucose removal from N-linked oligosaccharides is required for efficient maturation of cerain secretory glycoproteins from the rough endoplasmic reticulum to the golgi complex. J Cell Biol 98:1720–1729, 1984.

    Google Scholar 

  163. Davis CG, Elhammer A, Russell DW, Schneider WJ, Kornfeld S, Brown MS, Goldstein JL: Deletion of clustered O-linked carbohydrates does not impair function of low density lipoprotein receptor in transfected fibroblasts. J Biol Chem 261:2828–2838, 1986.

    Google Scholar 

  164. West CM, Loomis WF: Absence of a carbohydrate modification does not affect the level or the subcellular localization of three membrane glycoproteins in modB mutants of Dictyostelium discoideum. J Biol Chem 260:13803–13809, 1985.

    Google Scholar 

  165. Kingsley DM, Kozarsky KF, Hobbi L, Krieger M: Reversible defects in O-linked glycosylation and LDL receptor expression in a UDP-Gal/UDP-GalNAc 4-epimerase deficient mutant. Cell 44:749–759, 1986.

    Google Scholar 

  166. Gottschalk A, de St. Groth SF: Studies on mucoproteins. III. The accesibility to trypsin of the susceptible bonds in ovine submaxillary land mucoproteins. Biochim Biophys Acta 43:513–519, 1960.

    Google Scholar 

  167. Rogers GN, Herrler G, Paulson JC, Klenk H-D: Influenza C virus uses 9–0-Acetyl-N-Acetylneuraminic Acid as a high affinity receptor determinant for attachment to cells. J Biol Chem 261:5847–5951, 1986.

    Google Scholar 

  168. Firon N, Ofek I, Sharon N: Carbohydrate-binding sites of the mannose-specific fimbrial lectins of enterobacteria. Infect Immun 43:1088–1098, 1984.

    Google Scholar 

  169. Wassarman PM, Bleil JD, Florman HM, Greve JM, Roller RJ, Salzmann GS, Samuels FG: The mouse egg's receptor for sperm; What is it and how does it work? Cold Spring Harb Symp Quant Biol L:11–19, 1985.

    Google Scholar 

  170. Edelman GM: Cell adhesion molecules. Science 219:450–457, 1983.

    CAS  PubMed  Google Scholar 

  171. Cole GJ, Lowey A, Glaser L: Neuronal cell-cell adhesion depends on interactions of N-CAM with heparin-like molecules. Nature 320:445–447, 1986.

    Google Scholar 

  172. Misevic GN, Burger MM: Reconstitution of high cell binding affinity of a marine sponge aggregation factor by cross-linking of small low affinity fragments into a large polyvalent polymer. J Biol Chem 261:2853–2859, 1986.

    Google Scholar 

  173. Berger EG, Hesford FJ: Localization of galactosyl- and sialyltransferase by immunofluorescence: evidence for different sites. Proc Natl Acad Sci USA 82:4736–4739, 1985.

    Google Scholar 

  174. Nicolson G, Lacobiere M, Delmonte P: Outer membrane terminal saccharide of bovine liver nuclei and mitochondria. Exp Cell Res 71:468–472, 1972.

    Google Scholar 

  175. Baenziger JU: The role of glycosylation in protein recognition. Am J Path 121:382–391, 1985.

    Google Scholar 

  176. Lindahl U, Feingold DS, Roden L: Biosynthesis of heparin. TIBS 11:221–225, 1986.

    Google Scholar 

  177. Hendil KB: Ion exchange properties of the glycocalyx of the amoeba Chaos chaos and its relation to pinocytosis. Compt Rend Trav Lab Carlsberg 38:187–211, 1971.

    Google Scholar 

  178. Tavassoli M, Kishimoto T, Kataoka: Liver endothelium mediates the hepatocyte's uptake of ceruloplasmin. J Cell Biol 102:1298–1303, 1986.

    Google Scholar 

  179. Misevic GN, Burger MM: The molecular basis of species specific cell-cell recognition in marine sponges, and a study on organogenesis during metamorphosis. In: Em bryonic development, Part B: Cellular aspects. Alan R. Liss, NY, 1982, pp 193–209.

    Google Scholar 

  180. Pierce M, Arango J: Rous sarcoma virus-transformed baby hamster kidney cells express higher levels of asparagine-linked tri- and tetraantennary glycopeptides containing [GlcNAc-β(1,6)Man-α(1,6)Man] and poly-N-acetyllactosamine sequences than baby hamster kidney cells. J Biol Chem 261:10772–10777, 1986.

    Google Scholar 

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West, C.M. Current ideas on the significance of protein glycosylation. Mol Cell Biochem 72, 3–20 (1986). https://doi.org/10.1007/BF00230632

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