Glycoengineering of Erythropoietin

Post-translational Modification of Protein Biopharmaceuticals

Volumn , Issue , 2009, Pages 295-317

  Elliott, Steve ^a  

^a AMGEN INC   (United States)

Author keywords

Erythropoiesis stimulating agent; Erythroprotein; Glycoengineering; Glycosylation analogs; Hyperglycosylation

Indexed keywords

EID: 84889341048     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527626601.ch12     Document Type: Chapter

References (91)

1. Winearls, C.G., Forman, E., Wiffen, P. and Oliver, D.O. (1989) Recombinant human erythropoietin treatment in patients on maintenance home haemodialysis. Lancet, 2, 569.
2. Eschbach, J.W., Egrie, J.C., Downing, M.R., Browne, J.K. and Adamson, J.W. (1987) Correction of the anemia of end-stage renal disease with recombinant human erythropoietin. Results of a combined phase I and II clinical trial. New England Journal of Medicine, 316, 73-78.
3. Eschbach, J.W., Kelly, M.R., Haley, N.R., Abels, R.I. and Adamson, J.W. (1989) Treatment of the anemia of progressive renal failure with recombinant human erythropoietin. New England Journal of Medicine, 321, 158-163.
4. Sinclair, A.M. and Elliott, S. (2005) Glycoengineering: the effect of glycosylation on the properties of therapeutic proteins. Journal of Pharmaceutical Sciences, 94, 1626-1635.
5. Lai, P.H., Everett, R., Wang, F.F., Arakawa, T. and Goldwasser, E. (1986) Structural characterization of human erythropoietin. Journal of Biological Chemistry, 261, 3116-3121.
6. Lin, F.K., Suggs, S., Lin, C.H., Browne, J.K., Smalling, R., Egrie, J.C., Chen, K.K., Fox, G.M., Martin, F. and Stabinsky, Z. (1985) Cloning and expression of the human erythropoietin gene. Proceedings of the NationalAcademy of Sciences of the United States of America, 82, 7580-7584.
7. Lin, F.K., Lin, C.H., Lai, P.H., Browne, J.K., Egrie, J.C., Smalling, R., Fox, G.M., Chen, K.K., Castro, M. and Suggs, S. (1986) Monkey erythropoietin gene: cloning, expression and comparison with the human erythropoietin gene. Gene, 44, 201-209.
8. Browne, J.K., Cohen, A.M., Egrie, J.C., Lai, P.H., Lin, F.-K., Strickland, T., Watson, E. and Stebbing, N. (1986) Erythropoietin: gene cloning, protein structure, and biological properties. Cold Spring Harbor Symposia on, Quantitative Biology 51, 693-702.
9. Rush, R.S., Derby, P.L., Smith, D.M., Merry, C., Rogers, G., Rohde, M.F. and Katta, V. (1995) Microheterogeneity of erythropoietin carbohydrate structure. Analytical Chemistry, 67, 1442-1452.
10. Sasaki, H., Bothner, B., Dell, A. and Fukuda, M. (1987) Carbohydrate structure of erythropoietin expressed in Chinese hamster ovary cells by a human erythropoietin cDNA. Journal of Biological Chemistry, 262, 12059-12076.
11. Takeuchi, M. and Kobata, A. (1991) Structures and functional roles of the sugar chains of human erythropoietins. Glycobiology, 1, 337-346.
12. Egrie, J. and Browne, J. (2002) Darbepoetin alfa is more potent in vivo and can be administered less frequently than rHuEPO. British Journal of Cancer, 87, 476-477.
13. Takeuchi, M., Takasaki, S., Miyazaki, H., Kato, T., Hoshi, S., Kochibe, N. and Kobata, A. (1988) Comparative study of the asparagine-linked sugar chains of human erythropoietins purified from urine and the culture medium of recombinant Chinese hamster ovary cells. Journal of Biological Chemistry, 263, 3657-3663.
14. Egrie, J.C., Strickland, T.W., Lane, J., Aoki, K., Cohen, A.M., Smalling, R., Trail, G., Lin, F.K., Browne, J.K. and Hines, D.K. (1986) Characterization and biological effects of recombinant human erythropoietin. Immunobiology, 172, 213-224.
15. Wide, L. and Bengtsson, C. (1990) Molecular charge heterogeneity of human serum erythropoietin. British Journal of Haematology, 76, 121-127.
16. Lasne, F., Martin, L., Crepin, N. and De Ceaurriz, J. (2002) Detection of isoelectric profiles of erythropoietin in urine: Differentiation of natural and administered recombinant hormones. Analytical Biochemistry, 311, 119-126.
17. Noguchi, A., Mukuria, C.J., Suzuki, E. and Naiki, M. (1996) Failure of human immunoresponse toN-glycolylneuraminic acid epitope contained in recombinant human erythropoietin. Nephron, 72, 599-603.
18. Hokke, C.H., Bergwerff, A.A., Van Dedem, G.W., van, O.J., Kamerling, J.P. and Vliegenthart, J.F. (1990) Sialylated carbohydrate chains of recombinant human glycoproteins expressed in Chinese hamster ovary cells contain traces of N-glycolylneuraminic acid. FEBS Letters, 275, 9-14.
19. Strickland, T., Adler, B., Aoki, K., Asher, S., Derby, P., Goldwasser, E. and Rogers, G. (1992) Occurrence of sulfate on the Nlinked oligosaccharides of human erythropoietin. Journal of Cellular Biochemistry, (Supplement 16D), 167.
20. Kawasaki, N., Haishima, Y., Ohta, M., Itoh, S., Hyuga, M., Hyuga, S. and Hayakawa, T. (2001) Structural analysis of sulfated N-linked oligosaccharides in erythropoietin. Glycobiology, 11, 1043-1049.
21. Breidbach, A., Catlin, D.H., Green, G.A., Tregub, I., Truong, H. and Gorzek, J. (2003) Detection of recombinant human erythropoietin in urine by isoelectric focusing. Clinical Chemistry, 49, 901-907.
22. Catlin, D.H., Breidbach, A., Elliott, S. and Glaspy, J. (2002) Comparison of the isoelectric focusing patterns of darbepoetin alfa, recombinant human erythropoietin, and endogenous erythropoietin from human urine. Clinical Chemistry, 48, 2057-2059.
23. Lasne, F., Martin, L., Martin, J.A. and DeCeaurriz, J. (2007) Isoelectric profiles of human erythropoietin are different in serum and urine. International Journal of Biological, Macromolecules, 41, 354-357.
24. Bause, E. (1983) Structural requirements ofN-glycosylation of proteins. Studies with proline peptides as conformational probes. Biochemical Journal, 209, 331-336.
25. Roitsch, T. and Lehle, L. (1989) Structural requirements for protein N-glycosylation. Influence of acceptor peptides on cotranslational glycosylation of yeast invertase and site-directed mutagenesis around a sequon sequence. European Journal of Biochemistry, 181, 525-529.
26. Imperiali, B. and Shannon, K.L. (1991) Differences between Asn-Xaa-Thrcontaining peptides: a comparison of solution conformation and substrate behavior with oligosaccharyltransferase. Biochemistry, 30, 4374-4380.
27. Berg, D.T. and Grinnell, B.W. (1993) Pro to Gly (P219G) in a silent glycosylation site results in complete glycosylation in tissue plasminogen activator. Protein Science, 2, 126-127.
28. Elliott, S., Chang, D., Delorme, E., Eris, T. and Lorenzini, T. (2004) Structural requirements for additional N-linked carbohydrate on recombinant human erythropoietin. Journal of Biological Chemistry, 279, 16854-16862.
29. Gavel, Y. and von Heijne, G. (1990) Sequence differences between glycosylated and non-glycosylated Asn-XThr/Ser acceptor sites: implications for protein engineering. Protein Engineering, 3, 433-442.
30. Apweiler, R., Hermjakob, H. and Sharon, N. (1999) On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochimica et Biophysica Acta, 1473, 4-8.
31. Nilsson, I.M. and von Heijne, G. (1993) Determination of the distance between the oligosaccharyltransferase active site and the endoplasmic reticulummembrane. Journal of Biological Chemistry, 268, 5798-5801.
32. Chen, W., Helenius, J., Braakman, I. and Helenius, A. (1995) Cotranslational folding and calnexin binding during glycoprotein synthesis. Proceedings of the National Academy of Sciences of the United States of America, 92, 6229-6233.
33. Kornfeld, R. and Kornfeld, S. (1985) Assembly of asparagine-linked oligosaccharides. Annual Review of Biochemistry, 54, 631-664. A review with 283 references.
34. Bause, E. and Hettkamp, H. (1979) Primary structural requirements for N-glycosylation of peptides in rat liver. FEBS Letters, 108, 341-344.
35. Shakin-Eshleman, S.H., Spitalnik, S.L. and Kasturi, L. (1996) The amino acid at theXposition of an Asn-X-Ser sequon is an important determinant of N-linked coreglycosylation efficiency. Journal of Biological Chemistry, 271, 6363-6366.
36. Shakin-Eshleman, S.H., Wunner, W.H. and Spitalnik, S.L. (1993) Efficiency of N-linked core glycosylation at asparagine-319 of rabies virus glycoprotein is altered by deletions C-terminal to the glycosylation sequon. Biochemistry, 32, 9465-9472.
37. Elliott, S., Bartley, T., Delorme, E., Derby, P., Hunt, R., Lorenzini, T., Parker, V., Rohde, M.F. and Stoney, K. (1994) Structural requirements for addition of O-linked carbohydrate to recombinant erythropoietin. Biochemistry, 33, 11237-11245.
38. Imperiali, B. and Hendrickson, T.L. (1995) Asparagine-linked glycosylation: specificity and function of oligosaccharyl transferase. Bioorganic & Medicinal Chemistry, 3, 1565-1578.
39. Breuer, W., Klein, R.A., Hardt, B., Bartoschek, A. and Bause, E. (2001) Oligosaccharyltransferase is highly specific for the hydroxyamino acid in Asn-Xaa-Thr/Ser. FEBS Letters, 501, 106-110.
40. Kasturi, L., Eshleman, J.R., Wunner, W.H. and Shakin-Eshleman, S.H. (1995) The hydroxy amino acid in an Asn-X-Ser/Thr sequon can influence N-linked core glycosylation efficiency and the level of expression of a cell surface glycoprotein. Journal of Biological Chemistry, 270, 14756-14761.
41. Nishikawa, A. and Mizuno, S. (2001) The efficiency of N-linked glycosylation of bovine DNase I depends on the Asn-Xaa-Ser/Thr sequence and the tissue of origin. Biochemical Journal, 355, 1-8.
42. Nicolaes, G.A., Villoutreix, B.O. and Dahlback, B. (1999) Partial glycosylation of Asn2181 in human factor V as a cause of molecular and functional heterogeneity. Modulation of glycosylation efficiency by mutagenesis of the consensus sequence for N-linked glycosylation. Biochemistry, 38, 13584-13591.
43. Cheetham, J.C., Smith, D.M., Aoki, K.H., Stevenson, J.L., Hoeffel, T.J., Syed, R.S., Egrie, J. and Harvey, T.S. (1998) NMR structure of human erythropoietin and a comparison with its receptor bound conformation. Nature Structural Biology, 5, 861-866.
44. Delorme, E., Lorenzini, T., Giffin, J., Martin, F., Jacobsen, F., Boone, T. and Elliott, S. (1992) Role of glycosylation on the secretion and biological activity of erythropoietin. Biochemistry, 31, 9871-9876.
45. Tsuda, E., Kawanishi, G., Ueda, M., Masuda, S. and Sasaki, R. (1990) The role of carbohydrate in recombinant human erythropoietin. European Journal of Biochemistry, 188, 405-411.
46. Yamaguchi, K., Akai, K., Kawanishi, G., Ueda, M., Masuda, S. and Sasaki, R. (1991) Effects of site-directed removal of Nglycosylation sites in human erythropoietin on its production and biological properties. Journal of Biological Chemistry, 266, 20434-20439.
47. Dordal, M.S., Wang, F.F. and Goldwasser, E. (1985) The role of carbohydrate in erythropoietin action. Endocrinology, 116, 2293-2299.
48. Egrie, J.C. and Browne, J.K. (2001) Development and characterization of novel erythropoiesis stimulating protein (NESP). Nephrology Dialysis Transplantation, 16 (Suppl-13), 3-13.
49. Elliott, S., Egrie, J., Browne, J., Lorenzini, T., Busse, L., Rogers, N. and Ponting, I. (2004) Control of rHuEPO biological activity: the role of carbohydrate. Experimental Hematology, 32, 1146-1155.
50. Higuchi, M., Oh-eda, M., Kuboniwa, H., Tomonoh, K., Shimonaka, Y. and Ochi, N. (1992) Role of sugar chains in the expression of the biological activity of human erythropoietin. Journal of Biological Chemistry, 267, 7703-7709.
51. Narhi, L.O., Arakawa, T., Aoki, K., Wen, J., Elliott, S., Boone, T. and Cheetham, J. (2001) Asn to Lys mutations at three sites which are N-glycosylated in the mammalian protein decrease the aggregation of Escherichia coli-derived erythropoietin. Protein Engineering, 14, 135-140.
52. Toyoda, T., Itai, T., Arakawa, T., Aoki, K.H. and Yamaguchi, H. (2000) Stabilization of human recombinant erythropoietin through interactions with the highly branched N-glycans. Journal of Biochemistry, 128, 731-737.
53. Toyoda, T., Arakawa, T. and Yamaguchi, H. (2002) N-Glycans stabilize human erythropoietin through hydrophobic interactions with the hydrophobic protein surface: studies by surface plasmon resonance analysis. Journal of Biochemistry, 131, 511-515.
54. Narhi, L.O., Arakawa, T., Aoki, K.H., Elmore, R., Rohde, M.F., Boone, T. and Strickland, T.W. (1991) The effect of carbohydrate on the structure and stability of erythropoietin. Journal of Biological Chemistry, 266, 23022-23026.
55. Endo, Y., Nagai, H., Watanabe, Y., Ochi, K. and Takagi, T. (1992) Heat-induced aggregation of recombinant erythropoietin in the intact and deglycosylated states as monitored by gel permeation chromatography combined with a lowangle laser light scattering technique. Journal of Biochemistry, 112, 700-706.
56. Elliott, S., Lorenzini, T., Asher, S., Aoki, K., Brankow, D., Buck, L., Busse, L., Chang, D., Fuller, J., Grant, J., Hernday, N., Hokum, M., Hu, S., Knudten, A., Levin, N., Komorowski, R., Martin, F., Navarro, R., Osslund, T., Rogers, G., Rogers, N., Trail, G. and Egrie, J. (2003) Enhancement of therapeutic protein in vivo activities through glycoengineering. Nature Biotechnology, 21, 414-421.
57. Egrie, J.C., Dwyer, E., Browne, J.K., Hitz, A. and Lykos, M.A. (2003) Darbepoetin alfa has a longer circulating half-life and greater in vivo potency than recombinant human erythropoietin. Experimental Hematology, 31, 290-299.
58. Takeuchi, M., Takasaki, S., Shimada, M. and Kobata, A. (1990) Role of sugar chains in the in vitro biological activity of human erythropoietin produced in recombinant Chinese hamster ovary cells. Journal of Biological Chemistry, 265, 12127-12130.
59. Goldwasser, E., Kung, C.K. and Eliason, J. (1974) On the mechanism of erythropoietin-induced differentiation. 13. The role of sialic acid in erythropoietin action. Journal of Biological Chemistry, 249, 4202-4206.
60. Spivak, J.L. and Hogans, B.B. (1989) The in vivo metabolism of recombinant human erythropoietin in the rat. Blood, 73, 90-99.
61. Darling, R.J., Kuchibhotla, U., Glaesner, W., Micanovic, R., Witcher, D.R. and Beals, J.M. (2002) Glycosylation of erythropoietin affects receptor binding kinetics: role of electrostatic interactions. Biochemistry, 41, 14524-14531.
62. Elliott, S., Lorenzini, T., Chang, D., Barzilay, J. and Delorme, E. (1997) Mapping of the active site of recombinant human erythropoietin. Blood, 89, 493-502.
63. Elliott, S., Lorenzini, T., Chang, D., Barzilay, J., Delorme, E., Giffin, J. and Hesterberg, L. (1996) Fine-structure epitope mapping of antierythropoietin monoclonal antibodies reveals a model of recombinant human erythropoietin structure. Blood, 87, 2702-2713.
64. Syed, R.S., Reid, S.W., Li, C., Cheetham, J.C., Aoki, K.H., Liu, B., Zhan, H., Osslund, T.D., Chirino, A.J., Zhang, J., Finer-Moore, J., Elliott, S., Sitney, K., Katz, B.A., Matthews, D.J., Wendoloski, J.J., Egrie, J. and Stroud, R.M. (1998) Efficiency of signalling through cytokine receptors depends critically on receptor orientation. Nature, 395, 511-516.
65. Elliott, S., Chang, D., Delorme, E., Dunn, C., Egrie, J., Giffin, J., Lorenzini, T., Talbot, C. and Hesterberg, L. (1996) Isolation and characterization of conformation sensitive antierythropoietin monoclonal antibodies: effect of disulfide bonds and carbohydrate on recombinant human erythropoietin structure. Blood, 87, 2714-2722.
66. Macdougall, I.C., Gray, S.J., Elston, O., Breen, C., Jenkins, B., Browne, J. and Egrie, J. (1999) Pharmacokinetics of novel erythropoiesis stimulating protein compared with epoetin alfa in dialysis patients. Journal of the American Society of, Nephrology, 10, 2392-2395.
67. Nissenson, A.R. (2001) Novel erythropoiesis stimulating protein for managing the anemia of chronic kidney disease. American Journal of Kidney Diseases, 38, 1390-1397.
68. Nissenson, A.R., Swan, S.K., Lindberg, J.S., Soroka, S.D., Beatey, R., Wang, C., Picarello, N., McDermott-Vitak, A. and Maroni, B.J. (2002) Randomized, controlled trial of darbepoetin alfa for the treatment of anemia in hemodialysis patients. American Journal of Kidney Diseases, 40, 110-118.
69. Glaspy, J., Henry, D., Patel, R., Tchekmedyian, S., Applebaum, S., Berdeaux, D., Lloyd, R., Berg, R., Austin, M., Rossi, G. and Darbepoetin, A. (2005) Effects of chemotherapy on endogenous erythropoietin levels and the pharmacokinetics and erythropoietic response of darbepoetin alfa: a randomised clinical trial of synchronous versus asynchronous dosing of darbepoetin alfa. European Journal of Cancer, 41, 1140-1149.
70. Elliott, S., Aoki, K., Agoram, B., Brankow, D., Doshi, S. and Molineux, G. (2006) Evaluation of hyperglycosylated erythropoiesis stimulating proteins developed using glycoengineering. Proceedings of the American Association for Cancer Research, 47, abstract 2176.
71. Osterborg, A., De Boer, R., Clemens, M., Renczes, G., Kotasek, D., Prausova, J., Marschner, N., Hedenus, M., Hendricks, L. and Amado, R. (2006) A novel erythropoiesis-stimulating agent (AMG114) with 131-hour half-life effectively treats chemotherapy-induced anemia when administered as 200 mcg every 3 weeks. Journal of Clinical Oncology, 24, 8626.
72. Sasu, B.A., Hartley, C., McElroy, T., Khaja, R., Elliott, S., Egrie, J.C., Browne, J.K., Begley, C.G. and Molineux, G. (2004) HastheUnit oferythropoieticactivity outlived its usefulness? Blood, 102, 4386.
73. Tolman, C., Richardson, D., Bartlett, C. and Will, E. (2005) Structured conversion from thrice weekly to weekly erythropoietic regimens using a computerized decisionsupport system: a randomized clinical study. Journal of the American Society of Nephrology 16, 1463-1470.
74. Fukuda, M.N., Sasaki, H., Lopez, L. and Fukuda, M. (1989) Survival of recombinant erythropoietin in the circulation: the role of carbohydrates. Blood, 73, 84-89.
75. Dinkelaar, R.B., Engels, E.Y., Hart, A.A., Schoemaker, L.P., Bosch, E. and Chamuleau, R.A. (1981) Metabolic studies on erythropoietin (EP): II. The role of liver and kidney in the metabolism of Ep. Experimental Hematology, 9, 796-803.
76. Widness, J.A., Veng-Pedersen, P., Schmidt, R.L., Lowe, L.S., Kisthard, J.A. and Peters, C. (1996) In vivo 125Ierythropoietin pharmacokinetics are unchanged after anesthesia, nephrectomy and hepatectomy in sheep. Journal of Pharmacology & Experimental Therapeutics, 279, 1205-1210.
77. Jensen, J.D., Jensen, L.W., Madsen, J.K. and Poulsen, L. (1995) The metabolism of erythropoietin in liver cirrhosis patients compared with healthy volunteers. European Journal of Haematology, 54, 111-116.
78. Sawyer, S.T., Krantz, S.B. and Goldwasser, E. (1987) Binding and receptor-mediated endocytosis of erythropoietin in Friend virus-infected erythroid cells. Journal of Biological Chemistry, 262, 5554-5562.
79. Sawada, K., Krantz, S.B., Sawyer, S.T. and Civin, C.I. (1988) Quantitation of specific binding of erythropoietin to human erythroid colony-forming cells. Journal of Cellular Physiology, 137, 337-345.
80. Fraser, J.K., Lin, F.K. and Berridge, M.V. (1988) Expression of high affinity receptors for erythropoietin on human bone marrow cells and on the human erythroleukemic cell line, HEL. Experimental Hematology, 16, 836-842.
81. Gross, A.W. and Lodish, H.F. (2006) Cellular trafficking and degradation of erythropoietin and novel erythropoiesis stimulating protein (NESP). Journal of Biological Chemistry, 281, 2024-2032.
82. Chapel, S., Veng-Pedersen, P., Hohl, R.J., Schmidt, R.L., McGuire, E.M. and Widness, J.A. (2001) Changes in erythropoietin pharmacokinetics following busulfan-induced bone marrow ablation in sheep: evidence for bone marrow as a major erythropoietin elimination pathway. Journal of Pharmacology & Experimental Therapeutics, 298, 820-824.
83. Veng-Pedersen, P., Chapel, S., Al-Huniti, N.H., Schmidt, R.L., Sedars, E.M., Hohl, R.J. and Widness, J.A. (2004) Pharmacokinetic tracer kinetics analysis of changes in erythropoietin receptor population in phlebotomyinduced anemia and bone marrow ablation. Biopharmaceutics & Drug Disposition, 25, 149-156.
84. Hartley, C., Elliott, S., Begley, C.G., McElroy, P., Sutherland, W., Khaja, R., Heatherington, A.C., Graves, T., Schultz, H., Del Castillo, J. and Molineux, G. (2003) Kinetics of haematopoietic recovery after dose-intensive chemo/radiotherapy in mice: optimized erythroid support with darbepoetin alpha. British Journal of Haematology, 122, 623-636.
85. Piroso, E., Erslev, A.J., Flaharty, K.K. and Caro, J. (1991) Erythropoietin life span in rats with hypoplastic and hyperplastic bone marrows. American Journal of Hematology, 36, 105-110.
86. Agoram, B., Molineux, G., Jang, G., Aoki, K., Gegg, L., Narhi, L. and Elliott, S. (2007) Effects of altered receptor binding activity on the clearance of erythropoiesisstimulating proteins: a minor role of erythropoietin receptor-mediated pathways. Nephrology Dialysis Transplantation, 21, iv303-iv304.
87. Fu, J.-S., Lertora, J.J.L., Brookins, J., Rice, J.C. and Fisher, J.W. (1988) Pharmacokinetics of erythropoietin in intact and anephric dogs. Journal of Laboratory and Clinical, Medicine 111, 669-676.
88. Kindler, J., Eckardt, K.U., Ehmer, B., Jandeleit, K., Kurtz, A., Schreiber, A., Scigalla, P. and Sieberth, H.G. (1989) Single-dose pharmacokinetics of recombinant human erythropoietin in patients with various degrees of renal failure. Nephrology Dialysis Transplantation, 4, 345-349.
89. Macdougall, I.C., Roberts, D.E., Coles, G.A. and Williams, J.D. (1991) Clinical pharmacokinetics of epoetin (recombinant human erythropoietin). Clinical Pharmacokinetics, 20, 99-113.
90. Yoon, W.H., Park, S.J., Kim, I.C. and Lee, M.G. (1997) Pharmacokinetics of recombinant human erythropoietin in rabbits and 3/4 nephrectomized rats. Research Communications in Molecular Pathology & Pharmacology, 96, 227-240.
91. Flaharty, K.K. (1990) Clinical pharmacology of recombinant human erythropoietin (r-HuEPO). Pharmacotherapy, 10, 9S-14S.