Toward fully synthetic glycoproteins by ultimately convergent routes: A solution to a long-standing problem

Journal of the American Chemical Society

Volumn 126, Issue 21, 2004, Pages 6576-6578

  Warren, J David ^a   Miller, Justin S ^a   Keding, Stacy J ^a   Danishefsky, Samuel J ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Havemeyer Hall ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN;

ARTICLE; CARBOHYDRATE SYNTHESIS; DISSOCIATION; DISULFIDE BOND; EPIMERIZATION; GLYCOPROTEIN SYNTHESIS; GLYCOSYLATION; HYDROLYSIS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PEPTIDE SYNTHESIS; PROTON NUCLEAR MAGNETIC RESONANCE; REACTION ANALYSIS; REDUCTION;

ACYLATION; AMINO ACID SEQUENCE; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; ERYTHROPOIETIN; GLYCOPROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; PROTEIN CONFORMATION;

EID: 2542548800     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja0491836     Document Type: Article

References (44)

1. (a) Imperiali, B.; O'Connor, S. E.; Hendrickson, T.; Kellenberger, C. Pure Appl. Chem. 1999, 71, 777-787.
2. (b) Lis, H.; Sharon, N. Eur. J. Biochem. 1993, 218, 1-27.
3. (c) Rudd, P. M.; Elliott, T.; Cresswell, P.; Wilson, I. A.; Dwek, R. A. Science 2001, 291, 2370-2376.
4. (d) Bertozzi, C. R.; Kiessling, L. L. Science 2001, 291, 2357-2364.
5. (a) Calarese, D. A.; Scanlan, C. N.; Zwick, M. B.; Deechongkit, S.; Mimura, Y.; Kunert, R.; Zhu, P.; Wormald, M. R.; Stanfield, R. L.; Roux, K. H.; Kelly, J. W.; Rudd, P. M.; Dwek, R. A.; Katinger, H.; Burton, D. R.; Wilson, I. A. Science 2003, 300, 2065-2071.
6. (b) von Mensdorff-Pouilly, S.; Snijdewint, F. G.; Verstraeten, A. A.; Verheijen, R. H.; Kenemans, P. Int. J. Biol. Markers 2000, 15, 343-356.
7. (a) Dudkin, V. Y.; Miller, J. S.; Danishefsky, S. J. J. Am. Chem. Soc. 2004, 126, 736-738.
8. (b) Peracaula, R.; Tabares, G.; Royle, L.; Harvey, D. J.; Dwek, R. A.; Rudd, P. M.; de Llorens, R. Glycobiology 2003, 13, 457-470.
9. (a) Ridley, D. M.; Dawkins, F.; Perlin, E. J. Natl. Med. Assoc. 1994, 86, 129-135.
10. (b) Durand, G.; Seta, N. Clin. Chem. 2000, 46, 795-805.
11. (c) Koeller, K. M.; Wong, C. H. Nat. Biotechnol. 2000, 18, 835-841.
12. Rush, R. S.; Derby, P. L.; Smith, D. M.; Merry, C.; Rogers, G.; Rohde, M. F.; Katta, V. Anal. Chem. 1995, 67, 1442-1452.
13. Lai, P. H.; Everett, R.; Wang, F. F.; Arakawa, T.; Goldwasser, E. J. Biol. Chem. 1986, 261, 3116-3121.
14. Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N.; Weissig, H.; Shindyalov, I. N.; Boume, P. E. Nucleic Acids Res. 2000, 28, 235-242.
15. Cheetham, J. C.; Smith, D. M.; Aoki, K. H.; Stevenson, J. L.; Hoeffel, T. J.; Syed, R. S.; Egrie, J.; Harvey, T. S. Nat. Struct. Biol. 1998, 5, 861-866.
16. Rahbek-Nielsen, H.; Roepstorff, P.; Reischl, H.; Wozny, M.; Koll, H.; Haselbeck, A. J. Mass Spectrom. 1997, 32, 948-958.
17. (a) Kornfeld, R.; Kornfeld, S. Annu. Rev. Biochem. 1985, 54, 631-664.
18. (b) Roth, J. Chem. Rev. 2002, 102, 285-303.
19. Geyer, H.; Holschbach, C.; Hunsmann, G.; Schneider, J. J. Biol. Chem. 1988, 263, 11760-11767.
20. (a) Likhosherstov, L. M.; Novikova, O. S.; Derevitskaja, V. A.; Kochetkov, N. K. Carbohydr. Res. 1986, 146, C1-C5.
21. (b) Cohen-Anisfeld, S. T.; Lansbury, P. T. J. Am. Chem. Soc. 1993, 115, 10531-10537.
22. (c) Dawson, P. E.; Muir, T. W.; Clark-Lewis, I.; Kent, S. B. H. Science 1994, 266, 776-779.
23. Miller, J. S.; Dudkin, V. Y.; Lyon, G. J.; Muir, T. W.; Danishefsky, S. J. Angew. Chem., Int. Ed. 2003, 42, 431-434.
24. (a) Mandal, M.; Dudkin, V. Y.; Geng, X.; Danishefsky, S. J. Angew. Chem., Int. Ed. 2004, 43, 2557-2561.
25. (b) Geng, X.; Dudkin, V. Y.; Mandal, M.; Danishefsky, S. J. Angew. Chem., Int. Ed. 2004, 43. 2562-2575.
26. For the state of the art in biological approaches toward multiply glycosylated proteins, see: Zhang, Z.; Gildersleeve, J.; Yang, Y. Y.; Xu, R.; Loo, J. A.; Uryu, S.; Wong, C. H.; Schultz, P. G. Science 2004, 303, 371-373.
27. Significant advances in this type of problem arose through the use of Ellman's Fmoc-based sulfonamide linker (Shin, Y.; Winans, K. A.; Backes, B. J.; Kent, S. B. H.; Ellman, J. A.; Bertozzi, C. R. J. Am. Chem. Soc. 1999, 121, 11684-11689), which has been employed in the synthesis of glycopeptide thioesters. The method we practice here, however, insists on maximal convergence, as opposed to a "cassette" approach to glycan incorporation. We note that certain glycosidic linkages (e.g., fucosidic linkages in erythropoietin) are particularly unstable toward the acidic conditions (TFA) required for protecting group cleavage. Other "cassette"-based Fmoc solid-phase peptide synthesis (SPPS) techniques potentially leading to glycopeptide thioesters also include acidic conditions at some point. These methods involve alteration of the Fmoc deblocking conditions [(a) Li, X. Q.; Kawakami, T.; Aimoto, S. Tetrahedron Lett. 1998, 39, 8669-8672. (b) Clippingdale, A. B.; Barrow, C. J.; Wade, J. D. J. Pept. Sci. 2000, 6, 225-234. (c) Hojo, H.; Haginoya, E.; Matsumoto, Y.; Nakahara, Y.; Nabeshima, K.; Toole, B. P.; Watanabe, Y. Tetrahedron Lett. 2003, 44, 2961-2964], or direct conversion into thioesters of C-terminal acids (von Eggelkraut-Gottanka, R.; Klose, A.; Beck-Sickinger, A. G.; Beyermann, M. Tetrahedron Lett. 2003, 44, 3551-3554), esters (Swinnen, D.; Hilvert, D. Org. Lett. 2000, 2, 2439-2442), or trithioortho esters (Brask, J.; Albericio, F.; Jensen, K. J. Org. Lett. 2003, 5, 2951-2953). Boc-based SPPS employs strongly acidic cleavage conditions (liquid HF) that are incompatible with many glycosidic linkages.
28. Significant advances in this type of problem arose through the use of Ellman's Fmoc-based sulfonamide linker (Shin, Y.; Winans, K. A.; Backes, B. J.; Kent, S. B. H.; Ellman, J. A.; Bertozzi, C. R. J. Am. Chem. Soc. 1999, 121, 11684-11689), which has been employed in the synthesis of glycopeptide thioesters. The method we practice here, however, insists on maximal convergence, as opposed to a "cassette" approach to glycan incorporation. We note that certain glycosidic linkages (e.g., fucosidic linkages in erythropoietin) are particularly unstable toward the acidic conditions (TFA) required for protecting group cleavage. Other "cassette"-based Fmoc solid-phase peptide synthesis (SPPS) techniques potentially leading to glycopeptide thioesters also include acidic conditions at some point. These methods involve alteration of the Fmoc deblocking conditions [(a) Li, X. Q.; Kawakami, T.; Aimoto, S. Tetrahedron Lett. 1998, 39, 8669-8672. (b) Clippingdale, A. B.; Barrow, C. J.; Wade, J. D. J. Pept. Sci. 2000, 6, 225-234. (c) Hojo, H.; Haginoya, E.; Matsumoto, Y.; Nakahara, Y.; Nabeshima, K.; Toole, B. P.; Watanabe, Y. Tetrahedron Lett. 2003, 44, 2961-2964], or direct conversion into thioesters of C-terminal acids (von Eggelkraut-Gottanka, R.; Klose, A.; Beck-Sickinger, A. G.; Beyermann, M. Tetrahedron Lett. 2003, 44, 3551-3554), esters (Swinnen, D.; Hilvert, D. Org. Lett. 2000, 2, 2439-2442), or trithioortho esters (Brask, J.; Albericio, F.; Jensen, K. J. Org. Lett. 2003, 5, 2951-2953). Boc-based SPPS employs strongly acidic cleavage conditions (liquid HF) that are incompatible with many glycosidic linkages.
29. Significant advances in this type of problem arose through the use of Ellman's Fmoc-based sulfonamide linker (Shin, Y.; Winans, K. A.; Backes, B. J.; Kent, S. B. H.; Ellman, J. A.; Bertozzi, C. R. J. Am. Chem. Soc. 1999, 121, 11684-11689), which has been employed in the synthesis of glycopeptide thioesters. The method we practice here, however, insists on maximal convergence, as opposed to a "cassette" approach to glycan incorporation. We note that certain glycosidic linkages (e.g., fucosidic linkages in erythropoietin) are particularly unstable toward the acidic conditions (TFA) required for protecting group cleavage. Other "cassette"-based Fmoc solid-phase peptide synthesis (SPPS) techniques potentially leading to glycopeptide thioesters also include acidic conditions at some point. These methods involve alteration of the Fmoc deblocking conditions [(a) Li, X. Q.; Kawakami, T.; Aimoto, S. Tetrahedron Lett. 1998, 39, 8669-8672. (b) Clippingdale, A. B.; Barrow, C. J.; Wade, J. D. J. Pept. Sci. 2000, 6, 225-234. (c) Hojo, H.; Haginoya, E.; Matsumoto, Y.; Nakahara, Y.; Nabeshima, K.; Toole, B. P.; Watanabe, Y. Tetrahedron Lett. 2003, 44, 2961-2964], or direct conversion into thioesters of C-terminal acids (von Eggelkraut-Gottanka, R.; Klose, A.; Beck-Sickinger, A. G.; Beyermann, M. Tetrahedron Lett. 2003, 44, 3551-3554), esters (Swinnen, D.; Hilvert, D. Org. Lett. 2000, 2, 2439-2442), or trithioortho esters (Brask, J.; Albericio, F.; Jensen, K. J. Org. Lett. 2003, 5, 2951-2953). Boc-based SPPS employs strongly acidic cleavage conditions (liquid HF) that are incompatible with many glycosidic linkages.
30. Significant advances in this type of problem arose through the use of Ellman's Fmoc-based sulfonamide linker (Shin, Y.; Winans, K. A.; Backes, B. J.; Kent, S. B. H.; Ellman, J. A.; Bertozzi, C. R. J. Am. Chem. Soc. 1999, 121, 11684-11689), which has been employed in the synthesis of glycopeptide thioesters. The method we practice here, however, insists on maximal convergence, as opposed to a "cassette" approach to glycan incorporation. We note that certain glycosidic linkages (e.g., fucosidic linkages in erythropoietin) are particularly unstable toward the acidic conditions (TFA) required for protecting group cleavage. Other "cassette"-based Fmoc solid-phase peptide synthesis (SPPS) techniques potentially leading to glycopeptide thioesters also include acidic conditions at some point. These methods involve alteration of the Fmoc deblocking conditions [(a) Li, X. Q.; Kawakami, T.; Aimoto, S. Tetrahedron Lett. 1998, 39, 8669-8672. (b) Clippingdale, A. B.; Barrow, C. J.; Wade, J. D. J. Pept. Sci. 2000, 6, 225-234. (c) Hojo, H.; Haginoya, E.; Matsumoto, Y.; Nakahara, Y.; Nabeshima, K.; Toole, B. P.; Watanabe, Y. Tetrahedron Lett. 2003, 44, 2961-2964], or direct conversion into thioesters of C-terminal acids (von Eggelkraut-Gottanka, R.; Klose, A.; Beck-Sickinger, A. G.; Beyermann, M. Tetrahedron Lett. 2003, 44, 3551-3554), esters (Swinnen, D.; Hilvert, D. Org. Lett. 2000, 2, 2439-2442), or trithioortho esters (Brask, J.; Albericio, F.; Jensen, K. J. Org. Lett. 2003, 5, 2951-2953). Boc-based SPPS employs strongly acidic cleavage conditions (liquid HF) that are incompatible with many glycosidic linkages.
31. Significant advances in this type of problem arose through the use of Ellman's Fmoc-based sulfonamide linker (Shin, Y.; Winans, K. A.; Backes, B. J.; Kent, S. B. H.; Ellman, J. A.; Bertozzi, C. R. J. Am. Chem. Soc. 1999, 121, 11684-11689), which has been employed in the synthesis of glycopeptide thioesters. The method we practice here, however, insists on maximal convergence, as opposed to a "cassette" approach to glycan incorporation. We note that certain glycosidic linkages (e.g., fucosidic linkages in erythropoietin) are particularly unstable toward the acidic conditions (TFA) required for protecting group cleavage. Other "cassette"-based Fmoc solid-phase peptide synthesis (SPPS) techniques potentially leading to glycopeptide thioesters also include acidic conditions at some point. These methods involve alteration of the Fmoc deblocking conditions [(a) Li, X. Q.; Kawakami, T.; Aimoto, S. Tetrahedron Lett. 1998, 39, 8669-8672. (b) Clippingdale, A. B.; Barrow, C. J.; Wade, J. D. J. Pept. Sci. 2000, 6, 225-234. (c) Hojo, H.; Haginoya, E.; Matsumoto, Y.; Nakahara, Y.; Nabeshima, K.; Toole, B. P.; Watanabe, Y. Tetrahedron Lett. 2003, 44, 2961-2964], or direct conversion into thioesters of C-terminal acids (von Eggelkraut-Gottanka, R.; Klose, A.; Beck-Sickinger, A. G.; Beyermann, M. Tetrahedron Lett. 2003, 44, 3551-3554), esters (Swinnen, D.; Hilvert, D. Org. Lett. 2000, 2, 2439-2442), or trithioortho esters (Brask, J.; Albericio, F.; Jensen, K. J. Org. Lett. 2003, 5, 2951-2953). Boc-based SPPS employs strongly acidic cleavage conditions (liquid HF) that are incompatible with many glycosidic linkages.
32. Significant advances in this type of problem arose through the use of Ellman's Fmoc-based sulfonamide linker (Shin, Y.; Winans, K. A.; Backes, B. J.; Kent, S. B. H.; Ellman, J. A.; Bertozzi, C. R. J. Am. Chem. Soc. 1999, 121, 11684-11689), which has been employed in the synthesis of glycopeptide thioesters. The method we practice here, however, insists on maximal convergence, as opposed to a "cassette" approach to glycan incorporation. We note that certain glycosidic linkages (e.g., fucosidic linkages in erythropoietin) are particularly unstable toward the acidic conditions (TFA) required for protecting group cleavage. Other "cassette"-based Fmoc solid-phase peptide synthesis (SPPS) techniques potentially leading to glycopeptide thioesters also include acidic conditions at some point. These methods involve alteration of the Fmoc deblocking conditions [(a) Li, X. Q.; Kawakami, T.; Aimoto, S. Tetrahedron Lett. 1998, 39, 8669-8672. (b) Clippingdale, A. B.; Barrow, C. J.; Wade, J. D. J. Pept. Sci. 2000, 6, 225-234. (c) Hojo, H.; Haginoya, E.; Matsumoto, Y.; Nakahara, Y.; Nabeshima, K.; Toole, B. P.; Watanabe, Y. Tetrahedron Lett. 2003, 44, 2961-2964], or direct conversion into thioesters of C-terminal acids (von Eggelkraut-Gottanka, R.; Klose, A.; Beck-Sickinger, A. G.; Beyermann, M. Tetrahedron Lett. 2003, 44, 3551-3554), esters (Swinnen, D.; Hilvert, D. Org. Lett. 2000, 2, 2439-2442), or trithioortho esters (Brask, J.; Albericio, F.; Jensen, K. J. Org. Lett. 2003, 5, 2951-2953). Boc-based SPPS employs strongly acidic cleavage conditions (liquid HF) that are incompatible with many glycosidic linkages.
33. Significant advances in this type of problem arose through the use of Ellman's Fmoc-based sulfonamide linker (Shin, Y.; Winans, K. A.; Backes, B. J.; Kent, S. B. H.; Ellman, J. A.; Bertozzi, C. R. J. Am. Chem. Soc. 1999, 121, 11684-11689), which has been employed in the synthesis of glycopeptide thioesters. The method we practice here, however, insists on maximal convergence, as opposed to a "cassette" approach to glycan incorporation. We note that certain glycosidic linkages (e.g., fucosidic linkages in erythropoietin) are particularly unstable toward the acidic conditions (TFA) required for protecting group cleavage. Other "cassette"-based Fmoc solid-phase peptide synthesis (SPPS) techniques potentially leading to glycopeptide thioesters also include acidic conditions at some point. These methods involve alteration of the Fmoc deblocking conditions [(a) Li, X. Q.; Kawakami, T.; Aimoto, S. Tetrahedron Lett. 1998, 39, 8669-8672. (b) Clippingdale, A. B.; Barrow, C. J.; Wade, J. D. J. Pept. Sci. 2000, 6, 225-234. (c) Hojo, H.; Haginoya, E.; Matsumoto, Y.; Nakahara, Y.; Nabeshima, K.; Toole, B. P.; Watanabe, Y. Tetrahedron Lett. 2003, 44, 2961-2964], or direct conversion into thioesters of C-terminal acids (von Eggelkraut-Gottanka, R.; Klose, A.; Beck-Sickinger, A. G.; Beyermann, M. Tetrahedron Lett. 2003, 44, 3551-3554), esters (Swinnen, D.; Hilvert, D. Org. Lett. 2000, 2, 2439-2442), or trithioortho esters (Brask, J.; Albericio, F.; Jensen, K. J. Org. Lett. 2003, 5, 2951-2953). Boc-based SPPS employs strongly acidic cleavage conditions (liquid HF) that are incompatible with many glycosidic linkages.
34. A phenolic ester may function as an acylating agent when employed in conjunction with an intramolecularly disposed amine equivalent that is generated in situ via Staudinger chemistry. For examples, see: (a) Nilsson, B. L.; Kiessling, L. L.: Raines, R. T. Org. Lett. 2000, 2, 1939-1941.
35. (b) Saxon E.: Armstrong, J. I.; Bertozzi, C. R. Org Lett. 2000, 2, 2141-2143.
36. (c) Bianchi, A.; Bernardi, A. Tetrahedron Lett. 2004, 45, 2231-2234.
37. See: Verhaeghe, J.; Lacassie, E.; Bertrand, M.; Trudelle, Y. Tetrahedron Lett. 1993, 34, 461-464 and references therein.
38. Caserio, M. C.; Fisher, C. L.; Kim, J. K. J. Org. Chem. 1985, 50, 4390-4393.
39. The protected peptide acid was synthesized by Fmoc SPPS.
40. Glycopeptide 18 was prepared as described previously (ref 13).
41. O-Linked glycopeptide precursors to 20 and 21 were synthesized using a cassette approach, in which the Fmoc serine monomers used in SPPS contained pendant saccharides.
42. Kemp, D. S. In The Peptides: Analysis, Synthesis, Biology; Gross, E., Meienhofer, J., Eds.; Academic Press: New York, 1979; Vol. 1, Part A, pp 315-381.
43. Shaltiel, S.; Fridkin, M. Biochemistry 1970, 9, 5122-5127.
44. Wang, Z. G.; Zhang, X. F.; Live, D.; Danishefsky, S. J. Angew. Chem., Int. Ed. 2000, 39, 3652-3656.