Homogeneous Sulfopeptides and Sulfoproteins: Synthetic Approaches and Applications To Characterize the Effects of Tyrosine Sulfation on Biochemical Function

Accounts of Chemical Research

Volumn 48, Issue 8, 2015, Pages 2251-2261

  Stone, Martin J ^a   Payne, Richard J ^b  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR3; CHEMOKINE RECEPTOR CCR5; HIRUDIN DERIVATIVE; PEPTIDE; SULFATE; TYROSINE; TYROSINE O-SULFATE;

AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; BINDING SITE; CHEMISTRY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOLOGY; PHYSIOLOGY; PROTEIN PROCESSING; SOLID PHASE SYNTHESIS; SYNTHESIS;

AMINO ACID SEQUENCE; BINDING SITES; HIRUDINS; HIV INFECTIONS; HIV-1; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, CCR3; RECEPTORS, CCR5; SOLID-PHASE SYNTHESIS TECHNIQUES; SULFATES; TYROSINE;

EID: 84939526530     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/acs.accounts.5b00255     Document Type: Article

References (59)

1. Walsh, C. T.; Garneau-Tsodikova, S.; Gatto, G. J., Jr. Protein Posttranslational Modifications: The Chemistry of Proteome Diversifications Angew. Chem., Int. Ed. 2005, 44, 7342-7372 10.1002/anie.200501023
2. Stone, M. J.; Chuang, S.; Hou, X.; Shoham, M.; Zhu, J. Z. Tyrosine Sulfation: an Increasingly Recognised Post-Translational Modification of Secreted Proteins New Biotechnol. 2009, 25, 299-317 10.1016/j.nbt.2009.03.011
3. Moore, K. L. The Biology and Enzymology of Protein Tyrosine O-Sulfation J. Biol. Chem. 2003, 278 (27) 24243-24246 10.1074/jbc.R300008200
4. Kice, J. L.; Anderson, J. M. The Mechanism of the Acid Hydrolysis of Sodium Aryl Sulfates J. Am. Chem. Soc. 1966, 88, 5242-5245 10.1021/ja00974a038
5. Vázquez-Campos, S., St; Hilaire, P. M.; Damgaard, D.; Meldal, M. GAG Mimetic Libraries: Sulphated Peptide as Heparin-Like Glycosaminoglycan Mimics in their Interaction with FGF-1 QSAR Comb. Sci. 2005, 24, 923-942 10.1002/qsar.200420100
6. De Luca, S.; Morelli, G. Synthesis and Characterization of a Sulfated and a Non-Sulfated Cyclic CCK8 Analogue Functionalized with a Chelating Group for Metal Labelling J. Pept. Sci. 2004, 10, 265-273 10.1002/psc.527
7. Futaki, S.; Taike, T.; Akita, T.; Kitagawa, K. Syntheses of Two Tyrosine-Sulphate Containing Peptides. Leucosulfakinin (LSK)-II and Cholecystokinin (CCK)-12, Using the O-p-(Methylsulphinyl)benzyl Serine for the Selective Sulphation of Tyrosine Tetrahedron 1992, 48, 8899-8914 10.1016/S0040-4020(01)81989-X
8. Futaki, S.; Taike, T.; Yagami, T.; Ogawa, T.; Akita, T.; Kitagawa, K. Use of Dimethylformamide-Sulphur Trioxide Complex as a Sulphating Agent of Tyrosine J. Chem. Soc., Perkin Trans. 1 1990, 1739-1744 10.1039/p19900001739
9. Kitagawai, K.; Futaki, S.; Yagami, T.; Sumi, S.; Inoue, K. Solid-Phase Synthesis of Cionin, a Protochordate-Derived Octapeptide Related to the Gastrin/Cholecystokinin Family of Peptides, and its Mono-Tyrosine-Sulfate-Containing Derivatives Int. J. Pept. Protein Res. 1994, 43, 190-200 10.1111/j.1399-3011.1994.tb00522.x
10. Young, T.; Kiessling, L. L. A Strategy for the Synthesis of Sulfated Peptides Angew. Chem., Int. Ed. 2002, 41, 3449-3451 10.1002/1521-3773(20020916)41:18<3449::AID-ANIE3449>3.0.CO;2-U
11. Campos, S. V.; Miranda, L. P.; Meldal, M. Preparation of Novel O-Sulfated Amino Acid Building Blocks with Improved Acid Stability for Fmoc-Based Solid-Phase Peptide Synthesis J. Chem. Soc., Perkin Trans. 1 2002, 682-686 10.1039/b107320f
12. Kitagawa, K.; Aida, C.; Fujiwara, H.; Yagami, T.; Futaki, S. Efficient Solid-Phase Synthesis of Sulfated Tyrosine-Containing Peptides using 2-Chlorotrityl Resin: Facile Synthesis of Gastrin/Cholecystokinin Peptides Tetrahedron Lett. 1997, 38, 599-602 10.1016/S0040-4039(96)02401-X
13. Kitagawa, K.; Aida, C.; Fujiwara, H.; Yagami, T.; Futaki, S.; Kogire, M.; Ida, J.; Inoue, K. Facile Solid-Phase Synthesis of Sulfated Tyrosine-Containing Peptides: Total Synthesis of Human Big Gastrin-II and Cholecystokinin (CCK)-39 J. Org. Chem. 2001, 66, 1-10 10.1021/jo000895y
14. Yagami, T.; Shiwa, S.; Futaki, S.; Kitagawa, K. Evaluation of the Final Deprotection System for the Solid-Phase Synthesis of Tyr(SO3H)-Containing Peptides with 9-Fluorenylmethyloxycarbonyl (Fmoc)-Strategy and its Application to the Synthesis of Cholecystokinin (CCK)-12 Chem. Pharm. Bull. 1993, 41, 376-380 10.1248/cpb.41.376
15. Ueki, M.; Watanabe, S.; Ishii, Y.; Okunaka, O.; Uchino, K.; Saitoh, T.; Higashi, K.; Nakashima, H.; Yamamoto, N.; Ogawara, H. Synthesis and Anti-HIV Activity of Nonatyrosine N- and O1-9-Decasulfate Bioorg. Med. Chem. 2001, 9, 477-486 10.1016/S0968-0896(00)00269-8
16. Balsved, D.; Bundgaard, J. R.; Sen, J. W. Stability of Tyrosine Sulfate in Acidic Solutions Anal. Biochem. 2007, 363, 70-76 10.1016/j.ab.2006.12.003
17. Huttner, W. B. Determination and Occurrence of Tyrosine O-Sulfate in Proteins. In Posttranslation Modifications; Wold, F.; Moldave, K., Eds.; Methods in Enzymology; Academic Press: Orlando, FL, 1984; Vol. 107; pp 200-223.
18. Simpson, L. S.; Widlanski, T. S. A Comprehensive Approach to the Synthesis of Sulfate Esters J. Am. Chem. Soc. 2006, 128, 1605-1610 10.1021/ja056086j
19. Simpson, L. S.; Zhu, J. Z.; Widlanski, T. S.; Stone, M. J. Regulation of Chemokine Recognition by Site-Specific Tyrosine Sulfation of Receptor Peptides Chem. Biol. 2009, 16, 153-161 10.1016/j.chembiol.2008.12.007
20. Desoky, A. Y.; Hendel, J.; Ingram, L.; Taylor, S. D. Preparation of Trifluoroethyl- and Phenyl-Protected Sulfates using Sulfuryl Imidazolium Salts Tetrahedron 2011, 67, 1281-1287 10.1016/j.tet.2010.11.085
21. Taleski, D.; Butler, S. J.; Stone, M. J.; Payne, R. J. Divergent and Site-Selective Solid-Phase Synthesis of Sulfopeptides Chem.-Asian J. 2011, 6, 1316-1320 10.1002/asia.201100232
22. Ali, A. M.; Hill, B.; Taylor, S. D. Trichloroethyl Group as a Protecting Group for Sulfonates and its Application to the Synthesis of a Disulfonate Analog of the Tyrosine Sulfated PSGL-1(43-50) Peptide J. Org. Chem. 2009, 74, 3583-3586 10.1021/jo900122c
23. Taylor, S. D.; Desoky, A. Rapid and Efficient Chemoselective and Multiple Sulfations of Phenols using Sulfuryl Imidazolium Salts Tetrahedron Lett. 2011, 52, 3353-3357 10.1016/j.tetlet.2011.04.080
24. Ali, A. M.; Taylor, S. D. Efficient Solid-Phase Synthesis of Sulfotyrosine Peptides using a Sulfate Protecting-Group Strategy Angew. Chem., Int. Ed. 2009, 48, 2024-2026 10.1002/anie.200805642
25. Ali, A. M.; Taylor, S. D. Synthesis of Disulfated Peptides Corresponding to the N-Terminus of Chemokines Receptors CXCR6 (CXCR6(1-20)) and DARC (DARC(8-42)) Using a Sulfate-Protecting Group Strategy J. Pept. Sci. 2010, 16, 190-199 10.1002/psc.1220
26. Zhu, J. Z.; Millard, C. J.; Ludeman, J. P.; Simpson, L. S.; Clayton, D. J.; Payne, R. J.; Widlanski, T. S.; Stone, M. J. Tyrosine Sulfation Influences the Chemokine Binding Selectivity of Peptides Derived from Chemokine Receptor CCR3 Biochemistry 2011, 50, 1524-1534 10.1021/bi101240v
27. Ziarek, J. J.; Getschman, A. E.; Butler, S. J.; Taleski, D.; Stephens, B.; Kufareva, I.; Handel, T. M.; Payne, R. J.; Volkman, B. F. Sulfopeptide Probes of the CXCR4/CXCL12 Interface Reveal Oligomer-Specific Contacts and Chemokine Allostery ACS Chem. Biol. 2013, 8, 1955-1963 10.1021/cb400274z
28. Duncan, R. C.; Mohlin, F.; Taleski, D.; Coetzer, T. H.; Huntington, J. A.; Payne, R. J.; Blom, A. M.; Pike, R. N.; Wijeyewickrema, L. C. Identification of a Catalytic Exosite for Complement Component C4 on the Serine Protease Domain of C1s J. Immunol. 2012, 189, 2365-2373 10.4049/jimmunol.1201085
29. Hsieh, Y. S. Y.; Taleski, D.; Wilkinson, B. L.; Wijeyewickrema, L. C.; Adams, T. E.; Pike, R. N.; Payne, R. J. Effect of O-Glycosylation and Tyrosine Sulfation of Leech-Derived Peptides on Binding and Inhibitory Activity Against Thrombin Chem. Commun. 2012, 48, 1547-1549 10.1039/C1CC14773K
30. Roche, M.; Salimi, H.; Duncan, R.; Wilkinson, B. L.; Chikere, K.; Moore, M. S.; Webb, N. E.; Zappi, H.; Sterjovski, J.; Flynn, J. K.; Ellett, A.; Gray, L. R.; Lee, B.; Jubb, B.; Westby, M.; Ramsland, P. A.; Lewin, S. R.; Payne, R. J.; Churchill, M. J.; Gorry, P. R. A Common Mechanism of Clinical HIV-1 Resistance to the CCR5 Antagonist Maraviroc Despite Divergent Resistance Levels and Lack of Common gp120 Resistance Mutations Retrovirology 2013, 10, 43 10.1186/1742-4690-10-43
31. Bunschoten, A.; Kruijtzer, J. A. W.; Ippel, J. H.; de Haas, C. J. C.; van Strijp, J. A. G.; Kemmink, J.; Liskamp, R. M. J. A General Sequence Independent Solid Phase Method for the Site Specific Synthesis of Multiple Sulfated-Tyrosine Containing Peptides Chem. Commun. 2009, 21, 2999-3001 10.1039/b823425f
32. Green, T. W.; Wuts, P. G. M. Protective Groups in Organic Synthesis, 3 rd ed.; John Wiley & Sons, Inc.: Hoboken, NJ, 2002.
33. Berger, E. A.; Murphy, P. M.; Farber, J. M. Chemokine Receptors as HIV-1 Coreceptors: Roles in Viral Entry, Tropism, and Disease Annu. Rev. Immunol. 1999, 17, 657-700 10.1146/annurev.immunol.17.1.657
34. Moore, J. P.; Kitchen, S. G.; Pugach, P.; Zack, J. A. The CCR5 and CXCR4 Coreceptors-Central to Understanding the Transmission and Pathogenesis of Human Immunodeficiency Virus Type 1 Infection AIDS Res. Hum. Retroviruses 2004, 20, 111-126 10.1089/088922204322749567
35. Liu, X. Y.; Malins, L. R.; Roche, M.; Sterjovski, J.; Duncan, R.; Garcia, M. L.; Barnes, N. C.; Anderson, D. A.; Stone, M. J.; Gorry, P. R.; Payne, R. J. Site-Selective Solid-Phase Synthesis of a CCR5 Sulfopeptide Library To Interrogate HIV Binding and Entry ACS Chem. Biol. 2014, 9, 2074-2081 10.1021/cb500337r
36. Moser, B.; Wolf, M.; Walz, A.; Loetscher, P. Chemokines: Multiple Levels of Leukocyte Migration Control Trends Immunol. 2004, 25, 75-84 10.1016/j.it.2003.12.005
37. Muller, A.; Homey, B.; Soto, H.; Ge, N. F.; Catron, D.; Buchanan, M. E.; McClanahan, T.; Murphy, E.; Yuan, W.; Wagner, S. N.; Barrera, J. L.; Mohar, A.; Verastegui, E.; Zlotnik, A. Involvement of Chemokine Receptors in Breast Cancer Metastasis Nature 2001, 410, 50-56 10.1038/35065016
38. Farzan, M.; Mirzabekov, T.; Kolchinsky, P.; Wyatt, R.; Cayabyab, M.; Gerard, N. P.; Gerard, C.; Sodroski, J.; Choe, H. Tyrosine Sulfation of the Amino Terminus of CCR5 Facilitates HIV-1 Entry Cell 1999, 96, 667-676 10.1016/S0092-8674(00)80577-2
39. Choe, H.; Moore, M. J.; Owens, C. M.; Wright, P. L.; Vasilieva, N.; Li, W.; Singh, A. P.; Shakri, R.; Chitnis, C. E.; Farzan, M. Sulphated Tyrosines Mediate Association of Chemokines and Plasmodium vivax Duffy Binding Protein with the Duffy Antigen/Receptor for Chemokines (DARC) Mol. Microbiol. 2005, 55, 1413-1422 10.1111/j.1365-2958.2004.04478.x
40. Crump, M. P.; Gong, J. H.; Loetscher, P.; Rajarathnam, K.; Amara, A.; Arenzana-Seisdedos, F.; Virelizier, J. L.; Baggiolini, M.; Sykes, B. D.; Clark-Lewis, I. Solution Structure and Basis for Functional Activity of Stromal Cell-Derived Factor-1; Dissociation of CXCR4 Activation from Binding and Inhibition of HIV-1 EMBO J. 1997, 16, 6996-7007 10.1093/emboj/16.23.6996
41. Tan, J. H. Y.; Ludeman, J. P.; Wedderburn, J.; Canals, M.; Hall, P.; Butler, S. J.; Taleski, D.; Christopoulos, A.; Hickey, M. J.; Payne, R. J.; Stone, M. J. Tyrosine Sulfation of Chemokine Receptor CCR2 Enhances Interactions with both Monomeric and Dimeric Forms of the Chemokine Monocyte Chemoattractant Protein-1 (MCP-1) J. Biol. Chem. 2013, 288, 10024-10034 10.1074/jbc.M112.447359
42. Duma, L.; Haussinger, D.; Rogowski, M.; Lusso, P.; Grzesiek, S. Recognition of RANTES by Extracellular Parts of the CCR5 Receptor J. Mol. Biol. 2007, 365, 1063-1075 10.1016/j.jmb.2006.10.040
43. Veldkamp, C. T.; Seibert, C.; Peterson, F. C.; Sakmar, T. P.; Volkman, B. F. Recognition of a CXCR4 Sulfotyrosine by the Chemokine Stromal Cell-Derived Factor-1α (SDF-1α/CXCL12) J. Mol. Biol. 2006, 359, 1400-1409 10.1016/j.jmb.2006.04.052
44. Veldkamp, C. T.; Seibert, C.; Peterson, F. C.; De la Cruz, N. B.; Haugner, J. C., 3rd; Basnet, H.; Sakmar, T. P.; Volkman, B. F. Structural Basis of CXCR4 Sulfotyrosine Recognition by the Chemokine SDF-1/CXCL12 Sci. Signaling 2008, 1, ra4 10.1126/scisignal.1160755
45. Schnur, E.; Kessler, N.; Zherdev, Y.; Noah, E.; Scherf, T.; Ding, F. X.; Rabinovich, S.; Arshava, B.; Kurbatska, V.; Leonciks, A.; Tsimanis, A.; Rosen, O.; Naider, F.; Anglister, J. NMR Mapping of RANTES Surfaces Interacting with CCR5 Using Linked Extracellular Domains FEBS J. 2013, 280, 2068-2084 10.1111/febs.12230
46. Millard, C. J.; Ludeman, J. P.; Canals, M.; Bridgford, J. L.; Hinds, M. G.; Clayton, D. J.; Christopoulos, A.; Payne, R. J.; Stone, M. J. Structural Basis of Receptor Sulfotyrosine Recognition by a CC Chemokine: The N-Terminal Region of CCR3 Bound to CCL11/Eotaxin-1 Structure 2014, 22, 1571-1581 10.1016/j.str.2014.08.023
47. Proudfoot, A. E.; Handel, T. M.; Johnson, Z.; Lau, E. K.; LiWang, P.; Clark-Lewis, I.; Borlat, F.; Wells, T. N.; Kosco-Vilbois, M. H. Glycosaminoglycan Binding and Oligomerization are Essential for the In Vivo Activity of Certain Chemokines Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 1885-1890 10.1073/pnas.0334864100
48. Nasser, M. W.; Raghuwanshi, S. K.; Grant, D. J.; Jala, V. R.; Rajarathnam, K.; Richardson, R. M. Differential Activation and Regulation of CXCR1 and CXCR2 by CXCL8 Monomer and Dimer J. Immunol. 2009, 183, 3425-3432 10.4049/jimmunol.0900305
49. Tan, J. H.; Canals, M.; Ludeman, J. P.; Wedderburn, J.; Boston, C.; Butler, S. J.; Carrick, A. M.; Parody, T. R.; Taleski, D.; Christopoulos, A.; Payne, R. J.; Stone, M. J. Design and Receptor Interactions of Obligate Dimeric Mutant of Chemokine Monocyte Chemoattractant Protein-1 (MCP-1) J. Biol. Chem. 2012, 287, 14692-14702 10.1074/jbc.M111.334201
50. Huma, Z. E.; Ludeman, J. P.; Wilkinson, B. L.; Payne, R. J.; Stone, M. J. NMR Characterization of Cooperativity: Fast Ligand Binding Coupled to Slow Protein Dimerization Chem. Sci. 2014, 5, 2783-2788 10.1039/c4sc00131a
51. Ludeman, J. P.; Nazari-Robati, M.; Wilkinson, B. L.; Huang, C.; Payne, R. J.; Stone, M. J. Phosphate Modulates Receptor Sulfotyrosine Recognition by the Chemokine Monocyte Chemoattractant Protein-1 (MCP-1/CCL2) Org. Biomol. Chem. 2015, 13, 2162-2169 10.1039/C4OB02262A
52. Seibert, C.; Cadene, M.; Sanfiz, A.; Chait, B. T.; Sakmar, T. P. Tyrosine Sulfation of CCR5 N-Terminal Peptide by Tyrosylprotein Sulfotransferases 1 and 2 Follows a Discrete Pattern and Temporal Sequence Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 11031-11036 10.1073/pnas.172380899
53. Hsieh, Y. S.; Wijeyewickrema, L. C.; Wilkinson, B. L.; Pike, R. N.; Payne, R. J. Total Synthesis of Homogeneous Variants of Hirudin P6: A Post-Translationally Modified Anti-Thrombotic Leech-Derived Protein Angew. Chem., Int. Ed. 2014, 53, 3947-3951 10.1002/anie.201310777
54. Thompson, R. E.; Liu, X.; Alonso-García, N.; Pereira, P. J.; Jolliffe, K. A.; Payne, R. J. Trifluoroethanethiol: an Additive for Efficient One-Pot Peptide Ligation-Desulfurization Chemistry J. Am. Chem. Soc. 2014, 136, 8161-8164 10.1021/ja502806r
55. Greinacher, A.; Lubenow, N. Recombinant Hirudin in Clinical Practice-Focus on Lepirudin Circulation 2001, 103, 1479-1484 10.1161/01.CIR.103.10.1479
56. Corral-Rodríguez, M. A.; Macedo-Ribeiro, S.; Barbosa Pereira, P. J.; Fuentes-Prior, P. Leech-Derived Thrombin Inhibitors: From Structures to Mechanisms to Clinical Applications J. Med. Chem. 2010, 53, 3847-3861 10.1021/jm901743x
57. Steiner, V.; Knecht, R.; Bornsen, K. O.; Gassmann, E.; Stone, S. R.; Raschdorf, F.; Schlaeppi, J. M.; Maschler, R. Primary Structure and Function of Novel O-Glycosylated Hirudins from the Leech Hirudinaria manillensis Biochemistry 1992, 31, 2294-2298 10.1021/bi00123a012
58. Rydel, T. J.; Ravichandran, K. G.; Tulinsky, A.; Bode, W.; Huber, R.; Roitsch, C.; Fenton, J. W., 2nd The Structure of a Complex of Recombinant Hirudin and Human Alpha-Thrombin Science 1990, 249, 277-280 10.1126/science.2374926
59. Liu, C. C.; Brustad, E.; Liu, W.; Schultz, P. G. Crystal Structure of a Biosynthetic Sulfo-Hirudin Complexed to Thrombin J. Am. Chem. Soc. 2007, 129, 10648-10649 10.1021/ja0735002