Current status and future prospects for research on tyrosine sulfation

Current Pharmaceutical Biotechnology

Volumn 13, Issue 14, 2012, Pages 2632-2641

  Sasaki, Nobuya ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

TPST; Tyrosine O sulfation; Tyrosine sulfation; Tyrosylprotein sulfotransferase

Indexed keywords

ADENOSINE 3' PHOSPHATE 5' PHOSPHOSULFATE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CXCR4; GLYCOPROTEIN; GLYCOPROTEIN GP 120; P SELECTION GLYCOPROTEIN LIGAND; RECOMBINANT ERYTHROPOIETIN; SULFOTYROSINE; TYROSINE; UNCLASSIFIED DRUG;

COMPUTER PREDICTION; FLUORESCENCE MICROSCOPY; GOLGI COMPLEX; HEMOSTASIS; HOMEOSTASIS; HUMAN; ISOTOPE LABELING; LEUKOCYTE ADHERENCE; MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; PROTEIN ENGINEERING; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVIEW; SULFATION; TYROSINE SULFATION;

EID: 84872547816     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920101314151120122922     Document Type: Review

References (91)

1. Huttner, W.B. Sulphation of tyrosine residues-a widespread modification of proteins. Nature, 1982, 299, 273-276.
2. Huttner, W.B. Tyrosine sulfation and the secretory pathway. Annu. Rev. Physiol., 1988, 50, 363-376.
3. Ouyang, Y.; Lane, W.S.; Moore, K.L. Tyrosylprotein sulfotransferase: purification and molecular cloning of an enzyme that catalyzes tyrosine O-sulfation, a common posttranslational modification of eukaryotic proteins. Proc. Natl. Acad. Sci. USA, 1998, 95, 2896-2901.
4. Ouyang, Y.B.; Moore, K.L. Molecular cloning and expression of human and mouse tyrosylprotein sulfotransferase-2 and a tyrosylprotein sulfotransferase homologue in Caenorhabditis elegans. J. Biol. Chem., 1998, 273, 24770-24774.
5. Beisswanger, R.; Corbeil, D.; Vannier, C.; Thiele, C.; Dohrmann, U.; Kellner, R.; Ashman, K.; Niehrs, C.; Huttner, W.B. Existence of distinct tyrosylprotein sulfotransferase genes: molecular characterization of tyrosylprotein sulfotransferase-2. Proc. Natl. Acad. Sci. USA, 1998, 95, 11134-11139.
6. Niehrs, C.; Kraft, M.; Lee, R.W.; Huttner, W.B. Analysis of the substrate specificity of tyrosylprotein sulfotransferase using synthetic peptides. J. Biol. Chem., 1990, 265, 8525-8532.
7. Yu, Y.; Hoffhines, A.J.; Moore, K.L.; Leary, J.A. (2007) Determination of the sites of tyrosine O-sulfation in peptides and proteins. Nat. Methods, 4, 583-588.
8. 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. USA, 2002, 99, 11031-11036.
9. Sasaki, N.; Hosoda, Y.; Nagata, A.; Ding, M.; Cheng, J.M.; Miyamoto, T.; Okano, S.; Asano, A.; Miyoshi, I.; Agui, T. A mutation in Tpst2 encoding tyrosylprotein sulfotransferase causes dwarfism associated with hypothyroidism. Mol. Endocrinol., 2007, 21, 1713-1721.
10. Hosoda, Y.; Sasaki, N.; Agui, T. Female infertility in grt mice is caused by thyroid hormone deficiency, not by insufficient TPST2 activity in the reproductive organs. J. Vet. Med. Sci., 2008, 70, 1043-1049.
11. Ouyang, Y.B.; Crawley, J.T.; Aston, C.E.; Moore, K.L. Reduced body weight and increased postimplantation fetal death in tyrosylprotein sulfotransferase-1-deficient mice. J. Biol. Chem., 2002, 277, 23781-23787.
12. Borghei, A.; Ouyang, Y.B.; Westmuckett, A.D.; Marcello, M.R.; Landel, C.P.; Evans, J.P.; Moore, K.L. Targeted disruption of tyrosylprotein sulfotransferase-2, an enzyme that catalyzes posttranslational protein tyrosine O-sulfation, causes male infertility. J. Biol. Chem., 2006, 281, 9423-9431.
13. Westmuckett, A.D.; Hoffhines, A.J.; Borghei, A.; Moore, K.L. Early postnatal pulmonary failure and primary hypothyroidism in mice with combined TPST-1 and TPST-2 deficiency. Gen. Comp. Endocrinol., 2008, 156, 145-153.
14. The Universal Protein Resource (UniProt). http://www.uniprot.org/uniprot/ (Accessed May 3, 2010)
15. Moore, K.L. The biology and enzymology of protein tyrosine Osulfation. J. Biol. Chem., 2003, 278, 24243-24246.
16. The International HapMap Project. Nature, 2003, 426, 789-796.
17. Seibert, C.; Sakmar, T.P. Toward a framework for sulfoproteomics: Synthesis and characterization of sulfotyrosine-containing peptides. Biopolymers, 2008, 90, 459-477.
18. Mishiro, E.; Sakakibara, Y.; Liu, M.C.; Suiko, M. Differential enzymatic characteristics and tissue-specific expression of human TPST-1 and TPST-2. J. Biochem., 2006, 140, 731-737.
19. Liu, C.C.; Schultz, P.G. Recombinant expression of selectively sulfated proteins in Escherichia coli. Nat. Biotechnol., 2006, 24, 1436-1440.
20. Liu, C.C.; Cellitti, S.E.; Geierstanger, B.H.; Schultz, P.G. Efficient expression of tyrosine-sulfated proteins in E. coli using an expanded genetic code. Nat. Protoc., 2009, 4, 1784-1789.
21. Hortin, G.; Folz, R.; Gordon, J.I.; Strauss, A.W. Characterization of sites of tyrosine sulfation in proteins and criteria for predicting their occurrence. Biochem. Biophys. Res. Commun., 1986, 141, 326-333.
22. Lin, W.H.; Larsen, K.; Hortin, G.L.; Roth, J.A. Recognition of substrates by tyrosylprotein sulfotransferase. Determination of affinity by acidic amino acids near the target sites. J. Biol. Chem., 1992, 267, 2876-2879.
23. Niehrs, C.; Huttner, W.B. Purification and characterization of tyrosylprotein sulfotransferase. EMBO J., 1990, 9, 35-42.
24. Monigatti, F.; Gasteiger, E.; Bairoch, A.; Jung, E. The Sulfinator: predicting tyrosine sulfation sites in protein sequences. Bioinformatics, 2002, 18, 769-770.
25. Swiss Institute of Bioinformatics. The Sulfinator predicts tyrosine sulfation sites in protein sequences. http://ca.expasy.org/tools/sulfinator/ (Accessed May 3, 2010).
26. Yang, Z.R. Predicting sulfotyrosine sites using the random forest algorithm with significantly improved prediction accuracy. BMC Bioinformatics, 2009, 10, 361. Exeter computational systems biology at University of Exeter. Sulfotyrosine Residue predictor. http://ecsb.ex.ac.uk/sulfotyrosine/ (Accessed May 3, 2010)
27. Chang, W.C.; Lee, T.Y.; Shien, D.M.; Hsu, J.B.; Horng, J.T.; Hsu, P.C.; Wang, T.Y.; Huang, H.D.; Pan, R.L. Incorporating support vector machine for identifying protein tyrosine sulfation sites. J. Comput. Chem., 2009, 30, 2526-2537.
28. Institute of Bioinformatics, National Chiao Tung University. http://sulfosite.mbc.nctu.edu.tw/ (Accessed May 3, 2010)
29. Huttner, W.B. Determination and occurrence of tyrosine O-sulfate in proteins. Methods Enzymol., 1984, 107, 200-223.
30. Costagliola, S.; Panneels, V.; Bonomi, M.; Koch, J.; Many, M.C.; Smits, G.; Vassart, G. Tyrosine sulfation is required for agonist recognition by glycoprotein hormone receptors. EMBO J., 2002, 21, 504-513.
31. Hoffhines, A.J.; Damoc, E.; Bridges, K.G.; Leary, J.A.; Moore, K.L. Detection and purification of tyrosine-sulfated proteins using a novel anti-sulfotyrosine monoclonal antibody. J. Biol. Chem., 2006, 281, 37877-37887.
32. Kehoe, J.W.; Velappan, N.; Walbolt, M.; Rasmussen, J.; King, D.; Lou, J.; Knopp, K.; Pavlik, P.; Marks, J.D.; Bertozzi, C.R.; Bradbury, A.R.M. Using phage display to select antibodies recognizing post-translational modifications independently of sequence context. Mol. Cell Proteomics, 2006, 5, 2350-2363.
33. Wolfender, J.L.; Chu, F.; Ball, H.; Wolfender, F.; Fainzilber, M.; Baldwin, M.A.; Burlingame, A.L. Identification of tyrosine sulfation in Conus pennaceus conotoxins a-PnIA and a-PnIB:further investigation of labile sulfo-and phosphopeptides by electrospray, matrix-assisted laser desorption/Ionization (MALDI) and atmospheric pressure MALDI mass spectrometry. J. Mass Spectrom, 1999, 34, 447-454.
34. Talbo, G.; Roepstorff, P. Determination of sulfated peptides via prompt fragmentation by UV matrix-assisted laser desorption/ionization mass spectrometry. Rapid Commun. Mass Spectrom, 2005, 7, 201-204.
35. Monigatti, F.; Hekking, B.; Steen, H. Protein sulfation analysis-A primer. Biochim. Biophys. Acta., 2006, 1764, 1904-1913.
36. Stone, S.R.; Betz, A.; Parry, M.A.; Jackman, M.P.; Hofsteenge, J. Molecular basis for the inhibition of thrombin by hirudin. Adv. Exp. Med. Biol., 1993, 340, 35-49.
37. Hortin, G.L. Sulfation of tyrosine residues in coagulation factor V. Blood, 1990, 76, 946-952.
38. Leyte, A.; van Schijndel, H.B.; Niehrs, C.; Huttner, W.B.; Verbeet, M.P.; Mertens, K.; van Mourik, J.A. Sulfation of Tyr1680 of human blood coagulation factor VIII is essential for the interaction of factor VIII with von Willebrand factor. J. Biol. Chem., 1991, 266, 740-746.
39. Bond, M.; Jankowski, M.; Patel, H.; Karnik, S.; Strang, A.; Xu, B.; Rouse, J.; Koza, S.; Letwin, B.; Steckert, J. Amphlett, G. Scoble, H. Biochemical characterization of recombinant factor IX. Semin. Hematol., 1998, 35, 11-17.
40. Morita, T.; Jackson, C.M. Preparation and properties of derivatives of bovine factor X and factor Xa from which the gammacarboxyglutamic acid containing domain has been removed. J. Biol. Chem., 1986, 261, 4015-4023.
41. Farrell, D.H.; Mulvihill, E.R.; Huang, S.M.; Chung, D.W.; Davie, E.W. Recombinant human fibrinogen and sulfation of the gamma' chain. Biochemistry, 1991, 30, 9414-9420.
42. Dong, J.F.; Li, C.Q.; Lopez, J.A. Tyrosine sulfation of the glycoprotein Ib-IX complex: identification of sulfated residues and effect on ligand binding. Biochemistry, 1994, 33, 13946-13953.
43. Pouyani, T.; Seed, B. PSGL-1 recognition of P-selectin is controlled by a tyrosine sulfation consensus at the PSGL-1 amino terminus. Cell, 1995, 83, 333-343.
44. Rossi, B.; Constantin, G. Anti-selectin therapy for the treatment of inflammatory diseases. Inflamm. Allergy Drug Targets, 2008, 7, 85-93.
45. Mayadas, T.N.; Johnson, R.C.; Rayburn, H.; Hynes, R.O.; Wagner, D.D. Leukocyte rolling and extravasation are severely compromised in P selectin-deficient mice. Cell, 1993, 74, 541-554.
46. Xia, L.; Sperandio, M.; Yago, T.; McDaniel, J.M.; Cummings, R.D.; Pearson-White, S.; Ley, K.; McEver, R.P. P-selectin glycoprotein ligand-1-deficient mice have impaired leukocyte tethering to E-selectin under flow. J. Clin. Invest., 2002, 109, 939-950.
47. Wilkins, P.P.; Moore, K.L.; McEver, R.P.; Cummings, R.D. Tyrosine sulfation of P-selectin glycoprotein ligand-1 is required for high affinity binding to P-selectin. J. Biol. Chem., 1995, 270, 22677-22680.
48. Murdoch, C.; Finn, A. Chemokine receptors and their role in inflammation and infectious diseases. Blood, 2000, 95, 3032-3043.
49. 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.
50. Farzan, M.; Vasilieva, N.; Schnitzler, C.E.; Chung, S.; Robinson, J.; Gerard, N.P.; Gerard, C.; Choe, H.; Sodroski, J. A tyrosinesulfated peptide based on the N terminus of CCR5 interacts with a CD4-enhanced epitope of the HIV-1 gp120 envelope glycoprotein and inhibits HIV-1 entry. J. Biol. Chem., 2000, 275, 33516-33521.
51. Bannert, N.; Craig, S.; Farzan, M.; Sogah, D.; Santo, N.V.; Choe, H.; Sodroski, J. Sialylated O-glycans and sulfated tyrosines in the NH2-terminal domain of CC chemokine receptor 5 contribute to high affinity binding of chemokines. J. Exp. Med., 2001, 194, 1661-1673.
52. Choe, H.; Farzan, M.; Sun, Y.; Sullivan, N.; Rollins, B.; Ponath, P.D.; Wu, L.; Mackay, C.R.; LaRosa, G.; Newman, W.; Gerard, N.; Gerard, C.; Sodroski, J.; The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell, 1996, 85, 1135-1148.
53. Choe, H.; Li, W.; Wright, P.L.; Vasilieva, N.; Venturi, M.; Huang, C.C.; Grundner, C.; Dorfman, T.; Zwick, M.B.; Wang, L.; Rosenberg, E.S.; Kwong, P.D.; Burton, D.R.; Robinson, J.E.; Sodroski, J.G.; Farzan, M. Tyrosine sulfation of human antibodies contributes to recognition of the CCR5 binding region of HIV-1 gp120. Cell, 2003, 114, 161-170.
54. Huang, C.C.; Venturi, M.; Majeed, S.; Moore, M.J.; Phogat, S.; Zhang, M.Y.; Dimitrov, D.S.; Hendrickson, W.A.; Robinson, J.; Sodroski, Wyatt, R.; Choe, H.; Farzan, M.; Kwong, P. D. Structural basis of tyrosine sulfation and VH-gene usage in antibodies that recognize the HIV type 1 coreceptor-binding site on gp120. Proc. Natl. Acad. Sci. U S A, 2004, 101, 2706-2711.
55. Farzan, M.; Babcock, G.J.; Vasilieva, N.; Wright, P.L.; Kiprilov, E.; Mirzabekov, T.; Choe, H. The role of post-translational modifications of the CXCR4 amino terminus in stromal-derived factor 1 alpha association and HIV-1 entry. J. Biol. Chem., 2002, 277, 29484-29489.
56. Dorfman, T.; Moore, M.J.; Guth, A.C.; Choe, H.; Farzan, M. A tyrosine-sulfated peptide derived from the heavy-chain CDR3 region of an HIV-1-neutralizing antibody binds gp120 and inhibits HIV-1 infection. J. Biol. Chem., 2006, 281, 28529-28535.
57. 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.
58. Preobrazhensky, A.A.; Dragan, S.; Kawano, T.; Gavrilin, M.A.; Gulina, I.V.; Chakravarty, L.; Kolattukudy, P.E. Monocyte chemotactic protein-1 receptor CCR2B is a glycoprotein that has tyrosine sulfation in a conserved extracellular N-terminal region. J. Immunol., 2000, 165, 5295-5303.
59. Fong, A.M.; Alam, S.M.; Imai, T.; Haribabu, B.; Patel, D.D. CX3CR1 tyrosine sulfation enhances fractalkine-induced cell adhesion. J. Biol. Chem., 2002, 277, 19418-19423.
60. Gutierrez, J.; Kremer, L.; Zaballos, A.; Goya, I.; Martinez, A.C.; Marquez, G. Analysis of post-translational CCR8 modifications and their influence on receptor activity. J. Biol. Chem., 2004, 279, 14726-14733.
61. Colvin, R.A.; Campanella, G.S.; Manice, L.A.; Luster, A.D. CXCR3 requires tyrosine sulfation for ligand binding and a second extracellular loop arginine residue for ligand-induced chemotaxis. Mol. Cell Biol., 2006, 26, 5838-5849.
62. Farzan, M.; Schnitzler, C.E.; Vasilieva, N.; Leung, D.; Kuhn, J.; Gerard, C.; Gerard, N.P.; Choe, H. Sulfated tyrosines contribute to the formation of the C5a docking site of the human C5a anaphylatoxin receptor. J. Exp. Med., 2001, 193, 1059-1066.
63. Gao, J.; Choe, H.; Bota, D.; Wright, P.L.; Gerard, C.; Gerard, N.P. Sulfation of tyrosine 174 in the human C3a receptor is essential for binding of C3a anaphylatoxin. J. Biol. Chem., 2003, 278, 37902-37908.
64. Kehoe, J.W.; Bertozzi, C.R. Tyrosine sulfation: a modulator of extracellular protein-protein interactions. Chem. Biol., 2000, 7, 57-61.
65. Rossi, D.; Zlotnik, A. The biology of chemokines and their receptors. Annu. Rev. Immunol., 2000, 18, 217-242.
66. Lazennec, G.; Richmond, A. Chemokines and chemokine receptors: new insights into cancer-related inflammation. Trends Mol. Med., 2010, 16(3), 133-144.
67. Zernecke, A.; Weber, C. Chemokines in the vascular inflammatory response of atherosclerosis. Cardiovasc. Res., 2010, 86(2), 192-201.
68. Westmuckett, A.D.; Moore, K.L. Lack of tyrosylprotein sulfotransferase activity in hematopoietic cells drastically attenuates atherosclerosis in Ldlr-/-mice. Arterioscler. Thromb. Vasc. Biol., 2009, 29, 1730-1736.
69. Caltabiano, G.; Campillo, M.; De Leener, A.; Smits, G.; Vassart, G.; Costagliola, S.; Pardo, L. The specificity of binding of glycoprotein hormones to their receptors. Cell Mol. Life Sci., 2008, 65, 2484-2492.
70. Bonomi, M.; Busnelli, M.; Persani, L.; Vassart, G.; Costagliola, S. Structural differences in the hinge region of the glycoprotein hormone receptors: evidence from the sulfated tyrosine residues. Mol. Endocrinol., 2006, 20, 3351-3363.
71. Hortin, G.; Sims, H.; Strauss, A.W. Identification of the site of sulfation of the fourth component of human complement. J. Biol. Chem., 1986, 261, 1786-1793.
72. Liu, M.C.; Yu, S.; Sy, J.; Redman, C.M.; Lipmann, F. Tyrosine sulfation of proteins from the human hepatoma cell line HepG2. Proc. Natl. Acad. Sci. USA, 1985, 82, 7160-7164.
73. Bundgaard, J.R.; Vuust, J.; Rehfeld, J.F. Tyrosine O-sulfation promotes proteolytic processing of progastrin. EMBO J., 1995, 14, 3073-3079.
74. Johnsen, A.H. Phylogeny of the cholecystokinin/gastrin family. Front Neuroendocrinol., 1998, 19, 73-99.
75. Sleeman, J.P.; Rahmsdorf, U.; Steffen, A.; Ponta, H.; Herrlich, P. CD44 variant exon v5 encodes a tyrosine that is sulphated. Eur. J. Biochem., 1998, 255, 74-80.
76. Fieger, C.B.; Sassetti, C.M.; Rosen, S.D. Endoglycan, a member of the CD34 family, functions as an L-selectin ligand through modification with tyrosine sulfation and sialyl Lewis x. J. Biol. Chem., 2003, 278, 27390-27398.
77. Jukkola, A.; Risteli, J.; Niemela, O.; Risteli, L. Incorporation of sulphate into type III procollagen by cultured human fibroblasts. Identification of tyrosine O-sulphate. Eur. J. Biochem., 1986, 154, 219-224.
78. Liu, M.C.; Lipmann, F. Isolation of tyrosine-O-sulfate by Pronase hydrolysis from fibronectin secreted by Fujinami sarcoma virusinfected rat fibroblasts. Proc. Natl. Acad. Sci. USA, 1985, 82, 34-37.
79. Cha, S.W.; Tadjuidje, E.; White, J.; Wells, J.; Mayhew, C.; Wylie, C.; Heasman, J. Wnt11/5a complex formation caused by tyrosine sulfation increases canonical signaling activity. Curr. Biol., 2009, 19, 1573-1580.
80. Johnson, M.L.; Rajamannan, N. Diseases of Wnt signaling. Rev. Endocr. Metab. Disord., 2006, 7, 41-49.
81. Baeuerle, P.A.; Lottspeich, F.; Huttner, W.B. Purification of yolk protein 2 of Drosophila melanogaster and identification of its site of tyrosine sulfation. J. Biol. Chem., 1988, 263, 14925-14929.
82. Friederich, E.; Fritz, H.J.; Huttner, W.B. Inhibition of tyrosine sulfation in the trans-Golgi retards the transport of a constitutively secreted protein to the cell surface. J. Cell Biol., 1988, 107, 1655-1667.
83. Jensen, S.L.; Rehfeld, J.F.; Holst, J.J.; Fahrenkrug, J.; Nielsen, O.V.; Schaffalitzky de Muckadell, O.B. Secretory effects of gastrins on isolated perfused porcine pancreas. Am. J. Physiol., 1980, 238, 186-192.
84. Andersen, B.N.; Stadil, F. Sulfation of gastrin in Zollinger-Ellison sera: evidence for association between sulfation and proteolytic processing. Regul. Pept., 1983, 6, 231-239.
85. Chapman, E.; Best, M.D.; Hanson, S.R.; Wong, C.H. Sulfotransferases: structure, mechanism, biological activity, inhibition, and synthetic utility. Angew. Chem. Int. Ed. Engl., 2004, 43, 3526-3548.
86. Rath, V.L.; Verdugo, D.; Hemmerich, S. Sulfotransferase structural biology and inhibitor discovery. Drug Discov. Today, 2004, 9, 1003-1011.
87. Kehoe, J.W.; Maly, D.J.; Verdugo, D.E.; Armstrong, J.I.; Cook, B.N.; Ouyang, Y.B.; Moore, K.L.; Ellman, J.A.; Bertozzi, C.R. Tyrosylprotein sulfotransferase inhibitors generated by combinatorial target-guided ligand assembly. Bioorg. Med. Chem. Lett., 2002, 12, 329-332.
88. Hahn, S.K.; Oh, E.J.; Miyamoto, H.; Shimobouji, T. Sustained release formulation of erythropoietin using hyaluronic acid hydrogels crosslinked by Michael addition. Int. J. Pharm., 2006, 322, 44-51.
89. Macdougall, I.C. An overview of the efficacy and safety of novel erythropoiesis stimulating protein (NESP). Nephrol. Dial. Transplant, 2001, 16, 14-21.
90. Keppler, A.; Gendreizig, S.; Gronemeyer, T.; Pick, H.; Vogel, H.; Johnsson, K. A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat. Biotechnol., 2003, 21, 86-89.
91. Maurel, D.; Comps-Agrar, L.; Brock, C.; Rives, M.L.; Bourrier, E.; Ayoub, M.A.; Bazin, H.; Tinel, N.; Durroux, T.; Prezeau, L.; Trinquet, E.; Pin, J. P. Cell surface protein protein interaction analysis with time-resolved FRET and snap-tag technologies: application to GPCR oligomerization. Nat. Methods, 2008, 5, 561-567.