Structural basis of CXCR4 sulfotyrosine recognition by the chemokine SDF-1/CXCL12

Science Signaling

Volumn 1, Issue 37, 2008, Pages

  Veldkamp, Christopher T ^a   Seibert, Christoph ^b   Peterson, Francis C ^a   De La Cruz, Norberto B ^a   Haugner III, John C ^a   Basnet, Harihar ^a   Sakmar, Thomas P ^b   Volkman, Brian F ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CHEMOKINE RECEPTOR CXCR4; DRUG DERIVATIVE; STROMAL CELL DERIVED FACTOR 1; TYROSINE; TYROSINE O-SULFATE; TYROSINE SULFATE;

AMINO ACID SEQUENCE; ARTICLE; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; DIMERIZATION; HUMAN; METABOLISM; MOLECULAR GENETICS; NEUTROPHIL CHEMOTAXIS; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION;

AMINO ACID SEQUENCE; CALCIUM; CELL LINE; CHEMOKINE CXCL12; CHEMOTAXIS, LEUKOCYTE; DIMERIZATION; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; RECEPTORS, CXCR4; TYROSINE;

EID: 54849434087     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.1160755     Document Type: Article

References (57)

1. T. Nagasawa, S. Hirota, K. Tachibana, N. Takakura, S. Nishikawa, Y. Kitamura, N. Yoshida, H. Kikutani, T. Kishimoto, Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382, 635-638 (1996).
2. K. Tachibana, S. Hirota, H. Iizasa, H. Yoshida, K. Kawabata, Y. Kataoka, Y. Kitamura, K. Matsushima, N. Yoshida, S. Nishikawa, T. Kishimoto, T. Nagasawa, The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393, 591-594 (1998).
3. Y. R. Zou, A. H. Kottmann, M. Kuroda, I. Taniuchi, D. R. Littman, Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393, 595-599 (1998).
4. C. C. Bleul, M. Farzan, H. Choe, C. Parolin, I. Clark-Lewis, J. Sodroski, T. A. Springer, The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382, 829-833 (1996).
5. Y. Feng, C. C. Broder, P. E. Kennedy, E. A. Berger, HIV-1 entry cofactor: Functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272, 872-877 (1996).
6. M. P. D'Souza, V. A. Harden, Chemokines and HIV-1 second receptors. Confluence of two fields generates optimism in AIDS research. Nat. Med. 2, 1293- 1300 (1996).
7. M. P. D'Souza, J. S. Cairns, S. F. Plaeger, Current evidence and future directions for targeting HIV entry: Therapeutic and prophylactic strategies. JAMA 284, 215-222 (2000).
8. A. Muller, B. Homey, H. Soto, N. Ge, D. Catron, M. E. Buchanan, T. McClanahan, E. Murphy, W. Yuan, S. N. Wagner, J. L. Barrera, A. Mohar, E. Verastegui, A. Zlotnik, Involvement of chemokine receptors in breast cancer metastasis. Nature 410, 50-56 (2001).
9. A. Zlotnik, Chemokines and cancer. Int. J. Cancer 119, 2026-2029 (2006).
10. R. B. Gayle 3rd, P. R. Sleath, S. Srinivason, C. W. Birks, K. S. Weerawarna, D. P. Cerretti, C. J. Kozlosky, N. Nelson, T. Vanden Bos, M. P. Beckmann, Importance of the amino terminus of the interleukin-8 receptor in ligand interactions. J. Biol. Chem. 268, 7283-7289 (1993).
11. L. S. Mizoue, J. F. Bazan, E. C. Johnson, T. M. Handel, Solution structure and dynamics of the CX3C chemokine domain of fractalkine and its interaction with an N-terminal fragment of CX3CR1. Biochemistry 38, 1402-1414 (1999).
12. B. J. Doranz, M. J. Orsini, J. D. Turner, T. L. Hoffman, J. F. Berson, J. A. Hoxie, S. C. Peiper, L. F. Brass, R. W. Doms, Identification of CXCR4 domains that support coreceptor and chemokine receptor functions. J. Virol. 73, 2752-2761 (1999).
13. C. T. Veldkamp, C. Seibert, F. C. Peterson, T. P. Sakmar, B. F. Volkman, Recognition of a CXCR4 sulfotyrosine by the chemokine stromal cell- derived factor-1alpha (SDF-1alpha/CXCL12). J. Mol. Biol. 359, 1400-1409 (2006).
14. M. Farzan, G. J. Babcock, N. Vasilieva, P. L. Wright, E. Kiprilov, T. Mirzabekov, H. Choe, 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. 277, 29484-29489 (2002).
15. M. Farzan, T. Mirzabekov, P. Kolchinsky, R. Wyatt, M. Cayabyab, N.P. Gerard, C. Gerard, J. Sodroski, H. Choe, Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 96, 667 -676 (1999).
16. M. Farzan, S. Chung, W. Li, N. Vasilieva, P. L. Wright, C. E. Schnitzler, R. J. Marchione, C. Gerard, N. P. Gerard, J. Sodroski, H. Choe, Tyrosine-sulfated peptides functionally reconstitute a CCR5 variant lacking a critical amino-terminal region. J. Biol. Chem. 277, 40397-40402 (2002).
17. C. Seibert, M. Cadene, A. Sanfiz, B. T. Chait, T. P. Sakmar, 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. 99, 11031- 11036 (2002).
18. A. M. Fong, S. M. Alam, T. Imai, B. Haribabu, D. D. Patel, CX3CR1 tyrosine sulfation enhances fractalkine-induced cell adhesion. J. Biol. Chem. 277, 19418- 19423 (2002).
19. E. K. Gozansky, J. M. Louis, M. Caffrey, G. M. Clore, Mapping the binding of the N-terminal extracellular tail of the CXCR4 receptor to stromal cell-derived factor-1alpha. J. Mol. Biol. 345, 651-658 (2005).
20. G. J. Babcock, M. Farzan, J. Sodroski, Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor. J. Biol. Chem. 278, 3378-3385 (2003).
21. Y. Ohnishi, T. Senda, N. Nandhagopal, K. Sugimoto, T. Shioda, Y. Nagal, Y. Mitsui, Crystal structure of recombinant native SDF-1alpha with additional mutagenesis studies: An attempt at a more comprehensive interpretation of accumulated structure-activity relationship data. J. Interferon. Cytokine Res. 20, 691-700 (2000).
22. C. T. Veldkamp, F. C. Peterson, A. J. Pelzek, B. F. Volkman, The monomer-dimer equilibrium of stromal cell-derived factor-1 (CXCL 12) is altered by pH, phosphate, sulfate, and heparin. Protein Sci. 14, 1071-1081 (2005).
23. O. K. Baryshnikova, B. D. Sykes, Backbone dynamics of SDF-1alpha determined by NMR: Interpretation in the presence of monomer- dimer equilibrium. Protein Sci. 15, 2568-2578 (2006).
24. J. Vijayalakshmi, K. P. Padmanabhan, K. G. Mann, A. Tulinsky, The isomorphous structures of prethrombin2, hirugen-, and PPACK-thrombin: Changes accompanying activation and exosite binding to thrombin. Protein Sci. 3, 2254- 2271 (1994).
25. W. S. Somers, J. Tang, G. D. Shaw, R. T. Camphausen, Insights into the molecular basis of leukocyte tethering and rolling revealed by structures of P- and E-selectin bound to SLe(X) and PSGL-1. Cell 103, 467-479 (2000).
26. M. P. Crump, J. H. Gong, P. Loetscher, K. Rajarathnam, A. Amara, F. Arenzana-Seisdedos, J. L. Virelizier, M. Baggiolini, B. D. Sykes, I. Clark-Lewis, 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. 16, 6996-7007 (1997).
27. N. Heveker, M. Montes, L. Germeroth, A. Amara, A. Trautmann, M. Alizon, J. Schneider-Mergener, Dissociation of the signalling and antiviral properties of SDF-1- derived small peptides. Curr. Biol. 8, 369 -376 (1998).
28. F. C. Peterson, J. A. Thorpe, A. G. Harder, B. F. Volkman, S. R. Schwarze, Structural determinants involved in the regulation of CXCL14/BRAK expression by the 26 S proteasome. J. Mol. Biol. 363, 813-822 (2006).
29. 2+ signaling by fluorometric imaging plate reader (FLIPR) and flow cytometry. Cytometry 51A, 35-45 (2003).
30. G. A. Donzella, D. Schols, S. W. Lin, J. A. Este, K. A. Nagashima, P. J. Maddon, G. P. Allaway, T. P. Sakmar, G. Henson, E. De Clercq, J. P. Moore, AMD3100, a small molecule inhibitor of HIV-1 entry via the CXCR4 co-receptor. Nat. Med. 4, 72-77 (1998).
31. C. Seibert, T. P. Sakmar, Toward a framework for sulfoproteomics: Synthesis and characterization of sulfotyrosine-containing peptides. Biopolymers 90, 459-477 (2008).
32. J. Liu, S. Louie, W. Hsu, K. M. Yu, H. B. Nicholas Jr., G. L. Rosenquist, Tyrosine sulfation is prevalent in human chemokine receptors important in lung disease. Am. J. Respir. Cell Mol. Biol. 38, 738-743 (2008).
33. G. Williams, N. Borkakoti, G. A. Bottomley, I. Cowan, A. G. Fallowfield, P. S. Jones, S. J. Kirtland, G. J. Price, L. Price, Mutagenesis studies of interleukin-8. Identification of a second epitope involved in receptor binding. J. Biol. Chem. 271, 9579-9586 (1996).
34. S. R. Leong, H. B. Lowman, J. Liu, S. Shire, L. E. Deforge, B. L. Gillece-Castro, R. McDowell, C. A. Hebert, IL-8 single-chain homodimers and heterodimers: Interactions with chemokine receptors CXCR1, CXCR2, and DARC. Protein Sci. 6, 609-617 (1997).
35. H. Fernando, C. Chin, J. Rosgen, K. Rajarathnam, Dimer dissociation is essential for interleukin-8 (IL-8) binding to CXCR1 receptor. J. Biol. Chem. 279, 36175-36178 (2004).
36. K. Rajarathnam, G. N. Prado, H. Fernando, I. Clark-Lewis, J. Navarro, Probing receptor binding activity of interleukin-8 dimer using a disulfide trap. Biochemistry 45, 7882-7888 (2006).
37. W. Schnitzel, U. Monschein, J. Besemer, Monomer-dimer equilibria of interleukin-8 and neutrophil-activating peptide 2. Evidence for IL-8 binding as a dimer and oligomer to IL-8 receptor B. J. Leukoc. Biol. 55, 763-770 (1994).
38. H. Jin, X. Shen, B. R. Baggett, X. Kong, P. J. Liwang, The human CC chemokine MIP-1beta dimer is not competent to bind to the CCR5 receptor. J. Biol. Chem. 282, 27976-27983 (2007).
39. A. E. Proudfoot, T. M. Handel, Z. Johnson, E. K. Lau, P. LiWang, I. Clark-Lewis, F. Borlat, T. N. Wells, M. H. Kosco-Vilbois, Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc. Natl. Acad. Sci. U.S.A. 100, 1885-1890 (2003).
40. G. S. Campanella, J. Grimm, L. A. Manice, R. A. Colvin, B. D. Medoff, G. R. Wojtkiewicz, R. Weissleder, A. D. Luster, Oligomerization of CXCL10 is necessary for endothelial cell presentation and in vivo activity. J. Immunol. 177, 6991-6998 (2006).
41. M. Baggiolini, B. Dewald, B. Moser, Human chemokines: An update. Annu. Rev. Immunol. 15, 675- 705 (1997).
42. G. M. Clore, A. M. Gronenborn, Three-dimensional structures of alpha and beta chemokines. FASEB J. 9, 57-62 (1995).
43. J. W. Murphy, Y. Cho, A. Sachpatzidis, C. Fan, M. E. Hodsdon, E. Lolis, Structural and functional basis of CXCL12 (stromal cell-derived factor-1 alpha) binding to heparin. J. Biol. Chem. 282, 10018-10027 (2007).
44. G. Milligan, N. J. Smith, Allosteric modulation of heterodimeric G-protein-coupled receptors. Trends Pharmacol. Sci. 28, 615-620 (2007).
45. L. El-Asmar, J. Y. Springael, S. Ballet, E. U. Andrieu, G. Vassart, M. Parmentier, Evidence for negative binding cooperativity within CCR5-CCR2b heterodimers. Mol. Pharmacol. 67, 460-469 (2005).
46. J. Y. Springael, E. Urizar, M. Parmentier, Dimerization of chemokine receptors and its functional consequences. Cytokine Growth Factor Rev. 16, 611-623 (2005).
47. M. Bouvier, N. Heveker, R. Jockers, S. Marullo, G. Milligan, BRET analysis of GPCR oligomerization: Newer does not mean better. Nat. Methods 4, 3-4; author reply 4 (2007).
48. J. R. James, M. I. Oliveira, A. M. Carmo, A. Iaboni, S. J. Davis, A rigorous experimental framework for detecting protein oligomerization using bioluminescence resonance energy transfer. Nat. Methods 3, 1001-1006 (2006).
49. M. Chabre, M. le Maire, Monomeric G-protein-coupled receptor as a functional unit. Biochemistry 44, 9395-9403 (2005).
50. P. Loetscher, J. H. Gong, B. Dewald, M. Baggiolini, I. Clark-Lewis, N-terminal peptides of stromal cell-derived factor-1 with CXC chemokine receptor 4 agonist and antagonist activities. J. Biol. Chem. 273, 22279-22283 (1998).
51. D. M. Rosenbaum, V. Cherezov, M. A. Hanson, S. G. Rasmussen, F. S. Thian, T. S. Kobilka, H. J. Choi, X. J. Yao, W. I. Weis, R. C. Stevens, B. K. Kobilka, GPCR engineering yields high-resolution structural insights into beta2-adrenergic receptor function. Science 318, 1266-1273 (2007).
52. V. Cherezov, D. M. Rosenbaum, M. A. Hanson, S. G. Rasmussen, F. S. Thian, T. S. Kobilka, H. J. Choi, P. Kuhn, W. I. Weis, B. K. Kobilka, R. C. Stevens, High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 318, 1258-1265 (2007).
53. J. L. Markley, E. L. Ulrich, W. M. Westler, B. F. Volkman, Macromolecular structure determination by NMR spectroscopy. Methods Biochem. Anal. 44, 89-113 (2003).
54. G. Cornilescu, F. Delaglio, A. Bax, Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302 (1999).
55. T. Herrmann, P. Guntert, K. Wuthrich, Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol. 319, 209-227 (2002).
56. J. P. Linge, M. A. Williams, C. A. Spronk, A. M. Bonvin, M. Nilges, Refinement of protein structures in explicit solvent. Proteins 50, 496-506 (2003).
57. C. T. Veldkamp, F. C. Peterson, P. L. Hayes, J. E. Mattmiller, J. C. Haugner 3rd, N. de la Cruz, B. F. Volkman, On-column refolding of recombinant chemokines for NMR studies and biological assays. Protein Expr. Purif. 52, 202-209 (2007).