The N-terminal Region of CXCL11 as Structural Template for CXCR3 Molecular Recognition: Synthesis, Conformational Analysis, and Binding Studies

Chemical Biology and Drug Design

Volumn 80, Issue 2, 2012, Pages 254-265

  Palladino, Pasquale ^a   Portella, Luigi ^a   Colonna, Giovanni ^b   Raucci, Raffaele ^a   Saviano, Gabriella ^c   Rossi, Filomena ^d   Napolitano, Maria ^a   Scala, Stefania ^a   Castello, Giuseppe ^a   Costantini, Susan ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

^c UNIVERSITY OF MOLISE   (Italy)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Antagonists; Cancer; CXC chemokines; CXCR3; Inflammation; Molecular docking; Molecular dynamics; Molecular recognition; NMR

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; CHEMOKINE RECEPTOR CXCR4; CXCL11 CHEMOKINE;

AMINO TERMINAL SEQUENCE; ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; IN VIVO STUDY; MOLECULAR DOCKING; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL LINE, TUMOR; CHEMOKINE CXCL11; DRUG DESIGN; HUMANS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES; PROTEIN CONFORMATION; RECEPTORS, CXCR3; SEQUENCE ALIGNMENT;

EID: 84864019145     PISSN: 17470277     EISSN: 17470285     Source Type: Journal    
DOI: 10.1111/j.1747-0285.2012.01397.x     Document Type: Article

References (56)

1. Booth V., Keizer D.W., Kamphuis M.B., Clark-Lewis I., Sykes B.D. (2002) The CXCR3 binding chemokine IP-10/CXCL10: structure and receptor interactions. Biochemistry;41:10418-10425.
2. Booth V., Clark-Lewis I., Sykes B.D. (2004) NMR structure of CXCR3 binding chemokine CXCL11 (ITAC). Protein Sci;13:2022-2028.
3. Cole K.E., Strick C.A., Paradis T.J., Ogborne K.T., Loetscher M., Gladue R.P., Lin W., Boyd J.G., Moser B., Wood D.E., Sahagan B.G., Neote K. (1998) Interferon inducible T cell α chemoattractant (I-TAC): a novel ELR-CXC chemokine with potent activity on activated T cells through selective high affinity binding to CXCR3. J Exp Med;187:2009-2021.
4. Zeremski M., Petrovic L.M., Talal A.H. (2007) The role of chemokines as inflammatory mediators in chronic hepatitis C virus infection. J Viral Hepat;14:675-687.
5. Colvin R.A., Campanella G.S.V., Sun J., Luster A.D. (2004) Intracellular domain of CXCR3 that mediate CXCL9, CXCL10, and CXCL11 function. J Biol Chem;279:30219-30227.
6. Zeremski M., Petrovic L.M., Chiriboga L., Brown Q.B., Yee H.T., Kinklabwala M., Jacobson I.M., Dimova R., Markatou M., Talal A.H. (2008) Intrahepatic levels of CXCR3-associated chemokines correlate with liver inflammation and fibrosis in chronic hepatitis C. Hepatology;48:1440-1450.
7. Zemerski M., Dimova R., Brown Q., Jacobson I.M., Markatou M., Talal A.H. (2009) Peripheral CXCR3-associated chemokines as biomarkers of fibrosis in chronic hepatitis C virus infection. J Infect Dis;200:1774-1780.
8. O'Donovan N., Galvin M., Morgan J.G. (1999) Physical mapping of the CXC chemokine locus on human chromosome 4. Cytogenet Cell Genet;84:39-42.
9. Tensen C.P., Flier J., Van Der Raaij-Helmer E.M., Sampat-Sardjoepersad S., Van Der Schors R.C., Leurs R., Scheper R.J., Boorsma D.M., Willemze R. (1999) Human IP-9: a keratinocyte-derived high affinity CXC-chemokine ligand for the IP-10/Mig receptor (CXCR3). J Invest Dermatol;112:716-722.
10. Laich A., Meyer M., Werner E.R., Werner-Felmayer G. (1999) Structure and expression of the human small cytokine B subfamily member 11 (SCYB11/formerly SCYB9B, alias I-TAC) gene cloned from IFN-γ-treatedhumanmonocytes (THP-1). J Interferon Cytokine Res;19:505-513.
11. Nishioka Y., Manabe K., Kishi J., Wang W., Inayama M., Azuma M., Sone S. (2007) CXCL9 and 11 in patients with pulmonary sarcoidosis: a role of alveolar macrophages. Clin Exp Immunol;149:317-326.
12. Rotondi M., Chiovato L., Romagnani S., Serio M., Romagnani P. (2007) Role of chemokines in endocrine autoimmune disease. Endocr Rev;28:492-520.
13. Costantini S., Capone F., Guerriero E., Maio P., Colonna G., Castello G. (2010) Serum cytokine levels as putative prognostic markers in the progression of chronic HCV hepatitis leading to cirrhosis. Eur Cytokine Netw;21:251-256.
14. Xanthou G., Williams T.J., Pease J.E. (2003) Molecular characterization of the chemokine receptor CXCR3: evidence for the involvement of distinct extracellular domains in a multi-step model of ligand binding and receptor activation. Eur J Immunol;33:2927-2936.
15. Liu J., Fu Z., Li A.R., Johnson M., Zhu L., Marcus A., Danao J., Sullivan T., Tonn G., Collins T., Medina J. (2009) Optimization of a series of quinazolinone-derived antagonists of CXCR3. Bioorg Med Chem Lett;19:5114-5118.
16. Bastani S., Sherman W., Schnickel G.T., Hsieh G.R., Bhatia R., Fishbein M.C., Ardehali A. (2009) Chemokine receptor blockade with a synthetic nonpeptide compound attenuates cardiac allograft vasculopathy. Transplantation;88:995-1001.
17. Thoma G., Baenteli R., Lewis I., Wagner T., Oberer L., Blum W., Glickman F., Streiff M.B., Zerwes H.G. (2009) Special ergolines are highly selective, potent antagonists of the chemokine receptor CXCR3: discovery, characterization and preliminary SAR of a promising lead. Bioorg Med Chem Lett;19:6185-6188.
18. Proudfoot A.E. (2002) Chemokine receptors: multifaceted therapeutic targets. Nat Rev Immunol;2:106-115.
19. Trotta T., Costantini S., Colonna G. (2009) Modelling of the membrane receptor CXCR3 and its complexes with CXCL9, CXCL10 and CXCL11 chemokines: putative target for new drug design. Mol Immunol;47:332-339.
20. Chang W.C., White P.D. (2000) Fmoc Solid Phase Peptide Synthesis. New York: Oxford University Press.
21. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., Bax A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR;6:77-293.
22. Johnson A., Blevins R.A. (1994) NMRView. J Biomol NMR;4:603-614.
23. Wüthrich K. (1986) NMR of Proteins and Nucleic Acids. New York: Wiley.
24. Van Der Spoel D., Lindahl E., Hess B., Groenhof G., Mark A.E., Berendsen H.J. (2005) GROMACS: fast, flexible, and free. J Comput Chem;26:1701-1718.
25. Autiero I., Costantini S., Colonna G. (2009) Human sirt-1: molecular modeling and structure-function relationships of an unordered protein. PLoS ONE;4:e7350.
26. Paladino A., Costantini S., Colonna G., Facchiano A.M. (2008) Molecular modelling of miraculin: structural analyses and functional hypotheses. Biochem Biophys Res Commun;367:26-32.
27. Paladino A., Colonna G., Facchiano A.M., Costantini S. (2010) Functional hypothesis on Miraculin' sweetness by a molecular dynamics approach. Biochem Biophys Res Commun;396:726-730.
28. Wu B., Chien E.Y., Mol C.D., Fenalti G., Liu W., Katritch V., Abagyan R., Brooun A., Wells P., Bi F.C., Hamel D.J., Kuhn P., Handel T.M., Cherezov V., Stevens R.C. (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science;330:1066-1071.
29. Palczewski K., Kumasaka T., Hori T., Behnke C.A., Motoshima H., Fox B.A., Le Trong I., Teller D.C., Okada T., Stenkamp R.E., Yamamoto M., Miyano M. (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science;289:739-745.
30. Thompson J.D., Higgins D.G., Gibson T. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res;2: 4673-4680.
31. Sali A., Blundell T.L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol;234:779-815.
32. Sippl M.J. (1993) Recognition of errors in three-dimensional structures of proteins. Proteins;17:355-362.
33. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr;26:283-291.
34. Dalton J.A.R., Jackson R.M. (2007) An evaluation of automated homology modelling methods at low target-template sequence similarity. Bioinformatics;23:1901-1908.
35. Kabsch W., Sander C. (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers;2:2577-2637.
36. Schneidman-Duhovny D., Inbar Y., Nussinov R., Wolfson H.J. (2005) PatchDock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res;33:W363-W367.
37. Mashiach E., Nussinov R., Wolfson H.J. (2010) FiberDock: a web server for flexible induced-fit backbone refinement in molecular docking. Nucleic Acids Res;38:W457-W461.
38. Jones S., Thornton J.M. (1996) Principles of protein-protein interactions derived from structural studies. PNAS;93:13-20.
39. McDonald I.K., Thornton J.M. (1994) Satisfying hydrogen bonding potential in proteins. J Mol Biol;238:777-793.
40. Liu S., Zhang C., Zhou H., Zhou Y. (2004) A physical reference state unifies the structure-derived potential of mean force for protein folding and binding. Proteins;56:93-101.
41. Fricker S.P., Anastassov V., Cox J., Darkes M.C., Grujic O., Idzan S.R., Labrecque J., Lau G., Mosi R.M., Nelson K.L., Qin L., Santucci Z., Wong R.S. (2006) Characterization of the molecular pharmacology of AMD3100: a specific antagonist of the G-protein coupled chemokine receptor, CXCR4. Biochem Pharmacol;72:588-596.
42. Lehrer S.S., Fashman G.D. (1966) The fluorescence of lysozyme and lysozyme substrate complexes. Biochem Biophys Res Commun;2:133.
43. Chipman D.M., Grisaro V., Shanon N. (1967) The binding of oligosaccharides containing N-acetylglucosamine and N-acetylmuramic acid to lysozyme. The specificity of binding studies. J Biol Chem;242:4388-4394.
44. Prilusky J., Felder C.E., Zeev-Ben-Mordehai T., Rydberg E.H., Man O., Beckmann J.S., Silman I., Sussman J.L. (2005) FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics;21:3435-3438.
45. Linding R., Russell R.B., Neduva V., Gibson T.J. (2003) GlobPlot: exploring protein sequences for globularity and disorder. Nucleic Acids Res;31:3701-3708.
46. Dosztanyi Z., Csizmok V., Tompa P., Simon I. (2005) IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics;21:3433-3434.
47. Yang Z.R., Thomson R., McNeil P., Esnouf R.M. (2005) RONN: the bio-basis function neural network technique applied to the detection of natively unordered regions in proteins. Bioinformatics;1:3369-3376.
48. Woody R.W. (1978) Aromatic side-chain contributions to the far ultraviolet circular dichroism of peptides and proteins. Biopolymers;17:1451-1467.
49. Krittanai C., Johnson W.C. Jr. (1997) Correcting the circular dichroism spectra of peptides for contributions of absorbing side chains. Anal Biochem;253:57-64.
50. Kawada K., Hosogi H., Sonoshita M., Sakashita H., Manabe T., Shimahara Y., Sakai Y., Takabayashi A., Oshima M., Taketo M.M. (2007) Chemokine receptor CXCR3 promotes colon cancer metastasis to lymph nodes. Oncogene;26:4679-4688.
51. Smit M.J., Verdijk P., van der Raaij-Helmer E.M., Navis M., Hensbergen P.J., Leurs R., Tensen C.P. (2003) CXCR3-mediated chemotaxis of human T cells is regulated by a Gi -and phospholipase C-dependent pathway and not via activation of MEK/p44/p42 MAPK nor Akt/PI-3 kinase. Blood;102:1959-1965.
52. Collins T.L., Johnson M.G., Medina J.C. (2007) Antagonists of CXCR3: a review of current progress. In: Neote K., Letts G.L., Moser B., editors. Chemokine Biology - Basic Research and Clinical Application, Volume II. Basel/Switzerland: Birkhäuser Verlag; p. 79-88.
53. Watson R.J., Allen D.R., Birch H.L., Chapman G.A., Galvin F.C., Jopling L.A., Knight R.L., Meier D., Oliver K., Meissner J.W., Owen D.A., Thomas E.J., Tremayne N., Williams S.C. (2008) Development of CXCR3 antagonists part 3: tropenyl and homotropenyl-piperidine urea derivatives. Bioorg Med Chem Lett;18:147-151.
54. Horuk R. (2009) Chemokine receptor antagonists: overcoming developmental hurdles. Nat Rev Drug Discovery;8:23-33.
55. Walser T.C., Rifat S., Ma X., Kundu N., Ward C., Goloubeva O., Johnson M.G., Medina J.C., Collins T.L., Fulton A.M. (2006) Antagonism of CXCR3 inhibits lung metastasis in a murine model of metastatic breast cancer. Cancer Res;66:7701-7707.
56. Jenh C.-H., Cox M.A., Cui L., Reich E.-P., Sullivan L., Chen S.-C., Kinsley D., Qian S., Kim S.H., Rosenblum S., Kozlowski J., Fine J.S., Zavodny P.J., Lundell D. (2012) A selective and potent CXCR3 antagonist SCH 546738 attenuates the development of autoimmune diseases and delays graft rejection. BMC Immunol;13:2.