Structural Insights into Neutrophilic Migration Revealed by the Crystal Structure of the Chemokine Receptor CXCR2 in Complex with the First PDZ Domain of NHERF1

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Lu, Guorong ^a   Wu, Yanning ^a   Jiang, Yuanyuan ^a   Wang, Shuo ^a   Hou, Yuning ^a   Guan, Xiaoqing ^a   Brunzelle, Joseph ^b   Sirinupong, Nualpun ^c   Sheng, Shijie ^a   Li, Chunying ^a   Yang, Zhe ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ARGONNE NATIONAL LABORATORY   (United States)

^c PRINCE OF SONGKLA UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR2; SCAFFOLD PROTEIN; SODIUM PROTON EXCHANGER REGULATORY FACTOR 1; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; HUMAN; HUMAN CELL; LIGAND BINDING; NEUTROPHIL CHEMOTAXIS; PDZ DOMAIN; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; STRUCTURE ANALYSIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BINDING SITES; DRUG DESIGN; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEUTROPHILS; PDZ DOMAINS; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, INTERLEUKIN-8B; SEQUENCE ALIGNMENT; SODIUM-HYDROGEN ANTIPORTER;

EID: 84884851733     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076219     Document Type: Article

References (45)

1. Chapman RW, Phillips JE, Hipkin RW, Curran AK, Lundell D, et al. (2009) CXCR2 antagonists for the treatment of pulmonary disease. Pharmacol Ther 121: 55-68. doi:10.1016/j.pharmthera.2008.10.005. PubMed: 19026683.
2. Tsai HH, Frost E, To V, Robinson S, Ffrench-Constant C, et al. (2002) The chemokine receptor CXCR2 controls positioning of oligodendrocyte precursors in developing spinal cord by arresting their migration. Cell 110: 373-383. doi:10.1016/S0092-8674(02)00838-3. PubMed: 12176324.
3. Vandercappellen J, Van Damme J, Struyf S, (2008) The role of CXC chemokines and their receptors in cancer. Cancer Lett 267: 226-244. doi:10.1016/j.canlet.2008.04.050. PubMed: 18579287.
4. Jamieson T, Clarke M, Steele CW, Samuel MS, Neumann J, et al. (2012) Inhibition of CXCR2 profoundly suppresses inflammation-driven and spontaneous tumorigenesis. J Clin Invest 122: 3127-3144. doi:10.1172/JCI61067. PubMed: 22922255.
5. Addison CL, Daniel TO, Burdick MD, Liu H, Ehlert JE, et al. (2000) The CXC chemokine receptor 2, CXCR2, is the putative receptor for ELR+ CXC chemokine-induced angiogenic activity. J Immunol 165: 5269-5277. PubMed: 11046061.
6. Wu Y, Wang S, Farooq SM, Castelvetere MP, Hou Y, et al. (2012) A chemokine receptor CXCR2 macromolecular complex regulates neutrophil functions in inflammatory diseases. J Biol Chem 287: 5744-5755. doi:10.1074/jbc.M111.315762. PubMed: 22203670.
7. Geng JG, (2001) Directional migration of leukocytes: their pathological roles in inflammation and strategies for development of anti-inflammatory therapies. Cell Res 11: 85-88. doi:10.1038/sj.cr.7290071. PubMed: 11453550.
8. Harris BZ, Lim WA, (2001) Mechanism and role of PDZ domains in signaling complex assembly. J Cell Sci 114: 3219-3231. PubMed: 11591811.
9. Tonikian R, Zhang Y, Sazinsky SL, Currell B, Yeh JH, et al. (2008) A specificity map for the PDZ domain family. PLOS Biol 6: e239. doi:10.1371/journal.pbio.0060239. PubMed: 18828675.
10. Sheng M, Sala C, (2001) PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci 24: 1-29. doi:10.1146/annurev.neuro.24.1.1. PubMed: 11283303.
11. Lee HJ, Zheng JJ, (2010) PDZ domains and their binding partners: structure, specificity, and modification. Cell Commun Signal 8: 8. doi:10.1186/1478-811X-8-8. PubMed: 20509869.
12. Karthikeyan S, Leung T, Ladias JA, (2001) Structural basis of the Na+/H+ exchanger regulatory factor PDZ1 interaction with the carboxyl-terminal region of the cystic fibrosis transmembrane conductance regulator. J Biol Chem 276: 19683-19686. doi:10.1074/jbc.C100154200. PubMed: 11304524.
13. Karthikeyan S, Leung T, Ladias JA, (2002) Structural determinants of the Na+/H+ exchanger regulatory factor interaction with the beta 2 adrenergic and platelet-derived growth factor receptors. J Biol Chem 277: 18973-18978. doi:10.1074/jbc.M201507200. PubMed: 11882663.
14. te Velthuis AJ, Sakalis PA, Fowler DA, Bagowski CP, (2011) Genome-wide analysis of PDZ domain binding reveals inherent functional overlap within the PDZ interaction network. PLOS ONE 6: e16047. doi:10.1371/journal.pone.0016047. PubMed: 21283644.
15. Münz M, Hein J, Biggin PC, (2012) The role of flexibility and conformational selection in the binding promiscuity of PDZ domains. PLOS Comput Biol 8: e1002749. PubMed: 23133356.
16. Cushing PR, Fellows A, Villone D, Boisguérin P, Madden DR, (2008) The relative binding affinities of PDZ partners for CFTR: a biochemical basis for efficient endocytic recycling. Biochemistry 47: 10084-10098. doi:10.1021/bi8003928. PubMed: 18754678.
17. Ardura JA, Friedman PA, (2011) Regulation of G protein-coupled receptor function by Na+/H+ exchange regulatory factors. Pharmacol Rev 63: 882-900. doi:10.1124/pr.110.004176. PubMed: 21873413.
18. Beuming T, Skrabanek L, Niv MY, Mukherjee P, Weinstein H, (2005) PDZBase: a protein-protein interaction database for PDZ-domains. Bioinformatics 21: 827-828. doi:10.1093/bioinformatics/bti098. PubMed: 15513994.
19. Zhang Y, Yeh S, Appleton BA, Held HA, Kausalya PJ, et al. (2006) Convergent and divergent ligand specificity among PDZ domains of the LAP and zonula occludens (ZO) families. J Biol Chem 281: 22299-22311. doi:10.1074/jbc.M602902200. PubMed: 16737968.
20. Elkins JM, Papagrigoriou E, Berridge G, Yang X, Phillips C, et al. (2007) Structure of PICK1 and other PDZ domains obtained with the help of self-binding C-terminal extensions. Protein Sci 16: 683-694. doi:10.1110/ps.062657507. PubMed: 17384233.
21. Sheng R, Chen Y, Yung Gee H, Stec E, Melowic HR, et al. (2012) Cholesterol modulates cell signaling and protein networking by specifically interacting with PDZ domain-containing scaffold proteins. Nat Commun 3: 1249. doi:10.1038/ncomms2221. PubMed: 23212378.
22. Bhattacharya S, Ju JH, Orlova N, Khajeh JA, Cowburn D, et al. (2013) Ligand-Induced Dynamic Changes in Extended PDZ Domains from NHERF1. J Mol Biol 425: 2509-2528. doi:10.1016/j.jmb.2013.04.001. PubMed: 23583913.
23. Cardone RA, Greco MR, Capulli M, Weinman EJ, Busco G, et al. (2012) NHERF1 acts as a molecular switch to program metastatic behavior and organotropism via its PDZ domains. Mol Cell Biol 23: 2028-2040. doi:10.1091/mbc.E11-11-0911. PubMed: 22496422.
24. Mamonova T, Kurnikova M, Friedman PA, (2012) Structural basis for NHERF1 PDZ domain binding. Biochemistry 51: 3110-3120. doi:10.1021/bi201213w. PubMed: 22429102.
25. Stein A, Aloy P, (2008) Contextual specificity in peptide-mediated protein interactions. PLOS ONE 3: e2524. doi:10.1371/journal.pone.0002524. PubMed: 18596940.
26. Wang S, Raab RW, Schatz PJ, Guggino WB, Li M, (1998) Peptide binding consensus of the NHE-RF-PDZ1 domain matches the C-terminal sequence of cystic fibrosis transmembrane conductance regulator (CFTR). FEBS Lett 427: 103-108. doi:10.1016/S0014-5793(98)00402-5. PubMed: 9613608.
27. Molina JR, Agarwal NK, Morales FC, Hayashi Y, Aldape KD, et al. (2012) PTEN, NHERF1 and PHLPP form a tumor suppressor network that is disabled in glioblastoma. Oncogene 31: 1264-1274. doi:10.1038/onc.2011.324. PubMed: 21804599.
28. Voltz JW, Weinman EJ, Shenolikar S, (2001) Expanding the role of NHERF, a PDZ-domain containing protein adapter, to growth regulation. Oncogene 20: 6309-6314. doi:10.1038/sj.onc.1204774. PubMed: 11607833.
29. Runyon ST, Zhang Y, Appleton BA, Sazinsky SL, Wu P, et al. (2007) Structural and functional analysis of the PDZ domains of human HtrA1 and HtrA3. Protein Sci 16: 2454-2471. doi:10.1110/ps.073049407. PubMed: 17962403.
30. Morales FC, Takahashi Y, Momin S, Adams H, Chen X, et al. (2007) NHERF1/EBP50 head-to-tail intramolecular interaction masks association with PDZ domain ligands. Mol Cell Biol 27: 2527-2537. doi:10.1128/MCB.01372-06. PubMed: 17242191.
31. Wang B, Bisello A, Yang Y, Romero GG, Friedman PA, (2007) NHERF1 regulates parathyroid hormone receptor membrane retention without affecting recycling. J Biol Chem 282: 36214-36222. doi:10.1074/jbc.M707263200. PubMed: 17884816.
32. Raghuram V, Mak DO, Foskett JK, (2001) Regulation of cystic fibrosis transmembrane conductance regulator single-channel gating by bivalent PDZ-domain-mediated interaction. Proc Natl Acad Sci U S A 98: 1300-1305. doi:10.1073/pnas.98.3.1300. PubMed: 11158634.
33. Raghuram V, Hormuth H, Foskett JK, (2003) A kinase-regulated mechanism controls CFTR channel gating by disrupting bivalent PDZ domain interactions. Proc Natl Acad Sci U S A 100: 9620-9625. doi:10.1073/pnas.1633250100. PubMed: 12881487.
34. Voltz JW, Brush M, Sikes S, Steplock D, Weinman EJ, et al. (2007) Phosphorylation of PDZ1 domain attenuates NHERF-1 binding to cellular targets. J Biol Chem 282: 33879-33887. doi:10.1074/jbc.M703481200. PubMed: 17895247.
35. Takahashi Y, Morales FC, Kreimann EL, Georgescu MM, (2006) PTEN tumor suppressor associates with NHERF proteins to attenuate PDGF receptor signaling. EMBO J 25: 910-920. doi:10.1038/sj.emboj.7600979. PubMed: 16456542.
36. Glynn PC, Henney E, Hall IP, (2002) The selective CXCR2 antagonist SB272844 blocks interleukin-8 and growth-related oncogene-alpha-mediated inhibition of spontaneous neutrophil apoptosis. Pulm Pharmacol Ther 15: 103-110. doi:10.1006/pupt.2001.0323. PubMed: 12090783.
37. Weinman EJ, Minkoff C, Shenolikar S, (2000) Signal complex regulation of renal transport proteins: NHERF and regulation of NHE3 by PKA. Am J Physiol Renal Physiol 279: F393-F399. PubMed: 10966919.
38. Wang B, Yang Y, Abou-Samra AB, Friedman PA, (2009) NHERF1 regulates parathyroid hormone receptor desensitization: interference with beta-arrestin binding. Mol Pharmacol 75: 1189-1197. doi:10.1124/mol.108.054486. PubMed: 19188335.
39. Otwinowski Z, Minor W, (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode. Methods Enzymol 276: 307-326. doi:10.1016/S0076-6879(97)76066-X.
40. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674. doi:10.1107/S0021889807021206. PubMed: 19461840.
41. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132. doi:10.1107/S0907444904019158. PubMed: 15572765.
42. Blanc E, Roversi P, Vonrhein C, Flensburg C, Lea SM, et al. (2004) Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr D Biol Crystallogr 60: 2210-2221. doi:10.1107/S0907444904016427. PubMed: 15572774.
43. Terwilliger TC, Grosse-Kunstleve RW, Afonine PV, Moriarty NW, Adams PD, et al. (2008) Iterative-build OMIT maps: map improvement by iterative model building and refinement without model bias. Acta Crystallogr D Biol Crystallogr 64: 515-524. doi:10.1107/S0907444908004319. PubMed: 18453687.
44. Laskowski RA, MacArthur MW, Moss DS, Thornton JM, (1993) PROCHECK: A program to check the stereochemical quality of protein structures. J Appl Crystallogr 26: 283-291. doi:10.1107/S0021889892009944.
45. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948. doi:10.1093/bioinformatics/btm404. PubMed: 17846036.