Stable formyl peptide receptor agonists that activate the neutrophil NADPH-oxidase identified through screening of a compound library

Biochemical Pharmacology

Volumn 81, Issue 3, 2011, Pages 402-411

  Forsman, Huamei ^a   Kalderén, Christina ^b   Nordin, Anna ^a   Nordling, Erik ^b   Jensen, Annika Jernmalm ^a,b   Dahlgren, Claes ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b BIOVITRUM AB   (Sweden)

Author keywords

Chemoattractant receptors; Formyl peptide receptors; NADPH oxidase; Neutrophils; Receptor antagonists; Signal transduction

Indexed keywords

ANTIINFLAMMATORY AGENT; CALCIUM; CALCIUM ION; CYCLOSPORINE H; ENZYME ACTIVATOR; FORMYL PEPTIDE RECEPTOR 1; FORMYL PEPTIDE RECEPTOR 2; FORMYLMETHIONYLLEUCYLPHENYLALANINE; FORMYLPEPTIDE RECEPTOR; FORMYLPEPTIDE RECEPTOR LIKE 1; PBP 10; REACTIVE OXYGEN METABOLITE; RECEPTOR BLOCKING AGENT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; SYNTHETIC PEPTIDE; TYROSYLLYSYLTYROSYLMETHIONYLVALYLMETHIONINE; UNCLASSIFIED DRUG;

AGONIST; ARTICLE; CALCIUM CELL LEVEL; CELL GRANULE; CELL MOTILITY; CELL SECRETION; DRUG IDENTIFICATION; DRUG INACTIVATION; DRUG POTENCY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; MOLECULAR LIBRARY; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; PRIORITY JOURNAL;

ADULT; CALCIUM; CALCIUM SIGNALING; ENZYME ACTIVATION; ENZYME ACTIVATORS; HUMANS; NADPH OXIDASE; NEUTROPHILS; REACTIVE OXYGEN SPECIES; RECEPTORS, FORMYL PEPTIDE; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; SMALL MOLECULE LIBRARIES; SUPEROXIDES;

EID: 78650687885     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.11.005     Document Type: Article

References (50)

1. P.M. Murphy The molecular biology of leukocyte chemoattractant receptors Annu Rev Immunol 12 1994 593 633
2. A.F. Miller, and J.J. Falke Chemotaxis receptors and signaling Adv Protein Chem 68 2004 393 444
3. R.D. Ye, and F. Boulay Structure and function of leukocyte chemoattractant receptors Adv Pharmacol 39 1997 221 289
4. H. Fu, J. Karlsson, J. Bylund, C. Movitz, A. Karlsson, and C. Dahlgren Ligand recognition and activation of formyl peptide receptors in neutrophils J Leukoc Biol 79 2 2006 247 256
5. R.D. Ye, F. Boulay, J.M. Wang, C. Dahlgren, C. Gerard, and M. Parmentier International union of basic and clinical pharmacology. LXXIII. Nomenclature for the formyl peptide receptor (FPR) family Pharmacol Rev 61 2 2009 119 161
6. M.A. Arruda, and C. Barja-Fidalgo NADPH oxidase activity: In the crossroad of neutrophil life and death Front Biosci 14 2009 4546 4556
7. W.M. Nauseef How human neutrophils kill and degrade microbes: an integrated view Immunol Rev 219 2007 88 102
8. R.P. Hayhoe, A.M. Kamal, E. Solito, R.J. Flower, D. Cooper, and M. Perretti Annexin 1 and its bioactive peptide inhibit neutrophil-endothelium interactions under flow: indication of distinct receptor involvement Blood 107 5 2006 2123 2130
9. G.R. Martin, M. Perretti, R.J. Flower, and J.L. Wallace Annexin-1 modulates repair of gastric mucosal injury Am J Physiol Gastrointest Liver Physiol 294 3 2008 G764 G769
10. I. Hecht, J. Rong, A.L. Sampaio, C. Hermesh, C. Rutledge, and R. Shemesh A novel peptide agonist of formyl-peptide receptor-like 1 (ALX) displays anti-inflammatory and cardioprotective effects J Pharmacol Exp Ther 328 2 2009 426 434
11. C.N. Serhan, S. Yacoubian, and R. Yang Anti-inflammatory and proresolving lipid mediators Annu Rev Pathol 3 2008 279 312
12. T. Christophe, A. Karlsson, M.J. Rabiet, F. Boulay, and C. Dahlgren Phagocyte activation by Trp-Lys-Tyr-Met-Val-Met, acting through FPRL1/LXA4R, is not affected by lipoxin A4 Scand J Immunol 56 5 2002 470 476
13. H. Forsman, and C. Dahlgren Lipoxin A(4) metabolites/analogues from two commercial sources have no effects on TNF-alpha-mediated priming or activation through the neutrophil formyl peptide receptors Scand J Immunol 70 4 2009 396 402
14. H. Forsman, E. Salomonsson, K. Onnheim, J. Karlsson, A. Bjorstad, and H. Leffler The beta-galactoside binding immunomodulatory lectin galectin-3 reverses the desensitized state induced in neutrophils by the chemotactic peptide f-Met-Leu-Phe: role of reactive oxygen species generated by the NADPH-oxidase and inactivation of the agonist Glycobiology 18 11 2008 905 912
15. C. Zhou, S. Zhang, M. Nanamori, Y. Zhang, Q. Liu, and N. Li Pharmacological characterization of a novel nonpeptide antagonist for formyl peptide receptor-like 1 Mol Pharmacol 72 4 2007 976 983 (Pubitemid 47481420)
16. I.A. Schepetkin, L.N. Kirpotina, A.I. Khlebnikov, and M.T. Quinn High-throughput screening for small-molecule activators of neutrophils: identification of novel N-formyl peptide receptor agonists Mol Pharmacol 71 4 2007 1061 1074
17. Y. Sogawa, A. Shimizugawa, T. Ohyama, H. Maeda, and K. Hirahara The pyrazolone originally reported to be a formyl peptide receptor (FPR) 2/ALX-selective agonist is instead an FPR1 and FPR2/ALX dual agonist J Pharmacol Sci 111 3 2009 317 321
18. Kirpotina LN, Khlebnikov AI, Schepetkin IA, Ye RD, Rabiet MJ, Jutila MA, et al. Identification of novel small-molecule agonists for human formyl peptide receptors and pharmacophore models of their recognition. Mol Pharmacol 2010;77(2):159-70.
19. R.W. Burli, H. Xu, X. Zou, K. Muller, J. Golden, and M. Frohn Potent hFPRL1 (ALXR) agonists as potential anti-inflammatory agents Bioorg Med Chem Lett 16 14 2006 3713 3718
20. S.L. Dixon, A.M. Smondyrev, E.H. Knoll, S.N. Rao, D.E. Shaw, and R.A. Friesner PHASE: a new engine for pharmacophore perception, 3D QSAR model development, and 3D database screening: 1. Methodology and preliminary results J Comput Aided Mol Des 20 10-11 2006 647 671
21. E. Abrahamian, P.C. Fox, L. Naerum, I.T. Christensen, H. Thogersen, and R.D. Clark Efficient generation, storage, and manipulation of fully flexible pharmacophore multiplets and their use in 3-D similarity searching J Chem Inf Comput Sci 43 2 2003 458 468
22. C.C. Cunningham, R. Vegners, R. Bucki, M. Funaki, N. Korde, and J.H. Hartwig Cell permeant polyphosphoinositide-binding peptides that block cell motility and actin assembly J Biol Chem 276 46 2001 43390 43399
23. A. Boyum, D. Lovhaug, L. Tresland, and E.M. Nordlie Separation of leucocytes: improved cell purity by fine adjustments of gradient medium density and osmolality Scand J Immunol 34 6 1991 697 712
24. H. Lundqvist, and C. Dahlgren Isoluminol-enhanced chemiluminescence: a sensitive method to study the release of superoxide anion from human neutrophils Free Radic Biol Med 20 6 1996 785 792
25. C. Dahlgren, A. Karlsson, and J. Bylund Measurement of respiratory burst products generated by professional phagocytes Methods Mol Biol 412 2007 349 363
26. C. Dahlgren, and A. Karlsson Respiratory burst in human neutrophils J Immunol Methods 232 1-2 1999 3 14
27. A. Betten, C. Dahlgren, U.H. Mellqvist, S. Hermodsson, and K. Hellstrand Oxygen radical-induced natural killer cell dysfunction: role of myeloperoxidase and regulation by serotonin J Leukoc Biol 75 6 2004 1111 1115
28. J. Karlsson, J. Bylund, C. Movitz, L. Bjorkman, H. Forsman, and C. Dahlgren A methodological approach to studies of desensitization of the formyl peptide receptor: role of the read out system, reactive oxygen species and the specific agonist used to trigger neutrophils J Immunol Methods 2009
29. J. Karlsson, H. Fu, F. Boulay, J. Bylund, and C. Dahlgren The peptide Trp-Lys-Tyr-Met-Val-D-Met activates neutrophils through the formyl peptide receptor only when signaling through the formylpeptide receptor like 1 is blocked. A receptor switch with implications for signal transduction studies with inhibitors and receptor antagonists Biochem Pharmacol 71 10 2006 1488 1496
30. K. Wenzel-Seifert, and R. Seifert Cyclosporin H is a potent and selective formyl peptide receptor antagonist. Comparison with N-t-butoxycarbonyl-L- phenylalanyl-L-leucyl-L-phenylalanyl-L-leucyl-L-phenylalanine and cyclosporins A, B, C, D, and E J Immunol 150 10 1993 4591 4599
31. A.L. Stenfeldt, J. Karlsson, C. Wenneras, J. Bylund, H. Fu, and C. Dahlgren Boc-MLF and Boc-FLFLF are antagonists that preferentially inhibit activity triggered through the formyl peptide receptor Inflammation 30 6 2007 224 229
32. H. Fu, L. Bjorkman, P. Janmey, A. Karlsson, J. Karlsson, and C. Movitz The two neutrophil members of the formylpeptide receptor family activate the NADPH-oxidase through signals that differ in sensitivity to a gelsolin derived phosphoinositide-binding peptide BMC Cell Biol 5 1 2004 50
33. Forsman H, Dahlgren C. The FPR2-induced rise in cytosolic calcium in human neutrophils relies on an emptying of intracellular calcium stores and is inhibited by a gelsolin-derived PIP2-binding peptide. BMC Cell Biol 2010;11(1):52.
34. B. Heit, S. Tavener, E. Raharjo, and P. Kubes An intracellular signaling hierarchy determines direction of migration in opposing chemotactic gradients J Cell Biol 159 1 2002 91 102
35. H. Fu, J. Bylund, A. Karlsson, S. Pellme, and C. Dahlgren The mechanism for activation of the neutrophil NADPH-oxidase by the peptides formyl-Met-Leu-Phe and Trp-Lys-Tyr-Met-Val-Met differs from that for interleukin-8 Immunology 112 2 2004 201 210
36. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 2010;464(7285):104-7.
37. Dufton N, Perretti M. Therapeutic anti-inflammatory potential of formyl-peptide receptor agonists. Pharmacol Ther 2010;127(2):175-88.
38. J.B. Arterburn, T.I. Oprea, E.R. Prossnitz, B.S. Edwards, and L.A. Sklar Discovery of selective probes and antagonists for G-protein-coupled receptors FPR/FPRL1 and GPR30 Curr Top Med Chem 9 13 2009 1227 1236
39. S.M. Young, C. Bologa, E.R. Prossnitz, T.I. Oprea, L.A. Sklar, and B.S. Edwards High-throughput screening with HyperCyt flow cytometry to detect small molecule formylpeptide receptor ligands J Biomol Screen 10 4 2005 374 382 (Pubitemid 40800566)
40. S.M. Young, C.M. Bologa, D. Fara, B.K. Bryant, J.J. Strouse, and J.B. Arterburn Duplex high-throughput flow cytometry screen identifies two novel formylpeptide receptor family probes Cytometry A 75 3 2009 253 263
41. M. Frohn, H. Xu, X. Zou, C. Chang, M. McElvaine, and M.H. Plant New 'chemical probes' to examine the role of the hFPRL1 (or ALXR) receptor in inflammation Bioorg Med Chem Lett 17 23 2007 6633 6637
42. M. Nanamori, X. Cheng, J. Mei, H. Sang, Y. Xuan, and C. Zhou A novel nonpeptide ligand for formyl peptide receptor-like 1 Mol Pharmacol 66 5 2004 1213 1222
43. M. Perretti, and J. Dalli Exploiting the Annexin A1 pathway for the development of novel anti-inflammatory therapeutics Br J Pharmacol 158 4 2009 936 946
44. R.A. Clark Chemotactic factors trigger their own oxidative inactivation by human neutrophils J Immunol 129 6 1982 2725 2728
45. D. Reumaux, P.L. Hordijk, P. Duthilleul, and D. Roos Priming by tumor necrosis factor-alpha of human neutrophil NADPH-oxidase activity induced by anti-proteinase-3 or anti-myeloperoxidase antibodies J Leukoc Biol 80 6 2006 1424 1433
46. S.C. Hsieh, H.S. Yu, S.H. Cheng, K.J. Li, M.C. Lu, and C.H. Wu Anti-myeloperoxidase antibodies enhance phagocytosis, IL-8 production, and glucose uptake of polymorphonuclear neutrophils rather than anti-proteinase 3 antibodies leading to activation-induced cell death of the neutrophils Clin Rheumatol 26 2 2007 216 224
47. J. Almkvist, C. Dahlgren, H. Leffler, and A. Karlsson Newcastle disease virus neuraminidase primes neutrophils for stimulation by galectin-3 and formyl-Met-Leu-Phe Exp Cell Res 298 1 2004 74 82
48. J. Bylund, A. Karlsson, F. Boulay, and C. Dahlgren Lipopolysaccharide- induced granule mobilization and priming of the neutrophil response to Helicobacter pylori peptide Hp(2-20), which activates formyl peptide receptor-like 1 Infect Immun 70 6 2002 2908 2914
49. J. Bylund, S. Pellme, H. Fu, U.H. Mellqvist, K. Hellstrand, and A. Karlsson Cytochalasin B triggers a novel pertussis toxin sensitive pathway in TNF-alpha primed neutrophils BMC Cell Biol 5 1 2004 21
50. A. Karlsson, P. Follin, H. Leffler, and C. Dahlgren Galectin-3 activates the NADPH-oxidase in exudated but not peripheral blood neutrophils Blood 91 9 1998 3430 3438