Intracellular signaling triggered by formyl-peptide receptors in nonphagocytic cells

Current Signal Transduction Therapy

Volumn 3, Issue 2, 2008, Pages 88-96

  Iaccio, Annalisa ^b,c   Angiolillo, Antonella ^a   Ammendola, Rosario ^a,b  

^a UNIVERSITY OF MOLISE   (Italy)

^b CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Formyl peptide receptors; Kinases; NADPH oxidase; Nonphagocytic cells; Reactive oxygen species; Transduction signals

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; 2 MORPHOLINO 8 PHENYLCHROMONE; AMYLOID A PROTEIN; ANTINEOPLASTIC AGENT; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; FORMYLMETHIONYLLEUCYLPHENYLALANINE; FORMYLPEPTIDE RECEPTOR; GLUCOCORTICOID; HEXAPEPTIDE; HUMANIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOCORTIN 1; LIPOXIN A; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; NORDY; PHOSPHATIDYLINOSITOL 3 KINASE; POBILUKAST; PROTEIN KINASE B; PROTEIN KINASE C; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; STRESS ACTIVATED PROTEIN KINASE; TRYPTOPHYLLYCYLTYROSYLMETHIONYLVALYLMETHIONINE; UNCLASSIFIED DRUG; UROKINASE; UROKINASE RECEPTOR; VASCULOTROPIN; WORTMANNIN;

ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; CANCER CELL CULTURE; CELL COMMUNICATION; CELL MOTILITY; CELL PROLIFERATION; CELL PROTECTION; CELLULAR DISTRIBUTION; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; FIBRINOLYSIS; GENE OVEREXPRESSION; GENE TRANSLOCATION; GENETIC TRANSCRIPTION; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; TRANSACTIVATION; UPREGULATION;

EID: 54949118361     PISSN: 15743624     EISSN: None     Source Type: Journal    
DOI: 10.2174/157436208784223152     Document Type: Review

References (83)

1. Bao L, Gerard NP, Eddy RL Jr, Shows TB, Gerard C. Mapping of genes for the human C5a receptor (C5AR), human FMLP receptor (FPR), and two FMLP receptor homologue orphan receptors (FPRH1, FPRH2) to chromosome 19. Genomics 1992; 13: 437-40.
2. Ye RD, Cavanagh SL, Quehenberger O, Prossnitz ER, Cochrane CG. Isolation of a cDNA that encodes a novel granulocyte N-formyl peptide receptor. Biochem Biophys Res Commun 1992; 184: 582-9.
3. Perez HD, Holmes R, Kelly E, Maclasy J, Chou Q, Andrews WH. Cloning of the gene coding for the human receptor for formyl-peptides. Characterization of a promoter region and evidence for polymorphic expression. Biochemistry 1992; 31: 11595-9.
4. Murphy PM, Ozcelik T, Kinney RT, Tiffany HL, McDermott D, Francke U. A structural homologue of the N-formyl peptide receptor. Characterization and chromosome mapping of a peptide chemoattractant receptor family. J Biol Chem 1992; 267: 7637-43.
5. Alvarez V, Coto E, Setien F, Lopezlarrea C. A physical map of two clusters containing the genes for 6 proinflammatory receptors. Immunogenetics 1994; 10: 100-3.
6. Le YY, Oppenheim JJ, Wang JM, et al. Pleiotropic roles of formyl peptide receptors. Cytokine Growth Factor Rev 2001; 12: 91-105.
7. Le YY, Murphy PM, Wang JM. Formyl-peptide receptors revisited. Trends Immunol 2002; 23: 541-8.
8. Wenzel-Seifert K, Arthur JM, Liu HY, Seifert R. Quantitative analysis of formyl peptide receptor coupling to G(i)alpha(1) G(i)alpha(2), and G(i)alpha(3). J Biol Chem 1999; 274: 33259-66.
9. Del Prete A, Vermin W, Dander E, et al. Defective dendritic cell migration and activation of adaptive immunity in PI3K gamma-deficient mice. EMBO J 2004; 23: 3305-15.
10. Durstin M, Gao JL, Tiffany HL, McDermott D, Murphy PM. Differential expression of members of the N-formylpeptide receptor gene-cluster in human phagocytes. Biochem Biophys Res Commun 1994; 201: 174-9.
11. Becker EL, Forouhar FA, Grunnet ML, et al. Broad immunocytochemical localization of the formylpeptide-receptor in human organs, tissues and cells. Cell Tissue Res 1998; 292: 129-35.
12. Harada M, Habata Y, Hosoya M, et al. N-formylated humanin activates both formyl peptide receptor-Like 1 and 2. Biochem Biophys Res Commun 2004; 324: 255-61.
13. Gwinn MR, Sharma A, De Nardin E, et al. Single nucleotide polymorphisms of the N-formyl peptide receptor in localized juvenile periodontitis. J Periodontol 1999; 70: 1194-201.
14. Migeotte I, Communi D, Parmentier M, et al. Formyl peptide receptors: A promiscuous subfamily of G protein-coupled receptors controlling immune system. Cytokine and Growth Factor Reviews 2006; 17: 501-19.
15. Gao JL, Becker EL, Freer RJ, Muthukumaraswamy N, Murphy PM. A high potency nonformylated peptide agonist for the phagocyte N-formylpeptide chemotactic receptor. J Exp Med 1994; 180: 2191-7.
16. Higgins JD, Bridger GJ, Derian CK, et al. N-terminus urea-substituted chemotactic peptides: new potent agonists and antagonists toward the neutrophil fMLF receptor. J Med Chem 1996; 39: 1013-5.
17. Derian CK, Solomon HF, Higgins JD, et al. Selective inhibition of N-formylpeptide-induced neutrophil activation by carboamate-modified peptide analogues. Biochemistry 1996; 35: 1265-9.
18. Rabiet MJ, Huet E,Boulay F, et al. Human mitochondria-derived N-formylated peptides are novel agonists equally active on FPR and FPRL1, while Listeria monocytogenes-derived peptides preferentially activate FPR. Eur J Immunol 2005; 35: 2486-95.
19. Le Y, Hu J, Gong W, et al. Expression of functional formyl peptide receptors by human astrocytoma cell lines. J Neuroimmunol 2000; 111: 102-8.
20. Zhou Y, Bian X, Le Y, et al. Formylpeptide receptor FPR and the rapid growth of malignant human gliomas. J Natl Cancer Inst 2005; 97: 823-35.
21. Vivanco I, Sawyers CL. The 3-kinase-Akt pathway in human cancer. Nat Rev Cancer 2002; 2: 489-501.
22. Harris AL. Hypoxia-a key regulator factor in tumor growth. Nat Rev Cancer 2002; 2: 38-47.
23. Wong M, Fish EN. RANTES and MIP-1α activates STATS in T cells. J Biol Chem 1998; 273: 309-14.
24. Mellado M, Rodriguez-Frade JM, Manes S, Martinez AC. Chemokine signaling and functional responses: the role of receptor dimerization and TK pathway activation. Annu Rev Immunol 2001; 19: 397-421.
25. Gross A, McDonnell JM, Dorsmeyer SJ, et al. Bcl-2 members and the mitochondria in apoptosis. Genes Dev 1999; 13: 1899-911.
26. Murphy KM, Ranganathan V, Farnsworth ML, Kavallaris M, Lock RB. Bcl-2 inhibits Bax translocation from cytosol to mitochondria during drug-induced apoptosis of human tumor cells. Cell Death Differ 2000; 7: 102-11.
27. Le Y, Iribarren P, Zhou Y, et al. Silencing the formylpeptide receptor FPR by short-interfering RNA. Mol Pharmacol 2004; 66: 1022-28.
28. Chen J-h, Bian X-w, Yao X-h, et al. Nordy, a synthetic lipoxygenase inhibitor, inhibits the expression of formylpeptide receptor and induces differentiation of malignant glioma cells. Biochem Biophys Res Commun 2006; 342: 1368-74.
29. Viswanathan A, Painter RG, Lanson NA, Wang G. Functional expression of N-formyl peptide receptors in human bone marrow-derived mesenchymal stem cells. Stem Cells 2007; 25: 1263-9.
30. VanCompernolle SE, Clark KL, Rummel KA, Todd SC. Expression and function of formyl peptide receptors on human fibroblasts cells. J Immunol 2003; 171: 2050-6.
31. Baek SN, Seo JK, Chae CB, Suh PC, Ryu SB. Identification of the peptides that stimulate the phosphoinositide hydrolysis in lymphocyte cell lines from peptide libraries. J Biol Chem 1996; 271: 8170-5.
32. Bae YS, Kim Y, Kim Y, Kim JH, Suh PG, Ryu SH. Trp-Lys-Tyr-Met-Val-D-Met is a chemoattractant for human phagocytic cells. J Leukoc Biol 1999; 66: 915-22.
33. Le YY, Gong WH, Li BQ, et al. Utilization of two seven-membrane, G protein-coupled receptors, formyl-peptide receptor- like 1 and formyl-peptide receptor, by the synthetic hexapeptide WKYMVm for human phagocyte activation. J Immunol 1999; 163: 6777-84.
34. Karlsson J, Fu HM, Boulay F, Bylund J, Dahlgren C. 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 2006; 71: 1488-96.
35. Ammendola R, Ruocchio MR, Chirico G, et al. Inhibition of NADH/ NADPH oxidase affects signal transduction by growth factor receptors in normal fibroblasts. Arch Biochem Biophys 2002; 397: 253-7.
36. Ammendola R, Russo L, De Felice C, Esposito F, Russo T, Cimino F. Low-affinity receptor-mediated induction of superoxide by N-formyl-methionyl-leucyl-phenylalanine and WKYMVm in IMR90 human fibroblasts. Free Rad Biol Med 2004; 36: 189-200.
37. Iaccio A, Collinet C, Montesane Gesualdi N, Ammendola R. Protein kinase C-α and -δ are required for NADPH oxidase activation in WKYMVm-stimulated IMR90 fibroblasts. Arch Biochem Biophys 2007; 459: 288-94.
38. Walther A, Riehemann K, Gerke V, et al. A novel ligand of the formyl-peptide receptor: annexin 1 regulates neutrophils extravasation interacting with the FPR. Mol Cell 2000; 5: 831-40.
39. Perretti M, Croxtall JD, Wheller SK, Goulding NJ, Hannon K, Flower RJ. Mobilizing lipocortin1 in adherent human leukocytes downregulates their transmigration. Nat Med 1996; 2: 1259-62.
40. Rescher U, Danielczyk A, Maskoff A, Gerke V. Functional activation of the formyl peptide receptor by a new endogenous ligand in human lung A549 cells. J Immunol 2002; 169: 1500-4.
41. McCoy K, Haviland DL, Molmenti EP, Ziambras T, Wetsel RA, Perlmutter DH. N-formylpeptide and complement C5a receptors are expressed in liver cells and mediate hepatic acute phase gene regulation. J Exp Med 1995; 182: 207-17.
42. Alldridge LC, Bryant CE. Annexin 1 regulates cell proliferation by disruption of cell morphology and inhibition of cyclin D1 expression through sustained activation of the ERK 1/2 MAPK signal. Exp Cell Res 2003; 290: 93-107.
43. Wang Y, Serfass L, Roy MO, Wong J, Bonneau AM, Georges E. Annexin-I expression modulates drug resistance in tumor cells. Biochem Biophys Res Commun 2004; 314: 565-70.
44. Babbin BA, Winston YL, Parkos CA, et al. Annexin 1 regulates SKCO-15 cell invasion by signaling through formyl peptide receptors. J Biol Chem 2006; 281: 19588-99.
45. Chodniewicz D, Zhelev DV. Novel pathways of F-actin polymerization in the human neutrophil. Blood 2003; 101: 1181-4.
46. Katanaev VL. Signal transduction in neutrophil chemotaxis. Biochemistry (Mosc) 2001; 66: 351-68.
47. Fiore S, Maddox JF, Perez HD, Serhan CN. Identification of a human cDNA-encoding a functional high-affinity lipoxin A(4) receptor. J Exp Med 1994; 180: 253-60.
48. Chiang N, Fierro IM, Gronert K, Serhan CM. Activation of lipoxin A4 receptors by aspirin-triggered lipoxins and select peptides evokes ligand-specific responses in inflammation. J Exp Med 2000; 191: 1197-207.
49. Ariel A, Chiang N, Arita M, Petasis NA, Serhan CN. Aspirin-triggered lipoxin A4 and B4 analogs block extracellular signal-regulated kinase-dependent TNF-α secretion from human T-cells. J Immunol 2003; 170: 6266-72.
50. Fierro IM, Colgan SP, Bernasconi G, et al. Lipoxin A4 and aspirin-triggered 15-epi-lipoxin A4 inhibit human neutrophil migration: Comparisons between synthetic 15 epimers in chemotaxis and transmigration with microvessel endothelial cells and epithelial cells. J Immunol 2003; 170: 2688-94.
51. Maddox JF, Hachicha M, Takano T, Petasis NA, Fokin VV, Serhan CN. Lipoxin A4 stable analogs are potent mimetics that stimulate human monocytes and THP-1 cells via a G protein-linked lipoxin A4 receptor. J Biol Chem 1997; 272: 6972-8.
52. Maddox JF, Serhan CM. Lipoxin A4 and B4 are potent stimuli for human monocyte migration and adhesion: selective inactivation by dehydrogenation and reduction. J Exp Med 1996; 183: 137-46.
53. McMahon B, Stenson C, McPhillips F, Fanning A, Brady HR, Godson C. Lipoxin A4 antagonizes the mitogenic effects of leukotriene D4 in human renal mesengial cells. J Biol Chem 2000; 275: 27566-75.
54. Mitchell D, Rodgers K, Hanly J, et al. Lipoxins inhibit Akt/PKB activation and cell cycle progression in human mesangial cells. Am J Pathol 2004; 164: 937-46.
55. Rodgers K, McMahon B, Mitchell D, Sadlier D, Godson C. Lipoxin A4 modifies platelet-derived growth factor-induced profibrotic gene expression in human renal mesangial cells. Am J Pathol 2005; 167: 683-94.
56. Sodin-Semrl S, Taddeo B, Tseng D, Varga J, Fiore S. Lipoxina A4 inhibits IL1β-induced IL-6, IL-8 and matrix metalloproteinase-3 production in human synovial fibroblasts and enhances synthesis of tissue inhibitors of metalloproteinases. J Immunol 2000; 164: 2660-6.
57. Fiore S, Antico G, Aloman M, Sodin-Semrl S. Lipoxin A4 biology in the human synovium. Role of the ALX signaling pathways in modulation of inflammatory arthritis. Prostaglandins Leukot Essent Fatty Acids 2005; 73: 189-96.
58. Wu S-H, Wu X-H, Lu C, Dong L, Chen Z-Q. Lipoxin A4 inhibits proliferation of human lung fibroblasts induced by connective tissue growth factor. Am J Respir Cell Mol Biol 2006; 34: 65-72.
59. Hoyer-Hansen G, Pessara U, Holm A, et al. Urokinase-catalysed cleavage of the urokinase receptor requires an intact glycolipid anchor. Biochem J 2001; 358: 673-9.
60. Resnati M, Pallavicini I, Wang JM, et al. The fibrinolytic receptor for urokinase activates the G protein-coupled chemotactic receptor FPRL1/LXA4R. Proc Natl Acad Sci USA 2002; 99: 1359-64.
61. Daub H, Weiss FU, Wallasch C, Ullrich A. Role of transactivation of the EGF receptor in signalling by C-protein-coupled receptors. Nature 1996; 379: 557-60.
62. Jo M, Thomas KS, Marozkina N, et al. Dynamic assembly of the urokinase-type plasminogen activator signaling receptor complex determines the mitogenic activity of urokinase-type plasminogen activator. J Biol Chem 2005; 280: 17449-57.
63. Pierce K, Tohgo A, Ahn S, Field ME, Luttrell LM, Lefkowitz RJ. Epidermal growth factor (EGF) receptor-dependent ERK activation by G protein-coupled receptors: a co-culture system for identifying intermediates upstream and downstream of heparin-binding EGF shedding. J Biol Chem 2001; 276: 23155-60.
64. Mazzieri K, D'Alessio S, Kenmoe RK, Ossowski L, Blasi F. An uncleavable uPAR mutant allows dissection of signaling pathways in uPA-dependent cell migration. Mol Biol Cell 2006. 17: 367-78.
65. Fazioli F, Resnati M, Sidenius N, Higashimoto Y, Appella E, Blasi F. A urokinase-sensitive region of the human urokinase receptor is responsible for its chemotactic activity. EMBO J 1997; 16: 7279-86.
66. Glenner GG. Amyloid deposits and amyloidosis. N Engl J Med 1980; 302: 1283-92.
67. Stone MJ. Amyloidosis: a final common pathway for protein deposition in tissues. Blood 1990; 75: 531-45.
68. Su SB, Gong W, Gao JL, et al. A seven-transmebrane, C protein-coupled receptor, FPRL1, mediates the chemotactic activity of serum amyloid A for human phagocytic cells. J Exp Med 1999; 189: 395-402.
69. Sodin-Semrl S, Spagnolo A, Mikus R, Barbaro R, Varga J, Fiore S. Opposing regulation of interleukin-8 and Nf-kappaB responses by lipoxin A4 and serum amyloid A via the common lipoxin A receptor. Int J Immunopathol Pharmacol 2004; 17: 145-56.
70. Lee MS, Yoo SA, Cho CS, Suh PG, Kim WU, Ryu SN. Serum amyloid A binding formyl peptide receptor-like 1 induces synovial hyperplasia and angiogenesis. J Immunol 2006; 177: 5585-94.
71. Jo S, Yun J, Kim J, Lee C, Baek S, Bae Y. Serum amyloid A induces WISH cell apoptosis. Acta Pharmacol Sci 2007; 28: 73-80.
72. Hashimoto Y, Niikura T, Tajima H, et al. A rescue factor abolishing neuronal cell death by a wide spectrum of familial Alzheimers diseases genes and Aβ42. Proc Natl Acad Sci USA 2001; 98: 6336-41.
73. Tajima H, Niikura T, Hashimoto Y. et al. Evidence for in vivo production of Humanin peptide, a neuroprotective factor against Alzheimer's disease-related insults. Neurosci Lett 2002; 324: 227-31.
74. Hashimoto Y, Niikura T, Ito Y, et al. Detailed characterization of neuroprotection by a rescue factor humanin against various Alzheimer's disease-relevant insults. J Neurosci 2001; 21: 9235-45.
75. Ying G, Iribarren P, Zhou Y, et al. Humanin, a newly identified neuroprotective factor, uses the G protein-coupled formylpeptide receptor-like 1 as a functional receptor. J Immunol 2004; 172: 7078-85.
76. Ranger AM, Malynn BA, Korsmeyer SJ, et al. Mouse models of cell death. Nature Genet 2001; 28: 113-8.
77. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ. Movement of Bax from the cytosol to mitochondria dating apoptosis J Cell Biol 1997; 139: 1281-92.
78. Guo B, ZD, Cabezas E, et al. Humanin peptide suppresses apoptosis by interfering with Bax activation. Nature 2003; 423: 456-61.
79. Zhai D, Luciano F, Zhu X, Guo B, Satterthwait AC, Redd JC. Humanin binds and nullifies Bid activity by blocking its activation of Bax and Bak. J Biol Chem 2005; 280: 15815-24.
80. Tjabringa GS, Ninaber DK, Drijfhout SW, Rabe KF, Hiemstra PS. Human cathelicidin LL-37 is a chemoattractant for eosinophils and neutrophils that acts via formyl-peptide receptors. Int Arch Allergy Immunol 2006; 140: 103-12.
81. Koczulla R, Von Degenfeld G, Kupatt C, et al. An angiogenic role for the human peptide antibiotic LL-37/hCAP-18. J Clin Invest 2003; 111: 1665-72.
82. Shaykhiev R, Beisswenger C, Kandler K, et al. Human endogenous antibiotic LL-37 stimulates airway epithelial cell proliferation and wound closure. Am J Physiol Lung Cell Mol Physiol 2005; 289: 842-8.
83. Karp CL, Flick LM, Park KW, et al. Defective lipoxin-mediated anti-inflammatory activity in the cystic fibrosis airway. Nat Immun 2004; 5: 388-92.