The formyl peptide receptor 1 exerts a tumor suppressor function in human gastric cancer by inhibiting angiogenesis

Oncogene

Volumn 34, Issue 29, 2015, Pages 3826-3838

  Prevete, N ^a   Liotti, F ^a   Visciano, C ^a   Marone, G ^a   Melillo, R M ^a   De Paulis, A ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

FORMYLPEPTIDE RECEPTOR LIKE 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 1ALPHA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; VASCULOTROPIN; FORMYLMETHIONYLLEUCYLPHENYLALANINE; FORMYLPEPTIDE RECEPTOR; FPR1 PROTEIN, HUMAN; HIF1A PROTEIN, HUMAN; OLIGOPEPTIDE; TRP-LYS-TYR-MET-VAL-MET; TUMOR SUPPRESSOR PROTEIN; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; GENE EXPRESSION; GENE SILENCING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STOMACH CANCER; UPREGULATION; AGONISTS; ANIMAL; APOPTOSIS; C57BL MOUSE; CELL CULTURE; CELL MOTION; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); NUDE MOUSE; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SCID MOUSE; STOMACH TUMOR; TUMOR CELL LINE; VASCULARIZATION;

MUS;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; MICE, INBRED C57BL; MICE, NUDE; MICE, SCID; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; NEOVASCULARIZATION, PATHOLOGIC; OLIGOPEPTIDES; RECEPTORS, FORMYL PEPTIDE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; STOMACH NEOPLASMS; TUMOR SUPPRESSOR PROTEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84937500843     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.309     Document Type: Article

References (35)

1. Ye RD, Boulay F, Wang JM, Dahlgren C, Gerard C, Parmentier M et al. International Union of Basic and Clinical Pharmacology. LXXIII. Nomenclature for the formyl peptide receptor (FPR) family. Pharmacol Rev 2009; 61: 119-161.
2. Le Y, Murphy PM, Wang JM. Formyl-peptide receptors revisited. Trends Immunol 2002; 23: 541-548.
3. de Paulis A, Prevete N, Fiorentino I, Walls AF, Curto M, Petraroli A et al. Basophils infiltrate human gastric mucosa at sites of Helicobacter pylori infection, and exhibit chemotaxis in response to H. pylori-derived peptide Hp(2-20). J Immunol 2004; 172: 7734-7743.
4. de Paulis A, Montuori N, Prevete N, Fiorentino I, Rossi FW, Visconte V et al. Urokinase induces basophil chemotaxis through a urokinase receptor epitope that is an endogenous ligand for formyl peptide receptor-like 1 and -like 2. J Immunol 2004; 173: 5739-5748.
5. Gao JL, Guillabert A, Hu J, Le Y, Urizar E, Seligman E et al. F2L, a peptide derived from heme-binding protein, chemoattracts mouse neutrophils by specifically activating Fpr2, the low-affinity N-formylpeptide receptor. J Immunol 2007; 178: 1450-1456.
6. Migeotte I, Communi D, Parmentier M. Formyl peptide receptors: a promiscuous subfamily of G protein-coupled receptors controlling immune responses. Cytokine Growth Factor Rev 2006; 17: 501-519.
7. Pott J, Hornef M. Innate immune signalling at the intestinal epithelium in homeostasis and disease. EMBO Rep 2012; 13: 684-698.
8. de Paulis A, Prevete N, Rossi FW, Rivellese F, Salerno F, Delfino G et al. Helicobacter pylori Hp(2-20) promotes migration and proliferation of gastric epithelial cells by interacting with formyl peptide receptors in vitro and accelerates gastric mucosal healing in vivo. J Immunol 2009; 183: 3761-3769.
9. Babbin BA, Jesaitis AJ, Ivanov AI, Kelly D, Laukoetter M, Nava P et al. Formyl peptide receptor-1 activation enhances intestinal epithelial cell restitution through phosphatidylinositol 3-kinase-dependent activation of Rac1 and Cdc42. J Immunol 2007; 179: 8112-8121.
10. Shao G, Julian MW, Bao S, McCullers MK, Lai JP, Knoell DL et al. Formyl peptide receptor ligands promote wound closure in lung epithelial cells. Am J Respir Cell Mol Biol 2011; 44: 264-269.
11. Zhang XG, Hui YN, Huang XF, Du HJ, Zhou J, Ma JX. Activation of formyl peptide receptor-1 enhances restitution of human retinal pigment epithelial cell monolayer under electric fields. Invest Ophthalmol Vis Sci 2011; 52: 3160-3165.
12. Zhou Y, Bian X, Le Y, Gong W, Hu J, Zhang X et al. Formylpeptide receptor FPR and the rapid growth of malignant human gliomas. J Natl Cancer Inst 2005; 97: 823-835.
13. Huang J, Chen K, Chen J, Gong W, Dunlop NM, Howard OM et al. The G-proteincoupled formyl peptide receptor FPR confers a more invasive phenotype on human glioblastoma cells. Br J Cancer 2010; 102: 1052-1060.
14. Chen K, Liu M, Liu Y, Yoshimura T, Shen W, Le Y et al. Formyl peptide receptor-2 contributes to colonic epithelial homeostasis, inflammation, and tumorigenesis. J Clin Invest 2013; 123: 1694-1704.
15. Otani T, Ikeda S, Lwin H, Arai T, Muramatsu M, Sawabe M. Polymorphisms of the formylpeptide receptor gene (FPR1) and susceptibility to stomach cancer in 1531 consecutive autopsy cases. Biochem Biophys Res Commun 2011; 405: 356-361.
16. Seifert R, Wenzel-Seifert K. Defective Gi protein coupling in two formyl peptide receptor mutants associated with localized juvenile periodontitis. J Biol Chem 2001; 276: 42043-42049.
17. Thiery JP. Epithelial-mesenchymal transitions in development and pathologies. Curr Opin Cell Biol 2003; 15: 740-746.
18. Radisky ES, Radisky DC. Matrix metalloproteinase-induced epithelial-mesenchymal transition in breast cancer. J Mammary Gland Biol Neoplasia 2010; 15: 201-212.
19. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009; 119: 1420-1428.
20. de Paulis A, Ciccarelli A, de Crescenzo G, Cirillo R, Patella V, Marone G. Cyclosporin H is a potent and selective competitive antagonist of human basophil activation by N-formyl-methionyl-leucyl-phenylalanine. J Allergy Clin Immunol 1996; 98: 152-164.
21. Prevete N, Staiano RI, Granata F, Detoraki A, Necchi V, Ricci V et al. Expression and function of Angiopoietins and their tie receptors in human basophils and mast cells. J Biol Regul Homeost Agents 2013; 27: 827-839.
22. Pang M, Ma L, Gong R, Tolbert E, Mao H, Ponnusamy M et al. A novel STAT3 inhibitor, S3I-201, attenuates renal interstitial fibroblast activation and interstitial fibrosis in obstructive nephropathy. Kidney Int 2010; 78: 257-268.
23. Kalia S, Bansal MP. Diethyl maleate-induced oxidative stress leads to testicular germ cell apoptosis involving Bax and Bcl-2. J Biochem Mol Toxicol 2008; 22: 371-381.
24. D'Acquisto F, Perretti M, Flower RJ. Annexin-A1: a pivotal regulator of the innate and adaptive immune systems. Br J Pharmacol 2008; 155: 152-169.
25. Paul SA, Simons JW, Mabjeesh NJ. HIF at the crossroads between ischemia and carcinogenesis. J Cell Physiol 2004; 200: 20-30.
26. Cheng TY, Wu MS, Lin JT, Lin MT, Shun CT, Huang HY et al. Annexin A1 is associated with gastric cancer survival and promotes gastric cancer cell invasiveness through the formyl peptide receptor/extracellular signalregulated kinase/integrin beta-1-binding protein 1 pathway. Cancer 2012; 118: 5757-5767.
27. Devosse T, Dutoit R, Migeotte I, DE Nadai P, Imbault V, Communi D et al. Processing of HEBP1 by cathepsin D gives rise to F2L, the agonist of formyl peptide receptor 3. J Immunol 2011; 187: 1475-1485.
28. Leoni G, Alam A, Neumann PA, Lambeth JD, Cheng G, McCoy J et al. Annexin A1, formyl peptide receptor, and NOX1 orchestrate epithelial repair. J Clin Invest 2013; 123: 443-454.
29. Jing YY, Han ZP, Sun K, Zhang SS, Hou J, Liu Y et al. Toll-like receptor 4 signaling promotes epithelial-mesenchymal transition in human hepatocellular carcinoma induced by lipopolysaccharide. BMC Med 2012; 10: 98-109.
30. Cooray SN, Gobetti T, Montero-Melendez T, McArthur S, Thompson D, Clark AJ et al. Ligand specific conformational change of the G-protein coupled receptor ALX/FPR2 determines proresolving functional responses. Proc Natl Acad Sci USA 2013; 110: 18232-18237.
31. Takahashi A, Kono K, Itakura J, Amemiya H, Feng Tang R, Iizuka H et al. Correlation of vascular endothelial growth factor-C expression with tumor-infiltrating dendritic cells in gastric cancer. Oncology 2002; 62: 121-127.
32. Liu L, Ma XL, Xiao ZL, Li M, Cheng SH, Wei YQ. Prognostic value of vascular endothelial growth factor expression in resected gastric cancer. Asian Pac J Cancer Prev 2012; 13: 3089-3097.
33. Cheng WL, Wang CS, Huang YH, Tsai MM, Liang Y, Lin KH. Overexpression of CXCL1 and its receptor CXCR2 promote tumor invasion in gastric cancer. Ann Oncol 2011; 22: 2267-2276.
34. Avilla E, Guarino V, Visciano C, Liotti F, Svelto M, Krishnamoorthy G et al. Activation of TYRO3/AXL tyrosine kinase receptors in thyroid cancer. Cancer Res 2011; 71: 1792-1804.
35. Detoraki A, Staiano RI, Granata F, Giannattasio G, Prevete N, de Paulis A et al. Vascular endothelial growth factors synthesized by human lung mast cells exert angiogenic effects. J Allergy Clin Immunol 2009; 123: 1142-1149.