New development in studies of formyl-peptide receptors: Critical roles in host defense

Journal of Leukocyte Biology

Volumn 99, Issue 3, 2016, Pages 425-435

  Li, Liangzhu ^a,b   Chen, Keqiang ^b,c   Xiang, Yi ^d   Yoshimura, Teizo ^b   Su, Shaobo ^c   Zhu, Jianwei ^a   Bian, Xiu Wu ^e,f   Wang, Ji Ming ^b  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b NATIONAL CANCER INSTITUTE   (United States)

^c TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^d SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^e THIRD MILITARY MEDICAL UNIVERSITY   (China)

^f Department of Colorectal Surgery   (China)

Author keywords

Cancer; Immunity; Inflammation; Leukocytes; Trafficking

Indexed keywords

CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR2; FORMYLPEPTIDE RECEPTOR; FORMYLPEPTIDE RECEPTOR LIKE 1; FORMYLPEPTIDE RECEPTOR LIKE 2; G PROTEIN COUPLED RECEPTOR; UNCLASSIFIED DRUG; LIPOXIN; LIPOXIN A;

ALLERGIC AIRWAY INFLAMMATION; CANCER GROWTH; CARCINOGENESIS; CELL MEMBRANE DEPOLARIZATION; COLITIS; COLON MUCOSA; GLIOMA; HOMEOSTASIS; HOST RESISTANCE; HUMAN; IMMUNOPATHOGENESIS; LEUKOCYTE MIGRATION; LISTERIA MONOCYTOGENES; LISTERIOSIS; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; WOUND HEALING; ANIMAL; CELL MOTION; CHEMOTAXIS; IMMUNOLOGY; INFLAMMATION; LEUKOCYTE; NEOPLASMS; PHYSIOLOGY;

ANIMALS; CELL MOVEMENT; CHEMOTAXIS; HUMANS; INFLAMMATION; LEUKOCYTES; LIPOXINS; MACROPHAGES; NEOPLASMS; RECEPTORS, CCR7; RECEPTORS, FORMYL PEPTIDE; RECEPTORS, INTERLEUKIN-8B; WOUND HEALING;

EID: 84961254763     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.2RI0815-354RR     Document Type: Review

References (117)

1. Wang, J. M., Deng, X., Gong, W., Su, S. (1998) Chemokines and their role in tumor growth and metastasis. J. Immunol. Methods 220, 1-17.
2. Kristiansen, K. (2004) Molecular mechanisms of ligand binding, signaling, and regulation within the superfamily of G-protein-coupled receptors: molecular modeling and mutagenesis approaches to receptor structure and function. Pharmacol. Ther. 103, 21-80.
3. Griffith, J. W., Sokol, C. L., Luster, A. D. (2014) Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu. Rev. Immunol. 32, 659-702.
4. Lira, S. A., Furtado, G. C. (2012) The biology of chemokines and their receptors. Immunol. Res. 54, 111-120.
5. Ye, R. D., Cavanagh, S. L., Quehenberger, O., Prossnitz, E. R., Cochrane, C. G. (1992) Isolation of a cDNA that encodes a novel granulocyte Nformyl peptide receptor. Biochem. Biophys. Res. Commun. 184, 582-589.
6. Murphy, P. M., Ozçelik, T., Kenney, R. T., Tiffany, H. L., McDermott, D., Francke, U. (1992) A structural homologue of the N-formyl peptide receptor: characterization and chromosome mapping of a peptide chemoattractant receptor family. J. Biol. Chem. 267, 7637-7643.
7. Bao, L., Gerard, N. P., Eddy, Jr., R. L., Shows, T. B., Gerard, C. (1992) 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 13, 437-440.
8. Le, Y., Murphy, P. M., Wang, J. M. (2002) Formyl-peptide receptors revisited. Trends Immunol. 23, 541-548.
9. Ye, R. D., Boulay, F., Wang, J. M., Dahlgren, C., Gerard, C., Parmentier, M., Serhan, C. N., Murphy, P. M. (2009) International Union of Basic and Clinical Pharmacology, LXXIII: Nomenclature for the formyl peptide receptor (FPR) family. Pharmacol. Rev. 61, 119-161.
10. Hartt, J. K., Barish, G., Murphy, P. M., Gao, J. L. (1999) Nformylpeptides induce two distinct concentration optima for mouse neutrophil chemotaxis by differential interaction with two Nformylpeptide receptor (FPR) subtypes. Molecular characterization of FPR2, a second mouse neutrophil FPR. J. Exp. Med. 190, 741-748.
11. Cattaneo, F., Parisi, M., Ammendola, R. (2013) Distinct signaling cascades elicited by different formyl peptide receptor 2 (FPR2) agonists. Int. J. Mol. Sci. 14, 7193-7230.
12. Murphy, P. M. (1994) The molecular biology of leukocyte chemoattractant receptors. Annu. Rev. Immunol. 12, 593-633.
13. Chadwick, V. S., Mellor, D. M., Myers, D. B., Selden, A. C., Keshavarzian, A., Broom, M. F., Hobson, C. H. (1988) Production of peptides inducing chemotaxis and lysosomal enzyme release in human neutrophils by intestinal bacteria in vitro and in vivo. Scand. J. Gastroenterol. 23, 121-128.
14. Schiffmann, E., Corcoran, B. A., Wahl, S. M. (1975) N-formylmethionyl peptides as chemoattractants for leucocytes. Proc. Natl. Acad. Sci. U. S. A. 72, 1059-1062.
15. Marasco, W. A., Phan, S. H., Krutzsch, H., Showell, H. J., Feltner, D. E., Nairn, R., Becker, E. L., Ward, P. A. (1984) Purification and identification of formyl-methionyl-leucyl-phenylalanine as the major peptide neutrophil chemotactic factor produced by Escherichia coli. J. Biol. Chem. 259, 5430-5439.
16. Gao, J. L., Lee, E. J., Murphy, P. M. (1999) Impaired antibacterial host defense in mice lacking the N-formylpeptide receptor. J. Exp. Med. 189, 657-662.
17. Liu, M., Chen, K., Yoshimura, T., Liu, Y., Gong, W., Wang, A., Gao, J. L., Murphy, P. M., Wang, J. M. (2012) Formylpeptide receptors are critical for rapid neutrophil mobilization in host defense against Listeria monocytogenes. Sci. Rep. 2, 786.
18. Zhang, Q., Raoof, M., Chen, Y., Sumi, Y., Sursal, T., Junger, W., Brohi, K., Itagaki, K., Hauser, C. J. (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464, 104-107.
19. McDonald, B., Pittman, K., Menezes, G. B., Hirota, S. A., Slaba, I., Waterhouse, C. C., Beck, P. L., Muruve, D. A., Kubes, P. (2010) Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330, 362-366.
20. Molloy, M. J., Grainger, J. R., Bouladoux, N., Hand, T. W., Koo, L. Y., Naik, S., Quinones, M., Dzutsev, A. K., Gao, J. L., Trinchieri, G., Murphy, P. M., Belkaid, Y. (2013) Intraluminal containment of commensal outgrowth in the gut during infection-induced dysbiosis. Cell Host Microbe 14, 318-328.
21. Yang, Y., Liu, Y., Yao, X., Ping, Y., Jiang, T., Liu, Q., Xu, S., Huang, J., Mou, H., Gong, W., Chen, K., Bian, X., Wang, J. M. (2011) Annexin 1 released by necrotic human glioblastoma cells stimulates tumor cell growth through the formyl peptide receptor 1 [published correction in Am. J. Pathol. (2011), 179, 2674]. Am. J. Pathol. 179, 1504-1512.
22. Sun, R., Iribarren, P., Zhang, N., Zhou, Y., Gong, W., Cho, E. H., Lockett, S., Chertov, O., Bednar, F., Rogers, T. J., Oppenheim, J. J., Wang, J. M. (2004) Identification of neutrophil granule protein cathepsin G as a novel chemotactic agonist for the G protein-coupled formyl peptide receptor. J. Immunol. 173, 428-436.
23. Su, S. B., Gong, W., Gao, J. L., Shen, W., Murphy, P. M., Oppenheim, J. J., Wang, J. M. (1999) A seven-transmembrane, G protein-coupled receptor, FPRL1, mediates the chemotactic activity of serum amyloid A for human phagocytic cells. J. Exp. Med. 189, 395-402.
24. Le, Y., Gong, W., Tiffany, H. L., Tumanov, A., Nedospasov, S., Shen, W., Dunlop, N. M., Gao, J. L., Murphy, P. M., Oppenheim, J. J., Wang, J. M. (2001) Amyloid b42 activates a G-protein-coupled chemoattractant receptor, FPR-like-1. J. Neurosci. 21, RC123.
25. De Yang, Chen, Q., Schmidt, A. P., Anderson, G. M., Wang, J. M., Wooters, J., Oppenheim, J. J., Chertov, O. (2000) LL-37, the neutrophil granule-and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J. Exp. Med. 192, 1069-1074.
26. Kurosaka, K., Chen, Q., Yarovinsky, F., Oppenheim, J. J., Yang, D. (2005) Mouse cathelin-related antimicrobial peptide chemoattracts leukocytes using formyl peptide receptor-like 1/mouse formyl peptide receptorlike 2 as the receptor and acts as an immune adjuvant. J. Immunol. 174, 6257-6265.
27. De Santo, C., Arscott, R., Booth, S., Karydis, I., Jones, M., Asher, R., Salio, M., Middleton, M., Cerundolo, V. (2010) Invariant NKT cells modulate the suppressive activity of IL-10-secreting neutrophils differentiated with serum amyloid A. Nat. Immunol. 11, 1039-1046.
28. Liang, T. S., Wang, J. M., Murphy, P. M., Gao, J. L. (2000) Serum amyloid A is a chemotactic agonist at FPR2, a low-affinity Nformylpeptide receptor on mouse neutrophils. Biochem. Biophys. Res. Commun. 270, 331-335.
29. Cui, Y. H., Le, Y., Gong, W., Proost, P., Van Damme, J., Murphy, W. J., Wang, J. M. (2002) Bacterial lipopolysaccharide selectively up-regulates the function of the chemotactic peptide receptor formyl peptide receptor 2 in murine microglial cells. J. Immunol. 168, 434-442.
30. Coffelt, S. B., Marini, F. C., Watson, K., Zwezdaryk, K. J., Dembinski, J. L., LaMarca, H. L., Tomchuck, S. L., Honer zu Bentrup, K., Danka, E. S., Henkle, S. L., Scandurro, A. B. (2009) The pro-inflammatory peptide LL-37 promotes ovarian tumor progression through recruitment of multipotent mesenchymal stromal cells. Proc. Natl. Acad. Sci. U. S. A. 106, 3806-3811.
31. Babbin, B. A., Lee, W. Y., Parkos, C. A., Winfree, L. M., Akyildiz, A., Perretti, M., Nusrat, A. (2006) Annexin I regulates SKCO-15 cell invasion by signaling through formyl peptide receptors. J. Biol. Chem. 281, 19588-19599.
32. Southgate, E. L., He, R. L., Gao, J. L., Murphy, P. M., Nanamori, M., Ye, R. D. (2008) Identification of formyl peptides from Listeria monocytogenes and Staphylococcus aureus as potent chemoattractants for mouse neutrophils. J. Immunol. 181, 1429-1437.
33. Chen, K., Liu, M., Liu, Y., Wang, C., Yoshimura, T., Gong, W., Le, Y., Tessarollo, L., Wang, J. M. (2013) Signal relay by CC chemokine receptor 2 (CCR2) and formylpeptide receptor 2 (Fpr2) in the recruitment of monocyte-derived dendritic cells in allergic airway inflammation. J. Biol. Chem. 288, 16262-16273.
34. Leoni, G., Alam, A., Neumann, P. A., Lambeth, J. D., Cheng, G., McCoy, J., Hilgarth, R. S., Kundu, K., Murthy, N., Kusters, D., Reutelingsperger, C., Perretti, M., Parkos, C. A., Neish, A. S., Nusrat, A. (2013) Annexin A1, formyl peptide receptor, and NOX1 orchestrate epithelial repair. J. Clin. Invest. 123, 443-454.
35. Buss, N. A., Gavins, F. N., Cover, P. O., Terron, A., Buckingham, J. C. (2015) Targeting the annexin 1-formyl peptide receptor 2/ALX pathway affords protection against bacterial LPS-induced pathologic changes in the murine adrenal cortex. FASEB J. 29, 2930-2942.
36. Dalli, J., Jones, C. P., Cavalcanti, D. M., Farsky, S. H., Perretti, M., Rankin, S. M. (2012) Annexin A1 regulates neutrophil clearance by macrophages in the mouse bone marrow. FASEB J. 26, 387-396.
37. Resnati, M., Pallavicini, I., Wang, J. M., Oppenheim, J., Serhan, C. N., Romano, M., Blasi, F. (2002) The fibrinolytic receptor for urokinase activates the G protein-coupled chemotactic receptor FPRL1/LXA4R. Proc. Natl. Acad. Sci. U. S. A. 99, 1359-1364.
38. Migeotte, I., Riboldi, E., Franssen, J. D., Grégoire, F., Loison, C., Wittamer, V., Detheux, M., Robberecht, P., Costagliola, S., Vassart, G., Sozzani, S., Parmentier, M., Communi, D. (2005) Identification and characterization of an endogenous chemotactic ligand specific for FPRL2. J. Exp. Med. 201, 83-93.
39. Gao, J. L., Guillabert, A., Hu, J., Le, Y., Urizar, E., Seligman, E., Fang, K. J., Yuan, X., Imbault, V., Communi, D., Wang, J. M., Parmentier, M., Murphy, P. M., Migeotte, I. (2007) F2L, a peptide derived from hemebinding protein, chemoattracts mouse neutrophils by specifically activating Fpr2, the low-affinity N-formylpeptide receptor. J. Immunol. 178, 1450-1456.
40. Rabiet, M. J., Macari, L., Dahlgren, C., Boulay, F. (2011) N-formyl peptide receptor 3 (FPR3) departs from the homologous FPR2/ALX receptor with regard to the major processes governing chemoattractant receptor regulation, expression at the cell surface, and phosphorylation. J. Biol. Chem. 286, 26718-26731.
41. Dorward, D. A., Lucas, C. D., Chapman, G. B., Haslett, C., Dhaliwal, K., Rossi, A. G. (2015) The role of formylated peptides and formyl peptide receptor 1 in governing neutrophil function during acute inflammation. Am. J. Pathol. 185, 1172-1184.
42. Stavru, F., Archambaud, C., Cossart, P. (2011) Cell biology and immunology of Listeria monocytogenes infections: novel insights. Immunol. Rev. 240, 160-184.
43. Kasper, S., Huhulescu, S., Auer, B., Heller, I., Karner, F., Würzner, R., Wagner, M., Allerberger, F. (2009) Epidemiology of listeriosis in Austria. Wien. Klin. Wochenschr. 121, 113-119.
44. Goulet, V., Hedberg, C., Le Monnier, A., de Valk, H. (2008) Increasing incidence of listeriosis in France and other European countries. Emerg. Infect. Dis. 14, 734-740.
45. Watson, R. (2009) Listeriosis remains a cause for concern in Europe. BMJ 338, b319.
46. Allerberger, F., Wagner, M. (2010) Listeriosis: a resurgent foodborne infection. Clin. Microbiol. Infect. 16, 16-23.
47. Tilney, L. G., Portnoy, D. A. (1989) Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109, 1597-1608.
48. Mengaud, J., Ohayon, H., Gounon, P., Mege R-M, Cossart, P. (1996) Ecadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84, 923-932.
49. Yu, W. L., Dan, H., Lin, M. (2008) InlA and InlC2 of Listeria monocytogenes serotype 4b are two internalin proteins eliciting humoral immune responses common to listerial infection of various host species. Curr. Microbiol. 56, 505-509.
50. Zenewicz, L. A., Shen, H. (2007) Innate and adaptive immune responses to Listeria monocytogenes: a short overview. Microbes Infect. 9, 1208-1215.
51. Bonazzi, M., Lecuit, M., Cossart, P. (2009) Listeria monocytogenes internalin and E-cadherin: from bench to bedside. Cold Spring Harb. Perspect. Biol. 1, a003087.
52. Cossart, P., Toledo-Arana, A. (2008) Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect. 10, 1041-1050.
53. Hamon, M., Bierne, H., Cossart, P. (2006) Listeria monocytogenes: a multifaceted model. Nat. Rev. Microbiol. 4, 423-434.
54. Drevets, D. A., Bronze, M. S. (2008) Listeria monocytogenes: epidemiology, human disease, and mechanisms of brain invasion. FEMS Immunol. Med. Microbiol. 53, 151-165.
55. Pamer, E. G. (2004) Immune responses to Listeria monocytogenes. Nat. Rev. Immunol. 4, 812-823.
56. Cousens, L. P., Wing, E. J. (2000) Innate defenses in the liver during Listeria infection. Immunol. Rev. 174, 150-159.
57. Torres, D., Barrier, M., Bihl, F., Quesniaux, V. J., Maillet, I., Akira, S., Ryffel, B., Erard, F. (2004) Toll-like receptor 2 is required for optimal control of Listeria monocytogenes infection. Infect. Immun. 72, 2131-2139.
58. Chapman, R. W., Minnicozzi, M., Celly, C. S., Phillips, J. E., Kung, T. T., Hipkin, R. W., Fan, X., Rindgen, D., Deno, G., Bond, R., Gonsiorek, W., Billah, M. M., Fine, J. S., Hey, J. A. (2007) A novel, orally active CXCR1/2 receptor antagonist, Sch527123, inhibits neutrophil recruitment, mucus production, and goblet cell hyperplasia in animal models of pulmonary inflammation. J. Pharmacol. Exp. Ther. 322, 486-493.
59. Rose, J. J., Foley, J. F., Murphy, P. M., Venkatesan, S. (2004) On the mechanism and significance of ligand-induced internalization of human neutrophil chemokine receptors CXCR1 and CXCR2. J. Biol. Chem. 279, 24372-24386.
60. Cunha, T. M., Barsante, M. M., Guerrero, A. T., Verri, W. A., Jr., Ferreira, S. H., Coelho, F. M., Bertini, R., Di Giacinto, C., Allegretti, M., Cunha, F. Q., Teixeira, M. M. (2008) Treatment with DF 2162, a noncompetitive allosteric inhibitor of CXCR1/2, diminishes neutrophil influx and inflammatory hypernociception in mice. Br. J. Pharmacol. 154, 460-470.
61. Reichel, C. A., Khandoga, A., Anders, H. J., Schlöndorff, D., Luckow, B., Krombach, F. (2006) Chemokine receptors Ccr1, Ccr2, and Ccr5 mediate neutrophil migration to postischemic tissue. J. Leukoc. Biol. 79, 114-122.
62. Chintakuntlawar, A. V. Chodosh, J. (2009) Chemokine CXCL1/KC and its receptor CXCR2 are responsible for neutrophil chemotaxis in adenoviral keratitis. J. Interferon Cytokine Res. 29, 657-666.
63. Zhang, L., Ran, L., Garcia, G. E., Wang, X. H., Han, S., Du, J., Mitch, W. E. (2009) Chemokine CXCL16 regulates neutrophil and macrophage infiltration into injured muscle, promoting muscle regeneration. Am. J. Pathol. 175, 2518-2527.
64. Burdon, P. C., Martin, C., Rankin, S. M. (2005) The CXC chemokine MIP-2 stimulates neutrophil mobilization from the rat bone marrow in a CD49d-dependent manner. Blood 105, 2543-2548.
65. Monson, K. M., Dowlatshahi, S., Crockett, E. T. (2007) CXCchemokine regulation and neutrophil trafficking in hepatic ischemiareperfusion injury in P-selectin/ICAM-1-deficient mice. J. Inflamm. (Lond.) 4, 11.
66. Oldekamp, S., Pscheidl, S., Kress, E., Soehnlein, O., Jansen, S., Pufe, T., Wang, J. M., Tauber, S. C., Brandenburg, L. O. (2014) Lack of formyl peptide receptor 1 and 2 leads to more severe inflammation and higher mortality in mice with of pneumococcal meningitis. Immunology 143, 447-461.
67. Nathan, C. (2002) Points of control in inflammation. Nature 420, 846-852.
68. Ley, K., Laudanna, C., Cybulsky, M. I., Nourshargh, S. (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7, 678-689.
69. Chtanova, T., Schaeffer, M., Han, S. J., van Dooren, G. G., Nollmann, M., Herzmark, P., Chan, S. W., Satija, H., Camfield, K., Aaron, H., Striepen, B., Robey, E. A. (2008) Dynamics of neutrophil migration in lymph nodes during infection. Immunity 29, 487-496.
70. Peters, N. C., Egen, J. G., Secundino, N., Debrabant, A., Kimblin, N., Kamhawi, S., Lawyer, P., Fay, M. P., Germain, R. N., Sacks, D. (2008) In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321, 970-974.
71. Bruns, S., Kniemeyer, O., Hasenberg, M., Aimanianda, V., Nietzsche, S., Thywissen, A., Jeron, A., Latgé, J. P., Brakhage, A. A., Gunzer, M. (2010) Production of extracellular traps against Aspergillus fumigatus in vitro and in infected lung tissue is dependent on invading neutrophils and influenced by hydrophobin RodA. PLoS Pathog. 6, e1000873.
72. Yipp, B. G., Petri, B., Salina, D., Jenne, C. N., Scott, B. N., Zbytnuik, L. D., Pittman, K., Asaduzzaman, M., Wu, K., Meijndert, H. C., Malawista, S. E., de Boisfleury Chevance, A., Zhang, K., Conly, J., Kubes, P. (2012) Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat. Med. 18, 1386-1393.
73. Liese, J., Rooijakkers, S. H., van Strijp, J. A., Novick, R. P., Dustin, M. L. (2013) Intravital two-photon microscopy of host-pathogen interactions in a mouse model of Staphylococcus aureus skin abscess formation. Cell. Microbiol. 15, 891-909.
74. Harvie, E. A., Green, J. M., Neely, M. N., Huttenlocher, A. (2013) Innate immune response to Streptococcus iniae infection in zebrafish larvae. Infect. Immun. 81, 110-121.
75. Kreisel, D., Nava, R. G., Li, W., Zinselmeyer, B. H., Wang, B., Lai, J., Pless, R., Gelman, A. E., Krupnick, A. S., Miller, M. J. (2010) In vivo twophoton imaging reveals monocyte-dependent neutrophil extravasation during pulmonary inflammation. Proc. Natl. Acad. Sci. U. S. A. 107, 18073-18078.
76. Nakasone, E. S., Askautrud, H. A., Kees, T., Park, J. H., Plaks, V., Ewald, A. J., Fein, M., Rasch, M. G., Tan, Y. X., Qiu, J., Park, J., Sinha, P., Bissell, M. J., Frengen, E., Werb, Z., Egeblad, M. (2012) Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance. Cancer Cell 21, 488-503.
77. Chen, K., Le, Y., Liu, Y., Gong, W., Ying, G., Huang, J., Yoshimura, T., Tessarollo, L., Wang, J. M. (2010) A critical role for the g proteincoupled receptor mFPR2 in airway inflammation and immune responses. J. Immunol. 184, 3331-3335.
78. Provoost, S., Maes, T., Joos, G. F., Tournoy, K. G. (2012) Monocytederived dendritic cell recruitment and allergic TH2 responses after exposure to diesel particles are CCR2 dependent. J. Allergy Clin. Immunol. 129, 483-491.
79. Serbina, N. V., Pamer, E. G. (2006) Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7, 311-317.
80. Chen, K., Xiang, Y., Huang, J., Gong, W., Yoshimura, T., Jiang, Q., Tessarollo, L., Le, Y., Wang, J. M. (2014) The formylpeptide receptor 2 (Fpr2) and its endogenous ligand cathelin-related antimicrobial peptide (CRAMP) promote dendritic cell maturation. J. Biol. Chem. 289, 17553-17563.
81. Richardson, R. M., Ali, H., Tomhave, E. D., Haribabu, B., Snyderman, R. (1995) Cross-desensitization of chemoattractant receptors occurs at multiple levels: evidence for a role for inhibition of phospholipase C activity. J. Biol. Chem. 270, 27829-27833.
82. Caux, C., Vanbervliet, B., Massacrier, C., Ait-Yahia, S., Vaure, C., Chemin, K., Dieu-Nosjean, M. C., Vicari, A. (2002) Regulation of dendritic cell recruitment by chemokines. Transplantation 73(1:, Suppl) S7-S11.
83. Ng, L. G., Qin, J. S., Roediger, B., Wang, Y., Jain, R., Cavanagh, L. L., Smith, A. L., Jones, C. A., de Veer, M., Grimbaldeston, M. A., Meeusen, E. N., Weninger, W. (2011) Visualizing the neutrophil response to sterile tissue injury in mouse dermis reveals a three-phase cascade of events. J. Invest. Dermatol. 131, 2058-2068.
84. Lämmermann, T., Bader, B. L., Monkley, S. J., Worbs, T., Wedlich-Söldner, R., Hirsch, K., Keller, M., Förster, R., Critchley, D. R., Fässler, R., Sixt, M. (2008) Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453, 51-55.
85. Lämmermann, T., Afonso, P. V., Angermann, B. R., Wang, J. M., Kastenmüller, W., Parent, C. A., Germain, R. N. (2013) Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo. Nature 498, 371-375.
86. Liu, M., Chen, K., Yoshimura, T., Liu, Y., Gong, W., Le, Y., Gao, J. L., Zhao, J., Wang, J. M., Wang, A. (2014) Formylpeptide receptors mediate rapid neutrophil mobilization to accelerate wound healing. PLoS One 9, e90613.
87. Liu, X., Ma, B., Malik, A. B., Tang, H., Yang, T., Sun, B., Wang, G., Minshall, R. D., Li, Y., Zhao, Y., Ye, R. D., Xu, J. (2012) Bidirectional regulation of neutrophil migration by mitogen-activated protein kinases. Nat. Immunol. 13, 457-464.
88. Clevers, H. (2004) At the crossroads of inflammation and cancer. Cell 118, 671-674.
89. Balkwill, F., Mantovani, A. (2001) Inflammation and cancer: back to Virchow? Lancet 357, 539-545.
90. Coussens, L. M., Werb, Z. (2002) Inflammation and cancer. Nature 420, 860-867.
91. Coussens, L. M., Tinkle, C. L., Hanahan, D., Werb, Z. (2000) MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 103, 481-490.
92. Xiao, H., Gulen, M. F., Qin, J., Yao, J., Bulek, K., Kish, D., Altuntas, C. Z., Wald, D., Ma, C., Zhou, H., Tuohy, V. K., Fairchild, R. L., de la Motte, C., Cua, D., Vallance, B. A., Li, X. (2007) The Toll-interleukin-1 receptor member SIGIRR regulates colonic epithelial homeostasis, inflammation, and tumorigenesis. Immunity 26, 461-475.
93. Babbin, B. A., Jesaitis, A. J., Ivanov, A. I., Kelly, D., Laukoetter, M., Nava, P., Parkos, C. A., Nusrat, A. (2007) Formyl peptide receptor-1 activation enhances intestinal epithelial cell restitution through phosphatidylinositol 3-kinase-dependent activation of Rac1 and Cdc42. J. Immunol. 179, 8112-8121.
94. Alam, A., Leoni, G., Wentworth, C. C., Kwal, J. M., Wu, H., Ardita, C. S., Swanson, P. A., Lambeth, J. D., Jones, R. M., Nusrat, A., Neish, A. S. (2014) Redox signaling regulates commensal-mediated mucosal homeostasis and restitution and requires formyl peptide receptor 1. Mucosal Immunol. 7, 645-655.
95. Wentworth, C. C., Jones, R. M., Kwon, Y. M., Nusrat, A., Neish, A. S. (2010) Commensal-epithelial signaling mediated via formyl peptide receptors. Am. J. Pathol. 177, 2782-2790.
96. Chen, K., Liu, M., Liu, Y., Yoshimura, T., Shen, W., Le, Y., Durum, S., Gong, W., Wang, C., Gao, J. L., Murphy, P. M., Wang, J. M. (2013) Formylpeptide receptor-2 contributes to colonic epithelial homeostasis, inflammation, and tumorigenesis. J. Clin. Invest. 123, 1694-1704.
97. Prevete, N., Liotti, F., Visciano, C., Marone, G., Melillo, R. M., de Paulis, A. (2015) The formyl peptide receptor 1 exerts a tumor suppressor function in human gastric cancer by inhibiting angiogenesis [published online ahead of print September 29, 2014]. Oncogene 34, 3826-3838.
98. Zhou, Y., Bian, X., Le, Y., Gong, W., Hu, J., Zhang, X., Wang, L., Iribarren, P., Salcedo, R., Howard, O. M., Farrar, W., Wang, J. M. (2005) Formylpeptide receptor FPR and the rapid growth of malignant human gliomas. J. Natl. Cancer Inst. 97, 823-835.
99. Yao, X. H., Ping, Y. F., Chen, J. H., Chen, D. L., Xu, C. P., Zheng, J., Wang, J. M., Bian, X. W. (2008) Production of angiogenic factors by human glioblastoma cells following activation of the G-protein coupled formylpeptide receptor FPR. J. Neurooncol. 86, 47-53.
100. Huang, J., Hu, J., Bian, X., Chen, K., Gong, W., Dunlop, N. M., Howard, O. M., Wang, J. M. (2007) Transactivation of the epidermal growth factor receptor by formylpeptide receptor exacerbates the malignant behavior of human glioblastoma cells. Cancer Res. 67, 5906-5913.
101. Huang, J., Chen, K., Chen, J., Gong, W., Dunlop, N. M., Howard, O. M., Gao, Y., Bian, X. W., Wang, J. M. (2010) The G-protein-coupled formylpeptide receptor FPR confers a more invasive phenotype on human glioblastoma cells. Br. J. Cancer 102, 1052-1060.
102. Huang, J., Chen, K., Huang, J., Gong, W., Dunlop, N. M., Howard, O. M., Bian, X., Gao, Y., Wang, J. M. (2009) Regulation of the leucocyte chemoattractant receptor FPR in glioblastoma cells by cell differentiation. Carcinogenesis 30, 348-355.
103. Yao, X. H., Ping, Y. F., Chen, J. H., Xu, C. P., Chen, D. L., Zhang, R., Wang, J. M., Bian, X. W. (2008) Glioblastoma stem cells produce vascular endothelial growth factor by activation of a G-protein coupled formylpeptide receptor FPR. J. Pathol. 215, 369-376.
104. Khau, T., Langenbach, S. Y., Schuliga, M., Harris, T., Johnstone, C. N., Anderson, R. L., Stewart, A. G. (2011) Annexin-1 signals mitogenstimulated breast tumor cell proliferation by activation of the formyl peptide receptors (FPRs) 1 and 2. FASEB J. 25, 483-496.
105. Boer, J. C., Domanska, U. M., Timmer-Bosscha, H., Boer, I. G., de Haas, C. J., Joseph, J. V., Kruyt, F. A., de Vries, E. G., den Dunnen, W. F., van Strijp, J. A., Walenkamp, A. M. (2013) Inhibition of formyl peptide receptor in high-grade astrocytoma by chemotaxis inhibitory protein of S. aureus. Br. J. Cancer 108, 587-596.
106. Vakkila, J., Lotze, M. T. (2004) Inflammation and necrosis promote tumour growth. Nat. Rev. Immunol. 4, 641-648.
107. Mantovani, A., Sozzani, S., Locati, M., Allavena, P., Sica, A. (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23, 549-555.
108. Joyce, J. A., Pollard, J. W. (2009) Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252.
109. Talmadge, J. E., Donkor, M., Scholar, E. (2007) Inflammatory cell infiltration of tumors: Jekyll or Hyde. Cancer Metastasis Rev. 26, 373-400.
110. Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A., Locati, M. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25, 677-686.
111. Mosser, D. M., Edwards, J. P. (2008) Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8, 958-969.
112. Pollard, J. W. (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 4, 71-78.
113. Jin, G., Kawsar, H. I., Hirsch, S. A., Zeng, C., Jia, X., Feng, Z., Ghosh, S. K., Zheng, Q. Y., Zhou, A., McIntyre, T. M., Weinberg, A. (2010) An antimicrobial peptide regulates tumor-associated macrophage trafficking via the chemokine receptor CCR2, a model for tumorigenesis. PLoS One 5, e10993.
114. Qian, B. Z., Li, J., Zhang, H., Kitamura, T., Zhang, J., Campion, L. R., Kaiser, E. A., Snyder, L. A., Pollard, J. W. (2011) CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475, 222-225.
115. Yadav, A., Saini, V., Arora, S. (2010) MCP-1: chemoattractant with a role beyond immunity-a review. Clin. Chim. Acta 411, 1570-1579.
116. Frossard, J. L., Lenglet, S., Montecucco, F., Steffens, S., Galan, K., Pelli, G., Spahr, L., Mach, F., Hadengue, A. (2011) Role of CCL-2, CCR-2 and CCR-4 in cerulein-induced acute pancreatitis and pancreatitisassociated lung injury. J. Clin. Pathol. 64, 387-393.
117. Liu, Y., Chen, K., Wang, C., Gong, W., Yoshimura, T., Liu, M., Wang, J. M. (2013) Cell surface receptor FPR2 promotes antitumor host defense by limiting M2 polarization of macrophages. Cancer Res. 73, 550-560.