Definition of a novel pathway centered on lysophosphatidic acid to recruit monocytes during the resolution phase of tissue inflammation

Journal of Immunology

Volumn 195, Issue 3, 2015, Pages 1139-1151

  McArthur, Simon ^a   Gobbetti, Thomas ^a   Kusters, Dennis H M ^b,c   Reutelingsperger, Christopher P ^b,c   Flower, Roderick J ^a   Perretti, Mauro ^a  

^a UNIVERSITY OF WESTMINSTER   (United Kingdom)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM INDEPENDENT PHOSPHOLIPASE A2; CD14 ANTIGEN; CD16 ANTIGEN; CHEMOATTRACTANT; G PROTEIN COUPLED RECEPTOR; LIPOCORTIN 1; LYSOPHOSPHATIDIC ACID; LYSOPHOSPHATIDIC ACID RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOLIPASE A2; ZYMOSAN; ANNEXIN A1, MOUSE; FC RECEPTOR; FORMYL PEPTIDE RECEPTOR 2, MOUSE; FORMYLPEPTIDE RECEPTOR; LYSOPHOSPHOLIPID; SMALL INTERFERING RNA;

ACTIN FILAMENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE ACTIVATION; MALE; MONOCYTE; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; WILD TYPE; ZYMOSAN-INDUCED PERITONITIS; ANIMAL; APOPTOSIS; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; GENETICS; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE; METABOLISM; RNA INTERFERENCE; TRANSPLANTATION;

ACTIN CYTOSKELETON; ANIMALS; ANNEXIN A1; ANTIGENS, CD14; APOPTOSIS; CELLS, CULTURED; ENZYME ACTIVATION; HUMANS; INFLAMMATION; LYSOPHOSPHOLIPIDS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; NEUTROPHILS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOLIPASES A2, CALCIUM-INDEPENDENT; RECEPTORS, FORMYL PEPTIDE; RECEPTORS, IGG; RECEPTORS, LYSOPHOSPHATIDIC ACID; RNA INTERFERENCE; RNA, SMALL INTERFERING; ZYMOSAN;

EID: 84937713087     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500733     Document Type: Article

References (52)

1. Couzin-Frankel, J. 2010. Inflammation bares a dark side. Science 330: 1621.
2. Serhan, C. N., and J. Savill. 2005. Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6: 1191-1197.
3. Tabas, I., and C. K. Glass. 2013. Anti-inflammatory therapy in chronic disease: challenges and opportunities. Science 339: 166-172.
4. Rossi, A. G., D. A. Sawatzky, A. Walker, C. Ward, T. A. Sheldrake, N. A. Riley, A. Caldicott, M. Martinez-Losa, T. R. Walker, R. Duffin, et al. 2006. Cyclindependent kinase inhibitors enhance the resolution of inflammation by promoting inflammatory cell apoptosis. Nat. Med. 12: 1056-1064.
5. Maslin, C. L. V., K. Kedzierska, N. L. Webster, W. A. Muller, and S. M. Crowe. 2005. Transendothelial migration of monocytes: the underlying molecular mechanisms and consequences of HIV-1 infection. Curr. HIV Res. 3: 303-317.
6. Melgarejo, E., M. A. Medina, F. Sánchez-Jiménez, and J. L. Urdiales. 2009. Monocyte chemoattractant protein-1: a key mediator in inflammatory processes. Int. J. Biochem. Cell Biol. 41: 998-1001.
7. Soehnlein, O., L. Lindbom, and C. Weber. 2009. Mechanisms underlying neutrophil-mediated monocyte recruitment. Blood 114: 4613-4623.
8. Gallin, J. I., M. P. Fletcher, B. E. Seligmann, S. Hoffstein, K. Cehrs, and N. Mounessa. 1982. Human neutrophil-specific granule deficiency: a model to assess the role of neutrophil-specific granules in the evolution of the inflammatory response. Blood 59: 1317-1329.
9. Soehnlein, O., A. Zernecke, E. E. Eriksson, A. G. Rothfuchs, C. T. Pham, H. Herwald, K. Bidzhekov, M. E. Rottenberg, C. Weber, and L. Lindbom. 2008. Neutrophil secretion products pave the way for inflammatory monocytes. Blood 112: 1461-1471.
10. Fiore, S., J. F. Maddox, H. D. Perez, and C. N. Serhan. 1994. Identification of a human cDNA encoding a functional high affinity lipoxin A4 receptor. J. Exp. Med. 180: 253-260.
11. Hartt, J. K., G. Barish, P. M. Murphy, and J. L. Gao. 1999. N-formylpeptides induce two distinct concentration optima for mouse neutrophil chemotaxis by differential interaction with two N-formylpeptide receptor (FPR) subtypes: molecular characterization of FPR2, a second mouse neutrophil FPR. J. Exp. Med. 190: 741-747.
12. Francis, J. W., K. J. Balazovich, J. E. Smolen, D. I. Margolis, and L. A. Boxer. 1992. Human neutrophil annexin I promotes granule aggregation and modulates Ca(2+)-dependent membrane fusion. J. Clin. Invest. 90: 537-544.
13. Scannell, M., M. B. Flanagan, A. deStefani, K. J. Wynne, G. Cagney, C. Godson, and P. Maderna. 2007. Annexin-1 and peptide derivatives are released by apoptotic cells and stimulate phagocytosis of apoptotic neutrophils by macrophages. J. Immunol. 178: 4595-4605.
14. Arur, S., U. E. Uche, K. Rezaul, M. Fong, V. Scranton, A. E. Cowan, W. Mohler, and D. K. Han. 2003. Annexin I is an endogenous ligand that mediates apoptotic cell engulfment. Dev. Cell 4: 587-598.
15. Cooray, S. N., T. Gobbetti, T. Montero-Melendez, S. McArthur, D. Thompson, A. J. L. Clark, R. J. Flower, and M. Perretti. 2013. Ligand-specific conformational change of the G-protein-coupled receptor ALX/FPR2 determines proresolving functional responses. Proc. Natl. Acad. Sci. USA 110: 18232-18237.
16. Maddox, J. F., and C. N. Serhan. 1996. Lipoxin A4 and B4 are potent stimuli for human monocyte migration and adhesion: selective inactivation by dehydrogenation and reduction. J. Exp. Med. 183: 137-146.
17. Dufton, N., R. Hannon, V. Brancaleone, J. Dalli, H. B. Patel, M. Gray, F. D'Acquisto, J. C. Buckingham, M. Perretti, and R. J. Flower. 2010. Antiinflammatory role of the murine formyl-peptide receptor 2: ligand-specific effects on leukocyte responses and experimental inflammation. J. Immunol. 184: 2611-2619.
18. Hannon, R., J. D. Croxtall, S. J. Getting, F. Roviezzo, S. Yona, M. J. Paul-Clark, F. N. E. Gavins, M. Perretti, J. F. Morris, J. C. Buckingham, and R. J. Flower. 2003. Aberrant inflammation and resistance to glucocorticoids in annexin 1-/-mouse. FASEB J. 17: 253-255.
19. Gobbetti, T., S. M. Coldewey, J. Chen, S. McArthur, P. le Faouder, N. Cenac, R. J. Flower, C. Thiemermann, and M. Perretti. 2014. Nonredundant protective properties of FPR2/ALX in polymicrobial murine sepsis. Proc. Natl. Acad. Sci. USA 111: 18685-18690.
20. Dalli, J., T. Montero-Melendez, S. McArthur, and M. Perretti. 2012. Annexin A1 N-terminal derived peptide ac2-26 exerts chemokinetic effects on human neutrophils. Front. Pharmacol. 3: 28.
21. Matayoshi, S., S. Chiba, Y. Lin, K. Arakaki, H. Matsumoto, T. Nakanishi, M. Suzuki, and S. Kato. 2013. Lysophosphatidic acid receptor 4 signaling potentially modulates malignant behavior in human head and neck squamous cell carcinoma cells. Int. J. Oncol. 42: 1560-1568.
22. Perretti, M., S. K. Wheller, R. J. Flower, S. Wahid, and C. Pitzalis. 1999. Modulation of cellular annexin I in human leukocytes infiltrating DTH skin reactions. J. Leukoc. Biol. 65: 583-589.
23. Yona, S., and S. Jung. 2010. Monocytes: subsets, origins, fates and functions. Curr. Opin. Hematol. 17: 53-59.
24. Perretti, M., and F. D'Acquisto. 2009. Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat. Rev. Immunol. 9: 62-70.
25. Wantha, S., J.-E. Alard, R. T. A. Megens, A. M. van der Does, Y. Döring, M. Drechsler, C. T. N. Pham, M.-W. Wang, J.-M. Wang, R. L. Gallo, et al. 2013. Neutrophil-derived cathelicidin promotes adhesion of classical monocytes. Circ. Res. 112: 792-801.
26. Hale, K. K., D. Trollinger, M. Rihanek, and C. L. Manthey. 1999. Differential expression and activation of p38 mitogen-Activated protein kinase alpha, beta, gamma, and delta in inflammatory cell lineages. J. Immunol. 162: 4246-4252.
27. Carnevale, K. A., and M. K. Cathcart. 2001. Calcium-independent phospholipase A(2) is required for human monocyte chemotaxis to monocyte chemoattractant protein 1. J. Immunol. 167: 3414-3421.
28. Willier, S., E. Butt, and T. G. P. Grunewald. 2013. Lysophosphatidic acid (LPA) signalling in cell migration and cancer invasion: a focused review and analysis of LPA receptor gene expression on the basis of more than 1700 cancer microarrays. Biol. Cell 105: 317-333.
29. Mutoh, T., R. Rivera, and J. Chun. 2012. Insights into the pharmacological relevance of lysophospholipid receptors. Br. J. Pharmacol. 165: 829-844.
30. Cristante, E., S. McArthur, C. Mauro, E. Maggioli, I. A. Romero, M. Wylezinska-Arridge, P. O. Couraud, J. Lopez-Tremoleda, H. C. Christian, B. B. Weksler, et al. 2013. Identification of an essential endogenous regulator of blood-brain barrier integrity, and its pathological and therapeutic implications. Proc. Natl. Acad. Sci. USA 110: 832-841.
31. Saab-Aoudé, S., A. M. Bron, C. P. Creuzot-Garcher, L. Bretillon, and N. Acar. 2013. A mouse model of in vivo chemical inhibition of retinal calciumindependent phospholipase A2 (iPLA2). Biochimie 95: 903-911.
32. Devchand, P. R., M. Arita, S. Hong, G. Bannenberg, R.-L. Moussignac, K. Gronert, and C. N. Serhan. 2003. Human ALX receptor regulates neutrophil recruitment in transgenic mice: roles in inflammation and host defense. FASEB J. 17: 652-659.
33. Perretti, M., E. Solito, and L. Parente. 1992. Evidence that endogenous interleukin-1 is involved in leukocyte migration in acute experimental inflammation in rats and mice. Agents Actions 35: 71-78.
34. Damazo, A. S., S. Yona, R. J. Flower, M. Perretti, and S. M. Oliani. 2006. Spatial and temporal profiles for anti-inflammatory gene expression in leukocytes during a resolving model of peritonitis. J. Immunol. 176: 4410-4418.
35. McArthur, S., E. Cristante, M. Paterno, H. Christian, F. Roncaroli, G. E. Gillies, and E. Solito. 2010. Annexin A1: a central player in the anti-inflammatory and neuroprotective role of microglia. J. Immunol. 185: 6317-6328.
36. Tan, C., R. Day, S. Bao, J. Turk, and Q. D. Zhao. 2014. Group VIA phospholipase A2 mediates enhanced macrophage migration in diabetes mellitus by increasing expression of nicotinamide adenine dinucleotide phosphate oxidase 4. Arterioscler. Thromb. Vasc. Biol. 34: 768-778.
37. Vergnolle, N., C. Coméra, and L. Buéno. 1995. Annexin 1 is overexpressed and specifically secreted during experimentally induced colitis in rats. Eur. J. Biochem. 232: 603-610.
38. Elssner, A., M. Duncan, M. Gavrilin, and M. D. Wewers. 2004. A novel P2X7 receptor activator, the human cathelicidin-derived peptide LL37, induces IL-1 beta processing and release. J. Immunol. 172: 4987-4994.
39. Bowdish, D. M. E., D. J. Davidson, D. P. Speert, and R. E. W. Hancock. 2004. The human cationic peptide LL-37 induces activation of the extracellular signalregulated kinase and p38 kinase pathways in primary human monocytes. J. Immunol. 172: 3758-3765.
40. Pupjalis, D., J. Goetsch, D. J. Kottas, V. Gerke, and U. Rescher. 2011. Annexin A1 released from apoptotic cells acts through formyl peptide receptors to dampen inflammatory monocyte activation via JAK/STAT/SOCS signalling. EMBO Mol. Med. 3: 102-114.
41. Soehnlein, O., S. Wantha, S. Simsekyilmaz, Y. Döring, R. T. A. Megens, S. F. Mause, M. Drechsler, R. Smeets, S. Weinandy, F. Schreiber, et al. 2011. Neutrophil-derived cathelicidin protects from neointimal hyperplasia. Sci. Transl. Med. 3: 103ra98.
42. Drechsler, M., R. de Jong, J. Rossaint, J. R. Viola, G. Leoni, J. M. Wang, J. Grommes, R. Hinkel, C. Kupatt, C. Weber, et al. 2015. Annexin A1 counteracts chemokine-induced arterial myeloid cell recruitment. Circ. Res. 116: 827-835.
43. Hayhoe, R. P. G., A. M. Kamal, E. Solito, R. J. Flower, D. Cooper, and M. Perretti. 2006. Annexin 1 and its bioactive peptide inhibit neutrophilendothelium interactions under flow: indication of distinct receptor involvement. Blood 107: 2123-2130.
44. Locati, M., G. Lamorte, W. Luini, M. Introna, S. Bernasconi, A. Mantovani, and S. Sozzani. 1996. Inhibition of monocyte chemotaxis to C-C chemokines by antisense oligonucleotide for cytosolic phospholipase A2. J. Biol. Chem. 271: 6010-6016.
45. Zhou, D., W. Luini, S. Bernasconi, L. Diomede, M. Salmona, A. Mantovani, and S. Sozzani. 1995. Phosphatidic acid and lysophosphatidic acid induce haptotactic migration of human monocytes. J. Biol. Chem. 270: 25549-25556.
46. Park, G. Y., Y. G. Lee, E. Berdyshev, S. Nyenhuis, J. Du, P. Fu, I. A. Gorshkova, Y. Li, S. Chung, M. Karpurapu, et al. 2013. Autotaxin production of lysophosphatidic acid mediates allergic asthmatic inflammation. Am. J. Respir. Crit. Care Med. 188: 928-940.
47. Gorrasi, A., A. Li Santi, G. Amodio, D. Alfano, P. Remondelli, N. Montuori, and P. Ragno. 2014. The urokinase receptor takes control of cell migration by recruiting integrins and FPR1 on the cell surface. PLoS One 9: e86352.
48. Guilluy, C., R. Garcia-Mata, and K. Burridge. 2011. Rho protein crosstalk: another social network? Trends Cell Biol. 21: 718-726.
49. McArthur, S., S. Yazid, H. Christian, R. Sirha, R. Flower, J. Buckingham, and E. Solito. 2009. Annexin A1 regulates hormone exocytosis through a mechanism involving actin reorganization. FASEB J. 23: 4000-4010.
50. Bandeira-Melo, C., A. G. C. Bonavita, B. L. Diaz, P. M. E Silva, V. F. Carvalho, P. J. Jose, R. J. Flower, M. Perretti, and M. A. Martins. 2005. A novel effect for annexin 1-derived peptide ac2-26: reduction of allergic inflammation in the rat. J. Pharmacol. Exp. Ther. 313: 1416-1422.
51. Van Leeuwen, F. N., C. Olivo, S. Grivell, B. N. G. Giepmans, J. G. Collard, and W. H. Moolenaar. 2003. Rac activation by lysophosphatidic acid LPA1 receptors through the guanine nucleotide exchange factor Tiam1. J. Biol. Chem. 278: 400-406.
52. Corminboeuf, O., and X. Leroy. 2015. FPR2/ALXR agonists and the resolution of inflammation. J. Med. Chem. 58: 537-559.