Cyclooxygenase-2 deficiency in macrophages leads to defective p110γ PI3K signaling and impairs cell, adhesion and migration

Journal of Immunology

Volumn 191, Issue 1, 2013, Pages 395-406

  Díaz Muñoz, Manuel D ^a,b   Osma García, Inés C ^a   Íñiguez, Miguel A ^a   Fresno, Manuel ^a  

^a not available

^b BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CHEMOKINE RECEPTOR; CYCLOOXYGENASE 2; FIBRONECTIN; INTERCELLULAR ADHESION MOLECULE 1; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; PAXILLIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN CDC42; PROTEIN KINASE B; PROTEIN P110; PROTEIN P110 GAMMA; RAC1 PROTEIN; RANTES; THIOGLYCOLIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COX 2 GENE; ENZYME ACTIVE SITE; ENZYME PHOSPHORYLATION; FOCAL ADHESION; GENE; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE ADHERENCE; LYMPH NODE; MACROPHAGE; MACROPHAGE MIGRATION; MESOTHELIUM; MOUSE; NONHUMAN; PERITONEAL CAVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 84879640742     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202002     Document Type: Article

References (78)

1. Luster, A. D., R. Alon, and U. H. von Andrian. 2005. Immune cell migration in inflammation: present and future therapeutic targets. Nat. Immunol. 6: 1182-1190. (Pubitemid 43045626)
2. Ley, K., C. Laudanna, M. I. Cybulsky, and S. Nourshargh. 2007. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7: 678-689. (Pubitemid 47327397)
3. Huttenlocher, A., and M. C. Poznansky. 2008. Reverse leukocyte migration can be attractive or repulsive. Trends Cell Biol. 18: 298-306.
4. Massberg, S., P. Schaerli, I. Knezevic-Maramica, M. Köllnberger, N. Tubo, E. A. Moseman, I. V. Huff, T. Junt, A. J. Wagers, I. B. Mazo, and U. H. von Andrian. 2007. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131: 994-1008. (Pubitemid 350138089)
5. Randolph, G. J. 2008. Emigration of monocyte-derived cells to lymph nodes during resolution of inflammation and its failure in atherosclerosis. Curr. Opin. Lipidol. 19: 462-468.
6. Bertho, N., H. Adamski, L. Toujas, M. Debove, J. Davoust, and V. Quillien. 2005. Efficient migration of dendritic cells toward lymph node chemokines and induction of T(H)1 responses require maturation stimulus and apoptotic cell interaction. Blood 106: 1734-1741. (Pubitemid 41208588)
7. Allan, R. S., J. Waithman, S. Bedoui, C. M. Jones, J. A. Villadangos, Y. Zhan, A. M. Lew, K. Shortman, W. R. Heath, and F. R. Carbone. 2006. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 25: 153-162. (Pubitemid 44066832)
8. Chtanova, T., M. Schaeffer, S. J. Han, G. G. van Dooren, M. Nollmann, P. Herzmark, S. W. Chan, H. Satija, K. Camfield, H. Aaron, et al. 2008. Dynamics of neutrophil migration in lymph nodes during infection. Immunity 29: 487-496.
9. Tabas, I. 2010. Macrophage death and defective inflammation resolution in atherosclerosis. Nat. Rev. Immunol. 10: 36-46.
10. Bellingan, G. J., H. Caldwell, S. E. Howie, I. Dransfield, and C. Haslett. 1996. In vivo fate of the inflammatory macrophage during the resolution of inflammation: inflammatory macrophages do not die locally, but emigrate to the draining lymph nodes. J. Immunol. 157: 2577-2585. (Pubitemid 126450472)
11. Broche, F., and J. M. Tellado. 2001. Defense mechanisms of the peritoneal cavity. Curr. Opin. Crit. Care 7: 105-116. (Pubitemid 32411399)
12. Harris, S. G., J. Padilla, L. Koumas, D. Ray, and R. P. Phipps. 2002. Prostaglandins as modulators of immunity. Trends Immunol. 23: 144-150. (Pubitemid 34178297)
13. Wang, D., and R. N. Dubois. 2006. Prostaglandins and cancer. Gut 55: 115-122. (Pubitemid 41820645)
14. Iñiguez, M. A., A. Rodríguez, O. V. Volpert, M. Fresno, and J. M. Redondo. 2003. Cyclooxygenase-2: a therapeutic target in angiogenesis. Trends Mol. Med. 9: 73-78.
15. Wymann, M. P., and R. Schneiter. 2008. Lipid signalling in disease. Nat. Rev. Mol. Cell Biol. 9: 162-176. (Pubitemid 351158917)
16. Blanco, J. C., C. Contursi, C. A. Salkowski, D. L. DeWitt, K. Ozato, and S. N. Vogel. 2000. Interferon regulatory factor (IRF)-1 and IRF-2 regulate interferon gamma-dependent cyclooxygenase 2 expression. J. Exp. Med. 191: 2131-2144. (Pubitemid 30416360)
17. Crofford, L. J. 1997. COX-1 and COX-2 tissue expression: implications and predictions. J. Rheumatol. Suppl. 49: 15-19.
18. Vila-del Sol, V., and M. Fresno. 2005. Involvement of TNF and NF-kappa B in the transcriptional control of cyclooxygenase-2 expression by IFN-gamma in macrophages. J. Immunol. 174: 2825-2833. (Pubitemid 40279699)
19. Ryan, E. P., C. M. Malboeuf, M. Bernard, R. C. Rose, and R. P. Phipps. 2006. Cyclooxygenase-2 inhibition attenuates antibody responses against human papillomavirus-like particles. J. Immunol. 177: 7811-7819. (Pubitemid 44846297)
20. Carey, M. A., J. A. Bradbury, J. M. Seubert, R. Langenbach, D. C. Zeldin, and D. R. Germolec. 2005. Contrasting effects of cyclooxygenase-1 (COX-1) and COX-2 deficiency on the host response to influenza Aviral infection. J. Immunol. 175: 6878-6884. (Pubitemid 41598933)
21. Sharma, S., S. C. Yang, L. Zhu, K. Reckamp, B. Gardner, F. Baratelli, M. Huang, R. K. Batra, and S. M. Dubinett. 2005. Tumor cyclooxygenase-2/ prostaglandin E2-dependent promotion of FOXP3 expression and CD4+ CD25+ T regulatory cell activities in lung cancer. Cancer Res. 65: 5211-5220. (Pubitemid 40827331)
22. Sharma, S., L. Zhu, S. C. Yang, L. Zhang, J. Lin, S. Hillinger, B. Gardner, K. Reckamp, R. M. Strieter, M. Huang, et al. 2005. Cyclooxygenase 2 inhibition promotes IFN-gamma-dependent enhancement of antitumor responses. J. Immunol. 175: 813-819. (Pubitemid 41094963)
23. Gosset, P., M. Pichavant, C. Faveeuw, F. Bureau, A. B. Tonnel, and F. Trottein. 2005. Prostaglandin D2 affects the differentiation and functions of human dendritic cells: impact on the T cell response. Eur. J. Immunol. 35: 1491-1500. (Pubitemid 40691431)
24. Wallace, A. E., K. J. Sales, R. D. Catalano, R. A. Anderson, A. R. Williams, M. R. Wilson, J. Schwarze, H. Wang, A. G. Rossi, and H. N. Jabbour. 2009. Prostaglandin F2alpha-F-prostanoid receptor signaling promotes neutrophil chemotaxis via chemokine (C-X-C motif) ligand 1 in endometrial adenocarcinoma. Cancer Res. 69: 5726-5733.
25. Hoggatt, J., P. Singh, J. Sampath, and L. M. Pelus. 2009. Prostaglandin E2 enhances hematopoietic stem cell homing, survival, and proliferation. Blood 113: 5444-5455.
26. Panzer, U., and M. Uguccioni. 2004. Prostaglandin E2 modulates the functional responsiveness of human monocytes to chemokines. Eur. J. Immunol. 34: 3682-3689. (Pubitemid 40012186)
27. Luft, T., M. Jefford, P. Luetjens, T. Toy, H. Hochrein, K. A. Masterman, C. Maliszewski, K. Shortman, J. Cebon, and E. Maraskovsky. 2002. Functionally distinct dendritic cell (DC) populations induced by physiologic stimuli: prostaglandin E(2) regulates the migratory capacity of specific DC subsets. Blood 100: 1362-1372. (Pubitemid 34864293)
28. Côté, S. C., S. Pasvanis, S. Bounou, and N. Dumais. 2009. CCR7-specific migration to CCL19 and CCL21 is induced by PGE(2) stimulation in human monocytes: Involvement of EP(2)/EP(4) receptors activation. Mol. Immunol. 46: 2682-2693.
29. Yen, J. H., T. Khayrullina, and D. Ganea. 2008. PGE2-induced metalloproteinase-9 is essential for dendritic cell migration. Blood 111: 260-270.
30. Imhof, B. A., and M. Aurrand-Lions. 2004. Adhesion mechanisms regulating the migration of monocytes. Nat. Rev. Immunol. 4: 432-444. (Pubitemid 38745555)
31. Scandella, E., Y. Men, D. F. Legler, S. Gillessen, L. Prikler, B. Ludewig, and M. Groettrup. 2004. CCL19/CCL21-triggered signal transduction and migration of dendritic cells requires prostaglandin E2. Blood 103: 1595-1601. (Pubitemid 38268947)
32. Matsuoka, T., and S. Narumiya. 2007. Prostaglandin receptor signaling in disease. Scientific World Journal 7: 1329-1347. (Pubitemid 47435437)
33. Vicente-Manzanares, M., D. Sancho, M. Yáñez-Mó, and F. Sánchez-Madrid. 2002. The leukocyte cytoskeleton in cell migration and immune interactions. Int. Rev. Cytol. 216: 233-289. (Pubitemid 34552690)
34. Worthylake, R. A., and K. Burridge. 2001. Leukocyte transendothelial migration: orchestrating the underlying molecular machinery. Curr. Opin. Cell Biol. 13: 569-577. (Pubitemid 32817015)
35. Pankov, R., Y. Endo, S. Even-Ram, M. Araki, K. Clark, E. Cukierman, K. Matsumoto, and K. M. Yamada. 2005. A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170: 793-802. (Pubitemid 41242111)
36. van Helden, S. F., D. J. Krooshoop, K. C. Broers, R. A. Raymakers, C. G. Figdor, and F. N. van Leeuwen. 2006. A critical role for prostaglandin E2 in podosome dissolution and induction of high-speed migration during dendritic cell maturation. J. Immunol. 177: 1567-1574.
37. van Helden, S. F., M. M. Oud, B. Joosten, N. Peterse, C. G. Figdor, and F. N. van Leeuwen. 2008. PGE2-mediated podosome loss in dendritic cells is dependent on actomyosin contraction downstream of the RhoA-Rho-kinase axis. J. Cell Sci. 121: 1096-1106. (Pubitemid 351639428)
38. Cantrell, D. A. 2001. Phosphoinositide 3-kinase signalling pathways. J. Cell Sci. 114: 1439-1445. (Pubitemid 32427831)
39. Weiss-Haljiti, C., C. Pasquali, H. Ji, C. Gillieron, C. Chabert, M. L. Curchod, E. Hirsch, A. J. Ridley, R. Hooft van Huijsduijnen, M. Camps, and C. Rommel. 2004. Involvement of phosphoinositide 3-kinase gamma, Rac, and PAK signaling in chemokine-induced macrophage migration. J. Biol. Chem. 279: 43273-43284. (Pubitemid 39372223)
40. Liu, L., K. D. Puri, J. M. Penninger, and P. Kubes. 2007. Leukocyte PI3Kgamma and PI3Kdelta have temporally distinct roles for leukocyte recruitment in vivo. Blood 110: 1191-1198. (Pubitemid 47281416)
41. Hirsch, E., V. L. Katanaev, C. Garlanda, O. Azzolino, L. Pirola, L. Silengo, S. Sozzani, A. Mantovani, F. Altruda, and M. P. Wymann. 2000. Central role for G protein-coupled phosphoinositide 3-kinase gamma in inflammation. Science 287: 1049-1053.
42. Chang, J. D., G. K. Sukhova, P. Libby, E. Schvartz, A. H. Lichtenstein, S. J. Field, C. Kennedy, S. Madhavarapu, J. Luo, D.Wu, and L. C. Cantley. 2007. Deletion of the phosphoinositide 3-kinase p110gamma gene attenuates murine atherosclerosis. Proc. Natl. Acad. Sci. USA 104: 8077-8082. (Pubitemid 47185878)
43. Díaz-Muñoz, M. D., I. C. Osma-García, C. Cacheiro-Llaguno, M. Fresno, and M. A. Iñiguez. 2010. Coordinated up-regulation of cyclooxygenase-2 and microsomal prostaglandin E synthase 1 transcription by nuclear factor kappa B and early growth response-1 in macrophages. Cell. Signal. 22: 1427-1436.
44. Hume, D. A. 2008. Macrophages as APC and the dendritic cell myth. J. Immunol. 181: 5829-5835.
45. Bellingan, G. J., P. Xu, H. Cooksley, H. Cauldwell, A. Shock, S. Bottoms, C. Haslett, S. E. Mutsaers, and G. J. Laurent. 2002. Adhesion molecule-dependent mechanisms regulate the rate of macrophage clearance during the resolution of peritoneal inflammation. J. Exp. Med. 196: 1515-1521. (Pubitemid 35424945)
46. Pixley, F. J. 2012. Macrophage Migration and Its Regulation by CSF-1. Int. J. Cell Biol. 2012: 501962.
47. Zaidel-Bar, R., R. Milo, Z. Kam, and B. Geiger. 2007. A paxillin tyrosine phosphorylation switch regulates the assembly and form of cell-matrix adhesions. J. Cell Sci. 120: 137-148. (Pubitemid 46206656)
48. Li, S., P. Butler, Y. Wang, Y. Hu, D. C. Han, S. Usami, J. L. Guan, and S. Chien. 2002. The role of the dynamics of focal adhesion kinase in the mechanotaxis of endothelial cells. Proc. Natl. Acad. Sci. USA 99: 3546-3551. (Pubitemid 34252144)
49. Thomas, P. E., M. Peters-Golden, E. S. White, V. J. Thannickal, and B. B. Moore. 2007. PGE(2) inhibition of TGF-beta1-induced myofibroblast differentiation is Smad-independent but involves cell shape and adhesion-dependent signaling. Am. J. Physiol. Lung Cell. Mol. Physiol. 293: L417-L428. (Pubitemid 47205022)
50. Williams, L. M., and A. J. Ridley. 2000. Lipopolysaccharide induces actin reorganization and tyrosine phosphorylation of Pyk2 and paxillin in monocytes and macrophages. J. Immunol. 164: 2028-2036. (Pubitemid 30108760)
51. Hazeki, K., N. Masuda, K. Funami, N. Sukenobu, M. Matsumoto, S. Akira, K. Takeda, T. Seya, and O. Hazeki. 2003. Toll-like receptor-mediated tyrosine phosphorylation of paxillin via MyD88-dependent and -independent pathways. Eur. J. Immunol. 33: 740-747. (Pubitemid 36367677)
52. Choi, S. H., S. Aid, U. Choi, and F. Bosetti. 2010. Cyclooxygenases-1 and -2 differentially modulate leukocyte recruitment into the inflamed brain. Pharmacogenomics J. 10: 448-457.
53. Dinchuk, J. E., B. D. Car, R. J. Focht, J. J. Johnston, B. D. Jaffee, M. B. Covington, N. R. Contel, V. M. Eng, R. J. Collins, P. M. Czerniak, et al. 1995. Renal abnormalities and an altered inflammatory response in mice lacking cyclooxygenase II. Nature 378: 406-409.
54. Kamei, D., K. Yamakawa, Y. Takegoshi, M. Mikami-Nakanishi, Y. Nakatani, S. Oh-Ishi, H. Yasui, Y. Azuma, N. Hirasawa, K. Ohuchi, et al. 2004. Reduced pain hypersensitivity and inflammation in mice lacking microsomal prostaglandin e synthase-1. J. Biol. Chem. 279: 33684-33695. (Pubitemid 39063018)
55. Galli, S. J., N. Borregaard, and T. A. Wynn. 2011. Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat. Immunol. 12: 1035-1044.
56. Gordon, S., and P. R. Taylor. 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5: 953-964. (Pubitemid 41746764)
57. -/- mice during disease regression. J. Clin. Invest. 121: 2025-2036.
58. van Gils, J. M., M. C. Derby, L. R. Fernandes, B. Ramkhelawon, T. D. Ray, K. J. Rayner, S. Parathath, E. Distel, J. L. Feig, J. I. Alvarez-Leite, et al. 2012. The neuroimmune guidance cue netrin-1 promotes atherosclerosis by inhibiting the emigration of macrophages from plaques. Nat. Immunol. 13: 136-143.
59. Zaidel-Bar, R., S. Itzkovitz, A. Ma'ayan, R. Iyengar, and B. Geiger. 2007. Functional atlas of the integrin adhesome. Nat. Cell Biol. 9: 858-867. (Pubitemid 47190436)
60. Alique, M., L. Calleros, A. Luengo, M. Griera, M. A. Iñiguez, C. Punzón, M. Fresno, M. Rodríguez-Puyol, and D. Rodríguez- Puyol. 2011. Changes in extracellular matrix composition regulate cyclooxygenase-2 expression in human mesangial cells. Am. J. Physiol. Cell Physiol. 300: C907-C918.
61. Calle, Y., S. Burns, A. J. Thrasher, and G. E. Jones. 2006. The leukocyte podosome. Eur. J. Cell Biol. 85: 151-157.
62. Tomar, A., and D. D. Schlaepfer. 2009. Focal adhesion kinase: switching between GAPs and GEFs in the regulation of cell motility. Curr. Opin. Cell Biol. 21: 676-683.
63. McLean, G. W., N. O. Carragher, E. Avizienyte, J. Evans, V. G. Brunton, and M. C. Frame. 2005. The role of focal-adhesion kinase in cancer - a new therapeutic opportunity. Nat. Rev. Cancer 5: 505-515. (Pubitemid 40942827)
64. Choi, C. K., M. Sukhthankar, C. H. Kim, S. H. Lee, A. English, K. D. Kihm, and S. J. Baek. 2010. Cell adhesion property affected by cyclooxygenase and lipoxygenase: Opto-electric approach. Biochem. Biophys. Res. Commun. 391: 1385-1389.
65. Bai, X. M., W. Zhang, N. B. Liu, H. Jiang, K. X. Lou, T. Peng, J. Ma, L. Zhang, H. Zhang, and J. Leng. 2009. Focal adhesion kinase: important to prostaglandin E2-mediated adhesion, migration and invasion in hepatocellular carcinoma cells. Oncol. Rep. 21: 129-136.
66. Meng, F., and C. A. Lowell. 1998. A beta 1 integrin signaling pathway involving Src-family kinases, Cbl and PI-3 kinase is required for macrophage spreading and migration. EMBO J. 17: 4391-4403. (Pubitemid 28362629)
67. Wong, M. M., and E. N. Fish. 2003. Chemokines: attractive mediators of the immune response. Semin. Immunol. 15: 5-14. (Pubitemid 36092174)
68. Alfranca, A., M. A. Iñiguez, M. Fresno, and J. M. Redondo. 2006. Prostanoid signal transduction and gene expression in the endothelium: role in cardiovascular diseases. Cardiovasc. Res. 70: 446-456.
69. Welch, H. C., W. J. Coadwell, L. R. Stephens, and P. T. Hawkins. 2003. Phosphoinositide 3-kinase-dependent activation of Rac. FEBS Lett. 546: 93-97. (Pubitemid 36782287)
70. Beemiller, P., Y. Zhang, S. Mohan, E. Levinsohn, I. Gaeta, A. D. Hoppe, and J. A. Swanson. 2010. A Cdc42 activation cycle coordinated by PI 3-kinase during Fc receptor-mediated phagocytosis. Mol. Biol. Cell 21: 470-480.
71. Larson, Y., J. Liu, P. D. Stevens, X. Li, J. Li, B. M. Evers, and T. Gao. 2010. Tuberous sclerosis complex 2 (TSC2) regulates cell migration and polarity through activation of CDC42 and RAC1. J. Biol. Chem. 285: 24987-24998.
72. Tybulewicz, V. L., and R. B. Henderson. 2009. Rho family GTPases and their regulators in lymphocytes. Nat. Rev. Immunol. 9: 630-644.
73. Vadas, O., J. E. Burke, X. Zhang, A. Berndt, and R. L.Williams. 2011. Structural basis for activation and inhibition of class I phosphoinositide 3-kinases. Sci. Signal. 4: re2.
74. Díaz-Muñoz, M. D., I. C. Osma-García, M. Fresno, and M. A. Iñiguez. 2012. Involvement of PGE2 and the cAMP signalling pathway in the up-regulation of COX-2 and mPGES-1 expression in LPS-activated macrophages. Biochem. J. 443: 451-461.
75. Babaev, V. R., J. D. Chew, L. Ding, S. Davis, M. D. Breyer, R. M. Breyer, J. A. Oates, S. Fazio, and M. F. Linton. 2008. Macrophage EP4 deficiency increases apoptosis and suppresses early atherosclerosis. Cell Metab. 8: 492-501.
76. Tajima, T., T. Murata, K. Aritake, Y. Urade, H. Hirai, M. Nakamura, H. Ozaki, and M. Hori. 2008. Lipopolysaccharide induces macrophage migration via prostaglandin D(2) and prostaglandin E(2). J. Pharmacol. Exp. Ther. 326: 493-501.
77. Feig, J. E., I. Pineda-Torra, M. Sanson, M. N. Bradley, Y. Vengrenyuk, D. Bogunovic, E. L. Gautier, D. Rubinstein, C. Hong, J. Liu, et al. 2010. LXR promotes the maximal egress of monocyte-derived cells from mouse aortic plaques during atherosclerosis regression. J. Clin. Invest. 120: 4415-4424.
78. Llodrá, J., V. Angeli, J. Liu, E. Trogan, E. A. Fisher, and G. J. Randolph. 2004. Emigration of monocyte-derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques. Proc. Natl. Acad. Sci. USA 101: 11779-11784. Investigación en Enfermedades Cardiovasculares Tropicales Networks of the Instituto de Salud Carlos III