The prostaglandin E2 receptor EP4 is integral to a positive feedback loop for prostaglandin E2 production in human macrophages infected with Mycobacterium tuberculosis

FASEB Journal

Volumn 27, Issue 9, 2013, Pages 3827-3836

  Nishimura, Tomoyasu ^a,b   Zhao, Xiaomin ^a   Gan, Huixian ^a   Koyasu, Shigeo ^b,c   Remold, Heinz G ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c Institute of Physical and Chemical Research   (Japan)

Author keywords

Cyclooxygenase 2; P38 mitogen activated protein kinase; Toll like receptor 2

Indexed keywords

CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; MICROSOMAL PROSTAGLANDIN E SYNTHASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; PROSTAGLANDIN E RECEPTOR 4; PROSTAGLANDIN E SYNTHASE; PROSTAGLANDIN E SYNTHASE 1; PROSTAGLANDIN E2; PROSTAGLANDIN RECEPTOR STIMULATING AGENT; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG;

ANTIGEN RECOGNITION; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUBERCULOSIS; CHEMISTRY; GENETICS; IMMUNOBLOTTING; METABOLISM; MICROBIOLOGY; P38 MITOGEN-ACTIVATED PROTEIN KINASE; PATHOGENICITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

CYCLOOXYGENASE 2; P38 MITOGEN-ACTIVATED PROTEIN KINASE; TOLL-LIKE RECEPTOR 2;

CYCLOOXYGENASE 2; DINOPROSTONE; HUMANS; IMMUNOBLOTTING; MACROPHAGES; MYCOBACTERIUM TUBERCULOSIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, PROSTAGLANDIN E, EP4 SUBTYPE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2;

EID: 84883430746     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-228858     Document Type: Article

References (51)

1. World Health Organization (2012) Global Tuberculosis Report 2012, World Health Organization, Geneva, Switzerland
2. Chen, M., Gan, H., and Remold, H. G. (2006) A mechanism of virulence: virulent Mycobacterium tuberculosis strain H37Rv, but not attenuated H37Ra, causes significant mitochondrial inner membrane disruption in macrophages leading to necrosis. J. Immunol. 176, 3707-3716
3. Park, J. S., Tamayo, M. H., Gonzalez-Juarrero, M., Orme, I. M., and Ordway, D. J. (2006) Virulent clinical isolates of Mycobacterium tuberculosis grow rapidly and induce cellular necrosis but minimal apoptosis in murine macrophages. J. Leukoc. Biol. 79, 80-86
4. Sohn, H., Lee, K. S., Kim, S. Y., Shin, D. M., Shin, S. J., Jo, E. K., Park, J. K., and Kim, H. J. (2009) Induction of cell death in human macrophages by a highly virulent Korean isolate of Mycobacterium tuberculosis and the virulent strain H37Rv. Scand. J. Immunol. 69, 43-50
5. Chen, M., Divangahi, M., Gan, H., Shin, D. S., Hong, S., Lee, D. M., Serhan, C. N., Behar, S. M., and Remold, H. G. (2008) Lipid mediators in innate immunity against tuberculosis: opposing roles of PGE2 and LXA4 in the induction of macrophage death. J. Exp. Med. 205, 2791-2801
6. Sugimoto, Y., and Narumiya, S. (2007) Prostaglandin E receptors. J. Biol. Chem. 282, 11613-11617
7. Legler, D. F., Bruckner, M., Uetz-von Allmen, E., and Krause, P. (2010) Prostaglandin E2 at new glance: novel insights in functional diversity offer therapeutic chances. Int. J. Biochem. Cell Biol. 42, 198-201
8. Tabata, H., Tanaka, S., Sugimoto, Y., Kanki, H., Kaneko, S., and Ichikawa, A. (2002) Possible coupling of prostaglandin E receptor EP(1) to TRP5 expressed in Xenopus laevis oocytes. Biochem. Biophys. Res. Commun. 298, 398-402
9. Namba, T., Sugimoto, Y., Negishi, M., Irie, A., Ushikubi, F., Kakizuka, A., Ito, S., Ichikawa, A., and Narumiya, S. (1993) Alternative splicing of C-terminal tail of prostaglandin E receptor subtype EP3 determines G-protein specificity. Nature 365, 166-170
10. Arakawa, T., Laneuville, O., Miller, C. A., Lakkides, K. M., Wingerd, B. A., DeWitt, D. L., and Smith, W. L. (1996) Prostanoid receptors of murine NIH 3T3 and RAW 264.7 cells. Structure and expression of the murine prostaglandin EP4 receptor gene. J. Biol. Chem. 271, 29569-29575
11. Katsuyama, M., Ikegami, R., Karahashi, H., Amano, F., Sugimoto, Y., and Ichikawa, A. (1998) Characterization of the LPS-stimulated expression of EP2 and EP4 prostaglandin E receptors in mouse macrophage-like cell line, J774.1. Biochem. Biophys. Res. Commun. 251, 727-731
12. Regan, J. W. (2003) EP2 and EP4 prostanoid receptor signaling. Life Sci. 74, 143-153
13. Fujino, H., West, K. A., and Regan, J. W. (2002) Phosphorylation of glycogen synthase kinase-3 and stimulation of T-cell factor signaling following activation of EP2 and EP4 prostanoid receptors by prostaglandin E2. J. Biol. Chem. 277, 2614-2619
14. Vichai, V., Suyarnsesthakorn, C., Pittayakhajonwut, D., Sriklung, K., and Kirtikara, K. (2005) Positive feedback regulation of COX-2 expression by prostaglandin metabolites. Inflamm. Res. 54, 163-172
15. Obermajer, N., Muthuswamy, R., Lesnock, J., Edwards, R. P., and Kalinski, P. (2011) Positive feedback between PGE2 and COX2 redirects the differentiation of human dendritic cells toward stable myeloid-derived suppressor cells. Blood 118, 5498-5505
16. Diaz-Munoz, M. D., Osma-Garcia, I. C., Fresno, M., and Iniguez, M. A. (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
17. Coleman, R. A., Grix, S. P., Head, S. A., Louttit, J. B., Mallett, A., and Sheldrick, R. L. (1994) A novel inhibitory prostanoid receptor in piglet saphenous vein. Prostaglandins 47, 151-168
18. Wilson, R. J., Rhodes, S. A., Wood, R. L., Shield, V. J., Noel, L. S., Gray, D. W., and Giles, H. (2004) Functional pharmacology of human prostanoid EP2 and EP4 receptors. Eur. J. Pharmacol. 501, 49-58
19. Gan, H., Lee, J., Ren, F., Chen, M., Kornfeld, H., and Remold, H. G. (2008) Mycobacterium tuberculosis blocks crosslinking of annexin-1 and apoptotic envelope formation on infected macrophages to maintain virulence. Nat. Immunol. 9, 1189-1197
20. Gan, H., He, X., Duan, L., Mirabile-Levens, E., Kornfeld, H., and Remold, H. G. (2005) Enhancement of antimycobacterial activity of macrophages by stabilization of inner mitochondrial membrane potential. J. Infect. Dis. 191, 1292-1300
21. Shoji, M., Tanabe, N., Mitsui, N., Tanaka, H., Suzuki, N., Takeichi, O., Sugaya, A., and Maeno, M. (2006) Lipopolysaccharide stimulates the production of prostaglandin E2 and the receptor Ep4 in osteoblasts. Life Sci. 78, 2012-2018
22. Ferronato, S., Lira, M. G., Olivato, S., Scuro, A., Veraldi, G. F., Romanelli, M. G., Patuzzo, C., Malerba, G., Pignatti, P. F., and Mazzucco, S. (2011) Upregulated expression of Toll-like receptor 4 in peripheral blood of ischaemic stroke patients correlates with cyclooxygenase 2 expression. Eur. J. Vasc. Endovasc. Surg. 41, 358-363
23. Hiraiwa, H., Sakai, T., Mitsuyama, H., Hamada, T., Yamamoto, R., Omachi, T., Ohno, Y., Nakashima, M., and Ishiguro, N. (2011) Inflammatory effect of advanced glycation end products on human meniscal cells from osteoarthritic knees. Inflamm. Res. 60, 1039-1048
24. Zaslona, Z., Serezani, C. H., Okunishi, K., Aronoff, D. M., and Peters-Golden, M. (2012) Prostaglandin E2 restrains macrophage maturation via E prostanoid receptor 2/protein kinase A signaling. Blood 119, 2358-2367
25. Park, J. Y., Pillinger, M. H., and Abramson, S. B. (2006) Prostaglandin E2 synthesis and secretion: the role of PGE2 synthases. Clin. Immunol. 119, 229-240
26. Diaz-Munoz, M. D., Osma-Garcia, I. C., Cacheiro-Llaguno, C., Fresno, M., and Iniguez, M. A. (2010) Coordinated up-regulation of cyclooxygenase-2 and microsomal prostaglandin E synthase 1 transcription by nuclear factor-κB and early growth response-1 in macrophages. Cell. Signal. 22, 1427-1436
27. Chen, M., Boilard, E., Nigrovic, P. A., Clark, P., Xu, D., Fitzgerald, G. A., Audoly, L. P., and Lee, D. M. (2008) Predominance of cyclooxygenase 1 over cyclooxygenase 2 in the generation of proinflammatory prostaglandins in autoantibody-driven K/BxN serum-transfer arthritis. Arthritis Rheum. 58, 1354-1365
28. Aronoff, D. M., Canetti, C., and Peters-Golden, M. (2004) Prostaglandin E2 inhibits alveolar macrophage phagocytosis through an E-prostanoid 2 receptor-mediated increase in intracellular cyclic AMP. J. Immunol. 173, 559-565
29. Medeiros, A. I., Serezani, C. H., Lee, S. P., and Peters-Golden, M. (2009) Efferocytosis impairs pulmonary macrophage and lung antibacterial function via PGE2/EP2 signaling. J. Exp. Med. 206, 61-68
30. Serezani, C. H., Kane, S., Medeiros, A. I., Cornett, A. M., Kim, S. H., Marques, M. M., Lee, S. P., Lewis, C., Bourdonnay, E., Ballinger, M. N., White, E. S., and Peters-Golden, M. (2012) PTEN directly activates the actin depolymerization factor cofilin- 1 during PGE2-mediated inhibition of phagocytosis of fungi. Sci. Signal. 5, ra12
31. Guan, Z., Baier, L. D., and Morrison, A. R. (1997) p38 mitogenactivated protein kinase down-regulates nitric oxide and upregulates prostaglandin E2 biosynthesis stimulated by interleukin- 1β. J. Biol. Chem. 272, 8083-8089
32. Oikawa, A., Kobayashi, M., Okamatsu, Y., Shinki, T., Kamijo, R., Yamamoto, M., and Hasegawa, K. (2007) Mitogen-activated protein kinases mediate interleukin-1α-induced receptor activator of nuclear factor-B ligand expression in human periodontal ligament cells. J. Periodontal Res. 42, 367-376
33. Bansal, K., Narayana, Y., Patil, S. A., and Balaji, K. N. (2009) M. bovis BCG induced expression of COX-2 involves nitric oxidedependent and -independent signaling pathways. J. Leukoc. Biol. 85, 804-816
34. Kleinnijenhuis, J., Oosting, M., Joosten, L. A., Netea, M. G., and Van Crevel, R. (2011) Innate immune recognition of Mycobacterium tuberculosis. Clin. Dev. Immunol. 2011:405310
35. Stenger, S., and Modlin, R. L. (2002) Control of Mycobacterium tuberculosis through mammalian Toll-like receptors. Curr. Opin. Immunol. 14, 452-457
36. Krutzik, S. R., and Modlin, R. L. (2004) The role of Toll-like receptors in combating mycobacteria. Semin. Immunol. 16, 35-41
37. Matsumoto, H., Naraba, H., Murakami, M., Kudo, I., Yamaki, K., Ueno, A., and Oh-ishi, S. (1997) Concordant induction of prostaglandin E2 synthase with cyclooxygenase-2 leads to preferred production of prostaglandin E2 over thromboxane and prostaglandin D2 in lipopolysaccharide-stimulated rat peritoneal macrophages. Biochem. Biophys. Res. Commun. 230, 110-114
38. Iona, E., Pardini, M., Gagliardi, M. C., Colone, M., Stringaro, A. R., Teloni, R., Brunori, L., Nisini, R., Fattorini, L., and Giannoni, F. (2012) Infection of human THP-1 cells with dormant Mycobacterium tuberculosis. Microbes Infect. 14, 959-967
39. Martin, C. J., Booty, M. G., Rosebrock, T. R., Nunes-Alves, C., Desjardins, D. M., Keren, I., Fortune, S. M., Remold, H. G., and Behar, S. M. (2012) Efferocytosis is an innate antibacterial mechanism. Cell Host Microbe 12, 289-300
40. Inada, M., Matsumoto, C., Uematsu, S., Akira, S., and Miyaura, C. (2006) Membrane-bound prostaglandin E synthase-1-mediated prostaglandin E2 production by osteoblast plays a critical role in lipopolysaccharide-induced bone loss associated with inflammation. J. Immunol. 177, 1879-1885
41. Stichtenoth, D. O., Thoren, S., Bian, H., Peters-Golden, M., Jakobsson, P. J., and Crofford, L. J. (2001) Microsomal prostaglandin E synthase is regulated by proinflammatory cytokines and glucocorticoids in primary rheumatoid synovial cells. J. Immunol. 167, 469-474
42. Quesniaux, V., Fremond, C., Jacobs, M., Parida, S., Nicolle, D., Yeremeev, V., Bihl, F., Erard, F., Botha, T., Drennan, M., Soler, M. N., Le Bert, M., Schnyder, B., and Ryffel, B. (2004) Toll-like receptor pathways in the immune responses to mycobacteria. Microbes Infect. 6, 946-959
43. Drage, M. G., Pecora, N. D., Hise, A. G., Febbraio, M., Silverstein, R. L., Golenbock, D. T., Boom, W. H., and Harding, C. V. (2009) TLR2 and its co-receptors determine responses of macrophages and dendritic cells to lipoproteins of Mycobacterium tuberculosis. Cell. Immunol. 258, 29-37
44. Basu, S., Pathak, S. K., Banerjee, A., Pathak, S., Bhattacharyya, A., Yang, Z., Talarico, S., Kundu, M., and Basu, J. (2007) Execution of macrophage apoptosis by PE-PGRS33 of Mycobacterium tuberculosis is mediated by Toll-like receptor 2-dependent release of tumor necrosis factor-α. J. Biol. Chem. 282, 1039-1050
45. Thuong, N. T., Hawn, T. R., Thwaites, G. E., Chau, T. T., Lan, N. T., Quy, H. T., Hieu, N. T., Aderem, A., Hien, T. T., Farrar, J. J., and Dunstan, S. J. (2007) A polymorphism in human TLR2 is associated with increased susceptibility to tuberculous meningitis. Genes Immun. 8, 422-428
46. Caws, M., Thwaites, G., Dunstan, S., Hawn, T. R., Lan, N. T., Thuong, N. T., Stepniewska, K., Huyen, M. N., Bang, N. D., Loc, T. H., Gagneux, S., van Soolingen, D., Kremer, K., van der Sande, M., Small, P., Anh, P. T., Chinh, N. T., Quy, H. T., Duyen, N. T., Tho, D. Q., Hieu, N. T., Torok, E., Hien, T. T., Dung, N. H., Nhu, N. T., Duy, P. M., van Vinh Chau, N., and Farrar, J. (2008) The influence of host and bacterial genotype on the development of disseminated disease with Mycobacterium tuberculosis. PLoS Pathog. 4, e1000034
47. Rand, L., Green, J. A., Saraiva, L., Friedland, J. S., and Elkington, P. T. (2009) Matrix metalloproteinase-1 is regulated in tuberculosis by a p38 MAPK-dependent, p-aminosalicylic acidsensitive signaling cascade. J. Immunol. 182, 5865-5872
48. Faour, W. H., He, Y., He, Q. W., de Ladurantaye, M., Quintero, M., Mancini, A., and Di Battista, J. A. (2001) Prostaglandin E2 regulates the level and stability of cyclooxygenase-2mRNAthrough activation of p38 mitogen-activated protein kinase in interleukin-1 α-treated human synovial fibroblasts. J. Biol. Chem. 276, 31720-31731
49. Khan, K. M., Kothari, P., Du, B., Dannenberg, A. J., and Falcone, D. J. (2012) Matrix metalloproteinase-dependent microsomal prostaglandin E synthase-1 expression in macrophages: role of TNF-α and the EP4 prostanoid receptor. J. Immunol. 188, 1970-1980
50. Sugimoto, Y., Narumiya, S., and Ichikawa, A. (2000) Distribution and function of prostanoid receptors: studies from knockout mice. Prog. Lipid Res. 39, 289-314
51. Forstermann, U., and Neufang, B. (1983) Elimination from the circulation of cats of 6-keto-prostaglandin E1 compared with prostaglandins E2 and I2. J. Pharm. Pharmacol. 35, 724-728