Eosinophils as a novel cell source of prostaglandin D 2: Autocrine role in allergic inflammation

Journal of Immunology

Volumn 187, Issue 12, 2011, Pages 6518-6526

  Luna Gomes, Tatiana ^a   Magalhães, Kelly G ^b   Mesquita Santos, Fabio P ^a,b   Bakker Abreu, Ilka ^a   Samico, Rafaela F ^a   Molinaro, Raphael ^b   Calheiros, Andrea S ^b   Diaz, Bruno L ^a   Bozza, Patrícia T ^b   Weller, Peter F ^c   Bandeira Melo, Christianne ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID; CALCIMYCIN; EOTAXIN; ICOSANOID; LEUKOTRIENE C4; PROSTAGLANDIN D2; PROSTAGLANDIN E RECEPTOR 1; PROSTAGLANDIN E RECEPTOR 2;

ALLERGY; ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; BIOGENESIS; CELL ACTIVATION; CELL DIFFERENTIATION; CELL NUCLEUS MEMBRANE; CELL POPULATION; CONTROLLED STUDY; EOSINOPHIL; EOSINOPHIL COUNT; FEMALE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MAST CELL; MOUSE; NONHUMAN; PARACRINE SIGNALING; PLEURISY; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; AUTOCRINE COMMUNICATION; CATALYSIS; EOSINOPHILS; FEMALE; HEMATOPOIESIS; HUMANS; HYPERSENSITIVITY; INFLAMMATION; INTRACELLULAR FLUID; INTRAMOLECULAR OXIDOREDUCTASES; LIPOCALINS; MALE; MICE; MICE, INBRED BALB C; PARACRINE COMMUNICATION; PROSTAGLANDIN D2; RECEPTORS, IMMUNOLOGIC; RECEPTORS, PROSTAGLANDIN;

EID: 83755195727     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101806     Document Type: Article

References (57)

1. Barrett, N. A., and K. F. Austen. 2009. Innate cells and T helper 2 cell immunity in airway inflammation. Immunity 31: 425-437.
2. Boyce, J. A. 2003. The role of mast cells in asthma. Prostaglandins Leukot. Essent. Fatty Acids 69: 195-205. (Pubitemid 36980620)
3. Ogawa, Y., and W. J. Calhoun. 2006. The role of leukotrienes in airway inflammation. J. Allergy Clin. Immunol. 118: 789-798, quiz 799-800.
4. Lee, T. H., G. Woszczek, and S. P. Farooque. 2009. Leukotriene E4: perspective on the forgotten mediator. J. Allergy Clin. Immunol. 124: 417-421.
5. Kanaoka, Y., and Y. Urade. 2003. Hematopoietic prostaglandin D synthase. Prostaglandins Leukot. Essent. Fatty Acids 69: 163-167. (Pubitemid 36976171)
6. Bandeira-Melo, C., P. T. Bozza, and P. F. Weller. 2002. The cellular biology of eosinophil eicosanoid formation and function. J. Allergy Clin. Immunol. 109: 393-400. (Pubitemid 34234186)
7. Nantel, F., C. Fong, S. Lamontagne, D. H. Wright, A. Giaid, M. Desrosiers, K. M. Metters, G. P. O'Neill, and F. G. Gervais. 2004. Expression of prostaglandin D synthase and the prostaglandin D2 receptors DP and CRTH2 in human nasal mucosa. Prostaglandins Other Lipid Mediat. 73: 87-101. (Pubitemid 38450719)
8. Lewis, R. A., N. A. Soter, P. T. Diamond, K. F. Austen, J. A. Oates, and L. J. Roberts, II. 1982. Prostaglandin D2 generation after activation of rat and human mast cells with anti-IgE. J. Immunol. 129: 1627-1631. (Pubitemid 12031103)
9. O'Sullivan, S., B. Dahlén, S. E. Dahlén, and M. Kumlin. 1996. Increased urinary excretion of the prostaglandin D2 metabolite 9 alpha, 11 beta-prostaglandin F2 after aspirin challenge supports mast cell activation in aspirin-induced airway obstruction. J. Allergy Clin. Immunol. 98: 421-432.
10. Bochenek, G., K. Nagraba, E. Nizankowska, and A. Szczeklik. 2003. A controlled study of 9alpha,11beta-PGF2 (a prostaglandin D2 metabolite) in plasma and urine of patients with bronchial asthma and healthy controls after aspirin challenge. J. Allergy Clin. Immunol. 111: 743-749. (Pubitemid 36470243)
11. Dahlén, S. E., and M. Kumlin. 2004. Monitoring mast cell activation by prostaglandin D2 in vivo. Thorax 59: 453-455. (Pubitemid 38797513)
12. Hamberg, M., and B. B. Fredholm. 1976. Isomerization of prostaglandin H2 into prostaglandin D2 in the presence of serum albumin. Biochim. Biophys. Acta 431: 189-193.
13. Taba, Y., T. Sasaguri, M. Miyagi, T. Abumiya, Y. Miwa, T. Ikeda, and M. Mitsumata. 2000. Fluid shear stress induces lipocalin-type prostaglandin D(2) synthase expression in vascular endothelial cells. Circ. Res. 86: 967-973. (Pubitemid 30324309)
14. Tanaka, K., K. Ogawa, K. Sugamura, M. Nakamura, S. Takano, and K. Nagata. 2000. Cutting edge: differential production of prostaglandin D2 by human helper T cell subsets. J. Immunol. 164: 2277-2280. (Pubitemid 30115452)
15. Shimura, C., T. Satoh, K. Igawa, K. Aritake, Y. Urade, M. Nakamura, and H. Yokozeki. 2010. Dendritic cells express hematopoietic prostaglandin D synthase and function as a source of prostaglandin D2 in the skin. Am. J. Pathol. 176: 227-237.
16. Joo, M., M. Kwon, R. T. Sadikot, P. J. Kingsley, L. J. Marnett, T. S. Blackwell, R. S. Peebles, Jr., Y. Urade, and J. W. Christman. 2007. Induction and function of lipocalin prostaglandin D synthase in host immunity. J. Immunol. 179: 2565-2575.
17. Gandhi, U. H., N. Kaushal, K. C. Ravindra, S. Hegde, S. M. Nelson, V. Narayan, H. Vunta, R. F. Paulson, and K. S. Prabhu. 2011. Selenoprotein- dependent upregulation of hematopoietic prostaglandin D2 synthase in macrophages is mediated through the activation of peroxisome proliferator-activated receptor (PPAR) g. J. Biol. Chem. 286: 27471-27482.
18. Ugajin, T., T. Satoh, T. Kanamori, K. Aritake, Y. Urade, and H. Yokozeki. 2011. FcεRI, but not FcgR, signals induce prostaglandin D2 and E2 production from basophils. Am. J. Pathol. 179: 775-782.
19. Parsons, W. G., III, and L. J. Roberts, II. 1988. Transformation of prostaglandin D2 to isomeric prostaglandin F2 compounds by human eosinophils: a potential mast cell-eosinophil interaction. J. Immunol. 141: 2413-2419.
20. Hyo, S., R. Kawata, K. Kadoyama, N. Eguchi, T. Kubota, H. Takenaka, and Y. Urade. 2007. Expression of prostaglandin D2 synthase in activated eosinophils in nasal polyps. Arch. Otolaryngol. Head Neck Surg. 133: 693-700. (Pubitemid 47080422)
21. Okano, M., T. Fujiwara, Y. Sugata, D. Gotoh, Y. Masaoka, M. Sogo, W. Tanimoto, M. Yamamoto, R. Matsumoto, N. Eguchi, et al. 2006. Presence and characterization of prostaglandin D2-related molecules in nasal mucosa of patients with allergic rhinitis. Am. J. Rhinol. 20: 342-348. (Pubitemid 44083419)
22. Hirai, H., K. Tanaka, O. Yoshie, K. Ogawa, K. Kenmotsu, Y. Takamori, M. Ichimasa, K. Sugamura, M. Nakamura, S. Takano, and K. Nagata. 2001. Prostaglandin D2 selectively induces chemotaxis in T helper type 2 cells, eosinophils, and basophils via seven-transmembrane receptor CRTH2. J. Exp. Med. 193: 255-261. (Pubitemid 32524457)
23. Monneret, G., S. Gravel, M. Diamond, J. Rokach, and W. S. Powell. 2001. Prostaglandin D2 is a potent chemoattractant for human eosinophils that acts via a novel DP receptor. Blood 98: 1942-1948.
24. Kabashima, K., and S. Narumiya. 2003. The DP receptor, allergic inflammation and asthma. Prostaglandins Leukot. Essent. Fatty Acids 69: 187-194. (Pubitemid 36976174)
25. Hardy, C. C., C. Robinson, A. E. Tattersfield, and S. T. Holgate. 1984. The bronchoconstrictor effect of inhaled prostaglandin D2 in normal and asthmatic men. N. Engl. J. Med. 311: 209-213. (Pubitemid 14087661)
26. Patterson, R., K. E. Harris, and P. A. Greenberger. 1980. Effect of prostaglandin D2 and I2 on the airways of rhesus monkeys. J. Allergy Clin. Immunol. 65: 269-273. (Pubitemid 10084858)
27. Hirata, M., A. Kakizuka, M. Aizawa, F. Ushikubi, and S. Narumiya. 1994. Molecular characterization of a mouse prostaglandin D receptor and functional expression of the cloned gene. Proc. Natl. Acad. Sci. USA 91: 11192-11196. (Pubitemid 24349652)
28. Boie, Y., N. Sawyer, D. M. Slipetz, K. M. Metters, and M. Abramovitz. 1995. Molecular cloning and characterization of the human prostanoid DP receptor. J. Biol. Chem. 270: 18910-18916.
29. Nagata, K., H. Hirai, K. Tanaka, K. Ogawa, T. Aso, K. Sugamura, M. Nakamura, and S. Takano. 1999. CRTH2, an orphan receptor of T-helper-2-cells, is expressed on basophils and eosinophils and responds to mast cell-derived factor (s). FEBS Lett. 459: 195-199. (Pubitemid 29475029)
30. Schuligoi, R., E. Sturm, P. Luschnig, V. Konya, S. Philipose, M. Sedej, M.Waldhoer, B. A. Peskar, and A. Heinemann. 2010. CRTH2 and D-type prostanoid receptor antagonists as novel therapeutic agents for inflammatory diseases. Pharmacology 85: 372-382.
31. 2 and T(H)2 inflammation in the pathogenesis of bronchial asthma. Korean J. Intern. Med. 26: 8-18.
32. Mesquita-Santos, F. P., I. Bakker-Abreu, T. Luna-Gomes, P. T. Bozza, B. L. Diaz, and C. Bandeira-Melo. 2011. Co-operative signalling through DP(1) and DP(2) prostanoid receptors is required to enhance leukotriene C(4) synthesis induced by prostaglandin D(2) in eosinophils. Br. J. Pharmacol. 162: 1674-1685.
33. Sandig, H., D. Andrew, A. A. Barnes, I. Sabroe, and J. Pease. 2006. 9α,11b- PGF2 and its stereoisomer PGF2a are novel agonists of the chemoattractant receptor, CRTH2. FEBS Lett. 580: 373-379. (Pubitemid 43089659)
34. Sawyer, N., E. Cauchon, A. Chateauneuf, R. P. Cruz, D. W. Nicholson, K. M. Metters, G. P. O'Neill, and F. G. Gervais. 2002. Molecular pharmacology of the human prostaglandin D2 receptor, CRTH2. Br. J. Pharmacol. 137: 1163-1172. (Pubitemid 36071733)
35. Gazi, L., S. Gyles, J. Rose, S. Lees, C. Allan, L. Xue, R. Jassal, G. Speight, V. Gamble, and R. Pettipher. 2005. Delta12-prostaglandin D2 is a potent and selective CRTH2 receptor agonist and causes activation of human eosinophils and Th2 lymphocytes. Prostaglandins Other Lipid Mediat. 75: 153-167. (Pubitemid 40248385)
36. Monneret, G., H. Li, J. Vasilescu, J. Rokach, and W. S. Powell. 2002. 15-Deoxy-delta 12,14-prostaglandins D2 and J2 are potent activators of human eosinophils. J. Immunol. 168: 3563-3569. (Pubitemid 34250426)
37. Heinemann, A., R. Schuligoi, I. Sabroe, A. Hartnell, and B. A. Peskar. 2003. Delta 12-prostaglandin J2, a plasma metabolite of prostaglandin D2, causes eosinophil mobilization from the bone marrow and primes eosinophils for chemotaxis. J. Immunol. 170: 4752-4758. (Pubitemid 36519984)
38. Böhm, E., G. J. Sturm, I. Weiglhofer, H. Sandig, M. Shichijo, A. McNamee, J. E. Pease, M. Kollroser, B. A. Peskar, and A. Heinemann. 2004. 11-Dehydrothromboxane B2, a stable thromboxane metabolite, is a full agonist of chemoattractant receptor-homologous molecule expressed on TH2 cells (CRTH2) in human eosinophils and basophils. J. Biol. Chem. 279: 7663-7670. (Pubitemid 38294647)
39. Naclerio, R. M., H. L. Meier, A. Kagey-Sobotka, N. F. Adkinson, Jr., D. A. Meyers, P. S. Norman, and L. M. Lichtenstein. 1983. Mediator release after nasal airway challenge with allergen. Am. Rev. Respir. Dis. 128: 597-602. (Pubitemid 13014103)
40. Murray, J. J., A. B. Tonnel, A. R. Brash, L. J. Roberts, II, P. Gosset, R. Workman, A. Capron, and J. A. Oates. 1986. Release of prostaglandin D2 into human airways during acute antigen challenge. N. Engl. J. Med. 315: 800-804. (Pubitemid 16014343)
41. Balzar, S., M. L. Fajt, S. A. Comhair, S. C. Erzurum, E. Bleecker, W. W. Busse, M. Castro, B. Gaston, E. Israel, L. B. Schwartz, et al. 2011. Mast cell phenotype, location, and activation in severe asthma: data from the Severe Asthma Research Program. Am. J. Respir. Crit. Care Med. 183: 299-309.
42. Charlesworth, E. N., A. Kagey-Sobotka, R. P. Schleimer, P. S. Norman, and L. M. Lichtenstein. 1991. Prednisone inhibits the appearance of inflammatory mediators and the influx of eosinophils and basophils associated with the cutaneous late-phase response to allergen. J. Immunol. 146: 671-676.
43. Mesquita-Santos, F. P., A. Vieira-de-Abreu, A. S. Calheiros, I. H. Figueiredo, H. C. Castro-Faria-Neto, P. F. Weller, P. T. Bozza, B. L. Diaz, and C. Bandeira-Melo. 2006. Cutting edge: prostaglandin D2 enhances leukotriene C4 synthesis by eosinophils during allergic inflammation: synergistic in vivo role of endogenous eotaxin. J. Immunol. 176: 1326-1330. (Pubitemid 43134273)
44. Dyer, K. D., J. M. Moser, M. Czapiga, S. J. Siegel, C. M. Percopo, and H. F. Rosenberg. 2008. Functionally competent eosinophils differentiated ex vivo in high purity from normal mouse bone marrow. J. Immunol. 181: 4004-4009.
45. Bandeira-Melo, C., P. F. Weller, and P. T. Bozza. 2011. EicosaCell: an immunofluorescent-based assay to localize newly synthesized eicosanoid lipid mediators at intracellular sites. Methods Mol. Biol. 689: 163-181.
46. Le Mée, S., O. Hennebert, C. Ferrec, E. Wülfert, and R. Morfin. 2008. 7beta-Hydroxy-epiandrosterone-mediated regulation of the prostaglandin synthesis pathway in human peripheral blood monocytes. Steroids 73: 1148-1159.
47. Bozza, P. T., R. C. Melo, and C. Bandeira-Melo. 2007. Leukocyte lipid bodies regulation and function: contribution to allergy and host defense. Pharmacol. Ther. 113: 30-49. (Pubitemid 46001820)
48. Bozza, P. T., J. L. Payne, S. G. Morham, R. Langenbach, O. Smithies, and P. F. Weller. 1996. Leukocyte lipid body formation and eicosanoid generation: cyclooxygenase-independent inhibition by aspirin. Proc. Natl. Acad. Sci. USA 93: 11091-11096. (Pubitemid 26333123)
49. Moreira, L. S., B. Piva, L. B. Gentile, F. P. Mesquita-Santos, H. D'Avila, C. M. Maya-Monteiro, P. T. Bozza, C. Bandeira-Melo, and B. L. Diaz. 2009. Cytosolic phospholipase A2-driven PGE2 synthesis within unsaturated fatty acids-induced lipid bodies of epithelial cells. Biochim. Biophys. Acta 1791: 156-165.
50. Bandeira-Melo, C., M. Phoofolo, and P. F. Weller. 2001. Extranuclear lipid bodies, elicited by CCR3-mediated signaling pathways, are the sites of chemokine-enhanced leukotriene C4 production in eosinophils and basophils. J. Biol. Chem. 276: 22779-22787.
51. Devchand, P. R., H. Keller, J. M. Peters, M. Vazquez, F. J. Gonzalez, and W. Wahli. 1996. The PPARalpha-leukotriene B4 pathway to inflammation control. Nature 384: 39-43.
52. Bhattacharya, M., K. Peri, A. Ribeiro-da-Silva, G. Almazan, H. Shichi, X. Hou, D. R. Varma, and S. Chemtob. 1999. Localization of functional prostaglandin E2 receptors EP3 and EP4 in the nuclear envelope. J. Biol. Chem. 274: 15719-15724.
53. Bandeira-Melo, C., L. J. Woods, M. Phoofolo, and P. F. Weller. 2002. Intracrine cysteinyl leukotriene receptor-mediated signaling of eosinophil vesicular transport-mediated interleukin-4 secretion. J. Exp. Med. 196: 841-850.
54. Vieira-de-Abreu, A., E. F. Assis, G. S. Gomes, H. C. Castro-Faria-Neto, P. F. Weller, C. Bandeira-Melo, and P. T. Bozza. 2005. Allergic challenge-elicited lipid bodies compartmentalize in vivo leukotriene C4 synthesis within eosinophils. Am. J. Respir. Cell Mol. Biol. 33: 254-261. (Pubitemid 41254292)
55. Vieira-de-Abreu, A., A. S. Calheiros, F. P. Mesquita-Santos, E. S. Magalhaes, D. Mourao-Sa, H. C. Castro-Faria-Neto, M. T. Bozza, C. Bandeira-Melo, and P. T. Bozza. 2011. Cross-talk between macrophage migration inhibitory factor and eotaxin in allergic eosinophil activation forms leukotriene C4-synthesizing lipid bodies. Am. J. Respir. Cell Mol. Biol. 44: 509-516.
56. Dyer, K. D., K. E. Garcia-Crespo, K. E. Killoran, and H. F. Rosenberg. 2011. Antigen profiles for the quantitative assessment of eosinophils in mouse tissues by flow cytometry. J. Immunol. Methods 369: 91-97.
57. Philip, G., J. van Adelsberg, T. Loeys, N. Liu, P. Wong, E. Lai, S. B. Dass, and T. F. Reiss. 2009. Clinical studies of the DP1 antagonist laropiprant in asthma and allergic rhinitis. J. Allergy Clin. Immunol. 124: 942-948, e1-e9.