Prostaglandin I2 signaling and inhibition of group 2 innate lymphoid cell responses

American Journal of Respiratory and Critical Care Medicine

Volumn 193, Issue 1, 2016, Pages 31-42

  Zhou, Weisong ^a   Toki, Shinji ^a   Zhang, Jian ^a   Goleniewksa, Kasia ^a   Newcomb, Dawn C ^a   Cephus, Jacqueline Y ^a   Dulek, Daniel E ^b   Bloodworth, Melissa H ^a   Stier, Matthew T ^a   Polosuhkin, Vasiliy ^a   Gangula, Rama D ^a   Mallal, Simon A ^a   Broide, David H ^c   Peebles, R Stokes ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Allergy; Asthma; ILC2; PGI2

Indexed keywords

ALTERNARIA ALTERNATA EXTRACT; CD45 ANTIGEN; CICAPROST; CYCLIC AMP DEPENDENT PROTEIN KINASE; FUNGAL EXTRACT; INTERLEUKIN 13; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 33; INTERLEUKIN 5; INTERLEUKIN 7 RECEPTOR; PROSTACYCLIN; PROSTACYCLIN RECEPTOR; UNCLASSIFIED DRUG;

AIRWAY; AIRWAY MUCUS; ALLERGIC ASTHMA; ALTERNARIA ALTERNATA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; DISEASE EXACERBATION; DISEASE SEVERITY; DRUG EFFICACY; DRUG MECHANISM; EOSINOPHIL; FLOW CYTOMETRY; GROUP 2 INNATE LYMPHOID CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; INTRACELLULAR SIGNALING; LYMPHOID CELL; MOUSE; MUCUS; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN RELEASE; PROTEIN EXPRESSION; WILD TYPE MOUSE; ALTERNARIA; ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; CYTOLOGY; DRUG EFFECTS; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; LYMPHOCYTE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ALTERNARIA; ANIMALS; EPOPROSTENOL; HUMANS; IN VITRO TECHNIQUES; INTERLEUKIN-13; INTERLEUKIN-33; INTERLEUKIN-5; LUNG; LYMPHOCYTES; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; SIGNAL TRANSDUCTION;

EID: 84988878696     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201410-1793OC     Document Type: Article

References (50)

1. Eder W, Ege MJ, von Mutius E. The asthma epidemic. N Engl J Med 2006;355:2226-2235.
2. Jarvis D, Burney P. ABC of allergies: the epidemiology of allergic disease. BMJ 1998;316:607-610.
3. Marquis A, Strippoli MP, Spycher BD, Rebholz CE, von der Weid NX, Kuehni CE; Swiss Pediatric Oncology Group. Paracetamol, nonsteroidal anti-inflammatory drugs, and risk of asthma in adult survivors of childhood cancer. J Allergy Clin Immunol 2011;127:270-272.
4. Shaheen SO, Newson RB, Henderson AJ, Headley JE, Stratton FD, Jones RW, Strachan DP; ALSPAC Study Team. Prenatal paracetamol exposure and risk of asthma and elevated immunoglobulin E in childhood. Clin Exp Allergy 2005;35:18-25.
5. Thomsen SF, Kyvik KO, Skadhauge LR, Steffensen I, Backer V. Regular use of non-steroidal anti-inflammatory drugs increases the risk of adult-onset asthma: a population-based follow-up study. Clin Respir J 2009;3:82-84.
6. Carey MA, Germolec DR, Bradbury JA, Gooch RA, Moorman MP, Flake GP, Langenbach R, Zeldin DC. Accentuated T helper type 2 airway response after allergen challenge in cyclooxygenase-1-/- but not cyclooxygenase-2-/- mice. Am J Respir Crit Care Med 2003;167: 1509-1515.
7. Gavett SH, Madison SL, Chulada PC, Scarborough PE, Qu W, Boyle JE, Tiano HF, Lee CA, Langenbach R, Roggli VL, et al. Allergic lung responses are increased in prostaglandin H synthase-deficient mice. J Clin Invest 1999;104:721-732.
8. Hashimoto K, Sheller JR, Morrow JD, Collins RD, Goleniewska K, O?Neal J, Zhou W, Ji S, Mitchell DB, Graham BS, et al. Cyclooxygenase inhibition augments allergic inflammation through CD4-dependent, STAT6-independent mechanisms. J Immunol 2005;174:525-532.
9. Laouini D, Elkhal A, Yalcindag A, Kawamoto S, Oettgen H, Geha RS. COX-2 inhibition enhances the TH2 immune response to epicutaneous sensitization. J Allergy Clin Immunol 2005;116:390-396.
10. Peebles RS Jr, Dworski R, Collins RD, Jarzecka K, Mitchell DB, Graham BS, Sheller JR. Cyclooxygenase inhibition increases interleukin 5 and interleukin 13 production and airway hyperresponsiveness in allergic mice. Am J Respir Crit Care Med 2000;162:676-681.
11. Peebles RS Jr, Hashimoto K, Morrow JD, Dworski R, Collins RD, Hashimoto Y, Christman JW, Kang KH, Jarzecka K, Furlong J, et al. Selective cyclooxygenase-1 and -2 inhibitors each increase allergic inflammation and airway hyperresponsiveness in mice. Am J Respir Crit Care Med 2002;165:1154-1160.
12. Peebles RS Jr, Hashimoto K, Sheller JR, Moore ML, Morrow JD, Ji S, Elias JA, Goleniewska K, O?neal J, Mitchell DB, et al. Allergeninduced airway hyperresponsiveness mediated by cyclooxygenase inhibition is not dependent on 5-lipoxygenase or IL-5, but is IL-13 dependent. J Immunol 2005;175:8253-8259.
13. Zhou W, Newcomb DC, Moore ML, Goleniewska K, O?Neal JF, Peebles RS Jr. Cyclooxygenase inhibition during allergic sensitization increases STAT6-independent primary and memory Th2 responses. J Immunol 2008;181:5360-5367.
14. Idzko M, Hammad H, van Nimwegen M, Kool M, Vos N, Hoogsteden HC, Lambrecht BN. Inhaled iloprost suppresses the cardinal features of asthma via inhibition of airway dendritic cell function. J Clin Invest 2007;117:464-472.
15. Jaffar Z, Wan KS, Roberts K. A key role for prostaglandin I2 in limiting lung mucosal Th2, but not Th1, responses to inhaled allergen. J Immunol 2002;169:5997-6004.
16. Jaffar Z, Ferrini ME, Buford MC, Fitzgerald GA, Roberts K. Prostaglandin I2-IP signaling blocks allergic pulmonary inflammation by preventing recruitment of CD41 Th2 cells into the airways in a mouse model of asthma. J Immunol 2007;179:6193-6203.
17. Nagao K, Tanaka H, Komai M, Masuda T, Narumiya S, Nagai H. Role of prostaglandin I2 in airway remodeling induced by repeated allergen challenge in mice. Am J Respir Cell Mol Biol 2003;29:314-320.
18. Takahashi Y, Tokuoka S, Masuda T, Hirano Y, Nagao M, Tanaka H, Inagaki N, Narumiya S, Nagai H. Augmentation of allergic inflammation in prostanoid IP receptor deficient mice. Br J Pharmacol 2002;137: 315-322.
19. Zhou W, Hashimoto K, Goleniewska K, O?Neal JF, Ji S, Blackwell TS, Fitzgerald GA, Egan KM, Geraci MW, Peebles RS Jr. Prostaglandin I2 analogs inhibit proinflammatory cytokine production and T cell stimulatory function of dendritic cells. J Immunol 2007;178: 702-710.
20. ZhouW, Blackwell TS, Goleniewska K, O?Neal JF, Fitzgerald GA, LucittM, Breyer RM, Peebles RS Jr. Prostaglandin I2 analogs inhibit Th1 and Th2 effector cytokine production by CD4 T cells. J Leukoc Biol 2007; 81:809-817.
21. Boie Y, Rushmore TH, Darmon-Goodwin A, Grygorczyk R, Slipetz DM, Metters KM, Abramovitz M. Cloning and expression of a cDNA for the human prostanoid IP receptor. J Biol Chem 1994;269: 12173-12178.
22. Hébert RL, O?Connor T, Neville C, Burns KD, Laneuville O, Peterson LN. Prostanoid signaling, localization, and expression of IP receptors in rat thick ascending limb cells. Am J Physiol 1998;275:F904-F914.
23. Katsuyama M, Sugimoto Y, Namba T, Irie A, Negishi M, Narumiya S, Ichikawa A. Cloning and expression of a cDNA for the human prostacyclin receptor. FEBS Lett 1994;344:74-78.
24. Lawler OA, Miggin SM, Kinsella BT. Protein kinase A-mediated phosphorylation of serine 357 of the mouse prostacyclin receptor regulates its coupling to G(s)-, to G(i)-, and to G(q)-coupled effector signaling. J Biol Chem 2001;276:33596-33607.
25. Mjösberg J, Eidsmo L. Update on innate lymphoid cells in atopic and non-atopic inflammation in the airways and skin. Clin Exp Allergy 2014;44:1033-1043.
26. Halim TY, Krauss RH, Sun AC, Takei F. Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergeninduced airway inflammation. Immunity 2012;36:451-463.
27. Barlow JL, Bellosi A, Hardman CS, Drynan LF,Wong SH, Cruickshank JP, McKenzie AN. Innate IL-13-producing nuocytes arise during allergic lung inflammation and contribute to airways hyperreactivity. J Allergy Clin Immunol 2012;129:191-8.e1, 4.
28. Doherty TA, Khorram N, Chang JE, Kim HK, Rosenthal P, Croft M, Broide DH. STAT6 regulates natural helper cell proliferation during lung inflammation initiated by Alternaria. Am J Physiol Lung Cell Mol Physiol 2012;303:L577-L588.
29. Klein Wolterink RG, Kleinjan A, van Nimwegen M, Bergen I, de Bruijn M, Levani Y, Hendriks RW. Pulmonary innate lymphoid cells are major producers of IL-5 and IL-13 in murine models of allergic asthma. Eur J Immunol 2012;42:1106-1116.
30. Mjösberg J, Bernink J, Peters C, Spits H. Transcriptional control of innate lymphoid cells. Eur J Immunol 2012;42:1916-1923.
31. Klein Wolterink RG, Serafini N, van Nimwegen M, Vosshenrich CA, de Bruijn MJ, Fonseca Pereira D, Veiga Fernandes H, Hendriks RW, Di Santo JP. Essential, dose-dependent role for the transcription factor Gata3 in the development of IL-51 and IL-131 type 2 innate lymphoid cells. Proc Natl Acad Sci USA 2013;110:10240-10245.
32. Bartemes KR, Iijima K, Kobayashi T, Kephart GM, McKenzie AN, Kita H. IL-33-responsive lineage- CD251 CD44(hi) lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs. J Immunol 2012;188:1503-1513.
33. Iijima K, Kobayashi T, Hara K, Kephart GM, Ziegler SF, McKenzie AN, Kita H. IL-33 and thymic stromal lymphopoietin mediate immune pathology in response to chronic airborne allergen exposure. J Immunol 2014;193:1549-1559.
34. Kouzaki H, O?Grady SM, Lawrence CB, Kita H. Proteases induce production of thymic stromal lymphopoietin by airway epithelial cells through protease-activated receptor-2. J Immunol 2009;183:1427-1434.
35. Kouzaki H, Iijima K, Kobayashi T, O?Grady SM, Kita H. The danger signal, extracellular ATP, is a sensor for an airborne allergen and triggers IL-33 release and innate Th2-type responses. J Immunol 2011;186:4375-4387.
36. Dorris SL, Peebles RS Jr. PGI(2) as a regulator of inflammatory diseases. Mediator Inflamm 2012;2012:926968.
37. Lynch NR, Dunand P, Newcomb RW, Chai H, Bigley J. Influence of IgG antibody and glycopeptide allergens on the correlation between the radioallergosorbent test (RAST) and skin testing or bronchial challenge with Alternaria. Clin Exp Immunol 1975;22:35-46.
38. Holtzman MJ. Arachidonic acid metabolism: implications of biological chemistry for lung function and disease. Am Rev Respir Dis 1991; 143:188-203.
39. Wenzel SE. Arachidonic acid metabolites: mediators of inflammation in asthma. Pharmacotherapy 1997;17:3S-12S.
40. Barnig C, Cernadas M, Dutile S, Liu X, Perrella MA, Kazani S,Wechsler ME, Israel E, Levy BD. Lipoxin A4 regulates natural killer cell and type 2 innate lymphoid cell activation in asthma. Sci Transl Med 2013;5:174ra26.
41. Doherty TA, Khorram N, Lund S, Mehta AK, Croft M, Broide DH. Lung type 2 innate lymphoid cells express cysteinyl leukotriene receptor 1, which regulates TH2 cytokine production. J Allergy Clin Immunol 2013;132:205-213.
42. Palmer G, Gabay C. Interleukin-33 biology with potential insights into human diseases. Nat Rev Rheumatol 2011;7:321-329.
43. Chen YC, Chu LY, Yang SF, Chen HL, Yet SF, Wu KK. Prostacyclin and PPARa agonists control vascular smooth muscle cell apoptosis and phenotypic switch through distinct 14-3-3 isoforms. PLoS One 2013;8:e69702.
44. Peshavariya HM, Liu GS, Chang CW, Jiang F, Chan EC, Dusting GJ. Prostacyclin signaling boosts NADPH oxidase 4 in the endothelium promoting cytoprotection and angiogenesis. Antioxid Redox Signal 2014;20:2710-2725.
45. Zhou W, Dowell DR, Geraci MW, Blackwell TS, Collins RD, Polosukhin VV, Lawson WE, Wu P, Sussan T, Biswal S, et al. PGI synthase overexpression protects against bleomycin-induced mortality and is associated with increased Nqo 1 expression. Am J Physiol Lung Cell Mol Physiol 2011;301:L615-L622.
46. Holgate ST. Innate and adaptive immune responses in asthma. Nat Med 2012;18:673-683.
47. Sturm EM, Schuligoi R, Konya V, Sturm GJ, Heinemann A. Inhibitory effect of prostaglandin I2 on bone marrow kinetics of eosinophils in the guinea pig. J Leukoc Biol 2011;90:285-291.
48. Konya V, Sturm EM, Schratl P, Beubler E, Marsche G, Schuligoi R, Lippe IT, Peskar BA, Heinemann A. Endothelium-derived prostaglandin I(2) controls the migration of eosinophils. J Allergy Clin Immunol 2010;125:1105-1113.
49. Zhou W, Goleniewska K, Zhang J, Dulek DE, Toki S, Lotz MT, Newcomb DC, Boswell MG, Polosukhin VV, Milne GL, et al. Cyclooxygenase inhibition abrogates aeroallergen-induced immune tolerance by suppressing prostaglandin I2 receptor signaling. J Allergy Clin Immunol 2014;134:698-705.e5.
50. Lee IY, Ko EM, Kim SH, Jeoung DI, Choe J. Human follicular dendritic cells express prostacyclin synthase: a novel mechanism to control T cell numbers in the germinal center. J Immunol 2005;175:1658-1664.