Reciprocal crosstalk between dendritic cells and natural killer cells under the effects of PGE2 in immunity and immunopathology

Cellular and Molecular Immunology

Volumn 10, Issue 3, 2013, Pages 213-221

  Harizi, Hedi ^a  

^a CNRS Bordeaux Segalen University   (France)

Author keywords

DC NK cell crosstalk; immunopathology; NSAIDs; PGE2

Indexed keywords

6 [3 (4 CHLORO 2 METHYLPHENYLSULFONYLAMINOMETHYL)BICYCLO[2.2.2]OCTAN 2 YL] 5 HEXENOIC ACID; 7 [5 (4 BIPHENYLYLMETHOXY) 2 MORPHOLINO 3 OXOCYCLOPENTYL] 4 HEPTENOIC ACID; CELECOXIB; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; FRONDOSIDE A; GAMMA INTERFERON; INDOMETACIN; INTERLEUKIN 10; INTERLEUKIN 12; NONSTEROID ANTIINFLAMMATORY AGENT; ONO AE3 208; ONO AE3 240; PF 04418948; PROSTAGLANDIN E RECEPTOR 1; PROSTAGLANDIN E RECEPTOR 2; PROSTAGLANDIN E RECEPTOR 3; PROSTAGLANDIN E RECEPTOR 4; PROSTAGLANDIN E2; PROSTAGLANDIN RECEPTOR BLOCKING AGENT; PROSTANOID RECEPTOR; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ALLERGIC DISEASE; ANTINEOPLASTIC ACTIVITY; AUTOCRINE EFFECT; BREAST METASTASIS; CANCER PREVENTION; CELL ACTIVATION; CELL INTERACTION; CELL MATURATION; CELL MIGRATION; CELLULAR IMMUNITY; COLON CANCER; CYTOKINE PRODUCTION; DENDRITIC CELL; DIGESTIVE SYSTEM ULCER; GASTROINTESTINAL TOXICITY; HUMAN; IMMUNITY; IMMUNOMODULATION; IMMUNOPATHOLOGY; INNATE IMMUNITY; METASTASIS INHIBITION; MOUTH SQUAMOUS CELL CARCINOMA; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; PARACRINE SIGNALING; PROSTAGLANDIN SYNTHESIS; REVIEW; TH2 CELL; TONGUE CANCER; TUMOR ASSOCIATED LEUKOCYTE; VIRUS INFECTION;

ANIMALS; CELL COMMUNICATION; DENDRITIC CELLS; DINOPROSTONE; HUMANS; IMMUNE SYSTEM DISEASES; IMMUNITY; KILLER CELLS, NATURAL;

EID: 84877626335     PISSN: 16727681     EISSN: None     Source Type: Journal    
DOI: 10.1038/cmi.2013.1     Document Type: Review

References (124)

1. Moretta A. Natural killer cells and dendritic cellsRendezvous in abused tissues. Nat Rev Immunol 2002; 12: 957-964.
2. Fernandez NC, Lozier A, Flament C, Ricciardi-Castagnoli P, Bellet D, Suter M et al. Dendritic cells directly trigger NK cell functions: Crosstalk relevant in innate anti-tumor immune responses in vivo. Nat Med 1999; 5: 405-411.
3. Andoniou CE, van Dommelen SL, Voigt V. Interaction between conventional dendritic cells and natural killer cells is integral to the activation of effective antiviral immunity. Nat Immunol 2005; 6: 1011-1019.
4. Munz C, Steinman RM, Fujii S. Dendritic cell maturation by innate lymphocytes: Coordinated stimulation of innate and adaptive immunity. J Exp Med 2005; 202: 203-207.
5. Luft T, Jefford M, Luetjens P, Toy T, Hochrein H, Masterman KA et al. Functionally distinct dendritic cell populations induced by physiologic stimuliProstaglandin E2 regulates the migratory capacity of specific DC subsets. Blood 2002; 100: 1362-1372.
6. Reschner A, Hubert P, Delvenne P, Boniver J, Jacobs N. Innate lymphocyte and dendritic cell cross-talk: A key factor in the regulation of the immune response. Clin Exp Immunol 2008; 152: 219-226.
7. Moser M. Dendritic cells in immunity and tolerance - do they display opposite functions? Immunity 2003; 19: 5-8.
8. Morelli AE, Thomson AW. Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol 2007; 7: 610-621.
9. Torres-Aguilar H, Aguilar-Ruiz SR, Gonzá lez-Pé rez G, Munguía R, Bajan a S, Meraz-Ríos MA, et al. Tolerogenic dendritic cells generated with different immunosuppressive cytokines induce antigen-specific anergy and regulatory properties in memory CD41 T cells. J Immunol 2010; 184: 1765-1775.
10. Morelli AE, Larregina AT, Shufesky WJ, Zahorchak AF, Logar AJ, Papworth GD et al. Internalization of circulating apoptotic cells by splenic marginal zone dendritic cells: Dependence on complement receptors and effect on cytokine production. Blood 2003; 101: 611-620.
11. Walzer T, Dalod M, Vivier E, Zitvogel L. Natural killer cell- dendritic cell crosstalk in the initiation of immune responses. Expert Opin Biol Ther 2005; 5S49- S59.
12. Battistini A. Interferon regulatory factors in hematopoietic cell differentiation and immuneregulation. J Interferon Cytokine Res 2009; 29: 765-780.
13. Gattoni A, Parlato A, Vangieri B, Bresciani M, Derna R. Interferongamma: Biologic functions and HCV therapy (type I/II) (2 of 2 parts). Clin Ter 2006; 157: 457-468.
14. Cooper MA, Fehinger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol 2001; 22: 633-640.
15. Hayakawa Y, Smyth MJ. CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J Immunol 2006; 176: 1517-1724.
16. Chong WP, Zhou J, Law HK, Tu W, Lau YL. Natural killer cells become tolerogenic after interaction with apoptotic cells. Eur J Immunol 2010; 40: 1718-1727.
17. Jacobs B Ullrich E. The interaction of NK cells and dendritic cells in the tumor environment: How to enforce NK cell and DC action under immunosuppressive conditions? Curr Med Chem 2012; 19: 1771-1779.
18. van Elssen CH, Vanderlocht J, Oth T, Senden-Gijsbers BL, Germeraad WT, Bos GM. Inflammation-restraining effects of prostaglandin E2 on natural killer- dendritic cell (NK- DC) interaction are imprinted during DC maturation. Blood 2011; 118: 2473-2482.
19. Walzer T, Dalod M, Robbins SH, Zitvogel L, Vivier E. Natural-killer cells and dendritic cells: ''l'union fait la force''. Blood 2005; 1: 2252-2258.
20. Trinchieri G. Biology of natural killer cells. Adv Immunol 1989; 47: 187-376.
21. Gerosa F, Baldani-Guerra B, Nisii C, Marchesini V, Carra G, Trinchieri G. Reciprocal activating interaction between natural killer cells and dendritic cells. J Exp Med 2002; 195: 327-333.
22. Piccioli D, Sbrana S, Melandri E, Valiante NM. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J Exp Med 2002; 195: 335-341.
23. Ferlazzo G, Tsang ML, Moretta L, Melioli G, Steinman RM, Münz C. Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells. J Exp Med 2002; 195: 343-51
24. Vitale M, Della Chiesa M, Carlomagno S, Romagnani C, Thiel A, Moretta L et al. The small subset of CD56brightCD162 natural killer cells is selectively responsible for both cell proliferation and interferon-gamma production upon interaction with dendritic cells. Eur J Immunol 2004; 34: 1715-1722.
25. Della Chiesa MM, Vitale S, Carlomagno G, Ferlazzo L, Moretta A. The natural killer cell-mediated killing of autologous dendritic cells is confined to a cell subset expressing CD94/NKG2A, but lacking inhibitory killer Ig-like receptors. Eur J Immunol 2003; 33: 1657-1666.
26. Degli-Esposti MA, Smyth MJ. Close encounters of different kinds: Dendritic cells and NK cells take centre stage. Nat Rev Immunol 2005; 5: 112-124.
27. Mailliard RB, Son YI, Redlinger R, Coates PT, Giermasz A, Morel PA et al. Dendritic cells mediate NK cell help for Th1 and CTL responsesTwo-signal requirement for the induction of NK cell helper function. J Immunol 2003; 171: 2366-2373.
28. Agaugue S, Marcenaro E, Ferranti B, Moretta L, Moretta A. Human natural killer cells exposed to IL-2, IL-12, IL-18, or IL-4 differently modulate priming of naive T cells by monocyte-derived dendritic cells. Blood 2008; 112: 1776-1783.
29. Morandi B, Mortara L, Chiossone L, Accolla RS, Mingari MC, Moretta L et al. Dendritic cell editing by activated natural killer cells results in amore protective cancer-specific immune response. PLoS ONE 2012; 7: E39170.
30. Siddiqui N, Hope J. Differential recruitment and activation of natural killer cell sub-populations by Mycobacterium bovis-infected dendritic cells. Eur J Immunol; e-pub ahead of print 2 November 2012; doi:10.1002/eji.201242736.
31. Vitale M, Della Chiesa M, Carlomagno S, Pende D, Arico M, Moretta L et al. NK-dependent DC maturation is mediated by TNFa and IFNc released upon engagement of the NKp30 triggering receptor. Blood 2005; 106: 566-571.
32. Morandi B, Mortara L, Carrega P, Cantoni C, Costa G, Accolla RS et al. NK cells provide helper signal for CD81 T cells by inducing the expression of membrane-bound IL-15 on DCs. Int Immunol 2009; 21: 599-606.
33. Tilley SL, Coffman TM, Koller BH. Mixed messagesModulation of inflammation and immune responses by prostaglandins and thromboxanes. J Clin Invest 2001; 108: 15-23.
34. Gualde N, Harizi H. Prostanoids and their receptors that modulate dendritic cell-mediated immunity. Immunol Cell Biol 2004; 82: 353-360.
35. Harris SG, Padilla J, Koumas L, Ray D, Phipps RP. Prostaglandins as modulators of immunity. Trends Immunol 2002; 23: 144-150.
36. Phipps RP, Stein SH, Roper RL. A new view of prostaglandin E regulation of the immune response. Immunol Today 1991; 12: 349-352.
37. Harizi H, Juzan M, Pitard V, Moreau JF, Gualde N. Cyclooxygenase-2-issued prostaglandin E2 enhances the production of endogenous IL-10, which down-regulates dendritic cell functions. J Immunol 2002; 168: 2255-2263.
38. Harizi H, Juzan M, Moreau JF, Gualde N. Prostaglandins inhibit 5-lipoxygenase-activating protein expression and leukotriene B4 production from dendritic cells via an IL-10-dependent mechanism. J Immunol 2003; 170: 139-146.
39. Smith WL, DeWitt DL. Biochemistry of prostaglandin endoperoxide H synthase-1 and synthase-2 and their differential susceptibility to nonsteroidal anti-inflammatory drugs. Semin Nephrol 1995; 15: 179-194.
40. Harizi H, Juzan M, Grosset G, Rashedi M, Gualde N. Dendritic cells issued in vitro from bone marrow produce PGE2 that contributes to the immunomodulation induced by antigen-presenting cells. Cell Immunol 2001; 209: 19-28.
41. Harizi H, Limem I, Gualde N. CD40 engagement on dendritic cells induces cyclooxygenase-2 and EP2 receptor via p38 and ERK MAPKs. Immunol Cell Biol 2011; 89: 275-282.
42. Minghetti L, Walsh DT, Levi G, Perry VH. In vivo expression of cyclooxygenase-2 in rat brain following intraparenchymal injection of bacterial endotoxin and inflammatory cytokines. J Neuropathol Exp Neurol 1999; 58: 1184-1191.
43. Jó zefowski S, Bobek M, Marcinkiewicz J. Exogenous but not endogenous prostanoids regulate cytokine secretion from murine bone marrow dendritic cells: EP2, DP, and IP but not EP1, EP3, and FP prostanoid receptors are involved. Int Immunopharmacol 2003; 3: 865-878.
44. Vassiliou E, Jing H, Ganea D. Prostaglandin E2 inhibits TNF-a production in murine bone marrow-derived dendritic cells. Cell Immunol 2003; 223: 120-132.
45. Fogel-Petrovic M, Long JA, Knight DA, Thompson PT, Upham JW. Activated human dendritic cells express inducible cyclo-oxygenase and synthesize prostaglandin E2 but not prostaglandin D2. Immunol Cell Biol 2004; 82: 47-54.
46. Whittaker DS, Bahjat KS, Moldawer LL, Clare-Salzler MJ. Autoregulation of human monocyte-derived dendritic cell maturation and IL-12 production by cyclooxygenase-2-mediated prostanoid production. J Immunol 2000; 165: 4298-4304.
47. Mahic MS, Yaqub CC, Johansson K, Taskén E, Aandahl M. FOXP31CD41CD251 adaptive regulatory T cells express cyclooxygenase-2 and suppress effector T cells by a prostaglandin E2-dependent mechanism. J Immunol 2006; 177: 246-254.
48. Fedyk ER, Phipps RP. Prostaglandin E2 receptors of the EP2 and EP4 subtypes regulate activation and differentiation of mouse B lymphocytes to IgE-secreting cells. Proc Natl Acad Sci USA 1996; 1: 10978-10983.
49. Rocca B, Spain LM, Puré E, Langenbach R, Patrono C, FitzGerald GA. Distinct roles of prostaglandin H synthases 1 and 2 in T-cell development. J Clin Invest 1999; 15: 1469-1477.
50. Harizi H, Grosset C, Gualde N. Prostaglandin E2 modulates dendritic cell function via EP2 and EP4 receptor subtypes. J Leukoc Biol 2003; 73: 756-763.
51. Russell SW, Pace JL. Both the kind and magnitude of stimulus are important in overcoming the negative regulation of macrophage activation by PGE2. J Leukoc Biol 1984: 35: 291-301.
52. Sugimoto Y, Narumiya S, Ichikawa A. Distribution and function of prostanoid receptorsStudies from knockout mice. Prog Lipid Res 2000; 39: 289-314.
53. Narumiya S, Sugimoto Y, Ushikubi F. Prostanoid receptors. Physio Rev 1999; 79: 1193-1226.
54. Harizi H, Gualde N. Eicosanoids: An emerging role in dendritic cell biology. Arch Immunol Ther Exp (Warsz) 2004; 52: 1-5.
55. Vassiliou E, Sharma V, Fedyk ER, Jing H, Sheibanie F, Ganea D. Prostaglandin E2 promotes the survival of bone marrow-derived dendritic cells. J Immunol 2004; 173: 6955-6964.
56. Scandella E, Men Y, Gillessen S, Forster R, Groettrup M. Prostaglandin E2 is a key factor for CCR7 surface expression and migration of monocyte-derived dendritic cells. Blood 2002; 100: 1354-1361.
57. Goodwin JS. Are prostaglandins proinflammatory, antiinflammatory, both or neither? J Rheumatol Suppl 1991; 28: 26-29.
58. Jonuleit H, Kuhn U, Muller G, Steinbrink K, Paragnik L, SchmittE et al. Proinflammatory cytokines and prostaglandins reduce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur J Immunol 1997; 27: 3135-3142.
59. Zelle-Rieser C, Ramoner R, Artner-Dworzak E, Casari A, Bartsch G, Thurnher M. Human monocyte-derived dendritic cells are deficient in prostaglandin E2 production. FEBS Lett 2002; 30: 123-126.
60. Rieser C, Bock G, Klocker H, Bartsch G, Thurnher M. Prostaglandin E2 and tumor necrosis factor a cooperate to activate human dendritic cellsSynergistic activation of interleukin 12 production. J Exp Med 1997; 186: 1603-1608.
61. Jing H, Vassiliou E, Ganea D. Prostaglandin E2 inhibits production of the inflammatory chemokines CCL3 and CCL4 in dendritic cells. J Leukoc Biol 2003; 74: 868-879.
62. D'Andrea A, Aste-Amezaga M, Valiante M, Ma X, Kubin M, Trinchieri G. Interleukin-10 (IL-10) inhibits human lymphocyte IFNc production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 1993; 178: 1041-1048.
63. Enk AH, Angeloni VL, Udey MC, Katz SI. Inhibition of antigenpresenting function by IL-10. J. Immunol 1993; 151: 2390-2398.
64. Steinbrink K, Wolfl M, Jonuleit H, Knop J, Enk AH. Induction of tolerance by IL-10-treated dendritic cells. J Immunol 1997; 159: 4772-4780.
65. Snijdewint FG, Kalinski P, Wierenga EA, Bos JD, Kapsenberg ML. Prostaglandin E2 differentially modulates cytokine secretion profiles of human T helper lymphocytes. J Immunol 1993; 150: 5321-5329.
66. Kuroda E, Sugiura T, Zeki K, Yoshida Y, Yamashita U. Sensitivity difference to the suppressive effect of prostaglandin E2 among mouse strains: A possible mechanism to polarize Th2 type response in BALB/c mice. J Immunol 2000; 164: 2386-2395.
67. Nataraj C, Thomas DW, Tilley SL, Nguyen MT, Mannon R, Koller BH et al. Receptors for prostaglandin E2 that regulate cellular immune responses in the mouse. J Clin Invest 2001; 108: 1229-1235.
68. Kabashima K, Sakata KD, Nagamachi M, Miyachi Y, Inaba K, Narumiya S. Prostaglandin E2- EP4 signaling initiates skin immune responses by promoting migration and maturation of Langerhans cells. Nat Med 2003; 9: 744-749.
69. Walker W, Rotondo D. Prostaglandin E2 is a potent regulator of interleukin-12- and interleukin-18-induced natural killer cell interferon-gamma synthesis. Immunology 2004; 111: 298-305.
70. Goto T, Herberman RB, Maluish A, Strong DM. Cyclic AMP as a mediator of prostaglandin E-induced suppression of human natural killer cell activity. J Immunol 1983; 130: 1350-1355.
71. Vaillier D, Daculsi R, Gualde N. Effect of prostaglandin E2 on cytotoxic activity and granzyme A protease release by murine adherent IL-2 activated killer cells. Immunobiology 1994; 190: 275-289.
72. Joshi PC, Zhou X, Cuchens M, Jones Q. Prostaglandin E2 suppressed IL-15-mediated human NK cell function through down-regulation of common gamma-chain. J Immunol 2001; 166: 885-891.
73. Holt DH, Ma X, Kundu N, Collin PD, Fulton AM. Modulation of host natural killer cell functions in breast cancer via prostaglandin E2 receptors EP2 and EP4. J Immunother 2012; 35: 179-188.
74. Holt DH, Ma X, Kundu N, Fulton AM. Prostaglandin E2 suppresses natural killer cell function primarily through the PGE2 receptor EP4. Cancer Immunol Immunother 2011; 60: 1577-1586.
75. Martinet L, Jean C, Dietrich D, Fournié JJ, Poupot R. PGE2 inhibits natural killer and gamma delta T cell cytotoxicity triggered by NKR and TCR through a cAMP-mediated PKA type I-dependent signaling. Biochem Pharmacol 2010; 15: 838-845.
76. Zeddou M, Rahmouni S, Vandamme A, Jacobs N, Frippiat F, Leonard P et al. Prostaglandin E2 induces the expression of functional inhibitory CD94/NKG2A receptors in human CD81 T lymphocytes by a cAMPdependent protein kinase A type I pathway. Biochem Pharmacol 2005; 70: 714-724.
77. Gustafsson K, Ingelsten M, Bergqvist L, Nystrom J, Andersson B, Karlsson-Parra A. Recruitment and activation of natural killer cells in vitro by a human dendritic cell vaccine. Cancer Res 2008; 68: 5965-597.
78. Mailliard RB, Alber SM, Shen H, Watkins SC, Kirkwood JM, Herberman RB et al. IL-18-induced CD831CCR71 NK helper cells. J Exp Med 2005; 202: 941-953.
79. Serhan CN, Levy CN. Success of prostaglandin E2 in structure- function is a challenge for structure-based therapeutics. Proc Nat Aca Sci USA 2003; 100: 8609-8611.
80. Harizi H, Corcuff JB, Gualde N. Arachidonic-acid-derived eicosanoidsRoles in biology and immunopathology. Trends Mol Med 2008; 14: 461-469.
81. Wang D, Wang DW, Shi Q, Katkuri S, Walhi W, Desvergne B et al. Prostaglandin E2 promotes colorectal adenoma growth via transactivation of the nuclear peroxisome proliferatorsactivated receptor delta. Cancer Cell 2004; 6: 285-295.
82. Berens ME, Salmon SE, Davis TP. Quantitative analysis of prostaglandins in cell culture medium by high-resolution gas chromatography with electron-capture detection. J Chromatogr 1984; 307: 251-260.
83. Gately S. The contributions of cyclooxygenase-2 to tumor angiogenesis. Cancer Metastasis Rev 2000; 19: 19-27.
84. Tsujii M, Kawano S, Tsuji S, Sawaoka H, Hori M, DuBois RN. Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell 1998; 29: 705-716.
85. Yang L, Yamagata N, Yadav R, Brandon S, Courtney RL, Morrow JD et al. Cancer-associated immunodeficiency and dendritic cell abnormalities mediated by the prostaglandin EP2 receptor. J Clin Invest 2003; 111: 727-735.
86. Kusmartsev S, Gabrilovich DI. Effect of tumor-derived cytokines and growth factors on differentiation and immune suppressive features of myeloid cells in cancer. Cancer Metastasis Rev 2006; 25: 323-331.
87. Pinzon-Charry A, Maxwell T, Lopez JA. Dendritic cell dysfunction in cancer: A mechanism for immunosuppression. Immunol Cell Biol 2005; 83: 451-461.
88. Pietra G, Manzini C, Rivara S, Vitale M, Cantoni C, Petretto A et al. Melanoma cells inhibit natural killer cell function by modulating the expression of activating receptors and cytolytic activity. Cancer Res 2012; 15: 1407-1415.
89. Kundu N, Walser TC, Ma X, Fulton AM. Cyclooxygenase inhibitors modulate NK activities that control metastatic disease. Cancer Immunol Immunother 2005; 54: 981-987.
90. Rabinovich GA, Gabrilovich D, Sotomayor EM. Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 2007; 25: 267-296.
91. Tsujii M, Kawano S, DuBois RN. Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. Proc Natl Acad Sci USA 1997; 94: 3336-3340.
92. Simpson JL, Brooks C, Douwes J. Innate immunity in asthma. Paediatr Respir Rev 2008; 9: 263-270.
93. Timonen T, Stenius-Aarniala B. Natural killer cell activity in asthma. Clin Exp Immunol 1985; 59: 85-90.
94. Umetsu DT, Dekruyff RH. Natural killer T cells are important in the pathogenesis of asthmaThe many pathways to asthma. J Allergy Clin Immunol 2010; 125: 975-979.
95. Stock P, Akbari O. Recent advances in the role of NKT cells in allergic diseases and asthma. Curr Allergy Asthma Rep 2008; 8: 165-170.
96. Korsgren M. NK cells and asthma. Curr Pharm Des 2002; 8: 1871-1876.
97. Schmidt LM, Belvisi MG, Bode KA, Bauer G, Schmidt C, Suchy MT et al. Bronchial epithelial cell-derived prostaglandin E2 dampens the reactivity of dendritic cells. J Immunol 2011; 186: 2095-2105.
98. Vancheri C, Mastruzzo C, Sortino MA, Crimi N. The lung as a privileged site for the beneficial actions of PGE2. Trends Immunol 2004; 25: 40-46.
99. Pavord ID, Wong CS, Williams J, Tattersfield AE. Effect of inhaled prostaglandin E2 on allergen-induced asthma. Am RevRespir Dis 1993; 148: 87-90.
100. Tilley SL, Hartney JM, Erikson CJ, Jania C, Nguyen M, Stock J et al. Receptors and pathways mediating the effects of prostaglandin E2 on airway tone. Am J Physiol Lung Cell Mol Physiol 2003; 284: 599-606.
101. Biron CA Brossay L. NK cells and NKT cells in innate defense against viral infections. Curr Opin Immunol 2001; 13: 458-464.
102. Andrews DM, Scalzo AA, Yokoyama WM. Functional interactions between dendritic cells and NK cells during viral infection. Nat Immunol 2003; 4: 175-181.
103. Wang D, Dubois RN. Prostaglandins and cancer. Gut 2006; 55: 115-122.
104. Balch CM, Dougherty PA, Cloud GA, Tilden AB. Prostaglandin E2-mediated suppression of cellular immunity in colon cancer patients. Surgery 1984; 95: 71-77.
105. Vane Jr. Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat New Biol 1971; 231: 232-235.
106. Khanapure SP, Garvey DS, Janero DR, Letts LG. Eicosanoids in inflammation: Biosynthesis, pharmacology, and therapeutic frontiers. Curr Top Med.Chem 2007; 7: 311-340.
107. Mé ric JB, Rottey S, Olaussen K, Soria JC, Khayat D, Rixe O et al. Cyclooxygenase-2 as a target for anticancer drug development. Crit Rev Oncol Hematol 2006; 59: 51-64.
108. Eisenthal A. Indomethacin up-regulates the generation of lymphokine activated killer cell activity and antibody-dependent cellular toxicity mediated by interleukin-2. Cancer Immunol. Immunother 1990; 31: 342-348.
109. Hussain M, Javeed A, Ashraf M, Al-Zaubai N, Stewart A, Mukhtar MM. Non-steroidal anti-inflammatory drugs, tumour immunity and immunotherapy. Pharmacol Res 2012; 66: 7-18.
110. Robak P, Smolewski P, Robak T. The role of non-steroidal antiinflammatory drugs in the risk of development and treatment of hematologic malignancies. Leuk Lymphoma 2008; 2: 1-11.
111. Agrawal A, Fentiman IS. NSAIDs and breast cancer: A possible prevention and treatment strategy. Int J Clin Pract 2008; 62: 444-449.
112. Hahn T, Alvarez I, Kobie JJ, Ramanathapuram L, Dial S, Fulton A et al. Short-term dietary administration of celecoxib enhances the efficacy of tumor lysate-pulsed dendritic cell vaccines in treating murine breast cancer. Int J Cancer 2006; 118: 2220-2231.
113. Haas AR, Sun J, Vachani A, Wallace AF, Silverberg M, Kapoor V et al. Cycloxygenase-2 inhibition augments the efficacy of a cancer vaccine. Clin Cancer Res 2006; 12: 214-222.
114. Marnett LJ. The COXIB experience: A look in the rearview mirror. Annu Rev Pharmacol Toxicol 2009; 49: 265-290.
115. Wang D, Wang M, Cheng Y, Fitzgerald GA. Cardiovascular hazard and nonsteroidal anti-inflammatory drugs. Curr Opin Pharmacol 2005; 5: 204-210.
116. Mosenden R, Tasken K. Cyclic AMP-mediated immune regulation - overview of mechanisms of action in T cells. Cell Signal 2010; 23: 1009-1016.
117. Jones RL, Giembycz MA, Woodward DF. Prostanoid receptor antagonists: Development strategies and therapeutic applications. Br J Pharmacol 2009; 158: 104-45.
118. Af Forselles K, Root J, Clarke T, Davey D, Aughton K, Dack K. In vitro and in vivo characterization of PF-04418948, a novel, potent and selective prostaglandin EP2 receptor antagonist. Br J Pharmacol 2011; 164: 1847-5186.
119. Makita H, Mutoh M, Maruyama T, Yonemoto K, Kobayashi A, Fujitsuka H. A prostaglandin E2 receptor subtype EP1-selective antagonist, ONO-8711, suppresses 4-nitroquinoline 1-oxide-induced rat tongue carcinogenesis. Carcinogenesis 2007; 28: 677-84.
120. Niho N, Mutoh M, Kitamura T, Takahashi M, Sato H, Yamamoto H. Suppression of azoxymethane-induced colon cancer development in rats by a prostaglandin E receptor EP1-selective antagonist. Cancer Sci 2005; 96: 260-264.
121. Hoshikawa H, Goto R, Mori T, Mitani T, Mori N. Expression of prostaglandin E2 receptors in oral squamous cell carcinomas and growth inhibitory effects of an EP3 selective antagonist, ONO-AE3-240. Int J Oncol 2009; 34: 847-852.
122. Kundu N, Ma X, Holt D, Goloubeva O, Ostrand-Rosenberg S, Fulton AM. Antagonism of the prostaglandin E receptor EP4 inhibits metastasis and enhances NK function. Breast Cancer Res Treat 2009; 117: 235-242.
123. Ma X, Kundu N, Rifat S, Walser T, Fulton AM. Prostaglandin E receptor EP4 antagonism inhibits breast cancer metastasis. Cancer Res 2006; 66: 2923-2927.
124. Ma X, Kundu N, Collin P, Goloubeva O, Fulton AM. Frondoside A inhibits breast cancer metastasis and antagonizes prostaglandin E receptors EP4 and EP2. Breast Cancer Res Treat 2011; 132: 1001-1008.