Cooperation of adenosine and prostaglandin E2 (PGE2) in amplification of cAMP-PKA signaling and immunosuppression

Cancer Immunology, Immunotherapy

Volumn 57, Issue 11, 2008, Pages 1611-1623

  Su, Yunyun ^a   Huang, Xiaojun ^a   Raskovalova, Tatiana ^a   Zacharia, Lefteris ^b   Lokshin, Anna ^a   Jackson, Edwin ^c   Gorelik, Elieser ^a  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Adenosine; Cytokine production; Cytotoxicity; Immunosuppression; PGE2

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ADENOSINE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; PROSTAGLANDIN E2; PROTEIN KINASE B INHIBITOR; RP 8 BROMO CYCLIC AMP; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; WORTMANNIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; DRUG MECHANISM; FEMALE; IMMUNOCOMPETENT CELL; IMMUNOSUPPRESSIVE TREATMENT; LYMPHOKINE ACTIVATED KILLER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADENOSINE; ANIMALS; BLOTTING, WESTERN; CELL SURVIVAL; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DINOPROSTONE; FEMALE; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; IMMUNE TOLERANCE; IMMUNOSUPPRESSION; INTERFERON TYPE II; INTERLEUKIN-10; KILLER CELLS, LYMPHOKINE-ACTIVATED; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; OXYTOCICS; RECEPTORS, PROSTAGLANDIN E; RECEPTORS, PURINERGIC P1; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 50649108394     PISSN: 03407004     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00262-008-0494-5     Document Type: Article

References (52)

1. AN Hata RM Breyer 2004 Pharmacology and signaling of prostaglandin receptors: multiple roles in inflammation and immune modulation Pharmacol Ther 103 147 166
2. H Fujino S Salvi JW Regan 2005 Differential regulation of phosphorylation of the cAMP response element-binding protein after activation of EP2 and EP4 prostanoid receptors by prostaglandin E2 Mol Pharmacol 68 251 259
3. AJ Dannenberg K Subbaramaiah 2003 Targeting cyclooxygenase-2 in human neoplasia: rationale and promise Cancer Cell 4 431 436
4. C Denkert KJ Winzer S Hauptmann 2004 Prognostic impact of cyclooxygenase-2 in breast cancer Clin Breast Cancer 4 428 433
5. J Mrena JP Wiksten A Thiel A Kokkola L Pohjola J Lundin S Nordling A Ristimaki C Haglund 2005 Cyclooxygenase-2 is an independent prognostic factor in gastric cancer and its expression is regulated by the messenger RNA stability factor HuR Clin Cancer Res 11 7362 7368
6. A Eisenthal 1990 Indomethacin up-regulates the generation of lymphokine-activated killer-cell activity and antibody-dependent cellular cytotoxicity mediated by interleukin-2 Cancer Immunol Immunother 31 342 348
7. N Kundu AM Fulton 2002 Selective cyclooxygenase (COX)-1 or COX-2 inhibitors control metastatic disease in a murine model of breast cancer Cancer Res 62 2343 2346
8. N Kundu TC Walser X Ma AM Fulton 2005 Cyclooxygenase inhibitors modulate NK activities that control metastatic disease Cancer Immunol Immunother 54 981 987
9. PK Lala RS Parhar 1988 Cure of B16F10 melanoma lung metastasis in mice by chronic indomethacin therapy combined with repeated rounds of interleukin 2: characteristics of killer cells generated in situ Cancer Res 48 1072 1079
10. PC Chulada MB Thompson JF Mahler CM Doyle BW Gaul C Lee HF Tiano SG Morham O Smithies R Langenbach 2000 Genetic disruption of Ptgs-1, as well as Ptgs-2, reduces intestinal tumorigenesis in Min mice Cancer Res 60 4705 4708
11. KS Chun JK Akunda R Langenbach 2007 Cyclooxygenase-2 inhibits UVB-induced apoptosis in mouse skin by activating the prostaglandin E2 receptors, EP2 and EP4 Cancer Res 67 2015 2021
12. R Langenbach CD Loftin C Lee H Tiano 1999 Cyclooxygenase-deficient mice. A summary of their characteristics and susceptibilities to inflammation and carcinogenesis Ann N Y Acad Sci 889 52 61
13. M Oshima JE Dinchuk SL Kargman H Oshima B Hancock E Kwong JM Trzaskos JF Evans MM Taketo 1996 Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2) Cell 87 803 809
14. CH Liu SH Chang K Narko OC Trifan MT Wu E Smith C Haudenschild TF Lane T Hla 2001 Overexpression of cyclooxygenase-2 is sufficient to induce tumorigenesis in transgenic mice J Biol Chem 276 18563 18569
15. X Ma N Kundu S Rifat T Walser AM Fulton 2006 Prostaglandin E receptor EP4 antagonism inhibits breast cancer metastasis Cancer Res 66 2923 2927
16. M Majima H Amano I Hayashi 2003 Prostanoid receptor signaling relevant to tumor growth and angiogenesis Trends Pharmacol Sci 24 524 529
17. YM Sung G He SM Fischer 2005 Lack of expression of the EP2 but not EP3 receptor for prostaglandin E2 results in suppression of skin tumor development Cancer Res 65 9304 9311
18. JG Rozic C Chakraborty PK Lala 2001 Cyclooxygenase inhibitors retard murine mammary tumor progression by reducing tumor cell migration, invasiveness and angiogenesis Int J Cancer 93 497 506
19. SH Chang CH Liu R Conway DK Han K Nithipatikom OC Trifan TF Lane T Hla 2004 Role of prostaglandin E2-dependent angiogenic switch in cyclooxygenase 2-induced breast cancer progression Proc Natl Acad Sci USA 101 591 596
20. JL Masferrer KM Leahy AT Koki BS Zweifel SL Settle BM Woerner DA Edwards AG Flickinger RJ Moore K Seibert 2000 Antiangiogenic and antitumor activities of cyclooxygenase-2 inhibitors Cancer Res 60 1306 1311
21. SG Harris J Padilla L Koumas D Ray RP Phipps 2002 Prostaglandins as modulators of immunity Trends Immunol 23 144 150
22. G Burnstock 1997 The past, present and future of purine nucleotides as signalling molecules Neuropharmacology 36 1127 1139
23. BN Cronstein 1994 Adenosine, an endogenous anti-inflammatory agent J Appl Physiol 76 5 13
24. G Hasko BN Cronstein 2004 Adenosine: an endogenous regulator of innate immunity Trends Immunol 25 33 39
25. MV Sitkovsky D Lukashev S Apasov H Kojima M Koshiba C Caldwell A Ohta M Thiel 2004 Physiological control of immune response and inflammatory tissue damage by hypoxia-inducible factors and adenosine A2A receptors Annu Rev Immunol 22 657 682
26. MV Sitkovsky A Ohta 2005 The 'danger' sensors that STOP the immune response: the A2 adenosine receptors? Trends Immunol 26 299 304
27. A Ohta E Gorelik SJ Prasad F Ronchese D Lukashev MK Wong X Huang S Caldwell K Liu P Smith JF Chen EK Jackson S Apasov S Abrams M Sitkovsky 2006 A2A adenosine receptor protects tumors from antitumor T cells Proc Natl Acad Sci USA 103 13132 13137
28. A Lokshin T Raskovalova X Huang LC Zacharia EK Jackson E Gorelik 2006 Adenosine-mediated inhibition of the cytotoxic activity and cytokine production by activated natural killer cells Cancer Res 66 7758 7765
29. T Raskovalova X Huang M Sitkovsky LC Zacharia EK Jackson E Gorelik 2005 Gs protein-coupled adenosine receptor signaling and lytic function of activated NK cells J Immunol 175 4383 4391
30. T Raskovalova A Lokshin X Huang EK Jackson E Gorelik 2006 Adenosine-mediated inhibition of cytotoxic activity and cytokine production by IL-2/NKp46-activated NK cells: involvement of protein kinase A isozyme I (PKA I) Immunol Res 36 91 100
31. T Raskovalova A Lokshin X Huang Y Su M Mandic HM Zarour EK Jackson E Gorelik 2007 Inhibition of cytokine production and cytotoxic activity of human antimelanoma specific CD8+ and CD4+ T lymphocytes by adenosine-protein kinase A type I signaling Cancer Res 67 5949 5956
32. Y Gunji NL Vujanovic JC Hiserodt RB Herberman E Gorelik 1989 Generation and characterization of purified adherent lymphokine-activated killer cells in mice J Immunol 142 1748 1754
33. JR Ortaldo EW Bere D Hodge HA Young 2001 Activating Ly-49 NK receptors: central role in cytokine and chemokine production J Immunol 166 4994 4999
34. E Gorelik DP Landsittel AM Marrangoni F Modugno L Velikokhatnaya MT Winans WL Bigbee RB Herberman AE Lokshin 2005 Multiplexed immunobead-based cytokine profiling for early detection of ovarian cancer Cancer Epidemiol Biomarkers Prev 14 981 987
35. EK Jackson LC Zacharia M Zhang DG Gillespie C Zhu RK Dubey 2006 cAMP-adenosine pathway in the proximal tubule J Pharmacol Exp Ther 317 1219 1229
36. ER Fedyk JM Ripper DM Brown RP Phipps 1996 A molecular analysis of PGE receptor (EP) expression on normal and transformed B lymphocytes: coexpression of EP1, EP2, EP3beta and EP4 Mol Immunol 33 33 45
37. AT Bender JA Beavo 2006 Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use Pharmacol Rev 58 488 520
38. BS Skalhegg K Tasken 2000 Specificity in the cAMP/PKA signaling pathway. Differential expression,regulation, and subcellular localization of subunits of PKA Front Biosci 5 D678 693
39. K Jiang B Zhong DL Gilvary BC Corliss E Hong-Geller S Wei JY Djeu 2000 Pivotal role of phosphoinositide-3 kinase in regulation of cytotoxicity in natural killer cells Nat Immunol 1 419 425
40. KV Chin WL Yang R Ravatn T Kita E Reitman D Vettori ME Cvijic M Shin L Iacono 2002 Reinventing the wheel of cyclic AMP: novel mechanisms of cAMP signaling Ann N Y Acad Sci 968 49 64
41. YS Cho-Chung M Nesterova KG Becker R Srivastava YG Park YN Lee YS Cho MK Kim C Neary C Cheadle 2002 Dissecting the circuitry of protein kinase A and cAMP signaling in cancer genesis: antisense, microarray, gene overexpression, and transcription factor decoy Ann N Y Acad Sci 968 22 36
42. KM Torgersen JT Vaage FO Levy V Hansson B Rolstad K Tasken 1997 Selective activation of cAMP-dependent protein kinase type I inhibits rat natural killer cell cytotoxicity J Biol Chem 272 5495 5500
43. L Gorelik RA Flavell 2001 Immune-mediated eradication of tumors through the blockade of transforming growth factor-beta signaling in T cells Nat Med 7 1118 1122
44. R Kim M Emi K Tanabe K Arihiro 2006 Tumor-driven evolution of immunosuppressive networks during malignant progression Cancer Res 66 5527 5536
45. S Desai H April C Nwaneshiudu B Ashby 2000 Comparison of agonist-induced internalization of the human EP2 and EP4 prostaglandin receptors: role of the carboxyl terminus in EP4 receptor sequestration Mol Pharmacol 58 1279 1286
46. H Fujino JW Regan 2006 EP(4) prostanoid receptor coupling to a pertussis toxin-sensitive inhibitory G protein Mol Pharmacol 69 5 10
47. B Johansson L Halldner TV Dunwiddie SA Masino W Poelchen L Gimenez-Llort RM Escorihuela A Fernandez-Teruel Z Wiesenfeld-Hallin XJ Xu A Hardemark C Betsholtz E Herlenius BB Fredholm 2001 Hyperalgesia, anxiety, and decreased hypoxic neuroprotection in mice lacking the adenosine A1 receptor Proc Natl Acad Sci USA 98 9407 9412
48. D Gabrilovich V Pisarev 2003 Tumor escape from immune response: mechanisms and targets of activity Curr Drug Targets 4 525 536
49. DA Thomas J Massague 2005 TGF-beta directly targets cytotoxic T cell functions during tumor evasion of immune surveillance Cancer Cell 8 369 380
50. H Koehler D Kofler A Hombach H Abken 2007 CD28 costimulation overcomes transforming growth factor-beta-mediated repression of proliferation of redirected human CD4+ and CD8+ T cells in an antitumor cell attack Cancer Res 67 2265 2273
51. RB Smeltz J Chen EM Shevach 2005 Transforming growth factor-beta1 enhances the interferon-gamma-dependent, interleukin-12-independent pathway of T helper 1 cell differentiation Immunology 114 484 492
52. J Blay TD White DW Hoskin 1997 The extracellular fluid of solid carcinomas contains immunosuppressive concentrations of adenosine Cancer Res 57 2602 2605