Prostaglandin E 2 suppresses NK activity in vivo and promotes postoperative tumor metastasis in rats

Annals of Surgical Oncology

Volumn 10, Issue 4, 2003, Pages 469-479

  Yakar, Ilan ^a   Melamed, Rivka ^a   Shakhar, Guy ^a   Shakhar, Keren ^a   Rosenne, Ella ^a   Abudarham, Naphtali ^a   Page, Gayle G ^b   Ben Eliyahu, Shamgar ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Animals; Cytotoxicity; NK cells; Tumor immunology

Indexed keywords

INDOMETACIN; PROSTAGLANDIN E2; PROSTAGLANDIN SYNTHASE INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER RECURRENCE; CELL COUNT; CONTROLLED STUDY; DOSE RESPONSE; IMMUNE DEFICIENCY; LAPAROTOMY; LUNG METASTASIS; MALE; NONHUMAN; POSTOPERATIVE PERIOD; PROSTAGLANDIN BLOOD LEVEL; PROSTAGLANDIN RELEASE; RAT; RAT STRAIN; TUMOR IMMUNOLOGY; ADENOCARCINOMA; ANIMAL; CYTOTOXICITY; DRUG EFFECT; EVALUATION; EXPERIMENTAL NEOPLASM; FEMALE; FISCHER 344 RAT; NATURAL KILLER CELL; RANDOMIZATION;

ADENOCARCINOMA; ANIMALS; CYCLOOXYGENASE INHIBITORS; CYTOTOXICITY, IMMUNOLOGIC; DINOPROSTONE; DOSE-RESPONSE RELATIONSHIP, DRUG; EVALUATION STUDIES; FEMALE; INDOMETHACIN; KILLER CELLS, NATURAL; MALE; MAMMARY NEOPLASMS, EXPERIMENTAL; RANDOM ALLOCATION; RATS; RATS, INBRED F344;

EID: 0041660554     PISSN: 10689265     EISSN: 15344681     Source Type: Journal    
DOI: 10.1245/ASO.2003.08.017     Document Type: Article

References (64)

1. Kim S, Iizuka K, Aguila HL, et al. In vivo natural killer cell activities revealed by natural killer cell- deficient mice. Proc Natl Acad Sci U S A 2000;97:2731-6.
2. Lanier LL. On guard - activating NK cell receptors. Nat Immunol 2001;2:23-7.
3. Ogawa K, Hirai M, Katsube T, et al. Suppression of cellular immunity by surgical stress. Surgery 2000;127:329-36.
4. Ben-Eliyahu S. The promotion of tumor metastasis by surgery and stress: immunological basis and implications for psychoneuroimmunology (PNI). Brain Behav Immun 2003;17:S27-S36.
5. Ben-Eliyahu S, Page GG, Yirmiya R, Shakhar G. Evidence that stress and surgical interventions promote tumor development by suppressing natural killer cell activity. Int J Cancer 1999;80: 880-8.
6. Zoller M, Heumann U, Betzler M, et al. Depression of nonadaptive immunity after surgical stress: influence on metastatic spread. Invasion Metastasis 1989;9:46-68.
7. Toft P, Dagnaes-Hansen F, Tonnesen E, Basse PM. The effect of surgical stress and endotoxin-induced sepsis on the NK-cell activity, distribution and pulmonary clearance of YAC-1 and melanoma cells. APMIS 1999;107:359-64.
8. Da Costa ML, Redmond P, Bouchier-Hayes DJ. The effect of laparotomy and laparoscopy on the establishment of spontaneous tumor metastases. Surgery 1998;124:516-25.
9. Liedtke CM. Differentiated properties of rabbit tracheal epithelial cells in primary culture. Am J Physiol 1988;255(6 Pt 1):C760-70.
10. Ueda F, Ideguchi K, Taniguchi N, Kimura K. Adrenergic regulation of prostaglandin biosynthesis in cultured rabbit gastric epithelial cells. Jpn J Pharmacol 1994;65:113-20.
11. Baxevanis CN, Reclos GJ, Gritzapis AD, et al. Elevated prostaglandin E2 production by monocytes is responsible for the depressed levels of natural killer and lymphokine-activated killer cell function in patients with breast cancer. Cancer 1993;72:491-501.
12. Skibinski G, Kelly RW, Harrison CM, et al. Relative immunosuppressive activity of human seminal prostaglandins. J Reprod Immunol 1992;22:185-95.
13. Specht C, Bexten S, Kolsch E, Pauels HG. Prostaglandins, but not tumor-derived IL-10, shut down concomitant tumor-specific CTL responses during murine plasmacytoma progression. Int J Cancer 2001;91:705-12.
14. Goodwill JS, Ceuppens J. Regulation of the immune response by prostaglandins. J Clin Immunol 1983;3:295-315.
15. Uotila P. The role of cyclic AMP and oxygen intermediates in the inhibition of cellular immunity in cancer. Cancer Immunol Immunother 1996;43:1-9.
16. Leung KH, Koren HS. Regulation of human natural killing. III. Mechanism for interferon induction of loss of susceptibility to suppression by cyclic AMP elevating agents. J Immunol 1984;132: 1445-50.
17. Rhind SG, Gannon GA, Suzui M, et al. Indomethacin inhibits circulating PGE2 and reverses postexercise suppression of natural killer cell activity. Am J Physiol 1999;276(5 Pt 2):R1496-505.
18. Nieman DC, Ahle JC, Henson DA, et al. Indomethacin does not alter natural killer cell response to 2.5 h of running. J Appl Physiol 1995;79:748-55.
19. Leung KH. Inhibition of human NK cell and LAK cell cytotoxicity and differentiation by PGE2. Cell Immunol 1989;123:384-95.
20. Garcia-Penarrubia P, Bankhurst AD, Koster FT. Prostaglandins from human T suppressor/cytotoxic cells modulate natural killer antibacterial activity. J Exp Med 1989;170:601-6.
21. Lauzon W, Lemaire I. Alveolar macrophage inhibition of lung-associated NK activity: involvement of prostaglandins and transforming growth factor-beta 1. Exp Lung Res 1994;20:331-49.
22. Goodwill JS, Webb DR. Regulation of the immune response by prostaglandins. Clin Immunol Immunopathol 1980;15:106-22.
23. Baxevanis CN, Papilas K, Dedoussis GV, et al. Abnormal cytokine serum levels correlate with impaired cellular immune responses after surgery. Clin Immunol Immunopathol 1994;71:82-8.
24. Vitoratos N, Hassiakos D, Louridas C, et al. Prostaglandin F1a and prostaglandin E2 plasma levels after transvaginal cervical cerclage. Clin Exp Obstet Gynecol 1996;23:21-5.
25. Brinkmann A, Seeling W, Wolf CF, et al. Ibuprofen does not impair renal function in patients undergoing infrarenal aortic surgery with epidural anaesthesia. Intensive Care Med 1998;24:322-8.
26. Okuno K, Jinnai H, Lee YS, et al. A high level of prostaglandin E2 (PGE2) in the portal vein suppresses liver-associated immunity and promotes liver metastases. Surg Today 1995;25:954-8.
27. Parsson HN, Lord RS, Scott K, Zemack G. Maintaining carotid flow by shunting during carotid endarterectomy diminishes the inflammatory response mediating ischaemic brain injury. Eur J Vasc Endovasc Surg 2000;19:124-30.
28. Bash JA, Vogel D. Cellular immunosenescence in F344 rats: decreased natural killer (NK) cell activity involves changes in regulatory interactions between NK cells, interferon, prostaglandin and macrophages. Mech Ageing Dev 1984;24:49-65.
29. Koren HS, Leung KH. Modulation of human NK cells by interferon and prostaglandin E2. Mol Immunol 1982;19:1341-6.
30. Ben-Eliyahu S, Shakhar G. The impact of stress, catecholamines, and the menstrual cycle on NK activity and tumor development: from in vitro studies to biological significance. In: Ader R, Felten DL, Cohen N, eds. Psychoneuroimmunology, vol 2. San Diego: Academic Press, 2001:545-63.
31. Hellstrand K, Hermodsson S, Strannegard O. Evidence for a beta-adrenoceptor-mediated regulation of human natural killer cells. J Immunol 1985;134:4095-9.
32. Huribal M, Cunningham ME, D'Aiuto ML, et al. Endothelin-1 and prostaglandin E2 levels increase in patients with burns. J Am Coll Surg 1995;180:318-22.
33. Ben-Eliyahu S, Page GG, Shakhar G, Taylor AN. Increased susceptibility to metastasis during pro-oestrus/oestrus in rats: possible role of oestradiol and natural killer cells. Br J Cancer 1996;74:1900-7.
34. Page GG, Ben-Eliyahu S, Liebeskind JC. The role of LGL/NK cells in surgery-induced promotion of metastasis and its attenuation by morphine. Brain Behav Immun 1994;8:241-50.
35. Barlozzari T, Leonhardt J, Wiltrout RH, et al. Direct evidence for the role of LGL in the inhibition of experimental tumor metastases. J Immunol 1985;134:2783-9.
36. Barlozzari T, Reynolds CW, Herberman RB. In vivo role of natural killer cells: involvement of large granular lymphocytes in the clearance of tumor cells in anti-asialo GM1-treated rats. J Immunol 1983;131:1024-7.
37. Shakhar G, Ben-Eliyahu S. In vivo beta-adrenergic stimulation suppresses natural killer activity and compromises resistance to tumor metastasis in rats. J Immunol 1998;160:3251-8.
38. Page GG, Ben-Eliyahu S. A role for NK cells in greater susceptibility of young rats to metastatic formation. Dev Comp Immunol 1999;23:87-96.
39. Hodgson DM, Yirmiya R, Chiappelli F, Taylor AN. Intracerebral interleukin-1beta impairs response to tumor invasion: involvement of adrenal catecholamines. Brain Res 1999;816:200-8.
40. Yirmiya R, Ben-Eliyahu S, Gale RP, et al. Ethanol increases tumor progression in rats: possible involvement of natural killer cells. Brain Behav Immun 1992;6:74-86.
41. dim subpopulations of rat natural killer cells. J Immunol 1992;148:3658-65.
42. Chambers WH, Vujanovic NL, DeLeo AB, et al. Monoclonal antibody to a triggering structure expressed on rat natural killer cells and adherent lymphokine-activated killer cells. J Exp Med 1989;169:1373-89.
43. Ben-Eliyahu S, Page GG. In vivo assessment of natural killer cell activity in rats. Prog Neuroendocrineimmunol 1992;5:199-214.
44. Ben-Eliyahu S, Page GG, Yirmiya R, Taylor AN. Acute alcohol intoxication suppresses natural killer cell activity and promotes tumor metastasis. Nat Med 1996;2:457-60.
45. von Horsten S, Helfritz A, Kuhlmann S, et al. Stereological quantification of carboxyfluorescein-labeled rat lung metastasis: a new method for the assessment of natural killer cell activity and tumor adhesion in vivo and in situ. J Immunol Methods 2000;239:25-34.
46. Ben-Eliyahu S, Abudarham N, Shakhar G, et al. Protecting cellular immunity from suppression by surgery and stress hormones: an approach to prevent surgery-induced tumor progression (abstract). Brain Behav Immun 2002;16:176.
47. Shingu K, Helfritz A, Kuhlmann S, et al. Kinetics of the early recruitment of leukocyte subsets at the sites of tumor cells in the lungs: natural killer (NK) cells rapidly attract monocytes but not lymphocytes in the surveillance of micrometastasis. Int J Cancer 2002;99:74-81.
48. Kong LY, Luster MI, Dixon D, et al. Inhibition of lung immunity after intratracheal instillation of benzo(a)pyrene. Am J Respir Crit Care Med 1994;150:1123-9.
49. Ben-Eliyahu S, Shakhar G, Rosenne E, et al. Hypothermia in barbiturate-anesthetized rats suppresses natural killer cell activity and compromises resistance to tumor metastasis: a role for adrenergic mechanisms. Anesthesiology 1999;91:732-40.
50. Page GG, Ben Eliyahu S, Yirmiya R, Liebeskind JC. Morphine attenuates surgery-induced enhancement of metastatic colonization in rats. Pain 1993;54:21-8.
51. Bothwell W, Verburg M, Wynalda M, et al. A radioimmunoassay for the unstable pulmonary metabolites of prostaglandin E1 and E2: an indirect index of their in vivo disposition and pharmacokinetics. J Pharmacol Exp Ther 1982;220:229-35.
52. Huang M, Sharma S, Mao JT, Dubinett SM. Non-small cell lung cancer-derived soluble mediators and prostaglandin E2 enhance peripheral blood lymphocyte IL-10 transcription and protein production. J Immunol 1996;157:5512-20.
53. Chambrier C, Chassard D, Bienvenu J, et al. Cytokine and hormonal changes after cholecystectomy. Effect of ibuprofen pretreatment. Ann Surg 1996;224:178-82.
54. Wojtowicz-Praga S. Reversal of tumor-induced immunosuppression: a new approach to cancer therapy. J Immunother 1997;20:165-77.
55. Menetrier-Caux C, Bain C, Favrot MC, et al. Renal cell carcinoma induces interleukin 10 and prostaglandin E2 production by monocytes. Br J Cancer 1999;79:119-30.
56. Carter JJ. The immunologic consequences of laparoscopy in oncology. Surg Oncol Clin North Am 2001;10:655-77.
57. Brittenden J, Heys SD, Ross J, Eremin O. Natural killer cells and cancer. Cancer 1996;77:1226-43.
58. Andreesen R, Hennemann B, Krause SW. Adoptive immunotherapy of cancer using monocyte-derived macrophages: rationale, current status, and perspectives. J Leukoc Biol 1998;64:419-26.
59. Fidler IJ. Therapy of cancer metastasis by systemic activation of macrophages. Adv Pharmacol 1994;30:271-326.
60. Faist E, Schinkel C, Zimmer S. Update on the mechanisms of immune suppression of injury and immune modulation. World J Surg 1996;20:454-9.
61. Koda K, Saito N, Takiguchi N, et al. Preoperative natural killer cell activity: correlation with distant metastases in curatively research colorectal carcinomas. Int Surg 1997;82:190-3.
62. McCoy JL, Rucker R, Petros JA. Cell-mediated immunity to tumor-associated antigens is a better predictor of survival in early stage breast cancer than stage, grade or lymph node status. Breast Cancer Res Treat 2000;60:227-34.
63. Fujisawa T, Yamaguchi Y. Autologous tumor killing activity as a prognostic factor in primary resected nonsmall cell carcinoma of the lung. Cancer 1997;79:474-81.
64. Schantz SP, Brown BW, Lira E, et al. Evidence for the role of natural immunity in the control of metastatic spread of head and neck cancer. Cancer Immunol Immunother 1987;25:141-8.