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Eicosanoids and the immunology of cancer

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Summary

Studies in both cancer patients and in animal tumor models have shown that immune defenses can mediate destruction of tumor, but these defenses are often functioning at a suppressed or suboptimal level. Frequently, prostaglandins, mainly PGE2, have been implicated in this tumor-associated subversion of immune function, with immune reactivities to tumor typically being enhanced by prostaglandin synthesis inhibitor. Both the tumor and tumor-induced host immune suppressive macrophages have the capacity to suppress immune functions through their production of PGE2. Although the inhibitory functions have been more widely studied, recent evaluations of the effects of PGE2 have led to the surprising realization that not all of the PGE2's effects are inhibitory to immune function. Summarized below are some of the well characterized inhibitory effects of PGE2, as well as the lesser studied stimulatory effects of PGE2 toward the effector cells that are considered to be important in the immune defense against cancer.

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References

  1. Katz AE: Update on immunology of head and neck cancer. Med Clin N Am 77: 625–631, 1993

    Google Scholar 

  2. McGrath PC, Hamby LS, Freeman JW: Phorbol dibutyrate plus ionomycin improves the generation of cytotoxic T cells from draining lymph nodes of patients with advanced head and neck cancer. Am J Surgery 164: 610–614, 1992

    Google Scholar 

  3. Pisani RJ: Bronchogenic carcinoma: immunologic aspects. Mayo Clin Proc 68: 386–392, 1993

    Google Scholar 

  4. Faradji A, Bahbot A, Schmitt-Goguel M, Roeslin N, Dumont S, Wiesel ML, Lallot C, Eber M, Bartholeyns J, Poindron P: Phase I trial of intravenous infusion ofex-vivo-activated autologous blood-derived macrophages in patients with non-small cell lung cancer: toxicity and immunomodulatory effects. Cancer Immunol Immunother 33: 319–326, 1991

    Google Scholar 

  5. Whiteside TL, Letessier E, Hirabayashi H, Vitolo D, Bryant J, Barnmes L, Snyderman C, Johnson JT, Myers E, Herbermann RB, Rubin J, Kirkwood JM, Vlock DR: Evidence for local and systemic activation of immune cells by peritumoral injections of interleukin 2 in patients with advanced squamous cell carcinoma of the head and neck. Cancer Res 53: 5654–5662, 1993

    Google Scholar 

  6. Yoshino I, Yano T, Murata M, Ishida T, Sugimachi K, Kimura G: Tumor-reactive T-cells accumulate in lung cancer tissues but fail to respond due to tumor cell-derived factor. Cancer Res 52: 775–781, 1992

    Google Scholar 

  7. Lakhdar M, Ben Aribia MH, Maalej M, Ladgham A: Selective homing of phenotypically lytic cells within nasopharyngeal carcinoma biopsies: numerous CD8- and CD16-positive cells in the tumor. Int J Cancer 48: 57–61, 1991

    Google Scholar 

  8. Komaki G, Arimura A, Koves K: Effect of intravenous injection on IL-1 beta on PGE2 levels in several brain areas as determined by microdialysis. Am J Physiology 262: E246-E251, 1992

    Google Scholar 

  9. Lazio M, Calabrese F, Coluccia C, Giacomasso S, Casadio C, Mancuso M, Negril L, Mastromatteo V: The LMI test in colon, breast and lung cancer long survivors. Panminerva Med 34: 60–64, 1992

    Google Scholar 

  10. Stewart TH, Hollinshead AC, Raman S: Tumour dormancy: initiation, maintenance and termination in animals and humans. Can J Surg 34: 321–325, 1991

    Google Scholar 

  11. Zocchi MR, Ferrarini M, Rugarli C: Selective lysis of the autologous tumor by delta TCS1+ gamma/delta+ tumor-infiltrating lymphocytes from human lung carcinomas. Eur J Immunol 20: 2685–2689, 1990

    Google Scholar 

  12. Yoshino I, Yano T, Yoshikai Y, Murata M, Sugimachi K, Kimura G, Nomoto K: Oligoclonal T lymphocytes infiltrating human lung cancer tissues. Int J Cancer 47: 654–658, 1991

    Google Scholar 

  13. Stanojevic-Bakic N, Vuckovic-Dekic L, Susnjar S, Spuzic I:In vitro effect of indomethacin on mitogen-induced lymphoproliferative response in lung cancer patients. Neoplasma 39: 129–132, 1992

    Google Scholar 

  14. Farinas MC, Rodriguez-Valverde V, Zarrabeitia MT, Parra-Blanco JA, Sanz-Ortiz J: Contribution of monocytes to the decreased lymphoproliferative response to phytohemagglutinin in patients with lung cancer. Cancer 68: 1279–1284, 1991

    Google Scholar 

  15. Yano T, Ishida T, Yoshino I, Murata M, Yasumoto K, Kimura G, Nomoto K, Sugimachi K: A regimen of surgical adjuvant immunotherapy for cancer with interleukin 2 and lymphokine-activated killer cells. Biotherapy 32: 245–251, 1992

    Google Scholar 

  16. Bukowski RM, Sharfman W, Murthy S, Rayman P, Tubbs R, Alexander J, Budd GT, Sergi JS, Bauer L, Gibson V, Stanley J, Boyett J, Pontes E, Finke J: Clinical results and characterization of tumor-infiltrating lymphocytes with or without recombinant interleukin 2 in human metastatic renal cell carcinoma. Cancer Res 51: 4199–4205, 1991

    Google Scholar 

  17. Scudeletti M, Filaci G, Imro MA, Motta G, Di Gaetano M, Pierri I, Tongiani S, Indiveri F, Puppo F: Immunotherapy with intralesional and systemic interleukin-2 of patients with non-small-cell lung cancer. Cancer Immunol Immunother 37: 119–124, 1993

    Google Scholar 

  18. Yoshizawa H, Chang AE, Shu S: Cellular interactions in effector cell generation and tumor regression mediated by anti-CD3/interleukin 2-activated tumor-draining lymph node cells. Cancer Res 52: 1129–1136, 1992

    Google Scholar 

  19. Urba SG, Forastiere AA, Wolf GT, Amrein PC: Intensive recombinant interleukin-2 and alpha-interferon therapy in patients with advanced head and neck squamous carcinoma. Cancer 71: 2326–2331, 1993

    Google Scholar 

  20. Edwards MJ, Miller FN, Sims DE, Abney DL, Schuschke DA, Corey TS: Interleukin 2 acutely induces platelet and neutrophil-endothelial adherence and macromolecular leakage. Cancer Res 52: 3425–3431, 1992

    Google Scholar 

  21. Maas RA, Dullens HF, Den Otter W: Interleukin-2 in cancer treatment: disappointing or (still) promising? Cancer Immunol Immunother 36: 141–148, 1993

    Google Scholar 

  22. Sosman JA, Weiss GR, Margolin DA, Aronson FR, Sznol M, Atkins MB, O'Boyle K, Fisher RI, Boldt DH, Doroshow J,et al.: Phase IB clinical trial of anti-CD3 followed by highdose bolus interleukin-2 in patients with metastatic melanoma and advanced renal cell carcinoma: clinical and immunologic effects. J Clin Oncol 11: 1496–1505, 1993

    Google Scholar 

  23. Gately MK, Desai BB, Wolitzky AG, Quinn PM, Dwyer CM, Podlaski FJ, Familletti PC, Sinigaglia F, Chizonnite R, Gubler U, Stem AS: Regulation of human lymphocyte proliferation by a heterodimeric cytokine, IL-12 (cytotoxic lymphocyte maturation factor). J Immunol 147: 874–882, 1991

    Google Scholar 

  24. Bertagnolli MM, Lin B, Young D, Herrmann SH: IL-12 augments antigen-dependent proliferation of activated T lymphocytes. J Immunol 149: 3378–3783, 1992

    Google Scholar 

  25. Gately MK, Wolitzky AG, Quinn PM, Chizzonite R: Regulation of human cytolytic lymphocyte responses by interleukin-12. Cell Immunol 143: 127–142, 1992

    Google Scholar 

  26. Perussia B, Chan SH, D'Andrea A, Tsuji K, Santoli D, Pospisil M, Young D, Wolf F, Trinchieri G: Natural killer (NK) cell stimulatory factor or IL-12 has differential effects on the proliferation of TCR-alpha beta+ TCR-gamma delta+ T lymphocytes, and NK cells. J Immunol 149: 3495–3502, 1992

    Google Scholar 

  27. Verstovsek S, Maccubin D, Ehrke MJ, Mihich E: Tumoricidal activation of murine resident peritoneal macrophages by interleukin 2 and tumor necrosis factor α. Cancer Res 52: 3880–3885, 1992

    Google Scholar 

  28. Liebes L, Walsh CM, Chachoua A, Oratz R, Richards D, Hochster H, Peace D, Marino D, Alba S, Le Sher D, Blum RH, Vilcek J: Modulation of monocyte functions by muramyl tripeptide phosphatidylethanolamine in a phase II study in patients with metastatic melanoma. J Natl Cancer Inst 84: 694–699, 1992

    Google Scholar 

  29. Fidler IJ: Systemic macrophage activation with liposomeentrapped immunomodulators for therapy of cancer metastasis. Res Immunol 143: 199–204, 1992

    Google Scholar 

  30. Watson J, Chuah SY: Technique for the primary culture of human breast cancer cells and measurement of their prostaglandin secretion. Clin Sci 83: 347–352, 1992

    Google Scholar 

  31. Klapan I, Katic V, Culo F, Sabolovic D, Cuk V, Fumic K, Simovic S: Lipid-bound sialic acid, prostaglandin E and histamine in head and neck cancer. Eur J Cancer 29A: 839–845, 1993

    Google Scholar 

  32. Kubota Y, Sunouchi K, Ono M, Sawada T, Muto T: Local immunity and metastasis of colorectal carcinoma. Dis Colon Rectum 35: 645–650, 1992

    Google Scholar 

  33. Rigas B, Goldman IS, Levine L: Altered eicosanoid levels in human colon cancer. J Lab Clin Med 122: 518–523, 1993

    Google Scholar 

  34. Iizumi T, Yazaki T, Umeda T, Soma G: Promotion of metastases by tumor necrosis factor in rats bearing Dunning R3327 MAT-LyLu prostatic cancer. Urologia Int 51: 85–88, 1993

    Google Scholar 

  35. Young MRI, Duffie GP, Lozano Y, Young ME, Wright MA: Association of a functional prostaglandin E2-protein kinase A coupling with responsiveness of metastatic Lewis lung carcinoma variants to prostaglandin E2 and to prostaglandin E2-producing nonmetastatic Lewis lung carcinoma variants. Cancer Res 50: 2973–2978, 1990

    Google Scholar 

  36. Lapointe H, Lampe H, Banerjee D: Head and neck squamous cell carcinoma cell line-induced suppression ofin vitro lymphocyte proliferative responses. Otolaryngology 106: 149–158, 1992

    Google Scholar 

  37. Cross DS, Platt JL, Juhn SK, Bach FH, Adam GL: Administration of a prostaglandin synthetase inhibitor associated with an increased immune cell infiltrate in squamous cell carcinoma of the head and neck. Arch Otolaryngol Head Neck Surg 118: 526–528, 1992

    Google Scholar 

  38. Valdez JC, Mercau G, Vitalone H, Perdigon G: Histological study of murine fibrosarcoma treated with prostaglandin inhibitors. Int J Immunopathol Pharmacol 5: 201–206, 1992

    Google Scholar 

  39. Nakazawa I, Iwaizumi M, Ohuchi K: A difference in prostaglandin-producing ability between cancer cells metastasized into liver and kidney. Tohoku J Exp Med 165: 299–304, 1991

    Google Scholar 

  40. Young MRI, Okada F, Tada M, Hosokawa M, Kobayashi H: Association of increased tumor cell responsiveness to prostaglandin E2 with more aggressive tumor behavior. Invasion Met 11: 48–57, 1991

    Google Scholar 

  41. Young MRI, Young ME, Lozano Y, Coogan M, Bagash JM: Regulation of protein kinase A activation and prostaglandin E2-stimulated migration of Lewis lung carcinoma clones. Int J Cancer 49: 150–155, 1991

    Google Scholar 

  42. Young MRI, Young ME, Lozano Y, Bagash JM: Activation of protein kinase A increases thein vitro invasion, migration, and adherence to reconstituted basement membrane by Lewis lung carcinoma tumor cells. Invasion Met 12: 253–263, 1992

    Google Scholar 

  43. Young MRI, Lozano Y, Djordjevic A, Maier GD: Protein phosphatases limit tumor motility. Int J Cancer 54: 1036–1041, 1993

    Google Scholar 

  44. Young MR, Young ME: Effects of fish oil diets on prostaglandin-dependent and myelopoiesis-associated immune suppressor mechanisms of mice bearing metastatic Lewis lung carcinoma tumors. Cancer Res 49: 1931–1936, 1989

    Google Scholar 

  45. Young MRI, McCloskey G, Wright MA, Schmidt Pak A: Increasing infiltration and activation of CD8+ tumor-infiltrating lymphocytes after eliminating immune suppressive granulocyte-macrophage progenitor cells with low doses of interferon-γ plus tumor necrosis factor-α. Cancer Immunol Immunother 38: 9–15, 1994

    Google Scholar 

  46. Walker TM, Yurochko AD, Burger CJ, Elgert KD: Cytokines and suppressor macrophages cause tumor-bearing host CD-8+ T cells to suppress recognition of allogeneic and syngeneic MHC class II molecules. J Leuko Biol 52: 661–669, 1992

    Google Scholar 

  47. Alleva DG, Burger CJ, Elgert KD: Interferon-gamma reduces tumor-induced Ia− macrophage-mediated suppression: role of prostaglandin E2, Ia, and tumor necrosis factoralpha. Immunopharmacol 25: 215–227, 1993

    Google Scholar 

  48. Alleva DG, Burger CJ, Elgert KD: Tumor growth increases Ia− macrophage synthesis of tumor necrosis factor-α and prostaglandin E2: changes in macrophage suppressor activity. J Leukocyte Biol 53: 550–558, 1993

    Google Scholar 

  49. Walker TM, Yurochko AD, Burger CJ: Ia− macrophages and cytokine networks contribute to tumor-induced suppression of CD4+ autoreactive T cells. Immunol Invest 22: 169–187, 1993

    Google Scholar 

  50. Young MRI, Wright MA: Myelopoiesis-associated immune suppressor cells in mice bearing metastatic Lewis lung carcinoma tumors: interferon-γplus tumor necrosis factor-α synergistically reduce immune suppressor and tumor growth-promoting activities of bone marrow cells, and diminish tumor recurrence and metastasis. Cancer Res 52: 6335–6340, 1992

    Google Scholar 

  51. Young MRI, Wright MA, Coogan M, Young ME, Bagash J: Tumor-derived cytokines induce bone marrow suppressor cells that mediate immunosuppression through transforming growth factor β. Cancer Immunol Immunother 35: 14–18, 1992

    Google Scholar 

  52. Young MRI, Wright MA, Young ME: Antibodies to colonystimulating factors block Lewis lung carcinoma cell-stimulation of immune suppressive bone marrow cells. Cancer Immunol Immunother 33: 146–152, 1991

    Google Scholar 

  53. Inge TH, Hoover SK, Frank JL, Kawabata TT, Bethke KP, Bear HD: Enhancement of cytotoxic T lymphocyte growth from spleens of P815-tumor-bearing host mice with mafosfamide. Cancer Immunol Immunother 35: 119–126, 1992

    Google Scholar 

  54. Khoo NK, Chan FP, Saarloos MN, Lala PK: Immunotherapy of mammary adenocarcinoma metastases in C3H/HeN mice with chronic administration of cyclo-oxygenase inhibitors alone or in combination with IL-2. Clin Exp Metastasis 10: 239–252, 1992

    Google Scholar 

  55. Gelin J, Andersson C, Lundholm K: Effects of indomethacin, cytokines, and cyclosporin A on tumor growth and the subsequent development of cancer cachexia. Cancer Res 51: 880–885, 1991

    Google Scholar 

  56. Bursuker I, Petty BA, Neddermann KM, Keller LS: Immunomodulation in an apparently non-immunogenic murine tumor. Int J Cancer 49: 414–420, 1991

    Google Scholar 

  57. Oghiso Y, Yamada Y, Ando K, Ishihara H, Shibata Y: Differential induction of prostaglandin E2-dependent and -independent immune suppressor cells by tumor-derived GM-CSF and M-CSF. J Leuko Biol 53: 86–92, 1993

    Google Scholar 

  58. Fu Y-X, Watson GA, Kasahara M, Lopez DM: The role of tumor-derived cytokines on the immune system of mice bearing a mammary adenocarcinoma. I. Induction of regulatory macrophages in normal mice by thein vivo administration of rGM-CSF. J Immunol 146: 783–789, 1991

    Google Scholar 

  59. Beckerman KP, Schreiber RD, Needleman P: Cytokine modulation of immune activation associated suppression of macrophage cyclooxygenase activityin vivo. Prostaglandins Leukotrienes Essential Fatty Acids 47: 231–238, 1992

    Google Scholar 

  60. Diaz A, Reginato AM, Jimenez SA: Alternative splicing of human prostaglandin G/H synthase messenger RNA and evidence of differential regulation of the resulting transcripts by transforming growth factor-beta1, interleukin-1beta, and tumor necrosis factor-alpha. J Biol Chem 267: 10816–10822, 1992

    Google Scholar 

  61. Shibata Y, McCaffrey PG, Minowada J, Volkman A, Oghiso Y: Regulation of phospholipase A2 activation and arachidonic acid metabolism in an interleukin-3-dependent macrophage-like cell line. J Leukocyte Biol 51: 32–38, 1992

    Google Scholar 

  62. Baxevanis CN, Reclos GJ, Gritzapis AD, Dedousis GV, Missitzis I, Papamichail M: 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 72: 491–501, 1993

    Google Scholar 

  63. Braun DP, Ahn M, Harris JE, Chu E, Casey L, Wilbands G, Siziopikou KP: Sensitivity of tumoricidal function in macrophages from different anatomical sites of cancer patients to modulation of arachidonic acid metabolism. Cancer Res 53: 3362–3368, 1993

    Google Scholar 

  64. Li T-K, Fox SB: Effect of prostaglandin E2 (PGE2) on IL-3/granulocyte-macrophage colony-stimulating factor production by T helper cells. J Immunol 150: 1680–1690, 1993

    Google Scholar 

  65. Cox FEG, Liew FY: T-cell subsets and cytokines in parasitic infections. Immunol Today 13: 445–448, 1992

    Google Scholar 

  66. Ferreri NR, Sarr T, Askenase PW, Ruddle NH: Molecular regulation of necrosis factor-alpha and lymphotoxin production in T cells. Inhibition by prostaglandin E2. J Biol Chem 267: 9443–9449, 1992

    Google Scholar 

  67. Phipps RP, Stein SH, Roper RL: A new view of prostaglandin E regulation of the immune response. Immunol Today 12: 349–351, 1991

    Google Scholar 

  68. Sunder-Plabmann R, Majdic O, Knapp W, Holter W:In vitro andin vivo activated T cells display increased sensitivity to PGE2. Cell Immunol 138: 289–299, 1991

    Google Scholar 

  69. Ertel W, Singh G, Morrison MH, Ayala A, Chaudry IH: Chemically induced hypotension increases PGE2 release and depresses macrophage antigen presentation. Am J Physiol 264: 655–660, 1993

    Google Scholar 

  70. Raddassi K, Petit JF, Lemaire G: LPS-induced activation of primed murine peritoneal macrophages is modulated by prostaglandins and cyclic nucleotides. Cell Immunol 149: 50–64, 1993

    Google Scholar 

  71. Buchmuller-Rouiller Y, Betz-Corradin S, Mauel J: Differential effects of prostaglandins on macrophage activation induced by calcium ionophore A23178 or INF-γ. J Immunol 148: 1171–1175, 1992

    Google Scholar 

  72. Utsugi T, Fidler IJ: Prostaglandin E2 does not inhibit tumoricidal activity of mouse macrophages against adherent tumor cells. J Immunol 146: 2066–2071, 1991

    Google Scholar 

  73. Rahal MD, Reinish E, Osmond DG: Changes in the populations of null, NK1.1+, and Thyl1° lymphocytes in the bone marrow of tumor-bearing mice: effect of indomethacin treatment. Cell Immunol 139: 218–228, 1992

    Google Scholar 

  74. Vaillier D, Daculski R, Gualde N, Bezian JH: Effect of LTB4 on the inhibition of natural cytotoxic activity by PGE2. Cell Immunol 139: 248–258, 1992

    Google Scholar 

  75. Anastassiou ED, Paliogianni F, Balow JP, Yamada H, Boumpas DT: Prostaglandin E2 and other cyclic AMP-elevating agents modulate IL-2 and IL-2R gene expression at multiple levels. J Immunol 148: 2845–2852, 1992

    Google Scholar 

  76. Laude M, Siessmann KL, Mokyr MB, Dray S: Advantages of adoptive chemoimmunotherapy with polyethylene glycol-cultured, antigen-activated, tumor-infiltrated spleen cells for the complete eradication of lethal MOPC-315 plasmacytomas. Cancer Res 51: 4516–4522, 1991

    Google Scholar 

  77. Young MR, Wheeler E, Newby M: Macrophage-mediated suppression of natural killer cell activity in mice bearing Lewis lung carcinoma. J Natl Cancer Inst 76: 745–750, 1986

    Google Scholar 

  78. Young MR, Hoover CS: Inhibition of the spleen cell cytotoxic capacity toward tumor by the elevated prostaglandin E2 levels in mice bearing Lewis lung carcinoma. J Natl Cancer Inst 77: 425–429, 1986

    Google Scholar 

  79. Young MR, Knies S: Prostaglandin E production by Lewis lung carcinoma: Mechanism for tumor establishmentin vivo. J Natl Cancer Inst 72: 919–922, 1984

    Google Scholar 

  80. Lala PK, Parhar RS: Eradication of spontaneous and experimental adenocarcinoma metastases with chronic indomethacin and intermittent IL-2 therapy. Int J Canc 54: 677–684, 1993

    Google Scholar 

  81. Thun MJ, Namboodiri MM, Calle EE, Flanders WD, Heath CWJ: Aspirin use and risk of fatal cancer. Cancer Res 53: 1322–1327, 1993

    Google Scholar 

  82. Mertens WC, Bramwell VH, Gwadry-Sridhar F, Romano W, Banerjee D, Lala PK: Effects of indomethacin plus ranitidine in advanced melanoma patients on high-dose interleukin-2. Lancet 340: 397–398, 1992

    Google Scholar 

  83. Sato NL, Fujisawa N, Kato A, Maeda Y, Yamamoto Y: Tumor dormancy and the effect of selected drugs on the tumordormant state. Lab Anim Sci 42: 555–560, 1992

    Google Scholar 

  84. Fulton AM, Chong YC: Prostaglandin E2 receptor activity and susceptibility to natural killer cells. J Leukocyte Biol 51: 176–180, 1992

    Google Scholar 

  85. Waymack JP, Klimpel G, Haithcoat J, Rutan RL, Herndon DN: Effect of prostaglandin E on immune function in normal healthy volunteers. Surg Gynecol Obstet 175: 329–332, 1992

    Google Scholar 

  86. Gaillard T, Mulsch A, Klein H, Decker K: Regulation by prostaglandin E2 of cytokine-elicited nitric oxide synthesis in rat liver macrophages. Biol Chem Hoppe-Seyler 373: 897–902, 1992

    Google Scholar 

  87. Young MR, Young ME, Kim K: Regulation of tumor-induced myelopoiesis and the associated immune suppressor cells in mice bearing metastatic Lewis lung carcinomas by prostaglandin E2. Cancer Res 48: 6826–6831, 1988

    Google Scholar 

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  1. Research Service, Department of Veterans Affairs, Hines VA Hospital, Hines, IL, USA

    M. Rita I. Young

  2. Department of Pathology, Loyola University Stritch School of Medicine, Maywood, IL, USA

    M. Rita I. Young

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Young, M.R.I. Eicosanoids and the immunology of cancer. Cancer Metast Rev 13, 337–348 (1994). https://doi.org/10.1007/BF00666103

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