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Allosensitized Helper and Cytotoxic T-lymphocyte Clones Differentially Modulate Endotoxin-Stimulated Macrophage Function

Allosensitized Helper and Cytotoxic T-lymphocyte Clones Differentially Modulate... Abstract • Alterations in macrophage function may render the immunocompromised host more susceptible to infectious complications. Although allograft recipients are at increased risk of infection primarily because of pharmacologic immunosuppression, whether the process of allosensitization per se alters this risk is unknown. We therefore studied the effects of cloned allosensitized murine helper or cytotoxic T cells on both interleukin 1 (IL-1) and prostaglandin E2 (PGE2) production by syngeneic resident murine peritoneal macrophages. Endotoxin (lipopolysaccharide [LPS]) stimulated both IL-1 and PGE2 production in macrophages. Cloned T cells alone, with or without LPS pretreatment, produced neither IL-1 nor PGE2. After 48 hours of coculture with LPS-treated macrophages, cloned helper cells augmented IL-1 release by macrophages but inhibited PGE2 production. In contrast, cytotoxic T cells not only reduced IL-1 production by macrophages but also potentiated PGE2 release. These effects were not observed when macrophages were not first exposed to LPS. Thus, endotoxin renders macrophages more susceptible to allosensitized "help" (↑ IL-1, ↓ PGE2) or "suppression" (↓ IL-1, ↑ PGE2) by cytotoxic T cells. We hypothesize that, even in the absence of immunosuppression, the process of allosensitization itself may modulate the response to sepsis by altering host macrophage function. (Arch Surg 1988;123:182-187) References 1. Matas AJ, Simmons RL, Najarian JS: Sepsis following kidney transplantation , in Hardy JD (ed): Critical Surgical Illness . Philadelphia, WB Saunders Co, 1980, pp 552-590. 2. Simmons RL, Weil R III, Tallent MB, et al: Do mild infections trigger the rejection of renal allografts? Transplant Proc 1970;2:419. 3. Jordan ML, Hoffman RA, Debe EF, et al: In vitro locomotion of allosensitized T lymphocyte clones in response to metabolites of arachidonic acid is subset specific . J Immunol 1986;137:661-668. 4. Mizel SB, Oppenheim JJ, Rosenstreich DL: Characterization of lymphocyte-activating factor (LAF) produced by the macrophage cell line P388D1: I. Enhancement of LAF production by activated T lymphocytes . J Immunol 1978;120:1497-1503. 5. Adams DO: Macrophage activation and secretion . Fed Proc 1982;41: 2193-2197. 6. Humes JL, Sadowski S, Galavage M, et al: Evidence for two sources of arachidonic acid for oxidative metabolism by mouse peritoneal macrophages . J Biol Chem 1982;257:1591-1594. 7. Rouyer CA, Scott WA, Kempe J, et al: Prostaglandin synthesis by macrophages requires a specific receptor-ligand interaction . Proc Natl Acad Sci USA 1980;77:4279-4282.Crossref 8. Amento EP, Kurnick JT, Krane SM: Interleukin 1 production by the human monocyte cell line U937 requires a lymphokine induction signal distinct from interleukin 2 or interferons . J Immunol 1985;134:350-357. 9. Unanue ER, Kiely JM, Calderon J: The modulation of lymphocyte functions by molecules secreted by macrophages: II. Conditions leading to increased secretion . J Exp Med 1976;144:155-166.Crossref 10. Kunkel SL, Chensue SW, Phan SH: Prostaglandins as endogenous mediators of interleukin 1 production . J Immunol 1986;136:186-192. 11. Christou NV, Mannick JA, West MA, et al: Lymphocyte-macrophage interactions in the response to surgical infections . Arch Surg 1987;22:239-251.Crossref 12. Shevach EM: Macrophages and other accessory cells , in Paul WE (ed): Fundamental Immunology . New York, Raven Press, 1984, pp 77-107. 13. Dinarello CA: Interleukin-1 . Rev Infect Dis 1984;6:51-95.Crossref 14. Aggarwal BB, Kohr PE, Moffat B, et al: Human tumor necrosis factor: Production, purification and characterization . J Biol Chem 1985; 260:2345-2354. 15. Kovacs EJ, Kelley J: Lymphokine regulation of macrophage-derived growth secretion following pulmonary injury . Am J Pathol 1985;21:261-268. 16. Jordan ML, Hoffman RA, Debe EF, et al: Prostaglandin E2 mediates subset-specific effects on the functional responses of allosensitized T lymphocyte clones . Transplantation 1987;43:117-123.Crossref 17. Goodwin JS, Ceuppens J: Regulation of the immune response by prostaglandins . J Clin Immunol 1983;3:295-315.Crossref 18. Ferreri NR, Howland WC, Spiegelberg HL: Release of leukotrienes C4 and B4 and prostaglandin E2 from human monocytes stimulated with aggregated IgG, IgA, and IgE . J Immunol 1986;136:4188-4193. 19. Jordan ML, Hoffman RA, Simmons RL: Leukotriene B4 (LTB4) augments IL2-dependent proliferation of T lymphocyte clones . Transplant Proc 1986;18:224-227. 20. Unanue ER: Antigen-presenting function of the macrophage . Ann Rev Immunol 1984;2:395.Crossref 21. Weaver CT, Unanue ER: T cell induction of membrane IL1 on macrophages . J Immunol 1986;137:3868-3873. 22. Steeg PS, Moore RN, Johnson H: Regulation of murine Ia antigen expression by a lymphokine with immune interferon activity . J Exp Med 1982;156:1780-1793.Crossref 23. Aderem AA, Cohen DS, Wright SD, et al: Bacterial lipopolysaccharides prime macrophages for enhanced release of arachidonic acid metabolites . J Exp Med 1986;164:165-179.Crossref 24. Rola-Pleszczynski M, Lemaine I: Leukotrienes augment interleukin 1 production by human monocytes . J Immunol 1985;135:3958-3961. 25. Fischer A, Durandy A, Griscellio G: Role of prostaglandin E2 at the induction of nonspecific T lymphocyte suppressive activities . J Immunol 1981;126:1452-1455. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of Surgery American Medical Association

Allosensitized Helper and Cytotoxic T-lymphocyte Clones Differentially Modulate Endotoxin-Stimulated Macrophage Function

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References (27)

Publisher
American Medical Association
Copyright
Copyright © 1988 American Medical Association. All Rights Reserved.
ISSN
0004-0010
eISSN
1538-3644
DOI
10.1001/archsurg.1988.01400260062007
Publisher site
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Abstract

Abstract • Alterations in macrophage function may render the immunocompromised host more susceptible to infectious complications. Although allograft recipients are at increased risk of infection primarily because of pharmacologic immunosuppression, whether the process of allosensitization per se alters this risk is unknown. We therefore studied the effects of cloned allosensitized murine helper or cytotoxic T cells on both interleukin 1 (IL-1) and prostaglandin E2 (PGE2) production by syngeneic resident murine peritoneal macrophages. Endotoxin (lipopolysaccharide [LPS]) stimulated both IL-1 and PGE2 production in macrophages. Cloned T cells alone, with or without LPS pretreatment, produced neither IL-1 nor PGE2. After 48 hours of coculture with LPS-treated macrophages, cloned helper cells augmented IL-1 release by macrophages but inhibited PGE2 production. In contrast, cytotoxic T cells not only reduced IL-1 production by macrophages but also potentiated PGE2 release. These effects were not observed when macrophages were not first exposed to LPS. Thus, endotoxin renders macrophages more susceptible to allosensitized "help" (↑ IL-1, ↓ PGE2) or "suppression" (↓ IL-1, ↑ PGE2) by cytotoxic T cells. We hypothesize that, even in the absence of immunosuppression, the process of allosensitization itself may modulate the response to sepsis by altering host macrophage function. (Arch Surg 1988;123:182-187) References 1. Matas AJ, Simmons RL, Najarian JS: Sepsis following kidney transplantation , in Hardy JD (ed): Critical Surgical Illness . Philadelphia, WB Saunders Co, 1980, pp 552-590. 2. Simmons RL, Weil R III, Tallent MB, et al: Do mild infections trigger the rejection of renal allografts? Transplant Proc 1970;2:419. 3. Jordan ML, Hoffman RA, Debe EF, et al: In vitro locomotion of allosensitized T lymphocyte clones in response to metabolites of arachidonic acid is subset specific . J Immunol 1986;137:661-668. 4. Mizel SB, Oppenheim JJ, Rosenstreich DL: Characterization of lymphocyte-activating factor (LAF) produced by the macrophage cell line P388D1: I. Enhancement of LAF production by activated T lymphocytes . J Immunol 1978;120:1497-1503. 5. Adams DO: Macrophage activation and secretion . Fed Proc 1982;41: 2193-2197. 6. Humes JL, Sadowski S, Galavage M, et al: Evidence for two sources of arachidonic acid for oxidative metabolism by mouse peritoneal macrophages . J Biol Chem 1982;257:1591-1594. 7. Rouyer CA, Scott WA, Kempe J, et al: Prostaglandin synthesis by macrophages requires a specific receptor-ligand interaction . Proc Natl Acad Sci USA 1980;77:4279-4282.Crossref 8. Amento EP, Kurnick JT, Krane SM: Interleukin 1 production by the human monocyte cell line U937 requires a lymphokine induction signal distinct from interleukin 2 or interferons . J Immunol 1985;134:350-357. 9. Unanue ER, Kiely JM, Calderon J: The modulation of lymphocyte functions by molecules secreted by macrophages: II. Conditions leading to increased secretion . J Exp Med 1976;144:155-166.Crossref 10. Kunkel SL, Chensue SW, Phan SH: Prostaglandins as endogenous mediators of interleukin 1 production . J Immunol 1986;136:186-192. 11. Christou NV, Mannick JA, West MA, et al: Lymphocyte-macrophage interactions in the response to surgical infections . Arch Surg 1987;22:239-251.Crossref 12. Shevach EM: Macrophages and other accessory cells , in Paul WE (ed): Fundamental Immunology . New York, Raven Press, 1984, pp 77-107. 13. Dinarello CA: Interleukin-1 . Rev Infect Dis 1984;6:51-95.Crossref 14. Aggarwal BB, Kohr PE, Moffat B, et al: Human tumor necrosis factor: Production, purification and characterization . J Biol Chem 1985; 260:2345-2354. 15. Kovacs EJ, Kelley J: Lymphokine regulation of macrophage-derived growth secretion following pulmonary injury . Am J Pathol 1985;21:261-268. 16. Jordan ML, Hoffman RA, Debe EF, et al: Prostaglandin E2 mediates subset-specific effects on the functional responses of allosensitized T lymphocyte clones . Transplantation 1987;43:117-123.Crossref 17. Goodwin JS, Ceuppens J: Regulation of the immune response by prostaglandins . J Clin Immunol 1983;3:295-315.Crossref 18. Ferreri NR, Howland WC, Spiegelberg HL: Release of leukotrienes C4 and B4 and prostaglandin E2 from human monocytes stimulated with aggregated IgG, IgA, and IgE . J Immunol 1986;136:4188-4193. 19. Jordan ML, Hoffman RA, Simmons RL: Leukotriene B4 (LTB4) augments IL2-dependent proliferation of T lymphocyte clones . Transplant Proc 1986;18:224-227. 20. Unanue ER: Antigen-presenting function of the macrophage . Ann Rev Immunol 1984;2:395.Crossref 21. Weaver CT, Unanue ER: T cell induction of membrane IL1 on macrophages . J Immunol 1986;137:3868-3873. 22. Steeg PS, Moore RN, Johnson H: Regulation of murine Ia antigen expression by a lymphokine with immune interferon activity . J Exp Med 1982;156:1780-1793.Crossref 23. Aderem AA, Cohen DS, Wright SD, et al: Bacterial lipopolysaccharides prime macrophages for enhanced release of arachidonic acid metabolites . J Exp Med 1986;164:165-179.Crossref 24. Rola-Pleszczynski M, Lemaine I: Leukotrienes augment interleukin 1 production by human monocytes . J Immunol 1985;135:3958-3961. 25. Fischer A, Durandy A, Griscellio G: Role of prostaglandin E2 at the induction of nonspecific T lymphocyte suppressive activities . J Immunol 1981;126:1452-1455.

Journal

Archives of Surgery – American Medical Association

Published: Feb 1, 1988

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