This Article  • References  • Full text PDF  • Send to a friend  • Save in My Folder  • Save to citation manager  • Permissions  Citing Articles  • Citation map  • Citing articles on HighWire  • Citing articles on Web of Science (137)  • Contact me when this article is cited  Related Content  • Similar articles in this journal  Social Bookmarking   What's this?

Interleukin-10 Suppression of T-Cell Response Is Mediated by Eicosanoid-Induced Interleukin-4 Release

Alfred Ayala, PhD; Donna L. Lehman; Crystal D. Herdon; Irshad H. Chaudry, PhD

Arch Surg. 1994;129(11):1172-1178.

Abstract
Objectives
To determine (1) whether interleukin-10 (IL-10) contributes to depressed T-cell responses observed following hemorrhage and (2) what effect other immunosuppressive agents known to play a role in hemorrhage have on IL-10 release.

Design
Hemorrhage was induced in C3H/HeN mice. The mice were resuscitated and then killed 2 hours after hemorrhage to obtain plasma, splenocytes, splenic macrophages, and splenic T cells.

Results and Conclusions
Decreased splenocyte/T-cell proliferation was associated with enhanced release of IL-10 by cells from hemorrhaged mice. However, unlike T cells, IL-10 release by macrophages was not comparatively elevated. While no changes were seen in systemic plasma levels of IL-10, the role of IL-10 as a localized immunosuppressant was demonstrated by the ability of IL-10 monoclonal antibody to restore T-cell proliferation following hemorrhage. Furthermore, elevated IL-10 release was prevented by the addition of ibuprofen or monoclonal antibody against transforming growth factor β or IL-6. Since these agents have direct or indirect influences on prostanoid synthesis, studies were carried out examining the capacity of varying concentrations of prostaglandin E₂ (PGE₂) to augment IL-10 release by murine cloned T_h2 cells (D10.G4.1) and by T cells from sham-operated or hemorrhaged mice. While the addition of PGE₂, 10–⁹ mol/L, potentiated the release of IL-10, this effect appears to be indirect, since the incorporation of monoclonal antibody to IL-4 prevented the release of IL-10 by PGE₂-treated cells from sham-operated or hemorrhaged mice. Such a mechanism of eicosanoid-induced IL-4/IL-10 cell-mediated immunosuppression may directly contribute to the decreased capacity to ward off infectious challenge seen following hemorrhage.

(Arch Surg. 1994;129:1172-1178)

Author Affiliations
From the Shock and Trauma Research Laboratories, Department of Surgery (Drs Ayala and Chaudry and Mss Lehman and Herdon), Microbiology (Dr Ayala), and Physiology (Dr Chaudry), Michigan State University, East Lansing.

CiteULike    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter     What's this?

THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES

The Evolving Rationale for Early Enteral Nutrition Based on Paradigms of Multiple Organ Failure: A Personal Journey
Moore and Moore
Nutr Clin Pract 2009;24:297-304.
FULL TEXT  

Invited review: Deterioration of the immune system after trauma: signals and cellular mechanisms
Flohe et al.
Innate Immunity 2008;14:333-344.
ABSTRACT  

Comparison of longitudinal leukocyte gene expression after burn injury or trauma-hemorrhage in mice
Lederer et al.
Physiol. Genomics 2008;32:299-310.
ABSTRACT | FULL TEXT  

Cell Response to Surgery
Ni Choileain and Redmond
Arch Surg 2006;141:1132-1140.
ABSTRACT | FULL TEXT  

Role of infection and bleeding in multiple organ involvement and failure
Akashi
Br. J. Radiol. 2005;Supplement_27:69-74.
ABSTRACT | FULL TEXT  

Gamma Interferon Does Not Enhance Clearance of Pseudomonas aeruginosa but Does Amplify a Proinflammatory Response in a Murine Model of Postseptic Immunosuppression
Murphey et al.
Infect. Immun. 2004;72:6892-6901.
ABSTRACT | FULL TEXT  

Akt Decreases Lymphocyte Apoptosis and Improves Survival in Sepsis
Bommhardt et al.
J. Immunol. 2004;172:7583-7591.
ABSTRACT | FULL TEXT  

Burn Injury Initiates a Shift in Superantigen-Induced T Cell Responses and Host Survival
Zang et al.
J. Immunol. 2004;172:4883-4892.
ABSTRACT | FULL TEXT  

Injury, sepsis, and the regulation of Toll-like receptor responses
Murphy et al.
J. Leukoc. Biol. 2004;75:400-407.
ABSTRACT | FULL TEXT  

Cardiac effects of burn injury complicated by aspiration pneumonia-induced sepsis
White et al.
Am. J. Physiol. Heart Circ. Physiol. 2003;285:H47-H58.
ABSTRACT | FULL TEXT  

Interleukin-10 Therapy--Review of a New Approach
Asadullah et al.
Pharmacol. Rev. 2003;55:241-269.
ABSTRACT | FULL TEXT  

Cyclooxygenase 2-mediated suppression of macrophage interleukin-12 production after thermal injury
Schwacha et al.
Am. J. Physiol. Cell Physiol. 2002;282:C263-C270.
ABSTRACT | FULL TEXT  

17beta -Estradiol normalizes immune responses in ovariectomized females after trauma-hemorrhage
Knoferl et al.
Am. J. Physiol. Cell Physiol. 2001;281:C1131-C1138.
ABSTRACT | FULL TEXT  

Hypertonicity rescues T cells from suppression by trauma-induced anti-inflammatory mediators
Loomis et al.
Am. J. Physiol. Cell Physiol. 2001;281:C840-C848.
ABSTRACT | FULL TEXT  

MAPK p38 antagonism as a novel method of inhibiting lymphoid immune suppression in polymicrobial sepsis
Song et al.
Am. J. Physiol. Cell Physiol. 2001;281:C662-C669.
ABSTRACT | FULL TEXT  

Long-term-impaired expression of nuclear factor-{kappa}B and I{kappa}B{alpha} in peripheral blood mononuclear cells of trauma patients
Adib-Conquy et al.
J. Leukoc. Biol. 2001;70:30-38.
ABSTRACT | FULL TEXT  

Severe hypoxemia in the absence of blood loss causes a gender dimorphic immune response
Knoferl et al.
Am. J. Physiol. Cell Physiol. 2000;279:C2004-C2010.
ABSTRACT | FULL TEXT  

Do Female Sex Steroids Adversely or Beneficially Affect the Depressed Immune Responses in Males After Trauma-Hemorrhage?
Knoferl et al.
Arch Surg 2000;135:425-433.
ABSTRACT | FULL TEXT  

Reversal of sexual dimorphism in splenic T lymphocyte responses after trauma-hemorrhage with aging
Kahlke et al.
Am. J. Physiol. Cell Physiol. 2000;278:C509-C516.
ABSTRACT | FULL TEXT  

Male Gender Is a Risk Factor for Major Infections After Surgery
Offner et al.
Arch Surg 1999;134:935-940.
ABSTRACT | FULL TEXT  

Sex steroids regulate pro- and anti-inflammatory cytokine release by macrophages after trauma-hemorrhage
Angele et al.
Am. J. Physiol. Cell Physiol. 1999;277:C35-C42.
ABSTRACT | FULL TEXT  

Microbiological and Inflammatory Effects of Murine Recombinant Interleukin-10 in Two Models of Polymicrobial Peritonitis in Rats
Montravers et al.
Infect. Immun. 1999;67:1579-1584.
ABSTRACT | FULL TEXT  

Hyporesponsiveness in leukocytes in sepsis: in vitro models reveal paradoxical effects of IL-10
Cavaillon et al.
Innate Immunity 1999;5:81-85.
ABSTRACT  

A Cytokine Cascade Including Prostaglandin E2, IL-4, and IL-10 Is Responsible for UV-Induced Systemic Immune Suppression
Shreedhar et al.
J. Immunol. 1998;160:3783-3789.
ABSTRACT | FULL TEXT  

Increased Mucosal B-Lymphocyte Apoptosis During Polymicrobial Sepsis Is a Fas Ligand But Not an Endotoxin-Mediated Process
Ayala et al.
Blood 1998;91:1362-1372.
ABSTRACT | FULL TEXT  

Testosterone Receptor Blockade After Hemorrhage in Males: Restoration of the Depressed Immune Functions and Improved Survival Following Subsequent Sepsis
Angele et al.
Arch Surg 1997;132:1207-1214.
ABSTRACT  

Male sex steroids are responsible for depressing macrophage immune function after trauma-hemorrhage
Wichmann et al.
Am. J. Physiol. Cell Physiol. 1997;273:C1335-C1340.
ABSTRACT | FULL TEXT  

Interleukin-10: A Role in the Development of Postoperative Immunosuppression
Klava et al.
Arch Surg 1997;132:425-429.
ABSTRACT  

Dominance of T-Helper 2-Type Cytokines After Severe Injury
Mack et al.
Arch Surg 1996;131:1303-1309.
ABSTRACT  

Mechanism of Immunosuppression in Males Following Trauma-Hemorrhage: Critical Role of Testosterone
Wichmann et al.
Arch Surg 1996;131:1186-1192.
ABSTRACT  

Depressed Splenic Function After Hemorrhage Results From Gastrointestinal Tract Stimulation of Hepatic-Mediator Release: Correction With Portacaval Shunt
Ayala et al.
Arch Surg 1996;131:1209-1215.
ABSTRACT  

Immune Function Is More Compromised After Closed Bone Fracture and Hemorrhagic Shock Than Hemorrhage Alone
Wichmann et al.
Arch Surg 1996;131:995-1000.
ABSTRACT  

Interleukin-10 Attenuates the Release of Proinflammatory Cytokines but Depresses Splenocyte Functions in Murine Endotoxemia
Ertel et al.
Arch Surg 1996;131:51-56.
ABSTRACT  

Interleukin-13 Effectively Down-regulates the Monocyte Inflammatory Potential During Traumatic Stress
Kim et al.
Arch Surg 1995;130:1330-1336.
ABSTRACT