Essential role for IL-10 in resistance to lipopolysaccharide-induced preterm labor in mice

Journal of Immunology

Volumn 177, Issue 7, 2006, Pages 4888-4896

  Robertson, Sarah A ^a   Skinner, Rebecca J ^a   Care, Alison S ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; RECOMBINANT INTERLEUKIN 10; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; DOWN REGULATION; FEMALE; FETUS; FETUS WASTAGE; GENE EXPRESSION; INTRAUTERINE GROWTH RETARDATION; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PLACENTA; PREMATURE LABOR; PRIORITY JOURNAL; SURVIVAL; THIRD TRIMESTER PREGNANCY; TISSUE DISTRIBUTION; UTERUS;

EID: 33749141509     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.7.4888     Document Type: Article

References (62)

1. Romero, R., M. Sirtori, E. Oyarzun, C. Avila, M. Mazor, R. Callahan, V. Sabo, A. P. Athanassiadis, and J. C. Hobbins. 1989. Infection and labor V: prevalence, microbiology, and clinical significance of intraamniotic infection in women with preterm labor and intact membranes. Am. J. Obstet. Gynecol. 161: 817-824.
2. Meis, P. J., R. L. Goldenberg, B. Mercer, A. Moawad, A. Das, D. McNellis, F. Johnson, J. D. Iams, E. Thom, and W. W. Andrews. 1995. The preterm prediction study: significance of vaginal infections. Am. J. Obstet. Gynecol. 173: 1231-1235.
3. Lamont, R. F. 2003. Recent evidence associated with the condition of preterm prelabour rupture of the membranes. Curr. Opin. Obstet. Gynecol. 15: 91-99.
4. Challis, J. R., D. M. Sloboda, N. Alfaidy, S. J. Lye, W. Gibb, F. A. Patel, W. L. Whittle, and J. P. Newnham. 2002. Prostaglandins and mechanisms of preterm birth. Reproduction 124: 1-17.
5. Peltier, M. R. 2003. Immunology of term and preterm labor. Reprod. Biol. Endocrinol. 1: 122.
6. Lumley, J. 2003. Defining the problem: the epidemiology of preterm birth. Br. J. Obstet. Gynaecol. 20 (Suppl. 110): 3-7.
7. Mohan, A. R., J. A. Loudon, and P. R. Bennett. 2004. Molecular and biochemical mechanisms of preterm labour. Semin. Fetal Neonatal Med. 9: 437-444.
8. Dudley, D. J., C. L. Chen, D. W. Branch, E. Hammond, and M. D. Mitchell. 1993. A murine model of preterm labor: inflammatory mediators regulate the production of prostaglandin E2 and interleukin-6 by murine decidua. Biol. Reprod. 48: 33-39.
9. Hirsch, E., and H. Wang. 2005. The molecular pathophysiology of bacterially induced preterm labor: insights from the murine model. J. Soc. Gynecol. Investig. 12: 145-155.
10. Moore, K. W., R. de Waal Malefytqq, R. L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19: 683-765.
11. de Waal Malefytqq, R., J. Abrams, B. Bennett, C. G. Figdor, and J. E. de Vries. 1991. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174: 1209-1220.
12. Fiorentino, D. F., A. Zlotnik, T. R. Mosmann, M. Howard, and A. O'Garra. 1991. IL-10 inhibits cytokine production by activated macrophages. J. Immunol. 147: 3815-3822.
13. Hart, P. H., E. K. Hunt, C. S. Bonder, C. J. Watson, and J. J. Finlay-Jones. 1996. Regulation of surface and soluble TNF receptor expression on human monocytes and synovial fluid macrophages by IL-4 and IL-10. J. Immunol. 157: 3672-3680.
14. Lin, H., T. R. Mosmann, L. Guilbert, S. Tuntipopipat, and T. G. Wegmann. 1993. Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J. Immunol. 151: 4562-4573.
15. Chaouat, G., V. Cayol, V. Mairovitz, and S. Dubanchet. 1999. Localisation of the Th2 cytokines IL-3, IL-4, IL-10 at the murine feto-maternal interface during pregnancy. In Reproductive Immunology. S. K. Gupta, ed. Narosa, New Delhi, pp. 61-70.
16. Sallinen, K., E. Verajankorva, and P. Pollanen. 2000. Expression of antigens involved in the presentation of lipid antigens and induction of clonal anergy in the female reproductive tract. J. Reprod. Immunol. 46: 91-101.
17. Wessells, J., D. Wessner, R. Parsells, K. White, D. Finkenzeller, W. Zimmermann, and G. Dveksler. 2000. Pregnancy specific glycoprotein 18 induces IL-10 expression in murine macrophages. Eur. J. Immunol. 30: 1830-1840.
18. Roth, I., D. B. Corry, R. M. Locksley, J. S. Abrams, M. J. Litton, and S. J. Fisher. 1996. Human placental cytotrophoblasts produce the immunosuppressive cytokine interleukin 10. J. Exp. Med. 184: 539-548.
19. Trautman, M. S., D. Collmer, S. S. Edwin, W. White, M. D. Mitchell, and D. J. Dudley. 1997. Expression of interleukin-10 in human gestational tissues. J. Soc. Gynecol. Investig. 4: 247-253.
20. Hanna, N., I. Hanna, M. Hleb, E. Wagner, J. Dougherty, D. Balkundi, J. Padbury, and S. Sharma. 2000. Gestational age-dependent expression of IL-10 and its receptor in human placental tissues and isolated cytotrophoblasts. J. Immunol. 164: 5721-5728.
21. Sacks, G. P., L. M. Clover, D. R. Bainbridge, C. W. Redman, and I. L. Sargent. 2001. Flow cytometric measurement of intracellular Th1 and Th2 cytokine production by human villous and extravillous cytotrophoblast. Placenta 22: 550-559.
22. Dudley, D. J., S. Spencer, S. Edwin, and M. D. Mitchell. 1994. Interleukin-10 inhibits cytokine production by human gestational tissues. Cytokine 6: 545.
23. Fortunato, S. J., R. Menon, K. F. Swan, and S. J. Lombardi. 1996. Interleukin-10 inhibition of interleukin-6 in human amniochorionic membrane: transcriptional regulation. Am. J. Obstet. Gynecol. 175: 1057-1065.
24. Fortunato, S. J., R. Menon, and S. J. Lombardi. 1997. Interleukin-10 and transforming growth factor-β inhibit amniochorion tumor necrosis factor-α production by contrasting mechanisms of action: therapeutic implications in prematurity. Am. J. Obstet. Gynecol. 177: 803-809.
25. +-dependent 15-hydroxyprostaglandin dehydrogenase in cultured term human villous trophoblast and chorion trophoblast cells. J. Clin. Endocrinol. Metab. 84: 4645-4651.
26. Greig, P. C., W. N. Herbert, B. L. Robinette, and L. A. Teot. 1995. Amniotic fluid interleukin-10 concentrations increase through pregnancy and are elevated in patients with preterm labor associated with intrauterine infection. Am. J. Obstet. Gynecol. 173: 1223-1227.
27. Sharma, S., M. Plevyak, and N. Hanna. 2000. Regulation of IL-10 in human gestational tissues: attenuated expression at term and in missed abortions and preterm labour. Placenta 21: A38 (abstract).
28. Rivera, D. L., S. M. Olister, X. Liu, J. H. Thompson, X. J. Zhang, K. Pennline, R. Azuero, D. A. Clark, and M. J. Miller. 1998. Interleukin-10 attenuates experimental fetal growth restriction and demise. FASEB J. 12: 189-197.
29. Terrone, D. A., B. K. Rinehart, J. P. Granger, P. S. Barrilleaux, J. N. Martin, Jr., and W. A. Bennett. 2001. Interleukin-10 administration and bacterial endotoxin-induced preterm birth in a rat model. Obstet. Gynecol. 98: 476-480.
30. Rodts-Palenik, S., J. Wyatt-Ashmead, Y. Pang, B. Thigpen, Z. Cai, P. Rhodes, J. N. Martin, J. Granger, and W. A. Bennett. 2004. Maternal infection-induced white matter injury is reduced by treatment with interleukin-10. Am. J. Obstet. Gynecol. 191: 1387-1392.
31. Kuhn, R., J. Lohler, D. Rennick, K. Rajewsky, and W. Muller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75: 263-274.
32. Svensson, L., M. Arvola, M. A. Sallstrom, R. Holmdahl, and R. Mattsson. 2001. The Th2 cytokines IL-4 and IL-10 are not crucial for the completion of allogeneic pregnancy in mice. J. Reprod. Immunol. 51: 3-7.
33. White, C. A., M. Johansson, C. T. Roberts, A. J. Ramsay, and S. A. Robertson. 2004. Effect of interleukin-10 null mutation on maternal immune response and reproductive outcome in mice. Biol. Reprod. 70: 123-131.
34. Berg, D. J., R. Kuhn, K. Rajewsky, W. Muller, S. Menon, N. Davidson, G. Grunig, and D. Rennick. 1995. Interleukin-10 is a central regulator of the response to LPS in murine models of endotoxic shock and the Shwartzman reaction but not endotoxin tolerance. J. Clin. Invest. 96: 2339-2347.
35. Rennick, D., N. Davidson, and D. Berg. 1995. Interleukin-10 gene knock-out mice: a model of chronic inflammation. Clin. Immunol. Immunopathol. 76: S174-S178.
36. Murphy, S. P., L. D. Fast, N. N. Hanna, and S. Sharma. 2005. Uterine NK cells mediate inflammation-induced fetal demise in IL-10-null mice. J. Immunol. 175: 4084-4090.
37. Gerard, C., Bruyns, C., Marchant, A., Abramowicz, D., Vandenabeele, P., Delvaux A., Friers W., Goldman M., Velu, T. 1993. Interleukin 10 reduces the release of tumor necrosis factor and prevents lethality in experimental endotoxemia. J. Exp. Med. 177: 547-550.
38. Marchant, A., C. Bruyns, P. Vandenabeele, M. Ducarme, C. Gerard, A. Delvaux, D. De Groote, D. Abramowicz, T. Velu, and M. Goldman. 1994. Interleukin-10 controls interferon-γ and tumor necrosis factor production during experimental endotoxemia. Eur. J. Immunol. 24: 1167-1171.
39. Howard, M., T. Muchamuel, S. Andrade, and S. Menon. 1993. Interleukin 10 protects mice from lethal endotoxemia. J. Exp. Med. 177: 1205-1208.
40. Dickensheets, H. L., S. L. Freeman, M. F. Smith, and R. P. Donnelly. 1997. Interleukin-10 up-regulates tumor necrosis factor receptor type-II (p75) gene expression in endotoxin-stimulated human monocytes. Blood 90: 4162-4171.
41. Dammann, O., and A. Leviton. 1997. Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr. Res. 42: 1-8.
42. Hirsch, E., R. Blanchard, and S. P. Mehta. 1999. Differential fetal and maternal contributions to the cytokine milieu in a murine model of infection-induced preterm birth. Am. J. Obstet. Gynecol. 180: 429-434.
43. Bry, K., and M. Hallman. 1993. Transforming growth factor-β2 prevents preterm delivery induced by interleukin-1α and tumor necrosis factor-α in the rabbit. Am. J. Obstet. Gynecol. 168: 1318-1322.
44. Yoshimura, K., and E. Hirsch. 2003. Interleukin-6 is neither necessary nor sufficient for preterm labor in a murine infection model. J. Soc. Gynecol. Investig. 10: 423-427.
45. Romero, R., and B. Tartakovsky. 1992. The natural interleukin-1 receptor antagonist prevents interleukin-1-induced preterm delivery in mice. Am. J. Obstet. Gynecol. 167: 1041-1045.
46. Wang, Y. Y., O. Tawfik, and G. W. Wood. 1998. Endotoxin-induced abortion in mice is mediated by activated fetal macrophages. J. Leukocyte Biol. 63: 40-50.
47. Haddad, E. K., A. J. Duclos, E. Antecka, W. S. Lapp, and M. G. Baines. 1997. Role of interferon-γ in the priming of decidual macrophages for nitric oxide production and early pregnancy loss. Cell Immunol. 181: 68-75.
48. Haddad, E. K., A. J. Duclos, and M. G. Baines. 1995. Early embryo loss is associated with local production of nitric oxide by decidual mononuclear cells. J. Exp. Med. 182: 1143-1151.
49. Sato, T. A., J. A. Keelan, and M. D. Mitchell. 2003. Critical paracrine interactions between TNF-α and IL-10 regulate lipopolysaccharide- stimulated human choriodecidual cytokine and prostaglandin E2 production. J. Immunol. 170: 158-166.
50. Abrahams, V. M., P. Bole-Aldo, Y. M. Kim, S. L. Straszewski-Chavez, T. Chaiworapongsa, R. Romero, and G. Mor. 2004. Divergent trophoblast responses to bacterial products mediated by TLRs. J. Immunol. 173: 4286-4296.
51. Mitchell, M. D., K. L. Simpson, and J. A. Keelan. 2004. Paradoxical proinflammatory actions of interleukin-10 in human amnion: potential roles in term and preterm labour. J. Clin. Endocrinol. Metab. 89: 4149-4152.
52. Endo, T., F. Ogushi, and S. Sone. 1996. LPS-dependent cyclooxygenase-2 induction in human monocytes is down-regulated by IL-13, but not by IFN-γ. J. Immunol. 156: 2240-2246.
53. Berg, D. J., J. Zhang, D. M. Lauricella, and S. A. Moore. 2001. Il-10 is a central regulator of cyclooxygenase-2 expression and prostaglandin production. J. Immunol. 166: 2674-2680.
54. Williams, L., L. Bradley, A. Smith, and B. Foxwell. 2004. Signal transducer and activator of transcription 3 is the dominant mediator of the anti-inflammatory effects of IL-10 in human macrophages. J. Immunol. 172: 567-576.
55. Chaouat, G., E. Menu, D. A. Clark, M. Dy, M. Minkowski, and T. G. Wegmann. 1990. Control of fetal survival in CBA × DBA/2 mice by lymphokine therapy. J. Reprod. Fertil. 89: 447-458.
56. Clark, D. A., G. Chaouat, P. C. Arck, H. W. Mittruecker, and G. A. Levy. 1998. Cytokine-dependent abortion in CBA × DBA/2 mice is mediated by the procoagulant fg12 prothombinase. J. Immunol. 160: 545-549.
57. Heyborne, K. D., S. S. Witkin, and J. A. McGregor. 1992. Tumor necrosis factor-α in midtrimester amniotic fluid is associated with impaired intrauterine fetal growth. Am. J. Obstet. Gynecol. 167: 920-925.
58. Yui, J., M. Garcia-Lloret, T. G. Wegmann, and L. J. Guilbert. 1994. Cytotoxicity of tumor necrosis factor-α and γ-interferon against primary human placental trophoblasts. Placenta 15: 819-835.
59. Roberts, C. T., C. A. White, N. G. Wiemer, A. Ramsay, and S. A. Robertson. 2003. Altered placental development in interleukin-10 null mutant mice. Placenta 24: S94-S99.
60. Myatt, L. 1992. Control of vascular resistance in the human placenta. Placenta 13: 329-341.
61. Heyborne, K. D., J. A. McGregor, G. Henry, S. S. Witkin, and J. S. Abrams. 1994. Interleukin-10 in amniotic fluid at midtrimester: immune activation and suppression in relation to fetal growth. Am. J. Obstet. Gynecol. 111: 55-59
62. Asadullah, K., W. Sterry, and H. D. Volk. 2003. Interleukin-10 therapy: review of a new approach. Pharmacol. Rev. 55: 241-269.