MD-1 is a critical part of the mechanism causing Th1-cytokine-triggered murine fetal loss syndrome

American Journal of Reproductive Immunology

Volumn 49, Issue 5, 2003, Pages 297-307

  Clark, David A ^a,b   Yu, Gary ^b   Arck, Petra C ^c   Levy, Gary A ^b   Gorczynski, Reginald M ^b  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Abortion; Cytokines; Innate immunity; MD 1; Pregnancy; Toll receptors

Indexed keywords

CD14 ANTIGEN; CYTOKINE; ENDOTOXIN; GAMMA INTERFERON; LIPOPOLYSACCHARIDE; PROTEIN; PROTEIN MD 1; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA RECEPTOR; TUMOR NECROSIS FACTOR ALPHA RECEPTOR 1; UNCLASSIFIED DRUG;

ABORTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; DECIDUA; ESCHERICHIA COLI; FEMALE; FETUS WASTAGE; IMMUNITY; IN SITU HYBRIDIZATION; MALE; MATING; MOUSE; MOUSE STRAIN; NONHUMAN; PATHOGENESIS; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SALMONELLA ENTERITIDIS; SIGNAL TRANSDUCTION; TH1 CELL; TROPHOBLAST; UTERUS;

ABORTION, SPONTANEOUS; ANIMALS; ANTIGENS, SURFACE; CYTOKINES; FEMALE; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, INBRED DBA; PREGNANCY; SIGNAL TRANSDUCTION; TH1 CELLS;

EID: 0038025919     PISSN: 87558920     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-0897.2003.00045.x     Document Type: Article

References (56)

1. Clark DA, Arck PC, Chaouat G: Why did your mother reject you? Immunogenetic determinants of the response to environmental selective pressure expressed at the uterine level. Am J Reprod Immunol 1999; 41:5-22.
2. Clark DA, Chaouat G, Arck PC, Mittruecker HW, Levy GA: The cutting edge: Cytokine dependent abortion in CBA × DBA/2 mice is mediated by the procoagulant fg12 prothrombinase. J Immunol 1998; 160:545-549 (erratum 162:3105).
3. Clark DA, Ding JW, Yu G, Levy GA, Gorczynski RM: Fg12 prothrombinase expression in mouse trophoblast and decidua triggers abortion but may be countered by OX-2. Mol Hum Reprod 2001; 7:185-194.
4. Clark DA, Yu G, Levy GA, Gorczynski RM: Procoagulants in fetus rejection: Role of the OX-2 (CD200) tolerance signal. Semin Immunol 2001; 13:255-263.
5. Gorczynski RM, Yu K, Clark DA: Receptor engagement on cells expressing a ligand for the tolerance-inducing molecule CD200 induces an immunoregulatory population that inhibits alloreactivity in vitro and in vivo. J Immunol 2000; 165:4854-4860.
6. Hoek RM, Ruuls SR, Murphy CA, Wright GJ, Goddard R, Zurawski SM, Blom B, Homola ME, Streit WJ, Brown MH, Barclay AN, Sedgwick JD: Down-regulation of the macrophage lineage through interaction with CD200 (OX-2). Science 200: 290:1768-1771.
7. Gendron RL, Nestel FP, Lapp WS, Baines MG: Lipopolysaccharide-induced fetal resorption in mice is associated with the intrauterine production of tumor necrosis factor-α. J Reprod Fertil 1990; 90:395-402.
8. Clark DA, McDermott MR, Szewczuk MR: Impairment of host versus graft reaction in pregnant mice. II. Selective suppression of cytotoxic T cell generation correlates with soluble suppressor activity and successful allogeneic pregnancy. Cell Immunol 1980; 52:106-108.
9. Chaouat G, Clark DA, Wegmann TG: Genetic aspects of the CBA × DBA/2 and B10 × B10A models of murine pregnancy failure and its prevention by lymphocyte immunization. In Early Pregnancy Failure: Mechanism and Treatment, RW Beard, F Sharp (eds). Ashton-under-Lyne, UK, Peacock Press, 1988, pp. 89-102.
10. Arck P, Merali F, Stead R, Chaouat G, Clark DA: Stress-triggered abortion: Inhibition of protective suppression and promotion of tumor necrosis factor-α (TNF-α) release as a mechanism of triggering resorptions in mice. Am J Reprod Immunol 1995; 33:74-80.
11. Muzikova E, Clark DA: Is spontaneous resorption in the DBA/2-mated CBA/J mouse due to a defect in 'seed' or in 'soil'? Am J Reprod Immunol 1995; 33:81-85.
12. + T cells influence success or failure of pregnancy in CBA × DBA/2 matings. Cell Immunol 1999; 196:71-79.
13. Clark DA, Croitoru K: TH1/TH2,3 imbalance due to cytokine-producing NK, γδ T, and NKγδ T cells in murine pregnancy decidua in success or failure of pregnancy. Am J Reprod Immunol 2001; 45:257-265.
14. Hamilton MS, Hamilton BL: Environmental influences on immunologically associated spontaneous abortions in CBA/J mice. J Reprod Immunol 1987; 11:237-241.
15. Clark DA, Quarrington C, Banwatt D, Manuel J, Fulop G: Spontaneous abortion in immunodeficienct SCID mice. Am J Reprod Immunol 1994; 32:15-25.
16. Guha-Thakurta N, Majde JA: Early induction of proinflammatory cytokine and type I interferon mRNAs following Newcastle disease virus, poly [rI:rC], or low-dose LPS challenge of the mouse. J Interferon Cytokine Res 1997; 17:197-204.
17. Clark DA, Banwatt D, Chaouat G: Effect of prostaglandin synthesis inhibitors on spontaneous and endotoxin-induced abortion in mice. J Reprod Immunol 1993; 24:29-44.
18. Haller D, Blum S, Bode C, Hammes WP, Schiffrin EJ: Activation of human peripheral blood mononuclear cells by nonpathologenic bacteria in vitro: Evidence of NK cells as primary targets. Infect Immunity 2000; 68:752-759.
19. Senaldi G, Shaklee CL, Guo J, Martin L, Boone T, Mak TW, Ulich TR: Protection against the mortality associated with disease models mediated by TNF and IFN-γ in mice lacking IFN regulatory factor-1. J Immunol 1999; 163:6820-6826.
20. Yao YM, Redl H, Bahrami S, Schlag G: The inflammatory basis of trauma/shock-associated multiple organ failure. Inflamm Res 1998; 47:201-210.
21. Doig CJ, Sutherland LR, Sandham JD, Fick GH, Verhoef M, Meddings JB: Increased intestinal permeability is associated with the development of multiple organ dysfunction syndrome in critically ill ICU patients. Am J Resp Crit Care Med 1998; 158:444-451.
22. Deitch EA, Winterton J, Berg R: Thermal injury promotes bacterial translocation from the gastrointestinal tract in mice with impaired T cell-mediated immunity. Arch Surg 1986; 121:97-101.
23. + lymphocytes in the stress-induced reactivation of experimental colitis. Nat Med 1999; 5: 1178-1182.
24. Clark DA, Chaouat G, Gorczynski RM: Thinking outside the box: Mechanisms of environmental selective pressures on the outcome of the materno-fetal relationship. Am J Reprod Immunol 2002; 47:275-282.
25. Giroir BP, Johnson JJ, Brown T, Allen GL, Beutler B: The tissue distribution of tumor necrosis factor biosynthesis during endotoxemia. J Clin Invest 1992; 90:693-698.
26. Neilson IR, Neilson KA, Yunis EJ, Rowe MI: Failure of tumor necrosis factor to produce hypotensive shock in the absence of endotoxin. Surgery 1989; 106;439-443.
27. Perera PY, Mayadas TN, Takeuchi O, Akira S, Zaks-Zilberman M, Goyert SM, Vogel SN: CD11b/CD18 acts in concert with CD14 and toll-like receptor (tlr) 4 to elicit full lipopolysaccharide and taxol-inducible gene expression. J Immunol 2001; 166:574-581.
28. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenbeg M, Ricciardi-Castagnoli P, Layton B, Beutler B: Defective LPS signaling in C3H/HeJ and C57B1/10ScCr mice: Mutation in tlr4 gene. Science 1998; 282:2085-2088.
29. Hirschfeld M, Ma Y, Weiss JH, Vogel SN, Weis JJ: The cutting edge: Repurification of lipopolysaccharide eliminates signaling through both human and murine toll-like receptor 2. J Immunol 2000; 165:618-622.
30. Jeffries C, O'Neill LAJ: Signal transduction pathway activated by toll-like receptors. Mod Aspects Immunobiol 2002; 2:169-175.
31. Gorczynski RM, Chen Z, Clark DA, Hu J, Yu K, Li X, Tsang W, Hadidi S: Regulation of gene expression of murine MD-1 regulates subsequent T cell activation and cytokine production. J Immunol 2000; 165:1925-1932.
32. Hadidi S, Yu K, Chen Z, Gorczynski RM: Preparation and functional properties of polyclonal and monoclonal antibodies to murine MD-1. Immunol Lett 2001; 77:97-103.
33. Begum NA, Tsuji S, Nomura M, Shida K, Azuma I, Hayashi A, Matsumoto M, Seya T, Toyoshima K: Human MD-1 homolog is a BCG-regulated gene product in monocytes: Its identification by differential display. Biochem Biophys Res Commun 1999; 256:325-329.
34. Nagai Y, Shimazu R, Ogata H, Akashi S, Sudo K, Yamashita Y, Hayashi S, Iwakura Y, Kimoto M, Miyake M: Requirement for MD-1 in cell surface expression of RP105/CD180 and B-cell responsiveness to lipopolysaccharide. Blood 2002; 99:1699-1705.
35. Dziarski R, Wang Q, Miyake K, Kirschning CJ, Gupta D. MD-2 enables toll-like receptor 2 (tlr-2)-mediated responses to lipopolysaccharide and enhances tlr2-mediated responses to gram-positive and gram-negative bacteria and their cell wall components. J Immunol 2001; 166: 1938-1944.
36. Parand M, Chelid L: Protective effect of chlorpromazine against endotoxin induced abortion. Proc Soc Exp Biol Med 1964: 116:906-915.
37. Rioux-Darrieulat F, Parant F, Chedid L: Prevention of endotoxin-induced abortion by treatment of mice with antisera. J Infect Dis 1978; 137:7-13.
38. Chaouat G: Synergy of lipopolysaccharide and inflammatory cytokines in murine pregnancy: Alloimmunization prevents abortion but does not affect the induction of preterm delivery. Cell Immunol 1994; 157:328-340.
39. Kato I, Kimura S, Furahashi T, Nakayoshi H, Takayama S, Uenishi N: Effects of recombinant murine interferon-γ on pregnant mice and their fetuses. Fundam Appl Toxicol 1990; 14:658-665.
40. Mattsson R, Mattsson A, Holmdahl R, Scheynius A, Van Der Meide PH: In vivo treatment with interferon-γ during early pregnancy in mice induces strong expression of major histocompatibility complex class I and II molecules in uterus and decidua but not in extra-embryonic tissue. Biol Reprod 1992; 46:1176-1186.
41. Ashkar AA, DiSanto JP, Croy BA: Interferon γcontributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal uterine pregnancy. J Exp Med 2000; 192:259-270.
42. Suk K, Kim S, Kim YH, Kim YA, Chang I, Yagita H, Shong M, Lee MS: IFN-γ/TNF-α synergism as the final effector in autoimmune diabetes: A key role for STAT1?IFN regulatory factor-1 pathway in pancreatic β cell death. J Immunol 2001; 166:4481-4489.
43. Kovarik P, Stoiber D, Novy M, Decker T: Stat1 combines signals derived fro IFN-γ and LPS receptors during macrophage activation. EMBO J 1998; 17:3660-3668.
44. Ozes ON, Taylor MW: Reversal of interferon-γ -resistant phenotype by poly (I:C): Possible involvement of ISGF2 (IRFI) in interferon-γ -mediated induction of the IDO gene. J Interferon Res 1994; 14:25-32.
45. Ostojic S, Dubanchet S, Abdelkarim M, Truyens C, Capron F, Chaouat G: Localization of IL-16, IL-17, and IL-18 at the mouse meternal-fetal interface. Am J Reprod Immunol 2001; 46:42.
46. + T cells as a basis for stress-triggered substance P-mediated abortion in mice. Cell Immunol 1996; 171:226-230.
47. + T cell-dependent suppression of natural effector cell cytotoxicity against trophoblast target cells. Cell Immunol 1994; 154:143-152.
48. Clark DA, Banwatt D, Chaouat G: Stress-induced abortion in mice is prevented by alloimmunization. Am J Reprod Immunol 1993; 29:141-147.
49. Kinsky R, Menu E, Chaouat G, Kapovic M, Jaulin C, Kourilsky P, Wegmann TG, Thang N: The role of defined major histocompatibility antigen in preventing fetal death. In Immunology of Pregnancy, G Chaouat (ed.). Boca Raton, FL, CRC Press, 1993, pp. 47-60.
50. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA: Recognition of double-stranded RNA and activation of NK-κB by toll-like receptor 3. Nature 2001; 413:732-738.
51. Clark DA, Drake B, Head JR, Stedronska-Clark J, Banwatt D: Decidua-associated suppressor activity and viability of individual implantation sites of allopregnant C3H mice. J Reprod Immunol 1990; 17:253-264.
52. Sebastiani G, Leveque G, Zlariviere L, Laroche J, Skamene E, Gros P, Malo D: Cloning and characterization of the murine toll-like receptor 5 (tlr5) gene: Sequence and mRNA sequence in Salmonella-susceptible MOFL/Ei mice. Genomics 2000; 64:230-240.
53. Baines MG, Duclos AJ, De Fougerolles AR, Gendron RL: Immunological prevention of spontaneous early embryo resorption is mediated by non-specific immunostimulation. Am J Reprod Immunol 1996; 35:34-42.
54. Ugwumadu AH: Bacterial vaginosis in pregnancy. Curr Opin Obstet Gynecol 2002; 14:115-118.
55. Matzinger, P: Tolerance, danger, and the extended family. Annu Rev Immunol 1994; 12:991-1045.
56. Bonney EA, Matzinger P: The maternal immune system's interaction with circulating fetal cells. J Immunol 1997; 158:40-47.