Introduction a mouse model for pre-eclampsia: Adoptive transfer of activated Th1 cells leads to pre-eclampsia-like symptoms exclusively in pregnant mice

European Journal of Immunology

Volumn 34, Issue 2, 2004, Pages 377-387

  Zenclussen, Ana C ^a   Fest, Stefan ^a   Joachim, Ricarda ^a   Klapp, Burghard F ^a   Arck, Petra C ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Blood pressure; Cytokine; Pre eclampsia; Pregnancy; Th1 cell

Indexed keywords

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE MEASUREMENT; CONTROLLED STUDY; FEMALE; FETUS WASTAGE; GLOMERULONEPHRITIS; IMMUNOCOMPETENT CELL; INFLAMMATION; MOUSE; NONHUMAN; PREECLAMPSIA; PREGNANCY; PREGNANCY COMPLICATION; PRIORITY JOURNAL; PROTEINURIA; RECIPIENT; SPLEEN CELL; SYMPTOMATOLOGY; T LYMPHOCYTE ACTIVATION; TH1 CELL; THIRD TRIMESTER PREGNANCY; ANIMAL; BAGG ALBINO MOUSE; BLOOD; BLOOD PRESSURE; C57BL MOUSE; DISEASE MODEL; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MALE; METABOLISM; PATHOLOGY; RANDOMIZATION; UTERUS;

CHEMOKINE RECEPTOR CCR5; INTERLEUKIN 12; TUMOR NECROSIS FACTOR ALPHA;

ADOPTIVE TRANSFER; ANIMALS; BLOOD PRESSURE; DISEASE MODELS, ANIMAL; FEMALE; FLOW CYTOMETRY; INTERLEUKIN-12; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; PRE-ECLAMPSIA; PREGNANCY; PROTEINURIA; RANDOM ALLOCATION; RECEPTORS, CCR5; TH1 CELLS; TUMOR NECROSIS FACTOR-ALPHA; UTERUS;

EID: 1642298263     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200324469     Document Type: Article

References (49)

1. Robillard, P. Y., Interest in preeclampsia for researchers in reproduction. J. Reprod. Immunol. 2002. 53: 279-287.
2. Pijnenborg, R., Luyten, C., Vercruysse, L. and Van Assche, F. A., Attachment and differentiation in vitro of trophoblast from normal and preeclamptic human placentas. Am. J. Obstet. Gynecol. 1996. 175: 30-36.
3. Zhou, Y., Damsky, C. and Fisher, S., Pre-eclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. J. Clin. Invest. 1999. 99: 2152-2164.
4. Redman, C. W. G., Sacks, G. P. and Sargent, I. L., Preeclampsia: An excessive maternal inflammatory response to pregnancy. Am. J. Obstet. Gynecol. 1999. 180: 499-506.
5. Roberts, J. M., Taylor, R. N. and Goldfien, A., Clinical and biochemical evidence of endothelial cell dysfunction in the pregnancy syndrome preeclampsia. Am. J. Hypertens. 1991. 8: 700-708.
6. Faas, M. M., Schuiling, G., Bailer, J. F. W., Visscher, C. A. and Bakker, W. W., A new animal model for human preeclampsia: ultralow dose endotoxin infusion in pregnant rats. Am. J. Obstet. Gynecol. 1994. 171: 158-164.
7. Faas, M. M. and Schuiling, G. A., Pre-eclampsia and the inflammatory response. Eur. J. Obstet. and Gynecol. and Reprod. Biol. 2001. 95: 213-217.
8. Saito, S., Umekage, H., Sakamoto, Y., Sakai, M., Tanebe, K., Sasaki, Y. and Morikawa, H., Increased T-helper-1-type immunity and decreased T-helper-2-type immunity in patients with preeclampsia. Am. J. Reprod. Immunol. 1999. 5: 297-306.
9. Sacks, G. P., Studena, K., Sargent, I. L. and Redman, C. W., CD11b expression on circulating neutrophils in pre-eclampsia. Clin. Sci. 1997. 93: 187-189.
10. Oian, P., Omsjo, I., Maltau, J. M. and Osterud, B., Increased sensitivity to thromboplastin synthesis in blood monocytes from pre-eclamptic patients. Br. J. Obstet. Gynaecol. 1985. 92: 511-517.
11. Greer, I. A., Haddad, N. G., Dawes, J., Johnstone, F. D. and Calder, A. A., Neutrophil activation in pregnancy-induced hypertension. Br. J. Obstet. Gynaecol. 1989. 96: 978-982.
12. Darmochwal-Kolarz, D., Leszczynska-Gorzelak, B., Rolinski, I. and Oleszczuk, J., T helper 1- and T helper 2-type cytokine imbalance in pregnant women with pre-eclampsia. Eur. J. Obstet. Gynecol. Reprod. Biol. 1999. 86: 165-170.
13. Stark, J. M., Pre-eclampsia and cytokine induced oxidative stress. Br. J. Obstet. Gynaecol. 1993. 100: 105-109.
14. Ma, C., Zhuang, Y. and Xu, Y., The effect of inhibition of nitric oxide synthesis on vasoregulatory factors in pregnant rats. Zhonghua Fu Chan Ke Za Zhi. 1999. 34: 521-524.
15. Takimoto, E., Ishida, J., Sugiyama, F., Horiguchi, H., Murakami, K. and Fukamizu, A., Hypertension induced in pregnant mice by placental renin and maternal angiotensinogen. Science 1996. 274: 995-998.
16. Kanayama, N., Tsujimura, R., She, L., Maehara, K. and Terao, T., Cold-induced stress stimulates the sympathetic nervous system, causing hypertension and proteinuria in rats. J. Hypertens. 1997. 15: 383-389.
17. Halim, A., Kanayama, N., Maehara, K., Takahashi, M. and Terao, T., HELLP syndrome-like biochemical parameters obtained with endothelin-1 injections in rabbits. Gynecol. Obstet. Invest. 1993. 35: 193-198.
18. Hayakawa, S., Fujikawa, T., Fukuoka, H., Chisima, F., Karasaki-Suzuki, M., Ohkoshi, E., Ohi, T., Kiyoshi Fujii, M., Tochigi, K., Satoh, T. et al., Murine fetal resorption and experimental pre-eclampsia are induced by both excessive Th1 and Th2 activation. J. Peprod. Immunol. 2000. 47: 121-138.
19. Davisson, R. L., Hoffmann, D. S., Butz, G. M., Aldape, G., Schlager, G., Merrill, D. C., Sethi, S., Weiss, R. M. and Bates, J. N., Discovery of a spontaneous genetic mouse model of preeclampsia. Hypertension 2002. 39: 337-342.
20. Anderson, P. M., Blazar, B. R., Bach, F. H. and Ochoa, A. C., Anti-CD3 + IL-2-stimulated murine killer cells. In vitro generation and in vivo antitumor activity. J. Immunol. 1989. 142: 1383-1394.
21. Saxton, M. L., Longo, D. L., Wetzel, H. E., Tribble, H., Alvord, W. G., Kwak, L. W., Leonard, A. S., Ullmann, C. D., Curti, B. D. and Ochoa, A. C., Adoptive transfer of anti-CD3-activated CD4+ T cells plus cyclophosphamide and liposome-encapsulated interleukin-2 cure murine MC-38 and 3LL tumors and establish tumor-specific immunity. Blood 1997. 89: 2529-2536.
22. Onodera, K., Chandraker, A., Volk, H. D., Lehmann, M., Korom, S., Stadlbauer, T. H., Kato, K., Kasai, S., Sayegh, M. H. and Kupiec-Weglinski, J. W., Role of regulatory T cells in the " infectious" tolerance pathway in transplant recipients. Transplant. Proc. 1998. 30: 13-15.
23. Schmidt, H., Filantenkov, A., Reutzel-Selke, A., Seifert, M., Doebis, C., Jurisch, A., Pratschke, J., Neuhaus, P., Tullius, S. G. and Volk, H. D., Adoptive transfer of regulatory T cells following chronic allograft rejection induces tolerance for secondary allografts. Transplant. Proc. 2002. 34: 2893-2894.
24. Lin, H., Mossmann, T. R., Guilbert, L., Tuntipopipat, S. and Wegmann, T. G., Synthesis of T helper 2-type cytokines at the feto-maternal interface. J. Immunol. 1993. 151: 4562-4573.
25. Wegmann, T. G., Lin, H., Guilbert, L. and Mossmann, T., Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a Th2 phenomen? Immunol. Today. 1993. 14: 353-356.
26. Raghupathy, R., Th1-type immunity is incompatible with successful pregnancy. Immunol. Today. 1997. 10: 434-437.
27. Zenclussen, A. C., Fest, S., Sehmsdorf, U.-S., Hagen, E., Klapp, B. F. and Arck, P. C., Up-regulation of decidual P-selectin is associated with increased number of Th1 producing cells populations in patients with spontaneous abortion. Cell. Immunol. 2001. 213: 94-103.
28. Mellor, A. L., Sivakumar, J., Chandler, P., Smith, K., Molina, H., Mao, D. and Munn, D. H., Prevention of T cell-driven complement activation and inflammation by tryptophan catabolism during pregnancy. Nat. Immunol. 2001. 2: 64-68.
29. Hefler, L. A., Tempfer, C. B., Moreno, R. M., O'Brien, W. E. and Gregg, A. R., Endothelial-derived nitric oxide and angiotensinogen: blood pressure and metabolism during mouse pregnancy. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001. 280: 174-182.
30. Nakajima, A., Hirose, S., Yagita, H. and Okumura, K., Roles of IL-4 and IL-12 in the development of lupus in NZB/W F1 mice. J. Immunol. 1997. 158: 1466-1472.
31. Torii, I., Morikawa, S. and Harada, T., MD41, a novel T helper 0 clone, mediates mast-cell dependent delayed-type hypersensitivity in mice. Immunology 2002. 107: 426-434.
32. Oelke, M., Moehrle, U., Chen, J. L., Behringer, D., Cerundolo, V., Lindemann, A. and Mackensen, A., Geneytion and purification of CD8+ melan-A-specific cytotoxic T lymphocytes for adoptive transfer in tumor immunotherapy. Clin. Cancer Res. 2000. 6: 1997-2005.
33. Pober, J. S., Activation and injury of endothelial cells by cytokines. Pathol. Biol. (Paris) 1998. 46: 159-163.
34. von Dadelzen, P. and Magee, L., Could an infectious trigger explain the differential maternal response to the shared placental pathology of preeclampsia and normotensive intrauterine growth restriction? Acta Obstet. Gynecol. Scand. 2002. 81: 642-648.
35. Medawar, P. B., Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. Symp. Soc. Exp. Biol. 1953. 44: 320-338.
36. Sargent, I. L., Maternal and fetal immune responses during pregnancy. Exp. Clin. Immunogenet. 1993. 10: 85-102.
37. Mellor, A. L. and Munn, D. H., Tryptophan catabolism and T-cell tolerance: immunosuppression by starvation? Immunol. Today 1999. 20: 469-473.
38. Annunziato, F., Galli, G., Romagnani, P., Cosmi, L., Manetti, R., Maggi, E. and Romagnani, S., Chemokine receptors and other surface molecules preferentially associated with human Th1 or Th2 cells. Microbes Infect. 1999. 1: 103-106.
39. Weber, C., Weber, K., Klier, C., Gu, S., Wank, R., Horuk, R. and Nelson, P. J., Specialized roles of the chemokine receptors CCR1 and CCR5 in the recruitment of monocytes and Th1-like/CD45RO+ T cells. Blood 2001. 97: 1144-1146.
40. Clausen, T., Djurovic, S., Brosstad, F. R., Berg, K. and Henriksen, T., Altered circulating levels of adhesion molecules at 18 weeks' gestation among women with eventual preeclampsia: indicators of disturbed placentation in absence of evidence of endothelial dysfunction? Am. J. Obstet. Gynecol. 2000. 182: 321-325.
41. Hill, J. A., Haimovici, F. and Anderson, D. J., Products of activated lymphocytes and macrophages inhibit mouse embryo development in vitro. J. Immunol. 1987. 139: 2250-2254.
42. Todt, J. C., Yang, Y., Lei, J., Lauria, M. R., Sorokin, Y., Cotton, D. B. and Yelian, F. D., Effects of tumor necrosis factor-alpha on human trophoblast cell adhesion and motility. Am. J. Reprod. Immunol. 1996. 36: 65-71.
43. Guo, G., Morrissey, J., Mc Cracken, R., Tolley, T., Liapis, H. and Klahr, S., Contributions of angiotensin II and tumor necrosis factor-alpha to the development of renal fibrosis. Am. J. Physiol. Renal Physiol. 2001. 280: 777-785.
44. Knotek, M., Rogachev, B., Wang, W., Ecder, T., Melnikov, V., Gengaro, P. E., Esson, M., Edelstein, C. L., Dinarello, C. A. and Schrier, R. W., Endotoxemic renal failure in mice: Role of tumor necrosis factor independent of inducible nitric oxide synthase. Kidney Int. 2001. 59: 2243-2249.
45. Bochner, B. S., Klunk, D. A., Sterbinsky, S. A., Coffman, R. L. and Schleimer, R. P., IL-13 selectively induces vascular cell adhesion molecule-1 expression in human endothelial cells. J. Immunol. 1995. 154: 799-803.
46. de Kossodo, S., Moore, R., Gschmeissner, S., East, N., Upton, C. and Balkwill, F. R., Changes in endogenous cytokines, adhesion molecules and platelets during cytokine-induced tumour necrosis. Br. J. Cancer 1995. 72: 1165-1172.
47. Croy, B. A., Ashkar, A. A., Minhas, K. and Greenwood, J. D., Can murine uterine natural killer cells give insights into the pathogenesis of preeclampsia? J. Soc. Gynecol. Investig. 2000. 7: 12-20.
48. Ashkar, A. A., Di Santo, J. P. and Croy, B. A., Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J. Exp. Med. 2000. 192: 259-270.
49. Hammer, M. H., Zhai, Y., Katori, M., Ritter, T., Volk, H. D., Coito, A. J. and Kupiec-Weglinski, J. W., Homing of in vitro-generated donor antigen-reactive CD4+ T lymphocytes to renal allografts is alpha 4 beta 1 but not alpha L beta 2 integrin dependent. J. Immunol. 2001. 166: 596-601.