Establishment of the porcine epitheliochorial placenta is associated with endometrial T-cell recruitment

American Journal of Reproductive Immunology

Volumn 57, Issue 4, 2007, Pages 250-261

  Dimova, Tanya ^a   Mihaylova, Anastassia ^b   Spassova, Petia ^b   Georgieva, Rayna ^a  

^a BULGARIAN ACADEMY OF SCIENCES   (Bulgaria)

^b UNIVERSITY HOSPITAL ALEXANDROVSKA   (Bulgaria)

Author keywords

Epitheliochorial placenta; Pigs; Tcell clusters; Tlymphocytes

Indexed keywords

T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN;

ANIMAL CELL; ARTICLE; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EMBRYO; ENDOMETRIUM CELL; FLOW CYTOMETRY; GESTATION PERIOD; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE COUNT; NIDATION; NONHUMAN; PLACENTA DEVELOPMENT; PREGNANCY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SWINE; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH2 CELL;

ANIMALS; CHEMOTAXIS, LEUKOCYTE; EMBRYO IMPLANTATION; ENDOMETRIUM; FEMALE; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; PLACENTA; PREGNANCY; SWINE; T-LYMPHOCYTES;

EID: 33947139212     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2007.00472.x     Document Type: Article

References (46)

1. King A, Wellings V, Gardner L, Loke YW: Immunocytochemical characterization of the unusual large granulated lymphocytes in human endometrium throughout the menstrual cycle. Hum Immunol 1989; 24: 195-205.
2. King A, Burrows T, Loke YW: Human uterine natural killer cells. Nat Immunol 1997; 15: 41-50.
3. Mincheva-Nilsson L, Kling M, Hammarstrom S, Nagaeva O, Sundqvist KG, Hammarstrom ML, Baranov V: γ δ T cells of human early pregnancy decidua-evidence for local proliferation, phenotypic heterogeneity and extra-thymic differentiation. J Immunol 1997; 159: 3266-3277.
4. Aluvihare V, Kallikourdis M, Betz A: Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 2004; 5: 266-271.
5. Somerset D, Zheng Y, Kilby M, Sansom D, Drayson M: Normal human pregnancy is associated with an elevation in the immune suppressive CD25+ CD4+ regulatory T-cell subset. Immunology 2004; 112: 38-43.
6. Haller H, Radillo O, Rukavina D: An immunohistochemical study of leukocytes in human endometrium, first and third trimester basal deciduas. J Reprod Immunol 1993; 23: 41-49.
7. Amoroso EC: Placentation. In Marshall's Physiology of Reproduction, AS Parkes (Ed). London, Longmans Green, 1952, pp. 127-311.
8. Leiser R, KaufmInn P: Placental structure: in a comparative aspect. Exp Clin Endocrinol 1994; 102: 122-134.
9. Georgieva R: Dynamics of T-suppressor and T-helper lymphocytes and haemolytique plaque-forming cells during normal pregnancy in the sow. J Reprod Immunol 1984; 6: 151-156.
10. Croy BA, Wood W, King GJ: Evaluation of intrauterine suppression during pregnancy in a spesies with epitheliochorial placentation. J Immunol 1987; 139: 1088-1095.
11. Whyte A, Binns RM: Adhesion molecule expression and infiltrating maternal leukocyte phenotypes during blastocyst implantation in the pig. Cell Biol Int 1994; 18: 759-767.
12. Bischof R, Brandon M, Lee CS: Cellular immune responses in the pig uterus during pregnancy. J Reprod Immunol 1995; 29: 161-178.
13. Engelhardt H, Croy BA, King GJ: Conceptus Influences the Distribution of Uterine Leucocytes during early porcine pregnancy. Biol Reprod 2002; 66: 1875-1880.
14. Ziming Y, Croy BA, Chapeau C, King G: Elevated endometrial natural killer cell activity during early porcine pregnancy is conceptus-mediated. J Reprod Immunol 1993; 24: 153-164.
15. Kaeoket K, Dalin A, Magnusson U, Persson E: The sow endometrium at different stages of the oestrous cycle: Studies on the distribution of CD2, CD4, CD8 and MHC class II expressing cells. Anim Reprod Sci 2001; 68: 99-109.
16. Meeusen E, Bischof R, Lee CS: Comparative T-cell responses during pregnancy in large animals and humans. Am J Reprod Immunol 2001; 46: 169-179.
17. Engelhardt H, Croy BA, King JG: Evaluation of natural killer cell recruitment to embryonic attachment sites during early porcine pregnancy. Biol Reprod 2002; 66: 1185-1192.
18. Mincheva-Nilsson L, Baranov V, Yeung MM, Hammarstrom S, Hammarstrom ML: Immunomorphologic studies of human decidua-associated lymphoid cells in normal early pregnancy. J Immunol 1994; 152: 2020-2032.
19. White HD, Crassi KM, Givan AL, Stern JE, Gonzales JL, Memoli VA, Green WR, Wira CR: CD3+CD8+ CTL activity within the human female reproductive tract. J Immunol 1997; 158: 3017-3027.
20. Mosmann T, Li L, Sad S: Functions of CD8 T cell subsets secreting different cytokine patterns. Semin Immunol 1997; 9: 87-92.
21. Shao L, Jacobs A, Johnson V, Mayer L: Activation of CD8+ T cells by human placental trophoblasts. J Immunol 2005; 174: 7539-7547.
22. O'Leary S, Jasper MJ, Warnes GM, Armstrong DT, Robertson SA: Seminal plasma regulates endometrial cytokines expression, leukocyte recruitment and embryo development in the pig. Reproduction 2004; 128: 237-247.
23. Robertson S, Sharkey DJ: The role of semen in induction of maternal immune tolerance to pregnancy. Semin Immunol 2001; 13: 243-254.
24. Wegmann T, Lin H, Guilbert L, Mosmann T: Bidirectorial cytokine interactions in the maternal-fetal relationship: Is successful pregnancy a Th2 phenomenon? Immunol Today 1993; 14: 353-356.
25. Sakagushi S, Sakagushi N, Shimizu J, Yamazaki S, Skihama T, Itoh M, Kuniyasu Y, Nomura T, Toda M, Takagashi T: Immunological tolerance maintained by CD25+CD4+ regulatory T cells: Their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol Rev 2001; 182: 18-32.
26. Chaouat G, Zourbas S, Ostoji S, Lapree-Delage G, Dubanchet S, Ledee N, Martal J: A brief review of recent data on some cytokine expression at materno-foetal interface which might challenge the classical Th1/Th2 dichotomy. J Reprod Immunol 2002; 53: 241-256.
27. Nagaeva O, Jonsson L, Mincheva-Nilsson L: Dominant Il-10 and TGF β mRNA expression in gamma/delta T cells in human early pregnancy deciduas suggests immunoregulatory potential. Am J Reprod Immunol 2002; 48: 9-17.
28. Gupta A, Dekaney C, Bazer F, Madrigal M, Jaeder L: Beta transgorming grouth factor beta (TGF β) at the porcine conceptus-maternal interface. Part II: Uterine TGF β bioactivity and expression of immunoreactive TGF β (TGF β 1, TGF β 2, TGF β 3) and their receptors (type I and type II). Biol Reprod 1998; 59: 911-917.
29. Liu W, Gottshall S, Hansen P: Increased expression of cell surface markers on endometrial gamma/delta T cell receptor intraepithelial lymphocytes induced by the local presence of the sheep conceptus. Am J Reprod Immunol 1997; 37: 199-205.
30. Yeh CG, Bulmer JN, His B, Tian W, Rittershaus C, Ip SH: Monoclonal antibodies to T cell receptor gamma/delta complex react with human endometrial glandular epithelium. Placenta 1990; 11: 253-261.
31. Mincheva-Nilsson L, Hamarstrom S, Hamarstrom ML: Human decidual leukocytes from early pregnancy contain hifh number of γ δ T cells and show selective down-regulation of alloreactivity. J Immunol 1992; 149: 2203-2211.
32. Heyborne K, Fu Y, Nelson A, Farr A, O'Brien R, Born W: Recognition of trophoblasts by gamma/delta T cells. J Immunol 1994; 153: 2918-2926.
33. Bonneville M, Jneway C, Ito K, Haser W, Ishida I, Nakanishit N, Tonegawa S: Intestinal intra-epithelial lymphocytes are a distinct subset of γ δ T cells. Nature 1988; 336: 479-481.
34. Mincheva-Nilsson L, Nagaeva O, Sundqvist KG, Hammarstrom ML, Hammarstrom S, Baranov V: γ δ T cells of human early pregnancy decidua: evidence for cytotoxyc potency. Int Immunol 2000; 12: 585-596.
35. Szekeres-Bartho J, Barakonyi A, Polgar B, Par G, Faust Z, Palkovics T, Szereday L: The role of γ δ T cells in progesterone-mediated immunomodulation during pregnancy: A review. Am J Reprod Immunol 1999; 42: 44-48.
36. King GJ: Reduction of uterine intra-epithelial lymphocytes during early gestation in pigs. J Reprod Immunol 1988; 14: 41-46.
37. Engelhardt H, Croy BA, King GJ: Role of uterine immune cells in early pregnancy in pigs. J Reprod Fertil Suppl 1997; 52: 115-131.
38. Pescovitz M, Sakopoulos A, Gaddy J, Husmann R, Zuckermann F: Porcine peripheral blood CD4+/CD8+ dual expressing T cells. Vet Immunol Immunopathol 1994; 43: 53-62.
39. Butitini M, Westland C, Maslial E, Yafeh A, Wyss-Coray T, Mucke L: Novel role of human CD4 molecule identified in neurodegeneration. Nat Med 1998; 4: 441-446.
40. Georgieva R: Some immunological problems of pregnancy. Doctoral Thesis, Sofia, Institute of Biology and Immunology of Reproduction, 1985.
41. Hayakawa S, Saito S, Nemoto N, Chishima F, Akiyama K, Shiraishi H, Hayakawa J, Karasaki-Suzuki M, Fujii M, Ichijo M, Sakurai I, Satoh K: Expression of recombinase-activating genes (RAG-1 and 2) in human decidual mononuclear cells. J Immunol 1994; 153: 4934-4939.
42. Bazer FW, Spencer TE, Ott TL: Placental interferons. Am J Reprod Immunol 1996; 35: 297-308.
43. Cencic A, Guillomot M, Koren S, La Bonnardiere C: Trophoblastic interferons: Do they modulate uterine cellular markers at the time of conceptus attachment in the pig. Placenta 2003; 24: 862-869.
44. Sauty A, Dziejman M, Taha R, Iarossi A, Neote K, Garcia-Zepeda E, Hamid Q, Luster A: The T cell specific CXC chemokines IP-10, Mig, and I-TAG are expressed by activated human bronchial epithelial cells. J Immunol 1999; 162: 3549-3558.
45. Gasperini S, Marchi M, Calzetti F, Laudanna C, Vicentini L, Olsen H, Murphy M, Liao F, Farber J, Cassatella M: Gene expression and production of the monokine induced by IFN γ (MIG), IFN-inducible T cell γ chemoattractant (I-TAG), and IFN γ-inducible protein-10 (IP-10) chemokines by human neutrophils. J Immunol 1999; 162: 4928-4937.
46. Taub D, Longo D, Murphy W: Human IP-10 induces mononuclear cell infiltration in mice and promotes the migration of human T lymphocytes into the peripheral tissues of human peripheral blood lymphocytes-SCID mice. Blood 1996; 87: 1423-1431.