Immunological mechanisms to establish embryo tolerance in early bovine pregnancy

Reproduction, Fertility and Development

Volumn 23, Issue 5, 2011, Pages 619-632

  Groebner, A E ^a   Schulke, K ^a   Schefold, J C ^b   Fusch, G ^e   Sinowatz, F ^c   Reichenbach, H D ^d   Wolf, E ^c   Meyer, H H D ^a   Ulbrich, S E ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

^d Bavarian State Institute for Agriculture   (Germany)

^e UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

3 dioxygenase; Bos taurus; endometrium; indoleamine 2; peri implantation

Indexed keywords

CD45 ANTIGEN; INDOLEAMINE 2,3 DIOXYGENASE; KYNURENINE; MESSENGER RNA; TRYPTOPHAN;

ALLOGRAFT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ARTIFICIAL INSEMINATION; CELLULAR DISTRIBUTION; COCULTURE; CONTROLLED STUDY; COW; CRYOPRESERVATION; EMBRYO; ENDOMETRIUM; ENDOMETRIUM CELL; ENZYME ACTIVITY; ENZYME INDUCTION; ESTRUS; FEMALE; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; IMMUNOLOGICAL TOLERANCE; IN SITU HYBRIDIZATION; IN VITRO STUDY; LEUKOCYTE; NIDATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PREGNANCY; PREIMPLANTATION EMBRYO; PROTEIN EXPRESSION; SEMINAL PLASMA; SPERMATOZOON; STROMA CELL; TANDEM MASS SPECTROMETRY;

ANIMALS; CATTLE; CELLS, CULTURED; COCULTURE TECHNIQUES; EMBRYO IMPLANTATION; EMBRYO, MAMMALIAN; ENDOMETRIUM; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GESTATIONAL AGE; IMMUNE TOLERANCE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INSEMINATION, ARTIFICIAL; KYNURENINE; LEUKOCYTES; PREGNANCY; RNA, MESSENGER; TANDEM MASS SPECTROMETRY; TRYPTOPHAN; UP-REGULATION;

ANIMALIA; BOS TAURUS; BOVINAE;

EID: 79958145612     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD10230     Document Type: Article

References (48)

1. Bauersachs, S., Ulbrich, S. E., Gross, K., Schmidt, S. E., Meyer, H. H., Einspanier, R., Wenigerkind, H., Vermehren, M., Blum, H., Sinowatz, F., and Wolf, E. (2005). Gene expression profiling of bovine endometrium during the oestrous cycle: detection of molecular pathways involved in functional changes. J. Mol. Endocrinol. 34, 889-908. doi:10.1677/JME. 1.01799 (Pubitemid 40903609)
2. Bauersachs, S., Ulbrich, S. E., Gross, K., Schmidt, S. E., Meyer, H. H., Wenigerkind, H., Vermehren, M., Sinowatz, F., Blum, H., and Wolf, E. (2006). Embryo-induced transcriptome changes in bovine endometrium reveal species-specific and common molecular markers of uterine receptivity. Reproduction 132, 319-331. doi:10.1530/REP.1.00996 (Pubitemid 44269713)
3. Bazer, F. W., Burghardt, R. C., Johnson, G. A., Spencer, T. E., and Wu, G. (2008). Interferons and progesterone for establishment and maintenance of pregnancy: interactions among novel cell signaling pathways. Reprod. Biol. 8, 179-211.
4. Bondurant, R. H. (1999). Inflammation in the bovine female reproductive tract. J. Anim. Sci. 77 (Suppl. 2), 101-110.
5. Choi, Y., Johnson, G. A., Burghardt, R. C., Berghman, L. R., Joyce, M. M., Taylor, K. M., Stewart, M. D., Bazer, F. W., and Spencer, T. E. (2001). Interferon regulatory factor-two restricts expression of interferonstimulated genes to the endometrial stroma and glandular epithelium of the ovine uterus. Biol. Reprod. 65, 1038-1049. doi:10.1095/BIOL REPROD65.4.1038 (Pubitemid 32927568)
6. Choi, Y., Johnson, G. A., Spencer, T. E., and Bazer, F. W. (2003). Pregnancy and interferon tau regulate major histocompatibility complex class I and beta2-microglobulin expression in the ovine uterus. Biol. Reprod. 68, 1703-1710. doi:10.1095/BIOLREPROD.102.012708 (Pubitemid 36519775)
7. Croy, B. A., van den Heuvel, M. J., Borzychowski, A. M., and Tayade, C. (2006). Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol. Rev. 214, 161-185. doi:10.1111/J.1600-065X.2006. 00447. X (Pubitemid 44707910)
8. Dacal, V., Colwell, D. D., Lopez, C., Perez, V., Vazquez, L., Cienfuegos, S., Diaz, P., Morrondo, P., ez-Banos, P., and Panadero, R. (2009). Local and systemic cytokine responses during larval penetration in cattle experimentally infested with Hypoderma lineatum (Diptera: Oestridae). Vet. Immunol. Immunopathol. 131, 59-64. doi:10.1016/J. VETIMM.2009. 03.011
9. Davies, C. J., Fisher, P. J., and Schlafer, D. H. (2000). Temporal and regional regulation of major histocompatibility complex class I expression at the bovine uterine/placental interface. Placenta 21, 194-202. doi:10.1053/PLAC.1999.0475 (Pubitemid 30240785)
10. Davies, C. J., Eldridge, J. A., Fisher, P. J., and Schlafer, D. H. (2006). Evidence for expression of both classical and non-classical major histocompatibility complex class I genes in bovine trophoblast cells. Am. J. Reprod. Immunol. 55, 188-200. doi:10.1111/J.1600-0897.2005. 00364. X (Pubitemid 43329495)
11. Davies, D., Meade, K. G., Herath, S., Eckersall, P. D., Gonzalez, D., White, J. O., Conlan, R. S., O'Farrelly, C., and Sheldon, I. M. (2008). Tolllike receptor and antimicrobial peptide expression in the bovine endometrium. Reprod. Biol. Endocrinol. 6, 53. doi:10.1186/1477-7827-6-53
12. Della Chiesa, M., Carlomagno, S., Frumento, G., Balsamo, M., Cantoni, C., Conte, R., Moretta, L., Moretta, A., and Vitale, M. (2006). The tryptophan catabolite L-kynurenine inhibits the surface expression of NKp46-and NKG2D-activating receptors and regulates NK-cell function. Blood 108, 4118-4125. doi:10.1182/BLOOD-2006-03-006700 (Pubitemid 44913283)
13. Dore Jr., J. J., Wilkinson, J. E., and Godkin, J. D. (1996). Ovine endometrial expression of transforming growth factor beta isoforms during the periimplantation period. Biol. Reprod. 54, 1080-1087. doi:10.1095/BIOL REPROD54.5.1080 (Pubitemid 26126753)
14. Doyle, J., Ellis, S. A., O'Gorman, G. M., paricio Donoso, I. M., Lonergan, P., and Fair, T. (2009). Classical and non-classical major histocompatibility complex class I gene expression in in vitro derived bovine embryos. J. Reprod. Immunol. 82, 48-56. doi:10.1016/J. JRI.2009.06.125
15. Drenzek, J. G., Breburda, E. E., Burleigh, D. W., Bondarenko, G. I., Grendell, R. L., and Golos, T. G. (2008). Expression of indoleamine 2, 3-dioxygenase in the rhesus monkey and common marmoset. J. Reprod. Immunol. 78, 125-133. doi:10.1016/J. JRI.2008.03.005
16. Fallarino, F., Grohmann, U., You, S., McGrath, B. C., Cavener, D. R., Vacca, C., Orabona, C., Bianchi, R., Belladonna, M. L., Volpi, C., Santamaria, P., Fioretti, M. C., and Puccetti, P. (2006). The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naive T cells. J. Immunol. 176, 6752-6761. (Pubitemid 43787857)
17. Flynn, R. J., and Mulcahy, G. (2008). Possible role for Toll-like receptors in interaction of Fasciola hepatica excretory/secretory products with bovine macrophages. Infect. Immun. 76, 678-684. doi:10.1128/IAI. 00732-07 (Pubitemid 351251739)
18. Gao, H., Wu, G., Spencer, T. E., Johnson, G. A., and Bazer, F. W. (2009). Select nutrients in the ovine uterine lumen. IV. Expression of neutral and acidic amino acid transporters in ovine uteri and peri-implantation conceptuses. Biol. Reprod. 80, 1196-1208. doi:10.1095/BIOLRE PROD.108.075440
19. Gogolin-Ewens, K. J., Lee, C. S., Mercer, W. R., and Brandon, M. R. (1989). Site-directed differences in the immune response to the fetus. Immunology 66, 312-317. (Pubitemid 19065813)
20. Groebner, A. E., Schulke, K., Unterseer, S., Reichenbach, H. D., Reichenbach, M., Buttner, M., Wolf, E., Meyer, H. H., and Ulbrich, S. E. (2010). Enhanced proapoptotic gene expression of XAF1, CASP8 and TNFSF10 in the bovine endometrium during early pregnancy is not correlated with augmented apoptosis. Placenta 31, 168-177. doi:10.1016/J. PLACENTA.2009.12.017
21. Hill, J. R., Schlafer, D. H., Fisher, P. J., and Davies, C. J. (2002). Abnormal expression of trophoblast major histocompatibility complex class I antigens in cloned bovine pregnancies is associated with a pronounced endometrial lymphocytic response. Biol. Reprod. 67, 55-63. doi:10.1095/ BIOLREPROD67.1.55 (Pubitemid 34680635)
22. Imakawa, K., Nagaoka, K., Nojima, H., Hara, Y., and Christenson, R. K. (2005). Changes in immune cell distribution and IL-10 production are regulated through endometrial IP-10 expression in the goat uterus. Am. J. Reprod. Immunol. 53, 54-64. doi:10.1111/J.1600-0897.2004. 00243. X (Pubitemid 40246485)
23. Jeddi-Tehrani, M., Abbasi, N., Dokouhaki, P., Ghasemi, J., Rezania, S., Ostadkarampour, M., Rabbani, H., Akhondi, M. A., Fard, Z. T., and Zarnani, A. H. (2009). Indoleamine 2, 3-dioxygenase is expressed in the endometrium of cycling mice throughout the oestrous cycle. J. Reprod. Immunol. 80, 41-48. doi:10.1016/J. JRI.2009.02.003
24. Klein, C., Bauersachs, S., Ulbrich, S. E., Einspanier, R., Meyer, H. H., Schmidt, S. E., Reichenbach, H. D., Vermehren, M., Sinowatz, F., Blum, H., and Wolf, E. (2006). Monozygotic twin model reveals novel embryoinduced transcriptome changes of bovine endometrium in the preattachment period. Biol. Reprod. 74, 253-264. doi:10.1095/BIOLREPROD. 105.046748 (Pubitemid 43122276)
25. Lee, C. S., Meeusen, E., Gogolin-Ewens, K., and Brandon, M. R. (1992). Quantitative and qualitative changes in the intraepithelial lymphocyte population in the uterus of nonpregnant and pregnant sheep. Am. J. Reprod. Immunol. 28, 90-96. (Pubitemid 23017928)
26. Leung, S. T., Derecka, K., Mann, G. E., Flint, A. P., and Wathes, D. C. (2000). Uterine lymphocyte distribution and interleukin expression during early pregnancy in cows. J. Reprod. Fertil. 119, 25-33. (Pubitemid 30312724)
27. Lewis, G. S. (2003). Steroidal regulation of uterine resistance to bacterial infection in livestock. Reprod. Biol. Endocrinol. 1, 117. doi:10.1186/1477-7827-1-117 (Pubitemid 39130408)
28. Low, B. G., Hansen, P. J., Drost, M., and Gogolin-Ewens, K. J. (1990). Expression of major histocompatibility complex antigens on the bovine placenta. J. Reprod. Fertil. 90, 235-243. doi:10.1530/JRF.0.0900235 (Pubitemid 20293748)
29. Meeusen, E., Fox, A., Brandon, M., and Lee, C. S. (1993). Activation of uterine intraepithelial gamma delta T cell receptor-positive lymphocytes during pregnancy. Eur. J. Immunol. 23, 1112-1117. doi:10.1002/EJI. 1830230520 (Pubitemid 23120174)
30. Meeusen, E. N., Bischof, R. J., and Lee, C. S. (2001). Comparative T-cell responses during pregnancyinlarge animals and humans. Am. J. Reprod. Immunol. 46, 169-179. doi:10.1111/J.8755-8920.2001.460208. X (Pubitemid 32691200)
31. Mellor, A. L., and Munn, D. H. (1999). Tryptophan catabolism and T-cell tolerance: immunosuppression by starvation? Immunol. Today 20, 469-473. doi:10.1016/S0167-5699 (99) 01520-0 (Pubitemid 29476077)
32. Mellor, A. L., and Munn, D. H. (2000). Immunology at the maternal-fetal interface: lessons for T cell tolerance and suppression. Annu. Rev. Immunol. 18, 367-391. doi:10.1146/ANNUREV. IMMUNOL. 18.1.367 (Pubitemid 30365385)
33. Mellor, A. L., Sivakumar, J., Chandler, P., Smith, K., Molina, H., Mao, D., and Munn, D. H. (2001). Prevention of T cell-driven complement activation and inflammation by tryptophan catabolism during pregnancy. Nat. Immunol. 2, 64-68. doi:10.1038/83183 (Pubitemid 33704955)
34. Padua, M. B., Tekin, S., Spencer, T. E., and Hansen, P. J. (2005). Actions of progesterone on uterine immunosuppression and endometrial gland development in the uterine gland knockout (UGKO) ewe. Mol. Reprod. Dev. 71, 347-357. doi:10.1002/MRD.20301 (Pubitemid 40770389)
35. Prakash, B. S., Meyer, H. H., Schallenberger, E., and van de Wiel, D. F. (1987). Development of a sensitive enzymeimmunoassay (EIA) for progesterone determination in unextracted bovine plasma using the second antibody technique. J. Steroid Biochem. 28, 623-627. doi:10.1016/0022-4731 (87) 90389-X (Pubitemid 18024982)
36. Puccetti, P., and Grohmann, U. (2007). IDO and regulatory T cells: a role for reverse signalling and non-canonical NF-kappaB activation. Nat. Rev. Immunol. 7, 817-823. doi:10.1038/NRI2163 (Pubitemid 47480306)
37. Roberts, R. M., Liu, L., Guo, Q., Leaman, D., and Bixby, J. (1998). The evolution of the type I interferons. J. Interferon Cytokine Res. 18, 805-816. doi:10.1089/JIR.1998.18.805 (Pubitemid 28489658)
38. Roussev, R. G., and Coulam, C. B. (2007). HLA-G and its role in implantation. J. Assist. Reprod. Genet. 24, 288-295. [Review] doi:10.1007/S10815-007-9148-3 (Pubitemid 47593599)
39. Schallenberger, E., Schams, D., and Meyer, H. H. (1989). Sequences of pituitary, ovarian and uterine hormone secretion during the first 5 weeks of pregnancy in dairy cattle. J. Reprod. Fertil. Suppl. 37, 277-286.
40. Schefold, J. C., Zeden, J. P., Pschowski, R., Hammoud, B., Fotopoulou, C., Hasper, D., Fusch, G., VonHaehling, S., Volk, H. D., Meisel, C., Schutt, C., and Reinke, P. (2010). Treatment with granulocyte-macrophage colony-stimulating factor is associated with reduced indoleamine 2, 3-dioxygenase activity and kynurenine pathway catabolites in patients with severe sepsis and septic shock. Scand. J. Infect. Dis. 42, 164-171. doi:10.3109/00365540903405768
41. Ulbrich, S. E., Frohlich, T., Schulke, K., Englberger, E., Waldschmitt, N., Arnold, G. J., Reichenbach, H. D., Reichenbach, M., Wolf, E., Meyer, H. H., and Bauersachs, S. (2009). Evidence for estrogen-dependent uterine serpin (SERPINA14) expression during estrus in the bovine endometrial glandular epithelium and lumen. Biol. Reprod. 81, 795-805. doi:10.1095/BIOLREPROD.108. 075184
42. Vander Wielen, A. L., and King, G. J. (1984). Intraepithelial lymphocytes in the bovine uterus during the oestrous cycle and early gestation. J. Reprod. Fertil. 70, 457-462. doi:10.1530/JRF.0.0700457 (Pubitemid 14157714)
43. von Rango, U. (2008). Fetal tolerance inhuman pregnancy: acrucial balance between acceptance and limitation of trophoblast invasion. Immunol. Lett. 115, 21-32. doi:10.1016/J. IMLET.2007.09.014
44. von Rango, U., Krusche, C. A., Beier, H. M., and Classen-Linke, I. (2007). Indoleamine-dioxygenase is expressed in human decidua at the time maternal tolerance is established. J. Reprod. Immunol. 74, 34-45. doi:10.1016/J. JRI.2006.11.001 (Pubitemid 46679063)
45. Wolf, E., Arnold, G. J., Bauersachs, S., Beier, H. M., Blum, H., Einspanier, R., Frohlich, T., Herrler, A., Hiendleder, S., Kolle, S., Prelle, K., Reichenbach, H. D., Stojkovic, M., Wenigerkind, H., and Sinowatz, F. (2003). Embryo-maternal communication in bovine: strategies for deciphering a complex cross-talk. Reprod. Domest. Anim. 38, 276-289. doi:10.1046/J.1439-0531.2003. 00435. X (Pubitemid 37053849)
46. Wooding, F. B., and Wathes, D. C. (1980). Binucleate cell migration in the bovine placentome. J. Reprod. Fertil. 59, 425-430. doi:10.1530/JRF. 0.0590425 (Pubitemid 10012877)
47. Yoon, H. J., Jeon, S. B., Kim, I. H., and Park, E. J. (2008). Regulation of TLR2 expression by prostaglandins in brain glia. J. Immunol. 180, 8400-8409.
48. Zenclussen, A. C., Schumacher, A., Zenclussen, M. L., Wafula, P., and Volk, H. D. (2007). Immunology of pregnancy: cellular mechanisms allowing fetal survival within the maternal uterus. Expert Rev. Mol. Med. 9, 1-14. doi:10.1017/S1462399407000294 (Pubitemid 47108089)