Modulation of maternal immune system during pregnancy in the cow

Reproduction in Domestic Animals

Volumn 47, Issue SUPPL.4, 2012, Pages 384-393

  Oliveira, L J ^a   Barreto, R S N ^a   Perecin, F ^a   Mansouri Attia, N ^b   Pereira, F T V ^c   Meirelles, F V ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ARTICLE; BREEDING; CATTLE; FEMALE; GENE EXPRESSION REGULATION; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT;

ANIMALS; CATTLE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNE TOLERANCE; PREGNANCY; PREGNANCY, ANIMAL;

BOVINAE;

EID: 84864303321     PISSN: 09366768     EISSN: 14390531     Source Type: Journal    
DOI: 10.1111/j.1439-0531.2012.02102.x     Document Type: Article

References (117)

1. Abrahams VM, Kim YM, Straszewski SL, Romero R, Mor G, 2004: Macrophages and apoptotic cell clearance during pregnancy. Am J Reprod Immunol 51, 275-282.
2. Al Naib A, Mamo S, O'Gorman GM, Lonergan P, Swales A, Fair T, 2011: Regulation of non-classical major histocompatability complex class I mRNA expression in bovine embryos. J Reprod Immunol 91, 31-40.
3. Almeria S, Serrano B, Yaniz JL, Darwich L, Lopez-Gatius F, 2012: Cytokine gene expression profiles in peripheral blood mononuclear cells from Neospora caninum naturally infected dams throughout gestation. Vet Parasitol 183, 237-243.
4. Aluvihare VR, Kallikourdis M, Betz AG, 2004: Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 5, 266-271.
5. Atay S, Gercel-Taylor C, Suttles J, Mor G, Taylor DD, 2011: Trophoblast-derived exosomes mediate monocyte recruitment and differentiation. Am J Reprod Immunol 65, 65-77.
6. Bainbridge DR, Sargent IL, Ellis SA, 2001: Increased expression of major histocompatibility complex (MHC) class I transplantation antigens in bovine trophoblast cells before fusion with maternal cells. Reproduction 122, 907-913.
7. Band MR, Olmstead C, Everts RE, Liu ZL, Lewin HA, 2002: A 3800 gene microarray for cattle functional genomics: comparison of gene expression in spleen, placenta, and brain. Anim Biotechnol 13, 163-172.
8. Barreto RS, Bressan FF, Oliveira LJ, Pereira FT, Perecin F, Ambrosio CE, Meirelles FV, Miglino MA, 2011: Gene expression in placentation of farm animals: an overview of gene function during development. Theriogenology 76, 589-597.
9. Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M, 2008: Growth factors and cytokines in wound healing. Wound Repair Regen 16, 585-601.
10. Bauersachs S, Mitko K, Ulbrich SE, Blum H, Wolf E, 2008: Transcriptome studies of bovine endometrium reveal molecular profiles characteristic for specific stages of estrous cycle and early pregnancy. Exp Clin Endocrinol Diabetes 116, 371-384.
11. Benedictus L, Thomas AJ, Jorritsma R, Davies CJ, Koets AP, 2012: Two-way calf to dam major histocompatibility class I compatibility increases risk for retained placenta in cattle. Am J Reprod Immunol 67, 224-230.
12. Boysen P, Storset AK, 2009: Bovine natural killer cells. Vet Immunol Immunopathol 130, 163-177.
13. Bulmer JN, Johnson PM, 1985: Antigen expression by trophoblast populations in the human placenta and their possible immunobiological relevance. Placenta 6, 127-140.
14. Chen L, Belton RJ Jr, Nowak RA, 2009: Basigin-mediated gene expression changes in mouse uterine stromal cells during implantation. Endocrinology 150, 966-976.
15. Cobb SP, Watson ED, 1995: Immunohistochemical study of immune cells in the bovine endometrium at different stages of the oestrous cycle. Res Vet Sci 59, 238-241.
16. Cormican P, Meade KG, Cahalane S, Narciandi F, Chapwanya A, Lloyd AT, O'Farrelly C, 2008: Evolution, expression and effectiveness in a cluster of novel bovine beta-defensins. Immunogenetics 60, 147-156.
17. Cronin JG, Turner ML, Goetze L, Bryant CE, Sheldon IM, 2012: Toll-Like Receptor 4 and MYD88-Dependent Signaling Mechanisms of the Innate Immune System Are Essential for the Response to Lipopolysaccharide by Epithelial and Stromal Cells of the Bovine Endometrium. Biol Reprod 86, 51.
18. Croy BA, van den Heuvel MJ, Borzychowski AM, Tayade C, 2006: Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol Rev 214, 161-185.
19. Dantzer V, 1999: Epitheliochorial placentation. In: Knobil E, Neill J (eds), Encyclopedia of Reproduction, Vol. 1, 1 edn. Academic Press, San Diego, pp. 18-28.
20. Davies CJ, Fisher PJ, Schlafer DH, 2000: Temporal and regional regulation of major histocompatibility complex class I expression at the bovine uterine/placental interface. Placenta 21, 194-202.
21. Davies CJ, Hill JR, Edwards JL, Schrick FN, Fisher PJ, Eldridge JA, Schlafer DH, 2004: Major histocompatibility antigen expression on the bovine placenta: its relationship to abnormal pregnancies and retained placenta. Anim Reprod Sci 82-83, 267-280.
22. Davies CJ, Eldridge JA, Fisher PJ, Schlafer DH, 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.
23. Davies D, Meade KG, Herath S, Eckersall PD, Gonzalez D, White JO, Conlan RS, O'Farrelly C, Sheldon IM, 2008: Toll-like receptor and antimicrobial peptide expression in the bovine endometrium. Reprod Biol Endocrinol 18, 53.
24. Detilleux JC, Kehrli ME Jr, Stabel JR, Freeman AE, Kelley DH, 1995: Study of immunological dysfunction in periparturient Holstein cattle selected for high and average milk production. Vet Immunol Immunopathol 44, 251-267.
25. Donaldson WL, Zhang CH, Oriol JG, Antczak DF, 1990: Invasive equine trophoblast expresses conventional class I major histocompatibility complex antigens. Development 110, 63-71.
26. Duncan WC, Shaw JL, Burgess S, McDonald SE, Critchley HO, Horne AW, 2011: Ectopic pregnancy as a model to identify endometrial genes and signaling pathways important in decidualization and regulated by local trophoblast. PLoS ONE 6, e23595.
27. Emond V, Fortier MA, Murphy BD, Lambert RD, 1998: Prostaglandin E2 regulates both interleukin-2 and granulocyte-macrophage colony-stimulating factor gene expression in bovine lymphocytes. Biol Reprod 58, 143-151.
28. Emond V, Asselin E, Fortier MA, Murphy BD, Lambert RD, 2000: Interferon-tau stimulates granulocyte-macrophage colony-stimulating factor gene expression in bovine lymphocytes and endometrial stromal cells. Biol Reprod 62, 1728-1737.
29. Fahey JV, Rossoll RM, Wira CR, 2005a: Sex hormone regulation of anti-bacterial activity in rat uterine secretions and apical release of anti-bacterial factor(s) by uterine epithelial cells in culture. J Steroid Biochem Mol Biol 93, 59-66.
30. Fahey JV, Schaefer TM, Channon JY, Wira CR, 2005b: Secretion of cytokines and chemokines by polarized human epithelial cells from the female reproductive tract. Hum Reprod 20, 1439-1446.
31. Fair T, Gutierrez-Adan A, Murphy M, Rizos D, Martin F, Boland MP, Lonergan P, 2004: Search for the bovine homolog of the murine ped gene and characterization of its messenger RNA expression during bovine preimplantation development. Biol Reprod 70, 488-494.
32. Foldi J, Kulcsar M, Pecsi A, Huyghe B, de Sa C, Lohuis JA, Cox P, Huszenicza G, 2006: Bacterial complications of postpartum uterine involution in cattle. Anim Reprod Sci 96, 265-281.
33. Forde N, Carter F, Spencer TE, Bazer FW, Sandra O, Mansouri-Attia N, Okumu LA, McGettigan PA, Mehta JP, McBride R, O'Gaora P, Roche JF, Lonergan P, 2011: Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biol Reprod 85, 144-156.
34. Gabler C, Fischer C, Drillich M, Einspanier R, Heuwieser W, 2010: Time-dependent mRNA expression of selected pro-inflammatory factors in the endometrium of primiparous cows postpartum. Reprod Biol Endocrinol 8, 152.
35. Galvao KN, Santos NR, Galvao JS, Gilbert RO, 2011: Association between endometritis and endometrial cytokine expression in postpartum Holstein cows. Theriogenology 76, 290-299.
36. Gerner W, Stadler M, Hammer SE, Klein D, Saalmuller A, 2010: Sensitive detection of Foxp3 expression in bovine lymphocytes by flow cytometry. Vet Immunol Immunopathol 138, 154-158.
37. Gogolin-Ewens K, Lee C, Mercer W, Brandon M, 1989: Site-directed differences in the immune response to the fetus. Immunology 66, 312-317.
38. Gordon S, 2003: Alternative activation of macrophages. Nat Rev Immunol 3, 23-35.
39. Groebner AE, Schulke K, Schefold JC, Fusch G, Sinowatz F, Reichenbach HD, Wolf E, Meyer HH, Ulbrich SE, 2011: Immunological mechanisms to establish embryo tolerance in early bovine pregnancy. Reprod Fertil Dev 23, 619-632.
40. Gustafsson C, Mjosberg J, Matussek A, Geffers R, Matthiesen L, Berg G, Sharma S, Buer J, Ernerudh J, 2008: Gene expression profiling of human decidual macrophages: evidence for immunosuppressive phenotype. PLoS ONE 3, e2078.
41. Han H, Austin KJ, Rempel LA, Hansen TR, 2006: Low blood ISG15 mRNA and progesterone levels are predictive of non-pregnant dairy cows. J Endocrinol 191, 505-512.
42. Hashizume K, 2007: Analysis of uteroplacental-specific molecules and their functions during implantation and placentation in the bovine. J Reprod Dev 53, 1-11.
43. Hashizume K, Ushizawa K, Patel OV, Kizaki K, Imai K, Yamada O, Nakano H, Takahashi T, 2007: Gene expression and maintenance of pregnancy in bovine: roles of trophoblastic binucleate cell-specific molecules. Reprod Fertil Dev 19, 79-90.
44. Heemskerk B, Lankester AC, van Vreeswijk T, Beersma MF, Claas EC, Veltrop-Duits LA, Kroes AC, Vossen JM, Schilham MW, van Tol MJ, 2005: Immune reconstitution and clearance of human adenovirus viremia in pediatric stem-cell recipients. J Infect Dis 191, 520-530.
45. Herath S, Lilly ST, Santos NR, Gilbert RO, Goetze L, Bryant CE, White JO, Cronin J, Sheldon IM, 2009: Expression of genes associated with immunity in the endometrium of cattle with disparate postpartum uterine disease and fertility. Reprod Biol Endocrinol 7, 55.
46. Hill JR, Schlafer DH, Fisher PJ, Davies CJ, 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.
47. Hoek A, Rutten VP, Kool J, Arkesteijn GJ, Bouwstra RJ, Van Rhijn I, Koets AP, 2009: Subpopulations of bovine WC1(+) gammadelta T cells rather than CD4(+)CD25(high) Foxp3(+) T cells act as immune regulatory cells ex vivo. Vet Res 40, 6.
48. Hunt JS, Manning LS, Mitchell D, Selanders JR, Wood GW, 1985: Localization and characterization of macrophages in murine uterus. J Leukoc Biol 38, 255-265.
49. Ishiwata H, Katsuma S, Kizaki K, Patel OV, Nakano H, Takahashi T, Imai K, Hirasawa A, Shiojima S, Ikawa H, Suzuki Y, Tsujimoto G, Izaike Y, Todoroki J, Hashizume K, 2003: Characterization of gene expression profiles in early bovine pregnancy using a custom cDNA microarray. Mol Reprod Dev 65, 9-18.
50. Joosten I, Sanders MF, Hensen EJ, 1991: Involvement of major histocompatibility complex class I compatibility between dam and calf in the aetiology of bovine retained placenta. Anim Genet 22, 455-463.
51. Karcher EL, Beitz DC, Stabel JR, 2008: Parturition invokes changes in peripheral blood mononuclear cell populations in Holstein dairy cows naturally infected with Mycobacterium avium subsp. paratuberculosis. Vet Immunol Immunopathol 124, 50-62.
52. Kimura K, Goff JP, Kehrli ME Jr, Harp JA, 1999: Phenotype analysis of peripheral blood mononuclear cells in periparturient dairy cows. J Dairy Sci 82, 315-319.
53. Kimura K, Goff JP, Kehrli ME Jr, Harp JA, Nonnecke BJ, 2002: Effects of mastectomy on composition of peripheral blood mononuclear cell populations in periparturient dairy cows. J Dairy Sci 85, 1437-1444.
54. Koga K, Mor G, 2010: Toll-like receptors at the maternal-fetal interface in normal pregnancy and pregnancy disorders. Am J Reprod Immunol 63, 587-600.
55. Krishnan L, Guilbert LJ, Wegmann TG, Belosevic M, Mosmann TR, 1996: T helper 1 response against Leishmania major in pregnant C57BL/6 mice increases implantation failure and fetal resorptions. Correlation with increased IFN-gamma and TNF and reduced IL-10 production by placental cells. J Immunol 156, 653-662.
56. Kumar CG, Larson JH, Band MR, Lewin HA, 2007: Discovery and characterization of 91 novel transcripts expressed in cattle placenta. BMC Genomics 8, 113.
57. Kumar CG, Everts RE, Loor JJ, Lewin HA, 2010: Functional annotation of novel lineage-specific genes using co-expression and promoter analysis. BMC Genomics 11, 161.
58. Kydd JH, Butcher GW, Antczak DF, Allen WR, 1991: Expression of major histocompatibility complex (MHC) class 1 molecules on early trophoblast. J Reprod Fertil Suppl 44, 463-477.
59. Larson JH, Kumar CG, Everts RE, Green CA, Everts-van der Wind A, Band MR, Lewin HA, 2006: Discovery of eight novel divergent homologs expressed in cattle placenta. Physiol Genomics 25, 405-413.
60. Leslie MV, Hansen PJ, 1991: Progesterone-regulated secretion of the serpin-like proteins of the ovine and bovine uterus. Steroids 56, 589-597.
61. Leung ST, Derecka K, Mann GE, Flint AP, Wathes DC, 2000: Uterine lymphocyte distribution and interleukin expression during early pregnancy in cows. J Reprod Fertil 119, 25-33.
62. Loureiro B, Bonilla L, Block J, Fear JM, Bonilla AQ, Hansen PJ, 2009: Colony-stimulating factor 2 (CSF-2) improves development and posttransfer survival of bovine embryos produced in vitro. Endocrinology 150, 5046-5054.
63. Loureiro B, Block J, Favoreto MG, Carambula S, Pennington KA, Ealy AD, Hansen PJ, 2011: Consequences of conceptus exposure to colony-stimulating factor 2 on survival, elongation, interferon-tau secretion, and gene expression. Reproduction 141, 617-624.
64. Low BG, Hansen PJ, 1988: Actions of steroids and prostaglandins secreted by the placenta and uterus of the cow and ewe on lymphocyte proliferation in vitro. Am J Reprod Immunol Microbiol 18, 71-75.
65. Low BG, Hansen PJ, Drost M, Gogolin-Ewens KJ, 1990: Expression of major histocompatibility complex antigens on the bovine placenta. J Reprod Fertil 90, 235-243.
66. Luo SS, Ishibashi O, Ishikawa G, Ishikawa T, Katayama A, Mishima T, Takizawa T, Shigihara T, Goto T, Izumi A, Ohkuchi A, Matsubara S, Takeshita T, 2009: Human villous trophoblasts express and secrete placenta-specific microRNAs into maternal circulation via exosomes. Biol Reprod 81, 717-729.
67. Majeed AF, Al-Sadi HI, Ridha AM, 1995: Ovine placenta related to binucleated cells in fetal membrane retention. Small Rumin Res 17, 97-99.
68. Mansouri-Attia N, Aubert J, Reinaud P, Giraud-Delville C, Taghouti G, Galio L, Everts RE, Degrelle S, Richard C, Hue I, Yang X, Tian XC, Lewin HA, Renard JP, Sandra O, 2009a: Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation. Physiol Genomics 39, 14-27.
69. Mansouri-Attia N, Sandra O, Aubert J, Degrelle S, Everts RE, Giraud-Delville C, Heyman Y, Galio L, Hue I, Yang X, Tian XC, Lewin HA, Renard JP, 2009b: Endometrium as an early sensor of in vitro embryo manipulation technologies. Proc Natl Acad Sci U S A 106, 5687-5692.
70. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A, 2002: Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23, 549-555.
71. Martinez FO, Gordon S, Locati M, Mantovani A, 2006: Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol 177, 7303-7311.
72. Mincheva-Nilsson L, Baranov V, 2010: The role of placental exosomes in reproduction. Am J Reprod Immunol 63, 520-533.
73. Miyoshi M, Sawamukai Y, Iwanaga T, 2002: Reduced phagocytotic activity of macrophages in the bovine retained placenta. Reprod Domest Anim 37, 53-56.
74. Miyazawa K, Aso H, Honda M, Kido T, Minashima T, Kanaya T, Watanabe K, Ohwada S, Rose MT, Yamaguchi T, 2006: Identification of bovine dendritic cell phenotype from bovine peripheral blood. Res Vet Sci. 81, 40-5. Available at
75. Mjosberg J, Berg G, Ernerudh J, Ekerfelt C, 2007: CD4+ CD25+ regulatory T cells in human pregnancy: development of a Treg-MLC-ELISPOT suppression assay and indications of paternal specific Tregs. Immunology 120, 456-466.
76. Moffett A, Loke C, 2006: Immunology of placentation in eutherian mammals. Nat Rev Immunol 6, 584-594.
77. Moffett-King A, 2002: Natural killer cells and pregnancy. Nat Rev Immunol 2, 656-663.
78. Monterroso VH, Hansen PJ, 1993: Regulation of bovine and ovine lymphocyte proliferation by progesterone: modulation by steroid receptor antagonists and physiological status. Acta Endocrinol (Copenh) 129, 532-535.
79. de Moraes AA, Paula-Lopes FF, Chegini N, Hansen PJ, 1999: Localization of granulocyte-macrophage colony-stimulating factor in the bovine reproductive tract. J Reprod Immunol 42, 135-145.
80. Nonnecke BJ, Kimura K, Goff JP, Kehrli ME Jr, 2003: Effects of the mammary gland on functional capacities of blood mononuclear leukocyte populations from periparturient cows. J Dairy Sci 86, 2359-2368.
81. O'Gorman GM, Al Naib A, Ellis SA, Mamo S, O'Doherty AM, Lonergan P, Fair T, 2010: Regulation of a bovine nonclassical major histocompatibility complex class I gene promoter. Biol Reprod 83, 296-306.
82. Oliveira LJ, Hansen PJ, 2008: Deviations in populations of peripheral blood mononuclear cells and endometrial macrophages in the cow during pregnancy. Reproduction 136, 481-490.
83. Oliveira LJ, Hansen PJ, 2009: Phenotypic characterization of macrophages in the endometrium of the pregnant cow. Am J Reprod Immunol 62, 418-426.
84. Oliveira LJ, McClellan S, Hansen PJ, 2010: Differentiation of the endometrial macrophage during pregnancy in the cow. PLoS ONE 5, e13213.
85. O'Neill RG, Fitzpatrick JL, Glass EJ, Williams JL, Woolliams JA, 2007: Optimisation of the response to respiratory virus vaccines in cattle. Vet Rec 161, 269-270.
86. Oshima K, Watanabe H, Yoshihara K, Kojima T, Dochi O, Takenouchi N, Fukushima M, Komatsu M, 2003: Gene expression of leukemia inhibitory factor (LIF) and macrophage colony stimulating factor (M-CSF) in bovine endometrium during early pregnancy. Theriogenology 60, 1217-1226.
87. Padua MB, Hansen PJ, 2008: Regulation of DNA synthesis and the cell cycle in human prostate cancer cells and lymphocytes by ovine uterine serpin. BMC Cell Biol 9, 5.
88. Petzl N, 2007: Peripartale Expression von Toll-like-Rezeptoren und β-Defe Rindes Diss., Tierärztliche Hochschule, Hannover Available at
89. Racicot KE, Schimitt AP, Ott TL, 2009: Characterization of an MX1-positive population of exosomes secreted by uterin glandular epithelial cells. Am J Reprod Immunol 61, 417.
90. Riddell MR, Winkler-Lowen B, Chakrabarti S, Dunk C, Davidge ST, Guilbert LJ, 2012: The characterization of fibrocyte-like cells: a novel fibroblastic cell of the placenta. Placenta 33, 143-150.
91. Robertson SA, Care AS, Skinner RJ, 2007: Interleukin 10 regulates inflammatory cytokine synthesis to protect against lipopolysaccharide-induced abortion and fetal growth restriction in mice. Biol Reprod 76, 738-748.
92. Rosbottom A, Gibney EH, Guy CS, Kipar A, Smith RF, Kaiser P, Trees AJ, Williams DJ, 2008: Upregulation of cytokines is detected in the placentas of cattle infected with Neospora caninum and is more marked early in gestation when fetal death is observed. Infect Immun 76, 2352-2361.
93. Rosbottom A, Gibney H, Kaiser P, Hartley C, Smith RF, Robinson R, Kipar A, Williams DJ, 2011: Up regulation of the maternal immune response in the placenta of cattle naturally infected with Neospora caninum. PLoS ONE 6, e15799.
94. Salamonsen LA, Hannan NJ, Dimitriadis E, 2007: Cytokines and chemokines during human embryo implantation: roles in implantation and early placentation. Semin Reprod Med 25, 437-444.
95. Salilew-Wondim D, Holker M, Rings F, Ghanem N, Ulas-Cinar M, Peippo J, Tholen E, Looft C, Schellander K, Tesfaye D, 2010: Bovine pretransfer endometrium and embryo transcriptome fingerprints as predictors of pregnancy success after embryo transfer. Physiol Genomics 42, 201-218.
96. Schaefer TM, Fahey JV, Wright JA, Wira CR, 2005a: Innate immunity in the human female reproductive tract: antiviral response of uterine epithelial cells to the TLR3 agonist poly(I:C). J Immunol 174, 992-1002.
97. Schaefer TM, Fahey JV, Wright JA, Wira CR, 2005b: Migration inhibitory factor secretion by polarized uterine epithelial cells is enhanced in response to the TLR3 agonist poly (I:C). Am J Reprod Immunol 54, 193-202.
98. a edn. Pullman (WA): Current Conceptions, Inc, 1997. 271p.
99. Sheldon IM, Roberts MH, 2010: Toll-like receptor 4 mediates the response of epithelial and stromal cells to lipopolysaccharide in the endometrium. PLoS ONE 5, e12906.
100. Sheldon IM, Williams EJ, Miller AN, Nash DM, Herath S, 2008: Uterine diseases in cattle after parturition. Vet J 176, 115-121.
101. Shima T, Sasaki Y, Itoh M, Nakashima A, Ishii N, Sugamura K, Saito S, 2010: Regulatory T cells are necessary for implantation and maintenance of early pregnancy but not late pregnancy in allogeneic mice. J Reprod Immunol 85, 121-129.
102. Skopets B, Li J, Thatcher WW, Roberts RM, Hansen PJ, 1992: Inhibition of lymphocyte proliferation by bovine trophoblast protein-1 (type I trophoblast interferon) and bovine interferon-alpha I1. Vet Immunol Immunopathol 34, 81-96.
103. Somerset DA, Zheng Y, Kilby MD, Sansom DM, Drayson MT, 2004: Normal human pregnancy is associated with an elevation in the immune suppressive CD25+ CD4+ regulatory T-cell subset. Immunology 112, 38-43.
104. Spencer TE, Johnson GA, Bazer FW, Burghardt RC, 2004: Implantation mechanisms: insights from the sheep. Reproduction 128, 657-668.
105. Storset AK, Kulberg S, Berg I, Boysen P, Hope JC, Dissen E, 2004: NKp46 defines a subset of bovine leukocytes with natural killer cell characteristics. Eur J Immunol 34, 669-676.
106. Svensson J, Jenmalm MC, Matussek A, Geffers R, Berg G, Ernerudh J, 2011: Macrophages at the fetal-maternal interface express markers of alternative activation and are induced by M-CSF and IL-10. J Immunol 187, 3671-3682.
107. Tekin S, Hansen PJ, 2004: Regulation of numbers of macrophages in the endometrium of the sheep by systemic effects of pregnancy, local presence of the conceptus, and progesterone. Am J Reprod Immunol 51, 56-62.
108. Tekin S, Ealy AD, Wang SZ, Hansen PJ, 2000: Differences in lymphocyte-regulatory activity among variants of ovine IFN-tau. J Interferon Cytokine Res 20, 1001-1005.
109. Thaxton JE, Romero R, Sharma S, 2009: TLR9 activation coupled to IL-10 deficiency induces adverse pregnancy outcomes. J Immunol 183, 1144-1154.
110. The Bovine Genome Sequencing and Analysis Consortium, Elsik CG, Tellman RL, Worley KC, 2009: The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 324, 522-528.
111. Turin L, Invernizzi P, Woodcock M, Grati FR, Riva F, Tribbioli G, Laible G, 2007a: Bovine fetal microchimerism in normal and embryo transfer pregnancies and its implications for biotechnology applications in cattle. Biotechnol J 2, 486-491.
112. Turin L, Tribbioli G, Invernizzi P, Grati FR, Crema S, Laible G, Riva F, 2007b: Fetal microchimerism in normal and embryo transfer bovine pregnancies. Vet Res Commun 31(Suppl 1), 205-207.
113. Van Kampen C, Mallard BA, 1997: Effects of peripartum stress and health on circulating bovine lymphocyte subsets. Vet Immunol Immunopathol 59, 79-91.
114. Vanselow J, Furbass R, Tiemann U, 2008: Cultured bovine trophoblast cells differentially express genes encoding key steroid synthesis enzymes. Placenta 29, 531-538.
115. Wooding FB, 1980: Electron microscopic localization of binucleate cells in the sheep placenta using phosphotungstic acid. Biol Reprod 22, 357-365.
116. Xi J, Jia B, Li R, Chen W, Wang D, Yang S, 2006: Rapid sex identification of embryos in different developmental stages by blood of pregnant dairy cattle. J Shihezi Univ (Nat Sci) 24, 446-449.
117. Yang H, Qiu L, Chen G, Ye Z, Lu C, Lin Q, 2008: Proportional change of CD4+CD25+ regulatory T cells in decidua and peripheral blood in unexplained recurrent spontaneous abortion patients. Fertil Steril 89, 656-661.