Uterine natural killer cells in species with epitheliochorial placentation

Natural Immunity

Volumn 15, Issue 1, 1996, Pages 53-69

  Engelhardt, Heidi ^a   King, Gordon J ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

T cell; Cow; Epitheliochorial placenta; Horse; NK cell; Pig; Pregnancy; Sheep; Uterus

Indexed keywords

ANIMAL CELL; BOVIDS; CATTLE; DOMESTIC ANIMAL; ENDOMETRIUM; FEMALE; HORSE; LYMPHOKINE ACTIVATED KILLER CELL; NATURAL KILLER CELL; NONHUMAN; PLACENTA DEVELOPMENT; PREGNANCY; REPRODUCTION; REVIEW; SHEEP; STROMA; SUPPRESSOR CELL; SWINE; T LYMPHOCYTE; UTERUS;

ANIMALS; CATTLE; FEMALE; HORSES; KILLER CELLS, NATURAL; PLACENTATION; PREGNANCY; PREGNANCY, ANIMAL; SHEEP; SWINE; UTERUS;

EID: 0030469562     PISSN: 10188916     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (95)

1. King GJ: Comparative placentation in ungulates. J Exp Zool 1993;266: 588-602.
2. Leiser R, Kaufmann P: Placental structure: In a comparative aspect. Exp Clin Endocrinol 1994;102:122-134.
3. Wooding FBP: Electron microscope localisation of binucleate cells in the sheep placenta using phosphotungstic acid. Biol Reprod 1980;22:357-365.
4. Hoffman LH, Wooding FBP: Giant and binucleate trophoblast cells of mammals. J Exp Zool 1993;266: 559-577.
5. Wooding FBP: Frequency and localization of binucleate cells in the placentomes of ruminants. Placenta 1983;4:527-540.
6. Staples LD, Heap RB, Wooding FBP, King GJ: Migration of leukocytes into the uterus after acute removal of ovarian progesterone during early pregnancy in the sheep. Placenta 1983;4:339-350.
7. Van der Wielen AL, King GJ: Intraepithelial lymphocytes in the bovine uterus during the oestrous cycle and early gestation. J Reprod Fertil 1984;70:457-462.
8. Low BG, Hansen PJ, Drost M, Gogolin-Ewens KJ: Expression of major histocompatibility complex antigens on the bovine placenta. J Reprod Fertil 1990;90:234-243.
9. Gogolin-Ewens KJ, Lee CS, Mercer WR, Brandon MR: Site-directed differences in the immune response to the fetus. Immunology 1989;66: 312-317.
10. Lee CS, Meeusen E, Gogolin-Ewens K, Brandon MR: Quantitative and qualitative changes in the intraepithelial lymphocyte population in the uterus of nonpregnant and pregnant sheep. Am J Reprod Immunol 1992; 28:90-96.
11. Meeusen E, Fox A, Brandon M, Lee CS: Activation of uterine intraepithelial γδ T cell receptor-positive lymphocytes during pregnancy. Eur J Immunol 1993;23:1112-1117.
12. Mackay CR, Maddox JF, Brandon MR: A monoclonal antibody to the p220 component of sheep LCA identifies B cells and a unique lymphocyte subset. Cell Immunol 1987; 110:46-55.
13. Kellas LM: An intra-epithelial granular cell in the uterine epithelium of some ruminant species during the pregnancy cycle. Acta Anat (Basel) 1961;44:109-130.
14. Lee CS, Wooding FBP, Morgan G: Quantitative analysis of intraepithelial large granular lymphocyte distribution and maternofetal cellular interactions in the synepitheliochorial placenta of the deer. J Anat 1995; 187:445-460.
15. Wooding FBP, Flint APF: Placentation; in Lamming CE (ed): Marshall's Physiology of Reproduction. Chapman & Hall, London, 1994, vol 3, pp 230-460.
16. Mackay CR, Maddox JF, Brandon MR: Three distinct subpopulations of sheep T lymphocytes. Eur J Immunol 1986;16:19-25.
17. Hein WR, Mackay CR: Prominence of γδ T cells in the ruminant immune system. Immunol Today 1991;12:30-34.
18. Guy-Grand D, Cerf-Bensussan N, Malissen B, Malassis-Seris ML, Briottet C, Vassalli P: Two gut intraepithelial CD8+ lymphocyte populations with different T cell receptors: A role for the gut epithelium in T cell differentiation. J Exp Med 1991;173:471-481.
19. +γ/δ T cells isolated from Babesia bovis-stimulated T cell lines. Cell Immunol 1994;153: 9-27.
20. Segerson EC, Gunsett FC: In vitro and in vivo effects of lymphokine-activated killer cells upon preattachment ovine conceptuses. J Immunol 1994;152:2938-2951.
21. Tuo W, Ott TL, Bazer FW: Natural killer cell activity of lymphocytes exposed to ovine, type I, trophoblast interferon. Am J Reprod Immunol 1993;29:26-34.
22. Roberts RM, Cross JC, Leaman DW: Interferons as hormones of pregnancy. Endocr Rev 1992;13: 432-452.
23. Jensen J, Schultz RD: Bovine natural cell mediated cytotoxicity (NCMC): Activation by cytokines. Vet Immunol Immunopathol 1990; 24:113-124.
24. Campos M, Bielefeldt Ohmann H, Rapin N, Babiuk LA: Demonstration of the in vitro antiviral properties of bovine lymphokine-activated killer (LAK) cells. Viral Immunol 1991;4:259-268.
25. Campos M, Rossi CR, Bielefeldt Ohmann H, Beskorwayne T, Rapin N, Babiuk LA: Characterization and activation requirements of bovine lymphocytes acquiring cytotoxic activity after interleukin-2 treatment. Vet Immunol Immunopathol 1992; 32:205-223.
26. Yamamoto S, Onuma M, Kodama H, Koyama H, Mikami T, Izawa H: Existence of cytotoxic activity against BLV-transformed cells in lymphocytes from normal cattle and sheep. Vet Immunol Immunopathol 1985;8:63-78.
27. Campos M, Rossi CR, Lawman MJP: Natural cell-mediated cytotoxicity of bovine mononuclear cells against virus-infected cells. Infect Immun 1982;36:1054-1059.
28. Chung S, Rossi CR: Natural cell-mediated cytotoxicity to cells infected with infectious bovine rhinotracheitis virus. Vet Immunol Immunopathol 1987;14:45-56.
29. Cook CG, Splitter GA: Characterization of bovine mononuclear cell populations with natural cytolytic activity against bovine herpesvirus 1-infected cells. Cell Immunol 1989; 120:240-249.
30. Cook CG, Splitter GA: Comparison of bovine mononuclear cells with other species for cytolytic activity against virally-infected cells. Vet Immunol Immunopathol 1989;20: 239-261.
31. Goddeeris BM, Dunlap S, Bensaid A, MacHugh ND, Morrison WI: Cell surface phenotype of two cloned populations of bovine lymphocytes displaying non-specific cytotoxic activity. Vet Immunol Immunopathol 1991;27:195-199.
32. Betteridge KJ: The structure and function of the equine capsule in relation to embryo manipulation and transfer. Equine Vet J 1989;8 (suppl):92-100.
33. van Niekerk CD, Allen WR: Early embryonic development in the horse. J Reprod Fertil 1975;23 (suppl):495-498.
34. Steven D: Placentation in the mare. J Reprod Fertil 1982;31(suppl):41-55.
35. Enders AC, Liu IK: Lodgement of the equine blastocyst in the uterus from fixation through endometrial cup formation. J Reprod Fertil 1991;44(suppl):427-438.
36. Allen WR: Maternal recognition of pregnancy and immunological implications of trophoblast-endometrial interactions in equids; in Maternal Recognition of Pregnancy. Amsterdam, Ciba Foundation Symposium, Excerpta Medica, 1979, ser 64, pp 323-352.
37. Enders AC, Liu IKM: Trophoblast-uterine interactions during equine chorionic girdle cell maturation, migration, and transformation. Am J Anat 1991;192:366-381.
38. Allen WR, Moor RM: The origin of equine endometrial cups. I. The production of PMSG by fetal trophoblast. J Reprod Fertil 1972;29:313-316.
39. Allen WR, Hamilton DW, Moor RM: The origin of equine endometrial cups. II. Invasion of the endometrium by trophoblast. Anat Rec 1973;177:485-501.
40. Amoroso EC: The endocrinology of pregnancy. Br Med Bull 1955;17: 117-125.
41. Antczak DF, Miller J, Remick L: Lymphocyte alloantigens of the horse. II. Antibodies to ELA antigens produced during equine pregnancy. J Reprod Immunol 1984;6: 283-287.
42. Sargent IL, Arenas J, Redman CWG: Maternal cell-mediated sensitization to paternal HLA may occur, but it is not a regular event in normal human pregnancy. J Reprod Immunol 1987;10:111-120.
43. Donaldson WL, Crump A, Zhang CH, Kornbluth J, Kamoun M, Davis W, Antczak DF: At least two loci encode polymorphic class I MHC antigens in the horse. Anim Genet 1988;19:379-390.
44. Allen WR, Kydd JH, Miller JM, Antczak DF: Immunological studies on fetomaternal relationships in equine pregnancy; in Crighton DB (ed): Immunological Aspects of Reproduction in Mammals. Butterworths, London, 1984, pp 183-193.
45. Kydd J, Miller JM, Antczak DF, Allen WR: Maternal anti-fetal cytotoxic antibody responses of equids during pregnancy. J Reprod Fertil 1982;32(suppl):361-369.
46. Crump A, Donaldson WL, Miller J, Kydd J, Allen WR, Antczak DR: Expression of major histocompatibility complex (MHC) antigens on equine trophoblast. J Reprod Fertil 1987; 35(suppl):379-388.
47. Donaldson WL, Zhang CH, Oriol JG, Antczak DF: Invasive equine trophoblast expresses conventional class I major histocompatibility complex antigens. Development 1990;110:63-71.
48. Kydd J, Butcher GW, Antczak DF, Allen WR: Expression of major histocompatibility complex (MHC) class I molecules on early trophoblast. J Reprod Fertil 1991;44 (suppl):463-477.
49. Grünig G, Triplett L, Canady LK, Allen WR, Antczak DF: The maternal leucocyte response to the endometrial cups in horses is correlated with the developmental stages of the invasive trophoblast cells. Placenta 1995;16:539-559.
50. Oriol JG, Donaldson WL, Dougherty DA, Antczak DF: Molecules of the early equine trophoblast. J Reprod Fertil 1989;44(suppl):455-462.
51. Antczak DF, Allen WR: Maternal immunological recognition of pregnancy in equids. J Reprod Fertil 1989;37(suppl):69-78.
52. Clark DA, Chaput A, Tutton D: Active suppression of host-versus-graft reaction in pregnancy mice. VII. Spontaneous abortion of allogeneic DBA/2 x CBA/J fetuses in the uterus of CBA/J mice correlates with deficient non-T suppressor cell activity. J Immunol 1986;136:1668-1675.
53. Clark DA, Lea RG, Podor T, Daya S, Banwatt D, Harley CB: Cytokines determining the success or failure of pregnancy; in Seppala M, Hamberger L (eds): Frontiers in Human Reproduction. New York, New York Academy of Sciences, 1991, pp 524-544.
54. Lea RG, Stewart F, Allen WR, Ohno I, Clark DA: Accumulation of chromotrope 2R positive cells in equine endometrium during early pregnancy and expression of transforming growth factor-β2 (TGF-β2). J Reprod Fertil 1995;103:339-347.
55. Lunn DP, McClure JT, Schobert S, Holmes A: Abnormal patterns of equine leucocyte differentiation antigen expression in severe combined immunodeficiency foals suggests the phenotype of normal equine natural killer cells. Immunology 1995;84: 495-499.
56. Mathias S, Meadows S, Allen WR: The cytotoxicity of endometrial cup lymphocytes on equine trophoblast in vitro (abstract 10). J Reprod Fertil 1991; ser No. 8.
57. Hormanski CE, Truax R, Pourciau SS, Folsom RW, Horohov DW: Induction of lymphokine-activated killer cells of equine origin: Specificity for equine target cells. Vet Immunol Immunopathol 1992;32:25-36.
58. Dhindsa DS, Dziuk PJ, Norton W: Time of transuterine migration and distribution of embryos in the pig. Anat Rec 1967;159:325-330.
59. Samuel CA: The development of pig trophoblast in ectopic sites. J Reprod Fertil 1971;27:494-499.
60. Samuel CA, Perry JS: The ultrastructure of pig trophoblast transplanted to an ectopic site in the uterine wall. J Anat 1972;113:139-149.
61. King GJ: Reduction in uterine intraepithelial lymphocytes during early gestation in pigs. J Reprod Immunol 1988;14:41-46.
62. Bischof RJ, Brandon MR, Lee C-S: Cellular immune responses in the pig uterus during pregnancy. J Reprod Immunol 1995;29:161-178.
63. Keys JL, King GJ: Microscopic examination of porcine conceptus-maternal interface between days 10 and 19 of pregnancy. Am J Anat 1990; 188:221-238.
64. Swatman J, King GJ, Engelhardt H: Leukocyte distribution in the pig uterus relative to sites of conceptus attachment during early pregnancy (abstract 475). Biol Reprod 1996;54 (suppl 1).
65. Zuckerman FA, Binns RM, Husmann R, Yang H, Carr MM, Kim YB, Davis WC, Misfeldt M, Lunney JK: Analyses of monoclonal antibodies reactive with porcine CD44 and CD45. Vet Immunol Immunopathol 1994;43:293-305.
66. Engelhardt H, Small MR, King GJ: Exposure of pigs to seminal plasma at estrus recruits leukocytes to the uterine epithelium (abstract 476). Biol Reprod 1996;54(suppl 1).
67. Bischof RJ, Brandon MR, Lee C-S: Studies on the distribution of immune cells in the uteri of prepubertal and cycling gilts. J Reprod Immunol 1994;26:111-129.
68. Croy BA, Wood W, King GJ: Evaluation of intrauterine immune suppression during pregnancy in a species with epitheliochorial placentation. J Immunol 1987;139:1088-1095.
69. Hirt W, Saalmüller A, Reddehase MJ: Distinct γ/δ T cell receptors define two subsets of circulating porcine CD2-CD4-CD8- T lymphocytes. Eur J Immunol 1990;20:265-269.
70. Pinto A, Ferguson F: Characteristics of Yorkshire swine natural killer cells. Vet Immunol Immunopathol 1988;20:15-29.
71. Yang WC, Schultz RD, Spano JS: Isolation and characterization of porcine natural killer (NK) cells. Vet Immunol Immunopathol 1987;14: 345-356.
72. Kim YB, Huh ND, Koren HS, Amos DB: Natural killing (NK) and antibody-dependent cellular cytotoxicity (ADCC) in specific pathogen-free (SPF) miniature swine and germfree piglets. J Immunol 1980; 125:755-762.
73. Dato ME, Kim YB: Characterization and utilization of a monoclonal antibody inhibiting porcine natural killer cell activity for isolation of natural killer and killer cells. J Immunol 1990;144:4452-4462.
74. Martin S, Wardley RC: Natural cytotoxicity detected in swine using Aujeszky's disease virus infected targets. Res Vet Sci 1984;37:211-218.
75. Pescovitz MD, Lowman MA, Sachs DH: Expression of T-cell associated antigens by porcine natural killer cells. Immunology 1988;65:267-271.
76. Croy BA, Waterfield A, Wood W, King GJ: Normal murine and porcine embryos recruit NK cells to the uterus. Cell Immunol 1988;115: 471-480.
77. Yu Z, Croy BA, Chapeau C, King GJ: Elevated endometrial natural killer cell activity during early porcine pregnancy is conceptus-mediated. J Reprod Immunol 1993;24: 153-164.
78. Drake BL, Head JR: Murine trophoblast can be killed by lymphokine-activated killer cells. J Immunol 1989;143:9-14.
79. King A, Birkby A, Loke YW: Early human decidual cells exhibit NK activity against the K562 cell line but not first trimester trophoblast. Cell Immunol 1989;118:337-344.
80. King A, Loke YW: Human trophoblast and JEG choriocarcinoma cells are sensitive to lysis by IL-2-stimulated decidual NK cells. Cell Immunol 1990;127:230-237.
81. Yu Z, Croy BA, King GJ: Lysis of porcine trophoblast cells by endometrial natural killer-like effector cells in vitro does not require interleukin-2. Biol Reprod 1994;51: 1279-1284.
82. Dato ME, Wierda WG, Kim YB: A triggering structure recognized by G7 monoclonal antibody on porcine lymphocytes and granulocytes. Cell Immunol 1992;140:468-477.
83. King A, Burrows T, Loke YW: Human uterine natural killer cells. Nat Immun 1996/97;15:41-52.
84. Wilson AD, Stokes CR, Bourne FJ: Morphology and functional characteristics of isolated porcine intraepithelial lymphocytes. Immunology 1986;59:109-113.
85. Cross JC, Roberts RM: Porcine conceptuses secrete an interferon during the preattachment period of early pregnancy. Biol Reprod 1989;40: 1109-1118.
86. Mirando MA, Harney JP, Beers S, Pontzer CH, Torres BA, Johnson HM, Bazer FW: Onset of secretion of proteins with antiviral activity by pig conceptuses. J Reprod Fertil 1990;88:197-203.
87. La Bonnardière C, Martinat-Botté F, Terqui M, Lefèvre F, Zouari K, Martal J, Bazer FW: Production of two species of interferon by Large White and Meishan pig conceptuses during the peri-attachment period. J Reprod Fertil 1991;91:469-478.
88. Lefèvre F, Martinat-Botté F, Guillomot M, Zouari K, Charley B, La Bonnardière C: Interferon-gamma gene and protein are spontaneously expressed by the trophectoderm early in gestation. Eur J Immunol 1990; 20:2485-2490.
89. Lefèvre F, Boulay V: A novel and atypical type one interferon gene expressed by trophoblast during early pregnancy. J Biol Chem 1993;268: 19760-19768.
90. H2 phenomenon? Immunol Today 1993;14:353-356.
91. Vileck J, Gray TW, Rinderknecht E, Sevastopoulos CG: Interferon gamma: A lymphokine for all seasons; in Pick E (ed): Lymphokines. Orlando, Academic Press/Harcourt Brace Jovanovich, 1985, vol 11, pp 1-32.
92. Reiter ZVI: Interferon - a major regulator of natural killer cell-mediated cytotoxicity. J Interferon Res 1993; 13:247-257.
93. Hartley JP, Bazer FW: Effect of porcine conceptus secretory proteins on interestrous interval and uterine secretion of prostaglandins. Biol Reprod 1989;41:277-284.
94. Bazer FW, Ott TL, Spencer TE: Pregnancy recognition in ruminants, pigs and horses: Signals from the trophoblast. Theriogenology 1994;41:79-94.
95. Fox HS, Nond BL, Parslow TG: Estrogen regulates the IFN-γ promoter. J Immunol 1991;146:4362-4367.