Luteal microenvironment directs resident T lymphocyte function in cows

Biology of Reproduction

Volumn 86, Issue 2, 2012, Pages

  Poole, Daniel H ^a,b   Pate, Joy L ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Bovine; Corpus luteum; Cytokines; Immunology; Ovary; Reproductive immunology; T lymphocytes

Indexed keywords

TRANSCRIPTION FACTOR FOXP3; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ISOLATION; CONTROLLED STUDY; CORPUS LUTEUM; COW; FLOW CYTOMETRY; GAMMA DELTA T LYMPHOCYTE; LUTEOLYSIS; LYMPHOCYTE FUNCTION; NONHUMAN; PHENOTYPE; PREGNANCY; PRIORITY JOURNAL; RESIDENY T LYMPHOCYTE; T LYMPHOCYTE; ANIMAL; ANIMAL MODEL; CATTLE; CELL COMMUNICATION; CELL DIFFERENTIATION; CYTOLOGY; FEMALE; PHYSIOLOGY; REGULATORY T LYMPHOCYTE; TUMOR MICROENVIRONMENT;

ANIMALIA; BOVINAE;

ANIMALS; CATTLE; CD8-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; CELL DIFFERENTIATION; CELLULAR MICROENVIRONMENT; CORPUS LUTEUM; FEMALE; FLOW CYTOMETRY; MODELS, ANIMAL; PHENOTYPE; PREGNANCY; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY;

EID: 84860238692     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.092296     Document Type: Article

References (79)

1. O'Shea J, Rodgers R, D'Occhio M. Cellular composition of the cyclic corpus luteum of the cow. J Reprod Fertil 1989; 85:483-487.
2. Hafs H, Armstrong D. Corpus luteum growth and progesterone synthesis during the bovine estrous cycle. J Anim Sci 1968; 27:134-141.
3. Zheng J, Fricke P, Reynolds L, Redmer D. Evaluation of growth, cell proliferation, and cell death in bovine corpora lutea throughout the estrous cycle. Biol Reprod 1994; 51:623-632.
4. Lobel B, Levy E. Enzymic correlates of development, secretory function and regression of follicles and corpora lutea in the bovine ovary. Acta Endocrinol Suppl 1968; 132:5-63.
5. Wang L, Pascoe V, Petrucco O, Norman R. Distribution of leukocyte subpopulations in the human corpus luteum. Hum Reprod 1992; 7:197-202.
6. Petrovská M, Sedlák R, Nouza K, Presl J, Kinský R. Development and distribution of the white blood cells within various structures of the human menstrual corpus luteum examined using an image analysis system. Am J Reprod Immunol 1992; 28:77-80.
7. Bukovský A, Caudle MR, Keenan JA, Wimalasena J, Upadhyaya NB, Van Meter SE. Is corpus luteum regression an immune-mediated event? Localization of immune system components and luteinizing hormone receptor in human corpora lutea. Biol Reprod 1995; 53:1373-1384.
8. Best CL, Pudney J, Welch WR, Burger N, Hill JA. Localization and characterization of white blood cell populations within the human ovary throughout the menstrual cycle and menopause. Hum Reprod 1996; 11:790-797.
9. Suzuki T, Sasano H, Takaya R, Fukaya T, Yajima A, Date F, Nagura H. Leukocytes in normal-cycling human ovaries: immunohistochemical distribution and characterization. Hum Reprod 1998; 13:2186-2191.
10. Bauer M, Reibiger I, Spanel-Borowski K. Leukocyte proliferation in the bovine corpus luteum. Reproduction 2001; 121:297-305.
11. Pate JL, Toyokawa K, Walusimbi S, Brzezicka E. The interface of the immune and reproductive systems in the ovary: lessons learned from the corpus luteum of domestic animal models. Am J Reprod Immunol 2010; 64:275-286.
12. Kedzierska K, La Gruta NL, Stambas J, Turner SJ, Doherty PC. Tracking phenotypically and functionally distinct T cell subsets via T cell repertoire diversity. Mol Immunol 2008; 45:607-618.
13. Krusche CA, Vloet TD, Herrler A, Black S, Beier HM. Functional and structural regression of the rabbit corpus luteum is associated with altered luteal immune cell phenotypes and cytokine expression patterns. Histochem Cell Biol 2002; 118:479-489.
14. Komatsu K, Manabe N, Kiso M, Shimabe M, Miyamoto H. Changes in localization of immune cells and cytokines in corpora lutea during luteolysis in murine ovaries. J Exp Zool 2003; 296:152-159.
15. Sander V, Piehl L, Facorro G, Rubín de Celis E, Motta A. Regulation of functional and regressing stages of corpus luteum development in mice. Role of reactive oxygen species. Reprod Fertil Dev 2008; 20:760-769.
16. Lawler D, Hopkins J, Watson E. Immune cell populations in the equine corpus luteum throughout the oestrous cycle and early pregnancy: an immunohistochemical and flow cytometric study. J Reprod Fertil 1999; 117:281-290.
17. Bierer BE, Sleckman BP, Ratnofsky SE, Burakoff SJ. The biologic roles of CD2, CD4, and CD8 in T-cell activation. Annu Rev Immunol 1989; 7:579-599.
18. Davis T, Pate J. Bovine luteal cells stimulate proliferation of major histocompatibility nonrestricted gamma delta T cells. Biol Reprod 2007; 77:914-922.
19. Ferrick DA, Schrenzel MD, Mulvania T, Hsieh B, Ferlin WG, Lepper H. Differential production of interferon-gamma and interleukin-4 in response to Th1- and Th2-stimulating pathogens by gamma delta T cells in vivo. Nature 1995; 373:255-257.
20. Hsieh B, Schrenzel MD, Mulvania T, Lepper HD, DiMolfetto-Landon L, Ferrick DA. In vivo cytokine production in murine listeriosis. J Immunol 1996; 156:232-237.
21. Troye-Blomberg M, Worku S, Tangteerawatana P, Jamshaid R, Soderstrom K, Elghazali G. Human γδ T cells that inhibit the in vitro growth of the asexual blood stages of the Plasmodium falciparum parasite express cytolytic and proinflammatory molecules. Scan J Immunol 1999; 50:642-650.
22. Wen L, Barber DF, Pao W, Wong FS, Owen MJ, Hayday A. Primary γδ cell clones can be defined phenotypically and functionally as Th1/Th2 cells and illustrate the association of CD4 with Th2 differentiation. J Immunol 1998; 160:1965-1974.
23. Wyatt CR, Madruga C, Cluff C, Parish S, Hamilton MJ, Goff W, Davis WC. Differential distribution of gamma delta T-cell receptor lymphocyte subpopulations in blood and spleen of young and adult cattle. Vet Immunol Immunopathol 1994; 40:187-199.
24. Davis WC, Zuckermann FA, Hamilton MJ, Barbosa JI, Saalmüller A, Binns RM, Licence ST. Analysis of monoclonal antibodies that recognize gamma delta T/null cells. Vet Immunol Immunopathol 1998; 60:305-316.
25. Machugh ND, Mburu JK, Carol MJ, Wyatt CR, Orden JA, Davis WC. Identification of two distinct subsets of bovine gamma delta T cells with unique cell surface phenotype and tissue distribution. Immunology 1997; 92:340-345.
26. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299:1057-1061.
27. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003; 4:330-336.
28. Hoek A, Rutten VP, Kool J, Arkesteijn GJ, Bouwstra RJ, Van Rhijn I, Koets AP. Subpopulations of bovine WC1[+] gammadelta T cells rather than CD4[+]CD25[high] Foxp3[+] T cells act as immune regulatory cells ex vivo. Vet Res 2009; 40:6-20.
29. Seo K, Lee SU, Park YH, Davis WC, Fox LK, Bohach GA. Long-term staphylococcal enterotoxin C1 exposure induces soluble factor-mediated immunosuppression by bovine CD4+ and CD8+ T cells. Infect Immun 2007; 75:260-269.
30. Roncador G, Brown PJ, Maestre L, Hue S, Martínez-Torrecuadrada JL, Ling KL, Pratap S, Toms C, Fox BC, Cerundolo V, Powrie F, Banham AH. Analysis of FOXP3 protein expression in human CD4+CD25+ regulatory T cells at the single-cell level. Eur J Immunol 2005; 35:1681-1691.
31. Askenasy N, Kaminitz A, Yarkoni S. Mechanisms of T regulatory cell function. Autoimmun Rev 2008; 7:370-375.
32. Adashi E, Resnick C, Packman J, Hurwitz A, Payne D. Cytokine-mediated regulation of ovarian function: tumor necrosis factor alpha inhibits gonadotropin-supported progesterone accumulation by differentiating and luteinized murine granulosa cells. Am J Obstet Gynecol 1990; 162:889-896.
33. Townson D, Pate J. Regulation of prostaglandin synthesis by interleukin-1 beta in cultured bovine luteal cells. Biol Reprod 1994; 51:480-485.
34. Townson D, Pate J. Mechanism of action of TNF-alpha-stimulated prostaglandin production in cultured bovine luteal cells. Prostaglandins 1996; 52:361-373.
35. Pate J, Landis Keyes P. Immune cells in the corpus luteum: friends or foes? Reproduction 2001; 122:665-676.
36. Castro A, Castro O, Troncoso JL, Kohen P, Simón C, Vega M, Devoto L. Luteal leukocytes are modulators of the steroidogenic process of human mid-luteal cells. Hum Reprod 1998; 13:1584-1589.
37. Nothnick W, Pate J. Interleukin-1 beta is a potent stimulator of prostaglandin synthesis in bovine luteal cells. Biol Reprod 1990; 43:898-903.
38. Fairchild D, Pate J. Modulation of bovine luteal cell synthetic capacity by interferon-gamma. Biol Reprod 1991; 44:357-363.
39. Fukuoka M, Yasuda K, Fujiwara H, Kanzaki H, Mori T. Interactions between interferon gamma, tumour necrosis factor alpha, and interleukin-1 in modulating progesterone and oestradiol production by human luteinized granulosa cells in culture. Hum Reprod 1992; 7:1361-1364.
40. Fairchild DL, Pate J. Interferon-gamma induction of major histocompatibility complex antigens on cultured bovine luteal cells. Biol Reprod 1989; 40:453-457.
41. Petroff M, Coggeshall K, Jones L, Pate J. Bovine luteal cells elicit major histocompatibility complex class II-dependent T-cell proliferation. Biol Reprod 1997; 57:887-893.
42. Cannon M, Petroff M, Pate J. Effects of prostaglandin F2alpha and progesterone on the ability of bovine luteal cells to stimulate T lymphocyte proliferation. Biol Reprod 2003; 69:695-700.
43. Cannon MJ, Davis JS, Pate JL. The class II major histocompatibility complex molecule BoLA-DR is expressed by endothelial cells of the bovine corpus luteum. Reproduction 2007; 133:991-1003.
44. Lucy M, Billings HJ, Butler WR, Ehnis LR, Fields MJ, Kesler DJ, Kinder JE, Mattos RC, Short RE, Thatcher WW, Wettemann RP, Yelich JV, et al. Efficacy of an intravaginal progesterone insert and an injection of PGF2alpha for synchronizing estrus and shortening the interval to pregnancy in postpartum beef cows, peripubertal beef heifers, and dairy heifers. J Anim Sci 2001; 79:982-995.
45. Ndiaye K, Poole D, Expression Pate J. and regulation of functional oxytocin receptors in bovine T lymphocytes. Biol Reprod 2008; 78:786-793.
46. Pate J. Isolation and culture of fully differentiated bovine luteal cells. Methods Toxicol 1993; 3B:360-370.
47. Sakaguchi S, Sakaguchi N, Shimizu J, Yamazaki S, Sakihama T, Itoh M, Kuniyasu Y, Nomura T, Toda M, Takahashi T. Immunologic 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.
48. Bergmann C, Strauss L, Zeidler R, Lang S, Whiteside T. Expansion and characteristics of human T regulatory type 1 cells in co-cultures simulating tumor microenvironment. Cancer Immunol Immunother 2007; 56:1429-1442.
49. Havran W, Jameson J, Witherden D. Epithelial cells and their neighbors. III. Interactions between intraepithelial lymphocytes and neighboring epithelial cells. Am J Physiol Gastrointest Liver Physiol 2005; 289:G627-630.
50. Hedges J, Graff J, Jutila M. Transcriptional profiling of gamma delta T cells. J Immunol 2003; 171:4959-4964.
51. Wilczynski JR, Radwan M, Kalinka J. The characterization and role of regulatory T cells in immune reactions. Front Biosci 2008; 13:2266-2274.
52. Fantini MC, Becker C, Monteleone G, Pallone F, Galle PR, Neurath MF. Cutting edge: TGF-beta induces a regulatory phenotype in CD4+CD25- T cells through Foxp3 induction and down-regulation of Smad7. J Immunol 2004; 172:5149-5153.
53. Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, McGrady G, Wahl SM. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 2003; 198:1875-1886.
54. Horwitz DA, Zheng SG, Gray JD. The role of the combination of IL-2 and TGF-beta or IL-10 in the generation and function of CD4+ CD25+ and CD8+ regulatory T cell subsets. J Leukoc Biol 2003; 74:471-478.
55. Wan YY, Flavell RA. The roles for cytokines in the generation and maintenance of regulatory T cells. Immunol Rev 2006; 212:114-130.
56. Dietl J, Engel J, Wischhusen J. The role of regulatory T cells in ovarian cancer. Int J Gynecol Cancer 2007; 17:764-770.
57. Bacchetta R, Gambineri E, Roncarolo M. Role of regulatory T cells and FOXP3 in human diseases. J Allergy Clin Immunol 2007; 120:227-235.
58. Arosh J, Banu SK, Chapdelaine P, Madore E, Sirois J, Fortier MA. Prostaglandin biosynthesis, transport, and signaling in corpus luteum: a basis for autoregulation of luteal function. Endocrinol 2004; 145:2551-2560.
59. Gangrade B, Gotcher E, Davis J, May J. The secretion of transforming growth factor-beta by bovine luteal cells in vitro. Mol Cell Endocrinol 1993; 93:117-123.
60. Pate J. Cellular components involved in luteolysis. J Anim Sci 1994; 72:1884-1890.
61. Niswender G, Juengel J, Silva P, Rollyson M, McIntush E. Mechanisms controlling the function and life span of the corpus luteum. Physiol Rev 2000; 80:1-29.
62. Penny L, Armstrong DG, Baxter G, Hogg C, Kindahl H, Bramley T, Watson ED, Webb R. Expression of monocyte chemoattractant protein-1 in the bovine corpus luteum around the time of natural luteolysis. Biol Reprod 1998; 59:1464-1469.
63. Bauer M, Reibiger I, Spanel-Borowski K. Leucocyte proliferation in the bovine corpus luteum. Reproduction 2001; 121:297-305.
64. Townson D, O'Connor C, Pru J. Expression of monocyte chemoattractant protein-1 and distribution of immune cell populations in the bovine corpus luteum throughout the estrous cycle. Biol Reprod 2002; 66:361-366.
65. Giblin PA, Leahy DJ, Mennone J, Kavathas PB. The role of charge and multiple faces of the CD8 alpha/alpha homodimer in binding to major histocompatibility complex class I molecules: support for a bivalent model. Proc Natl Acad Sci U S A 1994; 91:1716-1720.
66. Hayday A, Theodoridis E, Ramsburg E, Shires J. Intraepithelial lymphocytes: exploring the third way in immunology. Nat Immunol 2001; 2:997-1003.
67. Sheridan BS, Lefrançois L. Intraepithelial lymphocytes: to serve and protect. Curr Gastroenterol Rep 2010; 12:513-521.
68. Cox MA, Harrington LE, Zajac AJ. Cytokines and the inception of CD8 T cell responses. Trends Immunol 2011; 32:180-186.
69. Madakamutil LT, Christen U, Lena CJ, Wang-Zhu Y, Attinger A, Sundarrajan M, Ellmeier W, von Herrath MG, Jensen P, Littman DR, Cheroutre H. CD8alphaalpha-mediated survival and differentiation of CD8 memory T cell precursors. Science 2004; 304:590-593.
70. Fujiura Y, Kawaguchi M, Kondo Y, Obana S, Yamamoto H, Nanno M, Ishikawa H. Development of CD8 alpha alpha+ intestinal intraepithelial T cells in beta 2-microglobulin- and/or TAP1-deficient mice. J Immunol 1996; 156:2710-2715.
71. Zhou C, Wu J, Borillo J, Torres L, McMahon J, Lou YH. Potential roles of a special CD8 alpha alpha+ cell population and CC chemokine thymusexpressed chemokine in ovulation related inflammation. J Immunol 2009; 182:596-603.
72. Espey LL. Ovulation as an inflammatory reaction-a hypothesis. Biol Reprod 1980; 22:73-106.
73. Parker CM, Groh V, Band H, Porcelli SA, Morita C, Fabbi M, Glass D, Strominger JL, Brenner MB. Evidence for extrathymic changes in the T cell receptor gamma/delta repertoire. J Exp Med 1990; 171:1597-1612.
74. Bandeira A, Itohara S, Bonneville M, Burlen-Defranoux O, Mota-Santos T, Coutinho A, Tonegawa S. Extrathymic origin of intestinal intraepithelial lymphocytes bearing T-cell antigen receptor gamma delta. Proc Natl Acad Sci U S A 1991; 88:43-47.
75. Kapp J, Kapp L, McKenna K. Gammadelta T cells play an essential role in several forms of tolerance. Immunol Res 2004; 29:93-102.
76. Patarca R, Freeman GJ, Singh RP, Wei FY, Durfee T, Blattner F, Regnier DC, Kozak CA, Mock BA, Morse HC III, et al. Structural and functional studies of the early T lymphocyte activation 1 (Eta-1) gene. Definition of a novel T cell-dependent response associated with genetic resistance to bacterial infection. J Exp Med 1989; 170:145-161.
77. Ashkar S, Weber GF, Panoutsakopoulou V, Sanchirico ME, Jansson M, Zawaideh S, Rittling SR, Denhardt DT, Glimcher MJ, Cantor H. Eta-1 (osteopontin): an early component of type-1 (cell-mediated) immunity. Science 2000; 287:860-864.
78. Meeusen E, Fox A, Brandon M, Lee C. Activation of uterine intraepithelial gamma delta T cell receptor-positive lymphocytes during pregnancy. Eur J Immunol 1993; 23:1112-1117.
79. Tuo W, Bazer F, Davis W, Zhu D, Brown W. Differential effects of type I IFNs on the growth of WC1- CD8+ gamma delta T cells and WC1+ CD8- gamma delta T cells in vitro. J Immunol 1999; 62:245-253.