Skip to main content
SpringerLink
Log in

Immune Cells and Their Effects on the Bovine Corpus Luteum

  • Chapter
  • First Online:
Book cover The Life Cycle of the Corpus Luteum

Abstract

In the past two decades, accumulating evidence has indicated that various types of immune cells (T cells, macrophages, neutrophils, eosinophils, and dendritic cells) exist within the CL and regulate luteal function. These immune cells accumulate during luteal development and support angiogenesis and progesterone production. PGF2α stimulates the production of inflammatory cytokines and chemokines in the mature CL; these factors recruit immune cells into the CL to enhance luteolytic cascades through inflammatory responses. When pregnancy is established, the embryo secretes interferon-tau (IFNT) as a pregnancy recognition signal; this indirectly maintains the CL by inhibiting luteolysis. In addition to its uterine function, IFNT regulates immune cell function and is associated with the transformation of the cyclic CL into the pregnancy CL. This review describes the current state of research on the effect of immune cells on the bovine CL, which is essential for a better understanding of reproductive physiology.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Lobel BL, Levy E. Enzymic correlates of development, secretory function and regression of follicles and corpora lutea in the bovine ovary. Acta Endocrinol (Copenh). 1968;(Suppl 132):5–63.

    Google Scholar 

  2. Alila HW, Hansel W. Induction of lymphopenia causes luteal dysfunction in cattle. Biol Reprod. 1984;31(4):671–8.

    Article  CAS  PubMed  Google Scholar 

  3. Bukovsky A, Presl J, Krabec Z, Bednarik T. Ovarian function in adult rats treated with antithymocyte serum. Experientia (Basel). 1977;33(2):280–1.

    Article  CAS  Google Scholar 

  4. 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(4):275–86.

    Article  CAS  PubMed  Google Scholar 

  5. Walusimbi SS, Pate JL. Physiology and Endocrinology Symposium: role of immune cells in the corpus luteum. J Anim Sci. 2013;91:1650–9.

    Article  CAS  PubMed  Google Scholar 

  6. Bukulmez O, Arici A. Leukocytes in ovarian function. Hum Reprod Update. 2000;6:1–15.

    Article  CAS  PubMed  Google Scholar 

  7. Kizuka F, Tokuda N, Takagi K, Adachi Y, Lee L, Tamura I, Maekawa R, Taketani T, Tamura H, Suzuki T, Owada Y, Sugino N. Involvement of bone marrow-derived vascular progenitor cells in neovascularization during formation of the corpus luteum in mice. Biol Reprod. 2012;87:1–7.

    Article  CAS  Google Scholar 

  8. Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, Figueiredo JL, Kohler RH, Chudnovskiy A, Waterman P, Aikawa E, Mempel TR, Libby P, Weissleder R, Pittet MJ. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science. 2009;325:612–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Oakley OR, Kim H, El-Amouri I, Lin PC, Cho J, Bani-Ahmad M, Ko C. Periovulatory leukocyte infiltration in the rat ovary. Endocrinology. 2010;151(9):4551–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Endo T, Kanayama K. Effects of splenectomy on luteal function in pseudopregnant rabbits. J Int Med Res. 1998;26:93–7.

    CAS  PubMed  Google Scholar 

  11. Penny LA, Armstrong D, Bramley TA, Webb R, Collins RA, Watson ED. Immune cells and cytokine production in the bovine corpus luteum throughout the oestrous cycle and after induced luteolysis. J Reprod Fertil. 1999;115:87–96.

    Article  CAS  PubMed  Google Scholar 

  12. Poole DH, Pate JL. Luteal microenvironment directs resident T lymphocyte function in cows. Biol Reprod. 2012;86(2):29.

    Article  PubMed  CAS  Google Scholar 

  13. Hashii K, Fujiwara H, Yoshioka S, Kataoka N, Yamada S, Hirano T, Mori T, Fujii S, Maeda M. Peripheral blood mononuclear cells stimulate progesterone production by luteal cells derived from pregnant and non-pregnant women: possible involvement of interleukin-4 and interleukin-10 in corpus luteum function and differentiation. Hum Reprod. 1998;13:2738–44.

    Article  CAS  PubMed  Google Scholar 

  14. Walusimbi SS, Pate JL. Luteal cells from functional and regressing bovine corpora lutea differentially alter the function of gamma delta T cells. Biol Reprod. 2014;90:1–7.

    Article  CAS  Google Scholar 

  15. Szekeres-Bartho J, Wegmann TG. A progesterone-dependent immunomodulatory protein alters the Th1/Th2 balance. J Reprod Immunol. 1996;31:81–95.

    Article  CAS  PubMed  Google Scholar 

  16. Petroff M, Coggeshall KM, Jones LS, Pate JL. Bovine luteal cells elicit major histocompatibility complex class II-dependent T-cell proliferation. Biol Reprod. 1997;57:887–93.

    Article  CAS  PubMed  Google Scholar 

  17. Cannon MJ, Pate JL. The role of major histocompatibility complex molecules in luteal function. Reprod Biol Endocrinol. 2003;1:93.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Ndiaye K, Poole DH, Walusimbi S, Cannon MJ, Toyokawa K, Maalouf SW, Dong J, Thomas P, Pate JL. Progesterone effects on lymphocytes may be mediated by membrane progesterone receptors. J Reprod Immunol. 2012;95:15–26.

    Article  CAS  PubMed  Google Scholar 

  19. 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;11:790–7.

    Article  CAS  PubMed  Google Scholar 

  20. Gaytan F, Morales C, Garcia-Pardo L, Reymundo C, Bellido C, Sanchez-Criado JE. Macrophages, cell proliferation, and cell death in the human menstrual corpus luteum. Biol Reprod. 1998;59:417–25.

    Article  CAS  PubMed  Google Scholar 

  21. Standaert FE, Zamora CS, Chew BP. Quantitative and qualitative changes in blood leukocytes in the porcine ovary. Am J Reprod Immunol. 1991;25:163–8.

    Article  CAS  PubMed  Google Scholar 

  22. Turner EC, Hughes J, Wilson H, Clay M, Mylonas KJ, Kipari T, Duncan WC, Fraser HM. Conditional ablation of macrophages disrupts ovarian vasculature. Reproduction. 2011;141:821–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Care AS, Diener KR, Jasper MJ, Brown HM, Ingman WV, Robertson SA. Macrophages regulate corpus luteum development during embryo implantation in mice. J Clin Invest. 2013;123:3472–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Emi N, Kanzaki H, Yoshida M, Takakura K, Kariya M, Okamoto N, Imai K, Mori T. Lymphocytes stimulate progesterone production by cultured human granulosa luteal cells. Am J Obstet Gynecol. 1991;165:1469–74.

    Article  CAS  PubMed  Google Scholar 

  25. Halme J, Hammond MG, Syrop CH, Talbert LM. Peritoneal macrophages modulate human granulosa-luteal cell progesterone production. J Clin Endocrinol Metab. 1985;61:912–6.

    Article  CAS  PubMed  Google Scholar 

  26. Adashi EY. The potential relevance of cytokines to ovarian physiology: the emerging role of resident ovarian cells of the white blood cell series. Endocr Rev. 1990;11:454–64.

    Article  CAS  PubMed  Google Scholar 

  27. Polec A, Tanbo T, Fedorcsak P. Cellular interaction regulates interleukin-8 secretion by granulosa-lutein cells and monocytes/macrophages. Am J Reprod Immunol. 2009;61:85–94.

    Article  CAS  PubMed  Google Scholar 

  28. Polec A, Raki M, Abyholm T, Tanbo TG, Fedorcsak P. Interaction between granulosa-lutein cells and monocytes regulates secretion of angiogenic factors in vitro. Hum Reprod. 2011;26:2819–29.

    Article  CAS  PubMed  Google Scholar 

  29. Murdoch WJ. Treatment of sheep with prostaglandin F2 alpha enhances production of a luteal chemoattractant for eosinophils. Am J Reprod Immunol Microbiol. 1987;15:52–6.

    Article  CAS  PubMed  Google Scholar 

  30. Aust G, Simchen C, Heider U, Hmeidan FA, Blumenauer V, Spanel-Borowski K. Eosinophils in the human corpus luteum: the role of RANTES and eotaxin in eosinophil attraction into periovulatory structures. Mol Hum Reprod. 2000;6:1085–91.

    Article  CAS  PubMed  Google Scholar 

  31. Jiemtaweeboon S, Shirasuna K, Nitta A, Kobayashi A, Schuberth HJ, Shimizu T, Miyamoto A. Evidence that polymorphonuclear neutrophils infiltrate into the developing corpus luteum and promote angiogenesis with interleukin-8 in the cow. Reprod Biol Endocrinol. 2011;9:79.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Brannstrom M, Pascoe V, Norman RJ, McClure N. Localization of leukocyte subsets in the follicle wall and in the corpus luteum throughout the human menstrual cycle. Fertil Steril. 1994;61:488–95.

    Article  CAS  PubMed  Google Scholar 

  33. Brannstrom M, Giesecke L, Moore IC, van den Heuvel CJ, Robertson SA. Leukocyte subpopulations in the rat corpus luteum during pregnancy and pseudopregnancy. Biol Reprod. 1994;50:1161–7.

    Article  CAS  PubMed  Google Scholar 

  34. Shimizu T, Kaji A, Murayama C, Magata F, Shirasuna K, Wakamiya K, Okuda K, Miyamoto A. Effects of interleukin-8 on estradiol and progesterone production by bovine granulosa cells from large follicles and progesterone production by luteinizing granulosa cells in culture. Cytokine. 2012;57:175–81.

    Article  CAS  PubMed  Google Scholar 

  35. Talbott H, Delaney A, Zhang P, Yu Y, Cushman RA, Cupp AS, Hou X, Davis JS. Effects of IL8 and immune cells on the regulation of luteal progesterone secretion. Reproduction. 2014;148:21–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Nozawa H, Chiu C, Hanahan D. Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci USA. 2006;103:12493–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Koch AE, Polverini PJ, Kunkel SL, Harlow LA, DiPietro LA, Elner VM, Elner SG, Strieter RM. Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science. 1992;258:1798–801.

    Article  CAS  PubMed  Google Scholar 

  38. Goto J, Suganuma N, Takata K, Kitamura K, Asahina T, Kobayashi H, Muranaka Y, Furuhashi M, Kanayama N. Morphological analyses of interleukin-8 effects on rat ovarian follicles at ovulation and luteinization in vivo. Cytokine. 2002;20:168–73.

    Article  CAS  PubMed  Google Scholar 

  39. Yasuda M, Shimizu S, Tokuyama S, Watanabe T, Kiuchi Y, Yamamoto T. A novel effect of polymorphonuclear leukocytes in the facilitation of angiogenesis. Life Sci. 2000;66:2113–21.

    Article  CAS  PubMed  Google Scholar 

  40. Schruefer R, Lutze N, Schymeinsky J, Walzog B. Human neutrophils promote angiogenesis by a paracrine feedforward mechanism involving endothelial interleukin-8. Am J Physiol Heart Circ Physiol. 2005;288(3):H1186–92.

    Article  CAS  PubMed  Google Scholar 

  41. Mueller MD, Lebovic DI, Garrett E, Taylor RN. Neutrophils infiltrating the endometrium express vascular endothelial growth factor: potential role in endometrial angiogenesis. Fertil Steril. 2000;74:107–12.

    Article  CAS  PubMed  Google Scholar 

  42. Heryanto B, Girling JE, Rogers PA. Intravascular neutrophils partially mediate the endometrial endothelial cell proliferative response to oestrogen in ovariectomised mice. Reproduction. 2004;127:613–20.

    Article  CAS  PubMed  Google Scholar 

  43. Ancelin M, Chollet-Martin S, Herve MA, Legrand C, El Benna J, Perrot-Applanat M. Vascular endothelial growth factor VEGF189 induces human neutrophil chemotaxis in extravascular tissue via an autocrine amplification mechanism. Lab Invest. 2004;84:502–12.

    Article  CAS  PubMed  Google Scholar 

  44. Zittermann SI, Issekutz AC. Endothelial growth factors VEGF and bFGF differentially enhance monocyte and neutrophil recruitment to inflammation. J Leukoc Biol. 2006;80:247–57.

    Article  CAS  PubMed  Google Scholar 

  45. Freitag N, Tirado-Gonzalez I, Barrientos G, Herse F, Thijssen VL, Weedon-Fekjaer SM, Schulz H, Wallukat G, Klapp BF, Nevers T, Sharma S, Staff AC, Dechend R, Blois SM. Interfering with Gal-1-mediated angiogenesis contributes to the pathogenesis of preeclampsia. Proc Natl Acad Sci USA. 2013;110:11451–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Spanel-Borowski K. Ovulation as danger signaling event of innate immunity. Mol Cell Endocrinol. 2011;333:1–7.

    Article  CAS  PubMed  Google Scholar 

  47. Cohen-Fredarow A, Tadmor A, Raz T, Meterani N, Addadi Y, Nevo N, Solomonov I, Sagi I, Mor G, Neeman M, Dekel N. Ovarian dendritic cells act as a double-edged pro-ovulatory and anti-inflammatory sword. Mol Endocrinol. 2014;28:1039–54.

    Article  PubMed  CAS  Google Scholar 

  48. Furukawa K, Fujiwara H, Sato Y, Zeng BX, Fujii H, Yoshioka S, Nishi E, Nishio T. Platelets are novel regulators of neovascularization and luteinization during human corpus luteum formation. Endocrinology. 2007;148:3056–64.

    Article  CAS  PubMed  Google Scholar 

  49. Reibiger I, Spanel-Borowski K. Difference in localization of eosinophils and mast cells in the bovine ovary. J Reprod Fertil. 2000;118:243–9.

    Article  CAS  PubMed  Google Scholar 

  50. Murdoch WJ, Van Kirk EA. Aetiology of attenuated luteal development in prednisolone-induced eosinopenic ewes. Reprod Fertil Dev. 2000;12:127–32.

    Article  CAS  PubMed  Google Scholar 

  51. Kliem H, Rodler D, Ulbrich SE, Sinowatz F, Berisha B, Meyer HH, Schams D. Dexamethasone-induced eosinopenia is associated with lower progesterone production in cattle. Reprod Domest Anim. 2013;48:137–48.

    Article  CAS  PubMed  Google Scholar 

  52. McCracken JA, Schramm W, Barcikowski B, Wilson Jr L. The identification of prostaglandin F2 alpha as a uterine luteolytic hormone and the hormonal control of its synthesis. Acta Vet Scand Suppl. 1981;77:71–88.

    CAS  PubMed  Google Scholar 

  53. Bauer M, Reibiger I, Spanel-Borowski K. Leucocyte proliferation in the bovine corpus luteum. Reproduction. 2001;121:297–305.

    Article  CAS  PubMed  Google Scholar 

  54. Al-Zi'abi MO, Fraser HM, Watson ED. Cell death during natural and induced luteal regression in mares. Reproduction. 2002;123:67–77.

    Article  PubMed  Google Scholar 

  55. Petrovska M, Dimitrov DG, Michael SD. Quantitative changes in macrophage distribution in normal mouse ovary over the course of the estrous cycle examined with an image analysis system. Am J Reprod Immunol. 1996;36:175–83.

    Article  CAS  PubMed  Google Scholar 

  56. 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 A Comp Exp Biol. 2003;296:152–9.

    Article  PubMed  CAS  Google Scholar 

  57. Brannstrom M, Friden B. Immune regulation of corpus luteum function. Semin Reprod Endocrinol. 1997;15:363–70.

    Article  CAS  PubMed  Google Scholar 

  58. Townson DH, Liptak AR. Chemokines in the corpus luteum: implications of leukocyte chemotaxis. Reprod Biol Endocrinol. 2003;1:94.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Penny LA. Monocyte chemoattractant protein 1 in luteolysis. Rev Reprod. 2000;5:63–6.

    Article  CAS  PubMed  Google Scholar 

  60. Okuda K, Sakumoto R. Multiple roles of TNF super family members in corpus luteum function. Reprod Biol Endocrinol. 2003;95:1–10.

    Google Scholar 

  61. Pate JL, Landis KP. Immune cells in the corpus luteum: friends or foes? Reproduction. 2001;122:665–76.

    Article  CAS  PubMed  Google Scholar 

  62. Shima T, Sasaki Y, Itoh M, Nakashima A, Ishii N, Sugamura K, Saito S. Regulatory T cells are necessary for implantation and maintenance of early pregnancy but not late pregnancy in allogeneic mice. J Reprod Immunol. 2010;85:121–9.

    Article  CAS  PubMed  Google Scholar 

  63. 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;118:479–89.

    CAS  PubMed  Google Scholar 

  64. Pate JL. Involvement of immune cells in regulation of ovarian function. J Reprod Fertil Suppl. 1995;49:365–77.

    CAS  PubMed  Google Scholar 

  65. Bowen JM, Towns R, Warren JS, Landis KP. Luteal regression in the normally cycling rat: apoptosis, monocyte chemoattractant protein-1, and inflammatory cell involvement. Biol Reprod. 1999;60:740–6.

    Article  CAS  PubMed  Google Scholar 

  66. Townson DH, O’Connor CL, Pru JK. Expression of monocyte chemoattractant protein-1 and distribution of immune cell populations in the bovine corpus luteum throughout the estrous cycle. Biol Reprod. 2002;66:361–6.

    Article  CAS  PubMed  Google Scholar 

  67. Neuvians TP, Schams D, Berisha B, Pfaffl MW. Involvement of pro-inflammatory cytokines, mediators of inflammation, and basic fibroblast growth factor in prostaglandin F2alpha-induced luteolysis in bovine corpus luteum. Biol Reprod. 2004;70:473–80.

    Article  CAS  PubMed  Google Scholar 

  68. Sawyer HR, Niswender KD, Braden TD, Niswender GD. Nuclear changes in ovine luteal cells in response to PGF2 alpha. Domest Anim Endocrinol. 1990;7:229–37.

    Article  CAS  PubMed  Google Scholar 

  69. Juengel JL, Garverick HA, Johnson AL, Youngquist RS, Smith MF. Apoptosis during luteal regression in cattle. Endocrinology. 1993;132:249–54.

    CAS  PubMed  Google Scholar 

  70. Kato S, Shiratsuchi A, Nagaosa K, Nakanishi Y. Phosphatidylserine- and integrin-mediated phagocytosis of apoptotic luteal cells by macrophages of the rat. Dev Growth Differ. 2005;47:153–61.

    Article  CAS  PubMed  Google Scholar 

  71. Sakumoto R, Vermehren M, Kenngott RA, Okuda K, Sinowatz F. Localization of gene and protein expressions of tumor necrosis factor-{alpha} (TNF), and TNF receptor types I and II in the bovine corpus luteum during the estrous cycle. J Anim Sci. 2011;89(10):3040–7.

    Article  CAS  PubMed  Google Scholar 

  72. Taniguchi H, Yokomizo Y, Okuda K. Fas-Fas ligand system mediates luteal cell death in bovine corpus luteum. Biol Reprod. 2002;66:754–9.

    Article  CAS  PubMed  Google Scholar 

  73. Pru JK, Lynch MP, Davis JS, Rueda BR. Signaling mechanisms in tumor necrosis factor alpha-induced death of microvascular endothelial cells of the corpus luteum. Reprod Biol Endocrinol. 2003;1:17.

    Article  PubMed  PubMed Central  Google Scholar 

  74. Fairchild DL, Pate JL. Interferon-gamma induction of major histocompatibility complex antigens on cultured bovine luteal cells. Biol Reprod. 1989;40:453–7.

    Article  CAS  PubMed  Google Scholar 

  75. Fairchild DL, Pate JL. Modulation of bovine luteal cell synthetic capacity by interferon-gamma. Biol Reprod. 1991;44:357–63.

    Article  CAS  PubMed  Google Scholar 

  76. Paape MJ, Bannerman DD, Zhao X, Lee JW. The bovine neutrophil: structure and function in blood and milk. Vet Res. 2003;34:597–627.

    Article  CAS  PubMed  Google Scholar 

  77. Shirasuna K, Jiemtaweeboon S, Raddatz S, Nitta A, Schuberth HJ, Bollwein H, Shimizu T, Miyamoto A. Rapid accumulation of polymorphonuclear neutrophils in the corpus luteum during prostaglandin F(2alpha)-induced luteolysis in the cow. PLoS One. 2012;7, e29054.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Diez-Fraile A, Meyer E, Duchateau L, Paape MJ, Burvenich C. In vitro regulation of Mac-1 expression on bovine polymorphonuclear leukocytes by endotoxin and tumor necrosis factor-alpha at different stages of lactation. Can J Vet Res. 2004;68:232–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Sohn EJ, Paape MJ, Connor EE, Bannerman DD, Fetterer RH, Peters RR. Bacterial lipopolysaccharide stimulates bovine neutrophil production of TNF-alpha, IL-1beta, IL-12 and IFN-gamma. Vet Res. 2007;38:809–18.

    Article  CAS  PubMed  Google Scholar 

  80. Benyo DF, Haibel GK, Laufman HB, Pate JL. Expression of major histocompatibility complex antigens on the bovine corpus luteum during the estrous cycle, luteolysis, and early pregnancy. Biol Reprod. 1991;45:229–34.

    Article  CAS  PubMed  Google Scholar 

  81. Minegishi K, Tanaka M, Nishimura O, Tanigaki S, Miyakoshi K, Ishimoto H, Yoshimura Y. Reactive oxygen species mediate leukocyte-endothelium interactions in prostaglandin F2alpha -induced luteolysis in rats. Am J Physiol Endocrinol Metab. 2002;283:E1308–15.

    Article  CAS  PubMed  Google Scholar 

  82. Pepperell JR, Wolcott K, Behrman HR. Effects of neutrophils in rat luteal cells. Endocrinology. 1992;130:1001–8.

    CAS  PubMed  Google Scholar 

  83. Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, Worthen GS, Albelda SM. Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer Cell. 2009;16:183–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Shen L, Smith JM, Shen Z, Eriksson M, Sentman C, Wira CR. Inhibition of human neutrophil degranulation by transforming growth factor-beta1. Clin Exp Immunol. 2007;149:155–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Piccard H, Muschel RJ, Opdenakker G. On the dual roles and polarized phenotypes of neutrophils in tumor development and progression. Crit Rev Oncol Hematol. 2012;82(3):296–309.

    Article  CAS  PubMed  Google Scholar 

  86. Coffelt SB, Hughes R, Lewis CE. Tumor-associated macrophages: effectors of angiogenesis and tumor progression. Biochim Biophys Acta. 1796;2009:11–8.

    Google Scholar 

  87. Nagamatsu T, Schust DJ. The contribution of macrophages to normal and pathological pregnancies. Am J Reprod Immunol. 2010;63:460–71.

    Article  CAS  PubMed  Google Scholar 

  88. Gordon S. Alternative activation of macrophages. Nat Rev Immunol. 2003;3:23–35.

    Article  CAS  PubMed  Google Scholar 

  89. Wang Y, Oliver G. Current views on the function of the lymphatic vasculature in health and disease. Genes Dev. 2010;24:2115–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Yamada Y, Nezu J, Shimane M, Hirata Y. Molecular cloning of a novel vascular endothelial growth factor VEGF-D. Genomics. 1997;42:483–8.

    Article  CAS  PubMed  Google Scholar 

  91. Joukov V, Sorsa T, Kumar V, Jeltsch M, Claesson-Welsh L, Cao Y, Saksela O, Kalkkinen N, Alitalo K. Proteolytic processing regulates receptor specificity and activity of VEGF-C. EMBO J. 1997;16:3898–911.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, Petrova TV, Jeltsch M, Jackson DG, Talikka M, Rauvala H, Betsholtz C, Alitalo K. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol. 2004;5:74–80.

    Article  CAS  PubMed  Google Scholar 

  93. Xu F, Stouffer RL. Existence of the lymphatic system in the primate corpus luteum. Lymphat Res Biol. 2009;7:159–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Nitta A, Shirasuna K, Haneda S, Matsui M, Shimizu T, Matsuyama S, Kimura K, Bollwein H, Miyamoto A. Possible involvement of IFNT in lymphangiogenesis in the corpus luteum during the maternal recognition period in the cow. Reproduction. 2011;142:879–92.

    Article  CAS  PubMed  Google Scholar 

  95. Imakawa K, Anthony RV, Kazemi M, Marotti KR, Polites HG, Roberts RM. Interferon-like sequence of ovine trophoblast protein secreted by embryonic trophectoderm. Nature (Lond). 1987;330:377–9.

    Article  CAS  Google Scholar 

  96. Hein WR, Shelton JN, Simpson-Morgan MW, Seamark RF, Morris B. Flow and composition of lymph from the ovary and uterus of cows during pregnancy. J Reprod Fertil. 1988;83:309–23.

    Article  CAS  PubMed  Google Scholar 

  97. Oliveira JF, Henkes LE, Ashley RL, Purcell SH, Smirnova NP, Veeramachaneni DN, Anthony RV, Hansen TR. Expression of interferon (IFN)-stimulated genes in extrauterine tissues during early pregnancy in sheep is the consequence of endocrine IFN-tau release from the uterine vein. Endocrinology. 2008;149:1252–9.

    Article  CAS  PubMed  Google Scholar 

  98. Han H, Austin KJ, Rempel LA, Hansen TR. Low blood ISG15 mRNA and progesterone levels are predictive of non-pregnant dairy cows. J Endocrinol. 2006;191:505–12.

    Article  CAS  PubMed  Google Scholar 

  99. Gifford CA, Racicot K, Clark DS, Austin KJ, Hansen TR, Lucy MC, Davies CJ, Ott TL. Regulation of interferon-stimulated genes in peripheral blood leukocytes in pregnant and bred, nonpregnant dairy cows. J Dairy Sci. 2007;90:274–80.

    Article  CAS  PubMed  Google Scholar 

  100. Yang L, Wang XL, Wan PC, Zhang LY, Wu Y, Tang DW, Zeng SM. Up-regulation of expression of interferon-stimulated gene 15 in the bovine corpus luteum during early pregnancy. J Dairy Sci. 2010;93:1000–11.

    Article  CAS  PubMed  Google Scholar 

  101. Green JC, Okamura CS, Poock SE, Lucy MC. Measurement of interferon-tau (IFN-tau) stimulated gene expression in blood leukocytes for pregnancy diagnosis within 18-20 d after insemination in dairy cattle. Anim Reprod Sci. 2010;121:24–33.

    Article  CAS  PubMed  Google Scholar 

  102. Shirasuna K, Matsumoto H, Kobayashi E, Nitta A, Haneda S, Matsui M, Kawashima C, Kida K, Shimizu T, Miyamoto A. Upregulation of interferon-stimulated genes and interleukin-10 in peripheral blood immune cells during early pregnancy in dairy cows. J Reprod Dev. 2012;58:84–90.

    Article  CAS  PubMed  Google Scholar 

  103. Shirasuna K, Matsumoto H, Matsuyama S, Kimura K, Bollwein H, Miyamoto A. Possible role of IFNT on the bovine corpus luteum and neutrophils during the early pregnancy. Reproduction. 2015;150(3):217–25.

    Article  CAS  PubMed  Google Scholar 

  104. Fujiwara H. Do circulating blood cells contribute to maternal tissue remodeling and embryo-maternal cross-talk around the implantation period? Mol Hum Reprod. 2009;15:335–43.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the Grant-in-Aid for Scientific Research of the Japan Society for the Promotion of Science (JSPS) and the Global COE Program, Ministry of Education, Culture, Science and Technology, Japan.

Author information

Authors and Affiliations

  1. Faculty of Agriculture, Department of Animal Science, Tokyo University of Agriculture, Atsugi, Kanagawa, 243-0034, Japan

    Koumei Shirasuna

  2. Graduate School of Animal and Food Hygiene, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, 080-8555, Japan

    Akio Miyamoto

Authors
  1. Koumei Shirasuna
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Akio Miyamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Akio Miyamoto .

Editor information

Editors and Affiliations

  1. The Robert H. Smith Faculty of Agriculture Food and Environment Department of Animal Sciences, The Hebrew University of Jerusalem, Rehovot, Jerusalem, Israel

    Rina Meidan

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Shirasuna, K., Miyamoto, A. (2017). Immune Cells and Their Effects on the Bovine Corpus Luteum. In: Meidan, R. (eds) The Life Cycle of the Corpus Luteum. Springer, Cham. https://doi.org/10.1007/978-3-319-43238-0_6

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-43238-0_6

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-43236-6

  • Online ISBN: 978-3-319-43238-0

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation