Skip to main content
SpringerLink
Log in
Book cover

Molecular and Cellular Aspects of Periimplantation Processes pp 205–230Cite as

Cytokine Gene Expression and Distribution of Inflammatory Leukocytes in the Periimplantation Mouse Uterus

  • Conference paper

Part of the book series: Serono Symposia USA ((SERONOSYMP))

Abstract

During both the estrous cycle and pregnancy, the uterus undergoes significant changes that have many similarities to inflammatory processes. These changes include edema, prostaglandin and leukotriene production, neovascularization, and infiltration of blood-borne cells including macrophages (1), lymphocytes (2), neutrophils (3, 4) and eosinophils (5); each of these responses occurs as part of the normal physiology of this organ. Leukocyte influx in the rodent uterus occurs in response to estrogen in ovariectomized adult and in immature animals (5), and this infiltration resembles one of the major events in a classical inflammatory response (6). Classical inflammatory processes entail complex interactions between many cell types and involve not only the infiltration, but also the activation of leukocytes. The concomitant production of various soluble mediators, including macrophage-derived cytokines (7, 8), is central to the inflammatory response. Although the presence of macrophages and other inflammatory cells within the endometrial stroma has been detected by morphological and histochemical means, their activation in the uterus during early pregnancy has not been examined.

This is a preview of subscription content, 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   84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight 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

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Tachi C, Tachi S. Role of macrophages in the maternal recognition of pregnancy J Reprod Fertil Suppl 1989; 37: 63–70.

    PubMed  CAS  Google Scholar 

  2. Noun A, Acker GM, Chaouat G, Antoine JC, Garabedian M. Cells bearing granulocyte-macrophage and T lymphocyte antigens in the rat uterus before and during ovum implantation. Clin Exp Immunol 1989; 78: 494–8.

    PubMed  CAS  Google Scholar 

  3. McMaster MT, Teng CT, Dey SK, Andrews GK. Lactoferrin in the mouse uterus: analyses of the preimplantation period and regulation by ovarian steroids. Mol Endocrinol 1992; 6: 101–11.

    Article  PubMed  CAS  Google Scholar 

  4. Finn CA, Pope MD. Infiltration of neutrophil polymorphonuclear leukocytes into the endometrial stroma at the time of implantation of ova and the initiation of the oil decidual cell reaction in mice. J Reprod Fertil 1991; 91: 365–9.

    Article  PubMed  CAS  Google Scholar 

  5. Zheng Y, Zhou Z-Z, Lyttle CR, Teuscher C. Immunohistochemical characterization of the estrogen-stimulated leukocyte influx in the immature rat uterus. J Leukoc Biol 1988; 44: 27–32.

    PubMed  CAS  Google Scholar 

  6. Larsen GL, Henson PH. Mediators of inflammation. Annu Rev Immunol 1983; 1: 335–59.

    Article  PubMed  CAS  Google Scholar 

  7. Papadimitriou JM, Ashman RB. Macrophages: current views on their differentiation, structure and function. Ultrastruct Pathol 1989; 13: 343–72.

    Article  PubMed  CAS  Google Scholar 

  8. Arai KI, Lee F, Miyajima A, Miyatake S, Arai N, Yokota T. Cytokines: coordinators of immune and inflammatory responses. Annu Rev Biochem 1990; 59: 783–836.

    Article  PubMed  CAS  Google Scholar 

  9. De SK, McMaster MT, Andrews GK. Endotoxin induction of murine metallothionein gene expression. J Biol Chem 1990; 265: 15267–74.

    PubMed  CAS  Google Scholar 

  10. Dumm SK, Schmidt JA, Oppenheim JJ. Interleukin-1: an immunological perspective. Annu Rev Immunol 1985; 3: 263–87.

    Article  Google Scholar 

  11. Dinarello CA. The biology of interleukin 1 and comparison to tumor necrosis factor. Immunol Lett 1987; 16: 227–31.

    Article  PubMed  CAS  Google Scholar 

  12. Bentler B, Cerami A. The biology of cachectin/TNF-α primary mediator of the host response. Annu Rev Immunol 1989; 7: 625–55.

    Article  Google Scholar 

  13. Beer AE. Billingham RE. Immunoregulatory aspects of pregnancy. Fed Proc 1978; 37: 2374–8.

    PubMed  CAS  Google Scholar 

  14. Psychoyos A. Endocrine control of egg implantation. In: Greep RO, Astwood EG, Geiger SR, eds. Handbook of physiology. Washington, DC: American Physiological Society, 1973: 187–215.

    Google Scholar 

  15. Potts DM. The ultrastructure of implantation in the mouse. J Anat 1968; 103: 77–90.

    PubMed  CAS  Google Scholar 

  16. Kennedy TG. Evidence for a role of prostaglandins in the initiation of blastocyst implantation in the rat. Biol Reprod 1977; 16: 286–91.

    Article  PubMed  CAS  Google Scholar 

  17. Tachi C, Tachi S, Knyszynski A, Linder HR. Possible involvement of macrophages in embryo-maternal relationships during embryo implantation in the rat. J Exp Zool 1981; 217: 81–92.

    Article  PubMed  CAS  Google Scholar 

  18. McMaster MT, Dey SK, Andrews GK. Association of monocytes and neutrophils with early events in the process of blastocyst implantation in the mouse. J Reprod Fertil 1993; 99: 561–9.

    Article  PubMed  CAS  Google Scholar 

  19. Huet-Hudson YM, Chakraborty C, De SK, Suzuki Y, Andrews GK, Dey SK. Estrogen regulates the synthesis of epidermal growth factor in mouse uterine epithelial cells. Mol Endocrinol 1990; 4: 510–23.

    Article  PubMed  CAS  Google Scholar 

  20. McMaster MT, Newton RC, Dey SK, Andrews GK. Activation and distribution of inflammatory cells in the mouse uterus during the preimplantation period. J Immunol 1992; 148: 1699–705.

    PubMed  CAS  Google Scholar 

  21. Andrews GK, Lehman LD, Huet YM, Dey SK. Metallothionein gene regulation in the preimplantation rabbit blastocyst. Development 1987; 100: 463–5.

    PubMed  CAS  Google Scholar 

  22. De SK, McMaster MT, Dey SK, Andrews GK. Cell-specific metallothionein gene expression in mouse decidua and placentae. Development 1989; 107: 611–21.

    PubMed  CAS  Google Scholar 

  23. Teng CT, Walker MP, Bhattacharyya SN, Klapper DG, DiAugustine RP, McLachlan JA. Purification and properties of an oestrogen-stimulated mouse uterine glycoprotein (approx. 70 kDa). Biochem J 1986; 240: 413–22.

    PubMed  CAS  Google Scholar 

  24. Keeping HS, Lyttle CR. Monoclonal antibody to rat uterine peroxidase and its use in identification of the peroxidase as being of eosinophil origin. Biochim Biophys Acta 1984; 802: 399–406.

    PubMed  CAS  Google Scholar 

  25. King WJ, Allen TC, DeSombre ER. Localization of uterine peroxidase activity in estrogen treated rats. Biol Reprod 1981; 25: 859–70.

    Article  PubMed  CAS  Google Scholar 

  26. Jacobs AL, Carson DD. Uterine epithelial cell secretion of interleukin-lα induces prostaglandin E2 (PGE2) and PGF2α secretion by uterine stromal cells in vitro. Endocrinology 1993; 132: 300–8.

    Article  PubMed  CAS  Google Scholar 

  27. Jacobs AL, Sehgal PB, Julian J, Carson DD. Secretion and hormonal regulation of interleukin-6 production by mouse uterine stromal and polarized epithelial cells cultured in vitro. Endocrinology 1992; 131: 1037–46.

    Article  PubMed  CAS  Google Scholar 

  28. Robertson SA, Mayrhofer G, Seamark RF. Uterine epithelial cells synthesize granulocyte-macrophage colony-stimulating factor and interleukin-6 in pregnant and nonpregnant mice. Biol Reprod 1992; 46: 1069–79.

    Article  PubMed  CAS  Google Scholar 

  29. Hunt JS, Chen H-L, Hu X-L, Pollard JW. Normal distribution of tumor necrosis factor-α messenger ribonucleic acid and protein in the uteri, placentas and embryos of osteopetrotic (op/op) mice lacking colony stimulating factor-1. Biol Reprod 1993; 49: 441–52.

    Article  PubMed  CAS  Google Scholar 

  30. Tamada H, Das SJ, Andrews GK, Dey SK. Cell-type-specific expression of transforming growth factor-α in the mouse uterus during the peri-implantation period. Biol Reprod 1991; 45: 365–72.

    Article  PubMed  CAS  Google Scholar 

  31. Dalton T, Kover K, Dey SK, Andrews GK. Analysis of the expression of growth factor, interleukin and lactoferrin genes and the distribution of inflammatory leukocytes in the preimplantation mouse oviduct. Biol Reprod 1994; 51: 597–606.

    Article  PubMed  CAS  Google Scholar 

  32. Naz R, Mehta K. Cell-mediated responses to sperm antigens: effects on mouse sperm and embryos. Biol Reprod 1989; 41: 533–42.

    Article  PubMed  CAS  Google Scholar 

  33. Robertson SA, Seamark RF. Granulocyte macrophage colony stimulating factor (GM-CSF) in the murine reproductive tract: stimulation by seminal factors. Reprod Fertil Dev 1990; 2: 359–68.

    Article  PubMed  CAS  Google Scholar 

  34. Tchemitchin A, Roorijck J, Tchemitchin X, Vandenhende J, Galand P. Dramatic early increase in uterine eosinophils after oestrogen administration. Nature 1974; 248: 142–3.

    Article  Google Scholar 

  35. De M, Wood GW. Influence of oestrogen and progesterone on macrophage distribution in the mouse uterus. J Endocrinol 1990; 126: 417–24.

    Article  PubMed  CAS  Google Scholar 

  36. Lee YH, Howe RS, Sha S-J, Teuscher C, Sheehan DM, Lyttle CR. Estrogen regulation of an eosinophil chemotactic factor in the immature rat uterus. Endocrinology 1989; 125: 3022–8.

    Article  PubMed  CAS  Google Scholar 

  37. Malathy PV, Cheng HC, Dey SK. Production of leukotrienes and Prostaglandins in the rat uterus during periimplantation period. Prostaglandins 1986; 32: 605–14.

    Article  PubMed  CAS  Google Scholar 

  38. Issekutz AC, Movat HZ. The effect of vasodilator prostaglandine on polymorphonuclear leukocyte infiltration and vascular injury. Am J Pathol 1982; 107: 300–9.

    PubMed  CAS  Google Scholar 

  39. Reibman J, Meixler S, Lee TC, et al. Transforming growth factor β1, a potent chemoattractant for human neutrophils, bypasses classic signal-transduction pathways. Proc Natl Acad Sci USA 1991; 88: 6805–9.

    Article  PubMed  CAS  Google Scholar 

  40. Tamada H, McMaster MT, Flanders KC, Andrews GK, Dey SK. Cell type-specific expression of TGF-β1 in the mouse uterus during the peri-implantation period. Mol Endocrinol 1990; 4: 965–72.

    Article  PubMed  CAS  Google Scholar 

  41. De M, Sanford TR, Wood GW. Interleukin-1, interleukin-6 and tumor necrosis factor-α are produced in the mouse uterus during the estrous cycle and are induced by estrogen and progesterone. Dev Biol 1992; 151: 297–305.

    Article  PubMed  CAS  Google Scholar 

  42. Shanker G, Sorci-Thomas M, Register TC, Adams MR. The inducible expression of THP-1 cell interleukin-1 mRNA: effects of estrogen on differential response to phorbol ester and lipopolysaccharide. Lymphok Cytok Res 1994; 13: 1–7.

    CAS  Google Scholar 

  43. Polan ML, Daniele A, Kuo A. Gonadal steroids modulate human monocyte interleukin-1 (IL-1) activity. Fertil Steril 1988; 49: 964–8.

    PubMed  CAS  Google Scholar 

  44. Hu SK, Mitcho YL, Rath NC. Effect of estradiol on interleukin-1 synthesis by macrophages. Int J Immunopharmacol 1988; 10: 247–52.

    Article  PubMed  CAS  Google Scholar 

  45. Polan ML, Loukides J, Nelson P, et al. Progesterone and estradiol modulate interleukin-1β mmessenger ribonucleic acid levels in cultured human peripheral monocytes. J Clin Endocrinol Metab 1989; 89: 1200–6.

    Article  Google Scholar 

  46. Takacs L, Kovacs EJ, Smith MR, Young HA, Durum SK. Detection of IL-1α and IL-1β gene expression by in situ hybridization: tissue localization of IL-1 mRNA in the normal C57BL/6 mouse. J Immunol 1988; 141: 3081–95.

    PubMed  CAS  Google Scholar 

  47. Finn CA. Implantation, menstruation and inflammation. Biol Rev 1986; 61: 313–28.

    Article  PubMed  CAS  Google Scholar 

  48. King A, Loke YW. Uterine large granular lymphocytes: a possible role in embryonic implantation? Am J Obstet Gynecol 1990; 162: 308–10.

    PubMed  CAS  Google Scholar 

  49. Pollard JW, Hunt JS, Wiktor-Jedzejczar W, Stanley ER. A pregnancy defect in the osteopetrotic (op/op) mouse demonstrates the requirement for CSF-1 in female fertility. Dey Biol 1991; 148: 273–83.

    Article  CAS  Google Scholar 

  50. Simon C, Frances A, Piquette GN, et al. Embryonic implantation in mice is blocked by interleukin-1 receptor antagonist. Endocrinology 1994; 143: 521–8.

    Article  Google Scholar 

  51. Rogers PAW, Macpherson AM, Beaton L. Reduction in endometrial neutrophils in proximity to implanting rat blastocysts. J Reprod Fertil 1992; 96: 283–8.

    Article  PubMed  CAS  Google Scholar 

  52. Heck LW, Blackburn WD, Irwin MH, Abrahamson DR. Degradation of basement membrane laminin by human neutrophil elastase and cathepsin G. Am J Pathol 1990; 136: 1267–74.

    PubMed  CAS  Google Scholar 

  53. Kapp A, Zeck-Kapp G. Activation of the oxidative metabolism in human polymorphonuclear neutrophilic granulocytes: the role of immuno-modulating cytokines. J Invest Dermatol 1990; 95: 945–9S.

    Article  Google Scholar 

  54. Halliwell B, Gutteridge JMC. Free radicals and metal ions in human disease. Methods Enzymol 1990; 186: 1–85.

    Article  PubMed  CAS  Google Scholar 

  55. Baumann JW, Liu J, Liu YP, Klaassen CD. Increase in metallothionein produced by chemicals that induce oxidative stress. Toxicol Appl Pharmacol 1991; 110: 347–54.

    Article  Google Scholar 

  56. Kishimoto TK. A dynamic model for neutrophil localization to inflammatory sites. J NIH Res 1991; 3: 75–7.

    Google Scholar 

  57. Sayers TJ, Wiltrout TA, Bull CA, Denn AC, Pilaro AM, Lokesh B. Effects of cytokines on polymorphonuclear neutrophil infiltration in the mouse: prostaglandin-and leukotriene-independent induction of infiltration by IL-1 and tumor necrosis factor. J Immunol 1988; 141: 1670–7.

    PubMed  CAS  Google Scholar 

  58. Mason MJ, Van Epps DE. In vivo neutrophil emigration in response to interleukin-1 and tumor necrosis factor-alpha. J Leukoc Biol 1989; 45: 62–8.

    PubMed  CAS  Google Scholar 

  59. Schlayer HJ, Laaff H, Peters T, et al. Involvement of tumor necrosis factor in endotoxin-triggered neutrophil adherence to sinusoidal endothelial cells of mouse liver and its modulation in acute phase. J Hepatol 1989; 7: 239–49.

    Article  Google Scholar 

  60. Strieter RM, Kunkel SL, Showell HJ, et al. Endothelial cell gene expression of a neutrophil chemotactic factor by TNF-α, LPS, and IL-1β. Science 1989; 243: 1467–9.

    Article  PubMed  CAS  Google Scholar 

  61. Strieter RM, Phan SH, Showell HJ, et al. Monokine-induced neutrophil chemotactic factor gene expression in human fibroblasts. J Biol Chem 1989; 264: 10621–6.

    PubMed  CAS  Google Scholar 

  62. Matsushima K, Morishita K, Yoshimura T, et al. Molecular cloning of a human monocyte-derived neutrophil chemotactic factor (MDNCF) and the induction of MDNCF mRNA by interleukin 1 and tumor necrosis factor. J Exp Med 1988; 167: 1883–93.

    Article  PubMed  CAS  Google Scholar 

  63. Rappolee DA, Brenner CA, Schultz R, Mark D, Werb Z. Developmental expression of PDGF, TGF-α, and TGF-β genes in preimplantation mouse embryos. Science 1988; 242: 1823–5.

    Article  Google Scholar 

  64. Paria BC, Jones KL, Flanders KC, Dey SK. Localization and binding of transforming growth factor-β isoforms in preimplantation mouse embryos and in delayed and activated blastocysts. Dev Biol 1992; 151: 91–104.

    Article  PubMed  CAS  Google Scholar 

Download references

Authors
  1. Glen K. Andrews
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael T. McMaster
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luchuan Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Karen Kover
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sudhansu K. Dey
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Physiology, University of Kansas Medical Center, Kansas City, KS, 66160, USA

    S. K. Dey Ph.D.

Rights and permissions

Reprints and permissions

Copyright information

© 1995 Springer-Verlag New York, Inc.

About this paper

Cite this paper

Andrews, G.K., McMaster, M.T., Liang, L., Kover, K., Dey, S.K. (1995). Cytokine Gene Expression and Distribution of Inflammatory Leukocytes in the Periimplantation Mouse Uterus. In: Dey, S.K. (eds) Molecular and Cellular Aspects of Periimplantation Processes. Serono Symposia USA. Springer, New York, NY. https://doi.org/10.1007/978-1-4612-2548-5_13

Download citation

  • DOI: https://doi.org/10.1007/978-1-4612-2548-5_13

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4612-7575-6

  • Online ISBN: 978-1-4612-2548-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation