Skip to main content
SpringerLink
Log in

Immunosuppressor activity of rat endometrial granulated cells and their differentiation

  • Cell Differentiation and Proliferation
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

Natural killer and natural suppressor activities of the rat endometrial granulated cells were assayed on days 13 and 14 of pregnancy or pseudopregnancy. Metrial gland granulated cells were used as endometrial granulated cells. The natural killer activities of metrial gland granulated cells and other cells were determined by means of Hashimoto-Sudo test with K562 cells as targets. The estimation of natural killer activity included removal of the cells sticking to glass from a suspension of material gland granulated cells. Cytochemically, metrial gland granulated cells were identified by the presence of PAS-positive granules in the cytoplasm after treatment of the cells with diastase and identification of a specific antigen with the help of specific antisera. The natural killer activity of metrial gland granulated cells was twice weaker than that of splenocytes from the same pregnant or pseudopregnant females. The level of natural killer activity was proportional to the content of metrial gland granulated cells in a cell system. These data suggest that the natural killer activity of metrial gland granulated cells is realized via their contact with cell targets. Natural killer and suppressor activities were determined simultaneously for metrial gland granulated cells and splenocytes of the same rat with common cell targets. When estimating the natural suppressor activity of metrial gland granulated cells, the splenocytes of the same rat were used as an effector in a natural killer test. Various amounts of metrial gland granulated cells were added to the effector: target system at a ratio of 50 : 1. The natural suppressor activity of metrial gland granulated cells did not depend on the amount of metrial gland granulated cells present in a natural killer system. After fractionation in a Percoll gradient, the highest natural killer activity was recorded in a 60% Percoll fraction. The highest and lowest natural suppressor activities were recorded in 30% and 60% Percoll fractions, respectively. The culture medium was characterized by natural suppressor activity as well. The differences in mean areas of metrial gland granulated cells in 30 and 60% Percoll fractions between the pregnant (144.7 ± 13.4 and 75.0 ± 12.5 µm2, respectively) and pseudopregnant (97.5 ± 4.9 and 69.2 ± 3.5 µm2, respectively) females were reliable. The natural killer activity was estimated in all studied 23 samples of metrial gland granulated cells, among which 18 (79.6 ± 7.8%) displayed the natural suppressor activity as well. The absence of natural suppressor activity in five samples was combined with the absence of this activity in their culture medium and with a reduction in the mean area of metrial gland granulated cells in 30% Percoll fraction to 109 ± 5 µm2. The data obtained confirm the known data on a low killer activity of metrial gland granulated cells and demonstrated for the first time the natural suppressor activity of these cells. It was concluded that the natural suppressor activity of metrial gland granulated cells is due to their differentiation from metrial gland granulated cells with natural killer activity.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  • Ashkar, A.A., Santo, J.P., and Cray, B.A., Interferon Contributes to Initiation of Uterine Vascular Modification, Decidua Integrity, and Uterine Natural Killer Cell Maturation during Normal Murine Pregnancy, J. Exp. Med., 2000, vol. 192, pp. 259–270.

    Google Scholar 

  • Baker, B.L., Histochemical Variations in the Metrial Gland of the Rat during Pregnancy, Proc. Soc. Exp. Biol. Med., 1948, vol. 68, pp. 492–496.

    Google Scholar 

  • Beer, A.E. and Billingham, R.E., Immunology of Mammalian Reproduction, Adv. Immunol., 1971, vol. 14, pp. 1–84.

    Google Scholar 

  • Boyum, A., Separation of Lymphocytes from Blood and Bone Marrow, Scand. J. Clin. Lab. Invest., 1968, vol. 97, pp. 77–82.

    Google Scholar 

  • Bulmer, D., Further Studies on the Granulated Metrial Gland Cells of the Pregnant Rat, J. Anat. (L.), 1968, vol. 103, pp. 479–489.

    Google Scholar 

  • Bulmer, D. and Peel, S., An Autoradiographical Study of Cellular Proliferation in the Uterus and Placenta of the Pregnant Rat, J. Anat. (L.), 1974, vol. 117, pp. 433–441.

    Google Scholar 

  • Bulmer, D. and Peel, S., The Demonstration of Immunoglobulin in the Metrial Gland of the Rat Placenta, J. Reprod. Fert., 1977, vol. 49, pp. 143–145.

    Google Scholar 

  • Bulmer, J.N., Pace, D., and Ritson, A., Immunoregulatory Cells in Human Decidua. Morphology, Immunochemistry and Function, Reprod. Nutr. Devel., 1988, vol. 28, pp. 1599–1614.

    Google Scholar 

  • Cardell, R.R., Hisaw, F.L., and Dawson, A.B., The Fine Structure of Granular Cells in the Uterine Endometrium of the Rhesus Monkey (Macaca mulata) with a Discussion of the Possible Function of These Cells in Relaxin Secretion, Am. J. Anat., 1969, vol. 124, pp. 307–316.

    Google Scholar 

  • Cudkowicz, G. and Hochman, P.S., Carrageenan-Induced Decline of Natural Killer Activity. 1. In vivo Activation of Adherent Non-T-Suppressor Cells, Cell Immunol., 1980, vol. 53, pp. 395–404.

    Google Scholar 

  • Dallenbach-Hellweg, G., Histopathology of Endometrium, Heidelberg: Springer, 1981.

    Google Scholar 

  • Finn, C.A., Implantation, Menstruation and Inflammation, Biol. Rev., 1986, vol. 61, pp. 313–328.

    Google Scholar 

  • Frank, G.R., Brar, A.K., Cedars, M.I., and Handwerger, S., Prostaglandin E2 Enhances Human Endometrial Stromal Cell Differentiation, Endocrinology, 1994, vol. 134, pp. 258–263.

    Google Scholar 

  • Hashimoto, Y. and Sudo, E., Evaluation of Cell Damage in Immune Reaction by Release of Radioactivity from 3H-Uridine Labeled Cells, Gann, 1971, vol. 62, pp. 139–145.

    Google Scholar 

  • Jollie, W.P. and Bencosme, S.A., Electron Microscope Observations on Primary Decidua Formation in the Rat, Am. J. Anat., 1965, vol. 116, pp. 217–236.

    Google Scholar 

  • Khesin, Ya.E., Razmery yader i funktsional’noe sostoyanie kletok (Nuclear Sizes and Functional State of Cells), Moscow: Meditsina, 1967.

    Google Scholar 

  • King, A., Uterine Leukocytes and Decidualization, Hum. Reprod. Update, 2000, vol. 6, pp. 28–36.

    Google Scholar 

  • Lala, P.K., Kennedy, T.G., and Parhar, R.S., Suppression of Lymphocyte Alloreactivity by Early Gestational Human Decidua, Cell Immunol., 1988, vol. 116, pp. 411–422.

    Google Scholar 

  • Larkin, L.H., Electron Microscopy of the Granule Release in Metrial Gland Cells of the Pregnant Rat, Anal. Rec., 1972, vol. 172, pp. 109–126.

    Google Scholar 

  • Larkin, L.H. and Schultz, R.L., Histochemical and Autoradiographic Studies of the Formation of the Metrial Gland in the Pregnant Rat, Am. J. Anat., 1968, vol. 122, pp. 607–620.

    Google Scholar 

  • Lee, C.-C., Parr, E.L., and Young, L.D., Granulated Lymphoid Cells of the Pregnant Uterus: Morphological and Functional Features, Int. Rev. Cytol., 1994, vol. 153, pp. 105–136.

    Google Scholar 

  • Linde, V.A., Podporina, A.T., and Mikhailov, V.M., Killer and Suppressor Properties of Lymphoid Cells of Human Decidua, Tsitologiya, 1992, vol. 34, no. 9, pp. 77–78.

    Google Scholar 

  • Linnemeyer, P.A. and Pollack, S.B., Murine Granulated Metrial Gland Cells at Uterine Implantation Sites Are Natural Killer Lineage Cells, J. Immunol., 1991, vol. 147, pp. 2530–2535.

    Google Scholar 

  • Linnemeyer, P.A. and Pollack, S.B., Prostaglandin E2-Induced Changes in Phenotype, Morphology, and Lytic Activity of IL-2-Activated Natural Killer Cells, J. Immunol., 1993, vol. 150, pp. 3747–3754.

    Google Scholar 

  • Luppa, Kh., Osnovy gistokhimii (Foundations of Histochemistry), Moscow: Mir, 1980.

    Google Scholar 

  • Maier, T., Holda, J.H., and Claman, Y.N., Natural Supressor (NS) Cells. Members of LGL Regulatory Family, Immunol. Today, 1986, vol. 7, pp. 312–315.

    Google Scholar 

  • Merviel, P., Evain-Brion, D., Challier, J.C., et al., The Molecular Basis of Embryo Implantation in Humans, Zentralbl. Gynakol., 2001, vol. 123, pp. 328–239.

    Google Scholar 

  • Mikhailov, V.M., Pathogenic Effect of Nephrocytotoxic Serum on Embryogenesis in White Rats, Byull. Eksperim. Biol. Med., 1967, vol. 63, no. 6, pp. 97–100.

    Google Scholar 

  • Mikhailov, V.M., Tissue-Specific Antigens of Decidua in White Rats, Tsitologiya, 1977, vol. 19, no. 11, pp. 477–480.

    Google Scholar 

  • Mikhailov, V.M., Secretory Function of Cells in the Rat Metriai Gland, Biomed. Sci. (London-Moscow), 1991, vol. 2, pp. 477–480.

    Google Scholar 

  • Mikhailov, V.M., Life Cycle of Decidual Cells, Doctoral (Biol.) Dissertation, St. Petersburg: In-t tsitologii Ross. Akad. Nauk, 1998.

    Google Scholar 

  • Mikhailov, V.M., Life Cycle of Decidual Cells, Int. Rev. Cytol., 2003, vol. 227, pp. 1–63.

    Google Scholar 

  • Mikhailov, V.M. and Kottsova, N.A., Immunological Function and Differentiation of Endometrium Granulated Cells, Mater. I Vsesoyuz. Immunologich. S’‘ezda (Materials of the I All-Union Immunological Congress), Moscow: Nauka, 1989, vol. 2, p. 89.

    Google Scholar 

  • Mikhailov, V.M. and Malygin, A.M., On the Role of Decidual Cells in Immunobiological Relations of Mother and Fetus, Tsitologiya, 1981, vol. 23, no. 2, pp. 211–216.

    Google Scholar 

  • Mikhailov, V.M., Bystrova, O.A., Lukin, V.A., et al., Cell-Specific Antigen of Human Endometrium, Tsitologiya, 1986, vol. 28, no. 9, pp. 986–992.

    Google Scholar 

  • Mikhailov, V.M., Linde, V.A., Podporina, A.T., et al., Granulated Cells of Endometrium as a Special Type of Leucocytes, Morfologiya, 1993a, vol. 105, no. 9–10, p. 114.

    Google Scholar 

  • Mikhailov, V.M., Peel, S., and Stewart, I., Antibodies to Rat Metrial Gland, J. Anat. (L), 1993b, vol. 182, pp. 150–151.

    Google Scholar 

  • Mikhailov, V.M., Podporina, A.T., and Malygin, A.M., Immunological Functions of Granulated Ceils, 8th Internat. Conf. Internat. Soc. Differentiation, Hiroshima, 1994, p. 93.

  • Mitchell, B.S., Cruggs, R.I., and Peel, S., Localisation of Immunoglobulin (IgG) within the Rat Metrial Gland, J. Rep. Immunol., 1981, vol. 3, pp. 237–241.

    Google Scholar 

  • Palkovits, M. and Fischer, J., Karyometric Investigations, Budapest: Akademiai Kiado, 1968.

    Google Scholar 

  • Parr, E.L., Young, L.H., Parr, M.B., and Young, J.D., Granulated Metrial Gland Cells of Pregnant Mouse Are Natural Killer-Like Cells That Contain Perforin and Serine Esterase, J. Immunol., 1990, vol. 145, pp. 2365–2372.

    Google Scholar 

  • Peel, S., Granulated Metrial Gland Cells, Heidelberg: Springer, 1989.

    Google Scholar 

  • Peel, S. and Adam, E., The Killing of the Placenta Cells by Rat and Mouse Granulated Metrial Gland Cells in vitro, Placenta, 1991, vol. 12, pp. 161–171.

    Google Scholar 

  • Podporina, A.T., Immunoregulatory Properties of Endometrium Granulated Cells, Cand. Sci. (Biol.) Dissertation, St. Petersburg: In-t tsitologii Ross. Akad. Nauk, 1994.

    Google Scholar 

  • Podporina, A.T., Malygin, A.M., and Mikhailov, V.M., Immunoregulatory Properties of Rat Metrial Gland Cells, Tsitologiya, 1992, vol. 34, no. 9, pp. 93–94.

    Google Scholar 

  • Repina, M.A., Linde, V.A., Podporina, A.T., et al., Functional Activity of Lymphoid Cells of the Decidual Membrane during Later Pregnancy, Morfologiya, 1994, vol. 105, nos. 7–12, pp. 155–158.

    Google Scholar 

  • Scodras, J.M., Parhar, R.S., Kennedy, T.G., and Lala, P.K., Prostaglandin-Mediated Inactivation of Natural Killer Cells in the Uterine Decidua, Cell Immunol., 1990, vol. 127, pp. 352–367.

    Google Scholar 

  • Stewart, I., Immunoglobulin G in the Decidua Basalis and Metrial Gland of the Pregnant Mouse Uterus, J. Rep. Immunol., 1985, vol. 7, pp. 275–278.

    Google Scholar 

  • Stewart, I., Granulated Metrial Gland Cells: Pregnancy Specific Leukocytes?, J. Leukocyt. Biol., 1991, vol. 50, pp. 198–207.

    Google Scholar 

  • Stewart, I. and Mukhtar, D.D.J., The Killing of Mouse Trophoblast Cells by Granulated Metrial Gland Cells in vitro, Placenta, 1988, vol. 9, pp. 417–423.

    Google Scholar 

  • Timonen, T. and Saksela, E., Isolation of Human NK Cells by Density Gradient Centrifugation, J. Immunol. Methods, 1980, vol. 36, pp. 285–289.

    Google Scholar 

  • Timonen, T., Ortaldo, L.R., and Herberman, R.B., Characteristics of Human Large Granular Lymphocytes and Relationship to Natural Killer and K Cells J. Exp. Med., 1981, vol. 153, pp. 569–582.

    Google Scholar 

  • Tokin, B.P., Immunitet zarodyshei (Immunity of Embryos), Leningrad: Leningr. Gos. Univ., 1955.

    Google Scholar 

  • Trapani, J.A. and Smith, M.J., Killing by Cytotoxic T Cells and Natural Killer Cells: Multiple Granule Serine Proteases as Initiators of DNA Fragmentation, Immunol. Cell Res., 1993, vol. 71, pp. 201–208.

    Google Scholar 

  • Ulezko-Stroganova, L.P., Normal’naya i patologicheskaya anatomiya i gistologiya zhenskikh polovykh organov (Normal and Pathological Anatomy and Histology of Female Genitalia), Moscow: Medgiz, 1939.

    Google Scholar 

  • Zybina, E.V., Cytological Observations of the Rat Metrial Gland Cells, Dokl. Akad. Nauk SSSR, 1958, vol. 120, no. 4, pp. 882–885.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Cytology, Russian Academy of Sciences, Tikhoretskii pr. 4, 194064, St. Petersburg, Russia

    A. T. Podporina & V. M. Mikhailov

Authors
  1. A. T. Podporina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. M. Mikhailov
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Translated from Ontogenez, Vol. 36, No. 1, 2005, pp. 26–34.

Original Russian Text Copyright © 2005 by Podporina, Mikhailov.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Podporina, A.T., Mikhailov, V.M. Immunosuppressor activity of rat endometrial granulated cells and their differentiation. Russ J Dev Biol 36, 21–28 (2005). https://doi.org/10.1007/s11174-005-0004-z

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11174-005-0004-z

Key words

Search

Navigation