Skip to main content
Log in

Luteinization of human granulosa cells in vivo is associated with expression of MHC Class II antigens

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

We previously described the presence of MHC class II (HLA-DR) antigens, structurally similar to those on lymphoid cells and bearing the genetically-appropriate allotypic determinants, on human adrenocortical cells in the zona reticularis of normal glands. We now report a similar expression by granulosa-lutein cells (GLC) in corpora lutea (CL) of normal ovaries, as detected by indirect immunofluorescence techniques with the use of mouse monoclonal antibodies (MAb). In some cases, GLC were also positive for HLA-DQ and-DP antigen expression. Neither granulosa nor theca interna cells in large antral follicles of the same ovaries showed any detectable expression of MHC class II antigens. Moreover, theca-lutein (paralutein) cells, identified by their reactivity with specific human autoantibodies in 5 of the 7 human CL examined, were also negative. Similarly, GLC, but not paralutein cells, in rhesus monkey CL showed significant cross-reactivity with anti-HLA-DR MAb. In contrast, lutein cells in ovaries from either cycling or 7-day-pregnant rats were negative for MHC class II (Ia) antigen expression. Expression of MHC class II antigens by human granulosa cells after their luteal transformation confirms the normal inducibility of certain human steroidogenic cells at the time of their further functional differentiation and enhanced biosynthetic activity, and suggests that these molecules, may have additional functions beyond serving as restriction elements in the immune response.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

MHC :

major histocompatibility complex

HLA :

human leukocyte antigen

ACTH :

adrenocorticotropic hormone

S-D :

Sprague-Dawley

Mab :

monoclonal antibody (ies)

CL :

corpus luteum (corpora lutea)

IF :

immunofluorescence

FITC :

fluorescein isothiocyanate

TRITC :

tetramethylrhodamine isothiocyanate

PBS :

phosphate-buffered saline

GLC :

granulosa-lutein cells

TLC :

theca-lutein or paralutein cells

Ia :

murine MHC class II

TNFα:

tumor necrosis factor alpha

LH :

luteotropin hormone

PG :

prostaglandin

References

  • Auletta FJ, Flint APF (1988) Mechanisms controlling corpus luteum function in sheep, cows, nonhuman primates, and women especially in relation to the time of luteolysis. Endocr Rev 9:88–105

    Google Scholar 

  • Bagavandoss P, Kunkel SL, Wiggins RC, Keyes PL (1988) Tumor necrosis factor-a (TNF-a) production and localization of macrophages and T lymphocytes in rabbit corpus luteum. Endocrinology 122: 1185–1187

    Google Scholar 

  • Barclay AN (1981) The localization of populations of lymphocytes defined by monoclonal antibodies in rat lymphoid tissues. Immunology 42: 593–600

    Google Scholar 

  • Beverley PCL (1980) Production and use of monoclonal antibodies in transplantation and immunology. In: Touraine JL, Traeger J, Betuel H, Brochier J, Dubernard JM, Revillard JP, Train R (eds) Transplantation and clinical immunology, XI. Excerpta Medica, Amsterdam, pp 87–94

    Google Scholar 

  • Breard J, Reinherz EL, Kung PC, Goldstein G, Schlossman SF (1980) A monoclonal antibody reactive with human peripheral blood monocytes. J Immunol 124: 1301–1307

    Google Scholar 

  • Brodsky F (1984) A matrix approach to human class II histocom-patibility antigens: reactions of four monoclonal antibodies with the products of nine haplotypes. Immunogenetics 19: 179–194

    Google Scholar 

  • Bulmer JN, Earl U (1987) The expression of class II MHC gene products by Fallopian tube epithelium in pregnancy and throughout the menstrual cycle. Immunology 61: 207–213

    Google Scholar 

  • Buscema M, Todd I, Deuss U, Hammond L, Mirakian R, Pujol-Borrell R, Bottazzo GF (1989) Influence of tumor necrosis factor-α on the modulation by interferon-γ of HLA class II molecules in human thyroid cells and its effect on interferon-γ binding. J Clin Endocrinol Metab 69: 433–439

    Google Scholar 

  • Charron DJ, McDevitt HL (1979) Analysis of HLA-D regionassociated molecules with monoclonal antibody. Proc Natl Acad Sci USA 76: 6567–6571

    Google Scholar 

  • Claas FHJ, van Ree JM, Verhoeven WMA, van der Poel JJ, Verduyn W, de Wied D, van Rood JJ (1986) The interaction between γ-type endorphins and HLA class I antigens. Human Immunol 15: 347–356

    Google Scholar 

  • Collins T, Pober JS, Strominger JL (1986) Physiologic reaction of class II major histocompatibility complex gene expression. In: Solheim BG, Møller E, Ferrone S (eds) HLA class II antigens. Springer, Berlin Heidelberg New York, pp 14–31

    Google Scholar 

  • Corner GW Jr (1956) The histological dating of the human corpus luteum of menstruation. Am J Anat 98: 377–401

    Google Scholar 

  • Daar AS, Fuggle SV, Fabre JW, Ting A, Morris PJ (1984) The detailed distribution of MHC class II antigens in normal human organs. Transplantation 38: 293–298

    Google Scholar 

  • De Meyts P, Hallez S, Gur JL, Merchez M, Economidis I, Rousseau GG, van Snick J, Spinel C, Squifflet JP, Ravoet AM, de Bruyère M, Willard K, Vessière F, Lemoine C, Boon T, Toyoda H, Chen F, Shively J (1986) Aberrant expression of HLA-DR determinants on human thyroid cells treated with phytohemagglutinin and gamma-interferon and on human melanoma cells. In: Schwartz RS, Rose NR (eds) Autoimmunity: experimental and clinical aspects. New York Academy of Sciences, New York, pp 359–360

    Google Scholar 

  • Dimitriu-Bona A, Burmester GR, Waters SJ, Winchester RJ (1983) Human mononuclear phagocyte differentiation antigens. I. Patterns of antigenic expression on the surface of human monocytes and macrophages defined by monoclonal antibodies. J Immunol 130: 145–152

    Google Scholar 

  • Dohr GA, Motte W, Leitinger S, Desoye G, Urdl W, Winter R, Wilders-Truschnig MM, Uchanska-Ziegler B, Ziegler A (1987) Lack of expression of histocompatibility leukocyte antigen class II and class II molecules on the human oocyte. J Immunol 138: 3766–3770

    Google Scholar 

  • Due C, Simonsen M, Olsson L (1986) The major histocompatibility complex class I heavy chain as a structural subunit of the human cell membrane insulin receptor: implications for the range of biological functions of histocompatibility antigens. Proc Natl Acad Sci USA 83: 6007–6011

    Google Scholar 

  • Edidin M (1983) MHC antigens and non-immune functions. Immunology Today 4: 269–270

    Google Scholar 

  • Folkman J, Klagsbrun M (1987) A family of angiogenic peptides. Nature 329: 671–672

    Google Scholar 

  • Gillim SW, Christensen AK, McLennan CE (1969) Fine structure of the human menstrual corpus luteum at its stage of maximum secretory activity. Am J Anat 126: 409–428

    Google Scholar 

  • Hill JA, Anderson DJ (1988) Enhancement of class I and induction of class II major histocompatibility complex (MHC) antigens in human granulosa cells (GC) by gamma interferon (G-IFN). 35th Annual Meeting, Society for Gynecologic Investigation, Baltimore, MD, Abst #78

  • Hornsby PJ (1985) The regulation of adrenocortical function by control of growth and structure. In: Anderson DL, Winter JSD (eds) Adrenal Cortex. Butterworths, Boston London, pp 1–31

    Google Scholar 

  • Hsueh AJW, Adashi EY, Jones PBC, Welsh TH (1984) Hormonal regulation of the differentiation of cultured ovarian granulosa cells. Endocrinol Rev 5: 76–127

    Google Scholar 

  • Keyes PL, Gadsby JE, Yuh K-CM, Bill CH (1983) The corpus luteum. In: Greep RO (ed) Reproductive Physiology IV. Int Rev Physiol 27: 57–97

  • Khoury EL, Greenspan JS, Greenspan FS (1987) Adrenocortical cells of the zona reticularis normally express HLA-DR antigenic determinants. Am J Pathol 127: 580–591

    Google Scholar 

  • Khoury EL, Berline JW (1988) HLA-DR expression by adrenocortical cells of the zona reticularis: structural and allotypic characterization. Tissue Antigens 31: 191–203

    Google Scholar 

  • Klareskog L, Forsum U, Peterson PA (1980) Hormonal regulation of the expression of Ia antigens on mammary gland epithelium. Eur J Immunol 10: 958–963

    Google Scholar 

  • Klareskog L, Forsum U (1986) Tissue distribution of class II transplantation antigens: presence on normal cells. In: Solheim BG, Møller E, Ferrone S (eds) HLA Class II Antigens: A Comprehensive Review of Structure and Function. Springer, Berlin Heidelberg New York, pp 339–355

    Google Scholar 

  • Lampson LA, Levy R (1980) Two populations of Ia-like molecules on a human B cell line. J Immunol 125: 293–299

    Google Scholar 

  • Lo D, Burkly LC, Widera G, Cowing C, Flavell RA, Palmiter RD, Brinster RL (1988) Diabetes and tolerance in transgenic mice expressing class II MHC molecules in pancreatic beta cells. Cell 53: 159–168

    Google Scholar 

  • Neville AM, O'Hare MJ (1982) The Human Adrenal Cortex Pathology and Biology—An Integrated Approach. Springer, Berlin Heidelberg New York, p 30

    Google Scholar 

  • Newman RA, Ormerod MG, Greaves MF (1980) The presence of HLA-DR antigens on lactating human breast epithelium and milk fat globule membranes. Clin Exp Immunol 41: 478–486

    Google Scholar 

  • Orentreich N, Brind JL, Rizer RL, Vogelman JH (1984) Age changes and sex differences in serum dehydroepiandrosterone sulfate concentrations throughout adulthood. J Clin Endocrinol Metab 59: 551–555

    Google Scholar 

  • Pepe GJ, Rothchild I (1974) A comparative study of serum progesterone levels in pregnancy and in various types of pseudopregnancy in the rat. Endocrinology 95: 275–279

    Google Scholar 

  • Pfizenmaier K, Scheurich P, Schlüter C, Krönke M (1987) Tumor necrosis factor enhances HLA-A,B,C and HLA-DR gene expression in human tumor cells. J Immunol 138: 975–980

    Google Scholar 

  • Phillips ML, Moule ML, Delovitch TL, Yip CC (1986) Class I histocompatibility antigens and insulin receptors: evidence for interactions. Proc Natl Acad Sci USA 83: 3474–3478

    Google Scholar 

  • Pujol-Borrell R, Todd I, Doshi M, Bottazzo GF, Sutton R, Gray D, Adolf GR, Feldmann M (1987) HLA class II induction in human islet cells by interferon-γ plus tumour necrosis factor or lymphotoxin. Nature 326: 304–306

    Google Scholar 

  • Sarvetnick N, Liggitt D, Pitts SL, Hansen SE, Stewart TA (1988) Insulin-dependent diabetes mellitus induced in transgenic mice by ectopic expression of class II MHC and interferon-gamma. Cell 52: 773–782

    Google Scholar 

  • Schreiber AB, Schlessinger J, Edidin M (1984) Interaction between major histocompatibility complex antigens and epidermal growth factor receptors on human cells. J Cell Biol 98: 725–731

    Google Scholar 

  • Simonsen M, Olsson L (1983) Possible roles of compound membrane receptors in the immune system. Ann Immunol (Institut Pasteur) 134D: 85–92

    Google Scholar 

  • Simonsen M, Skjodt K, Crone M, Sanderson A, Fujita-Yamaguchi Y, Due C, Rønne E, Linnet K, Olsson L (1985) Compound receptors in the cell membrane: ruminations from the borderland of immunology and physiology. Prog Allergy 36: 151–176

    Google Scholar 

  • Solano AR, Sanchez ML, Sardañons ML, Dada L, Podesta EJ (1988) Luteinizing hormone triggers a molecular association between its receptors and the major histocompatibility complex class I antigen to produce cell activation. Endocrinology 122: 2080–2083

    Google Scholar 

  • Solano AR, Cremaschi G, Sanchez ML, Borda E, Sterin-Borda L, Podesta EJ (1988) Molecular and biological interaction between major histocompatibility complex class I antigens and luteinizing hormone receptors or β-adrenergic receptors triggers cellular response in mice. Proc Natl Acad Sci USA 85: 5087–5091

    Google Scholar 

  • Sotsiou F, Bottazzo GF, Doniach D (1980) Immunofluorescence studies on autoantibodies to steroid-producing cells, and to germline cells in endocrine disease and infertility. Clin Exp Immunol 39: 97–111

    Google Scholar 

  • Unanue ER, Allen PM (1986) Comment on the finding of Ia expression in nonlymphoid cells. Lab Invest 55: 123–125

    Google Scholar 

  • Watson AJ, DeMars R, Trowbridge IS, Bach FH (1983) Detection of a novel human class II HLA antigen. Nature 304: 358–361

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Khoury, E.L., Marshall, L.A. Luteinization of human granulosa cells in vivo is associated with expression of MHC Class II antigens. Cell Tissue Res 262, 217–224 (1990). https://doi.org/10.1007/BF00309876

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00309876

Key words

Navigation