Progesterone effects on lymphocytes may be mediated by membrane progesterone receptors

Journal of Reproductive Immunology

Volumn 95, Issue 1-2, 2012, Pages 15-26

  Ndiaye, Kalidou ^a,b   Poole, Daniel H ^a,b   Walusimbi, Sadhat ^b   Cannon, Matthew J ^a   Toyokawa, Koji ^b   Maalouf, Samar W ^b   Dong, Jing ^c   Thomas, Peter ^c   Pate, Joy L ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Corpus luteum; Lymphocytes; MPR; PGRMC1; Progesterone

Indexed keywords

CALCIUM ION; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; MESSENGER RNA; PROGESTERONE; PROGESTERONE RECEPTOR; PROTEIN KINASE ZAP 70;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BINDING COMPETITION; CALCIUM CELL LEVEL; CONTROLLED STUDY; CORPUS LUTEUM; COW; ENZYME PHOSPHORYLATION; FEMALE; HORMONE ACTION; LYMPHOCYTE; LYMPHOCYTE MEMBRANE; MONOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; RNA ANALYSIS; T LYMPHOCYTE;

ANIMALS; CATTLE; CELL MEMBRANE; CORPUS LUTEUM; FEMALE; GENE EXPRESSION REGULATION; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; PROGESTERONE; RECEPTORS, PROGESTERONE; RNA, MESSENGER; T-LYMPHOCYTES;

EID: 84865542939     PISSN: 01650378     EISSN: 18727603     Source Type: Journal    
DOI: 10.1016/j.jri.2012.04.004     Document Type: Article

References (48)

1. Abraham R.T., Weiss A. Jurkat T cells and development of the T-cell receptor signaling paradigm. Nat. Rev. Immunol. 2004, 4:301-308.
2. Ashley R.L., Clay C.M., Farmerie T.A., Niswender G.D., Nett T.M. Cloning and characterization of an ovine intracellular seven transmembrane receptor for progesterone that mediates calcium mobilization. Endocrinology 2006, 147:4151-4159.
3. Bartis D., Boldizsár F., Szabó M., Pálinkás L., Németh P., Berki T. Dexamethasone induces rapid tyrosine-phosphorylation of ZAP-70 in Jurkat cells. J. Steroid Biochem. Mol. Biol. 2006, 98:147-154.
4. Cai Z., Stocco C. Expression and regulation of progestin membrane receptors in the rat corpus luteum. Endocrinology 2005, 146:5522-5532.
5. Cannon M.J., Petroff M.G., Pate J.L. Effects of prostaglandin F2alpha and progesterone on the ability of bovine luteal cells to stimulate T lymphocyte proliferation. Biol. Reprod. 2003, 69:695-700.
6. Chien E.J., Chang C.-P., Lee W.-F., Su T.-H., Wu C.-H. Nongenomic immunosuppressive actions of progesterone inhibits PHA-induced alkalinization and activation in T cells. J. Cell. Biochem. 2006, 99:292-304.
7. Chien C.H., Lai J.N., Liao C.F., Wang O.Y., Lu L.M., Huang M.I., Lee W.F., Shie M.C., Chien E.J. Mifepristone acts as progesterone antagonist of nongenomic responses but inhibits phytohemagglutinin-induced proliferation in human T cells. Hum. Reprod. 2009, 1:1-8.
8. Chitko-McKown C.G., Ruef B.J., Rice-Ficht A.C., Brown W.C. Interleukin-10 downregulates proliferation and expression of interleukin-2 receptor p55 chain and interferon-gamma, but not interleukin-2 or interleukin-4, by parasite-specific helper T cell clones obtained from cattle chronically infected with Babesia bovis or Fasciola hepatica. J. Interferon Cytokine Res. 1995, 15:915-922.
9. Diaz F.J., Wiltbank M.C. Acquisition of luteolytic capacity: changes in prostaglandin F2alpha regulation of steroid hormone receptors and estradiol biosynthesis in pig corpora lutea. Biol. Reprod. 2004, 70:1333-1339.
10. Dosiou C., Hamilton A.E., Pang Y., Overgaard M.T., Tulac S., Dong J., Thomas P., Giudice L.C. Expression of membrane progesterone receptors on human T lymphocytes and Jurkat cells and activation of G-proteins by progesterone. J. Endocrinol. 2008, 196:67-77.
11. Dressing G., Pang Y., Dong J., Thomas P. Progestin signaling through mPRα in Atlantic croaker granulosa/theca cell co-cultures and its involvement in progestin inhibition of apoptosis. Endocrinology 2010, 151:5914-5928.
12. 2+ signaling, and gene expression in T lymphocytes. J. Exp. Med. 1998, 188:1593-1602.
13. Falkenstein E., Meyer C., Eisen C., Sciba P.C., Wehling M. Full-length cDNA sequence of progesterone membrane-binding protein from porcine vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 1996, 229:86-89.
14. Gaffen S.L. Signaling domains of the interleukin 2 receptor. Cytokine 2001, 14:63-77.
15. Hafs H.D., Armstrong D.T. Corpus luteum growth and progesterone synthesis during the bovine estrous cycle. J. Anim. Sci. 1968, 27:134-141.
16. Hanna R., Pang Y., Thomas P., Zhu Y. Cell-surface expression, progestin binding, and rapid nongenomic signaling of zebrafish membrane progestin receptors alpha and beta in transfected cells. J. Endocrinol. 2006, 190:247-260.
17. Haukkamaa M. High affinity progesterone binding sites of human uterine microsomal membranes. J. Steroid Biochem. 1984, 20:569-573.
18. Herrera L.A., Montero R., Leon-Cazares J.M., Rojas E., Gonsebatt M.E., Ostrosky-Wegman P. Effects of progesterone and estradiol on the proliferation of phytohemagglutinin-stimulated human lymphocytes. Mutat. Res. 1992, 270:211-218.
19. Karteris E., Zervou S., Pang Y., Dong J., Hillhouse E.W., Randeva H.S., Thomas P. Progesterone signaling in human myometrium through two novel membrane G protein-coupled receptors: potential role in functional progesterone withdrawal at term. Mol. Endocrinol. 2006, 20:1519-1534.
20. Kelder J., Azevedo R., Pang Y., de Vlieg J., Dong J., Thomas P. Comparison between steroid binding to membrane progesterone receptor alpha (mPRalpha) and to nuclear progesterone receptor: correlation with physicochemical properties assessed by comparative molecular field analysis and identification of mPRalpha-specific agonists. Steroids 2010, 75:314-322.
21. Krebs C.J., Jarvis E.D., Chan J., Lydon J.P., Ogawa S., Pfaff D.W. A membrane-associated progesterone-binding protein, 25-Dx, is regulated by progesterone in brain regions involved in female reproductive behaviors. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:12816-12821.
22. Krietsch T., Fernandes M.S., Kero J., Losel R., Heyens M., Lam E.W., Huhtaniemi I., Brosens J.J., Gellersen B. Human homologs of the putative G protein-coupled membrane progestin receptors (mPRalpha, beta, and gamma) localize to the endoplasmic reticulum and are not activated by progesterone. Mol. Endocrinol. 2006, 20:3146-3164.
23. Low B.G., Hansen P.J. Actions of steroids and prostaglandins secreted by the placenta and uterus of the cow and ewe on lymphocyte proliferation in vitro. Am. J. Reprod. Immunol. Microbiol. 1988, 18:71-75.
24. McEwen B.S. Non-genomic and genomic effects of steroids on neural activity. Trends Pharmacol. Sci. 1991, 12:141-147.
25. Meizel S., Turner K.O. Progesterone acts at the plasma membrane of human sperm. Mol. Cell. Endocrinol. 1991, 77:R1-R5.
26. Monterroso V.H., Hansen P.J. Regulation of bovine and ovine lymphocyte proliferation by progesterone: modulation by steroid receptor antagonists and physiological status. Acta Endocrinol. 1993, 129:532-535.
27. Morris T.R. Experimental Design and Analysis in Animal Sciences 1999, CABI Publishing, New York.
28. Ndiaye K., Poole D.H., Pate J.L. Expression and regulation of functional oxytocin receptors in bovine T lymphocytes. Biol. Reprod. 2008, 78:786-793.
29. Nelson B.H., Willerford D.M. Biology of the interleukin-2 receptor. Adv. Immunol. 1998, 70:1-81.
30. Pate J.L. Regulation of prostaglandin synthesis by progesterone in the bovine corpus luteum. Prostaglandins 1988, 36:303-315.
31. Peluso J.J., Fernandez G., Pappalardo A., White B.A. Membrane-initiated events account for progesterone's ability to regulate intracellular free calcium levels and inhibit rat granulosa cell mitosis. Biol. Reprod. 2002, 67:379-385.
32. Peluso J.J., Pappalardo A., Losel R., Wehling M. Expression and function of PAIRBP1 within gonadotropin-primed immature rat ovaries: PAIRBP1 regulation of granulosa and luteal cell viability. Biol. Reprod. 2005, 73:261-270.
33. Petroff M., Coggeshall K.M., Jones L.S., Pate J.L. Bovine luteal cells elicit major histocompatibility complex class II-dependent T-cell proliferation. Biol. Reprod. 1997, 57:887-893.
34. Poole D.H., Pate J.L. Luteal microenvironment directs resident T lymphocyte function in cows. Biol. Reprod. 2012, 86:29.
35. Rueda B., Hendry I.R., Hendry W.J., Stormshak F., Slayden O.D. Decreased progesterone levels and progesterone receptor antagonists promote apoptotic cell death in bovine luteal cells. Biol. Reprod. 2000, 62:269-276.
36. Schumacher M., Coirini H., Pfaff D.W., McEwen B.S. Behavioral effects of progesterone associated with rapid modulation of oxytocin receptors. Science 1990, 250:691-694.
37. Smith J.L., Kupchak B.R., Garitaonandia I., Haong L.K., Maina A.S., Regall L.M., Lyons L.K. Heterologous expression of human mPRα, mPRβ and mPRγ in yeast confirms their ability to function as membrane progesterone receptors. Steroids 2008, 73:1160-1173.
38. Sokal R.R., Rohlf F.J. Biometry: The Principles and Practice of Statistics in Biological Research 1969, W. H. Freeman and Co, New York, pp. 157-161.
39. Stites D.P., Bugbee S., Siiteri P.K. Differential actions of progesterone and cortisol on lymphocyte and monocyte interaction during lymphocyte activation-relevance to immunosuppression in pregnancy. J. Reprod. Immunol. 1983, 5:215-228.
40. Stouffer R.L. Progesterone as a mediator of gonadotrophin action in the corpus luteum: beyond steroidogenesis. Hum. Reprod. Update 2003, 9:99-117.
41. Thomas P., Pang Y., Don J., Groenen P., Kelder J., de Vlieg J., Zhu Y., Tubbs C. Steroid and G protein binding characteristics of the seatrout and human progestin and membrane receptor alpha subtypes and their evolutionary origins. Endocrinology 2007, 148:705-718.
42. Tian J., Kim S., Heilig E., Ruderman J.V. Identification of XPR-1, a progesterone receptor required for Xenopus oocyte activation. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:14358-14363.
43. Van Voorhis B.J., Anderson D.J., Hill J.A. The effects of RU486 on immune function and steroid-induced immunosuppression in vitro. J. Clin. Endocrinol. Metab. 1989, 69:1195-1199.
44. Von Laethem F., Baus E., Smyth L.A., Andris F., Bex F., Urbain J., Kioussis D., Leo O. Glucocorticoids attenuate T cell receptor signaling. J. Exp. Med. 2001, 193:803-814.
45. Williams B.L., Irvin B.J., Sutor S.L., Chini C.C.S., Yacyshyn E., Wardenburg J.B., Dalton M., Chan A.C., Abraham R.T. Phosphorylation of Tyr319 in ZAP-70 is required for T-cell antigen receptor-dependent phospholipase C-g1 and Ras activation. EMBO J. 1999, 18:1832-1844.
46. Zhang W., Sloan-Lancaster J., Kitchen J., Trible R.P., Samelson L.E. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 1998, 92:83-92.
47. Zhu Y., Rice C.D., Pang Y., Pace M., Thomas P. Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:2231-2236.
48. Zhu Y., Bond J., Thomas P. Identification, classification, and partial characterization of genes in humans and other vertebrates homologous to a fish membrane progestin receptor. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:2237-2242.