Conditional ablation of progesterone receptor membrane component 1 results in subfertility in the female and development of endometrial cysts

Endocrinology

Volumn 157, Issue 9, 2016, Pages 3309-3319

  Mccallum, Melissa L ^a   Pru, Cindy A ^a   Niikura, Yuichi ^a   Yee, Siu Pok ^b   Lydon, John P ^c   Peluso, John J ^b   Pru, James K ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; CRE RECOMBINASE; ESTROGEN RECEPTOR; GONADOTROPIN; MESSENGER RNA; PROGESTERONE RECEPTOR; PROGESTERONE RECEPTOR MEMBRANE COMPONENT 1; UNCLASSIFIED DRUG; ESTROGEN RECEPTOR ALPHA; MEMBRANE PROTEIN; PGRMC1 PROTEIN, MOUSE;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CONTROLLED STUDY; CYST; ENDOMETRIAL DISEASE; EXON; FEMALE; FEMALE SUBFERTILITY; FERTILITY; GENOTYPE; LOXP SITE; MOUSE; NONHUMAN; OOCYTE; PHENOTYPE; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUPEROVULATION; ANIMAL; C57BL MOUSE; CYSTS; ENDOMETRIUM; GENE SILENCING; METABOLISM; PHYSIOLOGY; RANDOMIZATION;

ANIMALS; CYSTS; ENDOMETRIUM; ESTROGEN RECEPTOR ALPHA; FEMALE; FERTILITY; GENE SILENCING; MEMBRANE PROTEINS; MICE, INBRED C57BL; RANDOM ALLOCATION; RECEPTORS, PROGESTERONE;

EID: 84985991099     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2016-1081     Document Type: Article

References (67)

1. Szekeres-Bartho J, Barakonyi A, Par G, Polgar B, Palkovics T, Sz-ereday L. Progesterone as an immunomodulatory molecule. Int Im- munopharmacol. 2001;1:1037-1048.
2. Burney RO, Talbi S, Hamilton AE, et al. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology. 2007;148:3814-3826.
3. Boruban MC, Altundag K, Kilic GS, Blankstein J. From endometrial hyperplasia to endometrial cancer: insight into the biology and possible medical preventive measures. Eur J Cancer Prev. 2008;17:133-138.
4. Wu Y, Strawn E, Basir Z, Halverson G, Guo SW. Promoter hyper- methylation of progesterone receptor isoform B (PR-B) in endometriosis. Epigenetics. 2006;1:106-111.
5. Salazar EL, Calzada L. The role of progesterone in endometrial es- Tradiol- And progesterone-receptor synthesis in women with menstrual disorders and habitual abortion. Gynecol Endocrinol. 2007; 23:222-225.
6. Ismail PM, Amato P, Soyal SM, et al. Progesterone involvement in breast development and tumorigenesis- As revealed by progesterone receptor "knockout" and "knockin" mouse models. Steroids. 2003; 68:779-787.
7. Ehn NL, Cooper ME, Orr K, et al. Evaluation of fetal and maternal genetic variation in the progesterone receptor gene for contributions to preterm birth. Pediatr Res. 2007;62:630-635.
8. Pan H, Deng Y, Pollard JW. Progesterone blocks estrogen-induced DNA synthesis through the inhibition of replication licensing. Proc Natl Acad Sci USA. 2006;103:14021-14026.
9. Vasquez YM, DeMayo FJ. Role of nuclear receptors in blastocyst implantation. Semin Cell Dev Biol. 2013;24:724-735.
10. Wetendorf M, DeMayo, FJ. The progesterone receptor regulates implantation, decidualization, and glandular development via a complex paracrine signaling network. Mol Cell Endocrinol. 2012;357: 108-118.
11. Peluso JJ, Pru JK. Non-canonical progesterone signaling in granulosa cell function. Reproduction. 2014;147:R169-R178.
12. Rothchild I. The corpus luteum revisited: Are the paradoxical effects of RU486 a clue to how progesterone stimulates its own secretion? Biol Reprod. 1996;55:1-4.
13. Stouffer RL, Bishop CV, Bogan RL, Xu F. Hennebold JD. Endocrine and local control of the primate corpus luteum. Reprod Biol. 2013; 13:259-271.
14. Viero C, Mechaly I, Aptel H. Rapid inhibition of Ca2+ influx by neurosteroids in murine embryonic sensory neurones. Cell Calcium. 2006;40:383-391.
15. Barbagallo M, Dominguez LJ, Licata G, et al. Vascular effects of progesterone: role of cellular calcium regulation. Hypertension. 2001;37:142-147.
16. Head GM, DowningJE, Brucker C, Mentlein R, Kendall MD. Rapid progesterone actions on thymulin-secreting epithelial cells cultured from rat thymus. Neuroimmunomodulation. 1999;6:31-38.
17. Finidori-Lepicard J, Schorderet-Slatkine S, Hanoune J, Baulieu EE. Progesterone inhibits membrane-bound adenylate cyclase in Xeno- pus laevis oocytes. Nature. 1981;292:255-257.
18. Foresta C, Rossato M, Di Virgilio, F. Ion fluxes through the progesterone- Activated channel of the sperm plasma membrane. Biochem J. 1993;294:279-283.
19. Losel R, Dorn-Beineke A, Falkenstein E, Wehling M, Feuring M. Porcine spermatozoa contain more than one membrane progesterone receptor. Int J Biochem Cell Biol. 2004;36:1532-1541.
20. Frye CA, Sumida K, Lydon JP, O'Malley BW, Pfaff DW. Mid- Aged and aged wild-type and progestin receptor knockout (PRKO) mice demonstrate rapid progesterone and 3a, 5a-THP-facilitated lordosis. Psychopharmacology. 2006;185:423-432.
21. Ehring GR, Kerschbaum HH, Eder C, et al. A nongenomic mechanism for progesterone-mediated immunosuppression: inhibition of K+ channels, Ca2+ signaling, and gene expression in T lymphocytes. J Exp Med. 1998;188:1593-1602.
22. Peluso JJ, DeCerbo J, Lodde V. Evidence for a genomic mechanism of action for progesterone receptor membrane component-1. Steroids. 2012;77:1007-1012.
23. Peluso JJ, Lodde V, Liu X. Progesterone regulation of progesterone receptor membrane component 1 (PGRMC1) sumoylation and transcriptional activity in spontaneously immortalized granulosa cells. Endocrinology. 2012;153:3929-3939.
24. Kaluka D, Batabyal D, Chiang BY, Poulos TL, Yeh SR. Spectroscopic and mutagenesis studies of human PGRMC1. Biochemistry. 2015;54:1638-1647.
25. Peluso JJ, Liu X, Gawkowska A, Johnston-MacAnanny E. Progesterone activates a progesterone receptor membrane component 1-dependent mechanism that promotes human granulosa/luteal cell survival but not progesterone secretion. J Clin Endocrinol Metab. 2009;94:2644-2649.
26. Peluso JJ. Progesterone signaling mediated through progesterone receptor membrane component-1 in ovarian cells with special emphasis on ovarian cancer. Steroids. 2011;76:903-909.
27. Peluso JJ. Progesterone receptor membrane component 1 and its role in ovarian follicle growth. Front Neurosci. 2013;7:99.
28. Peluso JJ, Gawkowska A, Liu X, Shioda T, Pru JK. Progesterone receptor membrane component-1 regulates the development and Cisplatin sensitivity of human ovarian tumors in athymic nude mice. Endocrinology. 2009;150:4846-4854.
29. Friel AM, Zhang L, Pru CA, et al. Progesterone receptor membrane component 1 deficiency attenuates growth while promoting chemo- sensitivity of human endometrial xenograft tumors. Cancer Lett. 2015;356:434-442.
30. Cahill MA. Progesterone receptor membrane component 1: An in- Tegrative review. J Steroid Biochem Mol Biol. 2007;105:16-36.
31. Losel RM, Besong D, Peluso JJ, Wehling M. Progesterone receptor membrane component 1-many tasks for a versatile protein. Steroids. 2008;73:929-934.
32. Keator CS, Mah K, Slayden OD. Alterations in progesterone receptor membrane component 2 (PGRMC2) in the endometrium of macaques afflicted with advanced endometriosis. Mol Hum Reprod. 2012;18:308-319.
33. Chen JI, Hannan NJ, Mak Y, et al. Proteomic characterization of midproliferative and midsecretory human endometrium. J Pro- Teome Res. 2009;8:2032-2044.
34. Ace CI, Okulicz WC. Microarray profiling of progesterone-regulated endometrial genes during the rhesus monkey secretory phase. Reprod Biol Endocrionol. 2004;2:54.
35. Zhang L, Kanda Y, Roberts DJ, et al. Expression of progesterone receptor membrane component 1 and its partner serpine 1 mRNA binding protein in uterine and placental tissues of the mouse and human. Mol Cell Endocrinol. 2008;287:81-89.
36. Pru JK, Clark NC. PGRMC1 and PGRMC2 in uterine physiology and disease. Front Neurosci. 2013;19:168.
37. Feng L, Antczak BC, Lan L, et al. Progesterone receptor membrane component 1 (PGRMC1) expression in fetal membranes among women with preterm premature rupture of the membranes (PPROM). Placenta. 2014;35:331-333.
38. Bunch K, Tinnemore D, HuffS, Hoffer ZS, Burney RO, Stallings JD. Expression patterns of progesterone receptor membrane components 1 and 2 in endometria from women with and without endometriosis. Reprod Sci. 2014;21:191-197.
39. Garrido-Gomez T, Quinonero A, Antunez O, et al. Deciphering the proteomic signature of human endometrial receptivity. Hum Reprod. 2014;29:1957-1967.
40. Lee EC, Yu D, Martinez de Velasco J, et al. A highly efficient Esch- erichia coli-based chromosome engineering system adapted for re- combinogenic targeting and subcloning of BAC DNA. Genomics. 2001;73:56-65.
41. Soyal SM, Mukherjee A, Lee KY, et al. Cre-mediated recombination in cell lineages that express the progesterone receptor. Genesis. 2005;41:58-66.
42. Jamin SP, Arango NA, Mishina Y, Hanks MC, Behringer RR. Requirement of Bmpr1a for Mullerian duct regression during male sexual development. Nat Genet. 2002;32:408-410.
43. Kashiwagi A, DiGirolamo CM, Kanda Y, et al. The postimplanta- Tion embryo differentially regulates endometrial gene expression and decidualization. Endocrinology. 2007;148:4173-4184.
44. Lydon JP, DeMayo FJ, Funk CR, et al. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev. 1995;9:2266-2278.
45. Peluso JJ. Multiplicity of progesterone's actions and receptors in the mammalian ovary. Biol Reprod. 2006;75:2-8.
46. Peluso JJ. Non-genomic actions of progesterone in the normal and neoplastic mammalian ovary. Semin Reprod. 2007;25:198-207.
47. Peluso JJ, Pappalardo A, Losel R, Wehling M. Progesterone membrane receptor component 1 expression in the immature rat ovary and its role in mediating progesterone's antiapoptotic action. Endocrinology. 2006;147:3133-3140.
48. Tang YT, Hu T, Arterburn M, et al. PAQR proteins: A novel membrane receptor family defined by an ancient 7-transmembrane pass motif. J Mol Evol. 2005;61:372-380.
49. Thomas P. Characteristics of membrane progestin receptor a (mPRa) and progesterone membrane receptor component 1 (PGRMC1) and their roles in mediating rapid progestin actions. Front Neuroendocrinol. 2008;29:292-312.
50. Thomas P, Pang Y. Membrane progesterone receptors: evidence for neuroprotective, neurosteroid signaling and neuroendocrine functions in neuronal cells. Neuroendocrinology. 2012;96:162-171.
51. 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 USA. 2003;100:2237-2242.
52. Karteris E, Zervou S, Pang Y, et al. 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.
53. Krietsch T, Fernandes MS, Kero J, et al. Human homologs of the putative G protein-coupled membrane progestin receptors (mPRa, 7) localize to the endoplasmic reticulum and are not activated by progesterone. Mol Endocrinol. 2006;20:2146-3164.
54. Fernandes MS, Brosens JJ, Gellersen B. Honey, we need to talk about the membrane progestin receptors. Steroids. 2008;73:942-952.
55. Falkenstein E, Meyer C, Eisen C, Scriba PC, Wehling M. Full-length cDNA sequence of progesterone membrane-binding protein from porcine vascular smooth muscle cells. Biochem Biophys Res Com- mun. 1996;229:86-89.
56. Meyer C, Schmid R, Scriba PC, Wehling M. Purification and partial sequencing of high- Affinity progesterone-binding site(s) from porcine liver membranes. Eur J Biochem. 1996;239:726-731.
57. Gerdes D, Wehling M, Leube B, Falkenstein E. Cloning and tissue expression of two putative steroid membrane receptors. Biol Chem. 1998;379:907-911.
58. Dey S, Chamero P, Pru JK, et al. Cyclic regulation of sensory perception by a female hormone alters behavior. Cell.2015;161:1334-1344.
59. Thomas P, Pang Y, Dong J. Enhancement of cell surface expression and receptor functions of membrane progestin receptor a (mPRa) by progesterone receptor membrane component 1 (PGRMC1): evidence for a role of PGRMC1 as an adaptor protein for steroid receptors. Endocrinology. 2014;155:1107-1119.
60. Sueldo C, Liu X, Peluso JJ. Progestin and AdipoQ receptor 7, progesterone membrane receptor component 1 (PGRMC1), and PGRMC2 and their role in regulating progesterone's ability to suppress human granulosa/luteal cells from entering into the cell cycle. Biol Reprod. 2015;93:1-11.
61. Peluso JJ, Romak J, Liu X. Progesterone receptor membrane component-1 (PGRMC1) is the mediator of progesterone's antiapoptotic action in spontaneously immortalized granulosa cells as revealed by PGRMC1 small interfering ribonucleic acid treatment and functional analysis of PGRMC1 mutations. Endocrinology. 2008; 149:534-543.
62. Hampton KK, Craven RJ. Pathways driving the endocytosis of mutant and wild-type EGFR in cancer. Oncoscience. 2014;1:504-512.
63. Ahmed IS, Rohe HJ, Twist KE, Craven RJ. Pgrmc1 (progesterone receptor membrane component 1) associates with epidermal growth factor receptor and regulates erlotinib sensitivity. J Biol Chem. 2010;285:24775-24782.
64. Large MJ, Wetendorf M, Lanz RB, et al. The epidermal growth factor receptor critically regulates endometrial function during early pregnancy. PLoS Genet. 2014;10:e1004451.
65. Peluso JJ, Griffin D, Liu X, Horne M. Progesterone receptor membrane component-1 (PGRMC1) and PGRMC2 interact to suppress entry into the cell cycle in spontaneously immortalized rat granulosa cells. Biol Reprod. 2014;91:104.
66. Griffin D, Liu X, Pru C, Pru JK, Peluso JJ. Expression of progesterone receptor membrane component-2 within the immature rate ovary and its role in regulating mitosis and apoptosis of spontaneously immortalized granulosa cells. Biol Reprod. 2014;91:36.
67. Clark NC, Friel AM, Pru CA, et al. Progesterone receptor membrane component 1 promotes survival of human breast cancer cells and the growth of xenograft tumors. Cancer Biol Ther. 2016;17:262-271.