Progesterone receptor-dependent regulation of genes in the oviducts of female mice

Physiological Genomics

Volumn 46, Issue 16, 2014, Pages 583-592

  Akison, Lisa K ^a   Boden, Michael J ^a   Kennaway, David J ^a   Russell, Darryl L ^a   Robker, Rebecca L ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Embryo transport; Fallopian tube; PRKO; PRlacZ

Indexed keywords

ACTG2 PROTEIN; ADAMTS1 PROTEIN; CHORIONIC GONADOTROPIN; DES PROTEIN; EDN3 PROTEIN; ITGA8 PROTEIN; MESSENGER RNA; MYOCD PROTEIN; PRLR PROTEIN; PROGESTERONE; PROGESTERONE RECEPTOR; PROTEIN; PTGFR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; FEMALE; GENETIC REGULATION; HISTOLOGY; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OOCYTE TRANSPORT; OVIDUCT; OVULATION; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; 129 MOUSE; ANIMAL; C57BL MOUSE; DNA MICROARRAY; DRUG EFFECTS; EMBRYO DEVELOPMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HORSE; HUMAN; KNOCKOUT MOUSE; METABOLISM; PREGNANCY; PROCEDURES; TRANSGENIC MOUSE;

ANIMALS; CHORIONIC GONADOTROPIN; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HORSES; HUMANS; MALE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OVIDUCTS; OVULATION; PREGNANCY; RECEPTORS, PROGESTERONE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84906093146     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00044.2014     Document Type: Article

References (63)

1. Akison LK, Robker RL. The critical roles of progesterone receptor (PGR) in ovulation, oocyte developmental competence and oviductal transport in mammalian reproduction. Reprod Domest Anim 47, Suppl 4: 288-296, 2012.
2. Amso NN, Crow J, Shaw RW. Comparative immunohistochemical study of oestrogen and progesterone receptors in the fallopian tube and uterus at different stages of the menstrual cycle and the menopause. Hum Reprod 9: 1027-1037, 1994.
3. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Statist Soc Ser B 57: 289-300, 1995.
4. Bowen NJ, Logani S, Dickerson EB, Kapa LB, Akhtar M, Benigno BB, McDonald JF. Emerging roles for PAX8 in ovarian cancer and endosalpingeal development. Gynecol Oncol 104: 331-337, 2007.
5. Brown HM, Dunning KR, Robker RL, Boerboom D, Pritchard M, Lane M, Russell DL. ADAMTS1 cleavage of versican mediates essential structural remodeling of the ovarian follicle and cumulus-oocyte matrix during ovulation in mice. Biol Reprod 83: 549-557, 2010.
6. Buhi WC. Characterization and biological roles of oviduct-specific, oestrogen-dependent glycoprotein. Reproduction 123: 355-362, 2002.
7. Bylander A, Lind K, Goksor M, Billig H, Larsson DJ. The classical progesterone receptor mediates the rapid reduction of fallopian tube ciliary beat frequency by progesterone. Reprod Biol Endocrinol 11: 33, 2013.
8. Caligioni CS. Assessing reproductive status/stages in mice. Curr Protoc Neurosci 4: Appendix 4I, 2009.
9. Chen S, Einspanier R, Schoen J. In vitro mimicking of estrous cycle stages in porcine oviduct epithelium cells: estradiol and progesterone regulate differentiation, gene expression, and cellular function. Biol Reprod 89: 54, 2013.
10. Cretoiu SM, Cretoiu D, Suciu L, Popescu LM. Interstitial Cajal-like cells of human Fallopian tube express estrogen and progesterone receptors. J Mol Histol 40: 387-394, 2009.
11. Croxatto HB. Physiology of gamete and embryo transport through the fallopian tube. Reprod Biomed Online 4: 160-169, 2002.
12. Cui X, Churchill GA. Statistical tests for differential expression in cDNA microarray experiments. Genome Biol 4: 210, 2003.
13. Diaz P, Solar P, Juica N, Orihuela P, Cardenas H, Christodoulides M, Vargas R, Velasquez L. Differential expression of extracellular matrix components in the Fallopian tubes throughout the menstrual cycle. Reprod Biol Endocrinol 10: 56, 2012.
14. Dixon RE, Ramsey KH, Schripsema JH, Sanders KM, Ward SM. Time-dependent disruption of oviduct pacemaker cells by Chlamydia infection in mice. Biol Reprod 83: 244-253, 2010.
15. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210, 2002.
16. Familiari G, Verlengia C, Nottola SA, Renda T, Micara G, Aragona C, Zardi L, Motta PM. Heterogeneous distribution of fibronectin, tenascin-C, and laminin immunoreactive material in the cumulus-corona cells surrounding mature human oocytes from IVF-ET protocols-evidence that they are composed of different subpopulations: an immunohistochemical study using scanning confocal laser and fluorescence microscopy. Mol Reprod Dev 43: 392-402, 1996.
17. Fuentealba B, Nieto M, Croxatto HB. Ovum transport in pregnant rats is little affected by RU486 and exogenous progesterone compared with cycling rats. Biol Reprod 37: 768-774, 1987.
18. Gunnet JW, Freeman ME. The mating-induced release of prolactin: a unique neuroendocrine response. Endocr Rev 4: 44-61, 1983.
19. Guo C, Wang Y, Liang H, Zhang J. ADAMTS-1 contributes to the antifibrotic effect of captopril by accelerating the degradation of type I collagen in chronic viral myocarditis. Eur J Pharmacol 629: 104-110, 2010.
20. Helm G, Owman C, Sjoberg NO, Walles B. Motor activity of the human Fallopian tube in vitro in relation to plasma concentration of oestradiol and progesterone, and the influence of noradrenaline. J Reprod Fertil 64: 233-242, 1982.
21. Horne AW, King AE, Shaw E, McDonald SE, Williams AR, Saunders PT, Critchley HO. Attenuated sex steroid receptor expression in fallopian tube of women with ectopic pregnancy. J Clin Endocrinol Metab 94: 5146-5154, 2009.
22. Hunter RH. Components of oviduct physiology in eutherian mammals. Biol Rev Camb Philos Soc 87: 244-255, 2011.
23. Ismail PM, Li J, DeMayo FJ, O'Malley BW, Lydon JP. A novel LacZ reporter mouse reveals complex regulation of the progesterone receptor promoter during mammary gland development. Mol Endocrinol 16: 2475-2489, 2002.
24. Jeoung M, Lee S, Hawng HK, Cheon YP, Jeong YK, Gye MC, Iglarz M, Ko C, Bridges PJ. Identification of a novel role for endothelins within the oviduct. Endocrinology 151: 2858-2867, 2010.
25. Johnson MC, Castro A, Troncoso JL, Vantman D, Devoto L, Vega M. Presence of angiotensin II and expression of angiotensin II type-2 receptor in human fallopian tube. Fertil Steril 70: 740-746, 1998.
26. Lantz KC, Enders AC, Liu IK. Possible significance of cells within intraluminal collagen masses in equine oviducts. Anat Rec 252: 568-579, 1998.
27. Li HZ, Sun X, Stavreus-Evers A, Gemzell-Danielsson K. Effect of mifepristone on the expression of cytokines in the human Fallopian tube. Mol Hum Reprod 10: 489-493, 2004.
28. Li S, Wang DZ, Wang Z, Richardson JA, Olson EN. The serum response factor coactivator myocardin is required for vascular smooth muscle development. Proc Natl Acad Sci USA 100: 9366-9370, 2003.
29. Li Z, Mericskay M, Agbulut O, Butler-Browne G, Carlsson L, Thornell LE, Babinet C, Paulin D. Desmin is essential for the tensile strength and integrity of myofibrils but not for myogenic commitment, differentiation, and fusion of skeletal muscle. J Cell Biol 139: 129-144, 1997.
30. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-Delta Delta C(T) method. Methods 25: 402-408, 2001.
31. Luciano AM, Corbani D, Lodde V, Tessaro I, Franciosi F, Peluso JJ, Modina S. Expression of progesterone receptor membrane component-1 in bovine reproductive system during estrous cycle. Eur J Histochem 55: e27, 2011.
32. Luconi M, Francavilla F, Porazzi I, Macerola B, Forti G, Baldi E. Human spermatozoa as a model for studying membrane receptors mediating rapid nongenomic effects of progesterone and estrogens. Steroids 69: 553-559, 2004.
33. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery CA Jr, Shyamala G, Conneely OM, O'Malley BW. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9: 2266-2278, 1995.
34. Mahmood T, Saridogan E, Smutna S, Habib AM, Djahanbakhch O. The effect of ovarian steroids on epithelial ciliary beat frequency in the human Fallopian tube. Hum Reprod 13: 2991-2994, 1998.
35. McHugh KM, Crawford K, Lessard JL. A comprehensive analysis of the developmental and tissue-specific expression of the isoactin multigene family in the rat. Dev Biol 148: 442-458, 1991.
36. Nakahari T, Nishimura A, Shimamoto C, Sakai A, Kuwabara H, Nakano T, Tanaka S, Kohda Y, Matsumura H, Mori H. The regulation of ciliary beat frequency by ovarian steroids in the guinea pig Fallopian tube: interactions between oestradiol and progesterone. Biomed Res (Tokyo) 32: 321-328, 2011.
37. Nishimura A, Sakuma K, Shimamoto C, Ito S, Nakano T, Daikoku E, Ohmichi M, Ushiroyama T, Ueki M, Kuwabara H, Mori H, Nakahari T. Ciliary beat frequency controlled by oestradiol and progesterone during ovarian cycle in guinea-pig Fallopian tube. Exp Physiol 95: 819-828, 2010.
38. Nutu M, Weijdegard B, Thomas P, Thurin-Kjellberg A, Billig H, Larsson DG. Distribution and hormonal regulation of membrane progesterone receptors beta and gamma in ciliated epithelial cells of mouse and human fallopian tubes. Reprod Biol Endocrinol 7: 89, 2009.
39. Ormandy CJ, Camus A, Barra J, Damotte D, Lucas B, Buteau H, Edery M, Brousse N, Babinet C, Binart N, Kelly PA. Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev 11: 167-178, 1997.
40. Peluso JJ. Multiplicity of progesterone's actions and receptors in the mammalian ovary. Biol Reprod 75: 2-8, 2006.
41. Pollow K, Inthraphuvasak J, Manz B, Grill HJ, Pollow B. A comparison of cytoplasmic and nuclear estradiol and progesterone receptors in human fallopian tube and endometrial tissue. Fertil Steril 36: 615-622, 1981.
42. Popescu LM, Ciontea SM, Cretoiu D, Hinescu ME, Radu E, Ionescu N, Ceausu M, Gherghiceanu M, Braga RI, Vasilescu F, Zagrean L, Ardeleanu C. Novel type of interstitial cell (Cajal-like) in human fallopian tube. J Cell Mol Med 9: 479-523, 2005.
43. Ricciardelli C, Frewin KM, Tan ID, Williams ED, Opeskin K, Pritchard MA, Ingman WV, Russell DL. The ADAMTS1 protease gene is required for mammary tumor growth and metastasis. Am J Pathol 179: 3075-3085, 2011.
44. Robker RL, Russell DL, Espey LL, Lydon JP, O'Malley BW, Richards JS. Progesterone-regulated genes in the ovulation process: ADAMTS-1 and cathepsin L proteases. Proc Natl Acad Sci USA 97: 4689-4694, 2000.
45. Ruscheinsky M, De la Motte C, Mahendroo M. Hyaluronan and its binding proteins during cervical ripening and parturition: dynamic changes in size, distribution and temporal sequence. Matrix Biol 27: 487-497, 2008.
46. Saridogan E, Djahanbakhch O, Puddefoot JR, Demetroulis C, Collingwood K, Mehta JG, Vinson GP. Angiotensin II receptors and angiotensin II stimulation of ciliary activity in human fallopian tube. J Clin Endocrinol Metab 81: 2719-2725, 1996.
47. Schnapp LM, Breuss JM, Ramos DM, Sheppard D, Pytela R. Sequence and tissue distribution of the human integrin alpha 8 subunit: a beta 1-associated alpha subunit expressed in smooth muscle cells. J Cell Sci 108: 537-544, 1995.
48. Schnapp LM, Hatch N, Ramos DM, Klimanskaya IV, Sheppard D, Pytela R. The human integrin alpha 8 beta 1 functions as a receptor for tenascin, fibronectin, and vitronectin. J Biol Chem 270: 23196-23202, 1995.
49. Shao R, Norstrom A, Weijdegard B, Egecioglu E, Fernandez-Rodriguez J, Feng Y, Stener-Victorin E, Brannstrom M, Billig H. Distinct expression pattern of Dicer1 correlates with ovarian-derived steroid hormone receptor expression in human Fallopian tubes during ovulation and the midsecretory phase. J Clin Endocrinol Metab 96: E869-E877, 2011.
50. Shao R, Nutu M, Weijdegard B, Egecioglu E, Fernandez-Rodriguez J, Tallet E, Goffin V, Ling C, Billig H. Differences in prolactin receptor (PRLR) in mouse and human fallopian tubes: evidence for multiple regulatory mechanisms controlling PRLR isoform expression in mice. Biol Reprod 79: 748-757, 2008.
51. Shao R, Weijdegard B, Ljungstrom K, Friberg A, Zhu C, Wang X, Zhu Y, Fernandez-Rodriguez J, Egecioglu E, Rung E, Billig H. Nuclear progesterone receptor A and B isoforms in mouse fallopian tube and uterus: implications for expression, regulation, and cellular function. Am J Physiol Endocrinol Metab 291: E59-E72, 2006.
52. Spilman CH, Shaikh AA, Harper MJ. Oviductal motility amplitude and ovarian steroid secretion during egg transport in the rabbit. Biol Reprod 18: 409-417, 1978.
53. Sun Q, Taurin S, Sethakorn N, Long X, Imamura M, Wang DZ, Zimmer WE, Dulin NO, Miano JM. Myocardin-dependent activation of the CArG box-rich smooth muscle gamma-actin gene: preferential utilization of a single CArG element through functional association with the NKX3.1 homeodomain protein. J Biol Chem 284: 32582-32590, 2009.
54. Szoltys M, Galas J, Jablonka A, Tabarowski Z. Some morphological and hormonal aspects of ovulation and superovulation in the rat. J Endocrinol 141: 91-100, 1994.
55. Talbot P, Geiske C, Knoll M. Oocyte pickup by the mammalian oviduct. Mol Biol Cell 10: 5-8, 1999.
56. Teilmann SC, Clement CA, Thorup J, Byskov AG, Christensen ST. Expression and localization of the progesterone receptor in mouse and human reproductive organs. J Endocrinol 191: 525-535, 2006.
57. Verdugo P, Rumery RE, Tam PY. Hormonal control of oviductal ciliary activity: effect of prostaglandins. Fertil Steril 33: 193-196, 1980.
58. Vinijsanun A, Martin L. Effects of progesterone antagonists RU486 and ZK98734 on embryo transport, development and implantation in laboratory mice. Reprod Fertil Dev 2: 713-727, 1990.
59. Wanggren K, Lalitkumar PG, Stavreus-Evers A, Stabi B, Gemzell-Danielsson K. Prostaglandin E2 and F2alpha receptors in the human Fallopian tube before and after mifepristone treatment. Mol Hum Reprod 12: 577-585, 2006.
60. Wanggren K, Stavreus-Evers A, Olsson C, Andersson E, Gemzell-Danielsson K. Regulation of muscular contractions in the human Fallopian tube through prostaglandins and progestagens. Hum Reprod 23: 2359-2368, 2008.
61. Wessel T, Schuchter U, Walt H. Ciliary motility in bovine oviducts for sensing rapid non-genomic reactions upon exposure to progesterone. Horm Metab Res 36: 136-141, 2004.
62. Wijayagunawardane MP, Miyamoto A, Taquahashi Y, Acosta TJ, Nishimura M, Sato K. Angiotensin II and atrial natriuretic peptide in the cow oviductal contraction in vitro: direct effect and local secretion of prostaglandins, endothelin-1, and angiotensin II. Biol Reprod 65: 799-804, 2001.
63. Zargham R, Thibault G. Alpha 8 integrin expression is required for maintenance of the smooth muscle cell differentiated phenotype. Cardiovasc Res 71: 170-178, 2006.