Remodeling of the cervix and parturition in mice lacking the progesterone receptor B isoform

Biology of Reproduction

Volumn 85, Issue 3, 2011, Pages 498-502

  Yellon, Steven M ^a   Oshiro, Bryan T ^a   Chhaya, Tejas Y ^a   Lechuga, Thomas J ^a   Dias, Rejane M ^a   Burns, Alexandra E ^a   Force, Lindsey ^a   Apostolakis, Ede M ^b  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Birth; Cervix; Inflammation; Macrophage; Neutrophil; Parturition; Progesterone progesterone receptor; Ripening

Indexed keywords

COLLAGEN; PROGESTERONE RECEPTOR B;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; INFLAMMATION; KNOCKOUT MOUSE; MACROPHAGE; MALE; MORPHOLOGY; MOUSE; NEUTROPHIL; NONHUMAN; OPTICAL DENSITY; PRENATAL PERIOD; PRIORITY JOURNAL; TERM BIRTH; UTERINE CERVIX; UTERINE CERVIX REMODELING; UTERINE CERVIX RIPENING; UTERUS FUNCTION; UTERUS WEIGHT; WILD TYPE;

ANIMALS; CERVIX UTERI; EXTRACELLULAR MATRIX; FEMALE; MICE; MICE, KNOCKOUT; PARTURITION; PREGNANCY; PROTEIN ISOFORMS; RECEPTORS, PROGESTERONE;

MUS;

EID: 80052516800     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.091983     Document Type: Article

References (45)

1. Mesiano S, Wang Y, Norwitz ER. Progesterone receptors in the human pregnancy uterus: do they hold the key to birth timing? Reprod Sci 2011; 18:6-19.
2. Astle S, Slater DM, Thornton S. The involvement of progesterone in the onset of human labor. Eur J Obstet Gynecol Reprod Biol 2003; 108:177-181.
3. Mitchell BF, Taggart MJ. Are animal models relevant to key aspects of human parturition? Am J Physiol Regul Integr Comp Physiol 2009; 297:R525-R545.
4. Csapo AI, Wiest WG. An examination of the quantitative relationship between progesterone and the maintenance of pregnancy. Endocrinology 1969; 85:735-746.
5. Conneely OM, Mulac-Jericevic B, DeMayo F, Lydon JP, O'Malley BW. Reproductive functions of progesterone receptors. Recent Prog Horm Res 2002; 57:339-355.
6. Sleiter N, Pang Y, Park C, Horton TH, Dong J, Thomas P, Levine JE. Progesterone receptor A (PGR-A) and PGR-B-independent effects of progesterone on gonadotropin-releasing hormone release. Endocrinology 2009; 150:3833-3844.
7. Conneely OM, Mulac-Jericevic B, Lydon JP. Progesterone-dependent regulation of female reproductive activity by two distinct progesterone receptor isoforms. Steroids 2003; 68:771-778.
8. Conneely OM, Mulac-Jericevic B, Lydon JP, De Mayo FJ. Reproductive functions of the progesterone receptor isoforms: lessons from knock-out mice. Mol Cell Endocrinol 2001; 179:97-103.
9. Mulac-Jericevic B, Mullinax RA, DeMayo FJ, Lydon JP, Conneely OM. Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science 2000; 289:1751-1754.
10. Mulac-Jericevic B, Lydon JP, DeMayo FJ, Conneely OM. Defective mammary gland morphogenesis in mice lacking the progesterone receptor B isoform. Proc Natl Acad Sci U S A 2003; 100:9744-9749.
11. Vegeto E, Shahbaz MM, Wen DX, Goldman ME, O'Malley BW, McDonnell DP. Human progesterone receptor A form is a cell- and promoter-specific repressor of human progesterone receptor B function. Mol Endocrinol 1993; 7:1244-1255.
12. Kraus WL, Weis KE, Katzenellenbogen BS. Inhibitory cross-talk between steroid hormone receptors: differential targeting of estrogen receptor in the repression of its transcriptional activity by agonist- and antagonistoccupied progestin receptors. Mol Cell Biol 1995; 15:1847-1857.
13. Graham JD, Yager ML, Hill HD, Byth K, O'Neill GM, Clarke CL. Altered progesterone receptor isoform expression remodels progestin responsiveness of breast cancer cells. Mol Endocrinology 2005; 19:2713-2735.
14. Boroditsky RS, Reyes FI, Winter JS, Faiman C. Maternal serum estrogen and progesterone concentrations preceding normal labor. Obstet Gynecol 1978; 51:686-691.
15. Burden HW, Lawrence IE Jr. Experimental studies on the acetylcholinesterase-positive nerves in the ovary of the rat. Anat Rec 1978; 190:233-241.
16. Bridges RS. A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat. Endocrinology 1984; 114:930-940.
17. Junqueira LC, Zugaib M, Montes GS, Toledo OM, Krisztan RM, Shigihara KM. Morphologic and histochemical evidence for the occurrence of collagenolysis and for the role of neutrophilic polymorphonuclear leukocytes during cervical dilation. Am J Obstet Gynecol 1980; 138:273-281.
18. Kirby LS, Kirby MA, Warren JW, Tran LT, Yellon SM. Increased innervation and ripening of the prepartum murine cervix. J Soc Gynecol Investig 2005; 12:578-585.
19. Ledingham MA, Thomson AJ, Jordan F, Young A, Crawford M, Norman JE. Cell adhesion molecule expression in the cervix and myometrium during pregnancy and parturition. Obstet Gynecol 2001; 97:235-242.
20. Luque EH, Munoz de Toro MM, Ramos JG, Rodriguez HA, Sherwood OD. Role of relaxin and estrogen in the control of eosinophilic invasion and collagen remodeling in rat cervical tissue at term. Biol Reprod 1998; 59:795-800.
21. Mackler AM, Iezza G, Akin MR, McMillan P, Yellon SM. Macrophage trafficking in the uterus and cervix precedes parturition in the mouse. Biol Reprod 1999; 61:879-883.
22. Yellon SM, Mackler AM, Kirby MA. The role of leukocyte traffic and activation in parturition. J Soc Gynecol Investig 2003; 10:323-338.
23. Boyd JW, Lechuga TJ, Ebner CA, Kirby MA, Yellon SM. Cervix remodeling and parturition in the rat: lack of a role for hypogastric innervation. Reproduction 2009; 137:739-748.
24. Clyde LA, Lechuga TJ, Ebner CA, Burns AE, Kirby MA, Yellon SM. Transection of the pelvic or vagus nerve forestalls ripening of the cervix and delays birth in rats. Biol Reprod 2011; 84:587-594.
25. Word RA, Li XH, Hnat M, Carrick K. Dynamics of cervical remodeling during pregnancy and parturition: mechanisms and current concepts. Semin Reprod Med 2007; 25:69-79.
26. Sakamoto Y, Moran P, Bulmer JN, Searle RF, Robson SC. Macrophages and not granulocytes are involved in cervical ripening. J Reprod Immunol 2005; 66:161-173.
27. Stjernholm-Vladic Y, Stygar D, Mansson C, Masironi B, Akerberg S, Wang H, Ekman-Ordeberg G, Sahlin L. Factors involved in the inflammatory events of cervical ripening in humans. Reprod Biol Endocrinol 2004; 2:74.
28. Yellon SM, Burns AE, See JL, Lechuga TJ, Kirby MA. Progesterone withdrawal promotes remodeling processes in the nonpregnant mouse cervix. Biol Reprod 2009; 81:1-6.
29. Yellon SM, Ebner CA, Elovitz MA. Medroxyprogesterone acetate modulates remodeling, immune cell census, and nerve fibers in the cervix of a mouse model for inflammation-induced preterm birth. Reprod Sci 2009; 16:257-264.
30. Magyar DM, Elsner CW, Fridshal D, Eliot J, Klein A, Glatz T, Lowe KC, Nathanielsz PW, Buster JE. Time-trend analysis of plasma 11-desoxycorticosterone, corticosterone, cortisol, and aldosterone in fetal and maternal sheep during the last 18 days of gestation. J Steroid Biochem 1981; 14:1091-1099.
31. Fata JE, Chaudhary V, Khokha R. Cellular turnover in the mammary gland is correlated with systemic levels of progesterone and not 17beta-estradiol during the estrous cycle. Biol Reprod 2001; 65:680-688.
32. Mahendroo MS, Porter A, Russell DW, Word RA. The parturition defect in steroid 5alpha-reductase type 1 knockout mice is due to impaired cervical ripening. Mol Endocrinol 1999; 13:981-992.
33. Mackler AM, Ducsay CA, Veldhuis JD, Yellon SM. Maturation of spontaneous and agonist-induced uterine contractions in the peripartum mouse uterus. Biol Reprod 1999; 61:873-878.
34. Zakar T, Hertelendy F. Progesterone withdrawal: key to parturition. Am J Obstet Gynecol 2007; 196:289-296.
35. Sasaki S, Nagata K, Kobayashi Y. Regulation of the estrous cycle by neutrophil infiltration into the vagina. Biochem Biophys Res Commun 2009; 382:35-40.
36. Robertson SA, Christiaens I, Dorian CL, Zaragoza DB, Care AS, Banks AM, Olson DM. Interleukin-6 is an essential determinant of on-time parturition in the mouse. Endocrinology 2010; 151:3996-4006.
37. Wilson L Jr, Parsons M. Endocrinology of human gestation. In: Adashi EY, Rock A, Rosenwakr Z (eds.), Reproductive Endocrinology, Surgery and Technology. Philadelphia: Lippincott-Raven; 1996:458.
38. Condon JC, Hardy DB, Kovaric K, Mendelson CR. Upregulation of the progesterone receptor (PR)-C isoform in laboring myometrium by activation of NF-{kappag}B may contribute to the onset of labor through inhibition of PR function. Mol Endocrinol 2006; 20:764-775.
39. Andersson S, Minjarez D, Yost NP, Word RA. Estrogen and progesterone metabolism in the cervix during pregnancy and parturition. J Clin Endocrinol Metab 2008; 93:2366-2374.
40. Rodriguez HA, Kass L, Varayoud J, Ramos JG, Ortega HH, Durando M, Munoz de Toro M, Luque EH. Collagen remodeling in the guinea-pig uterine cervix at term is associated with a decrease in progesterone receptor expression. Mol Hum Reprod 2003; 9:807-813.
41. Chapman NR, Kennelly MM, Harper KA, Europe-Finner GN, Robson SC. Examining the spatio-temporal expression of mRNA encoding the membrane-bound progesterone receptor-alpha isoform in human cervix and myometrium during pregnancy and labor. Mol Hum Reprod 2006; 12:19-24.
42. Mani S, Portillo W. Activation of progestin receptors in female reproductive behavior: interactions with neurotransmitters. Front Neuroendocrinol 2010; 31:157-171.
43. Christiaens I, Zaragoza DB, Guilbert L, Robertson SA, Mitchell BF, Olson DM. Inflammatory processes in preterm and term parturition. J Reprod Immunol 2008; 79:50-57.
44. Yellon SM, Ebner CA, Sugimoto Y. Parturition and recruitment of macrophages in cervix of mice lacking the prostaglandin F receptor. Biol Reprod 2008; 78:438-444.
45. Berry SM, Romero R, Gomez R, Puder KS, Ghezzi F, Cotton DB, Bianchi DW. Premature parturition is characterized by in utero activation of the fetal immune system. Am J Obstet Gynecol 1995; 173:1315-1320.