A prostaglandin E2 receptor antagonist prevents pregnancies during a preclinical contraceptive trial with female macaques

Human Reproduction

Volumn 29, Issue 7, 2014, Pages 1400-1412

  Peluffo, M C ^a,b   Stanley, J ^b   Braeuer, N ^c   Rotgeri, A ^c   Fritzemeier, K H ^d   Fuhrmann, U ^c   Buchmann, B ^c   Adevai, T ^b   Murphy, M J ^b   Zelinski, M B ^b,e   Lindenthal, B ^c   Hennebold, J D ^b,e   Stouffer, R L ^b,e  

^a HOSPITAL DE NIÑOS RICARDO GUTIÉRREZ   (Argentina)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c BAYER PHARMA AG   (Germany)

^d UNIVERSITY OF DUISBURG ESSEN   (Germany)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

contraceptive trial; cumulus oocyte expansion; primates; prostaglandin E2 receptor

Indexed keywords

BAY 06; CONTRACEPTIVE AGENT; HYALURONIC ACID; INDOMETACIN; MESSENGER RNA; PROSTAGLANDIN E RECEPTOR; PROSTAGLANDIN E2; PROSTAGLANDIN RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BLOOD CELL COUNT; CONFOCAL MICROSCOPY; CONTRACEPTION; CONTROLLED STUDY; CUMULUS CELL; ECHOGRAPHY; ENZYME IMMUNOASSAY; FEMALE; IMMUNOFLUORESCENCE MICROSCOPY; MACACA; NONHUMAN; OOCYTE; OVULATION; OVULATION INDUCTION; PREGNANCY; PROSTAGLANDIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; RHESUS MONKEY; ANIMAL; ANTAGONISTS AND INHIBITORS; BREEDING; DRUG EFFECTS; GENE EXPRESSION REGULATION; MACACA FASCICULARIS; METABOLISM; OVARY; OVARY FOLLICLE; PROCEDURES; TIME;

ANIMALS; CONTRACEPTION; CONTRACEPTIVE AGENTS; FEMALE; GENE EXPRESSION REGULATION; INDOMETHACIN; MACACA; MACACA FASCICULARIS; OOCYTES; OVARIAN FOLLICLE; OVARY; OVULATION; PREGNANCY; PREGNANCY, ANIMAL; RECEPTORS, PROSTAGLANDIN E; RNA, MESSENGER; TIME FACTORS;

EID: 84902676650     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/deu083     Document Type: Article

References (48)

1. Back SA, Tuohy TM, Chen H, Wallingford N, Craig A, Struve J, Luo NL, Banine F, Liu Y, Chang A et al. Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitor maturation. Nat Med 2005;11:966-972.
2. Bata MS, Al-Ramahi M, Salhab AS, Gharaibeh MN, Schwartz J. Delay of ovulation by meloxicam in healthy cycling volunteers: a placebocontrolled, double-blind, crossover study. J Clin Pharmacol 2006; 46:925-932.
3. Bodo E, Kromminga A, Biro T, Borbiro I, Gaspar E, Zmijewski MA, van Beek N, Langbein L, Slominski AT, Paus R. Human female hair follicles are a direct, nonclassical target for thyroid-stimulating hormone. J Invest Dermatol 2009;129:1126-1139.
4. Bogan RL, Murphy MJ, Stouffer RL, Hennebold JD. Prostaglandin synthesis, metabolism, and signaling potential in the rhesus macaque corpus luteum throughout the luteal phase of the menstrual cycle. Endocrinology 2008a;149:5861-5871.
5. Bogan RL, Murphy MJ, Stouffer RL, Hennebold JD. Systematic determination of differential gene expression in the primate corpus luteum during the luteal phase of the menstrual cycle. Mol Endocrinol 2008b;22:1260-1273.
6. Chaffin CL, Dissen GA, Stouffer RL. Hormonal regulation of steroidogenic enzyme expression in granulosa cells during the peri-ovulatory interval in monkeys. Mol Hum Reprod 2000;6:11-18.
7. Chen L, Mao SJ, Larsen WJ. Identification of a factor in fetal bovine serum that stabilizes the cumulus extracellular matrix. A role for a member of the inter-Alpha-trypsin inhibitor family. J Biol Chem 1992;267:12380-12386.
8. Chen L, Russell PT, Larsen WJ. Functional significance of cumulus expansion in the mouse: roles for the preovulatory synthesis of hyaluronic acid within the cumulus mass. Mol Reprod Dev 1993;34:87-93.
9. Duffy DM, Stouffer RL. The ovulatory gonadotrophin surge stimulates cyclooxygenase expression and prostaglandin production by the monkey follicle. Mol Hum Reprod 2001;7:731-739.
10. Duffy DM, Stouffer RL. Follicular administration of a cyclooxygenase inhibitor can prevent oocyte release without alteration of normal luteal function in rhesus monkeys. Hum Reprod 2002;17:2825-2831.
11. Duffy DM, Chaffin CL, Stouffer RL. Expression of estrogen receptor alpha and beta in the rhesus monkey corpus luteum during the menstrual cycle: regulation by luteinizing hormone and progesterone. Endocrinology 2000;141:1711-1717.
12. Duffy DM, Seachord CL, Dozier BL. Microsomal prostaglandin E synthase-1 (mPGES-1) is the primary form of PGES expressed by the primate periovulatory follicle. Hum Reprod 2005;20:1485-1492.
13. Eppig JJ. Gonadotropin stimulation of the expansion of cumulus oophori isolated from mice: general conditions for expansion in vitro. J Exp Zool 1979;208:111-120.
14. Eppig JJ. Regulation of cumulus oophorus expansion by gonadotropins in vivo and in vitro. Biol Reprod 1980a;23:545-552.
15. Eppig JJ. Role of serum in FSH stimulated cumulus expansion by mouse oocyte-cumulus cell complexes in vitro. Biol Reprod 1980b;22:629-633.
16. Eppig JJ. Prostaglandin E2 stimulates cumulus expansion and hyaluronic acid synthesis by cumuli oophori isolated from mice. Biol Reprod 1981; 25:191-195.
17. Fulop C, Salustri A, Hascall VC. Coding sequence of a hyaluronan synthase homologue expressed during expansion of the mouse cumulus-oocyte complex. Arch Biochem Biophys 1997;337:261-266.
18. Fulop C, Szanto S, MukhopadhyayD, BardosT, KamathRV, Rugg MS, Day AJ, Salustri A, Hascall VC, Glant TT et al. Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development 2003;130:2253-2261.
19. Hall JM, Couse JF, Korach KS. The multifaceted mechanisms of estradiol and estrogen receptor signaling. J Biol Chem 2001;276:36869-36872.
20. Harper M. In search of a second contraceptive revolution. Sex Reprod Menopause 2005;3:59-67.
21. Harris SM, Aschenbach LC, Skinner SM, Dozier BL, Duffy DM. Prostaglandin E2 receptors are differentially expressed in subpopulations of granulosa cells from primate periovulatory follicles. Biol Reprod 2011;85:916-923.
22. Hibbert ML, Stouffer RL, Wolf DP, Zelinski-Wooten MB. Midcycle administration of a progesterone synthesis inhibitor prevents ovulation in primates. Proc Natl Acad Sci USA 1996;93:1897-1901.
23. Hizaki H, Segi E, Sugimoto Y, Hirose M, Saji T, Ushikubi F, Matsuoka T, Noda Y, Tanaka T, Yoshida N et al. Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP(2). Proc Natl Acad Sci USA 1999;96:10501-10506.
24. Jesam C, Salvatierra AM, Schwartz JL, Croxatto HB. Suppression of follicular rupture with meloxicam, a cyclooxygenase-2 inhibitor: potential for emergency contraception. Hum Reprod 2010;25:368-373.
25. Kimura N, Konno Y, Miyoshi K, Matsumoto H, Sato E. Expression of hyaluronan synthases and CD44 messenger RNAs in porcine cumulus-oocyte complexes during in vitro maturation. Biol Reprod 2002;66:707-717.
26. Massai MR, Forcelledo ML, Brache V, Tejada AS, Salvatierra AM, Reyes MV, Alvarez F, Faundes A, Croxatto HB. Does meloxicam increase the incidence of anovulation induced by single administration of levonorgestrel in emergency contraception? A pilot study. Hum Reprod 2007;22:434-439.
27. Micks E, Shekell T, Stanley J, Zelinski M, Martin L, Riefenberg S, Adevai T, Jensen J. Medical termination of pregnancy in cynomolgus macaques. J Med Primatol 2012;41:394-402.
28. Mukhopadhyay D, Hascall VC, Day AJ, Salustri A, Fulop C. Two distinct populations of tumor necrosis factor-stimulated gene-6 protein in the extracellular matrix of expanded mouse cumulus cell-oocyte complexes. Arch Biochem Biophys 2001;394:173-181.
29. Mulac-Jericevic B, Conneely OM. Reproductive tissue selective actions of progesterone receptors. Reproduction 2004;128:139-146.
30. Munro CJ, Laughlin LS, Illera JC, Dieter J, Hendrickx AG, Lasley BL. ELISA for the measurement of serum and urinary chorionic gonadotropin concentrations in the laboratorymacaque. AmJ Primatol 1997;41:307-322.
31. Narumiya S, Sugimoto Y, Ushikubi F. Prostanoid receptors: structures, properties, and functions. Physiol Rev 1999;79:1193-1226.
32. Norman RJ. Reproductive consequences of COX-2 inhibition. Lancet 2001; 358:1287-1288.
33. Ochsner SA, Russell DL, Day AJ, Breyer RM, Richards JS. Decreased expression of tumor necrosis factor-Alpha-stimulated gene 6 in cumulus cells of the cyclooxygenase-2 and EP2 null mice. Endocrinology 2003; 144:1008-1019.
34. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 2004; 303:682-684.
35. Peng XR, Hsueh AJ, LaPolt PS, Bjersing L, Ny T. Localization of luteinizing hormone receptor messenger ribonucleic acid expression in ovarian cell types during follicle development and ovulation. Endocrinology 1991; 129:3200-3207.
36. Peng J, Li Q, Wigglesworth K, Rangarajan A, Kattamuri C, Peterson RT, Eppig JJ, Thompson TB, Matzuk MM. Growth differentiation factor 9: bone morphogenetic protein 15 heterodimers are potent regulators of ovarian functions. Proc Natl Acad Sci USA 2013;110:E776-E785.
37. Richards JS. Ovulation: new factors that prepare the oocyte for fertilization. Mol Cell Endocrinol 2005;234:75-79.
38. Ruan YC, Guo JH, Liu X, Zhang R, Tsang LL, Dong JD, Chen H, Yu MK, Jiang X, Zhang XH et al. Activation of the epithelial Na+ channel triggers prostaglandin E(2) release and production required for embryo implantation. Nat Med 2012;18:1112-1117.
39. Salustri A, Garlanda C, Hirsch E, De Acetis M, Maccagno A, Bottazzi B, Doni A, Bastone A, Mantovani G, Beck Peccoz P et al. PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development 2004;131:1577-1586.
40. Sirois J, Boerboom D, Sayasith K. Prostaglandin Biosynthesis and Action in the Ovary. In Leung PCK, Adashi EY (eds). The Ovary. San Diego, CA: Elsevier Inc, Academic Press, 2004, pp. 233-247.
41. Sugimoto Y, Narumiya S. Prostaglandin E receptors. J Biol Chem 2007; 282:11613-11617.
42. Tamba S,Yodoi R,MorimotoK, InazumiT, SukenoM, Segi-Nishida E,OkunoY, Tsujimoto G,Narumiya S, Sugimoto Y. Expression profiling of cumulus cells reveals functional changes during ovulation and central roles of prostaglandin EP2 receptor in cAMP signaling. Biochimie 2010;92:665-675.
43. Ueno S, Yoshida N, Niimura S. Amount of hyaluronan produced by mouse oocytes and role of hyaluronan in enlargement of the perivitelline space. J Reprod Dev 2009;55:496-501.
44. Wolf DP, Thomson JA, Zelinski-Wooten MB, Stouffer RL. In vitro fertilization-embryo transfer in nonhuman primates: the technique and its applications. Mol Reprod Dev 1990;27:261-280.
45. Xu F, Stouffer RL, Muller J, Hennebold JD, Wright JW, Bahar A, Leder G, Peters M, Thorne M, Sims M et al. Dynamics of the transcriptome in the primate ovulatory follicle. Mol Hum Reprod 2011;17:152-165.
46. Yamashita Y, Okamoto M, Kawashima I, Okazaki T, Nishimura R, Gunji Y, Hishinuma M, Shimada M. Positive feedback loop between prostaglandin E2 and Egf-like factors is essential for sustainable activation of MAPK3/1 in cumulus cells during in vitro maturation of porcine cumulus oocyte complexes. Biol Reprod 2011;85:1073-1082.
47. Young KA, Hennebold JD, Stouffer RL. Dynamic expression of mRNAs and proteins for matrix metalloproteinases and their tissue inhibitors in the primate corpus luteum during the menstrual cycle. Mol Hum Reprod 2002;8:833-840.
48. Young KA, Chaffin CL, Molskness TA, Stouffer RL. Controlled ovulation of the dominant follicle: a critical role for LH in the late follicular phase of the menstrual cycle. Hum Reprod 2003;18:2257-2263.