Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Priming anoestrous Corriedale ewes with progesterone and gonadotrophin-releasing hormone causes cervical tissue remodelling due to metalloproteinase-2 (MMP-2) activity

M. Rodríguez-Piñón A C , C. Tasende A , P. Genovese B , A. Bielli B , D. Casuriaga A and E. G. Garófalo A
+ Author Affiliations
- Author Affiliations

A Biochemistry, Department of Molecular and Cellular Biology, Veterinary Faculty, Universidad de la República, Uruguay. A. Lasplaces 1620, P. Box 11600, Montevideo, Uruguay.

B Histology and Embryology, Department of Morphology and Development, Veterinary Faculty, Universidad de la República, Uruguay. A. Lasplaces 1620, P. Box 11600, Montevideo, Uruguay.

C Corresponding author. Email: marodri@adinet.com.uy

Animal Production Science - https://doi.org/10.1071/AN16138
Submitted: 5 March 2016  Accepted: 5 September 2016   Published online: 13 October 2016

Abstract

The aim was to obtain experimental evidence of cervical collagen degradation in anoestrous Corriedale adult ewes induced to ovulate with progesterone (P) and gonadotrophin-releasing hormone (GnRH), at the expected time of induced ovulation and early luteal phase. In Experiment 1, anoestrous ewes were treated with P for 10 days (P, n = 4), with nine micro-doses of GnRH followed by a GnRH bolus injection (GnRH, n = 4) or with P plus GnRH treatments (P+GnRH, n = 3), and cervices were obtained either without treatment (A, n = 4), when P was removed, or 24 h after the GnRH bolus injection. In Experiment 2, cervices were obtained 1 (group P+GnRH, n = 5) or 5 (P+GnRH 5, n = 6) days after the GnRH bolus injection with P pretreatment. MMP-2 activity was detected in all samples; however, MMP-9 activity was only detected in 15% of the samples. The activity of the latent (L) form of MMP-2 in the cranial zone of group A was higher than in the cranial zone of groups P, GnRH and P+GnRH, and was also higher than that in the caudal zone of the same group (P < 0.05). The collagen concentration was lower in group P+GnRH 1 than in group P+GnRH 5 (P < 0.04). The activity of the activated (A) form of MMP-2 and the A/L MMP-2 ratio were higher in group P+GnRH 1 than in group P+GnRH 5 (P < 0.05). Data suggest that the L form of MMP-2 was expressed mainly in a constitutive form in the cervix of anoestrous ewes and that an oestrogen-dependent activation mechanisms due to the GnRH treatment may be responsible for the lowest collagen content at the moment of the induced ovulation. This work provides evidence about cervical collagen remodelling in anoestrous ewes treated with P + GnRH.

Additional keywords: collagen remodeling, gelatinase, sheep.


References

Amălinei C, Căruntu ID, Bălan RA (2007) Biology of metalloproteinases. Romanian Journal of Morphology and Embryology 48, 323–334.

Anuradha P, Thampan RV (1993) Hormonal regulation of rat uterine collagenase. Archives of Biochemistry and Biophysics 303, 81–89.
Hormonal regulation of rat uterine collagenase.CrossRef | 1:CAS:528:DyaK3sXktVWhs74%3D&md5=5b3ca984d837fc7e0a62f8172b786700CAS | 8489268PubMed |

Bannister DW, Burns AB (1970) Adaptation of the Bergman and Loxley technique for hydroxyproline determination to the autoanalyzer and its use in determining plasma hydroxyproline in the domestic fowl. Analyst (London) 95, 596–600.
Adaptation of the Bergman and Loxley technique for hydroxyproline determination to the autoanalyzer and its use in determining plasma hydroxyproline in the domestic fowl.CrossRef | 1:CAS:528:DyaE3cXksleks70%3D&md5=aefc88872eeb27cb36a1e2a972b91e0aCAS |

Bartlewski PM, Aravindakshan J, Beard AP, Nelson ML, Batista-Arteaga M, Cook SJ, Rawlings NC (2004) Effects of medroxyprogesterone acetate (MAP) on ovarian antral follicle development, gonadotrophin secretion and response to ovulation induction with gonadotrophin-releasing hormone (GnRH) in seasonally anoestrous ewes. Animal Reproduction Science 81, 63–75.
Effects of medroxyprogesterone acetate (MAP) on ovarian antral follicle development, gonadotrophin secretion and response to ovulation induction with gonadotrophin-releasing hormone (GnRH) in seasonally anoestrous ewes.CrossRef | 1:CAS:528:DC%2BD2cXmvFylsA%3D%3D&md5=7c44fb36a0758ad052a6ec42287a03fdCAS | 14749049PubMed |

Birkedal-Hansen H, Moore WG, Bodden MK, Windsor LJ, Birkedal-Hansen B, DeCarlo A, Engler JA (1993) Matrix metalloproteinases: a review. Critical Reviews in Oral Biology and Medicine 4, 197–250.

Bramley TA, Stirling D, Menzies GS, Baird DT (2005) Corpora lutea induced by gonadotrophin-releasing hormone treatment of anoestrous Welsh Mountain ewes: reduced sensitivity to luteinizing hormone in vivo and to chorionic gonadotrophin in vitro. Reproduction (Cambridge, England) 129, 61–73.
Corpora lutea induced by gonadotrophin-releasing hormone treatment of anoestrous Welsh Mountain ewes: reduced sensitivity to luteinizing hormone in vivo and to chorionic gonadotrophin in vitro.CrossRef | 1:CAS:528:DC%2BD2MXht1eltbs%3D&md5=2f9cded794a23553d72471d51b0dc74aCAS |

Candappa IBR, Bartlewski PM (2011) A review of advances in artificial insemination (AI) and embryo transfer (ET) in sheep, with the special reference to hormonal induction of cervical dilation and its implications for controlled animal reproduction and surgical techniques. The Open Reproductive Science Journal 3, 162–175.
A review of advances in artificial insemination (AI) and embryo transfer (ET) in sheep, with the special reference to hormonal induction of cervical dilation and its implications for controlled animal reproduction and surgical techniques.CrossRef |

Clark K, Ji H, Feltovich H, Janowski J, Carroll C, Chien EK (2006) Mifepristone-induced cervical ripening: structural, biomechanical, and molecular events. American Journal of Obstetrics and Gynecology 194, 1391–1398.
Mifepristone-induced cervical ripening: structural, biomechanical, and molecular events.CrossRef | 1:CAS:528:DC%2BD28XktVGhtbg%3D&md5=ba83cd0a328b1d97bed9d6eee8d9b42cCAS | 16647925PubMed |

Etherington DJ, Sims TJ (1981) Detection and estimation of collagen. Journal of the Science of Food and Agriculture 32, 539–546.
Detection and estimation of collagen.CrossRef | 1:CAS:528:DyaL3MXls1Oitbo%3D&md5=eb5ce0516496370750f9206c6fe38b54CAS |

Falchi L, Scaramuzzi RJ (2013) The expression of ERα, OTR, cPLA(2), COX-2, and PPARγ in the cervix of the ewe during the estrous cycle. Theriogenology 79, 40–47.
The expression of ERα, OTR, cPLA(2), COX-2, and PPARγ in the cervix of the ewe during the estrous cycle.CrossRef | 1:CAS:528:DC%2BC38XhsF2ru77N&md5=56d4a91c2cd0beaacaa12ea837083168CAS | 23117133PubMed |

Filipiak K, Kubiński K, Hellman U, Ramos A, de Pascual-Teresa B (2014) Human protein kinase CK2 phosphorylates matrix metalloproteinase 2 and inhibits its activity. ChemBioChem 15, 1873–1876.
Human protein kinase CK2 phosphorylates matrix metalloproteinase 2 and inhibits its activity.CrossRef | 1:CAS:528:DC%2BC2cXhtFWiurnM&md5=e4cd8dd45c086b56295c7cf8e2ca12b2CAS | 25044410PubMed |

Fosang AJ, Handley CJ (1988) Connective tissue remodelling in the ovine cervix during pregnancy and at term. Connective Tissue Research 17, 277–285.
Connective tissue remodelling in the ovine cervix during pregnancy and at term.CrossRef | 1:CAS:528:DyaL1cXksFagur8%3D&md5=76cdbaec855d4bdc03f1bc75380f4b06CAS | 3208512PubMed |

Halbert GW, Dobson H, Walton JS, Buckrell BC (1990) The structure of the cervical canal of the ewe. Theriogenology 33, 977–992.
The structure of the cervical canal of the ewe.CrossRef | 1:STN:280:DC%2BD283pvFGmtQ%3D%3D&md5=1edf9cf06db08c1004fd196d81595cf6CAS | 16726794PubMed |

Hulboy DL, Rudolph LA, Matrisian LM (1997) Matrix metalloproteinases as mediators of reproductive function. Molecular Human Reproduction 3, 27–45.
Matrix metalloproteinases as mediators of reproductive function.CrossRef | 1:CAS:528:DyaK2sXhvVeisLY%3D&md5=acba370f23f68385f17f95bc7a684e0dCAS | 9239706PubMed |

Husein MQ, Kridli RT (2003) Effect of progesterone prior to GnRH-PGF2alpha treatment on induction of oestrus and pregnancy in anoestrous Awassi ewes. Reproduction in Domestic Animals 38, 228–232.
Effect of progesterone prior to GnRH-PGF2alpha treatment on induction of oestrus and pregnancy in anoestrous Awassi ewes.CrossRef | 1:CAS:528:DC%2BD3sXkvFWlu7o%3D&md5=48105664153f6ae5473f7e9e038d085fCAS | 12753559PubMed |

Jacob-Ferreira AL, Kondo MY, Baral PK, James MN, Holt A, Fan X, Schulz R (2013) Phosphorylation status of 72 kDa MMP-2 determines its structure and activity in response to peroxynitrite. PLoS One 8, e71794
Phosphorylation status of 72 kDa MMP-2 determines its structure and activity in response to peroxynitrite.CrossRef | 1:CAS:528:DC%2BC3sXhsVWhsbbK&md5=bde93a9b49a0d2c3d586eb8ef05a6bb3CAS | 24013357PubMed |

Kandasamy AD, Chow AK, Ali MA, Schulz R (2010) Matrix metalloproteinase-2 and myocardial oxidative stress injury: beyond the matrix. Cardiovascular Research 85, 413–423.
Matrix metalloproteinase-2 and myocardial oxidative stress injury: beyond the matrix.CrossRef | 1:CAS:528:DC%2BC3cXkt1emsA%3D%3D&md5=2be5633fdd9df1b3c8c367e040bd859eCAS | 19656780PubMed |

Kershaw CM, Khalid M, McGowan MR, Ingram K, Leethongdee S, Wax G, Scaramuzzi RJ (2005) The anatomy of the sheep cervix and its influence on the transcervical passage of an inseminating pipette into the uterine lumen. Theriogenology 64, 1225–1235.
The anatomy of the sheep cervix and its influence on the transcervical passage of an inseminating pipette into the uterine lumen.CrossRef | 15904956PubMed |

Kershaw-Young CM, Khalid M, McGowan MR, Pitsillides AA, Scaramuzzi RJ (2009) The mRNA expression of prostaglandin E receptors EP2 and EP4 and the changes in glycosaminoglycans in the sheep cervix during the estrous cycle. Theriogenology 72, 251–261.
The mRNA expression of prostaglandin E receptors EP2 and EP4 and the changes in glycosaminoglycans in the sheep cervix during the estrous cycle.CrossRef | 1:CAS:528:DC%2BD1MXnsFSjtrc%3D&md5=41eeeba80e80b5f5085092842de3bc9cCAS | 19359033PubMed |

Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. The Journal of Biological Chemistry 193, 265–275.

Luque EH, Ramos JG, Rodriguez HA, Muñoz de Toro MM (1996) Dissociation in the control of cervical eosinophilic infiltration and collagenolysis at the end of pregnancy or after pseudopregnancy in ovariectomized steroid-treated rats. Biology of Reproduction 55, 1206–1212.
Dissociation in the control of cervical eosinophilic infiltration and collagenolysis at the end of pregnancy or after pseudopregnancy in ovariectomized steroid-treated rats.CrossRef | 1:CAS:528:DyaK2sXkvV2gug%3D%3D&md5=50cec9508768e4ca052537ed36299c25CAS | 8949875PubMed |

Luque EH, Bassani MM, Ramos JG, Maffini M, Canal A, Kass L, Caldini EG, Ferreira Júnior JM, Muñoz de Toro M, Montes GS (1997) Leukocyte infiltration and collagenolysis in cervical tissue from intrapartum sheep. Zentralblatt fur Veterinarmedizin. Reihe A. 44, 501–510.
Leukocyte infiltration and collagenolysis in cervical tissue from intrapartum sheep.CrossRef | 1:STN:280:DyaK1c%2Fotlyksw%3D%3D&md5=cd6978983c2a2bea4e2be8d022a3d771CAS | 9421953PubMed |

McLeod BJ, Haresign W, Lamming GE (1982) The induction of ovulation and luteal function in seasonally anoestrous ewes treated with small dose multiple injections of GnRH. Journal of Reproduction and Fertility 65, 215–221.
The induction of ovulation and luteal function in seasonally anoestrous ewes treated with small dose multiple injections of GnRH.CrossRef | 1:CAS:528:DyaL38XktVWisLw%3D&md5=47035b38b19691ead6535f62b7efab17CAS | 7042966PubMed |

Mishra B, Kizaki K, Sato T, Ito A, Hashizume K (2012) The role of extracellular matrix metalloproteinase inducer (EMMPRIN) in the regulation of bovine endometrial cell functions. Biology of Reproduction 87, 149
The role of extracellular matrix metalloproteinase inducer (EMMPRIN) in the regulation of bovine endometrial cell functions.CrossRef | 23115270PubMed |

Myers KM, Paskaleva AP, House M, Socrate S (2008) Mechanical and biochemical properties of human cervical tissue. Acta Biomaterialia 4, 104–116.
Mechanical and biochemical properties of human cervical tissue.CrossRef | 1:STN:280:DC%2BD2snpvVemtw%3D%3D&md5=5ba0e2ef44efdc621f5eb35a7b81bdaaCAS | 17904431PubMed |

Nagase H, Suzuki K, Morodomi T, Enghild JJ, Salvesen G (1992) Activation mechanisms of the precursors of matrix metalloproteinases 1, 2 and 3. Matrix (Stuttgart, Germany). Supplement 1, 237–244.

Okada Y, Morodomi T, Enghild JJ, Suzuki K, Yasui A, Nakanishi I, Salvesen G, Nagase H (1990) Matrix metalloproteinase 2 from human rheumatoid synovial fibroblasts. Purification and activation of the precursor and enzymic properties. European Journal of Biochemistry 194, 721–730.
Matrix metalloproteinase 2 from human rheumatoid synovial fibroblasts. Purification and activation of the precursor and enzymic properties.CrossRef | 1:CAS:528:DyaK3MXpvFeqsg%3D%3D&md5=831d0c35bc9e5a0242e8268d15910dbeCAS | 2269296PubMed |

Perry K, Haresign W, Wathes DC, Khalid M (2010) Intracervical application of hyaluronan improves cervical relaxation in the ewe. Theriogenology 74, 1685–1690.
Intracervical application of hyaluronan improves cervical relaxation in the ewe.CrossRef | 1:CAS:528:DC%2BC3cXhtlKhsLbE&md5=4ee9be8556d2396ece438da56c754c47CAS | 20833422PubMed |

Rajabi MR, Solomon S, Poole AR (1991) Biochemical evidence of collagenase-mediated collagenolysis as a mechanism of cervical dilatation at parturition in the guinea pig. Biology of Reproduction 45, 764–772.
Biochemical evidence of collagenase-mediated collagenolysis as a mechanism of cervical dilatation at parturition in the guinea pig.CrossRef | 1:CAS:528:DyaK3MXmsFaqsbg%3D&md5=fc3781f1f3d4cb88b2af5ce484a0e1afCAS | 1661617PubMed |

Ramos JG, Varayoud J, Bosquiazzo VL, Luque EH, Muñoz-de-Toro M (2002) Cellular turnover in the rat uterine cervix and its relationship to estrogen and progesterone receptor dynamics. Biology of Reproduction 67, 735–742.
Cellular turnover in the rat uterine cervix and its relationship to estrogen and progesterone receptor dynamics.CrossRef | 1:CAS:528:DC%2BD38XmsV2js7o%3D&md5=5a802e532f2bac2af2c8a416f230124fCAS | 12193379PubMed |

Regassa F, Noakes DE (2001) Changes in the weight, collagen concentration and content of the uterus and cervix of the ewe during pregnancy. Research in Veterinary Science 70, 61–66.
Changes in the weight, collagen concentration and content of the uterus and cervix of the ewe during pregnancy.CrossRef | 1:CAS:528:DC%2BD3MXit1eqs74%3D&md5=d003c4ddf627e204418b1284b559a625CAS | 11170854PubMed |

Robinson JJ, McKelvey WA, King ME, Mitchell SE, Mylne MJ, McEvoy TG, Dingwall WS, Williams LM (2011) Traversing the ovine cervix – a challenge for cryopreserved semen and creative science. Animal 5, 1791–1804.
Traversing the ovine cervix – a challenge for cryopreserved semen and creative science.CrossRef | 1:STN:280:DC%2BC38vovFSksQ%3D%3D&md5=017e7d21a0330866af57958dd066c07dCAS | 22440420PubMed |

Rodríguez-Piñón M, Tasende C, Puime P, Garófalo EG (2008) Oestrogens and progesterone receptor binding proteins and oestrogens receptor alpha expression (ERalpha mRNA) along the cervix in cycling ewes. Reproduction, Fertility and Development 20, 350–356.
Oestrogens and progesterone receptor binding proteins and oestrogens receptor alpha expression (ERalpha mRNA) along the cervix in cycling ewes.CrossRef |

Rodríguez-Piñón M, Tasende C, Garófalo EG (2011) Expression of genes for oestrogen and progesterone receptors in the cervix of anestrous ewes treated with gonadotrophin releasing hormone with or without progesterone priming. Animal Reproduction Science 126, 50–56.
Expression of genes for oestrogen and progesterone receptors in the cervix of anestrous ewes treated with gonadotrophin releasing hormone with or without progesterone priming.CrossRef | 21601386PubMed |

Rodríguez-Piñón M, Gonzalez R, Tasende C, Bielli A, Genovese P, Garófalo EG (2014) Cervical changes in estrogen receptor alpha, oxytocin receptor, LH receptor, and cyclooxygenase-2 depending on the histologic compartment, longitudinal axis, and day of the ovine estrous cycle. Theriogenology 81, 813–824.
Cervical changes in estrogen receptor alpha, oxytocin receptor, LH receptor, and cyclooxygenase-2 depending on the histologic compartment, longitudinal axis, and day of the ovine estrous cycle.CrossRef | 24485556PubMed |

Rodríguez-Piñón M, Tasende C, Casuriaga D, Bielli A, Genovese P, Garófalo EG (2015) Collagen degradation by extracellular matrix metalloproteinases-2 and-9 (MMP-2 and -9) in the cervix of cycling ewes. Theriogenology 84, 818–826.
Collagen degradation by extracellular matrix metalloproteinases-2 and-9 (MMP-2 and -9) in the cervix of cycling ewes.CrossRef | 26116057PubMed |

Russo LA, Peano BJ, Trivedi SP, Cavalcanto TD, Olenchock BA, Caruso JA, Smolock AR, Vishnevsky O, Gardner RM (2009) Regulated expression of matrix metalloproteinases, inflammatory mediators, and endometrial matrix remodeling by 17beta-estradiol in the immature rat uterus. Reproductive Biology and Endocrinology 7, 124
Regulated expression of matrix metalloproteinases, inflammatory mediators, and endometrial matrix remodeling by 17beta-estradiol in the immature rat uterus.CrossRef | 19889233PubMed |

Salamon S, Maxwell WMC (1995) Frozen storage of ram semen II. Causes of low fertility after cervical insemination and methods of improvement. Animal Reproduction Science 38, 1–36.
Frozen storage of ram semen II. Causes of low fertility after cervical insemination and methods of improvement.CrossRef |

Sariahmetoglu M, Crawford BD, Leon H, Sawicka J, Li L, Ballermann BJ, Holmes C, Berthiaume LG, Holt A, Sawicki G, Schulz R (2007) Regulation of matrix metalloproteinase-2 (MMP-2) activity by phosphorylation. The FASEB Journal 21, 2486–2495.
Regulation of matrix metalloproteinase-2 (MMP-2) activity by phosphorylation.CrossRef | 1:CAS:528:DC%2BD2sXptFKhurk%3D&md5=0e57ec74844e0269e3960c659b51d618CAS | 17435175PubMed |

Shan B, Li W, Yang SY, Li ZR (2013) Estrogen up-regulates MMP2/9 expression in endometrial epithelial cell via VEGF-ERK1/2 pathway. Asian Pacific Journal of Tropical Medicine 6, 826–830.
Estrogen up-regulates MMP2/9 expression in endometrial epithelial cell via VEGF-ERK1/2 pathway.CrossRef | 1:CAS:528:DC%2BC3sXhtFektr7M&md5=a9a3ec425f40315da23082ba49c53a8dCAS | 23870474PubMed |

Stetler-Stevenson WG, Krutzsch HC, Wacher MP, Margulies IMK, Liotta LA (1989) The activation of human type IV collagenase proenzyme: sequence identification of the major conversion product following organomercurial activation. The Journal of Biological Chemistry 264, 1353–1356.

Stygar D, Wang H, Vladic YS, Ekman G, Eriksson H, Sahlin L (2002) Increased level of matrix metalloproteinases 2 and 9 in the ripening process of the human cervix. Biology of Reproduction 67, 889–894.
Increased level of matrix metalloproteinases 2 and 9 in the ripening process of the human cervix.CrossRef | 1:CAS:528:DC%2BD38XmsV2jsbo%3D&md5=588acf361c408fd68ebad3da72c51fd1CAS | 12193399PubMed |

Tardif G, Reboul P, Pelletier JP, Martel-Pelletier J (2004) Ten years in the life of an enzyme: the story of the human MMP–13 (collagenase–3). Modern Rheumatology 14, 197–204.
Ten years in the life of an enzyme: the story of the human MMP–13 (collagenase–3).CrossRef | 1:CAS:528:DC%2BD2cXmtVWgsr8%3D&md5=455603ed3b4a58888baee5c6aef19f44CAS | 17143675PubMed |

Tasende C, Meikle A, Rodríguez-Piñón M, Forsberg M, Garófalo EG (2002) Estrogen and progesterone receptor content in the pituitary gland and uterus of progesterone-primed and gonadotropin releasing hormone-treated anestrous ewes. Theriogenology 57, 1719–1731.
Estrogen and progesterone receptor content in the pituitary gland and uterus of progesterone-primed and gonadotropin releasing hormone-treated anestrous ewes.CrossRef | 1:CAS:528:DC%2BD38XktlWnurk%3D&md5=d565a5d7e43f7c7b95308e5df3909beaCAS | 12035981PubMed |

Tasende C, Forsberg M, Rodríguez-Piñón M, Acuña S, Garófalo EG (2005a) Experimentally induced subnormal or normal luteal phases in sheep: reproductive hormone profiles and uterine sex steroid receptor expression. Reproduction, Fertility and Development 17, 565–571.
Experimentally induced subnormal or normal luteal phases in sheep: reproductive hormone profiles and uterine sex steroid receptor expression.CrossRef | 1:CAS:528:DC%2BD2MXktlejt7w%3D&md5=0e9b543e4441893a8126d8f98df88085CAS |

Tasende C, Rodríguez-Piñón M, Acuña S, Garófalo EG, Forsberg M (2005b) Corpus luteum life span and pituitary oestrogen and progesterone receptors in cyclic and gonadotrophin-releasing hormone-treated anoestrus ewes. Reproduction, Fertility and Development 17, 721–726.
Corpus luteum life span and pituitary oestrogen and progesterone receptors in cyclic and gonadotrophin-releasing hormone-treated anoestrus ewes.CrossRef | 1:CAS:528:DC%2BD2MXhtFKkt77F&md5=5331bb1e7c35305f5d0cb14c0d495b34CAS |

Uldbjerg N, Ulmsten U (1990) The physiology of cervical ripening and cervical dilatation and the effect of abortifacient drugs. Bailliere’s Clinical Obstetrics and Gynaecology 4, 263–282.
The physiology of cervical ripening and cervical dilatation and the effect of abortifacient drugs.CrossRef | 1:STN:280:DyaK3M%2FjtVajug%3D%3D&md5=16808fb3ad5a625c23b4748d6e4e30adCAS | 2225599PubMed |

Wang Y, Feng G, Wang J, Zhou Y, Liu Y, Shi Y, Zhu Y, Lin W, Xu Y, Li Z (2015) Differential effects of tumor necrosis factor-α on matrix metalloproteinase-2 expression in human myometrial and uterine leiomyoma smooth muscle cells. Human Reproduction (Oxford, England) 30, 61–70.
Differential effects of tumor necrosis factor-α on matrix metalloproteinase-2 expression in human myometrial and uterine leiomyoma smooth muscle cells.CrossRef | 1:CAS:528:DC%2BC2MXpsFygt70%3D&md5=f939366171353c9c76c3fd9a5608f723CAS |

Woessner JF (1991) Matrix metalloproteinases and their inhibitors in connective tissue remodeling. The FASEB Journal 5, 2145–2154.

Word RA, Li XH, Hnat M, Carrick K (2007) Dynamics of cervical remodeling during pregnancy and parturition: mechanisms and current concepts. Seminars in Reproductive Medicine 25, 69–79.
Dynamics of cervical remodeling during pregnancy and parturition: mechanisms and current concepts.CrossRef | 1:CAS:528:DC%2BD2sXhvFynurk%3D&md5=34d115b24eef1794fa4a5ce8a1d9ea6dCAS | 17205425PubMed |

Zeng L, An S, Goetzl EJ (1996) Selective regulation of RNK-16 cell matrix metalloproteinases by the PTGER4 subtype of prostaglandin E2 receptor. Biochemistry 35, 7159–7164.
Selective regulation of RNK-16 cell matrix metalloproteinases by the PTGER4 subtype of prostaglandin E2 receptor.CrossRef | 1:CAS:528:DyaK28XivFSlsrY%3D&md5=208a8dca5f3d966b62e93348e5c3cb77CAS | 8679543PubMed |



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