Ovarian expression and regulation of the stromelysins during the periovulatory period in the human and the rat

Biology of Reproduction

Volumn 86, Issue 3, 2012, Pages

  Mccord, Lauren A ^a   Li, Feixue ^a   Rosewell, Katherine L ^a   Brännström, Mats ^b   Curry, Thomas E ^b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Extracellular matrix; Granulosa cells; Matrix metalloproteinase; Ovulation; Ovulatory cycle; Proteinases; Theca cells

Indexed keywords

4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; CHORIONIC GONADOTROPIN; FORSKOLIN; MESSENGER RNA; MIFEPRISTONE; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; STROMELYSIN; STROMELYSIN 2; STROMELYSIN 3; EPIDERMAL GROWTH FACTOR; HORMONE ANTAGONIST; QUINAZOLINE DERIVATIVE; TYRPHOSTIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; FEMALE; GRANULOSA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUTEINIZATION; NONHUMAN; OVARY FOLLICLE; OVULATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SITE DIRECTED MUTAGENESIS; THECA CELL; ANIMAL; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; OVARY; SPECIES DIFFERENCE; SPRAGUE DAWLEY RAT;

ANIMALIA; EQUIDAE; RATTUS;

ANIMALS; CELLS, CULTURED; EPIDERMAL GROWTH FACTOR; FEMALE; GRANULOSA CELLS; HORMONE ANTAGONISTS; HUMANS; MATRIX METALLOPROTEINASE 10; MATRIX METALLOPROTEINASE 11; MATRIX METALLOPROTEINASE 3; MIFEPRISTONE; OVARY; OVULATION; QUINAZOLINES; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SPECIES SPECIFICITY; THECA CELLS; TYRPHOSTINS;

EID: 84860607228     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.095588     Document Type: Article

References (46)

1. Curry TE Jr, Smith MF. Impact of extracellular matrix remodeling on ovulation and the folliculo-luteal transition. Semin Reprod Med 2006;24:228-241.
2. Curry TE Jr, Osteen KG. The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev 2003; 24:428-465.
3. Ohnishi J, Ohnishi E, Shibuya H, Takahashi T. Functions for proteinases in the ovulatory process. Biochim Biophys Acta 2005; 1751:95-109.
4. Goldman S, Shalev E. MMPs and TIMPS in ovarian physiology and pathophysiology. Front Biosci 2004; 9:2474-2483.
5. Murdoch WJ, Gottsch ML. Proteolytic mechanisms in the ovulatory folliculo-luteal transformation. Connect Tissue Res 2003; 44:50-57.
6. Ny T, Wahlberg P, Brandstrom IJ. Matrix remodeling in the ovary: regulation and functional role of the plasminogen activator and matrix metalloproteinase systems. Mol Cell Endocrinol 2002; 187:29-38.
7. Smith MF, Ricke WA, Bakke LJ, Dow MPD, Smith GW. Ovarian tissue remodeling: role of matrix metalloproteinases and their inhibitors. Mol Cell Endocrinol 2002; 191:45-56.
8. Chin JR, Murphy G, Werb Z. Stromelysin, a connective tissue-degrading metalloendopeptidase secreted by stimulated rabbit synovial fibroblasts in parallel with collagenase. Biosynthesis, isolation, characterization, and substrates. J Biol Chem 1985; 260:12367-12376.
9. Muller D, Quantin B, Gesnel MC, Million-Collard R, Abecassis J, Breathnach R. The collagenase gene family in humans consists of at least four members. Biochem J 1988; 253:187-192.
10. Basset P. A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas. Nature 1990; 348:699-704.
11. Van TC, Potworowski EF, St-Pierre Y. Stromelysin-1 (MMP-3) is inducible in T lymphoma cells and accelerates the growth of lymphoid tumors in vivo. Biochem Biophys Res Commun 2004; 315:884-891.
12. Van TC, Alain T, Kossakowska AE, Urbanski S, Potworowski EF, St- Pierre Y. Stromelysin-2 (matrix metalloproteinase 10) is inducible in lymphoma cells and accelerates the growth of lymphoid tumors in vivo. J Immunol 2004; 173:3605-3611.
13. Okada A, Saez S, Misumi Y, Basset P. Rat stromelysin 3: cDNA cloning from healing skin wound, activation by furin and expression in rat tissues. Gene 1997; 185:187-193.
14. Hagglund AC, Ny A, Leonardsson G, Ny T. Regulation and localization of matrix metalloproteinases and tissue inhibitors of metalloproteinases in the mouse ovary during gonadotropin-induced ovulation. Endocrinology 1999; 140:4351-4358.
15. Hagglund AC, Basset P, Ny T. Stromelysin-3 is induced in mouse ovarian follicles undergoing hormonally controlled apoptosis, but this metalloproteinase is not required for follicular atresia. Biol Reprod 2001;64:457-463.
16. Ogiwara K, Matsui H, Kimura A, Takahashi T. Molecular cloning and partial characterization of medaka fish stromelysin-3 and its restricted expression in the oocytes of small growing follicles of the ovary. Mol Reprod Dev 2002; 61:21-31.
17. Kimura A, Kihara T, Ohkura R, Ogiwara K, Takahashi T. Localization of bradykinin B(2) receptor in the follicles of porcine ovary and increased expression of matrix metalloproteinase-3 and -20 in cultured granulosa cells by bradykinin treatment. Biol Reprod 2001; 65:1462-1470.
18. Bogusiewicz M, Rechberger T, Jakimiuk AJ, Skorupski P, Jakowicki JA. Evaluation of matrix metalloproteinases-1 and -3 concentrations in the tunic albuginea, the apical wall of atretic follicles and the corpus luteum of normal human ovaries. Gynecol Endocrinol 2000; 14:25-31.
19. Lind AK, Dahm-Kahler P, Weijdegard B, Sundfeldt K, Brannstrom M. Gelatinases and their tissue inhibitors during human ovulation: increased expression of tissue inhibitor of matrix metalloproteinase-1. Mol Hum Reprod 2006; 12:725-736.
20. Andersen AG. Als-Nielsen B, Hornnes PJ, Franch Andersen L. Time interval from human chorionic gonadotrophin (HCG) injection to follicular rupture. Hum Reprod 1995; 10:3202-3205.
21. Mann JS, Kindy MS, Edwards DR, Curry TE Jr. Hormonal regulation of matrix metalloproteinase inhibitors in rat granulosa cells and ovaries. Endocrinology 1991; 128:1825-1832.
22. Wu Q, Sucheta S, Azhar S, Menon KM. Lipoprotein enhancement of ovarian theca-interstitial cell steroidogenesis: relative contribution of scavenger receptor class B (type I) and adenosine 50-triphosphate-binding cassette (type A1) transporter in high-density lipoprotein-cholesterol transport and androgen synthesis. Endocrinology 2003; 144:2437-2445.
23. Jo M, Gieske MC, Payne CE, Wheeler-Price SE, Gieske JB, Ignatius IV, Curry TE Jr, Ko C. Development and application of a rat ovarian gene expression database (rOGED). Endocrinology 2004; 145:5384-5396.
24. Liu J, Park ES, Curry TE Jr, Jo M. Periovulatory expression of hyaluronan and proteoglycan link protein 1 (Hapln1) in the rat ovary: hormonal regulation and potential function. Mol Endocrinol 2010; 24:1203-1217.
25. Sridaran R, Rodriguez-Sierra JF, Blake CA. Ovarian involvement in the timing mechanism that controls ovulation in rats. Biol Reprod 1979;21:505-509.
26. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001; 17:463-516.
27. Woessner JF, Jr. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J 1991; 5:2145-2154.
28. Barksby HE, Milner JM, Patterson AM, Peake NJ, Hui W, Robson T, Lakey R, Middleton J, Cawston TE, Richards CD, Rowan AD. Matrix metalloproteinase 10 promotion of collagenolysis via procollagenase activation: implications for cartilage degradation in arthritis. Arthritis Rheum 2006; 54:3244-3253.
29. He C, Wilhelm SM, Pentland AP, Marmer BL, Grant GA, Eisen AZ, Goldberg GI. Tissue cooperation in a proteolytic cascade activating human interstitial collagenase. Proc Natl Acad Sci U S A 1989; 86:2632-2636.
30. Knauper V, WilhelmSM, Seperack PK, DeClerck YA, Langley KE, Osthues A, Tschesche H. Direct activation of human neutrophil procollagenase by recombinant stromelysin. Biochem J 1993; 295(pt 2): 581-586.
31. Fraser HM. Regulation of the ovarian follicular vasculature. Reprod Biol Endocrinol 2006; 4:18.
32. Chang S, Young BD, Li S, Qi X, Richardson JA, Olson EN. Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase 10. Cell 2006; 126:321-334.
33. Rodriguez JA, Orbe J, Martinez de LS, Calvayrac O, Rodriguez C, Martinez-Gonzalez J, Paramo JA. Metalloproteinases and atherothrombosis: MMP-10 mediates vascular remodeling promoted by inflammatory stimuli. Front Biosci 2008; 13:2916-2921.
34. Espey LL. Ovulation as an inflammatory reaction-a hypothesis. Biol Reprod 1980; 22:73-106.
35. Richards JS, Russell DL, Ochsner S, Espey LL. Ovulation: new dimensions and new regulators of the inflammatory-like response. Annu Rev Physiol 2002; 64:69-92.
36. Sharma SC, Richards JS. Regulation of AP1 (Jun/Fos) factor expression and activation in ovarian granulosa cells. Relation of JunD and Fra2 to terminal differentiation. J Biol Chem 2000; 275:33718-33728.
37. Katoh M, Katoh M. AP1- and NF-kappaB-binding sites conserved among mammalian WNT10B orthologs elucidate the TNFalpha-WNT10B signaling loop implicated in carcinogenesis and adipogenesis. Int J Mol Med 2007; 19:699-703.
38. Orbe J, Rodriguez JA, Calvayrac O, Rodriguez-Calvo R, Rodriguez C, Roncal C, Martinez de LS, Barrenetxe J, Reverter JC, Martinez-Gonzalez J, Paramo JA. Matrix metalloproteinase-10 is upregulated by thrombin in endothelial cells and increased in patients with enhanced thrombin generation. Arterioscler Thromb Vasc Biol 2009; 29:2109-2116.
39. Hess AP, Hamilton AE, Talbi S, Dosiou C, Nyegaard M, Nayak N, Genbecev-Krtolica O, Mavrogianis P, Ferrer K, Kruessel J, Fazleabas AT, Fisher SJ, et al. Decidual stromal cell response to paracrine signals from the trophoblast: amplification of immune and angiogenic modulators. Biol Reprod 2007; 76:102-117.
40. Zhao Y, Garcia J, Kolp L, Cheadle C, Rodriguez A, Vlahos NF. The impact of luteal phase support on gene expression of extracellular matrix protein and adhesion molecules in the human endometrium during the window of implantation following controlled ovarian stimulation with a GnRH antagonist protocol. Fertil Steril 2010; 94:2264-2271.
41. Xie G, Cheng K, Shant J, Raufman JP. Acetylcholine-induced activation of M3 muscarinic receptors stimulates robust matrix metalloproteinase gene expression in human colon cancer cells. Am J Physiol Gastrointest Liver Physiol 2009; 296:G755-G763.
42. Park-Sarge OK, Mayo KE. Transient expression of progesterone receptor messenger RNA in ovarian granulosa cells after the preovulatory luteinizing hormone surge. Mol Endocrinol 1991; 5:967-978.
43. Natraj U, Richards JS. Hormonal regulation, localization, functional activity of the progesterone receptor in granulosa cells of rat preovulatory follicles. Endocrinology 1993; 133:761-769.
44. Sekiguchi T, Mizutani T, Yamada K, Kajitani T, Yazawa T, Yoshino M, Miyamoto K. Expression of epiregulin and amphiregulin in the rat ovary. J Mol Endocrinol 2004; 33:281-291.
45. Hsieh M, Zamah AM, Conti M. Epidermal growth factor-like growth factors in the follicular fluid: role in oocyte development and maturation. Semin Reprod Med 2009; 27:52-61.
46. Peluffo MC, Murphy MJ, Talcott BS, Stouffer RL, Hennebold JD. Systematic analysis of protease gene expression in the rhesus macaque ovulatory follicle: metalloproteinase involvement in follicle rupture. Endocrinology 2011; 152:3963-3974.