Systematic analysis of protease gene expression in the rhesus macaque ovulatory follicle: Metalloproteinase involvement in follicle rupture

Endocrinology

Volumn 152, Issue 10, 2011, Pages 3963-3974

  Peluffo, Marina C ^a   Murphy, Melinda J ^a   Baughman, Serena Talcott ^a   Stouffer, Richard L ^a,b   Hennebold, Jon D ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAMTS1 PROTEIN; AGGRECANASE 1; CATHEPSIN L; CHORIONIC GONADOTROPIN; DISINTEGRIN; GELATINASE B; ILOMASTAT; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE 19; MESSENGER RNA; METALLOPROTEINASE; METALLOPROTEINASE ADAMTS15; METALLOPROTEINASE ADAMTS9; PEPSINOGEN 5; PROGESTERONE; STROMELYSIN 2; UNCLASSIFIED DRUG; UROKINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME INHIBITION; ESTROGEN SYNTHESIS; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; HISTOLOGY; LUTEAL PHASE; NONHUMAN; OOCYTE; OVARY FOLLICLE CELL; OVULATION; PRIORITY JOURNAL; PROGESTERONE SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; RHESUS MONKEY; UPREGULATION;

ANIMALS; CHORIONIC GONADOTROPIN; ESTROGENS; FEMALE; MACACA MULATTA; METALLOPROTEASES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OVARIAN FOLLICLE; PROGESTERONE; RNA, MESSENGER;

EID: 80053156224     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-1172     Document Type: Article

References (55)

1. Curry Jr TE, Osteen KG 2003 The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev 24:428-465 (Pubitemid 37056240)
2. Morales TI, Woessner Jr JF, Marsh JM, Le Maire WJ 1983 Collagen, collagenase and collagenolytic activity in rat Graafian follicles during follicular growth and ovulation. Biochim Biophys Acta 756:119-122 (Pubitemid 13130184)
3. Fukumoto M, Yajima Y, Okamura H, Midorikawa O 1981 Collagenolytic enzyme activity in human ovary: an ovulatory enzyme system. Fertil Steril 36:746-750 (Pubitemid 12193592)
4. Espey LL 1976 The distribution of collagenous connective tissue in rat ovarian follicles. Biol Reprod 14:502-506
5. Espey LL 1967 Ultrastructure of the apex of the rabbit graafian follicle during the ovulatory process. Endocrinology 81:267-276
6. Hazzard TM, Stouffer RL 2000 Angiogenesis in ovarian follicular and luteal development. Baillieres Best Pract Res Clin Obstet Gynaecol 14:883-900 (Pubitemid 32123679)
7. Brown HM, Dunning KR, Robker RL, Boerboom D, Pritchard M, Lane M, Russell DL 2010 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
8. D'Alessandris C, Canipari R, Di Giacomo M, Epifano O, Camaioni A, Siracusa G, Salustri A 2001 Control of mouse cumulus cell-oocyte complex integrity before and after ovulation: plasminogen activator synthesis and matrix degradation. Endocrinology 142:3033-3040 (Pubitemid 32575541)
9. Ny T, Wahlberg P, Brändström IJ 2002 Matrix remodeling in the ovary: regulation and functional role of the plasminogen activator and matrix metalloproteinase systems. Mol Cell Endocrinol 187:29-38 (Pubitemid 34441038)
10. Shindo T, Kurihara H, Kuno K, Yokoyama H, Wada T, Kurihara Y, Imai T, Wang Y, Ogata M, Nishimatsu H, Moriyama N, Oh-hashi Y, Morita H, Ishikawa T, Nagai R, Yazaki Y, Matsushima K 2000 ADAMTS-1: a metalloproteinase-disintegrin essential for normal growth, fertility, and organ morphology and function. J Clin Invest 105:1345-1352 (Pubitemid 30322400)
11. Leonardsson G, Peng XR, Liu K, Nordström L, Carmeliet P, Mulligan R, Collen D, Ny T 1995 Ovulation efficiency is reduced in mice that lack plasminogen activator gene function: functional redundancy among physiological plasminogen activators. Proc Natl Acad Sci USA 92:12446-12450 (Pubitemid 26014086)
12. Sternlicht MD, Werb Z 2001 How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17:463-516 (Pubitemid 33096184)
13. Ny A, Leonardsson G, Hägglund AC, Hägglöf P, Ploplis VA, Carmeliet P, Ny T 1999 Ovulation in plasminogen-deficient mice. Endocrinology 140:5030-5035
14. Huang YY, Bach ME, Lipp HP, Zhuo M, Wolfer DP, Hawkins RD, Schoonjans L, Kandel ER, Godfraind JM, Mulligan R, Collen D, Carmeliet P 1996 Mice lacking the gene encoding tissue-type plasminogen activator show a selective interference with late-phase long-term potentiation in both Schaffer collateral and mossy fiber pathways. Proc Natl Acad Sci USA 93:8699-8704 (Pubitemid 26269623)
15. Carmeliet P, Schoonjans L, Kieckens L, Ream B, Degen J, Bronson R, De Vos R, Van den Oord JJ, Collen D, Mulligan RC 1994 Physiological consequences of loss of plasminogen activator gene function in mice. Nature 368:419-424 (Pubitemid 24115347)
16. Puente XS, Sánchez LM, Overall CM, López-Otín C 2003 Human and mouse proteases: a comparative genomic approach. Nat Rev Genet 4:544-558 (Pubitemid 36781345)
17. Xu F, Stouffer RL, Müller J, Hennebold JD, Wright JW, Bahar A, Leder G, Peters M, Thorne M, Sims M, Wintermantel T, Lindenthal B 2011 Dynamics of the transcriptome in the primate ovulatory follicle. Mol Hum Reprod 17:152-165
18. Young KA, Chaffin CL, Molskness TA, Stouffer RL 2003 Controlled ovulation of the dominant follicle: a critical role for LH in the late follicular phase of the menstrual cycle. Hum Reprod 18:2257-2263 (Pubitemid 37427800)
19. Wolf DP, Thomson JA, Zelinski-Wooten MB, Stouffer RL 1990 In vitro fertilization-embryo transfer in nonhuman primates: the technique and its applications. Mol Reprod Dev 27:261-280 (Pubitemid 20369549)
20. Duffy DM, Chaffin CL, Stouffer RL 2000 Expression of estrogen receptor alpha and beta in the rhesus monkey corpus luteum during the menstrual cycle: regulation by luteinizing hormone and progesterone. Endocrinology 141:1711-1717 (Pubitemid 32274401)
21. Xu F, Stouffer RL 2005 Local delivery of angiopoietin-2 into the preovulatory follicle terminates the menstrual cycle in rhesus monkeys. Biol Reprod 72:1352-1358 (Pubitemid 40696078)
22. Duffy DM, Stouffer RL 2002 Follicular administration of a cyclooxygenase inhibitor can prevent oocyte release without alteration of normal luteal function in rhesus monkeys. Hum Reprod 17:2825-2831 (Pubitemid 35350896)
23. Hazzard TM, Rohan RM, Molskness TA, Fanton JW, D'Amato RJ, Stouffer RL 2002 Injection of antiangiogenic agents into the macaque preovulatory follicle: disruption of corpus luteum development and function. Endocrine 17:199-206 (Pubitemid 34701365)
24. Hibbert ML, Stouffer RL, Wolf DP, Zelinski-Wooten MB 1996 Midcycle administration of a progesterone synthesis inhibitor prevents ovulation in primates. Proc Natl Acad Sci USA 93:1897-1901 (Pubitemid 26079851)
25. Rawson JM, Dukelow WR 1973 Observation of ovulation in Macaca fascicularis. J Reprod Fertil 34:187-190
26. Bogan RL, Murphy MJ, Stouffer RL, Hennebold JD 2008 Systematic determination of differential gene expression in the primate corpus luteum during the luteal phase of the menstrual cycle. Mol Endocrinol 22:1260-1273 (Pubitemid 351629624)
27. Young KA, Hennebold JD, Stouffer RL 2002 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 8:833-840 (Pubitemid 35012471)
28. Jo M, Curry Jr TE 2004 Regulation of matrix metalloproteinase-19 messenger RNA expression in the rat ovary. Biol Reprod 71:1796-1806 (Pubitemid 39586922)
29. Balbín M, Fueyo A, López JM, Díez-Itza I, Velasco G, López-Otín C 1996 Expression of collagenase-3 in the rat ovary during the ovulatory process. J Endocrinol 149:405-415 (Pubitemid 26196072)
30. Reich R, Daphna-Iken D, Chun SY, Popliker M, Slager R, Adelmann-Grill BC, Tsafriri A 1991 Preovulatory changes in ovarian expression of collagenases and tissue metalloproteinase inhibitor messenger ribonucleic acid: role of eicosanoids. Endocrinology 129:1869-1875
31. Hägglund AC, Ny A, Leonardsson G, Ny T 1999 Regulation and localization of matrix metalloproteinases and tissue inhibitors of metalloproteinases in the mouse ovary during gonadotropin-induced ovulation. Endocrinology 140:4351-4358 (Pubitemid 30647134)
32. Yamashita Y, Kawashima I, Yanai Y, Nishibori M, Richards JS, Shimada M 2007 Hormone-induced expression of tumor necrosis factor alpha-converting enzyme/A disintegrin and metalloprotease-17 impacts porcine cumulus cell oocyte complex expansion and meiotic maturation via ligand activation of the epidermal growth factor receptor. Endocrinology 148:6164-6175 (Pubitemid 350146189)
33. Miyakoshi K, Murphy MJ, Yeoman RR, Mitra S, Dubay CJ, Hennebold JD 2006 The identification of novel ovarian proteases through the use of genomic and bioinformatic methodologies. Biol Reprod 75:823-835 (Pubitemid 44845587)
34. Young KA, Tumlinson B, Stouffer RL 2004 ADAMTS-1/METH-1 and TIMP-3 expression in the primate corpus luteum: divergent patterns and stage-dependent regulation during the natural menstrual cycle. Mol Hum Reprod 10:559-565 (Pubitemid 39136814)
35. Yung Y, Maman E, Konopnicki S, Cohen B, Brengauz M, Lojkin I, Dal Canto M, Fadini R, Dor J, Hourvitz A 2010 ADAMTS-1: a new human ovulatory gene and a cumulus marker for fertilization capacity. Mol Cell Endocrinol 328:104-108
36. Espey LL, Yoshioka S, Russell DL, Robker RL, Fujii S, Richards JS 2000 Ovarian expression of a disintegrin and metalloproteinase with thrombospondin motifs during ovulation in the gonadotropin-primed immature rat. Biol Reprod 62:1090-1095 (Pubitemid 30173826)
37. Robker RL, Russell DL, Espey LL, Lydon JP, O'Malley BW, Richards JS 2000 Progesterone-regulated genes in the ovulation process: ADAMTS-1 and cathepsin L proteases. Proc Natl Acad Sci USA 97:4689-4694 (Pubitemid 30238619)
38. Russell DL, Doyle KM, Ochsner SA, Sandy JD, Richards JS 2003 Processing and localization of ADAMTS-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation. J Biol Chem 278:42330-42339 (Pubitemid 37310502)
39. Madan P, Bridges PJ, Komar CM, Beristain AG, Rajamahendran R, Fortune JE, MacCalman CD 2003 Expression of messenger RNA for ADAMTS subtypes changes in the periovulatory follicle after the gonadotropin surge and during luteal development and regression in cattle. Biol Reprod 69:1506-1514 (Pubitemid 37362832)
40. Doyle KM, Russell DL, Sriraman V, Richards JS 2004 Coordinate transcription of the ADAMTS-1 gene by luteinizing hormone and progesterone receptor. Mol Endocrinol 18:2463-2478 (Pubitemid 39335981)
41. Richards JS, Hernandez-Gonzalez I, Gonzalez-Robayna I, Teuling E, Lo Y, Boerboom D, Falender AE, Doyle KH, LeBaron RG, Thompson V, Sandy JD 2005 Regulated expression of ADAMTS family members in follicles and cumulus oocyte complexes: evidence for specific and redundant patterns during ovulation. Biol Reprod 72:1241-1255 (Pubitemid 40547989)
42. Murphy G, Stanton H, Cowell S, Butler G, Knäuper V, Atkinson S, Gavrilovic J 1999 Mechanisms for pro matrix metalloproteinase activation. APMIS 107:38-44 (Pubitemid 29133521)
43. Gritti I, Banfi G, Roi GS 2000 Pepsinogens: physiology, pharmacology pathophysiology and exercise. Pharmacol Res 41:265-281 (Pubitemid 30663131)
44. Rojo JV, Merino AM, González LO, Vizoso F 2002 Expression and clinical significance of pepsinogen C in epithelial ovarian carcinomas. Eur J Obstet Gynecol Reprod Biol 104:58-63 (Pubitemid 34786393)
45. Hirsch-Marie H, Bara J, Loisillier F, Burtin P, Bachimont J, Van Eggenpoel MJ 1978 Evidence of pepsinogens in ovarian tumors. Eur J Cancer 14:593-598 (Pubitemid 8336080)
46. Curry Jr TE, Song L, Wheeler SE 2001 Cellular localization of gelatinases and tissue inhibitors of metalloproteinases during follicular growth, ovulation, and early luteal formation in the rat. Biol Reprod 65:855-865 (Pubitemid 32777373)
47. Mittaz L, Russell DL, Wilson T, Brasted M, Tkalcevic J, Salamonsen LA, Hertzog PJ, Pritchard MA 2004 Adamts-1 is essential for the development and function of the urogenital system. Biol Reprod 70:1096-1105 (Pubitemid 38387721)
48. Liu K, Wahlberg P, Leonardsson G, Hägglund AC, Ny A, Bodén I, Wibom C, Lund LR, Ny T 2006 Successful ovulation in plasminogen-deficient mice treated with the broad-spectrum matrix metalloproteinase inhibitor galardin. Dev Biol 295:615-622 (Pubitemid 43927698)
49. Gottsch ML, Van Kirk EA, Murdoch WJ 2002 Role of matrix metalloproteinase 2 in the ovulatory folliculo-luteal transition of ewes. Reproduction 124:347-352 (Pubitemid 35023567)
50. Young KA, Stouffer RL 2004 Gonadotropin and steroid regulation of matrix metalloproteinases and their endogenous tissue inhibitors in the developed corpus luteum of the rhesus monkey during the menstrual cycle. Biol Reprod 70:244-252 (Pubitemid 38063573)
51. Brew K, Nagase H 2010 The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim Biophys Acta 1803:55-71
52. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M 2004 EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303:682-684 (Pubitemid 38141636)
53. Panigone S, Hsieh M, Fu M, Persani L, Conti M 2008 Luteinizing hormone signaling in preovulatory follicles involves early activation of the epidermal growth factor receptor pathway. Mol Endocrinol 22:924-936 (Pubitemid 351482828)
54. Ashkenazi H, Cao X, Motola S, Popliker M, Conti M, Tsafriri A 2005 Epidermal growth factor family members: endogenous mediators of the ovulatory response. Endocrinology 146:77-84 (Pubitemid 40051726)
55. Rawlings ND, Barrett AJ, Bateman A 2010 MEROPS: the peptidase database. Nucleic Acids Res 38:D227-D233