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Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2010

Open Access 01-12-2010 | Research

Ovarian matrix metalloproteinases are differentially regulated during the estrous cycle but not during short photoperiod induced regression in Siberian hamsters (Phodopus sungorus)

Authors: Lisa A Vrooman, Kelly A Young

Published in: Reproductive Biology and Endocrinology | Issue 1/2010

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Abstract

Background

Matrix metalloproteinases (MMPs) are implicated as mediators for ovarian remodeling events, and are involved with ovarian recrudescence during seasonal breeding cycles in Siberian hamsters. However, involvement of these proteases as the photoinhibited ovary undergoes atrophy and regression had not been assessed. We hypothesized that 1) MMPs and their tissue inhibitors, the TIMPs would be present and differentially regulated during the normal estrous cycle in Siberian hamsters, and that 2) MMP/TIMP mRNA and protein levels would increase as inhibitory photoperiod induced ovarian degeneration.

Methods

MMP-2, -9, -14 and TIMP-1 and -2 mRNA and protein were examined in the stages of estrous (proestrus [P], estrus [E], diestrus I [DI], and diestrus II [DII]) in Siberian hamsters, as well as after exposure to 3, 6, 9, and 12 weeks of inhibitory short photoperiod (SD).

Results

MMP-9 exhibited a 1.6-1.8 fold decrease in mRNA expression in DII (p < 0.05), while all other MMPs and TIMPs tested showed no significant difference in mRNA expression in the estrous cycle. Extent of immunostaining for MMP-2 and -9 peaked in P and E then significantly declined in DI and DII (p < 0.05). Extent of immunostaining for MMP-14, TIMP-1, and TIMP-2 was significantly more abundant in P, E, and DI than in DII (p < 0.05). Localization of the MMPs and TIMPs had subtle differences, but immunostaining was predominant in granulosa and theca cells, with significant differences noted in staining intensity between preantral follicles, antral follicles, corpora lutea, and stroma classifications. No significant changes were observed in MMP and TIMP mRNA or extent of protein immunostaining with exposure to 3, 6, 9, or 12 weeks of SD, however protein was present and was localized to follicular and luteal steroidogenic cells.

Conclusions

Although MMPs appear to be involved in the normal ovarian estrus cycle at the protein level in hamsters, those examined in the present study are unlikely to be key players in the slow atrophy of tissue as seen in Siberian hamster ovarian regression.
Appendix
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Literature
1.
Bronson FH: Mammalian Reproductive Biology. 1989, Chicago: University of Chicago Press
2.
Goldman BD: Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J Biol Rhythms. 2001, 16: 283-301. 10.1177/074873001129001980.CrossRefPubMed
3.
Seegal RF, Goldman BD: Effects of photoperiod on cyclicity and serum gonadotropins in the Syrian hamster. Biol Reprod. 1975, 12: 223-231. 10.1095/biolreprod12.2.223.CrossRefPubMed
4.
Schlatt S, Niklowitz P, Hoffmann K, Nieschlag E: Influence of short photoperiods on reproductive organs and estrous cycles of normal and pinealectomized female Djungarian hamsters, Phodopus sungorus. Biol Reprod. 1993, 49: 243-250. 10.1095/biolreprod49.2.243.CrossRefPubMed
5.
Moffatt-Blue CS, Sury JJ, Young KA: Short photoperiod-induced ovarian regression is mediated by apoptosis in Siberian hamsters (Phodopus sungorus). Reproduction. 2006, 131: 771-782. 10.1530/rep.1.00870.PubMedCentralCrossRefPubMed
6.
Salverson TJ, McMichael GE, Sury JJ, Shahed A, Young KA: Differential expression of matrix metalloproteinases during stimulated ovarian recrudescence in Siberian hamsters (Phodopus sungorus). Gen Comp Endocrinol. 2008, 155: 749-761. 10.1016/j.ygcen.2007.09.003.PubMedCentralCrossRefPubMed
7.
8.
Smith MF, McIntush EW, Ricke WA, Kojima FN, Smith GW: Regulation of ovarian extracellular matrix remodelling by metalloproteinases and their tissue inhibitors: effects on follicular development, ovulation and luteal function. J Reprod Fertil Suppl. 1999, 54: 367-381.PubMed
9.
Curry TE, Osteen KG: The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev. 2003, 24: 428-465. 10.1210/er.2002-0005.CrossRefPubMed
10.
Bagavandoss P: Differential distribution of gelatinases and tissue inhibitor of metalloproteinase-1 in the rat ovary. J Endocrinol. 1998, 158: 221-228. 10.1677/joe.0.1580221.CrossRefPubMed
11.
Curry TE, Song L, Wheeler SE: Cellular localization of gelatinases and tissue inhibitors of metalloproteinases during follicular growth, ovulation, and early luteal formation in the rat. Biol Reprod. 2001, 65: 855-865. 10.1095/biolreprod65.3.855.CrossRefPubMed
12.
Simpson KS, Byers MJ, Curry TE: Spatiotemporal messenger ribonucleic acid expression of ovarian tissue inhibitors of metalloproteinases throughout the rat estrous cycle. Endocrinology. 2001, 142: 2058-2069. 10.1210/en.142.5.2058.PubMed
13.
Goldman S, Shalev E: MMPS and TIMPS in ovarian physiology and pathophysiology. Front Biosci. 2004, 9: 2474-2483. 10.2741/1409.CrossRefPubMed
14.
Liu K, Olofsson JI, Wahlberg P, Ny T: Distinct expression of gelatinase A [matrix metalloproteinase (MMP)-2], collagenase-3 (MMP-13), membrane type MMP 1 (MMP-14), and tissue inhibitor of MMPs type 1 mediated by physiological signals during formation and regression of the rat corpus luteum. Endocrinology. 1999, 140: 5330-5338. 10.1210/en.140.11.5330.PubMed
15.
Pitzel L, Ludemann S, Wuttke W: Secretion and gene expression of metalloproteinases and gene expression of their inhibitors in porcine corpora lutea at different stages of the luteal phase. Biol Reprod. 2000, 62: 1121-1127. 10.1095/biolreprod62.5.1121.CrossRefPubMed
16.
Young KA, Stouffer RL: 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. 2004, 70: 244-252. 10.1095/biolreprod.103.022053.CrossRefPubMed
17.
Jo M, Thomas LE, Wheeler SE, Curry TE: Membrane type 1-matrix metalloproteinase (MMP)-associated MMP-2 activation increases in the rat ovary in response to an ovulatory dose of human chorionic gonadotropin. Biol Reprod. 2004, 70: 1024-1032. 10.1095/biolreprod.103.023499.CrossRefPubMed
18.
Garcia R, Ballesteros LM, Hernandez-Perez O, Rosales AM, Espinosa R, Soto H, Diaz de Leon L, Rosado A: Metalloproteinase activity during growth, maturation and atresia in the ovarian follicles of the goat. Anim Reprod Sci. 1997, 47: 211-228. 10.1016/S0378-4320(96)01637-5.CrossRefPubMed
19.
Robker RL, Russell DL, Espey LL, Lydon JP, O'Malley BW, Richards JS: Progesterone-regulated genes in the ovulation process: ADAMTS-1 and cathepsin L proteases. Proc Natl Acad Sci USA. 2000, 97: 4689-4694. 10.1073/pnas.080073497.PubMedCentralCrossRefPubMed
20.
Chaffin CL, Stouffer RL: Expression of matrix metalloproteinases and their tissue inhibitor messenger ribonucleic acids in macaque periovulatory granulosa cells: time course and steroid regulation. Biol Reprod. 1999, 61: 14-21. 10.1095/biolreprod61.1.14.CrossRefPubMed
21.
Nagase H, Visse R, Murphy G: Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res. 2006, 69: 562-573. 10.1016/j.cardiores.2005.12.002.CrossRefPubMed
22.
Bakke LJ, Dow MP, Cassar CA, Peters MW, Pursley JR, Smith GW: Effect of the preovulatory gonadotropin surge on matrix metalloproteinase (MMP)-14, MMP-2, and tissue inhibitor of metalloproteinases-2 expression within bovine periovulatory follicular and luteal tissue. Biol Reprod. 2002, 66: 1627-1634. 10.1095/biolreprod66.6.1627.CrossRefPubMed
23.
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. 10.1210/en.140.9.4351.PubMed
24.
Zhang B, Yan L, Moses MA, Tsang PC: Bovine membrane-type 1 matrix metalloproteinase: molecular cloning and expression in the corpus luteum. Biol Reprod. 2002, 67: 99-106. 10.1095/biolreprod67.1.99.CrossRefPubMed
25.
Gomez DE, Alonso DF, Yoshiji H, Thorgeirsson UP: Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur J Cell Biol. 1997, 74: 111-122.PubMed
26.
Baker AH, Edwards DR, Murphy G: Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci. 2002, 115: 3719-3727. 10.1242/jcs.00063.CrossRefPubMed
27.
Reich R, Daphna-Iken D, Chun SY, Popliker M, Slager R, Adelmann-Grill BC, Tsafriri A: Preovulatory changes in ovarian expression of collagenases and tissue metalloproteinase inhibitor messenger ribonucleic acid: role of eicosanoids. Endocrinology. 1991, 129: 1869-1875. 10.1210/endo-129-4-1869.CrossRefPubMed
28.
Smith GW, Goetz TL, Anthony RV, Smith MF: Molecular cloning of an ovine ovarian tissue inhibitor of metalloproteinases: ontogeny of messenger ribonucleic acid expression and in situ localization within preovulatory follicles and luteal tissue. Endocrinology. 1994, 134: 344-352. 10.1210/en.134.1.344.PubMed
29.
McIntush EW, Pletz JD, Smith GD, Long DK, Sawyer HR, Smith MF: Immunolocalization of tissue inhibitor of metalloproteinases-1 within ovine periovulatory follicular and luteal tissues. Biol Reprod. 1996, 54: 871-878. 10.1095/biolreprod54.4.871.CrossRefPubMed
30.
Lind AK, Dahm-Kahler P, Weijdegard B, Sundfeldt , 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. 10.1093/molehr/gal086.CrossRefPubMed
31.
Peters H, McNatty KP: The Ovary. 1980, Berkeley and Los Angeles, CA: University of California Press
32.
Numazawa A, Kawashima S: Morphometric studies on ovarian follicles and corpora lutea during the oestrous cycle in the mouse. J Reprod Fertil. 1982, 64: 275-283. 10.1530/jrf.0.0640275.CrossRefPubMed
33.
Hirshfield AN: Size-frequency analysis of atresia in cycling rats. Biol Reprod. 1988, 38: 1181-1188. 10.1095/biolreprod38.5.1181.CrossRefPubMed
34.
Scotti MA, Place NJ, Demas GE: Short-day increases in aggression are independent of circulating gonadal steroids in female Siberian hamsters (Phodopus sungorus). Horm Behav. 2007, 52: 183-190. 10.1016/j.yhbeh.2007.03.029.CrossRefPubMed
35.
Oksjoki S, Sallinen S, Vuorio E, Anttila L: Cyclic expression of mRNA transcripts for connective tissue components in the mouse ovary. Mol Hum Reprod. 1999, 5: 803-808. 10.1093/molehr/5.9.803.CrossRefPubMed
36.
Guo H, Zucker S, Gordon MK, Toole BP, Biswas C: Stimulation of matrix metalloproteinase production by recombinant extracellular matrix metalloproteinase inducer from transfected Chinese hamster ovary cells. J Biol Chem. 1997, 272: 24-27. 10.1074/jbc.272.1.24.CrossRefPubMed
37.
Ramos-DeSimone N, Hahn-Dantona E, Sipley J, Nagase H, French DL, Quigley JP: Activation of matrix metalloproteinase-9 (MMP-9) via a converging plasmin/stromelysin-1 cascade enhances tumor cell invasion. J Biol Chem. 1999, 274: 13066-13076. 10.1074/jbc.274.19.13066.CrossRefPubMed
38.
Monea S, Lehti K, Keski-Oja J, Mignatti P: Plasmin activates pro-matrix metalloproteinase-2 with a membrane-type 1 matrix metalloproteinase-dependent mechanism. J Cell Physiol. 2002, 192: 160-170. 10.1002/jcp.10126.CrossRefPubMed
39.
Zhang X, Christenson LK, Nothnick WB: Regulation of MMP-9 expression and activity in the mouse uterus by estrogen. Mol Reprod Dev. 2007, 74: 321-331. 10.1002/mrd.20582.CrossRefPubMed
40.
Puistola U, Westerlund A, Kauppila A, Turpeenniemi-Hujanen T: Regulation of 72-kd type IV collagenase-matrix metalloproteinase-2 by estradiol and gonadotropin-releasing hormone agonist in human granulosa-lutein cells. Fertil Steril. 1995, 64: 81-87.PubMed
Metadata
Title
Ovarian matrix metalloproteinases are differentially regulated during the estrous cycle but not during short photoperiod induced regression in Siberian hamsters (Phodopus sungorus)
Authors
Lisa A Vrooman
Kelly A Young
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2010
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-8-79

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