Localization and hormonal regulation of endometrial matrix metalloproteinase-26 in the rhesus macaque

Human Reproduction

Volumn 27, Issue 6, 2012, Pages 1723-1734

  Almeida Francia, C C D ^a   Keator, C S ^b   Mah, K ^c   Holden, L ^c   Hergert, C ^c   Slayden, O D ^c  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b ROSS UNIVERSITY SCHOOL OF MEDICINE   (Dominica)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Endometrium; Estradiol; Matrix metalloproteinase 26; Progesterone; Rhesus macaque

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR ALPHA; MATRIX METALLOPROTEINASE 26; PROGESTERONE; PROGESTERONE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DECIDUALIZATION; ENDOMETRIUM; FEMALE; HORMONAL REGULATION; MACACA; MENSTRUAL CYCLE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ANIMALIA; MACACA; MACACA MULATTA; PRIMATES;

EID: 84861541166     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/des086     Document Type: Article

References (54)

1. Afonso S, Romagnano L, Babiarz B. Expression of cathepsin proteinases by mouse trophoblast in vivo and in vitro. Dev Dyn 1999;216:374-384.
2. Alexander CM, Hansell EJ, Behrendtsen O, Flannery ML, Kishnani NS, Hawkes SP, Werb Z. Expression and function of matrix metalloproteinases and their inhibitors at the maternal-embryonic boundary during mouse embryo implantation. Development 1996; 122:1723-1736.
3. Bischof P, Campana A. Molecular mediators of implantation. Baillieres Best Pract Res Clin Obstet Gynaecol 2000;14:801-814.
4. Bister VO, Salmela MT, Karjalainen-Lindsberg ML, Uria J, Lohi J, Puolakkainen P, Lopez-Otin C, Saarialho-Kere U. Differential expression of three matrix metalloproteinases, MMP-19, MMP-26, and MMP-28, in normal and inflamed intestine and colon cancer. Dig Dis Sci 2004;49:653-661.
5. Brenner RM, Slayden OD. Cyclic changes in the primate oviduct and endometrium. In: Knobil E, Neill JD (eds). The Physiology of Reproduction. New York: Raven Press, 1994,541-569.
6. Bruner KL, Rodgers WH, Gold LI, Korc M, Hargrove JT, Matrisian LM, Osteen KG. Transforming growth factor beta mediates the progesterone suppression of an epithelial metalloproteinase by adjacent stroma in the human endometrium. Proc Natl Acad Sci USA 1995;92:7362-7366.
7. Carroll RL, Mah K, Fanton JW, Maginnis GN, Brenner RM, Slayden OD. Assessment of menstruation in the Vervet (Cercopithecus aethiops). Am J Primatol 2007;69:901-916.
8. Chakraborti S, Mandal M, Das S, Mandal A, Chakraborti T. Regulation of matrix metalloproteinases: an overview. Mol Cell Biochem 2003; 253:269-285.
9. Chegini N, Zhao Y, Williams RS, Flanders KC. Human uterine tissue throughout the menstrual cycle expresses transforming growth factor-beta 1 (TGF beta 1), TGF beta 2, TGF beta 3, and TGF beta type II receptor messenger ribonucleic acid and protein and contains [125I]TGF beta 1-binding sites. Endocrinology 1994;135:439-449.
10. Clark JH, Peck EJ Jr. Female sex steroids: receptors and function. In: Gross F, Grumbach MM, Labhart A, Lipsett MB, Mann T, Samuels LT, Zander J (eds). 'Monographs on Endocrinology'. NY: Springer-Verlag, 1979.
11. Cohen M, Bischof P. Factors regulating trophoblast invasion. Gynecol Obstet Invest 2007;64:126-130.
12. Deng Y, Li W, Li Y, Yang H, Xu H, Liang S, Zhang L, Li Y. Expression of matrix metalloproteinase-26 promotes human glioma U251 cell invasion in vitro and in vivo. Oncol Rep 2010;23:69-78.
13. Fadare O, Zheng W. Histologic dating of the endometrium: accuracy, reproducibility, and practical value. Adv Anat Pathol 2005;12:39-46.
14. Fata JE, Ho AT, Leco KJ, Moorehead RA, Khokha R. Cellular turnover and extracellular matrix remodeling in female reproductive tissues: functions of metalloproteinases and their inhibitors. Cell Mol Life Sci 2000; 57:77-95.
15. Gaide Chevronnay HP, Cornet PB, Delvaux D, Lemoine P, Courtoy PJ, Henriet P, Marbaix E. Opposite regulation of transforming growth factors-beta2 and-beta3 expression in the human endometrium. Endocrinology 2008;149:1015-1025.
16. Galewska Z, Romanowicz L, Jaworski S, Bankowski E. Matrix metalloproteinases, MMP-7 and MMP-26, in plasma and serum of control and preeclamptic umbilical cord blood. Eur J Obstet Gynecol Reprod Biol 2010;150:152-156.
17. Ghosh D, Najwa AR, Khan MA, Sengupta J. IGF2, IGF binding protein 1, and matrix metalloproteinases 2 and 9 in implantation-stage endometrium following immunoneutralization of vascular endothelial growth factor in the rhesus monkey. Reproduction 2011;141:501-509.
18. Goffin F, Munaut C, Frankenne F, Perrier DS, Beliard A, Fridman V, Nervo P, Colige A, Foidart JM. Expression pattern of metalloproteinases and tissue inhibitors of matrix-metalloproteinases in cycling human endometrium. Biol Reprod 2003;69:976-984.
19. Gray CA, Bartol FF, Tarleton BJ, Wiley AA, Johnson GA, Bazer FW, Spencer TE. Developmental biology of uterine glands. Biol Reprod 2001;65:1311-1323.
20. Grevin D, Chen JH, Raes MB, Stehelin D, Vandenbunder B, Desbiens X. Involvement of the proto-oncogene c-ets 1 and the urokinase plasminogen activator during mouse implantation and placentation. Int J Dev Biol 1993;37:519-529.
21. Hurst PR, Palmay RD. Matrix metalloproteinases and their endogenous inhibitors during the implantation period in the rat uterus. Reprod Fertil Dev 1999;11:395-402.
22. Kao LC, Tulac S, Lobo S, Imani B, Yang JP, Germeyer A, Osteen K, Taylor RN, Lessey BA, Giudice LC. Global gene profiling in human endometrium during the window of implantation. Endocrinology 2002; 143:2119-2138.
23. Keator CS, Mah K, Ohm L, Slayden OD. Estrogen and progesterone regulate expression of the endothelins in the rhesus macaque endometrium. Hum Reprod 2011;26:1715-1728.
24. Li Q, Wang H, Zhao Y, Lin H, Sang QA, Zhu C. Identification and specific expression of matrix metalloproteinase-26 in rhesus monkey endometrium during early pregnancy. Mol Hum Reprod 2002; 8:934-940.
25. Marchenko GN, Ratnikov BI, Rozanov DV, Godzik A, Deryugina EI, Strongin AY. Characterization of matrix metalloproteinase-26, a novel metalloproteinase widely expressed in cancer cells of epithelial origin. Biochem J 2001;356:705-718.
26. Marchenko GN, Marchenko ND, Leng J, Strongin AY. Promoter characterization of the novel human matrix metalloproteinase-26 gene: regulation by the T-cell factor-4 implies specific expression of the gene in cancer cells of epithelial origin. Biochem J 2002; 363:253-262.
27. Menino AR Jr, Hogan A, Schultz GA, Novak S, Dixon W, Foxcroft GH. Expression of proteinases and proteinase inhibitors during embryo-uterine contact in the pig. Dev Genet 1997;21:68-74.
28. Murray MJ, Meyer WR, Zaino RJ, Lessey BA, Novotny DB, Ireland K, Zeng D, Fritz MA. A critical analysis of the accuracy, reproducibility, and clinical utility of histologic endometrial dating in fertile women. Fertil Steril 2004;81:1333-1343.
29. Nolan T, Hands RE, Bustin SA. Quantification of mRNA using real-time RT-PCR. Nat Protoc 2006;1:1559-1582.
30. Noyes RW, Hertig AT, Rock J. Dating the endometrial biopsy. Fertil Steril 1950;1:3-25.
31. Paria BC, Lim H, Das SK, Reese J, Dey SK. Molecular signaling in uterine receptivity for implantation. Semin Cell Dev Biol 2000;11:67-76.
32. Parmar T, Gadkar-Sable S, Savardekar L, Katkam R, Dharma S, Meherji P, Puri CP, Sachdeva G. Protein profiling of human endometrial tissues in the midsecretory and proliferative phases of the menstrual cycle. Fertil Steril 2009;92:1091-1103.
33. Petersen RG. Design and Analysis of Experiments, 66th edn. New York: Marcel Dekker, Inc., 1985.
34. Pilka R, Whatling C, Domanski H, Hansson S, Eriksson P, Casslen B. Epithelial expression of matrix metalloproteinase-26 is elevated at mid-cycle in the human endometrium. Mol Hum Reprod 2003; 9:271-277.
35. Pilka R, Domanski H, Hansson S, Eriksson P, Casslen B. Endometrial TIMP-4 mRNA is high at midcycle and in hyperplasia, but down-regulated in malignant tumours. Coordinated expression with MMP-26. Mol Hum Reprod 2004a;10:641-650.
36. Pilka R, Norata GD, Domanski H, Andersson C, Hansson S, Eriksson P, Casslen B. Matrix metalloproteinase-26 (matrilysin-2) expression is high in endometrial hyperplasia and decreases with loss of histological differentiation in endometrial cancer. Gynecol Oncol 2004b;94:661-670.
37. Pilka R, Oborna I, Lichnovsky V, Havelka P, Fingerova H, Eriksson P, Hansson S, Casslen B. Endometrial expression of the estrogen-sensitive genes MMP-26 and TIMP-4 is altered by a substitution protocol without down-regulation in IVF patients. Hum Reprod 2006;21:3146-3156.
38. Rudolph-Owen LA, Slayden OD, Matrisian LM, Brenner RM. Matrix metalloproteinase expression in Macaca mulatta endometrium: evidence for zone-specific regulatory tissue gradients. Biol Reprod 1998;59:1349-1359.
39. Salamonsen LA. Role of proteases in implantation. Rev Reprod 1999; 4:11-22.
40. Salamonsen LA, Woolley DE. Matrix metalloproteinases and their tissue inhibitors in endometrial remodelling and menstruation. Reprod Med Rev 1996;5:185-203.
41. SAS Institute, Inc. SAS/INSIGHT 9.2 User's Guide, Vol. 1, 2nd edn. Cary, NC: SAS Institute Inc., 2008.
42. Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, Gassmann M, Lightfoot S, Menzel W, Granzow M, Ragg T. The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 2006;7:3.
43. Shibata S, Marushima H, Asakura T, Matsuura T, Eda H, Aoki K, Matsudaira H, Ueda K, Ohkawa K. Three-dimensional culture using a radial flow bioreactor induces matrix metalloprotease 7-mediated EMT-like process in tumor cells via TGFbeta1/Smad pathway. Int J Oncol 2009;34:1433-1448.
44. Singh H, Aplin JD. Adhesion molecules in endometrial epithelium: tissue integrity and embryo implantation. J Anat 2009;215:3-13.
45. Skoog T, Ahokas K, Orsmark C, Jeskanen L, Isaka K, Saarialho-Kere U. MMP-21 is expressed by macrophages and fibroblasts in vivo and in culture. Exp Dermatol 2006;15:775-783.
46. Slayden OD, Brenner RM. Hormonal regulation and localization of estrogen, progestin and androgen receptors in the endometrium of nonhuman primates: effects of progesterone receptor antagonists. Arch Histol Cytol 2004;67:393-409.
47. Slayden OD, Keator CS. Role of progesterone in nonhuman primate implantation. Semin Reprod Med 2007;25:418-430.
48. Slayden OD, Koji T, Brenner RM. Microwave stabilization enhances immunocytochemical detection of estrogen receptor in frozen sections of macaque oviduct. Endocrinology 1995;136:4012-4021.
49. Slayden OD, Chwalisz K, Brenner RM. Reversible suppression of menstruation with progesterone antagonists in rhesus macaques. Hum Reprod 2001;16:1562-1574.
50. Sokal RR, Rohlf FJ. Introduction to Biostatistics, 2nd edn. New York: W.H. Freeman and Company, 1987.
51. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001;17:463-516.
52. Uria JA, Lopez-Otin C. Matrilysin-2, a new matrix metalloproteinase expressed in human tumors and showing the minimal domain organization required for secretion, latency, and activity. Cancer Res 2000;60:4745-4751.
53. Zhang J, Li S, Tian Y, Zhao Y, Qing-Xiang AS, Duan E. Effect of matrix metalloproteinase-26 (MMP-26) during embryo implantation in the mouse. Chin Sci Bull 2002;47:1884-1888.
54. Zhao YG, Xiao AZ, Cao XM, Zhu C. Expression of matrix metalloproteinase-2,-9 and tissue inhibitors of metalloproteinase-1,-2,-3 mRNAs in rat uterus during early pregnancy. Mol Reprod Dev 2002;62:149-158.