Doxycycline causes regression of endometriotic implants: A rat model

Human Reproduction

Volumn 24, Issue 8, 2009, Pages 1900-1908

  Akkaya, Pinar ^a   Onalan, Gogsen ^a   Haberal, Nihan ^a   Bayraktar, Nilufer ^a   Mülayim, Bari ^a   Zeyneloglu, Hulusi B ^a  

^a BASKENT UNIVERSITY   (Turkey)

Author keywords

Doxycycline; Endometriosis; MMP; Rat; Treatment

Indexed keywords

DOXYCYCLINE; GELATINASE A; GELATINASE B; INTERLEUKIN 6; LEUPRORELIN; MONODOKS; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; DRUG MEGADOSE; ENDOMETRIOSIS; FEMALE; IMMUNOHISTOCHEMISTRY; IMPLANT; LAPAROTOMY; LOW DRUG DOSE; NONHUMAN; PERITONEAL FLUID; PROTEIN EXPRESSION; RAT; SCORING SYSTEM;

ANIMALIA; RATTUS;

EID: 67651121821     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/dep106     Document Type: Article

References (95)

1. Acharya MR, Venitz J, Figg WD, Sparreboom A. Chemically modified etracyclines as inhibitors of matrix metalloproteinases. Drug Resist. Update 2004;7:195-208.
2. Amsterdam LL, Gentry W, Jobanputra S, Wolf M, Rubin SD, Bulun SE. Anastrazole and oral contraceptives: a novel treatment for endometriosis. Fertil Steril 2005;84:300-304.
3. Axisa B, Loftus IM, Naylor AR, Goodall S, Jones L, Bell PR, Thompson MM. Prospective, randomized, double-blind trial investigating the effect of doxycycline on matrix metalloproteinase expression within atherosclerotic carotid plaques. Stroke 2002; 33:2858-2864.
4. Bedaiwy MA, Falcone T, Sharma RK, Goldberg JM, Attaran M, Nelson DR, Agarwal A. Prediction of endometriosis with serum and peritoneal fluid markers: a prospective controlled trial. Hum Reprod 2002;17:426-431.
5. Bendeck MP, Conte M, Zhang M, Nili N, Strauss BH, Farwell SM. Doxycycline and chemically modified tetracyclines inhibit gelatinase A (MMP-2) gene expression in human skin keratinocytes. Ann NY Acad Sci 2002a;732:140-151.
6. Bendeck MP, Conte M, Zhang M, Nili N, Strauss BH, Farwell SM. Doxycycline modulates smooth muscle cell growth, migration, and matrix remodeling after arterial injury. Am J Pathol 2002b; 160:1089-1095.
7. Biffl WL, Moore EE, Moore FA, Peterson VM. Interleukin-6 in the injured patient. Marker of injury or mediator of inflammation? Ann Surg 1996; 224:647-664.
8. Bjornsson MJ, Havemose-Poulsen A, Stoltze K, Holmstrup P. Influence of the matrix metalloproteinase inhibitor batimastat (BB-94) on periodontal bone destruction in Sprague-Dawley rats. J Periodontal Res2004;39:269- 274.
9. Braundmeier AG, Fazleabas AT, Lessey BA, Guo H, Toole BP, Nowak RA. Extracellular matrix metalloproteinase inducer regulates metalloproteinases in human uterine endometrium. J Clin Endocrinol Metab 2006;91:2358- 2365.
10. Brown DL, Desai KK, Vakili BA, Nouneh C, Lee H, Golub LM. Clinical and biochemical results of the metalloproteinase inhibition with subantimicrobial doses of doxycycline to prevent acute coronary syndromes (MIDAS) pilot trial. Arterioscler Tromb Vasc Biol 2004; 24:733-738.
11. Bruner-Tran KL, Eisenberg E, Yeaman GR, Anderson TA, McBean J, Osteen KG. Steroid and cytokine regulation of matrix metalloproteinase expression in endometriosis and the establishment of experimental endometriosis in nude mice. J Clin Endocrinol Metab2002;87:4782-4791.
12. Bruner-Tran KL, Zhang Z, Eisenberg E, Winneker RC, Osteen KG. Down-regulation of endometrial matrix metalloproteinase-3 and-7 expression in vitro and therapeutic regression of experimental endometriosis in vivo by a novel nonsteroidal progesterone receptor agonist, tanaproget. J Clin Endocrinol Metab 2006;91:1554-1560.
13. Burggraf D, Trinkl A, Dichgans M, Hamann GF. Doxycycline inhibits MMPs via modulation of plasminogen activators in focal cerebral ischemia. Neurobiol Dis 2007;25:506-513.
14. Choi DH, Moon IS, Choi BK, Paik JW, Kim YS, Choi SH, Kim CK. Effects of sub-antimicrobial dose doxycycline therapy on crevicular fluid MMP-8, and gingival issue MMP-9, TIMP-1 and IL-6 levels in chronic periodontitis. J Periodont Res 2004;39:20-26.
15. Chen QH, Qu JY, Xu YY, Qiu NX, Zhuang YZ, Zhong S, Fang QQ. Expressions of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 in ectopic and eutopic endometrium. Zhonghua Fu Chan Ke Za Zhi 2004;39:809-812.
16. Chung HW, Wen Y, Chun SH, Nezhat C, Woo BH, Lake Polan M. Matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-3 mRNA expression in ectopic and eutopic endometrium in women with endometriosis: a rationale for endometriotic invasiveness. Fertil Steril2001;75:152-159.
17. Chung HW, Lee JY, Moon HS, Hur SE, Park MH,Wen Y, Polan ML. Matrix metalloproteinase-2, membranous type 1 matrix metalloproteinase, and tissue inhibitor of metalloproteinase-2 expression in ectopic and eutopic endometrium. Fertil Steril 2002;78:787-795.
18. Chwalisz K, Perez MC, Demanno D, Winkel C, Schubert G, Elger W. Selective progesterone receptor modulator development and use in the treatment of leiomyomata and endometriosis. Endocr Rev 2005; 26:423-438.
19. Cobellis L, Razzi S, De Simone S, Sartini A, Fava A, Danero S, Gioffrè W, Mazzini M, Petraglia F. The treatment with a COX-2 specific inhibitor is effective in the management of pain related to endometriosis. Eur J Obstet Gynecol Reprod Biol 2004;116:100-102.
20. Collette T, Bellehumeur C, Kats R, Maheux R, Mailloux J, Villeneuve M, Akoum A. Evidence for an increased release of proteolytic activity by the eutopic endometrial tissue in women with endometriosis and for involvement of matrix metalloproteinase-9. Hum Reprod 2004; 19:1257-1264.
21. Collette T, Maheux R, Mailloux J, Akoum A. Increased expression of matrix metalloproteinase-9 in the eutopic endometrial tissue of women with endometriosis. Hum Reprod 2006;21:3059-3067.
22. Courtman DW, Franco CD, Meng Q, Bendeck MP. Inward remodeling of the rabbit aorta is blocked by the matrix metalloproteinase inhibitor doxycycline. J Vasc Res 2004;41:57-65.
23. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 2002; 295:2387-2392.
24. Cox KE, Piva M, Sharpe-Timms KL. Differential regulation of matrix metalloproteinase-3 gene expression in endometriotic lesions compared with endometrium. Biology of reproduction 2001; 65:1297-1303.
25. 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.
26. De Paiva CS, Corrales RM, Villarreal AL, Farley WJ, Li DQ, Stern ME, Pflugfelder SC. Corticosteroid and doxycycline suppress MMP-9 and inflammatory cytokine expression, MAPK activation in the corneal epithelium in experimental dry eye. Exp Eye Res 2004;83:526-535.
27. Dogan E, Saygili U, Posaci C, Tuna B, Caliskan S, Altunyurt S, Saatli B. Regression of endometrial explants in rats treated with the cyclooxygenase-2 inhibitor rofecoxib. Fertil Steril 2004;l82:1115-1120.
28. Fife RS, Sledge GW Jr. Effects of doxycycline on in vitro growth, migration, and gelatinase activity of breast carcinoma cells. J Lab Clin Med 1995; 125:407-411.
29. Freitas S, Meduri G, Le Nestour E, Bausero P, Perrot-Applanat M. Expression of metalloproteinases and their inhibitors in blood vessels in human endometrium. Biol Reprod 1999;61:1070-1082.
30. Folgueras AR, Pendas AM, Sanchez LM, Lopez-Otin C. Matrix metalloproteinases in cancer: from new functions to improved inhibition strategies. Int J Dev Biol 2004;48:411-424.
31. Folwarczna J, Janiec W, Firlus K, Kaczmarczyk-Sedlak I. Effects of doxycycline on the development of bone damage caused by prednisolone in rats. Pol J Pharmacol 1999;51:243-251.
32. Gilabert-Estelles J, Estelles A, Gilabert J, Castello R, Espana F, Falco C, Romeu A, Chirivella M, Zorio E, Aznar J. Expression of several components of the plasminogen activator and matrix metalloproteinase systems in endometriosis. Hum Reprod 2003; 18:1516-1522.
33. Golub LM, Ramamurthy NS, McNamara TF, Greenwald RA, Rifkin BR. Tetracyclines inhibit connective tissue breakdown: new therapeutic implications for an old family of drugs. Crit Rev Oral Biol Med 1991; 2:297-321.
34. Golub LM, Evans RT, McNamara TF, Lee HM. A nonantimicrobial tetracycline inhibits gingival matrix metalloproteinases and bone loss in porphyromonas gingivalis-induced periodontitis in rats. Ann N Y Acad Sci 1994a;732:96-111.
35. Golub LM, Wolff M, Roberts S, Lee HM, Leung M, Payonk GS. Treating periodontal diseases by blocking tissue-destructive enzymes. J Am Dent Assoc 1994b;125:163-169. discussion 169-71.
36. Golub LM, Lee HM, Ryan ME, Giannobile WV, Payne J, Sorsa T. Tetracyclines inhibit connective tissue breakdown by multiple nonantimicrobial mechanisms. Adv Dent Res 1998;12:12-26.
37. Golub LM, McNamara TF, Ryan ME, Kohut B, Blieden T, Payonk G, Sipos T, Baron HJ. Adjunctive treatment with subantimicrobial doses of doxycycline: effects on gingival fluid collagenase activity and attachment loss in adult periodontitis. J Clin Periodontol 2001;28: 146-156.
38. Hoyt JC, Ballering J, Numanami H, Hayden JM, Robbins RA. Doxycycline modulates nitric oxide production in murine lung epithelial cells. J Immunol 2006;176:567-572.
39. Hudelist G, Lass H, Keckstein J, Walter I, Wieser F, Wenzl R, Mueller R, Czerwenka K, Kubista E, Singer CF. Interleukin 1alpha and tissue-lytic matrix metalloproteinase-1 are elevated in ectopic endometrium of patients with endometriosis. Hum Reprod 2005;20:1695-1701.
40. Iwabe T, Harada T, Sakamoto Y, Iba Y, Horie S, Mitsunari M, Terakawa N. Gonadotropin-releasing hormone agonist treatment reduced serum interleukin-6 concentrations in patients with ovarian endometriomas. Fertil Steril 2003;80:300-304.
41. Keenan JA, Chen TT, Chadwell NL, Torry DS, Caudle MR. Interferon-gamma (INF-gamma) and interleukin-6 (IL-6) in peritoneal fluid and macrophage-conditioned media of women with endometriosis. Am J Reprod Immunol 1994;32:180-183.
42. Keenan JA, Williams-Boyce PK, Massey PJ, Chen TT, Caudle MR, Bukovsky A. Regression of endometrial explants in a rat model of endometriosis treated with the immune modulators loxoribine and levamisole. Fertil Steril 1999;72:135-141.
43. Khan KN, Masuzaki H, Fujishita A, Hamasaki T, Kitajima M, Hasuo A, Miyamura Y, Ishimaru T. Association of interleukin-6 and estradiol with hepatocyte growth factor in peritoneal fluid of women with endometriosis. Acta Obstet Gynecol Scand 2002;81:764-771.
44. Kim HS, Luo L, Pflugfelder SC, Li DQ. Doxycycline inhibits TGF-beta1-induced MMP-9 via Smad and MAPK pathways in human corneal epithelial cells. Invest Ophthalmol Vis Sci 2005;46:840-848.
45. Kivelä-Rajamäki M, Maisi P, Srinivas R, Tervahartiala T, Teronen O, Husa V, Salo T, Sorsa T. Levels and molecular forms of MMP-7 (matrilysin-1) and MMP-8 (collagenase-2) in diseased human peri-implant sulcular fluid. J Periodontal Res 2003;38:583-590.
46. Kyama CM, Overbergh L, Debrock S, Valckx D, Vander Perre S, Meuleman C, Mihalyi A, Mwenda JM, Mathieu C, D'Hooghe TM. Increased peritoneal and endometrial gene expression of biologically relevant cytokines and growth factors during the menstrual phase in women with endometriosis. Fertil Steril 2006;85:1667-1675.
47. Lamparter S, Slight SH, Weber KT. Doxycycline and tissue repair in rats. J Lab Clin Med 2002;139:295-302.
48. Lebovic DI, Kir M, Casey CL. Peroxisome proliferator-activated receptor-gamma induces regression of endometrial explants in a rat model of endometriosis. Fertil Steril 2004;82(Suppl 3):1008-1013.
49. Lee KS, Jin SM, Kim SS, Lee YC. Doxycycline reduces airway inflammation and hyperresponsiveness in a murine model of toluene diisocyanateinduced asthma. J Allergy Clin Immunol 2004a;113:902-909.
50. Lee HM, Ciancio SG, Tuter G, Ryan ME, Komaroff E, Golub LM. Subantimicrobial dose doxycycline efficacy as a matrix metalloproteinase inhibitor in chronic periodontitis patients is enhanced when combined with a non-steroidal antiinflammatory drug. J Periodontol 2004b;75:453- 463.
51. Lee CZ, Yao JS, Huang Y, Zhai W, Liu W, Guglielmo BJ, Lin E, Yang GY, Young WL. Dose-response effect of tetracyclines on cerebral matrix metalloproteinase-9 after vascular endothelial growth factor hyperstimulation. J Cereb Blood Flow Metab 2006;26:1157-1164.
52. Li R, Luo X, Pan Q, Zineh I, Archer D, Williams RS, Chegini N. Doxycycline alters the expression of inflammatory and immune related cytokines/chemokines in human endometrial cells: implication in dysfunctional uterine bleeding. Hum Reprod 2006;21:2555-2563.
53. Li R, Luo X, Archer DF, Chegini N. Doxycycline alters the expression of matrix metalloproteases in the endometrial cells exposed to ovarian steroids and pro-inflammatory cytokine. J Reprod Immunol 2007; 73:118-129.
54. Liu XJ, He YL, Peng DX. Expression of metalloproteinase-9 in ectopic endometrium in women with endometriosis. Di Yi Jun Yi Da Xue Xue Bao 2002;22:467-469.
55. Lovejoy B, Clearsby A, Hassell AM, Luther MA, Weigl D, McGeehan G et al. Structural analysis of the catalytic domain of human fibroblast collagenase. Ann N Y Acad Sci 1994;732:375-378.
56. Luo L, Li DQ, Doshi A, Farley W, Corrales RM, Pflugfelder SC. Experimental dry eye stimulates production of inflammatory cytokines and MMP-9 and activates MAPK signaling pathways on the ocular surface. Invest Ophthalmol Vis Sci 2004;45:4293-4301.
57. MartÍnez S, Garrido N, Coperias JL, Pardo F, Desco J, GarcÍa-Velasco JA, Simón C, Pellicer A. Serum interleukin-6 levels are elevated in women with minimal-mild endometriosis. Hum Reprod 2007;22:836-842.
58. Mott JD, Werb Z. Regulation of matrix biology by matrix metalloproteinases. Curr Opin Cell Biol 2004;16:558-564.
59. Nap AW, Dunselman GA, de Goeij AF, Evers JL, Groothuis PG. Inhibiting MMP activity prevents the development of endometriosis in the chicken chorioallantoic membrane model. Hum Reprod 2004;19:2180-2187.
60. Nap AW, Dunselman GA, Griffioen AW, Mayo KH, Evers JL, Groothuis PG. Angiostatic agents prevent the development of endometriosis-like lesions in the chicken chorioallantoic membrane. Fertil Steril 2005;83:793-795.
61. Nelson AR, Fingleton B, Rothenberg ML, Matrisian LM. Matrix metalloproteinases: biologic activity and clinical implications. J Clin Oncol 2000;18:1135-1149.
62. Nip LH, Uitto VJ, Golub LM. Inhibition of epithelial cell matrix metalloproteinases by tetracyclines. J Periodontal Res 1993;28:379-385.
63. Onoda T, Ono T, Dhar DK, Yamanoi A, Fujii T, Nagasue N. Doxycycline inhibits cell proliferation and invasive potential: combination therapy with cyclooxygenase-2 inhibitor in human colorectal cancer cells. J Lab Clin Med 2004;143:207-216.
64. Osteen KG, Bruner KL, Sharpe-Timms KL. Steroid and growth factor regulation of matrix metalloproteinase expression and endometriosis. Semin Reprod Endocrinol 1996;14:247-255.
65. Osteen KG, Keller NR, Feltus FA, Melner MH. Paracrine regulation of matrix metalloproteinase expression in the normal human endometrium. Gynecol Obstet Invest 1999;48:2-13.
66. Osteen KG, Bruner-Tran KL, Keller NR, Eisenberg E. Progesteronemediated endometrial maturation limits matrix metalloproteinase (MMP) expression in an inflammatory-like environment: a regulatory system altered in endometriosis. Ann NY Acad Sci 2002;955:37-47.
67. Pan H, Sheng JZ, Tang L, Zhu R, Zhou TH, Huang HF. Increased expression of c-fos protein associated with increased matrix metalloproteinase-9 protein expression in the endometrium of endometriotic patients. Fertil Steril 2008;90:1000-1007.
68. Pellicer A, Albert C, Mercader A, Bonilla-Musoles F, Remohi J, Simón C. The follicular and endocrine environment in women with endometriosis: local and systemic cytokine production. Fertil Steril1998;70:425-431.
69. Petrinec D, Liao S, Holmes DR, Reilly JM, Parks WC, Thompson RW. Doxycycline inhibition of aneurysmal degeneration in an elastaseinduced rat model of abdominal aortic aneurysm: preservation of aortic elastin associated with suppressed production of 92 kD gelatinase. J Vasc Surg 1996;23:336-346.
70. Prall AK, Longo GM, Mayhan WG, Waltke EA, Fleckten B, Thompson RW, Baxter BT. Doxycycline in patients with abdominal aortic aneurysms and in mice: comparison of serum levels and effect on aneurysm growth in mice. J Vasc Surg 2002;35:923-929.
71. Preshaw PM, Hefti AF, Jepsen S, Etienne D, Walker C, Bradshaw MH. Subantimicrobial dose doxycycline as adjunctive treatment for periodontitis. A review. J Clin Periodontol 2004;31:697-707.
72. Ramamurthy NS, Vernillo AT, Greenwald RA, Lee HM, Sorsa T, Golub LM, Rifkin BR. Reactive oxygen species activate and tetracyclines inhibit rat osteoblast collagenase. J Bone Miner Res 1993; 8:1247-1253.
73. Ramamurthy NS, Schroeder KL, McNamara TF, Gwinnett AJ, Evans RT, Bosko C, Golub LM. Root-surface caries in rats and humans: inhibition by a non-antimicrobial property of tetracyclines. Adv Dent Res 1998;1243-1250.
74. Ria R, Loverro G, Vacca A, Ribatti D, Cormio GM, Roccaro A, Selvaggi L. Angiogenesis extent and expression of matrix metalloproteinase-2 and-9 agree with progression of ovarian endometriomas. Eur J Clin Invest2002; 32:199-206.
75. Rier SE, Zarmakoupis PN, Hu X, Becker JL. Dysregulation of interleukin-6 responses in ectopic endometrial stromal cells: correlation with decreased soluble receptor levels in peritoneal fluid of women with endometriosis. J Clin Endocrinol Metab 1995;80:1431-1437.
76. Ruiyuan S. Quantitative Pharmacology, 1st edn. Beijing: People's Health Publishing House, 1987.
77. Ryan ME, Ramamurthy S, Golub LM. Matrix metalloproteinases and their inhibition in periodontal treatment. Curr Opin Periodontol 1996; 3:85-96.
78. Salmassi A, Acil Y, Schmutzler AG, Koch K, Jonat W, Metler L. Differential interleukin-6 messenger ribonucleic acid expression and its distribution pattern in eutopic and ectopic endometrium. Fertil Steril 2008; 89:1578-1584.
79. Sampson J. Peritoneal endometriosis due to the menstrual dissemination of endothelial tissue into the peritoneal cavity. Am J Obstet Gynecol1927;14:422-469.
80. Sapadin AN, Fleischmajer R. Tetracyclines: nonantibiotic properties and their clinical implications. J Am Acad Dermatol 2006;54:258-265. Review.
81. Sharpe-Timms KL, Cox KE. Paracrine regulation of matrix metalloproteinase expression in endometriosis. Ann NY Acad Sci 2002; 955:147-156.
82. Sillem M, Prifti S, Neher M, Runnebaum B. Extracellular matrix remodelling in the endometrium and its possible relevance to the pathogenesis of endometriosis. Hum Reprod Update 1998;4:730-735.
83. Smith GN Jr, Mickler EA, Hasty KA, Brandt KD. Specificity of inhibition of matrix metalloproteinase activity by doxycycline: relationship to structure of the enzyme. Arthritis Rheum 1999;42:1140-1146.
84. Sorsa T, Lindy O, Konttinen YT, Suomalainen K, Ingman T, Saari H, Halinen S, Lee HM, Golub LM, Hall J et al. Doxycycline in the protection of serum alpha-1-antitrypsin from human neutrophil collagenase and gelatinase. Antimicrob Agents Chemother 1993;37:592-594.
85. Sorsa T, Ding Y, Salo T, Lauhio A, Teronen O, Ingham T et al. Effects of tetracyclines on neutrophil, gingival and salivary collagenases: a functional and Western blot assessment with specific reference to their cellular sources in periodontal disease. Ann N Y Acad Sci 1994; 732:112-131.
86. Sorsa T, Golub LM. Is the excessive inhibition of matrix metalloproteinases (MMPs) by potent synthetic MMP inhibitors (MMPIs) desirable in periodontitis and other inflammatory diseases? That is: 'Leaky' MMPIs vs excessively efficient drugs. Oral Dis 2005;11:408-409.
87. Uchiide I, Ihana T, Sugamata M. Pathological evaluation of the rat endometriosis model. Fertil Steril 2002;78:782-786.
88. Uitto VJ, Firth JD, Nip L, Golub LM. Doxycycline and chemically modified tetracyclines inhibit gelatinase A (MMP-2) gene expression in human skin keratinocytes. Ann N Y Acad Sci 1994;6:140-151.
89. Uitto VJ, Overall CM, McCulloch C. Proteolytic host cell enzymes in gingival crevice fluid. Periodontol 2000 2003;3:177-104.
90. Witz CA, Bedaiwy MA, Falcone T, Sharma RK, Goldberg JM, Attaran M, Nelson DR, Agarwal A. Interleukin-6: another piece of the endometriosis-cytokine puzzle. Fertil Steril 2000;73:212-214.
91. Wu MH, Shoji Y, Wu MC, Chuang PC, Lin CC, Huang MF, Tsai SJ. Suppression of matrix metalloproteinase-9 by prostaglandin E(2) in peritoneal macrophage is associated with severity of endometriosis. Am J Pathol 2005;167:1061-1069.
92. Yao JS, Shen F, Young LW, Yang G-Y. Comparison of doxycycline and minocycline in the inhibition of VEGF-induced smooth muscle cell migration. Neurochemistry International 2007;50:524-530.
93. Yavuz E, Oktem M, Esinler I, Arat Toru S, Zeyneloglu HB. Genistein causes regression of endometriotic implants in the rat model. Fertil Steril 2007; 88:1129-1134.
94. Yu J,Wang Y, Zhou WH,Wang L, He YY, Li DJ. Combination of estrogen and dioxin is involved in the pathogenesis of endometriosis by promoting chemokine secretion and invasion of endometrial stromal cells. Hum Reprod 2008;23:1614-1626.
95. Zhang J, Hampton AL, Nie G, Salamonsen LA. Progesterone inhibits activation of latent matrix metalloproteinase (MMP)-2 by membranetype 1 MMP: enzymes coordinately expressed in human endometrium. Biol Reprod 2000;62:85-94.