Medical management of endometriosis: Novel targets and approaches towards the development of future treatment regimes

Gynecologic and Obstetric Investigation

Volumn 55, Issue 4, 2003, Pages 189-198

  Nothnick, Warren B ^a   D'Hooghe, Thomas M ^b,c  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c INSTITUTE OF PRIMATE RESEARCH   (Kenya)

Author keywords

Autoimmmunity; Baboon; Cytokine; Endometriosis; Treatment, endometriosis; Tumor necrosis factor

Indexed keywords

11BETA (4 ACETYLPHENYL) 17BETA HYDROXY 17ALPHA (1,1,2,2,2 PENTAFLUOROETHYL)ESTRA 4,9 DIEN 3 ONE; 4 [N (4 BROMOBENZYL) N (1,2,4 TRIAZOL 4 YL)AMINO]BENZONITRILE; ANASTROZOLE; ANTIGESTAGEN; AROMATASE INHIBITOR; DANAZOL; ESTROGEN; ETANERCEPT; FADROZOLE; GESTAGEN; GESTRINONE; GONADORELIN AGONIST; IMMUNOMODULATING AGENT; INFLIXIMAB; LEFLUNOMIDE; LEUPRORELIN; MATRIX METALLOPROTEINASE INHIBITOR; MIFEPRISTONE; NONSTEROID ANTIINFLAMMATORY AGENT; ONAPRISTONE; PENTOXIFYLLINE; PROGESTERONE; TERIFLUNOMIDE; TUMOR NECROSIS FACTOR ALPHA ANTIBODY; TUMOR NECROSIS FACTOR BINDING PROTEIN ANTIBODY; UNCLASSIFIED DRUG; ZK 136799;

ACNE; ALLERGIC REACTION; ALOPECIA; AMENORRHEA; BLEEDING; BONE DISEASE; BONE METABOLISM; CLINICAL TRIAL; COUGHING; DEPRESSION; DIARRHEA; DRUG ACTIVITY; DRUG HALF LIFE; ENDOMETRIOSIS; GASTROINTESTINAL DISEASE; HEADACHE; HORMONAL THERAPY; HOT FLUSH; HUMAN; MENTAL DISEASE; METABOLIC DISORDER; MOOD DISORDER; MUSCLE CRAMP; NAUSEA; NONHUMAN; OSTEOLYSIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RESPIRATORY TRACT INFECTION; REVIEW; SEBORRHEA; SIDE EFFECT; SINUSITIS; VASOMOTOR DISORDER; WEIGHT GAIN;

ADJUVANTS, IMMUNOLOGIC; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; AROMATASE INHIBITORS; ENDOMETRIOSIS; FEMALE; HUMANS; MATRIX METALLOPROTEINASES; PROGESTERONE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0041571731     PISSN: 03787346     EISSN: None     Source Type: Journal    
DOI: 10.1159/000072073     Document Type: Review

References (94)

1. Halme J, Hammond MG, Hulka JF, Raj SG, Talbert L: Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol 1984;64:151-154.
2. Liu DTY, Hitchcock A: Endometriosis: Its association with retrograde menstruation, dysmenorrhea, and tubal pathology. Br J Obstet Gynaecol 1986;93:859-886.
3. Oral E, Olive DL, Arici A: The peritoneal environmental in endometriosis. Hum Reprod Update 1997;2:385-398.
4. Iwabe T, Harada T, Tsudo T, Nagano Y, Yoshida S, Tanikawa M, Terakawa N: Tumor necrosis factor-α promotes proliferation of endometriotic stromal cells by inducing interleukin-8 gene and protein expression. J Clin Endocrinol Metab 2000;85:824-829.
5. Sillem M, Prifti S, Monga B, Arslic T, Runnebau B: Integrin-mediated adhesion of uterine endometrial cells from endometriosis patients to extracellular matrix proteins is enhanced by tumor necrosis factor alpha (TNFα) and interleukin-1 (IL-1). Eur J Obstet Gynecol Reprod Biol 1999;87:123-127.
6. Witz CA, Monotoya-Rodriquez IA, Schenken RS: Whole explants of peritoneum and endometrium: A novel model of the early endometriosis lesion. Fertil Steril 1999;71:56-60.
7. Witz CA, Takahashi A, Montoya-Rodriguez IA, Cho S, Schenken RS: Expression of the α2β1 and α3β1 integrins at the surface of mesothelial cells: A potential attachment site of endometrial cells. Fertil Steril 2000;74:579-584.
8. Witz CA, Thomas MR, Montoya-Rodriguez IA, Nair AS, Centonze VE, Schenken RS: Short-term culture of peritoneum explants confirms attachment of endometrium to intact peritoneal mesothelium. Fertil Steril 2001;75:385-390.
9. Gaetje R, Kotzian S, Herrmann G, Baumann R, Starzinski-Powitz A: Invasiveness of endometriotic cells in vitro. Lancet 1995;346:1463-1464.
10. Cornillie FJ, Oosterlynck D, Lauweryns JM, Koninckx PR: Deeplying infiltrating pelvic endometriosis: Histology and clinical significance. Fertil Steril 1990;53:978-983.
11. Spuijbroek MDEH, Dunselman GAJ, Menheere PPCA, Evers JL: Early endometriosis invades the extracellular matrix. Fertil Steril 1992;58:929-933.
12. Moghissi KS: Medical treatment of endometriosis. Clin Obstet Gynecol 1999;42:620-632.
13. Vercellini P, Trespide L, Colombo A, Ventola N, Marchini M, Crosignani PG: A gonadotropin releasing hormone agonist versus a low-dose oral contraceptive for pelvic pain associated with endometriosis. Fertil Steril1993;60:75-79.
14. Vercellini P, De Giorgi O, Mosconi P, Stellato G, Vicentini S, Crosignani PG: Cyproterone acetate versus a continuous monophasic oral contraceptive in the treatment of recurrent pelvic pain after conservative surgery for symptomatic endometriosis. Fertil Steril 2002;77:52-61.
15. Vercellini P, Cortesi I, Crosignani PG: Progestins for symptomatic endometriosis: A critical analysis of the evidence. Fertil Steril 1997;68:393-401.
16. Clemens LE, Sitter PK, Stites DP: Mechanism of immunosuppression of progesterone on maternal lymphocyte activation during pregnancy. J Immunol 1979;122:1978-1985.
17. Schust DJ, Anderson DJ, Hill JA: Progesterone-induced immunosuppression is not mediated through the progesterone receptor. Hum Reprod 1996;11:980-985.
18. Osteen KG, Keller NR, Feltus FA, Melner MH: Paracrine regulation of matrix metalloproteinase expression in the normal endometrium. Gynecol Obstet Invest 1999;48(suppl 1):2-13.
19. Hill JA, Barbieri RL, Anderson DJ: Immunosuppressive effects of danazol in vitro. Fertil Steril 1987;48:414-418.
20. Mori H, Nakagawa M, Itoh N, Wada K, Tamaya T: Danazol suppresses the production of interleukin-1β and tumor necrosis factor by human monocytes. Am J Reprod Immunol 1990:24:45-50.
21. Ota H, Igarashi S, Hayakawa M, Matsui T, Tanaka H, Tanaka T: Effect of danazol on the immunocompetent cells in the eutopic endometrium in patients with endometriosis: A multicenter cooperative study. Fertil Steril 1996;65:545-551.
22. Wu M-Y, Chao K-H, Chen S-U, Chen H-F, Yang Y-S, Huang S-C, Ho H-N: The suppression of peritoneal cellular immunity in women with endometriosis could be restored after gonadotropin releasing hormone agonist treatment. Am J Reprod Immunol 1996;35:510-516.
23. Chen HF, Jeung EB, Stephenson M, Leung PC: Human peripheral blood mononuclear cells express gonadotropin-releasing hormone (GnRH), GnRH receptor and interleukin-2 receptor gamma-chain messenger ribonucleic acids that are regulated by GnRH in vitro. J Clin Endocrinol Metab 1999;84:743-750.
24. Harada T, Enatsu A, Mitsunari M, Nagano Y, Ito M, Tsudo T, Taniguchi F, Iwabe T, Tanikawa M, Terakawa N: Role of cytokines in progression of endometriosis. Gynecol Obstet Invest 1999;47(suppl 1):34-40.
25. Imai A, Ohno T, Iida K, Fuseya T, Furui T, Tamaya T: Presence of gonadotropin-releasing hormone receptor and its messenger ribonucleic acid in endometrial carcinoma and endometrium. Gynecol Oncol 1994;55:144-148.
26. Ikeda M, Taga M, Kurogi K, Minaguchi G: Gene expression of gonadotropin-releasing hormone, but not its receptor in human endometrium and decidua. Mol Cell Endocrinol 1997;135:165-168.
27. Borroni R, Di Blasio AM, Gaffuri B, Santorsola R, Busacca M, Vigano P, et al: Expression of GnRH receptor gene in human ectopic endometrial cells and inhibition of their proliferation by leuprolide acetate. Mol Cell Endocrinol 2000;159:37-43.
28. Adashi EY: Long-term gonadotropin-releasing hormone agonist therapy: The evolving issue of steroidal 'add-back' paradigms. Hum Reprod Update 1994;7:1380-1397.
29. Kiesel L, Schweppe KW, Sillem M, Siebzehnrubl E: Should add-back therapy for endometriosis be deferred for optimal results? Br J Obstet Gynaecol 1996;103(suppl 14):15-17.
30. Watanabe Y, Nakamura G, Matsuguchi H, Nozaki M, Sano M, Nakano H: Efficacy of a low-dose leuprolide acetate depot in the treatment of uterine leiomyomata in Japanese women. Fertil Steril 1992;58:66-71.
31. Wheeler JM, Knittle JD, Miller JD: Depot leuprolide acetate versus danazol in the treatment of women with symptomatic endometriosis: A multicenter, double-blind randomized clinical trial. II. Assessment of safety. The Lupron Endometriosis Study Group. Am J Obstet Gynecol 1993;169:26-33.
32. Warnock JK, Bundren JC, Morris DW: Depressive symptoms associated with gonadotropin-releasing hormone agonists. Depress Anxiety 1998;7:171-177.
33. Rachman M, Garfield DA, Rachman I, Cohen R: Lupron-induced mania. Biol Psychiatry 1999;45:243-244.
34. Murphy AA, Zhou MH, Malkapuram S, Santanam N, Parthasarathy S, Sidell N: RU486-induced growth inhibition of human endometrial cells. Fertil Steril 2000;74:1014-1019.
35. Koide SS: Mifepristone: Auxiliary therapeutic use in cancer and related disorders. J Reprod Med 1998;43:551-560.
36. Kettel LM, Murphy AA, Morales AJ, Ulmann A, Baulieu EE, Yen SSC: Treatment of endometriosis with the antiprogesterone mifepristone (RU486). Fertil Steril 1996;65:23-28.
37. Kettel LM. Murphy AA, Morales AJ, Yen SSC: Preliminary report on the treatment of endometriosis with low-dose mifepristone (RU486). Am J Obstet Gynecol 1998;178:1151-1156.
38. Stoeckemann K, Hegele-Hartung C, Chwalisz K: Effects of the progesterone antagonists onapristone (ZK 98 299) and ZK 136 799 on surgically induced endometriosis in intact rats. Hum Reprod 1995;10:3264-3271.
39. Fuhrmann U, Hess Stummp H, Cleve A, Neef G, Schwede W, Hoffmann J, Fritzemeier KH, Chwalisz K: Synthesis and biological activity of a novel, highly potent progesterone receptor antagonist. J Med Chem 2000;43:5010-5016.
40. Slayden OD, Chwalisz K, Brenner RM: Reversible suppression of menstruation with progesterone antagonists in rhesus macaques. Hum Reprod 2001;8:1562-1574.
41. Brosens IA, Verleyen A, Cornillie FJ: The morphologic effect of short-term medical therapy of endometriosis. Am J Obstet Gynecol 1987;157:1215-1221.
42. Fedele L, Bianchi S, Viezzoli T, Arcaini L, Candiani GB: Gestrinone versus danazol in the treatment of endometriosis. Fertil Steril 1989;51:781-785.
43. Wingfield M, Healy DL: Endometriosis: Medical therapy. Baillières Clin Obstet Gynecol 1993;7:813-838.
44. Hornstein MD, Gleason RE, Barbieri RL: A randomized double-blind prospective trial of two doses of gestrinone in the treatment of endometriosis. Fertil Steril 1990;53:237-241.
45. Dawood MY, Obasiulu CW, Ramos J, Khan Dawood FS: Clinical, endocrine, and metabolic effects of two doses of gestrinone in treatment of pelvic endometriosis. Am J Obstet Gynecol 1997;176:387-394.
46. Gestrinone Italian Study Group: Gestrinone versus a GnRHa for the treatment of pelvic pain associated with endometriosis: A multicenter, randomized, double-blind study. Fertil Steril 1996;66:911-919.
47. Noble LS, Simpson ER, Johns A, Bulun SE: Aromatase expression in endometriosis. J. Clin Endocrinol Metab 1996;81:174-179.
48. Bulun SE, Yang S, Fang Z, Gurates B, Tamura M, Sebastian S: Estrogen production and metabolism in endometriosis. Ann NY Acad Sci 2002;955:75-85.
49. Takayama K, Zeitoun K, Gunby RT, Sasano H, Carr BR, Bulun SE: Treatment of severe postmenopausal endometriosis with an aromatase inhibitor. Fertil Steril 1998;69:709-713.
50. Yano S, Ikegami Y, Nakao K: Studies on the effect of the new non-steroidal aromatase inhibitor fadrozole hydrochloride in an endometriosis model in rats. Arzneimittelforschung 1996;46:192-195.
51. Kudoh M, Susaki Y, Ideyama Y, Nanya T, Mori M, Shikama H: Inhibitory effects of a novel aromatase inhibitor, YM511, in rats with experimental endometriosis. J Steroid Biochem Mol Biol 1997;63:1-3.
52. Gottschalk C, Malberg K, Arndt M, Schmitt J, Roessner A, Schultze D, Kleinstein J, Ansorge S: Matrix metalloproteinases and TACE play a role in the pathogenesis of endometriosis. Adv Exp Med Biol 2000;477:483-486.
53. Kokorine I, Nisolle M, Donnez J, Eeckhout Y, Courtoy PJ, Marbaix E: Expression of interstitial collagenase (matrix metalloproteinase-1) is related to the activity of human endometriotic lesions. Fertil Steril 1997;68:246-251.
54. Wenzl RJ, Heinzl H: Localization of matrix metalloproteinase-2 in uterine endometrium and ectopic implants. Gynecol Obstet Invest 1998;45:253-257.
55. 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.
56. Saito T, Mizumoto H, Kuroki K, Fujii M, Mori S, Kudo R: Expression of MMP-3 and TIMP-1 in the endometriosis and the influence of danazol. Nippon Sanka Fujinka Gakkai Zasshi 1995;47:495-496.
57. Rodgers W, Matrisian LM, Giudice LC, Dsupin B, Cannon P, Svitek C, Gorstein F, Osteen KG: Patterns of matrix metalloproteinase expression in cycling endometrium imply differential functions and regulation by steroid hormones. J Clin Invest 1994;94:946-953.
58. 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 Steril 2001;75:152-159.
59. Bruner KL, Matrisian LM, Rodgers WH, Gorstein F, Osteen KG: Suppression of matrix metalloproteinases inhibits establishment of ectopic lesions by human endometrium in nude mice. J Clin Invest 1997;99:2851-2857.
60. Bruner KL, Eisenberg E, Gorstein F, Osteen KG: Progesterone and transforming growth factor-beta coordinately regulate suppression of endometrial matrix metalloproteinases in a model of experimental endometriosis. Steroids 1999;64:648-653.
61. Bruner-Tran KL, Webster-Clair D, Osteen KG: Experimental endometriosis: The nude mouse as a xenograft host. Ann NY Acad Sci 2002;955:328-339.
62. Oral E, Arici A: Pathogenesis of endometriosis. Obstet Gynecol Clin North Am 1997;24:219-233.
63. Sidell N, Han SW, Parthasarathy S: Regualtion and modulation of abnormal immune responses in endometriosis. Ann NY Acad Sci 2002;955:159-173.
64. Gazvani R, Templeton A: Peritoneal environment, cytokines and angiogenesis in the pathophysiology of endometriosis. Reproduction 2002;123:217-226.
65. Tabibzadeh S: The signals and molecular pathways involved in human menstruation, a unique process of tissue destruction and remodelling. Mol Hum Reprod 1996;2:77-92.
66. Sillem M, Prifti S, Koch A, Neher M, Jauckus J, Runnebaum B: Regulation of matrix metalloproteinases and their inhibitors in uterine endometrial cells of patients with and without endometriosis. Eur J Obstet Gynecol Reprod Biol 2001;95:167-174.
67. D'Antonio M, Martelli F, Peano S, Papoian R, Borrelli F: Ability of recombinant human TNF binding protein-1 (r-hTBP-1) to inhibit the development of experimentally induced endometriosis in rats. J Reprod Immunol 2000;48:81-98.
68. D'Hooghe TM, Nugent N, Cuneo S, Chai D, Deer F, Debrock S, Mwenda J: Recombinant human TNF binding protein (r-hTBP-1) inhibits the development of endometriosis in baboons: A prospective, randomized, placebo- and drug-controlled study. Fertil Steril 2001;76:(suppl 1):S1.
69. Vihinen P, Kahari V-M: Matrix metalloproteinases in cancer: Prognostic markers and therapeutic targets. Int J Cancer 2002;99:157-166.
70. Nelson AR, Fingleton B, Rotherberg ML, Matrisian LM: Matrix metalloproteinases: Biological activity and clinical applications. J Clin Oncol 2000;18:1135-1149.
71. D'Hooghe TM, Debrock S: Endometriosis, retrograde menstruation and peritoneal inflammation in women and in baboons. Hum Reprod Update 2002;8:84-88.
72. Vinatier D, Orazi G, Cosson M, Dufour P: Theories on endometriosis. Eur J Obstet Gynecol Reprod Biol 2001;96:21-34.
73. Ota H, Igarashi S, Sasaki M, Tanaka T: Distribution of cyclooxygenase-2 in eutopic and ectopic endometrium in endometriosis and adenomyosis. Hum Reprod 2001;16:561-566.
74. Chishima F, Hayakawa S, Sugita K, Kinukawa N, Aleemuzzman S, Nemoto N, Yamamoto T, Honda M: Increased expression of cyclooxygenase-2 in local lesions of endometriosis patients. Am J Reprod Immunol 2002;48:50-56.
75. Abu JI, Konje JC: Leukotrienes in gynaecology: The hypothetical value of anti-leukotriene therapy in dysmenorrhea and endometriosis. Hum Reprod Update 2000;6:200-205.
76. Yamaguchi M, Mori N: Prostaglandin and leukotriene concentration of the peritoneal fluid of endometriosis and other gynecologic disorders in the secretory phase. Prostaglandins Leukot Essent Fatty Acids 1990;39:43-45.
77. Steinleitner A, Lambert H, Roy S: Immunomodulation with pentoxifylline abrogates macrophage-mediated infertility in an in vivo model: A paradigm for a novel approach to the treatment of endometriosis-associated subfertility. Fertil Steril 1991;55:26-31.
78. Nothnick WB, Curry TE, Vernon MW: Immunomodulation of rat endometriotic implant growth and protein production. Am J Reprod Immunol 1994;31:151-162.
79. Balasch J, Creus M, Fabregues F, Carmona F, Martinez-Roman S, Manau D, et al: Pentoxifylline versus placebo in the treatment of infertility associated with minimal or mild endometriosis: A pilot randomized clinical trial. Hum Reprod 1997;12:2046-2050.
80. Ward A, Clissold SP: Pentoxifylline: A review of its pharmacodynamic and pharmacokinetic properties, and its therapeutic efficacy. Drugs 1987;34:50-97.
81. Alkharfy KM, Kellum JA, Matzke GR: Unintended immunomodulation. Part II: Effects of pharmacological agents on cytokine activity. Shock 2000;13:346-360.
82. Maksymowych WP, Avina-Zubieta A, Luong MH, Russel A-S: An open study of pentoxifylline in the treatment of severe refractory rheumatoid arthritis. J Rheumatol 1995;22:625-629.
83. Reimund JM, Bumont S, Muller CD, Kenney JS, Kedinger M, Baumann R, Poindron P, Duclos B: In vitro effects of pentoxifylline on inflammatory cytokine release in patients with inflammatory bowel disease. Gut 1997;40:475-480.
84. Strieter RM, Remick DG, Ward PA, Spengler RN, Lynch JP III, Larrick J, et al: Cellular and molecular regulation of tumor necrosis factor-alpha by pentoxifylline. Biochem Biophys Res Commun 1988;155:1230-1236.
85. Sullivan GW, Carper HT, Novick WJ Jr, Mandell GL: Inhibition of the inflammatory action of interleukin-1 and tumor necrosis factor (alpha) on neutrophil function by pentoxifylline. Infect Immun 1988;56:1722-1729.
86. Fox RI, Herrmann ML, Frangou CG, Wahl GM, Morris RE, Strand V, et al: Mechanism of action for leflunomide in rheumatoid arthritis. Clin Immunol 1999;93:198-208.
87. Jarvis B, Faulds D: Etanercept: A review of its use in rheumatoid arthritis. Drugs 1999;57:945-966.
88. Markham A, Lamb HM: Infliximab: A review of its use in the management of rheumatoid arthritis. Drugs 2000;59:1341-1359.
89. Maini RN, Breedveld FC, Kalden JR, Smolen JS, Davis D, Macfarlane JD, Antoni C, Leeb B, Elliott MJ, Woody JN, Schaible TF, Feldmann M: Therapeutic efficacy of multiple intravenous infusions of anti-tumor necrosis factor α monoclonal antibody combined with low-dose weekly methotrexate in rheumatoid arthritis. Arthritis Rheum 1998;41:1552-1563.
90. Maini R, St. Clair EW, Breedveld F, Furst D, Kalden J, Weisman M, Smolen J, Emery P, Harriman G, Feldmann M, Lipsky P: Infliximab (chimeric anti-tumour necrosis factor α monoclonal antibody) versus placebo in rheumatoid arthritis patients receiving concomitant methotrexate: A randomized phase III trial. Lancet 1999;354:1932-1939.
91. Kavanaugh A, St. Clair EW, McCune WJ, Braakman T, Lipsky P: Chimeric anti-tumour necrosis factor-α monoclonal antibody treatment of patients with rheumatoid arthritis receiving methotrexate therapy. J Rheumatol 2000;27:841-850.
92. Maini RN, Elliott MJ, Long-Fox A: Clinical response of rheumatoid arthritis (RA) to anti-TNF-α monoclonal antibody (mab) is related to administered dose and persistence of circulating antibody. Arthritis Rheum 1995;38(suppl):S186.
93. D'Hooghe TM: Clinical relevance of the baboon as a model for the study of endometriosis. Fertil Steril 1997;68:613-625.
94. D'Hooghe TM, Debrock S, Chai DC, Cuneo S, Hill JA, Mwenda JM: Baboon model for fundamental and preclinical research in endometriosis. Gynecol Obstet Invest 2003; in press.