Role of cytokines in the endometrial-peritoneal cross-talk and development of endometriosis

Frontiers in Bioscience - Elite

Volumn 1 E, Issue 2, 2009, Pages 444-454

  Kyama, Cleophas M ^a,c   Mihalyi, Attila ^a   Simsa, Peter ^a,d   Falconer, Henrik ^b   Fulop, Vilmos ^d   Mwenda, Jason M ^c   Peeraer, Karen ^a   Tomassetti, Carla ^a   Meuleman, Christel ^a   D'Hooghe, Thomas M ^a,c  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c INSTITUTE OF PRIMATE RESEARCH   (Kenya)

^d National Health Center   (Hungary)

Author keywords

Adhesion factors; Chemokines; Cytokines; Endometriosis; Endometriotic lesion; Endometrium; Matrix metalloproteinases; Peritoneal fluid; Peritoneum; Review

Indexed keywords

CYTOKINE; HERMES ANTIGEN; INTEGRIN; MATRIX METALLOPROTEINASE;

ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; HUMAN; IMMUNOLOGY; METABOLISM; PERITONEUM; REVIEW; SIGNAL TRANSDUCTION;

ANTIGENS, CD44; CYTOKINES; ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; HUMANS; INTEGRINS; MATRIX METALLOPROTEINASES; PERITONEUM; RECEPTOR CROSS-TALK; SIGNAL TRANSDUCTION;

EID: 77953648914     PISSN: 19450494     EISSN: 19450508     Source Type: Journal    
DOI: 10.2741/e40     Document Type: Review

References (107)

1. Nisolle M & J Donnez. Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities, Fertil Steril 68, 585-596 (1997) (Pubitemid 27454315)
2. Sampson J. Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 14, 422-469 (1927)
3. Witz CA, Montoya-Rodriguez AI & RS, Schenken. Whole peritoneal explants: a novel model of the early endometriosis lesion. Fertil Steril 71, 56-60 (1999) (Pubitemid 29042343)
4. Debrock S, Vander Perre, Meuleman C, Moerman Ph, Hill JA & TM D'Hooghe. In vitro adhesion of endometrium to autologous peritoneal membranes: effect of the cycle phase and the stage of endometriosis. Hum Reprod, 17, 2523-28 (2002) (Pubitemid 35174097)
5. Debrock S, Hill JA & TM D'Hooghe. Quantitative assessment of endometrial-peritoneal interaction in vitro: a non-invasive diagnostic test for women with endometriosis? Gynecol Obstet Invest ;57:49-51 (2004) (Pubitemid 38186434)
6. Groothuis PG, Koks CA, de Goeij AF, Dunselman GA, Arends JW & JL Evers. Adhesion of human endometrial fragments to peritoneum in vitro. Fertil Steril 71, 1119-1124 (1999) (Pubitemid 29252507)
7. Debrock S, De Strooper B, Vander Perre S, Hill JA & TM D'Hooghe. Tumour necrosis factor-A, interleukin-6 and interleukin-8 do not promote adhesion of human endometrial epithelial cells to mesothelial cells in a quantitative in vitro model. Hum Reprod 21, 605-609 (2006) (Pubitemid 43372962)
8. Kyama CM, Mihalyi A, Simsa P, Falconer H, Fulop V, Mwenda JM, Peeraer K, Meuleman C & TM D'Hooghe. Endometrial-peritoneal interactions and endometriosis. World Endometriosis Soci ety e-Journal 8: 3-5 ( 2006)
9. Witz CA, Thomas MR, Montoya-Rodriguez AI, Nair AS, Centonze VE & RS Schenken . Short-Term culture of peritoneum explants confirms attachment of endometrium to intact peritoneal mesothelium. Fertil Steril 75,385-390 (2001) (Pubitemid 32112119)
10. Van der Linden PJ, de Goeij AF, Dunselman GA, Erkens HW & JL Evers. Endometrial cell adhesion in an in vitro model using intact amniotic membranes. Fertil Steril 5, 76-80 (1996) (Pubitemid 26006651)
11. Groothuis PG, Koks CA, de Goeij AF, Dunselman GA, Arends JW & JL Evers. Adhesion of human endometrium to the epithelial lining and extracellular matrix of amnion in vitro: an electron microscopic study. Hum Reprod 13:2275-2281 (1998)
12. Kyama CM, Debrock S, Mwenda JM & TM D'Hooghe. Potential involvement of the immune system in the development of endometriosis. Reprod Biol Endocrinol 1,123-127 (2003)
13. Mihalyi A, Kyama CM, Simsa P, Debrock S, Mwenda JM & TM D'Hooghe. Role of immunologic factors in the development of endometriosis: Indications for treatment strategies. Therapy 2, 623-639 (2005) (Pubitemid 41015144)
14. Wieser F, Fabjani G, Tempfer C, Schneeberger C, Zeillinger R, Huber JC & R Wenzl. Tumor necrosis factor-Alpha promotor polymorphisms and endometriosis. J Soc Gynecol Investig 9, 313-318 (2002) (Pubitemid 35292301)
15. Harada T, Iwabe T & N Tarakawa. Role of cytokines in endometriosis. Fertil Steril 76, 1-10 (2001) (Pubitemid 32600952)
16. Nothnick WB. Treating endometriosis as an autoimmune disease. Fertil Steril 7,223-231 (2001) (Pubitemid 32705520)
17. Witz CA, Montoya-Rodriguez IA, Miller DM, Schneider BG & RS Schenken. Mesothelium expression of integrins in vivo and in vitro. J Soc Gyn Invest 5, 87-93 (1998) (Pubitemid 28099767)
18. Kyama CM, Overbergh L, Debrock S, Valckx D, Vander Perre S, Meuleman C, Mihalyi A, Mathieu C, Mwenda JM & TM D'Hooghe. Increased peritoneal and endometrial gene expression of biologically relevant cytokines and growth factors during menstrual phase in women with endometriosis. Fertil Steril 85, 1667-1675 (2006) (Pubitemid 43816424)
19. Jabbour HN, Kelly RW, Fraser HM & HOD Critchley. Endocrine regulation of menstruation. Endocr rev 27, 17-46 (2006) (Pubitemid 43228237)
20. Tabibzadeh S. The signals and molecular pathways involved in human menstruation, a unique process of tissue destruction and remodelling. Mol Hum Reprod 2, 77-92 (1996) (Pubitemid 126715854)
21. Osteen KG, Bruner-Tran KL, Keller NR & E Eisenberg. Progesterone-mediated endometrial maturation limits matrix metalloproteinase (MMP) expression in an inflammatory-like environment: a regulatory system altered in endometriosis. Ann N Y Acad Sci 55:37-47 ( 2002) (Pubitemid 34271061)
22. Cheewadhanaraks S. Effect of tubal ligation on pelvic endometriosis externa in multiparous women with chronic pelvic pain. J Med Assoc Thai;87:735-9 (2004) (Pubitemid 39166071)
23. Fasciani A, Bocci G, Xu J, Bielecki R, Greenblatt E, Leyland N & RF Casper. Three-dimensional in vitro culture of endometrial explants mimics the early stages of endometriosis. Fertil Steril 80, 1137-43 (2003) (Pubitemid 37377740)
24. Sillem M, Prifti S, Monga B, Arslic T & B Runnebaum. Integrin-mediated adhesion of uterine endometrial cells from endometriosis patients to extracellular matrix proteins is enhanced by tumor necrosis factor alpha (TNF alpha) and interleukin-1 (IL-1) Eur J Obstet Gynecol Reprod Biol 87, 123-127 (1999) (Pubitemid 29476528)
25. Lessey BA, Castelbaum AJ, Sawin SW, Buck CA, Schinnar R, Bilker W & BL Strom. Aberrant integrin expression in the endometrium of women with endometriosis. J Clin Endocrinol Metab 79, 643-649 (1994) (Pubitemid 24256567)
26. Lessey BA, Damjanovich L & C Coutifaris. Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle. J. Clin Invest 90, 188-195 (1992)
27. Regidor PA, Vogel C, Regidor M, Schindler AE & E Winterhager. Expression pattern of integrin and adhesion molecules in endometriosis and human endometrium. Hum Reprod 4, 710-718 (1998) (Pubitemid 29041484)
28. Koks CAM, Groothuis PG, Dunselman GA, De Goiej AFPM & JLH Evers. Adhesion of menstrual endometrium to extracellular matrix : the possible role of integrin a6β1 and laminin interaction. Mol Hum Reprod 6, 170-7 (2000) (Pubitemid 30094280)
29. Dechaud H, Witz CA, Montoya-Rodriguez IA, Degraffenreid LA & RS Schenken. Mesothelial cell-Associated hyaluronic acid promotes adhesion of endometrial cells to mesothelium. Fertil Steril 76, 1012-8 (2001) (Pubitemid 33031330)
30. Braundmeier AG & RA Nowak. Cytokines regulate matrix metalloproteinases in human uterine endometrial fibroblast cells through a mechanism that does not involve increases in extracellular matrix metalloproteinase inducer. Am J Reprod Immunol. 56, 201-214 (2006) (Pubitemid 44151494)
31. Ulukus M, Cakmak H & A Arici. The role of endometrium in endometriosis. J Soc Gynecol Investign 13,467-476 (2006) (Pubitemid 44528303)
32. Mulayim N, Savlu A, Guzeloglu-Kayisli O, Kayisli UA & A Arici. Regulation of endometrial stromal cell matrix metalloproteinase activity and invasiveness by interleukin-8. Fertil Steril 81, 904-911 (2004) (Pubitemid 38333079)
33. Chung HW, Wen Y, Chun SH, Nezhat C, Woo BH & M Lake Polan. 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 75, 152-9 (2001) (Pubitemid 32041238)
34. Sillem M, Prifti S, Koch A, Neher M, Jauckus J & B Runnebaum. Regulation of matrix metalloproteinases and their inhibitors in uterine endometrial cells of patients with and without endometriosis. Eur J Obstet Gynecol Reprod Biol 95, 167-74 (2001) (Pubitemid 32297710)
35. Osteen KG, Keller NR, Feltus FA & MH Melner. Paracrine regulation of matrix metalloproteinase expression in the normal human endometrium. Gynecol Obstet Invest 48, 2-13 (1999) (Pubitemid 30088794)
36. Bruner-Tran KL, Zhang Z, Eisenberg E, Winneker RC & KG Osteen. 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 91,1554-1560 (2006)
37. Bruner KL, Eisenberg E, Gorstein F & KG Osteen. Progesterone and transforming growth factor-beta coordinately regulate suppression of endometrial matrix metalloproteinases in a model of experimental endometriosis. Steroids 64:648-53 ( 1999) (Pubitemid 29424104)
38. Curry TE Jr & KG Osteen. Cyclic changes in the matrix metalloproteinase system in the ovary and uterus. Biol Reprod 64, 1285-1296 (2001) (Pubitemid 32373046)
39. Fazleabas AT, Brudney A, Gurates B, Chai D & SA Bulun. A modified model for endometriosis. Ann N Y Acad Sci 955, 308-317 (2002)
40. Bruner-Tran KL, Eisenberg E, Yeaman GR, Anderson TA, McBean J & KG Osteen; Steroid and cytokine regulation of matrix metalloproteinase expression in endometriosis and the establishment of experimental endometriosis in nude mice. J Clin Endocrinol Metab 87, 4782-4791 (2002) (Pubitemid 35247076)
41. Gaetje R, Kotzian S, Herrmann G, Baumann R & A Starzinski-Powitz. Nonmalignant epithelial cells, potentially invasive in human endometriosis, lack the tumor suppressor molecule E-cadherin. Am J Pathol 150, 461-467 (1997) (Pubitemid 27073776)
42. Bergqvist A, Ferno M & S Mattson. A comparison of cathepsin D levels in endometriotic tissue and in uterine endometrium. Fertil Steril 65, 1130-1134 (1996) (Pubitemid 26158628)
43. Kyama CM, T'Jampens D, Mihalyi A, Simsa P, Debrock S, Waelkens E, Landuyt B, Meuleman C, Fulop V, Mwenda JM & TM D'Hooghe. ProteinChip technology is a useful method in the pathogenesis and diagnosis of endometriosis: a preliminary study. Fertil Steril 86, 203-209 (2006)
44. Ryu JW, Kim HJ, Lee YS, Myong NH, Hwang CH, Lee GS & HC Yom. The proteomics approach to find biomarkers in gastric cancer. J Korean Med Sci 18, 505-9 (2003)
45. Shi YY, Wang HC, Yin YH, Sun WS, Li Y, Zhang CQ, Wang Y, Wang S & WF Chen. Identification and analysis of tumour-Associated antigens in hepatocellular carcinoma. Br J Cancer 92, 929-34 (. 2005) (Pubitemid 40462641)
46. Yoshida S, Harada T, Mitsunari M, Iwabe T, Sakamoto Y, Tsukihara S, Iba Y, Horie S & N Terakawa. Hepatocyte growth factor/Met system promotes endometrial and endometriotic stromal cell invasion via autocrine and paracrine pathways. J Clin Endocrinol Metab 89, 823-32 ( 2004) (Pubitemid 38269898)
47. Dobbie JW. Morphology of the peritoneum in CAPD. Curr Concepts of CAPD; Blood Purif 7, 74-85 (1989) (Pubitemid 19115540)
48. Di Paolo N & G Sacchi. Anatomy and physiology of the peritoneal membrane. Contrib Nephrol 84,10-26 (l990)
49. Cao X, Yang D, Song M, Murphy A & S Parthasarathy. The presence of endometrial cells in the peritoneal cavity enhances monocyte recruitment and induces inflammatory cytokines in mice: implications for endometriosis. Fertil Steril 82, 999-1007 (2004) (Pubitemid 39335908)
50. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Kohno T, Sekine I, Matsuyama T & T Ishimaru. Regulation of hepatocyte growth factor by basal and stimulated macrophages in women with endometriosis. Hum Reprod 20, 49-60 (2005)
51. Witz CA. Cell adhesion molecules and endometriosis. Semin Reprod Med 21, 173-182 (2003)
52. Witz CA, Takahashi A, Montoya-Rodriguez IA, Cho S & RS Schenken. Expression of the alpha2beta1 and alpha3beta1 integrins at the surface of mesothelial cells: a potential attachment site of endometrial cells. Fertil Steril. 74,579-84 (2000)
53. van der Linden PJ, de Goeij AF, Dunselman GA, van der Linden EP, Ramaekers FC & JL Evers. Expression of integrins and E-cadherin in cells from menstrual effluent, endometrium, peritoneal fluid, peritoneum, and endometriosis. Fertil Steril 61,\85-90 (1994) (Pubitemid 24030683)
54. Fagerholm SC, Varis M, Stefanidakis M, Hilden TJ & CG Gahmberg. alpha-Chain phosphorylation of the human leukocyte CD11b/CD18 (Mac-1) integrin is pivotal for integrin activation to bind ICAMs and leukocyte extravasation. Blood 108, 3379-86 (2006)
55. Rana N, Gebel H, Braun DP, Rotman C, House R & WP Dmowski. Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis. Fertil Steril 65, 925-930 (1996) (Pubitemid 26126822)
56. Calhaz-Jorge C, Costa AP, Santos MC & ML Palma-Carlos. Soluble intercellular adhesion molecule 1 in the peritoneal fluid of patients with endometriosis correlates with the extension of peritoneal implants. Eur J Obstet Gynecol Reprod Biol 106, 170-174 (2003) (Pubitemid 36120466)
57. Vigano P, Somigliana E, Di Blasio AM, Cozzolino S, Candiani M & M Vignali. Suppression of natural killer cell function and production of soluble ICAM-1: endometrial stroma versus melanoma. Am J Reprod Immunol 46, 342-348 (2001) (Pubitemid 33034818)
58. Vigano P, Gaffuri B, Somigliana E, Busacca M, Di Blasio AM & M Vignali: Expression of intercellular adhesion molecule (ICAM)-1 mRNA and protein is enhanced in endometriosis versus endometrial stromal cells in culture. Mol Hum Reprod 4,1150-1156 (1998) (Pubitemid 28552799)
59. Becker JC, Termeer C, Schmidt RE & EB Brocker. Soluble intercellular adhesion molecule-1 inhibits MHCrestricted specific T cell/tumor interaction. J Immunol 151,7224-7232 (1993) (Pubitemid 24001097)
60. Halme J, Becker S, Hammond MG & S Raj. Pelvic macrophages in normal and infertile women: the role of patent tubes. Am. J. Obstet. Gynecol 142, 890-895 (1982) (Pubitemid 12142951)
61. Halme J, Becker S & S Haskill. Altered maturation and function of peritoneal macrophages: possible role in pathogenesis of endometriosis. Am J Obstet Gynecol 156, 783-789 (1987) (Pubitemid 17058777)
62. Oral E, Olive DL & A Arici. The peritoneal environment in endometriosis. Hum Reprod Update 2, 385-398 (1997) (Pubitemid 27087175)
63. D'Hooghe, TM & JA Hill. Immunobiology of endometriosis. In: Bronston R, Anderson DJ., editor. Immunology of reproduction. Cambridge, MA: Blackwell Scientific; pp. 322-356 (1996)
64. Nakamura T, Nishizawa T, Hagiya M, Seki T, Shimonishi M, Sugimura A, Tashiro K & S Shimizu. Molecular cloning and expression of hepatocyte growth factor. Nature 342, 440-443 (1989) (Pubitemid 19277521)
65. Khan KN, Masuzaki H, Fujishita A, Hamasaki T, Kitajima M, Hasuo A, Miyamura Y & T Ishimaru. Association of interleukin-6 and estradiol with hepatocyte growth factor in peritoneal fluid of women with endometriosis. Acta Obstet Gynecol Scand, 81:764-71 (2002) (Pubitemid 34953709)
66. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I & T Ishimaru. Immunoexpression of hepatocyte growth factor and c-Met receptor in eutopic endometrium predicts the activity of ectopic endometrium. Fertil Steril 79, 173-81 (2003) (Pubitemid 36071258)
67. Ishimaru T, Khan KN, Fujishita A, Kitajima M & H Masuzaki. Hepatocyte growth factor may be involved in cellular changes to the peritoneal mesothelium adjacent to pelvic endometriosis. Fertil Steril 81,810-8 (2004) (Pubitemid 38333065)
68. Sugiwara J, Fukaya T, Murakami T, Yoshida H & A Yajima. Hepatocyte growth factor stimulates proliferation, migration, and lumen formation of human endometrial epithelial cells in vitro. Biol Reprod 57, 936-42 (1997) (Pubitemid 27407216)
69. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I & T Ishimaru. Differential macrophage infiltration in early and advanced endometriosis and adjacent peritoneum. Fertil Steril 81,652-61 (2004) (Pubitemid 38376124)
70. Koks CA, Demir Weusten AY, Groothuis PG, Dunselman GA, de Goeij AF, Evers JL. Menstruum induces changes in mesothelial cell morphology. Gynecol Obstet Invest 50,13-8 (2000) (Pubitemid 30445748)
71. Yashiro M, Chung YS, Inoue T, Nishimura S, Matsuoka T, Fujihara T & Sowa M. Hepatocyte growth factor (HGF) produced by peritoneal fibroblasts may effect mesothelial cell morphology and promote peritoneal dissemination. Int J Cancer 67,289-93 (1996) (Pubitemid 26274163)
72. Halme J, White C, Kauma S, Estes J & S Haskill, Peritoneal macrophages from patients with endometriosis release growth factor activity in vitro. J Clin Endocrinol Metab 66 , 1044-1049 (1988)
73. Groothuis PG, Nap AW, Winterhager E & R Grummer. Vascular development in endometriosis. Angiogenesis 8,47-56 (2005)
74. Lebovic DI, Mueller MD & RNTaylor. Immunobiology of endometriosis. Fertil Steril 75, 1-10 ( 2001) (Pubitemid 32041217)
75. Becker JL, Widen RH, Mahan CS, Yeko TR, Parsons AK & WN Spellacy. Human peritoneal macrophage and T lymphocyte populations in mild and severe endometriosis. Am J Reprod Immunol 34, 179-187 (1995)
76. D'Hooghe TM, Bambra CS, Ling Xiao & JA Hill. The effect of menstruation and intrapelvic injection of endometrium on peritoneal fluid parameters in the baboon. Am J Obstet Gynecol 184, 917-925 (2001) (Pubitemid 32368110)
77. D'Hooghe TM, Bambra CS, Raeymaekers BM & JA Hill. Pelvic inflammation induced by diagnostic laparoscopy in baboons. Fertil Steril 72:1134-1141 (1999)
78. Kyama CM, Overbergh L, Mihalyi A, Meuleman C, Mwenda JM, Mathieu C & TM D'Hooghe. Endometrial and peritoneal mRNA expression of aromatase, cytokines and adhesion factors in women with endometriosis. Fertil Steril 2007 In press
79. Butcher EC, Williams M, Youngman K, Rott L & M Briskin. Lymphocyte trafficking and regional immunity. Adv. Immunol. 72, 209-253 (1999) (Pubitemid 30224828)
80. Matsuura K, Ohtake H, Katabuchi H & H Okamura. Coelomic metaplasia theory of endometriosis: evidence from in vivo studies and an in vitro experimental model. Gynecol Obstet Invest 47, 18-20 (. 1999)
81. Antsiferova YS, Sotnikova NY, Posiseeva LV & AL Shor. Changes in the T-helper cytokine profile and in lymphocyte activation at the systemic and local levels in women with endometriosis. Fertil Steril 84,1705-11 (2005) (Pubitemid 41785668)
82. Akoum A, Lemay A, McColl SR, Paradis I & R Maheux. Increased monocyte chemotactic protein-1 level and activity in the peripheral blood of women with endometriosis. Le Groupe d'Investigation en Gynecologie. Am J Obstet Gynecol 175, 1620-1625 (1996) (Pubitemid 27021037)
83. Iwabe T, Harada T, Tsudo T, Nagano Y, Yoshida S, Tanikawa M & N Terakawa. Tumor necrosis factor-Alpha promotes proliferation of endometriotic stromal cells by inducing interleukin-8 gene and protein expression. J Clin Endocrinol Metab 85, 824-829 (2000) (Pubitemid 32273674)
84. Sakamoto Y, Harada T, Horie S, Iba Y, Taniguchi F, Yoshida S, Iwabe T & N Terakawa. Tumor necrosis factoralpha-induced interleukin-8 (IL-8) expression in endometriotic stromal cells, probably through nuclear factor-kappa B activation: gonadotropin-releasing hormone agonist treatment reduced IL-8 expression. J Clin Endocrinol Metab 88, 730-735 (2003) (Pubitemid 36207815)
85. Lebovic DI, Chao VA & RN Taylor. Peritoneal macrophages induce RANTES (regulated on activation, normal T cell expressed and secreted) chemokine gene transcription in endometrial stromal cells. J Clin Endocrinol Metab 89,1397-1401 ( 2004) (Pubitemid 38368443)
86. Akoum A, Lemay A & R Maheux. Estradiol and interleukin-1beta exert a synergistic stimulatory effect on the expression of the chemokine regulated upon activation, normal T cell expressed, and secreted in endometriotic cells. J Clin Endocrinol Metab 87,5785-92 (2002 ) (Pubitemid 36034390)
87. Beliard A, Noël A, Goffin F, Frankenne F & JM Foidart. Adhesion of endometrial cells labeled with 111Indium-Tropolonate to peritoneum: a novel in vitro model to study endometriosis. Fertil Steril 79, 724-729 (2003) (Pubitemid 36279676)
88. Martinez S, Garrido N, Coperias JL, Pardo F, Desco J, Garcia-Velasco JA, Simon C & A Pellicer. Serum interleukin-6 levels are elevated in women with minimalmild endometriosis. Hum Reprod 22, 836-42 (2007)
89. Zhang R, Wild RA & JM Ojago. Effect of tumor necrosis factor-A on adhesion of human endometrial stromal cells to peritoneal mesothelial cells: an in vitro system. Fertil Steril 59, 1196-201 (1993) (Pubitemid 23163191)
90. Garcia-Velasco JA & A Arici. Interleukin-8 stimulates the adhesion of endometrial stromal cells to fibronectin. Fertil Steril 72, 336-340 (1999) (Pubitemid 29364635)
91. Piva M, Horowitz GM & KL Sharpe-Timms. Interleukin-6 differentially stimulates haptoglobin production by peritoneal and endometriotic cells in vitro: a model for endometrial-peritoneal interaction in endometriosis. J Clin Endocrinol Metab 86,2553-2561 (2001) (Pubitemid 32545706)
92. Kyama CM, Mwenda JM & TM D'Hooghe. Animal studies. In: Sutton, Adamson &Jones Eds. Modern Management of Endometriosis: Taylor & Francis Medical Books, 41-49pp (2005)
93. Mwenda JM, Kyama CM, Chai DC, Debrock S & TM D'Hooghe. The baboon as an appropriate model for study of multifactorial aspects of human endometriosis. In: S. Wolfe-Coote, Ed. The Laboratory Primate, Part II: Use of Primate Model in Research. Elsevier books, 551-561pp (2005)
94. Story L & S Kennedy. Animal studies in endometriosis: a review. ILAR J 45,132-138 (2004)
95. D'Hooghe TM, Debrock S, Meuleman C, Hill JA & JM Mwenda. Future directions in endometriosis research. Obstet Gynecol Clin North America 30, 221-244 (2003) (Pubitemid 36356723)
96. D'Hooghe TM, Bambra CS, Raeymaekers BM, De Jonge I, Lauweryns JM & PR Koninckx. Intrapelvic injection of menstrual endometrium causes endometriosis in baboons (Papio cynocephalus, Papio anubis) Am J Obstet Gynecol 173, 125-134 (1995)
97. D'Hooghe TM, Bambra CS, Cornillie FJ, Isahakia M & PR Koninckx. Prevalence and laparoscopic appearance of spontaneous endometriosis in the baboon (Papio anubis-Papio cynocephalus) Biol Reprod 45, 411-416 (1991)
98. Cornillie FJ, D'Hooghe TM, Bambra CS, Lauweryns JM, Isahakia M & PR Koninckx. Morphological characteristics of spontaneous endometriosis in the baboon (Papio anubis, Papio Cynocephalus) Gynecol Obstet Invest 34, 225-228 (1992) (Pubitemid 23023099)
99. D'Hooghe TM, Kyama C, Debrock S, Meuleman C & JM Mwenda. The future of Endometriosis Research. Ann NY Acad Sciences 1034, 316-325 ( 2004)
100. D'Hooghe TM, Hill JA, Oosterlynck DJ, Koninckx PR & CS Bambra. Effect on endometriosis and the menstrual cycle on white blood cell subpopulations in the peripheral blood and peritoneal of baboons. Hum Reprod. 11, 1736-1740 (1996) (Pubitemid 26318918)
101. D'Hooghe TM. Clinical relevance of the baboon as a model for the study of endometriosis. Fertil Steril. 68, 613-625 (1997) (Pubitemid 27454319)
102. D'Hooghe TM, Nugent N, Cuneo S, Chai D, Deer F, Debrock S, Kyama CM, Mihalyi A & JM Mwenda. Recombinant human TNF binding protein (r-hTBP-1) inhibits the development of endometriosis in baboons: a prospective, randomised, placebo-And drug controlled study. Biol Reprod 74, 131-136 (2006)
103. Barrier BF, Bates GW, Leland MM, Leach DA, Robinson RD & AM Propst. Efficacy of anti-Tumor necrosis factor therapy in the treatment of spontaneous endometriosis in baboons. Fertil Steril 81,775-779 (2004) (Pubitemid 38333059)
104. Falconer H, Mwenda JM, Chai DC, Wagner C, Song XY, Mihalyi A, Simsa P, Kyama C, Cornillie FJ, Bergqvist A, Fried G & TM D'Hooghe. Treatment with Anti-TNF Antibody c5N reduces the extent of induced endometriosis in the baboon. Hum Reprod. 21, 1856-1862 (2006) (Pubitemid 44028261)
105. Gashaw I, Hastings JM, Jackson KS, Winterhager Elke & AT Fazleabas. Induced endometriosis in the baboon (Papio anubis) increases the expression of the proangiogenic factor CYR61 (CCN1) in eutopic and ectopic endometria. Biol Reprod 74, 1060-1066 (2006) (Pubitemid 47394277)
106. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I & T Ishimaru. Higher activity by opaque endometriotic lesions than nonopaque lesions. Acta Obstet Gynecol Scand 83, 375-82 (2004) (Pubitemid 38406819)
107. Absenger Y, Hess-Stump H, Kreft B, Kratzschmar J, Haendler B, Schutze N, Regidor PA & E Winterhager. Cyr61, a deregulated gene in endometriosis. Mol Hum Reprod 10, 399-407 (2004) (Pubitemid 38714372)