Endometriosis research: Animal models for the study of a complex disease

Journal of Reproductive Immunology

Volumn 86, Issue 2, 2010, Pages 141-147

  Tirado González, Irene ^a   Barrientos, Gabriela ^a   Tariverdian, Nadja ^a   Arck, Petra C ^a,b   García, Mariana G ^a,c   Klapp, Burghard F ^a   Blois, Sandra M ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b MCMASTER UNIVERSITY   (Canada)

^c UNIVERSIDAD AUSTRAL   (Argentina)

Author keywords

Animals models; Endometriosis; Therapy

Indexed keywords

AZATHIOPRINE; ESTROGEN; GONADORELIN DERIVATIVE; METHYLPREDNISOLONE; MIFEPRISTONE; PROGESTERONE; VASCULOTROPIN;

ALLOTRANSPLANTATION; ANIMAL MODEL; DISEASE COURSE; ENDOMETRIOSIS; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; MOUSE; PELVIS; PRIMATE; PRIORITY JOURNAL; REVIEW; UTERUS;

ANIMALS; BIOMEDICAL RESEARCH; DISEASE MODELS, ANIMAL; ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; HUMANS;

EID: 77957252962     PISSN: 01650378     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jri.2010.05.001     Document Type: Review

References (51)

1. Attia G.R., Zeitoun K., Edwards D., Johns A., Carr B.R., Bulun S.E. Progesterone receptor isoform A but not B is expressed in endometriosis. J. Clin. Endocrinol. Metab. 2000, 85(Aug (8)):2897-2902.
2. Awwad J.T., Sayegh R.A., Tao X.J., Hassan T., Awwad S.T., Isaacson K. The SCID mouse: an experimental model for endometriosis. Hum. Reprod. 1999, 14(December (12)):3107-3111.
3. Becker C.M., Wright R.D., Satchi-Fainaro R., Funakoshi T., Folkman J., Kung A.L., et al. A novel noninvasive model of endometriosis for monitoring the efficacy of antiangiogenic therapy. Am. J. Pathol. 2006, 168(June (6)):2074-2084.
4. Bischoff F.Z., Simpsom J.L. Heritability and molecular genetic studies of endometriosis. Ann. N.Y. Acad. Sci. 2002, 955(March):239-251.
5. Borthwick J.M., Charnock-Jones D.S., Tom B.D., Hull M.L., Teirney R., Phillips S.C., Smith S.K. Determination of the transcript profile of human endometrium. Mol. Hum. Reprod. 2003, 9(January (1)):19-33.
6. Bruner-Tran K.L., Webster-Clair D., Osteen K.G. Experimental endometriosis: the nude mouse as a xenographic host. Ann. N.Y. Acad. Sci. 2002, 955(March):328-339. discussion 340-2, 396-406.
7. Bulun S.E., Cheng Y.H., Yin P., Imir G., Utsunomiya H., Attar E., Innes J., Julie Kim J. Progesterone resistance in endometriosis: link to failure to metabolize estradiol. Mol. Cell. Endocrinol. 2006, 248(March (1/2)):94-103.
8. Cummings A.M., Metcalf J.L. Induction of endometriosis in mice: a new model sensitive to estrogen. Reprod. Toxicol. 1995, 9(May-June (3)):233-238.
9. D'Hooghe T.M., Debrock S. Endometriosis, retrograde menstruation and peritoneal inflammation in women and in baboons. Hum. Reprod. Update 2002, 8(January-February (1)):84-88.
10. D'Hooghe T.M., Bambra C.S., Suleman M.A., Dunselman G.A., Evers H.L., Koninckx P.R. Development of a model of retrograde menstruation in baboons (Papio anubis). Fertil. Steril. 1994, 62(September (3)):635-638.
11. D'Hooghe T.M., Bambra C.S., Raeymaekers B.M., De Jonge I., Lauweryns J.M., Koninckx P.R. Intrapelvic injection of menstrual endometrium causes endometriosis in baboons (Papio cynocephalus and Papio anubis). Am. J. Obstet. Gynecol. 1995, 173(July (1)):125-134.
12. D'Hooghe T.M., Bambra C.S., Raeymaekers B.M., De Jonge I., Hill J.A., Koninckx P.R. The effects of immunosuppression on development and progression of endometriosis in baboons (Papio anubis). Fertil. Steril. 1995, 64(Jul (1)):172-178.
13. D'Hooghe T.M., Bambra C.S., De Jonge I., Lauweryns J.M., Koninckx P.R. Determination of the transcript profile of human endometrium. The prevalence of spontaneous endometriosis in the baboon (Papio anubis, Papio cynocephalus) increases with the duration of captivity. Acta Obstet. Gynecol. Scand. 1996, 75(February (2)):98-101.
14. D'Hooghe T.M., Bambra C.S., Raeymaekers B.M., Koninckx P.R. Serial laparoscopies over 30 months show that endometriosis in captive baboons (Papio anubis, Papio cynocephalus) is a progressive disease. Fertil. Steril. 1996, 65(March (3)):645-649.
15. D'Hooghe T.M., Hill J.A., Oosterlynck D.J., Koninckx P.R., Bambra C.S. Effect on endometriosis and the menstrual cycle on white blood cell subpopulations in the peripheral blood and peritoneal of baboons. Hum. Reprod. 1996, 11(August (8)):1736-1740.
16. D'Hooghe T.M., Bambra C.S., Xiao L., Peixe K., Hill J.A. The effect of menstruation and intrapelvic injection of endometrium on peritoneal fluid parameters in the baboon. Am. J. Obstet. Gynecol. 2001, 184(April (5)):917-925.
17. D'Hooghe T.M., Nugent N.P., Cuneo S., Chai D.C., Deer F., Debrock S., et al. Recombinant human TNFRSF1A (r-hTBP1) inhibits the development of endometriosis in baboons: a prospective, randomized, placebo- and drug-controlled study. Biol. Reprod. 2006, 74(January (1)):131-136.
18. Eskenazi B., Warner M.L. Epidemiology of endometriosis. Obstet. Gynecol. Clin. North Am. 1997, 24(June):235-258.
19. Evers J.L., Dunselman G.A., Land J.A., Bouckaert P.X., 1991. Is there a solution for recurrent endometriosis?, Br. J. Clin. Pract. Suppl. Autumn; 72, 45-50; discussion 51-53.
20. Fainaru O., Adini A., Benny, Adini I., Short S., Bazinet L., Nakai K., Pravda E., Hornstein M.D., D'Amato R.J., Folkman J. Research communication dendritic cells support angiogenesis and promote lesion growth in a murine model of endometriosis. FASEB J. 2008, 22(February (2)):522-529.
21. Falconer H., Mwenda J.M., Chai D.C., Wagner C., Song X.Y., Mihalyi A., et al. Treatment with anti-TNF monoclonal antibody (c5N) reduces the extent of induced endometriosis in the baboon. Hum. Reprod. 2006, 21(July (7)):1856-1862.
22. Fazleabas A.T., Brudney A., Gurates B., Chai D., Bulun S. A modified baboon model for endometriosis. Ann. N.Y. Acad. Sci. 2002, 955(March):308-317. discussion 340-342, 396-406.
23. Golan A., Winston R.M., Dargenio R. Experimental endometriosis: a microsurgical animal model in rats. Isr. J. Med. Sci. 1984, 20(November (11)):1094-1096.
24. Grow D.R., Williams R.F., Hsiu J.G., Hodgen G.D. Antiprogestin and/or gonadotropin-releasing hormone agonist for endometriosis treatment and bone maintenance: a 1-year primate study. J. Clin. Endocrinol. Metab. 1996, 81(May (5)):1933-1939.
25. Grümmer R., Schwarzer F., Bainczyk K., Hess-Stumpp H., Regidor P.A., Schindler A.E., et al. Peritoneal endometriosis: validation of an in-vivo model. Hum. Reprod. 2001, 16(August (8)):1736-1743.
26. Hadfield R.M., Yudkin P.L., Coe C.L., Scheffler J., Uno H., Barlow D.H., et al. Risk factors for endometriosis in the rhesus monkey (Macaca mulatta): a case-control study. Hum. Reprod. Update 1997, 3(March-April (2)):109-115.
27. Halme J., Hammond M.G., Hulka J.F., Raj S.G., Talbert L.M. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet. Gynecol. 1984, 64(August (2)):151-154.
28. Hirata T., Osuga Y., Yoshino O., Hirota Y., Harada M., Takemura Y., et al. Development of an experimental model of endometriosis using mice that ubiquitously express green fluorescent protein. Hum. Reprod. 2005, 20(August (8)):2092-2096.
29. Kyama C.M., Debrock S., Mwenda J.M., D'Hooghe T.M. Potential involvement of the immune system in the development of endometriosis. Reprod. Biol. Endocrinol. 2003, 1(December):123.
30. Kyama C.M., Overbergh L., Mihalyi A., Cuneo S., Chai D., Debrock S., et al. Effect of recombinant human TNF-binding protein-1 and GnRH antagonist on mRNA expression of inflammatory cytokines and adhesion and growth factors in endometrium and endometriosis tissues in baboons. Fertil. Steril. 2008, 89(May (5 Suppl.)):1306-1313.
31. Lebovic D.I., Mwenda J.M., Chai D.C., Mueller M.D., Santi A., Fisseha S., et al. PPAR-gamma receptor ligand induces regression of endometrial explants in baboons: a prospective, randomized, placebo- and drug-controlled study. Fertil. Steril. 2007, 88(October (4 Suppl.)):1108-1119.
32. Legrand N., Ploss A., Balling R., Becker P.D., Borsotti C., Brezillon N., Debarry J., de Jong Y., Deng H., Di Santo J.P., Eisenbarth S., Eynon E., Flavell R.A., Guzman C.A., Huntington N.D., Kremsdorf D., Manns M.P., Manz M.G., Mention J.J., Ott M., Rathinam C., Rice C.M., Rongvaux A., Stevens S., Spits H., Strick-Marchand H., Takizawa H., van Lent A.U., Wang C., Weijer K., Willinger T., Ziegler P. Humanized mice for modeling human infectious disease: challenges, progress, and outlook. Cell Host Microbes 2009, 6(July (1)):5-9.
33. Nisolle M., Casanas-Roux F., Donnez J. Early-stage endometriosis: adhesion and growth of human menstrual endometrium in nude mice. Fertil. Steril. 2000, 74(August (2)):306-312.
34. Masuda H., Maruyama T., Hiratsu E., Yamane J., Iwanami A., Nagashima T., Ono M., Miyoshi H., Okano H.J., Ito M., Tamaoki N., Nomura T., Okano H., Matsuzaki Y., Yoshimura Y. Noninvasive and real-time assessment of reconstructed functional human endometrium in NOD/SCID/gamma c (null) immunodeficient mice. Proc. Natl. Acad. Sci. U S A 2007, 104(February (6)):1925-1930.
35. Rossi G., Somigliana E., Moschetta M., Santorsola R., Cozzolino S., Filardo P., et al. Dynamic aspects of endometriosis in a mouse model through analysis of implantation and progression. Arch. Gynecol. Obstet. 2000, 263(February (3)):102-107.
36. Sampson J.A. Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the pelvic cavity. Am. J. Obstet. Gynecol. 1927, 14:422-469.
37. Sharpe K.L., Bertero M.C., Muse K.N., Vernon M.W. Spontaneous and steroid-induced recurrence of endometriosis after suppression by a gonadotropin-releasing hormone antagonist in the rat. Am. J. Obstet. Gynecol. 1991, 164(January (1 Pt 1)):187-194.
38. Shultz L.D., Lyons B.L., Burzenski L.M., Gott B., Chen X., Chaleff S., Kotb M., Gillies S.D., King M., Mangada J., et al. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J. Immunol. 2005, 174:6477-6489.
39. Somigliana E., Viganò P., Rossi G., Carinelli S., Vignali M., Panina-Bordignon P. Endometrial ability to implant in ectopic sites can be prevented by interleukin-12 in a murine model of endometriosis. Hum. Reprod. 1999, 14(December (12)):2944-2950.
40. Steinleitner A., Lambert H., Suarez M., Serpa N., Robin B., Cantor B. Periovulatory calcium channel blockade enhances reproductive performance in an animal model for endometriosis-associated subfertility. Am. J. Obstet. Gynecol. 1991, 164(April (4)):949-952.
41. Story L., Kennedy S. Animal studies in endometriosis: a review. ILAR J. 2004, 45(2):132-138.
42. Te Linde R.W., Scott R.B. Experimental endometriosis. Am. J. Obstet. Gynecol. 1950, 60(November (5)):1147-1173.
43. Trukhacheva E., Lin Z., Reierstad S., Cheng Y.H., Milad M., Bulun S.E. Estrogen receptor (ER) beta regulates ERalpha expression in stromal cells derived from ovarian endometriosis. J. Clin. Endocrinol. Metab. 2009, 94(February (2)):615-622.
44. Umezawa M., Tanaka N., Tainaka H., Takeda K., Ihara T., Sugamata M. Microarray analysis provides insight into the early steps of pathophysiology of mouse endometriosis model induced by autotransplantation of endometrium. Life Sci. 2009, 84(June (23/24)):832-837.
45. Van Duyne R., Pedati C., Guendel I., Carpio L., Kehn-Hall K., Saifuddin M., Kashanchi F. The utilization of humanized mouse models for the study of human retroviral infections. Retrovirology 2009, 6(August):76.
46. Vernon M.W., Wilson E.A. Studies on the surgical induction of endometriosis in the rat. Fertil. Steril. 1985, 44(November (5)):684-694.
47. Wang D.B., Zhang S.L., Niu H.Y., Lu J.M. A nude mouse model of endometriosis and its biological behaviors. Chin. Med. J. (Engl.) 2005, 118(September (18)):1564-1567.
48. Winkel C.A., Scialli A.R. Medical and surgical therapies for pain associated with endometriosis. J. Womens Health Gend. Based Med. 2001, 10:137-162.
49. Yang J.Z., Agarwal S.K., Foster W.G. Subchronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin modulates the pathophysiology of endometriosis in the cynomolgus monkey. Toxicol. Sci. 2000, 56(August (2)):374-381.
50. Zamah N.M., Dodson M.G., Stephens L.C., Buttram V.C., Besch P.K., Kaufman R.H. Transplantation of normal and ectopic human endometrial tissue into athymic nude mice. Am. J. Obstet. Gynecol. 1984, 149(July (6)):591-597.
51. Zondervan K.T., Weeks D.E., Colman R., Cardon L.R., Hadfield R., Schleffler J., et al. Familial aggregation of endometriosis in a large pedigree of rhesus macaques. Hum. Reprod. 2004, 19(February (2)):448-455.