Mixed origin of neovascularization of human endometrial grafts in immunodeficient mouse models

Human Reproduction

Volumn 24, Issue 9, 2009, Pages 2217-2224

  Alvarez Gonzalez, M L ^a   Frankenne, F ^a   Galant, C ^b   Marbaix, E ^b   Foidart, J M ^a,c   Nisolle, M ^a,c   Beliard A ^a,c  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^c UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Angiogenesis; Chimeric vessels; Endometrium; Fluorescence in situ hybridization; Lectin

Indexed keywords

COLLAGEN TYPE 4; ESTRADIOL; LECTIN; LEVONORGESTREL; PROGESTERONE; VON WILLEBRAND FACTOR;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL; CONTROLLED STUDY; ENDOMETRIUM; ERYTHROCYTE; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE PROBE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMPLANTATION; MOUSE; NONHUMAN; SCID MOUSE; TISSUE TRANSPLANTATION; VASCULARIZATION; X CHROMOSOME; XENOGRAFT;

MURINAE; MUS;

ANIMALS; CHIMERA; ENDOMETRIUM; FEMALE; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MICE; MICE, NUDE; MICE, SCID; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; TRANSPLANTATION, HETEROLOGOUS;

EID: 68949211182     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/dep203     Document Type: Article

References (43)

1. Abulafia O, Sherer DM. Angiogenesis of the endometrium. Obstet Gynecol 1999;94:148-153.
2. Alvarez Gonzalez ML, Galant C, Frankenne F, Nisolle M, Labied S, Foidart JM, Marbaix E, Beliard A. Development of an animal experimental model to study the effects of levonorgestrel on the human endometrium. Hum Reprod 2008;24:697-704.
3. Asahara T, Murohara T, Sullivan A, Silver M, van der ZR, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997;275:964-967.
4. Becker CM, D'Amato RJ. Angiogenesis and antiangiogenic therapy in endometriosis. Microvasc Res 2007;74:121-130.
5. Bruner-Tran KL, Webster-Clair D, Osteen KG. Experimental endometriosis: the nude mouse as a xenographic host. Ann N Y Acad Sci 2002;955:328-339.
6. Critchley HO, Wang H, Jones RL, Kelly RW, Drudy TA, Gebbie AE, Buckley CH, McNeilly AS, Glasier AF. Morphological and functional features of endometrial decidualization following long-term intrauterine levonorgestrel delivery. Hum Reprod 1998;13:1218-1224.
7. Debbage PL, Solder E, Seidl S, Hutzler P, Hugl B, Ofner D, Kreczy A. Intravital lectin perfusion analysis of vascular permeability in human micro- and macro- blood vessels. Histochem Cell Biol 2001; 116:349-359.
8. Donnez J, Smoes P, Gillerot S, Casanas-Roux F, Nisolle M. Vascular endothelial growth factor (VEGF) in endometriosis. Hum Reprod 1998; 13:1686-1690.
9. Eggermont J, Donnez J, Casanas-Roux F, Scholtes H, Van Langendonckt A. Time course of pelvic endometriotic lesion revascularization in a nude mouse model. Fertil Steril 2005;84:492-499.
10. Fraser HM, Lunn SF. Angiogenesis and its control in the female reproductive system. Br Med Bull 2000;56:787-797.
11. Galili U. Abnormal expression of alpha-galactosyl epitopes in man. A trigger for autoimmune processes? Lancet 1989;2:358-361.
12. Galili U, Shohet SB, Kobrin E, Stults CL, Macher BA. Man, apes, and Old World monkeys differ from other mammals in the expression of alpha-galactosyl epitopes on nucleated cells. J Biol Chem 1988; 263:17755-17762.
13. Gargett CE, Rogers PA. Human endometrial angiogenesis. Reproduction 2001;121:181-186.
14. Girling JE, Rogers PA. Recent advances in endometrial angiogenesis research. Angiogenesis 2005;8:89-99.
15. Gordon JD, Shifren JL, Foulk RA, Taylor RN, Jaffe RB. Angiogenesis in the human female reproductive tract. Obstet Gynecol Surv 1995; 50:688-697.
16. Grummer R. Animal models in endometriosis research. Hum Reprod Update 2006;12:641-649.
17. Grummer R, Schwarzer F, Bainczyk K, Hess-Stumpp H, Regidor PA, Schindler AE, Winterhager E. Peritoneal endometriosis: validation of an in-vivo model. Hum Reprod 2001;16:1736-1743.
18. Hickey M, Dwarte D, Fraser IS. Superficial endometrial vascular fragility in Norplant users and in women with ovulatory dysfunctional uterine bleeding. Hum Reprod 2000;15:1509-1514.
19. Hull ML, Charnock-Jones DS, Chan CL, Bruner-Tran KL, Osteen KG, Tom BD, Fan TP, Smith SK. Antiangiogenic agents are effective inhibitors of endometriosis. J Clin Endocrinol Metab 2003;88:2889-2899.
20. Jaffe RB. Importance of angiogenesis in reproductive physiology. Semin Perinatol 2000;24:79-81.
21. Jondet M, Letellier B, Verdys MT. Endometrial vascularization in levonorgestrel intrauterine device users; computerized microvessel measurement study. Contraception 2005;71:60-64.
22. Kawashima H, Sueyoshi S, Li H, Yamamoto K, Osawa T. Carbohydrate binding specificities of several poly-N-acetyllactosamine-binding lectins. Glycoconj J 1990;7:323-334.
23. Krikun G, Schatz F, Lockwood CJ. Endometrial angiogenesis: from physiology to pathology. Ann N Y Acad Sci 2004;1034:27-35.
24. Masuda H, Maruyama T, Hiratsu E, Yamane J, Iwanami A, Nagashima T, Ono M, Miyoshi H, Okano HJ, Ito M et al. Noninvasive and real-time assessment of reconstructed functional human endometrium in NOD/SCID/gamma c(null) immunodeficient mice. Proc Natl Acad Sci USA 2007;104:1925-1930.
25. Matsuura-Sawada R, Murakami T, Ozawa Y, Nabeshima H, Akahira J, Sato Y, Koyanagi Y, Ito M, Terada Y, Okamura K. Reproduction of menstrual changes in transplanted human endometrial tissue in immunodeficient mice. Hum Reprod 2005;20:1477-1484.
26. McCluggage WG, Sumathi VP, Maxwell P. CD10 is a sensitive and diagnostically useful immunohistochemical marker of normal endometrial stroma and of endometrial stromal neoplasms. Histopathology 2001;39:273- 278.
27. Mints M, Blomgren B, Falconer C, Fianu-Jonasson A, Palmblad J. Microvascular density, vascular endothelial growth factor A, and its receptors in endometrial blood vessels in patients with menorrhagia. Fertil Steril 2005;84:692-700.
28. Mints M, Hultenby K, Zetterberg E, Blomgren B, Falconer C, Rogers R, Palmblad J. Wall discontinuities and increased expression of vascular endothelial growth factor-A and vascular endothelial growth factor receptors 1 and 2 in endometrial blood vessels of women with menorrhagia. Fertil Steril 2007;88:691-697.
29. Mints M, Jansson M, Sadeghi B, Westgren M, Uzunel M, Hassan M, Palmblad J. Endometrial endothelial cells are derived from donor stem cells in a bone marrow transplant recipient. Hum Reprod 2008; 23:139-143.
30. Murphy TJ, Thurston G, Ezaki T, McDonald DM. Endothelial cell heterogeneity in venules of mouse airways induced by polarized inflammatory stimulus. Am J Pathol 1999;155:93-103.
31. Nap AW, Griffioen AW, Dunselman GA, Bouma-Ter Steege JC, Thijssen VL, Evers JL, Groothuis PG. Antiangiogenesis therapy for endometriosis. J Clin Endocrinol Metab 2004;89:1089-1095.
32. Nisolle M, Casanas-Roux F, Donnez J. Early-stage endometriosis: adhesion and growth of human menstrual endometrium in nude mice. Fertil Steril 2000;74:306-312.
33. Noyes RW, Hertig AT, RocK J. Dating the endometrial biopsy. Fertil Steril 1950;1:3-25.
34. Pena LA, Fuks Z, Kolesnick RN. Radiation-induced apoptosis of endothelial cells in the murine central nervous system: protection by fibroblast growth factor and sphingomyelinase deficiency. Cancer Res 2000;60:321- 327.
35. Risau W. Mechanisms of angiogenesis. Nature 1997;386:671- 674.
36. Rogers PA, Plunkett D, Affandi B. Perivascular smooth muscle alpha-actin is reduced in the endometrium of women with progestin-only contraceptive breakthrough bleeding. Hum Reprod 2000;15:78-84.
37. Rydberg L, Holgersson J, Samuelsson BE, Breimer ME. Alpha-Gal epitopes in animal tissue glycoproteins and glycolipids. Subcell Biochem 1999; 32:107-125.
38. Saito M, Sato Y, Watanabe J, Kuramoto H, Kaba S, Fukuda T. Angiogenic factors in normal endometrium and endometrial adenocarcinoma. Pathol Int 2007;57:140-147.
39. Smith SK. Regulation of angiogenesis in the endometrium. Trends Endocrinol Metab 2001;12:147-151.
40. Stephanie R, Labied S, Blacher S, Frankenne F, Munaut C, Fridman V, Beliard A, Foidart JM, Nisolle M. Endometrial vessel maturation in women exposed to levonorgestrel-releasing intrauterine system for a short or prolonged period of time. Hum Reprod 2007;22: 3084-3091.
41. Story L, Kennedy S. Animal studies in endometriosis: a review. ILAR J 2004; 45:132-138.
42. Van Cauwenberge D, Pierard GE, Foidart JM, Lapiere CM. Immunohistochemical localization of laminin, type IV and type V collagen in basal cell carcinoma. Br J Dermatol 1983;108:163-170.
43. Zeng X, Murata T, Kawagishi H, Usui T, Kobayashi K. Analysis of specific interactions of synthetic glycopolypeptides carrying N-acetyllactosamine and related compounds with lectins. Carbohydr Res 1998;312: 209-217.