Local delivery of angiopoietin-2 into the preovulatory follicle terminates the menstrual cycle in rhesus monkeys

Biology of Reproduction

Volumn 72, Issue 6, 2005, Pages 1352-1358

  Xu, Fuhua ^a   Stouffer, Richard L ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Angiogenesis; Angiopoietin 1; Angiopoietin 2; Corpus luteum; Follicle; Menstrual cycle; Ovary; Ovulation; Preovulatory follicle; Rhesus monkeys

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN 2; ESTRADIOL; PROGESTERONE;

ANGIOGENESIS; ARTICLE; CONTROLLED STUDY; CORPUS LUTEUM; ESTRADIOL BLOOD LEVEL; FEMALE; LAPAROSCOPY; LUTEINIZATION; MATURATION; MENSTRUAL CYCLE; MONKEY; NONHUMAN; OVARY; OVARY CYCLE; OVARY FOLLICLE MATURATION; OVULATION; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL;

ANGIOPOIETIN-1; ANGIOPOIETIN-2; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; FEMALE; INJECTIONS, INTRALESIONAL; MACACA MULATTA; MENSTRUAL CYCLE; OVARIAN FOLLICLE; OVULATION; PROGESTERONE;

ANIMALIA; MACACA MULATTA; PRIMATES;

EID: 18844374203     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.104.037143     Document Type: Article

References (45)

1. Koos RD. Ovarian angiogenesis. In: Adashi EY, Leung PCK (eds). The Ovary. New York: Raven Press; 1993:433-453.
2. Reynolds LP, Redmer DA. Expression of the angiogenic factors, basic fibroblast growth factor and vascular endothelial growth factor, in the ovary. J Anim Sci 1998; 76:1671-1681.
3. Ferrara N, Henzel WJ. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun 1989; 161:851-858.
4. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, Compton D, McClain J, Aldrich TH, Papadopoulos N, Daly TJ, Davis S, Sato TN, Yancopoulos GD. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 1997; 277:55-60.
5. Hazzard TM, Molskness TA, Chaffin CL, Stouffer RL. Vascular endothelial growth factor (VEGF) and angiopoietin regulation by gonadotrophin and steroids in macaque granulosa cells during the periovulatory interval. Mol Hum Reprod 1999; 5:1115-1121.
6. Hazzard TM, Christenson LK, Stouffer RL. Changes in expression of vascular endothelial growth factor and angiopoietin-1 and -2 in the macaque corpus luteum during the menstrual cycle. Mol Hum Reprod 2000; 6:993-998.
7. Hazzard TM, Stouffer RL. Angiogenesis in ovarian follicular and luteal development. Baillieres Best Pract Res Clin Obstet Gynaecol 2000; 14:883-900.
8. Fraser HM, Wulff C. Angiogenesis in the primate ovary. Reprod Fertil Dev 2001; 13:557-566.
9. Fraser HM, Wulff C. Angiogenesis in the corpus luteum. Reprod Biol Endocrinol 2003; 1:88.
10. Davis S, Aldrich TH, Jones PF, Acheson A, Compton DL, Jain V, Ryan TE, Bruno J, Radziejewski C, Maisonpierre PC, Yancopoulos GD. Isolation of angiopoietin-I, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 1996; 87:1161-1169.
11. Valenzuela DM, Griffiths JA, Rojas J, Aldrich TH, Jones PF, Zhou H, McClain J, Copeland NG, Gilbert DJ, Jenkins NA, Huang T, Papadopoulos N, Maisonpierre PC, Davis S, Yancopoulos GD. Angiopoietins 3 and 4: diverging gene counterparts in mice and humans. Proc Natl Acad Sci U S A 1999; 96:1904-1909.
12. Lee HJ, Cho CH, Hwang SJ, Choi HH, Kim KT, Ahn SY, Kim JH, Oh JL, Lee GM, Koh GY. Biological characterization of angiopoietin-3 and angiopoietin-4. FASEB J 2004; 18:1200-1208.
13. Hanahan D. Signaling vascular morphogenesis and maintenance. Science 1997; 277:48-50.
14. Hammes HP, Lin J, Wagner P, Feng Y, Vom Hagen F, Krzizok T, Renner O, Breier G, Brownlee M, Deutsch U. Angiopoietin-2 causes pericyte dropout in the normal retina: evidence for involvement in diabetic retinopathy. Diabetes 2004; 53:1104-1110.
15. Wulff C, Wilson H, Largue P, Duncan WC, Armstrong DG, Fraser HM. Angiogenesis in the human corpus luteum: localization and changes in angiopoietins, tie-2, and vascular endothelial growth factor messenger ribonucleic acid. J Clin Endocrinol Metab 2000; 85:4302-4309.
16. Hata K, Udagawa J, Fujiwaki R, Nakayama K, Otani H, Miyazaki K. Expression of angiopoietin-1, angiopoietin-2, and Tie2 genes in normal ovary with corpus luteum and in ovarian cancer. Oncology 2002; 62:340-348.
17. Klauber N, Rohan RM, Flynn E, D'Amato RJ. Critical components of the female reproductive pathway are suppressed by the angiogenesis inhibitor AGM-1470. Nat Med 1997; 3:443-446.
18. Hazzard TM, Xu F, Stouffer RL. Injection of soluble vascular endothelial growth factor receptor 1 into the preovulatory follicle disrupts ovulation and subsequent luteal function in rhesus monkeys. Biol Reprod 200267:1305-1312.
19. Zimmermann RC, Xiao E, Husami N, Sauer MV, Lobo R, Kitajewski J, Ferin M. Short-term administration of antivascular endothelial growth factor antibody in the late follicular phase delays follicular development in the rhesus monkey. J Clin Endocrinol Metab 2001; 86:768-772.
20. Zimmermann RC, Hartman T, Bohlen P, Sauer MV, Kitajewski J. Preovulatory treatment of mice with anti-VEGF receptor 2 antibody inhibits angiogenesis in corpora lutea. Microvasc Res 2001; 62:15-25.
21. Fraser HM, Dickson SE, Lunn SF, Wulff C, Morris KD, Carroll VA, Bicknell R. Suppression of luteal angiogenesis in the primate after neutralization of vascular endothelial growth factor. Endocrinology 2000; 141:995-1000.
22. Wolf DP, Thomson JA, Zelinski-Wooten MB, Stouffer RL. In vitro fertilization-embryo transfer in nonhuman primates: the technique and applications. Mol Reprod Dev 1990; 27:261-280.
23. National Academy of Sciences. Guide for the Care and Use of Laboratory Animals. Washington: National Academy Press; 1996.
24. Young KA, Stouffer RL. Gonadotropin and steroid regulation of matrix metalloproteinases and their endogenous tissue inhibitors in the developed corpus luteum of the rhesus monkey during the menstrual cycle. Biol Reprod 2004; 70:244-252.
25. Ellinwood WE, Norman RL, Spies HG. Changing frequency of pulsatile luteinizing hormone and progesterone secretion during the luteal phase of the menstrual cycle of rhesus monkeys. Biol Reprod 1984; 31:714-722.
26. Xu F, Hazzard TM, Evans A, Charnock-Jones S, Smith S, Stouffer RL. Intraovarian actions of anti-angiogenic agents disrupt peri-ovulatory events during the menstrual cycle in monkeys. Contraception 2005; (in press).
27. Zelinski-Wooten MB, Slayden OD, Chwalisz K, Hess DL, Brenner RM, Stouffer RL. Chronic treatment of female rhesus monkeys with low doses of the antiprogestin ZK 137 316: establishment of a regimen that permits normal menstrual cyclicity. Hum Reprod 1998; 13:259-267.
28. Hayashi KG, Acosta TJ, Tetsuka M, Berisha B, Matsui M, Schams D, Ohtani M, Miyamoto A. Involvement of angiopoietin-tie system in bovine follicular development and atresia: messenger RNA expression in theca interna and effect on steroid secretion. Biol Reprod 2003; 69:2078-2084.
29. Hayashi KG, Berisha B, Matsui M, Schams D, Miyamoto A. Expression of mRNA for the angiopoietin-tie system in granulosa cells during follicular development in cows. J Reprod Dev 2004; 50:477-480.
30. Hazzard TM, Rohan RM, Molskness TA, Fanton JW, D'Amato RJ, Stouffer RL. Injection of antiangiogenic agents into the macaque preovulatory follicle. Endocrine 2002; 17:199-206.
31. Suri C, McClain J, Thurston G, McDonald DM, Zhou H, Oldmixon EH, Sato TN, Yancopoulos GD. Increased vascularization in mice overexpressing angiopoietin-1. Science 1998; 282:468-471.
32. Thurston G, Suri C, Smith K, McClain J, Sato TN, Yancopoulos GD, McDonald DM. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science 1999; 286:2511-2514.
33. Yamauchi A, Ito Y, Morikawa M, Kobune M, Huang J, Sasaki K, Takahashi K, Nakamura K, Dehari H, Niitsu Y, Abe T, Hamada H. Pre-administration of angiopoietin-1 followed by VEGF induces functional and mature vascular formation in a rabbit ischemic model. J Gene Med 2003; 5:994-1004.
34. Wulff C, Wilson H, Rudge JS, Wiegand SJ, Lunn SF, Fraser HM. Luteal angiogenesis: prevention and intervention by treatment with vascular endothelial growth factor trap(A40). J Clin Endocrinol Metab 2001; 86:3377-3386.
35. Ferrara N, Frantz G, LeCouter J, Dillard-Telm L, Pham T, Draksharapu A, Giordano T, Peale F. Differential expression of the angiogenic factor genes vascular endothelial growth factor (VEGF) and endocrine gland-derived VEGF in normal and polycystic human ovaries. Am J Pathol 2003; 162:1881-1893.
36. Kisliouk T, Levy N, Hurwitz A, Meidan R. Presence and regulation of endocrine gland vascular endothelial growth factor/prokineticin-1 and its receptors in ovarian cells. J Clin Endocrinol Metab 2003; 88:3700-3707.
37. Dickson SE, Bicknell R, Fraser HM. Mid-luteal angiogenesis and function in the primate is dependent on VEGF. J Endocrinol 2001; 168:409-416.
38. Lobov IB, Brooks PC, Lang RA. Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo. Proc Natl Acad Sci U S A 2002; 99:11205-11210.
39. Jones PF. Not just angiogenesis - wider roles for the angiopoietins. J Pathol 2003; 201:515-527.
40. Jiang JY, Macchiarelli G, Tsang BK, Sato E. Capillary angiogenesis and degeneration in bovine ovarian antral follicles. Reproduction 2003; 125:211-223.
41. Goodman AL, Nixon WE, Johnson DK, Hodgen GD. Regulation of folliculogenesis in the cycling rhesus monkey: selection of the dominant follicle. Endocrinology 1977; 100:155-161.
42. Goodman AL, Koering MJ, Nixon WE, Williams RF, Hodgen GD. Follicle dominance and ovarian asymmetry after luteectomy in rhesus monkeys. Am J Physiol 1982; 243:E325-E331.
43. Araki S, Chikazawa K, Akabori A, Ijima K, Tamada T. Hormonal profile after removal of the dominant follicle and corpus luteum in women. Endocrinol Jpn 1983; 30:55-70.
44. Baird DT, Backstrom T, McNeilly AS, Smith SK, Wathen CG. Effect of enucleation of the corpus luteum at different stages of the luteal phase of the human menstrual cycle on subsequent follicular development. J Reprod Fertil 1984; 70:615-624.
45. Check JH, Dietterich C, Houck MA. Ipsilateral versus contralateral ovary selection of dominant follicle in succeeding cycle. Obstet Gynecol 1991; 77:247-249.