Injection of soluble vascular endothelial growth factor receptor 1 into the preovulatory follicle disrupts ovulation and subsequent luteal function in rhesus monkeys

Biology of Reproduction

Volumn 67, Issue 4, 2002, Pages 1305-1312

  Hazzard, Timothy M ^a   Xu, Fuhua ^a   Stouffer, Richard L ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Ovary; Ovulation

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; CD31 ANTIGEN; LUTEINIZING HORMONE; PROGESTERONE; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORPUS LUTEUM FUNCTION; DOSE RESPONSE; EXTRACELLULAR SPACE; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LUTEINIZATION; LUTEINIZING HORMONE RELEASE; MENSTRUAL CYCLE; NONHUMAN; OVULATION; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; RHESUS MONKEY; TUNICA ALBUGINEA;

ANIMALIA; MACACA MULATTA; PRIMATES;

EID: 0036785248     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod67.4.1305     Document Type: Article

References (43)

1. Redmer DA, Reynolds LP. Angiogenesis in the ovary. Rev Reprod 1996;1:182-192.
2. Ferrara N, Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev 1997; 18:4-25.
3. Hazzard TM. Christenson LK, Stouffer RL. Changes in expression of vascular endothelial growth factor (VEGF), angiopoietin (Ang)-1 and Ang-2 in the macaque corpus luteum during the menstrual cycle. Mol Hum Reprod 2000; 6:993-998.
4. Christenson LK, Stouffer RL. Follicle-stimulating hormone and luteinizing hormone/chorionic gonadotropin stimulation of vascular endothelial growth factor production by macaque granulosa cells from pre- and periovulatory follicles. J Clin Endocrinol Metab 1997; 82: 2135-2142.
5. Zachary I, Gliki G. Signaling transduction mechanisms mediating biological actions of the vascular endothelial growth factor family. Cardiovasc Res 2001; 49:568-581.
6. Fong G-H, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 1995; 376:66-69.
7. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu X-F, Breitman ML, Schuh AC. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995; 376:62-66.
8. Sugino N, Kashida S, Takiguchi S, Karube A, Kato H. Expression of vascular endothelial growth factor and its receptors in the human corpus luteum during the menstrual cycle and in early pregnancy. J Clin Endocrinol Metab 2000; 85:3919-3924.
9. Hazzard TM, Nayak NR, Stouffer RL. Localized expression of mRNAs for angiopoietins (Ang-1, Ang-2) and their specific receptor (Tie-2) in the primate corpus luteum (CL) during the menstrual cycle. In: Program of the 34th annual meeting of the Society for the Study of Reproduction; 2001; Ottawa, ON, Canada. Abstract 326.
10. Scheffler LJ, Hazzard TM, Nayak NR, Stouffer RL. First evidence for expression of neuropilin-1 (NP-1), an isoform-specific vascular endothelial growth factor (VEGF) coreceptor, in the primate corpus luteum. In: Program of the 34th annual meeting of the Society for the Study of Reproduction; 2001; Ottawa, ON, Canada. Abstract 327.
11. Kendall RL, Wang G, Thomas KA. Identification of a natural soluble form of the vascular endothelial growth factor receptor, FLT-1, and its heterodimerization with KDR. Biochem Biophys Res Commun 1996; 226:324-328.
12. Clark DE, Smith SK, He Y, Day KA, Licence DR, Corps AN, Lammoglia R, Charnock-Jones DS. A vascular endothelial growth factor antagonist is produced by the human placenta and released into the maternal circulation. Biol Reprod 1998; 59:1540-1548.
13. Hornig C, Behn T, Bartsch W, Yayon A, Weich HA. Detection and quantification of complexed and free soluble human vascular endothelial growth factor receptor-1 (sVEGFR-1) by ELISA. J Immunol Methods 1999; 226:169-177.
14. Ferrara N, Chen H, Davis-Smyth T, Gerber H-P, Nguyen T-H. Peers D, Chisholm V, Hillan KJ, Schwall RH. Vascular endothelial growth factor is essential for corpus luteum angiogenesis. Nat Med 1998; 4: 336-340.
15. 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.
16. 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.
17. Hazzard TM, Molskness TA. Rohan RM, D'Amato RJ, Stouffer RL. Injection of an angiogenesis inhibitor (TNP-470) into the periovulatory follicle causes luteal dysfunction in rhesus monkeys. Endocrine 2002; 17:199-206.
18. Wolf DP. Thomson JA, Zelinski-Wooten MB, Stouffer RL. In vitro fertilization-embryo transfer in nonhuman primates: the technique and its applications. Mol Reprod Dev 1990; 27:261-280.
19. National Academy of Sciences. Guide for the Care and Use of Laboratory Animals. Washington: National Academy Press; 1996.
20. Resko JA. Ploem JG, Stadelman HL. Estrogens in fetal and maternal plasma of the rhesus monkey. Endocrinology 1975; 97:425-430.
21. Hess DL, Spies HG, Hendrickx AG. Diurnal steroid patterns during gestation in the rhesus macaque: onset, daily variation, and the effects of dexamethasone treatment. Biol Reprod 1981;24:609-616.
22. Stouffer RL, Dahl KD, Hess DL, Woodruff TK, Mather JP, Molskness TA. Systemic and intraluteal infusion of inhibin A or activin A in rhesus monkeys during the luteal phase of the menstrual cycle. Biol Reprod 1994; 50:888-895.
23. Ginther OJ, Kot K, Kulik LJ, Wiltbank MC. Sampling follicular fluid without altering follicular status in cattle: oestradiol concentrations early in a follicular wave. J Reprod Fertil 1997; 109:181-186.
24. Duffy DM, Chaffin CL, Stouffer RL. Expression of estrogen receptor α and β in the rhesus monkey corpus luteum during the menstrual cycle: regulation by luteinizing hormone and progesterone. Endocrinology 2000; 141: 1711-1717.
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. Christenson LK, Stouffer RL. Proliferation of microvascular endothelial cells in the primate corpus luteum during the menstrual cycle and simulated early pregnancy. Endocrinology 1996; 137:367-374.
27. Hild-Petito S, Stouffer RL, Brenner RM. Immunocytochemical localization of estradiol and progesterone receptors in the monkey ovary throughout the menstrual cycle. Endocrinology 1988; 123:2896-2905.
28. Tsoi SCM, Zheng J, Xu F, Kay HH. Differential expression of lactate dehydrogenase isozymes (LDH) in human placenta with high expression of LDH-A4 isozymes in the endothelial cells of pre-eclampsia villi. Placenta 2001; 22:317-322.
29. Brasaemle DL, Attie AD. Microelisa reader quantitation of fixed, stained, solubilized cells in microtitre dishes. Biotechniques 1988; 6: 418-419.
30. Zelinski-Wooten MB, Slayden OD, Chwalisz K, Hess DL. Brenner RM, Stouffer RL. Outstanding contribution. 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.
31. Hibbert ML. Stouffer RL, Wolf DP, Zelinski-Wooten MF. Midcycle administration of a progesterone synthesis inhibitor prevents ovulation in primates. Proc Natl Acad Sci U S A 1996; 93:1897-1901.
32. Ravindranath N, Little-Ihrig L, Phillips HS, Ferrara N, Zeleznik AJ. Vascular endothelial growth factor messenger ribonucleic acid expression in the primate ovary. Endocrinology 1992; 131:254-260.
33. LeCouter J, Kowalski J, Foster J, Hass P, Zhang Z, Dillard-Telm L, Frantz G, Rangell L, DeGuzman L, Keller GA, Peale F. Gurney A, Hillan KJ, Ferrara N. Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature 2001; 412:877-884.
34. Comer GW, Hartman CG, Bartelmez GW. Development, organization, and breakdown of the corpus luteum in the rhesus monkey. Contrib Embryol 1945; 204:119-146.
35. Saraste A, Pulkki K. Morphologic and biochemical hallmarks of apoptosis. Cardiovasc Res 2000; 45:528-537.
36. Dickson SE, Bicknell R, Fraser HM. Mid-luteal angiogenesis and function in the primate is dependent on vascular endothelial growth factor. J Endocrinol 2001; 168:409-416.
37. Lammert E, Cleaver O, Melton D. Induction of pancreatic differentiation by signals from blood vessels. Science 2001; 294:564-567
38. Meidan R, Milvae RA, Weiss S, Levy N, Friedman A. Intraovarian regulation of luteolysis. J Reprod Fertil Suppl 1999; 54:217-228
39. Bateman BG, Kolp LA, Nunley WC Jr, Thomas TS, Mills SE. Oocyte retention after follicle luteinization. Fertil Steril 1990; 54:793.
40. Glock JL, Brumsted JR. Color flow pulsed Doppler ultrasound in diagnosing luteal phase defect. Fertil Steril 1995; 64:500-504.
41. Ghosh D, Lalitkumar PGL, Wong V, Dhawan L, Rosario JF, Hendrickx AG, Lasley BL, Overstreet JW, Sengupta J. Effect of vaginally administered fumagillin on the morphology of implantation stage endometrium in the rhesus monkey. Contraception 2001; 63:95-102.
42. Levin ER, Rosen GF, Cassidenti DL, Yee B, Meldrum D, Wisot A, Pedram A. Role of vascular endothelial cell growth factor in ovarian hyperstimulation syndrome. J Clin Invest 1998; 102:1978-1995.
43. Cao Y. Endogenous angiogenesis inhibitors and their therapeutic implications. Int J Biochem Cell Biol 2001; 33:357-369.