Inhibition of delta-like ligand 4 induces luteal hypervascularization followed by functional and structural luteolysis in the primate ovary

Endocrinology

Volumn 153, Issue 4, 2012, Pages 1972-1983

  Fraser, Hamish M ^a   Hastings, Julie M ^a   Allan, Deborah ^a   Morris, Keith D ^a   Rudge, John S ^b   Wiegand, Stanley J ^b  

^a MRC Reproductive Biology Unit   (United Kingdom)

^b REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DELTA LIKE LIGAND 4; IMMUNOGLOBULIN G; LIGAND; NEUTRALIZING ANTIBODY; NOTCH RECEPTOR; PROGESTERONE; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL EXPERIMENT; ARTICLE; CALLITRICHINAE; CELL DEATH; CONTROLLED STUDY; FEMALE; FOLLICULAR PHASE; IMMUNOHISTOCHEMISTRY; INHIBITION KINETICS; LUTEAL HYPERVASCULARIZATION; LUTEAL PHASE; LUTEOLYSIS; NONHUMAN; OVARY; OVARY FOLLICLE DEVELOPMENT; OVULATION; PRIMATE; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; VASCULARIZATION;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIGENS, CD31; APOPTOSIS; CALLITHRIX; CORPUS LUTEUM; FEMALE; IMMUNOGLOBULIN G; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LUTEOLYSIS; MEMBRANE PROTEINS; MODELS, ANIMAL; NEOVASCULARIZATION, PHYSIOLOGIC; OVARY; PROGESTERONE; RECEPTORS, NOTCH; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84859390615     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-1688     Document Type: Article

References (54)

1. Reynolds LP, Killilea SD, Redmer DA 1992 Angiogenesis in the female reproductive system. FASEB J 6:886-892
2. Hazzard TM, Stouffer RL 2000 Angiogenesis in ovarian follicular and luteal development. Baillieres Best Pract Res Clin Obstet Gynaecol 14:883-900 (Pubitemid 32123679)
3. Stocco C, Telleria C, Gibori G 2007 The molecular control of corpus luteum formation, function, and regression. Endocr Rev 28:117-149 (Pubitemid 46220852)
4. Robinson RS, Woad KJ, Hammond AJ, Laird M, Hunter MG, Mann GE 2009 Angiogenesis and vascular function in the ovary. Reproduction 138:869-881
5. Fraser HM, Duncan WC 2009 Regulation and manipulation of angiogenesis in the ovary and endometrium. Reprod Fertil Dev 21:377-392
6. Kaczmarek MM, Schams D, Ziecik AJ 2005 Role of vascular endothelial growth factor in ovarian physiology-an overview. Reprod Biol 5:111-136
7. Delgado-Rosas F, Gaytán M, Morales C, Gómez R, Gaytán F 2009 Superficial ovarian cortex vascularization is inversely related to the follicle reserve in normal cycling ovaries and is increased in polycystic ovary syndrome. Hum Reprod 24:1142-1151
8. Gómez R, Simón C, Remohi J, Pellicer A 2002 Vascular endothelial growth factor receptor 2 activation induces vascular permeability in hyperstimulated rats, and this effect is prevented by receptor blockade. Endocrinology 143:4339-4348 (Pubitemid 35239566)
9. Rodewald M, Herr D, Duncan WC, Fraser HM, Hack G, Konrad R, Gagsteiger F, Kreienberg R, Wulff C 2009 Molecular mechanisms of ovarian hyperstimulation syndrome: paracrine reduction of endothelial claudin 5 by hCG in vitro is associated with increased endothelial cell permeability. Hum Reprod 24:1191-1199
10. Fraser HM, Dickson SE, Lunn SF, Wulff C, Morris KD, Carroll VA, Bicknell R 2000 Suppression of luteal angiogenesis in the primate after neutralization of vascular endothelial growth factor. Endocrinology 141:995-1000 (Pubitemid 32260443)
11. Wulff C, Wilson H, Rudge JS, Wiegand SJ, Lunn SF, Fraser HM 2001 Luteal angiogenesis: prevention and intervention by treatment with vascular endothelial growth factor trap A40. J Clin Endocrinol Metab 86:3377-3386 (Pubitemid 32673511)
12. Fraser HM, Wilson H, Rudge JS, Wiegand SJ 2005 Single injections of vascular endothelial growth factor trap block ovulation in the macaque and produce a prolonged, dose-related suppression of ovarian function. J Clin Endocrinol Metab 90:1114-1122 (Pubitemid 40279242)
13. Fraser HM, Wilson H, Morris KD, Swanston I, Wiegand SJ 2005 Vascular endothelial growth factor Trap suppresses ovarian function at all stages of the luteal phase in the macaque. J Clin Endocrinol Metab 90:5811-5818 (Pubitemid 41415497)
14. Fraser HM, Wilson H, Wulff C, Rudge JS, Wiegand SJ 2006 Administration of vascular endothelial growth factor Trap during the 'post-angiogenic' period of the luteal phase causes rapid functional luteolysis and selective endothelial cell death in the marmoset. Reproduction 132:589-600 (Pubitemid 44660533)
15. Taylor PD, Wilson H, Hillier SG, Wiegand SJ, Fraser HM 2007 Effects of inhibition of vascular endothelial growth factor at time of selection on follicular angiogenesis, expansion, development and atresia in the marmoset. Mol Hum Reprod 13:729-736 (Pubitemid 47543411)
16. Wulff C, Wilson H, Wiegand SJ, Rudge JS, Fraser HM 2002 Prevention of thecal angiogenesis, antral follicular growth, and ovulation in the primate by treatment with vascular endothelial growth factor Trap R1R2. Endocrinology 143:2797-2807 (Pubitemid 34701344)
17. Ferrara N, Chen H, Davis-Smyth T, Gerber, HP, Nguyen, TN, Peers D, Chisholm V, Hillan KJ, Schwall RH 1998 Vascular endothelial growth factor is essential for corpus luteum angiogenesis. Nat Med 4:336-340 (Pubitemid 28144094)
18. Zimmermann RC, Xiao E, Husami N, Sauer MV, Lobo R, Kitajewski J, Ferin M 2001 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 86:768-772 (Pubitemid 32207494)
19. Zimmermann RC, Xiao E, Bohlen P, FerinM2002 Administration of antivascular endothelial growth factor receptor 2 antibody in the early follicular phase delays follicular selection and development in the rhesus monkey. Endocrinology 143:2496-2502 (Pubitemid 34701311)
20. Zimmermann RC, Hartman T, Kavic S, Pauli SA, Bohlen P, Sauer MV, Kitajewski J 2003 Vascular endothelial growth factor receptor 2-mediated angiogenesis is essential for gonadotropin-dependent follicle development. J Clin Invest 112:659-669 (Pubitemid 38057707)
21. Hazzard TM, Xu F, Stouffer RL 2002 Injection of soluble vascular endothelial growth factor receptor 1 into the preovulatory follicle disrupts ovulation and subsequent luteal function in rhesus monkey. Biol Reprod 67:1305-1312
22. Pauli SA, Tang H, Wang J, Bohlen P, Posser R, Hartman T, Sauer MV, Kitajewski J, Zimmermann RC 2005 The vascular endothelial growth factor (VEGF)/VEGF receptor pathway is critical for blood vessel survival in corpora lutea of pregnancy in the rodent. Endocrinology 146:1301-1311 (Pubitemid 40289317)
23. Clapp C, Thebault S, Jeziorski MC, Martínez De La Escalera G 2009 Peptide hormone regulation of angiogenesis. Physiol Rev 89:1117-1215
24. Bicknell R, Harris AL 2004 Novel angiogenic signalling pathways and vascular targets. Annu Rev Pharmacol Toxicol 44:219-238 (Pubitemid 38263840)
25. Gale NW, Dominguez MG, Noguera I, Pan L, Hughes V, Valenzuela DM, Murphy AJ, Adams NC, Lin HC, Holash J, Thurston G, Yancopoulos GD 2004 Haploinsufficiency δ-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proc Natl Acad Sci USA 101:15949-15954 (Pubitemid 39507907)
26. Lobov IB, Renard RA, Papadopoulos N, Gale NW, Thurston G, Yancopoulos GD, Wiegand SJ 2007 Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc Natl Acad Sci USA 104:3219-3224 (Pubitemid 46364140)
27. Hellström M, Phng LK, Hofmann JJ, Wallgard E, Coultas L, Lindblom P, Alva J, Nilsson AK, Karlsson L, Gaiano N, Yoon K, Rossant J, Iruela-Arispe ML, Kalén M, Gerhardt H, Betsholtz C 2007 Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445:776-780 (Pubitemid 46279716)
28. Suchting S, Freitas C, le Noble F, Benedito R, Bréant C, Duarte A, Eichmann A 2007 The Notch ligand δ-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc Natl Acad Sci USA 104:3225-3230 (Pubitemid 46364141)
29. Noguera-Troise I, Daly C, Papadopoulos NJ, Coetzee S, Boland P, Gale NW, Lin HC, Yancopoulos GD, Thurston G 2006 Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 444:1032-1037 (Pubitemid 46018516)
30. Ridgway J, Zhang G, Wu Y, Stawicki S, Liang WC, Chanthery Y, Kowalski J, Watts RJ, Callahan C, Kasman I, Singh M, Chien M, Tan C, Hongo JA, de Sauvage F, Plowman G, Yan M 2006 Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 444:1083-1087 (Pubitemid 46018529)
31. Thurston G, Noguera-Troise I, Yancopoulos GD 2007 The δ paradox: DLL4. blockade leads to more tumor vessels but less tumour growth. Nat Rev Cancer 7:327-331 (Pubitemid 46652486)
32. Thurston G, Kitajewski J 2008 VEGF and δ-Notch: interacting signalling pathways in tumour angiogenesis. Br J Cancer 99:1204-1209
33. Christenson LK, Stouffer RL 1996 Proliferation of microvascular endothelial cells in the primate corpus luteum during the menstrual cycle and simulated early pregnancy. Endocrinology 137:367-374 (Pubitemid 26005012)
34. Gaytán F, Morales C, García-Pardo L, Reymundo C, Bellido C, Sánchez-Criado JE 1999 A quantitative study of changes in the human corpus luteum microvasulature during the menstrual cycle. Biol Reprod 60:914-919 (Pubitemid 29149377)
35. Dickson SE, Fraser HM 2000 Inhibition of early luteal angiogenesis by gonadotropin-releasing hormone antagonist treatment in the primate. J Clin Endocrinol Metab 85:2339-2344 (Pubitemid 32269266)
36. Wulff C, Dickson SE, Duncan WC, Fraser HM 2001 Angiogenesis in the human corpus luteum: simulated early pregnancy by HCG treatment is associated with both angiogenesis and vessel stabilization. Hum Reprod 16:2515-2524 (Pubitemid 34007465)
37. Johnson J, Espinoza T, McGaughey RW, Rawls A, Wilson-Rawls J 2001 Notch pathway genes are expressed in mammalian ovarian follicles. Mech Dev 109:355-361 (Pubitemid 33112048)
38. Vorontchikhina MA, Zimmermann RC, Shawber CJ, Tang H, Kitajewski J 2005 Unique patterns of Notch1, Notch4 and jagged 1 expression in ovarian vessels during folliculogenesis and corpus luteum formation. Gene Expr Patterns 5:701-709 (Pubitemid 40796616)
39. Hernandez F, Peluffo MC, Stouffer RL, Irusta G, Tesone M 2011 Role of the DLL4-Notch system in PGEF2 α induced luteolysis in the pregnant rat. Biol Reprod 84:859-865
40. Mazella J, Liang S, Tseng L 2008 Expression of delta-like protein 4 in the human endometrium. Endocrinology 149:15-19
41. Bray SJ 2006 Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7:678-689 (Pubitemid 44268213)
42. Xu F, Stouffer RL 2005 Local delivery of angiopoietin-2 into the preovulatory follicle terminates the menstrual cycle in rhesus monkeys. Biol Reprod 72:1352-1358 (Pubitemid 40696078)
43. Morales C, Garcia-Pardo L, Reymundo C, Bellido C, Sánchez-Criado JE, Gaytán F 2000 Different patterns of structural luteolysis in the human corpus luteum of menstruation. Hum Reprod 15:2119-2128
44. Young FM, Illingworth PJ, Lunn SF, Harrison DJ, Fraser HM 1997 Cell death during luteal regression in the marmoset monkey (Callithrix jacchus). J Reprod Fertil 111:109-119
45. Fraser HM, Lunn SF, Harrison DJ, Kerr JB 1999 Luteal regression in the primate: different forms of cell death during natural and gonadotropin-releasing hormone antagonist or prostaglandin analogue-induced luteolysis. Biol Reprod 61:1468-1479
46. Rowe AJ, Morris KD, Bicknell R, Fraser HM 2002 Angiogenesis in the corpus luteum of early pregnancy in the marmoset and the effects of vascular endothelial growth factor immunoneutralization on establishment of pregnancy. Biol Reprod 67:1180-1188
47. Baum O, Suter F, Gerber B, Tschanz SA, Buergy R, Blank F, Hlushchuk R, Djonov V 2010 VEGF-A promotes intussusceptive angiogenesis in the developing chicken chorioallantoic membrane. Microcirculation 17:447-457
48. Pettersson A, Nagy JA, Brown LF, Sundberg C, Morgan E, Jungles S, Carter R, Krieger JE, Manseau EJ, Harvey VS, Eckelhoefer IA, Feng D, Dvorak AM, Mulligan RC, Dvorak HF 2000 Heterogeneity of the angiogenic response induced in different normal adult tissues by vascular permeability/vascular endothelial growth factor. Lab Invest 80:99-115 (Pubitemid 30067385)
49. Macchiarelli G, Jiang JY, Nottola SA, Sato E 2006 Morphological patterns of angiogenesis in ovarian follicle capillary networks. A scanning electron microscopy study of corrosion cast. Microsc Res Tech 69:459-468 (Pubitemid 43878056)
50. Garcia C, Gomez R, Kitajewski J, Carrie S, Pellicer A, Zimmermann RC 2011 Notch (N1) signalling regulates sprouting angiogenesis (SA) in corpora lutea (CL) through tip cells (TC) and stalk cells (SC). 58th Annual Meeting SGI, Miami Beach, FL, 2011, Suppl Rep Sci 18:O-060, p 173A
51. Levine BA, Jovanovic V, Sauer CM, Shawber CJ, Gomez R, Sauer MV, Kitajewski J, Zimmermann RC 2011 Role of Notch in gonadotropin-dependent folliculogenesis in the rodent. 58th Annual Meeting SGI, Miami Beach, FL, 2011, Suppl Rep Sci 18:S-163. p 341A
52. Yan M, Callahan CA, Beyer JC, Allamneni KP, Zhang G, Ridgway JB, Niessen K, Plowman GD 2010 Chronic Dll4 blockade induces vascular neoplasms. Nature 463:E6-E7
53. Liu Z, Turkoz A, Jackson EN, Corbo JC, Engelbach JA, Garbow JR, Piwnica-Worms DR, Kopan R 2011 Notch1 loss of heterozygosity causes vascular tumors and lethal hemorrhage in mice. J Clin Invest 121:800-808
54. Ryeom SW 2011 A cautionary tale of side effects of Notch 1 inhibition. J Clin Invest 121:508-509