Inhibition of vascular endothelial growth factor receptor signal transduction blocks follicle progression but does not necessarily disrupt vascular development in perinatal rat ovaries

Biology of Reproduction

Volumn 81, Issue 5, 2009, Pages 966-977

  McFee, Renee M ^a   Artac, Robin A ^b   McFee, Ryann M ^b   Clopton, Debra T ^b   Longfellow Smith, Robyn A ^b   Rozell, Timothy G ^a   Cupp, Andrea S ^b  

^a KANSAS STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Follicle; Ovary; Tyrosine kinase inhibitor; Vascular development; VEGF

Indexed keywords

MESSENGER RNA; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN A;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GRANULOSA CELL; NONHUMAN; OVARY DEVELOPMENT; OVARY FOLLICLE CELL; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; AGE; ANALYSIS OF VARIANCE; ANGIOGENESIS; ANIMAL; CONFOCAL MICROSCOPY; DRUG EFFECT; FEMALE; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; METABOLISM; ORGAN CULTURE TECHNIQUE; OVARY; OVARY FOLLICLE; PHYSIOLOGY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; VASCULARIZATION;

RATTUS;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; NEOVASCULARIZATION, PHYSIOLOGIC; ORGAN CULTURE TECHNIQUES; OVARIAN FOLLICLE; OVARY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 73349142707     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.078071     Document Type: Article

References (75)

1. Hirshfield AN. Relationship between the supply of primordial follicles and the onset of follicular growth in rats. Biol Reprod 1994; 50:421-428.
2. Mazaud S, Guigon CJ, Lozach A, Coudouel N, Forest MG, Coffigny H, Magre S. Establishment of the reproductive function and transient fertility of female rats lacking primordial follicle stock after fetal gamma-irradiation. Endocrinology 2002; 143:4775-4787.
3. Guigon CJ, Mazaud S, Forest MG, Brailly-Tabard S, Magre S. Role of the first waves of growing follicles in rat ovarian maturation. Ann Endocrinol (Paris) 2003; 64:85.
4. Konishi I, Fujii S, Okamura H, Parmley T, Mori T. Development of interstitial cells and ovigerous cords in the human fetal ovary: an ultrastructural study. J Anat 1986; 148:121-135.
5. Hirshfield AN. Heterogeneity of cell populations that contribute to the formation of primordial follicles in rats. Biol Reprod 1992; 47:466-472.
6. Rajah R, Glaser EM, Hirshfield AN. The changing architecture of the neonatal rat ovary during histogenesis. Dev Dyn 1992; 194:177-192.
7. Pepling ME, Spradling AC. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol 2001; 234:339-351.
8. Gelety TJ, Magoffin DA. Ontogeny of steroidogenic enzyme gene expression in ovarian theca-interstitial cells in the rat: regulation by a paracrine theca-differentiating factor prior to achieving luteinizing hormone responsiveness. Biol Reprod 1997; 56:938-945.
9. Peters H, Levy E, Crone M. Deoxyribonucleic acid synthesis in oocytes of mouse embryos. Nature 1962; 195:915-916.
10. Kezele PR, Ague JM, Nilsson E, Skinner MK. Alterations in the ovarian transcriptome during primordial follicle assembly and development. Biol Reprod 2005; 72:241-255.
11. Roberts AE, Arbogast LK, Friedman CI, Cohn DE, Kaumaya PT, Danforth DR. Neutralization of endogenous vascular endothelial growth factor depletes primordial follicles in the mouse ovary. Biol Reprod 2007; 76:218-223.
12. Carmeliet P, Collen D. Role of vascular endothelial growth factor and vascular endothelial growth factor receptors in vascular development. Curr Top Microbiol Immunol 1999; 237:133-158.
13. Grunstein J, Masbad JJ, Hickey R, Giordano F, Johnson RS. Isoforms of vascular endothelial growth factor act in a coordinate fashion to recruit and expand tumor vasculature. Mol Cell Biol 2000; 20:7282-7291.
14. Springer M, Hortelano G, Bouley DM, Wong J, Kraft PE, Blau HM. Induction of angiogenesis by implantation of encapsulated primary myoblasts expressing vascular endothelial growth factor. J Gene Med 2000; 2:279-288.
15. Claesson-Welsh L. Signal transduction by vascular endothelial growth factor receptors. Biochem Soc Trans 2003; 31:20-24.
16. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995; 376:62-66.
17. Fong GH, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 1995; 376:66-70.
18. Shibuya M. Structure and dual function of vascular endothelial growth factor receptor-1 (Flt-1). Int J Biochem Cell Biol 2001; 33:409-420.
19. Bott RC, McFee RM, Clopton DT, Toombs C, Cupp AS. Vascular endothelial growth factor and kinase domain region receptor are involved in both seminiferous cord formation and vascular development during testis morphogenesis in the rat. Biol Reprod 2006; 75:56-67.
20. Itoh N, Patel U, Cupp A, Skinner M. Developmental and hormonal regulation of transforming growth factor-beta1 (TGFbeta1), -2, and -3 gene expression in isolated prostatic epithelial and stromal cells: epidermal growth factor and TGFbeta interactions. Endocrinology 1998; 139:1378-1388.
21. Dulak J, Jozkowicz A, Dembinska-Kiec A, Guevara I, Zdzienicka A, Zmudzinska-Grochot D, Florek I, Wojtowicz A, Szuba A, Cooke JP. Nitric oxide induces the synthesis of vascular endothelial growth factor by rat vascular smooth muscle cells. Arterioscler Thromb Vase Biol 2000; 20:659-666.
22. Ergun S, Luttmer W, Fiedler W, Holstein AF. Functional expression and localization of vascular endothelial growth factor and its receptors in the human epididymis. Biol Reprod 1998; 58:160-168.
23. Wesolowski SR, Allan MF, Nielsen MK, Pomp D. Evaluation of hypothalamic gene expression in mice divergently selected for heat loss. Physiol Genomics 2003; 13:129-137.
24. Wood JR, Nelson VL, Ho C, Jansen E, Wang CY, Urbanek M, McAllister JM, Mosselman S, Strauss JF. The molecular phenotype of polycystic ovary syndrome (PCOS) theca cells and new candidate PCOS genes defined by microarray analysis. J Biol Chem 2003; 278:26380-26390.
25. Cupp AS, Dufour JM, Kim G, Skinner MK, Kim KH. Action of retinoids on embryonic and early postnatal testis development. Endocrinology 1999; 140:2343-2352.
26. Hennequin L, Thomas A, Johnstone C, Stokes E, Pie P, Lohmann JJ, Ogilvie D, Dukes M, Wedge S, Curwen J, Kendrew J, Lambert-van der Brempt C. Design and structure: activity relationship of a new class of potent VEGF receptor tyrosine kinase inhibitors. J Med Chem 1999; 42:5369-5389.
27. Binetruy-Tournaire R, Demangel C, Malavaud B, Vassy R, Rouyre S, Kraemer M, Plouet J, Derbin C, Perret G, Claude Mazie J. Identification of a peptide blocking vascular endothelial growth factor (VEGF)-mediated angiogenesis. EMBO J 2000; 19:1525-1533.
28. Parrott JA, Skinner MK. Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 1999; 140:4262-4271.
29. Cupp AS, Kim G, Skinner MK. Expression and action of transforming growth factor beta (TGFbeta1, TGFbeta2, and TGFbeta3) during embryonic rat testis development. Biol Reprod 1999; 60:1304-1313.
30. Pepling ME, Spradling AC. Female mouse germ cells form synchronously dividing cysts. Development 1998; 125:3323-3328.
31. Aumailley M, Krieg T. Laminins: a family of diverse multifunctional molecules of basement membranes. J Invest Dermatol 1996; 106:209-214.
32. Vecchi A, Garlanda C, Lampugnani MG, Resnati M, Matteucci C, Stoppacciaro A, Schnurch H, Risau W, Ruco L, Mantovani A, Dejana E. Monoclonal antibodies specific for endothelial cells of mouse blood vessels: their application in the identification of adult and embryonic endothelium. Eur J Cell Biol 1994; 63:247-254.
33. Zimmermann R, Hartman T, Bohlen P, Sauer M, Kitajewski J. Preovulatory treatment of mice with anti-VEGF receptor 2 antibody inhibits angiogenesis in corpora lutea. Microvasc Res 2001; 62:15-25.
34. Zimmermann RC, Xiao E, Bohlen P, Ferin M. Administration of antivascular endothelial growth factor receptor 2 antibody in the early follicular phase delays follicular selection and development in the rhesus monkey. Endocrinology 2002; 143:2496-2502.
35. Fraser HM, Wulff C. Angiogenesis in the primate ovary. Reprod Fertil Dev 2001; 13:557-566.
36. Bristol-Gould SK, Kreeger PK, Selkirk CG, Kilen SM, Cook RW, Kipp JL, Shea LD, Mayo KE, Woodruff TK. Postnatal regulation of germ cells by activin: the establishment of the initial follicle pool. Dev Biol 2006; 298:132-148.
37. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003; 9:669-676.
38. Iguchi T, Takasugi N. Polyovular follicles in the ovary of immature mice exposed prenatally to diethylstilbestrol. Anat Embryol (Berl) 1986; 175:7 53-55.
39. Iguchi T, Takasugi N, Bern HA, Mills KT. Frequent occurrence of polyovular follicles in ovaries of mice exposed neonatally to diethylstilbestrol. Teratology 1986; 34:29-35.
40. Jefferson W, Newbold R, Padilla-Banks E, Pepling M. Neonatal genistein treatment alters ovarian differentiation in the mouse: inhibition of oocyte nest breakdown and increased oocyte survival. Biol Reprod 2006; 74:161-168.
41. Jefferson WN, Couse JF, Padilla-Banks E, Korach KS, Newbold RR. Neonatal exposure to genistein induces estrogen receptor (ER)alpha expression and multioocyte follicles in the maturing mouse ovary: evidence for ERbeta-mediated and nonestrogenic actions. Biol Reprod 2002; 67:1285-1296.
42. Jefferson WN, Padilla-Banks E, Newbold RR. Disruption of the female reproductive system by the phytoestrogen genistein. Reprod Toxicol 2007; 23:308-316.
43. Kezele P, Skinner MK. Regulation of ovarian primordial follicle assembly and development by estrogen and progesterone: endocrine model of follicle assembly. Endocrinology 2003; 144:3329-3337.
44. Mueller MD, Vigne JL, Minchenko A, Lebovic DI, Leitman DC, Taylor RN. Regulation of vascular endothelial growth factor (VEGF) gene transcription by estrogen receptors alpha and beta. Proc Natl Acad Sci U S A 2000; 97:10972-10977.
45. Mueller MD, Vigne JL, Pritts EA, Chao V, Dreher E, Taylor RN. Progestins activate vascular endothelial growth factor gene transcription in endometrial adenocarcinoma cells. Fertil Steril 2003; 79:386-392.
46. Wu J, Richer J, Horwitz KB, Hyder SM. Progestin-dependent induction of vascular endothelial growth factor in human breast cancer cells: preferential regulation by progesterone receptor B. Cancer Res 2004; 64:2238-2244.
47. Hyder SM, Stancel GM. Inhibition of progesterone-induced VEGF production in human breast cancer cells by the pure antiestrogen ICI 182,780. Cancer Lett 2002; 181:47-53.
48. Hyder SM, Chiappetta C, Stancel GM. Pharmacological and endogenous progestins induce vascular endothelial growth factor expression in human breast cancer cells. Int J Cancer 2001; 92:469-473.
49. Hyder SM, Chiappetta C, Stancel GM. Induction of the angiogenic factor VEGF in the uterus by the antiprogestin onapristone. Cancer Lett 2000; 156:101-107.
50. Koos RD, Kazi AA, Roberson MS, Jones JM. New insight into the transcriptional regulation of vascular endothelial growth factor expression in the endometrium by estrogen and relaxin. Ann N Y Acad Sci 2005; 1041:233-247.
51. Shi Q, Le X, Abbruzzese JL, Peng Z, Qian CN, Tang H, Xiong Q, Wang B, Li XC, Xie K. Constitutive Sp1 activity is essential for differential constitutive expression of vascular endothelial growth factor in human pancreatic adenocarcinoma. Cancer Res 2001; 61:4143-4154.
52. Schafer G, Cramer T, Suske G, Kemmner W, Wiedenmann B, Hocker M. Oxidative stress regulates vascular endothelial growth factor-A gene transcription through Sp1- and Sp3-dependent activation of two proximal GC-rich promoter elements. J Biol Chem 2003; 278:8190-8198.
53. Nishijima K, Ng YS, Zhong L, Bradley J, Schubert W, Jo N, Akita J, Samuelsson SJ, Robinson GS, Adamis AP, Shima DT. Vascular endothelial growth factor-A is a survival factor for retinal neurons and a critical neuroprotectant during the adaptive response to ischemic injury. Am J Pathol 2007; 171:53-67.
54. Jin KL, Mao XO, Greenberg DA. Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc Natl Acad Sci U S A 2000; 97:10242-10247.
55. Abramovich D, Parborell F, Tesone M. Effect of a vascular endothelial growth factor (VEGF) inhibitory treatment on the folliculogenesis and ovarian apoptosis in gonadotropin-treated prepubertal rats. Biol Reprod 2006; 75:434-441.
56. Garrett WM, Guthrie HD. Expression of bcl-2 and 3-beta hydroxysteroid dehydrogenase protein during oocyte and follicle development in fetal and post-natal pig ovaries. Reprod Fertil Dev 1999; 11:463-470.
57. Celik-Ozenci C, Akkoyunlu G, Ali Kayisli U, Arici A, Demir R. Localization of vascular endothelial growth factor in the zona pellucida of developing ovarian follicles in the rat: a possible role in destiny of follicles. Histochem Cell Biol 2003; 120:383-390.
58. Otani N, Minami S, Yamoto M, Shikone T, Otani H, Nishiyama R, Otani T, Nakano R. The vascular endothelial growth factor/fms-like tyrosine kinase system in human ovary during the menstrual cycle and early pregnancy. J Clin Endocrinol Metab 1999; 84:3845-3851.
59. Harata T, Ando H, Iwase A, Nagasaka T, Mizutani S, Kikkawa F. Localization of angiotensin II, the AT1 receptor, angiotensin-converting enzyme, aminopeptidase A, adipocyte-derived leucine aminopeptidase, and vascular endothelial growth factor in the human ovary throughout the menstrual cycle. Fertil Steril 2006; 86:433-439.
60. Berisha B, Schams D, Kosmann M, Amselgruber W, Einspanier R. Expression and localisation of vascular endothelial growth factor and basic fibroblast growth factor during the final growth of bovine ovarian follicles. J Endocrinol 2000; 167:371-382.
61. Garrido N, Albert C, Krussel JS, O'Connor JE, Remohi J, Simon C, Pellicer A. Expression, production, and secretion of vascular endothelial growth factor and interleukin-6 by granulosa cells is comparable in women with and without endometriosis. Fertil Steril 2001; 76:568-575.
62. Greenaway J, Connor K, Pedersen HG, Coomber BL, LaMarre J, Petrik J. Vascular endothelial growth factor and its receptor, Flk-1/KDR, are cytoprotective in the extravascular compartment of the ovarian follicle. Endocrinology 2004; 145:2896-2905.
63. Greenaway J, Gentry PA, Feige JJ, LaMarre J, Petrik JJ. Thrombospondin and vascular endothelial growth factor are cyclically expressed in an inverse pattern during bovine ovarian follicle development Biol Reprod 2005; 72:1071-1078.
64. Nilsson E, Parrott JA, Skinner MK. Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Mol Cell Endocrinol 2001; 175:123-130.
65. Nilsson EE, Kezele P, Skinner MK. Leukemia inhibitory factor (LIF) promotes the primordial to primary follicle transition in rat ovaries. Mol Cell Endocrinol 2002; 188:65-73.
66. Kezele PR, Nilsson EE, Skinner MK. Insulin but not insulin-like growth factor-1 promotes the primordial to primary follicle transition. Mol Cell Endocrinol 2002; 192:37-43.
67. Nilsson EE, Skinner MK. Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol Reprod 2003; 69:1265-1272.
68. Kezele P, Nilsson EE, Skinner MK. Keratinocyte growth factor acts as a mesenchymal factor that promotes ovarian primordial to primary follicle transition. Biol Reprod 2005; 73:967-973.
69. Durlinger AL, Gruijters MJ, Kramer P, Karels B, Ingraham HA, Nachtigal MW, Uilenbroek JT, Grootegoed JA, Themmen AP. Anti-mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 2002; 143:1076-1084.
70. Dissen GA, Romero C, Hirshfield AN, Ojeda SR. Nerve growth factor is required for early follicular development in the mammalian ovary. Endocrinology 2001; 142:2078-2086.
71. Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, Du C, Tang W, Hämäläinen T, Peng S, Lan Z, Cooney A, et al. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 2008; 319:611-613.
72. Abid M, Guo S, Minami T, Spokes K, Ueki K, Skurk C, Walsh K, Aird W. Vascular endothelial growth factor activates PI3K/Akt/forkhead signaling in endothelial cells. Arterioscler Thromb Vase Biol 2004; 24:294-300.
73. Fujio Y, Walsh K. Akt mediates cytoprotection of endothelial cells by vascular endothelial growth factor in an anchorage-dependent manner. J Biol Chem 1999; 274:16349-16354.
74. Guo D, Jia Q, Song H, Warren R, Donner D. Vascular endothelial cell growth factor promotes tyrosine phosphorylation of mediators of signal transduction that contain SH2 domains: association with endothelial cell proliferation. J Biol Chem 1995; 270:6729-6733.
75. Yang MY, Fortune JE. Vascular endothelial growth factor stimulates the primary to secondary follicle transition in bovine follicles in vitro. Mol Reprod Dev 2007; 74:1095-1104.