Donald School Journal of Ultrasound in Obstetrics and Gynecology

Register      Login

SEARCH WITHIN CONTENT

FIND ARTICLE

Volume / Issue

Online First

Archive
Volume  18 (2024)
Volume  17 (2023)
Volume  16 (2022)
Volume  15 (2021)
Volume  14 (2020)
Volume  13 (2019)
Volume  12 (2018)
Volume  11 (2017)
Volume  10 (2016)
Volume  9 (2015)
Volume  8 (2014)
Volume  7 (2013)
Volume  6 (2012)
Volume  5 (2011)
Volume  4 (2010)
Volume  3 (2009)
Volume  2 (2008)
Volume  1 (2007)
Related articles

VOLUME 14 , ISSUE 2 ( April-June, 2020 ) > List of Articles

REVIEW ARTICLE

Cyclical Changes in Ovarian Angiogenesis and Its Controls

Sonal Panchal, Chaitanya Nagori

Keywords : Cyclical vascular changes in ovary, Ovarian angiogenesis, Ovarian vascularity

Citation Information : Panchal S, Nagori C. Cyclical Changes in Ovarian Angiogenesis and Its Controls. Donald School J Ultrasound Obstet Gynecol 2020; 14 (2):117-124.

DOI: 10.5005/jp-journals-10009-1635

License: CC BY-NC 4.0

Published Online: 30-07-2020

Copyright Statement:  Copyright © 2020; The Author(s).


Abstract

The ovary is supplied by the ovarian artery and the ovarian branch of the uterine artery. Ovarian endocrinological function and ovulation is dependent on the establishment and continual remodeling of a complex vascular system. In the ovary, the development of new capillaries from preexisting ones (angiogenesis) is a complex event regulated by several hormones and angiogenic factors and also cellular changes. Expression of hormones and angiogenic factors varies throughout the cycle. Understanding of these factors and the control mechanism is essential to understand and correct abnormalities of ovulation and improve the treatment outcome of ovulation induction, in patients with subfertility.

HTML PDF Share
  1. Martelli A, Palmerini MG, Russo V, et al. Blood vessel remodeling in pig ovarian follicles during the periovulatory period: an immunohistochemistry and SEM-corrosion casting study. Reprod Biol Endocrinol 2009;16(1):72–85. DOI: 10.1186/1477-7827-7-72.
  2. Hafez S, Caceci T. Microvascular corrosion casting of the ovary in nonpregnant and pregnant does. FASEB J 2017;31:lb28.
  3. Berisha B, Schams D, Rodler D, et al. Angiogenesis in the ovary - the most important regulatory event for follicle and corpus luteum development and function in cow - an overview. Anat Histol Embryol 2016;45(2):124–130. DOI: 10.1111/ahe.12180.
  4. Camussi G, Deregibus MC, Bruno S, et al. Exosomes/microvesicles as a mechanism of cell-to cell communication. Kidney Int 2010;78(9):838–848. DOI: 10.1038/ki.2010.278.
  5. Olfert IM, Baum O, Hellsten Y, et al. Advances and challenges in skeletal muscle angiogenesis. Am J Physiol Heart Circ Physiol 2016;310(3):326–336. DOI: 10.1152/ajpheart.00635.2015.
  6. Hazzard TM, Stouffer RL. Angiogenesis in ovarian follicular and luteal development. Baillieres Best Pract Res Obstet Gynecol 2000;14(6):883–900.
  7. Gougeon A. Dynamics of human follicular growth: morphologic, dynamic and functional aspects 2nd ed. The Ovary 2004.
  8. Wulff C, Wilson H, Wiegand SJ, et al. Prevention of thecal angiogenesis, antral follicular growth, and ovulation in the primate by treatment with vascular endothelial growth factor trap R1R2. Endocrinology 2002;143(7):2797–2807. DOI: 10.1210/endo.143.7.8886.
  9. Feng Y, Cui P, Lu X, et al. CLARITY reveals dynamics of ovarian follicular architecture and vasculature in three-dimensions. Sci Rep 2017;7(1):44810. DOI: 10.1038/srep44810.
  10. Mattioli M, Barboni B, Turriani M, et al. Follicle activation involves vascular endothelial growth factor production and increased blood vessel extension. Biol Reprod 2001;65(4):1014–1019. DOI: 10.1095/biolreprod65.4.1014.
  11. Carmeliet P, Jair RK. Angiogenesis in cancer and other diseases. Nature 2000;407(6801):249–257. DOI: 10.1038/35025220.
  12. Redmer DA, Reynolds LP. Angiogenesis in the ovary. Rev Reprod 1996;1(3):182–192. DOI: 10.1530/ror.0.0010182.
  13. Zaidi J, Barber J, Kyei-mensah A, et al. Relationship of ovarian stromal blood flow at the baseline ultrasound scan to subsequent follicular response in an in vitro fertilization program. Obstet Gynecol 1996;88(5):779–784. DOI: 10.1016/0029-7844(96)00316-X.
  14. Engmann L, Sladkevicius P, Agrawal R, et al. Value of ovarian stromal blood flow velocity measurement after pituitary suppression in the prediction of ovarian responsiveness and outcome of in vitro fertilization treatment. Fertil Steril 1999;71(1):22–29. DOI: 10.1016/s0015-0282(98)00406-3.
  15. Berardinelli P, Martelli A, Russo V, et al. Correlation between VEGF production and blood vessels density in steroidogenic activated pig antral follicles. Italian J Anat Embryol. 2002;107:115–126.
  16. Young JM, McNeilly AS. Theca: the forgotten cell of the ovarian follicle. Reproduction 2010;140(4):489–504. DOI: 10.1530/REP-10-0094.
  17. McFee RM, Rozell TG, Cupp AS. The balance of proangiogenic and antiangiogenic VEGFA isoforms regulate follicle development. Cell Tissue Res 2012;349(3):635–647. DOI: 10.1007/s00441-012-1330-y.
  18. Acosta TJ, Hayashi KG, Ohtani M, et al. Local changes in blood flow within the preovulatory follicle wall and early corpus luteum in cows. Reproduction 2003;125(5):759–767. DOI: 10.1530/rep.0. 1250759.
  19. Martelli A, Russo V, Mauro A, et al. Insights into ovarian follicle angiogenesis: morphological and chronological vascular remodeling from primordial to ovulating follicles SM. Vasc Med 2017;2(1): 1009.
  20. Kupesic S, Kurjak A. Uterine and ovarian perfusion during the periovulatory period assessed by transvaginal colour doppler. Fertil Steril 1993;3:439–443. DOI: 10.1016/s0015-0282(16)56157-3.
  21. Grazul-Bilska AT, Navanukraw C, Johnson ML, et al. Vascularity and expression of angiogenic factors in bovine dominant follicles of the first follicular wave. J Anim Sci 2007;85(8):1914–1922. DOI: 10.2527/jas.2007-0044.
  22. Fraser HM, Lunn SF. Regulation and manipulation of angiogenesis in the primate corpus luteum CL. Reproduction 2001;121(3):355–362. DOI: 10.1530/rep.0.1210355.
  23. Martelli A, Berardinelli P, Russo V, et al. Spatiotemporal analysis of vascular endothelial growth factor expression and blood vessel remodelling in pig ovarian follicles during the periovulatory period. J Mol Endocrinol 2006;36(1):107–119. DOI: 10.1677/jme. 1.01921.
  24. Tesone M, Stouffer RL, Borman SM, et al. Vascular endothelial growth factor (VEGF) production by the monkey corpus luteum during the menstrual cycle: isoform-selective mRNA expression in vivo and hypoxia-regulated protein secretion in vitro. Biol Reprod 2005;73(5):927–934. DOI: 10.1095/biolreprod.105.039875.
  25. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev 2004;25(4):581–611. DOI: 10.1210/er.2003-2027.
  26. Zeleznik AJ, Schuler HM, Reichert LJ. Gonadotropin-binding sites in the rhesus monkey ovary: role of the vasculature in the selective distribution of human chorionic gonadotropin to the preovulatory follicle. Endocinology 1981;109(2):356–362. DOI: 10.1210/endo-109-2-356.
  27. Furukawa K, Fujiwara H, Sato Y, et al. Platelets are novel regulators of neovascularization and luteinization during human corpus luteum formation. Endocrinology 2007;148(7):3056–3064. DOI: 10.1210/en.2006-1687.
  28. Duggavathi R, Bartlewski P, Barrett D, et al. Use of high-resolution transrectal ultrasonography to assess changes in numbers of small ovarian antral follicles and their relationships to the emergence of follicular waves in cyclic ewes. Theriogenology 2003;60(3):495–510. DOI: 10.1016/s0093-691x(03)00041-4.
  29. Robinson RS, Woad KJ, Hammond AJ, et al., 2009, unpublished observations.
  30. Mauro A, Martelli A, Berardinelli P, et al. Effect of antiprogesterone RU486 on VEGF expression and blood vessel remodelling on ovarian follicles before ovulation. PLoS ONE 2014;9(4):1–13. DOI: 10.1371/journal.pone.0095910.
  31. Abe K, Minegishi T, Ibuki Y, et al. Expression of adrenomedullin in the human corpus luteum. Fertil Steril 2000;74(1):141–145. DOI: 10.1016/s0015-0282(00)00585-9.
  32. Kaczmarek MM, Schams D, Ziecik AJ. Role of vascular endothelial growth factor in ovarian physiology—an overview. Reprod Biol 2005;5(2):111–136.
  33. Levin ER, Rosen GF, Cassidenti DL, et al. Role of vascular endothelial cell growth factor in ovarian hyperstimulation syndrome. J Clin Invest 1998;102(11):1978–1985. DOI: 10.1172/JCI4814.
  34. Le Couter J, Lin R, Ferrara N. Endocrine gland-derived VEGF and the emerging hypothesis of organ-specific regulation of angiogenesis. Nat Med 2002;8(9):913–917. DOI: 10.1038/nm0902-913.
  35. LeCouter J, Kowalski J, Foster J, et al. Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature 2001;412(6850):877–884. DOI: 10.1038/35091000.
  36. Li M, Bullock CM, Knauer DJ, et al. Identification of two prokineticin cDNAs: recombinant proteins potently contract gastrointestinal smooth muscle. Mol Pharmacol 2001;59(4):692–698. DOI: 10.1124/mol.59.4.692.
  37. Lin DC, Bullock CM, Ehlert FJ, et al. Identification and molecular characterisation of two closely related G protein-coupled receptors activated by prokineticins/endocrine gland vascular endothelial growth factor. J Biol Chem 2001;277(22):19276–19280. DOI: 10.1074/jbc.M202139200.
  38. Lin R, Le Couter J, Kowalski J, et al. Characterization of EGVEGF signaling in adrenal cortex capillary endothelial cells. J Biol Chem 2002;277(10):8724–8729. DOI: 10.1074/jbc.M110594200.
  39. Ferrara N, Frantz G, LeCouter J, et al. Differential expression of the angiogenic factor genes VEGF and EG-VEGF in normal and polycystic human ovaries. Am J Pathol 2003;162(6):1881–1893. DOI: 10.1016/S0002-9440(10)64322-2.
  40. Corner GWJ. The histological dating of the human corpus luteum of menstruation. Am J Anat 1956;9(3):377–401. DOI: 10.1002/aja.1000980304.
  41. Maisonpierre PC, Suri C, Jones PF, et al. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 1997;277(5322):55–60. DOI: 10.1126/science.277.5322.55.
  42. Duncan WC, van den Driesche S, Fraser HM. Inhibition of vascular endothelial growth factor in the primate ovary up-regulates hypoxia-inducible factor-1 alpha in the follicle and corpus luteum. Endocrinology 2008;14(9):3313–3320. DOI: 10.1210/en.2007-1649.
  43. Abramovich D, Parborel 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(3):434–441. DOI: 10.1095/biolreprod.106. 051052.
  44. Nilsson EE, Detzel C, Skinner MK. Platelet-derived growth factor modulates the primordial to primary follicle transition. Reproduction 2006;13(1):1007–1015. DOI: 10.1530/rep.1.00978.
  45. van WezelI L, Umapathysivam K, Tilley WD, et al. Immunohistochemical localization of basic fibroblast growth factor in bovine ovarian follicles. Mol Cell Endocrinol 1995;11(5):133–140. DOI: 10.1016/0303-7207(95)03678-4.
  46. Augustin HG. Development of the vascular system of the corpus luteum. In: Risau W. Morphogenesis of Endothelium. U.K: Harwood Academic Publishers; 2000. pp. 237–254.
  47. Torres-Ortiz MC, Gutiérrez-Ospina G, Gómez-Chavarín M, et al. The presence of VEGF and Notch2 during preantral-antral follicular transition in infantile rats: anatomical evidence and its implications. Gen Comp Endocrinol 2017;249:82–92. DOI: 10.1016/j.ygcen.2017.05.006.
  48. Grazul-Bilska A, Navanukraw C, Johnson M, et al. Expression of endothelial nitric oxide synthase in the ovine ovary throughout the estrous cycle. Reproduction 2006;13(2):579–587. DOI: 10.1530/REP-06-0009.
  49. Beckman JD, Grazul-Bilska AT, Johnson ML, et al. Isolation and characterization of ovine luteal pericytes and effects of nitric oxide on pericyte expression of angiogenic factors. Endocrine 2006;29(3): 467–476. DOI: 10.1385/endo:29:3:467.
  50. Mitsube K, Zackrisson U, Brannstrom M. Nitric oxide regulates ovarian blood flow in the rat during the periovulatory period. Hum Reprod 2002;17(10):2509–2516. DOI: 10.1093/humrep/17.10.2509.
  51. Kim KH, Moriarty K, Bender JR. Vascular cell signaling by membrane estrogen receptors. Steroids 2008;73(9-10):864–869. DOI: 10.1016/j.steroids.2008.01.008.
  52. Harlow CR, Hillier SG. Connective tissue growth factor in the ovarian paracrine system. Mol Cell Endocrinol 2002;187(1-2):23–27. DOI: 10.1016/s0303-7207(01)00702-x.
  53. Cavander JL, Murdoch WJ. Morphological studies of the microcirculatory system of periovulatory ovine follicles. Biol Reprod 1990;42(1):139–149. DOI: 10.1095/biolreprod42.1.139.
  54. Campbell S, Bourne T, Waterstone J, et al. Transvaginal color blood flow imaging of the preovulatory follicle. Fertil Steril 1993;60(3): 433–438. DOI: 10.1016/S0015-0282(16)56156-1.
  55. Reynolds LP, Redmer DA. Growth and development of the corpus luteum. J Reprod Fertil Suppl 1999;54:181–191.
  56. Kurjak A, Kupesic-Urek S. Infertility. In: Kurjak A. Transvaginal color Doppler. Carnforth, UK: Parthenon Publishing; 1991. pp. 33–38.
  57. Tamanini C, De Ambrogi M. Angiogenesis in developing follicle and corpus luteum. Reprod Domest Anim 2004;39(4):206–216. DOI: 10.1111/j.1439-0531.2004.00505.x.
  58. Kamat BR, Brown LF, Manseau EJ, et al. Expression of vascular permeability factor/vascular endothelial growth factor by human granulosa and theca lutein cells. Am J Pathol 1995;146(1):157–165.
  59. Rodger FE, Young FM, Fraser HM, et al. Endothelial cell proliferation follows the mid-cycle luteinizing hormone surge, but not human chorionic gonadotrophin rescue, in the human corpus luteum. Hum Reprod 1997;12(8):1723–1729. DOI: 10.1093/humrep/12.8.1723.
  60. Gaytán F, Morales C, García-Pardo L, et al. Macrophages, cell proliferation, and cell death in the human menstrual corpus luteum. Biol Reprod 1998;59(2):417–425. DOI: 10.1095/biolreprod59. 2.417.
  61. Shweiki D, Itin A, Neufeld G, et al. Patterns of vascular endothelial growth factor (VEGF) and VEGF receptors in mice suggest a role in hormonally regulated angiogenesis. J Clin Invest 1993;91(5): 2235–2243. DOI: 10.1172/JCI116450.
  62. Gaytán F, Morales C, García-Pardo L, et al. A quantitative study of changes in the human corpus luteum microvasulature during the menstrual cycle. Biol Reprod 1999;60(4):914–919. DOI: 10.1095/biolreprod60.4.914.
  63. Wulff C, Dickson SE, Duncan WC, et al. Angiogenesis in the human corpus luteum: simulated early pregnancy by HCG treatment is associated with both angiogenesis and vessel stabilization. Hum Reprod 2001;16(12):2515–2524. DOI: 10.1093/humrep/16.12.2515.
  64. Sugino N, Kashida S, Takiguchi S, et al. 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(10):3919–3924. DOI: 10.1210/jcem.85.10.6888.
  65. van den Driesche S, Myers M, Gay E, et al. HCG up-regulates hypoxia inducible factor-1 alpha in luteinized granulosa cells: Implications for the hormonal regulation of vascular endothelial growth factor A in the human corpus luteum. Mol Hum Reprod 2008;14(8):455–464. DOI: 10.1093/molehr/gan040.
  66. Ferrara N, Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev 1997;18(1):4–25. DOI: 10.1210/edrv.18.1.0287.
  67. Neulen J, Raczek S, Pogorzelski M, et al. Secretion of vascular endothelial growth factor/vascular permeability factor from human luteinized granulosa cells is human chorionic gonadotrophin dependent. Molec Hum Reprod 1998;4(3):203–206. DOI: 10.1093/molehr/4.3.203.
  68. Wulff C, Wilson H, Largue P, et al. 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(11):4302–4309. DOI: 10.1210/jcem.85.11.6942.
  69. Woad JK, Robinson RS. Luteal angiogenesis and its control. Theriogenology 2016;86(1):221–228. DOI: 10.1016/j.theriogenology. 2016.04.035.
  70. Otani N, Sawako M, Yamoto M, et al. 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(10):3845–3851. DOI: 10.1210/jcem.84.10.6025.
  71. Dickson SE, Fraser HM. Inhibition of early luteal angiogenesis by gonadotropin-releasing hormone antagonist treatment in the primate. J Clin Endocrinol Metab 2000;85(6):2339–2344. DOI: 10.1210/jcem.85.6.6621.
  72. Laitinen M, Ristimäki A, Honkasalo M, et al. Differential hormonal regulation of vascular endothelial growth factors VEGF, VEGF-B, and VEGF-C messenger ribonucleic acid levels in cultured human granulosa-luteal cells. Endocrinology 1997;138(11):4748–4756. DOI: 10.1210/endo.138.11.5500.
  73. Berisha B, Schams D, Kosmann M, et al. Expression and tissue concentration of vascular endothelial growth factor, its receptors, and localization in the bovine corpus luteum during estrous cycle and pregnancy. Biol Reprod 2000;63(4):1106–1114. DOI: 10.1095/biolreprod63.4.1106.
  74. Kaczmarek MM, Kowalczyk AE, Waclawik A, et al. Expression of vascular endothelial growth factor and its receptors in the porcine corpus luteum during the estrous cycle and early pregnancy. Mol Reprod Dev 2007;74(6):730–739. DOI: 10.1002/mrd.20638.
  75. Robinson RS, Nicklin LT, Hammond AJ, et al. Fibroblast growth factor 2 is more dynamic than vascular endothelial growth factor A during the follicle–luteal transition in the cow. Biol Reprod 2007;7(1):728–736. DOI: 10.1095/biolreprod.106.055434.
  76. Wandji SA, Gadsby JE, Barber JA, et al. Messenger ribonucleic acids for MAC25 and connective tissue growth factor (CTGF) are inversely regulated during folliculogenesis and early luteogenesis. Endocinology 2000;141(7):2648–2657. DOI: 10.1210/endo.141.7.7576.
  77. Perbal B. CCN proteins: multifunctional signalling regulators. Lancet 2004;363(9402):62–64. DOI: 10.1016/S0140-6736(03)15172-0.
  78. Fraser HM, Lunn SF, Kim H, et al. Insulin-like growth factor binding protein-3 (IGFBP-3) mRNA in the endothelial cells of the primate corpus luteum. Hum Reprod 1998;13(8):2180–2185. DOI: 10.1093/humrep/13.8.2180.
  79. Schams D, Kosmann M, Berisha B, et al. Stimulatory and synergistic effects of luteinising hormone and insulin-like growth factor 1 on the secretion of vascular endothelial growth factor and progesterone of cultured bovine granulosa cells. Exp Clin Endocrinol Diabetes 2001;109(3):155–162. DOI: 10.1055/s-2001-14839.
  80. Kupesic S, Kurjak A. The assessment of normal and abnormal luteal function by transvaginal colour doppler sonography. Eur J Obstet Gynecol 1997;72(1):83–87. DOI: 10.1016/s0301-2115(96)02666-8.
  81. Salim A, Kurjak A, Zalud I. Ovarian luteal flow in normal and abnormal early pregnancies. J Matern Fetal Invest 1992;2:119.
  82. Fraser HM, Wulff C. Angiogenesis in corpus luteum. Reprod Biol Endocrinol 2003;1(1):88. DOI: 10.1186/1477-7827-1-88.
  83. Woodruff TK, Shea LD. A new hypothesis regarding ovarian follicle development: Ovarian rigidity as a regulator of selection and health. J Assist Reprod Genet 2011;28(1):3–6. DOI: 10.1007/s10815-010- 9478-4.
  84. Endo T, Kitajima Y, Nishikawa A, et al. Cyclic changes in expression of mRNA of vascular endothelial growth factor, its receptors Flt-1 and KDR/Flk-1, and Ets-1 in human corpora lutea. Fertil Steril 2001;76(4):762–768. DOI: 10.1016/s0015-0282(01)02012-x.
  85. Thompson JG, Brown HM, Kind KL, et al. The ovarian antral follicle: living on the edge of hypoxia or not? Biol Reprod 2015;92(6):153. DOI: 10.1095/biolreprod.115.128660.
  86. Seli E, Zeyneloglu HB, Senturk LM, et al. Basic fibroblast growth factor: peritoneal and follicular fluid levels and its effect on early embryonic development. Fertil Steril 1998;69(6):1145–1148. DOI: 10.1016/s0015-0282(98)00074-0.
  87. Phan B, Rakenius A, Pietrowski D, et al. hCG-dependent regulation of angiogenic factors in human granulosa lutein cells. Mol Reprod Dev 2006;73(7):878–884. DOI: 10.1002/mrd.20465.
  88. Morales C, Garcia-Pardo L, Reymundo C, et al. Different patterns of structural luteolysis in the human corpus luteum of menstruation. Hum Reprod 2000;15(10):2119–2128. DOI: 10.1093/humrep/15.10.2119.
PDF Share
PDF Share

© Jaypee Brothers Medical Publishers (P) LTD.