Endometrial Angiogenesis, Vascular Maturation, and Lymphangiogenesis

Peter A W Rogers, Jacqueline F Donoghue, Lisa M Walter, Jane E Girling
Reproductive sciences (Thousand Oaks, Calif.) · 2008 · vol. 16(2) , pp. 147–151 · doi:10.1177/1933719108325509 · PMID:19001552 · W2053951615
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⚙ AI-generated summary by claude@2026-06+body, 2026-06-07 ⓘ

Estrogen can be pro- or antiangiogenic in mouse endometrium, while progesterone is proangiogenic and promotes arteriogenesis, and lymphatics are more prevalent in the basalis layer.

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⚙ AI-generated deep summary by claude@2026-06, 2026-06-07 · read from full text ⓘ

This paper reviews and synthesizes experimental mouse-model evidence on how estrogen and progesterone regulate endometrial angiogenesis, arteriogenesis/vascular maturation, and lymphangiogenesis, alongside human histological data on lymphatic vessel distribution in the endometrium. It reports that estrogen can act as either pro- or anti-angiogenic in mouse endometrium, that progesterone alone is pro-angiogenic (with estrogen pretreatment moderating this), and that progesterone increases arteriogenesis without being inhibited by estrogen; it also notes that basalis regions contain lymphatics closely associated with spiral arterioles, suggesting possible paracrine communication. The authors explicitly frame these findings as relevant to multiple gynecological conditions, while the overall caveat is that conclusions rely on animal models and summarized histology rather than a single unified clinical dataset. Relevance to endometriosis: the paper explicitly lists endometriosis among gynecological disorders in which endometrial angiogenesis/lymphangiogenesis are of clinical interest, though its main focus is broader endometrial vascular biology rather than endometriosis mechanisms specifically.

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Abstract

Angiogenesis, arteriogenesis or vessel maturation, and lymphangiogenesis comprise a continuum of vascular development, with overlap and interaction between the mechanisms by which they are controlled. These processes are of clinical interest because they play roles in endometrial repair, placental development, and in gynecological disorders including endometrial cancer, endometriosis and abnormal uterine bleeding. Using mouse models we have shown that estrogen can be either proangiogenic or antiangiogenic in endometrium. Progesterone alone is proangiogenic, although this can be moderated by pretreatment with estrogen. Arteriogenesis also increases in response to progesterone, and this effect is not inhibited by estrogen. Lymphatics account for 13% of all vessels in the human functionalis compared to 57% in the basalis. Many of the basalis lymphatic vessels are closely associated with spiral arterioles and this intimate connection may provide a mechanism for paracrine communication between the functionalis and the arteries supplying the endometrium. Similar content being viewed by others

References

Girling JE, Rogers PAW. Recent advances in endometrial angiogenesis. Angiogenesis. 2005;8:89–99. Gargett CE, Rogers PAW. Human endometrial angiogenesis. Rev Reprod. 2001;121:181–186. Walter LM, Rogers PAW, Girling JE. The role of progesterone in endometrial angiogenesis in pregnant and ovariectomised mice. Reproduction. 2005;129:765–777. Heryanto B, Rogers PAW. Regulation of endometrial endothelial cell proliferation by oestrogen and progesterone in the ovariectomised mouse. Reproduction. 2002;123:107–113. Heryanto B, Lipson KE, Rogers PAW. Effect of angiogenesis inhibitors on oestrogen-mediated endometrial endothelial cell proliferation in the ovariectomised mouse. Reproduction. 2003;125:337–346. Heryanto B, Girling JE, Rogers PAW. Intravascular neutrophils partially mediate the endometrial endothelial cell proliferative response to oestrogen in ovariectomised mice. Reproduction. 2004;127:613–620. Rogers PA, Abberton KM. Endometrial arteriogenesis: vascular smooth muscle cell proliferation and differentiation during the menstrual cycle and changes associated with endometrial bleeding disorders. Microsc Res Tech. 2003;60:412–419. Jain RK. Molecular regulation of vessel maturation. Nat Med. 2003;9:685–693. Abberton KM, Taylor NH, Healy DL, Rogers PA. Vascular smooth muscle alpha-α distribution around endometrial arterioles during the menstrual cycle: increased expression during the perimenopause and lack of correlation with menorrhagia. Hum Reprod. 1996;11:204–211. Abberton KM, Healy DL, Rogers PA. Smooth muscle alpha actin and myosin heavy chain expression in the vascular smooth muscle cells surrounding human endometrial arterioles. Hum Reprod. 1999;14:3095–3100. Abberton KM, Taylor NH, Healy DL, Rogers PA. Vascular smooth muscle cell proliferation in arterioles of the human endometrium. Hum Reprod. 1999;14:1072–1079. Kohnen G, Campbell S, Jeffers MD, Cameron IT. Spatially regulated differentiation of endometrial vascular smooth muscle cells. Hum Reprod. 2000;15:284–292. Girling JE, Lederman FL, Walter LM, Rogers PAW. Progesterone, but not estrogen, stimulates vessel maturation in the mouse endometrium. Endocrinology. Han SJ, Tsai SY, Tsai MJ, O’Malley BW. Distinct temporal and spatial activities of RU486 on progesterone receptor function in reproductive organs of ovariectomized mice. Endocrinology. 2007;148:2471–2486. Ueki M. Histologic study of endometriosis and examination of lymphatic drainage in and from the uterus. J Obstet Gynecol. 1991;165:201–209. Uchino S, Ichikawa S, Okubo M, Nakamura Y, Iimura A. Methods of detection of lymphatics and their changes with oestrous cycle. Inter Angio. 1987;6:271–278. Blackwell P, Fraser I. Superficial lymphatics in the functional zone of normal human endometrium. Microvasc Res. 1981;21:142–152. Donoghue JF, Lederman FL, Susil BJ, Rogers PA. Lymphangiogenesis of normal endometrium and endometrial adenocarcinoma. Hum Reprod. 2007;22:1705–1713. Red-Horse K, Rivera J, Schanz A, et al. Cytotrophoblast induction of arterial apoptosis and lymphangiogenesis in an in vivo model of human placentation. J Clin Invest. 2006;116:2643–2652. Koukourakis M, Giatromanolaki A, Sivridis E, et al. LYVE-1 immunohistochemical assessment of lymphangiogenesis in endometrial and lung cancer. J Clin Pathol. 2005;58:202–206. Noyes RW, Hertig AT, Rock J. Dating the endometrial biopsy. Fertil Steril. 1950;1:3–25. Author information Authors and Affiliations Corresponding author Additional information PAWR and JEG were supported by NH&MRC Project Grant No. 384195. JFD was supported by an Australian Postgraduate Award. PAWR’s salary was provided by NH&MRC Fellowship No. 334063. Rights and permissions About this article Cite this article Rogers, P.A.W., Donoghue, J.F., Walter, L.M. et al. Endometrial Angiogenesis, Vascular Maturation, and Lymphangiogenesis. Reprod. Sci. 16, 147–151 (2009). https://doi.org/10.1177/1933719108325509 Published: Issue date: DOI: https://doi.org/10.1177/1933719108325509

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MeSH descriptors

Endometrium Lymphangiogenesis Neovascularization, Physiologic Animals Endometrium Endometrium Estrogens Estrogens Female Humans Progesterone Progesterone

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