Structural organization of the uterus circulatory system

Written by Khramova I.A., Chertok V.M., Kotsyuba A.E., Chertok A.G.

  UDK: 618.14:611.16 | Pages: 13–23 | Full text PDF | Open PDF 


The review analyzes literature data and authors’ materials on organization of uterus microvasculature and its regulatory mechanisms. It justifies the hypothesis that the adaptation of the microcirculatory system of the uterus to the changing conditions of the organ functioning is provided by regulatory mechanisms acting indirectly, by changing the lumen of the inflow and outflow vessels, or directly through the structural elements of the vessel wall, mainly the endothelium. It discusses the role of gasotransmitters in this process: nitric oxide, Обсуждается роль в этом процессе газотрансмиттеров: оксида азота, carbon monooxide, hydrogen sulfide.

Links to authors:

I.A. Khramova, V.M. Chertok, A.E. Kotsyuba, A.G. Chertok
Pacific State Medical University (2 Ostryakova Ave. Vladivostok 690002 Russian Federation)

1. Afanasiev A.A., Chertok V.M. Application of automated system of image analysis AllegroMC for quantitative biomicroscopy of microcirculatory channel // Pacific Medical Journal. 2004. No. 2. P. 82–86.
2. Getsova V.M. Permeability of uterine and placental barriers for serotonin and sodium fluorescein: Thesis of MD dissertation. Moscow, 1972. 19 p.
3. Gusakova S.V., Kovalev I.V., Smagliy L.V. [et al.]. Gas signalling in mammalian cells // Advances in Physiology Sciences. 2015. Vol. 46, No. 4. P. 53–73.
4. Kozlov V.I. Capillaroscopy in clinical practice. Moscow: Prakticheskaya Meditsina, 2015. 232 p.
5. Kokov L.S., Sitkin I.I., Samoylova T.E. Arterial blood supply of the uterus and its appendages in normal, at different age periods and in pathological conditions with reference to endovascular occlusion of the uterine artery // Gynecology. 2004. Vol. 6, No. 5. P. 259–262.
6. Kotsyuba A.E., Chertok V.M., Chertok A.G. Age features of COmediated reaction of pial arteries of different diameter in rats // Bulletin of Experimental Biology and Medicine. 2016. Vol. 162, No. 11. P. 612–617.
7. Kotsyuba A.E., Chertok V.M., Babich E.V., Kotsyuba E.P. Organic features of mast cells cytochemistry in rats // Cell and Tissue Biology. 2008. Vol. 50, No. 12. P. 1023–1029.
8. Kupriyanov V.V., Banin V.V., Alimov G.A. Organization and transport properties of microvessel endothelium // Bulletin of the Academy of Medical Sciences of the USSR. 1988. No. 2. P. 4–9.
9. Motavkin P.A., Lomakin A.V., Chertok V.M. Capillaries of the brain. Vladivostok: FESC of USSR AS, 1983. 140 p.
10. Nedobylskaya Yu.P. Histochemistry of ATPase of the capillary bed of the uterus of rats with combined action of laser radiation and female sex hormones: PhD dissertation. Vladivostok, 1994. 183 p.
11. Nemkov Yu.K. Functional morphology of the capillary bed of the rat uterus when exposed to optical radiation sources: PhD dissertation. Vladivostok, 1991. 212 p.
12. Nemkov Yu.K., Chertok A.G., Chertok V.M. Changes in the capillary bed of the endometrium of the uterus of rats during the estrous cycle (histochemical study) // Morphology. 1992. Vol. 102, No. 4. P. 56–59.
13. Orlov V.I., Ovsyannikov V.G. Microcirculation in the serous cover of the uterus in intact rats // Patologicheskaya Fiziologiya I Eksperimentalnaya Terapiya. 1984. No. 2. P. 66–67.
14. Rakitskaya V.V., Proymina F.I., Chudinov Yu.V. Adrenergic innervation of the uterus of the rat in different phases of the estrous cycle // Fisiologichesky Zhurnal SSSR. 1986. Vol. 72, No. 7. P. 987–991.
15. Reutov V.P., Chertok V.M. The new understanding of the autonomic nervous system role and the nitric oxide generating system in the brain vessels // Pacific Medical Journal. 2016. No. 2. P. 10–19.
16. Reutov V.P., Sorokina E.G., Kositsyn N.S. Nitric oxide and cyclicity problems in biology and medicine // Biology Bulletin Reviews. 2005. Vol. 125, No. 1. P. 41–65.
17. Chernuh A.M., Aleksandrov P.N., Alekseev O.V. Microcirculation. Moscow: Meditsina, 1975. 456 p.
18. Chertok A.G. Histochemical characteristics of the vascular capillary bed of the human and animal uterus: PhD dissertation. Vladivostok, 1987. 216 p.
19. Chertok A.G., Nemkov Yu.K., Chertok V.M. Functional morphology of capillary bed of uterus after introduction of synestrol // Bulletin of Experimental Biology and Medicine. 1990. Vol. 108, No. 6. P. 605–607.
20. Chertok V.M. Mast cells of the outer shell of arteries of the base of the brain // Archives of Anatomy, Histology, and Embryology. 1980. Vol. 79, No. 11. P. 72–79.
21. Chertok V.M. Histochemical characteristics of transport ATPase in brain capillaries of the man // Bulletin of Experimental Biology and Medicine. 1984. Vol. 97, No. 3. P. 375–377.
22. Chertok V.M. Age changes in capillaries of the human brain (histochemical study) // Archives of Anatomy, Histology, and Embryology. 1985. Vol. 88, No. 2. P. 28–34.
23. Chertok V.M., Zenkina V.G. Regulation of ovarian function: Part of the gas transmitters NO, CO and H2S // Advances in Physiology Sciences. 2015. Vol. 46, No. 4. P. 74–89.
24. Chertok V.M., Kotsyuba A.E. Structural organization of the bulbar department of the cardiovascular center. Vladivostok: Medicina DV, 2013. 164 p.
25. Chertok V.M., Kotsyuba A.E. Age-associated characteristics of vasomotor regulation of the pia mater arteries in rats // Bulletin of Experimental Biology and Medicine. 2010. Vol. 149, No. 3. P. 340–344.
26. Chertok V.M., Kotsyuba A.E. Features of the distribution of H2S synthesis enzymes in the wall of cerebral arteries in rats // Bulletin of Experimental Biology and Medicine. 2012. Vo. 154, No. 7. P. 116–120.
27. Chertok V.M., Kotsyuba A.E. The neurochemical features of intranuclear neurons of the medulla oblongata in normo- and hypertensive rats // Neurochemical Journal. 2016. Vol. 33, No. 3. P. 244–252.
28. Chertok V.M., Chertok A.G. Regulatory capacity of the brain capillaries // Pacific Medical Journal. 2016. No. 2. P. 72–80.
29. Chertok V.M., Zenkina V.G., Kargalova E.P. Functional ovary morphology. Vladivostok: Medicina DV, 2015. 154 p.
30. Chertok V.M., Kotsyuba A.E., Kotsyuba E.P. Heme oxygenase-2 neurons brain and spinal cord of human // Annals of the Russian academy of medical sciences. 2012, No. 6. P. 36–41.
31. Chertok V.M., Kotsyuba A.E., Chertok A.G. Distribution of hemoxygenases in the wall of the arteries of the soft shell of rat brain // Morphology. 2017. Vol. 151, No. 1. P. 33–38.
32. Chertok V.M., Nevzorova V.A., Zaharchuk N.V. A comparative study of HIF-1A and HIF-2A immunopositive neurons and capillaries in the cerebral cortex of rats with tissue hypoxia // Bulletin of Experimental Biology and Medicine. 2018. Vol. 165, No. 4. P. 513–517.
33. Chertok V.M., Startseva M.S., Kotsyuba A.E. The application of a "pixel method" for the quantitative assessment of the results of the histochemical studies // Morphology. 2012. Vol. 142, No. 5. P. 71–75.
34. Chertok V.M., Chertok A.G., Zenkina V.G. Endotelial-dependent of the regulation of angiogenesis // Cell and Tissue Biology. 2017. Vol. 59, No. 4. P. 243–258.
35. Chertok V.M., Kotsyuba A.E., Startseva M.S., Kotsyuba E.P. Two pools of interneurons in the bulbar region of the cardiovascular center of rats // Proceedings of the Russian Academy of Sciences. 2015. Vol. 463, No. 5. P. 619–623.
36. Chertok V.M., Nedobyl'skaya Yu.P., Nemkov Yu.K., Shakunov S.A. Effect of laser radiation against the background of folliculin on the capillaries of rat uterus// Bulletin of Experimental Biology and Medicine. Vol. 123, No. 6. P. 718–720.
37. Shirinsky V.P. Molecular physiology of endothelium and mechanisms of vascular permeability // Advances in Physiology Sciences. 2011. Vol. 42, No. 1. P. 18–32.
38. Ablove T.S., Austin J.L., Phernetton T.M., Magness R.R. Effects of endogenous ovarian estrogen versus exogenous estrogen replacement on blood flow and ERβα and ERβ levels in the bladder // Reprod. Sci. 2009. Vol. 16, No. 7. Р. 657–664.
39. Acevedo C.H., Ahmed A. Hemeoxygenase-1 inhibits human myometrial contractility via carbon monoxide and is upregulated by progesterone during pregnancy // J. Clin. Invest. 1998. Vol. 101. Р. 949–955.
40. Alexandreanu I.C., Lawson D.M. Effects of chronic administration of a heme oxygenase substrate or inhibitor on progression of the estrous cycle, pregnancy and lactation of Sprague-Dawley rats // Life Sci. 2002. Vol. 29, No. 2. P.153–162.
41. Ali M.Y., Ping C.Y., Mok Y.Y. [et al.]. Regulation of vascular nitric oxide in vitro and in vivo; a new role for endogenous hydrogen sulphide? // Br. J. Pharmacol. 2006. Vol. 149. P. 625–634.
42. Barber A., Robson S.C., Lyall F. Hemoxygenase and nitric oxide synthase do not maintain human uterine quiescence during pregnancy // Am. J. Pathol. 1999. Vol. 155, No. 3. Р. 831–840.
43. Bertler A., Falck B., Rosengren J. The direct demonstration of a barrier mechanism in the brain capillaries // Acta Pharmacol. Тoxicol. 1966. Vol. 20. P. 317–321.
44. Boehning D., Snyder S.H. Novel neural modulators // Ann. Rev. Neurosci. 2003. Vol. 26. P. 105–131.
45. Byers M.J., Zangl A., Phernetton T.M. [et al.]. Endothelial vasodilator production by ovine uterine and systemic arteries: ovarian steroid and pregnancy control of ERalpha and ERbeta levels // J. Physiol. 2005. Vol. 565 (Pt1). Р. 85–99.
46. Carter T.D., Ogden D. Acetylcholine-stimulated changes of membrane potential and intracellular Ca2+ concentration recorded in endothelial cells in situ in the isolated rat aorta // Pflugers Arch. 1994. Vol. 428. P. 476–484.
47. Cicinelli E., Einer-Jensen N., Galantino P. [et al.]. The vascular cast of the human uterus: from anatomy to physiology // Ann. NY Acad. Sci. 2004. Vol. 1034. Р. 19–26.
48. D'Emmanuele di Villa Bianca R., Fusco F., Mirone V. [et al.]. The role of the hydrogen sulfide pathway in male and female urogenital system in health and disease // Antioxid. Redox Signal. 2017. Vol. 27, No. 10. Р. 654–668.
49. Freedman J.E., Loscalzo J. Nitric oxide and its relationship to thrombotic disorders // J. Thromb. Haemost. 2003. Vol. 1, No. 6. Р. 1183–1188.
50. Garris D.R. Uterine blood flow, pH, and pCO2 during nidation in the guinea pig: ovarian regulation // Endocrinology. 1984. Vol. 114, No. 4. Р. 1219–1224.
51. Garris D.R., McConnaughey M.M., Dar M.S. Estrogen modulation of uterine adrenergic-cholinergic interaction: effects on vasoactivity and adrenergic receptors in the guinea pig // J. Pharmacol. Exp. Ther. 1986. Vol. 239, No. 1. Р. 270–278.
52. Guzman M.A., Navarro M.A., Carnicer R. [et al.]. Cystathionine β-synthase is essential for female reproductive function // Human Molecular Genetics. 2006. Vol. 15. P. 3168−3176.
53. Harvey C.A., Owen D.A. Changes in uterine and ovarian blood flow during the oestrous cycle in rats // J. Endocrinol. 1976. Vol. 71, No. 3. Р. 367–369.
54. Herrnberger L., Ebner K., Junglas B. [et al.]. The role of plasmalemma vesicle-associated protein (PLVAP) in endothelial cells of Schlemm's canal and ocular capillaries // Exp. Eye Res. 2012. Vol. 105. Р. 27–33.
55. Kardon R.H., Farley D.B., Heidger P.M. [et al.]. Intraarterial cushions of the rat uterine artery: a scanning electron microscope evaluation utilizing vascular casts // Anat. Rec. 1982. Vol. 203, No. 1. Р. 19–29.
56. Kisu I., Mihara M., Banno K. [et al.]. A new surgical technique of uterine auto-transplantation in cynomolgus monkey: preliminary report about two cases // Arch. Gynecol. Obstet. 2012. Vol. 285. Р. 135–140.
57. Krzymowski T., Stefańczyk-Krzymowska S. The role of the endometrium in endocrine regulation of the animal oestrous cycle // Reprod. Domest. Anim. 2008. Vol. 43, No. 1. Р. 80–91.
58. Kukoba T.V., Pivovar S.M., Moibenko A.A. Participation of carbon monooxide system in regulation of coronary vessels tone // Clin. Experim. Pathol. 2006. Vol. 5, No. 4. P. 46–49.
59. Lechuga T.J., Zhang H.H., Sheibani L. [et al.]. Estrogen replacement therapy in ovariectomized nonpregnant ewes stimulates uterine artery hydrogen sulfide biosynthesis by selectively upregulating Cystathionine β-Synthase expression // Endocrinology. 2015. Vol. 156, No. 6. P. 2288–2298.
60. Magness R.R., Shaw C.E., Phernetton T.M. [et al.]. Endothelial vasodilator production by uterine and systemic arteries, II: pregnancy effects on NO synthase expression // Am. J. Physiol. 1997. Vol. 272. P. H1730–H1740.
61. Marazioti A., Bucci M., Ciro C. [et al.]. Inhibition of nitric oxide-stimulated vasorelaxation by carbon monoxide-releasing molecules // Arterioscler. Thromb. Vasc. Biol. 2011. Vol. 31. P. 2570–2576.
62. Marshall S.A., Senadheera S.N., Jelinic M. [et al.]. Relaxin Deficiency leads to uterine artery dysfunction during pregnancy in mice // Front. Physiol. 2018. Vol. 22, No. 9. P. 255–267.
63. Mayra P.R., Rosalina V.L., López G. [et al.] Regulation of uterine blood flow. I. Functions of estrogen and estrogen receptor α/β in the uterine vascular endothelium during pregnancy // Rev. Chil. Obstet. Ginecol. 2014. Vol. 79, No. 2. Р. 129–139.
64. Mehta D., Malik A.B. Signaling mechanisms regulating endothelial permeability // Physiol. Rev. 2006. Vol. 86, No. 1 P. 279–367.
65. Mitidieri E., Tramontano T., Donnarumma E. [et al.]. l-Cys/CSE/ H2S pathway modulates mouse uterus motility and sildenafil effect // Pharmacol Res. 2016. Vol. 111. Р. 283–289.
66. Morris A.W., Sharp M.M., Albargothy N.J. Vascular basement membranes as pathways for the passage of fluid into and out of the brain // Acta Neuropathol. 2016. Vol. 131, No. 5. Р. 725–736.
67. Nagpure B.V., Bian J.S. Interaction of hydrogen sulfide with nitric oxide in the cardiovascular system // Oxid Med. Cell Longev. 2016. Vol. 2016. Article ID: 6904327.
68. Nelson Sh.H., Steinsland O.S., Wang Yu. [et al.]. Increased nitric oxide synthase activity and expression in the human uterine artery during pregnancy // Circ. Res. 2000. Vol. 87. Р. 406–411.
69. Němeček D., Dvořáková M., Sedmíková M. Heme oxygenase/ carbon monoxide in the female reproductive system: an overlooked signalling pathway // Int. J. Biochem. Mol. Biol. 2017. Vol. 8, No. 1. P. 1–12.
70. Ogawa K.S., Fujimotok K., Ogawa K. Ultracytochemical studies of adenosine nucleotides in aortiс endothelial and smooth muscle cells – Ca2+-ATPase and Na+, К+-ATFase // Acta Histochem. Cytochem. 1986. Vol. 19. Р. 601–612.
71. Pastore M.B., Talwar S., Conley M.R. [et al.]. Identification of differential ER-alpha versus ER-beta mediated activation of eNOS in ovine uterine artery endothelial cells // Biol. Reprod. 2016. Vol. 94, No. 6. Р. 139.
72. Sheibani L., Lechuga T.J., Zhang H. [et al.]. Augmented H2S production via cystathionine-beta-synthase upregulation plays a role in pregnancy-associated uterine vasodilation / Biol. Reprod. 2017. Vol. 96, No. 3. P. 664–672.
73. Song Y., Fukuda N., Bai C. [et al.]. Role of aquaporins in alveolar fluid clearance in neonatal and adult lung, and in oedema formation following acute lung injury: studies in transgenic aquaporin null mice // J. Physiol. 2000. Vol. 525, No. 3. P. 771–779.
74. Stahl W.L., Baskin D.G. Histochemistry of ATPases // J. Histochem. Cytochem. 1990. Vol. 38, No. 8. Р. 1099–1122.
75. Theoharides T.C., Stewart J.M. Genitourinary mast cells and survival // Trans. Androl. Urol. 2015. Vol. 4, No. 5. Р. 579–586.
76. Toda N., Ayajiki K., Okamura T. Cerebral blood flow regulation by nitric oxide: recent advances // Pharmacol. Rev. 2009. Vol. 61, Nо. 1. Р. 62–97.
77. Toda N., Okamura T. Modulation of renal blood flow and vascular tone by neuronal nitric oxide synthase-derived nitric oxide // J. Vasc. Res. 2011. Vol. 48, Nо. 1. Р. 1–10.
78. Tropea T., De Francesco E.M., Rigiracciolo D. [et al.]. Pregnancy Augments G Protein Estrogen Receptor (GPER) Induced Vasodilation in Rat Uterine Arteries via the Nitric Oxide - cGMP Signaling Pathway // PLoS One. 2015. Vol. 10, No. 11. Р. e0141997.
79. Väisänen-Tommiska M., Butzow R., Ylikorkala O., Mikkola T.S. Mifepristone-induced nitric oxide release and expression of nitric oxide synthases in the human cervix during early pregnancy // Hum. Reprod. 2006. Vol. 21, No. 8. Р. 2180–2184.
80. Wang H., Wang A.X., Aylor K. [et al.]. Nitric oxide directly promotes vascular endothelial insulin transport // Diabetes. 2013. Vol. 62, No. 12. P. 4030–4042.
81. Woidacki K., Jensen F., Zenclussen A.C. Mast cells as novel mediators of reproductive processes // Front. Immunol. 2013. Vol. 4. Р. 29–36.
82. Yang G., Wu B. Jiang L. [et al.]. H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine -lyase // Science. 2008. Vol. 322. Р. 587–590.
83. Zenclussen M.L., Casalis P.A., Jensen F. [et al.]. Hormonal fluctuations during the estrous cycle modulate heme oxygenase-1 expression in the uterus // Front. Endocrinol. 2014. Vol. 5. P. 32.
84. Zhang H.H., Chen J.C., Sheibani L. [et al.]. Pregnancy augments VEGF-stimulated in vitro angiogenesis and vasodilator (NO and H2S) production in human uterine artery endothelial cells // J. Clin. Endocrinol. Metab. 2017. Vol. 102, No. 7. P. 2382–2393.


Founded in 1997  |  Editions in a year: 4, Articles in one issue: 30 |  ISSN of print version: 1609-1175  |  Ind.: 18410 (Agency "Rospechat’")  |  Edition: 1000 c.