The site of the Media Sphera Publishers contains materials intended solely for healthcare professionals.
By closing this message, you confirm that you are a certified medical professional or a student of a medical educational institution.

Burlev V.A.

Nauchnyĭ tsentr akusherstva, ginekologii i perinatologii im. akad. V.I. Kulakova, Moskva

Il'iasova N.A.

Nauchnyĭ tsentr akusherstva, ginekologii i perinatologii im. akad. V.I. Kulakova, Moskva

Neuroangiogenesis in endometrium of women with endometriosis and chronic pelvic pain: high expression of vasoactive intestinal peptide

Authors:

Burlev V.A., Il'iasova N.A.

More about the authors

Journal: Russian Journal of Human Reproduction. 2017;23(4): 87‑97

Read: 843 times


To cite this article:

Burlev VA, Il'iasova NA. Neuroangiogenesis in endometrium of women with endometriosis and chronic pelvic pain: high expression of vasoactive intestinal peptide. Russian Journal of Human Reproduction. 2017;23(4):87‑97. (In Russ.)
https://doi.org/10.17116/repro201723487-97

Recommended articles:
Use of gona­dotropic releasing hormone agonists in hype­rplastic syndrome in gyne­cology. Russian Bulletin of Obstetrician-Gynecologist. 2025;(4):51-58
Influence of limb reva­scularization and therapeutic angiogenesis on concentration of angiogenic factors. Russian Journal of Cardiology and Cardiovascular Surgery. 2025;(5):539-546

References:

  1. Burlev VA, Ilyasova NA. AlphaB-crystallin expression in eutopic and ectopic endometrium among the patients with peritoneal form endometriosis: pregnancy outcome. Problemy reproduktsii. 2016;22(1):12-19. (In Russ.). https://doi.org/10.17116/repro201622112-19
  2. Burlev VA, Ilyasova NA. Particular signaling LIF/LIFE/gp130/SOCS1 pathway in patients with peritoneal endometriosis and infertility. Problemy reproduktsii. 2016; 22(2):24-32. (In Russ.). https://doi.org/10.17116/repro201622224-32
  3. Burlev VA, Ilyasova NA. Sex hormone levels and the nucleons isoforms expression of estrogen and progesterone receptors in eutopic endometrium of patients with peritoneal form endometriosis and infertility. Problemy reproduktsii. 2016;22(4):66-75. (In Russ.). https://doi.org/10.17116/repro201622466-75
  4. Kogan EA, Paramonova NB, Demura TA, Faĭzullina NM, Ovakimian AS, Adamian LV. The morphological substrate and pathogenetic mechanisms of pelvic pain syndrome in endometriosis. Arkhiv patologii. 2014;6:37-43. (In Russ.).
  5. Овакимян А.С., Адамян Л.В., Коган Е.А., Козаченко И.Ф., Чернов Д.Н., Арсланян К.Н. Болевой синдром при эндометриозе: клинико-морфологические и молекулярные механизмы. Проблемы репродукции. 2015;6:31-38. [Ovakimyan AS, Adamyan LV, Kogan EA, Kozachenko IF, Chernov DN, Arslanyan KN. Pain syndrome in endometriosis: clinical, morphological and molecular mechanisms. Problemy reproduktsii. 2015;6:31-38. https://doi.org/10.17116/repro201521631-38/
  6. Chernukha GE. The endometriosis and chronic pelvic pain: the causes and effects. Problemy reproduktsii. 2011;5:83-89. (In Russ.). Available at: https://elibrary.ru/item.asp?id=18949312 Accessed June 01,2017
  7. Ahn SH, Edwards AK, Singh SS, Young SL, Lessey BA, Tayade C. IL-17A Contributes to the pathogenesis of endometriosis by triggering proinflammatory cytokines and angiogenic growth factors. J Immunol. 2015;195(6):2591-2600. https://doi.org/10.4049/jimmunol.1501138
  8. Apodaca-Torrez FR, Triviño M, Lobo EJ, Goldenberg A, Triviño T. Extra-pancreatic vipoma. Abcd arq bras cir dig. 2014;27(2):222-224. https://doi.org/10.1590/S0102-67202014000300015
  9. Arosh JA, Lee JeH, Balasubbramanian D, Stanley JA, Long CR, Meagher MW, Osteen KG, Bruner-Tran KL, Burghardt RC, Starzinski-Powitz A, Banua SK. Molecular and preclinical basis to inhibit PGE2 receptors EP2 and EP4 as a novel nonsteroidal therapy for endometriosis. Proc Natl Acad Sci USA. 2015;112(31):9716-9721. https://doi.org/10.1073/pnas.1507931112
  10. Asante A, Taylor RN. Endometriosis: the role of neuroangiogenesis. Annu Rev Physiol. 2011;73:163-182. https://doi.org/10.1146/annurev-physiol-012110-142158
  11. Bajo AM, Juarranz MG, Valenzuel P, Martı́nez P, Prietoa JC, Guijarro LG. Expression of vasoactive intestinal peptide (VIP) receptors in human uterus. Peptides. 2000;21(9):1383-1388. https://doi.org/10.1016/S0196-9781(00)00282-5
  12. Berkley KJ, Rapkin AJ, Papka RE. The pains of endometriosis. Science. 2005;308(5728):1587-1589. https://doi.org/10.1126/science.1111445
  13. Bokor A, Kyama CM, Vercruysse L, Fassbender A, Gevaert O, Vodolazkaia A, De Moor B, Fülöp V, D’Hooghe T. Density of small diameter sensory nerve fibres in endometrium: a semi-invasive diagnostic test for minimal to mild endometriosis. Hum Reprod. 2009;24(12):3025-3032. https://doi.org/10.1093/humrep/dep283
  14. Bourcier ME, Vinik AI. sunitinib for the treatment of metastatic paraganglioma and vasoactive intestinal polypeptide-producing tumor (VIPoma) pancreas. 2013;42(2):348-352. https://doi.org/10.1097/MPA.0b013e31825c53fa
  15. Bourlev V, Moberg C, Ilyasova N, Davey E, Kunovac Kallak Th, Olovsson M. Vasoactive intestinal peptide is upregulated in women with endometriosis and chronic pelvic pain. In thesis: The Human endometrium. Stadies on Angiogenesis and Endometriosis. 2016;identifiers Available at: URN: urn:nbn:se:uu:diva-314225 OAI: 2017oai:DiVA.org:uu-314225 DiVA: diva2:1070106 Accessed June 01,2017
  16. Bourlev V, Volkov N, Pavlovitch S, Lets N, Larsson A., Olovsson M. The relationship between microvessel density, proliferative activity and expression of vascular endothelial growth factor-A and its receptors in eutopic endometrium and endometriotic lesions. Reproduction. 2006;132(3):501-509. https://doi.org/10.1530/rep.1.01110
  17. Collado B, Carmena MJ, Clemente C, Prieto JC, Bajo AM. Vasoactive intestinal peptide enhances growth and angiogenesis of human experimental prostate cancer in a xenograft model. Peptides. 2007;28(9):1896-1990. https://doi.org/10.1016/j.peptides.2007.04.015
  18. Couvineau A, Laburthe M. VPAC receptors: structure, molecular pharmacology and interaction with accessory proteins. Br J Pharmacol. 2012;166(1):42-50. https://doi.org/10.1111/j.1476-5381.2011.01676.x
  19. Danese S, Deban L. Does the mucosal microcirculation play a role in IBD? Inflamm Bowel Dis. 2008;14:Suppl 2:125-126. https://doi.org/10.1002/ibd.20716
  20. Dickinson T, Fleetwood-Walker SM. VIP and PACAP: very important in pain? Trends Pharmacol Sci. 1999;20(8):324-329. https://doi.org/10.1016/S0165-6147(99)01340-1
  21. Di Spiezio Sardo A, Florio P, Fernandez LM, Guerra G, Spinelli M, Di Carlo C, Filippeschi M, Nappi C. The potential role of endometrial nerve fibers in the pathogenesis of pain during endometrial biopsy at office hysteroscopy. Reprod Sci. 2015; 22(1):124-131. https://doi.org/10.1177/1933719114534536
  22. Ellett L, Readman E, Newman M, McIlwaine K, Villegas R, Jagasia N, Maher P. Are endometrial nerve fibres unique to endometriosis? A prospective case-control study of endometrial biopsy as a diagnostic test for endometriosis in women with pelvic pain. Hum Reprod. 2015;30(12):2808-2815. https://doi.org/10.1093/humrep/dev259
  23. Ganea D, Hooper KM, Kong W. The neuropeptide vasoactive intestinal peptide: direct effects on immune cells and involvement in inflammatory and autoimmune diseases. Acta Physiol (Oxf). 2015;213(2):442-452. https://doi.org/10.1111/apha.12427
  24. Garcia-Manero M, Alcazar JL, Toledo G. Vascular endothelial growth factor (VEGF) and ovarian endometriosis: correlation between VEGF serum levels, VEGF cellular expression, and pelvic pain. Fertil Steril. 2007;88(2):513-515. https://doi.org/10.1016/j.fertnstert.2006.11.117
  25. Giudice LC. Clinical practice. Endometriosis. N Engl J Med. 2010;362(25):2389-2398. https://doi.org/10.1056 /NEJMcp1000274
  26. Greaves E, Collins F, Esnal-Zufiaurre A, Giakoumelou S, Horne AW, Saunders PT. Estrogen receptor (ER) agonists differentially regulate neuroangiogenesis in peritoneal endometriosis via the repellent factor SLIT3. Endocrinology. 2014;155(10):4015-4026. https://doi.org/10.1210/en.2014-1086
  27. Greene AD, Lang SA, Kendziorski JA, Sroga-Rios JM, Herzog TJ, Burns KA. Endometriosis: where are we and where are we going? Reproduction. 2016;152(3):R63-R78. https://doi.org/10.1530/REP-16-0052
  28. Hu DE, Hiley CR, Fan TP. Comparative studies of the angiogenic activity of vasoactive intestinal peptide, endothelins-1 and -3 and angiotensin II in a rat sponge model. Br J Pharmacol. 1996;117(3): 545-551. https://doi.org/10.1111/j.1476-5381.1996.tb15225.x
  29. Johnson JB, Marsden L, Samadder NJ. A rare cause of diarrhea: pancreatic VIPoma. Endoscopy. 2013;45:E311-E312. https://doi.org/10.1055/с-0033-1344411
  30. Küpker W, Schultze-Mosgau A, Diedrich K. Paracrine changes in the peritoneal environment of women with endometriosis. Hum Reprod Update. 1998;4(5):719-723. https://doi.org/10.1093/humupd/4.5.719
  31. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T). Method. Methods. 2001;25(4):402-408. https://doi.org/10.1006/meth.2001.1262
  32. Maharajaa SPK, Black KI, Manconi F, Ng CHM, Hey-Cunningham A, Fraser IS, Berbic M. An investigation of the relationship between pelvic pain and density of nerve fibers in peritoneal lesions of endometriosis. Journal of Endometriosis and Pelvic Pain Disorders. 2014;6(2):84-91. https://doi.org/10.5301/je.5000185
  33. Martınez C, Ortiz AM, Juarranz Y, Lamana A, Seoane IV, Leceta J, Garcıa-Vicuna R, Gomariz RP, Gonzalez-Alvaro I. Serum levels of vasoactive intestinal peptide as a prognostic marker in early arthritis. PLoS One. 2014;9(1):1-8. https://doi.org/10.1371/journal.pone.0085248
  34. Miller EJ, Fraser IS. The importance of pelvic nerve fibers in endometriosis. Womens Health (Lond). 2015;11(5):611-618. https://doi.org/10.2217/whe.15.47
  35. Moberg С, Bourlev V, Ilyasova N, Olovsson M. Endometrial expression of LIF and its receptor and peritoneal fluid levels of IL-1α and IL-6 in women with endometriosis are associated with the probability of pregnancy. Arch Gynecol Obstet. 2015;292(2):429-437. https://doi.org/10.1007/s00404-015-3626-0
  36. Morotti M, Vincent K, Brawn J, Zondervan KT, Becker CM. Peripheral changes in endometriosis-associated pain. Hum Reprod Update. 2014;20(5):717-736. https://doi.org/10.1093/humupd/dmu021
  37. Newman TA, Bailey JL, Stocker LJ, Woo YL, Macklon NS, Cheong YC. Expression of neuronal markers in the endometrium of women with and those without endometriosis. Hum Reprod. 2013;28(9):2502-2510. https://doi.org/10.1093/humrep/det274
  38. Nisenblat V, Bossuyt PM, Shaikh R, Farquhar C, Jordan V, Scheffers CS, Mol BW, Johnson N, Hull ML. Blood biomarkers for the non-invasive diagnosis of endometriosis. Cochrane Database Syst Rev. 2016;1(5):CD012179. https://doi.org/10.1002/14651858.CD012179
  39. Nnoaham KE, Hummelshoj L, Webster P, d’Hooghe T, de Cicco Nardone F, de Cicco Nardone C, Jenkinson C, Kennedy SH, Zondervan KT; World Endometriosis Research Foundation Global Study of Women’s Health consortium. Impact of endometriosis on quality of life and work productivity: a multicenter study across ten countries. Fertil Steril. 2011;96(2):366-373. https://doi.org/10.1016/j.fertnstert.2011.05.090
  40. Overton C, Fernandez-Shaw S, Hicks B, Barlow D, Starkey P. Peritoneal fluid cytokines and the relationship with endometriosis and pain. Hum Reprod. 1996;11(2):380-386. https://doi.org/10.1093/HUMREP/11.2.380
  41. Rakhila H, Al-Akoum M, Doillon C, Lacroix-Pépin N, Leboeuf M, Lemyre M, Akoum A, Pouliot M. Augmented angiogenic factors expression via FP signaling pathways in peritoneal endometriosis. J Clin Endocrinol Metab. 2016;101(12):4752-4763. https://doi.org/10.1210/jc.2016-1569
  42. Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril. 1997;67:817-821. https://doi.org/10.1016/S0015-0282(97)81391-X
  43. Maheshwari RR, Desai M, Rao VP, Palanki RR, Namburi RP, Reddy KT, Reddy AP. Indian Ischemic stroke as a presenting feature of VIPoma due to MEN1 syndrome. Journal of Endocrinology and Metabolism. 2013;17(S1):215-218. https://doi.org/10.4103/2230-8210.119576
  44. Svensson CI. Interleukin-6: a local pain trigger? Arthritis Res Ther. 2010;12(5):145. https://doi.org/10.1186/ar3138
  45. Tokushige N, Markham R, Russell P, Fraser IS. Nerve fibres in peritoneal endometriosis. Hum Reprod. 2006;21(11):3001-3007. https://doi.org/10.1093/humrep/del260
  46. Tokushige N, Markham R, Russell P, Fraser IS. Effects of hormonal treatment on nerve fibers in endometrium and myometrium in women with endometriosis. Fertility and Sterility. 2008;90(5): 1589-1598. https://doi.org/10.1016/j.fertnstert.2007.08.074
  47. Velasco I, Acien P, Campos A, Acien MI, Ruiz-Macia E. Interleukin-6 and other soluble factors in peritoneal fluid and endometriomas and their relation to pain and aromatase expression. J Reprod Immunol. 2010;84(2):199-205. https://doi.org/10.1016/j.jri.2009.11.004
  48. Wallengren J. Vasoactive peptides in the skin. J Investig Dermatol Symp Proc. 1997;2(1):49-55. https://doi.org/10.1038/jidsymp.1997.11
  49. Wang G, Tokushige N, Russell P, Dubinovsky S, Markham R, Fraser IS. Hyperinnervation in intestinal deep infiltrating endometriosis. J Minim Invasive Gynecol. 2009;16(6):713-719. https://doi.org/10.1016/j.jmig.2009.07.012
  50. Wang G, Tokushige N, Markham R, Fraser IS. Rich innervation of deep infiltrating endometriosis. Hum Reprod. 2009;24(4):827-834. https://doi.org/10.1093/humrep/den464
  51. Yang J, Shi QD, Song TB, Feng GF, Zang WJ, Zong CH, Chang L. Vasoactive intestinal peptide increases VEGF expression to promote proliferation of brain vascular endothelial cells via the cAMP/PKA pathway after ischemic insult in vitro. Peptides. 2013;42:105-111. https://doi.org/10.1016/j.peptides.2013.01.007
  52. Young VJ, Brown JK, Saunders PT, Horne AW. The role of the peritoneum in the pathogenesis of endometriosis. Hum Reprod Update. 2013;19(5):558-569. https://doi.org/10.1093/humupd/dmt024
  53. Zhou YQ, Liu Z, Liu ZH, Chen SP, Li M, Shahveranov A, Ye DW, Tian YK. Interleukin-6: an emerging regulator of pathological pain. J Neuroinflammation. 2016;13(1):141. https://doi.org/10.1186/s12974-016-0607-6

Email Confirmation

An email was sent to test@gmail.com with a confirmation link. Follow the link from the letter to complete the registration on the site.

Email Confirmation

We use cооkies to improve the performance of the site. By staying on our site, you agree to the terms of use of cооkies. To view our Privacy and Cookie Policy, please. click here.