Functional Morphology of the Human Uterine Tubes in the 21st Century: Anatomical Novelties and Their Possible Clinical Applications

. 2022 Dec 27 ; 71 (Suppl 1) : S151-S159.

Jazyk angličtina Země Česko Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36592451

The uterine tube (UT) pathologies account for 25-35% of female factor infertility. Although these peculiar organs were first studied several hundred years ago, they have become overlooked and neglected mainly due to the successes of reproductive medicine. Nevertheless, the reproductive medicine still faces many challenges regarding the fertility outcomes of in vitro fertilization (IVF). Many obstacles and problems can be resolved by a more detailed understanding of the UT morphology and function during normal reproduction. Over the course of the 21st century, many new insights have been obtained: the presence of a population of telocytes in the tubal wall responsible for normal motility and hormone sensory function, the demonstration of lymphatic lacunae of the mucosal folds necessary for oocyte capture and tubal fluid recirculation, or a thorough profiling of the immune makeup of the UT epithelial lining with the discovery of regulatory T cells presumably important for maternal tolerance towards the semi-allogenic embryo. New discoveries also include the notion that the UT epithelium is male sex hormone-sensitive, and that the UT is not sterile, but harbors a complex microbiome. The UT epithelial cells were also shown to be the cells-of-origin of high-grade serous ovarian carcinomas. Finally, yet importantly, several modern morphological directions have been emerging recently, including cell culture, development of tubal organoids, in silico modelling, tissue engineering and regenerative medicine. All these novel insights and new approaches can contribute to better clinical practice and successful pregnancy outcomes.

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Feinberg EC. True, true, and unrelated: tubal patency, tubal architecture, and tubal function. Fertil Steril. 2018;110:646–647. doi: 10.1016/j.fertnstert.2018.06.007. PubMed DOI

López-Úbeda R, García-Vázquez FA, Gadea J, Matás C. Oviductal epithelial cells selected boar sperm according to their functional characteristics. Asian J Androl. 2017;19:396–403. doi: 10.4103/1008-682X.173936. PubMed DOI PMC

Ezzati M, Djahanbakhch O, Arian S, Carr BR. Tubal transport of gametes and embryos: a review of physiology and pathophysiology. J Assist Reprod Genet. 2014;31:1337–1347. doi: 10.1007/s10815-014-0309-x. PubMed DOI PMC

Kajanová M, Danihel L, Polak S, Miko M, Urban L, Bokor T, Varga I. [The structural basis for transport through the Fallopian tube] Ceska Gynekol. 2012;77:566–571. PubMed

Csöbönyeiová M, Varga I, Lapides L, Pavlíková L, Feitscherová C, Klein M. From a passive conduit to highly dynamic organ. what are the roles of uterine tube epithelium in reproduction? Physiol Res. 2022;71(Suppl 1):S11–S20. doi: 10.33549/physiolres.934954. PubMed DOI PMC

Practice Committee of the American Society for Reproductive Medicine. Role of tubal surgery in the era of assisted reproductive technology: a committee opinion. Fertil Steril. 2021;115:1143–1150. doi: 10.1016/j.fertnstert.2021.01.051. PubMed DOI

Xiang J, Venkatesan S. The role of Vesalius and his contemporaries in the transfiguration of human anatomical science. J Anat. 2022 doi: 10.1111/joa.13773. PubMed DOI PMC

Thiery M. [Vesalius and the anatomy of the female genital tract] Verh K Acad Geneeskd Belg. 1993;55:609–682. PubMed

van Gijn J, Gijselhart JP. [Falloppius and his uterine tubes] Ned Tijdschr Geneeskd. 2011;155:A3639. PubMed

Popescu LM, Ciontea SM, Cretoiu D, Hinescu ME, Radu E, Ionescu N, Ceausu M, Gherghiceanu M, Braga RI, Vasilescu F, Zagrean L, Ardeleanu C. Novel type of interstitial cell (Cajal-like) in human Fallopian tube. J Cell Mol Med. 2005;9:479–523. doi: 10.1111/j.1582-4934.2005.tb00505.x. PubMed DOI PMC

Abd-Elhafeez HH, Soliman SA. New description of telocyte sheaths in the bovine uterine tube: an immunohistochemical and scanning microscopic study. Cells Tissues Organs. 2017;203:295–315. doi: 10.1159/000452243. PubMed DOI

Cretoiu D, Ciontea SM, Popescu LM, Ceafalan L, Ardeleanu C. Interstitial Cajal-like cells (ICLC) as steroid hormone sensors in human myometrium: immunocytochemical approach. J Cell Mol Med. 2006;10:789–795. doi: 10.1111/j.1582-4934.2006.tb00438.x. PubMed DOI PMC

Varga I, Urban L, Kajanová M, Polák Š. Functional histology and possible clinical significance of recently discovered telocytes inside the female reproductive system. Arch Gynecol Obstet. 2016;294:417–422. doi: 10.1007/s00404-016-4106-x. PubMed DOI

Klein M, Csöbönyeiová M, Danišovič L’, Lapides L, Varga I. Telocytes in the female reproductive system: up-to-date knowledge, challenges and possible clinical applications. Life (Basel) 2022;12:267. doi: 10.3390/life12020267. PubMed DOI PMC

Klein M, Lapides L, Fecmanova D, Varga I. From TELOCYTES to TELOCYTOPATHIES. Do recently described interstitial cells play a role in female idiopathic infertility? Medicina (Kaunas) 2020;56:688. doi: 10.3390/medicina56120688. PubMed DOI PMC

Klein M, Lapides L, Fecmanová D, Varga I. Novel cellular entities and their role in the etiopathogenesis of female idiopathic infertility-a review article. CEOG. 2021;48:461–465. doi: 10.31083/j.ceog.2021.03.2395. DOI

Varga I, Kachlík D, Žišková M, Miko M. Lymphatic lacunae of the mucosal folds of human uterine tubes - A rediscovery of forgotten structures and their possible role in reproduction. Ann Anat. 2018;219:121–128. doi: 10.1016/j.aanat.2018.06.005. PubMed DOI

Ferraz M, Rho HS, Hemerich D, Henning HHW, van Tol HTA, Hölker M, Besenfelder U, Mokry M, Vos P, Stout TAE, Le Gac S, Gadella BM. An oviduct-on-a-chip provides an enhanced in vitro environment for zygote genome reprogramming. Nat Commun. 2018;9:4934. doi: 10.1038/s41467-018-07119-8. PubMed DOI PMC

Wang M, Zhu T, Liu C, Jin L, Fei P, Zhang B. Oviduct-mimicking microfluidic chips decreased the ROS concentration in the in vitro fertilized embryos of CD-1 mice. Biomed Pharmacother. 2022;154:113567. doi: 10.1016/j.biopha.2022.113567. PubMed DOI

Marey MA, Yousef MS, Kowsar R, Hambruch N, Shimizu T, Pfarrer C, Miyamoto A. Local immune system in oviduct physiology and pathophysiology: attack or tolerance? Domest Anim Endocrinol. 2016;56(Suppl):S204–211. doi: 10.1016/j.domaniend.2016.02.005. PubMed DOI

Ardighieri L, Lonardi S, Moratto D, Facchetti F, Shih Ie M, Vermi W, Kurman RJ. Characterization of the immune cell repertoire in the normal Fallopian tube. Int J Gynecol Pathol. 2014;33:581–591. doi: 10.1097/PGP.0000000000000095. PubMed DOI PMC

Rigby CH, Aljassim F, Powell SG, Wyatt JNR, Hill CJ, Hapangama DK. The immune cell profile of human Fallopian tubes in health and benign pathology: a systematic review. J Reprod Immunol. 2022;152:103646. doi: 10.1016/j.jri.2022.103646. PubMed DOI

Varga I, Miko M, Kachlík D, Žišková M, Danihel L’, Jr, Babál P. How many cell types form the epithelial lining of the human uterine tubes? Revision of the histological nomenclature of the human tubal epithelium. Ann Anat. 2019;224:73–80. doi: 10.1016/j.aanat.2019.03.012. PubMed DOI

Agostinis C, Mangogna A, Bossi F, Ricci G, Kishore U, Bulla R. Uterine immunity and microbiota: a shifting paradigm. front immunol. 2019;10:2387. doi: 10.3389/fimmu.2019.02387. PubMed DOI PMC

Pelzer ES, Willner D, Huygens F, Hafner LM, Lourie R, Buttini M. Fallopian tube microbiota: evidence beyond DNA. Future Microbiol. 2018;13:1355–1361. doi: 10.2217/fmb-2018-0118. PubMed DOI

Schröder R. Die Weiblichen Genitalorgane. In: von Möllendorff W, editor. Handbuch der Mikroskopuschen Anatomie des Mensech. Verlag von Julius Springer; 1930. DOI

Lyons RA, Djahanbakhch O, Mahmood T, Saridogan E, Sattar S, Sheaff MT, Naftalin AA, Chenoy R. Fallopian tube ciliary beat frequency in relation to the stage of menstrual cycle and anatomical site. Hum Reprod. 2002;17:584–588. doi: 10.1093/humrep/17.3.584. PubMed DOI

Brodowska A, Grabowska M, Bittel K, Ciećwież S, Brodowski J, Szczuko M, Szydłowska I, Piasecka M. Estrogen and progesterone receptor immunoexpression in Fallopian tubes among postmenopausal women based on time since the last menstrual period. Int J Environ Res Public Health. 2021;18:9195. doi: 10.3390/ijerph18179195. PubMed DOI PMC

Dulohery K, Trottmann M, Bour S, Liedl B, Alba-Alejandre I, Reese S, Hughes B, Stief CG, Kölle S. How do elevated levels of testosterone affect the function of the human Fallopian tube and fertility?-New insights. Mol Reprod Dev. 2020;87:30–44. doi: 10.1002/mrd.23291. PubMed DOI

Zhang S, Dolgalev I, Zhang T, Ran H, Levine DA, Neel BG. Both Fallopian tube and ovarian surface epithelium are cells-of-origin for high-grade serous ovarian carcinoma. Nat Commun. 2019;10:5367. doi: 10.1038/s41467-019-13116-2. PubMed DOI PMC

El Bairi K, Al Jarroudi O, Le Page C, Afqir S. Does the "Devil" originate from the Fallopian tubes? Semin Cancer Biol. 2021;77:56–66. doi: 10.1016/j.semcancer.2021.03.018. PubMed DOI

Höhn AK, Klagges S, Gläser A, Taubenheim S, Dornhöfer N, Einenkel J, Hiller GGR, Brambs CE, Horn LC. Increase of Fallopian tube and decrease of ovarian carcinoma: fact or fake? J Cancer Res Clin Oncol. 2021;147:911–925. doi: 10.1007/s00432-020-03387-4. PubMed DOI PMC

Kyo S, Ishikawa N, Nakamura K, Nakayama K. The Fallopian tube as origin of ovarian cancer: Change of diagnostic and preventive strategies. Cancer Med. 2020;9:421–431. doi: 10.1002/cam4.2725. PubMed DOI PMC

Bahar-Shany K, Brand H, Sapoznik S, Jacob-Hirsch J, Yung Y, Korach J, Perri T, Cohen Y, Hourvitz A, Levanon K. Exposure of Fallopian tube epithelium to follicular fluid mimics carcinogenic changes in precursor lesions of serous papillary carcinoma. Gynecol Oncol. 2014;132:322–327. doi: 10.1016/j.ygyno.2013.12.015. PubMed DOI

Venturella R, Morelli M, Zullo F. The fallopian tube in the 21st century: when, why, and how to consider removal. Oncologist. 2015;20:1227–1229. doi: 10.1634/theoncologist.2015-0172. PubMed DOI PMC

Salvador S, Scott S, Francis JA, Agrawal A, Giede C. No. 344-opportunistic salpingectomy and other methods of risk reduction for ovarian/Fallopian tube/peritoneal cancer in the general population. J Obstet Gynaecol Can. 2017;39:480–493. doi: 10.1016/j.jogc.2016.12.005. PubMed DOI

McQueen BE, Kiatthanapaiboon A, Fulcher ML, Lam M, Patton K, Powell E, Kollipara A, Madden V, Suchland RJ, Wyrick P, O'Connell CM, Reidel B, Kesimer M, Randell SH, Darville T, Nagarajan UM. Human Fallopian tube epithelial cell culture model to study host responses to chlamydia trachomatis infection. Infect Immun. 2020;88:e00105–20. doi: 10.1128/IAI.00105-20. PubMed DOI PMC

Álamos-Musre AS, Escobar A, Tapia CV, Christodoulides M, Rodas PI. Use of human Fallopian tube organ in culture (FTOC) and primary fallopian tube epithelial cells (FTEC) to study the biology of neisseria gonorrhoeae infection. Methods Mol Biol. 2019;1997:377–402. doi: 10.1007/978-1-4939-9496-0_22. PubMed DOI

Mohammadi R, Mousavi SO, Sheibak N, Amjadi F, Zandieh Z, Aghajanpour S, Aflatoonian K, Sabbaghian M, Eslami M, Aflatoonian R. Sperm-oviduct interaction: Differential gene expression of growth factors induced by sperm DNA fragmentation. Andrologia. 2022;54:e14378. doi: 10.1111/and.14378. PubMed DOI

Mousavi SO, Mohammadi R, Amjadi F, Zandieh Z, Aghajanpour S, Aflatoonian K, Sabbaghian M, Eslami M, Madani T, Aflatoonian R. Immunological response of Fallopian tube epithelial cells to spermatozoa through modulating cytokines and chemokines. J Reprod Immunol. 2021;146:103327. doi: 10.1016/j.jri.2021.103327. PubMed DOI

Zhu J, Xu Y, Rashedi AS, Pavone ME, Kim JJ, Woodruff TK, Burdette JE. Human Fallopian tube epithelium co-culture with murine ovarian follicles reveals cross-talk in the reproductive cycle. Mol Hum Reprod. 2016;22:756–767. doi: 10.1093/molehr/gaw041. PubMed DOI PMC

Zhu M, Iwano T, Takeda S. Fallopian tube basal stem cells reproducing the epithelial sheets in vitro-stem cell of fallopian epithelium. Biomolecules. 2020;10:1270. doi: 10.3390/biom10091270. PubMed DOI PMC

Lawrenson K, Notaridou M, Lee N, Benjamin E, Jacobs IJ, Jones C, Gayther SA. In vitro three-dimensional modeling of Fallopian tube secretory epithelial cells. BMC Cell Biol. 2013;14:43. doi: 10.1186/1471-2121-14-43. PubMed DOI PMC

Venkata VD, Jamaluddin MFB, Goad J, Drury HR, Tadros MA, Lim R, Karakoti A, O'Sullivan R, Ius Y, Jaaback K, Nahar P, Tanwar PS. Development and characterization of human fetal female reproductive tract organoids to understand Müllerian duct anomalies. Proc Natl Acad Sci U S A. 2022;119:e2118054119. doi: 10.1073/pnas.2118054119. PubMed DOI PMC

Ford MJ, Harwalkar K, Pacis AS, Maunsell H, Wang YC, Badescu D, Teng K, Yamanaka N, Bouchard M, Ragoussis J, Yamanaka Y. Oviduct epithelial cells constitute two developmentally distinct lineages that are spatially separated along the distal-proximal axis. Cell Rep. 2021;36:109677. doi: 10.1016/j.celrep.2021.109677. PubMed DOI

Diemer J, Hahn J, Goldenbogen B, Müller K, Klipp E. Sperm migration in the genital tract-In silico experiments identify key factors for reproductive success. PLoS Comput Biol. 2021;17:e1009109. doi: 10.1371/journal.pcbi.1009109. PubMed DOI PMC

Francés-Herrero E, Lopez R, Hellström M, de Miguel-Gómez L, Herraiz S, Brännström M, Pellicer A, Cervelló I. Bioengineering trends in female reproduction: a systematic review. Hum Reprod Update. 2022;28:798–837. doi: 10.1093/humupd/dmac025. PubMed DOI PMC

Sittadjody S, Criswell T, Jackson JD, Atala A, Yoo JJ. Regenerative medicine approaches in bioengineering female reproductive tissues. Reprod Sci. 2021;28:1573–1595. doi: 10.1007/s43032-021-00548-9. PubMed DOI

Wang J, Zhao Y, Wu X, Yin S, Chuai Y, Wang A. The utility of human Fallopian tube mucosa as a novel source of multipotent stem cells for the treatment of autologous reproductive tract injury. Stem Cell Res Ther. 2015;6:98. doi: 10.1186/s13287-015-0094-1. PubMed DOI PMC

Almasry SM, Elfayomy AK, El-Sherbiny MH. Regeneration of the Fallopian tube mucosa using bone marrow mesenchymal stem cell transplantation after induced chemical injury in a rat model. Reprod Sci. 2018;25:773–781. doi: 10.1177/1933719117725824. PubMed DOI

Li S, Winuthayanon W. Oviduct: roles in fertilization and early embryo development. J Endocrinol. 2017;232:R1–r26. doi: 10.1530/JOE-16-0302. PubMed DOI

Dissanayake K, Nõmm M, Lättekivi F, Ord J, Ressaissi Y, Godakumara K, Reshi QUA, Viil J, Jääger K, Velthut-Meikas A, Salumets A, Jaakma Ü, Fazeli A. Oviduct as a sensor of embryo quality: deciphering the extracellular vesicle (EV)-mediated embryo-maternal dialogue. J Mol Med (Berl) 2021;99:685–697. doi: 10.1007/s00109-021-02042-w. PubMed DOI

Dissanayake K, Nõmm M, Lättekivi F, Ressaissi Y, Godakumara K, Lavrits A, Midekessa G, Viil J, Bæk R, J⊘rgensen MM, Bhattacharjee S, Andronowska A, Salumets A, Jaakma Ü, Fazeli A. Individually cultured bovine embryos produce extracellular vesicles that have the potential to be used as non-invasive embryo quality markers. Theriogenology. 2020;149:104–116. doi: 10.1016/j.theriogenology.2020.03.008. PubMed DOI

Besenfelder U, Brem G, Havlicek V. Review: Environmental impact on early embryonic development in the bovine species. Animal. 2020;14:s103–s112. doi: 10.1017/S175173111900315X. PubMed DOI

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