Mucociliary apparatus of the fallopian tubes and related pathogenetic aspects contributing to infertility and prospects for correction (analytical review)
https://doi.org/10.17749/2313-7347/ob.gyn.rep.2021.166
Abstract
Introduction. The mucociliary apparatus (MCA) of the fallopian tubes (MTр) represents one of the key mechanisms and arms in functioning of female reproductive system. A prominent role of impaired MCA in the pathogenesis of reproductive system diseases and infertility, on the one hand, as well as insufficient knowledge and elucidation of this topic, on the other hand, spurred current study.
Aim: to improve our understanding about a role for reproductive system MCA and its impairment in developing diseases and infertility, as well as to identify potential perspectives for their correction.
Materials and Methods. We searched for publications and analyzed literature data from 1980 to 2020 using various scientific databases, including Index Medicus, PubMed/MEDLINE, Embase, Cochrane Library and Russian scholarly journals related to gynecology, obstetrics and reproduction.
Results. The analysis conducted allowed to originally assess the morpho-functional, structural-genetic features and other important aspects of MCA MTр. In addition, we demonstrated an impact of various factors on developing diverse types of pathological processes, including those capable of causing infertility. Moreover, we also elucidated a state of MCA MTр coupled to various diseases, including genetically determined disorders.
Conclusion. The role of impaired MCA MTр in developing pathological process and infertility was of tremendous importance and deserves close attention, because they are often remained undiagnosed by standard methods and require use of morphological and functional research methods for verification. Perspectives for diagnostics and correction of MCA MTр disorders are further discussed.
About the Author
V. I. Kobylyansky
Federal Pulmonology Research Institute, Federal Medical and Biological Agency of Russia
Russian Federation
Russian Federation
Vyacheslav I. Kobylyansky – MD, Dr Sci Med, Professor, Educational Center, Federal Pulmonology Research Institute
32 bldg. 4, 11th Parkovaya Str., Moscow 105077
References
1. De Angelis C., Nardone A., Garifalos F. et al. Smoke, alcohol and drug addiction and female fertility. Reprod Biol Endocrinol. 2020;18(1):21. https://doi.org/10.1186/s12958-020-0567-7.
2. Lyons R.A., Saridogan E., Djahanbakhch1 O. The reproductive significance of human Fallopian tube cilia. Hum Reprod Update. 2006;12(4):363–72. https://doi.org/10.1093/humupd/dml012.
3. Marra A.N., Li Y., Wingert R.A. Antennas of organ morphogenesis: the roles of cilia in vertebrate kidney development. Genesis. 2016;54(9):457– 69. https://doi.org/10.1002/dvg.22957.
4. Van der Linden P.J. Theories on pathogenesis of endometriosis. Hum Reprod. 1996;11(Suppl 3):53–65. https://doi.org/10.1093/humrep/11.suppl_3.53.
5. Sleigh M.A., Blake J.R., Liron N. The propulsion of mucus cilia. Am Rev Respir Dis. 1988;137(3):726–41. https://doi.org/10.1164/ajrccm/137.3.726.
6. Sanderson M.J., Sleigh M.A. Ciliary activity of cultured rabbit tracheal epithelium: beat pattern and metachrony. J Cell Sci. 1981;47:331–47.
7. Paltieli Y., Weichselbaum A., Hoffman N. et al. Physiology: Laser scattering instrument for real time in vivo measurement of ciliary activity in human Fallopian tubes. Hum Reprod. 1995;10(7):638–41. https://doi.org/10.1093/oxfordjournals.humrep.a136147.
8. Raidt J., Werner C., Menchen T.et al. Ciliary function and motor protein composition of Human Fallopian Tubes. Hum Reprod. 2015;30(12):2871– 80. https://doi.org/10.1093/humrep/dev227.
9. Anokhin P.K. Selected works. Cybernetics of functional systems. Ed. K.V. Sudakov. [Izbrannye trudy. Kibernetika funkcional'nyh sistem. Pod red. K.V. Sudakova]. Moscow: Medicina, 1998. 400 p. (In Russ.).
10. Vasques G., Boeckx W., Brosens I. Prospective study of tubal mucosal lesions and fertility in hydrosalpinges. Hum Reprod. 1995;10:1075–8. https://doi.org/10.1093/oxfordjournals.humrep.a136097.
11. Tabolt P., Geiske C., Knoll M. et al. Oocyte pickup by the mаmmalian oviduct. Mol Biol Cеll. 1999;10(1):5–8. https://doi.org/10.1091/mbc.10.1.5.
12. Di Carlantonio G., Shaoulian R., Knoll M. et al. Analysis of ciliary beat frequencies in hamster oviducal explants. J Exp Zool. 1995;272(2):142– 52. https://doi.org/10.1002/jez.1402720208.
13. Leese H.J., Tay J.I., Reischl J., Downing S.J. Formation of Fallopian tubal fluid: role of a neglected epithelium. Reproduction. 2001;121(3):339–46. https://doi.org/10.1530/rep.0.1210339.
14. Saint-Dizier M., Schoen J., Chen S. et al. Composing the early embryonic microenvironment: physiology and regulation of oviductal secretions. Int J Mol Sci. 2020;21(1):223. https://doi.org/10.3390/ijms21010223.
15. Paltieli Y., Eibschitz I., Ziskind G. et al. High progesterone levels and ciliary dysfunction: a possible cause of ectopic pregnancy. J Assist Reprod Genet. 2000;17(2):103–6. https://doi.org/10.1023/a:1009465900824.
16. Abe H., Oikawa T. Observations by scanning electron microscopy of oviductal epithelial cells from cows at follicular and luteal phases. Anat Rec. 1993;235(3):399–410. https://doi.org/10.1002/ar.1092350309.
17. Rozhdestvenskaya A.I. Egg transport from the ovary to the uterus (Motor ability of the human fallopian tube). [O transporte yajca iz yaichnika v matku (Motornaya sposobnost' fallopievoj truby cheloveka)]. Leningrad: tipografiya im. Lohankova, 1947. 71 p. (In Russ.).
18. Schwaiger T. An updated review on hormone replacement therapy for menopausal women. Natural Medicine J. 2020;12(2). Available at: https://www.naturalmedicinejournal.com/journal/2020-02/updated-reviewhormone-replacement-therapy-menopausal-women.
19. Halbert S.A., Becer D.R., Szal S.E. Ovum transport in the rat oviductal ampulla in the absence of muscle contractility. Biol Reprod. 1989;40:1131–6. https://doi.org/10.1095/biolreprod40.6.1131.
20. Becker-Heck A., Loges N.T., Omran H. Dynein dysfunction as a cause of primary ciliary dyskinesia and other ciliopathies. In: Dyneins. Structure, Biology and Disease. Ed. S.M. King. Academic Press: Elsevier, 2012. 602–27.
21. Shirley B., Reeder R.L. Cyclic changes in the ampulla of the rat oviduct. J Exp Zool. 1996;276(2):164–73.
22. Frappart L., Berger G., Bethouart M. et al. L'epithelium tubaire. Microscopie electronique a balayage au cours du cycle menstruel, de la grossesse et de la menopause. J Gynecol Obstet Biol Reprod (Paris). 1980;9(3):307–13.
23. Hagiwara H., Shibasaki S., Ohwada N. Ciliogenesis in the human oviduct epithelium during the normal menstrual cycle. J Electron Microsc (Tokyo). 1992;41(5):321–9.
24. Mahmood T., Saridogan E., Smutna S. et al. The effect of ovarian steroids on epithelial ciliary beat frequency in the human Fallopian tube. Hum Reprod. 1998;13(11):2991–4. https://doi.org/10.1093/humrep/13.11.2991.
25. Saridogan E., Djahanbakhch O., Puddefoot J.R. et al. Angiotensin II receptors and angiotensin II stimulation of ciliary activity in human fallopian tube. J Clin Endocrinol Metab. 1996;81(7):2719–25. https://doi.org/10.1210/jcem.81.7.8675601.
26. Rizos D., V. Maillo V. Lonergan P. Role of the oviduct and oviduct-derived products in ruminant embryo development. Anim Reprod. 2016;13(3):160–7. https://doi.org/10.21451/1984-3143-AR863.
27. Eddy C.A, Pauerstein C.J. Anatomy and physiology of the fallopian tube. Clin Obstet Gynecol. 1980;23(4):1177–93. https://doi.org/10.1097/00003081-198012000-00023.
28. Wollen A.L., Flood P.R., Sandvei R., Steier J.A. Morphological changes in tubal mucosa associated with the use of intrauterine contraceptive devices. Br J Obstet Gynaecol. 1984;91(11):1123–8. https://doi.org/10.1111/j.1471-0528.1984.tb15088.x.
29. Brosens I.A., Vasgues G. Fimbrial microbiopsy. J Reprod Med. 1976;16(4):171–8.
30. Zhao W., Yan M., Li Ch. et al. Levonorgestrel decreases cilia beat frequency of human fallopian tubes and rat oviducts without changing morphological structure. Clin Exp Pharmacol Physiol. 2015;42(2):171–8. https://doi.org/10.1111/1440-1681.12337.
31. Li C., Zhang H.-Y., Liang Y. et al. Effects of Levonorgestrel and progesterone on Oviductal physiology in mammals. Reprod Biol Endocrinol. 2018;16(1):59. https://doi.org/10.1186/s12958-018-0377-3.
32. Talbot P., Lin S. The effect of cigarette smoke on fertilization and pre-implantation development: assessment using animal models, clinical data, and stem cells. Biol Res. 2011;44(2):189–94.
33. Knoll M., Talbot P. Cigarette smoke inhibits oocyte cumulus complex pick-up by the oviduct in vitro independent of ciliary beat frequency. Reprod Toxicol. 1998;12(1):57–68. https://doi.org/10.1016/s0890-6238(97)00100-7.
34. Leng Z., Moore D.E., Mueller B.A. at al. Characterization of ciliary activity in distal Fallopian tube biopsies of women with obstructive tubal infertility. Hum Reprod. 1998;13(11):3121–7. https://doi.org/10.1093/humrep/13.11.3121.
35. Guerri G., Maniscalchi T., Barati S. et al. Syndromic infertility. Acta Biomed. 2019;90(Suppl 10):75–82. https://doi.org/10.23750/abm.v90i10-S.8764.
36. Healy D.L., Trounson A.O., Andersen A.N. Female infertility: course and treatment. Lancet. 1994;343(8912):1539–44. https://doi.org/10.1016/s0140-6736(94)92941-6.
37. Hafner L.M. Pathogenesis of fallopian tube damage caused by Chlamydia trachomatis infections. Contraception. 2015;92(2):108–15. https://doi.org/10.1016/j.contraception.2015.01.004.
38. Torrone E., Papp J., Weinstock H. Prevalence of Chlamydia trachomatis genital infection among persons aged 14–39 years – United States, 2007– 2012. MMWR Morb Mortal Wkly Rep. 2014;63(38):834–8.
39. Geisler W.M. Diagnosis and management of uncomplicated Chlamydia trachomatis infections in adolescents and adults: summary of evidence reviewed for the 2015 Centers for Disease Control and Prevention Sexually Transmitted Diseases Treatment Guidelines. Clin Infect Dis. 2015;61(Suppl 8):S774–S784. https://doi.org/10.1093/cid/civ694.
40. Wyrick P.B. Intracellular survival by Chlamydia. Cell Microbiol. 2000;2(4):275–82. https://doi.org/10.1046/j.1462-5822.2000.00059.x.
41. Patton D.L., Moore D.E., Spadoni L.R. et al. A comparison of the fallopian tube's response to overt and silent salpingitis. Obstet Gynecol. 1989;73(4):622–30.
42. Schuchardt L., Rupp J. Chlamydia trachomatis as the cause of infectious infertility: acute, repetitive or persistent long-term infection? Curr Top Microbiol Immunol. 2016;412:159–80. https://doi.org/10.1007/82_2016_15.
43. Lenz J.D., Dillard J.P. Pathogenesis of Neisseria gonorrhoeae and the host defense in ascending infections of human Fallopian tube. Front Immunol. 2018;9:2710. https://doi.org/10.3389/fimmu.2018.02710.
44. Baczynska A., Funch P., Fedder J. et al. Morphology of human Fallopian tubes after infection With Mycoplasma genitalium and Mycoplasma hominis – in vitro organ culture study. Hum Reprod. 2007;22(4):968–79. https://doi.org/10.1093/humrep/del455.
45. Biolatti B., Pau S., Galloni M. The epithelial pathology of bovine genital tuberculosis. J Comp Pathol. 1989;100(2):137–44. http://doi.org/10.1016/0021-9975(89)90124-2.
46. Ahmadi F., Zafarani F. Shahrzad G. Hysterosalpingographic appearances of female genital tracttuberculosis: Part I. Fallopian tube. Int J Fertil Steril. 2014;7(4):245–52.
47. Chowdhury N.N. Overview of tuberculosis of the female genital tract. J Indian Med Assoc. 1996;94(9):345–6.
48. Kurilo L.F., Lyubashevskaya I.A., Dubinskaya V.P., Gaeva G.N. Karyological analysis of the count of immature germ cells of the ejaculate. [Kariologicheskij analiz sostava nezrelyh polovyh kletok eyakulyata]. Urologiya i nefrologiya. 1993;(2):45–7. (In Russ.).
49. Ajonuma L.C., Ng E.H., Chow P.H. et al. Increased cystic fibrosis transmembrane conductance regulator (CFTR) expression in the human hydrosalpinx. Hum Reprod. 2005;20(5):1228–34. http://doi.org/10.1093/humrep/deh773.
50. He Q., Tsang L.L., Ajonuma L.C., Chan H.C. Abnormally up-regulated cystic fibrosis transmembrane conductance regulator expression and uterine fluid accumulation contribute to Chlamydia trachomatis-induced female infertility. Fertil Steril. 2010;93(8):2608–14. https://doi.org/10.1016/j.fertnstert.2010.01.040.
51. Mansour R.T., Aboulghar M.A., Serour G.I., Riad R. Fluid accumulation of the uterine cavity before embryo transfer: a possible hindrance for implantation. J Vitro Fert Embryo Transfer. 1991;8:157–159. https://doi.org/10.1007/BF01131707.
52. Lyons R.A., Djahanbakhch O., Saridogan E., Naftalin A.A. Peritoneal fluid, endometriosis, and ciliary beat frequency in the human fallopian tube. Lancet. 2002;360(9341):1221–2. https://doi.org/10.1016/S0140-6736(02)11247-5.
53. Reeve L., Lashen H., Pacey A. Endometriosis affects spermendosalpingeal interactions. Hum Reprod. 2005;20(2):448–51. https://doi.org/10.1093/humrep/deh606.
54. Xia W., Zhang D., Ouyang J. et al. Effects of pelvic endometriosis and adenomyosis on ciliary beat frequency and muscular contractions in the human fallopian tube. Reprod Biol Endocrinol. 2018;16(1):48. https://doi.org/10.1186/s12958-018-0361-y.
55. Papathanasiou А., Djahanbakhch O., Saridogan E., Lyons R.A. The effect of interleukin-6 on ciliary beat frequency in the human fallopian tube. Fertil Steril. 2008;90(2):391–4. https://doi.org/10.1016/j.fertnstert.2007.1379.
56. Lyons R.A., Djahanbakhch O., Mahmood T. et al. Fallopian tube ciliary beat frequency in relation to the stage of menstrual cycle and anatomical site. Hum Reprod. 2002;17(3):584–8. https://doi.org/10.1093/humrep/17.3.58457.
57. Polyanskikh L.S., Petrosyan M.A., Morozkina S.N., Baziyan E.V. Current understanding of selective estrogen receptor modulators. [Sovremennye predstavleniya o selektivnyh modulyatorah receptorov estrogenov]. Zhurnal akusherstva i zhenskih boleznej. 2019;68(6):99–106. (In Russ.). https://doi.org/10.17816/VOWD68699-106.
58. Barra F., Romano A., Grandi G. et al. Future directions in endometriosis treatment: discovery and development of novel inhibitors of estrogen biosynthesis. Expert Opin Investig Drugs. 2019;28(6):501–4. https://doi.org/10.1080/13543784.2019.1618269.
59. Sugamata M., Ihara T., Uchiide I. A new therapy for human endometriosis: the therapeutic value of leukotriene receptor antagonist for endometriosis. Open J Obstet Gynecol. 2015;5(6):313–8. https://doi.org/10.4236/ojog.2015.56045.
60. Afzelius B.A. Ciliary structure in health and disease. Аcta Otorhinolaryngol Belg. 2000;54(3):287–91.
61. Zivert A.N. A case of congenital bronchiectasis in a patient with situs inversus. [Sluchaj vrozhdennoj bronxoe`ktazii u bol`nogo s obratny`m raspolozheniem vnutrennostej (situs inversus)]. Russkij vrach. 1902;1(38):1361–2. (In Russ.).
62. Kartagener M. Zur hatogenese der Bronchiektasen. I. Metteilung: Bronchiektasen bei Situs viscerum inversus. Beitr Klein Tuberk. 1933;83:498–501.
63. Raid J., Werner C., Menchen T. et al. Ciliary function and motor protein composition of human fallopian tubes. Hum Reprod. 2015;30(12):2871– 80. https://doi.org/10.1093/humrep/dev227.
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For citations:
Kobylyansky V.I. Mucociliary apparatus of the fallopian tubes and related pathogenetic aspects contributing to infertility and prospects for correction (analytical review). Obstetrics, Gynecology and Reproduction. 2021;15(5):586-598. (In Russ.) https://doi.org/10.17749/2313-7347/ob.gyn.rep.2021.166
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