Histological structure and functional properties of the tunica albuginea of the ovary

Yıl 2025, Cilt: 18 Sayı: 2, 20 - 20

Hale Yetgin , Murat Serkant Ünal , Cihan Kabukçu , Ahmet Çevik Tufan

https://doi.org/10.31362/patd.1467619

Öz

Just below the surface epithelium of the ovary is the tunica albuginea, which is a tight irregular connective tissue structure that gives the tissue its white color and contains fibroblast cells. Tunica albuginea, which is more resistant to environmental factors, contains fewer cells and is rich in collagen fibers, is observed as the niche of preantral follicles. It has been observed that fibroblasts forming collagen fibers provide the development of follicles with the paracrine factors and cytokines they secrete and function as a nourishing cell layer. After the graaf follicle forms the corpus luteum, fibroblasts in the adjacent tunica albuginea proliferate and the thickness of this structure increases. The tunica albuginea undergoes frequent renewal due to the corpus luteum structures formed in rats. When the corpus luteum is formed, new capillaries and venules are formed in the adjacent tunica albuginea. This structure may be a suitable model for investigating the migration of cells from the bone marrow to the ovary via vessels. It can be suggested that mesenchymal cells and very small embryonic-like stem cells (VSELs), which show pluripotent stem cell characteristics, may migrate from the bone marrow to the tunica albuginea through vascular structures and that the bone marrow may be the source of these cells, which have been previously shown to be present in the ovary. The aim of this review is to examine the effects of the tunica albuginea on the development of follicles and the dynamic structure of the ovary.

Anahtar Kelimeler

Ovary, tunica albuginea, collagen fibers, follicle, corpus luteum

Ovaryum tunika albugineasının histolojik yapısı ve fonksiyonel özellikleri

Öz

Ovaryumda yüzey epitelinin hemen altında dokuya beyaz rengini veren, sıkı düzensiz bir bağ doku yapısında olan ve içinde fibroblast hücrelerini içeren tunika albuginea bulunur. Çevresel etkenlere daha dirençli olan, az sayıda hücre içeren ve kollajen liflerden zengin olan tunika albuginea preantral foliküllerin nişi olarak gözlenmektedir. Kollajen lifleri oluşturan fibroblastların salgıladıkları parakrin faktörlerle ve sitokinlerle foliküllerin gelişimlerini sağladıkları ve besleyici hücre tabakası gibi fonksiyon gördükleri izlenmiştir. Graaf folikülün korpus luteumu oluşturmasından sonra ise hemen bitişiğindeki tunika albugineadaki fibroblastların prolifere olduğu ve bu yapının kalınlığının arttığı izlenmiştir. Ratlarda oluşan korpus luteum yapıları nedeniyle tunika albuginea sık sık yenilenmeye uğramaktadır. Korpus luteum oluştuğu zaman bitişiğindeki tunika albugineada yeni kapillerler ve venüller meydana gelmektedir. Bu yapı; hücrelerin kemik iliğinden, damarlarla ovaryuma migrasyonlarının araştırılması için uygun bir model olabilir. Mezenkimal hücrelerin ve pluripotent kök hücre özelliği gösteren çok küçük embriyonik benzeri kök hücrelerin (VSELs) vasküler yapılar aracılığıyla kemik iliğinden tunika albugineaya gelebileceği ve ovaryumda bulundukları daha önce gösterilen bu hücrelerin kaynağının kemik iliği olabileceği ileri sürülebilir. Bu derlemedeki amacımız tunika albugineanın foliküllerin gelişimine ve ovaryumun dinamik yapısı üzerine olan etkilerini incelemektir.

Anahtar Kelimeler

Ovaryum, tunika albuginea, kollajen lifler, folikül, korpus luteum

Kaynakça

• 1. Özgünen T, Polat S, Balcıoğlu E. Güncel Fizyoloji Histoloji Embriyoloji Çalışmaları,Ovaryum Histolojisi, Ankara: Akademisyen Kitabevi, 2019;113-124. Available at: https://books.akademisyen.net/index.php/akya/catalog/view/1223/1226/26056. Accessed January 22, 2024
• 2. Menter DG, Dubois RN. Prostaglandins in cancer cell adhesion, migration, and invasion. Int J Cell Biol 2012;2012:723419. https://doi.org/10.1155/2012/723419
• 3. Ünal MS, Seçme M. Ovaryum yüzey epiteli primordial folikül ve primer folikül öncüsü yapılara farklılaşıyor mu? Cukurova Med J 2022;47:1256-1262. https://doi.org/10.17826/cumj.1134852
• 4. Hartanti MD, Hummitzsch K, Bonner WM, Bastian NA, Irving Rodgers HF, Rodgers RJ. Formation of the bovine ovarian surface epithelium during fetal development. J Histochem Cytochem 2020;68:113-126. https://doi.org/10.1369/0022155419896797
• 5. Rajah R, Glaser EM, Hirshfield AN. The changing architecture of the neonatal rat ovary during histogenesis. Dev Dyn 1992;194:177-192. https://doi.org/10.1002/aja.1001940303
• 6. Philippart C, Masciangelo R, Camboni A, Donnez J, Dolmans MM. Basal lamina characterization in frozen-thawed and long-term grafted human prepubertal ovarian tissue. Reprod Biomed Online 2021;42:859-869. https://doi.org/10.1016/j.rbmo.2021.02.012
• 7. Kinnear HM, Tomaszewski CE, Chang FL, et al. The ovarian stroma as a new frontier. Reproduction 2020;160:25-39. https://doi.org/10.1530/REP-19-0501
• 8. Orisaka M, Tajima K, Mizutani T, et al. Granulosa cells promote differentiation of cortical stromal cells into theca cells in the bovine ovary. Biol Reprod 2006;75:734-740. https://doi.org/10.1095/biolreprod.105.050344
• 9. Orisaka M, Tajima K, Tsang BK, Kotsuji F. Oocyte-granulosa-theca cell interactions during preantral follicular development. J Ovarian Res 2009;2:9. https://doi.org/10.1186/1757-2215-2-9
• 10. Jokela H, Lokka E, Kiviranta M, et al. Fetal-derived macrophages persist and sequentially maturate in ovaries after birth in mice. Eur J Immunol 2020;50:1500-1514. https://doi.org/10.1002/eji.202048531
• 11. Umehara T, Winstanley YE, Andreas E, et al. Female reproductive life span is extended by targeted removal of fibrotic collagen from the mouse ovary. Sci Adv 2022;8:eabn4564. https://doi.org/10.1126/sciadv.abn4564
• 12. Hen G, Sela Donenfeld D. “A narrow bridge home”: the dorsal mesentery in primordial germ cell migration. Semin Cell Dev Biol 2019;92:97-104. https://doi.org/10.1016/j.semcdb.2018.08.010
• 13. Himelreich Perić M, Takahashi M, Ježek D, Cunha GR. Early development of the human embryonic testis. Differentiation 2023;129:4-16. https://doi.org/10.1016/j.diff.2022.07.001
• 14. Xu X, Mu L, Li L, et al. Imaging and tracing the pattern of adult ovarian angiogenesis implies a strategy against female reproductive aging. Sci Adv 2022;8:eabi8683. https://doi.org/10.1126/sciadv.abi8683
• 15. Overland MR, Li Y, Derpinghaus A, et al. Development of the human ovary: fetal through pubertal ovarian morphology, folliculogenesis and expression of cellular differentiation markers. Differentiation 2023;129:37-59. https://doi.org/10.1016/j.diff.2022.10.005
• 16. Hummitzsch K, Irving Rodgers H, Schwartz J, Rodgers RJ. Development of the Mammalian Ovary and Follicles. The Ovary 2019:71-82. https://doi.org/10.1016/B978-0-12-813209-8.00004-2
• 17. Sawyer HR, Smith P, Heath DA, Juengel JL, Wakefield SJ, McNatty KP. Formation of ovarian follicles during fetal development in sheep. Biol Reprod 2002;66:1134- 1150. https://doi.org/10.1095/biolreprod66.4.1134
• 18. Islam MR, Ichii O, Nakamura T, et al. Developmental changes of the ovary in neonatal cotton rat (Sigmodon hispidu s). Front Physiol 2021;11:601927. https://doi.org/10.3389/fphys.2020.601927
• 19. Brieno Enríquez MA, Faykoo Martinez M, Goben M, et al. Postnatal oogenesis leads to an exceptionally large ovarian reserve in naked mole-rats. Nat Commun 2023;14:670. https://doi.org/10.1038/s41467-023-36284-8
• 20. McKey J, Anbarci DN, Bunce C, Ontiveros AE, Behringer RR, Capel B. Integration of mouse ovary morphogenesis with developmental dynamics of the oviduct, ovarian ligaments, and rete ovarii. Elife 2022;11:e81088. https://doi.org/10.7554/eLife.81088
• 21. Virant Klun I. Postnatal oogenesis in humans: a review of recent findings. Stem Cells Cloning 2015;8:49-60. https://doi.org/10.2147/SCCAA.S32650
• 22. Ernst LM, Ruchelli ED, Carreon CK, Huff DS. Color Atlas of human fetal and neonatal histology. Switzerland: 2nd Ed, Springer Nature, 2019; 175-176. Available at https://books.google.com.tr/books?id=3WOsDwAAQBAJ&pg=PA105&hl=tr&source=gbs_toc_r&cad=2#v=onepage&q&f=false. Accessed February 2, 2024
• 23. Chandra PK, Atala AA. Genitourinary System. Reference Module in Biomedical Sciences Encyclopedia of Tissue Engineering and Regenerative Medicine 2019;361-379. https://doi.org/10.1016/B978-0-12-801238-3.65846-4
• 24. Heeren AM, Van Iperen L, Klootwijk DB, et al. Development of the follicular basement membrane during human gametogenesis and early folliculogenesis. BMC Dev Biol 2015;15:4. https://doi.org/10.1186/s12861-015-0054-0
• 25. Tullington JE, Blecker N. Pelvic Trauma. StatPearls Publishing, 2023.
• 26. Middendorff R, Müller D, Mewe M, Mukhopadhyay AK, Holstein AF, Davidoff MS. The tunica albuginea of the human testis is characterized by complex contraction and relaxation activities regulated by cyclic GMP. J Clin Endocrinol Metab 2002;87:3486-3499. https://doi.org/10.1210/jcem.87.7.8696
• 27. Raad G, Massaad V, Serdarogullari M, et al. Functional histology of human scrotal wall layers and their overlooked relation with infertility: a narrative review. Int J Impot Res 2023;35:428-438. https://doi.org/10.1038/s41443-022-00573-5
• 28. Bukovsky A, Caudle MR, Svetlikova M, Upadhyaya NB. Origin of germ cells and formation of new primary follicles in adult human ovaries. Reprod Biol Endocrinol 2004;2:20. https://doi.org/10.1186/1477-7827-2-20
• 29. Nistal M, Paniagua R. Urologic Surgical Pathology. Saunders, 2nd ed, 2008; 614-755. https://doi.org/10.1016/B978-0-323-01970-5.50014-2 Available at: https://www.sciencedirect.com/science/article/pii/B9780323019705500142. Accessed March 11, 2024
• 30. Ferré Pujol P, Otsuki J, Funahashi H, Nakatsuka M. The thickness and density of the ovarian tunica albuginea increases with age in transgender patients. Reprod Sci 2021;28:1339-1346. https://doi.org/10.1007/s43032-020-00390-5
• 31. Ross MH, Pawlina W, Histoloji Konu Anlatımı ve Atlas 6.ed, Ankara: Lippincott Williams & Wilkins, 2013;837-839. 32. Della Corte L, Boccia D, Palumbo M, et al. Is there still a place for surgery in patients with PCOS? A review. Life (Basel) 2023;13:1270. https://doi.org/10.3390/life13061270
• 33. Lind AK, Weijdegård B, Dahm Kähler P, Mölne J, Sundfeldt K, Brännström M. Collagens in the human ovary and their changes in the perifollicular stroma during ovulation. Acta Obstet Gynecol Scand 2006;85:1476-1484. https://doi.org/10.1080/00016340601033741
• 34. Postawski K, Rechberger T, Skorupski P, Jakowicki JA. Extracellular matrix remodelling within the normal human ovarian capsule. Eur J Obstet Gynecol Reprod Biol 1996;67:173-177. https://doi.org/10.1016/0301-2115(96)02468-2
• 35. Bogusiewicz M, Rechberger T, Jakimiuk AJ, Skorupski P, Jakowicki JA, Postawski K. Evaluation of matrix metalloproteinases-1 and -3 concentrations in the tunica albuginea, the apical wall of atretic follicles and the corpus luteum of normal human ovaries. Gynecol Endocrinol 2000;14:25-31. https://doi.org/10.3109/09513590009167656
• 36. Murdoch WJ, McDonnel AC. Roles of the ovarian surface epithelium in ovulation and carcinogenesis. Reproduction 2002;123:743-750. https://doi.org/10.1530/rep.0.1230743
• 37. Piccinno M, Zupa R, Corriero A, et al. In vitro effect of isotocin on ovarian tunica albuginea contractility of gilthead seabream (Sparus aurata L.) in different reproductive conditions. Fish Physiol Biochem 2014;40:1191-1199. https://doi.org/10.1007/s10695-014-9915-x
• 38. Hummitzsch K, Hatzirodos N, Macpherson AM, Schwartz J, Rodgers RJ, Irving Rodgers HF. Transcriptome analyses of ovarian stroma: tunica albuginea, interstitium and theca interna. Reproduction 2019;157:545-565. https://doi.org/10.1530/REP-18-0323
• 39. Bukovsky A, Caudle MR, Svetlikova M, Wimalasena J, Ayala ME, Dominguez R. Oogenesis in adult mammals, including humans: a review. Endocrine 2005;26:301-316. https://doi.org/10.1385/ENDO:26:3:301
• 40. Bukovsky A, Svetlikova M, Caudle MR. Oogenesis in cultures derived from adult human ovaries. Reprod Biol Endocrinol 2005;3:17. https://doi.org/10.1186/1477-7827-3-17
• 41. Çil N, Abban Mete G. The effect of adipose-derived mesenchymal stem cell treatment on mTOR and p-mTOR expression in ovarian damage due to cyclophosphomide. Reprod Toxicol 2021;103:71-78. https://doi.org/10.1016/j.reprotox.2021.06.003
• 42. Kabasakal G, Tural E, Ünal MS. Deneysel overyan yetmezliklerde mezenkimal kök hücrelerin ovaryum dokusuna etkisi. Kocatepe Tıp Dergisi 2023;24:249-253. https://doi.org/10.18229/kocatepetip.849512
• 43. Ünal MS, Tan S, Seçme M. Changes in structure during the corpus luteum’s formation. Pamukkale Med J 2024;17:285-301. https://doi.org/10.31362/patd.1383988