Epithelial ovarian tumors embryogenesis and function

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Editor-In-Chief: C. Michael Gibson, M.S., M.D. [1]Associate Editor(s)-in-Chief: Hannan Javed, M.D.[2]

Surface epithelium of ovaries

Surface epithelium of ovaries (OSE), once mistakenly referred as germinal epithelium, consists of single layer of flat to cuboidal epithelial cells. It is characterized by keratin types found in simple epithelium and functions in exchange between peritoneal cavity and the ovaries in addition to ovarian cycle.

Embryogenesis

Celomic epithelium → Peritoneal mesothelium surrounding the ovary → Metaplasia to ovarian surface epithelium[1][2]

  • During embryonic development, surface epithelium of ovaries is a part of celomic epithelium.[2]
  • Celomic epithelium itself is derived from mesothelium and forms lining of intraembryonic celom.[2]
  • The future surface epithelium of ovaries then forms part of gonadal blastema and then undergoes a transformation cycle, multilayered papillary epithelium develops from simple flat to cuboidal epithelium but reverts back to simple flat to cuboidal epithelium by term.[2]
  • It is important to note that ovarian surface epithelium is the part of celomic epithelium that overlies the presumptive gonads and the celomic epithelium in proximity of gonads also gives rise to Mullerian (paramesonephric) ducts, that in future will develop into epthelium of most of the female reproductive tract including oviducts, endometrium and a part of cervix.[2][3]
  • Ovarian surface epithelium has also been postulated to give rise or form a part of ovarian granulosa cells during embryonic development.[2][3]

Structural characteristics of ovarian surface epithelium in human adults

Cell type Surface expression Intercellular connection Basement membrane
  • Single layer
  • squamous-to-cuboidal epithelium
  • Keratin
  • Mucin antigen MUC1
  • 17β-hydroxysteroid dehydrogenase
  • Cilia
  • Simple desmosomes
  • Incomplete tight junctions
  • Integrins
  • Cadherins
  • Loosely attached
  • Tunica albuginea that is less conspicuous of its testicular counterpart
  • Keratin types that are expressed by ovarian surface epithelium are characteristic of simple epithelia such as keratin type 7, 8, 18 and 19.[2][4]
  • Catherins expressed by surface epithelium of ovaries may indicate potential for neoplastic transformation as summarized:[2][4][5][6][7]
    • Surface epithelium of ovaries typically express N-cadherin.
    • E-cadherin is typically expressed in regions where cells are columnar.
    • This selective expression of E-cadherin in regions of metaplastic epithelium may indicate propensity for neoplastic transformation.
    • P-catherin, normally absent in adult surface epithelium of ovaries, is expressed in adenocarcinoma of ovaries.

Functions

  • Two most important functions of human surface epithelium of ovaries are its role in transport and exchange between peritoneal cavity and ovaries, and its function in repair and rupture during ovulation.[2][5][8]
  • At present, its role in ovulatory rupture is not well-understood and is controversial. It is hypothesized that it contributes to follicular rupture through production of proteolytic enzymes.[2][5]
  • Epithelial need and ability of proliferation for repair of rupture and ovulatory defects is well-established and is thought to contribute the most in carcinogenesis of ovarian epithelium tumors.[2]
  • Ovarian surface epithelium undergo epithelio-mesenchymal transformation to replace ovarian stroma in ovulatory repair.[2]
  • The differentiation of surface epithelium of ovaries is, however, different from other epithelia because of its ability of differentiate into ectopic epithelium such as that of epithelium formed by Mullerian ducts.[2]

Role of hormones and growth factors on surface epithelium

Gonadotropin-releasing hormone

and gonadotropins[2] [9]

  • Cell proliferation
Epidermal growth factor (EGF)[2] [4][10][11]
  • Cell proliferation and differentiation
  • Increased survival
Steroids[2] [12][13]
  • Decreased expression of GnRH receptors (estrogen)
  • Regulation of hepatocyte growth factor and epidermal growth factor 9estrogen)
  • Decreased expression of Transfroming growth factor β receptors (5α-dihydrotestosterone)
  • May have direct effect on proliferation stimulation
Fibroblast growth factor (FGF)[2] [14]
  • Cell proliferation
  • Increased survival
Platelet-derived growth factor (PDGF)[2] [15]
  • Cell proliferation
Tissue necrosis factor-α (TNF-α)[2] [16][17]
  • Cell proliferation
  • Increased TNFα expression
Transfroming growth factor β (TGF-β)[2] [18]
  • Decreased growth
Hepatocyte growth factor (HGF)[2] [19][20]
  • Decreased cellular adhesion
  • Increased survival and growth
Cytokines[2] [21][22]
  • Regulation of immune response
  • May increase vasculogenesis and survival

References

  1. ↑ Saad AF, Hu W, Sood AK (December 2010). "Microenvironment and pathogenesis of epithelial ovarian cancer". Horm Cancer. 1 (6): 277–90. doi:10.1007/s12672-010-0054-2. PMC 3199131. PMID 21761359.
  2. ↑ 2.00 2.01 2.02 2.03 2.04 2.05 2.06 2.07 2.08 2.09 2.10 2.11 2.12 2.13 2.14 2.15 2.16 2.17 2.18 2.19 2.20 2.21 Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC (April 2001). "Ovarian surface epithelium: biology, endocrinology, and pathology". Endocr. Rev. 22 (2): 255–88. doi:10.1210/edrv.22.2.0422. PMID 11294827.
  3. ↑ 3.0 3.1 Yoshinaga K, Hess DL, Hendrickx AG, Zamboni L (January 1988). "The development of the sexually indifferent gonad in the prosimian, Galago crassicaudatus crassicaudatus". Am. J. Anat. 181 (1): 89–105. doi:10.1002/aja.1001810110. PMID 3348150.
  4. ↑ 4.0 4.1 4.2 Siemens CH, Auersperg N (March 1988). "Serial propagation of human ovarian surface epithelium in tissue culture". J. Cell. Physiol. 134 (3): 347–56. doi:10.1002/jcp.1041340305. PMID 2450877.
  5. ↑ 5.0 5.1 5.2 Kruk PA, Uitto VJ, Firth JD, Dedhar S, Auersperg N (November 1994). "Reciprocal interactions between human ovarian surface epithelial cells and adjacent extracellular matrix". Exp. Cell Res. 215 (1): 97–108. doi:10.1006/excr.1994.1320. PMID 7525326.
  6. ↑ Davies BR, Worsley SD, Ponder BA (January 1998). "Expression of E-cadherin, alpha-catenin and beta-catenin in normal ovarian surface epithelium and epithelial ovarian cancers". Histopathology. 32 (1): 69–80. PMID 9522220.
  7. ↑ Sundfeldt K, Piontkewitz Y, Ivarsson K, Nilsson O, Hellberg P, Brännström M, Janson PO, Enerback S, Hedin L (June 1997). "E-cadherin expression in human epithelial ovarian cancer and normal ovary". Int. J. Cancer. 74 (3): 275–80. PMID 9221804.
  8. ↑ Osterholzer HO, Streibel EJ, Nicosia SV (August 1985). "Growth effects of protein hormones on cultured rabbit ovarian surface epithelial cells". Biol. Reprod. 33 (1): 247–58. PMID 3933584.
  9. ↑ Davies BR, Finnigan DS, Smith SK, Ponder BA (April 1999). "Administration of gonadotropins stimulates proliferation of normal mouse ovarian surface epithelium". Gynecol. Endocrinol. 13 (2): 75–81. PMID 10399050.
  10. ↑ Rodriguez GC, Berchuck A, Whitaker RS, Schlossman D, Clarke-Pearson DL, Bast RC (March 1991). "Epidermal growth factor receptor expression in normal ovarian epithelium and ovarian cancer. II. Relationship between receptor expression and response to epidermal growth factor". Am. J. Obstet. Gynecol. 164 (3): 745–50. PMID 2003535.
  11. ↑ Evangelou A, Jindal SK, Brown TJ, Letarte M (February 2000). "Down-regulation of transforming growth factor beta receptors by androgen in ovarian cancer cells". Cancer Res. 60 (4): 929–35. PMID 10706107.
  12. ↑ Kang SK, Choi KC, Tai CJ, Auersperg N, Leung PC (February 2001). "Estradiol regulates gonadotropin-releasing hormone (GnRH) and its receptor gene expression and antagonizes the growth inhibitory effects of GnRH in human ovarian surface epithelial and ovarian cancer cells". Endocrinology. 142 (2): 580–8. doi:10.1210/endo.142.2.7982. PMID 11159828.
  13. ↑ Liu Y, Lin L, Zarnegar R (September 1994). "Modulation of hepatocyte growth factor gene expression by estrogen in mouse ovary". Mol. Cell. Endocrinol. 104 (2): 173–81. PMID 7988745.
  14. ↑ Basilico C, Moscatelli D (1992). "The FGF family of growth factors and oncogenes". Adv. Cancer Res. 59: 115–65. PMID 1381547.
  15. ↑ Dabrow MB, Francesco MR, McBrearty FX, Caradonna S (October 1998). "The effects of platelet-derived growth factor and receptor on normal and neoplastic human ovarian surface epithelium". Gynecol. Oncol. 71 (1): 29–37. doi:10.1006/gyno.1998.5121. PMID 9784315.
  16. ↑ Wu S, Rodabaugh K, Martinez-Maza O, Watson JM, Silberstein DS, Boyer CM, Peters WP, Weinberg JB, Berek JS, Bast RC (March 1992). "Stimulation of ovarian tumor cell proliferation with monocyte products including interleukin-1, interleukin-6, and tumor necrosis factor-alpha". Am. J. Obstet. Gynecol. 166 (3): 997–1007. PMID 1550178.
  17. ↑ Wu S, Boyer CM, Whitaker RS, Berchuck A, Wiener JR, Weinberg JB, Bast RC (April 1993). "Tumor necrosis factor alpha as an autocrine and paracrine growth factor for ovarian cancer: monokine induction of tumor cell proliferation and tumor necrosis factor alpha expression". Cancer Res. 53 (8): 1939–44. PMID 8385577.
  18. ↑ Berchuck A, Rodriguez G, Olt G, Whitaker R, Boente MP, Arrick BA, Clarke-Pearson DL, Bast RC (February 1992). "Regulation of growth of normal ovarian epithelial cells and ovarian cancer cell lines by transforming growth factor-beta". Am. J. Obstet. Gynecol. 166 (2): 676–84. PMID 1536252.
  19. ↑ Parrott JA, Skinner MK (March 2000). "Expression and action of hepatocyte growth factor in human and bovine normal ovarian surface epithelium and ovarian cancer". Biol. Reprod. 62 (3): 491–500. PMID 10684788.
  20. ↑ Gulati R, Peluso JJ (May 1997). "Opposing actions of hepatocyte growth factor and basic fibroblast growth factor on cell contact, intracellular free calcium levels, and rat ovarian surface epithelial cell viability". Endocrinology. 138 (5): 1847–56. doi:10.1210/endo.138.5.5137. PMID 9112378.
  21. ↑ Ziltener HJ, Maines-Bandiera S, Schrader JW, Auersperg N (September 1993). "Secretion of bioactive interleukin-1, interleukin-6, and colony-stimulating factors by human ovarian surface epithelium". Biol. Reprod. 49 (3): 635–41. PMID 7691194.
  22. ↑ Marth C, Zeimet AG, Herold M, Brumm C, Windbichler G, Müller-Holzner E, Offner F, Feichtinger H, Zwierzina H, Daxenbichler G (September 1996). "Different effects of interferons, interleukin-1beta and tumor necrosis factor-alpha in normal (OSE) and malignant human ovarian epithelial cells". Int. J. Cancer. 67 (6): 826–30. doi:10.1002/(SICI)1097-0215(19960917)67:6<826::AID-IJC12>3.0.CO;2-#. PMID 8824555.
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