Have a personal or library account? Click to login
Follicular renewal and stemness potency of follicular cells depended of telomerase activity and TERT expression – short review Cover

Follicular renewal and stemness potency of follicular cells depended of telomerase activity and TERT expression – short review

Open Access
|Apr 2022

References

  1. 1. Johnson J, Canning J, Kaneko T, Pru JK, Tilly JL. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature. 2004;428(6979):145–50; DOI:10.1038/NATURE02316.10.1038/nature02316
  2. 2. Woods DC, Tilly JL. Isolation, characterization and propagation of mitotically active germ cells from adult mouse and human ovaries. Nat Protoc. 2013;8(5):966–88; DOI:10.1038/NPROT.2013.047.10.1038/nprot.2013.047
  3. 3. OB O, AM M, D O. Ovarian stem cells: from basic to clinical applications. World J Stem Cells. 2015;7(4):757; DOI:10.4252/WJSC.V7.I4.757.10.4252/wjsc.v7.i4.757
  4. 4. Nikolic A, Volarevic V, Armstrong L, Lako M, Stojkovic M. Primordial germ cells: current knowledge and perspectives. Stem Cells Int. 2016;2016: 1741072; DOI:10.1155/2016/1741072.10.1155/2016/1741072
  5. 5. Baker TG, Wai Sum O. Development of the ovary and oogenesis. Clin Obstet Gynaecol. 1976;3(1):3–26; DOI:10.1016/s0306-3356(21)00330-7.10.1016/S0306-3356(21)00330-7
  6. 6. Dansereau DA, Lasko P. The development of germline stem cells in Drosophila. Methods Mol Biol. 2008;450:3; DOI:10.1007/978-1-60327-214-8_1.10.1007/978-1-60327-214-8_1
  7. 7. Wylie C. Germ Cells. Cell. 1999;96(2):165–74; DOI:10.1016/S0092-8674(00)80557-7.10.1016/S0092-8674(00)80557-7
  8. 8. Xie T, Spradling AC. A niche maintaining germ line stem cells in the Drosophila ovary. Science. 2000;290(5490):328–30; DOI:10.1126/SCIENCE.290.5490.328.10.1126/science.290.5490.32811030649
  9. 9. Nakamura S, Kobayashi K, Nishimura T, Higashijima SI, Tanaka M. Identification of germline stem cells in the ovary of the teleost medaka. Science. 2010;328(5985):1561–3; DOI:10.1126/SCIENCE.1185473.10.1126/science.118547320488987
  10. 10. Draper BW, McCallum CM, Moens CB. nanos1 is required to maintain oocyte production in adult zebrafish. Dev Biol. 2007;305(2):589; DOI:10.1016/J.YDBIO.2007.03.007.10.1016/j.ydbio.2007.03.007198672617418113
  11. 11. Kim J, Hyun M, Hibi M, You YJ. Maintenance of quiescent oocytes by noradrenergic signals. Nat Commun 2021 121. 2021;12(1):1–14; DOI:10.1038/s41467-021-26945-x.10.1038/s41467-021-26945-x862643834836956
  12. 12. Crane AM, Bhattacharya SK. The use of bromodeoxyuridine incorporation assays to assess corneal stem cell proliferation. Methods Mol Biol. 2013;1014:65–70; DOI:10.1007/978-1-62703-432-6_4.10.1007/978-1-62703-432-6_423690005
  13. 13. Birbrair A. Stem cells heterogeneity. Adv Exp Med Biol. 2019;1123:1–3; DOI:10.1007/978-3-030-11096-3_1.10.1007/978-3-030-11096-3_131016591
  14. 14. Shamsudeen S, Mahdy H. Granulosa theca cell cancer. Treasure Island:StatPearls; 2022. 8 p.
  15. 15. Auersperg N, Wong AST, Choi K-C, Kang SK, Leung PCK. Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr Rev. 2001;22(2):255–88; DOI:10.1210/EDRV.22.2.0422.10.1210/edrv.22.2.042211294827
  16. 16. Bast RC, Hennessy B, Mills GB. The biology of ovarian cancer: new opportunities for translation. Nat Rev Cancer. 2009;9(6):415; DOI:10.1038/NRC2644.10.1038/nrc2644281429919461667
  17. 17. Tudrej P, Kujawa KA, Cortez AJ, Lisowska KM. Characteristics of in vitro model systems for ovarian cancer studies. Oncol Clin Pract. 2019;15(5):246–59; DOI:10.5603/OCP.2019.0024.10.5603/OCP.2019.0024
  18. 18. Kossaï M, Leary A, Scoazec JY, Genestie C. Ovarian cancer: a heterogeneous disease. pathobiology. 2018;85(1–2):41–9; DOI:10.1159/000479006.10.1159/00047900629020678
  19. 19. Riva F, Omes C, Bassani R, Nappi RE, Mazzini G, Icaro Cornaglia A, Casasco A. In-vitro culture system for mesenchymal progenitor cells derived from waste human ovarian follicular fluid. Reprod Biomed Online. 2014;29(4):457–69; DOI:10.1016/J.RBMO.2014.06.006.10.1016/j.rbmo.2014.06.00625131558
  20. 20. Dzafic E, Stimpfel M, Novakovic S, Cerkovnik P, Virant-Klun I. Expression of mesenchymal stem cells-related genes and plasticity of aspirated follicular cells obtained from infertile women. Biomed Res Int. 2014;2014; DOI:10.1155/2014/508216.10.1155/2014/508216395878424724084
  21. 21. Kossowska-Tomaszczuk K, De Geyter C, De Geyter M, Martin I, Holzgreve W, Scherberich A, Zhang H. The multipotency of luteinizing granulosa cells collected from mature ovarian follicles. Stem Cells. 2009;27(1):210–9; DOI:10.1634/STEMCELLS.2008-0233.10.1634/stemcells.2008-023319224509
  22. 22. Riva F, Omes C, Bassani R, Nappi RE, Mazzini G, Icaro Cornaglia A, Casasco A. In-vitro culture system for mesenchymal progenitor cells derived from waste human ovarian follicular fluid. Reprod Biomed Online. 2014;29(4):457–69; DOI:10.1016/J.RBMO.2014.06.006.10.1016/j.rbmo.2014.06.00625131558
  23. 23. Simon LE, Rajendra Kumar T, Duncan FE. In vitro ovarian follicle growth: a comprehensive analysis of key protocol variables. Biol Reprod. 2020;103(3):455; DOI:10.1093/BIOLRE/IOAA073.10.1093/biolre/ioaa073744277732406908
  24. 24. Kossowska-Tomaszczuk K, De Geyter C, De Geyter M, Martin I, Holzgreve W, Scherberich A, Zhang H. The multipotency of luteinizing granulosa cells collected from mature ovarian follicles. Stem Cells. 2009;27(1):210–9; DOI:10.1634/STEMCELLS.2008-0233.10.1634/stemcells.2008-023319224509
  25. 25. Kossowska-Tomaszczuk K, De Geyter C. Cells with stem cell characteristics in somatic compartments of the ovary. Biomed Res Int. 2013;2013; DOI:10.1155/2013/310859.10.1155/2013/310859359121723484108
  26. 26. Varras M, Griva T, Kalles V, Akrivis C, Paparisteidis N. Markers of stem cells in human ovarian granulosa cells: is there a clinical significance in ART? J Ovarian Res. 2012;5(1); DOI:10.1186/1757-2215-5-36.10.1186/1757-2215-5-36353659423164047
  27. 27. Mattioli M, Gloria A, Turriani M, Berardinelli P, Russo V, Nardinocchi D, Curini V, Baratta M, Martignani E, Barboni B. Osteo-regenerative potential of ovarian granulosa cells: an in vitro and in vivo study. Theriogenology. 2012;77(7):1425–37; DOI:10.1016/J.THERIOGENOLOGY.2011.11.008.10.1016/j.theriogenology.2011.11.00822284224
  28. 28. Brązert M, Kranc W, Celichowski P, Jankowski M, Piotrowska-Kempisty H, Pawelczyk L, Bruska M, Zabel M, Nowicki M, Kempisty B. Expression of genes involved in neurogenesis, and neuronal precursor cell proliferation and development: Novel pathways of human ovarian granulosa cell differentiation and transdifferentiation capability in vitro. Mol Med Rep. 2020;21(4):1749–60; DOI:10.3892/mmr.2020.10972.10.3892/mmr.2020.10972705778132319615
  29. 29. Brązert M, Kranc W, Celichowski P, Ożegowska K, Budna-Tukan J, Jeseta M, Pawelczyk L, Bruska M, Zabel M, Nowicki M, Kempisty B. Novel markers of human ovarian granulosa cell differentiation toward osteoblast lineage: a microarray approach. Mol Med Rep. 2019;20(5):4403–14; DOI:10.3892/MMR.2019.10709.10.3892/mmr.2019.10709679795731702034
  30. 30. Hoang SN, Ho CNQ, Nguyen TTP, Doan CC, Tran DH, Le LT. Evaluation of stemness marker expression in bovine ovarian granulosa cells. Anim Reprod. 2019;16(2):277–81; DOI:10.21451/1984-3143-AR2018-0083.10.21451/1984-3143-AR2018-0083767359633224287
  31. 31. Stefańska K, Sibiak R, Hutchings G, Dompe C, Moncrieff L, Janowicz K, Jeseta M, Kempisty B, Machatkova M, Mozdziak P. Evidence for existence of molecular stemness markers in porcine ovarian follicular granulosa cells. Med J Cell Biol. 2019; DOI:10.2478/acb-2019-0025.10.2478/acb-2019-0025
  32. 32. Parte S, Bhartiya D, Telang J, Daithankar V, Salvi V, Zaveri K, Hinduja I. Detection, characterization, and spontaneous differentiation in vitro of very small embryonic-like putative stem cells in adult mammalian ovary. Stem Cells Dev. 2011;20(8):1451–64; DOI:10.1089/SCD.2010.0461.10.1089/scd.2010.0461314882921291304
  33. 33. 33. Parte S, Patel H, Sriraman K, Bhartiya D. Isolation and characterization of stem cells in the adult mammalian ovary. Methods Mol Biol. 2015;1235:203–29; DOI:10.1007/978-1-4939-1785-3_16.10.1007/978-1-4939-1785-3_1625388396
  34. 34. Woods DC, White YAR, Niikura Y, Kiatpongsan S, Lee HJ, Tilly JL. Embryonic stem cell-derived granulosa cells participate in ovarian follicle formation in vitro and in vivo. Reprod Sci. 2013;20(5):524–35; DOI:10.1177/1933719113483017.10.1177/1933719113483017363506823536570
  35. 35. Virant-Klun I, Skutella T, Stimpfel M, Sinkovec J. Ovarian surface epithelium in patients with severe ovarian infertility: a potential source of cells expressing markers of pluripotent/multipotent stem cells. J Biomed Biotechnol. 2011;2011; DOI:10.1155/2011/381928.10.1155/2011/381928323701722187524
  36. 36. Bukovsky A, Svetlikova M, Caudle MR. Oogenesis in cultures derived from adult human ovaries. Reprod Biol Endocrinol. 2005;3(1):1–13; DOI:10.1186/1477-7827-3-17/COMMENTS.
  37. 37. Virant-Klun I, Skutella T, Hren M, Gruden K, Cvjeticanin B, Vogler A, Sinkovec J. Isolation of small SSEA-4-positive putative stem cells from the ovarian surface epithelium of adult human ovaries by two different methods. Biomed Res Int. 2013;2013; DOI:10.1155/2013/690415.10.1155/2013/690415359061423509763
  38. 38. Virant-Klun I, Zech N, Rzǒman P, Vogler A, Cvjetičanin B, Klemenc P, Maličev E, Meden-Vrtovec H. Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes. Differentiation. 2008;76(8):843–56; DOI:10.1111/J.1432-0436.2008.00268.X.10.1111/j.1432-0436.2008.00268.x18452550
  39. 39. Rungsiwiwut R, Numchaisrika P, Thuwanut P, Pruksananonda K. Characterization of stem cells from human ovarian follicular fluid; a potential source of autologous stem cell for cell-based therapy. Hum Cell. 2021;34(2):300–9; DOI:10.1007/s13577-020-00439-2.10.1007/s13577-020-00439-233543452
  40. 40. Dompe C, Kulus M, Stefańska K, Kranc W, Chermuła B, Bryl R, Pieńkowski W, Nawrocki MJ, Petitte JN, Stelmach B, Mozdziak P, Jeseta M, Pawelczyk L, Jaśkowski JM, Piotrowska-Kempisty H, Spaczyński RZ, Nowicki M, Kempisty B. Human granulosa cells—stemness properties, molecular cross-talk and follicular angiogenesis. Cells. 2021;10(6); DOI:10.3390/cells10061396.10.3390/cells10061396822987834198768
  41. 41. Fàbregues F, Ferreri J, Méndez M, Calafell JM, Otero J, Farré R. In Vitro Follicular Activation and Stem Cell Therapy as a Novel Treatment Strategies in Diminished Ovarian Reserve and Primary Ovarian Insufficiency. Front Endocrinol (Lausanne). 2021;11:1135; DOI:10.3389/FENDO.2020.617704/BIBTEX.
  42. 42. Szczepańska MA, Jagodziński PP, Wender-Ożegowska E. The effect of endometrioma on ovarian reserve. J Med Sci. 2017;86(3):237–9; DOI:10.20883/JMS.2017.201.10.20883/jms.2017.201
  43. 43. Rasool S, Shah D. Fertility with early reduction of ovarian reserve: the last straw that breaks the Camel’s back. Fertil Res Pract 2017 31. 2017;3(1):1–12; DOI:10.1186/S40738-017-0041-1.10.1186/s40738-017-0041-1563724929046817
  44. 44. 44. Blackburn EH, Collins K. Telomerase: an RNP enzyme synthesizes DNA. Cold Spring Harb Perspect Biol. 2011;3(5):1–9; DOI:10.1101/CSHPERSPECT.A003558.10.1101/cshperspect.a003558310184820660025
  45. 45. Jiang J, Wang Y, Sušac L, Chan H, Basu R, Zhou ZH, Feigon J. Structure of telomerase with telomeric DNA. cell. 2018;173(5):1179-1190; DOI:10.1016/J.CELL.2018.04.038.10.1016/j.cell.2018.04.038599558329775593
  46. 46. Celtikci B, Erkmen GK, Dikmen ZG. Regulation and Effect of Telomerase and Telomeric Length in Stem Cells. Curr Stem Cell Res Ther. 2020;16(7):809–23; DOI:10.2174/1574888x15666200422104423.10.2174/1574888X1566620042210442332321410
  47. 47. Hiyama E, Hiyama K. Telomere and telomerase in stem cells. Br J Cancer. 2007;96(7):1020–4; DOI:10.1038/SJ.BJC.6603671.10.1038/sj.bjc.6603671236012717353922
  48. 48. Mondello C, Zongaro S. Telomerase expression in somatic Cells: fountain of youth or Damocles’ sword? Cell Cycle. 2006;5(5):465–6; DOI:10.4161/cc.5.5.2499.10.4161/cc.5.5.249916481747
  49. 49. Shay JW, Wright WE. Telomeres and telomerase: three decades of progress. Nat Rev Genet 2019 205. 2019;20(5):299–309; DOI:10.1038/s41576-019-0099-1.10.1038/s41576-019-0099-130760854
  50. 50. Kosebent EG, Uysal F, Ozturk S. Telomere length and telomerase activity during folliculogenesis in mammals. J Reprod Dev. 2018;64(6):477–84; DOI:10.1262/jrd.2018-076.10.1262/jrd.2018-076630584730270279
  51. 51. Lavranos TC, Mathis JM, Latham SE, Kalionis B, Shay JW, Rodgers RJ. Evidence for ovarian granulosa stem cells: telomerase activity and localization of the telomerase ribonucleic acid component in bovine ovarian follicles. Biol Reprod. 1999;61(2):358–66; DOI:10.1095/BIOLREPROD61.2.358.10.1095/biolreprod61.2.35810411512
  52. 52. Russo V, Berardinelli P, Martelli A, Di Giacinto O, Nardinocchi D, Fantasia D, Barboni B. Expression of telomerase reverse transcriptase subunit (TERT) and telomere sizing in pig ovarian follicles. J Histochem Cytochem. 2006;54(4):443–55; DOI:10.1369/JHC.4A6603.2006.10.1369/jhc.4A6603.200616400001
  53. 53. Tománek M, Chronowska E, Kott T, Czerneková V. Telomerase activity in pig granulosa cells proliferating and differentiating in vitro. Anim Reprod Sci. 2008;104(2–4):284–98; DOI:10.1016/J.ANIREPROSCI.2007.02.003.10.1016/j.anireprosci.2007.02.00317363198
  54. 54. Liu JP, Li H. Telomerase in the ovary. Reproduction. 2010;140(2):215–22; DOI:10.1530/REP-10-0008.10.1530/REP-10-000820562297
  55. 55. Yamagata Y, Nakamura Y, Umayahara K, Harada A, Takayama H, Sugino N, Kato H. Changes in telomerase activity in experimentally induced atretic follicles of immature rats. Endocr J. 2002;49(6):589–95; DOI:10.1507/ENDOCRJ.49.589.10.1507/endocrj.49.58912625407
  56. 56. Cheng EH, Chen SU, Lee TH, Pai YP, Huang LS, Huang CC, Lee MS. Evaluation of telomere length in cumulus cells as a potential biomarker of oocyte and embryo quality. Hum Reprod. 2013;28(4):929–36; DOI:10.1093/HUMREP/DET004.10.1093/humrep/det00423377770
  57. 57. Butts S, Riethman H, Ratcliffe S, Shaunik A, Coutifaris C, Barnhart K. Correlation of telomere length and telomerase activity with occult ovarian insufficiency. J Clin Endocrinol Metab. 2009;94(12):4835–43; DOI:10.1210/JC.2008-2269.10.1210/jc.2008-2269279565019864453
  58. 58. Chen H, Wang W, Mo Y, Ma Y, Ouyang N, Li R, Mai M, He Y, Bodombossou-Djobo MMA, Yang D. Women with high telomerase activity in luteinised granulosa cells have a higher pregnancy rate during in vitro fertilisation treatment. J Assist Reprod Genet. 2011;28(9):797–807; DOI:10.1007/S10815-011-9600-2.10.1007/s10815-011-9600-2316968321717175
  59. 59. Misiti S, Nanni S, Fontemaggi G, Cong Y-S, Wen J, Hirte HW, Piaggio G, Sacchi A, Pontecorvi A, Bacchetti S, Farsetti A. Induction of hTERT expression and telomerase activity by estrogens in human ovary epithelium cells. Mol Cell Biol. 2000;20(11):3764–71; DOI:10.1128/MCB.20.11.3764-3771.2000.10.1128/MCB.20.11.3764-3771.20008569210805720
  60. 60. Bayne S, Li H, Jones MEE, Pinto AR, van Sinderen M, Drummond A, Simpson ER, Liu JP. Estrogen deficiency reversibly induces telomere shortening in mouse granulosa cells and ovarian aging in vivo. Protein Cell. 2011;2(4):333–46; DOI:10.1007/S13238-011-1033-2.10.1007/s13238-011-1033-2487520421574023
Language: English
Page range: 29 - 33
Submitted on: Feb 14, 2022
Accepted on: Mar 23, 2022
Published on: Apr 10, 2022
Published by: Foundation for Cell Biology and Molecular Biology
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2022 Wiktoria Zgórecka, Afsaneh Golkar Narenji, Kornelia Krajnik, Paweł Antosik, Dorota Bukowska, Małgorzata Grzesiak, Radek Prochazka, Paul Mozdziak, Mariusz T. Skowroński, Wiesława Kranc, published by Foundation for Cell Biology and Molecular Biology
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.