{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,19]],"date-time":"2026-08-19T18:31:25Z","timestamp":1787164285161,"version":"build-2736575974"},"reference-count":50,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2026,1,16]],"date-time":"2026-01-16T00:00:00Z","timestamp":1768521600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2026,2,11]],"date-time":"2026-02-11T00:00:00Z","timestamp":1770768000000},"content-version":"vor","delay-in-days":26,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100012681","name":"Universit\u00e4tsklinikum K\u00f6ln","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100012681","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Ovarian Res"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Purpose<\/jats:title>\n                    <jats:p>To explore the in vitro 3D culture of ovarian tissue thawed in two different ways with TISSEEL Fibrin and assessed transcriptome differences by RNA sequencing.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>Human ovarian tissue samples were collected, and the fragments used for the experiments were obtained from tumor patients involved in a fertility treatment program. After cryopreservation (frozen and thawed after initial cryopreservation), with or without 3D culture with TISSEEL Fibrin. The culture flask is agitated at 75 times per minute using a rotary shaker during the entire culture process. Four experimental groups were formed. Frozen tissue after quick thawing at 100\u00a0\u00b0C (Group 1), frozen tissue after quick thawing at 100\u00a0\u00b0C and in vitro 3D culture for 7 days with TISSEEL Fibrin (Group 2), frozen tissue after slow thawing at 37\u00a0\u00b0C (Group 3), frozen tissue after slow thawing at 37\u00a0\u00b0C and in vitro 3D culture for 7 days with TISSEEL Fibrin (Group 4). All groups were followed by RNA sequencing and histological evaluation.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>Hematoxylin-eosin (HE) staining has shown that the follicle cells have the tendency to develop and actively migrate into the fiber. Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis shows that in comparison to groups 1 and 3 (thawing ovarian tissue without culture), Differential Expression Genes (DEGs) in groups 2 and 4 (thawing ovarian tissue with in vitro 3D culture), are mainly enriched and up-related in the lysosome pathway and protein processing in the endoplasmic reticulum pathway and mainly down-related in the cell adhesion molecules pathway.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>The technology of the described dynamic in vitro 3D-cultivation of ovarian tissue for 7 days with TISSEEL Fibrin is informative and demonstrates that it may promote follicular growth, actively migrate into the fiber, weaken cell adhesion, and cause little cell damage.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s13048-025-01896-9","type":"journal-article","created":{"date-parts":[[2026,1,16]],"date-time":"2026-01-16T05:55:05Z","timestamp":1768542905000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Dynamic in vitro 3D culture of cryopreserved human ovarian tissue: transcriptomic analysis by RNA sequencing"],"prefix":"10.1186","volume":"19","author":[{"given":"Qingduo","family":"Kong","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel","family":"Stavrev","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gohar","family":"Rahimi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Plamen","family":"Todorov","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cheng","family":"Pei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Evgenia","family":"Isachenko","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mahmoud","family":"Salama","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christine","family":"Skala","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Volodimir","family":"Isachenko","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2026,1,16]]},"reference":[{"key":"1896_CR1","doi-asserted-by":"publisher","first-page":"489","DOI":"10.1093\/humrep\/deac249","volume":"38","author":"E Fraison","year":"2023","unstructured":"Fraison E, Huberlant S, Labrune E, Cavalieri M, Montagut M, Brugnon F, Courbiere B. Live birth rate after female fertility preservation for cancer or Haematopoietic stem cell transplantation: a systematic review and meta-analysis of the three main techniques; embryo, oocyte and ovarian tissue cryopreservation. Hum Reprod (Oxford England). 2023;38:489\u2013502. https:\/\/doi.org\/10.1093\/humrep\/deac249.","journal-title":"Hum Reprod (Oxford England)"},{"key":"1896_CR2","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1016\/j.bpobgyn.2021.09.010","volume":"81","author":"L Cacciottola","year":"2022","unstructured":"Cacciottola L, Donnez J, Dolmans MM. Ovarian tissue and oocyte cryopreservation prior to iatrogenic premature ovarian insufficiency. Best Pract Res Clin Obstet Gynaecol. 2022;81:119\u201333. https:\/\/doi.org\/10.1016\/j.bpobgyn.2021.09.010.","journal-title":"Best Pract Res Clin Obstet Gynaecol"},{"key":"1896_CR3","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1016\/j.fertnstert.2024.05.167","volume":"122","author":"CE Dunlop","year":"2024","unstructured":"Dunlop CE, Anderson RA. Clinical dilemmas in ovarian tissue cryopreservation. Fertil Steril. 2024;122:559\u201364. https:\/\/doi.org\/10.1016\/j.fertnstert.2024.05.167.","journal-title":"Fertil Steril"},{"key":"1896_CR4","doi-asserted-by":"publisher","first-page":"574","DOI":"10.1016\/j.fertnstert.2024.07.005","volume":"122","author":"LM Gadek","year":"2024","unstructured":"Gadek LM, Joswiak C, Laronda MM. Thawing fertility: a view of ovarian tissue cryopreservation processes and review of ovarian transplant research. Fertil Steril. 2024;122:574\u201385. https:\/\/doi.org\/10.1016\/j.fertnstert.2024.07.005.","journal-title":"Fertil Steril"},{"key":"1896_CR5","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s10616-021-00510-2","volume":"74","author":"Z Ghezelayagh","year":"2022","unstructured":"Ghezelayagh Z, Khoshdel-Rad N, Ebrahimi B. Human ovarian tissue culture: primordial follicle activation as a new strategy for female fertility preservation. Cytotechnology. 2022;74:1\u201315. https:\/\/doi.org\/10.1007\/s10616-021-00510-2.","journal-title":"Cytotechnology"},{"key":"1896_CR6","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1016\/j.theriogenology.2017.04.029","volume":"97","author":"GDA Gastal","year":"2017","unstructured":"Gastal GDA, Aguiar FLN, Alves BG, Alves KA, de Tarso SGS, Ishak GM, et al. Equine ovarian tissue viability after cryopreservation and culture. Theriogenology. 2017;97:139\u201347. https:\/\/doi.org\/10.1016\/j.theriogenology.2017.04.029.","journal-title":"Theriogenology"},{"key":"1896_CR7","doi-asserted-by":"publisher","first-page":"635","DOI":"10.1017\/s096719941600006x","volume":"24","author":"MA Filatov","year":"2016","unstructured":"Filatov MA, Khramova YV, Kiseleva MV, Malinova IV, Komarova EV, Semenova ML. Female fertility preservation strategies: cryopreservation and ovarian tissue culture, current state of the art and future perspectives. Zygote (Cambridge England). 2016;24:635\u201353. https:\/\/doi.org\/10.1017\/s096719941600006x.","journal-title":"Zygote (Cambridge England)"},{"key":"1896_CR8","doi-asserted-by":"publisher","DOI":"10.3390\/medicina58111565","author":"E Labrune","year":"2022","unstructured":"Labrune E, Fournier C, Riche B, David L, Montembault A, Collardeau-Frachon S, et al. Development and survival of human ovarian cells in chitosan hydrogel micro-bioreactor. Medicina (Kaunas). 2022. https:\/\/doi.org\/10.3390\/medicina58111565.","journal-title":"Medicina (Kaunas)"},{"key":"1896_CR9","doi-asserted-by":"publisher","first-page":"1242","DOI":"10.1089\/ten.TEB.2021.0229","volume":"28","author":"S Khunmanee","year":"2022","unstructured":"Khunmanee S, Park H. Three-dimensional culture for folliculogenesis in the aspect of methods and materials. Tissue Eng Part B Rev. 2022;28:1242\u201357. https:\/\/doi.org\/10.1089\/ten.TEB.2021.0229.","journal-title":"Tissue Eng Part B Rev"},{"key":"1896_CR10","doi-asserted-by":"publisher","DOI":"10.1016\/j.biopha.2021.111422","volume":"140","author":"D Xiang","year":"2021","unstructured":"Xiang D, Liu Y, Zhou E, Wang Y. Advances in the applications of polymer biomaterials for in vitro follicle culture. Biomed Pharmacother. 2021;140:111422. https:\/\/doi.org\/10.1016\/j.biopha.2021.111422.","journal-title":"Biomed Pharmacother"},{"key":"1896_CR11","doi-asserted-by":"publisher","first-page":"915","DOI":"10.1071\/rd12401","volume":"26","author":"IR Brito","year":"2014","unstructured":"Brito IR, Lima IM, Xu M, Shea LD, Woodruff TK, Figueiredo JR. Three-dimensional systems for in vitro follicular culture: overview of alginate-based matrices. Reprod Fertil Dev. 2014;26:915\u201330. https:\/\/doi.org\/10.1071\/rd12401.","journal-title":"Reprod Fertil Dev"},{"key":"1896_CR12","doi-asserted-by":"publisher","first-page":"1676","DOI":"10.1007\/s10439-017-1823-7","volume":"45","author":"X He","year":"2017","unstructured":"He X. Microfluidic encapsulation of ovarian follicles for 3D culture. Ann Biomed Eng. 2017;45:1676\u201384. https:\/\/doi.org\/10.1007\/s10439-017-1823-7.","journal-title":"Ann Biomed Eng"},{"key":"1896_CR13","doi-asserted-by":"publisher","DOI":"10.3390\/ijms23063265","author":"S Braccini","year":"2022","unstructured":"Braccini S, Tacchini C, Chiellini F, Puppi D. Polymeric hydrogels for in vitro 3D ovarian cancer modeling. Int J Mol Sci. 2022. https:\/\/doi.org\/10.3390\/ijms23063265.","journal-title":"Int J Mol Sci"},{"key":"1896_CR14","doi-asserted-by":"publisher","first-page":"120","DOI":"10.1016\/j.theriogenology.2022.02.009","volume":"183","author":"C Matsushige","year":"2022","unstructured":"Matsushige C, Xu X, Miyagi M, Zuo YY, Yamazaki Y. RGD-modified dextran hydrogel promotes follicle growth in three-dimensional ovarian tissue culture in mice. Theriogenology. 2022;183:120\u201331. https:\/\/doi.org\/10.1016\/j.theriogenology.2022.02.009.","journal-title":"Theriogenology"},{"key":"1896_CR15","doi-asserted-by":"publisher","first-page":"240","DOI":"10.1016\/0268-960x(91)90015-5","volume":"5","author":"M Brennan","year":"1991","unstructured":"Brennan M. Fibrin glue. Blood Rev. 1991;5:240\u20134. https:\/\/doi.org\/10.1016\/0268-960x(91)90015-5.","journal-title":"Blood Rev"},{"key":"1896_CR16","doi-asserted-by":"publisher","first-page":"801","DOI":"10.3171\/jns.1984.61.4.0801","volume":"61","author":"J Haase","year":"1984","unstructured":"Haase J. Use of tisseel in neurosurgery. J Neurosurg. 1984;61:801. https:\/\/doi.org\/10.3171\/jns.1984.61.4.0801.","journal-title":"J Neurosurg"},{"key":"1896_CR17","doi-asserted-by":"publisher","first-page":"411","DOI":"10.1016\/s0003-4975(10)62298-9","volume":"38","author":"J Stark","year":"1984","unstructured":"Stark J, de Leval M. Experience with fibrin seal (Tisseel) in operations for congenital heart defects. Ann Thorac Surg. 1984;38:411\u20133. https:\/\/doi.org\/10.1016\/s0003-4975(10)62298-9.","journal-title":"Ann Thorac Surg"},{"key":"1896_CR18","doi-asserted-by":"publisher","first-page":"1015","DOI":"10.1136\/thx.43.12.1015","volume":"43","author":"RT Onotera","year":"1988","unstructured":"Onotera RT, Unruh HW. Closure of a post-pneumonectomy bronchopleural fistula with fibrin sealant (Tisseel). Thorax. 1988;43:1015\u20136. https:\/\/doi.org\/10.1136\/thx.43.12.1015.","journal-title":"Thorax"},{"key":"1896_CR19","doi-asserted-by":"publisher","DOI":"10.3390\/ijms232012419","author":"W Wang","year":"2022","unstructured":"Wang W, Pei C, Isachenko E, Zhou Y, Wang M, Rahimi G, et al. Automatic evaluation for bioengineering of human artificial ovary: a model for fertility preservation for prepubertal female patients with a malignant tumor. Int J Mol Sci. 2022. https:\/\/doi.org\/10.3390\/ijms232012419.","journal-title":"Int J Mol Sci"},{"key":"1896_CR20","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1017\/s0967199417000338","volume":"25","author":"NJ Donfack","year":"2017","unstructured":"Donfack NJ, Alves KA, Ara\u00fajo VR, Cordova A, Figueiredo JR, Smitz J, Rodrigues APR. Expectations and limitations of ovarian tissue transplantation. Zygote (Cambridge England). 2017;25:391\u2013403. https:\/\/doi.org\/10.1017\/s0967199417000338.","journal-title":"Zygote (Cambridge England)"},{"key":"1896_CR21","doi-asserted-by":"publisher","DOI":"10.3390\/ijms252413747","author":"Q Kong","year":"2024","unstructured":"Kong Q, Todorov P, Pei C, Isachenko E, Rahimi G, Mallmann-Gottschalk N, et al. Positive effect of elevated thawing rate for cryopreservation of human ovarian tissue: transcriptomic analysis of fresh and cryopreserved cells. Int J Mol Sci. 2024. https:\/\/doi.org\/10.3390\/ijms252413747.","journal-title":"Int J Mol Sci"},{"key":"1896_CR22","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1530\/rep-09-0039","volume":"138","author":"V Isachenko","year":"2009","unstructured":"Isachenko V, Lapidus I, Isachenko E, Krivokharchenko A, Kreienberg R, Woriedh M, Bader M, Weiss JM. Human ovarian tissue vitrification versus conventional freezing: morphological, endocrinological, and molecular biological evaluation. Reprod (Cambridge England). 2009;138:319\u201327. https:\/\/doi.org\/10.1530\/rep-09-0039.","journal-title":"Reprod (Cambridge England)"},{"key":"1896_CR23","doi-asserted-by":"publisher","first-page":"118","DOI":"10.1186\/s13048-020-00713-9","volume":"13","author":"V Isachenko","year":"2020","unstructured":"Isachenko V, Morgenstern B, Todorov P, Isachenko E, Mallmann P, Hanstein B, Rahimi G. Patient with ovarian insufficiency: baby born after anticancer therapy and re-transplantation of cryopreserved ovarian tissue. J Ovarian Res. 2020;13:118. https:\/\/doi.org\/10.1186\/s13048-020-00713-9.","journal-title":"J Ovarian Res"},{"key":"1896_CR24","doi-asserted-by":"publisher","DOI":"10.1186\/s12958-016-0213-6","volume":"14","author":"V Isachenko","year":"2016","unstructured":"Isachenko V, Todorov P, Isachenko E, Rahimi G, Hanstein B, Salama M, et al. Cryopreservation and xenografting of human ovarian fragments: medulla decreases the phosphatidylserine translocation rate. Reprod Biol Endocrinol. 2016;14:79. https:\/\/doi.org\/10.1186\/s12958-016-0213-6.","journal-title":"Reprod Biol Endocrinol"},{"key":"1896_CR25","doi-asserted-by":"publisher","DOI":"10.3390\/ijms25010214","author":"C Pei","year":"2023","unstructured":"Pei C, Todorov P, Cao M, Kong Q, Isachenko E, Rahimi G, et al. Comparative transcriptomic analyses for the optimization of thawing regimes during conventional cryopreservation of mature and immature human testicular tissue. Int J Mol Sci. 2023. https:\/\/doi.org\/10.3390\/ijms25010214.","journal-title":"Int J Mol Sci"},{"key":"1896_CR26","doi-asserted-by":"publisher","DOI":"10.1101\/pdb.prot5439","volume":"2010","author":"DC Rio","year":"2010","unstructured":"Rio DC, Ares M Jr., Hannon GJ, Nilsen TW. Purification of RNA using TRIzol (TRI reagent). Cold Spring Harb Protoc. 2010;2010:pdb.prot5439. https:\/\/doi.org\/10.1101\/pdb.prot5439.","journal-title":"Cold Spring Harb Protoc"},{"key":"1896_CR27","doi-asserted-by":"publisher","first-page":"2445","DOI":"10.1158\/1055-9965.Epi-10-0565","volume":"19","author":"W Ma","year":"2010","unstructured":"Ma W, Wang M, Wang ZQ, Sun L, Graber D, Matthews J, et al. Effect of long-term storage in TRIzol on microarray-based gene expression profiling. Cancer Epidemiol Biomarkers Prev. 2010;19:2445\u201352. https:\/\/doi.org\/10.1158\/1055-9965.Epi-10-0565.","journal-title":"Cancer Epidemiol Biomarkers Prev"},{"key":"1896_CR28","doi-asserted-by":"publisher","first-page":"1004","DOI":"10.1007\/s11033-024-09783-0","volume":"51","author":"N Chavoshinezhad","year":"2024","unstructured":"Chavoshinezhad N, Niknafs B. Innovations in 3D ovarian and follicle engineering for fertility preservation and restoration. Mol Biol Rep. 2024;51:1004. https:\/\/doi.org\/10.1007\/s11033-024-09783-0.","journal-title":"Mol Biol Rep"},{"key":"1896_CR29","doi-asserted-by":"publisher","first-page":"2743","DOI":"10.1093\/humrep\/deae240","volume":"39","author":"H Cheng","year":"2024","unstructured":"Cheng H, Wei F, Del Valle JS, Stolk THR, Huirne JA, Asseler JD, et al. In vitro growth of secondary follicles from cryopreserved-thawed ovarian cortex. Hum Reprod. 2024;39:2743\u201353. https:\/\/doi.org\/10.1093\/humrep\/deae240.","journal-title":"Hum Reprod"},{"key":"1896_CR30","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1016\/j.ejogrb.2020.09.002","volume":"254","author":"D Vatansever","year":"2020","unstructured":"Vatansever D, \u0130ncir S, Bildik G, Taskiran C, Oktem O. In-vitro AMH production of ovarian tissue samples in culture correlates with their primordial follicle pool. Eur J Obstet Gynecol Reprod Biol. 2020;254:138\u201340. https:\/\/doi.org\/10.1016\/j.ejogrb.2020.09.002.","journal-title":"Eur J Obstet Gynecol Reprod Biol"},{"key":"1896_CR31","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1007\/s13224-020-01362-0","volume":"70","author":"L Shrikhande","year":"2020","unstructured":"Shrikhande L, Shrikhande B, Shrikhande A. AMH and its clinical implications. J Obstet Gynaecol India. 2020;70:337\u201341. https:\/\/doi.org\/10.1007\/s13224-020-01362-0.","journal-title":"J Obstet Gynaecol India"},{"key":"1896_CR32","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1097\/gco.0000000000000943","volume":"36","author":"J Castillo","year":"2024","unstructured":"Castillo J, Kol S. Ideal frozen embryo transfer regime. Curr Opin Obstet Gynecol. 2024;36:148\u201354. https:\/\/doi.org\/10.1097\/gco.0000000000000943.","journal-title":"Curr Opin Obstet Gynecol"},{"key":"1896_CR33","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1038\/nrm3270","volume":"13","author":"C Hetz","year":"2012","unstructured":"Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. 2012;13:89\u2013102. https:\/\/doi.org\/10.1038\/nrm3270.","journal-title":"Nat Rev Mol Cell Biol"},{"key":"1896_CR34","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1146\/annurev-pathol-012513-104649","volume":"10","author":"SA Oakes","year":"2015","unstructured":"Oakes SA, Papa FR. The role of endoplasmic reticulum stress in human pathology. Annu Rev Pathol. 2015;10:173\u201394. https:\/\/doi.org\/10.1146\/annurev-pathol-012513-104649.","journal-title":"Annu Rev Pathol"},{"key":"1896_CR35","doi-asserted-by":"publisher","DOI":"10.1016\/j.plipres.2022.101198","volume":"89","author":"C Celik","year":"2023","unstructured":"Celik C, Lee SYT, Yap WS, Thibault G. Endoplasmic reticulum stress and lipids in health and diseases. Prog Lipid Res. 2023;89:101198. https:\/\/doi.org\/10.1016\/j.plipres.2022.101198.","journal-title":"Prog Lipid Res"},{"key":"1896_CR36","doi-asserted-by":"publisher","first-page":"326","DOI":"10.1038\/nmat4489","volume":"15","author":"O Chaudhuri","year":"2016","unstructured":"Chaudhuri O, Gu L, Klumpers D, Darnell M, Bencherif SA, Weaver JC, et al. Hydrogels with tunable stress relaxation regulate stem cell fate and activity. Nat Mater. 2016;15:326\u201334. https:\/\/doi.org\/10.1038\/nmat4489.","journal-title":"Nat Mater"},{"key":"1896_CR37","doi-asserted-by":"publisher","DOI":"10.1088\/1748-605X\/ac21a7","author":"S Yadav","year":"2021","unstructured":"Yadav S, Majumder A. Biomimicked hierarchical 2D and 3D structures from natural templates: applications in cell biology. Biomed Mater. 2021. https:\/\/doi.org\/10.1088\/1748-605X\/ac21a7.","journal-title":"Biomed Mater"},{"key":"1896_CR38","doi-asserted-by":"publisher","first-page":"1076","DOI":"10.1042\/bst0191076","volume":"19","author":"E Bock","year":"1991","unstructured":"Bock E. Cell-cell adhesion molecules. Biochem Soc Trans. 1991;19:1076\u201380. https:\/\/doi.org\/10.1042\/bst0191076.","journal-title":"Biochem Soc Trans"},{"key":"1896_CR39","doi-asserted-by":"publisher","DOI":"10.3390\/ijms21218264","author":"RP Piprek","year":"2020","unstructured":"Piprek RP, Kloc M, Mizia P, Kubiak JZ. The central role of cadherins in gonad development, reproduction, and fertility. Int J Mol Sci. 2020. https:\/\/doi.org\/10.3390\/ijms21218264.","journal-title":"Int J Mol Sci"},{"key":"1896_CR40","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1097\/00003086-198802000-00033","volume":"227","author":"G Schlag","year":"1988","unstructured":"Schlag G, Redl H. Fibrin sealant in orthopedic surgery. Clin Orthop Relat Res. 1988;227:269\u201385.","journal-title":"Clin Orthop Relat Res"},{"key":"1896_CR41","doi-asserted-by":"publisher","first-page":"621","DOI":"10.2183\/pjab.86.621","volume":"86","author":"H Ogita","year":"2010","unstructured":"Ogita H, Rikitake Y, Miyoshi J, Takai Y. Cell adhesion molecules Nectins and associating proteins: implications for physiology and pathology. Proc Jpn Acad Ser B Phys Biol Sci. 2010;86:621\u20139. https:\/\/doi.org\/10.2183\/pjab.86.621.","journal-title":"Proc Jpn Acad Ser B Phys Biol Sci"},{"key":"1896_CR42","doi-asserted-by":"publisher","DOI":"10.1093\/hropen\/hoad052","volume":"2024","author":"M Grubliauskait\u0117","year":"2024","unstructured":"Grubliauskait\u0117 M, Vlieghe H, Moghassemi S, Dadashzadeh A, Camboni A, Gudlevi\u010dien\u0117 \u017d, et al. Influence of ovarian stromal cells on human ovarian follicle growth in a 3D environment. Hum Reprod Open. 2024;2024:hoad052. https:\/\/doi.org\/10.1093\/hropen\/hoad052.","journal-title":"Hum Reprod Open"},{"key":"1896_CR43","doi-asserted-by":"publisher","first-page":"1538","DOI":"10.1093\/humrep\/dead122","volume":"38","author":"F Vitale","year":"2023","unstructured":"Vitale F, Cacciottola L, Yu FS, Barretta M, Hossay C, Donnez J, Dolmans MM. Importance of oxygen tension in human ovarian tissue in vitro culture. Hum Reprod (Oxford England). 2023;38:1538\u201346. https:\/\/doi.org\/10.1093\/humrep\/dead122.","journal-title":"Hum Reprod (Oxford England)"},{"key":"1896_CR44","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1002\/rmb2.12268","volume":"18","author":"S Takae","year":"2019","unstructured":"Takae S, Suzuki N. Current state and future possibilities of ovarian tissue transplantation. Reprod Med Biol. 2019;18:217\u201324. https:\/\/doi.org\/10.1002\/rmb2.12268.","journal-title":"Reprod Med Biol"},{"key":"1896_CR45","doi-asserted-by":"publisher","DOI":"10.1038\/s41419-023-06154-8","volume":"14","author":"S Liu","year":"2023","unstructured":"Liu S, Yao S, Yang H, Liu S, Wang Y. Autophagy: regulator of cell death. Cell Death Dis. 2023;14:648. https:\/\/doi.org\/10.1038\/s41419-023-06154-8.","journal-title":"Cell Death Dis"},{"key":"1896_CR46","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1002\/path.2697","volume":"221","author":"D Glick","year":"2010","unstructured":"Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010;221:3\u201312. https:\/\/doi.org\/10.1002\/path.2697.","journal-title":"J Pathol"},{"key":"1896_CR47","doi-asserted-by":"publisher","first-page":"728","DOI":"10.1016\/j.cell.2011.10.026","volume":"147","author":"N Mizushima","year":"2011","unstructured":"Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell. 2011;147:728\u201341. https:\/\/doi.org\/10.1016\/j.cell.2011.10.026.","journal-title":"Cell"},{"key":"1896_CR48","doi-asserted-by":"publisher","first-page":"918","DOI":"10.1111\/tra.12613","volume":"19","author":"F Wang","year":"2018","unstructured":"Wang F, G\u00f3mez-Sintes R, Boya P. Lysosomal membrane permeabilization and cell death. Traffic. 2018;19:918\u201331. https:\/\/doi.org\/10.1111\/tra.12613.","journal-title":"Traffic"},{"key":"1896_CR49","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1186\/1757-2215-6-83","volume":"6","author":"V Luyckx","year":"2013","unstructured":"Luyckx V, Dolmans MM, Vanacker J, Scalercio SR, Donnez J, Amorim CA. First step in developing a 3D biodegradable fibrin scaffold for an artificial ovary. J Ovarian Res. 2013;6:83. https:\/\/doi.org\/10.1186\/1757-2215-6-83.","journal-title":"J Ovarian Res"},{"key":"1896_CR50","doi-asserted-by":"publisher","first-page":"1149","DOI":"10.1016\/j.fertnstert.2013.12.025","volume":"101","author":"V Luyckx","year":"2014","unstructured":"Luyckx V, Dolmans MM, Vanacker J, Legat C, Fortu\u00f1o Moya C, Donnez J, et al. A new step toward the artificial ovary: survival and proliferation of isolated murine follicles after autologous transplantation in a fibrin scaffold. Fertil Steril. 2014;101:1149\u201356. https:\/\/doi.org\/10.1016\/j.fertnstert.2013.12.025.","journal-title":"Fertil Steril"}],"container-title":["Journal of Ovarian Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s13048-025-01896-9","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13048-025-01896-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13048-025-01896-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T16:46:55Z","timestamp":1781628415000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1186\/s13048-025-01896-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,1,16]]},"references-count":50,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2026,12]]}},"alternative-id":["1896"],"URL":"https:\/\/doi.org\/10.1186\/s13048-025-01896-9","relation":{},"ISSN":["1757-2215"],"issn-type":[{"value":"1757-2215","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,1,16]]},"assertion":[{"value":"7 July 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 November 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 January 2026","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The study was conducted by the Declaration of Helsinki and approved by the Institutional Ethics Committee of Cologne University (applications 999,184 and 13\u2013147) and by the Bulgarian Ethics Committee.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"The authors declare no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"55"}}