The limitations of testicular organoids: are they truly as promising as we believe?

Abumadighem A, Shuchat S, Lunenfeld E, Yossifon G, Huleihel M (2022) Testis on a chip – a microfluidic three-dimensional culture system for the development of spermatogenesis in-vitro. Biofabrication 14(3), 035004.
| Crossref | Google Scholar |

Agrimson KS, Onken J, Mitchell D, Topping TB, Chiarini-Garcia H, Hogarth CA, Griswold MD (2016) Characterizing the spermatogonial response to retinoic acid during the onset of spermatogenesis and following synchronization in the neonatal mouse testis. Biology of Reproduction 95(4), 81 1–15.
| Crossref | Google Scholar | PubMed |

Alves-Lopes JP, Söder O, Stukenborg J-B (2017) Testicular organoid generation by a novel in vitro three-layer gradient system. Biomaterials 130, 76-89.
| Crossref | Google Scholar | PubMed |

Amory JK, Muller CH, Shimshoni JA, Isoherranen N, Paik J, Moreb JS, Amory DW, Sr, Evanoff R, Goldstein AS, Griswold MD (2011) Suppression of spermatogenesis by bisdichloroacetyldiamines is mediated by inhibition of testicular retinoic acid biosynthesis. Journal of Andrology 32(1), 111-119.
| Crossref | Google Scholar | PubMed |

Arkoun B, Dumont L, Milazzo J-P, Way A, Bironneau A, Wils J, Macé B, Rives N (2015) Retinol improves in vitro differentiation of pre-pubertal mouse spermatogonial stem cells into sperm during the first wave of spermatogenesis. PLoS ONE 10(2), e0116660.
| Crossref | Google Scholar | PubMed |

Baert Y, De Kock J, Alves-Lopes JP, Söder O, Stukenborg J-B, Goossens E (2017) Primary human testicular cells self-organize into organoids with testicular properties. Stem Cell Reports 8(1), 30-38.
| Crossref | Google Scholar | PubMed |

Baert Y, Dvorakova-Hortova K, Margaryan H, Goossens E (2019) Mouse in vitro spermatogenesis on alginate-based 3D bioprinted scaffolds. Biofabrication 11(3), 035011.
| Crossref | Google Scholar | PubMed |

Baert Y, Ruetschle I, Cools W, Oehme A, Lorenz A, Marx U, Goossens E, Maschmeyer I (2020) A multi-organ-chip co-culture of liver and testis equivalents: a first step toward a systemic male reprotoxicity model. Human Reproduction 35(5), 1029-1044.
| Crossref | Google Scholar |

Bhaduri A, Andrews MG, Mancia Leon W, Jung D, Shin D, Allen D, Jung D, Schmunk G, Haeussler M, Salma J, Pollen AA, Nowakowski TJ, Kriegstein AR (2020) Cell stress in cortical organoids impairs molecular subtype specification. Nature 578(7793), 142-148.
| Crossref | Google Scholar | PubMed |

Boj SF, Hwang C-I, Baker LA, Chio IIC, Engle DD, Corbo V, Jager M, Ponz-Sarvise M, Tiriac H, Spector MS, Gracanin A, Oni T, Yu KH, van Boxtel R, Huch M, Rivera KD, Wilson JP, Feigin ME, Öhlund D, Handly-Santana A, Ardito-Abraham CM, Ludwig M, Elyada E, Alagesan B, Biffi G, Yordanov GN, Delcuze B, Creighton B, Wright K, Park Y, Morsink FHM, Molenaar IQ, Borel Rinkes IH, Cuppen E, Hao Y, Jin Y, Nijman IJ, Iacobuzio-Donahue C, Leach SD, Pappin DJ, Hammell M, Klimstra DS, Basturk O, Hruban RH, Offerhaus GJ, Vries RGJ, Clevers H, Tuveson DA (2015) Organoid models of human and mouse ductal pancreatic cancer. Cell 160(1), 324-338.
| Crossref | Google Scholar |

Cakir B, Xiang Y, Tanaka Y, Kural MH, Parent M, Kang Y-J, Chapeton K, Patterson B, Yuan Y, He C-S, Raredon MSB, Dengelegi J, Kim K-Y, Sun P, Zhong M, Lee S, Patra P, Hyder F, Niklason LE, Lee S-H, Yoon Y-S, Park I-H (2019) Engineering of human brain organoids with a functional vascular-like system. Nature Methods 16(11), 1169-1175.
| Crossref | Google Scholar | PubMed |

Cham T-C, Ibtisham F, Fayaz MA, Honaramooz A (2021a) Generation of a highly biomimetic organoid, including vasculature, resembling the native immature testis tissue. Cells 10(7), 1696.
| Crossref | Google Scholar |

Cham T-C, Chen X, Honaramooz A (2021b) Current progress, challenges, and future prospects of testis organoids. Biology of Reproduction 104(5), 942-961.
| Crossref | Google Scholar | PubMed |

Chen H, Murray E, Sinha A, Laumas A, Li J, Lesman D, Nie X, Hotaling J, Guo J, Cairns BR, Macosko EZ, Cheng CY, Chen F (2021) Dissecting mammalian spermatogenesis using spatial transcriptomics. Cell Reports 37(5), 109915.
| Crossref | Google Scholar |

Chung SSW, Vizcarra N, Wolgemuth DJ (2020) Filamentous actin disorganization and absence of apical ectoplasmic specialization disassembly during spermiation upon interference with retinoid signaling. Biology of Reproduction 103(2), 378-389.
| Crossref | Google Scholar | PubMed |

Cortez J, Leiva B, Torres CG, Parraguez VH, De los Reyes M, Carrasco A, Peralta OA (2022) Generation and characterization of bovine testicular organoids derived from primary somatic cell populations. Animals 12(17), 2283.
| Crossref | Google Scholar | PubMed |

Cunha GR, Cao M, Aksel S, Derpinghaus A, Baskin LS (2023) Mouse-human species differences in early testicular development and its implications. Differentiation 129, 79-95.
| Crossref | Google Scholar | PubMed |

Delessard M, Stalin L, Rives-Feraille A, Moutard L, Saulnier J, Dumont L, Rives N, Rondanino C (2022) Achievement of complete in vitro spermatogenesis in testicular tissues from prepubertal mice exposed to mono- or polychemotherapy. Scientific Reports 12(1), 7407.
| Crossref | Google Scholar | PubMed |

Di Persio S, Starace D, Capponi C, Saracino R, Fera S, Filippini A, Vicini E (2021) TNF-α inhibits GDNF levels in Sertoli cells, through a NF-κB-dependent, HES1-dependent mechanism. Andrology 9(3), 956-964.
| Crossref | Google Scholar | PubMed |

Dorostghoal M, Kazeminejad SR, Shahbazian N, Pourmehdi M, Jabbari A (2017) Oxidative stress status and sperm DNA fragmentation in fertile and infertile men. Andrologia 49(10), e12762.
| Crossref | Google Scholar |

Edmonds ME, Woodruff TK (2020) Testicular organoid formation is a property of immature somatic cells, which self-assemble and exhibit long-term hormone-responsive endocrine function. Biofabrication 12(4), 045002.
| Crossref | Google Scholar |

Endo T, Freinkman E, de Rooij DG, Page DC (2017) Periodic production of retinoic acid by meiotic and somatic cells coordinates four transitions in mouse spermatogenesis. Proceedings of the National Academy of Sciences 114(47), E10132-E10141.
| Crossref | Google Scholar |

Fayomi AP, Orwig KE (2018) Spermatogonial stem cells and spermatogenesis in mice, monkeys and men. Stem Cell Research 29, 207-214.
| Crossref | Google Scholar | PubMed |

Fayomi AP, Peters K, Sukhwani M, Valli-Pulaski H, Shetty G, Meistrich ML, Houser L, Robertson N, Roberts V, Ramsey C, Hanna C, Hennebold JD, Dobrinski I, Orwig KE (2019) Autologous grafting of cryopreserved prepubertal rhesus testis produces sperm and offspring. Science 363(6433), 1314-1319.
| Crossref | Google Scholar | PubMed |

Gewiss R, Topping T, Griswold MD (2020) Cycles, waves, and pulses: retinoic acid and the organization of spermatogenesis. Andrology 8(4), 892-897.
| Crossref | Google Scholar | PubMed |

Giandomenico SL, Mierau SB, Gibbons GM, Wenger LMD, Masullo L, Sit T, Sutcliffe M, Boulanger J, Tripodi M, Derivery E, Paulsen O, Lakatos A, Lancaster MA (2019) Cerebral organoids at the air–liquid interface generate diverse nerve tracts with functional output. Nature Neuroscience 22(4), 669-679.
| Crossref | Google Scholar | PubMed |

Gilleland Marchak J, Seidel KD, Mertens AC, Ritenour CWM, Wasilewski-Masker K, Leisenring WM, Sklar CA, Ford JS, Krull KR, Stovall M, Robison LL, Armstrong GT, Meacham LR (2018) Perceptions of risk of infertility among male survivors of childhood cancer: a report from the childhood cancer survivor study. Cancer 124(11), 2447-2455.
| Crossref | Google Scholar | PubMed |

Goldsmith TM, Sakib S, Webster D, Carlson DF, Van der Hoorn F, Dobrinski I (2020) A reduction of primary cilia but not hedgehog signaling disrupts morphogenesis in testicular organoids. Cell and Tissue Research 380(1), 191-200.
| Crossref | Google Scholar | PubMed |

Guerrero-Bosagna C, Savenkova M, Haque MM, Nilsson E, Skinner MK (2013) Environmentally induced epigenetic transgenerational inheritance of altered sertoli cell transcriptome and epigenome: molecular etiology of male infertility. PLoS ONE 8(3), e59922.
| Crossref | Google Scholar | PubMed |

Guo J, Nie X, Giebler M, Mlcochova H, Wang Y, Grow EJ, Kim R, Tharmalingam M, Matilionyte G, Lindskog C, Carrell DT, Mitchell RT, Goriely A, Hotaling JM, Cairns BR (2020) The dynamic transcriptional cell atlas of testis development during human puberty. Cell Stem Cell 26(2), 262-276.e4.
| Crossref | Google Scholar | PubMed |

Guo J, Sosa E, Chitiashvili T, Nie X, Rojas EJ, Oliver E, Plath K, Hotaling JM, Stukenborg J-B, Clark AT, Cairns BR (2021) Single-cell analysis of the developing human testis reveals somatic niche cell specification and fetal germline stem cell establishment. Cell Stem Cell 28(4), 764-778.e4.
| Crossref | Google Scholar | PubMed |

Iwamori T, Iwamori N, Matsumoto M, Imai H, Ono E (2020) Novel localizations and interactions of intercellular bridge proteins revealed by proteomic profiling. Biology of Reproduction 102(5), 1134-1144.
| Crossref | Google Scholar | PubMed |

Jensen CFS, Wang D, Mamsen LS, Giwercman A, Jørgensen N, Fode M, Ohl D, Dong L, Hildorf SE, Pors SE, Fedder J, Ntemou E, Andersen CY, Sønksen J (2022) Sertoli and germ cells within atrophic seminiferous tubules of men with non-obstructive azoospermia. Frontiers in Endocrinology 13, 825904.
| Crossref | Google Scholar | PubMed |

Jijiwa M, Kawai K, Fukihara J, Nakamura A, Hasegawa M, Suzuki C, Sato T, Enomoto A, Asai N, Murakumo Y, Takahashi M (2008) GDNF-mediated signaling via ret tyrosine 1062 is essential for maintenance of spermatogonial stem cells. Genes to Cells 13(4), 365-374.
| Crossref | Google Scholar | PubMed |

Kanbar M, Vermeulen M, Wyns C (2021) Organoids as tools to investigate the molecular mechanisms of male infertility and its treatments. Reproduction 161(5), R103-R112.
| Crossref | Google Scholar | PubMed |

Kirsanov O, Johnson TA, Niedenberger BA, Malachowski TN, Hale BJ, Chen Q, Lackford B, Wang J, Singh A, Schindler K, Hermann BP, Hu G, Geyer CB (2023) Retinoic acid is dispensable for meiotic initiation but required for spermiogenesis in the mammalian testis. Development 150 dev201638.
| Crossref | Google Scholar |

Kitadate Y, Jörg DJ, Tokue M, Maruyama A, Ichikawa R, Tsuchiya S, Segi-Nishida E, Nakagawa T, Uchida A, Kimura-Yoshida C, Mizuno S, Sugiyama F, Azami T, Ema M, Noda C, Kobayashi S, Matsuo I, Kanai Y, Nagasawa T, Sugimoto Y, Takahashi S, Simons BD, Yoshida S (2019) Competition for mitogens regulates spermatogenic stem cell homeostasis in an open niche. Cell Stem Cell 24(1), 79-92.e6.
| Crossref | Google Scholar |

Koskenniemi JJ, Virtanen HE, Toppari J (2017) Testicular growth and development in puberty. Current Opinion in Endocrinology, Diabetes & Obesity 24(3), 215-224.
| Crossref | Google Scholar | PubMed |

Lee JH, Kim HJ, Kim H, Lee SJ, Gye MC (2006) In vitro spermatogenesis by three-dimensional culture of rat testicular cells in collagen gel matrix. Biomaterials 27(14), 2845-2853.
| Crossref | Google Scholar | PubMed |

Lee JH, Oh JH, Lee JH, Kim MR, Min CK (2011) Evaluation of in vitro spermatogenesis using poly(D,L-lactic-co-glycolic acid) (PLGA)-based macroporous biodegradable scaffolds. Journal of Tissue Engineering and Regenerative Medicine 5(2), 130-137.
| Crossref | Google Scholar | PubMed |

Legendre A, Froment P, Desmots S, Lecomte A, Habert R, Lemazurier E (2010) An engineered 3D blood-testis barrier model for the assessment of reproductive toxicity potential. Biomaterials 31(16), 4492-4505.
| Crossref | Google Scholar | PubMed |

Lovell-Badge R, Anthony E, Barker RA, Bubela T, Brivanlou AH, Carpenter M, Charo RA, Clark A, Clayton E, Cong Y, Daley GQ, Fu J, Fujita M, Greenfield A, Goldman SA, Hill L, Hyun I, Isasi R, Kahn J, Kato K, Kim J-S, Kimmelman J, Knoblich JA, Mathews D, Montserrat N, Mosher J, Munsie M, Nakauchi H, Naldini L, Naughton G, Niakan K, Ogbogu U, Pedersen R, Rivron N, Rooke H, Rossant J, Round J, Saitou M, Sipp D, Steffann J, Sugarman J, Surani A, Takahashi J, Tang F, Turner L, Zettler PJ, Zhai X (2021) ISSCR guidelines for stem cell research and clinical translation: the 2021 update. Stem Cell Reports 16(6), 1398-1408.
| Crossref | Google Scholar | PubMed |

Mansour AAF, Gonçalves JT, Bloyd CW, Li H, Fernandes S, Quang D, Johnston S, Parylak SL, Jin X, Gage FH (2018) An in vivo model of functional and vascularized human brain organoids. Nature Biotechnology 36(5), 432-441.
| Crossref | Google Scholar | PubMed |

Masaki K, Sakai M, Kuroki S, Jo J-I, Hoshina K, Fujimori Y, Oka K, Amano T, Yamanaka T, Tachibana M, Tabata Y, Shiozawa T, Ishizuka O, Hochi S, Takashima S (2018) FGF2 has distinct molecular functions from GDNF in the mouse germline niche. Stem Cell Reports 10(6), 1782-1792.
| Crossref | Google Scholar | PubMed |

Masliukaite I, Hagen JM, Jahnukainen K, Stukenborg J-B, Repping S, van der Veen F, van Wely M, van Pelt AMM (2016) Establishing reference values for age-related spermatogonial quantity in prepubertal human testes: a systematic review and meta-analysis. Fertility and Sterility 106, 1652-1657.e2.
| Crossref | Google Scholar |

Mruk DD, Cheng CY (2015) The mammalian blood-testis barrier: its biology and regulation. Endocrine Reviews 36(5), 564-591.
| Crossref | Google Scholar | PubMed |

Mäkelä J-A, Hobbs RM (2019) Molecular regulation of spermatogonial stem cell renewal and differentiation. Reproduction 158(5), R169-R187.
| Crossref | Google Scholar | PubMed |

Naughton CK, Jain S, Strickland AM, Gupta A, Milbrandt J (2006) Glial cell-line derived neurotrophic factor-mediated RET signaling regulates spermatogonial stem cell fate. Biology of Reproduction 74(2), 314-321.
| Crossref | Google Scholar | PubMed |

Nikmahzar A, Koruji M, Jahanshahi M, Khadivi F, Shabani M, Dehghani S, Forouzesh M, Jabari A, Feizollahi N, Salem M, Ghanami Gashti N, Abbasi Y, Abbasi M (2023) Differentiation of human primary testicular cells in the presence of SCF using the organoid culture system. Artificial Organs 47, 1818-1830.
| Crossref | Google Scholar |

Ntemou E, Kadam P, Van Saen D, Wistuba J, Mitchell RT, Schlatt S, Goossens E (2019) Complete spermatogenesis in intratesticular testis tissue xenotransplants from immature non-human primate. Human Reproduction 34(3), 403-413.
| Crossref | Google Scholar | PubMed |

Oatley JM, Brinster RL (2012) The germline stem cell niche unit in mammalian testes. Physiological Reviews 92(2), 577-595.
| Crossref | Google Scholar | PubMed |

Oatley JM, Oatley MJ, Avarbock MR, Tobias JW, Brinster RL (2009) Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal. Development 136(7), 1191-1199.
| Crossref | Google Scholar | PubMed |

Ogawa T, Dobrinski I, Avarbock MR, Brinster RL (1998) Leuprolide, a gonadotropin-releasing hormone agonist, enhances colonization after spermatogonial transplantation into mouse testes. Tissue and Cell 30(5), 583-588.
| Crossref | Google Scholar | PubMed |

Oldak B, Wildschutz E, Bondarenko V, Comar M-Y, Zhao C, Aguilera-Castrejon A, Tarazi S, Viukov S, Pham TXA, Ashouokhi S, Lokshtanov D, Roncato F, Ariel E, Rose M, Livnat N, Shani T, Joubran C, Cohen R, Addadi Y, Chemla M, Kedmi M, Keren-Shaul H, Pasque V, Petropoulos S, Lanner F, Novershtern N, Hanna JH (2023) Complete human day 14 post-implantation embryo models from naïve es cells. Nature 622, 562-573.
| Crossref | Google Scholar |

Park MH, Park JE, Kim MS, Lee KY, Hwang JY, Yun JI, Choi JH, Lee E, Lee ST (2016) Effects of extracellular matrix protein-derived signaling on the maintenance of the undifferentiated state of spermatogonial stem cells from porcine neonatal testis. Asian-Australasian Journal of Animal Sciences 29(10), 1398.
| Crossref | Google Scholar | PubMed |

Pendergraft SS, Sadri-Ardekani H, Atala A, Bishop CE (2017) Three-dimensional testicular organoid: a novel tool for the study of human spermatogenesis and gonadotoxicity in vitro. Biology of Reproduction 96(3), 720-732.
| Crossref | Google Scholar | PubMed |

Plant TM (2015) Neuroendocrine control of the onset of puberty. Frontiers in Neuroendocrinology 38, 73-88.
| Google Scholar |

Pollen AA, Bhaduri A, Andrews MG, Nowakowski TJ, Meyerson OS, Mostajo-Radji MA, Di Lullo E, Alvarado B, Bedolli M, Dougherty ML, Fiddes IT, Kronenberg ZN, Shuga J, Leyrat AA, West JA, Bershteyn M, Lowe CB, Pavlovic BJ, Salama SR, Haussler D, Eichler EE, Kriegstein AR (2019) Establishing cerebral organoids as models of human-specific brain evolution. Cell 176(4), 743-756.e17.
| Crossref | Google Scholar |

Portela JMD, de Winter-Korver CM, van Daalen SKM, Meißner A, de Melker AA, Repping S, van Pelt AMM (2019a) Assessment of fresh and cryopreserved testicular tissues from (pre)pubertal boys during organ culture as a strategy for in vitro spermatogenesis. Human Reproduction 34(12), 2443-2455.
| Crossref | Google Scholar | PubMed |

Portela JMD, Mulder CL, van Daalen SKM, de Winter-Korver CM, Stukenborg J-B, Repping S, van Pelt AMM (2019b) Strains matter: success of murine in vitro spermatogenesis is dependent on genetic background. Developmental Biology 456(1), 25-30.
| Crossref | Google Scholar | PubMed |

Pryzhkova MV, Jordan PW (2020) Adaptation of human testicular niche cells for pluripotent stem cell and testis development research. Tissue Engineering and Regenerative Medicine 17, 223-235.
| Crossref | Google Scholar |

Qian X, Su Y, Adam CD, Deutschmann AU, Pather SR, Goldberg EM, Su K, Li S, Lu L, Jacob F, Nguyen PTT, Huh S, Hoke A, Swinford-Jackson SE, Wen Z, Gu X, Pierce RC, Wu H, Briand LA, Chen HI, Wolf JA, Song H, Ming G-L (2020) Sliced human cortical organoids for modeling distinct cortical layer formation. Cell Stem Cell 26(5), 766-781.e9.
| Crossref | Google Scholar | PubMed |

Quadrato G, Nguyen T, Macosko EZ, Sherwood JL, Min Yang S, Berger DR, Maria N, Scholvin J, Goldman M, Kinney JP, Boyden ES, Lichtman JW, Williams ZM, McCarroll SA, Arlotta P (2017) Cell diversity and network dynamics in photosensitive human brain organoids. Nature 545(7652), 48-53.
| Crossref | Google Scholar | PubMed |

Reuter K, Ehmcke J, Stukenborg J-B, Simoni M, Damm OS, Redmann K, Schlatt S, Wistuba J (2014) Reassembly of somatic cells and testicular organogenesis in vitro. Tissue and Cell 46(1), 86-96.
| Crossref | Google Scholar | PubMed |

Rezaei Topraggaleh T, Rezazadeh Valojerdi M, Montazeri L, Baharvand H (2019) A testis-derived macroporous 3D scaffold as a platform for the generation of mouse testicular organoids. Biomaterials Science 7(4), 1422-1436.
| Crossref | Google Scholar | PubMed |

Rezende-Melo CA, Caldeira-Brant AL, Drumond-Bock AL, Buchold GM, Shetty G, Almeida FRCL, Matzuk MM, Hara K, Yoshida S, Meistrich ML, Chiarini-Garcia H (2020) Spermatogonial asynchrony in Tex14 mutant mice lacking intercellular bridges. Reproduction 160(2), 205-215.
| Crossref | Google Scholar | PubMed |

Richer G, Hobbs RM, Loveland KL, Goossens E, Baert Y (2021) Long-term maintenance and meiotic entry of early germ cells in murine testicular organoids functionalized by 3D printed scaffolds and air-medium interface cultivation. Frontiers in Physiology 12, 757565.
| Crossref | Google Scholar |

Robinson M, Bedford E, Witherspoon L, Willerth SM, Flannigan R (2022) Using clinically derived human tissue to 3-dimensionally bioprint personalized testicular tubules for in vitro culturing: first report. F&S Science 3(2), 130-139.
| Crossref | Google Scholar |

Sakib S, Uchida A, Valenzuela-Leon P, Yu Y, Valli-Pulaski H, Orwig K, Ungrin M, Dobrinski I (2019a) Formation of organotypic testicular organoids in microwell culture. Biology of Reproduction 100(6), 1648-1660.
| Crossref | Google Scholar | PubMed |

Sakib S, Yu Y, Voigt A, Ungrin M, Dobrinski I (2019b) Generation of porcine testicular organoids with testis specific architecture using microwell culture. Journal of Visualized Experiments 2019(152), e60387.
| Crossref | Google Scholar |

Sakib S, Lara NLM, Huynh BC, Dobrinski I (2022) Organotypic rat testicular organoids for the study of testicular maturation and toxicology. Frontiers in Endocrinology 13, 892342.
| Crossref | Google Scholar | PubMed |

Sallam HN, Sallam NH (2016) Religious aspects of assisted reproduction. Facts, Views & Vision in ObGyn 8(1), 33-48.
| Google Scholar | PubMed |

Sandheinrich T, Wondmeneh SB, Mohrmann C, Gettinger K, Henry J, Hayashi RJ (2018) Knowledge and perceptions of infertility in female cancer survivors and their parents. Supportive Care in Cancer 26, 2433-2439.
| Crossref | Google Scholar | PubMed |

Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ, Clevers H (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459(7244), 262-265.
| Crossref | Google Scholar | PubMed |

Sato T, Katagiri K, Gohbara A, Inoue K, Ogonuki N, Ogura A, Kubota Y, Ogawa T (2011) In vitro production of functional sperm in cultured neonatal mouse testes. Nature 471(7339), 504-507.
| Crossref | Google Scholar | PubMed |

Saulnier J, Oblette A, Delessard M, Dumont L, Rives A, Rives N, Rondanino C (2021) Improving freezing protocols and organotypic culture: a histological study on rat prepubertal testicular tissue. Annals of Biomedical Engineering 49(1), 203-218.
| Crossref | Google Scholar | PubMed |

Shi Y, Sun L, Wang M, Liu J, Zhong S, Li R, Li P, Guo L, Fang A, Chen R, Ge W-P, Wu Q, Wang X, Ye B (2020) Vascularized human cortical organoids (vOrganoids) model cortical development in vivo. PLoS Biology 18(5), e3000705.
| Crossref | Google Scholar | PubMed |

Sohni A, Tan K, Song H-W, Burow D, de Rooij DG, Laurent L, Hsieh T-C, Rabah R, Hammoud SS, Vicini E, Wilkinson MF (2019) The neonatal and adult human testis defined at the single-cell level. Cell Reports 26(6), 1501-1517.e4.
| Crossref | Google Scholar |

Song K, Yang X, An G, Xia X, Zhao J, Xu X, Wan C, Liu T, Zheng Y, Ren S, Wang M, Chang G, Cronin SJF, Penninger JM, Jing T, Ou X, Rao S, Liu Z, Zhao X-Y (2022) Targeting APLN/APJ restores blood-testis barrier and improves spermatogenesis in murine and human diabetic models. Nature Communications 13(1), 7335.
| Crossref | Google Scholar | PubMed |

Strange DP, Zarandi NP, Trivedi G, Atala A, Bishop CE, Sadri-Ardekani H, Verma S (2018) Human testicular organoid system as a novel tool to study Zika virus pathogenesis. Emerging Microbes & Infections 7(1), 1-7.
| Crossref | Google Scholar |

Stukenborg J-B, Wistuba J, Luetjens CM, Elhija MA, Huleihel M, Lunenfeld E, Gromoll J, Nieschlag E, Schlatt S (2008) Coculture of spermatogonia with somatic cells in a novel three-dimensional soft-agar-culture-system. Journal of Andrology 29(3), 312-329.
| Crossref | Google Scholar | PubMed |

Takashima S, Kanatsu-Shinohara M, Tanaka T, Morimoto H, Inoue K, Ogonuki N, Jijiwa M, Takahashi M, Ogura A, Shinohara T (2015) Functional differences between GDNF-dependent and FGF2-dependent mouse spermatogonial stem cell self-renewal. Stem Cell Reports 4(3), 489-502.
| Crossref | Google Scholar | PubMed |

Tang S, Jones C, Mecca R, Davies J, Lane S, Coward K (2024) An in vitro three-dimensional (3D) testicular organoid culture system for efficient gonocyte maintenance and propagation using frozen/thawed neonatal bovine testicular tissues. Biomedical Materials 19, 025040.
| Crossref | Google Scholar |

Thalheim T, Siebert S, Quaas M, Herberg M, Schweiger MR, Aust G, Galle J (2021) Epigenetic drifts during long-term intestinal organoid culture. Cells 10(7), 1718.
| Crossref | Google Scholar | PubMed |

Turner DA, Girgin M, Alonso-Crisostomo L, Trivedi V, Baillie-Johnson P, Glodowski CR, Hayward PC, Collignon J, Gustavsen C, Serup P, Steventon B, Lutolf MP, Arias AM (2017) Anteroposterior polarity and elongation in the absence of extra-embryonic tissues and of spatially localised signalling in gastruloids: mammalian embryonic organoids. Development 144(21), 3894-3906.
| Crossref | Google Scholar | PubMed |

Vallet-Buisan M, Mecca R, Jones C, Coward K, Yeste M (2023) Contribution of semen to early embryo development: fertilization and beyond. Human Reproduction Update 29, 395-433.
| Crossref | Google Scholar |

Vermeulen M, Del Vento F, Kanbar M, Pyr dit Ruys S, Vertommen D, Poels J, Wyns C (2019) Generation of organized porcine testicular organoids in solubilized hydrogels from decellularized extracellular matrix. International Journal of Molecular Sciences 20(21), 5476.
| Crossref | Google Scholar | PubMed |

Vlachogiannis G, Hedayat S, Vatsiou A, Jamin Y, Fernández-Mateos J, Khan K, Lampis A, Eason K, Huntingford I, Burke R, Rata M, Koh D-M, Tunariu N, Collins D, Hulkki-Wilson S, Ragulan C, Spiteri I, Moorcraft SY, Chau I, Rao S, Watkins D, Fotiadis N, Bali M, Darvish-Damavandi M, Lote H, Eltahir Z, Smyth EC, Begum R, Clarke PA, Hahne JC, Dowsett M, de Bono J, Workman P, Sadanandam A, Fassan M, Sansom OJ, Eccles S, Starling N, Braconi C, Sottoriva A, Robinson SP, Cunningham D, Valeri N (2018) Patient-derived organoids model treatment response of metastatic gastrointestinal cancers. Science 359(6378), 920-926.
| Crossref | Google Scholar | PubMed |

Voigt AL, de Lima e Martins Lara N, Dobrinski I (2023) Comparing the adult and pre-pubertal testis: metabolic transitions and the change in the spermatogonial stem cell metabolic microenvironment. Andrology 6, 1132-1146.
| Crossref | Google Scholar |

Xiang Y, Tanaka Y, Cakir B, Patterson B, Kim K-Y, Sun P, Kang Y-J, Zhong M, Liu X, Patra P, Lee S-H, Weissman SM, Park I-H (2019) hESC-derived thalamic organoids form reciprocal projections when fused with cortical organoids. Cell Stem Cell 24(3), 487-497.e7.
| Crossref | Google Scholar | PubMed |

Yang Y, Huang R, Cao Z, Ma S, Chen D, Wang Z, Feng Y, Lei Y, Zhang Q, Huang Y (2022) In vitro reconstitution of the hormone-responsive testicular organoids from murine primary testicular cells. Biofabrication 15(1), 015001.
| Crossref | Google Scholar |

Yang W, Zhang C, Wu Y-H, Liu L-B, Zhen Z-D, Fan D-Y, Song Z-R, Chang J-T, Wang P-G, An J (2023) Mice 3D testicular organoid system as a novel tool to study Zika virus pathogenesis. Virologica Sinica 38(1), 66-74.
| Crossref | Google Scholar | PubMed |

Yokonishi T, Sato T, Katagiri K, Komeya M, Kubota Y, Ogawa T (2013) In vitro reconstruction of mouse seminiferous tubules supporting germ cell differentiation1. Biology of Reproduction 89(1), 108613.
| Crossref | Google Scholar |

Yokonishi T, McKey J, Ide S, Capel B (2020) Sertoli cell ablation and replacement of the spermatogonial niche in mouse. Nature Communications 11(1), 40.
| Crossref | Google Scholar | PubMed |

Yuan Y, Li L, Cheng Q, Diao F, Zeng Q, Yang X, Wu Y, Zhang H, Huang M, Chen J, Zhou Q, Zhu Y, Hua R, Tian J, Wang X, Zhou Z, Hao J, Yu J, Hua D, Liu J, Guo X, Zhou Q, Sha J (2020) In vitro testicular organogenesis from human fetal gonads produces fertilization-competent spermatids. Cell Research 30(3), 244-255.
| Crossref | Google Scholar | PubMed |

Zhang Y, Wang S, Wang X, Liao S, Wu Y, Han C (2012) Endogenously produced FGF2 is essential for the survival and proliferation of cultured mouse spermatogonial stem cells. Cell Research 22(4), 773-776.
| Crossref | Google Scholar | PubMed |

Zheng WL, Bucco RA, Schmitt MC, Wardlaw SA, Ong DE (1996) Localization of cellular retinoic acid-binding protein (CRABP) II and CRABP in developing rat testis. Endocrinology 137(11), 5028-5035.
| Crossref | Google Scholar | PubMed |

Zheng X, Li Z, Wang G, Wang H, Zhou Y, Zhao X, Cheng CY, Qiao Y, Sun F (2021) Sperm epigenetic alterations contribute to inter-and transgenerational effects of paternal exposure to long-term psychological stress via evading offspring embryonic reprogramming. Cell Discovery 7(1), 101.
| Crossref | Google Scholar | PubMed |

Ziloochi Kashani M, Bagher Z, Asgari HR, Najafi M, Koruji M, Mehraein F (2020) Differentiation of neonate mouse spermatogonial stem cells on three-dimensional agar/polyvinyl alcohol nanofiber scaffold. Systems Biology in Reproductive Medicine 66(3), 202-215.
| Crossref | Google Scholar | PubMed |