Relevance, strategies, and added value of mouse models in androgenetics.

Λεπτομέρειες βιβλιογραφικής εγγραφής
Τίτλος: Relevance, strategies, and added value of mouse models in androgenetics.
Συγγραφείς: Singh V; Department of Biomedical Sciences, Cornell College of Veterinary Medicine, Ithaca, New York, USA., Schimenti JC; Department of Biomedical Sciences, Cornell College of Veterinary Medicine, Ithaca, New York, USA.; Department of Molecular Biology & Genetics, Cornell University, Ithaca, New York, USA.
Πηγή: Andrology [Andrology] 2025 Jul; Vol. 13 (5), pp. 1158-1169. Date of Electronic Publication: 2024 Sep 19.
Τύπος έκδοσης: Journal Article; Review; Research Support, N.I.H., Extramural
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Wiley-Blackwell Country of Publication: England NLM ID: 101585129 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2047-2927 (Electronic) Linking ISSN: 20472919 NLM ISO Abbreviation: Andrology Subsets: MEDLINE
Imprint Name(s): Original Publication: Oxford : Wiley-Blackwell, 2013-
Ιατρικοί όροι (MeSH): Infertility, Male*/genetics , Fertility*/genetics , Disease Models, Animal*, Animals ; Mice ; Male ; Humans ; Female ; Mice, Knockout ; Models, Animal
Περίληψη: Background: Male Infertility is a prevalent condition worldwide, and a substantial fraction of cases are thought to have a genetic basis. Investigations into the responsible genes is limited experimentally, so mice have been used extensively to identify genes required for fertility and to understand their functions.
Objectives: To review the progress made in reproductive genetics based on experiments in mice, the impact upon clinical fertility genetics, and discuss how evolving technologies will continue to advance our understanding of human infertility genes.
Results and Discussion: Gene knockout studies in mice have shown that several hundreds of genes are required for normal fertility and that this number is much higher in males than in females. In addition to gene discovery, the mouse is a powerful platform for functionally dissecting genetic pathways, modeling putative human infertility variants, identifying contraceptive targets, and developing in vitro gametogenesis.
Conclusion: These ongoing studies in mice have made an enormous contribution to our understanding of the genetics of human reproduction in the sense that the "parts list" of genes for mammalian gametogenesis is being elucidated. This would have been impossible to do in humans, and in vitro systems are not yet adequate to associate genes with andrological phenotypes, especially in the germline.
(© 2024 American Society of Andrology and European Academy of Andrology.)
References: Nugent CN, Chandra A. Infertility and impaired fecundity in women and men in the United States, 2015–2019. Natl Health Stat Rep. 2024(202):1‐19.
Jamsai D, O'Bryan MK. Mouse models in male fertility research. Asian J Androl. 2011;13(1):139‐151. doi:10.1038/aja.2010.101.
Lilford R, Jones AM, Bishop DT, Thornton J, Mueller R. Case‐control study of whether subfertility in men is familial. BMJ. 1994;309(6954):570‐573.
Xavier MJ, Salas‐Huetos A, Oud MS, Aston KI, Veltman JA. Disease gene discovery in male infertility: past, present and future. Hum Genet. 2021;140(1):7‐19. doi:10.1007/s00439‐020‐02202‐x.
Hwang K, Yatsenko AN, Jorgez CJ, et al. Mendelian genetics of male infertility. Ann N Y Acad Sci. 2010;1214:E1‐E17. doi:10.1111/j.1749‐6632.2010.05917.x.
Krausz C, Riera‐Escamilla A. Genetics of male infertility. Nat Rev Urol. 2018;15(6):369‐384. doi:10.1038/s41585‐018‐0003‐3.
Sudhakar DVS, Shah R, Gajbhiye RK. Genetics of male infertility—present and future: a narrative review. J Hum Reprod Sci. 2021;14(3):217‐227. doi:10.4103/jhrs.jhrs_115_21.
Aitken RJ, De Iuliis GN, Nixon B. The sins of our forefathers: paternal impacts on de novo mutation rate and development. Annu Rev Genet. 2020;54:1‐24. doi:10.1146/annurev‐genet‐112618‐043617.
Aitken RJ. Role of sperm DNA damage in creating de‐novo mutations in human offspring: the “post‐meiotic oocyte collusion” hypothesis. Reprod Biomed Online. 2022;45(1):109‐124. doi:10.1016/j.rbmo.2022.03.012.
Oud MS, Smits RM, Smith HE, et al. A de novo paradigm for male infertility. Nat Commun. 2022;13(1):154. doi:10.1038/s41467‐021‐27132‐8.
Kosova G, Scott NM, Niederberger C, Prins GS, Ober C. Genome‐wide association study identifies candidate genes for male fertility traits in humans. Am J Hum Genet. 2012;90(6):950‐961. doi:10.1016/j.ajhg.2012.04.016.
Aston KI. Genetic susceptibility to male infertility: news from genome‐wide association studies. Andrology. 2014;2(3):315‐321. doi:10.1111/j.2047‐2927.2014.00188.x.
Venkatesh SS, Wittemans LBL, Palmer DS, et al. Genome‐wide analyses identify 21 infertility loci and over 400 reproductive hormone loci across the allele frequency spectrum. medRxiv. 2024. doi:10.1101/2024.03.19.24304530. medRxiv.
Ding X, Singh P, Schimenti K, et al. In vivo versus in silico assessment of potentially pathogenic missense variants in human reproductive genes. Proc Natl Acad Sci USA. 2023;120(30):e2219925120. doi:10.1073/pnas.2219925120.
Waterston RH, Lindblad‐Toh K, Birney E, et al.; Mouse Genome Sequencing Consortium. Initial sequencing and comparative analysis of the mouse genome. Nature. 2002;420(6915):520‐562. doi:10.1038/nature01262.
Nocka K, Tan JC, Chiu E, et al. Molecular bases of dominant negative and loss of function mutations at the murine c‐kit/white spotting locus: w37, Wv, W41 and W. EMBO J. 1990;9(6):1805‐1813. doi:10.1002/j.1460‐2075.1990.tb08305.x.
Buaas FW, Kirsh AL, Sharma M, et al. Plzf is required in adult male germ cells for stem cell self‐renewal. Nat Genet. 2004;36(6):647‐652. doi:10.1038/ng1366.
Olds‐Clarke P. Models for male infertility: the t haplotypes. Rev Reprod. 1997;2(3):157‐164. doi:10.1530/ror.0.0020157.
Schimenti JC, Handel MA. Unpackaging the genetics of mammalian fertility: strategies to identify the “reproductive genome”. Biol Reprod. 2018;99(6):1119‐1128. doi:10.1093/biolre/ioy133.
Handel MA, Lessard C, Reinholdt L, Schimenti J, Eppig JJ. Mutagenesis as an unbiased approach to identify novel contraceptive targets. Mol Cell Endocrinol. 2006;250(1‐2):201‐205. doi:10.1016/j.mce.2005.12.046.
Qiao H, Prasada Rao HBD, Yang Y, et al. Antagonistic roles of ubiquitin ligase HEI10 and SUMO ligase RNF212 regulate meiotic recombination. Nat Genet. 2014;46(2):194‐199. doi:10.1038/ng.2858.
Ward JO, Reinholdt LG, Motley WW, et al. Mutation in mouse Hei10, an e3 ubiquitin ligase, disrupts meiotic crossing over. PLoS Genet. 2007;3(8):e139. doi:10.1371/journal.pgen.0030139.
Bannister LA, Reinholdt LG, Munroe RJ, Schimenti JC. Positional cloning and characterization of mouse mei8, a disrupted allele of the meiotic cohesin Rec8. Genesis. 2004;40(3):184‐194. doi:10.1002/gene.20085.
Libby BJ, De La Fuente R, O'Brien MJ, et al. The mouse meiotic mutation mei1 disrupts chromosome synapsis with sexually dimorphic consequences for meiotic progression. Dev Biol. 2002;242(2):174‐187. doi:10.1006/dbio.2001.0535.
Libby BJ, Reinholdt LG, Schimenti JC. Positional cloning and characterization of Mei1, a vertebrate‐specific gene required for normal meiotic chromosome synapsis in mice. Proc Natl Acad Sci USA. 2003;100(26):15706‐15711. doi:10.1073/pnas.2432067100.
Sato H, Miyamoto T, Yogev L, et al. Polymorphic alleles of the human MEI1 gene are associated with human azoospermia by meiotic arrest. J Hum Genet. 2006;51(6):533‐540. doi:10.1007/s10038‐006‐0394‐5.
Pattabiraman S, Baumann C, Guisado D, Eppig JJ, Schimenti JC, De La Fuente R. Mouse BRWD1 is critical for spermatid postmeiotic transcription and female meiotic chromosome stability. J Cell Biol. 2015;208(1):53‐69. doi:10.1083/jcb.201404109.
Philipps DL, Wigglesworth K, Hartford SA, et al. The dual bromodomain and WD repeat‐containing mouse protein BRWD1 is required for normal spermiogenesis and the oocyte‐embryo transition. Dev Biol. 2008;317(1):72‐82. doi:10.1016/j.ydbio.2008.02.018.
Li Z, Huang Y, Li H, et al. Excess of rare variants in genes that are key epigenetic regulators of spermatogenesis in the patients with non‐obstructive azoospermia. Sci Rep. 2015;5:8785. doi:10.1038/srep08785.
Guo T, Tu C‐F, Yang D‐H, et al. Bi‐allelic BRWD1 variants cause male infertility with asthenoteratozoospermia and likely primary ciliary dyskinesia. Hum Genet. 2021;140(5):761‐773. doi:10.1007/s00439‐020‐02241‐4.
Fulton SL, Wenderski W, Lepack AE, et al. Rescue of deficits by Brwd1 copy number restoration in the Ts65Dn mouse model of Down syndrome. Nat Commun. 2022;13(1):6384. doi:10.1038/s41467‐022‐34200‐0.
Jain D, Puno MR, Meydan C, et al. Ketu mutant mice uncover an essential meiotic function for the ancient RNA helicase YTHDC2. eLife. 2018;7:e30919. doi:10.7554/eLife.30919.
Bishop DK, Park D, Xu L, Kleckner N. DMC1: a meiosis‐specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell. 1992;69(3):439‐456. doi:10.1016/0092‐8674(92)90446‐j.
Keeney S, Giroux CN, Kleckner N. Meiosis‐specific DNA double‐strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell. 1997;88(3):375‐384. doi:10.1016/s0092‐8674(00)81876‐0.
de Vries FAT, de Boer E, van den Bosch M, et al. Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev. 2005;19(11):1376‐1389. doi:10.1101/gad.329705.
Shin Y‐H, Choi Y, Erdin SU, et al. Hormad1 mutation disrupts synaptonemal complex formation, recombination, and chromosome segregation in mammalian meiosis. PLoS Genet. 2010;6(11):e1001190. doi:10.1371/journal.pgen.1001190.
Sun S, Jiang Y, Zhang Q, et al. Znhit1 controls meiotic initiation in male germ cells by coordinating with Stra8 to activate meiotic gene expression. Dev Cell. 2022;57(7):901‐913. doi:10.1016/j.devcel.2022.03.006.
Bianchi E, Doe B, Goulding D, Wright GJ. Juno is the egg Izumo receptor and is essential for mammalian fertilization. Nature. 2014;508(7497):483‐487. doi:10.1038/nature13203.
Cho C, Willis WD, Goulding EH, et al. Haploinsufficiency of protamine‐1 or ‐2 causes infertility in mice. Nat Genet. 2001;28(1):82‐86. doi:10.1038/ng0501‐82.
Saitou M, Hayashi K. Mammalian in vitro gametogenesis. Science. 2021;374(6563):eaaz6830. doi:10.1126/science.aaz6830.
Skarnes WC. The identification of new genes: gene trapping in transgenic mice. Curr Opin Biotechnol. 1993;4(6):684‐689. doi:10.1016/0958‐1669(93)90050‐7.
Austin CP, Battey JF, Bradley A, et al. The knockout mouse project. Nat Genet. 2004;36(9):921‐924. doi:10.1038/ng0904‐921.
Peterson KA, Murray SA. Progress towards completing the mutant mouse null resource. Mamm Genome. 2022;33(1):123‐134. doi:10.1007/s00335‐021‐09905‐0.
Miyata H, Castaneda JM, Fujihara Y, et al. Genome engineering uncovers 54 evolutionarily conserved and testis‐enriched genes that are not required for male fertility in mice. Proc Natl Acad Sci USA. 2016;113(28):7704‐7710. doi:10.1073/pnas.1608458113.
Robey PG. Stem cells near the century mark. J Clin Invest. 2000;105(11):1489‐1491. doi:10.1172/JCI10256.
Holtzer H. Cell lineages, stem cells and the quantal cell cycle concept. in: Lord BI, Potten CS, Cole RJ, eds. Stem Cells and Tissue Homeostasis. Cambridge University Press; 1978:1‐27.
Ehmcke J, Wistuba J, Schlatt S. Spermatogonial stem cells: questions, models and perspectives. Hum Reprod Update. 2006;12(3):275‐282. doi:10.1093/humupd/dmk001.
Phillips BT, Gassei K, Orwig KE. Spermatogonial stem cell regulation and spermatogenesis. Philos Trans R Soc Lond B Biol Sci. 2010;365(1546):1663‐1678. doi:10.1098/rstb.2010.0026.
de Rooij DG. Stem cells in the testis. Int J Exp Pathol. 1998;79(2):67‐80. doi:10.1046/j.1365‐2613.1998.00057.x.
Dettin L, Ravindranath N, Hofmann M‐C, Dym M. Morphological characterization of the spermatogonial subtypes in the neonatal mouse testis. Biol Reprod. 2003;69(5):1565‐1571. doi:10.1095/biolreprod.103.016394.
Clermont Y, Bustos‐Obregon E. Re‐examination of spermatogonial renewal in the rat by means of seminiferous tubules mounted “in toto”. Am J Anat. 1968;122(2):237‐247. doi:10.1002/aja.1001220205.
Huckins C, Oakberg EF. Morphological and quantitative analysis of spermatogonia in mouse testes using whole mounted seminiferous tubules, I. The normal testes. Anat Rec. 1978;192(4):519‐528. doi:10.1002/ar.1091920406.
Hess RA. Quantitative and qualitative characteristics of the stages and transitions in the cycle of the rat seminiferous epithelium: light microscopic observations of perfusion‐fixed and plastic‐embedded testes. Biol Reprod. 1990;43(3):525‐542. doi:10.1095/biolreprod43.3.525.
Nakagawa T, Sharma M, Nabeshima Y, Braun RE, Yoshida S. Functional hierarchy and reversibility within the murine spermatogenic stem cell compartment. Science. 2010;328(5974):62‐67. doi:10.1126/science.1182868.
Brinster RL, Avarbock MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci USA. 1994;91(24):11303‐11307. doi:10.1073/pnas.91.24.11303.
Bucci LR, Meistrich ML. Effects of busulfan on murine spermatogenesis: cytotoxicity, sterility, sperm abnormalities, and dominant lethal mutations. Mutat Res. 1987;176(2):259‐268. doi:10.1016/0027‐5107(87)90057‐1.
Kubota H, Brinster RL. Spermatogonial stem cells. Biol Reprod. 2018;99(1):52‐74. doi:10.1093/biolre/ioy077.
Wu Y, Zhou H, Fan X, et al. Correction of a genetic disease by CRISPR‐Cas9‐mediated gene editing in mouse spermatogonial stem cells. Cell Res. 2015;25(1):67‐79. doi:10.1038/cr.2014.160.
Li X, Sun T, Wang X, Tang J, Liu Y. Restore natural fertility of Kitw/Kitwv mouse with nonobstructive azoospermia through gene editing on SSCs mediated by CRISPR‐Cas9. Stem Cell Res Ther. 2019;10(1):271. doi:10.1186/s13287‐019‐1386‐7.
Brinster RL. Male germline stem cells: from mice to men. Science. 2007;316(5823):404‐405. doi:10.1126/science.1137741.
Kubota H, Brinster RL. Technology insight: in vitro culture of spermatogonial stem cells and their potential therapeutic uses. Nat Clin Pract Endocrinol Metab. 2006;2(2):99‐108. doi:10.1038/ncpendmet0098.
Sanou I, van Maaren J, Eliveld J, et al. Spermatogonial stem cell‐based therapies: taking preclinical research to the next level. Front Endocrinol. 2022;13:850219. doi:10.3389/fendo.2022.850219.
Anderson RA, Mitchell RT, Kelsey TW, Spears N, Telfer EE, Wallace WHB. Cancer treatment and gonadal function: experimental and established strategies for fertility preservation in children and young adults. Lancet Diabetes Endocrinol. 2015;3(7):556‐567. doi:10.1016/S2213‐8587(15)00039‐X.
Goossens E, Jahnukainen K, Mitchell RT, et al. Fertility preservation in boys: recent developments and new insights†. Hum Reprod Open. 2020;2020(3):hoaa016. doi:10.1093/hropen/hoaa016.
Anzalone AV, Randolph PB, Davis JR, et al. Search‐and‐replace genome editing without double‐strand breaks or donor DNA. Nature. 2019;576(7785):149‐157. doi:10.1038/s41586‐019‐1711‐4.
Xia K, Wang F, Tan Z, et al. Precise correction of lhcgr mutation in stem Leydig cells by prime editing rescues hereditary primary hypogonadism in mice. Adv Sci. 2023;10(29):e2300993. doi:10.1002/advs.202300993.
Hofmann MC, Narisawa S, Hess RA, Millán JL. Immortalization of germ cells and somatic testicular cells using the SV40 large T antigen. Exp Cell Res. 1992;201(2):417‐435. doi:10.1016/0014‐4827(92)90291‐F.
Hofmann MC, Hess RA, Goldberg E, Millán JL. Immortalized germ cells undergo meiosis in vitro. Proc Natl Acad Sci USA. 1994;91(12):5533‐5537. doi:10.1073/pnas.91.12.5533.
Cyranoski D, Contreras JL, Carrington VT. Intellectual property and assisted reproductive technology. Nat Biotechnol. 2023;41(1):14‐20. doi:10.1038/s41587‐022‐01592‐9.
Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell. 2011;146(4):519‐532. doi:10.1016/j.cell.2011.06.052.
Khampang S, Cho IK, Punyawai K, et al. Blastocyst development after fertilization with in vitro spermatids derived from nonhuman primate embryonic stem cells. F&S Science. 2021;2(4):365‐375. doi:10.1016/j.xfss.2021.09.001.
Hirota T, Ohta H, Powell BE, et al. Fertile offspring from sterile sex chromosome trisomic mice. Science. 2017;357(6354):932‐935. doi:10.1126/science.aam9046.
Matzuk MM, Georg GI, Yan W. A special issue on contraceptive development: past, present, and future. Biol Reprod. 2020;103(2):145‐146. doi:10.1093/biolre/ioaa120.
Gaucher J, Boussouar F, Montellier E, et al. Bromodomain‐dependent stage‐specific male genome programming by Brdt. EMBO J. 2012;31(19):3809‐3820. doi:10.1038/emboj.2012.233.
Shang E, Nickerson HD, Wen D, Wang X, Wolgemuth DJ. The first bromodomain of Brdt, a testis‐specific member of the BET sub‐family of double‐bromodomain‐containing proteins, is essential for male germ cell differentiation. Development. 2007;134(19):3507‐3515. doi:10.1242/dev.004481.
Yu Z, Ku AF, Anglin JL, et al. Discovery and characterization of bromodomain 2‐specific inhibitors of BRDT. Proc Natl Acad Sci USA. 2021;118(9). doi:10.1073/pnas.2021102118.
Xu Y, Liu R, Leu NA, et al. A cell‐based high‐content screen identifies isocotoin as a small molecule inhibitor of the meiosis‐specific MEIOB‐SPATA22 complex†. Biol Reprod. 2020;103(2):333‐342. doi:10.1093/biolre/ioaa062.
Syeda SS, Sánchez G, McDermott JP, Hong KH, Blanco G, Georg GI. The Na+ and K+ transport system of sperm (ATP1A4) is essential for male fertility and an attractive target for male contraception†. Biol Reprod. 2020;103(2):343‐356. doi:10.1093/biolre/ioaa093.
Ding X, Schimenti JC. Strategies to identify genetic variants causing infertility. Trends Mol Med. 2021;27(8):792‐806. doi:10.1016/j.molmed.2020.12.008.
Singh P, Fragoza R, Blengini CS, et al. Human MLH1/3 variants causing aneuploidy, pregnancy loss, and premature reproductive aging. Nat Commun. 2021;12(1):5005. doi:10.1038/s41467‐021‐25028‐1.
Yamamoto S, Kanca O, Wangler MF, Bellen HJ. Integrating non‐mammalian model organisms in the diagnosis of rare genetic diseases in humans. Nat Rev Genet. 2024;25(1):46‐60. doi:10.1038/s41576‐023‐00633‐6.
Kherraf Z‐E, Cazin C, Bouker A, et al. Whole‐exome sequencing improves the diagnosis and care of men with non‐obstructive azoospermia. Am J Hum Genet. 2022;109(3):508‐517. doi:10.1016/j.ajhg.2022.01.011.
Zhang Y, Li N, Ji Z, et al. Bi‐allelic MEI1 variants cause meiosis arrest and non‐obstructive azoospermia. J Hum Genet. 2023;68(6):383‐392. doi:10.1038/s10038‐023‐01119‐3.
Mori T, Kurahashi H, Shinka T, et al. Candidate genes for male factor infertility–validation. Fertil Steril. 2006;86(5):1553‐1554. doi:10.1016/j.fertnstert.2006.05.011. author reply 1554.
Hwang JY, Chung J‐J. Catsper calcium channels: 20 years on. Physiology. 2023;38(3):0. doi:10.1152/physiol.00028.2022.
Qi H, Moran MM, Navarro B, et al. All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc Natl Acad Sci USA. 2007;104(4):1219‐1223. doi:10.1073/pnas.0610286104.
Young S, Schiffer C, Wagner A, et al. Human fertilization in vivo and in vitro requires the CatSper channel to initiate sperm hyperactivation. J Clin Invest. 2024;134(1):e173564. doi:10.1172/JCI173564.
Jean C, Haghighirad F, Zhu Y, et al. JUNO, the receptor of sperm IZUMO1, is expressed by the human oocyte and is essential for human fertilisation. Hum Reprod. 2019;34(1):118‐126. doi:10.1093/humrep/dey340.
Cooke HJ, Saunders PTK. Mouse models of male infertility. Nat Rev Genet. 2002;3(10):790‐801. doi:10.1038/nrg911.
Eicher EM, Hutchison KW, Phillips SJ, Tucker PK, Lee BK. A repeated segment on the mouse Y chromosome is composed of retroviral‐related, Y‐enriched and Y‐specific sequences. Genetics. 1989;122(1):181‐192. doi:10.1093/genetics/122.1.181.
Morgan AP, Pardo‐Manuel de Villena F. Sequence and structural diversity of mouse Y chromosomes. Mol Biol Evol. 2017;34(12):3186‐3204. doi:10.1093/molbev/msx250.
Nishioka Y, Lamothe E. Isolation and characterization of a mouse Y chromosomal repetitive sequence. Genetics. 1986;113(2):417‐432. doi:10.1093/genetics/113.2.417.
Hughes JF, Page DC. The biology and evolution of mammalian Y chromosomes. Annu Rev Genet. 2015;49:507‐527. doi:10.1146/annurev‐genet‐112414‐055311.
Kuroda‐Kawaguchi T, Skaletsky H, Brown LG, et al. The AZFc region of the Y chromosome features massive palindromes and uniform recurrent deletions in infertile men. Nat Genet. 2001;29(3):279‐286. doi:10.1038/ng757.
Ruggiu M, Speed R, Taggart M, et al. The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature. 1997;389(6646):73‐77. doi:10.1038/37987.
Jequier AM, Ansell ID, Bullimore NJ. Congenital absence of the vasa deferentia presenting with infertility. J Androl. 1985;6(1):15‐19.
O'Neal WK, Hasty P, McCray PB, et al. A severe phenotype in mice with a duplication of exon 3 in the cystic fibrosis locus. Hum Mol Genet. 1993;2(10):1561‐1569. doi:10.1093/hmg/2.10.1561.
Berletch JB, Yang F, Disteche CM. Escape from X inactivation in mice and humans. Genome Biol. 2010;11(6):213. doi:10.1186/gb‐2010‐11‐6‐213.
San Roman AK, Godfrey AK, Skaletsky H, et al. The human inactive X chromosome modulates expression of the active X chromosome. Cell Genomics. 2023;3(2):100259. doi:10.1016/j.xgen.2023.100259.
San Roman AK, Skaletsky H, Godfrey AK, et al. The human Y and inactive X chromosomes similarly modulate autosomal gene expression. Cell Genomics. 2024;4(1):100462. doi:10.1016/j.xgen.2023.100462.
Taylor K, Alvarez LR. An estimate of the number of animals used for scientific purposes worldwide in 2015. Altern Lab Anim. 2019;47(5‐6):196‐213. doi:10.1177/0261192919899853.
Hackett J, Gibson H, Frelinger J, Buntzman A. Using the collaborative cross and diversity outbred mice in immunology. Curr Protoc. 2022;2(9):e547. doi:10.1002/cpz1.547.
Voelkl B, Altman NS, Forsman A, et al. Reproducibility of animal research in light of biological variation. Nat Rev Neurosci. 2020;21(7):384‐393. doi:10.1038/s41583‐020‐0313‐3.
Saul MC, Philip VM, Reinholdt LG, Chesler EJ. High‐diversity mouse populations for complex traits. Trends Genet. 2019;35(7):501‐514. doi:10.1016/j.tig.2019.04.003.
Shorter JR, Odet F, Aylor DL, et al. Male infertility is responsible for nearly half of the extinction observed in the mouse collaborative cross. Genetics. 2017;206(2):557‐572. doi:10.1534/genetics.116.199596.
Cheng J, Novati G, Pan J, et al. Accurate proteome‐wide missense variant effect prediction with AlphaMissense. Science. 2023;381(6664):eadg7492. doi:10.1126/science.adg7492.
Grant Information: R01 HD082568 United States HD NICHD NIH HHS; R01 HD082568 United States NH NIH HHS
Contributed Indexing: Keywords: gene editing; in vitro gametogenesis; infertility; mouse
Entry Date(s): Date Created: 20240920 Date Completed: 20250624 Latest Revision: 20260619
Update Code: 20260620
DOI: 10.1111/andr.13761
PMID: 39300831
Βάση Δεδομένων: MEDLINE
Περιγραφή
ISSN:2047-2927
DOI:10.1111/andr.13761