Transcriptomic landscape reveals germline potential of porcine skin-derived multipotent dermal fibroblast progenitors.
MAPK signaling pathway
Multipotent dermal fibroblast progenitors
Primordial germ cell‐like cells
Single-cell transcriptomes
Skin-derived stem cells
Journal
Cellular and molecular life sciences : CMLS
ISSN: 1420-9071
Titre abrégé: Cell Mol Life Sci
Pays: Switzerland
ID NLM: 9705402
Informations de publication
Date de publication:
22 Jul 2023
22 Jul 2023
Historique:
received:
16
03
2023
accepted:
10
07
2023
revised:
15
06
2023
medline:
15
8
2023
pubmed:
22
7
2023
entrez:
22
7
2023
Statut:
epublish
Résumé
According to estimations, approximately about 15% of couples worldwide suffer from infertility, in which individuals with azoospermia or oocyte abnormalities cannot be treated with assisted reproductive technology. The skin-derived stem cells (SDSCs) differentiation into primordial germ cell-like cells (PGCLCs) is one of the major breakthroughs in the field of stem cells intervention for infertility treatment in recent years. However, the cellular origin of SDSCs and their dynamic changes in transcription profile during differentiation into PGCLCs in vitro remain largely undissected. Here, the results of single-cell RNA sequencing indicated that porcine SDSCs are mainly derived from multipotent dermal fibroblast progenitors (MDFPs), which are regulated by growth factors (EGF/bFGF). Importantly, porcine SDSCs exhibit pluripotency for differentiating into three germ layers and can effectively differentiate into PGCLCs through complex transcriptional regulation involving histone modification. Moreover, this study also highlights that porcine SDSC-derived PGCLCs specification exhibit conservation with the human primordial germ cells lineage and that its proliferation is mediated by the MAPK signaling pathway. Our findings provide substantial novel insights into the field of regenerative medicine in which stem cells differentiate into germ cells in vitro, as well as potential therapeutic effects in individuals with azoospermia and/or defective oocytes.
Identifiants
pubmed: 37480481
doi: 10.1007/s00018-023-04869-7
pii: 10.1007/s00018-023-04869-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
224Subventions
Organisme : National Natural Science Foundation of China
ID : 32072734
Organisme : National Natural Science Foundation of China
ID : 32100683
Organisme : Natural Science Foundation of Shandong Province
ID : ZR2021QC003
Organisme : Natural Science Foundation of Shandong Province
ID : ZR2021QC041
Organisme : Taishan Scholar Foundation of Shandong Province
ID : ts20190946
Organisme : Taishan Scholar Foundation of Shandong Province
ID : tsqn202211194
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Switzerland AG.
Références
Agarwal A, Mulgund A, Hamada A, Chyatte MR (2015) A unique view on male infertility around the globe. Reprod Biol Endocrinol 13:37. https://doi.org/10.1186/s12958-015-0032-1 . (Epub 2015/05/01)
doi: 10.1186/s12958-015-0032-1
pubmed: 25928197
pmcid: 4424520
Qiao J, Wang ZB, Feng HL, Miao YL, Wang Q, Yu Y, Wei YC, Yan J, Wang WH, Shen W, Sun SC, Schatten H, Sun QY (2014) The root of reduced fertility in aged women and possible therapentic options: current status and future perspects. Mol Aspects Med 38:54–85. https://doi.org/10.1016/j.mam.2013.06.001 . (Epub 2013/06/26)
doi: 10.1016/j.mam.2013.06.001
pubmed: 23796757
Mouka A, Tachdjian G, Dupont J, Drevillon L, Tosca L (2016) In vitro gamete differentiation from pluripotent stem cells as a promising therapy for infertility. Stem Cells Dev 25(7):509–521. https://doi.org/10.1089/scd.2015.0230 . (Epub 2016/02/14)
doi: 10.1089/scd.2015.0230
pubmed: 26873432
Ge W, Chen C, De Felici M, Shen W (2015) In vitro differentiation of germ cells from stem cells: a comparison between primordial germ cells and in vitro derived primordial germ cell-like cells. Cell Death Dis 6(10):e1906. https://doi.org/10.1038/cddis.2015.265 . (Epub 2015/10/16)
doi: 10.1038/cddis.2015.265
pubmed: 26469955
pmcid: 4632295
Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M (2011) Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146(4):519–532. https://doi.org/10.1016/j.cell.2011.06.052 . (Epub 2011/08/09)
doi: 10.1016/j.cell.2011.06.052
pubmed: 21820164
Zhou Q, Wang M, Yuan Y, Wang X, Fu R, Wan H, Xie M, Liu M, Guo X, Zheng Y, Feng G, Shi Q, Zhao XY, Sha J, Zhou Q (2016) Complete meiosis from embryonic stem cell-derived germ cells in vitro. Cell Stem Cell 18(3):330–340. https://doi.org/10.1016/j.stem.2016.01.017 . (Epub 2016/03/01)
doi: 10.1016/j.stem.2016.01.017
pubmed: 26923202
Liu WX, Tan SJ, Wang YF, Zhang FL, Feng YQ, Ge W, Dyce PW, Reiter RJ, Shen W, Cheng SF (2022) Melatonin promotes the proliferation of primordial germ cell-like cells derived from porcine skin-derived stem cells: a mechanistic analysis. J Pineal Res 73(4):e12833. https://doi.org/10.1111/jpi.12833 . (Epub 2022/09/16)
doi: 10.1111/jpi.12833
pubmed: 36106819
Zhao XY, Li W, Lv Z, Liu L, Tong M, Hai T, Hao J, Guo CL, Ma QW, Wang L, Zeng F, Zhou Q (2009) iPS cells produce viable mice through tetraploid complementation. Nature 461(7260):86–90. https://doi.org/10.1038/nature08267 . (Epub 2009/08/13)
doi: 10.1038/nature08267
pubmed: 19672241
Irie N, Weinberger L, Tang WW, Kobayashi T, Viukov S, Manor YS, Dietmann S, Hanna JH, Surani MA (2015) SOX17 is a critical specifier of human primordial germ cell fate. Cell 160(1–2):253–268. https://doi.org/10.1016/j.cell.2014.12.013 . (Epub 2014/12/30)
doi: 10.1016/j.cell.2014.12.013
pubmed: 25543152
pmcid: 4310934
Zhu Q, Sang F, Withey S, Tang W, Dietmann S, Klisch D, Ramos-Ibeas P, Zhang H, Requena CE, Hajkova P, Loose M, Surani MA, Alberio R (2021) Specification and epigenomic resetting of the pig germline exhibit conservation with the human lineage. Cell Rep 34(6):108735. https://doi.org/10.1016/j.celrep.2021.108735 . (Epub 2021/02/11)
doi: 10.1016/j.celrep.2021.108735
pubmed: 33567277
pmcid: 7873836
Grabole N, Tischler J, Hackett JA, Kim S, Tang F, Leitch HG, Magnusdottir E, Surani MA (2013) Prdm14 promotes germline fate and naive pluripotency by repressing FGF signalling and DNA methylation. EMBO Rep 14(7):629–637. https://doi.org/10.1038/embor.2013.67 . (Epub 2013/05/15)
doi: 10.1038/embor.2013.67
pubmed: 23670199
pmcid: 3701237
Gutierrez K, Dicks N, Glanzner WG, Agellon LB, Bordignon V (2015) Efficacy of the porcine species in biomedical research. Front Genet 6:293. https://doi.org/10.3389/fgene.2015.00293 . (Epub 2015/10/07)
doi: 10.3389/fgene.2015.00293
pubmed: 26442109
pmcid: 4584988
Walters EM, Wells KD, Bryda EC, Schommer S, Prather RS (2017) Swine models, genomic tools and services to enhance our understanding of human health and diseases. Lab Anim (N Y) 46(4):167–172. https://doi.org/10.1038/laban.1215 . (Epub 2017/03/23)
doi: 10.1038/laban.1215
Kobayashi T, Zhang H, Tang WWC, Irie N, Withey S, Klisch D, Sybirna A, Dietmann S, Contreras DA, Webb R, Allegrucci C, Alberio R, Surani MA (2017) Principles of early human development and germ cell program from conserved model systems. Nature 546(7658):416–420. https://doi.org/10.1038/nature22812 . (Epub 2017/06/14)
doi: 10.1038/nature22812
pubmed: 28607482
pmcid: 5473469
Kanemura H, Go MJ, Shikamura M, Nishishita N, Sakai N, Kamao H, Mandai M, Morinaga C, Takahashi M, Kawamata S (2014) Tumorigenicity studies of induced pluripotent stem cell (iPSC)-derived retinal pigment epithelium (RPE) for the treatment of age-related macular degeneration. PLoS ONE 9(1):e85336. https://doi.org/10.1371/journal.pone.0085336 . (Epub 2014/01/24)
doi: 10.1371/journal.pone.0085336
pubmed: 24454843
pmcid: 3891869
Golchin A, Chatziparasidou A, Ranjbarvan P, Niknam Z, Ardeshirylajimi A (2021) Embryonic stem cells in clinical trials: current overview of developments and challenges. Adv Exp Med Biol 1312:19–37. https://doi.org/10.1007/5584_2020_592 . (Epub 2020/11/08)
doi: 10.1007/5584_2020_592
pubmed: 33159303
Sun R, Sun YC, Ge W, Tan H, Cheng SF, Yin S, Sun XF, Li L, Dyce P, Li J, Yang X, Shi QH, Shen W (2015) The crucial role of Activin A on the formation of primordial germ cell-like cells from skin-derived stem cells in vitro. Cell Cycle 14(19):3016–3029. https://doi.org/10.1080/15384101.2015.1078031 . (Epub 2015/09/26)
doi: 10.1080/15384101.2015.1078031
pubmed: 26406115
pmcid: 4825550
Ge W, Ma HG, Cheng SF, Sun YC, Sun LL, Sun XF, Li L, Dyce P, Li J, Shi QH, Shen W (2015) Differentiation of early germ cells from human skin-derived stem cells without exogenous gene integration. Sci Rep 5:13822. https://doi.org/10.1038/srep13822 . (Epub 2015/09/09)
doi: 10.1038/srep13822
pubmed: 26347377
pmcid: 4561906
Ge W, Cheng SF, Dyce PW, De Felici M, Shen W (2016) Skin-derived stem cells as a source of primordial germ cell- and oocyte-like cells. Cell Death Dis 7(11):e2471. https://doi.org/10.1038/cddis.2016.366 . (Epub 2016/11/11)
doi: 10.1038/cddis.2016.366
pubmed: 27831564
pmcid: 5260893
Zheng Y, Du X, Wang W, Boucher M, Parimoo S, Stenn K (2005) Organogenesis from dissociated cells: generation of mature cycling hair follicles from skin-derived cells. J Investig Dermatol 124(5):867–876. https://doi.org/10.1111/j.0022-202X.2005.23716.x . (Epub 2005/04/28)
doi: 10.1111/j.0022-202X.2005.23716.x
pubmed: 15854024
Sriram G, Bigliardi PL, Bigliardi-Qi M (2015) Fibroblast heterogeneity and its implications for engineering organotypic skin models in vitro. Eur J Cell Biol 94(11):483–512. https://doi.org/10.1016/j.ejcb.2015.08.001 . (Epub 2015/09/08)
doi: 10.1016/j.ejcb.2015.08.001
pubmed: 26344860
Driskell RR, Lichtenberger BM, Hoste E, Kretzschmar K, Simons BD, Charalambous M, Ferron SR, Herault Y, Pavlovic G, Ferguson-Smith AC, Watt FM (2013) Distinct fibroblast lineages determine dermal architecture in skin development and repair. Nature 504(7479):277–281. https://doi.org/10.1038/nature12783 . (Epub 2013/12/18)
doi: 10.1038/nature12783
pubmed: 24336287
pmcid: 3868929
Ge W, Tan SJ, Wang SH, Li L, Sun XF, Shen W, Wang X (2020) Single-cell transcriptome profiling reveals dermal and epithelial cell fate decisions during embryonic hair follicle development. Theranostics 10(17):7581–7598. https://doi.org/10.7150/thno.4430 . (Epub 2020/07/216)
doi: 10.7150/thno.4430
pubmed: 32685006
pmcid: 7359078
Ge W, Zhang W, Zhang Y, Zheng Y, Li F, Wang S, Liu J, Tan S, Yan Z, Wang L, Shen W, Qu L, Wang X (2021) A single-cell transcriptome atlas of cashmere goat hair follicle morphogenesis. Genom Proteo Bioinform. https://doi.org/10.1016/j.gpb.2021.07.003 . (Epub 2021/09/18)
doi: 10.1016/j.gpb.2021.07.003
Linher K, Dyce P, Li J (2009) Primordial germ cell-like cells differentiated in vitro from skin-derived stem cells. PLoS ONE 4(12):e8263. https://doi.org/10.1371/journal.pone.0008263 . (Epub 2009/12/17)
doi: 10.1371/journal.pone.0008263
pubmed: 20011593
pmcid: 2788220
Zhang MY, Tian Y, Zhang SE, Yan HC, Ge W, Han BQ, Yan ZH, Cheng SF, Shen W (2021) The proliferation role of LH on porcine primordial germ cell-like cells (pPGCLCs) through ceRNA network construction. Clin Transl Med 11(10):e560. https://doi.org/10.1002/ctm2.560 . (Epub 2021/10/29)
doi: 10.1002/ctm2.560
pubmed: 34709759
pmcid: 8516341
Yan HC, Li L, Liu JC, Wang YF, Liu XL, Ge W, Dyce PW, Li L, Sun XF, Shen W, Cheng SF (2019) RA promotes proliferation of primordial germ cell-like cells differentiated from porcine skin-derived stem cells. J Cell Physiol 234(10):18214–18229. https://doi.org/10.1002/jcp.28454 . (Epub 2019/03/13)
doi: 10.1002/jcp.28454
pubmed: 30859584
Dyce PW, Wen L, Li J (2006) In vitro germline potential of stem cells derived from fetal porcine skin. Nat Cell Biol 8(4):384–390. https://doi.org/10.1038/ncb1388 . (Epub 2006/03/28)
doi: 10.1038/ncb1388
pubmed: 16565707
Lai FN, Liu XL, Li N, Zhang RQ, Zhao Y, Feng YZ, Nyachoti CM, Shen W, Li L (2018) Phosphatidylcholine could protect the defect of zearalenone exposure on follicular development and oocyte maturation. Aging (Albany N Y) 10(11):3486–3506. https://doi.org/10.1863/aging.101660 . (Epub 2018/11/26)
doi: 10.1863/aging.101660
Em A (2007) Isolation and propagation of mouse embryonic fibroblasts and preparation of mouse embryonic feeder layer cells. Curr Protoc Stem Cell Biol Chapter 1(Unit1C):3. https://doi.org/10.1002/9780470151808.sc01c03s3 . (Epub 2008/09/12)
doi: 10.1002/9780470151808.sc01c03s3
Stuart T, Butler A, Hoffman P, Hafemeister C, Papalexi E, Mauck WM 3rd, Hao Y, Stoeckius M, Smibert P, Satija R (2019) Comprehensive integration of single-cell data. Cell 177(7):1888–902.e21. https://doi.org/10.1016/j.cell.2019.05.031 . (Epub 2019/06/11)
doi: 10.1016/j.cell.2019.05.031
pubmed: 31178118
pmcid: 6687398
Butler A, Hoffman P, Smibert P, Papalexi E, Satija R (2018) Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat Biotechnol 36(5):411–420. https://doi.org/10.1038/nbt.4096 . (Epub 2018/04/03)
doi: 10.1038/nbt.4096
pubmed: 29608179
pmcid: 6700744
Niu W, Spradling AC (2020) Two distinct pathways of pregranulosa cell differentiation support follicle formation in the mouse ovary. Proc Natl Acad Sci USA 117(33):20015–20026. https://doi.org/10.1073/pnas.2005570117 . (Epub 2020/08/08)
doi: 10.1073/pnas.2005570117
pubmed: 32759216
pmcid: 7443898
Street K, Risso D, Fletcher RB, Das D, Ngai J, Yosef N, Purdom E, Dudoit S (2018) Slingshot: cell lineage and pseudotime inference for single-cell transcriptomics. BMC Genomics 19(1):477. https://doi.org/10.1186/s12864-018-4772-0 . (Epub 20180619)
doi: 10.1186/s12864-018-4772-0
pubmed: 29914354
pmcid: 6007078
Liu WX, Donatella F, Tan SJ, Ge W, Wang JJ, Sun XF, Cheng SF, Shen W (2021) Detrimental effect of Bisphenol S in mouse germ cell cyst breakdown and primordial follicle assembly. Chemosphere 264(Pt 1):128445. https://doi.org/10.1016/j.chemosphere.2020.128445 . (Epub 2020/10/06)
doi: 10.1016/j.chemosphere.2020.128445
pubmed: 33017704
Liu WX, Tan SJ, Wang YF, Li L, Sun XF, Liu J, Klinger FG, De Felici M, Shen W, Cheng SF (2020) Melatonin ameliorates murine fetal oocyte meiotic dysfunction in F1 and F2 offspring caused by nicotine exposure during pregnancy. Environ Pollut 263(Pt A):114519. https://doi.org/10.1016/j.envpol.2020.114519 . (Epub 2020/04/24)
doi: 10.1016/j.envpol.2020.114519
pubmed: 32325354
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262 . (Epub 2002/02/16)
doi: 10.1006/meth.2001.1262
pubmed: 11846609
Yu G, Wang LG, Han Y, He QY (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16(5):284–287. https://doi.org/10.1089/omi.2011.0118 . (Epub 20120328)
doi: 10.1089/omi.2011.0118
pubmed: 22455463
pmcid: 3339379
Gupta K, Levinsohn J, Linderman G, Chen D, Sun TY, Dong D, Taketo MM, Bosenberg M, Kluger Y, Choate K, Myung P (2019) Single-cell analysis reveals a hair follicle dermal niche molecular differentiation trajectory that begins prior to morphogenesis. Dev Cell 48(1):17 e6-31 e6. https://doi.org/10.1016/j.devcel.2018.11.032 . (Epub 2019/01/01)
doi: 10.1016/j.devcel.2018.11.032
Deng CC, Hu YF, Zhu DH, Cheng Q, Gu JJ, Feng QL, Zhang LX, Xu YP, Wang D, Rong Z, Yang B (2021) Single-cell RNA-seq reveals fibroblast heterogeneity and increased mesenchymal fibroblasts in human fibrotic skin diseases. Nat Commun 12(1):3709. https://doi.org/10.1038/s41467-021-24110-y . (Epub 2021/06/19)
doi: 10.1038/s41467-021-24110-y
pubmed: 34140509
pmcid: 8211847
Ascension AM, Fuertes-Alvarez S, Ibanez-Sole O, Izeta A, Arauzo-Bravo MJ (2021) Human dermal fibroblast subpopulations are conserved across single-cell RNA sequencing studies. J Investig Dermatol 141(7):1735 e35-1744 e35. https://doi.org/10.1016/j.jid.2020.11.028 . (Epub 2021/01/02)
doi: 10.1016/j.jid.2020.11.028
Detmar M, Brown LF, Schon MP, Elicker BM, Velasco P, Richard L, Fukumura D, Monsky W, Claffey KP, Jain RK (1998) Increased microvascular density and enhanced leukocyte rolling and adhesion in the skin of VEGF transgenic mice. J Investig Dermatol 111(1):1–6. https://doi.org/10.1046/j.1523-1747.1998.00262.x . (Epub 1998/07/17)
doi: 10.1046/j.1523-1747.1998.00262.x
pubmed: 9665379
Kaucka M, Szarowska B, Kavkova M, Kastriti ME, Kameneva P, Schmidt I, Peskova L, Joven Araus A, Simon A, Kaiser J, Adameyko I (2021) Nerve-associated Schwann cell precursors contribute extracutaneous melanocytes to the heart, inner ear, supraorbital locations and brain meninges. Cell Mol Life Sci 78(16):6033–6049. https://doi.org/10.1007/s00018-021-03885-9 . (Epub 2021/07/19)
doi: 10.1007/s00018-021-03885-9
pubmed: 34274976
pmcid: 8316242
Fung CW, Zhou S, Zhu H, Wei X, Wu Z, Wu AR (2022) Cell fate determining molecular switches and signaling pathways in Pax7-expressing somitic mesoderm. Cell Discov 8(1):61. https://doi.org/10.1038/s41421-022-00407-0 . (Epub 2022/06/29)
doi: 10.1038/s41421-022-00407-0
pubmed: 35764624
pmcid: 9240041
Bondjers C, He L, Takemoto M, Norlin J, Asker N, Hellstrom M, Lindahl P, Betsholtz C (2006) Microarray analysis of blood microvessels from PDGF-B and PDGF-Rbeta mutant mice identifies novel markers for brain pericytes. FASEB J 20(10):1703–1705. https://doi.org/10.1096/fj.05-4944fje . (Epub 2006/06/30)
doi: 10.1096/fj.05-4944fje
pubmed: 16807374
Garcia FJ, Sun N, Lee H, Godlewski B, Mathys H, Galani K, Zhou B, Jiang X, Ng AP, Mantero J, Tsai LH, Bennett DA, Sahin M, Kellis M, Heiman M (2022) Single-cell dissection of the human brain vasculature. Nature 603(7903):893–899. https://doi.org/10.1038/s41586-022-04521-7 . (Epub 2022/02/15)
doi: 10.1038/s41586-022-04521-7
pubmed: 35158371
pmcid: 9680899
Pelekanou V, Villarroel-Espindola F, Schalper KA, Pusztai L, Rimm DL (2018) CD68, CD163, and matrix metalloproteinase 9 (MMP-9) co-localization in breast tumor microenvironment predicts survival differently in ER-positive and -negative cancers. Breast Cancer Res 20(1):154. https://doi.org/10.1186/s13058-018-1076-x . (Epub 2018/12/19)
doi: 10.1186/s13058-018-1076-x
pubmed: 30558648
pmcid: 6298021
Zhang Q, He Y, Luo N, Patel SJ, Han Y, Gao R, Modak M, Carotta S, Haslinger C, Kind D, Peet GW, Zhong G, Lu S, Zhu W, Mao Y, Xiao M, Bergmann M, Hu X, Kerkar SP, Vogt AB, Pflanz S, Liu K, Peng J, Ren X, Zhang Z (2019) Landscape and dynamics of single immune cells in hepatocellular carcinoma. Cell 179(4):829–845. https://doi.org/10.1016/j.cell.2019.10.003 . (Epub 2019/11/02)
doi: 10.1016/j.cell.2019.10.003
pubmed: 31675496
Saxena N, Mok KW, Rendl M (2019) An updated classification of hair follicle morphogenesis. Exp Dermatol 28(4):332–344. https://doi.org/10.1111/exd.13913 . (Epub 2019/03/20)
doi: 10.1111/exd.13913
pubmed: 30887615
pmcid: 7137758
Fan A, Ma K, An X, Ding Y, An P, Song G, Tang L, Zhang S, Zhang P, Tan W, Tang B, Zhang X, Li Z (2013) Effects of TET1 knockdown on gene expression and DNA methylation in porcine induced pluripotent stem cells. Reproduction 146(6):569–579. https://doi.org/10.1530/REP-13-0212 . (Epub 2013/09/21)
doi: 10.1530/REP-13-0212
pubmed: 24051058
Pan Y, Liu Z, Shen J, Kopan R (2005) Notch1 and 2 cooperate in limb ectoderm to receive an early Jagged2 signal regulating interdigital apoptosis. Dev Biol 286(2):472–482. https://doi.org/10.1016/j.ydbio.2005.08.037 . (Epub 2005/09/20)
doi: 10.1016/j.ydbio.2005.08.037
pubmed: 16169548
Cortes F, Debacker C, Peault B, Labastie MC (1999) Differential expression of KDR/VEGFR-2 and CD34 during mesoderm development of the early human embryo. Mech Dev 83(1–2):161–164. https://doi.org/10.1016/s0925-4773(99)00030-1 . (Epub 1999/06/25)
doi: 10.1016/s0925-4773(99)00030-1
pubmed: 10381576
Barnes RM, Firulli BA, VanDusen NJ, Morikawa Y, Conway SJ, Cserjesi P, Vincentz JW, Firulli AB (2011) Hand2 loss-of-function in Hand1-expressing cells reveals distinct roles in epicardial and coronary vessel development. Circ Res 108(8):940–949. https://doi.org/10.1161/CIRCRESAHA.110.233171 . (Epub 2011/02/26)
doi: 10.1161/CIRCRESAHA.110.233171
pubmed: 21350214
pmcid: 3086599
Burtscher I, Lickert H (2009) Foxa2 regulates polarity and epithelialization in the endoderm germ layer of the mouse embryo. Development 136(6):1029–1038. https://doi.org/10.1242/dev.028415 . (Epub 2009/02/24)
doi: 10.1242/dev.028415
pubmed: 19234065
Tang WW, Dietmann S, Irie N, Leitch HG, Floros VI, Bradshaw CR, Hackett JA, Chinnery PF, Surani MA (2015) A unique gene regulatory network resets the human germline epigenome for development. Cell 161(6):1453–1467. https://doi.org/10.1016/j.cell.2015.04.053 . (Epub 2015/06/06)
doi: 10.1016/j.cell.2015.04.053
pubmed: 26046444
pmcid: 4459712
Betto RM, Diamante L, Perrera V, Audano M, Rapelli S, Lauria A, Incarnato D, Arboit M, Pedretti S, Rigoni G, Guerineau V, Touboul D, Stirparo GG, Lohoff T, Boroviak T, Grumati P, Soriano ME, Nichols J, Mitro N, Oliviero S, Martello G (2021) Metabolic control of DNA methylation in naive pluripotent cells. Nat Genet 53(2):215–229. https://doi.org/10.1038/s41588-020-00770-2 . (Epub 2021/02/03)
doi: 10.1038/s41588-020-00770-2
pubmed: 33526924
pmcid: 7116828
Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448(7151):313–317. https://doi.org/10.1038/nature05934 . (Epub 2007/06/08)
doi: 10.1038/nature05934
pubmed: 17554338
Sierra RA, Hoverter NP, Ramirez RN, Vuong LM, Mortazavi A, Merrill BJ, Waterman ML, Donovan PJ (2018) TCF7L1 suppresses primitive streak gene expression to support human embryonic stem cell pluripotency. Development. https://doi.org/10.1242/dev.161075 . (Epub 2018/01/24)
doi: 10.1242/dev.161075
pubmed: 29361574
pmcid: 5869011
Rossant J (2015) Mouse and human blastocyst-derived stem cells: vive les differences. Development 142(1):9–12. https://doi.org/10.1242/dev.115451 . (Epub 2014/12/18)
doi: 10.1242/dev.115451
pubmed: 25516964
Davidson KC, Mason EA, Pera MF (2015) The pluripotent state in mouse and human. Development 142(18):3090–3099. https://doi.org/10.1242/dev.116061 . (Epub 2015/09/24)
doi: 10.1242/dev.116061
pubmed: 26395138
Kurimoto K, Saitou M (2018) Epigenome regulation during germ cell specification and development from pluripotent stem cells. Curr Opin Genet Dev 52:57–64. https://doi.org/10.1016/j.gde.2018.06.004 . (Epub 2018/06/17)
doi: 10.1016/j.gde.2018.06.004
pubmed: 29908427
Wei W, Qing T, Ye X, Liu H, Zhang D, Yang W, Deng H (2008) Primordial germ cell specification from embryonic stem cells. PLoS ONE 3(12):e4013. https://doi.org/10.1371/journal.pone.0004013 . (Epub 2008/12/25)
doi: 10.1371/journal.pone.0004013
pubmed: 19107197
pmcid: 2602984
Zhang W, Liu HT (2002) MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res 12(1):9–18. https://doi.org/10.1038/sj.cr.7290105 . (Epub 2002/04/11)
doi: 10.1038/sj.cr.7290105
pubmed: 11942415
Toma JG, Akhavan M, Fernandes KJ, Barnabe-Heider F, Sadikot A, Kaplan DR, Miller FD (2001) Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3(9):778–784. https://doi.org/10.1038/ncb0901-778 . (Epub 2001/09/05)
doi: 10.1038/ncb0901-778
pubmed: 11533656
Dyce PW, Zhu H, Craig J, Li J (2004) Stem cells with multilineage potential derived from porcine skin. Biochem Biophys Res Commun 316(3):651–658. https://doi.org/10.1016/j.bbrc.2004.02.093 . (Epub 2004/03/23)
doi: 10.1016/j.bbrc.2004.02.093
pubmed: 15033449
Jiang Y, Zou Q, Liu B, Li S, Wang Y, Liu T, Ding X (2021) Atlas of prenatal hair follicle morphogenesis using the pig as a model system. Front Cell Dev Biol 9:721979. https://doi.org/10.3389/fcell.2021.721979 . (Epub 2021/10/26)
doi: 10.3389/fcell.2021.721979
pubmed: 34692680
pmcid: 8529045
Sun YC, Ge W, Lai FN, Zhang RQ, Wang JJ, Cheng SF, Shen W, Dyce PW (2017) Oocyte-like cells induced from CD34-positive mouse hair follicle stem cells in vitro. J Genet Genomics 44(8):405–407. https://doi.org/10.1016/j.jgg.2017.08.001 . (Epub 2017/08/29)
doi: 10.1016/j.jgg.2017.08.001
pubmed: 28844672
Inagaki E, Arai E, Hatou S, Sayano T, Taniguchi H, Negishi K, Kanai Y, Sato Y, Okano H, Tsubota K, Shimmura S (2022) The anterior eye chamber as a visible medium for in vivo tumorigenicity tests. Stem Cells Transl Med 11(8):841–849. https://doi.org/10.1093/stcltm/szac036 . (Epub 2022/06/07)
doi: 10.1093/stcltm/szac036
pubmed: 35666752
pmcid: 9397653
Nelakanti RV, Kooreman NG, Wu JC (2015) Teratoma formation: a tool for monitoring pluripotency in stem cell research. Curr Protoc Stem Cell Biol 32:4a.8.1-4a.8.17. https://doi.org/10.1002/9780470151808.sc04a08s32 . (Epub 2015/02/03)
doi: 10.1002/9780470151808.sc04a08s32
pubmed: 25640819
Wang L, Zhao H, Wu J, Ren J, Luo H, Zuo X, Chen Q, Tang Y (2021) An induced pluripotent stem cell line (CSUi004-A) from skin fibroblasts of a healthy individual. Stem Cell Res 53:102336. https://doi.org/10.1016/j.scr.2021.102336 . (Epub 2021/04/18)
doi: 10.1016/j.scr.2021.102336
pubmed: 33865102
Martin RM, Fowler JL, Cromer MK, Lesch BJ, Ponce E, Uchida N, Nishimura T, Porteus MH, Loh KM (2020) Improving the safety of human pluripotent stem cell therapies using genome-edited orthogonal safeguards. Nat Commun 11(1):2713. https://doi.org/10.1038/s41467-020-16455-7 . (Epub 2020/06/03)
doi: 10.1038/s41467-020-16455-7
pubmed: 32483127
pmcid: 7264334
Choi KH, Lee DK, Kim SW, Woo SH, Kim DY, Lee CK (2019) Chemically defined media can maintain pig pluripotency network in vitro. Stem Cell Rep 13(1):221–234. https://doi.org/10.1016/j.stemcr.2019.05.028 . (Epub 2019/07/02)
doi: 10.1016/j.stemcr.2019.05.028
Gao X, Nowak-Imialek M, Chen X, Chen D, Herrmann D, Ruan D, Chen ACH, Eckersley-Maslin MA, Ahmad S, Lee YL, Kobayashi T, Ryan D, Zhong J, Zhu J, Wu J, Lan G, Petkov S, Yang J, Antunes L, Campos LS, Fu B, Wang S, Yong Y, Wang X, Xue SG, Ge L, Liu Z, Huang Y, Nie T, Li P, Wu D, Pei D, Zhang Y, Lu L, Yang F, Kimber SJ, Reik W, Zou X, Shang Z, Lai L, Surani A, Tam PPL, Ahmed A, Yeung WSB, Teichmann SA, Niemann H, Liu P (2019) Establishment of porcine and human expanded potential stem cells. Nat Cell Biol 21(6):687–699. https://doi.org/10.1038/s41556-019-0333-2 . (Epub 2019/06/05)
doi: 10.1038/s41556-019-0333-2
pubmed: 31160711
pmcid: 7035105
Yang J, Ryan DJ, Wang W, Tsang JC, Lan G, Masaki H, Gao X, Antunes L, Yu Y, Zhu Z, Wang J, Kolodziejczyk AA, Campos LS, Wang C, Yang F, Zhong Z, Fu B, Eckersley-Maslin MA, Woods M, Tanaka Y, Chen X, Wilkinson AC, Bussell J, White J, Ramirez-Solis R, Reik W, Göttgens B, Teichmann SA, Tam PPL, Nakauchi H, Zou X, Lu L, Liu P (2017) Establishment of mouse expanded potential stem cells. Nature 550(7676):393–397. https://doi.org/10.1038/nature24052 . (Epub 2017/10/12)
doi: 10.1038/nature24052
pubmed: 29019987
pmcid: 5890884