Human archetypal pluripotent stem cells differentiate into trophoblast stem cells via endogenous BMP5/7 induction without transitioning through naive state
Nenhuma Miniatura disponível
Citações na Scopus
0
Tipo de produção
article
Data de publicação
2024
Título da Revista
ISSN da Revista
Título do Volume
Editora
NATURE PORTFOLIO
Autores
TIETZE, Ethan
BARBOSA, Andre Rocha
ARAUJO, Bruno
SPIEGELBERG, Bailey
CHO, Hyeon Jin
LEE, Yong Kyu
WANG, Yanhong
MCCORD, Alejandra
LORENZETTI, Alan
Citação
SCIENTIFIC REPORTS, v.14, n.1, article ID 3291, 15p, 2024
Resumo
Primary human trophoblast stem cells (TSCs) and TSCs derived from human pluripotent stem cells (hPSCs) can potentially model placental processes in vitro. Yet, the pluripotent states and factors involved in the differentiation of hPSCs to TSCs remain poorly understood. In this study, we demonstrate that the primed pluripotent state can generate TSCs by activating pathways such as Epidermal Growth Factor (EGF) and Wingless-related integration site (WNT), and by suppressing tumor growth factor beta (TGF beta), histone deacetylases (HDAC), and Rho-associated protein kinase (ROCK) signaling pathways, all without the addition of exogenous Bone morphogenetic protein 4 (BMP4)-a condition we refer to as the TS condition. We characterized this process using temporal single-cell RNA sequencing to compare TS conditions with differentiation protocols involving BMP4 activation alone or BMP4 activation in conjunction with WNT inhibition. The TS condition consistently produced a stable, proliferative cell type that closely mimics first-trimester placental cytotrophoblasts, marked by the activation of endogenous retroviral genes and the absence of amnion expression. This was observed across multiple cell lines, including various primed induced pluripotent stem cell (iPSC) and embryonic stem cell (ESC) lines. Primed-derived TSCs can proliferate for over 30 passages and further specify into multinucleated syncytiotrophoblasts and extravillous trophoblast cells. Our research establishes that the differentiation of primed hPSCs to TSC under TS conditions triggers the induction of TMSB4X, BMP5/7, GATA3, and TFAP2A without progressing through a naive state. These findings propose that the primed hPSC state is part of a continuum of potency with the capacity to differentiate into TSCs through multiple routes.
Palavras-chave
Referências
- Abd El-Aleem SA, 2018, J MOL HISTOL, V49, P531, DOI 10.1007/s10735-018-9791-2
- al-Haddad BJS, 2019, AM J OBSTET GYNECOL, V221, P549, DOI 10.1016/j.ajog.2019.06.013
- Amita M, 2013, P NATL ACAD SCI USA, V110, pE1212, DOI 10.1073/pnas.1303094110
- Chen HD, 2019, NAT COMMUN, V10, DOI 10.1038/s41467-019-09670-4
- Chen IH, 2013, CARDIOVASC RES, V97, P443, DOI 10.1093/cvr/cvs355
- Cinkornpumin JK, 2020, STEM CELL REP, V15, P198, DOI 10.1016/j.stemcr.2020.06.003
- Cui KL, 2022, ADV SCI, V9, DOI 10.1002/advs.202100031
- Daniszewski M, 2018, ISCIENCE, V7, P30, DOI 10.1016/j.isci.2018.08.016
- Dong C, 2020, ELIFE, V9, DOI 10.7554/eLife.52504
- Erwin JA, 2012, GENETICS, V192, P857, DOI 10.1534/genetics.112.144121
- Frank JA, 2022, SCIENCE, V378, P422, DOI 10.1126/science.abq7871
- Fukamachi K, 2019, J TOXICOL PATHOL, V32, P135, DOI 10.1293/tox.2018-0062
- Gafni O, 2013, NATURE, V504, P282, DOI 10.1038/nature12745
- Glass K, 2013, PLOS ONE, V8, DOI 10.1371/journal.pone.0064832
- Guan L, 2019, J EXP CLIN CANC RES, V38, DOI 10.1186/s13046-019-1417-3
- Guleria I, 2000, NAT MED, V6, P589, DOI 10.1038/75074
- Hanna J, 2010, P NATL ACAD SCI USA, V107, P9222, DOI 10.1073/pnas.1004584107
- Hendee KE, 2018, HUM MOL GENET, V27, P1675, DOI 10.1093/hmg/ddy074
- Horii Mariko, 2019, Curr Protoc Stem Cell Biol, V50, pe96, DOI 10.1002/cpsc.96
- Huang DY, 2016, ACTA BIOCH BIOPH SIN, V48, P788, DOI 10.1093/abbs/gmw070
- Io S, 2021, CELL STEM CELL, V28, P1023, DOI 10.1016/j.stem.2021.03.013
- Jang YJ, 2022, P NATL ACAD SCI USA, V119, DOI 10.1073/pnas.2115709119
- Johnson WE, 2019, NAT REV MICROBIOL, V17, P355, DOI 10.1038/s41579-019-0189-2
- Kazanskaya O, 2004, DEV CELL, V7, P525, DOI 10.1016/j.devcel.2004.07.019
- Krendl C, 2017, P NATL ACAD SCI USA, V114, pE9579, DOI 10.1073/pnas.1708341114
- Lavialle C, 2013, PHILOS T R SOC B, V368, DOI 10.1098/rstb.2012.0507
- Lee CQE, 2018, DEVELOPMENT, V145, DOI 10.1242/dev.162305
- Liu AX, 2006, BIOL REPROD, V75, P414, DOI 10.1095/biolreprod.105.049379
- Liu XD, 2020, NATURE, V586, P101, DOI 10.1038/s41586-020-2734-6
- Liu YW, 2018, CELL RES, V28, P819, DOI 10.1038/s41422-018-0066-y
- Lv SM, 2013, MOL CELL BIOCHEM, V381, P283, DOI 10.1007/s11010-013-1713-8
- Macosko EZ, 2015, CELL, V161, P1202, DOI 10.1016/j.cell.2015.05.002
- Mangeney M, 2007, P NATL ACAD SCI USA, V104, P20534, DOI 10.1073/pnas.0707873105
- Messmer T, 2019, CELL REP, V26, P815, DOI 10.1016/j.celrep.2018.12.099
- Mischler A, 2021, J BIOL CHEM, V296, DOI 10.1016/j.jbc.2021.100386
- Myatt L, 2006, J PHYSIOL-LONDON, V572, P25, DOI 10.1113/jphysiol.2006.104968
- Niakan KK, 2013, DEV BIOL, V375, P54, DOI 10.1016/j.ydbio.2012.12.008
- Nichols J, 2009, CELL STEM CELL, V4, P487, DOI 10.1016/j.stem.2009.05.015
- Niwa H, 2005, CELL, V123, P917, DOI 10.1016/j.cell.2005.08.040
- Oh YM, 1996, J BIOL CHEM, V271, P30322, DOI 10.1074/jbc.271.48.30322
- Okae H, 2018, CELL STEM CELL, V22, P50, DOI 10.1016/j.stem.2017.11.004
- Osafune K, 2008, NAT BIOTECHNOL, V26, P313, DOI 10.1038/nbt1383
- Overgaard MT, 2001, J BIOL CHEM, V276, P21849, DOI 10.1074/jbc.M102191200
- Pastor WA, 2016, CELL STEM CELL, V18, P323, DOI 10.1016/j.stem.2016.01.019
- Pera MF, 2022, STEM CELL REP, V17, P1235, DOI 10.1016/j.stemcr.2022.05.011
- Petropoulos S, 2016, CELL, V165, P1012, DOI [10.1016/j.cell.2016.08.009, 10.1016/j.cell.2016.03.023]
- Porazinski S, 2015, NATURE, V521, P217, DOI 10.1038/nature14215
- Roberts RM, 2022, CELL MOL LIFE SCI, V79, DOI 10.1007/s00018-022-04478-w
- Roost MS, 2015, STEM CELL REP, V4, P1112, DOI 10.1016/j.stemcr.2015.05.002
- Rossant J, 2018, ANNU REV GENET, V52, P185, DOI 10.1146/annurev-genet-120116-024544
- Rostovskaya M, 2022, CELL STEM CELL, V29, P744, DOI 10.1016/j.stem.2022.03.014
- Sawada T, 2020, STEM CELL RES, V46, DOI 10.1016/j.scr.2020.101806
- Seetharam AS, 2022, STEM CELL REP, V17, P1289, DOI 10.1016/j.stemcr.2022.04.014
- Soncin F, 2022, STEM CELL REP, V17, P1303, DOI 10.1016/j.stemcr.2022.04.013
- Stirparo GG, 2018, DEVELOPMENT, V145, DOI 10.1242/dev.158501
- Stuart T, 2019, CELL, V177, P1888, DOI 10.1016/j.cell.2019.05.031
- Sudheer S, 2012, STEM CELLS DEV, V21, P2987, DOI 10.1089/scd.2012.0099
- Theunissen TW, 2016, CELL STEM CELL, V19, P502, DOI 10.1016/j.stem.2016.06.011
- Thomson JA, 1998, SCIENCE, V282, P1145, DOI 10.1126/science.282.5391.1145
- Tunster SJ, 2013, REPRODUCTION, V145, pR117, DOI 10.1530/REP-12-0511
- Ursini G, 2021, P NATL ACAD SCI USA, V118, DOI 10.1073/pnas.2019789118
- Vento-Tormo R, 2018, NATURE, V563, P347, DOI 10.1038/s41586-018-0698-6
- Viukov S, 2022, STEM CELL REP, V17, P2484, DOI 10.1016/j.stemcr.2022.09.008
- Wang RY, 2013, GASTROENTEROLOGY, V145, P1436, DOI 10.1053/j.gastro.2013.08.009
- Wei YX, 2021, SCI ADV, V7, DOI 10.1126/sciadv.abf4416
- Weinberger L, 2016, NAT REV MOL CELL BIO, V17, P155, DOI 10.1038/nrm.2015.28
- Xiang LF, 2020, NATURE, V577, P537, DOI 10.1038/s41586-019-1875-y
- Xu RH, 2002, NAT BIOTECHNOL, V20, P1261, DOI 10.1038/nbt761
- Xu XX, 2014, J NEUROSCI, V34, P1420, DOI 10.1523/JNEUROSCI.4488-13.2014
- Yabe S, 2016, P NATL ACAD SCI USA, V113, pE2598, DOI 10.1073/pnas.1601630113