Intercellular mRNA transfer alters the human pluripotent stem cell state

被引:0
作者
Yoneyama, Yosuke [1 ,2 ]
Zhang, Ran-Ran [3 ,4 ,5 ]
Maezawa, Mari [1 ]
Masaki, Hideki [6 ]
Kimura, Masaki [3 ,4 ,5 ]
Cai, Yuqi [3 ,4 ,5 ]
Adam, Mike [3 ,4 ,5 ]
Parameswaran, Sreeja [7 ]
Mizuno, Naoaki
Bhadury, Joydeep [8 ]
Maezawa, So [9 ]
Ochiai, Hiroshi [10 ]
Nakauchi, Hiromitsu [6 ,8 ]
Potter, S. Steven [3 ,5 ]
Weirauch, Matthew T. [3 ,4 ,5 ,11 ]
Takebe, Takanori [1 ,2 ,3 ,4 ,5 ,11 ,12 ,13 ]
机构
[1] Inst Sci Tokyo, Inst Integrated Res, Mechanist Immunol Res Unit, Bunkyo Ku, Tokyo 1138510, Japan
[2] Osaka Univ, Grad Sch Med, Dept Genome Biol, Suita, Osaka 5650871, Japan
[3] Cincinnati Childrens Hosp Med Ctr, Div Gastroenterol Hepatol & Nutr, Cincinnati, OH 45229 USA
[4] Cincinnati Childrens Hosp Med Ctr, Div Dev Biol, Cincinnati, OH 45229 USA
[5] Cincinnati Childrens Hosp Med Ctr, Div Biomed Informat, Cincinnati, OH 45229 USA
[6] Inst Sci Tokyo, Inst Integrated Res, Stem Cell Therapy Div, Bunkyo Ku, Tokyo 1138510, Japan
[7] Cincinnati Childrens Hosp Med Ctr, Ctr Autoimmune Genom & Etiol, Cincinnati, OH 45229 USA
[8] Stanford Univ, Sch Med, Inst Stem Cell Biol & Regenerat Med, Stanford, CA 94305 USA
[9] Tokyo Univ Sci, Fac Sci & Technol, Dept Appl Biol Sci, Chiba 2788510, Japan
[10] Kyushu Univ, Med Inst Bioregulat, Div Gene Express Dynam, Fukuoka 8120054, Japan
[11] Univ Cincinnati, Coll Med, Dept Pediat, Cincinnati, OH 45229 USA
[12] Cincinnati Childrens Hosp Med Ctr, Ctr Stem Cell & Organoid Med CuSTOM, Cincinnati, OH 45229 USA
[13] Cincinnati Childrens Hosp Med Ctr, Div Oncol, Suita, Osaka 5650871, Japan
基金
日本科学技术振兴机构; 日本学术振兴会;
关键词
mRNA transfer; reprogramming; pluripotency; cell-cell communication; TUNNELING NANOTUBES; SOMATIC-CELLS; HUMAN NAIVE; FIBROBLASTS; MICRORNAS; NUCLEI; MOUSE;
D O I
10.1073/pnas.2413351122
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Intercellular transmission of messenger RNA (mRNA) is being explored in mammalian species using immortal cell lines. Here, we uncover an intercellular mRNA transfer phenomenon that allows for the adaptation and reprogramming of human primed pluripotent stem cells (hPSCs). This process is induced by the direct cell contact- mediated coculture with mouse embryonic stem cells under the condition impermissible for primed hPSC culture. Mouse- derived mRNA contents are transmitted into adapted hPSCs only in the coculture. Transfer- specific mRNA analysis shows the enrichment for divergent biological pathways involving transcription/translational machinery and stress- coping mechanisms, wherein such transfer is diminished when direct cell contacts are lost. After 5 d of coculture with mouse embryonic stem cells, surface marker analysis and global gene profiling confirmed that knockdown experiments targeting mouse- specific transcription factor- coding mRNAs in in mammalian cells. Our results support that episodic mRNA transfer can occur in cell cooperative and competitive processes, which provides a fresh perspective on understanding the roles of mRNA mobility for intra- and interspecies cellular communications.
引用
收藏
页数:12
相关论文
共 67 条
[1]   Retrovirus-like Gag Protein Arc1 Binds RNA and Traffics across Synaptic Boutons [J].
Ashley, James ;
Cordy, Benjamin ;
Lucia, Diandra ;
Fradkin, Lee G. ;
Budnik, Vivian ;
Thomson, Travis .
CELL, 2018, 172 (1-2) :262-+
[2]   Large-Scale Analysis of Loss of Imprinting in Human Pluripotent Stem Cells [J].
Bar, Shiran ;
Schachter, Maya ;
Eldar-Geva, Talia ;
Benvenisty, Nissim .
CELL REPORTS, 2017, 19 (05) :957-968
[3]   Exosomes secreted by human cells transport largely mRNA fragments that are enriched in the 3′-untranslated regions [J].
Batagov, Arsen O. ;
Kurochkin, Igor V. .
BIOLOGY DIRECT, 2013, 8
[4]   Reprogramming towards pluripotency requires AID-dependent DNA demethylation [J].
Bhutani, Nidhi ;
Brady, Jennifer J. ;
Damian, Mara ;
Sacco, Alessandra ;
Corbel, Stephane Y. ;
Blau, Helen M. .
NATURE, 2010, 463 (7284) :1042-U57
[5]   The Cell-Surface Marker Sushi Containing Domain 2 Facilitates Establishment of Human Naive Pluripotent Stem Cells [J].
Bredenkamp, Nicholas ;
Stirparo, Giuliano Giuseppe ;
Nichols, Jennifer ;
Smith, Austin ;
Guo, Ge .
STEM CELL REPORTS, 2019, 12 (06) :1212-1222
[6]   Translational and post-translational control of human nai spacing diaeresis ve versus primed pluripotency [J].
Chen, Cheng ;
Zhang, Xiaobing ;
Wang, Yisha ;
Chen, Xinyu ;
Chen, Wenjie ;
Dan, Songsong ;
She, Shiqi ;
Hu, Weiwei ;
Dai, Jie ;
Hu, Jianwen ;
Cao, Qingyi ;
Liu, Qianyu ;
Huang, Yinghua ;
Qin, Baoming ;
Kang, Bo ;
Wang, Ying-Jie .
ISCIENCE, 2022, 25 (01)
[7]   Comprehensive Cell Surface Protein Profiling Identifies Specific Markers of Human Naive and Primed Pluripotent States [J].
Collier, Amanda J. ;
Panula, Sarita P. ;
Schell, John Paul ;
Chovanec, Peter ;
Reyes, Alvaro Plaza ;
Petropoulos, Sophie ;
Corcoran, Anne E. ;
Walker, Rachael ;
Douagi, Iyadh ;
Lanner, Fredrik ;
Rugg-Gunn, Peter J. .
CELL STEM CELL, 2017, 20 (06) :874-+
[8]   Physical nanoscale conduit-mediated communication between tumour cells and the endothelium modulates endothelial phenotype [J].
Connor, Yamicia ;
Tekleab, Sarah ;
Nandakumar, Shyama ;
Walls, Cherelle ;
Tekleab, Yonatan ;
Husain, Amjad ;
Gadish, Or ;
Sabbisetti, Venkata ;
Kaushik, Shelly ;
Sehrawat, Seema ;
Kulkarni, Ashish ;
Dvorak, Harold ;
Zetter, Bruce ;
Edelman, Elazer R. ;
Sengupta, Shiladitya .
NATURE COMMUNICATIONS, 2015, 6
[9]   Global analysis of contact-dependent human-to-mouse intercellular mRNA and lncRNA transfer in cell culture [J].
Dasgupta, Sandipan ;
Dayagi, Daniella Y. ;
Haimovich, Gal ;
Wyler, Emanuel ;
Olender, Tsviya ;
Singer, Robert H. ;
Landthaler, Markus ;
Gerst, Jeffrey E. .
ELIFE, 2023, 12
[10]   Extracellular vesicle cross-talk between pulmonary artery smooth muscle cells and endothelium during excessive TGF-β signalling: implications for PAH vascular remodelling [J].
de la Cuesta, Fernando ;
Passalacqua, Ilaria ;
Rodor, Julie ;
Bhushan, Raghu ;
Denby, Laura ;
Baker, Andrew H. .
CELL COMMUNICATION AND SIGNALING, 2019, 17 (01)