Global analysis of contact-dependent human-to-mouse intercellular mRNA and lncRNA transfer in cell culture

Author:

Dasgupta Sandipan1,Dayagi Daniella Y1ORCID,Haimovich Gal1ORCID,Wyler Emanuel2ORCID,Olender Tsviya1,Singer Robert H3ORCID,Landthaler Markus2,Gerst Jeffrey E1ORCID

Affiliation:

1. Department of Molecular Genetics, Weizmann Institute of Science

2. Berlin Institute of Medical Systems Biology and Systems Biology, Max Delbruck Center for Molecular Medicine

3. Department of Anatomy & Structural Biology, Albert Einstein College of Medicine

Abstract

Full-length mRNAs transfer between adjacent mammalian cells via direct cell-to-cell connections called tunneling nanotubes (TNTs). However, the extent of mRNA transfer at the transcriptome-wide level (the ‘transferome’) is unknown. Here, we analyzed the transferome in an in vitro human-mouse cell co-culture model using RNA-sequencing. We found that mRNA transfer is non-selective, prevalent across the human transcriptome, and that the amount of transfer to mouse embryonic fibroblasts (MEFs) strongly correlates with the endogenous level of gene expression in donor human breast cancer cells. Typically,<1% of endogenous mRNAs undergo transfer. Non-selective, expression-dependent RNA transfer was further validated using synthetic reporters. RNA transfer appears contact-dependent via TNTs, as exemplified for several mRNAs. Notably, significant differential changes in the native MEF transcriptome were observed in response to co-culture, including the upregulation of multiple cancer and cancer-associated fibroblast-related genes and pathways. Together, these results lead us to suggest that TNT-mediated RNA transfer could be a phenomenon of physiological importance under both normal and pathogenic conditions.

Funder

German-Israeli Foundation for Scientific Research and Development

US-Israel Binational Science Foundation-National Science Foundation

Joel and Mady Dukler Fund for Cancer Research

Jean-Jacques Brunschwig Fund for the Molecular Genetics of Cancer

Moross Integrated Cancer Center

Kekst Family Institute for Medical Genetics

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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