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[Preprint]. 2023 Mar 29:2023.03.27.534417. [Version 1] doi: 10.1101/2023.03.27.534417

Transcriptional Activation of Regenerative Hematopoiesis via Vascular Niche Sensing

Tomer Itkin, Sean Houghton, Ryan Schreiner, Yang Lin, Chaitanya R Badwe, Veronique Voisin, Alex Murison, Negar Seyedhassantehrani, Kerstin B Kaufmann, Laura Garcia-Prat, Gregory T Booth, Fuqiang Geng, Ying Liu, Jesus M Gomez-Salinero, Jae-Hung Shieh, David Redmond, Jenny Z Xiang, Steven Z Josefowicz, Cole Trapnell, Joel A Spencer, Lior Zangi, Brandon Hadland, John E Dick, Stephanie Z Xie, Shahin Rafii
PMCID: PMC10081204  PMID: 37034724

Abstract

Transition between activation and quiescence programs in hematopoietic stem and progenitor cells (HSC/HSPCs) is perceived to be governed intrinsically and by microenvironmental co-adaptation. However, HSC programs dictating both transition and adaptability, remain poorly defined. Single cell multiome analysis divulging differential transcriptional activity between distinct HSPC states, indicated for the exclusive absence of Fli-1 motif from quiescent HSCs. We reveal that Fli-1 activity is essential for HSCs during regenerative hematopoiesis. Fli-1 directs activation programs while manipulating cellular sensory and output machineries, enabling HSPCs co-adoptability with a stimulated vascular niche. During regenerative conditions, Fli-1 presets and enables propagation of niche-derived Notch1 signaling. Constitutively induced Notch1 signaling is sufficient to recuperate functional HSC impairments in the absence of Fli-1. Applying FLI-1 modified-mRNA transduction into lethargic adult human mobilized HSPCs, enables their vigorous niche-mediated expansion along with superior engraftment capacities. Thus, decryption of stem cell activation programs offers valuable insights for immune regenerative medicine.

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