Identification of a physiologic vasculogenic fibroblast state to achieve tissue repair

Durba Pal, Subhadip Ghatak, Kanhaiya Singh, Ahmed Safwat Abouhashem, Manishekhar Kumar, Mohamed S El Masry, Sujit K. Mohanty, Ravichand Palakurti, Yashika Rustagi, Saba Tabasum, Dolly K. Khona, Savita Khanna, Sedat Kacar, Rajneesh Srivastava, Pramod Bhasme, Sumit S. Verma, Edward Hernandez, Anu Sharma, Diamond Reese, Priyanka Verma, Nandini Ghosh, Mahadeo Gorain, Jun Wan, Sheng Liu, Yunlong Liu, Natalia Higuita Castro, Surya C. Gnyawali, William Lawrence, Jordan Moore, Daniel Gallego Perez, Sashwati Roy, Mervin C. Yoder and Chandan K. Sen ()
Additional contact information
Durba Pal: Indiana University School of Medicine
Subhadip Ghatak: Indiana University School of Medicine
Kanhaiya Singh: Indiana University School of Medicine
Ahmed Safwat Abouhashem: Indiana University School of Medicine
Manishekhar Kumar: Indiana University School of Medicine
Mohamed S El Masry: Indiana University School of Medicine
Sujit K. Mohanty: Indiana University School of Medicine
Ravichand Palakurti: Indiana University School of Medicine
Yashika Rustagi: Indiana University School of Medicine
Saba Tabasum: Indiana University School of Medicine
Dolly K. Khona: Indiana University School of Medicine
Savita Khanna: Indiana University School of Medicine
Sedat Kacar: Indiana University School of Medicine
Rajneesh Srivastava: Indiana University School of Medicine
Pramod Bhasme: Indiana University School of Medicine
Sumit S. Verma: Indiana University School of Medicine
Edward Hernandez: Indiana University School of Medicine
Anu Sharma: Indiana University School of Medicine
Diamond Reese: Indiana University School of Medicine
Priyanka Verma: Indiana University School of Medicine
Nandini Ghosh: Indiana University School of Medicine
Mahadeo Gorain: Indiana University School of Medicine
Jun Wan: Indiana University School of Medicine
Sheng Liu: Indiana University School of Medicine
Yunlong Liu: Indiana University School of Medicine
Natalia Higuita Castro: The Ohio State University
Surya C. Gnyawali: Indiana University School of Medicine
William Lawrence: The Ohio State University
Jordan Moore: The Ohio State University
Daniel Gallego Perez: The Ohio State University
Sashwati Roy: Indiana University School of Medicine
Mervin C. Yoder: Indiana University School of Medicine
Chandan K. Sen: Indiana University School of Medicine

Nature Communications, 2023, vol. 14, issue 1, 1-20

Abstract: Abstract Tissue injury to skin diminishes miR-200b in dermal fibroblasts. Fibroblasts are widely reported to directly reprogram into endothelial-like cells and we hypothesized that miR-200b inhibition may cause such changes. We transfected human dermal fibroblasts with anti-miR-200b oligonucleotide, then using single cell RNA sequencing, identified emergence of a vasculogenic subset with a distinct fibroblast transcriptome and demonstrated blood vessel forming function in vivo. Anti-miR-200b delivery to murine injury sites likewise enhanced tissue perfusion, wound closure, and vasculogenic fibroblast contribution to perfused vessels in a FLI1 dependent manner. Vasculogenic fibroblast subset emergence was blunted in delayed healing wounds of diabetic animals but, topical tissue nanotransfection of a single anti-miR-200b oligonucleotide was sufficient to restore FLI1 expression, vasculogenic fibroblast emergence, tissue perfusion, and wound healing. Augmenting a physiologic tissue injury adaptive response mechanism that produces a vasculogenic fibroblast state change opens new avenues for therapeutic tissue vascularization of ischemic wounds.

Date: 2023
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DOI: 10.1038/s41467-023-36665-z

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