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[Preprint]. 2024 Jul 31:2023.09.06.556606. [Version 2] doi: 10.1101/2023.09.06.556606

Macrophage-fibroblast crosstalk drives Arg1-dependent lung fibrosis via ornithine loading

Preeti Yadav, Javier Gómez Ortega, Whitney Tamaki, Charles Chien, Kai-chun Chang, Nivedita Biswas, Sixuan Pan, Julia Nilsson, Xiaoyang Yin, Aritra Bhattacharyya, Kaveh Boostanpour, Tanay Jujaray, Jasper Wang, Tatsuya Tsukui, Dean Sheppard, Baosheng Li, Mazharul Maishan, Hiroki Taenaka, Michael A Matthay, Rieko Muramatsu, Lenka Maliskova, Arnab Ghosh, Walter L Eckalbar, Ari B Molofsky, Paul J Wolters, Stanley J Tamaki, Trever Bivona, Adam R Abate, Allon Wagner, Kevin M Tharp, Mallar Bhattacharya
PMCID: PMC11360891  PMID: 39211079

Abstract

Monocyte-derived macrophages recruited to injured tissues induce a maladaptive fibrotic response characterized by excessive production of collagen by local fibroblasts. Macrophages initiate this programming via paracrine factors, but it is unknown whether reciprocal responses from fibroblasts enhance profibrotic polarization of macrophages. We identify macrophage-fibroblast crosstalk necessary for injury-associated fibrosis, in which macrophages induced interleukin 6 ( IL-6 ) expression in fibroblasts via purinergic receptor P2rx4 signaling, and IL-6, in turn, induced arginase 1 ( Arg1 ) expression in macrophages. Arg1 contributed to fibrotic responses by metabolizing arginine to ornithine, which fibroblasts used as a substrate to synthesize proline, a uniquely abundant constituent of collagen. Imaging of idiopathic pulmonary fibrosis (IPF) lung samples confirmed expression of ARG1 in myeloid cells, and arginase inhibition suppressed collagen expression in cultured precision-cut IPF lung slices. Taken together, we define a circuit between macrophages and fibroblasts that facilitates cross-feeding metabolism necessary for injury-associated fibrosis.

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