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Impaired phagocytic function in CX3CR1+ tissue-resident skeletal muscle macrophages prevents muscle recovery after influenza A virus-induced pneumonia in aged mice

By Constance E. Runyan, Lynn C. Welch, Emilia Lecuona, Masahiko Shigemura, Luciano Amarelle, Hiam Abdala-Valencia, Nikita Joshi, Ziyan Lu, Kiwon Nam, Nikolay S. Markov, Alexandra C. McQuattie-Pimentel, Raul Piseaux-Aillon, Yuliya Politanska, Lango Sichizya, Satoshi Watanabe, Kinola J.N. Williams, G.R. Scott Budinger, Jacob I. Sznajder, Alexander V. Misharin

Posted 07 Nov 2019
bioRxiv DOI: 10.1101/833236

Skeletal muscle dysfunction in survivors of pneumonia is a major cause of lasting morbidity that disproportionately affects older individuals. We found that skeletal muscle recovery was impaired in aged compared with young mice after influenza A virus-induced pneumonia. In young mice, recovery of muscle loss was associated with expansion of tissue-resident skeletal muscle macrophages and downregulation of MHC II expression, followed by a proliferation of muscle satellite cells. These findings were absent in aged mice and in mice deficient in Cx3cr1. Transcriptomic profiling of tissue-resident skeletal muscle macrophages from aged compared with young mice showed downregulation of pathways associated with phagocytosis and proteostasis, and persistent upregulation of inflammatory pathways. Consistently, skeletal muscle macrophages from aged mice failed to downregulate MHCII expression during recovery from influenza A virus-induced pneumonia and showed impaired phagocytic function in vitro. Like aged animals, mice deficient in the phagocytic receptor Mertk showed no macrophage expansion, MHCII downregulation or satellite cell proliferation and failed to recover skeletal muscle function after influenza A pneumonia. Our data suggest that a loss of phagocytic function in a CX3CR1+ tissue-resident skeletal muscle macrophage population in aged mice precludes satellite cell proliferation and recovery of skeletal muscle function after influenza A pneumonia.

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