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Neuronal innervation regulates the secretion of neurotrophic myokines and exosomes from skeletal muscle.
Huang, Kai-Yu; Upadhyay, Gaurav; Ahn, Yujin; Sakakura, Masayoshoi; Pagan-Diaz, Gelson J; Cho, Younghak; Weiss, Amanda C; Huang, Chen; Mitchell, Jennifer W; Li, Jiahui; Tan, Yanqi; Deng, Yu-Heng; Ellis-Mohr, Austin; Dou, Zhi; Zhang, Xiaotain; Kang, Sehong; Chen, Qian; Sweedler, Jonathan V; Im, Sung Gap; Bashir, Rashid; Chung, Hee Jung; Popescu, Gabriel; Gillette, Martha U; Gazzola, Mattia; Kong, Hyunjoon.
Afiliación
  • Huang KY; Department of Chemical and Biomolecular Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Upadhyay G; Department of Mechanical Science and Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Ahn Y; Department of Chemical and Biomolecular Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Sakakura M; Chan Zuckerberg Biohub Chicago, Chicago, IL 60642.
  • Pagan-Diaz GJ; Department of Electrical and Computer Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Cho Y; Department of Bioengineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Weiss AC; Department of Chemical and Biomolecular Engineering and KI for the Nano Century, Korea Advanced Institute of Science and Technology, Daejeon 305-701, Republic of Korea.
  • Huang C; Department of Molecular and Integrative Physiology, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Mitchell JW; Department of Chemistry, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Li J; Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Tan Y; Department of Materials Science and Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Deng YH; Department of Chemistry, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Ellis-Mohr A; Department of Chemical and Biomolecular Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Dou Z; Department of Electrical and Computer Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Zhang X; Department of Mechanical Science and Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Kang S; Department of Mechanical Science and Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Chen Q; Department of Mechanical Science and Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Sweedler JV; Department of Materials Science and Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Im SG; Chan Zuckerberg Biohub Chicago, Chicago, IL 60642.
  • Bashir R; Department of Chemistry, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Chung HJ; Department of Chemical and Biomolecular Engineering and KI for the Nano Century, Korea Advanced Institute of Science and Technology, Daejeon 305-701, Republic of Korea.
  • Popescu G; Chan Zuckerberg Biohub Chicago, Chicago, IL 60642.
  • Gillette MU; Department of Bioengineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Gazzola M; Department of Molecular and Integrative Physiology, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
  • Kong H; Department of Electrical and Computer Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
Proc Natl Acad Sci U S A ; 121(19): e2313590121, 2024 May 07.
Article en En | MEDLINE | ID: mdl-38683978
ABSTRACT
Myokines and exosomes, originating from skeletal muscle, are shown to play a significant role in maintaining brain homeostasis. While exercise has been reported to promote muscle secretion, little is known about the effects of neuronal innervation and activity on the yield and molecular composition of biologically active molecules from muscle. As neuromuscular diseases and disabilities associated with denervation impact muscle metabolism, we hypothesize that neuronal innervation and firing may play a pivotal role in regulating secretion activities of skeletal muscles. We examined this hypothesis using an engineered neuromuscular tissue model consisting of skeletal muscles innervated by motor neurons. The innervated muscles displayed elevated expression of mRNAs encoding neurotrophic myokines, such as interleukin-6, brain-derived neurotrophic factor, and FDNC5, as well as the mRNA of peroxisome-proliferator-activated receptor γ coactivator 1α, a key regulator of muscle metabolism. Upon glutamate stimulation, the innervated muscles secreted higher levels of irisin and exosomes containing more diverse neurotrophic microRNAs than neuron-free muscles. Consequently, biological factors secreted by innervated muscles enhanced branching, axonal transport, and, ultimately, spontaneous network activities of primary hippocampal neurons in vitro. Overall, these results reveal the importance of neuronal innervation in modulating muscle-derived factors that promote neuronal function and suggest that the engineered neuromuscular tissue model holds significant promise as a platform for producing neurotrophic molecules.
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Texto completo: 1 Colección: 01-internacional Banco de datos: MEDLINE Asunto principal: Músculo Esquelético / Factor Neurotrófico Derivado del Encéfalo / Exosomas Límite: Animals Idioma: En Revista: Proc Natl Acad Sci U S A Año: 2024 Tipo del documento: Article

Texto completo: 1 Colección: 01-internacional Banco de datos: MEDLINE Asunto principal: Músculo Esquelético / Factor Neurotrófico Derivado del Encéfalo / Exosomas Límite: Animals Idioma: En Revista: Proc Natl Acad Sci U S A Año: 2024 Tipo del documento: Article