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Reduced secretion of neuronal growth regulator 1 contributes to impaired adipose-neuronal crosstalk in obesity

Author

Listed:
  • Elisa Duregotti

    (School of Cardiovascular Medicine and Sciences)

  • Christina M. Reumiller

    (School of Cardiovascular Medicine and Sciences)

  • Ursula Mayr

    (School of Cardiovascular Medicine and Sciences)

  • Maria Hasman

    (School of Cardiovascular Medicine and Sciences)

  • Lukas E. Schmidt

    (School of Cardiovascular Medicine and Sciences)

  • Sean A. Burnap

    (School of Cardiovascular Medicine and Sciences)

  • Konstantinos Theofilatos

    (School of Cardiovascular Medicine and Sciences)

  • Javier Barallobre-Barreiro

    (School of Cardiovascular Medicine and Sciences)

  • Arne Beran

    (University Hospital Düsseldorf, Heinrich-Heine-University Düsseldorf)

  • Maria Grandoch

    (University Hospital Düsseldorf, Heinrich-Heine-University Düsseldorf)

  • Alessandro Viviano

    (University of London
    Imperial College London)

  • Marjan Jahangiri

    (University of London)

  • Manuel Mayr

    (School of Cardiovascular Medicine and Sciences)

Abstract

While the endocrine function of white adipose tissue has been extensively explored, comparatively little is known about the secretory activity of less-investigated fat depots. Here, we use proteomics to compare the secretory profiles of male murine perivascular depots with those of canonical white and brown fat. Perivascular secretomes show enrichment for neuronal cell-adhesion molecules, reflecting a higher content of intra-parenchymal sympathetic projections compared to other adipose depots. The sympathetic innervation is reduced in the perivascular fat of obese (ob/ob) male mice, as well as in the epicardial fat of patients with obesity. Degeneration of sympathetic neurites is observed in presence of conditioned media of fat explants from ob/ob mice, that show reduced secretion of neuronal growth regulator 1. Supplementation of neuronal growth regulator 1 reverses this neurodegenerative effect, unveiling a neurotrophic role for this protein previously identified as a locus associated with human obesity. As sympathetic stimulation triggers energy-consuming processes in adipose tissue, an impaired adipose-neuronal crosstalk is likely to contribute to the disrupted metabolic homeostasis characterising obesity.

Suggested Citation

  • Elisa Duregotti & Christina M. Reumiller & Ursula Mayr & Maria Hasman & Lukas E. Schmidt & Sean A. Burnap & Konstantinos Theofilatos & Javier Barallobre-Barreiro & Arne Beran & Maria Grandoch & Alessa, 2022. "Reduced secretion of neuronal growth regulator 1 contributes to impaired adipose-neuronal crosstalk in obesity," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34846-w
    DOI: 10.1038/s41467-022-34846-w
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    References listed on IDEAS

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    1. Xing Zeng & Mengchen Ye & Jon M. Resch & Mark P. Jedrychowski & Bo Hu & Bradford B. Lowell & David D. Ginty & Bruce M. Spiegelman, 2019. "Publisher Correction: Innervation of thermogenic adipose tissue via a calsyntenin 3β–S100b axis," Nature, Nature, vol. 570(7760), pages 32-32, June.
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    3. Xing Zeng & Mengchen Ye & Jon M. Resch & Mark P. Jedrychowski & Bo Hu & Bradford B. Lowell & David D. Ginty & Bruce M. Spiegelman, 2019. "Innervation of thermogenic adipose tissue via a calsyntenin 3β–S100b axis," Nature, Nature, vol. 569(7755), pages 229-235, May.
    4. Marion Peyrou & Rubén Cereijo & Tania Quesada-López & Laura Campderrós & Aleix Gavaldà-Navarro & Laura Liñares-Pose & Elena Kaschina & Thomas Unger & Miguel López & Marta Giralt & Francesc Villarroya, 2020. "The kallikrein–kinin pathway as a mechanism for auto-control of brown adipose tissue activity," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
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    1. Xun Huang & Xinmeng Li & Hongyu Shen & Yiheng Zhao & Zhao Zhou & Yushuang Wang & Jingfei Yao & Kaili Xue & Dongmei Wu & Yifu Qiu, 2023. "Transcriptional repression of beige fat innervation via a YAP/TAZ-S100B axis," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

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