SENP2 regulates UCP1-dependent thermogenesis in brown adipocytes via deSUMOylation of ERRα

Exp Mol Med. 2025 Jun;57(6):1283-1293. doi: 10.1038/s12276-025-01458-5. Epub 2025 Jun 27.

Abstract

Brown adipose tissue (BAT) is responsible for energy homeostasis and adaptive thermogenesis. SUMO-specific protease 2 (SENP2) plays an essential role in adipogenesis; however, the role of SENP2 in BAT metabolism has not been explored. Here we investigated the role of SENP2 in mature brown adipocytes with a brown adipocyte-specific SENP2 knockout (Senp2-BKO) mouse model generated using the uncoupling protein 1 (Ucp1)-Cre. High-fat diet-induced insulin resistance was aggravated in Senp2-BKO mice compared with control mice. In Senp2-BKO mice, adaptive thermogenesis upon acute cold exposure was impaired and UCP1 expression was barely induced upon cold or β-adrenergic stimulation. SENP2-mediated deSUMOylation of estrogen-related receptor alpha (ERRα) significantly enhanced Ucp1 promoter activity through activation of the ERRα/PGC1α complex. The absence of SENP2 inhibited formation of ERRα, cAMP-response element-binding protein (CREB) and RNA Polymerase II transcriptional complex at the Ucp1 promoter following β3-adrenergic stimulation. In addition, SUMOylation of ERRα severely interfered with binding of ERRα to its DNA-binding site (ERRE) in the promoter of Ucp1. Our findings revealed that SENP2 plays a role in the metabolic flexibility and thermogenic efficiency of BAT, particularly in response to β3-adrenergic activation.

MeSH terms

  • Adipocytes, Brown* / metabolism
  • Animals
  • Cysteine Endopeptidases* / genetics
  • Cysteine Endopeptidases* / metabolism
  • Diet, High-Fat
  • ERRalpha Estrogen-Related Receptor
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Receptors, Estrogen* / genetics
  • Receptors, Estrogen* / metabolism
  • Sumoylation
  • Thermogenesis*
  • Uncoupling Protein 1* / genetics
  • Uncoupling Protein 1* / metabolism

Substances

  • Uncoupling Protein 1
  • Cysteine Endopeptidases
  • Receptors, Estrogen
  • ERRalpha Estrogen-Related Receptor
  • Senp2 protein, mouse
  • Ucp1 protein, mouse