Dumont-UCLA Transplant Center, Division of Liver and Pancreas Transplantation, Department of Surgery, David Geffen School of Medicine at University of California, Los Angeles, Los Angeles, CA 90095.
Department of Liver Surgery, First Affiliated Hospital of Nanjing Medical University, Nanjing, Jiangsu 210008, China.
J Immunol. 2020 Aug 15;205(4):1147-1156. doi: 10.4049/jimmunol.2000397. Epub 2020 Jul 17.
Glycogen synthase kinase 3 (Gsk3) α and β are both constitutively active and inhibited upon stimulation by N-terminal serine phosphorylation. Although roles of active Gsk3 in liver ischemia reperfusion injury (IRI) have been well appreciated, whether Gsk3 N-terminal serine phosphorylation has any functional significance in the disease process remains unclear. In a murine liver partial warm ischemia model, we studied Gsk3 N-terminal serine mutant knock-in (KI) mice and showed that liver IRI was decreased in Gsk3αS21A but increased in Gsk3βS9A mutant KI mice. Bone marrow chimeric experiments revealed that the Gsk3α, but not β, mutation in liver parenchyma protected from IRI, and both mutations in bone marrow-derived cells exacerbated liver injuries. Mechanistically, mutant Gsk3α protected hepatocytes from inflammatory (TNF-α) cell death by the activation of HIV-1 TAT-interactive protein 60 (TIP60)-mediated autophagy pathway. The pharmacological inhibition of TIP60 or autophagy diminished the protection of the Gsk3α mutant hepatocytes from inflammatory cell death in vitro and the Gsk3α mutant KI mice from liver IRI in vivo. Thus, Gsk3 N-terminal serine phosphorylation inhibits liver innate immune activation but suppresses hepatocyte autophagy in response to inflammation. Gsk3 αS21, but not βS9, mutation is sufficient to sustain Gsk4 activities in hepatocytes and protect livers from IRI via TIP60 activation.
糖原合成酶激酶 3(Gsk3)α和β均为组成性激活,其 N 端丝氨酸磷酸化可被抑制。虽然活性 Gsk3 在肝缺血再灌注损伤(IRI)中的作用已得到充分认识,但 Gsk3 N 端丝氨酸磷酸化在疾病过程中是否具有功能意义仍不清楚。在小鼠肝脏部分热缺血模型中,我们研究了 Gsk3 N 端丝氨酸突变敲入(KI)小鼠,并表明 Gsk3αS21A 中的肝 IRI 减少,但 Gsk3βS9A 突变 KI 小鼠中的肝 IRI 增加。骨髓嵌合实验表明,肝脏实质中的 Gsk3α突变(而非β突变)可保护免受 IRI,而骨髓来源细胞中的两种突变均加重了肝损伤。从机制上讲,突变 Gsk3α通过激活 HIV-1 TAT 相互作用蛋白 60(TIP60)介导的自噬途径,保护肝细胞免受炎症(TNF-α)细胞死亡。TIP60 或自噬的药理学抑制减弱了突变 Gsk3α 肝细胞体外免受炎症细胞死亡的保护作用以及突变 Gsk3α KI 小鼠体内免受肝 IRI 的保护作用。因此,Gsk3 N 端丝氨酸磷酸化抑制肝脏固有免疫激活,但抑制肝细胞在炎症反应下的自噬。Gsk3αS21 而非 Gsk3βS9 的突变足以维持肝细胞中 Gsk4 的活性,并通过 TIP60 激活来保护肝脏免受 IRI。