Department of Neuropathology, Heinrich Heine University, Düsseldorf, Germany.
Department of Neuropathology, Heinrich Heine University, Düsseldorf, Germany; Institute of Pathobiochemistry, University Medical Center of the Johannes Gutenberg-University, Mainz, Germany.
J Biol Chem. 2023 Aug;299(8):104997. doi: 10.1016/j.jbc.2023.104997. Epub 2023 Jun 30.
Presenilin-1 (PSEN1) is the catalytic subunit of the intramembrane protease γ-secretase and undergoes endoproteolysis during its maturation. Heterozygous mutations in the PSEN1 gene cause early-onset familial Alzheimer's disease (eFAD) and increase the proportion of longer aggregation-prone amyloid-β peptides (Aβ42 and/or Aβ43). Previous studies had suggested that PSEN1 mutants might act in a dominant-negative fashion by functional impediment of wild-type PSEN1, but the exact mechanism by which PSEN1 mutants promote pathogenic Aβ production remains controversial. Using dual recombinase-mediated cassette exchange (dRMCE), here we generated a panel of isogenic embryonic and neural stem cell lines with heterozygous, endogenous expression of PSEN1 mutations. When catalytically inactive PSEN1 was expressed alongside the wild-type protein, we found the mutant accumulated as a full-length protein, indicating that endoproteolytic cleavage occurred strictly as an intramolecular event. Heterozygous expression of eFAD-causing PSEN1 mutants increased the Aβ42/Aβ40 ratio. In contrast, catalytically inactive PSEN1 mutants were still incorporated into the γ-secretase complex but failed to change the Aβ42/Aβ40 ratio. Finally, interaction and enzyme activity assays demonstrated the binding of mutant PSEN1 to other γ-secretase subunits, but no interaction between mutant and wild-type PSEN1 was observed. These results establish that pathogenic Aβ production is an intrinsic property of PSEN1 mutants and strongly argue against a dominant-negative effect in which PSEN1 mutants would compromise the catalytic activity of wild-type PSEN1 through conformational effects.
早发型家族性阿尔茨海默病(eFAD)的 PSEN1 基因突变会增加长聚集倾向的淀粉样β肽(Aβ42 和/或 Aβ43)的比例。先前的研究表明,PSEN1 突变体可能通过野生型 PSEN1 的功能障碍以显性负性方式起作用,但 PSEN1 突变体促进致病性 Aβ 产生的确切机制仍存在争议。使用双重组酶介导的盒交换(dRMCE),我们在此生成了一组具有异源、内源性表达 PSEN1 突变的胚胎和神经干细胞系。当与野生型蛋白一起表达无催化活性的 PSEN1 时,我们发现突变体作为全长蛋白积累,表明内切蛋白酶裂解严格作为分子内事件发生。eFAD 引起的 PSEN1 突变体的杂合表达增加了 Aβ42/Aβ40 比值。相比之下,无催化活性的 PSEN1 突变体仍被整合到γ-分泌酶复合物中,但未能改变 Aβ42/Aβ40 比值。最后,相互作用和酶活性测定表明突变 PSEN1 与其他 γ-分泌酶亚基结合,但未观察到突变和野生型 PSEN1 之间的相互作用。这些结果表明致病性 Aβ 产生是 PSEN1 突变体的固有特性,并强烈反对 PSEN1 突变体通过构象效应破坏野生型 PSEN1 的催化活性的显性负效应。