Tennakoon Mithila, Thotamune Waruna, Payton John L, Karunarathne Ajith
Department of Chemistry, Saint Louis University, Saint Louis, MO 63103, USA.
Department of Chemistry and Biochemistry, The University of Toledo, Toledo, OH 43606, USA.
bioRxiv. 2023 Jul 4:2023.07.04.547731. doi: 10.1101/2023.07.04.547731.
Prenylation is a universal and irreversible post-translational modification that supports membrane interactions of proteins involved in various cellular processes, including migration, proliferation, and survival. Thus, dysregulation of prenylation contributes to multiple disorders, including cancers, vascular diseases, and neurodegenerative diseases. During prenylation, prenyltransferase enzymes tether metabolically produced isoprenoid lipids to proteins via a thioether linkage. Pharmacological inhibition of the lipid synthesis pathway by statins has long been a therapeutic approach to control hyperlipidemia. Building on our previous finding that statins inhibit membrane association of G protein γ (Gγ) in a subtype-dependent manner, we investigated the molecular reasoning for this differential. We examined the prenylation efficacy of carboxy terminus (Ct) mutated Gγ in cells exposed to Fluvastatin and prenyl transferase inhibitors and monitored the subcellular localization of fluorescently tagged Gγ subunits and their mutants using live-cell confocal imaging. Reversible optogenetic unmasking-masking of Ct residues was used to probe their contribution to the prenylation process and membrane interactions of the prenylated proteins. Our findings suggest that specific Ct residues regulate membrane interactions of the Gγ polypeptide statin sensitivity, and prenylation efficacy. Our results also show that a few hydrophobic and charged residues at the Ct are crucial determinants of a protein's prenylation ability, especially under suboptimal conditions. Given the cell and tissue-specific expression of different Gγ subtypes, our findings explain how and why statins differentially perturb heterotrimeric G protein signaling in specific cells and tissues. Our results may provide molecular reasoning for repurposing statins as Ras oncogene inhibitors and the failure of using prenyltransferase inhibitors in cancer treatment.
异戊二烯化是一种普遍且不可逆的翻译后修饰,它支持参与各种细胞过程(包括迁移、增殖和存活)的蛋白质与膜的相互作用。因此,异戊二烯化失调会导致多种疾病,包括癌症、血管疾病和神经退行性疾病。在异戊二烯化过程中,异戊二烯基转移酶通过硫醚键将代谢产生的类异戊二烯脂质连接到蛋白质上。长期以来,他汀类药物对脂质合成途径的药理抑制一直是控制高脂血症的一种治疗方法。基于我们之前发现他汀类药物以亚型依赖性方式抑制G蛋白γ(Gγ)的膜结合这一结果,我们研究了这种差异的分子原因。我们检测了在暴露于氟伐他汀和异戊二烯基转移酶抑制剂的细胞中,羧基末端(Ct)突变的Gγ的异戊二烯化效率,并使用活细胞共聚焦成像监测荧光标记的Gγ亚基及其突变体的亚细胞定位。利用Ct残基的可逆光遗传学去掩盖-掩盖技术来探究它们对异戊二烯化过程以及异戊二烯化蛋白质的膜相互作用的贡献。我们的研究结果表明,特定的Ct残基调节Gγ多肽的膜相互作用、他汀类药物敏感性和异戊二烯化效率。我们的结果还表明,Ct处的一些疏水和带电荷残基是蛋白质异戊二烯化能力的关键决定因素,尤其是在次优条件下。鉴于不同Gγ亚型在细胞和组织中的特异性表达,我们的研究结果解释了他汀类药物如何以及为何在特定细胞和组织中差异地干扰异三聚体G蛋白信号传导。我们的结果可能为将他汀类药物重新用作Ras癌基因抑制剂以及在癌症治疗中使用异戊二烯基转移酶抑制剂失败提供分子依据。