Seet Li-Fong, Toh Li Zhen, Finger Sharon N, Chu Stephanie W L, Stefanovic Branko, Wong Tina T
Ocular Therapeutics and Drug Delivery, Singapore Eye Research Institute, Singapore, Singapore.
Department of Ophthalmology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore.
J Mol Med (Berl). 2016 Mar;94(3):321-34. doi: 10.1007/s00109-015-1358-z. Epub 2015 Oct 27.
Overproduction of type I collagen is associated with a wide range of fibrotic diseases as well as surgical failure such as in glaucoma filtration surgery (GFS). Its modulation is therefore of clinical importance. Valproic acid (VPA) is known to reduce collagen in a variety of tissues with unclear mechanism of action. In this report, we demonstrate that VPA inhibited collagen production in both conjunctival fibroblasts and the mouse model of GFS. In fibroblasts, VPA decreased type I collagen expression which intensified with longer drug exposure and suppressed steady-state type I collagen promoter activity. Moreover, VPA decreased Smad2, Smad3 and Smad4 but increased Smad6 expression with a similar intensity-exposure profile. Reduction of Smad3 using small hairpin RNA and/or overexpression of Smad6 resulted in decreased collagen expression which was exacerbated when VPA was simultaneously present. Furthermore, fibrogenic TGF-β2 failed to induce collagen when VPA was present, as opposed to the myofibroblast markers, beta-actin, alpha-smooth muscle actin and tenascin-C, which were elevated by TGF-β2. VPA suppressed p3TP-Lux luciferase activity and selectively rescued Smad6 expression from suppression by TGF-β2. Notably, SMAD6 overexpression reduced the effectiveness of TGF-β2 in inducing collagen expression. In corroboration, VPA inhibited type I collagen but increased Smad6 expression in the late phase of wound healing in the mouse model of GFS. Taken together, our data indicate that VPA has the capacity to effectively suppress both steady-state and fibrogenic activation of type I collagen expression by modulating Smad expression. Hence, VPA is potentially applicable as an anti-fibrotic therapeutic by targeting collagen. Key message: • VPA modulates type I collagen expression via members of the Smad family. • VPA suppresses Smad2, Smad3 and Smad4 but upregulates Smad6. • Smad3 and Smad6 are involved in VPA regulation of steady-state collagen expression. • Smad6 is involved in VPA modulation of TGF-β-stimulated collagen expression. • VPA reduces collagen and upregulates Smad6 in the mouse model of glaucoma filtration surgery.
I型胶原蛋白的过度产生与多种纤维化疾病以及手术失败相关,如青光眼滤过手术(GFS)。因此,对其进行调节具有临床重要性。已知丙戊酸(VPA)可减少多种组织中的胶原蛋白,但其作用机制尚不清楚。在本报告中,我们证明VPA可抑制结膜成纤维细胞和GFS小鼠模型中的胶原蛋白产生。在成纤维细胞中,VPA可降低I型胶原蛋白的表达,且随着药物暴露时间延长而增强,并抑制稳态I型胶原蛋白启动子活性。此外,VPA可降低Smad2、Smad3和Smad4的表达,但增加Smad6的表达,其强度-暴露曲线相似。使用小发夹RNA降低Smad3的表达和/或过表达Smad6会导致胶原蛋白表达降低,当同时存在VPA时,这种情况会加剧。此外,与肌成纤维细胞标志物β-肌动蛋白、α-平滑肌肌动蛋白和腱生蛋白-C不同,当存在VPA时,促纤维化的TGF-β2无法诱导胶原蛋白产生,而TGF-β2可使这些标志物升高。VPA可抑制p3TP-Lux荧光素酶活性,并选择性地挽救被TGF-β2抑制的Smad6表达。值得注意的是,SMAD6过表达可降低TGF-β2诱导胶原蛋白表达的有效性。与此相符的是,在GFS小鼠模型的伤口愈合后期,VPA可抑制I型胶原蛋白的表达,但增加Smad6的表达。综上所述,我们的数据表明VPA有能力通过调节Smad表达来有效抑制I型胶原蛋白表达的稳态和纤维化激活。因此,VPA有可能作为一种靶向胶原蛋白的抗纤维化治疗药物。关键信息:• VPA通过Smad家族成员调节I型胶原蛋白表达。• VPA抑制Smad2、Smad3和Smad4,但上调Smad6。• Smad3和Smad6参与VPA对稳态胶原蛋白表达的调节。• Smad6参与VPA对TGF-β刺激的胶原蛋白表达的调节。• 在青光眼滤过手术小鼠模型中,VPA可减少胶原蛋白并上调Smad6。