Pulmonary Hypertension Group, Center for Perinatal Research, Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH, USA.
Department of Pediatrics, The Ohio State University College of Medicine, Columbus, OH, USA.
Physiol Rep. 2020 Sep;8(17):e14559. doi: 10.14814/phy2.14559.
Phosphodiesterase 3 (PDE3), of which there are two isoforms, PDE3A and PDE3B, hydrolyzes cAMP and cGMP-cyclic nucleotides important in the regulation of pulmonary vascular tone. PDE3 has been implicated in pulmonary hypertension unresponsive to nitric oxide (NO); however, contributions of the two isoforms are not known. Furthermore, adenosine monophosphate-activated protein kinase (AMPK), a critical regulator of cellular energy homeostasis, has been shown to be modulated by PDE3 in varying cell types. While AMPK has recently been implicated in pulmonary hypertension pathogenesis, its role and regulation in the pulmonary vasculature remain to be elucidated. Therefore, we utilized human pulmonary artery smooth muscle cells (hPASMC) to test the hypothesis that NO increases PDE3 expression in an isoform-specific manner, thereby activating AMPK and inhibiting hPASMC proliferation. We found that in hPASMC, NO treatment increased PDE3A protein expression and PDE3 activity with a concomitant decrease in cAMP concentrations and increase in AMPK phosphorylation. Knockdown of PDE3A using siRNA transfection blunted the NO-induced AMPK activation, indicating that PDE3A plays an important role in AMPK regulation in hPASMC. Treatment with a soluble guanylate cyclase (sGC) stimulator increased PDE3A expression and AMPK activation similar to that seen with NO treatment, whereas treatment with a sGC inhibitor blunted the NO-induced increase in PDE3A and AMPK activation. These results suggest that NO increases PDE3A expression, decreases cAMP, and activates AMPK via the sGC-cGMP pathway. We speculate that NO-induced increases in PDE3A and AMPK may have implications in the pathogenesis and the response to therapies in pulmonary hypertensive disorders.
磷酸二酯酶 3(PDE3)有两种同工型,PDE3A 和 PDE3B,水解 cAMP 和 cGMP-环核苷酸,这些核苷酸在肺血管张力的调节中很重要。PDE3 与对一氧化氮(NO)无反应的肺动脉高压有关;然而,两种同工型的贡献尚不清楚。此外,腺苷单磷酸激活蛋白激酶(AMPK)是细胞能量稳态的关键调节剂,已经证明在不同的细胞类型中,PDE3 可以调节 AMPK。虽然 AMPK 最近被牵连到肺动脉高压发病机制中,但它在肺血管中的作用和调节仍有待阐明。因此,我们利用人肺动脉平滑肌细胞(hPASMC)来检验假设,即 NO 以同工型特异性的方式增加 PDE3 的表达,从而激活 AMPK 并抑制 hPASMC 的增殖。我们发现,在 hPASMC 中,NO 处理以同工型特异性的方式增加 PDE3A 蛋白表达和 PDE3 活性,同时降低 cAMP 浓度并增加 AMPK 磷酸化。使用 siRNA 转染进行 PDE3A 敲低削弱了 NO 诱导的 AMPK 激活,表明 PDE3A 在 hPASMC 中对 AMPK 调节起着重要作用。可溶性鸟苷酸环化酶(sGC)刺激剂的处理增加了 PDE3A 表达和 AMPK 激活,类似于 NO 处理,而 sGC 抑制剂的处理则削弱了 NO 诱导的 PDE3A 和 AMPK 激活增加。这些结果表明,NO 通过 sGC-cGMP 途径增加 PDE3A 表达、降低 cAMP 和激活 AMPK。我们推测,NO 诱导的 PDE3A 和 AMPK 增加可能对肺动脉高压疾病的发病机制和对治疗的反应有影响。