Division of Medical Genetics, Department of Biomedical Sciences and Human Oncology (DIMO), University of Bari "Aldo Moro", Piazza G. Cesare, 11, Bari, Italy.
Medical Genetics, National Institute for Gastroenterology, IRCCS 'S. de Bellis', Piazza G. Cesare, 11, Castellana Grotte, Bari, Italy.
Neurogenetics. 2018 May;19(2):77-91. doi: 10.1007/s10048-018-0540-1. Epub 2018 Mar 16.
Postzygotic mutations of the PIK3CA [phosphatidylinositol-4,5-bisphosphate 3-kinase catalytic subunit alpha] gene constitutively activate the PI3K/AKT/mTOR pathway in PIK3CA-related overgrowth spectrum (PROS) patients, causing congenital mosaic tissue overgrowth that even multiple surgeries cannot solve. mTOR inhibitors are empirically tested and given for compassionate use in these patients. PROS patients could be ideal candidates for enrolment in trials with PI3K/AKT pathway inhibitors, considering the "clean" cellular setting in which a unique driver, a PIK3CA mutation, is present. We aimed to assess the effects of blocking the upstream pathway of mTOR on PROS patient-derived cells by using ARQ 092, a potent, selective, allosteric, and experimental orally bioavailable and highly selective AKT-inhibitor with activity and long-term tolerability, currently under clinical development for treatment of cancer and Proteus syndrome. Cell samples (i.e., primary fibroblasts) were derived from cultured tissues obtained from six PROS patients [3 boys, 3 girls; aged 2 to 17 years] whose spectrum of PIK3A-related overgrowth included HHML [hemihyperplasia multiple lipomatosis; n = 1], CLOVES [congenital lipomatosis, overgrowth, vascular malformations, epidermal nevi, spinal/skeletal anomalies, scoliosis; n = 1], and MCAP [megalencephaly capillary malformation syndrome; n = 4]. We performed the following: (a) a deep sequencing assay of PI3K/AKT pathway genes in the six PROS patients' derived cells to identify the causative mutations and (b) a pathway analysis to assess the phosphorylation status of AKT [Ser473 and Thr308] and its downstream targets [pAKTS1 (Thr246), pRPS6 (Ser235/236), and pRPS6Kβ1 (Ser371)]. The anti-proliferative effect of ARQ 092 was tested and compared to other PI3K/AKT/mTOR inhibitors [i.e., wortmannin, LY249002, and rapamycin] in the six PROS patient-derived cells. Using ARQ 092 to target AKT, a critical node connecting PI3K and mTOR pathways, we observed the following: (1) strong anti-proliferative activity [ARQ 092 at 0.5, 1, and 2.5 μM blunted phosphorylation of AKT and its downstream targets (in the presence or absence of serum) and inhibited proliferation after 72 h; rapamycin at 100 nM did not decrease AKT phosphorylation] and (2) less cytotoxicity as compared to rapamycin and wortmannin. We demonstrated the following: (a) that PROS cells are dependent on AKT; (b) the advantage of inhibiting the pathway immediately downstream of PI3K to circumventing problems depending on multiple classes a PI3K kinases; and (c) that PROS patients benefit from inhibition of AKT rather than mTOR. Clinical development of ARQ 092 in PROS patients is on going in these patients.
PIK3CA [磷脂酰肌醇-4,5-二磷酸 3-激酶催化亚基 alpha] 基因的后合子突变使 PI3K/AKT/mTOR 通路在 PIK3CA 相关过度生长谱 (PROS) 患者中持续激活,导致先天性镶嵌组织过度生长,即使多次手术也无法解决。mTOR 抑制剂被经验性地用于这些患者的同情使用。鉴于存在独特的驱动因素 PIK3CA 突变,PROS 患者可能是 PI3K/AKT 通路抑制剂临床试验的理想候选者。我们旨在通过使用 ARQ 092 来评估阻断 mTOR 上游通路对 PROS 患者来源细胞的影响,ARQ 092 是一种有效的、选择性的、变构的、实验性的口服生物可利用的和高度选择性的 AKT 抑制剂,目前正在临床开发中用于治疗癌症和 Proteus 综合征。细胞样本(即原代成纤维细胞)来自于从 6 名 PROS 患者(3 名男孩,3 名女孩;年龄 2 至 17 岁)培养的组织中获得,其 PIK3A 相关过度生长谱包括 HHML[单侧多脂血症;n=1]、CLOVES[先天性脂肪过多症、过度生长、血管畸形、表皮痣、脊柱/骨骼异常、脊柱侧凸;n=1]和 MCAP[巨脑毛细血管畸形综合征;n=4]。我们进行了以下操作:(a)对 6 名 PROS 患者来源细胞中的 PI3K/AKT 通路基因进行深度测序分析,以确定致病突变;(b)进行通路分析,以评估 AKT[Ser473 和 Thr308]及其下游靶标[pAKTS1(Thr246)、pRPS6(Ser235/236)和 pRPS6Kβ1(Ser371)]的磷酸化状态。在 6 名 PROS 患者来源的细胞中,我们测试了 ARQ 092 的抗增殖作用,并将其与其他 PI3K/AKT/mTOR 抑制剂[即 wortmannin、LY249002 和 rapamycin]进行了比较。使用 ARQ 092 靶向 AKT,这是连接 PI3K 和 mTOR 通路的关键节点,我们观察到:(1)强烈的抗增殖活性[ARQ 092 在 0.5、1 和 2.5μM 时抑制 AKT 及其下游靶标的磷酸化(有或无血清),并在 72 小时后抑制增殖;100nM 的 rapamycin 并未降低 AKT 磷酸化]和(2)与 rapamycin 和 wortmannin 相比,细胞毒性更小。我们证明了以下几点:(a)PROS 细胞依赖于 AKT;(b)抑制 PI3K 下游通路的优势在于避免了依赖多种 PI3K 激酶类别的问题;(c)PROS 患者受益于 AKT 而不是 mTOR 的抑制。ARQ 092 在 PROS 患者中的临床开发正在这些患者中进行。