Benito-León María, Gil-Redondo Juan Carlos, Perez-Sen Raquel, Delicado Esmerilda G, Ortega Felipe, Gomez-Villafuertes Rosa
Department of Biochemistry and Molecular Biology, Faculty of Veterinary Medicine, University Complutense of Madrid, Madrid, Spain.
Instituto Universitario de Investigación en Neuroquímica (IUIN), Madrid, Spain.
Front Cell Dev Biol. 2022 Dec 15;10:1049566. doi: 10.3389/fcell.2022.1049566. eCollection 2022.
P2X7 receptor (P2RX7) is expressed strongly by most human cancers, including neuroblastoma, where high levels of P2RX7 are correlated with a poor prognosis for patients. Tonic activation of P2X7 receptor favors cell metabolism and angiogenesis, thereby promoting cancer cell proliferation, immunosuppression, and metastasis. Although understanding the mechanisms that control P2X7 receptor levels in neuroblastoma cells could be biologically and clinically relevant, the intracellular signaling pathways involved in this regulation remain poorly understood. Here we show that (E)-2-benzylidene-3-(cyclohexylamino)-2,3-dihydro-1H-inden-1-one (BCI), an allosteric inhibitor of dual specificity phosphatases (DUSP) 1 and 6, enhances the expression of P2X7 receptor in N2a neuroblastoma cells. We found that exposure to BCI induces the phosphorylation of mitogen-activated protein kinases p38 and JNK, while it prevents the phosphorylation of ERK1/2. BCI enhanced dual specificity phosphatase 1 expression, whereas it induced a decrease in the dual specificity phosphatase 6 transcripts, suggesting that BCI-dependent inhibition of dual specificity phosphatase 1 may be responsible for the increase in p38 and JNK phosphorylation. The weaker ERK phosphorylation induced by BCI was reversed by p38 inhibition, indicating that this MAPK is involved in the regulatory loop that dampens ERK activity. The PP2A phosphatase appears to be implicated in the p38-dependent dephosphorylation of ERK1/2. In addition, the PTEN phosphatase inhibition also prevented ERK1/2 dephosphorylation, probably through p38 downregulation. By contrast, inhibition of the p53 nuclear factor decreased ERK phosphorylation, probably enhancing the activity of p38. Finally, the inhibition of either p38 or Sp1-dependent transcription halved the increase in P2X7 receptor expression induced by BCI. Moreover, the combined inhibition of both p38 and Sp1 completely prevented the effect exerted by BCI. Together, our results indicate that dual specificity phosphatase 1 acts as a novel negative regulator of P2X7 receptor expression in neuroblastoma cells due to the downregulation of the p38 pathway.
P2X7受体(P2RX7)在大多数人类癌症中均有强烈表达,包括神经母细胞瘤,其中P2X7的高水平表达与患者的不良预后相关。P2X7受体的持续性激活有利于细胞代谢和血管生成,从而促进癌细胞增殖、免疫抑制和转移。尽管了解控制神经母细胞瘤细胞中P2X7受体水平的机制在生物学和临床上可能具有重要意义,但参与这种调节的细胞内信号通路仍知之甚少。在此,我们表明(E)-2-亚苄基-3-(环己基氨基)-2,3-二氢-1H-茚-1-酮(BCI),一种双特异性磷酸酶(DUSP)1和6的变构抑制剂,可增强N2a神经母细胞瘤细胞中P2X7受体的表达。我们发现,暴露于BCI会诱导丝裂原活化蛋白激酶p38和JNK的磷酸化,同时阻止ERK1/2的磷酸化。BCI增强了双特异性磷酸酶1的表达,而它诱导双特异性磷酸酶6转录本减少,这表明BCI依赖的双特异性磷酸酶1抑制可能是p38和JNK磷酸化增加的原因。BCI诱导的较弱的ERK磷酸化被p38抑制所逆转,表明该丝裂原活化蛋白激酶参与了抑制ERK活性的调节回路。PP2A磷酸酶似乎与ERK1/2的p38依赖性去磷酸化有关。此外,PTEN磷酸酶抑制也可能通过p38下调阻止了ERK1/2的去磷酸化。相比之下,p53核因子的抑制降低了ERK磷酸化,可能增强了p38的活性。最后,p38或Sp1依赖性转录的抑制使BCI诱导的P2X7受体表达增加减半。此外,p38和Sp1的联合抑制完全阻止了BCI所产生的作用。总之,我们的结果表明,由于p38途径的下调,双特异性磷酸酶1在神经母细胞瘤细胞中作为P2X7受体表达的新型负调节因子发挥作用。