Fontana Andrea O, Piffaretti Deborah, Marchi Francesco, Burgio Floriana, Faia-Torres Ana Bela, Paganetti Paolo, Pinton Sandra, Pieles Uwe, Reinert Michael
Laboratories of Biomedical Neurosciences (LBN), Department of Neurosurgery, Neurocenter of Southern Switzerland, Ente Ospedaliero Cantonale, Ticino, Switzerland.
FHNW, Muttenz, BL, Switzerland.
J Neurooncol. 2017 Jul;133(3):497-507. doi: 10.1007/s11060-017-2474-0. Epub 2017 May 12.
The extent of 5-aminolevulinic acid (5-ALA) guided tumor resection has a determining impact in high-grade glioma and glioblastoma surgery. Yet the intensity of the 5-ALA induced fluorescence may vary within the tumor. We aimed to correlate 5-ALA induced fluorescence with the expression of epithelial growth factor receptor (EGFR) and its constitutively active version EGFRvIII in different glioblastoma (GBM) cell lines. To elucidate the role of EGFR in the metabolism of 5-ALA in GBM cell lines with variable EGFR expression status, we analyzed the activation of EGFR by its primary ligand EGF, and its downstream effect on Heme oxygenase-1 (HO-1), a key enzyme regulating the metabolism of Protoporphyrin IX (PpIX), the fluorescent metabolite of 5-ALA. Effects of direct pharmacological inhibition by Tin(IV)-Protoporphyrin (SnPP) or gene knockdown by small interfering RNA (siRNA) on HO-1 enzyme were analyzed in respect to 5-ALA induced fluorescence. Furthermore, inhibition of EGFR by Gefitinib was tested. A significant difference in 5-ALA induced fluorescence was obtained in U87MG (low EGFR expression) and LN229EGFR cells (EGFR overexpression) compared to BS153 (EGFR overexpression/EGFRvIII+). Treatment of U87MG and LN229EGFR cells with EGF significantly reduced cellular fluorescence, by promoting HO-1 transcription and expression in a concentration-dependent manner. This effect could be reversed by EGFR-specific siRNA treatment, which reduced protein expression of about 80% in U87MG. Remarkably, inhibition of HO-1 activity by SnPP or reduction of HO-1 protein levels by siHO-1 treatment restored fluorescence in all cell lines, independently of EGFR quantitative and qualitative expression. Gefitinib treatment was able to restore fluorescence after EGF stimulation in U87MG cells but not in BS153 cells, overexpressing EGFR/EGFRvIII. In GBM cell lines, 5-ALA induced fluorescence is variable and influenced by EGF-induced downstream activation of HO-1. HO-1 protein expression was identified as a negative regulator of 5-ALA induced fluorescence in GBM cells. We further propose that co-expression of EGFRvIII but not quantitative EGFR expression influence HO-1 activity and therefore cellular fluorescence.
5-氨基酮戊酸(5-ALA)引导的肿瘤切除术范围在高级别胶质瘤和胶质母细胞瘤手术中具有决定性影响。然而,5-ALA诱导的荧光强度在肿瘤内可能会有所不同。我们旨在将5-ALA诱导的荧光与不同胶质母细胞瘤(GBM)细胞系中表皮生长因子受体(EGFR)及其组成型活性变体EGFRvIII的表达相关联。为了阐明EGFR在具有可变EGFR表达状态的GBM细胞系中5-ALA代谢中的作用,我们分析了EGFR被其主要配体表皮生长因子(EGF)激活的情况,以及其对血红素加氧酶-1(HO-1)的下游影响,HO-1是调节原卟啉IX(PpIX,5-ALA的荧光代谢产物)代谢的关键酶。分析了锡(IV)-原卟啉(SnPP)直接药理抑制或小干扰RNA(siRNA)基因敲低对HO-1酶的影响与5-ALA诱导荧光的关系。此外,还测试了吉非替尼对EGFR的抑制作用。与BS153(EGFR过表达/EGFRvIII阳性)相比,U87MG(低EGFR表达)和LN229EGFR细胞(EGFR过表达)在5-ALA诱导的荧光方面存在显著差异。用EGF处理U87MG和LN229EGFR细胞可通过以浓度依赖的方式促进HO-1转录和表达,显著降低细胞荧光。这种效应可通过EGFR特异性siRNA处理逆转,该处理使U87MG中的蛋白表达降低约80%。值得注意的是,SnPP抑制HO-1活性或siHO-1处理降低HO-1蛋白水平可在所有细胞系中恢复荧光,而与EGFR的定量和定性表达无关。吉非替尼处理能够在U87MG细胞中EGF刺激后恢复荧光,但在过表达EGFR/EGFRvIII的BS153细胞中则不能。在GBM细胞系中,5-ALA诱导的荧光是可变的,并受EGF诱导的HO-1下游激活影响。HO-1蛋白表达被确定为GBM细胞中5-ALA诱导荧光的负调节因子。我们进一步提出,EGFRvIII的共表达而非EGFR的定量表达会影响HO-1活性,进而影响细胞荧光。