Yee Patricia P, Wang Jianli, Chih Stephen Y, Aregawi Dawit G, Glantz Michael J, Zacharia Brad E, Thamburaj Krishnamoorthy, Li Wei
Division of Hematology and Oncology, Department of Pediatrics, Penn State College of Medicine, Hershey, PA, United States.
Medical Scientist Training Program, Penn State College of Medicine, Hershey, PA, United States.
Front Oncol. 2022 Oct 14;12:993649. doi: 10.3389/fonc.2022.993649. eCollection 2022.
Tumor necrosis is a poor prognostic marker in glioblastoma (GBM) and a variety of other solid cancers. Accumulating evidence supports that necrosis could facilitate tumor progression and resistance to therapeutics. GBM necrosis is typically first detected by magnetic resonance imaging (MRI), after prominent necrosis has already formed. Therefore, radiological appearances of early necrosis formation and the temporal-spatial development of necrosis alongside tumor progression remain poorly understood. This knowledge gap leads to a lack of reliable radiographic diagnostic/prognostic markers in early GBM progression to detect necrosis. Recently, we reported an orthotopic xenograft GBM murine model driven by hyperactivation of the Hippo pathway transcriptional coactivator with PDZ-binding motif (TAZ) which recapitulates the extent of GBM necrosis seen among patients. In this study, we utilized this model to perform a temporal radiographic and histological study of necrosis development. We observed tumor tissue actively undergoing necrosis first appears more brightly enhancing in the early stages of progression in comparison to the rest of the tumor tissue. Later stages of tumor progression lead to loss of enhancement and unenhancing signals in the necrotic central portion of tumors on T1-weighted post-contrast MRI. This central unenhancing portion coincides with the radiographic and clinical definition of necrosis among GBM patients. Moreover, as necrosis evolves, two relatively more contrast-enhancing rims are observed in relationship to the solid enhancing tumor surrounding the central necrosis in the later stages. The outer more prominently enhancing rim at the tumor border probably represents the infiltrating tumor edge, and the inner enhancing rim at the peri-necrotic region may represent locally infiltrating immune cells. The associated inflammation at the peri-necrotic region was further confirmed by immunohistochemical study of the temporal development of tumor necrosis. Neutrophils appear to be the predominant immune cell population in this region as necrosis evolves. This study shows central, brightly enhancing areas associated with inflammation in the tumor microenvironment may represent an early indication of necrosis development in GBM.
肿瘤坏死在胶质母细胞瘤(GBM)及多种其他实体癌中是一种预后不良的标志物。越来越多的证据支持坏死可促进肿瘤进展及对治疗的抵抗。GBM坏死通常在显著坏死已经形成后通过磁共振成像(MRI)首次检测到。因此,早期坏死形成的影像学表现以及坏死随肿瘤进展的时空发展仍知之甚少。这一知识空白导致在GBM早期进展中缺乏可靠的影像学诊断/预后标志物来检测坏死。最近,我们报道了一种由具有PDZ结合基序(TAZ)的Hippo通路转录共激活因子过度激活驱动的原位异种移植GBM小鼠模型,该模型概括了患者中所见的GBM坏死程度。在本研究中,我们利用该模型对坏死发展进行了时间性影像学和组织学研究。我们观察到,与肿瘤组织的其余部分相比,在进展早期,积极发生坏死的肿瘤组织最初表现出更明显的强化。肿瘤进展的后期导致T1加权增强后MRI上肿瘤坏死中央部分的强化消失和无强化信号。这个中央无强化部分与GBM患者中坏死的影像学和临床定义一致。此外,随着坏死的演变,在后期相对于围绕中央坏死的实性强化肿瘤观察到两个相对更强化的边缘。肿瘤边界处更明显强化的外缘可能代表浸润性肿瘤边缘,坏死周围区域的内缘强化可能代表局部浸润的免疫细胞。通过对肿瘤坏死时间发展的免疫组织化学研究进一步证实了坏死周围区域的相关炎症。随着坏死的演变,中性粒细胞似乎是该区域主要的免疫细胞群体。这项研究表明,肿瘤微环境中与炎症相关的中央、明显强化区域可能代表GBM坏死发展的早期迹象。