San Diego Biomedical Research Institute, 3525 John Hopkins Court, Suite 200, 92121, San Diego, CA, USA.
Acta Neuropathol Commun. 2024 Mar 20;12(1):45. doi: 10.1186/s40478-024-01749-4.
Interactions between extracellular matrix (ECM) proteins and β1 integrins play an essential role maintaining vascular integrity in the brain, particularly under vascular remodeling conditions. As blood vessels in the spinal cord are reported to have distinct properties from those in the brain, here we examined the impact of β1 integrin inhibition on spinal cord vascular integrity, both under normoxic conditions, when blood vessels are stable, and during exposure to chronic mild hypoxia (CMH), when extensive vascular remodeling occurs. We found that a function-blocking β1 integrin antibody triggered a small degree of vascular disruption in the spinal cord under normoxic conditions, but under hypoxic conditions, it greatly enhanced (20-fold) vascular disruption, preferentially in spinal cord white matter (WM). This resulted in elevated microglial activation as well as marked loss of myelin integrity and reduced density of oligodendroglial cells. To understand why vascular breakdown is localized to WM, we compared expression levels of major BBB components of WM and grey matter (GM) blood vessels, but this revealed no obvious differences. Interestingly however, hypoxyprobe staining demonstrated that the most severe levels of spinal cord hypoxia induced by CMH occurred in the WM. Analysis of brain tissue revealed a similar preferential vulnerability of WM tracts to show vascular disruption under these conditions. Taken together, these findings demonstrate an essential role for β1 integrins in maintaining vascular integrity in the spinal cord, and unexpectedly, reveal a novel and fundamental difference between WM and GM blood vessels in their dependence on β1 integrin function during hypoxic exposure. Our data support the concept that the preferential WM vulnerability described may be less a result of intrinsic differences in vascular barrier properties between WM and GM, and more a consequence of differences in vascular density and architecture.
细胞外基质 (ECM) 蛋白与β1 整合素之间的相互作用对于维持大脑血管的完整性至关重要,尤其是在血管重塑的情况下。由于脊髓血管被报道具有与大脑血管不同的特性,因此我们研究了在正常氧条件下(此时血管稳定)以及在慢性轻度缺氧 (CMH) 暴露下(此时广泛发生血管重塑),β1 整合素抑制对脊髓血管完整性的影响。我们发现,在正常氧条件下,阻断β1 整合素功能的抗体可引发脊髓血管的轻微破坏,但在低氧条件下,它会极大地增强(20 倍)血管破坏,优先发生在脊髓白质(WM)中。这导致小胶质细胞激活增加,髓鞘完整性显著丧失,少突胶质细胞密度降低。为了了解为什么血管破裂局限于 WM,我们比较了 WM 和灰质(GM)血管的主要 BBB 成分的表达水平,但这并未显示出明显差异。然而,有趣的是,低氧探针染色表明,CMH 引起的脊髓缺氧最严重的程度发生在 WM 中。对脑组织的分析表明,在这些条件下,WM 中的血管破坏在脑白质通路中表现出相似的易感性。总之,这些发现表明β1 整合素在维持脊髓血管完整性方面起着至关重要的作用,而且出乎意料的是,在低氧暴露下,WM 和 GM 血管对β1 整合素功能的依赖性之间存在着一种新的、基本的差异。我们的数据支持这样一种观点,即描述的 WM 易损性可能不是 WM 和 GM 血管之间内在的血管屏障特性差异的结果,而更多的是由于血管密度和结构的差异造成的。