Medina-Dols Aina, Cañellas Guillem, Capó Toni, Solé Montse, Mola-Caminal Marina, Cullell Natalia, Jaume Marina, Nadal-Salas Laura, Llinàs Jaume, Gómez Lluis, Tur Silvia, Jiménez Carmen, Díaz Rosa M, Carrera Caty, Muiño Elena, Gallego-Fabrega Cristina, Soriano-Tárraga Carolina, Ruiz-Guerra Laura, Pol-Fuster Josep, Asensio Víctor, Muncunill Josep, Fleischer Aarne, Iglesias Amanda, Giralt-Steinhauer Eva, Lazcano Uxue, Fernández-Pérez Isabel, Jiménez-Balado Joan, Gabriel-Salazar Marina, Garcia-Gabilondo Miguel, Lei Ting, Torres-Aguila Nuria-Paz, Cárcel-Márquez Jara, Lladó Jerònia, Olmos Gabriel, Rosell Anna, Montaner Joan, Planas Anna M, Rabionet Raquel, Hernández-Guillamon Mar, Jiménez-Conde Jordi, Fernández-Cadenas Israel, Vives-Bauzá Cristòfol
Neurobiology Laboratory, Research Unit, Hospital Universitari Son Espases, Health Research Institute of Balearic Islands (IdISBa), Palma, Spain.
Department of Biology, University of Balearic Islands (UIB), Institut Universitari d'Investigacions en Ciències de la Salut (IUNICS), Palma, Spain.
Cell Death Discov. 2024 Feb 17;10(1):85. doi: 10.1038/s41420-024-01857-z.
Through GWAS studies we identified PATJ associated with functional outcome after ischemic stroke (IS). The aim of this study was to determine PATJ role in brain endothelial cells (ECs) in the context of stroke outcome. PATJ expression analyses in patient's blood revealed that: (i) the risk allele of rs76221407 induces higher expression of PATJ, (ii) PATJ is downregulated 24 h after IS, and (iii) its expression is significantly lower in those patients with functional independence, measured at 3 months with the modified Rankin scale ((mRS) ≤2), compared to those patients with marked disability (mRS = 4-5). In mice brains, PATJ was also downregulated in the injured hemisphere at 48 h after ischemia. Oxygen-glucose deprivation and hypoxia-dependent of Hypoxia Inducible Factor-1α also caused PATJ depletion in ECs. To study the effects of PATJ downregulation, we generated PATJ-knockdown human microvascular ECs. Their transcriptomic profile evidenced a complex cell reprogramming involving Notch, TGF-ß, PI3K/Akt, and Hippo signaling that translates in morphological and functional changes compatible with endothelial to mesenchymal transition (EndMT). PATJ depletion caused loss of cell-cell adhesion, upregulation of metalloproteases, actin cytoskeleton remodeling, cytoplasmic accumulation of the signal transducer C-terminal transmembrane Mucin 1 (MUC1-C) and downregulation of Notch and Hippo signaling. The EndMT phenotype of PATJ-depleted cells was associated with the nuclear recruitment of MUC1-C, YAP/TAZ, β-catenin, and ZEB1. Our results suggest that PATJ downregulation 24 h after IS promotes EndMT, an initial step prior to secondary activation of a pro-angiogenic program. This effect is associated with functional independence suggesting that activation of EndMT shortly after stroke onset is beneficial for stroke recovery.
通过全基因组关联研究(GWAS),我们确定了与缺血性中风(IS)后功能结局相关的PATJ。本研究的目的是确定PATJ在中风结局背景下在脑内皮细胞(ECs)中的作用。对患者血液中的PATJ表达分析显示:(i)rs76221407的风险等位基因诱导PATJ更高的表达,(ii)IS后24小时PATJ表达下调,(iii)与那些有明显残疾(改良Rankin量表(mRS)=4-5)的患者相比,在3个月时用改良Rankin量表测量(mRS≤2)功能独立的患者中其表达显著更低。在小鼠脑中,缺血后48小时损伤半球的PATJ也下调。氧糖剥夺和缺氧诱导因子-1α的缺氧依赖性也导致ECs中PATJ耗竭。为了研究PATJ下调的影响,我们生成了PATJ敲低的人微血管ECs。它们的转录组谱证明了涉及Notch、TGF-β、PI3K/Akt和Hippo信号通路的复杂细胞重编程,这转化为与内皮向间充质转化(EndMT)相容的形态和功能变化。PATJ耗竭导致细胞间粘附丧失、金属蛋白酶上调、肌动蛋白细胞骨架重塑、信号转导器C末端跨膜粘蛋白1(MUC1-C)的细胞质积累以及Notch和Hippo信号通路下调。PATJ耗竭细胞的EndMT表型与MUC1-C、YAP/TAZ、β-连环蛋白和ZEB1的核募集相关。我们的结果表明,IS后24小时PATJ下调促进EndMT,这是促血管生成程序二次激活之前的初始步骤。这种作用与功能独立相关,表明中风发作后不久EndMT的激活有利于中风恢复。