Hongmei Yang, Brianne Elise Dillon, Dalila Mary Marzialo, Jaina Therese Dillon, Tian Cao, Emily S Levy, Lindsay Popeo, Shirin Jamali, David Wootton, Eva Grzegorczyk, Cameron Marie Beckey, Amir Davis, Nandita Karthik, Paige Ingrando, Riley L Stogsdill, Binh Minh Ngoc Nguyen, Ruxandra F Sirbulescu, Alexei Degterev, Michael J Whalen, Limin Wu
{"title":"EXPRESS: Sex-dependent roles for RIPK1 in the subacute period of intracerebral hemorrhage in mice.","authors":"Hongmei Yang, Brianne Elise Dillon, Dalila Mary Marzialo, Jaina Therese Dillon, Tian Cao, Emily S Levy, Lindsay Popeo, Shirin Jamali, David Wootton, Eva Grzegorczyk, Cameron Marie Beckey, Amir Davis, Nandita Karthik, Paige Ingrando, Riley L Stogsdill, Binh Minh Ngoc Nguyen, Ruxandra F Sirbulescu, Alexei Degterev, Michael J Whalen, Limin Wu","doi":"10.1177/0271678X261496694","DOIUrl":null,"url":null,"abstract":"<p><p>Receptor-interacting protein kinase-1 (RIPK1) is a serine-threonine kinase that is activated in the brain early after intracerebral hemorrhage (ICH), but its spatial and temporal course in the subacute period is unknown. We used mice deficient in RIPK1 kinase activity to investigate RIPK1 regulation of clinically relevant outcomes in a collagenase ICH model. At 35 days after ICH in wild-type males, RIPK1 was activated (increased in detergent-insoluble fractions) in striatal neurons, endothelium, and astrocytes. In neurons, RIPK1 activation was associated with loss of its regulators TAK1/TBK1, and RIPK1 regulated post-injury neuronal CaMKII𝛼 expression, pathological tau phosphorylation, and inflammasome activation. RIPK1 regulated post-injury gliosis, blood-brain barrier (BBB) damage and cognitive deficits in males. At 35 days after ICH in females, RIPK1 was activated exclusively in neurons but female neurons lacked the biochemical changes seen in males, and RIPK1 did not regulate increased gliosis, BBB damage, or most cognitive deficits in injured females. The studies are the first to describe cell-specific RIPK1 activation in the subacute period of experimental ICH and highlight important sex differences that should inform clinical trials of RIPK1 inhibitors in patients with ICH. Sex differences should be evaluated for RIPK1 in other brain injury models and neurodegenerative disease paradigms.</p>","PeriodicalId":520660,"journal":{"name":"Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism","volume":" ","pages":"271678X261496694"},"PeriodicalIF":4.5000,"publicationDate":"2026-10-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1177/0271678X261496694","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"","JCRName":"","Score":null,"Total":0}
引用次数: 0
Abstract
Receptor-interacting protein kinase-1 (RIPK1) is a serine-threonine kinase that is activated in the brain early after intracerebral hemorrhage (ICH), but its spatial and temporal course in the subacute period is unknown. We used mice deficient in RIPK1 kinase activity to investigate RIPK1 regulation of clinically relevant outcomes in a collagenase ICH model. At 35 days after ICH in wild-type males, RIPK1 was activated (increased in detergent-insoluble fractions) in striatal neurons, endothelium, and astrocytes. In neurons, RIPK1 activation was associated with loss of its regulators TAK1/TBK1, and RIPK1 regulated post-injury neuronal CaMKII𝛼 expression, pathological tau phosphorylation, and inflammasome activation. RIPK1 regulated post-injury gliosis, blood-brain barrier (BBB) damage and cognitive deficits in males. At 35 days after ICH in females, RIPK1 was activated exclusively in neurons but female neurons lacked the biochemical changes seen in males, and RIPK1 did not regulate increased gliosis, BBB damage, or most cognitive deficits in injured females. The studies are the first to describe cell-specific RIPK1 activation in the subacute period of experimental ICH and highlight important sex differences that should inform clinical trials of RIPK1 inhibitors in patients with ICH. Sex differences should be evaluated for RIPK1 in other brain injury models and neurodegenerative disease paradigms.
受体相互作用蛋白激酶-1 (Receptor-interacting protein kinase, RIPK1)是一种丝氨酸-苏氨酸激酶,在脑出血后早期在大脑中被激活,但其在亚急性期的时空变化尚不清楚。我们使用RIPK1激酶活性不足的小鼠,在胶原酶ICH模型中研究RIPK1对临床相关结果的调节。在野生型雄性脑出血后35天,RIPK1在纹状体神经元、内皮细胞和星形胶质细胞中被激活(在洗涤剂不溶性部分增加)。在神经元中,RIPK1的激活与其调节因子TAK1/TBK1的缺失有关,并且RIPK1调节损伤后神经元CaMKII的表达、病理性tau磷酸化和炎性体的激活。RIPK1调节雄性损伤后胶质瘤、血脑屏障(BBB)损伤和认知缺陷。在雌性脑出血后35天,RIPK1仅在神经元中被激活,但雌性神经元缺乏与雄性神经元相同的生化变化,并且RIPK1不能调节受损雌性神经胶质瘤的增加、血脑屏障损伤或大多数认知缺陷。这些研究首次描述了实验性脑出血亚急性期细胞特异性RIPK1激活,并强调了重要的性别差异,这应该为脑出血患者的RIPK1抑制剂的临床试验提供信息。RIPK1在其他脑损伤模型和神经退行性疾病中的性别差异有待评估。