Macrophage Lyn Kinase Is a Sex‐Specific Regulator of Post–Subarachnoid Hemorrhage Neuroinflammation

Background Lyn kinase is a member of the Src family of tyrosine kinases, primarily known for its role in regulating immune cell signaling. It can phosphorylate and modulate the activity of various proteins involved in immune responses, including Toll‐like receptor 4 (TLR4). TLR4‐mediated inflammator...

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Main Authors: Rezwanul Islam, Hadi Hasan Choudhary, Feng Zhang, Hritik Mehta, Jun Yoshida, Ajith Thomas, Khalid Hanafy
Format: Article
Language:English
Published: Wiley 2025-05-01
Series:Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease
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Online Access:https://www.ahajournals.org/doi/10.1161/JAHA.124.039409
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author Rezwanul Islam
Hadi Hasan Choudhary
Feng Zhang
Hritik Mehta
Jun Yoshida
Ajith Thomas
Khalid Hanafy
author_facet Rezwanul Islam
Hadi Hasan Choudhary
Feng Zhang
Hritik Mehta
Jun Yoshida
Ajith Thomas
Khalid Hanafy
author_sort Rezwanul Islam
collection DOAJ
description Background Lyn kinase is a member of the Src family of tyrosine kinases, primarily known for its role in regulating immune cell signaling. It can phosphorylate and modulate the activity of various proteins involved in immune responses, including Toll‐like receptor 4 (TLR4). TLR4‐mediated inflammatory pathways have been extensively studied; however, the sex‐specific interaction of TLR4 and Lyn in neuroinflammation after aneurysmal subarachnoid hemorrhage (SAH) has yet to be investigated. SAH occurs due to a ruptured aneurysm, and the consequences often lead to neuroinflammation and cognitive impairments. In our study, we investigated the sex‐specific involvement of Lyn kinase in regulating TLR4 signaling to understand the TLR4‐mediated inflammatory response after SAH. Methods Cell‐specific Lyn knockout mice of both sexes were used for this study. Wild‐type and conditional knockout mouse brains were analyzed by multicolor flow cytometry, immunohistochemistry, and western blotting at postoperative day 7 following SAH surgery. An unbiased spatial transcriptomic analysis was performed with the frozen mouse brain tissues. A 3‐dimensional brain stroke model and cerebrospinal fluid samples of patients with SAH were also used for this study. Results Our overall animal and patient data from flow cytometry, immunohistochemistry, western blot, cognitive function tests, and spatial transcriptomic data revealed that Lyn kinase is a sex‐specific regulator in inflammatory cytokine production, red blood cell phagocytosis, neuronal apoptosis, and cognitive function, as well as a negative regulator of TLR4 signaling pathways. Conclusions Our results highlight sex‐specific modulation of Lyn kinase activity in TLR4 signaling after hemorrhagic stroke and indicate that successful treatment of neuroinflammation may require sex‐specific treatments.
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spelling doaj-art-592f1666798040b9a7c2ceec2ae2d2942025-08-20T01:52:18ZengWileyJournal of the American Heart Association: Cardiovascular and Cerebrovascular Disease2047-99802025-05-0114910.1161/JAHA.124.039409Macrophage Lyn Kinase Is a Sex‐Specific Regulator of Post–Subarachnoid Hemorrhage NeuroinflammationRezwanul Islam0Hadi Hasan Choudhary1Feng Zhang2Hritik Mehta3Jun Yoshida4Ajith Thomas5Khalid Hanafy6Cooper Medical School of Rowan University Camden NJ USACooper Medical School of Rowan University Camden NJ USACooper Medical School of Rowan University Camden NJ USACooper Medical School of Rowan University Camden NJ USACooper Medical School of Rowan University Camden NJ USACooper Medical School of Rowan University Camden NJ USACooper Medical School of Rowan University Camden NJ USABackground Lyn kinase is a member of the Src family of tyrosine kinases, primarily known for its role in regulating immune cell signaling. It can phosphorylate and modulate the activity of various proteins involved in immune responses, including Toll‐like receptor 4 (TLR4). TLR4‐mediated inflammatory pathways have been extensively studied; however, the sex‐specific interaction of TLR4 and Lyn in neuroinflammation after aneurysmal subarachnoid hemorrhage (SAH) has yet to be investigated. SAH occurs due to a ruptured aneurysm, and the consequences often lead to neuroinflammation and cognitive impairments. In our study, we investigated the sex‐specific involvement of Lyn kinase in regulating TLR4 signaling to understand the TLR4‐mediated inflammatory response after SAH. Methods Cell‐specific Lyn knockout mice of both sexes were used for this study. Wild‐type and conditional knockout mouse brains were analyzed by multicolor flow cytometry, immunohistochemistry, and western blotting at postoperative day 7 following SAH surgery. An unbiased spatial transcriptomic analysis was performed with the frozen mouse brain tissues. A 3‐dimensional brain stroke model and cerebrospinal fluid samples of patients with SAH were also used for this study. Results Our overall animal and patient data from flow cytometry, immunohistochemistry, western blot, cognitive function tests, and spatial transcriptomic data revealed that Lyn kinase is a sex‐specific regulator in inflammatory cytokine production, red blood cell phagocytosis, neuronal apoptosis, and cognitive function, as well as a negative regulator of TLR4 signaling pathways. Conclusions Our results highlight sex‐specific modulation of Lyn kinase activity in TLR4 signaling after hemorrhagic stroke and indicate that successful treatment of neuroinflammation may require sex‐specific treatments.https://www.ahajournals.org/doi/10.1161/JAHA.124.039409Lyn kinasemicrogliasex‐specific inflammationsubarachnoid hemorrhagetoll‐like receptor‐4
spellingShingle Rezwanul Islam
Hadi Hasan Choudhary
Feng Zhang
Hritik Mehta
Jun Yoshida
Ajith Thomas
Khalid Hanafy
Macrophage Lyn Kinase Is a Sex‐Specific Regulator of Post–Subarachnoid Hemorrhage Neuroinflammation
Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease
Lyn kinase
microglia
sex‐specific inflammation
subarachnoid hemorrhage
toll‐like receptor‐4
title Macrophage Lyn Kinase Is a Sex‐Specific Regulator of Post–Subarachnoid Hemorrhage Neuroinflammation
title_full Macrophage Lyn Kinase Is a Sex‐Specific Regulator of Post–Subarachnoid Hemorrhage Neuroinflammation
title_fullStr Macrophage Lyn Kinase Is a Sex‐Specific Regulator of Post–Subarachnoid Hemorrhage Neuroinflammation
title_full_unstemmed Macrophage Lyn Kinase Is a Sex‐Specific Regulator of Post–Subarachnoid Hemorrhage Neuroinflammation
title_short Macrophage Lyn Kinase Is a Sex‐Specific Regulator of Post–Subarachnoid Hemorrhage Neuroinflammation
title_sort macrophage lyn kinase is a sex specific regulator of post subarachnoid hemorrhage neuroinflammation
topic Lyn kinase
microglia
sex‐specific inflammation
subarachnoid hemorrhage
toll‐like receptor‐4
url https://www.ahajournals.org/doi/10.1161/JAHA.124.039409
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