TY - JOUR
T1 - Age-related meningeal extracellular matrix remodeling compromises CNS lymphatic function
AU - Hitpass Romero, Kate
AU - Stevenson, Taylor J.
AU - Smyth, Leon C.D.
AU - Watkin, Ben
AU - McCullough, Samuel J.C.
AU - Vinnell, Luca
AU - Smith, Amy M.
AU - Schweder, Patrick
AU - Correia, Jason A.
AU - Kipnis, Jonathan
AU - Dragunow, Mike
AU - Rustenhoven, Justin
N1 - Publisher Copyright:
© The Author(s) 2025.
PY - 2025/12
Y1 - 2025/12
N2 - Efficient clearance of central nervous system (CNS) waste proteins and appropriate immune surveillance is essential for brain health. These processes are facilitated by lymphatic networks present in the meninges that drain cerebrospinal fluid (CSF). Age-related impairments to meningeal lymphatic drainage contribute to CNS waste accumulation and immune dysfunction, yet the underlying mechanisms remain poorly understood. Here, we identify extracellular matrix (ECM) remodeling in the aged dura as a key driver of CSF clearance deficits, demonstrating that peri-lymphatic collagen accumulation disrupts lymphatic function. Exploring immune-derived factors contributing to this ECM remodeling, we identify transforming growth factor beta 1 (TGFβ1) as a major regulator using primary human dural fibroblasts. Using a novel mouse model with constitutively active TGFβ receptor 1 (TGFβR1) signaling in dural fibroblasts, we show that excessive peri-lymphatic collagen deposition impairs meningeal lymphatic drainage and alters meningeal immunity. Mechanistically, we reveal that ECM-associated matrix stiffness disrupts lymphatic junction integrity and impairs lymphangiogenesis in human lymphatic endothelial cells. These findings establish dural immune cell and fibroblast-mediated ECM remodeling as a critical regulator of CSF clearance and highlight it as a potential therapeutic target for restoring brain waste clearance in aging.
AB - Efficient clearance of central nervous system (CNS) waste proteins and appropriate immune surveillance is essential for brain health. These processes are facilitated by lymphatic networks present in the meninges that drain cerebrospinal fluid (CSF). Age-related impairments to meningeal lymphatic drainage contribute to CNS waste accumulation and immune dysfunction, yet the underlying mechanisms remain poorly understood. Here, we identify extracellular matrix (ECM) remodeling in the aged dura as a key driver of CSF clearance deficits, demonstrating that peri-lymphatic collagen accumulation disrupts lymphatic function. Exploring immune-derived factors contributing to this ECM remodeling, we identify transforming growth factor beta 1 (TGFβ1) as a major regulator using primary human dural fibroblasts. Using a novel mouse model with constitutively active TGFβ receptor 1 (TGFβR1) signaling in dural fibroblasts, we show that excessive peri-lymphatic collagen deposition impairs meningeal lymphatic drainage and alters meningeal immunity. Mechanistically, we reveal that ECM-associated matrix stiffness disrupts lymphatic junction integrity and impairs lymphangiogenesis in human lymphatic endothelial cells. These findings establish dural immune cell and fibroblast-mediated ECM remodeling as a critical regulator of CSF clearance and highlight it as a potential therapeutic target for restoring brain waste clearance in aging.
KW - Aging
KW - Extracellular matrix
KW - Fibrosis
KW - Lymphatics
KW - Meningeal immunity
KW - Meninges
KW - Traumatic brain injury
UR - http://www.scopus.com/inward/record.url?scp=105003129916&partnerID=8YFLogxK
U2 - 10.1186/s12974-025-03436-0
DO - 10.1186/s12974-025-03436-0
M3 - Article
C2 - 40247257
AN - SCOPUS:105003129916
SN - 1742-2094
VL - 22
JO - Journal of Neuroinflammation
JF - Journal of Neuroinflammation
IS - 1
M1 - 109
ER -