PD-1+ Monocytes Mediate Cerebral Vasospasm Following Subarachnoid Hemorrhage

Neurosurgery. 2021 Mar 15;88(4):855-863. doi: 10.1093/neuros/nyaa495.

Abstract

Background: Cerebral vasospasm is a major source of morbidity and mortality following aneurysm rupture and has limited treatment options.

Objective: To evaluate the role of programmed death-1 (PD-1) in cerebral vasospasm.

Methods: Endovascular internal carotid artery perforation (ICAp) was used to induce cerebral vasospasm in mice. To evaluate the therapeutic potential of targeting PD-1, programmed death ligand-1 (PD-L1) was administered 1 h after ICAp and vasospasm was measured histologically at the level of the ICA bifurcation bilaterally. PD-1 expressing immune cell populations were evaluated by flow cytometry. To correlate these findings to patients and evaluate the potential of PD-1 as a biomarker, monocytes were isolated from the peripheral blood and analyzed by flow cytometry in a cohort of patients with ruptured cerebral aneurysms. The daily frequency of PD-1+ monocytes in the peripheral blood was correlated to transcranial Doppler velocities as well as clinical and radiographic vasospasm.

Results: We found that PD-L1 administration prevented cerebral vasospasm by inhibiting ingress of activated Ly6c+ and CCR2+ monocytes into the brain. Human correlative studies confirmed the presence of PD-1+ monocytes in the peripheral blood of patients with ruptured aneurysms and the frequency of these cells corresponded with cerebral blood flow velocities and clinical vasospasm.

Conclusion: Our results identify PD-1+ monocytes as mediators of cerebral vasospasm and support PD-1 agonism as a novel therapeutic strategy.

Keywords: Cerebral vasospasm; Monocyte; Programmed death ligand-1; Programmed death-1; Subarachnoid hemorrhage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / blood supply
  • Brain / diagnostic imaging
  • Brain / drug effects
  • Cerebrovascular Circulation / drug effects
  • Cerebrovascular Circulation / physiology
  • Cohort Studies
  • Mice
  • Mice, Inbred C57BL
  • Monocytes / drug effects
  • Monocytes / metabolism*
  • Programmed Cell Death 1 Receptor / administration & dosage*
  • Subarachnoid Hemorrhage / blood*
  • Subarachnoid Hemorrhage / diagnostic imaging
  • Subarachnoid Hemorrhage / drug therapy*
  • Ultrasonography, Doppler, Transcranial / methods
  • Vasospasm, Intracranial / blood*
  • Vasospasm, Intracranial / diagnostic imaging
  • Vasospasm, Intracranial / prevention & control*

Substances

  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor