LC-MS/MS-based in vitro and in vivo investigation of blood-brain barrier integrity by simultaneous quantitation of mannitol and sucrose

Fluids Barriers CNS. 2020 Oct 14;17(1):61. doi: 10.1186/s12987-020-00224-1.

Abstract

Background: Understanding the pathophysiology of the blood brain-barrier (BBB) plays a critical role in diagnosis and treatment of disease conditions. Applying a sensitive and specific LC-MS/MS technique for the measurement of BBB integrity with high precision, we have recently introduced non-radioactive [13C12]sucrose as a superior marker substance. Comparison of permeability markers with different molecular weight, but otherwise similar physicochemical properties, can provide insights into the uptake mechanism at the BBB. Mannitol is a small hydrophilic, uncharged molecule that is half the size of sucrose. Previously only radioactive [3H]mannitol or [14C]mannitol has been used to measure BBB integrity.

Methods: We developed a UPLC-MS/MS method for simultaneous analysis of stable isotope-labeled sucrose and mannitol. The in vivo BBB permeability of [13C6]mannitol and [13C12]sucrose was measured in mice, using [13C6]sucrose as a vascular marker to correct for brain intravascular content. Moreover, a Transwell model with induced pluripotent stem cell-derived brain endothelial cells was used to measure the permeability coefficient of sucrose and mannitol in vitro both under control and compromised (in the presence of IL-1β) conditions.

Results: We found low permeability values for both mannitol and sucrose in vitro (permeability coefficients of 4.99 ± 0.152 × 10-7 and 3.12 ± 0.176 × 10-7 cm/s, respectively) and in vivo (PS products of 0.267 ± 0.021 and 0.126 ± 0.025 µl g-1 min-1, respectively). Further, the in vitro permeability of both markers substantially increased in the presence of IL-1β. Corrected brain concentrations (Cbr), obtained by washout vs. vascular marker correction, were not significantly different for either mannitol (0.071 ± 0.007 and 0.065 ± 0.009 percent injected dose per g) or sucrose (0.035 ± 0.003 and 0.037 ± 0.005 percent injected dose per g). These data also indicate that Cbr and PS product values of mannitol were about twice the corresponding values of sucrose.

Conclusions: We established a highly sensitive, specific and reproducible approach to simultaneously measure the BBB permeability of two classical low molecular weight, hydrophilic markers in a stable isotope labeled format. This method is now available as a tool to quantify BBB permeability in vitro and in vivo in different disease models, as well as for monitoring treatment outcomes.

Keywords: Blood–brain barrier; Brain uptake clearance; In vitro and in vivo correlation; Mannitol; Permeability coefficient; Sucrose; Vascular space correction.

MeSH terms

  • Animals
  • Blood-Brain Barrier / drug effects*
  • Blood-Brain Barrier / physiology*
  • Carbon Isotopes
  • Endothelial Cells
  • Female
  • Gas Chromatography-Mass Spectrometry / methods*
  • Gas Chromatography-Mass Spectrometry / standards
  • Induced Pluripotent Stem Cells
  • Interleukin-1beta / metabolism
  • Mannitol / pharmacokinetics*
  • Mice
  • Mice, Inbred C57BL
  • Reproducibility of Results
  • Sucrose / pharmacokinetics*

Substances

  • Carbon Isotopes
  • IL1B protein, mouse
  • Interleukin-1beta
  • Mannitol
  • Sucrose