The Cervical and Meningeal Lymphatic Network as a Pathway for Retrograde Nanoparticle Transport to the Brain

Int J Nanomedicine. 2024 Oct 24:19:10725-10743. doi: 10.2147/IJN.S477159. eCollection 2024.

Abstract

Introduction: The meningeal lymphatic vessels have been described as a pathway that transports cerebrospinal fluid and interstitial fluid in a unidirectional manner towards the deep cervical lymph nodes. However, these vessels exhibit anatomical and molecular characteristics typical of initial lymphatic vessels, with the absence of surrounding smooth muscle and few or absent valves. Given its structure, this network could theoretically allow for bidirectional motion. Nevertheless, it has not been assessed as a potential route for nanoparticles to travel from peripheral tissues to the brain.

Methods: We employed superparamagnetic iron oxide nanoparticles (SPIONs), exosomes loaded with SPIONs, gold nanorods, and Chinese ink nanoparticles. SPIONs were prepared via chemical coprecipitation, while exosomes were isolated from the B16F10 melanoma cell line through the Exo-Spin column protocol and loaded with SPIONs through electroporation. Gold nanorods were functionalized with polyethylene glycol. We utilized C57BL/6 mice for post-mortem and in vivo procedures. To evaluate the retrograde directional flow, we injected each nanoparticle solution in the deep cervical lymph node. The head and neck were fixed for magnetic resonance imaging and histological analysis.

Results: Here we show that extracellular vesicles derived from the B16F10 melanoma cell line, along with superparamagnetic iron oxide nanoparticles, gold nanorods, and Chinese ink nanoparticles can reach the meningeal lymphatic vessels and the brain of C57BL/6 mice after administration within the deep cervical lymph nodes post-mortem and in vivo, exclusively through lymphatic structures.

Discussion: The functional anatomy of dural lymphatics has been found to be conserved between mice and humans, suggesting that our findings may have significant implications for advancing targeted drug delivery systems using nanoparticles. Understanding the retrograde transport of nanoparticles through the meningeal lymphatic network could lead to novel therapeutic approaches in nanomedicine, offering new insights into fluid dynamics in both physiological and neuropathological contexts. Further research into this pathway may unlock new strategies for treating neurological diseases or enhancing drug delivery to the brain.

Keywords: Chinese ink; SPIONs; extracellular vesicles; gold nanorods; meningeal lymphatic vessels; nanomedicine.

MeSH terms

  • Animals
  • Brain* / metabolism
  • Cell Line, Tumor
  • Exosomes / chemistry
  • Exosomes / metabolism
  • Gold* / chemistry
  • Gold* / pharmacokinetics
  • Lymph Nodes / metabolism
  • Lymphatic Vessels / metabolism
  • Magnetic Iron Oxide Nanoparticles / chemistry
  • Magnetic Resonance Imaging / methods
  • Magnetite Nanoparticles / chemistry
  • Melanoma, Experimental / metabolism
  • Meninges* / metabolism
  • Mice
  • Mice, Inbred C57BL*
  • Neck

Substances

  • Gold
  • Magnetite Nanoparticles

Grants and funding

This study was supported by ANID BECAS/DOCTORADO NACIONAL 21211334; ANID - Millennium Science Initiative Program - ICN2021_004, ANID – FONDECYTs 1220922, 1231773 and 1211482; CONICYT-FONDAP 15130011, FONDAP 1523A0008A, FONDEQUIP NTA (EQM160157), and FONDEQUIP SEM (EQM170111).