RNA interference targeting hypoxia-inducible factor 1α via a novel multifunctional surfactant attenuates glioma growth in an intracranial mouse model

J Neurosurg. 2015 Feb;122(2):331-41. doi: 10.3171/2014.10.JNS132363. Epub 2014 Nov 28.

Abstract

Object: High-grade gliomas are the most common form of adult brain cancer, and patients have a dismal survival rate despite aggressive therapeutic measures. Intratumoral hypoxia is thought to be a main contributor to tumorigenesis and angiogenesis of these tumors. Because hypoxia-inducible factor 1α (HIF-1α) is the major mediator of hypoxia-regulated cellular control, inhibition of this transcription factor may reduce glioblastoma growth.

Methods: Using an orthotopic mouse model with U87-LucNeo cells, the authors used RNA interference to knock down HIF-1α in vivo. The small interfering RNA (siRNA) was packaged using a novel multifunctional surfactant, 1-(aminoethyl) iminobis[N-(oleicylcysteinylhistinyl-1-aminoethyl)propionamide] (EHCO), a nucleic acid carrier that facilitates cellular uptake and intracellular release of siRNA. Stereotactic injection was used to deliver siRNA locally through a guide-screw system, and delivery/uptake was verified by imaging of fluorescently labeled siRNA. Osmotic pumps were used for extended siRNA delivery to model a commonly used human intracranial drug-delivery technique, convection-enhanced delivery.

Results: Mice receiving daily siRNA injections targeting HIF-1α had a 79% lower tumor volume after 50 days of treatment than the controls. Levels of the HIF-1 transcriptional targets vascular endothelial growth factor (VEGF), glucose transporter 1 (GLUT-1), c-MET, and carbonic anhydrase-IX (CA-IX) and markers for cell growth (MIB-1 and microvascular density) were also significantly lower. Altering the carrier EHCO by adding polyethylene glycol significantly increased the efficacy of drug delivery and subsequent survival.

Conclusions: Treating glioblastoma with siRNA targeting HIF-1α in vivo can significantly reduce tumor growth and increase survival in an intracranial mouse model, a finding that has direct clinical implications.

Keywords: CA-IX = carbonic anhydrase-IX; CED = convection-enhanced delivery; DAB = 3,3′-diaminobenzidine tetrahydrochloride; DCA = dichloroacetate; EHCO = 1-(aminoethyl)iminobis[N-(oleicylcysteinylhistinyl-1-aminoethyl)propionamide]; GFP = green fluorescent protein; GLUT-1 = glucose transporter 1; HIF-1α; HIF-1α = hypoxia-inducible factor 1α; IHC = immunohistochemistry; MVD = microvascular density; PEG = polyethylene glycol; PI = proliferation index; RNA interference; RNAi = RNA interference; VEGF = vascular endothelial growth factor; glioma; intracranial; knockdown; mouse; oncology; siRNA; siRNA = small interfering RNA; tumor.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Brain Neoplasms / mortality
  • Brain Neoplasms / pathology*
  • Brain Neoplasms / prevention & control
  • Carbonic Anhydrase IX
  • Carbonic Anhydrases / metabolism
  • Cell Proliferation / drug effects*
  • Dipeptides / pharmacology*
  • Dipeptides / therapeutic use
  • Disease Models, Animal
  • Gene Knockdown Techniques
  • Glioma / mortality
  • Glioma / pathology*
  • Glioma / prevention & control
  • Glucose Transporter Type 1 / metabolism
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / drug effects*
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Ki-67 Antigen / metabolism
  • Mice
  • Mice, Nude
  • Proto-Oncogene Proteins c-met / metabolism
  • RNA Interference*
  • RNA, Small Interfering / pharmacology*
  • RNA, Small Interfering / therapeutic use
  • Survival Rate
  • Vascular Endothelial Growth Factor A / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Dipeptides
  • Glucose Transporter Type 1
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Ki-67 Antigen
  • N-(1-aminoethyl)iminobis(N-(oleoyl-cysteinyl-histidyl-1-aminoethyl)propionamide)
  • RNA, Small Interfering
  • Slc2a1 protein, mouse
  • Vascular Endothelial Growth Factor A
  • Proto-Oncogene Proteins c-met
  • Carbonic Anhydrase IX
  • Carbonic Anhydrases
  • Car9 protein, mouse