A preclinical study evaluating how degrees of substitution beyond the pharmacopeial range of 2-hydroxypropyl-β-cyclodextrin affect therapeutic efficacy and auditory function after intracerebroventricular administration for Niemann–Pick disease type C

Authors:
  • MTMayuko Tanaka
    Mayuko Tanaka
  • HNHazuki Nakagawa
    Hazuki Nakagawa
  • KNKazuki Nakazono
    Kazuki Nakazono
  • KYKazunori Yanagihara
    Kazunori Yanagihara
  • KIKandai Ishikura
    Kandai Ishikura
  • NNNaomi Nakagata
    Naomi Nakagata
  • TMToru Miwa
    Toru Miwa
  • HTHiroki Takeda
    Hiroki Takeda
  • YOYorihisa Orita
    Yorihisa Orita

Abstract
Niemann-Pick disease type C (NPC) is a cholesterol-related disorder characterized by neurodegeneration that ultimately leads to premature death. A cholesterol-solubilizing agent, 2-hydroxypropyl-β-cyclodextrin (HP-β-CD), is currently under clinical investigation for treating NPC, but its ototoxicity remains problematic. HP-β-CD is a mixture with varying degrees of substitution (DS) of 2-hydroxypropyl groups. However, investigations have been limited to the DS range specified in the European and United States Pharmacopoeias, and the impact of exceeding this range in NPC treatment is unknown. Here, using five HP-β-CDs with DSs of 4.6, 8.4, 9.9 (within the pharmacopeial range), 13.7, and 16.7 (exceeding this range), we evaluated their therapeutic efficacy in Npc1-deficient mice and toxicity in wild-type mice, following their intracerebroventricular injection. At the therapeutic dose, all HP-β-CDs significantly improved the lifespan and disease phenotype of Npc1-deficient mice, regardless of the DS value; however, these effects diminished for DS exceeding the pharmacopeial range. Auditory brainstem response (ABR) indicated a significant elevation in hearing thresholds for all HP-β-CDs administered, regardless of DS values, even when the dose was reduced to half the therapeutic dose. These findings support prioritizing HP-β-CDs with DS values within, rather than beyond, the pharmacopeial range for clinical development.