Use of Human Induced Pluripotent Stem Cells and Kidney Organoids To Develop a Cysteamine/mTOR Inhibition Combination Therapy for Cystinosis

J Am Soc Nephrol. 2020 May;31(5):962-982. doi: 10.1681/ASN.2019070712. Epub 2020 Mar 20.

Abstract

Background: Mutations in CTNS-a gene encoding the cystine transporter cystinosin-cause the rare, autosomal, recessive, lysosomal-storage disease cystinosis. Research has also implicated cystinosin in modulating the mTORC1 pathway, which serves as a core regulator of cellular metabolism, proliferation, survival, and autophagy. In its severest form, cystinosis is characterized by cystine accumulation, renal proximal tubule dysfunction, and kidney failure. Because treatment with the cystine-depleting drug cysteamine only slows disease progression, there is an urgent need for better treatments.

Methods: To address a lack of good human-based cell culture models for studying cystinosis, we generated the first human induced pluripotent stem cell (iPSC) and kidney organoid models of the disorder. We used a variety of techniques to examine hallmarks of cystinosis-including cystine accumulation, lysosome size, the autophagy pathway, and apoptosis-and performed RNA sequencing on isogenic lines to identify differentially expressed genes in the cystinosis models compared with controls.

Results: Compared with controls, these cystinosis models exhibit elevated cystine levels, increased apoptosis, and defective basal autophagy. Cysteamine treatment ameliorates this phenotype, except for abnormalities in apoptosis and basal autophagy. We found that treatment with everolimus, an inhibitor of the mTOR pathway, reduces the number of large lysosomes, decreases apoptosis, and activates autophagy, but it does not rescue the defect in cystine loading. However, dual treatment of cystinotic iPSCs or kidney organoids with cysteamine and everolimus corrects all of the observed phenotypic abnormalities.

Conclusions: These observations suggest that combination therapy with a cystine-depleting drug such as cysteamine and an mTOR pathway inhibitor such as everolimus has potential to improve treatment of cystinosis.

Keywords: cystinosis; induced pluripotent stem cells; kidney disease; kidney organoids; new treatments.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Transport Systems, Neutral / deficiency
  • Amino Acid Transport Systems, Neutral / genetics
  • Animals
  • Autophagy / drug effects
  • CRISPR-Cas Systems
  • Cell Line
  • Cysteamine / pharmacology
  • Cysteamine / therapeutic use*
  • Cystine / blood
  • Cystinosis / drug therapy*
  • Disease Models, Animal*
  • Drug Evaluation, Preclinical
  • Drug Therapy, Combination
  • Everolimus / pharmacology
  • Everolimus / therapeutic use*
  • Gene Editing
  • Heterografts
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Induced Pluripotent Stem Cells / transplantation*
  • Induced Pluripotent Stem Cells / ultrastructure
  • Lysosomes / drug effects
  • Lysosomes / ultrastructure
  • Mice
  • Mice, SCID
  • Organoids / metabolism
  • Organoids / transplantation*
  • Phenotype
  • TOR Serine-Threonine Kinases / antagonists & inhibitors*

Substances

  • Amino Acid Transport Systems, Neutral
  • CTNS protein, human
  • Cystine
  • Cysteamine
  • Everolimus
  • TOR Serine-Threonine Kinases