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Abstract: FR-OR050

Deciphering the Effect of RAC1-SPTAN1 in Autosomal Recessive PKD (ARPKD) Cystogenesis Using Multifaceted Models

Session Information

Category: Development, Stem Cells, and Regenerative Medicine

  • 600 Development, Stem Cells, and Regenerative Medicine

Authors

  • Kuraoka, Shohei, Massachusetts General Hospital, Boston, Massachusetts, United States
  • Higashi, Yuhei, Massachusetts General Hospital, Boston, Massachusetts, United States
  • Saito, Suguru, Cedars-Sinai Medical Center, Los Angeles, California, United States
  • Harris, Peter C., Mayo Foundation for Medical Education and Research, Rochester, Minnesota, United States
  • Satlin, Lisa M., Icahn School of Medicine at Mount Sinai, New York, New York, United States
  • Yamashita, Michifumi, Cedars-Sinai Medical Center, Los Angeles, California, United States
  • Morizane, Ryuji, Massachusetts General Hospital, Boston, Massachusetts, United States
Background

ARPKD leads to severe renal cysts and progressive kidney dysfunction, with no approved treatments. We recently developed kidney organoid-on-chip models that mimic patients’ distal-nephron cysts, identifying RAC1/c-FOS as potential therapeutic targets for ARPKD patients. However, critical questions remain regarding RAC1’s precise role in cyst formation, cyst origins, and underlying molecular mechanisms.

Methods

We analyzed RNA-seq data from human kidney organoids derived from pluripotent stem cells with heterozygous or homozygous PKHD1 mutations, cultured using an organoid-on-chip system that models cyst formation in CDH1+ distal nephrons, resembling ARPKD pathology. Differential gene expression analyses were conducted to compare PKHD1+/– and PKHD1–/– organoids. To validate these findings, we used an integrated approach combining an enhanced microfluidic perfusion system, transgenic mice, and human kidney samples.

Results

We identified 27 RAC1 effectors with significantly altered expression in PKHD1-/- organoids compared to controls, with most being downregulated. Among these, SPTAN1 was the only effector associated with cystic biology and distal nephron localization. Immunostaining of organoids mirrored the expression pattern of SPTAN1 in the human kidney, demonstrating reduced SPTAN1 expression in PKHD1-/- organoids. Moreover, SPTAN1+/- kidney organoids exhibited distal-nephron cysts, and elevated RAC1/c-FOS expression, consistent with ARPKD patients. Consistently, Sptan1+/- mice exhibited distal-nephron cysts. Transcriptomics and live imaging revealed altered calcium signaling and increased intracellular calcium. Single-cell RNA-seq identified SLC8A1, a sodium/calcium exchanger, as a marker distinguishing distal/connecting tubules from collecting ducts in human kidneys, predominantly expressed in cystic epithelia in organoids and human ARPKD kidneys. Furthermore, Restoring SPTAN1 in PKHD1-/- organoids via CRISPR activation alleviated cystic phenotypes, normalized intracellular calcium, and reduced RAC1/c-FOS expression.

Conclusion

Through a multifaceted approach, we identified SPTAN1 as a key regulator of cystic pathology in ARPKD. These findings highlight epigenome editing of SPTAN1 as a potential therapeutic strategy, paving the way for the translation of findings from basic research into clinical practice.

Funding

  • NIDDK Support

Digital Object Identifier (DOI)