Assessing the Role of Metabolism in Polycystic Kidney Disease
Alyssa Hahn | Carroll College
akhahn@carroll.edu
Project Summary
Autosomal dominant polycystic kidney disease (ADPKD) is the most common heritable kidney disease, affecting 1:400-1:1000 individuals worldwide. ADPKD is caused by mutations in PKD1 or PKD2, which encode polycystin 1 (PC1) and polycystin 2 (PC2), respectively, and is characterized by the development and progressive enlargement of fluid-filled cysts in the kidneys. There is phenotypic variability in the clinical presentation of symptoms, severity of disease, rate of progression, and age of onset of end stage renal disease (ESRD). Truncating mutations in PKD1 are associated with a more severe phenotype (earlier symptom presentation, more and larger cysts, and faster rate of progression to renal failure) than non-truncating PKD1 mutations or PKD2 mutations. In all cases, renal cysts damage the surrounding tissue and ultimately lead to the decline in function.
ADPKD is often diagnosed by renal ultrasonography confirmation of cystic kidneys and a positive family history when patients present with symptoms such as abdominal and back pain, hypertension, urinary tract infections, hematuria, and kidney stones. However, current diagnostic methods do not determine the extent of damage to the kidneys due to early cyst formation or establish the rate of progression. The development of renal cysts may precede presentation of symptoms and subsequent decline in renal function by many decades. Knowing which patients have aggressive disease (either cysts or fibrosis) would allow for selection of patients for clinical trials and treatment with Tolvaptan, the only FDA-approved treatment. Thus, there is a need for new methods for diagnosing and monitoring disease progression in early-stage ADPKD to allow time for public health strategies and therapeutic interventions to be implemented or administered to slow or halt the progression toward ESRD.
An emerging area in ADPKD research is understanding the role of altered cellular metabolism driving cystogenesis. Recent studies investigating metabolic reprogramming in ADPKD cells and tissues have found shifts from oxidative phosphorylation to aerobic glycolysis (the Warburg Effect), elevated pentose phosphate pathway (PPP) activity, enhanced glutamine and amino acid metabolism, increased fatty acid biosynthesis, and decreased fatty acid oxidation. Our preliminary studies assessing the metabolic pathways driving the formation of in vitro renal microcysts further support altered cellular metabolism in ADPKD, identifying glutamate metabolism, vitamin metabolism, the TCA cycle, amino acid metabolism, butanoate metabolism, pyrimidine metabolism, sugar metabolism, fatty acid oxidation, and the carnitine shuttle as pathways perturbed. Expanding our understanding of metabolic reprogramming in ADPKD may lead to the identification of novel biochemical biomarkers for monitoring the progression of early stages of ADPKD and the response to clinical treatment.
Project Aims
The overall goal of this project is to expand our understanding of altered cellular metabolism in ADPKD toward the development of new diagnostics for earlier ADPKD detection. We hypothesize that metabolic reprogramming in ADPKD will lead to changes in metabolite concentrations in urine that may be candidate biomarkers of ADPKD. Specifically, we hypothesize that metabolic biomarkers of ADPKD will be involved in shifts in central carbon metabolism, consistent with current evidence of metabolic reprogramming in ADPKD. We will test this hypothesis with the following aim:
- Identify candidate biomarkers of ADPKD in urine from early-stage ADPKD donors.
Urine is well-suited for searching for early biomarkers of ADPKD because many of the initial cysts will still be connected to the collecting system and factors produced by the cysts will appear in urine. Urine samples will be obtained through our collaboration with the Kansas PKD Research and Translation Core Center, who has an established biomarker repository with clinical data including estimated glomerular filtration rate, blood urea nitrogen levels, creatinine, and total kidney volume measured by magnetic resonance imaging from a cohort of individuals (age ≤ 35 years old) with early stage ADPKD in the longitudinal Early PKD Observational Cohort (EPOC) study along with non-affected siblings and age-matched controls. Participants are asked to fast for 8 hours prior to the study visit and second morning urines are collected. Metabolites will be extracted from sex- and age-matched healthy (control) and ADPKD urine for global metabolomic profiling. Using a variety of univariate and multivariate statistical methods, we expect to identify differences in both metabolic pathways and specific candidate metabolite biomarkers of ADPKD and reveal subgroups of donors that correlate to ADPKD heterogeneity (e.g., rate of disease progression).
This will be the first study to search for metabolic biomarkers of early-stage ADPKD in human urine using mass-spectrometry-based global metabolomic profiling. Successful completion of this aim will add to the field of ADPKD by showcasing an innovative approach for biomarker discovery for ADPKD and identify candidate biomarkers of disease for further validation. Finally, the proposed pilot project will generate significant and substantial preliminary data for a publication supporting a future R01 project