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Disruption in iron homeostasis and impaired activity of iron-sulfur cluster containing proteins in the yeast model of Shwachman-Diamond syndrome

MetadataDetails
Publication Date2020-09-11
JournalCell & Bioscience
AuthorsAyushi Jain, Phubed Nilatawong, Narinrat Mamak, Laran T. Jensen, Amornrat Naranuntarat Jensen
InstitutionsMahidol University
Citations3
AnalysisFull AI Review Included

This research utilizes a Saccharomyces cerevisiae model (lacking the SDO1 gene, the ortholog of human SBDS) to investigate the molecular pathogenesis of Shwachman-Diamond Syndrome (SDS), focusing on iron homeostasis and mitochondrial function.

  • Core Defect: Deletion of SDO1 results in a three-fold over-accumulation of intracellular iron, mimicking iron overload conditions seen in other mitochondrial diseases.
  • Functional Impairment: This iron overload leads to impaired activity of critical Iron-Sulfur Cluster (ISC) containing enzymes, specifically Aconitase and Succinate Dehydrogenase (SDH), and reduces the activity of Manganese Superoxide Dismutase (Sod2p).
  • Oxidative Stress Mechanism: The excess iron contributes to elevated Reactive Oxygen Species (ROS) and protein oxidation, which can be mitigated by using the cell-impermeable iron chelator, Bathophenanthroline Disulfonic Acid (BPS).
  • VDAC Linkage: The iron accumulation and subsequent ISC enzyme impairment are linked to the over-expression of the mitochondrial Voltage-Dependent Anion Channel (VDAC), Por1p.
  • Mitigation Strategy: Deletion of POR1 in the sdo1Δ strain successfully limits iron accumulation and restores the activity of Aconitase and SDH, suggesting Por1p over-expression mediates the disease phenotype.
  • Proposed Pathway: Oxidative stress resulting from POR1 over-expression disrupts ISC protein activity and iron homeostasis, contributing to SDS pathogenesis.

The following table summarizes key quantitative data and experimental parameters derived from the study of the Saccharomyces cerevisiae model.

ParameterValueUnitContext
Intracellular Iron Overload3-fold higherRatioIron content in sdo1Δ yeast vs. Wild-Type (WT)
Iron Chelation Concentration (BPS)40 or 120”MBathophenanthroline Disulfonic Acid (BPS) used in YPD medium
Culture Temperature30°CStandard yeast growth conditions
Stationary Phase Culture Time40hoursUsed for Aconitase and SDH activity assays
Hydrogen Peroxide Stress2mmol/LUsed to induce oxidative damage for protein carbonylation analysis
Aconitase ActivityP < 0.001Statistical SignificanceReduction observed in sdo1Δ cells vs. WT
Succinate Dehydrogenase (SDH) ActivityP < 0.001Statistical SignificanceReduction observed in sdo1Δ cells vs. WT
Sod2p Activity EnhancementSignificant (P < 0.01)RatioImprovement in sdo1Δ cells following BPS treatment
ROS Level ReductionSignificant (P < 0.01)RatioReduction in sdo1Δ cells following BPS treatment

The study employed standard yeast genetics and biochemical assays, focusing on precise measurement of metal content, enzyme function, and oxidative stress markers.

  1. Strain Generation and Culture: Saccharomyces cerevisiae strains (BY4741/4742 background) were used, including deletion mutants (sdo1Δ, por1Δ, rhoÂș, and double mutants). Cells were cultured in enriched YPD medium at 30 °C.
  2. Iron Depletion: Iron chelation was achieved by supplementing the medium (adjusted to pH 6.0 with MOPS) with 40 ”M or 120 ”M BPS (Bathophenanthroline Disulfonic Acid).
  3. Intracellular Iron Measurement: Iron concentration was quantified using Graphite Furnace Atomic Absorption Spectroscopy (GFAAS) on washed cell pellets, normalized to cell count (nmole Fe/109 cells).
  4. Oxidative Stress Analysis (ROS): Intracellular ROS levels were measured using the fluorescent probe 2,7-dichorofluorescein diacetate (H2DCFDA), with fluorescence normalized to protein concentration.
  5. Protein Carbonylation: Oxidative damage to proteins was assessed by derivatization with 2,4-dinitrophenylhydrazine (DNPH), followed by immunoblotting using an anti-DNP antibody.
  6. Enzyme Activity Assays:
    • Sod2p (Superoxide Dismutase): Activity was analyzed by non-denaturing gel electrophoresis and staining with nitro blue tetrazolium (NBT).
    • Aconitase: Activity was monitored spectrophotometrically at 240 nm, tracking the conversion of cis-aconitate to isocitrate.
    • Succinate Dehydrogenase (SDH): Activity was measured in isolated mitochondria by monitoring the reduction of dichlorophenol indophenol at 600 nm.
  7. Gene Expression Monitoring: The induction of the high-affinity iron uptake gene FET3 was monitored using a FET3-lacZ reporter plasmid and subsequent ÎČ-galactosidase assays.

While this research is fundamentally biomedical, the underlying principles of precise trace metal control, management of reactive species, and monitoring of enzyme function are relevant to advanced materials engineering, particularly in high-purity synthesis environments.

  • High-Purity Precursor Management: The study highlights the extreme sensitivity of biological systems (and by extension, catalytic processes) to trace metal contamination (iron overload). This reinforces the need for rigorous control and purification of precursors used in CVD processes (e.g., those supplied by 6ccvd.com) to prevent catalytic poisoning or defect formation.
  • Environmental Control in Synthesis: The mechanism involves Reactive Oxygen Species (ROS) generated by misregulated iron, leading to material (protein) damage. In CVD and materials synthesis (e.g., 2D materials, graphene), managing the oxidative environment (analogous to ROS) and preventing unwanted side reactions caused by trace contaminants is critical for achieving high-quality, defect-free films.
  • Biosensor and Bioreactor Design: The use of enzyme activity (Aconitase, SDH) as a highly sensitive readout for cellular stress and metal status provides a model for developing advanced biosensors capable of detecting subtle changes in environmental toxicity or metal availability.
  • Drug/Inhibitor Screening: The successful mitigation of defects using BPS (a chelator) and POR1 deletion demonstrates a pathway for screening small molecules that target VDACs or metal homeostasis, potentially leading to new therapeutic agents or industrial inhibitors for metal-induced degradation.