Redox-proteomics of the effects of homogentisic acid in an in vitro human serum model of alkaptonuric ochronosis

J Inherit Metab Dis. 2011 Dec;34(6):1163-76. doi: 10.1007/s10545-011-9377-6. Epub 2011 Aug 27.

Abstract

Alkaptonuria (AKU) is a rare inborn error of metabolism associated with a deficient activity of homogentisate 1,2-dioxygenase (HGO), an enzyme involved in tyrosine and phenylalanine metabolism. Such a deficiency leads to the accumulation of homogentisic acid (HGA) and its oxidized/polymerized products in connective tissues, where melanin-like pigments accumulate (ochronosis). Ochronosis involves especially joints, where an ochronotic arthropathy develops. Little is known on the molecular mechanisms leading to ochronosis and ochronotic arthropathy in AKU. Previous works of ours showed that HGA in vitro propagates oxidative stress through its conversion into benzoquinone acetate (BQA). We hence used an in vitro model consisting of human serum treated with HGA and evaluated the activities of glutathione related anti-oxidant enzymes and levels of compounds indexes of oxidative stress. Proteomics and redox-proteomics were used to identify oxidized proteins and proteins more likely able to bind BQA. Overall, we found that the production of ochronotic pigment in HGA-treated serum is accompanied by lipid peroxidation, decreased activity of the enzyme glutathione peroxidase and massive depletion of thiol groups, together with increased protein carbonylation and thiol oxidation. We also found that BQA was likely to bind carrier proteins and naturally abundant serum proteins, eventually altering their chemico-physical properties. Concluding, our work points towards a critical importance of thiol compounds in counteracting HGA- and BQA- mediated stress in AKU, so that future research for disease biomarkers and pharmacological treatments for AKU and ochronosis will be more easily addressed.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alkaptonuria / blood*
  • Alkaptonuria / complications
  • Benzoquinones / metabolism
  • Glutathione Peroxidase / drug effects
  • Glutathione Peroxidase / metabolism
  • Glutathione Reductase / drug effects
  • Glutathione Reductase / metabolism
  • Homogentisic Acid / pharmacology*
  • Humans
  • In Vitro Techniques
  • Lipid Peroxidation / drug effects*
  • Ochronosis / blood*
  • Ochronosis / etiology
  • Oxidation-Reduction / drug effects
  • Protein Carbonylation / drug effects*
  • Proteomics / methods
  • Serum / drug effects
  • Serum / metabolism
  • Sulfhydryl Compounds / metabolism*

Substances

  • Benzoquinones
  • Sulfhydryl Compounds
  • quinone
  • Glutathione Peroxidase
  • Glutathione Reductase
  • Homogentisic Acid