Inhibition of papain by S-nitrosothiols. Formation of mixed disulfides

J Biol Chem. 2000 Jul 7;275(27):20467-73. doi: 10.1074/jbc.M001054200.

Abstract

S-Nitrosylation of protein thiols is one of the cellular regulatory mechanisms induced by NO. The cysteine protease papain has a critical thiol residue (Cys(25)). It has been demonstrated that NO or NO donors such as sodium nitroprusside and N-nitrosoaniline derivatives can reversibly inhibit this enzyme by S-NO bond formation in its active site. In this study, a different regulated mechanism of inactivation was reported using S-nitrosothiols as the NO donor. Five S-nitroso compounds, S-nitroso-N-acetyl-dl-penicillamine, S-nitrosoglutathione, S-nitrosocaptopril, glucose-S-nitroso-N-acetyl-dl-penicillamine-2, and the S-nitroso tripeptide acetyl-Phe-Gly-S-nitrosopenicillamine, exhibited different inhibitory activities toward the enzyme in a time- and concentration-dependent manner with second-order rate constants (k(i)/K(I)) ranging from 8.9 to 17.2 m(-1) s(-1). The inhibition of papain by S-nitrosothiol was rapidly reversed by dithiothreitol, but not by ascorbate, which could reverse the inhibition of papain by NOBF(4). Incubation of the enzyme with a fluorescent S-nitroso probe (S-nitroso-5-dimethylaminonaphthalene-1-sulfonyl) resulted in the appearance of fluorescence of the protein, indicating the formation of a thiol adduct. Moreover, S-transnitrosylation in the incubation of S-nitroso inactivators with papain was excluded. These results suggest that inactivation of papain by S-nitrosothiols is due to a direct attack of the highly reactive thiolate (Cys(25)) in the enzyme active site on the sulfur of S-nitrosothiols to form a mixed disulfide between the inactivator and papain.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Binding Sites
  • Cysteine / metabolism
  • Disulfides / chemistry
  • Dithiothreitol / pharmacology
  • Enzyme Activation / drug effects
  • Enzyme Inhibitors / pharmacology*
  • Fluorescent Dyes
  • Glutathione / analogs & derivatives
  • Glutathione / pharmacology
  • Kinetics
  • Mercaptoethanol*
  • Molecular Structure
  • Nitric Oxide / metabolism
  • Nitroso Compounds / pharmacology*
  • Papain / antagonists & inhibitors*
  • Papain / chemistry
  • S-Nitrosoglutathione
  • S-Nitrosothiols*
  • Spectrometry, Fluorescence
  • Sulfhydryl Compounds / metabolism

Substances

  • Disulfides
  • Enzyme Inhibitors
  • Fluorescent Dyes
  • Nitroso Compounds
  • S-Nitrosothiols
  • Sulfhydryl Compounds
  • Nitric Oxide
  • S-Nitrosoglutathione
  • Mercaptoethanol
  • S-nitrosomercaptoethanol
  • Papain
  • Glutathione
  • Cysteine
  • Dithiothreitol