Biophysical characterization of the cocaine binding pocket in the serotonin transporter using a fluorescent cocaine analogue as a molecular reporter

J Biol Chem. 2001 Feb 16;276(7):4717-23. doi: 10.1074/jbc.M008067200. Epub 2000 Nov 2.

Abstract

To explore the biophysical properties of the binding site for cocaine and related compounds in the serotonin transporter SERT, a high affinity cocaine analogue (3beta-(4-methylphenyl)tropane-2beta-carboxylic acid N-(N-methyl-N-(4-nitrobenzo-2-oxa-1,3-diazol-7-yl)ethanolamine ester hydrochloride (RTI-233); K(I) = 14 nm) that contained the environmentally sensitive fluorescent moiety 7-nitrobenzo-2-oxa-1,3-diazole (NBD) was synthesized. Specific binding of RTI-233 to the rat serotonin transporter, purified from Sf-9 insect cells, was demonstrated by the competitive inhibition of fluorescence using excess serotonin, citalopram, or RTI-55 (2beta-carbomethoxy-3beta-(4-iodophenyl)tropane). Moreover, specific binding was evidenced by measurement of steady-state fluorescence anisotropy, showing constrained mobility of bound RTI-233 relative to RTI-233 free in solution. The fluorescence of bound RTI-233 displayed an emission maximum (lambda(max)) of 532 nm, corresponding to a 4-nm blue shift as compared with the lambda(max) of RTI-233 in aqueous solution and corresponding to the lambda(max) of RTI-233 in 80% dioxane. Collisional quenching experiments revealed that the aqueous quencher potassium iodide was able to quench the fluorescence of RTI-233 in the binding pocket (K(SV =) 1.7 m(-)(1)), although not to the same extent as free RTI-233 (K(SV =) 7.2 m(-)(1)). Conversely, the hydrophobic quencher 2,2,6,6-tetramethylpiperidine-N-oxyl (TEMPO) quenched the fluorescence of bound RTI-233 more efficiently than free RTI-233. These data are consistent with a highly hydrophobic microenvironment in the binding pocket for cocaine-like uptake inhibitors. However, in contrast to what has been observed for small-molecule binding sites in, for example, G protein-coupled receptors, the bound cocaine analogue was still accessible for aqueous quenching and, thus, partially exposed to solvent.

Publication types

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

MeSH terms

  • Animals
  • Binding Sites
  • Carrier Proteins / metabolism*
  • Citalopram / metabolism
  • Cocaine / analogs & derivatives
  • Cocaine / chemical synthesis
  • Cocaine / metabolism*
  • Fluorescent Dyes / metabolism*
  • Membrane Glycoproteins / metabolism*
  • Membrane Transport Proteins*
  • Nerve Tissue Proteins*
  • Protein Binding
  • Rats
  • Recombinant Proteins / metabolism
  • Serotonin / metabolism
  • Serotonin Plasma Membrane Transport Proteins
  • Spectrometry, Fluorescence
  • Spodoptera / genetics
  • Transfection

Substances

  • 8-methyl-3-(4-methylphenyl)tropane--2-carboxylic acid N-methyl-N-(4-nitrobenzo-2-oxa-1,3-diazol-7-yl)ethanolamine ester
  • Carrier Proteins
  • Fluorescent Dyes
  • Membrane Glycoproteins
  • Membrane Transport Proteins
  • Nerve Tissue Proteins
  • Recombinant Proteins
  • Serotonin Plasma Membrane Transport Proteins
  • Slc6a4 protein, rat
  • Citalopram
  • Serotonin
  • 2beta-carbomethoxy-3beta-(4-iodophenyl)tropane
  • Cocaine